Short-Finned Pilot Whale

The genus Globicephala contains two currently accepted species: the long-finned pilot whale G. melas (Trail 1809) and the  short-finned pilot whale G. macrorhynchus Gray 1846 The former inhabits temperate and subpolar waters of the world, with exception of the North Pacific This type of distribution pattern is called anti-tropical distribution (Davies 1963; Barnes 1985)

The long-finned pilot whale does not currently inhabit the North Pacific but is known to have once occurred there, based on a subfossil specimen and relics in archaeological sites in the North Pacific Kasuya (1975) reported six skulls of the species from the western North Pacific and the northern Sea of Japan One was found in a stratum in the bed of the Hekuri River in Tateyama City (35°00′N, 139°52′E) The 14C dating of accompanying coral and oyster remains gave 6340 ± 140 years BP and 6430 ± 130 years BP, respectively, which corresponds in Japan to the era of the Jomon Culture (16,500-3000 years BP) The other five skulls were from two archaeological sites of the Okhotsk Sea Culture on Rebun Island (45°22′N, 141°02′E) in the northern Sea of Japan from the eleventh to thirteenth centuries They accompanied numerous skeletal remains of various other marine mammals (Kasuya 1981, in Japanese) The species was also identified at an archaeological site on Unalaska Island in the eastern Aleutian Islands from 3500 to 2500 years BP (Frey et al 2005) Thus, the long-finned pilot whale is believed to have been hunted by inhabitants of the northern North Pacific until relatively recently (Crockford 2008) Possible contribution of hunting activities to the disappearance from the North Pacific has not been evaluated The short-finned pilot whale is the only current inhabitant of the genus Globicephala in the North Pacific

Skull morphology, flipper length, and, to some extent, tooth counts help in morphologically distinguishing between the two species, but this cannot be accomplished by consideration of only body size or pigmentation, due to large geographical variation within the species (Kasuya and Matsui 1984; Kasuya et al 1988) Measurements of 3400 long-finned pilot whales in the North Atlantic revealed that flipper length measured on a straight line from the anterior insertion to the tip increased almost linearly with body length but allometrically Thus, the proportion flipper length to body length changed with body length The proportion decreased from around 25% in newborns at body length 15 m to 20% at body length 25 m It then increased proportionately to about 25% at body length of 6 m (Bloch et al 1993a,b) The proportion was 16%–29% for all the postnatal animals and 18%–29% for

adults Yonekura et al (1980) carried out a similar analysis on short-finned pilot whales off central Japan (Section 123) and showed that flipper length increased almost in proportion to body length of postnatal individuals; they presented the value of 158%–190% for 21 individuals, including newborns, and 158%–189% (mean 163%) for 18 adults Thus, flipper length expressed as a proportion of body length showed some overlap between adults of the two species Although Yonekura et  al (1980) also noted that short-finned pilot whales had a smaller proportional length from umbilicus to tail notch, the difference (56% vs 60%–61%) seemed too small to be relied on for distinction between the two species

Difference between the two species is most distinct in the shape of the premaxillae visible on the dorsal surface of the rostral portion of the skull Kasuya (1975) compared 29 skulls of long-finned pilot whales from both hemispheres (skull length 580-712 cm) and 37 skulls of short-finned pilot whales from both hemispheres, including the North Pacific (skull length 540-748  cm) In the long-finned pilot whales, width of the rostrum at mid-length was 268%–330% (mean 292%) of total skull length, while the proportion was 283%– 490% (mean 343%) in the short-finned pilot whales The width of the premaxillae measured at the same point ranged from 211% to 285% (mean 249%) in the former species and from 267% to 472% (mean 328%) in the latter The overlap between the two species was smaller in width across the premaxillae These morphological differences in the rostral portion of the skull are easily recognized visually or by plotting the measurements on skull length (Figure 1 of Kasuya 1975) (Figure 121) The premaxillae are narrow with almost parallel lateral margins and the underlying maxillae are exposed outside the premaxillae on the rostrum of the long-finned pilot whale, while the premaxillae in the short-finned pilot whale expand laterally in the anterior portion of the rostrum and cover the maxillae The short-finned pilot whale has slightly fewer teeth on average than the long-finned pilot whales Kasuya (1975) compared tooth counts between the two species Thirty-four upper tooth rows of long-finned pilot whales had 9-12 teeth (mean 101), while 74 tooth rows of shortfinned pilot whales had 6-10 teeth (mean 79) However, it was an error to have treated the tooth rows of the same individual as independent data The mandibular teeth were not examined because of uncertainty in species identification

The Japanese name kobire-gondo was a translation of “shortfinned pilot whale” proposed for G. macrorhynchus by Nishiwaki (1965, in Japanese), when presence of this species

was yet not established in Japanese waters Japanese whalers distinguished two forms of “pilot whales” segregating to the south and north with the boundary at around Choshi Point (35°42′N, 140°51′E) on the Pacific coast of Japan and called the northern one tappa-naga and the southern one ma-gondo, but we did not have a suitable name for the whole species G. macrorhynchus, which was later known to include these two forms off Japan The two vernacular names are still used in Japan for the two geographical forms of the species off Japan (Section 123) and remain as candidates for Japanese common names for them in case in the future the two geographical forms may be recognized as separate species They are distinguished in English as “northern form” and “southern form” respectively

The Japanese words gondo and goto probably mean a large robust head (Otsuki 1808, in Japanese; Hattori 1887-1888, in Japanese), and names such as gondo-kujira, goto-kujira, naisa-goto, ma-gondo, and shio-goto have been used for the short-finned pilot whale or for one of the two geographical forms of the species There are other examples of Japanese common names, including gondo: the Risso’s dolphin (hana-gondo) and the false killer (okigondo, oki-goto, dainan-goto, or o-onan-goto) These species also have robust heads The finless porpoise also has a round robust head and is called ze-gon or ze-gondo in the western Inland Sea, including Hiroshima Prefecture (Section 81) Other Japanese names, nyudo-iruka and bozu-iruka, were also used in various locations for the false killer whale or short-finned pilot whale (Sections 31, 37, 382, and Kasuya and Yamada 1995a, in Japanese) Both nyudo and bozu mean Japanese Buddhist monk, who usually has a shaved head, and iruka means dolphin or porpoise in Japanese

attains a body length of 4-7 m, and has a drum-shaped round head and a broad fan-shaped dorsal fin Okura (1826, in Japanese) described the fin as amigasa-hire, misprinted as ashigasa-hire in the reprint version of 1886, which has no meaning Amigasa is a basketry helmet of varying type that was worn perhaps until the mid-nineteenth century by either sex to remain unidentified in the street or to avoid strong sunlight Hire means fin The large dorsal fin and rounded head are distinct when a school of short-finned pilot whales is met in the ocean These two characters are indistinct on newborns, which have a dorsal fin only slightly broader than that of common dolphins and a head which is shaped like that of the Pacific white-sided dolphin or killer whale (Yonekura et al 1980) The head of the newborn short-finned pilot whale has a slender melon and a short beak projecting beyond the melon With growth the melon swells in three directions, that is, anteriorly, laterally and dorsally, and gradually covers the rostrum On southern-form individuals off Taiji (33°36′N, 135°57′E) the melon covers the rostrum at age 2-7 years or at body length 27-30 m and the head becomes barrel-shaped Development of the melon is particularly pronounced on adult males of the southern form, with the front end of the melon becoming flat as a drum (Figure 127) As short-finned pilot whales live in a school of 15-50 individuals of both sexes of various growth stages, including adult males, the form can be easily identified at a large distance, except in waters where both forms are expected

The English language “black fishes” includes not only the two species of Globicephala but also other species such as false killer whales, pigmy killer whale, melon-headed whales, and probably Risso’s dolphins Most of the pilot whale’s body is black, with various degree of pale portion behind the dorsal fin, posterior-dorsal area of eye, and ventral area from throat to anus This pale pigmentation becomes darker with postmortem time

The three pale areas are present on both species of Globicephala but are indistinct in neonates and become more distinct with growth (Bloch et  al 1993b) The shape and degree of distinctness of the pale patches show geographical variation and may be useful for identification of populations within a species However, caution is required in identifying the two species of Globicephala by pigmentation, because the geographical variation in pigmentation within a species can be of such degree that it is comparable to difference between the two species within the genus Also, the pigmentation may change with growth

The northern form of short-finned pilot whale off Japan has a broad saddle mark with distinct white pigmentation, and the southern form has only an indistinct slender saddle mark (Section 123; Figures 122 and 123; Kasuya et al 1988), but similar kinds of geographical variation possibly exist among long-finned pilot whales Davies (1960) reported that the saddle mark was common among long-finned pilot whales in the Southern Hemisphere but rare on the same species in the North Atlantic and proposed to deal with them as different subspecies Bloch et al (1993b) reported for the long-finned pilot whale in the North Atlantic that development of the saddle mark was a

function of age but not of sex A saddle mark was present on 3% of individuals below age 5, 30% at ages 6-10, and 61% at ages over 11 years In my view, the saddle mark identified by Bloch et al (1993b) on the long-finned pilot whales in the North Atlantic was shaped like that of southern-form short-finned pilot whales off Japan Thus, caution is required in analyzing geographical variation of pigmentation in the genus Globicephala

Short-finned pilot whales inhabit tropical and temperate waters of the world The limit of their northern range extends in the North Pacific from around 43°N off eastern Hokkaido

northern limit in the North Atlantic extends from the New Jersey coast (40°N) to the coast of France The Mediterranean Sea is inhabited by long-finned pilot whales and not by shortfinned pilot whales Our information on the southern limit of the short-finned pilot whale is limited, but it is known from Sao Paulo (23°S), the coast of South Africa, west and east coasts of Australia, and the southern tip of the North Island of New Zealand (41°S) (Rice 1998) The South African coast is inhabited by both species (van Bree et al 1978), with the boundary of the two species at around 30°S on the east coast, which is slightly north of Cape Agulhas, and at around 25°S on the west coast, where the cold Benguela Current runs northward Short-finned pilot whales range to the north of these latitudes (Best 2007) Thus, the distribution of the species is currently discontinuous between the Indian Ocean and the South Atlantic

Short-finned pilot whales are not evenly distributed within the range In Japanese coastal waters they are common off the Pacific coast but rare in the East China Sea and the Sea of Japan People around these seas use the word gondo for okigondo [false killer whale] I have only one reliable record of sighting of a school of pilot whales, most likely short-finned pilot whales, in the central Sea of Japan, encountered by myself on the Yamato Bank (38°51′N, 135°00′E) in August 1978 during a cruise of the research vessel Hakuho-maru In relation to the fishery/dolphin conflict in the Iki Island area, the Fisheries Agency requested records of cetacean sightings from vessels operated for fisheries research, fishery inspection, and fisheries education during September 1981 to August 1983, but there were no records identifiable as Globicephala (Nagasaki-ken Suisan Shikenjo [Nagasaki Prefecture Fisheries Experimental Laboratory] 1986, in Japanese) The Far Seas Fisheries Research Laboratory has annually operated cetacean sighting cruises around Japan since the early 1980s and reported the results of small-cetacean sightings to the Scientific Committee of the International Whaling Commission (IWC) until 2000; these cruises did not find pilot whales in the Sea of Japan

Short-finned pilot whales are known from the Okinawa Islands area in southwestern Japan and have been hunted in opportunistic drives at Nago (26°35′N, 127°59′E) (Section 310) The short-finned pilot whale was last driven at Nago in 1982; subsequent take of the species was in the crossbow fishery (Section 28) The products of the crossbow fishery were sent to markets in Osaka (34°42′N, 135°30′E) and Fukuoka (33°35′N, 130°24′E) when the supply of whale meat declined around 1987 due to the moratorium on commercial whaling (Table 15 and Chapter 7)

Short-finned pilot whales seem to be scarce in the main part of the East China Sea and the Yellow Sea Reliable records of the species are limited to two sightings in the Yellow Sea near the west coast of the Korean Peninsula (Wang 1999, in Chinese) and the holotype of Delphinus globiceps obtained off Nagasaki (32°45′N, 129°53′E) in northwestern Kyushu (Section 1231) The species has not been recorded along the East China Sea coast of mainland China Sightings of

the species off Taiwan are limited to the east coast in waters beyond the 1000 m isobath (Chou 1994, 2000, in Chinese; Wang and Yang 2007, in Chinese and English) A mounted skeleton of a short-finned pilot whale in Taiwan National University had a nameplate with the Japanese legend Shimazu Seisakusho, suggesting the possibility that it was imported for educational purposes during the Japanese occupation

The Far Seas Fisheries Research Laboratory has recorded sightings of short-finned pilot whales around Japan during its routine cetacean-sighting cruises since the early 1980s (Miyashita 1993) Sightings of the species were concentrated in the western North Pacific in latitudes 22°N-43°N, east of the Southwestern Islands of Japan, which lie between Taiwan and Kyushu and contain the Okinawa Islands, and west of 155°E Short-finned pilot whales are also known from the Hawaiian Islands area as well as off the west coast of North America, but these habitats are apparently discontinuous from the concentration in the western North Pacific off Japan (Figures 124 and 125)

In this section some details will be given on the two forms of short-finned pilot whales off Japan, where the “northern form” indicates a particular population of short-finned pilot whales inhabiting Pacific waters off northern Japan and the “southern form” a population in waters to the south The eastern extent of these populations has not yet been fully determined Although pilot whales similar to them may inhabit waters further east in the North Pacific (Section 1237), their

Japanese populations

First I will describe the long history of confusion in the taxonomy of the genus Globicephala in Japan It was in 1758 when Linnaeus published the first volume of the 10th edition of Systema Naturae, which became the basis for modern animal taxonomy in Europe Shortly after this date, in 1760, Harumasa Yamase published a book in Osaka titled Geishi [Natural History of Whales], which illustrated with descriptions 7 baleen and 6 toothed whale species found in his country in feudal times called Kii or Ki-shu, or the present Wakayama Prefecture (33°26′N-34°19′N, 135°00′E-135°59′E) He lived in the present Wakayama City (34°14′N, 135°10′E) and was also called Jiemon Kandoriya Prior to this publication, Gensen Kanda in 1731 wrote a book Nitto Gyofu [Illustrated Fishes of Japan], but it was not published Although he also listed the same number of species, the list of species was different and the drawings and descriptions were inferior to those of Yamase (1760, in Japanese) Species attributable to present-day blackfishes are  one species-goto-kujira-of Kanda and three speciesnaisa-goto, shiho-goto, and ohonan-goto-of Yamase Although the name goto-kujira of Kanda likely represented pilot whales, the drawing and description were totally confusing and thus it seems less reliable to me Of the three species of Yamase, the first two were described as “upper jaw covers the lower jaw,” while the third species ohonan-goto was described as having “both jaws meet,” which is different from the first two species Therefore, now ohonan-goto is thought to be the false killer whale (also see the following text in this section for my personal observation at Taiji in Wakayama Prefecture) and naisa-goto and shiho-goto to be some member of the genus Globicephala Yamase also stated that the shiho-goto had a cloud-shaped, that is, irregularly shaped, white patch behind the dorsal fin, but that the naisa-goto did not (Figure 126)

A long time after the publication of Yamase (1760, in Japanese), around 1827 Jubei Kuroda wrote a book titled Suizoku-shi [Natural History of Aquatic Animals], which was published posthumously in 1884 His book listed nagisa-gondo, shiho-gondo, dainan-gondo, and oho-uwokui as species attributable in my view to the current blackfishes The ohonan-goto of Yamase and dainan-gondo of Kuroda seem to represent the same species, that is, the false killer whale, because oho and dai have the same meaning of “large” or “great” The Oho-uwokui [great fish eater] of Kuroda is described as having a “slender body” of “length of 3-45 m,” and being “black in color”; it also seems to represent the false killer whale, although Kuroda did not so state

Almost in the same year when Kuroda wrote his book, around 1827 (published in 1884), Tsunenaga Okura in 1826 published a book Joko-roku [Leafhopper Control] with the intent of teaching Japanese farmers how to control leafhoppers in their rice paddies using whale oil Whale oil was used widely in those days for pest control in rice paddies (Section 13) His book listed 11 species (5 baleen and

6  toothed whales) of cetaceans with drawings and text, together with description of the quality of whale oil available from those species His book contained a drawing attributable to Globicephala, particularly to the southern form short-finned pilot whale, with the name koto-kujira He listed shiho-goto, nai-goto, dainan-goto, and ohonan-goto as synonyms of koto-kujira, but it seems to me that the last two names should be attributed to the false killer whale, which was shown by him with a drawing and the name oho-iwokui

Nihon Hogei Iko [Miscellanea of Japanese Whaling] by To-oru Hattori (1887-1888, in Japanese) stated that ohoiwokui and oki-goto were used in Wakayama Prefecture for the same species and gave a drawing that was similar to a drawing labeled oho-iwokui by Okura (1826, in Japanese)

He stated that the drawing was a copy from a whaling document of Atawa Village (33°48′N, 136°03′E) in Wakayama Prefecture

These records suggest that there were three series of vernacular names for the false killer whale, that is, (1) ohonangoto and dainan-goto, (2) oki-goto and oki-gondo, where oki means “offshore,” and (3) oho-iwokui and oho-uwokui, which mean “large-” or “great-fish eater” I observed in Taiji in the 1970s that both oho-iwokui and oki-goto were used for okigondo, which meant false killer whale

With cooperation of his students, Von Siebold brought whale specimens as well as their Japanese names that appeared in Geishi (Yamase 1760, in Japanese) to Europe (Ogawa 1950, in  Japanese) Temminck and Schlegel (1844)

identified a skull of a young pilot whale, 165  cm in body length, obtained by Siebold in Nagasaki with the Japanese name naisa-goto, as the same species as pilot whales in the northern North Atlantic (current G. melas) and used the name Delphinus globiceps for it They also stated that there was another species called siho-goto in Japan Later, Gray (1846) concluded that the Nagasaki specimen was different from the species in the northern North Atlantic and gave it a new name Globicephalus siebodii, and at the same time gave the name Globicephalus chinensis to a species said to inhabit the Chinese coast Gray (1871) further proposed another species name Globicephalus sibo for a species called sibo-golo in Japan At this stage he made two typographic errors, that is, changing siho to sibo and goto to golo According to Dall (1874, in Scammon 1874), another species of pilot whaleGlobicephalus scammoni (Cope, 1869)—was described based on a skull collected off California Thus, there have been a total of four species described by modern taxonomists for the genus Globicephala in the North Pacific

After the Meiji Revolution (1864-1871), modern zoology flooded into Japan, and Japanese biologists started their efforts to match existing Japanese species names to the imported scientific names Cetacean biology was not the exception but progressed at a slower pace than other zoological fields due to difficulties in accessing specimens and information In the early twentieth century, R C Andrews was sent to Japan by the American Museum of Natural History in New York and collected specimens of large cetaceans at Japanese whaling stations He found that Japanese whalers were still hunting gray whales, which had been thought to be extinct, on the Korean coast, and published a monograph on the species (Andrews 1914a) He also obtained a pilot whale at Ayukawa (38°18′N, 141°31′E) on the Pacific coast of northern Japan and used the name Globicephala scammoni for it (Andrews 1914b) Although he did not mention the basis for this conclusion, he must have considered the Ayukawa specimen to be the same species as pilot whales off California and apparently ignored Globicephalus sieboldii of Gray (1846) The Japanese zoologists Nagasawa (1916, in Japanese) and Kishida (1925, in Japanese) followed Andrews (1914b), but the latter cautiously stated that he would use the scientific name for the time being until the relationship between the scientific name and Japanese common names siho, naisa, and ohonan would be clarified (Kishida 1925, in Japanese) Taxonomy should be based on specimens, but that was not done by them

While he was studying the brain anatomy of cetaceans, Teizo Ogawa of the Tokyo Imperial University (later renamed Tokyo University) noticed unresolved problems in the taxonomy of small cetaceans around Japan and collected taxonomic materials from northern Kyushu, Taiji, and the Sanriku Region (Pacific coast of northern Honshu in latitudes 37°54′N-41°35′N, where Ayukawa is located) (Ogawa 1950, in Japanese) Although he made a great contribution to the taxonomy of Japanese Delphinidae, he did not apparently complete his work on taxonomy of the genus Globicephala off Japan He obtained a 236 cm juvenile pilot whale at Shiogama (38°19′N, 141°01E) on May 28, 1935 He identified it as Globicephalus melas (Traill) with the Japanese names naisa-goto and magondo, and he further stated that he would tentatively deal with G. melas as a synonym of G. sieboldii Gray, which he believed to be very closely related (Ogawa 1937, in Japanese) In the same article Ogawa stated that he obtained two specimens of Globicephalus scammoni at Ayukawa and gave them the Japanese name shiho-goto and tappa-naga It is probable that he had difficulty identifying the pigmentation pattern of those specimens due to postmortem change It seems to me that Ogawa, as an anatomist, attached great importance to the morphology of individual specimens and ignored the possible range of individual variation and the zoogeography of animal species The three Ogawa specimens collected in northern Japan were deposited in the National Science Museum in Tokyo and later identified as Globicephala macrorhynchus by Kasuya (1975) (see the following text in this section) Although it has not been confirmed, the collection locality of

belonged to the northern form

After Ogawa (1937, in Japanese), an erroneous concept became generally accepted in Japan, which was to assume the scientific name G. melas applied to pilot whales inhabiting southern waters from Chiba Prefecture (in latitudes of 34°55′N-35°44′N) to the Okinawa Islands (in latitudes 24°N-27°N) and locally called naisa-goto or ma-gondo, and to use G. scammoni for those inhabiting waters north of Chiba and locally called tappa-naga or shio-goto This meant that G. melas, which inhabits the North Atlantic in latitudes from 35°N to 70°N, was thought to live in the western North Pacific south of 35°N, where the warm Kuroshio Current prevails I remember one day in 1961-1964 when the late H Omura of the Whales Research Institute expressed at lunchtime his doubt about the taxonomy of Japanese pilot whales by pointing out this zoogeographic contradiction

In 1950, F C Fraser published the result of his osteological study on the genus Globicephala, concluding that the genus contains only the two species G. melas (Trail, 1809) and G. macrorhynchus (Gray, 1846), and that the latter name is a senior synonym of G. scammoni Then the late M Nishiwaki of the Ocean Research Institute started a US-Japan cooperative study on cetacean fauna in the North Pacific The project collected pilot whale specimens from the drive fishery at Arari (34°50′N, 138°46′E) and small-type whaling based at Taiji and Ayukawa, and concluded that all the pilot whales examined were G. macrorhynchus and that there was no trace of G. melas (Nishiwaki et  al 1967, in Japanese). This resolved one basic question on the taxonomy of pilot whales in Japanese waters

One of the remaining problems was the identity of G.sieboldii As this species was based on the skull of a young animal, characters of the species were indistinct, but Van Bree (1971) was able to conclude that this specimen belonged to G. macrorhynchus During the process of identifying skulls of long-finned pilot whales, G. melas, excavated from archaeological sites in Japan, I examined all the pilot whale skulls in the National Science Museum, which included Ogawa’s specimens, and confirmed that they were G. macrorhynchus (Kasuya 1975)

The pilot whale specimens used by Kasuya (1975) included a skull collected by M Nishiwaki and R L Brownell in the early 1960s at Ayukawa It seemed to me to belong to the short-finned pilot whale, but the size was extraordinary, larger than any pilot whale ever previously collected at Taiji or Arari I failed to pursue this problem, but it was later investigated by Miyazaki and Amano (1994) (Section 12375)

There still remained another question on the taxonomy of Japanese pilot whales Yamase (1760, in Japanese) listed two species of pilot whales, and Japanese modern whalers also had a similar conception In a study on long-finned pilot whales excavated in Japan, I analyzed the Monthly Report of Whaling Operation for the years 1949-1952, which was presented by small-type whalers to the Fisheries Agency, to see

whale in northern Japan I concluded from the zoogeographical point of view that the pilot whale called tappa-naga by small-type whalers must be the short-finned pilot whale and cannot be the long-finned pilot whale (Kasuya 1975)

This conclusion was correct, but it was a mistake to assume that the same individuals that wintered south of Chiba Prefecture would migrate in summer to the Sanriku coast The main target of Japanese small-type whaling was not pilot whales but minke and Baird’s beaked whales Therefore many, but not all, of these whalers migrated seasonally following movements of the main target species Those who recorded a peak pilot whale catch in early summer off Taiji were likely to have moved northward to reach the Sanriku coast in August and recorded another peak pilot whale catch in summer This apparent shift in peak pilot whaling grounds did not in reality indicate movement of the pilot whales Small-type whaling was allowed to take minke whales and toothed whales other than the sperm whale using a whaling cannon of less than 50 mm caliber and a vessel of less than 30 gross tons (later modified to 50 gross tons) (Chapter 4; Sections 54, 55, and 71; Ohsumi 1975) Ogawa also obtained his cetacean samples from such vessels

Initially I overlooked or misunderstood some information from small-type whalers (Kasuya 1975) While I was analyzing catch statistics of small-type whalers, I interviewed exwhalers in Taiji who hunted small cetaceans and asked what the tappa-naga and ma-gondo looked like Their answers and my interpretation are summarized as follows The word tappa-naga means “long flipper” and ma-gondo “the correct pilot whale”

1 “Generally speaking tappa-naga is larger than magondo” The whalers did not pay attention to the sex Males of the short-finned pilot whale grow to about 25% larger than the females So I thought that if pilot whales segregated by sex it would explain the geographical size difference This interpretation was not supported by data obtained later

2 “Tappa-naga has a longer flipper than ma-gondo.” Whalers did not clarify whether the difference was proportional or in absolute length It was later found that the latter was the case

3 “Tappa-naga is skinny and contains less oil than ma-gondo” This could be due to either seasonal physiological fluctuation or a population difference Later it was found that the latter was the case

It was in 1982 that the small-type whalers resumed hunting tappa-naga off Ayukawa, and the questions given earlier were resolved

Hereinafter I will refer to the two types of short-finned pilot whales off Japan, tappa-naga and ma-gondo, by our current English terminology of “northern form” and “southern form,” respectively It was in June 1975 that I saw a school of pilot

Research Institute, University of Tokyo, on a northbound cruise toward the Sanriku coast Approaching the school for further observation, we noted the white saddle patch, and both my colleague N Miyazaki and I were astonished by the beautiful patch shining in the sun In 1982, I was occupied with studying short-finned pilot whales taken in Taiji Every time I heard that Taiji had driven a school of pilot whales, I got on a night train and arrived at Taiji harbor early the next morning, examined carcasses the whole day, and got on the returning night train to Tokyo with samples in formalin The fishermen usually slaughtered all the whales in a school in a day if it contained around 20 or fewer animals, but they spent 2 or 3 days for larger schools The short-finned pilot whale I was examining at Taiji was called ma-gondo by fishermen, which is the “southern form” in our current terminology, and they did not have as distinct a saddle patch as I had seen in northern Japan in 1975 So I suspected that the pilot whales with a bright saddle patch were the shiho-goto of Yamase (1760, in Japanese) and tappa-naga of recent whalers and waited for the opportunity to examine them in detail

Such an opportunity occurred in October 1982 when I was examining southern form short-finned pilot whales at Taiji T Isone, a gunner captain of a small-type whaling vessel in Taiji, told me that several small-type whalers at Ayukawa had started hunting pilot whales off the Sanriku coast They used to operate on minke whales and made some additional catches of Baird’s beaked whales, but they resumed taking pilot whales in order to compensate for a diminishing minke whale quota under international regulation Since I was occupied with the task in Taiji, I called N Miyazaki of the National Science Museum and advised him to examine the pilot whales being landed at Ayukawa I told him that they could be the type of whales that we had encountered several years ago at sea With the cooperation of whalers in Ayukawa, Miyazaki examined their catch and returned to Tokyo with several

studies on osteology (Miyazaki and Amano 1994) and food habits (Kubodera and Miyazaki 1993)

On returning to Tokyo after the work in Taiji, I visited Miyazaki for an update He told me that the northern form which he examined at Ayukawa was easily distinguished from the southern form by a distinct saddle patch I was very impressed by the size and shape of several heads that had just been delivered on a truck while I was in his office The heads of both sexes were greater than those of adult males of the southern form, but the shape of the melon of the adult male was more like that of adult females or immature males of the southern form The front contour of the melon is flat and square-shaped in adult males of the southern form if seen from the dorsal or ventral side, but the heads in front of us did not have such a shape (Figure 127) Another morphological difference between the two forms I noticed in subsequent years in Ayukawa is in the shape of the dorsal fin In profile the front edge of the dorsal fin of the adult male southern form is expanded (Section 1212), but this is less distinct in the northern form In short, some of the secondary sexual characters other than body size are less pronounced in the northern form than the southern form Some of these findings were reported by Miyazaki (1983, in Japanese)

Concerning the secondary sexual characters of the shortfinned pilot whale, Y Toba, owner of a whaling vessel in Ayukawa, told me in 1983 about the following interesting experience of his gunner in the 1982 season This was the year when hunting of the northern form resumed On one day of the season the whalers encountered a school of southernform whales and took some of them From the shape of the dorsal fin the gunner believed that the whales he took would be of great size but was greatly disappointed when he was informed at the port that his catches were less than 5 m long A full-grown southern form male measures only 467 m on average (Table 121) This was the only take of southern-form

whales recorded in the whaling operation off Sanriku coast in the 1982-1996 seasons when I was able to directly monitor the operation I felt it interesting that Ayukawa whalers did not know about southern-form pilot whales, which indicated that the type was uncommon in northern waters

The question remains whether the northern form has ever been taken by dolphin fisheries off the coasts of the Izu Peninsula (34°36′N-35°05′N, 138°45′E-139°10′E) and Wakayama Prefecture Yamase (1760, in Japanese) described cetaceans taken in eighteenth-century whaling at Taiji and nearby Koza (33°31′N, 138°49′E), both in present-day Wakayama Prefecture, and listed naisa-goto and siho-goto, which are attributable to the southern and northern forms, respectively (Figure 126) This suggests past incidents of the northern form occurring off the Wakayama area, although the frequency is unknown If this was the case, the northern form could have also occurred off the Izu Coast, which is located between Sanriku and Wakayama However, I have not positively identified northern-form whales by external morphology among over 500 carcasses of both sexes of pilot whales examined at Taiji and Arari during 1962-1984 (Kasuya and Marsh 1984; Kasuya and Tai 1993), except for one ambiguous individual This was a male in a group of southern-form whales driven at Taiji and had a body length of 58 m and weight of a single testis of 17 kg Although these figures were reasonable for the northern form, the body size was too large and testis weight rather small for adult southern-form individuals, which have maximum body length of 52 m and testis weight in the range of 17-30 kg No additional information (eg, pigmentation and age) was available for this large male (Kasuya et al 1988)

In April 1983, I moved from the Ocean Research Institute of the University of Tokyo to the Whale Resources Section of the Far

as a project leader The task given to me included studying the biology and abundance of the northern-form short-finned pilot whale for fishery management I was extremely interested in comparing its life history with that of the southern form Because such a study was necessary for management, I requested a budget for the Fisheries Agency, but it was not forthcoming So, as is usually the case for university scientists, I proposed to use my personal fund for the project This seems to have caused a problem for the administration people in the laboratory Finally the Whaling Section of the Fisheries Agency persuaded the Japanese Association of Small-Type Whaling and the Japanese Whaling Association to pay the cost of my travel and an assistant, which I appreciated greatly The dependence on the industry continued for several seasons before the government became able to pay the full cost of the activity Summarized in the following are differences between the two forms of short-finned pilot whales, including results obtained through the project and other activities

12.3.5.1 Pigmentation The saddle patch in the northern form shows broad individual variation, but is generally broader (dorsal-ventral width) and more distinct than that of the southern form The posterior margin of the saddle patch is distinctly separated from the dark pigmentation of the dorsal area, and the margin extends anteroventrally with a more acute angle than in the southern form Thus, the ventral-dorsal width of the patch is greater and its anterior-caudal length is shorter in the northern form Compared with that of the northern form, the saddle patch of the southern form extends posteriorly beyond mid-length of the tail peduncle, the color is darker and indistinct, and the color fades into the dark pigmentation of the tail peduncle Although the eye patch seems to be slightly more distinct in the northern form, it cannot be used to differentiate between the two forms The saddle patch is not evident on neonates of the northern form but is distinct on 15-year-old juveniles (Kasuya et al 1988)

12.3.5.2 Shape of the Head Adult males of the southern form have a well-developed melon In profile it appears as a round protuberance beyond the tip of the upper jaw, but if seen from the top or bottom the front contour it is almost flat or slightly concave and the lateral corners are square-shaped This is different from females of the southern form and from adults of both sexes of the northern form (Figure 127) Thus secondary sexual characteristics of the melon are more distinct in the southern form

12.3.5.3 Shape of the Dorsal Fin The dorsal fin of the short-finned pilot whale becomes broad among adult males of both forms, but this secondary sexual character is more pronounced in the southern form

12.3.5.4 External Proportions Kishiro et al (1990, in Japanese) compared mean measurements of external proportions between 119 northern-form and

Mean Body Length of Two Forms of Short-Finned Pilot Whales off Japan

ence in two measurements: (1) mean distance from anterior end of the head to the blowhole measured along the body axis was slightly smaller among northern-form whales (males 82%, females 94%) than in the southern-form whales (males 95%, females 110%), and (2) mean distance from anterior insertion of the flipper to the center of the genital aperture (also measured parallel with body axis) was slightly greater in northern-form (males 418%, females 496%) than southernform whales (males 389%, females 450%)

Other measurements of the head region showed a similar trend, although the differences were not statistically significant This indicates that the northern form has a relatively shorter head and longer trunk Relative flipper length did not differ between the two forms Mean body length at several growth stages is compared between two forms in Table 121 The northern form has on average about a 30% greater body length than the southern form at the same growth stage Fully grown northern-form whales are 17-18 m (males) and 1 m (females) greater than southern-form whales

12.3.5.5 Skull Miyazaki and Amano (1994) compared proportions of adult skulls between northern and southern forms of the same sex, as is detailed in Section 12375 This analysis showed that the northern form had a proportionally broader rostrum and cranium compared with the southern form Their multivariate analysis of 32 skull measurements with independent variables of form and sex clearly separated the forms and sexes but was mostly influenced by difference in skull size

12.3.5.6 Body Weight Body weight has not been measured for the northern form The following relationships were obtained between body weight (W, kg) and body length (L, cm) of southern-form whales landed at Taiji

Fetuses (L ≤ 125cm): Log W =28772 log L + log 2432 × 10-5

Postnatals (275cm ≤ L ≤ 400cm): Log W = 26642 log L + log 8403 × 10-5

Since these equations were very similar, the two sets of data were combined to obtain the following equation (Kasuya and Matsui 1984),

All data (125cm ≤ L ≤ 400cm): Log W = 28873 log L + log 2377 × 10-5

This equation can be expressed also as W = 2377 × 10−5 L28873 This is compared with the following weight-length relation obtained for the long-finned pilot whale in the North Atlantic

G. melas: W = 000023 L2501, Bloch et al (1993a)

Using this equation fitted to all data for short-finned pilot whales, average body weights of the southern and northern

forms are estimated in Table 122 The northern-form neonates weigh about twice as much as those of the southern form and the adults about 2-25 times as much

The northern and southern forms have minor differences in their body proportions and shape of the melon, and a question may arise whether the combined equation is appropriate for both forms However, cetaceans exhibit large fluctuation in body weight reflecting seasonal changes in physiology or reproductive status For example, females accumulate lipids in their body during pregnancy and those in near-term pregnancy may weigh more than lactating females Because such fluctuation is ignored in the equation given earlier, body weight estimated from body length must be considered imprecise, and the effect of morphological difference on the estimated body weight of two forms can be ignored

12.3.5.7 Meat I did not pay much attention to the assertion by the whalers that the northern form has less oil, because oil content can vary seasonally and with physiology of animals However, it was very evident on the flensing platform that the amount of adipose tissue in the muscle was in general much less in the northern form than the southern form This difference was particularly distinct in adult males Males of the southern form have lipid-rich “tail meat,” but males of the northern form do not The “tail meat” in Japanese whaling anatomy means a particular part of the skeletal muscle on the tail peduncle Cetaceans have a total of four large muscle columns, with two columns above and two below the transverse processes of the dorsal and lumbar vertebrae Japanese whalers call the former se-niku [dorsal muscle] and the latter hara-niku [ventral muscle] The muscle above the transverse processes of the caudal vertebrae divides into two columns: upper and lower

Body Weight of Two Forms of Short-Finned Pilot Whales off Japan Calculated Using Single Length-Weight Equation (see text)

whaling anatomy The muscle of the tail meat contains thin layers of adipose tissue between layers of muscle tissue and is preferred by consumers However, similar structure may be found also in the dorsal or ventral muscles of well-nourished whales such as fin whales in near-term pregnancy In such cases the muscle can be classified commercially as “tail meat” Therefore whalers may say “I caught a whale full of tail meat” or “Minke whales usually have no tail meat”

Both forms of the short-finned pilot whale have the tail meat of whaling anatomy, but tail meat of commercial significance is limited to the tail part of adult males of the southern form, which is flavorful as sashimi [sliced raw meat], although it smells slightly strong and looks dark The tail meat of the northern form, even of the adult male, does not have the structure of tail meat in commercial terms, with the exception of thin muscle a few millimeters thick near the vertebrae This could be one of the reasons why the northern form has lower commercial value relative to body size

A difference in fat content was evident between the two forms of short-finned pilot whale taken in the same season, that is, September to November It is known that longfinned pilot whales in the North Atlantic accumulate lipid in autumn and winter, when they weigh 14%–23% more than in summer (Lockyer 1993) I was not able to identify such seasonal variation in physiology while I studied southern-form whales during 8 months of the year (Kasuya and Marsh 1984) or northern-form whales in 3  months of the year, September-November (Kasuya and Tai 1993) We have insufficient data to allow us to see seasonal change in nutrition in the northern form

The warm Kuroshio Current has its origin in an area east of Luzon Island in the Philippines, runs along the east coast of Taiwan, and reaches the east coast of Honshu in Japan It turns to the east at around Choshi Point to be called the Kuroshio Extension and then the North Pacific Current, and finally reaches the west coast of North America Inside, or on the right side, of this clockwise semicircle of the Kuroshio and the Kuroshio Extension, there is a clockwise current called the Kuroshio Counter Current, which flows back toward the Kuroshio Current in the western North Pacific The known range of the southern form short-finned pilot whale is within the area of the Kuroshio and the Kuroshio Counter Current system The range of the northern form is limited to a smaller area bounded by northern Honshu and Hokkaido to the west, the nutrition-rich cold Oyashio Current to the north and northeast, and the front of the Kuroshio and Kuroshio Extension to the south This area has an intrusion of an additional weak warm current called the Tsugaru Current in the northwestern corner (Figure 128) These currents create the habitat of the northern form as an area of high productivity, but they also make it an area of drastic seasonal change in the environment In the summer the sea surface temperature rises to 18°C off Kushiro (42°59′N, 144°23′E) near the northern boundary of

5°C, and sometimes ice floes can be seen Thus, the sea surface temperatures ranged from 8°C to 23°C at the position of sightings of northern form whales, including some schools only suspected to be of the northern form (Table 123)

Sea surface temperature in the habitat of the northern form fluctuates with seasonal fluctuation of the two major currents (Kuroshio and Oyashio) as well as with solar radiation and wind, but the temperature of deeper water is more stable seasonally Therefore, a water temperature of 15°C at a depth of 100 m has been used as the indicator of the position of the Kuroshio Front (Kawai 1972), which is stable seasonally at the latitude of Choshi Point Similarly, a water temperature of 5°C (spring) or 8°C (autumn) at 100 m has been used as an indicator of the Oyashio Front, which is located in summer near Kushiro and in winter on a line extending from the Tsugaru Strait (41°30′N, 140º30′E) to the south-east The northern limit of the northern form in summer almost agrees with the Oyashio Front and the southern limit with the Kuroshio Front in all seasons of the year (Figure 128)

The northern form makes maximum use of productivity of the area by expanding its range up to the front of the cold Oyashio Current in summer, and in winter it shifts its northern range down to the coast of Miyagi Prefecture (37°54′N-38°59′N) to avoid very low surface temperatures (Figure 128) However, it does not cross the Kuroshio Front to go further south in any season The Kuroshio and Oyashio Currents often function to limit distribution of small cetaceans off Japan Dall’s porpoises and perhaps harbor porpoises usually remain in summer to the north of the front of the cold Oyashio Current and may extend their range in winter further south, where surface water becomes colder, but they do not usually cross the Kuroshio Front even in winter (Section 931) The southern-form pilot whale may extend its range to 37°N (Figure 128) and striped dolphins to 40°N (Section 1042), between the Kuroshio Front (c. 34°N-35°N) and the summer front of the Oyashio Current (c. 43°N-44°N), but they retreat to south of the Kuroshio Front in winter (Miyashita 1993) The difference in the northern limit of the summer range between the two species probably reflects their differential dependence on deep water for feeding Striped dolphins feed probably at lesser depths than southern-form pilot whales; thus their summer range responds more directly to expansion of warm surface waters

Sea surface temperature at sightings differs between the northern and southern forms around Japan (Table 123) The temperature boundary between the two forms is at 24°C in summer Insufficient data suggest that it is around 17°C-19°C in winter Small-type whalers in recent years hunted northern-form whales in September through November and within a surface temperature range of 12°C-21°C, with a peak at 16°C-17°C This suggests that northern-form whales do not usually enter surface water of 10°C-15°C, which is the southern boundary of the cold Oyashio Current in that season (Kasuya et al 1988)

Both the northern and the southern forms undergo seasonal north-south shifts in their habitats This functions to

decrease seasonal change in their environmental temperature, but the degree of movement is insufficient to keep them in a particular temperature environment It appears to me that their strategy is to minimize seasonal movement within their range of temperature tolerance Since this strategy is more pronounced in the northern form that inhabits colder waters, it is likely to have a greater tolerance for a cold environment

Hibernation is one of the ways adopted by mammals to cope with scarcity of food or low temperature; they lower

body temperature and minimize activity in a den to decrease energy consumption until a season of high productivity arrives They spend winter in a half-dead condition without significant growth and usually without reproduction Cetaceans live in water and are unable to hibernate Another way to cope with cold is to maintain body temperature constant with improved thermal insulation and perhaps increase heat production that relies in part on nutrition stored in the body Cetaceans have lost body hair for insulation because

the maintenance of hair requires considerable cost and the insulation efficiency is extremely limited in deep water under high pressure Thus, their thermal regulation must depend on control of heat loss through control of blood circulation, lipid deposited in the blubber, and heat production, which is a function of body size Long-finned pilot whales are known to increase lipid deposition in the blubber during autumn and winter (see Section 12357; Lockyer 1993) This functions as nutrition storage as well as for insulation Larger body size also functions to increase heat production and to decrease relative heat loss by decreasing body surface relative to weight

Body temperature of mammals is maintained by heat produced by muscles and internal organs Thus heat production is proportional to body weight if body structure is constant If body structure and external temperature are constant, heat loss is proportional to the body surface Body weight is proportional to the cube of body length if the body shape is constant, while body surface is proportional to the square of body length In other words, body surface per body weight is in inverse proportion to body length The average body lengths of neonates of short-finned pilot whales, which are more sensitive to lower temperature than adults, are 185 cm in the northern form and 140  cm in the southern form (Section 12431) This means that body surface per body weight of the northern-form neonate is only 76% of that of the southern-form neonate, which suggests greater tolerance of the northern form to low environmental temperature This

is probably an adaptation by the northern form to the colder northern environment, which possibly offers a benefit of high productivity

Kasuya and Tai (1993) estimated the degree of resistance to a cold environment acquired by the northern form Many mammal species maintain body temperature in a narrow range, except in the case of hibernation If heat production increases through high activity, cetaceans increase heat dumping from the fins by increasing blood flow, and if heat production decreases or heat loss increases, they decrease blood flow to the body surface and increase retrieval of heat through a counter-current system of arteries and veins (Berta et  al 2006) However, if the environmental temperature goes below a critical temperature (Tl, °C) for the individual and maintaining body temperature at normal level (Tb, °C) becomes difficult, the individual will increase heat production to keep body temperature at a normal level Shivering is one such response Peters (1983) proposed the following equation among Tl, Tb, and body weight (W, kg):

Tl = Tb − 146W0182

The metabolic rate of cetaceans is probably the same as that of land mammals Their normal body temperature is 36°C-37°C (Gaskin 1982) Applying this body temperature and the neonatal body weights of short-finned pilot whales in Table 122 in the equation presented earlier, the critical environmental

Sea Surface Temperature (SST, in Celsius) at the Position of Sighting of Short-Finned Pilot Whales in the Western North Pacific

whales is estimated at 33°C-43°C and that of the southern form at 78°C-88°C The critical environmental temperature of newborn northern-form whales is 4°C-5°C lower than that of southern-form neonates

The equation of Peters (1983) is influenced by epidermis and subcutaneous fat, and the derived critical environmental temperature can vary by season in the same individuals Even if validity of the absolute figures for the estimated critical environmental temperature is questioned, the 4°C-5°C difference between the two forms of short-finned pilot whale is real

Parturition in the northern form is believed to be limited seasonally, mostly occurring in roughly a 4-month period from November to February The average sea surface temperature at the northern limit of the population in this season is around 12°C (Figure 125; Kasuya et al 1988) On the other hand, parturition can occur any time of the year in the southern form, with a peak period extending for 8  months from April to November The mean sea surface temperature at the northern limit of the southern form is about 24°C in summer and 18°C in winter Thus, the sea surface temperatures met by newborns of the two forms can differ by about 6°C, which is almost the same as the difference between the estimated critical environmental temperatures It is likely that selection has worked toward augmentation of body size of neonates during evolution toward that of the current northern form

Since body size of the mother is expected to have a positive correlation with that of the neonate, selection pressure could also have worked toward augmentation of female body size This would also influence the body size of males because many genes controlling body size are on the autosomal chromosomes The larger body size thus achieved contributes to increase in capacity for storage of nutrition and to reduction of heat loss, which both benefit life in colder waters and in an environment of seasonally fluctuating food supply Such selection will be stronger in populations inhabiting colder area with greater seasonal fluctuation in the environment Seasonal environment change is smaller in the Kuroshio and Kuroshio Counter Current area than in the area bound by the cold Oyashio Current and warm Kuroshio Current and its extension, which the northern form inhabits Thus, there may have been stronger pressure for large body size in the northern form

The next question to be answered is why the northern form has its parturition in a narrow period of the winter months One way of avoiding the disadvantage of parturition in a cold temperature is to have parturition in the summer, but this does not occur in the northern form The breeding season of mammals is controlled by several factors One is the nutritional condition of females, which have to go through estrus, implantation, fetal growth, and lactation A second is choice of a parturition season well suited for the growth and survival of neonates Food availability for nursing females is a key element for the survival of neonates and success of breeding because the energy requirement of lactating females is believed to be greater than that of pregnant females (Lockyer 1981) This explains why many herbivorous animals accumulate food stores in summer, have estrus in the autumn, and produce neonates in early spring

factor for breeding Thus, the timing for switching from milk to solid food must be in a season of best food availability The narrow breeding season of the northern form suggests that their reproductive success has been controlled seasonally more strongly than in the southern form

As pregnancy of short-finned pilot whales lasts about 15  months for both forms, the mating peak is in August to November in the northern form and September to January in the southern form (Section 12441; Kasuya and Tai 1993) Juveniles of the southern form start taking solid food at 6 months of age but continue suckling for a minimum of 25-3 years Although we do not know how long suckling continues in the northern form, the time to start taking solid food will not be different between the two forms because it seems to be a common feature among several toothed whales at age 3-6 months Juvenile northern-form whales probably start switching from milk to solid food in May-August Switching from milk to solid food is important for later growth in juveniles Once they succeed in this process, the importance of suckling decreases rapidly because their solid food is of high nutritional value

Southern-form pilot whales off Taiji consumed only squid, while northern-form whales killed off the Sanriku coasts in early winter ate some octopus and fish in addition to the major food of squid The squid species consumed by the northern form were, in decreasing order, Pacific flying squid (Todarodes pacificus), neon flying squid (Ommastrephes bartramii), and Eucleoteus luminosa (Kubodera and Miyazaki 1993) The Pacific flying squid, the most important food species for the northern form, is distributed in the most coastal waters, and the next important, the neon flying squid, is distributed more offshore Both species feed in summer in Pacific waters off Sanriku and Hokkaido (41°30′N-44′N) and have a southward migration in autumn to the spawning grounds The two squid species are fished off the Sanriku coast; the fishery has a peak catch in August-October Monthly landing of these species in other months of the year has been less than 30% of that in a peak month Thus, the peak of migration of the two most important food species for the northern form matches with the time when juveniles switch their major nutrition from milk to solid food In short, the large neonatal size of the northern form is necessary for the survival of neonates produced in early winter, and placing their parturition season in early winter benefits calves with successful weaning in a squid-rich season Having the mating season in August to November, when the food supply is abundant, also benefits females in successful maintenance of pregnancy and accumulation of food stores for subsequent nursing

12.3.7.1 Background of the Problem In my view, understanding the degree of difference between two animals is a part of biology, but classifying the animals is a product of human culture created for convenience in

characters only in one of two groups of animals in a common habitat Such a case is often interpreted to mean that they have established some mechanism of reproductive isolation, and the two groups are usually dealt with as separate species There might be a case where the habitats of the two animal groups do not overlap, as in the case of the northern and southern forms of short-finned pilot whales off Japan Even in such a case the two forms might be classified as separate species based on discontinuity of characters However, there may be another case where a character found to be discontinuous between two animal groups is of a type that is highly plastic or is only identifiable at a particular growth stage, or where the discontinuity becomes questionable if we assume a third group of intermediate type Difficulty may arise in the classification of such animal groups, as is possibly the case we encounter for the two allopatric populations of the shortfinned pilot whale off Japan

We have generally accepted the current classification of the genus Globicephala to include the two recent species of longfinned (G. melas) and short-finned (G. macrorhynchus) pilot whales by using skull morphology and supplemental external characters These morphological characters result in the classification of the two forms of pilot whale off Japan into the single species G. macrorhynchus Two questions remain: (1) whether there is any basis for dealing with the two forms as different species and (2) what their taxonomic status is if they are to be dealt as of the same species

12.3.7.2 Interpretation of Life History Pigmentation is one of the difference in the external morphology of the northern and southern forms (Kasuya and Tai 1993), but it is too variable within the two species of the genus Globicephala and is unsuitable even for differentiating between the two species (Section 1212)

Body size is the most distinct morphological difference between the two forms of short-finned pilot whales off Japan The northern form grows to about 2 m (males) or 1 m (females) greater than the southern form, or 13-14 times the body length and 25-3 times the body weight of the southern form (sexes combined) (Tables 121 and 122) Short-finned pilot whales in the Indian Ocean are known with body size intermediate between those of the northern and southern forms off Japan (Kasuya and Matsui 1984) Another delphinid species, Stenella longirostris, is known with broad geographical variation in body length, where individuals in one population grow to 14 times greater than those in another population (Perrin et al 1989) Mammals often exhibit large geographical variation in body size, and cetaceans and humans are no exception The body size difference between the northern and southern forms is of a magnitude that is expected between populations within a species

Life history is also a tool for describing the character of certain animal groups Kasuya and Tai (1993) identified common features of life history between the two forms of short-finned pilot whales: (1) females cease reproduction by age 37, (2) females cease ovulation at ages 30-40, and

45 years and the difference in maximum age between sexes is 17 years) Studies by Bloch et al (1993a) and Martin and Rothery (1993) revealed that the long-finned pilot whale in the North Atlantic continues ovulation for life, which is different from the case in short-finned pilot whales off Japan, but there was some degree of similarity with short-finned pilot whales in longevity (female 59 years, male 46) and cessation of pregnancy, with some exceptions, after age 46 Thus, the life history characters of the two forms of short-finned pilot whales off Japan are quite similar and different from those of long-finned pilot whales in the North Atlantic In addition to this, using the similarity in ecological niche occupied by two allopatric forms off Japan, Kasuya and Tai (1993) believed that the northern form of pilot whales off Japan constitutes a population within animals of similar morphological characters in a broader geographical range extending perhaps to the northwest coast of North America and that the two forms of the short-finned pilot whales in the North Pacific should be dealt with as geographically separate races or subspecies

12.3.7.3 Isozymes Compared with morphological characters, which often have problems in quantitative analysis and a risk of being subjective, genetic information can allow objective evaluation of evolutionary distance between animal groups Isozymes have been used as a tool to evaluate genetic difference between the two pilot whale populations Wada (1988) analyzed polymorphisms in 36 enzymes of 204 northern-form and 167 southern-forms pilot whales, and found that 31 enzymes were controlled by a single allele which was common between the two forms but that the remaining 5 enzymes were controlled by 2-3 alleles

One of the parameters he derived from the analysis was genetic distance (D) between the two forms calculated using the frequency of alleles controlling the 36 enzymes The value of D would be zero if genes and their frequency were the same between the two samples and infinite if they completely disagreed The value of D was 00004 for the two samples of pilot whales, which is quite small compared with the genetic distance between the striped dolphin and the pantropical spotted dolphin (D = 0026) or between the sei whale and Bryde’s whale (D = 0047) He noted that if sample size is over 50, the value of D is influenced by the number of genetic loci rather than by the sample size, calculated D assuming a 37th hypothetical locus that differed distinctly between the two samples, and confirmed that the D value was not significantly affected by such an extreme assumption

Another point identified by Wada (1988) was the frequency of alleles of the five polymorphic loci He found that the allele of the highest frequency for each of the five loci was common between the northern and southern forms He noted the allele of the highest frequency for one species would not be the most frequent one for another similar species He interpreted his finding as an indication that the two forms of pilot whales off Japan should be dealt with as a single species and that the distance between the two forms was of a level expected for different subspecies or even less

Miyazaki and Amano (1994) expressed a concern about the samples analyzed by Wada (1988) They accepted the northern-form sample of 204 individuals, which were taken individually by whalers, but had a problem with the southernform sample of 167, in that they would not represent the population because they were obtained from a limited number of matrilineal groups If their concern was justified, the genetic difference calculated by Wada (1988) could be biased either way In my view, the skull morphology analyzed by Miyazaki and Amano (1994) could also be biased However, their concern could be unjustified because Wada (1988) stated that his southern-form sample was obtained from 5 drives and that he confirmed Hardy-Weinberg equilibrium in the sample, which suggested that reproduction could not be assumed nonrandom Kage (1999, in Japanese) showed that each southernform school driven at Taiji and examined by him contained multiple maternal lines and suggested that paternal genes in his sample were most likely to have derived from outside the maternal lines

12.3.7.4 Mitochondrial DNA Kage (1999) analyzed 375 bases in the control region of mitochondrial DNA (mtDNA) of short-finned pilot whales and long-finned pilot whales of the world His material for the short-finned pilot whale was a total of 42 southern-form whales, including 37 from 7 schools driven at Taiji and 5 taken by the crossbow fishery at Nago in Okinawa, 4 northern-form whales taken by small-type whaling off Ayukawa, and data for 2 individuals from the eastern tropical Pacific obtained from GeneBank He identified some school-specific variation, but it was smaller than the difference between the two forms Difference in base sequence between individuals of the southern form was 03%–08% and that between individuals of two forms 14%, both much smaller than 37%, the corresponding figure between G. melas and G. macrorhynchus

A dendrogram derived from his analysis placed the two forms of short-finned pilot whales off Japan in a group together with the same species in the eastern tropical Pacific The North Atlantic long-finned pilot whales formed another group These two groups formed a group of the genus Globicephala Thus, Kage (1999) concluded that the northern and southern forms of pilot whales off Japan belong to the species G. macrorhynchus, which together with G. melas forms the genus Globicephala Another interesting result of his study was the position of northern-form short-finned pilot whales off Japan, which formed a group with the same species in the eastern tropical Pacific as well as that in the central North Atlantic This result allowed speculation on the evolution of short-finned pilot whales globally (see Section 12377)

12.3.7.5 Skull Morphology Miyazaki and Amano (1994) analyzed skull morphology to evaluate taxonomy of the two forms of short-finned pilot whale off Japan First they eliminated variation due to age by examining specimens aged 10 and over (southern form) or 17 and over (northern form) They employed 32 measurements The

and 15 females) and 17 northern-form skulls (8 males and 9 females) Length of the southern-form skulls ranged from 612 to 706 cm (males) and from 552 to 598 cm (females) and those of northern-form skulls from 700 to 783 cm (males) and from 610 to 648  cm (females) There was only slight overlap for males The maximum width of the southern-form skull was 459-519 cm (males) and 385-427 cm (females) and those for northern-form skulls 576-623  cm (males) and 449-489 cm (females); there was no overlap Skull size strongly reflected difference in body size

Miyazaki and Amano (1994) carried out an analysis of covariance using skull length as a covariate on log-transformed measurements They first compared the mean values between sexes of the same form and found significant difference in some measurements, most of which related to the widths of the rostrum and the cranium Males had larger values This means that males of both forms had skulls that were broader than those of females of the same form They compared the mean values between the two forms of the same sex and found significant difference in 20 (female) or 21 (male) measurements Many of these measurements with differences were again of width of rostrum and cranium and showed that both sexes of the northern form had a broader skull than the same sex of the southern form

They also carried out principal components analysis of the 32 measurements and made a two-dimensional scatter plot using two components They found that the specimens were separated into a total of four groups correlated with sex and geographical form However, as they stated, only the first component contributed to the separation of four groups (two  sexes and two geographical forms), and the first component was most strongly influenced by the size of the skull, particularly skull length, rostral width, and cranial width The second component only separated females of the northern form from males of the southern form but did not separate five other group pairs: sexes of the northern form, sexes of the southern form, males of the northern and southern forms, northern-form males and southern-form female, and females of the northern and southern forms The significance of skull size, which is a reflection of body size, in taxonomy of the genus Globicephala is questionable

Based on these analyses, Miyazaki and Amano (1994) proposed that the two forms of pilot whales off Japan should be dealt with as separate species However, the information presented by them appears to be insufficient to support this conclusion While their analysis indicating morphological difference between the two populations is convincing, I do not see a basis for classifying them into two species For that particular purpose, they should have added to their analysis a minimum of two additional samples, which would include a third sample of G. melas and fourth sample of a different population of either G. melas or G.  macrorhynchus This addition could have clarified the magnitude of morphological difference between the currently accepted two species of Globicephala and that between populations within a species, which could have contributed to evaluating the

two forms off Japan

12.3.7.6 Considerations on the Evolution of G. macrorhynchus

The northern form off Japan differs from the southern form in the presence of a distinct saddle patch, larger body size, and some other relatively minor morphological differences Table 124 lists available information on the saddle patch of short-finned pilot whales in the world (see also photograph in frontispiece) The records include those made by individual authors through the process of individual identification and can be considered to be reliable It is known that both pigmentation types occur and segregate geographically within the ocean basins of the North Pacific and North Atlantic

The pigmentation of short-finned pilot whales off the west coast of North America is close to that of the northern form off Japan Body length of a female stranded on the coast of British Columbia was 452 cm (Baird and Stacey 1993) Such large size occurs in the northern form off Japan but not in the southern form Although the saddle patch was not described for this particular female, it was likely to have had a distinct saddle patch as observed in the species off Seattle and California I interpret these observations to indicate that the northern form off Japan is morphologically closer to shortfinned pilot whales off the northwest coast of North America

Body lengths of 46 male and 108 female short-finned pilot whales were available in Ogden et al (unpublished and cited in Kasuya and Matsui 1984) The geographical range seems to cover the entire Atlantic coast of the United States, including the coasts of the Gulf of Mexico and New Jersey where different pigmentation types are known to occur (Table 124) Therefore the measurements probably come from two

(male) and 397 cm (female) are close to those for the Japanese southern form

Polisini (1980) studied geographical skull variation in the genus Globicephala using two discrimination functions One of the functions succeeded 100% in distinguishing between the two species in the genus The second function was able to identify the origin of most of the short-finned pilot whales from the North Pacific and North Atlantic, but there was some overlap Then he made a two-dimensional scatter plot using the two discriminate functions and found that the two species were fully separated from each other and that short-finned pilot whales from off California were fully separated from those from off the East Coast of the United States As expected, two individuals from Bermuda and Florida were included in a group of US East Coast individuals I note that two short-finned pilot whales, one from Ayukawa in northern Japan and the other from Alaska, joined the California group One animal from Arari on the coast of the Izu Peninsula was erroneously placed in the California group and another from California was misclassified with the Arari group, which I also felt was interesting

The analyses of Polisini (1980) caught my attention particularly because short-finned pilot whales in the broad geographical range of the West Indies, the South Atlantic, the Indian Ocean, the South Pacific, and the western North Pacific off central Japan were grouped together, including one specimen from the Bahamas, four from West Africa, one from the Cape Region of South Africa, one from Malacca, one from Timor, one from the Philippines, one from the Marquesas, one from Hawaii, and three from central Japan (Arari on the Izu Peninsula and Wakayama Prefecture, possibly represented by Taiji) It is reasonable to assume from the location that the three from central Japan belonged to the southern

TABLE 12.4 Variation of Saddle Mark of Short-Finned Pilot Whales in the Northern Hemisphere

tropical Atlantic The result indicates that short-finned pilot whales in the broad area from the western North Atlantic, the Indian Ocean, the western tropical Pacific, and the coast of central Japan have similar morphological characters, while those in the North Pacific area from Baja California, the west coast of the United States, and northern Japan have common features of the skull

During the summers of 1982 through 1987, sighting surveys for Dall’s porpoises were conducted in the northern North Pacific north of 35°N, or north of the Kuroshio Extension and North Pacific Current (see Section 933 and

ter short-finned pilot whales in the central area in longitudes from 150°E to 135°W This suggests that the northern form off Japan constitutes a population that is geographically separated from similar forms off the west coast of North America Similarly, it is reasonable to expect multiple tropical North Pacific populations that share morphological characters with the southern-form short-finned pilot whales off Japan

While Polisini (1980) addressed systematics of pilot whales using skull morphology, Oremus et al (2009) used mtDNA for the same purpose They analyzed a sequence of a maximum of 620 bases in the control region of mtDNA and calculated

This study was particularly interesting because it included Japanese specimens identified by Kage (1999) as of the northern and southern forms based on external morphology and location However, the study included problematic Japanese market sample from unknown locations of capture and thus not identifiable to geographical form They included all the specimens purchased in Chiba Prefecture or to the south in a southern Japan sample (SoJ) and those purchased in the north of the range into a northern Japan sample (NoJ) In view of the Japanese distribution system for whale products, such a classification seems to be too simplistic

Oremus et al (2009) created a dendrogram by a stepwise combination of closest haplotypes (Figure 129) and identified two distinct groups represented by the current G. melas and G. macrorhynchus The authors did not find common haplotypes between the two species and accepted the current taxonomy that recognizes two species in the genus

One of the two points of interest on the long-finned pilot whale in Oremus et al (2009) was genetic difference between the neighboring waters of New Zealand and Tasmania, suggesting presence of local populations A second point was the high genetic variability in the Southern Hemisphere (12 haplotypes), compared with only 3 haplotypes found in the North Atlantic, 2 of which were common with those in the Southern Hemisphere Based on this observation the authors supported a classification dealing with long-finned pilot whales in the two hemispheres as separate subspecies and concluded that the species in the North Atlantic had its origin in immigrants from the Southern Hemisphere

Long-finned pilot whales were present in the northern North Pacific up to at least about 6500 years BP to the thirteenth century (Section 1211) Two possibilities have been proposed for their origin One is that they crossed the equatorial region of the eastern tropical Pacific during the last glacial period that ended about 10,000 years ago The other is that they crossed the Arctic Ocean during a warmer period after the last glacial period (Kasuya 1975) Genetic analysis may yield an answer

Oremus et  al (2009) found the highest genetic variation in the short-finned pilot whale in the western North Pacific (11 haplotypes), followed by 3 in the South Pacific and 2 in both the eastern North Pacific and the North Atlantic The authors stated that the southern form off Japan had 9 haplotypes and the northern forms 2 haplotypes, although their understanding is based, in part, on market samples that were of dubious geographical origin in my view

The dendrogram of Oremus et  al (2009) separated the short-finned pilot whales into two indistinct subgroups One of them included individuals of Japanese origin identified by pigmentation as of the southern form (marked “sf” in Figure 129) and had higher genetic variation than the second subgroup that included northern-form whales from off Japan (“nf” in Figure 129) Genetic variation of the northern form was low and agrees with our understanding that the sample is likely from a small local population The second subgroup of short-finned pilot whales, including the northern form off Japan, covered a broad geographical range in the eastern

Northern Japan (Noj), and common haplotypes were found among two or three geographical areas

Oremus et al (2009) paid attention to haplotype C, which was found in the second subgroup of short-finned pilot whales and was shared by 17 South Pacific samples and 8 market samples out of the 82 purchased in southern Japan (Soj) The authors noted that this haplotype had a large difference from other haplotypes known from southern-form whales from off Japan They suggested two possibilities: (1) these 8 Japanese market samples were brought by fishermen from a distant fishing ground or (2) the southern form of short-finned pilot whales off Japan contained more than one population I would propose some additional possibilities

Although it can be true that most small cetaceans caught in southern Japan are consumed in southern Japan and that samples purchased in markets south of Chiba mostly represent animals taken in Chiba or to the south (Chiba, Izu, Taiji, and Nago in Okinawa), there is evidence that small cetaceans caught in northern Japan have been sold in southern Japan Endo (2008, in Japanese) reported cases where a wholesale market in Fukuoka City (33°35′N, 130°24′E), northern Kyushu, received meat of northern-form pilot whales caught off the Sanriku Region northeastern Japan as well as that of southern forms taken off Nago in Okinawa, southwestern Japan I have confirmed a case in the 1980s where a small-type whaler landed northern-form pilot whales at Ayukawa in the Sanriku Region and sent the meat to southwestern Japan, and another case in 2011 where Dall’s porpoises from the Sanriku Region as well as minke whales from Japanese scientific whaling were routinely processed by Maruko Shoji in Shimonoseki (33°57′N, 130°56′E) and distributed in Yamaguchi Prefecture (approximately 33°45′N-34°45N, 130°45′E-132°15′E) and the nearby area see Section 24 for Dall’s porpoise market)

Thus, there remains another possibility that the 8 of the 82 pilot whale meat samples purchased by Oremus et al (2009) in southern Japan (labeled “SoJ” and not identified as “sf “in Figure 129) and found to have haplotype C actually came from northern-form whales landed in northern Japan This disagrees with the interpretation of Oremus et al (2009) and requires further consideration in interpreting the zoogeography of the species

Oremus et al (2009) did not present an opinion on the taxonomic status of the northern and southern forms off Japan It is true that the genetic distance between the two subgroups in G. macrorhynchus was smaller than that between the two species of the genus Globicephala Before we determine their taxonomic status we will have to reevaluate differences between two subspecies of G. melas and compare those with our knowledge of geographical variation within the species G. macrorhynchus

12.3.7.7 Evolution and Zoogeography of Short-Finned Pilot Whales

The western tropical Pacific could have remained as an area of the highest sea surface temperatures in the entire Pacific area through past climate changes It could have functioned as

plied outward emigrants when a warm climate returned This applies to the short-finned pilot whale The currently identified range of the southern-form pilot whale is located in the northern part of this refuge This, together with the fact that pilot whales in this range exhibit the highest genetic variability, supports the hypothesis about their historical dispersal The small body size of these whales should also be noted

The current distribution of short-finned pilot whales in the Indian Ocean is discontinuous from that in the South Atlantic (Section 122), but contact is likely to have occurred during past periods of warmer climate, the last of which occurred after the last glacial period that ended about 10,000 years ago South America extends south to almost 56°S and both coasts are bordered by cold currents, so the possibility of shortfinned pilot whales passing around Cape Horn would have been smaller

An early type of short-finned pilot whale could have remained in the Kuroshio and its Counter Current area and evolved into the present southern-form short-finned pilot whale, while others expanded their range into the South Pacific and the Indian Ocean and further to the South Atlantic, passing Cape Agulhas in a warm period If this hypothesis is correct there should be a cline of genetic variability from the western tropical Pacific to the South Pacific, Indian Ocean, and South Atlantic, for which we do not have information

There would have been another group of early short-finned pilot whales that moved to the east beyond the Hawaiian Islands and reached waters off Baja California The gradient of sea surface temperature was small in the eastern tropical Pacific east of Hawaii and it was not a big obstacle for the dispersal; high ocean productivity could have invited the emigration These animals, after reaching the California Current area, could have started evolving toward the northern form of short-finned pilot whale Utilizing an abundant food supply and adjusting body size and reproductive cycle to the cold environment, they probably established a population off the Vancouver Island area At the final stage some members of the population could have proceeded further west along the Arctic Convergence to settle in waters of high productivity off northern Japan between the cold Oyashio and warm Kuroshio Currents These would be the current northern-form short-finned pilot whales off Japan Timing of these incidents remains to be investigated

This hypothesis assumes that the southern-form and northern-form pilot whales started from the same origin One group of them remained in the original environment which was available in the Kuroshio Counter Current area and achieved relatively minor differentiation to become the current southern form, and the other expanded the range counterclockwise while acquiring greater modification in body and way of life to finally reach northern Japan The two forms now face each other across the Kuroshio Front, where the environmental gradient is steep enough to be a barrier in their distribution If  this hypothesis is correct the genetic distance between the two forms off Japan should be greater than the distance between the Japanese northern-form and short-finned pilot

gested by the small samples in Figure 129 The idea regarding the eastward expansion of short-finned pilot whales in the North Pacific emerged in 1967 in discussions with RL Brownell at Arari in Japan, where we were collecting skulls of short-finned pilot whales for taxonomic research

For study of any biological aspect of any mammal species, background information on the targeted individual such as age and maturity is important The information would be the best if records of its whole life since birth were available Individual identification has often been used for studies on behavior and social structure of cetaceans The technique is particularly useful for species that have easily identifiable external characters, as in the case of northern-form shortfinned pilot whales, but is applicable only in certain area of the range where agreement exists to not harm the animals being studied I once attempted individual identification of the northern-form population off Sanriku on the Pacific coast of northern Japan but quickly realized the incompatibility of the methodology with the whaling operations, and I was obliged to switch my effort toward understanding life history through examination of whale carcasses brought back by whalers

Relationships between biological events and accompanying behavior can be understood by following the daily life of particular individuals Such efforts have increased our knowledge on individual variation in the breeding cycle of cetaceans and can contribute, with some caveats, to determining the variability of lifetime production among females and the causes of the individual variation This methodology still has some limitation for species that inhabit broad pelagic waters or have large population sizes, whereas carcass studies can still make some contribution by yielding biological information mostly in the form of averages for the population being studied

Their extended life span is another difficulty that accompanies studies on wild cetaceans Depending on species, they reach sexual maturity at 3-17 years and live for 20-100 years or more, which is almost equivalent to the lifetime career of a scientist and is sufficiently long to expect large changes in the environment surrounding the targeted cetaceans When we consider the magnitude of destruction of the marine environment that humans have perpetrated in the past 100 years, such as through increased underwater noise, accumulation of heavy metals and persistent organic compounds, and overexploitation of marine organisms, it is easy to imagine the possible additional destruction that may occur during the next 100 years We will face the difficulty of separating age-dependent change in cetacean life history from response to environmental change

Examination of cetacean carcasses available from whaling operations offers a quick view of a horizontal aspect of cetacean life history and can serve as a proxy for obtaining a vertical view The current world atmosphere surrounding cetacean biology does not tolerate killing whales for science

vation is expected Japan is one of the few exceptions, where over 10,000 small cetaceans are killed annually for commercial purposes and a kill of over 1000 large whales is planned for the stated purpose of science

All Japanese cetacean scientists enjoyed the generosity of dolphin and porpoise fishermen until 1997, during which time I worked for a university and then for the Fisheries Agency of Japan However, the research environment changed in 1998, or 1 year after I left the Fisheries Agency The fishery community, including both fishermen and related government sections, apparently started classifying scientists and controlling access to research opportunities For example, a university student who wanted pieces of skin of short-finned pilot whales for genetic study was asked by the fishermen to obtain approval of the Fisheries Agency or scientists working for it before taking the samples Some university scientists felt that their request for approval was ignored by the agency, or they received a counter proposal from agency scientists to have one of their names as a coauthor in exchange for the approval

Although fisheries are currently allowed to pursue private profit by exploiting marine biological resources, the marine resources are, in my view, common property of the world human community Therefore fisheries should offer opportunities for scientists to examine their catch for scientific purposes, and scientists in the community should make their results globally available

12.4.2.1 Principle of Age Determination Toothed whales are aged using growth layers in their teeth The teeth of recent toothed whales are monophyodont and homodont with a single cusp and single root and usually of similar shape They are not replaced during life (Section I13) As in the case of other mammalian teeth, they are composed of the three elements of enamel, dentine, and cementum Dentine constitutes a major part of the tooth The enamel, the hardest tissue, covers the distal tip of the dentine Cementum covers the root of the tooth and connects the dentine and surrounding soft tissue Tooth germs, shaped like a crushed tennis ball, are formed in the jaw at an early stage of fetal life, and enamel and dentine layers are deposited within them Deposition of these two tissues starts at a fetal size of 10-20 cm in the short-finned pilot whale Deposition of enamel layers occurs at the distal end of the fetal tooth and ends shortly before birth The dentine layers are deposited on the proximal side of the germ and continues for years after birth The deposition of cementum, the third element of the tooth, starts in the short-finned pilot whale near the time of tooth eruption and continues for life on the root of the tooth Each of the three tissues forms growth layers

The enamel contains fine growth layers visible under a light microscope in a polished thin section of the tooth These layers are likely to be a record of the daily physiological cycle and to have potential value for studying fetal growth, but such an attempt has not been published

recorded in the dentine, but, depending on the species and on the method of preparation, additional finer layers have also been detected Some of the fine structures have been interpreted as reflecting a monthly cycle (Myrick and Cornell 1990; Myrick 1991) As dentine is deposited on the wall of the pulp cavity, the cavity decreases in volume with age, finally leaving a narrow space for blood vessels when dentine deposition ceases The age when dentine deposition ceases depends mainly on tooth size, which depends on species and position in the jaw Aging of old individuals, where dentine deposition has ceased, has to rely on growth layers in the cementum

Cementum is deposited on the surface of the tooth root for life, but the layers are usually thinner and harder to read than the dentinal layers An exception is the cementum of the Baird’s beaked whale Cementum in the species is thick and contains numerous fine structures within an annual layer, which have been deduced to represent a cycle of about 30 days (Kasuya 1977; Section 1341)

It is important for each reader to train his/her eyes to get the same age estimate from both dentine and cementum of the same tooth with an open pulp cavity Short-finned pilot whales start to deposit cementum soon after birth, or at body length of 154-163 cm or estimated age of 15-35 months The lag time is small enough to be ignored in aging (Kasuya and Matsui 1984)

12.4.2.2 Sampling and Preparation of the Tooth I examined carcasses of short-finned pilot whales at the dockside of the fishing port while fishermen were processing their catch The task included taking a measurement of body length, examination and collection of histological materials from reproductive tracts including fetuses and mammarygland samples, and extraction of teeth for age determination Such activity was possible only with the consent of the fishermen, and I appreciate the cooperation of the dolphin fishermen of Arari (34°57′N, 139°07′E), Ayukawa, Futo (34°55′N, 139°08′E), Kawana, and Taiji

The lower teeth are more suited than the upper teeth for aging purposes The upper teeth are curved in two directions and are unable to be cut in one plane through the center, which is required in preparations for aging At the beginning of the work I used a hammer and chisel to extract 2 or 3 teeth from the jaw, which required daily training of my arms with a heavy hammer, but later I switched to a saw for the task Some scientists have recently used an electric saw for the purpose The teeth were placed in a perforated plastic bag together with a label and various histological samples and fixed in 10% formalin solution Acid in the formalin solution may damage the tooth tissue to some degree, but it did not cause a problem because these teeth were scheduled to be decalcified in formic acid for age determination The following processes, A to E, were carried out in the laboratory

A Using a knife, one tooth was cut out from the formalin-fixed block from the lower jaw The tooth was cleaned of soft tissue, leaving a thin layer of gum

most recent, cement layer on the tooth Then, using an IsoMet low-speed saw, the tooth was cut longitudinally on a plane near the center of the tooth The tooth had to be wet during the procedure; water was used as a lubricant The sawed-off surface was polished flat to the center of the tooth using whetstones of 1000 and 2000 mesh The surface of the whetstone had to be kept flat Waterproof sandpaper on a flat plate can be used for the same purpose If a tooth is polished through the center, the two rami of a growth layer meet with an acute point at the center of the tooth, but if the tooth is cut off center, the rami meet with a round curve at the center

B The tooth polished down to the center was glued on a clear plastic slide (eg, 1 mm thick plate of polyvinyl chloride) using cyanoacrylate resin During this operation the tooth had to be still wet, but the surface was wiped dry to keep the glue clear If it was felt that the glue was hardening slowly, the slide was placed inside a glass bell together with vapor of a hardening catalyst The half-cut tooth on the plastic slide was again placed on the diamond saw to cut off the other half, leaving a section about 1 mm thick on the slide The thin section on the plastic slide was polished down to a thickness of 30-80 μm using the same set of whetstones as the previous one and water as a lubricant The thickness was measured using the focusing dial of a microscope It was desirable to polish the cementum portion thinner than the dentine in the same preparation because growth layers in the cementum are thinner than those in the dentine This process must be completed in wet conditions before proceeding to the next step, C The tooth tissue will shrink if it dries and will separate from the plastic slide The reason for using a plastic slide plate was to compensate to some degree for this problem

C The thin section of the tooth glued on a plastic slide was placed in a 10% solution of formic acid for several hours The tooth section was not harmed by being left in the acid, even overnight The tooth tissue, when completely decalcified, appears transparent under the microscope, but the dentinal tubules will appear dark if decalcification is incomplete If an insufficiently decalcified tooth section is put through the subsequent process, the completed preparation appears to have a whitish brown hue The fully decalcified section was rinsed in running water overnight or for a full day to completely remove the formic acid Because the tooth section was much thicker than an ordinary histological section, the rinsing procedure required a longer time If acid remains in the tissue, the stain will fade quickly, perhaps in a few months

D The decalcified and rinsed tooth section can be stained with any type of hematoxylin Double staining with eosin should be avoided because it decreases

with Mayer’s hematoxylin for about 30  min, but slightly extending the time in this medium did not result in identifiable problems The stained section was rinsed in running water for about 24 h for complete removal of acid The process can be improved by placing the rinsed slide in water with a few drops of ammonia If the slide was stained too dark, it can be bleached in formic acid and the procedure obtained earlier can be repeated If darkly stained blotches are found on the slide, it is most probably due to partial separation of the tooth from the plastic plate This is not attractive and causes some trouble in reading growth layers, but the slide is still usable

E At this stage the thin tooth section appeared blue on a plastic slide and was wet with water It should go quickly through a series of alcohol rinses (ie, 50% ethanol, pure ethanol I, and II) and then be mounted using a mounting medium dissolved in alcohol Use of xylene should be avoided because it harms the plastic slide as well as the cyanoacrylate resin When the mounting medium hardens, the preparation is complete Caution was needed to avoid drying, particularly during step E For longer storage of the preparations, they should be stored in a refrigerator

This method of tooth preparation does not require costly machines but does require some experience, and it produces only one preparation from a single tooth A powerful cryostat is needed to cut a decalcified cetacean tooth because it is still hard after decalcification, but the machine can produce several tooth sections from a single tooth A strong decalcification agent is required for decalcification of a large tooth, and care should be taken to prevent overdecalcification of the outer portion of the tooth (eg, cement layers)

I prepared dentine of short-finned pilot whales to a thickness of 40-80 μm and the cementum to the thickness of 30-40 μm, because growth layers in the former tissue were thicker than those in the latter (Kasuya 1983, in Japanese) Such a minor adjustment was easy if the teeth are polished by hand, but would be hard with a cryostat Teeth as small as those of striped dolphins were able to be prepared with only a whetstone and without using a diamond saw Reliable age determination is only possible with high-quality tooth preparations, which must be cut through the center of the tooth at a suitable thickness and stained to a suitable density Unsatisfactory preparations should be discarded and replaced with good preparations from other teeth from the same animal

12.4.2.3 Accumulation Rate of Growth Layers Growth layers in the dentine were counted using a lighttransmitting microscope at about 10× magnification and those in the cementum at about 100× The microscope has to be well adjusted for lightning, and it is desirable to have a high-quality objective lens with a wide field and flat focal plane The enamel layer is completely lost in a decalcified stained tooth section and remains only as a mold in the resin

first dentine tissue next to the enamel is fetal dentine, which has an almost uniform structure Except in teeth of neonates, the inner border of the fetal dentine is bordered by a lightly stained dentinal layer of 15-65 μm thickness This is called neonatal dentine or the neonatal line, is dentin of weak calcification deposited just after birth, and is visually identifiable only after deposition of subsequent ordinary postnatal dentine The neonatal line becomes visually identifiable within 1 month after birth (Kasuya and Matsui 1984) The task of age determination is to count the alternating differentially stainable structures in the postnatal dentine or in the cementum

One growth layer is often described as a pair composed of a darkly stained and a less stained layer, but that definition is not precise enough and may be misleading It is usual to find several alternations of stainability in shorter, and often irregular, cycles in a set of layers representing an “annual cycle” Some such fine layers have been interpreted as monthly layers (in the pantropical spotted dolphin) or marks of pregnancy or parturition (sperm whale), but most such fine structures remain without interpretation (Perrin and Myrick 1980) The regular “annual layer” has been called “growth layer group” and the fine structures within it as “accessory layers,” although this terminology does not seem to me sufficiently satisfactory to avoid confusion or misunderstanding

Identifying the neonatal line is the first step in reading annual layers in the dentine The birth date of an individual dolphin probably affects the appearance of the dentine deposited next to the neonatal line, but this influence has not been well documented In the southern-form short-finned pilot whale, the thickness of dentin deposited in the first year after birth is 05-10 mm and then it declines with increasing age Some individuals cease deposition of dentine at age 25 and almost all individuals by age 40 Some individuals may still deposit dentine at age 30, but the thickness of the dentine of one cycle is only about 01 mm Aging of animals that have ceased dentine deposition must rely on reading growth layers in the cementum The total thickness of cementum at this stage will be 05-1 mm, wherein it is possible to count 30-40 growth layers

The short-finned pilot whale is one of the easiest species for which to read annual growth layers in the dentine and cementum, although readability of the latter tissue is inferior to that of the former (Figure 1210) Cautions in reading cemental layers are that they may contain some accessory layers and that annual layers deposited at age 1 or 2 years are identifiable only around the neck region of the tooth where layers of later deposition are not observed (see 5, 6, and 7 of Figure 1210a) This is because the teeth of young individuals increase in length rapidly and the neck region soon becomes exposed above the gum Deposition of cementum starts at age of a few months (see Section 12421), and a neonatal line is not formed in it

The accumulation rate of growth layers can be calibrated using teeth of known-age individuals or teeth that are stained in vivo using chemicals such as tetracycline, as was done with bottlenose dolphins (Myrick and Cornell 1990) In Japan, Nishiwaki and Yagi (1953) attempted this task by injecting

mine the accumulation rate because of short life of the dolphins in captivity Until recently, striped dolphins have not been successfully kept in Japanese aquariums Because such information was not available for short-finned pilot whales, the accumulation rate of growth layers in the dentine was estimated by examining seasonal alternation of the last dentinal layer in tooth samples that covered 8 months of the year

Kasuya and Matsui (1984) observed the stainability of dentine being deposited on the pulp cavity wall at the time of death In May-October 80%–90% of individuals were depositing dentine that was darkly stainable with hematoxylin, but the proportion decreased to 40% in December-January and to 20% in February A 100% score could not be expected in the data because there can be some misclassification due to the presence of accessory layers Taking this into account, the authors concluded that deposition of stainable dentine started in April-May and continued to October-November and unstainable dentine was deposited from November-December to March-April They also observed that older individuals switched the deposition from stainable to unstainable layer in an earlier season than younger individuals, which suggested that the proportion of time represented by stainable and unstainable layers may change with age Even accepting such minor uncertainties, it is safe to assume that a set of stainable and unstainable layers represents a period of one year

12.4.2.4 Aging Error and Differences between Teeth Every tooth in a jaw is under the influence of a common physiology, which can be recorded similarly in each tooth as growth layers However, difference in tooth size between positions in a jaw may influence the readability of the layers and the age when dentinal deposition ceases

Kasuya and Matsui (1984) examined readability difference of growth layers between positions in a jaw using teeth collected from three southern-form short-finned pilot whales aged between 20 and 45 The cusp in some teeth was lost by wear, leaving only a minor portion of the enamel layer, which meant that fetal dentine as well as the neonatal line was still present on the tooth for determination of the starting point for reading One or two teeth near the end of the tooth row tended to yield lower dentinal counts than a larger tooth near the middle of the row This was common in both a 45-yearold individual that had ceased dentinal deposition and in younger individuals with an open pulp cavity The reason for lower counts in small teeth near the end of the tooth row was probably the difficulty of reading compressed growth layers in the dentine of such teeth The readings for cemental layers showed reasonable agreement among teeth in a jaw This result suggests that small teeth near the end of a tooth row should be avoided for age reading, and if there is no other choice, cemental layers should be carefully examined

Kasuya and Matsui (1984) made three independent counts on the same tissue (dentine and cementum) of the same tooth and accepted the middle figure as the correct count for the tissue The reading error was calculated as the difference between the middle figure and the one closest to it and was

distributed on both sides of zero with a standard deviation of 2% This suggested that the 95% confidence interval of their age reading was about 4% on each side of the estimated age This was the major source of error in the age reading, but there

age to nearest year by estimating by eye the thickness of the first and the last incomplete layers If both errors are combined the true age of an individual was within ±09 year for animals estimated at 10 years old, ±18 years for 20-year-old

for 60-year-old animals (Kasuya and Matsui 1984) The magnitude of reading error depends also on experience of the readers and the quality of preparations

If we can correctly estimate the thickness of the first and the last growth layers, which are likely to be incomplete, we will be able to estimate the animal’s age with higher precision Although this was attempted by Kasuya and Matsui (1984), the accuracy of the estimates has not been verified Thus, in most of the cases they expressed the age of an animal to the nearest n + 05 years, n being an integer This did not mean that age was precise to 05 years, but that any age from n years to less than n + 1 years was expressed as n + 05 years Such a method is convenient in growth analysis This book uses this method as well as the method often used for humans, where age of n + 05 years is expressed by the integer n years

It is reasonable to expect annual deposition of growth layers in mammals, including cetaceans, because their lives are governed by the annual cycle of seasons However, there will be cases where layer deposition rate is unknown and life history analyzed by tentatively assuming annual deposition The results of such analysis must be carefully evaluated to determine if the derived life history is reasonable

12.4.3.1 Neonatal Body Length The life of an animal is said to begin at conception, but for management purposes it is convenient to start at parturition Thus, fetal life is included in the life of a pregnant female The neonatal size of humans is easily obtained by measuring newborns at a hospital, because in recent times human females have given birth in hospitals Such large samples will reveal even minor neonatal body size difference between the sexes It is almost impossible for scientists to observe parturitions of wild animals, particularly cetaceans, although nesting animals may offer a slightly easier situation The finless porpoise inhabits coastal or inland waters and has offered scientists better opportunities for obtaining stranded carcasses of neonates than the offshore species As the short-finned pilot whale inhabits offshore waters, information on neonatal size has relied mostly on carcasses obtained from fisheries

The northern-form pilot whale inhabits waters off the Pacific coast of northern Japan and attains a larger body size while the southern form inhabits Pacific waters off central and southern Japan and attains a smaller body size Samples of the northern forms were obtained from the catch of small-type whaling, and those of the southern form from the catch of dolphin-drive fisheries at Arari, Futo, and Kawana along the coast of the Izu Peninsula and at Taiji in Wakayama Prefecture in the 1960s to the early 1980s Arari and Kawana have now ceased operations and Futo appears to be very inactive in the fishery (Sections 38 and 39)

Among the southern-form individuals caught in these fisheries the smallest newborns were found at lengths of 142 cm (female) and 136 cm (male), and the largest fetuses at 144 cm (female) and 146 cm (male) (Kasuya and Marsh 1984) These

cm, when possible between-sex difference was ignored A middle figure, 141 cm, should be close to the average neonatal length

This simple method has the shortcoming of depending on only the two extremes and ignoring other data between them, and the result will be greatly influenced by sample size In order to overcome this, the proportion fetal and postnatal was examined in relation to body length in an attempt to find a body length where the ratios of the two categories were equal (Table 125) This procedure revealed another problem, a large discrepancy between the number of fetuses and of postnatals within the body-length range of 120-159  cm, where 29 fetuses, but only 7 postnatals (ie, 41:1), were recorded The exact same discrepancy was observed in striped dolphins (ie, 58 fetuses and 14 neonates or 41:1) and was interpreted as either due to bias in the sample collected at the beginning of the parturition season or loss of neonates during the drive (Section 1052)

Such disagreement can occur for several reasons, one of which is the timing of the sample relative to the parturition season The timing of birth of a particular fetus is probably affected by fetal body size as well as season A sample obtained at the beginning of the parturition season will have more fetuses than postnatals of the same body length The reverse will be true for a sample late in the parturition season Most of the parturitions of the southern-form pilot whale occur in June-October with a peak in August (see Section 12442) Kasuya and Marsh (1984) obtained most of the samples in the early half of the parturition season in June-August and only a few in the last half of the season in September to October (Figure 1223) This was probably the main reason for the deficiency of postnatals compared with full-term fetuses of the same body size in the sample This is alternative to the assumption of offshore segregation of schools with neonates, that is, one of the hypotheses tested by Kasuya and Marsh (1984), which failed to explain the imbalance between fetuses and young calves The question still remains of why the September-October sample of Kasuya and Marsh (1984) lacked near-term fetuses and neonates (Figures 1223 and 1224)

TABLE 12.5 An Attempt at Estimating Mean Neonatal Length of Southern-Form Short-Finned Pilot Whales Using Limited and Possibly Biased Samples

and postnatal counts are postnatal natural mortality and humancaused loss of postnatals during the drive, both of which can be higher in neonates than in near-term fetuses However, Kasuya and Marsh (1984) failed to explain the imbalance with either of these single factors I question whether loss of neonates during the drive can be of similar magnitude to that of striped dolphins that have often been driven in school of several hundred individuals, while short-finned pilot whales live in schools smaller in size and tighter in structure (Table 1220) Fishermen can more easily keep their eyes on the whole pilot whale school and pay attention to not losing a single pilot whale, since they have higher per capita value

Although the reason for the unbalanced fetus/postnatal ratio remains unresolved, Kasuya and Marsh (1984) raised the number of postnatals to the level of the fetuses (Table 125), fitted a linear regression to the proportion of neonates on body length, and obtained a body length where neonates were 50% The average body length at birth thus estimated was 1395 cm, which was almost the same as the 141  cm obtained earlier from the two extreme figures Thus, 140 cm is currently used as the average neonatal length of southern-form short-finned pilot whales off Japan (Kasuya and Marsh 1984)

The northern-form pilot whales were taken by small-type whalers They operated the fishery with a quota on the number of animals, so they were unlikely to catch neonates of low commercial value The materials analyzed by Kasuya and Tai (1993) covered the season from late September to November, and the fetal length frequency distribution was bimodal, with one mode below 20 cm and another less distinct mode at 150170  cm The latter mode was considered to represent nearterm fetuses Ohsumi (1966) presented a relationship between average neonatal body length (Y, m) and average body length of females at attainment of sexual maturity (X, m):

Y = 0532 X0916

Applying average female length at sexual maturity of 39-40 m (see Section 12432) to this equation, Kasuya and Tai (1993) obtained 185-189 cm as a range of average neonatal length of northern-form pilot whales They further noted that Ohsumi’s equation gave a slightly larger figure than the independent estimate of neonatal length of southern-form whales and concluded that the lower bound of the range, that is, 185 cm, would be suitable as the average neonatal length of northern-form whales This was 45 cm greater than the mean neonatal length of southern-form whales estimated earlier

12.4.3.2 Female Sexual Maturity Female age at sexual maturity can be defined either as the age at the first ovulation or at first parturition The latter is often used in population dynamics, because it directly indicates recruitment, albeit harder to be determined However, the former has been used in the study of life history, because it is easily determined by the presence of a corpus luteum or albicans formed in the ovaries after ovulation If an ovulation is followed by conception, the corpus luteum is maintained in

cans after parturition, but if the ovulation is not followed by conception the corpus luteum degenerates quickly to a corpus albicans (Marsh and Kasuya 1984) It has been believed that histology of the corpus albicans cannot distinguish between the two histories and that the corpora albicantia persist in the ovaries for life Thus, counting these corpora in the ovaries will give the number of ovulations experienced by a female but not the number of pregnancies (see Section 1056 for further discussion on this topic) As females will start behaving as adult individuals at around the first estrus, the first ovulation will be more suitable as a definition of attainment of sexual maturity for behavioral studies Among cetaceans the first ovulation is usually followed by conception (see Section 12448)

It is possible for some cetaceans to identify whether a female has had a past experience of pregnancy or lactation One of the methods is to examine the hue of the mammary gland in balaenopterids, where mammary glands that have undergone lactation show a brownish color while those which have not are pink This visual judgment is difficult for sperm whales, dolphins, and porpoises, but has potential to be tested histologically The other method is to note the existence of stretch marks in the uterus that can be seen in nonpregnant females with past experience of conception (Benirschke et al 1980) These stretch marks are apparently similar to the features seen in overstretched plastic film, and similar marks are seen on the breasts and abdomen of women with experience of childbirth

Ovaries of young immature females of the short-finned pilot whale are flattened and oval in shape, 3-35 cm-long and 1-2 cm wide, and weigh 2-6 g (both sides combined) At varying age over 2 years females start to have heavier ovaries; thus individual variation in total weight increases to 2-12 g This change is due to the development of Graafian follicles visible on the ovarian surface No particular bilateral asymmetry of ovarian development exists in the short-finned pilot whale (Marsh and Kasuya 1984), which is different from several dolphins such as the striped dolphin where the left ovary usually matures before the right (Section 10561; Ohsumi 1964)

The relationship between age and diameter of the largest Graafian follicle is shown in Figure 1211 Follicle size is expressed as the cube root of the product of three diameters in order to maintain a unified rule for follicles, corpora lutea, and corpora albicantia The geometric mean was considered better than the mathematic mean as an indicator of volume of these tissues which might be compressed by nearby structures through the process of degeneration (Marsh and Kasuya 1984) Some females aged over 2  years had the largest follicle measuring 5-8 mm in diameter, and this upper size limit remained unchanged among the immature individuals Since the southern-form pilot whales first ovulate at ages between 70 and 120 (see the following text in this section), this observation suggests that some immature females develop Graafian follicles only to the size of 5-8 mm and cease further development for several years until a time when follicle growth resumes However, it was unclear in the available data whether the follicle that remains dormant at 5-8 mm resumes growth for ovulation or another new follicle takes its place

Maximum follicle size in resting females (mature females neither pregnant nor lactating) was 15-16  mm in diameter (Figure 1211) Some lactating females also had large follicles These females were probably preparing for the next ovulation, but follicle size at ovulation would probably be more than 20  mm (for further information see Section 12447) The reason why we did not see such large follicles in immature females of maturing age would be explained by a rapid development of follicles before ovulation

Puberty is a stage when secondary or tertiary sexual characters become identifiable accompanied by development of the reproductive organs (primary sexual characters) and can, but not always, be a process of gradual development As cetacean females do not develop secondary sexual characters, identification of the pubertal stage must rely on tertiary sexual characters such as behavioral changes in the community Future studies should be directed toward finding change in social behavior or in direct measurement of sexual hormones in the blood to understand the pubertal stage

It is difficult, or impossible, to identify whether a particular female is in a pubertal stage by examining gonads extracted from a carcass of the short-finned pilot whale, other than inferring it from development of the Graafian follicles, which is a slow process of several years Past attempts for some toothed whales to identify the pubertal stage from information in the gonads often lacked sufficient support from behavioral information

Ovulation is known to occur only in females above a certain level of body mass, and it will cease if a female loses body mass below a certain nutritional level Body mass is

a function of both age and body size, but there have been no attempts to disentangle the two factors in attainment of sexual maturity of cetaceans

If sexual maturity is determined by experience of ovulation, the youngest mature female was aged at 85 and the oldest immature female at 115 years For technical reasons, this age range included the ages between 80 and 120 years (Section 12424) The proportion of females mature increased with increasing age, and the relation was expressed by an upwardly convex curve that transitioned to a horizontal line at higher ages Observing that the age where 50% of individuals were sexually mature was between age 85 and 95 years, Kasuya and Marsh (1984) applied a linear regression to the relationship between maturity and age using individuals aged 75-105 years and obtained age 90 as the age when 50% of females were sexually mature Individuals used in this calculation included four pregnant females that had only one corpus luteum and no corpora albicantia Fetal size in these females suggested that they had first ovulated at ages 74-81 years These four females became pregnant with their first ovulation and represent precocious cases There were two additional pregnant females included in the calculation obtained earlier One was aged 925, had three ovarian corpora, and was estimated to have conceived when she was 83 years old (fetal size was 100 cm) The other was aged 85 years, had four corpora, and was estimated to have conceived at age 84 (fetal size was 3 cm) Since these two females were not lactating, they were likely to have experienced their first conception at the third or fourth ovulation These ages and the age of the oldest immature female of 115 years allow the conclusion that southernform short-finned pilot whales first ovulate after age 70 years and before 120 years, which was about 5 years after the age when their ovaries started some degree of follicular development The status of the six pregnant females mentioned earlier indicated that three of them became pregnant at the first ovulation and the remaining two females presumably at their third or fourth ovulations

Body length on the mean growth curve (Figure 1221) at age 90 years (mean age at attainment of sexual maturity) was approximately 320 cm This could be affected by uncertainty in the mean growth curve Body lengths of the smallest sexually mature female and the largest immature female were 300 and 344 cm, respectively The proportion of sexually mature females plotted on body length showed, as in the case of the maturity-age relationship, an upwardly convex curve with a decreasing gradient at greater body length The gradient was steep at the lower half of the range, or at 300-330 cm Fitting a linear model to this range gave 3156 cm as the body length where 50% of individuals were sexually mature (Kasuya and Marsh 1984) Although the influence of including all of the age range in this regression was considered small in this species, which is avoided in the above calculation, the above calculation is not totally free from this effect (this problem was discussed in detail in Sections 11474 and 11483) This partly explains why body length at 50% maturity was smaller than body length at age 90 years

The corresponding growth parameters of the northernform short-finned pilot whale are listed in Table 126 in comparison with those of the southern form

12.4.3.3 Male Sexual Maturity 12.4.3.3.1 Definition The male process of sexual maturation includes various stages, for example (1) start of spermatogenesis in the testis, (2) attainment of physiological ability to fertilize females, (3) development of desire to approach estrous females, (4) identification by estrous females as a mature male, or (5) obtaining the opportunity for reproduction through competition among males The second stage has been used in cetaceans for estimating maturity, although the determination itself has problems The third example is probably equivalent to the pubertal stage The fourth and fifth stages will correspond to social maturity and require behavioral information for confirmation, which is hard to apply in carcass studies

Female sexual maturity leaves various morphological marks in the body, such as corpora in the ovaries, pregnancy, or lactation, but male maturity usually does not leave such morphological clues The following sections describe research to understand the process of sexual maturation of males using histological information The results of such studies need to be compared against behavioral information

12.4.3.3.2 Testicular Histology If a whole testis is examined histologically from one end to the other, a firm conclusion can be reached on whether the individual has started spermatogenesis However, such an attempt is like detecting a flea egg in a carpet and is certainly impractical The proxy for this has to be examination of a small sample of the testicular tissue Studies on sperm whales (Best 1969) and sei whales (Masaki 1976) revealed

the testes of young males The same was found for testes of Baird’s beaked whales Testes of the Baird’s beaked whale were examined in detail on six males at early stages of sexual maturity and revealed that spermatogenesis started near the anterior end of the testis and extended subsequently toward the posterior end (Kasuya et  al 1997) However, similar examination of testes of the southern-form pilot whale did not find such polarity in young males, and Kasuya and Marsh (1984) examined a piece of tissue 5-10 mm2 taken from the mid-center of the testis

Histological examination showed various stages, from being spermatogenic throughout the sample, spermatogenic in only in part of the sample, or aspermatogenic Kasuya and Marsh (1984) classified the maturity of the sampled tissue in southern-form whales based on proportion of seminiferous tubules that were spermatogenic into four categories: (1)  immature, no spermatogenic tubules present, (2) early maturing, more than 0% but less than 50% of tubules spermatogenic, (3) late maturing, 50% or more but less than 100% spermatogenic, and (4) mature, 100% spermatogenic This method had value in classifying maturity into four stages rather than two stages of “mature” and “immature,” but it is not free from misclassification of maturity between adjacent categories by chance in encountering particular tubules The risk can be avoided in part by analyzing other maturity-related parameters such as development determined from testicular and epididymal smears and by not placing great significance on difference between two adjacent categories, at least on an individual basis The same procedures were applied for the northern-form short-finned pilot whale (Kasuya and Tai 1993)

The results of examination of testicular histology are summarized in Figures 1212 and 1213, where the mean weight of both testes is plotted on age or body length Weight of a single testis was used if the other testis was not available for averaging Testis weight differed slightly between left and right testes of the same individual, but there was no systematic bilateral weight difference detected in the southern-form pilot whale (Kasuya and Marsh 1984) In order to cover the weight range, two orders of magnitude from juveniles to adults, testicular weights are plotted on a logarithmic scale in Figures 1212 and 1213, where the equation y = 10(ax + b) is expressed as a straight line and the usual linear relationship as an upwardly convex curve The following text relates to the southern-form pilot whale, but the northern form shows similar features, except for body size

The testis of southern-form males weighed 15-20 g at age 2 years, slowly increased in weight to age 7-8 years or body length 33 m, when some males started a low level of spermatogenesis (“early maturing”), with testis weight of 50-60 g Testis weight further continued a slow increase to reach an average weight of about 90 g at age 14 years The average rate of weight increase was about 54 g/year during the 6-7 years from ages 7-8 to 14

Rapid testicular growth occurred in most of the males between ages 14 and 18 and body length 38-42 m, which agrees with the time when southern-form pilot whales reached

Body Length and Age at the Attainment of Sexual Maturity of Female Short-Finned Pilot Whales off Japan

sexual maturity Most males attained the “mature” stage at this age, but there seemed to be a lag of 6-7 years between precocious and slow-maturing males This was expected from Figure 1212 which suggests that rapid testicular growth started in some individuals at age 14 and was completed by age 16, while slower males started rapid testicular growth as

late as age 23 Mean testis weight increased from about 90 g at age 14 to about 900 g at age 18, which was equivalent to increase of about 200 g/year This rate of mean annual testicular growth probably biased testicular growth of individual animals downward because of broad individual variation in the timing of the start of the growth spurt If the rapid process

of maturation is assumed to proceed within 2 years from 14 to 16 years of age, annual testicular growth could be 400 g/year It is reasonable to expect some behavioral change in males at these ages

This analysis suggests that a precocious male starts rapid testicular growth at age 14, but that slower males can start at age 23 These males are likely to achieve development from the “immature” stage to the “mature” stage within 2 years Testis at the “immature” stage weighed <170 g, “early maturing” 50-150 g, “late maturing” 150-900 g, and “mature” 400-3000 g Thus, males attained the “mature” stage at testicular weight of 400-900 g (single testis) Figure 1212 also shows that 50% of males attained the “mature” stage at testicular weight of 450 g Table 127 offers criteria to be used for determining male maturity using age, body length, or testicular weight

Sexual maturity of short-finned pilot whales is a function of body size as well as age (Kasuya and Marsh 1984) Larger animals have a greater probability of being sexually mature than smaller individuals of the same age, and older individuals have a greater probability of being sexually mature than younger individuals of the same body size Kasuya and Tai (1993) analyzed a sample of northern-form pilot whales obtained from small-type whaling, which selectively hunted larger individuals Therefore it was likely that body length at the attainment of sexual maturity estimated by them was biased upward to an unknown degree and age at the attainment of sexual maturity biased downward Because the differences in maturity-related age data in Tables 126 and 127 are in the direction to be expected due to the biases, the apparent difference between the two geographical forms in age at attainment of sexual maturity remains inconclusive

The observations on testicular growth in southern-form whales can be summarized as follows Weight of a single testis is about 15 g in neonates, reaches around 90 g at age 14 when rapid testicular growth starts, and attains the “mature” stage usually by age 18 at an average testicular weight of 450 g The growth in testicular weight continues at the same annual rate to reach 1000 g at around age 20, and testicular growth finally ceases at around age 27 or at testis weighs of 1500-2000 g on average (Figure 1212) The northern-form whales have heavier testes than the southern form, reflecting the difference in body size, but the testicular growth pattern is the same as in the southern form (Figure 1213)

With the rapid growth of the testis associated with sexual maturity there is a change in the diameter of the seminiferous tubules Kasuya and Marsh (1984) analyzed the relationship between testicular weight (X, g) and mean diameter of the seminiferous tubules (Y, μm) for the southern-form pilot whale (Figure 1214) The mean tubule diameter was obtained by measuring 20 tubules at the mid-center of the testis The relationship between the two was expressed by

Log Y = 01441 log X + 365452, X < 80 g

Log Y = 03828 log X + 127160, X > 80 g

The first equation indicates that testicular weight (X) is proportional to Y007 when the weight is less than 80 g, indicating limited contribution of tubule diameter to weight increase However, the latter equation indicates weight increase to be proportional to Y26 The rapid weight increase after age 14 years is mainly due to increase in tubule diameter The correlation was almost lost for testes weighing over 1500 g, which suggests that size of

Body Length and Age at the Attainment of Sexual Maturity of Male Short-Finned Pilot Whales off Japan

testes over 1500 g is likely a reflection of individual characteristics, not a reflection of growth stage or seasonal change This agrees with the observation that adult males of large body size tend to have heavier testes (see the following text in this section)

This analysis suggested a strong correlation between sexual maturity and diameter of the seminiferous tubules Figure 1215 presents the relationship between age and seminiferous tubule

of 15-16, when it started a rapid increase that continued until ages 18-20 Then a slower increase in the average diameter continued until around age 25 These features are similar to those observed in the growth in testis weight

Testicular weight showed great individual variation, ranging from 700 to 3000 g among individuals over age 27 where testicular growth had been completed One of the factors behind this was the tendency for males of larger body size to have heavier testes, which was supported by the facts that the correlation between age and body length was lost at age 27 and above (Figure 1221) and that between age and testis weight was lost at age 24 and over (Figure 1212), but there was a positive correlation between testis weight and body length among males of over 46 m (Figure 1212), which were again likely to have ceased growing Another factor behind the individual variation in testis weight among fully grown males was the possibility of seasonal fluctuation in reproductive activity, for which we did not have firm evidence but was suggested by wide individual variation of tubule diameter of 150-300 μm for males at age 27 or older (Figure 1215) Future study of the male reproductive cycle should be directed toward both possibilities of a seasonally synchronous reproductive cycle as well as a nonsynchronous, less seasonal, reproductive cycle

12.4.3.3.3 Ability to Reproduce Spermatozoa produced in the testis are transported to the epididymis for maturation and are stored in the epididymal lumen, which opens to the seminal vesicle Formation of spermatozoa alone is not evidence of the ability to reproduce They have to be stored in sufficient quantity in the epididymis for reproduction

Kasuya and Marsh (1984) examined development of the epididymal lumen with age in southern-form pilot whales At “immature” the lumen was simple and the epithelium little folded, in “early maturing” it had slightly developed folds, and in “late maturing” and “mature” testis the lumen was fully folded and showed no difference between the two testicular stages Thus maturation of the epididymis seemed to precede that of the testis

Detection of spermatozoa in the epididymis and testis is considered more effective with a smear than through examination of histology of the tissues, presumably because sperm at low density could be lost during the preparation process or localized in distribution (Kasuya and Marsh 1984) A smear was taken from each formalin-fixed tissue sample, dried, and stained with a solution of toluidine blue for light microscopy The testicular smear showed that some spermatozoa were present in 25% of testes that were classified as “immature” by histology This contrasted with the fact that only 5% of individuals with a negative testicular smear were positive in testicular histology (ie, classified at “early maturing” or later stages) This proved the higher efficiency of smears in detecting small amount of spermatozoa in the tissue

Density of spermatozoa in the smear was classified into the following five stages The microscopic field used in the classification was 182 mm in diameter

2 Doubtfully present: Very few, or only 1-2 spermato-

zoa in several fields, 3 Scanty: Fewer than 10 spermatozoa in each field, 4 Intermediate: Up to the maximum level found in an

testicular smear of an adult, 5 Copious: Density usually found only in epididymal

smear of fully grown male

Histological testis maturity stages are compared with sperm density in testicular and epididymal smears in Table 128 Among 45 individuals that showed no spermatozoa in a testicular smear, only one (2%) had spermatozoa in an epididymal smear This was reasonable, although the single case could indicate some deficiency of the method This contrasted with the fact that out of 99 individuals that had spermatozoa in a testicular smear, 12 (12%) had no spermatozoa in an epididymal smear These results indicated a lag between start of spermatogenesis in the testis and the arrival of spermatozoa to the epididymis

Density of epididymal sperm is compared with testicular maturity in Table 128 The proportion of males having spermatozoa in the epididymis increased from “early maturing” (7 out of 11 males, or 70%) and “late maturing” stages (47 out of 9 males, or 78%) to the “mature” stage (100% of 69 males) This showed that spermatozoa were transported to the epididymis in most of the spermatogenic males However, it was also true that sperm density in the epididymis increased with progress of histological maturity of the testis from “early maturing” to “mature” This was also shown by the fact that only 3 individuals (33%) out of 9 “late maturing” males showed epididymal sperm density of Stages 4 and 5, while 58 individuals (84%) out of

with “late maturing” testes showed epididymal sperm density lower than the density found in males having “mature” testis (Table 128) This fact throws some doubt on the conclusion of Kasuya and Marsh (1984) that all the males at the “late maturing” stage would be as functionally mature as males at the “mature” stage

Figure 1216 shows the relationship between epididymal sperm density and age of southern-form pilot whales A small number of spermatozoa first appeared in the epididymis at around 9 years, the highest Stage 5 appeared at age 15, and correlation between epididymal sperm density and age was almost lost at age 16 Individuals of the lower epididymal sperm densities, Stages 1 and 2, were not present at age 18 and higher This suggested that males with epididymal sperm density Stages 4 and 5 were physiologically capable of reproduction (Kasuya and Marsh 1984) The age of 16-18  years when epididymal sperm density reached full densities (Stages 4 and 5) almost agreed with the age of 17, when testis histology reached the “mature” stage Thus, it is correct to say that males of these stages, that is, histological “mature” stage or epididymal Stages 4 and 5, are physiologically capable of reproduction, and that about half of the males with testis at the “late maturing” stage also have reached the stage

I have already questioned whether all the “late maturing” males are capable of reproduction to the same degree as “mature” males, but there remains another question, whether all the “mature” males and some “late maturing” with high epididymal sperm density really participate in reproduction

TABLE 12.8 Sperm Density in Epididymal and Testicular Smears Compared with Histological Maturity of Testis of Southern-Form Short-Finned Pilot Whales off Japan

This question relates to so-called social maturity, which is a function of male interactions for access to estrous females as well as female choice of mating partners Kasuya and Marsh (1984) concluded from analysis of school structure of southern-form plot whales that “early maturing” or “late maturing” males were not functioning equally with “mature” males in their community, which suggested that these maturing males were not participating in reproduction equally with “mature” males (Section 12534) Northern-form pilot whales showed a similar feature as the southern form in age-related change of sperm density in testis and epididymal smears (Figure 1217)

In summary, males of both northern-form and southern-form pilot whales by age 17-18 reached a stage where the entire testicular tissue underwent spermatogenesis and the sperm density in epididymis reached a plateau (ie, correlation between sperm density and age was lost) They were considered to have attained the physiological capability of reproduction at that stage We do not have evidence that spermatogenetic activity declines at higher age, but at the same time we do not know if male reproductive activity remains at the same level for their life from ages 17-18 to 45 years at maximum

12.4.3.3.4 Seasonality in Reproduction Analyses of fetal body size of southern-form whales revealed that conception occurred in all months of the year, with a peak in the 5 months from March to July and a trough in the 5 months from September to January (see Section 12442) In  order to determine whether males have this seasonal change in reproductive activity, Kasuya and Marsh (1984)

diameter, and sperm density in testicular and epididymal smears Average testis weight at each histological maturity stage did not show seasonal change, which could have been due to the limited sample size relative to the large individual variation in weight or to parallel seasonal change in maturity stages and weight They next selected males measuring over 4 m, which excluded most “immature” and some “early maturing” males (Figure 1212), and stratified them into two groups of December and May-July in an attempt to find seasonal change in testis weight This analysis also failed to reveal seasonal change

Mean diameter of the seminiferous tubules was compared between the high-conception months of May-July and lowconception month of December by testicular maturity stage and body-length groups A significant but minor difference was identified in only one case Mean tubule diameter of males over 460  cm, which were considered fully grown animals (Figures 1212 and 1221), was significantly greater (p  <  001) in the high-conception months (217 μm, n = 21) than the low-conception month (193 μm, n = 14) This result suggests the possibility of some limited degree of seasonal changes in reproductive activity of adult males, but further confirmation is needed using larger samples

The analysis presented earlier suggested the possibility of greater mean diameter of seminiferous tubules of adult males during the mating season, but it did not distinguish between two possible underlying mechanisms, that is, whether the proportion of active males increased or all males increased activity synchronously We learned by examining males with testis weighing over 600 g (Table 129) that there were numerous active males even in a season of low conception frequency and that there were numerous males with high epididymal sperm density in every month of the year This indicates that reproductively active males are available for estrous females throughout the year, which is reasonable for the population of southern-form whales where estrus occurs in every month of the year Many males are ready, with some cost, for estrus of females that may occur only once in several years

TABLE 12.9 Seasonal Fluctuation of Sperm Density in Epididymal Smear of Southern-Form Short-Finned Pilot Whales off Japan, for Males with Testis Weighing 600 g or More Which Can Be Judged Sexually Mature (see Figures 12.12 and 12.13)

in the lower bound of the weight of a testis with spermatogenesis using sperm density in the testis and epididymal smears as indicators They noted the range between minimum testis weight with spermatozoa and maximum testis weight without spermatozoa and tested whether the range differed between the high-conception months (May-July) and low-conception months (December-January) The range for the epididymal smear was 50-80 g in the high-conception months and 140-180 g in the low-conception months The testicular smear also showed a similar seasonal trend: 40 g in the high-conception months and 90-160 g in the low-conception months In a comparison between samples from the same season, the range for the epididymal smear was always greater than the range for the testicular smear This reflects the lag between the start of spermatogenesis in the testis and transportation of the produced spermatozoa to the epididymis It was unlikely that all males in the range had the physiological ability to reproduce, but their physiology was probably responding to seasonal change in the environment as in the case of adult males

12.4.3.4 Growth Curve A growth curve is a way of describing age-related change in body size Body size can be expressed as body weight, head and body length, or head to tail length As weight is difficult to obtain for cetaceans, the last is often used and customarily called “body length” This is a linear length measured on a body placed on a flat place from the anterior-most point of the upper jaw (or head) to the base of the notch at the center of the tail flukes This principle has generally been accepted by biologists working on short-finned pilot whales but has caused trouble for some of them (Yonekura et al 1980) The tip of the upper lip is located at the anterior-most point of the head in young pilot whales, but it becomes covered by a fatty tissue body called the melon that develops between the upper lip and the blowhole and is located aft of the foremost extent of the melon at a body length of 240-300 cm or ages of 2-5 years Thus, the rule for measurement defined earlier causes anatomical inconsistency of the measurement occurring around the ages of 2-5 years

If body length of a particular individual is recorded for life and plotted on age, a growth curve for the individual will be obtained Growth curves thus obtained will be different between individuals A fast-growing individual is larger than other individuals of the same age, will show a pubertal growth spurt at a younger age, and may cease growth at an earlier age The opposite might be true for slow-growing individuals Averaging these growth curves creates a mean growth curve, which will not match any individual’s growth

Even beyond the time and cost required to construct the growth curves of individual dolphins, it is technically difficult to maintain even one short-finned pilot whale in good health for tens of years in captivity Some small cetaceans in captivity are known to have reached sexual maturity at ages younger than expected for wild animals, but those in captivity are also known to have a shorter life In order to avoid such difficulties and utilizing available fishery data, there have been attempts

fishery and to plot the average body sizes on ages estimated from tooth reading Such samples may cover just a few seasons or several years The growth curve thus created should be called a “pseudo”-mean growth curve, but cetacean biologists usually call it a “mean growth curve” This pseudo-mean growth curve can be accepted as a real mean growth curve only when the assumption is accepted that the growth pattern of the population did not change during the period covered by the sample, that is, the sampling period plus the lifetime of 50-60 years for short-finned pilot whales If growth rate has increased through improvement of nutrition during the period, the pseudo-mean growth curve gives the impression that body size decreases at high age, which has been reported for sperm whales in the western North Pacific (Kasuya 1991)

Figure 1218 shows body-length frequency of southernform short-finned pilot whales randomly examined from the catch of drive fisheries in the 15 years from 1965 to 1980 It reveals features such as (1) sex ratio biased to females, (2) a female peak at around 360 cm and that of males at around 470 cm, and (3) male maximum size that is about 1 m greater than that of females The first is explained by sexual segregation or longevity difference, and the latter two by sexual growth difference The body-length composition of northern-form short-finned pilot whales has a similar difference between sexes in body size, where males are greater than females by about 17 m (Figures 1219 and 1220) The sex ratio is biased toward males due to fishery selection for larger individuals

The “pseudo”-mean growth curves created using the data obtained earlier are shown in Figures 1221 and 1222 They are forced to pass through the mean neonatal lengths estimated earlier at age zero Most of the individual body lengths come within a range of two standard deviations on each side of the mean, or within 6%–10% of the range on each side of the mean length of southern-form whales aged at or over 1 year

However the standard deviation of southern-form whales aged between 0 and 1 was quite large, because their growth was rapid and any difference in birth time had a large influence on the body size of these individuals Further details of these data on southern-form whales, including sample size, mean body length, and standard deviations, are available in Kasuya and Matsui (1984)

Kasuya and Matsui (1984) described the mean growth curve of southern-form pilot whales in three stages The first stage was the period from birth to age of about 125 years, when growth was extremely fast and the whales reached an average length of 230 cm The mean growth rate of this 125-year period was 724 cm/year, which was 621% of the growth rate in the linear phase of fetal growth The available sample did not show evidence of sexual difference in growth in the period This first phase gradually transitioned into the second phase, and the timing seemed to be later among males

The second growth phase was a period of almost linear growth, begun at around age 2 The mean body length at age 25, shortly after the beginning of this stage, was about 254 cm for males, about 6 cm greater than that for females

This stage lasted until the ages of 9-10, when females attained sexual maturity, and could be considered a juvenile period The mean growth rate at this stage was 11-12 cm/year and did not show significant sexual difference However, males of this stage were always larger than females of the same age, mainly because males remained in the previous stage for a longer period

The third stage of the mean growth curve was characterized by a growth rate declining with age, which was interpreted as a reflection of decreasing growth rate of some individuals and increasing proportion of whales that had ceased growing Females entered this stage at around age 9 and ended it at around age 22, while males entered it at 10 years and remained there until age 27 The end of this stage should agree with the ages when all whales of a sex have ceased growing

The mean growth curve of males had one unique character This was a slight increase in growth rate at around ages 11-14 years or at the beginning of the third stage, a reflection of the pubertal growth spurt The available data were not sufficient to clarify individual variation of the timing and magnitude of the pubertal growth spurt, but the timing apparently agreed with the age when males enter the “early maturing” stage of testicular histology The “mature” stage was attained at a later age, or at 15-22 years The pubertal growth spurt is known in some other mammals, including pinnipeds and primates Among humans the growth spurt is distinct in an individual growth curve, but it is indistinct in a mean growth curve because the spurt lasts for a short period with broad individual variation in timing The same is expected for males of the short-finned pilot whale

A pubertal growth spurt is often observed in mammals where males grow larger than females and is thought to have evolved accompanied by a polygynous mating system that increased inter-male competition for mating opportunities However, the degree of sexual dimorphism does not necessarily reflect the degree of polygyny in a particular species or population There is no reason to assume that the mating

system and sexual dimorphism are in parallel A pubertal growth spurt could have followed development of a polygynous mating system, and abandonment of polygyny for some reason could have preceded the change in growth pattern In short, social structure and reproductive behavior in toothed whales are very flexible (Connor et al 2000), probably more flexible than growth pattern Killer whales are one of the species with distinct sexual dimorphism, but studies on the species off the Vancouver Island area has not produced evidence that they have strong inter-male competition for mating opportunities (Baird 2000)

Figure 1222 compares the mean growth curves of the two forms of short-finned pilot whale off Japan The mean growth curves of the northern form are likely to be upwardly biased to an unknown degree, because the samples were obtained from small-type whaling that selectively took larger individuals (the fishery had no minimum size limit but a quota set by number) The bias could be greater for females than males, and greater for individuals close to the lower bound of length in the catch, which was about 3-35 m (Figures 1219 and 1220) Thus the mean growth curves for ages below 10 are of limited reliability For both types of pilot whales the correlation between mean body length and age is lost at ages 25-30, when all the individuals are believed to have ceased growing (Kasuya and Tai 1993) Table 1210 gives mean body lengths at this stage, which are indirect estimates of mean body length at physical maturity Physical maturity is defined as evidenced by the complete fusion of the vertebral epiphyses to the centra, but examination of the vertebral epiphyses is often difficult for fishery-derived materials (Sections 9410 and 1345)

12.4.4.1 Fetal Growth and Gestation Time Huggett and Widdas (1951) found that the cube root of fetal weight plotted on time after conception falls on a line that is upwardly concave at the beginning and then linear until parturition The time (t0) when the left-ward extension of the linear growth phase crossed the axis of time was a

Mean and the 95% Confidence Interval of Body Length at Physical Maturity of Short-Finned Pilot Whales off Japan

0 = 01tg for species with  tg > 400 days, but the proportion increased for species with shorter gestation (Section 8522) Laws (1959) tested this rule on cetacean fetuses using body length as the indicator of body size and found that the value of t0 was 09 of t0 using the cube root of body weight This means that t0 = 009tg for gestation of tg > 400 if fetal size is expressed by body length This principle has been frequently used in the analysis of fetal growth of cetaceans

Figure 1223 presents the body-length frequencies of fetuses and juveniles of southern-form pilot whales taken by drive fisheries on the Izu coast and at Taiji The June-August sample had two major modes, one of near-term fetuses at around 130 cm and another of small fetuses below 10 cm, but the October-February sample had only one major mode at 40-100 cm With the assumption that these seasonal changes in fetal size reflected growth of the smaller fetuses and birth of the near-term fetuses, Kasuya and Marsh (1984) separated the fetuses into two arbitrary cohorts of conception divided by a dashed line in Figure 1223 and calculated mean body length of the cohort for each month Some neonates in the June-August sample were included in this calculation to obtain better resolution of seasonal growth

Out of the 11 mean body lengths, 9 from October to the next October fell on a line, but the 2 means representing small fetuses in June-August appeared above the line This was explained by the fact that the sample of small fetuses represented conceptions in the early part of the mating season The possibility of overlooking some small fetuses cannot be completely excluded, but Kasuya and Marsh (1984) considered that the possibility was small because uteri accompanied by a

regression to individual fetal lengths (Y, cm) representing the 9 means on number of days after the first of January (X), and obtained the following fetal growth equation:

Y = 03386 (±00425) X − 601, r = 082

The 95% confidence interval is given in parentheses (A regression fitted to the 9 mean values in Figure 1223 was expressed by Y = 03398 X − 601, which was very close to the equation fitted to the individual fetuses) The estimate of 03386 cm/day is the mean growth rate in the linear part of fetal growth The equation cut the axis of time on June 26 and reached the mean neonatal length of 140 cm (Section 12431) on August 11 (Figure 1223) Thus, the value of (tg − t0) was calculated as 411 days and total gestation period as 452 days or 149 months (assuming a month of 304 days) Some possible problems that might arise in the process of identifying conception season and fetal growth rate are reviewed as follows

The first problem was missing small fetuses during the field work That could happen for two reasons, and it would cause loss or bias in information on the conception season One potential reason was observation error by the scientists This error could be avoided if the whole uterus were collected together with ovaries that contained a corpus luteum for later careful examination, including histology of the endometrium The other potential reason was miscarriage at death in pregnant females I have confirmed this in both forms of pilot whale by finding a fragment of the placenta remaining in the intact uterus or a small fetus in the vagina Some fetuses, particularly those of early pregnancy, were delivered when the females were slaughtered by drive fishermen or shot by whaling cannon Histological examination of the endometrium helps to minimize both types of misidentification Kasuya and Marsh (1984) examined the endometrium of most of the southern-form females and Kasuya and Tai (1993) and Kasuya et al (1993) that of all the sexually mature females (both forms) They identified early pregnancy with an embryo of 15 (Table 1218) or 23 mm (Kasuya and Tai 1993) by a network of blood vessels developed beneath the epithelium, which was followed by development of epithelial villi

The second problem was inclusion of some postnatal specimens in the calculation of the growth regression It was theoretically correct to include some neonates that shared a conception peak with near-term fetuses, but inclusion of neonates of a broader age range would bias the fetal growth rate downward because the postnatal growth rate was slower than that of fetuses

A third problem comes from the fact that the growth rate of fetuses in the early period of gestation is slower than that in the later linear growth phase If data from small fetuses are included in the regression, it would underestimate the growth rate in the linear phase of growth This could cause a problem in the same manner as in the fourth problem mentioned in the following Kasuya and Marsh (1984) omitted fetal data that represented the ongoing conception peak to avoid this situation

tion season As seen in the fetal records for southern-form whales in June-August (Figure 1223), the sample obtained during a mating season underrepresented small fetuses to be conceived later in the season The effect of this bias could be decreased by excluding particular samples To the extent that we estimate fetal growth rate from the regression of body length on date, the obtained rate is not perfectly free from the possibility of such bias due to an extended breeding season (Martin and Rothery 1993) The problem of an extended mating season in the analysis of fetal growth also relates to grouping of fetuses by body length If the boundary between two fetal groups, a dashed line in Figure 1223, was incorrect, the resultant fetal growth rate and gestation time was incorrect

Information on the gestation period was obtained for some cetaceans in captivity at Sea World in the United States, where the start of conception was determined by monitoring the progesterone level in the serum or urine (Asper et al 1992) Mean gestation periods thus obtained were 345 days (n = 8) for Commerson’s dolphin, Cephalorhynchus commersonii, that were born at 100 cm, 370 days (n = 77) for the larger bottlenose dolphin (born at 117-127 cm) and 515 days or about 169 months (n = 7) for the much larger killer whale (born at 219-235 cm)

Many baleen whale species have annual migrations between feeding grounds in higher latitudes and breeding grounds in lower latitudes, which places a constraint on the gestation period, maintaining it at around 12  months Thus they are forced to increase their fetal growth rate while achieving augmentation of body size, both neonatal size and adult size Augmentation of body size benefited their breeding that occurred during winter months of starvation Some Bryde’s whales apparently do not have large-scale annual migrations and perhaps no seasonality of breeding, but they still seem to maintain gestation of about 1 year This is probably a reflection of their earlier life history Some toothed whales, on the other hand, stay in a similar environment for the whole year, are free from a seasonal constraint on reproduction, and extend the gestation time while achieving augmentation of body size (Kasuya 1995b) Such toothed whale species include female sperm whales, Baird’s beaked whales, short-finned pilot whales, and some killer whale populations

The fetal growth curve of the southern-form pilot whale matched reasonably well with fetal length frequency, and the estimated gestation period was not unreasonable in view of the gestation period known from some aquarium-reared species Perhaps the exclusion of small fetuses from the regression could have avoided the problem identified by Martin and Rothery (1993) They simulated the best fetal growth rate to meet both the observed fetal length frequency and assumed conception timing of long-finned pilot whales in the North Atlantic and concluded that the gestation period was 12 months I cannot conceive a convincing explanation why two species of similar body size in a genus could exhibit such different gestation times One possibility would be that a seasonal environmental cycle forced the long-finned pilot whale in higher latitudes to maintain parturition at a

whales (Kasuya 1995b)

12.4.4.2 Breeding Season 12.4.4.2.1 Southern Form Linear fetal growth of the southern-form whales reached the mean neonatal length of 140  cm on August 11 (see above) This was an estimate of mean parturition date of the population The monthly distribution of births was calculated by fitting the mean fetal growth rate to the body lengths of fetuses and date of the data, and a normal distribution was fitted to the distribution (Figure 1224) Births had a peak in July and August and a trough in December-March Another set of birth dates was obtained by back-calculating body lengths of juveniles below age 10 using their mean growth curve (bottom panel of Figure 1224), but the seasonal pattern did not agree well with the pattern obtained from the fetuses The disagreement was probably due to inferior accuracy of the postnatal growth curve

Several factors could have caused bias in the estimate of parturition season Error in the fetal growth rate biases birth date The bias is greater for dates calculated from smaller fetuses than those calculated from larger fetuses The fetal

for a correct estimate of the parturition season If females of near-term pregnancy tended to live outside the fishing ground, the resultant parturition peak would come after the real peak A seasonally biased sample may result in a biased parturition season The sample used in Figure 1224 had some seasonal bias and lacked data for March-May and September The season March through May corresponds to the early mating season and the beginning of the parturition season, and the lack of data for near-term fetuses for these months had the effect of placing the calculated parturition peak artificially later The absence of data for September had the opposite effect The total effect of these deficits in the samples was not evaluated by Kasuya and Marsh (1984)

The monthly distribution of conceptions is estimated by sliding forward from the monthly parturition date by 149 months or the estimated gestation period, which suggests a conception peak in May and a trough in November This is the best estimate currently available of the mating season of the southern-form pilot whale

12.4.4.2.2 Northern Form The biological data for the northern-form whale were obtained mostly in October and November, with a small number of samples in September due to the fishing season agreed between the whalers and the Fisheries Agency (Kasuya and Tai 1993) The small-type whalers used to make a slit in the abdomen of the whale carcass to cool it with seawater during on-deck transportation of several hours or towing for flensing at Ayukawa This often caused loss of fetuses in the sea, large fetuses in particular The whaling gunners retained some large fetuses found during the process for scientists when requested to do so (Kasuya and Tai 1993) This was one of the reasons why the histology of the endometrium had to be examined for confirmation of pregnancy The short sampling season and the biased fetal size inhibited applying the method used for the southern form in the analysis of reproductive seasonality of northern-form pilot whales

Kasuya and Tai (1993) analyzed fetuses measuring between 23 and 180 cm obtained in October and November, but their material should have contained two pregnant females later identified with embryos of 15 mm (Table 1218; Kasuya et al 1993) This suggested that conceptions occurred throughout the year as in the southern form However, the fetal length distribution suggested that seasonality of breeding was likely to be more distinct in the northern form (Figure 1225) Two peaks were identified in fetal size, one of small fetuses below body length of 15 cm and another with large fetuses of over 150 cm The latter were considered underrepresented in the sample Interpretation of the body-length difference between the two fetal modes, about 135  cm, was a basis for understanding reproductive seasonality

Mean neonatal length was estimated at 140  cm for the southern form and 185  cm for the northern form (Section 12431) The following equation between mean neonatal length (X, cm) and fetal growth rate in the linear phase of fetal

growth (Y, cm/day) applies to several species of Delphinoidea (Kasuya 1977):

Y = 0001462 X + 01622

Substituting the mean neonatal body lengths in this equation gave the following estimates of average fetal growth rate:

Southern form: 03668 cm/day Northern form: 04327 cm/day

The figure for the southern form was slightly greater than the corresponding figure of 03386 cm/day estimated directly from the fetal size distribution (Section 12441) and corresponded to a gestation period of about 1 month shorter than the estimate based on the fetal size distribution This suggests that the fetal growth rate predicted for the northern form likely underestimates the gestation period by about 1 month Using this possibly upwardly biased fetal growth rate, a minimum length of time between the two fetal modes, that is, 15 and 150 cm, was estimated:

(150 − 15 cm)/(04327 cm/day) = 312 days or 103 months

Even with the difficulty of determining the start and end of the mating season, it is safe to conclude from the given that the two fetal modes of the northern form observed in the October-November sample represented conceptions in 2  successive years (Kasuya and Tai 1993)

The calculation indicates that seasonality of mating in the northern form was unimodal as in the southern form, and that two successive mating peaks were 1 year apart Comparison of fetal size between October and November revealed an additional feature of the mating season (Figure  1225)

of fetuses at 5-10  cm, but this was reversed in November This also suggests that the mating peak had already passed in November and that the mating peak for the population was short However, if it is accepted that it took about 2 months for a fetus to grow to 15 cm (Kasuya et al 1993), then the mating season could have already started in early September, had a peak in October, and ended in December This allows about an 8-month interval between the two periods of high mating activity in successive years

Although we currently have insufficient data to draw firm conclusions on details of the mating season of the northern form, it is possible to say that most conceptions occur from autumn to early winter with a peak in October/November and in a more seasonally limited period than in the southern form (Kasuya and Tai 1993)

The larger fetuses of the northern form had a mode at around 160  cm in October/November It would take about 2 months before they grew to the mean neonatal length, that is, 58 days = (185 − 160)/0433 This means that parturition peaked in December/January This together with a possible conception peak in October/November suggests a gestation period of 14-15 months, which is reasonably close to the corresponding figure for the southern form

Uncertainty remains about seasonality of reproduction of the northern form due to small sample size, the short season covered by the sample, difficulty in obtaining near-term fetuses, and unavailability of neonates However, the currently available data suggest that the two forms of pilot whale off Japan mate about 5-6 months apart and that the northern form is a more seasonal breeder No evidence exists for a difference in gestation period between the two forms (Kasuya and Tai 1993)

12.4.4.3 Weaning Juvenile dolphins start taking solid food at the age of a few months, the start of the process of weaning The amount of solid food they consume increases and the proportion of nutrition from milk decreases with time until suckling finally ceases, the completion of weaning The period from the start of solid food ingestion to the end of suckling is called the weaning period There is evidence that the weaning period of the southern form extends for several years The weaning period functions as a period of learning foraging technique and adapting digestive physiology from milk to marine organisms However, only 6-12 months is needed for this function, as seen in the finless porpoise (Section 8523) and Dall’s porpoise (Section 946) Even herbivorous mammals such as horses, which must undergo greater physiological adaptation during the weaning period, start taking solid food at 2 months and complete weaning by the age of 6 months

Human infants start eruption of deciduous teeth at age 6 months, when taking of solid food may start, and complete the full set of teeth at around 25 years Completion of weaning among humans is affected by culture and availability of other sources of nutrition In the current Japanese community

longer in the past In the agricultural community of Kawagoe in the 1930s, where I was raised, it was not uncommon to suckle until the age of 3-4 years and in rare cases until the age of 6-7 years, close to the age for beginning elementary school The nutritional contribution of such extended suckling is questionable As lactation may suppress estrus, extended nursing can adversely affect the reproductive success of mothers The extended weaning period of some mammal species is likely explained by some function other than nutrition, as first proposed for cetaceans by Brodie (1969), who thought that the relatively long lactation period of toothed whales could function as a period of education or protection by the mother

Humans have two sets of tooth germs at birth that grow and erupt successively, which is called diphyodonty Sometime after completion of eruption of the deciduous teeth in humans, they start to be replaced by permanent teeth The situation is different among the recent toothed whales, which have only one set of teeth, a state called monophyodonty (Section I13) Tooth eruption starts in many toothed whales at the age of a few months, but it may occur much later in some species In sperm whales, tooth eruption starts at age 5-18 years (mean 9  years), which agrees with female age at sexual maturity and male age at puberty (Ohsumi 1963, in Japanese) Beaked whales (Ziphiidae) have erupted teeth usually only in sexually mature males; females usually have no erupted teeth (McCann 1974) These species mainly feed on squid using suction feeding, which does not require functional teeth (Marshall 2009) The southern-form pilot whales off Japan feed almost exclusively on squid, and the structure of the broad oral cavity is apparently suited for suction feeding

The drive fishery at Taiji in Wakayama Prefecture drove schools of southern-form pilot whales into a harbor for slaughter Juveniles in the school often died in the enclosure before being killed by the fishermen and were found floating in the water sometime after death The fishermen tied these juvenile carcasses together in the port before towing them to sea for dumping The scientists used such occasions to examine tooth eruption (19 individuals of 136-271 cm) or stomach contents (8 individuals ranging from 180 to >258 cm) (Kasuya and Marsh 1984)

Five newborns (136-142  cm in body length) and three older individual (154-182 cm and aged 1/10-1/4 year) examined by Kasuya and Marsh (1984) had no erupted teeth Three other individuals had erupted teeth only in the upper jaw at body lengths of 170, 190, and 207 cm and ages 1/4, 1/4, and 3/4 year, and eight individuals had erupted teeth in both jaws at body lengths of 163-272  cm and ages 1/4, 2/4, 3/4, and >20 Eruption started with teeth near the middle of the tooth row and advanced toward both ends of the row The ages were estimates based on annual growth layers in the dentine, and precision was poor for ages below 1 year The results suggest that upper teeth erupted in some individuals at age of 1/4 year and on all the individuals before the age of 3/4 year, soon followed by eruption of the lower teeth

The eight individuals examined for stomach contents were aged >1/2 year and had body lengths of >180 cm All of these

beaks, shrimp, or both) in the stomach The youngest of them, 180 cm long and aged 1/2 year, had squid beaks and shrimp remains in the stomach (no observation on tooth eruption) The squid beaks were seemingly smaller than those found in stomachs of adults driven in the same school I should have examined details of prey size to confirm whether young calves in the weaning stage selectively consumed smaller squids than those taken by adults Kasuya and Marsh (1984) did not examine individuals positively identified as having milk but no solid food in the stomach Another four individuals had only squid beaks in the stomach and were aged at 2/4, 3/4, 25, and 35 years Squid beaks and milk were found in a 25-year-old male, 25-year-old female, and two individuals of unknown sex whose ages were estimated at ≥25 and ≥30  years from teeth taken from sexually unidentifiable severed heads Five of the eight individuals were examined for tooth eruption as well as stomach contents One of them (aged 3/4 year) had erupted teeth only in the upper jaw and the other four had erupted teeth in both jaws

From these data, Kasuya and Marsh (1984) concluded that southern-form pilot whales start taking solid food at around 6  months of age and continue suckling at least to age 30 years They thought that the data were insufficient to determine the age at completion of weaning, because of the small sample size and difficulty in visually detecting small amounts of milk mixed with solid food in the stomach As noted earlier, nutritional requirement for milk at such high ages is questionable

Subsequent studies of long-finned pilot whales in the North Atlantic confirmed that they start taking solid food at age 65 months as in the case of short-finned pilot whales and that some individuals continue suckling until age 7 (males) and 12 (females) (Desportes and Mouritsen 1993) Such extended suckling has also been deduced for the southern-form shortfinned pilot whale by an indirect method

Examination of a limited number of juveniles led to the following conclusions on the early growth of southern-form pilot whales Tooth eruption starts at around 3-6 months Feeding on solid food is likely to accompany tooth eruption and starts by age 6 months, but some individuals continue suckling at least to the age of 3 years The stomach contents analysis did not exclude the possibility of suckling at greater ages

12.4.4.4 Lactation Period 12.4.4.4.1 Determining Lactation Lactation in short-finned pilot whales is easily identifiable, in most cases, by pressing the lactation externally, but slitting the gland is recommended for better accuracy If the situation permits, lactation status recorded in the field should be confirmed by histology of the mammary gland Pressing the grand externally will not be sufficient for carcasses of whales near the end of lactation Also, histology will be required for carcasses of whales that have been dead for a long time Histological examination of the mammary glands was not carried out for some southern-form whales (Kasuya and Marsh 1984) but was

field records (Kasuya and Tai 1993) The mammary sinus in cetaceans may contain a brownish liquid of variable coloration and viscosity Mammary glands of such females did not show secretory activity and were judged not lactating The liquid could have been a remnant from a previous lactation

Females with a full-term fetus often secrete colostrum Colostrum is identified through examination of the uterus and ovaries or through histology of the mammary gland, where milk in the mammary sinus contains numerous eosinstainable colostrum globules If colostrum secreted before parturition is misidentified as remnants of lactation associated with a previous parturition, this causes a serious error in estimation of the reproductive cycle and pregnancy rate A fetus may be aborted when the female is killed by harpooning This can be identified histologically by presence of a developed endometrium and dense underlying blood vessels (Section 12445) Although such an unusual abortion cannot be distinguished from an abortion due to a natural cause that has occurred just prior to the death in the fishery, such cases must be rare

The color of the milk of short-finned plot whales varies from creamy white to a green color similar to that of vegetable juice The viscosity is like that of cow milk and has no relationship with coloration I have seen milk with the green tinge in both the southern-form and northern-form pilot whales but never in other cetaceans The frequency of green milk did not change with postmortem time or time between drive and slaughter, but it apparently changed with season Out of 72 southern-form females in lactation, 39 secreted milk with various degrees of green tinge, the proportion varying from 0% (n = 17) in December, 20% (n = 5) in January to 77% (n = 17) in February, 82% (n  =  17) in June-July, and 69% (n = 16) in October The proportion of green milk was highest in summer Kasuya and Marsh (1984) thought from this seasonal change that the green pigmentation had some relationship with the food consumed by the female Through my histological examination of mammary glands of most of the southern-form females, I  identified only one case of pathology, suggesting that the green milk was not a pathological symptom Ullrey et  al (1984) analyzed milk composition of a female Mesoplodon stejnegeri, which live-stranded 20-40  days after parturition They noted that the milk had a blue-green color and identified the pigment as biliverdin, but they refrained from conclusion about the function of the pigment in the animal Biliverdin is one of the bile pigments and is contained in the bile fluid of herbivorous mammals The green pigment in milk of short-finned pilot whales could have been of the same type as observed in the beaked whale

In conclusion, colostrum may be secreted when approaching parturition and it must be distinguished from lactation associated with previous parturition Short-finned pilot whales and some other toothed whales may secrete milk with various degree of a green tinge Histological examination of the mammary gland is recommended for final determination of lactation status

Females in a School

Kasuya and Marsh (1984) compared the age composition of juveniles with the number of lactating females driven together in a school of southern-form pilot whales and attempted to identify possible suckling calves One example is shown in Table 1211, which lists composition of a school of 20 individuals driven at Taiji, believed by the fishermen to have contained all the members of a school found at sea We tentatively accepted the judgment of the fishermen, albeit without firm supporting evidence Three whales in the school were slaughtered and processed before my arrival at the fishing village I examined their viscera stored on the flensing platform and confirmed that they were sexually mature females either lactating or resting but certainly not pregnant The ages and status of mammary glands of these three females were unknown because their heads and mammary glands were discarded before they could be examined

Including six females positively identified as lactating and the three females not examined for mammary gland, this school could have contained 6-9 females in lactation If it is assumed that sexually mature individuals were not suckling, there were seven candidates for suckling animals The nursing system of the short-finned pilot whale was unknown There were three possibilities: (1) female nurses only her own calf, (2) female nurses her own calf as well as calves of other females, (3) female nurses younger calves of other females after weaning her own calf The first and second possibilities suggested that at least six calves among seven aged 0-16 years, or more, probably a minimum of six calves at 0-13 years of age, were suckling The third alternative, which seemed less

ling but still suggested that there was a female that continued lactation for 13 years

Kasuya and Marsh (1984) carried out a similar analysis on 12 schools driven at Taiji as summarized in Figure 1226, which shows the age composition of estimated suckling and weaned juveniles for driven groups that were believed by the fishermen to contain all the members of a school Some individuals were judged as weaned at age 2-3 years The proportion of suckling individuals decreased with age of the calf, reached 50% at age 4-5, and went to almost zero at ages over 10 years However, some males were classified as suckling at age 13 (2 males) and 15 (1 male) This result alone does not indicate that males suckle longer than females, because of the assumption that sexually mature individuals are not suckling

TABLE 12.11 An Example of School Composition of Southern-Form Short-Finned Pilot Whales off Japan (School No. 12 of Figures 12.26, 12.32, and 12.33)

age 11 (a female), 12 (a female), and 13 (a male)

Examination of stomach contents of long-finned pilot whales in the North Atlantic revealed incidents of high-age suckling, by a 7-year-old immature male and a 12-year-old pregnant female (Desportes and Mouritsen 1993) It would be extremely interesting if we could know the family structure where a sexually mature female suckled from some other female It is not generally an easy task to identify small quantities of milk mixed with remains of solid food in the stomach In order to overcome this difficulty, Best et  al (1984) used lactose in the stomach of sperm whales as evidence of suckling, because lactose occurs only in milk among marine organisms The oldest cases of suckling thus confirmed were a 75-year-old female and a 13-year-old male I note that these two species, particularly the sperm whale, are similar to the short-finned pilot whale in their life in matrilineal communities, presence of extended postreproductive life in females, and sexual maturity being attained in males much later than in females Extended suckling seems to be a common feature among cetaceans within matrilineal school structure

As the analysis of Kasuya and Marsh (1984) was based on several assumptions and lacked observation of the process of driving, it is hard to reach a firm conclusion on the extended suckling in the species One critical problem was the possibility of missing juveniles during the drive without this being noticed by the fishermen If the fishermen lost both mother and calf during the drive, it would not cause bias in the analysis presented earlier However, loss of calves alone could cause overestimation of weaning age, and loss of lactating females could cause underestimation The former possibility is greater than the latter However, as pilot whales live in smaller schools and remain in tight aggregations at sea, the possibility of losing particular individuals is less than in the case of other species such as striped dolphins (see Sections 1052 and 12431)

A second problem was the assumption that weaned individuals were always older than suckling calves, which was not based on any data and was likely to be wrong as suggested by the fact that older females were likely to lactate longer (Section 12444) This ungrounded assumption will not cause a bias in estimation of age when 50% of calves have weaned, but it will underestimate the upper range of length of suckling

A third problem in the analysis was ignoring the possibility of communal nursing Communal nursing is known in some matrilineal communities of mammals such as African elephants and hyenas, where females nurse their own calf as well as calves of other females Because all the mothers are related, the behavior contributes to the total reproductive success of the matrilineal group Even if this happened in the short-finned pilot whale, it would not cause bias in the estimation of the suckling period as far as each mother nursed her own calf as well However, the estimate of suckling period would be unreliable if a female continued nursing calves of other females after weaning her own calf If this happened, the estimate of Kasuya and Marsh (1984) would only have meaning as an indication of length of lactation

but possible case, where a female nurses orphans by starting lactation without conception or parturition Ridgway et  al (1995) reported cases where a captive female bottlenose dolphin placed together with an orphan calf of the same species started lactation Such an incident could occur if short-finned pilot whales were placed in the same situation in an aquarium environment, and it could be possible even in wild individuals in a cohesive matrilineal group of the species

In conclusion, matching the number of lactating females and the age composition of calves in the same school suggested that the suckling period in southern-form pilot whales lasts at least 2-3 years, half of the calves still suckle at age 4-5  years, and some few suckle to age 13-15 Even if this estimate is not accepted due to the technical questions summarized earlier, there is reason to believe that some females continue lactation for over 13 years after the last parturition

12.4.4.4.3 Lactation of Old Females Examination of carcasses of pilot whales killed in Japanese drive fisheries revealed that the oldest pregnant females were aged 355 for the southern form and 365 for the northern form (these ages may be expressed as 35 and 36 years, respectively) If they had not been killed, these pregnant females would have had their last parturition in the next year or at ages 36 and 37 (Kasuya and Marsh 1984; Marsh and Kasuya 1984; Kasuya and Tai 1993) School No 12 of the southern form shown in Table 1211 contained three females that were lactating at ages 36 or above Their ages were 36, 42, 43, and 48, which meant that they had been lactating for a minimum of 0, 6, 7, and 12 years, respectively This result matches quite well with the earlier conclusion that this school had females that lactated for 13 years and calves that perhaps suckled 13 years

Kasuya and Marsh (1984) examined the age composition of lactating females in other southern-form schools for cases of extended lactation of old females Using data common with those in Figure 1226, they constructed Table 1212 by the following procedure Lactating females over the age of the oldest known pregnant females (35 years) were extracted, and their ages were listed in column (1) of Table 1212 Their minimum lactation periods were estimated by subtracting 35 (not 36 as done earlier) from the ages as shown in column (3) This procedure ignores possible lactation before age 35 Then using the method of Table 1211, the oldest possible suckling calves were allocated to these females and their age and sex were placed in column (4) Finally, ages of these lactating females at the time of their last parturition were calculated by subtracting the age of their assumed calves from age of the lactating females at capture (column (2) of Table 1212)

School nos 18 and 22 were excluded from the analysis because they had no lactating females, and school nos 7, 14, and 15 were also excluded because they did not have lactating females aged over 35 The latter three schools did not have long-lactating females or long-suckling calves to be matched with them Schools identified with old lactating females tended to have presumed long-suckling calves (school nos 10, 12, 13, and 16) The oldest lactating female

in Table 1212 was aged 50 (which meant a minimum lactation period of 15 years), and her suspected calf was aged 14 by reading tooth layers This analysis showed that the population had females in extended lactation and that such extended lactation was likely to occur in females who had experienced their last parturition

Female southern-form pilot whales are likely to have extended lactation of 10-15 years after their last parturition

12.4.4.5 Reproductive Cycle Estrous cycles of cetaceans have been described in aquariumreared specimens (Schroeder and Keller 1990; Asper et  al 1992; Robeck et al 1993) Female cetaceans may ovulate in a mating season, mate if an adult male is available, and are likely to conceive Such a type of ovulation is called spontaneous ovulation and is considered common among cetaceans Ovulation usually occurs after weaning the calf of a previous pregnancy but may also occur soon after parturition during lactation as in the case of the Dall’s porpoise (Section 946) or near the end of lactation as suspected for some northern-form short-finned pilot whales (see Section 124452) If an ovulation is not followed by conception, the female may ovulate repeatedly during the same mating season, with an average interval of 42 days (killer whale: Robeck et al 1993) or 27 days (common bottlenose dolphin: Schroeder and Keller 1990)

4 to 12 months in a killer whale in an aquarium (Asper et al 1992) Because calves were artificially separated from the female killer whale, the derived lactation period and calving intervals (35 months in average) cannot be considered to represent the process in the natural environment

A female killer whale in captivity was reported to have mated in all periods of the estrous cycle and even during pregnancy (Asper et al 1992), but most of the copulations occurred within a total of 72 h surrounding an ovulation (Robeck et al 1993) or in a 5-to 10-day period around the ovulation (Asper et al 1992) Mating in nonestrous females was confirmed in short-finned pilot whales and was considered to be an important key in understanding their social structure (see Sections 12447 and 12 448) However, interpreting mating activity among captive animals requires caution, because it can be different from that among wild individuals

Seasonality of reproduction in the wild was maintained after introduction into an aquarium (Section 11423) Bottlenose dolphins in aquariums had 70% of their estrous period in 42% of the year (July-November) (Schroeder and Keller 1990) and killer whales in February and August (Asper et al 1992)

12.4.4.5.1 Reproductive Cycle of Southern-Form Females

Kasuya and Tai (1993) reported the composition by reproductive status of sexually mature females of southern-form and northern-form pilot whales taken by the drive fishery and small-type whaling, respectively (Tables 1213 and 1214) Biologists have analyzed these kinds of data for various

Females in Lactation at High Age (≥35.5 Years), Age at Presumable Last Parturition, and Age of Possible Last Calf in Southern-Form Short-Finned Pilot Whales off Japan

TABLE 12.13 Reproductive Status vs. Age of Southern-Form ShortFinned Pilot Whales off Japan, Showing a Rapid Decline in Reproductive Activity with Age

cetacean species in an attempt to estimate their reproductive cycles Such data are required to correctly represent the composition of the population For example, let us assume a population with gestation of 14  months, lactation of 12  months, and 10-month resting period (neither pregnant nor lactating) We assume no conception during lactation Then, the length of time from one conception to the next, or the mean reproductive cycle, will be 36 months, or 3 years The annual pregnancy rate is the probability of a mature female conceiving during a year and is calculated as the reciprocal of the reproductive cycle, that is, 1/3 ≈ 0333 If the reproductive cycles of females are not synchronized and proceed independent of season, then the proportion of pregnant, lactating, and resting females in the population will be 14:12:10 throughout the year The apparent pregnancy rate is the proportion of pregnant females in the total number of mature females and is calculated as 14/36 ≈ 0389 The annual pregnancy rate is calculated as [apparent pregnancy rate]/[gestation length], or [14/36]/[14/12] ≈ 0333 as obtained earlier In a similar way we can estimate the mean length of lactating or resting period from the data However, this method will be problematic if reproduction is seasonal and the sample is limited to a particular season or if females segregate geographically by reproductive status

Cetacean reproduction is seasonal to various degree depending on species and environment inhabited In order to understand the effect of this, we alter the condition of the hypothetical population given earlier to have all the conceptions in January and parturitions in March Then the composition of female reproductive status changes with season A sample in February contains pregnant females in two mating seasons, and the apparent pregnancy rate is double the annual pregnancy rate On the other hand the apparent pregnancy rate

in an April-December period The proportions of females in lactation and resting status also change seasonally Therefore it will be almost impossible to estimate the mean reproductive cycle of such a population using a seasonally biased sample The solution would be to obtain a seasonally unbiased sample, for example, a sample covering all months of the year equally

The southern-form pilot whales in our samples had a parturition peak in July-August with a standard deviation of 73 days (Kasuya and Marsh 1984), which meant that 95% of the parturitions were within a 94-month period surrounding the peak (Figure 1224) This was based on a sample containing some seasonal bias Backward shifting of this parturition curve by 149 months, the length of gestation, gave the distribution of conception and offered a way to estimate seasonal change in apparent pregnancy rate by adding the pregnancies of two successive seasons and subtracting parturitions The  result showed that the apparent pregnancy rate would reach the minimum figure of 1062 times the annual pregnancy rate in November and December and the maximum of 1443 times the annual pregnancy rate in May and June (Kasuya and Marsh 1984) The apparent pregnancy rate of the southern form estimated by Kasuya and Marsh (1984), who lacked data for March, April, and September, was likely to contain a bias within this range The possibility of geographical segregation was another problem, for which we do not have information to evaluate the effect

Sexually mature females in 385 southern-form pilot whales consisted of 112 pregnant (29%), 5 pregnant and simultaneously lactating (1%), 111 lactating (29%), and 157 resting females (41%) (Table 1213) The ratios of females in a particular reproductive status to pregnant females (117 in total) were 00427 for pregnant and simultaneous lactation, 09487 for simple pregnancy, and 13419 for resting females These figures, together with a gestation period of 149  months, gave an apparent average reproductive cycle of 064  months for pregnancy accompanied by lactation, 1414  months for lactation, and 1999  months for the resting period The total of these phases was 414  years, and the total lactation period was 148 months This reproductive cycle was felt to be too short in view of the results obtained from the analysis of school structure

Kasuya and Marsh (1984) compared the monthly estimates of apparent pregnancy rate of the sample against the theoretical monthly values of apparent pregnancy rate and found no correlation between them The reasons for this result were unknown but could include (1) the monthly figures of apparent pregnancy rate were unreliable due to small sample size, (2) the sample was biased, and (3) estimation of breeding seasonality was wrong The authors also found that the number of juveniles estimated to be younger than 149  months was only about 033 times the number of fetuses in the sample This figure was only slightly improved to about 04 with later-obtained additional samples (Kasuya 1990, in Japanese; Kasuya and Tai 1993) These results suggested some important unknown elements in the reproductive sample of southern-form short-finned

Reproductive Status vs. Age of Northern-Form ShortFinned Pilot Whales off Japan, Showing a Rapid Decline in Reproductive Activity with Age

juvenile mortality rate, (2) juveniles lost during the drive, (3) lactating females as well as their juveniles underrepresented in the sample for some unknown reason, (4) age of newborns overestimated, and (5) pregnancy rate increased during the sample period that covered 17 years Kasuya and Marsh (1984) tested for these possible causes and found that no single effect could explain the observed deficiency in the sample The authors did not evaluate a possible compound effect of several factors, and the cause of the bias was left uncertain I have an impression that their sample was biased toward the beginning of the parturition season (Sections 12431 and 12441)

After failing in attempts to determine the cause of the unexplained bias, the authors simply multiplied the number of pregnant females by 0315 (Kasuya and Marsh 1984) or 0405 (Kasuya and Tai 1993) to match the number of pregnant females with the number of juveniles and arrived at their presumably reasonable apparent pregnancy rate The apparent pregnancy rate thus created was divided by the gestation time of 149  months or 124  years to get an annual pregnancy rate Although it was questionable as to how reliable the resultant figures obtained through such large corrections were, Kasuya and Tai (1993), using larger samples than those of Kasuya and Marsh (1984), estimated the annual pregnancy rate at 128% and the mean calving interval at 783 years for the southern form

The estimations of mean pregnancy rate of 128% and mean calving interval of 783 years are figures for all females, including postreproductive females The corresponding values for reproductive females alone have not been estimated; this would require knowledge on the age-dependent proportion of postreproductive females Marsh and Kasuya (1984) concluded based on ovarian anatomy that the youngest postreproductive females occurred at ages 28-32 years, increased with age, and that all the females were postreproductive at least by age 40, but they presented evidence that females older than 36 years had already ceased calf production, that is, were postreproductive This age-dependent decline in fecundity can easily be seen in the apparent pregnancy rates in Tables 1213 and 1214

Most females aged 355  years or less were considered reproductive but must have included some proportion of postreproductive individuals Applying the procedure presented earlier to females aged 355 years and less resulted in a mean calving interval of 521 years and annual pregnancy rate of 192% (Table 1215) Integration of the annual pregnancy rate on age gave an estimate of 4-5 calves as the total production by a southern-form female that lived to postreproductive age (Kasuya and Marsh 1994)

Olesiuk et al (1990) analyzed data obtained through a long individual-identification study of killer whales off Vancouver Island and reported reproductive parameters comparable to the estimates for the short-finned pilot whale Their calving intervals ranged between 2 and 12 years with a mean interval of 53 years Females were expected to produce 5-6 calves if they lived to the age of 40, when they ceased reproduction

12.4.4.5.2 Reproductive Cycle of Northern-Form Females

Japanese small-type whaling resumed hunting these whales in 1982 after nearly 25  years of suspension This provided an opportunity for studies of their taxonomy and life history Kasuya and Tai (1994) reported the reproductive status of females collected in the five fishing seasons of 1983-1986 and 1988 Hunting was suspended in the 1987 season, because the whalers planned to use the 2 years’ quotas in the 1988 season when hunting of minke whales was banned and small-type whalers started to depend on small cetaceans The Government of Japan in July 1986 accepted the decision of the International Whaling Commission of 1982 and decided to close Antarctic whaling from the 1987-1988 season and North Pacific whaling from the season that would have started in 1988 (Chapter 7) It was the Japanese government position that hunting of small cetaceans was not bound by the IWC decision

The process of estimating the female reproductive cycle from the catch composition required information on neonatal length, gestation length, and seasonality of reproduction, but insufficient data were available from the short fishing season for the northern-form population A range of mean neonatal length in this population was obtained of 185-189 cm using an interspecies relationship between female body length and neonatal length, and the lower bound was accepted for the northern form based on experience that the method likely overestimated the true mean neonatal size for the species (Section 12431) This neonatal length was about 45  cm greater than that of the southern form

Mean Reproductive Cycle of Two Forms of Short-Finned Pilot Whales of Japan, with Correction for Possible Sample Bias due to Seasonality of Reproduction

ing seasons were composed of 40 pregnant (21%), 14 pregnant and simultaneously lactating (7%), 66 lactating (34%), and 61 resting females (32%) Out of the 54 gravid females only 32 had fetuses that were measured Therefore it was not possible to know details of the proportion of fetuses representing two successive mating seasons This was due to the fishermen slitting the carcass at sea for cooling The body temperature of cetaceans is around 36°C-37°C (Section 1236) Omura et al (1942, in Japanese) reported for balaenopterids that the carcass temperature of around 37°C-38°C at 2-3 h after death rose to 40°C-41°C within 24  h after death, causing degradation of meat quality Although we do not know how temperature changed in the pilot whale carcasses, it was evident that meat near the viscera changed in color to reddish brown within several hours after death In order to decrease this damage the whalers made a slit on the body in which they poured seawater while the carcasses were on the deck or towed them in the water Fetuses, particularly larger fetuses, were likely lost Large fetuses were retained only through continuing requests to the gunners

Kasuya and Tai (1993) reported body lengths of 32 fetuses in a range of 23-180 cm, but subsequent examination of small embryonic membranes identified two additional fetuses of 15  mm (Table 1218) Due to fishery selection toward large individuals, we had no chance to study neonates and juveniles and could not compare the upper range of fetal length with neonatal length This left some uncertainty in estimating mean neonatal length Of the 34 fetuses, 21 were below 20  cm, 6 were above 150  cm, and 7 were in between The mode of small fetuses represented a recent mating season and the mode at greater length mating in the previous year The time required for a 20  cm fetus to reach 150 cm was estimated at about 10 months Based on this information, gestation length of the northern form was assumed to be similar to that of the southern form, that is, about 15 months (Section 12442)

With the given information in mind, let us look at the reproductive data for northern-form females Of the 191 sexually mature females, 54 were pregnant, and 14 or 259% of the pregnant females were simultaneously lactating This figure was greater than the figure of 44% observed for the southern form, where only 5 females out of 117 pregnant females were simultaneously lactating All the 10 fetuses obtained from these 14 females in pregnancy and simultaneous lactation were below 60 cm in length, while 20 fetuses from the remaining 40 pregnant nonlactating females covered the entire fetal range from <10 to 180 cm and 12 were at or below 59 cm This means that at least about half of the females were lactating when they conceived The data also suggested that the females that became pregnant while in lactation would cease lactation by the next mating season In other words, about half of the northern-form females that conceived in the early part (September-November) of the mating season were near the end of lactation They would probably have ceased lactation shortly and certainly before the autumn of the next year The proportion of females that entered estrus while they

than in the southern form

A range of seasonal fluctuation in apparent pregnancy rate was estimated to be 1062-1443 times the annual pregnancy rate for the southern form using the seasonal distribution of conceptions and a gestation period of 149 months (see Section 124451) The highest apparent pregnancy rate was expected for the months between the end of a mating season and the start of a parturition season The upper limit of the range could be greater in a population with stronger seasonality of reproduction and could reach a value of 2 if seasons of mating and parturition were completely separated as hypothesized earlier Also, as mentioned earlier, reproduction in the northern form was likely to be more seasonal than in the southern form, but the mating peak could still last 4-5 months surrounding the months of September-December The reproductive data for the northern form presented earlier were obtained in the middle of the mating season and at the beginning of a parturition season Thus the obtained apparent pregnancy rate must be near the highest peak, which is likely between 1443 (a maximum possible figure in the southern form) and twice (hypothetical maximum) the annual pregnancy rate

Applying the range of the apparent pregnancy rate to the data for the northern form in October and November, when 54 mature females out of 191 were pregnant, a possible range of annual pregnancy rate was calculated at between 54/191/2 ≈ 014 and 54/191/1443 ≈ 020 (Kasuya and Tai 1993) The range of the mean calving interval was then estimated at 5-7 years as a reciprocal of the annual pregnancy rate The corresponding figure for the southern form was 783  years The currently available estimates of the reproductive cycles of the two short-finned pilot whale populations are compared in Table 1215 In view of various uncertainties surrounding these estimates, the real magnitude of difference in reproductive cycle between the two populations remains undetermined

12.4.4.6 Evidence of Postreproductive Females Here I will discuss age-related change in female reproductive status of the two forms of short-finned pilot whale off Japan The oldest females in the sample were aged at 625  years for the southern form and 615  years for the northern form (Kasuya and Marsh 1984; Kasuya and Tai 1993) These ages are expressed as 62 and 61 years, respectively, in the following parts of this chapter The oldest pregnant females in these samples were 35 and 36 They would have given birth at the latest at ages 36 and 37 years, respectively The 1-year difference between the two populations is insignificant Thus female short-finned pilot whales in Japan attain sexual maturity at 7-12  years (Section 12432), cease reproduction by age 36-37 at the latest, and live a subsequent maximum of 24-26 years Females 35 or older have almost no possibility of reproduction The proportion of such females in the total sexually mature female sample was 29% (southern form) and 18% (northern form) (Tables 1213 and 1214) This reproductive strategy has some similarity to that in human females, where menstruation starts at age 12-16  years (which does

repeated if not manipulated to age 40-55 years, and a postreproductive life of almost 30 years occurs before death at age 80-90  years The transitional phase between the regular estrous cycle and cessation of the cycle is called menopause or climacterium The term “menopause” is inappropriate for cetaceans because they do not have menstruation

Some similarities have been identified between the human climacterium and the age-dependent decline in reproductive activities of female southern-form pilot whales (Marsh and Kasuya 1984) These are expected to hold also for the northern form Table 1213 shows the age-dependent change in apparent pregnancy rate of the southern form The apparent pregnancy rate is extremely high, and the lactation rate appears low at ages 5-14 years, when females attain sexual maturity or experience their first ovulation This is due to the terminology of attainment of sexual maturity defined as the first ovulation and the fact that in most cases the first ovulation is followed by conception The apparent pregnancy rate declines with age, particularly after age 25, and reaches almost zero at ages over 35 This does not distinguish between the two components of (1) increase in calving interval of all females and (2) increase in proportion of females that cease ovulation Distinction between the two requires examination of ovaries A similar feature is observed in the northern form (Table 1214), although its age-dependent decline appears slightly slower than in the southern form The proportion of lactating females among total mature females showed a slight increase following a decrease in apparent pregnancy rate The change is particularly distinct if compared to the number of pregnant females and indicates a shift of female effort from calf production to calf rearing as already indicated in the earlier section The proportion of resting females increases with age The function of postreproductive females will be discussed later

Decline in the probability of ovulation followed by conception was identified in the southern-form population (Marsh and Kasuya 1984) Short-finned pilot whales ovulate spontaneously, and the ovulation is followed by formation of a corpus luteum of about 40 mm in diameter, called the corpus luteum of pregnancy or of ovulation The corpus luteum of pregnancy retains its size for the entire period of pregnancy, but that of ovulation quickly degenerates into a corpus albicans The corpora albicantia derived from either types of corpus luteum are believed to be indistinguishable and persist in the ovaries for life at a final average diameter of 5-6 mm (Marsh and Kasuya 1984), but some questions have been raised recently about this assumption (Section 1056) Luteal tissue may be formed in some Graafian follicles without ovulation to form accessory corpora lutea, which are not uncommon in cetacean ovaries but are identifiable by their small size and absence of ovulation scars (Marsh and Kasuya 1984) Some ambiguity may remain in the distinction between a corpus luteum of ovulation and that of pregnancy at a very early stage

Table 1216 compares the ratio of corpora lutea of pregnancy to that of ovulation between two different age classes

Corpora lutea of pregnancy comprised 96% of total corpora lutea observed in females aged 19  years or less, but they totaled only 69% in females aged 20 years or older The difference was statistically significant and indicated that ovulations of older females were less likely to be followed by conception Male preference for younger females or lower male availability for older females can be excluded from possible causes of the apparent fertility decline, because males of the population are known to mate even with nonestrous females (see Section 12447) Most of the corpora lutea identified as corpora lutea of ovulation in Table 1216 must have been in the process of degeneration toward corpora albicantia after failure in conception or of implantation of the fertilized ovum Such reproductive failures were considered to be a reflection of age-related change in female reproductive physiology (Marsh and Kasuya 1984)

This showed that ovulations of older females were less likely followed by conception than those of younger females Next to be considered is the possibility of age-related change in frequency of ovulation Figure 1227 presents the total number of corpora lutea and albicantia plotted on age of individual animals The scatter plot shows great individual variation, which is due to broad individual variation in age at the first ovulation and in the calving cycle The plot suggests an average annual ovulation rate of around 05 for ages between 10 and 20 years, declining with increasing age to reach almost zero at age 40 (Marsh and Kasuya 1984) The average annual ovulation rate in the upper left corner of Figure 1227 should be dealt with with caution, because it was calculated from the age-corpora regression and was model-dependent The model does not fit for ages around 10 as well as for ages above 40

In order to understand the background of accumulation of corpora in the ovaries, Marsh and Kasuya (1984) examined the process of regression of the corpus luteum in 245 southern-form females First, they confirmed that diameter of the corpus luteum of pregnancy was in a range of 304-475 mm with a mean of 376 mm and that the diameter was retained through pregnancy Then, based on histology, they classified

Age-Related Increase of Ovulations Not Followed by Conception in Southern-Form Short-Finned Pilot Whales off Japan

the regression of corpora albicantia into three stages and gave their diameters, which were “young” with diameter of 85285  mm (mean 152  mm), “medium” 55-165  mm (mean 104 mm), and “old” 25-12 mm (mean 64 mm) A conclusion was that degree of regression of a corpus albicans could not be determined by the diameter alone but required evaluation of the quantity of remaining luteal tissue and pigmentation The stage of “old corpus luteum” was considered to be the final stage of regression Marsh and Kasuya (1984) concluded that the corpus luteum in young females completed degeneration in 2 years, but that it took longer in older females This was deduced from the fact that “medium” corpora albicantia were observed even in females aged 55 years, while corpora lutea of ovulation were observed only until age of 39 years Regression was thought to be slower during pregnancy

Marsh and Kasuya (1984) found females with only “old” corpora albicantia and no Graafian follicles greater than 1 mm in diameter among southern-form whales aged 28 or older These females were likely to have not ovulated in the previous two years and were not preparing for ovulation in the near future, that is, were reproductively inactive This suggests that some of the females aged 28 or older were likely to have ceased reproductive activity Further they confirmed that “young” or “medium” corpora albicantia occurred only in females aged 40 or younger, which suggested that females ovulate the last time before age 40 We should note that the state of “young” corpus albicans will be retained some years after the last parturition or unsuccessful ovulation in old females These observations confirmed that some females of the southern form experience the last ovulation before

40 and allowed the conclusion, with consideration of the rate of regression, that females in the population experience their last ovulation at ages between 26 and 39  years with broad individual variation extending for 13 years This conclusion was further confirmed through observation of an age-related decline in density of oocytes in the ovarian cortex

Mammalian oocytes are formed during the fetal stage and remain in a sac of single layers of cells called a primordial follicle until development for ovulation starts At puberty, some of the primordial follicles start development to form an enlarged inner cavity with multiple cell layers surrounding it This is visible on the ovarian surface and called a Graafian follicle At the final stage of development, the Graafian follicle ruptures in ovulation Ovulation is followed under certain circumstances by fertilization and implantation Exact size of the Graafian follicle at ovulation has not been determined (see Section 12447) Many oocytes degenerate before ovulation The human female has about 7 million oocytes in the fetal stage, but only about 1%–2% of them at menopause, while only about 400-500 oocytes proceed to ovulation We do not have such statistics for small cetaceans, except for the total number of ovulations in the life of a female as indicated by the number of corpora lutea and albicantia For example, the maximum figure for the striped dolphin is 22 (Miyazaki 1984) and for the short-finned pilot whale 18 (Marsh and Kasuya 1984)

A deficiency of primordial follicles in the ovaries of old females was evidence of a climacterium among short-finned pilot whales In some toothed whales, such as striped dolphins, ovulation starts in the left ovary and it is followed by an equal frequency of ovulation from both ovaries (Section 10561; Ohsumi 1964) As short-finned pilot whales do not show a lateral difference at the age of first ovulation and ovulation frequency was not very different between the two sides (only 61% of total ovulations occurred on the left side, which was statistically significant), examination of either ovary is acceptable Therefore, Marsh and Kasuya (1984) randomly selected one ovary from 30 females and counted the primordial follicles in 10 microscope fields with a field size of 27 mm2 (Table 1217) Two whales were immature and aged

TABLE 12.17 Age-Related Decline in Density of Primordial Follicle in Ovaries in Southern-Form Short-Finned Pilot Whales off Japan

10-62 years Four immature and mature females below the age of 14 had primordial follicle density of over 50 per 10 fields, and 12 females aged 15-40 had a density of 10-50 Two females aged 29 and 38 years and all the 12 females aged 40-62 had a low follicle density of less than 2 per 10 fields, which was less than 4% of the level found in immature and young mature females This was similar to observations of human females in the climacterium, which was reached by short-finned pilot whales at various ages between the late 20s and around 40 This result agreed with information obtained from the earlier analyses

In female southern-form pilot whales the probability of ovulation followed by conception decreases with increasing age and ovulation finally ceases at ages between 26 at the earliest and 39 at the latest The oldest pregnant female was 35-36 years old in both northern-and southern-form whales, which was before the age of last ovulation Age analysis showed that female short-finned pilot whales at age 36 still have an average life expectancy of 14 years Marsh and Kasuya (1984) considered that this figure was comparable to 15 years life expectancy after the climacterium recorded for women of India in the nineteenth century, or before establishment of modern medical care Marsh and Kasuya (1986) reviewed then available information on reproductive biology of cetaceans and felt that such long postreproductive lifetime was uncommon among mammals (see Section 1257 for further details)

Marsh and Kasuya (1986) identified some degree of agerelated decline in ovulation rate in fin and sei whales but did not consider that it necessarily indicated fecundity decline, because age-related decline in apparent pregnancy rate has not been identified among the baleen whales reviewed by them Thus, they concluded that postreproductive females occurred rarely, if at all, in the population of baleen whales for which data are available Presence of postreproductive females was not confirmed for any of the Phocoenidae species and most of the Delphinidae species reviewed by them, and a conclusion similar to that for the baleen whales was reached The exception was sperm whales, false killer whales, and killer whales An absence of pregnant females in 22 sperm whales aged over 42 years (maximum age 61; Best et  al 1984) and in 12 false killer whales aged over 44  years (maximum age 62; Kasuya 1986, in Japanese) allowed Marsh and Kasuya (1986) to conclude that these had a postreproductive lifetime Photographic monitoring of killer whales off the Vancouver Island area has continued since 1973 and has revealed that 37 females, or 67% of adult females, did not experience parturition during a study of 10  years, and Marsh and Kasuya (1986) thought that these females included postreproductive individuals Many of these nonreproductive killer whales were later estimated to be over 40  years old and considered postreproductive (Olesiuk et al 1990)

12.4.4.7 Presence of Nonreproductive Mating Copulation is one of the important social activities of wildlife, but observing it in wild cetaceans is difficult and rare

females has supplemented information on the social behavior of both types of short-finned pilot whales off Japan and confirmed that nonestrous females participate in copulation that concludes with ejaculation (Kasuya et al 1993) The method was to make a small slit in an intact uterus for insertion of a pipette and collect a small amount of uterine fluid to be fixed in 10% formalin If there was not sufficient fluid in the uterus, a small amount of formalin was injected and mucus mixed with the formalin was retrieved The sample was allowed to settle for several days and the sediment was extracted with a micro-pipette, spread on a slide using a cover glass, air dried, and stained with a water solution of toluidine blue In humans, spermatozoa ejaculated in the vagina move through the uterus and reach the fallopian tube in 15 min Their maximum lifetime in female organs is believed to be 85  h The position of ejaculation varies among livestock species, but the travel time of spermatozoa from the ejaculation point to the fallopian tube is believed to vary from several minutes to several hours Dead spermatozoa are quickly ejected from the female body The position of ejaculation is unknown for cetaceans, but an assumption that ejaculation occurs in the uterine cavity (Ms E Katsumata, personal communication in 2009) seems to be reasonable in view of the lethal effect of seawater on ejaculated spermatozoa and the shape of the slender glans of the penis Cetaceans have not been known with the ability to store spermatozoa for later ovulation as is known in some bat species Therefore, presence of spermatozoa in the uteri of cetaceans is used as evidence of copulation that occurred within a few days and ended with ejaculation

Kasuya et  al (1993) examined uterine mucus from 33 southern-form whales in three schools driven at Taiji and 53 northern-form whales taken individually from an unknown number of schools by small-type whalers off the Sanriku coast The former sample was collected from individuals that were killed and processed after spending up to several days alive after the drive, and the latter sample was collected on the day of capture from carcasses towed to the land station at Ayukawa by the whalers In the case of the southern-form whales, the proportion of females having spermatozoa in the uterus was higher among females killed within 3 days after being driven or within about 54  h from completion of the drive (11 females had sperm of 18 females examined), and lower among females killed on the fifth day after the drive (2 females of 15 females) No data were obtained on the fourth day after the drive Two factors may have possibly affected the results: limited lifetime of spermatozoa in the female reproductive tract, or social or psychological effects that prevented copulations in the enclosure where the slaughter was progressing Although each of the three schools of the southern-form whales contained 2-6 adult males at the time of completion of the drive, the timing of slaughter of these adult males relative to sampling of uterine mucus has not been analyzed It is not known whether these adult males were mating partners of the females examined for uterine sperm The information obtained from these females was insufficient for analysis of seasonality of copulation but offered some information on the

tions as detailed as follows

Kasuya et  al (1993) examined 3-5 slides under a light microscope for each female and calculated the mean number of spermatozoa per slide This method had several sources of errors as an indicator of density or total abundance of spermatozoa in the uterus of a female: (1) position of ejaculation was ignored (most samples were taken from one uterine horn but ejaculation could have occurred in the other horn or in the vagina), (2) variation in the quantity of fluid contained in the uterus was not evaluated, (3) sampling and preparation was not quantitative For example the authors collected uterine mucus samples from each horn of the uterus of a female in early pregnancy with a 35 cm fetus and compared sperm density between them using three slides from each of the horns One horn showed an average sperm density of 110/ slide (sd = 82), while the other showed 680 (sd = 278) The bilateral difference was statistically significant, but the cause of the difference was unknown The probability of getting zero density depends on both the real sperm density as well as the number of slides examined Although the study of Kasuya et  al (1993) contained such uncertainties, it still has some value as evidence of the timing of copulation relative to the female reproductive cycle if we concentrate on presence of uterine sperm rather than absence

certain size and releases the ovum together with fluid in the follicle An estrogen surge occurs around this period and the female accepts males for copulation, which is called estrus We do not know what the follicle size is at ovulation but do know that follicle size in adult females usually remains below 8 mm and that females with larger follicles are often seen in the mating peak of May-July when immature females also exhibit some follicle growth to over 4 mm (Marsh and Kasuya 1984) Bottlenose dolphins are known to ovulate at a follicle diameter of 20-24 mm through ultrasonography (Katsumata 2005, in Japanese) A southern-form female that had a maximum follicle size of 222  mm had a high count of uterine sperm at 1562 (Table 1218) This female could have been in estrus Another southern-form female with a corpus luteum of ovulation had the largest follicle of 275 mm in her ovary and showed a sperm density of 103/slide The lack of histological examination of these large follicles precluded a firm conclusion about whether they were going to rupture or were or on the way to degeneration, but the high sperm counts suggest the females could have been near ovulation

First we concentrated on females in lactation or resting stage The latter category represents mature females neither pregnant nor lactating Spermatozoa were confirmed in  8 (258%) of the 31 lactating females and 10 (375%) of the

TABLE 12.18 Female Reproductive Status and Density of Spermatozoa in Uterus (Mean No. Spermatozoa/ Slide) as an Indication of Recent Copulation That Concluded with Ejaculation in Short-Finned Pilot Whales off Japan

Their sperm counts covered a broad range from less than 1 to over 10/slide It should be noted that there was no significant correlation between follicle size and sperm count, and spermatozoa were also found in females without measurable follicles (Table 1218, Figure 1228) This result indicates that copulations occur with nonestrous females in short-finned pilot whales

Next we considered females with a corpus luteum of ovulation, which represents females having a corpus luteum but without fetus or features of the endometrium that accompany conception These females had certainly recently ovulated, although it was uncertain if they were about to conceive or had experienced an unsuccessful ovulation As reasonably expected for these females, 10 (769%) of the 13 with a corpus luteum of ovulation had varying density of spermatozoa in the uterus, from less than 10/slide to over 10/slide The wide variety in sperm density reflects in part the qualitative nature of the methodology

Most ovulations are followed by pregnancy Pregnancy was identified by the presence of a fetus in the uterus or by histological features that are believed to accompany pregnancy, because some females could have aborted a fetus when killed by the fishermen The pregnancy symptoms include development of blood vessels below the endometrium, which is followed by development of dendriform villi Pregnant females examined for uterine sperm had fetuses in the range of 15 mm to 133 cm Uteri with larger fetuses were not sampled due to technical difficulties of handling the large placental tissue filling the uterus Eleven (917%) of the 12 pregnant females sampled, including a female with a 133 cm fetus, had spermatozoa in their uteri The counts were variable from 1 to 10/slide (6 females) to over 10/slide (5 females with a maximum of 57/slide) The gestation period of short-finned pilot whales is estimated at 452 days, with slower growth in

(Section 12441) Age of the fetus measured at 133 cm was probably between 1 and 2  months, when the parent female was still actively copulating

The relationship between female age and uterine sperm density is shown in Figure 1229 We have already determined that (1) the probability of an ovulation followed by conception declined with increasing age, (2) apparent pregnancy rate declined with increasing age and the oldest pregnant females was age 35 years (southern form) and 36 years (northern form), (3) the average annual ovulation rate declined with increasing age and the last ovulation occurred probably at age 39 years Thus, estrus and conception are not expected for females over age 40 However, one southern-form resting female without measurable follicles (≥1 mm in diameter) and aged at 42 years had a uterine sperm count of 10/slide There were two similar northern-form females in resting status; one with a follicle of 10 mm and age 44 had an uterine sperm count of 2990/slide and the other with follicle of 144 mm and aged 41 had an uterine sperm count of 172/slide The follicles of the last female were not histologically examined These three females, or at least the first two, were in nonestrous postreproductive status and had recently copulated

12.4.4.8 Function of Nonreproductive Mating Some mammalian females advertise their estrus Females of the bonobo (pygmy chimpanzee) develop bright swollen genital skin as a visual sign of estrus, and dogs and horses use chemical signs for the purpose Such signs are not developed in human females, and most males do not identify estrus in their partners It is currently uncertain whether cetacean females have any clues to advertise their estrus, but the possibility of

(Pryor 1990) Kuznetzov (1990) reported pseudo-olfaction in the bottlenose dolphin This has been described as a highly sensitive chemical receptor in the oral cavity and comparable to olfaction of land mammals, opening the possibility of a function in identifying chemical signs of female estrus

Female receptivity unrelated to the estrous cycle is not limited to species where estrus is not advertised Most mammalian females are receptive only around the period of estrus, but the restriction is lost in some species such as humans and bonobos, where copulations occur during any stage of the estrous cycle Kuroda (1982, in Japanese) observed copulation bouts when a group of bonobos was placed in front of food and tension increased among the members for food sharing and interpreted this to mean that copulation functions to lessen tension Waal (2005, Japanese translation) thought promiscuity of female bonobos unrelated to the estrous cycle functions to camouflage paternity and prevent infanticide It is well known that most human copulations are not aimed at reproduction and have other functions They usually accompany economic interactions and contribute to maintenance of partnership by lessening tensions between individuals or by increasing intimacy Exchanging partners, which existed in Inuit communities, was believed to have contributed to constructing a cooperative network among individuals of the same sex who share partners (Houston 1999, Japanese translation) There are various examples known where brothers or sisters share a common partner of the opposite sex, or nonrelated multiple males share a wife, for example, Nynba in Nepal, Nayar in India, Sinhala in Sri Lanka, and some indigenous communities in South and North America (Kasuya 2008; Schultz and Lavenda 2003, Japanese translation) These social systems could function to strengthen bonds between partner sharers under particular social and economic situations Extramarital copulations were allowed for community members following particular festivals of the communities in early Japan, which lasted until the 1920s in some locations (Ikeda 2003, in Japanese) and probably functioned to increase bonds among community members

Bottlenose dolphins in captivity copulated within 1-2 days of the period of estrus (Yoshioka et  al 1986) Asper et  al (1992) reported copulation in captive killer whales to occur mostly in a 5-to 12-day period around estrus, but some also sometimes outside the estrus period, including during pregnancy Interpretation of these observations on captive animals requires caution before extending them to wild individuals Kenney (2002) reported frequent copulations between male and female right whales outside the breeding season and interpreted them to have a social function other than reproduction These observations suggest that nonreproductive mating can exist in some cetacean species other than short-finned pilot whales Variability of copulation behavior in cetaceans is probably comparable to that of primates and is worth further investigation

Evidence of nonreproductive mating has been presented for short-finned pilot whales, and hypotheses formed to explain the function One of the key pieces of information missing

zoa found in female reproductive tracts The questions include (1) the number of male partners for a female, (2) the genetic relationship between the female and her partner, (3) the social origin of the male partners, and (4) the age and growth stage of these males Answers to some of these questions will be available by analyzing the DNA of individual spermatozoa in female reproductive tracts, and this will contribute to evaluation of the following hypotheses about the function of nonreproductive mating in the species Some of the following hypotheses assume that short-finned pilot whales identify school members individually (Kasuya et al 1993; Magnusson and Kasuya 1997; Kasuya 2008)

12.4.4.8.1 Education Some primates such as chimpanzees and humans, particularly males, are believed to require learning or experiences for accomplishment of normal copulation (Nadler 1981) Tutin and McGinnis (1981) interpreted copulations between mature female and immature male chimpanzees as having an educational significance Some precocious males of southern-form short-finned pilot whales produce spermatozoa at age 5 years and transport them to the epididymis at age 9 years, but they are believed to attain reproductive ability at age 17 on average Among 139 southern-form males almost randomly selected, 69 were sexually mature and another 17 were not identified as sexually mature but had various quantities of spermatozoa in their epididymides The remaining 53 males could have produced spermatozoa in the testis but did not have spermatozoa in their epididymides and were histologically classified as at the immature or maturing stages (Section 12433) Some of these males that were in the process of sexual maturation could have left spermatozoa in the uteri of some females If a nonestrous female gives mating education to young males in the same pod, members of which are likely to be genetically related with the female, it will contribute to total reproductive success of the female For this hypothesis to stand, copulation within the pod has to be identified

12.4.4.8.2 Enhancement of Bonds between Individuals Sexual intercourse and gift exchange are inseparable activities in some mammalian species, including humans Similar behavior is also known on some bird species as courtship feeding Both sexual contact and gift exchange probably have a similar social effect in bond development between individuals of these animal species Similar examples are known in bonobos as well as humans Thus it remains as a possibility that copulation between members in a pod or members of different pods functions to establish and maintain a stable community

12.4.4.8.3 Exchange of Greetings Every human community has particular stereotypical behavior exchanged when two individuals of the community meet, which functions to show friendship or absence of hostility and is called greetings Some human communities use handshakes for the purpose External genitalia are organs of

similar function for them as in shaking hands and to assume that there is a copulation bout when two pods occasionally meet This hypothesis agrees with our finding that a pregnant female with a 133 cm fetus had copious sperm in her uterus (Section 12447), while another fetus of similar size (136 cm) did not have its father in the school (Section 1254) Sexual intercourse in humans functions to diminish hostility or to increase friendship, as it does in bonobos Sperm whales are known to increase accumulation of body scars from intermale fighting for mating opportunities during the mating season (Kato 1984), but short-finned pilot whales do not show such scars and it is thought that incidents of inter-male fighting are uncommon among them The reason for the low intermale aggression is thought to be the generosity of females (Kasuya et al 1993) The sexual generosity of females functions to decrease aggressions, which contributes to production and rearing of calves in the school Gray whales (Jones and Swartz 2002) and right whales (Kenney 2002) are likely to have a similar mating system

12.4.4.8.4 Camouflage of Paternity Infanticide by males is known in various mammal species, which results in resumption of estrus of the mother and increases reproductive opportunities of the male but decreases that of the female Although infanticide has not been confirmed in cetaceans, the possibility has been reported for bottlenose dolphins (Connor et  al 2000; Campagna 2002) The receptivity of nonestrous females observed in the shortfinned pilot whale can camouflage paternity and decrease the incidence of infanticide, but it is unclear whether the social system of the species is likely to result in benefit to males of infanticide particularly in view of the study by Kage (1999, in Japanese), which did not find paternity of any fetuses within a school (Section 1254)

12.4.4.8.5 Decoy Hypothesis Adult male short-finned pilot whales are likely to be reproductive throughout the year An average school of the southern form contains 2 adult males, 13 adult females, and several immature and maturing individuals of both sexes (Table 1220) Twenty-five percent or more of adult females of the southern form are postreproductive Although the proportion of postreproductive females is likely lower in the northern form, the annual pregnancy rate calculated including the postreproductive females is estimated at around 17% for either population

Kasuya and Marsh (1984) estimated the number of ovulations experienced before the first conception of a female using corpus counts of 15 young females that were likely to be in their first pregnancy Nine of the females were thought to have become pregnant at the first ovulation, three at the second ovulation, and one female each at the third, fourth, and sixth ovulations These give an average of 19 ovulations before the first conception Accepting this figure for all the reproductive females, the annual number of estrous periods expected for the average school per year is calculated at

If these reproductive females accepted males only during a total of 4 days including before and after the ovulation, the two mature males in the average school would have mating opportunities on only 16 days in a year Males in such schools can have two strategies: a waiting strategy where males remain in a school for an average of 16 days of estrus in their school, and a searching strategy where males move between schools to seek estrous females Magnusson and Kasuya (1997) mathematically tested which of the two strategies would more benefit male reproduction and found that a key element was the abundance of female schools to be encountered by the searching male A reasonable range of the probability of encounter, which was not estimated from data, suggested either the possibility that waiting males have slightly better reproductive success or that the two strategies do not differ significantly

The observed nonreproductive mating confirmed for the short-finned pilot whales creates 50-60 times greater mating opportunities; that is, males will find mating partners throughout the year in a school and have no reason to move out of the school to seek estrous females From the female point of view, if postreproductive and young nonestrous females accept males and lure them to their school, it will help reproduction of genetically related females in real estrus This is the decoy hypothesis

Future scientists will determine whether any of the hypotheses mentioned earlier contain truth The correct answer may be that more than one of them be valid, but they may all be invalid The short-finned pilot whale is one of the few mammal species that has developed social functions in sexual contact between the two sexes Such nonreproductive sexual contact functions in maintaining the community and was called “social sex” by Kasuya (2008) Such social sex likely exists in some cetacean species other than the short-finned pilot whale

I call a school “mixed” if individuals of one cetacean species are found within or close to a group of another cetacean species However, the spatial relationship between individual of the two cetacean species is not the same as that between conspecific individuals The distances between conspecific individuals are usually smaller than those between individuals of different species in a mixed school

Table 1219 lists the incidence of mixed schools containing short-finned pilot whales sighted in the western North Pacific (Kasuya and Marsh 1984) Although the data do not distinguish between the two forms of short-finned pilot whales, the two forms have not been found together in a school except for an unconfirmed case (Section 1234) Mixed schools of the two forms must be rare because they are geographically segregated

The drive fishery offered information on other cetacean species found within or close to 17 schools of short-finned

pilot whales that were driven at Izu and Taiji Six schools were found without any other cetacean species, and nine were found close to other school(s) of the same species Four schools were found with schools of bottlenose dolphins (three or more schools of two species in one place) One school of southernform pilot whales was found with a school of bottlenose dolphins, and another was found with bottlenose dolphins and Pacific white-sided dolphins

Table 1219 also lists 21 schools of short-finned pilot whales observed by scientists on research vessels Twelve were found as solitary schools (without any nearby cetacean schools), two were found with an additional school of the same species, and eight with schools of other cetacean species, which included bottlenose dolphins and Pacific white-sided dolphins The information on mixed schools obtained from the two separate sources was similar, except for the latter source giving a relatively lower incidence of multiple schools of short-finned pilot whales in the same place, about which further mention will be made later

It is concluded that short-finned pilot whales off Japan often form a mixed school with common bottlenose dolphins and less frequently with Pacific white-sided dolphins

Nonlethal studies on the social structure of short-finned pilot whales have recently started and are continuing along both coasts of North America and in the Azores Islands area using an individual-identification technique with photography (eg, Heimlich-Boran 1993) These studies will produce valuable information on movement of individuals between schools as well as relationships between individuals within a school Japanese studies on the school structure of short-finned pilot

carcasses taken by drive fisheries (Kasuya and Marsh 1984) Some limited information was available from the drive fishermen on status of the school before the drive, but scientists were unable to observe the process of the drive and had difficulty in interpreting the data obtained

The 6-year period from 1975 to 1980 spent by Kasuya and Marsh (1984) for data collection must be taken into consideration in interpreting results of the analyses The species has a long history of exploitation at Izu, Taiji and Okinawa (Sections 38, 39, 310, 41, 42, and 126) and received high hunting pressure from the modern drive fishery that started at  Taiji in 1969 Kasuya and Marsh (1984) were unable to identify historical change in the catch composition in their sample covering the 6 years, but it remains to be confirmed whether the fishery exploited a single population during the period Kasuya and Marsh (1984) tentatively assumed that their material did not reflect historical change

Kasuya and Marsh (1984) reported the school size in 21 drives, including 15 drives with details of the school at the time of sighting at sea Eight of the latter were found alone, and all the members of the school were believed to have been driven These schools were called single schools The single schools were composed of 14-38 whales, with a mean of 246 and a mode of 21-30 (Figure 1230)

Seven other drives of the 15 were made on a single group selected from an aggregation of several groups of the same species in an area These schools ranged from 20 to 52 individuals with a mean of 351 and a mode of 21-40 These groups selected from an aggregation tended to contain more large males, which were preferred by the fishermen for greater

Cetacean Species Found Together with Schools of Short-Finned Pilot Whales

tent (see Section 1235)

Kasuya and Marsh (1984) examined only one drive where an entire aggregation of several groups was driven, on June 24, 1975, at Taiji (School No 9 in Figures 1232 and 1233) The aggregation was found scattered loosely over a broad range and was composed of several groups of pilot whales as well as group(s) of about 100 bottlenose dolphins Soon after the sighting the aggregation became tighter, which was believed by the fishermen to be a response to a killer whale group observed within a distance of 400-500 m, and made it possible for the fishermen to drive the entire aggregation After the drive, the fishermen selectively killed 173 pilot whales of larger size and on July 4 released all the bottlenose dolphins and about 60 pilot whales that were mostly females and juveniles, because the animals started to lose weight and the market was saturated Thus, the total number of pilot whales driven could have been about 230 This was about 10  times the size of a single school Driving of such large aggregations was also known at Arari on the Izu coast in the post-World War II period (Section 382)

Miyashita (1993) reported sizes of 45 schools of southernform pilot whales estimated from sighting survey vessels of the Fisheries Agency in the western North Pacific The estimates ranged from 10-20 to 300-400 with an average of 498 Precision of these estimates was limited, but I would note that there were no sightings of schools smaller than 10 whales My own shipboard observation on short-finned pilot whales off Japan recorded school sizes of 5-50 with a mean of 206 (n = 21, including both northern-and southern-form whales), which was close to the figure for a single group off Taiji Two of the 21 sightings occurred about 100-200 m apart and could be considered sightings of aggregations

The incidence of aggregation was higher in the records of the Taiji drive fishery than in my records This is due either to a better than average feeding environment off Taiji or to the searching operation using numerous fishing vessels (7-14 vessels) Sergeant (1962) reported for the long-finned pilot whale that groups of about 20 scattered in a broad area tended to form an aggregation if frightened by an approaching aircraft If such behavior were expected for the short-finned pilot whale, small groups would aggregate in response to drive vessels

Now I will compare short-finned pilot whales off Japan and those off the Canary Islands area reported by HeimlichBoran (1993) The whales in the Canary Islands area lived in “groups” of 3-33 that were slightly larger in summer than in winter The “group” is a unit of encounter similar to “school” used for Japanese short-finned pilot whales Data on movement of individuals between groups during the 2-year study revealed an existence of a stable core unit called a “pod” The pods were composed of 2-33 whales with a mean of 122 Most groups encountered were composed of a single pod (59%), but some contained 2-5 pods The proportion of groups containing multiple pods slightly increased in the summer In rare cases more than 10 pods formed a group This was apparently similar to the aggregation mentioned earlier, but the group

structure from group size

Forty-six pods were identified in the Canary Islands area, including 15 pods that were seen only once Among the remaining 31 pods, some frequently formed a group with some other particular pods but rarely with others However, there was no case where a particular pod completely avoided formation of a group with another particular pod This feature has similarity with the social structure of the sperm whale, where a matrilineal unit (pod) of several to less than 20 individuals forms a basic stable unit of daily life, with units joining temporarily (Whitehead 2003)

Each of the resident killer whale communities off the Vancouver Island area is composed of several pods that are families of matrilineal descent The pods in one community, which are believed to have derived from a single ancestral matriline, recognize each other and have temporary contact with each other, although it is rare for all the pods of one community to form one aggregation In addition to the resident whales in the coastal waters, there is another form known as transient killer whale Pods of the transient and resident killer whales have different vocal signals, do not merge with pods of the other form, and rather avoid or may show hostility toward each other (Baird 2000)

It is possible to assume a similar social structure for shortfinned pilot whales off Japan, where matrilineal pods function as a basic social unit and occasionally merge with other pods of the common matrilineage A single pod or an aggregation of several pods forms a “school” or the unit driven in the fishery We know that the geographical range of southern-form pilot whales apparently extends to the longitude of 160°E (Figure 124), but we do not know the community structure possibly existing within the range Information on community structure is urgently needed for safe management of the Japanese pilot whale fishery

It is well known that a particular population of cetaceans inhabits a particular geographical area, but this does not necessarily mean that it attempts to monopolize a particular geographical range by rejecting other group of the same species, that is, formation of a territory In the open marine environment where food species can move almost unpredictably, it would be technically difficult and economically unprofitable to monopolize a certain geographical range as a territory The situation is different for killer whales that inhabit estuarine waters where an anadromous salmonid aggregates and offers a stable feeding ground The whales benefit by monopolizing the feeding ground and rejecting members of other communities This is the situation we see in resident communities of killer whales in the northeastern North Pacific

12.5.3.1 Neonatal Sex Ratio Southern-form pilot whales had a fetal sex ratio of 61 males (513%) and 58 females (487%) among 119 fetuses at or over 5  cm in body length; fetuses below 5  cm were excluded to avoid uncertainty of sex determination The postnatal sex ratio

17 females (472%) Neither of these ratios was significantly different from parity The body length of 220 cm corresponds approximately with ages of 11 years in males and 12 years in females Combining these two sets of data gives a neonatal sex ratio (sex ratio can change through life) of 516% males (n = 155) This was again insignificantly different from parity (Kasuya and Marsh 1984) Although the possibility remains that males slightly exceed females at parturition, it has not been confirmed by the available data Such an analysis was not carried out for northern-form whales due to an insufficient sample size (Kasuya and Tai 1993)

12.5.3.2 Age-Dependent Change in Sex Ratio Males comprised 327% of 483 aged southern-form whales killed in the Japanese drive fishery The sex ratio changed with age: females exceeded males at every age from 1 to 5 years, fluctuated at around 50% at ages between 6 and 16  years, again exceeded 50% at every age from 17 to 45, and finally came to 100% at ages above 45 (Kasuya and Marsh 1984) Further examination of this change shows a gradual decline of the female proportion with increasing age until 8 years of age, and the opposite trend for ages above 8 years The age of 8 years is close to the average female age at sexual maturation and the male age at puberty Kasuya and Marsh (1984) examined change in social behavior, segregation between sexes, and sexual difference in natural mortality rate as a plausible cause of the age-related change in sex ratio and concluded that (1) higher male mortality was the main factor in age-related decline in the male ratio after age 8 and (2) further behavioral information was needed to interpret the background of the age-related sex ratio below age 8

The oldest individuals were age 455 (male) and 625 (female) in the sample from the drive fishery The following equation was obtained for the relationship between the proportion of female (Y, %) and age (X, years) of southern-form pilot whales killed in the drive fisheries:

Y = 0991X + 4174, 10 < X < 47 (r = 059) (Kasuya and Marsh 1984)

12.5.3.3 Mortality Rate Figure 1231 presents the age composition of southern-form whales taken by the Japanese drive fisheries during 19651981 It has been generally accepted that the mortality curve of mammals is U-shaped, high at young and old ages with a trough in the middle A similar trend is observed in the age composition of whales over 10 years old, but it was not possible to explain the deficiency of young individuals below age 10 with such an age-related mortality rate pattern A similar feature was met with in the age composition of striped dolphins (Figure 1014), pantropical spotted dolphins (Figure 1015), common bottlenose dolphin (Figure 115), and perhaps finless porpoises (Section 8527), which suggests a behavioral change that could cause a bias in age composition of the sample

continued fishing pressure that varied in intensity over years Thus the catch composition must reflect a combination of natural and fishing mortalities, which comprise total mortality If the population responded to the fishing pressure by altering the recruitment rate, that would also affect the catch curve Thus the right side slope of the catch curve is the sum of natural mortality, fishing mortality, and change in recruitment, disentanglement of which is not possible at present By ignoring such complicating factors and using the method of Robson and Chapman (1961), which is free from model-dependent bias, Kasuya and Marsh (1984) estimated the apparent annual survival rates of the southern-form pilot whales as follows The accompanying 95% confidence intervals take into account fluctuation of the age composition

One can calculate the relationships S = [1 − M] and S = e−Z, where S is the annual survival rate, M the annual mortality rate, and Z the instantaneous total annual mortality that corresponds to the right side slope of the age frequency

The apparent annual mortality rate of the population was about 25% (females) and 43% (males) at middle ages, which was lower than the figure for higher ages of 146% (females) and 97% (males) The mortality rate increased at certain ages, which differed between the sexes, that is, around 46 years in females and 29 years in males When the sexes are compared at the same age, males always exceeded females in apparent mortality rate, which must reflect difference in the true natural mortality rate

A similar mortality pattern is expected for the northernform pilot whale, because of the similarity in maximum ages (445 years in males and 615 years in females) and betweensex difference in the age at sexual maturation (Kasuya and Tai 1993)

12.5.3.4 Social Behavior of Males Male sperm whales visit breeding females in lower latitudes during the mating season and spend a solitary life in higher latitudes during the rest of the time (Best et al 1984; Kasuya and Miyashita 1988) However, it is unknown whether these males participate in reproduction annually or skip breeding in some seasons At the beginning of our study of short-finned pilot whales, we noticed a male deficiency in the age composition and thought about the possibility that adult males segregate from female schools Information from the drive fishery did not answer the question because solitary males would not attract fishermen as a target for the drive My own data confirmed the minimum school size in the species at five individuals, and study of the species in the Canary Island area revealed that they live in pods of 2-33, which may temporarily merge with other pods Sighting cruises conducted by the Fisheries Agency of Japan did not always have experienced

biologists on board, and their school-size estimates were often rounded to the nearest 10 However, the surveys covered a broad area of the North Pacific north of 25°N and west of 170°E, or most of the known range of the species in the western North Pacific School size recorded during these cruises ranged from 10-19 to 300-399, and the mean school size of the 42 schools, excluding the three extremely large schools of over 200, was 498 (SE = 6) (Miyashita 1993) These observations suggested that male short-finned pilot whales do not usually spend a solitary life as observed in the sperm whale Thus, the skewed sex ratio after puberty at around age 8 and the longevity gap observed between sexes are considered real and a reflection of difference in natural mortality rate

The number of adult males ranged from 1 to 18 in the 13 drives with detailed biological information (Table 1220) In addition, half of the schools contained 1-5 pubertal males (classified at the “early” or “late” maturing stages) The number of adult males differed slightly, but significantly, between

drives of a single school and drives of selected portions of aggregated schools In the former case the number of adult males per school ranged from 1 to 3 with a mean of 20 and median of 25, while in the latter case there were 1-18 males with a mean of 57 and median of 4 The difference was due to fishery selection for large males Thus, it can be generalized that the usual number of adult males in a school of southern form short-finned pilot whales is 1-3 (observed in 9 cases), and the two cases with 8 or 18 adult males were unusual In the last two cases, Schools Nos 16 and 18 in Figures 1232 and 1233, also contained 13 and 5  adult females, respectively

In addition to the 13 cases, another 14 schools offered some limited information on school structure Thirteen of the 14 had a minimum of one sexually mature male The highest number of adult males was found in 1 of the 14 schools (School No 18 in Figures 1232 and 1233), 18 adult males (with 5 adult females) The remaining (School No 20 in Figure 1233) had

no sexually mature males; this was a school of 14 driven at Taiji in January 1980 Thirteen whales were measured for body length and had sex confirmed, and the remaining one was judged an adult female based on estimated body length and external shape of the body Only two individuals in the school were confirmed to be male; they were judged sexually immature (less than 3 m in body length) If we trust the observations of the drive fishermen that they had driven all the whales in the school, this School No 20 was a rare school that contained no adult males but 8 adult females However, I once experienced a drive at Futo, on the east coast of the Izu Peninsula, where one large male of adult size escaped at the entrance of the Futo harbor leaving the rest of the school to be driven into the harbor (School No 14)

The ratio of adult males to adult females in the 13 schools mentioned earlier with better biological information ranged from 1:11 to 1:23, with 1:4 for the total Exclusion of females at postreproductive ages (>35 years) still results in an excess of adult females in a range of 1:11 to 1:21 This is a reflection of later sexual maturity and shorter life span of males As noted earlier, there has been no evidence for segregation of adult males from schools of adult females and juveniles of both sexes

with adult females and juveniles of both sexes, and it is still unclear whether all males attain maturity in their natal pod and live with their mother after sexual maturity or at least some of them move out to other pods, perhaps at around the time of attainment of sexual maturity For the latter case, it is also unknown whether adult males remain with a school for more than one mating season or move between schools When such information becomes available, we will be able to have better insight into the social structure of the species and obtain an answer to the broad variation in sex ratio among schools Kasuya and Marsh (1984) did not find a correlation between male ratio and female reproductive status in a school, and some of the hypotheses presented by them remained speculative The promising study of Kage (1999, in Japanese; see Sections 1254 and 1255) on genetics was based on sample sizes insufficient for full understanding of social structure The history of related studies is outlined as follows

Kasuya and Marsh (1984) noted that males at early or late maturing stages were always found in a school containing mature males, based on observation of seven schools that contained mature males but no maturing males and another six schools that contained both mature and maturing males (Figures 1232 and 1233) They deduced that maturing males were not functioning as adult males in a school and that they were not driven out by mature males, which was a feature different from that observed in sperm whales They also noted the broad variation in number of maturing males in a school, that is, five maturing males in School No 6, but none in School Nos 13, 16, and 18, and speculated that pubertal males at ages between 10 and 20 perhaps tended to leave their natal schools and aggregate together These authors did not estimate the probability at which such an imbalance in maturity composition of males could be created solely by chance

The hypothesis of Kasuya and Marsh (1984) automatically assumed that adult males in a school were not always in the matrilineage of the school The basis for this hypothesis was the clumped age structure of adult males in some schools, for example, School Nos 7, 9, and 13 They thought that aggregation and movement of pubertal males between schools could explain such age structure as well as the extremely high (School No 18) or low (School Nos 13 and 20) number of adult males There were some supporting evidences for this In observation of short-finned pilot whales in the Canary Islands area Heimlich-Boran (1993) identified 46 pods in the vicinity and obtained detailed information on the structure of some of them Twenty-eight pods contained adult individuals of both sexes and two other pods were known to contain only adult males: a pod of two males and another of six males In a second instance of supporting evidence, one school of longfinned pilot whales driven in the Faroe Islands was composed of only eight males, including two immature males (3 and 10 years old) and six maturing or mature males (16-24 years old) (Desportes et al 1992)

A weak point of the hypothesis presented earlier is that only data consistent with the hypothesis were used to construct it Data that might indicate other possibilities are ignored or

School Composition of Southern-Form Short-Finned Pilot Whales Taken by Japanese Drive Fishery

forgotten However, males not leaving their natal school have been recently suggested from genetic analyses of school structure of the two species of pilot whales (see Section 1255)

Sperm whale males leave their natal pods at puberty to live with other males of the same growth stage, which is followed by solitary life after attainment of full sexual maturity (Best et al 1984) The departure of pubertal males from their natal pods is likely promoted by competition with adult males that visit the pod during the mating season Young mature males of the species in a mating season tended to have scars caused by inter-male aggression for mating opportunities This contrasts with resident killer whales off Vancouver Island, where males remain in their natal pods with their mothers for life and inter-male aggressions are apparently absent within the resident population The situation is slightly different in the transient population of the same species that inhabits the same

waters of the northeastern North Pacific In the transients, the eldest son accompanies his mother, but younger males tend to leave their natal pods at puberty and live a solitary life However, the possibility remains that some interaction or cooperation may persist between the solitary sons and their mothers living in the same vicinity Baird (2000) suggested that the elder son obtains a benefit by living with the mother, who has greater experience and knowledge, and that younger sons are expelled by the elder son at puberty It seems to me that males in both populations could benefit from living with their mother, but that it is not allowed for younger sons in the transient form for some reason The reason is likely feeding economy and not a competition for mating opportunity as seen in the sperm whale While killer whales of the resident form in coastal waters live on salmon, those in the transient population feed mainly on seals and Dall’s porpoises Seals and porpoises live in a small school and the energy available from a single feeding opportunity can satisfy only a small number of killer whales So the transient killer whales are

whales Transient females leave their natal pods after maturity for the same reason, that is, because they cannot satisfy the appetites of their offspring if they remain in the natal pod The distribution of squids, a main food of short-finned pilot whales, is less patchy than that of seals and porpoises and will enable short-finned pilot whales to live in a group larger than that of transient killer whales Short-finned pilot whales, as in the resident killer whales, rarely have scars caused by teeth of the same species and are believed to have less inter-male competition

Kage (1999, in Japanese) attempted to further our understanding of movement of males in the population of shortfinned pilot whales by analyzing the DNA of four schools driven at Taiji, one of which was selected by fishermen from a greater aggregation and three were found as solitary schools at sea The fishermen believed that they did not miss any whales from the solitary schools during the drive operation Kage obtained a total of 12 fetuses (136-1055 cm in body length) from the four schools and tested paternity against all the 18 candidates, including mature, late maturing, and early maturing males taken with the pregnant females His method was to extract nuclear DNA from the fetus and process it with a restriction enzyme for electrophoresis The fetal genotype was compared with that of the mother and then with that of male candidates The fetal genotype must contain elements of both parents The result was negative He was unable to find possible fathers of the fetuses in the same school

Kage made additional tests to determine if any combination of adult female and adult male in the same school could be the parents of any member of the same school, and found no matches, as expected from the previous results on the fetuses As the smallest fetus of 136 cm could have been about 2 months of age or less (Sections 12441 and 12447), he concluded that the fathers of the fetuses had left the school of mating partners soon after estrus A similar result has been reported for the long-finned plot whale in the North Atlantic (Amos et al 1993) Two questions remain about the mating system of short-finned pilot whales The first is the nature of the affiliation of adult males in a school, which will be dealt with in a later section (Section 1255) The second question has to do with copulation: when and how it occurs This relates to the finding of copious spermatozoa in the uterus of ovulating or pregnant females (fetuses ≤133  cm) (Section 12447), while Kage’s study on other schools failed to find paternity of fetuses (136-1055 cm) there (see the preceding text in this section)

It is difficult to observe copulation in wild cetaceans; even the well-studied humpback and killer whales are not an exception Toothed whales appear to have frequent social contact, and distinguishing between copulation for reproduction and for sexual play is sometimes difficult I have not seen studies on relationships between male sexual behavior and resultant paternity in wild cetaceans It seems to me that observation of the daily activity of a pod, which is likely a group of individuals of one matriline, will help us understand the mating behavior of short-finned pilot whales Some pods join to form a group of tens of whales or even larger groups of over one

been called a “school,” corresponds to the pod or a group and “aggregated school” to a large group In the case of resident killer whales, copulations are believed to occur between individuals from different pods of the same community

It is likely that short-finned pilot whales can identify members of other pods of their community, and temporary merging of these pods may result in copulation bouts between members from different pods (Section 12448) The copulation bout is not limited to estrous females and full-grown males but involves nonestrous females, as confirmed by presence of spermatozoa in the uterus Although participation of maturing males has not been identified, it is also likely Such copulations may function not only for reproduction but also for decreasing stress and maintaining peace between the pods involved Identification of the origin of spermatozoa in female uteri will have a key role in evaluating this hypothesis

Amos et al (1993) analyzed this problem for two schools of long-finned pilot whales driven in the Faroe Islands Because genetically testing parent-offspring relationship for all the possible pairs would be an impractically large task for a large school as in their case, they noted the genetic characters of a particular individual of either sex and calculated the probability of finding its mother or father in the school The probability of having a father in the same school was almost negligible for individuals of any age, but the probability of having a mother was almost 100% for individuals below the age of 5 years and was still 30% for individuals aged over 20 The next analysis was to calculate the similarity of the genotype of a particular individual with that of other members of the school The similarity was not affected by the sex of the particular individual, but it slightly increased significantly with age It ranged from 008 to 042 for ages 5-10, and 017-07 for ages 30-45 Amos et al (1993) concluded that the age-related change in similarity was due to the addition of new genetic traits of fathers from other school These results indicate that fathers leave the school before the birth of their offspring, but the offspring accompany their mother even after attainment of sexual maturity Such a community is called a matrilineal community Their analyses did not indicate the number of matrilines in the schools examined It also remains to be answered how frequently, if at all, offspring (sons and daughters) emigrate to other schools

Andersen (1993) offered some information on school formation in long-finned pilot whales She analyzed allele frequency of three polymorphic loci in 1948 whales in 31 schools driven in the Faroe Islands She found that the allele frequencies of females, particularly those of adult females, contributed to the observed difference in allele frequency between schools This result did not disagree with the result of Amos et al (1993) and suggested that inter-school transfer of females is limited, if any Then she tested whether the proportions of heterozygotes and homozygotes agreed with Hardy-Weinberg equilibrium This was to see if mating was

ness for many of the schools, but males in some schools were far from Hardy-Weinberg equilibrium, which she interpreted as an indication of inter-school movement of males or biased reproductive success of particular males

The information on long-finned pilot whales suggested that matrilineal female groups formed a core element of schools of the species, with at least some males moving between schools These results led us to revisit the study of Kage (1999, in Japanese) for the same purpose carried out on short-finned pilot whales driven at Taiji He compared 13 alleles of nuclear DNA among four schools using a method called minisatellite fingerprinting He found significant differences in allele frequency in four pair-wise comparison of the four schools, which would be expected if mother and calf lived together He further examined the frequency of heterozygotes and found that it was higher than expected for a case of random mating, which he interpreted as a suggestion of (1) multiple genetic lineages in the school, (2) interbreeding between schools, or (3) inter-school movement of individuals Because Kage (1999, in Japanese) combined both sexes in this analysis, it was unknown which sex had a higher tendency of movement between schools

Kage (1999, in Japanese) also examined between-school variation in the control region of mitochondrial DNA (mtDNA), maternally inherited DNA, of southern-form pilot whale using samples from 248 individuals from 5 schools He digested the control region of mtDNA with a restriction enzyme and analyzed the fragments with electrophoresis; he found two haplotypes, A and B There could have been more variation in the portion of mtDNA, but the enzymes he used could only identify the two types School No 201 with 22 individuals contained both haplotypes, but the other four schools had only haplotype A Using this result he separated the 22 individuals of School No 201 into 2 matrilines, each containing a total of 11 individuals, with 1 mature male, 6 or 9 mature females, and 4 or 1 immature individuals This result suggested that the two adult males could have remained with their mothers

Kage applied similar electrophoresis to nuclear DNA to look for common elements between individuals (multi-locus DNA fingerprinting) In theory, half of the electrophoretic bands should be common between offspring and a parent, and values between 046 and 051 were identified between mother and fetus This parameter will decrease with increasing genetic distance Applying this analysis to all the pair-wise combinations in School No 201 (22 individuals), he obtained a mean of common bands of 0355, and the mean of all the combination of the 15 adult females (which probably contained two matrilines) was 035 The figure was higher between individuals of similar age (039-044) and lower between immature and mature individuals, 033-034 Comparisons between mature females and the two adult males gave similar figures (mean 039) with those between adult females (035) These results suggested that (1) males and females adhered similarly to their matriline, and (2) new genetic characters imported to the matriline increased with time and caused greater genetic

their young descendants Although this analysis alone did not indicate whether the new genetic characters were brought in by females or males, the mtDNA analysis suggested that the new genetic characters were due to sperm left by males in temporarily merging pods

Currently available information on the school composition of southern-form pilot whales driven at Taiji and on the Izu coast and some speculation allow the following hypothesis on the social structure of the species The most basic unit of their life is a matrilineal group of around 10 individuals, which corresponds to a pod of resident killer whales off the Vancouver Island area and to haplotype groups A and B identified in the School No 201 mentioned earlier Each pod is composed of matrilineal members and usually contains adults of both sexes and immature individuals The unit driven by the Japanese dolphin fisheries is a pod or an aggregation of pods The aggregation is likely to be very fluid, as seen in the same species off the Canary Islands area (Heimlich-Boran 1993)

Males usually accompany their mother after maturation, but the possibility that some males leave their natal pod for another pod is not fully excluded The timing of the possible male departure is not known, but could be at around attainment of sexual maturity, at death of their mother (a key individual in their pod identity), at splitting of a large pod into more than one pod, or at some still unknown time Conception follows copulation with males of another pod on the occasion of temporary merging of pods Such temporary merging of pods seems to be frequent, which is suggested by the fact that females in all the three schools examined for uterine fluid were found to contain sperm in the uterus (Section 12447) and due to observation of the species in the Canary Islands area A rather limited length of merging of multiple pods is suggested by the fact that a female pregnant with a 136 cm fetus (<2  months old) was not found with the father of the fetus in the same school (Section 1254) However, it would be premature to conclude that all the nonreproductive “social sex” occurs between individuals of different pods The possibility of copulation between matrilineal members remains to be investigated There has been no evidence of emigration of females from their matrilineal groups

12.5.7.1 Identification One of the two morphological types of short-finned pilot whale off Japan was studied in detail to examine age-related change in reproductive activity (Marsh and Kasuya 1984) and was found to have a high proportion of postreproductive females in the population, defined as females that had ceased reproduction due to great age The study concluded that this stage was reached by some females at ages in the latter half of the 20s and before age 40 by all the females The stage was

cles in the ovaries, which occurred in some females by age 29, cessation of conception that occurred by age 36, and cessation of ovulation that occurred at the latest by age 39 Maximum life span was 62 years Monitoring the physiology of a single female would reveal such age-related changes as a decline in conception following ovulation followed by complete cessation of ovulation This is a process known as menopause in human females, and the stage after menopause is the postreproductive stage Identification of the end of menopause and start of the postreproductive stage of an individual female is possible retrospectively only through continued observation of her physiology It is almost impossible to determine with certainty for every female if she is in the postreproductive stage by examining the reproductive tracts of short-finned pilot whales, and such a method is likely to underestimate the proportion of such females in the population

Noting that the oldest pregnant female was 355 years old in the southern form and 365 in the northern form (expressed in Table 1221 as 35 and 36 years, respectively) and assuming that females at ages 355 years and over are postreproductive, we get approximate proportions of postreproductive females in the southern-and northern-form populations at 29% and 18% of sexually mature females, respectively (Tables 1213 and 1214) Marsh and Kasuya (1984) identified 24% of sexually mature southern-form females as postreproductive through examination of their ovaries In view of the difficulty of ascertainment and difference in the sample sizes, the two figures for the southern form can be considered close The difference of the two figures between the populations is not due to difference in reproductive strategy but more likely to a difference in age composition, which could reflect the history of exploitation and subsequent recovery

The southern-and northern-form pilot whales had different histories of exploitation The northern-form was vigorously hunted off Sanriku and Hokkaido by small-type whaling during the post-World War II period with an annual take of 200-400 (−1953), 11-127 (1954-1971), and 11 or fewer (19721979) The catch from 1954 to 1972 was low at an annual average of 47 (Table 1222) This fishery selectively hunted large individuals, and a rapid decline of males was identified in the catch during the early operation (Section 126) This population was probably recovering during the nearly 27-year period from the middle 1950s to the 1982 season, when exploitation by small-type whaling resumed and the collection of reproductive data started (Kasuya and Tai 1993) Thus, there could have been an anomalously high proportion of young adult females in the population when their biology was first studied

The history of hunting of southern-form whales was more complicated in fishing methodology and geography of the fishing grounds Small-type whaling recorded an annual take of 200-400 in the post-World War II period (until 1953), and the drive fishery on the Izu coast recorded a take of 1891 in the seven seasons (1950−1956) for which statistics are available (Table 314) Although Nago in Okinawa operated an opportunistic drive, the catch statistics are available only since 1960 and recorded an annual take of over 100 until

1973 (Table 322) After these large takes, relatively low levels of catch were made by driving at Nago and on the Izu coast (Table 316) and by small-type whaling at Taiji (Table 1222) until 1969, when a regular drive operation started for the southern form off Taiji (Section 39; Tables 317 and 318) Most of the reproductive information on the southern form was obtained from the drive fishery at Taiji This history of exploitation as well as the uncertainty surrounding the mixing of individuals between the three major fishing grounds makes it difficult to speculate on the population trend before 1969 The effect of the catches on age structure of the short-finned pilot whales off Japan remains to be investigated

Postreproductive status, per se, has no reproductive benefit for lifetime reproduction; rather it can have an adverse effect on the survival of a female’s offspring through possible competition for nutrition For such a genetic trait to be selected to affect such a significant proportion of a population as observed in the short-finned pilot whale, it will have to generate some beneficial trait or traits to compensate for the apparent adverse effect on total lifetime reproduction Studying such beneficial traits, or the contribution of postreproductivity in females to the survival of their offspring, is an important research item in the study of behavior and social structure of short-finned pilot whales and can contribute to future management of the populations Before we speculate on the topic, we will briefly review the presence of postreproductive females in cetacean communities using information presented by Marsh and Kasuya (1986) and subsequently obtained

Table 1221 presents information on age and reproductive activity of toothed whales The ages of ovulation, pregnancy, and lactation represent values that have been confirmed If the observed pregnancy ends with parturition, which is not

observed, the age of oldest parturition will be about 1 year greater The length of lactation is presented as the known maximum range, which may differ depending on the sex of the offspring, and there remains the possibility of communal nursing The length of suckling is the maximum confirmed age of suckling, including the period when both milk and solid food are ingested This does not distinguish between cases whether a calf suckles from its own mother or from other females Maximum lengths of lactation are not available for the pantropical spotted dolphin and the common bottlenose dolphin, for which only values of the average duration of lactation are given

Marsh and Kasuya (1986) reviewed age-related reproductive data for 12 toothed whale species and 6 baleen whale species and concluded that a significant postreproductive period was unlikely to exist in baleen whale populations but likely existed in short-finned pilot whales, resident killer whales off Vancouver Island, and false killer whales in the Iki Island area in western Japan Some additional information then became available for sperm whales (Best et al 1984) and long-finned pilot whales (Martin and Rothery 1993) This is reviewed in the following

The information on false killer whales, 101 males and 116 females, was randomly collected from a larger number of carcasses driven and killed by the fishermen in the Iki Island area for culling purposes (Kasuya 1985a; Kasuya 1986, in Japanese) There were 64 mature females with age: 12 pregnant, 14 lactating, 31 resting and 7 of unknown status The greatest age of females in pregnancy was 43 years and of those in lactation 53 years (the next oldest female in lactation was age 43), while the oldest resting female was 62 This suggested that females cease reproduction by age 44, leaving a maximum

Life History Parameters of Selected Toothed Whalesa

prost-reproductive life of 18  years The number of mature females ≥44 years old was 16 (1 lactating, 12 resting, and 3 of unknown reproductive status) and that of mature females aged ≤43 was 48 (12 pregnant, 13 lactating, 19 resting, and 4 of unknown reproductive status) This suggests that over 20% of sexually mature females in the Japanese false killer whale population were likely in a postreproductive status As the ovaries were not examined in detail, it is unknown when ovulation ceases in this population (Kasuya 1986, in Japanese) The between-sex difference in observed maximum age was 6 years, which suggested a slightly greater longevity of females Further details on this Japanese material has been published together with data from South Africa (Ferreira et al 2013)

Killer whales off Vancouver Island have been studied since 1973 using individual identification with photography Olesiuk et  al (1990) estimated growth and reproductive parameters

using data thus obtained in the 15 years from 1973 to 1985 Numerous females did not breed for over 10 years In view of the information on Japanese short-finned pilot whales, these females were believed postreproductive Of particular interest was the age-dependent calving rate, which was the probability of an adult female calving in a year and identical with annual pregnancy rate if abortion can be ignored The calving rate of this killer whale population rapidly declined from an extremely high value near 100% at age 12 years to a still high value of about 25% at age 18 These high calving rates can be explained by recruitment of young females to the reproductive population I note that the calving rate declined linearly to below 5% at ages over 48 This age-related change was very similar to that observed in short-finned pilot whales The reason why the calving rate did not reach zero even after age 48 could be explained possibly as a model-specific artifact of tailing

Number of Short-Finned Pilot Whales Taken by Japanese Small-Type Whaling Given by Sex and Geographical Regions for 1948-1957, 1965, and 1968-1979, Compiled from Geiryo Geppo [Monthly Report of Whaling Operation] Received by the Fisheries Agency

of sperm whales taken for research purposes off South Africa Out of the 725 mature females there were 134 pregnant, 36 ovulating, 272 lactating, and 300 resting Their data showed that both pregnant and ovulating females occurred at ages ≤41 and lactating females at ≤48 years, while females lived to a maximum age of 61 years The number of females above age 41, the age of the oldest known pregnancy or ovulation, was 22 or about 3% of the total number of mature females Although the proportion of likely postreproductive females in the population was not high, Kasuya (1995b) thought that the sperm whale has a postreproductive lifetime extending at least 20 years Another interesting feature of the life history of this species was the similarity of longevity between the sexes (Table 1221) Kasuya (1990, in Japanese) felt that such great male longevity has some relationship with the segregation of males to higher latitudes apart from nursing females in lower latitudes, thus avoiding competition for resources

The reproductive data for long-finned pilot whales presented by Martin and Rothery (1993) are puzzling Corpus count in the ovaries increased linearly until the age of 50 This means that ovulation occurred at almost a constant frequency to age 50 The relationship is unclear for ages over 50 due to scarcity of samples (1 individual at age 51, 2 at 55, and 1 at  59) The apparent pregnancy rate, that is, proportion of pregnant females in a sample of mature females, decreased from 40% at age 10 to 20% at age 35 It further decreased to almost zero at 41 years and over However, among 41 females aged 40 or more (maximum age 59), there were two pregnant females aged 41 and 55 years Martin and Rothery (1993) concluded from these data that “it is possible that some animals had ceased to ovulate altogether and/or that only a small percentage of ovulations in these older females lead to a successful fertilization … The fact that one female…a 55 year old… was pregnant demonstrates that successful reproduction can potentially continue throughout life” It is possible to interpret the data given earlier to indicate that the whales live a rather short postreproductive stage at ages 50-59 years following a climactic stage at ages 41-50 when ovulations occur without conception The probability of ovulations of these old females being followed by conception may change by improvement of nutrition However, it seems to be also possible to interpret the data given earlier, by ignoring the pregnant female at age 55 as an outlier, to mean that long-finned pilot whales cease reproduction by age 41 and ovulation by age 50 while living to age 59 This interpretation means that females of long-finned and short-finned pilot whales are similar in having a considerable postreproductive life span, although the former species may have a slightly longer reproductive life and shorter postreproductive life Detailed examination of ovaries of long-finned pilot whales will throw further light on their reproduction

This allows the conclusion that the sperm whale, shortfinned pilot whale, killer whale, false killer whale, and possibly the long-finned pilot whale have significant postreproductive life spans The first three species are known to have a matrilineal social structure Sperm whales live in a matrilineal pod of 10-50 individuals, which occasionally merge and form a

off Vancouver Island, known as an ecotype, live in several communities that contain multiple matrilineal pods Pods may temporarily merge with other pods of the same community but not with those of other communities This feature is apparently the same as in sperm whales and short-finned pilot whales in the Atlantic Almost nothing is known on the social structure of false killer whales, but a matrilineal community is suspected

12.5.7.2 Function of Postreproductive Females Data in Table 1221 make it clear that species with postreproductive females (I will call them type-2 species) have greater female longevity than those without them (type-1) The two groups have no significant difference in breeding lifetime of females The female life history of type-2 species could have evolved from that of type-1 females by adding a life of nonreproduction to the life of type-1 females, while males were left unchanged (killer and short-finned pilot whales) For this view to be applied to females of the long-finned pilot whale the single old pregnant female aged 55 must be interpreted as an outlier Additional explanation is required for sperm and false killer whales where males live as long as postreproductive females The life history pattern of Baird’s beaked whales is quite different from either of the two major types mentioned earlier in great extension of male longevity (Section 1354) Their life history and social structure could have evolved in a direction quite different from those of the species mentioned earlier The life history patterns of toothed whales are not limited to these For example, the franciscana (Kasuya and Brownell 1979) and the porpoises (Chapter 9) apparently evolved early maturation, high annual reproductive rate, and short life expectancy (Kasuya 1995b)

Marsh and Kasuya (1986) suggested that postreproductive females would not exist if they did not have a positive function in the community and proposed that the function is a contribution to the welfare of juveniles If the postreproductive females take care of the offspring of their daughters (their grandchildren), it contributes to their total lifetime production and allows for their genetic traits to survive in the population Biological information of the time was already sufficient for Marsh and Kasuya (1984) to hypothesize matrilineal social structure for the killer and short-finned pilot whales Now we have more information on social structure of toothed whales, and there are reasons to believe that the various types of social structure seen on the killer, sperm, and short-finned pilot whales are in a top group among many toothed whale species that have evolved toward formation of matrilineal social structure

According to Lockyer (1981), who studied the energy requirements of cetaceans, the daily food consumption of a sperm whale is 3% of body weight in fully grown individual but 10% in young sexually mature females that are still growing Sperm whales live mainly on squid, like short-finned pilot whales The food requirement during pregnancy increases by 10% in young females and only 5% in fully grown females, which means that a pregnant female requires 20-40 kg of food

tenance of her own body weight This is not a great increase in burden compared with the burden accompanying lactation After parturition a mother must support the fast growth of her calf The energy requirement increases by 63% in a young mother and 32% in a fully grown mother This means that during lactation a young mother requires daily 685 kg of food and a fully grown mother 554  kg Such a great increase in energy requirement cannot be an easy burden

Young calves less than 1-year-old remain at the sea surface, while other members of the school dive for feeding, presumably because such young calves have limited diving ability A young calf is often accompanied by an adult female other than its mother, called a babysitter (Whitehead 2003) The mother cannot stay with her young calf at the surface because she has to satisfy her energy requirement The presence of a babysitter decreases the risk of the calf being attacked by predators such as killer whales or sharks, and offers a better feeding opportunity for the mother However, there is no firm evidence that postreproductive females are participating in the task of babysitter

As postreproductive females live with their daughters and grandchildren, they are able to increase their total lifetime production by taking care of survival and reproduction of their relatives in the pods, not by attempting production of their own offspring at a greater age This was a hypothesis proposed to explain the evolution of postreproductive females (Marsh and Kasuya 1986)

Acting as a carrier of information is another function expected of older individuals Accumulation of experience and information benefits animals in feeding, reproduction, and avoiding predators, and the importance is greater among the higher animals in general and probably in the aquatic environment For example terrestrial primates have less difficulty in visiting particular trees in the right season for feeding on the fruit compared with dolphins that must locate prey species in the water and cooperate in attacking it Fish schools move daily and their location is less predictable than the location of fruit trees Experience and information on the environment accumulated by postreproductive females, which are usually old, benefits life and reproduction of the members of the matrilineal pod

Information accumulated in some individuals and behavioral patterns derived from it will be transmitted to other members and maintained over generations to form a culture of the pod or community Although identifying culture in a cetacean community is not easy, the presence has been accepted by cetacean biologists (Whitehead 2002; Krutzen 2006) If experience and knowledge are accumulated by long-lived females, the quantity and quality of culture will increase Thus, postreproductive females function as carriers of culture of their community

Both culture and genetic traits function as tools of adaptation of the carrier to the environment Many animals and plants adapt themselves to changing or new environments by modifying their genetic traits, but the process requires a longer time to be accomplished However, culture is characterized by

In principle, new cultural traits will be acquired within less than one generation of a matrilineal pod of such species as short-finned pilot whales or killer whales and can be transmitted to other pods of the community with time Culture is a powerful tool of a pod to adapt itself to a newly encountered environment and increases adaptability of the community Cultural diversity within a species increases chances of the species to survive in a changing environment A currently agreed goal of cetacean management is to maintain genetic diversity and certain levels of population size, but it does not consider maintaining cultural diversity and the ability to acquire new cultural elements This simplistic management policy diminishes the ability of survival of some cetacean species, particularly species with long life spans*

Human activities affecting survival of short-finned pilot whales off Japan are not limited to intentional take by fisheries, incidental mortality in fishing gear, and competition with fisheries for food resources Other impacts include physiological and physical damage due to pollutants, underwater noise, ship strikes, and climate change (Introductory Chapter) Consideration of the latter four elements is beyond my expertise, and there are insufficient statistics on incidental mortality in fishing gear Interaction between short-finned pilot whales and fishing activities for food resources has not been studied to a reliable degree Currently available information suggests that the greatest factor affecting survival of the two forms of short-finned pilot whales is fishing activities targeting them, which are briefly summarized as follows Further details on the related fisheries are available in Part I

Short-finned pilot whales are rare in the Sea of Japan and the East China Sea (Section 122) Post-World War II operation of small-type whaling reported the take of a small number in the Sea of Japan off the west coast of the Oshima Peninsula (42°30′N-43°30′N) in southwestern Hokkaido (Figure 1234, Table 1222) Frequency of occurrence of the species in the region requires further confirmation to eliminate the possibility of confusion by whalers with the false killer whale, which is more common in the area and also called gondo (Sections 34 and 122) Here is a summary of the history of hunting of pilot whales off the Pacific coasts of Japan (from north to south)

Small-type whalers hunted pilot whales in the periWorld War II period from land stations at Kushiro, Akkeshi (43°03′N, 144°51′E), and Urakawa (42°10′N, 142°46′E) on the Pacific coast of Hokkaido (Figure 1234) The main target of their operation was minke whales, and the catch of

short-finned pilot whales was small at an annual average of 4-5 in the 1949-1952 seasons The low level of catch continued until the 1970s (Table 1222) The location suggests that their catch was of the northern form

Several villages on the Sanriku coast operated dolphindrive fisheries since the eighteenth century (Section 37) They were apparently authorized to conduct the operation by the government in the mid-nineteenth century (Section 51) One village, Oura (39°27′N, 142°01′E) in Yamada Bay (39°28′N, 142°00′E), listed three species as their targets: mai-ruka, nezumi-iruka, and goto-iruka (Kawabata 1986, in Japanese) The last species is the short-finned pilot whale, presumed from the location to have been the northern form These drive fisheries, which last operated in 1920, left no significant statistics (Section 37)

Small-type whaling and hand-harpoon fisheries increased during the peri-World War II period and caught northernform pilot whales off the Sanriku Region (Table 1222), while the hand-harpoon fisheries probably aimed mainly at smaller species The number of small-type whaling vessels was 10 in Miyagi Prefecture and 4 in Iwate Prefecture (Pacific coast at 38°59′N-40°27′N) in November 1943 (Nihon Hogeigyo Suisan Kumiai [Whale Fisheries Association of Japan] 1943, in Japanese) The total number of Japanese small-type whaling vessels increased from 43 in 1942 to 73 in 1948 and reached a peak of 80 in 1950 (Ohsumi 1975) (Sections 41 and 711)

Kasuya (1975) analyzed statistics of the short-finned pilot whales taken by the small-type whaling for 1949-1952 (Figure 1234, Table 1222) The peak year of catch of northern-form pilot whales was in 1949, when a total of 415 were taken The catch declined to about 200 in 1953 and to less than 50 during 1954-1971, when the fishery almost ceased, and continued until 1981 The change was most likely due to shift of operations to other species, for example, minke whales and perhaps poaching of sperm whales (Sections 1372 and 15323) However, Kasuya and Marsh (1984) noted that the change accompanied a decline in the proportion of large adult males in the catch, which was attributed to high hunting pressure (Section 1262) The small-type whalers resumed exploitation of the northern form in 1982, and the operation has continued to the present at a low level (Table 43)

A record exists at Choshi in Chiba prefecture on the Pacific coast of a mass stranding of pilot whales in 1932 or 1933, which was utilized by the local people (Kanari 1983, in Japanese) This area is still known for occasional stranding of pilot whales Whalers of the Chiba area before the early twentieth century took some short-finned pilot whales during their operation for Baird’s beaked whales (Section  1371) There were 11 (in 1941, Table 41) or 7 (in 1943, Nihon Hogeigyo Suisan Kumiai 1943, in Japanese) small-type whalers registered in Chiba Prefecture They recorded an annual take of about five pilot whales in 1949-1952 (Figure 1234)

ated from Wadaura (35°03′N, 140°01′E) for Baird’s beaked whales (Section 1372) and occasionally took small numbers of southern-form pilot whales Pilot whales taken south of Choshi Pont (35°42′N, 140°51′E) could have been of the southern form (Kasuya et al 1988)

Villages on the Izu coast operated a dolphin-drive fishery since the early seventeenth century At least since the midnineteenth century the striped dolphin was the major target, but they also took cetaceans called nyudo-iruka or o-iruka, which are believed to have been southern-form pilot whales (Section 382 and 383) Currently, the drive fishery is operated by the Futo group at a very low level (Tables 316 and 63) One person in Inatori (34°46′N, 139°02′E) on the east coast of Izu peninsula in 1910 started small-type whaling for pilot whales using a five-barrel harpoon gun introduced from Taiji, which was subsequently replaced by a three-barrel gun and then a single-barrel harpoon gun; the operation continued until about 1955 (Nakamura 1988, in Japanese) Nihon Hogeigyo Suisan Kumiai (1943, in Japanese) recorded a similar but different story that two small-type whaling vessels registered in Shizuoka Prefecture operated from Inatori in November 1943 Most operations of small-type whalers were likely unrecorded before December 1947, when they were placed under control of the Japanese government (Section 711) Kasuya (1975) did not identify the operation at Inatori in Fisheries Agency records for the years 1947-1952 (Figure 1234, Table 1222)

Hand-harpoon whaling in Mikawa Bay (34°45′N, 137°00′E) around 1570 is the earliest available record of Japanese commercial whaling This technology was transmitted to the present Chiba Prefecture in the east around 1558-1569 and survived as hand-harpoon whaling for Baird’s beaked whales until the nineteenth century (Section 137) The technology was also transmitted via the Shima Peninsula (34°20′N, 136°45′E) to western regions: the present Wakayama Prefecture in 1606, Kochi Prefecture (33°30′N, 133°30′E) in 1624, coasts and islands off northwestern Kyushu (33°30′N, 129°45′E) in 1630, and western Yamaguchi Prefecture (34°15′N, 131°00′E) in 1672 (Hashiura 1969, in Japanese) The fishery changed into so-called net whaling and continued to the late nineteenth century (Section 13) Some pilot whales could have been taken during the operation (Section 391 and see below), but details of the catches are unknown

Hand-harpoon whaling at Taiji in Wakayama Prefecture, where the southern form occurs, started in 1606, shifted to net whaling around 1677 (Sections I21 and 13), and continued until ship wreck 1878 The operation slumped in the nineteenth century, and the whalers hunted pilot whales as a side business (Hamanaka 1979, in Japanese) Small vessels called tento in Taiji in the mid-nineteenth century were involved in pilot whaling (Section 391) The tento hunters first introduced a whaling cannon in 1903 and engines in 1913 (Section 391) This resulted in a rapid increase in the catch of pilot whales from 120 in 1912 to 381 the next year, when 11 vessels operated In November 1943, there were 15 small-type whaling vessels registered in Wakayama Prefecture, and 11 of them belonged to Taiji (Nihon Hogeigyo Suisan Kumiai 1943,

of 12 vessels engaged in small-type whaling (9 operating bodies) and 8 tento vessels (8 operating bodies) as operated from Taiji in the post-World War II period The dates of statistics or distinction of the two types was not given, but the former type included vessels that were known to have seasonally migrated to other regions of Japan for minke whaling Thus, the latter could have been smaller vessels operating only locally All of these vessels were placed under a license system of the government in 1947 Responding to the policy of the Fisheries Agency to reduce the expanded fleet of small-type whaling vessels (Section 711), the licenses of all the small-type whaling vessels of Taiji, except one called Katsu-maru, were aggregated to be used for the establishment of a new largetype whaling company Nihon Kinkai Hogei [Japan Coastal Whaling] in 1950 (Hamanaka 1979, in Japanese) Supported by stable demand for the meat in Taiji, two small-type whalers currently operate from Taiji for pilot whales, Katsu-maru No.7 and Seiwa-maru (Table 71) (see Section 12632 for further details)

Taiji has a history of two types of dolphin-drive fisheries (Section 391) One was a traditional opportunistic drive for pilot whales, where community members joined in the activity when a school of the whales was sighted near the harbor The earlier history is unknown, but the village was approved for the operation by the government after the Meiji Revolution in 1867-1872 (Section 51) and continued the operation until 1951 The license was not renewed in 1993, possibly because of cessation of the operation for a long period In 1969, a group of fishermen succeeded in an attempt to drive a pilot whale school from offshore waters in order to supply live animals for the opening of the Taiji Whale Museum This was the start of the current dolphin-drive fishery in Taiji This operation is different from the earlier opportunistic drives in being based on daily searching activities in a radius of 15-20 nautical miles (28-37 km) Some Taiji fishermen once used seine nets for pilot whales, but the operation lasted only for a short period in 1933-1935

A small number of short-finned pilot whales were also taken by small-type whaling in Kochi Prefecture (from the ports of Tosa-shimizu (32°47′N, 132°57′E), Mizu (33°17′E, 134°11′E) and nearby Shiina), Miyazaki Prefecture, and northwestern Kyushu during the post-World War II period (Figure 1234 and Table 1222) Nihon Hogeigyo Suisan Kumiai (1943, in Japanese) recorded two small-type whaling vessels registered in Yobuko (33°32′N, 129°54′E) in Saga Prefecture in northern Kyushu, four in Ise-yamada (34°31′N, 136°46′E) in Mie Prefecture, and nine in Tokyo The last were owned by a whaling company in Tokyo and could have operated in various regions of Japan

Nago in Okinawa Prefecture was known to have opportunistic dolphin drives for pilot whales and other toothed whales, in which the local people cooperated in driving dolphin schools found near the harbor and shared the catch (Section 310) Miyasato (1988, in Japanese) described Norwegian-type whaling at Nago under US occupation that ended in 1972, as well as the dolphin-drive fishery in Nago

not obtain a license for the drive fishery in 1982, when it came under the license system of the prefecture, a document of the Coastal Division of the Fisheries Agency (dated July 7, 1988) stated that it retained a prefectural license (Section 65) The last operations of the drive could have been on 9 shortfinned pilot whales in 1982 and 20 bottlenose dolphins in 1989 (Kishiro and Kasuya 1993) As the supply of dolphin meat for Nago people almost ceased in the early 1970s, a new type of fishery called the crossbow fishery started in 1975 for pilot whales and other species The crossbow fishery is operated by shooting a harpoon with cable and detachable harpoon head from a catapult powered by a rubber belt This fishery supplied dolphin meat to the people in Nago and to markets in Shimonoseki and Osaka (Section 28; Endo 2008, in Japanese)

Attempts to estimate the abundance of Japanese pilot whales go back to the 1980s The IWC (1987) recorded a provisional estimate of northern-form pilot whales presented by T Miyashita to the Scientific Committee of the IWC in 1986 Miyashita revised this estimate using additional sighting data and presented it to the Scientific Committee in 1991 (IWC 1992) The latter estimate was based on shipboard sightings in September and October, 1982-1988 The mean abundance was 4239 (Table 1223) Although a confidence interval is not given, the large coefficient of variation of 061 suggests that the lower limit was close to zero

The abundance of southern-form whales was reported to the Scientific Committee in 1991 and later published in Miyashita (1993); it was based on shipboard sightings in August and September in nine seasons, 1983-1991 During these months

the latitude of 38°N Miyashita arbitrarily divided the western North Pacific into three areas: northern coastal Pacific west of 145°E between 30°N and 38°N (which included all the coastal whaling grounds mentioned earlier except for Nago), northern offshore Pacific at 30°N-38°N and 145°E-180°E, and southern waters at 23°N-30°N and 127°E-180°E, which included Nago (Table 1223) Although he did not specifically mention the basis for the division, the boundaries were close to the apparent distribution gap in the species in the western North Pacific (Figure 124), which separates the species into coastal waters west of the Kuroshio Current and offshore waters in the Kuroshio Counter Current area (southeast of the Kuroshio Current)

Minamikawa et al (2007, in Japanese) estimated the abundance of southern-form pilot whales in the western North Pacific using fewer data obtained in 4  years (1998-2001) They obtained an estimate of 15,000 with a CV of 07 for the entire area, where Miyashita (1993) had estimated a total of about 50,000 (Table 1223) The great CV of the more recent estimate makes it difficult to evaluate the difference Minamikawa et al (2007, in Japanese) did not give estimates by area, which also raises difficulty in using the results for management

12.6.3.1 Northern Form Northern-form pilot whales inhabit coastal waters to the north of Choshi Point and are hunted only by small-type whalers There was a considerable discussion in the Fisheries Agency of Japan about regulation of this fishery Scientists of the Agency wished to limit the catch to within 1% of the

TABLE 12.23 Abundance of Short-Finned Pilot Whales off the Pacific Coast of Japan Estimated from Sighting Data Assuming g(0) = 1

understanding in the Scientific Committee of the IWC that a catch of 1% would not harm the stock and on our observations of the population dynamics of killer whale communities off Vancouver Island, which were once depleted to about 60% of the initial level and exhibited at that time an annual recovery rate of 13%–26% If these killer whale populations have been experiencing decline in recent years, our earlier understanding should be reevaluated

Post-World War II catches of the northern form off Japan reached a peak of over 400 in 1949 and then rapidly declined to 10-100 in 1955-1957 (Table 1222) The decline arguably could be explained by a shift of the whaling operation to other cetacean species such as minke and sperm whales (see Sections 1372 and 15323) However, the decline was accompanied by a change in sex ratio; the male proportion declined from 68% in 1948 (n = 321) to 43% in 1953 (n = 224) Males are over twice as large as females and preferred by the whalers (Table 122) The same change was also observed in the catch of the more recent exploitation that started in 1982, that is, from 65% in 1983-1984 to 38% in 1985-1987 (Kasuya and Tai 1993) This change was noted by the Scientific Committee of IWC and interpreted as the reflection of a decline in male abundance or learning of males through experience with whaling vessels Although it was unknown which interpretation was correct, the change was interpreted as a suggestion of high hunting pressure on the small population

Under such circumstances the small-type whalers requested a large quota that was clearly unacceptable to us and unachievable by them (Section 712) They attempted to underreport the catch, which made us suspicious They reported the catch of the 1982 season, the first year of the resumption of exploitation, as 85 northern-form whales However, I felt that the catch was likely underreported and requested a correct figure Then the Small-type Whaling Association corrected the figure to a still suspicious figure of 172 (Table 43) In the 1984 season, I was in Ayukawa to examine the northern-form pilot whales at the whaling stations of Gaibo Whaling, Nihon Whaling (a descendant of Nihon Kinkai Whaling), and Toba Whaling As the season proceeded I had an impression that the daily catch became lower than expected for the good weather conditions that prevailed Their flensing work and the biological examination of the carcasses usually ended in the early evening, and I used to revisit the stations the next morning to see subsequent activities of the whaling One morning in a corner of the flensing platform of Gaibo Whaling I found a small fetus that I had not examined the previous evening Re-examination of my field note and ovary samples failed to identify a candidate mother of the fetus The chief flenser replied to my inquiry that no viscera had been brought from another whaling station This incident further increased my suspicion One cold evening the station manager of Gaibo Whaling announced the end of flensing for the day, and my assistant and I left the station for our hotel, which was about 2 km walk from the land station Hearing the sound of the crusher of the village ice plant in the late evening, we jumped out of bed and rushed to a small hill to see through binoculars a pilot whale being towed up to the

to examine several additional carcasses of the northern form Later the company made an amendment to the operation report of the day to the Fisheries Agency (Kasuya and Tai 1993) A villager later explained that a person in charge of watching us left his post due to the cold and failed to send an alarm to the station manager

Another example of similar goings-on by the whaling people was in Taiji a few years before the end of the Japanese coastal sperm whale fishery One day when I was in Taiji to examine sperm whales taken by Nihon Hogei, a station officer invited me for a drive to the Kumano Shrine saying that there was no sperm whale to be processed on that day He made telephone contacts with the land station during the drive and took me to a restaurant in Katsuura Town for a long dinner When I was allowed to leave and returned to my hotel in Taiji, I saw land station workers cleaning the flensing platform Thus I missed a chance of collecting data in exchange for a luxurious dinner, and the company successfully processed some whales outside the view of the Fisheries Agency biologist This kind of incident was more frequent for inspectors of the Fisheries Agency, who often left their duty for days at a hot spring (Section 15323; Kasuya 1999a, b, in Japanese)

The recent regulation of small-type whaling for the northern-form pilot whale changed as follows In the 1982 season there was no regulation, and the catch of 82 whales in the official report was corrected to 172 for the biologists (without official amendment) In the 1983 season 7 vessels operated with a quota of 175 whales and reported a take of 125 In the 1984 season 6 vessels operated with the same quota and reported a take of 160 whales Based on the incident of hiding catches described earlier, for the 1985 season the biologists insisted that there should be no catch limit but only regulation of fleet size and the fishing season, which ended with a catch of 62 whales In 1986 a quota of 50 was agreed and the take was 28 The 1988 season was expected to be the first year when Japanese small-type whalers would have to live without a minke whale quota In order to smooth the way, the fishermen carried the quota of 50 for the 1987 season over to the 1988 season, when they operated with a 2-year quota of 100 Their catch in 1988 was 98

The nearly stable annual catch of around 50 northernform whales during 1988-2002 was followed by an apparent decline (Table 43) Examination of the operation pattern and catch composition has not been carried out (see Appendix at the end of this chapter) A possible cause of the decline is a shift of the whaling season for northern-form pilot whales from autumn/early winter to summer (Table 71), which was required for participation in the coastal element of Japanese scientific whaling for minke whales that started full-scale operations in 2003 This possibly also caused a conflict with the Baird’s beaked whale hunt (Section 712)

The annual quota of 50 northern-form pilot whales remained unchanged until the 2005 season, when it was reduced to 36 The quota for the southern form allowed for small-type whaling also decreased from 50 to 36 in the 2006 season (Table 1224)

12.6.3.2 Southern Form Along the Pacific coast of Japan southern-form pilot whales usually occur south of Choshi Point at 35°45′N; they are rare off Ayukawa at around 38°15′N (Section 1234) In the offshore waters of the western North Pacific they occur south of 38°N in summer (Miyashita 1993) They have been hunted legally by small-type whaling, drive fisheries, and the crossbow fishery Although the pilot whale (both forms) was not recorded in the catch of the hand-harpoon fishery since 1972 and was not allowed in that fishery since at least 1993, the head of a hand harpoon in the carcass of a northern-form whale (Kasuya and Tai 1993) suggested some unreported take of the species by the hand-harpoon fishery

The current drive team in Taiji carried out its first operation in 1969 and increased to two teams in 1979 accompanied by doubling of the number of operating vessels The two teams merged in 1982, but the number of operating vessels remained at almost the same level (Section 391) The Taiji drive fishery made its first autonomous catch limit of 500 pilot whales (southern form) and 5000 other unspecified small cetaceans in 1982 This was carried out with a prefectural license beginning in 1986 In 1991, the dolphin quota decreased to 2900, while the quota for pilot whales was unchanged The quota was decreased in 1992 to a total of 2500 for all species of small cetaceans to be killed, which could include up to 300 pilot whales In 1993, the Fisheries Agency set catch quotas for each of the 6 small-cetacean species, totaling 2380 including 300 pilot whales (Tables 319, 43, and 63) It was my understanding that the series of quotas had only the function of approving the catch level of the time and did not function to cap the catch

There has been a change in the pilot whale fishery in Taiji since 1969 The annual number of southern-form pilot whales that landed at Taiji fluctuated between 50 and 150 before the establishment of a driving team in 1969 Since 1970 it increased to 91-479 during 1970-1979, and in 1980, when another team joined, it made the largest catch in the post-World War II history of the fishery in Taiji The take in 1980 was 605 according to Fisheries Agency statistics (Table 318), but it could have been 841 (Table 317) The latter figure is based on statistics

I have constructed from records of the Taiji Fishery Cooperative Union (FCU) with cooperation of a union staff member After  competing with the drive fishery, the only small-type whaling vessel (Katsu-maru) in Taiji shifted operations to the Chiba area in 1981, but it resumed the Taiji operation for pilot whales in 1988 together with a new small-type whaling vessel (Seishin-maru) (Table 43) (Note: the Taiji FCU started smalltype whaling with the Seishin-maru for minke whales in the 1983 season, paused in the 1989-1991 seasons, and resumed operations with the Seiwa-maru in 1992; the Katsu-maru was replaced by the Katsu-maru No. 7 in 1998)

Thus, the large landings of pilot whales at Taiji were made by the drive fishery After the peak catch in 1980 the landing of the species by the drive fishery declined annually, with considerable fluctuation, to 157 (or a total of 200, including 43  caught by small-type whaling) in 1993, when the quota was first set by species The catch of the drive fishery reached the quota only once, in 1996, and exceeded 100 in only half of the 14 seasons (1993-2006) with a quota of 300 (Table 319) Decline in the availability of the species to the Taiji fishery seems to be evident in the catch trend

The Fisheries Agency of Japan took the leadership in establishing a catch quota for 1993 for each fishery and species of small cetaceans (Section 65) The principle applied to the southern-form pilot whale was to multiply the abundance of 20,300 estimated for the coastal waters by 2%, and then add 50 to come to 450 The last portion, 50 individuals, was not shared among the fisheries but reserved by the government The basis for the supposed replacement yield of 2% was given in a document dated January 25, 1993, which I received from the Coastal Division of the Fisheries Agency as a division director of the Far Seas Fisheries Research Laboratory It was titled “Principle of the Fisheries Agency in [Managing] Small Cetacean Fisheries (Proposal),” and had “Strictly Confidential” handwritten in red ink

The document first stated that the replacement yield of 1% would be retained for the Baird’s beaked whale and northern-form pilot whale because it was accepted by the IWC, which was probably based on the judgment of the Scientific Committee that the current catch level of these species would

Quota of Short-Finned Pilot Whales Given to Japanese Fisheriesa

catch rate was about 1% The document then noted that the United States assumed 4% as an average Rmax for small cetaceans Rmax is the rate of increase expected for a population near zero density The document assumed 2% (50% of the Rmax) as a MSY rate for southern-form pilot whales and false killer whales and 3% (75% of the Rmax) for other Delphinidae The document assumed 6% as Rmax for the Dall’s porpoise after saying that Japanese biologists as well as those of other countries believe that the Dall’s porpoise has a high Rmax and used 4% (75% of the Rmax assumed for the species) as the MSY rate of the species The values of Rmax and MSY rate were not based on scientific evidence but created by the government staff, supposedly to support the already existing figures of 2%, 3%, and 4% that were necessary to create quotas acceptable to the fisheries (Section 65) It should be noted that these arbitrarily created catch quotas were retained for a subsequent 14 years

It was generally accepted among IWC scientists of the time for baleen whales that MSY is available at around 60% of the initial population level, and that setting a quota by multiplying current abundance by half of the Rmax will, in theory, stabilize the population at a level close to MSY production This assumes that Rmax and the current abundance are correctly estimated, that correct catch statistics are available, and that the population does not oscillate The population may start oscillating due to environmental as well as biological reasons Rmax has not been estimated reliably for any cetacean species, and US scientists assumed 4% for all small cetaceans as a basis of management with a “safety factor” arbitrarily determined for each situation

The Coastal Division probably needed the process presented earlier to create a quota that was close to the actual catch of the time and was acceptable by the fishermen and at the same time armed with quasi science The Coastal Division did not mention much about the management of Baird’s beaked whales and northern-form pilot whales because they were under control of the Offshore Division of the Fisheries Agency Before the earlier described document was issued on January 25, 1993, we scientists received from the Coastal Division a document dated August 5, 1992, titled “On Setting Quotas for Dolphin Fisheries of the 1992 [sic] Season” The document mentioned only the striped dolphin and the Dall’s porpoise and proposed zero quota for the striped dolphin and a total quota of 17,180 for two types of Dall’s porpoises (Section 931), which was 39% of the abundance estimate of the time, with a condition to stop operation of the season if catch of one of the two types exceeded 9000 Scientists of the FSL responded in a letter drafted by myself dated August 6, 1992, which stated that (1) the catch quota for Dall’s porpoises should be half of the proposed figure, which was close to the catch recorded before the explosion of the catch in late 1980s, and (2) management should be based on an abundance level smaller than the mean estimate to take into account uncertainty in the estimation After the field season we discussed the problem and Miyashita sent up a revised version of our agreed opinion (dated December 8, 1992), which proposed a catch level of 1% and quota of 200

letter for other species were 1% for the false killer whale, 2% for other delphinids, and 3% for Dall’s porpoise

The response of the Coastal Division to our suggestion was dated January 1, 1993, and titled “On Catch Quota of Small Cetacean for the 1993 Season.” It stated that 1% was added to the catch level proposed by the FSL scientists, that is, 2% for the southern-form pilot whale, the false killer whale, and the striped dolphin; 4% for the Dall’s porpoise; and 3% for other dolphins, which resulted in quotas of 406 southernform pilot whales and 9000 for each of the two types of Dall’s porpoise FSL scientists then sent a letter signed by Kasuya and Miyashita and dated January 6, 1993, which stated that if a large quota is applied for economic or political reasons, the date and target level of catch to be achieved in the future should be clarified This opinion was not accepted and resulted in the document of January 25, 1993, cited earlier

It seems to be clear that logic was created to explain the already existing quota for southern-form pilot whales of 1993 The person who worked on the issue probably borrowed the idea of a potential biological removal (PBR) accepted in the United States This was a tool developed to judge if an existing incidental mortality of cetaceans was at a safe level or not Thus I am suspicious whether it is a suitable tool for management of dolphin fisheries, because it places weight on safety and at the same time allows arbitrary use of parameters (Section 12) It is calculated as

PBR = Nmin × Rmax × 05 × Fr

where Nmin is minimum population size Fr is a recovery factor

A lower limit of the 95% confidence interval was used for Nmin, and 05 was used for Fr Since the abundance of southern-form pilot whales targeted by Japanese fisheries was estimated at 20,300 with CV = 03, the Nmin would be only 8,364 if a normal distribution of the error were assumed, and the PBR would be 83 The stock would be safe if the catch were less than this figure, which was probably correct but would not be accepted by the fishery The PBR was further tuned by Wade (1998), who noted that the only remaining uncertainty in management was the population size if Rmax were correctly estimated and correct catch statistics were available and showed by simulation that a population was safely managed by using Fr = 1 and using for Nmin the lower 20th percentile of the estimated abundance However, in many practical cases Rmax is unknown and catch statistics are often biased, so Fr = 05 has to be accepted The PBR is an extremely flexible method and has the risk of being used in an arbitrary way

The abundance of 20,300 (CV = 03) was the basis used for the management of the short-finned pilot whale The document dated December 8, 1992, stated that this figure was calculated by a staff member of the FSL, responding to a request by the Coastal Division of Fisheries Agency, by adding 6300 whales estimated for the Okinawa area in 20°N-30°N, 125°E-135°E to the abundance of 14,012 (Table 1223)

noted that the most recent abundance estimate of southernform pilot whales was only 15,000 for the entire western North Pacific (Minamikawa et al 2007, in Japanese) We do not know the population structure of southern form shortfinned pilot whales in this geographical range

In addition to the abundance estimate and population structure, the geographically biased operation of the drive fishery has to be considered for management The range of operation of the crossbow fishery (Okinawa) and the current drive fishery (Taiji) never exceeded 50 nautical miles (925  km) from the coast in the former and is likely to be within 15-20 nautical miles (28-37 km) from the port off Taiji, while the abundance estimate includes waters 200 nautical miles from shore and a broad latitudinal range We know nothing about short-term movement of schools of pilot whales in the western North Pacific Even if we were to assume long-term mixing based on genetic analyses or movement of marked individuals that would be available at some future time, it would be hard to assume free mixing of the species within the current management area inhabited by, for example, 20,300 individuals If schools of short-finned pilot whales have some degree of site fidelity, which is very likely, a density gradient from offshore to coastal waters will be created after years of extensive harvest in nearshore waters

12.6.3.3 Manageability of Short-Finned Pilot Whales The previous section describes some difficulties to be met while managing short-finned pilot whales as a fishery resource; they relate to abundance, reproductive rate, and desire of the fishermen for larger takes Here I will consider social structure and life history as elements that should be considered in the management of the species

Current fishery biology assumes that a population decline due to a fishery improves quality of life of the remaining individuals and results in increase in reproductive rate through improvement of growth, survival, and fecundity, and that the population will move toward recovery Thus, the fishery will arrive at a point where population size is stabilized under a certain catch (which is sustainable yield, SY) The ratio of the current population size to the initial population is called the population level or status, and the ratio of SY to the stabilized population size is called the sustainable yield rate (SYR) SYR is zero at initial population level but increases with decreasing population level and will reach a maximum value near zero population level, called Rmax, which still remains to be estimated for any cetacean species The product of the SYR and the population size is the SY and reaches a maximum value (MSY) at a certain population level called the maximum sustainable yield level (MSYL) The MSYL has not been determined for cetaceans, but the Scientific Committee of the IWC assumed it to be at 60% of the initial population for large baleen whales (not for toothed whales, which live with complex social systems) Various equations have been proposed for the relationship between SYR and population level

It should be noted that the hypothesis presented earlier assumes a stable population under fishing pressure, where

dance of cetaceans is difficult, and it is almost impossible to confirm whether a population is stabilized We do not find in the history of whaling any case where catch and the composition (age and sex) have been stabilized Even when the catch was apparently stable in number, the fishing effort and fishing ground could have changed Thus, whale management under an assumption of a stable population is not based on evidence Most fisheries record an explosion of catch at the beginning, and the stock could have declined before establishment of management It is hard to expect an ideal situation in which catch starts from a low level and increases slowly allowing response of the population to the new density The Taiji drive fishery for pilot whales saw an explosion of the catch in the 1970s, and nominal control started after the catch had started to decline by setting a high quota that was not often reached in subsequent operation of the fishery

A delay in biological response of the population is one of the difficulties to be met in the management of short-finned pilot whales The natural mortality rate may respond rather quickly, although measuring the change will be difficult Full response in birth rate of mature female will take at least 4 years because the gestation time is about 15 months and the nursing period lasts a minimum of 3 years Newborns thus produced might attain sexual maturity at a mean age of 7 years (currently 7-12 years) Therefore, it will take almost 11 years before the biology of the population completes response to a density decline caused by fisheries The fishery is likely to further deplete the population without waiting for the full response of the population Delayed response of a population to density change can cause oscillation of the population and further increase difficulty in management

There is another element as a cause of delay in response of a population to density decline that is expected when the unit of management is not individuals but pods or matrilineal groups, as seen on drive fisheries In a hypothetical situation where catches of pods and pod increase are balanced, the number of individuals (population size) and number of pods will be stable If a drive fishery is established on a population of short-finned pilot whales, the number of pods as well as number of individuals in the population will decline by the amount removed by the drive fishery, but the size of the remaining pods is not directly affected by the fishery This means that density of individuals in a pod remains the same, which is likely to cause further delay in populational response Although evaluation of this effect awaits further understanding of feeding strategy, the following scenario is a possibility

If a drive fishery reduces the number of pods in the population, the remaining pods will increase in size either at a faster speed by responding to the decline in pod density or at the same speed as before without responding to the change in pod density and finally split into more than one pod and achieve recovery of the number of pods in the population The mechanism of pod splitting is unknown but could include (1) death of a core female, (2) limitation of social ability to maintain a large pod, or (3) feeding economy There would be a large time lag between the loss of pods due to the fishery and the recovery by splitting

then decline in the stock (in number of pods) will continue

Fishery management should pay attention to conserving the social structure of short-finned pilot whales and the culture likely retained in the pod Small-type whaling may selectively take large individuals for economic reasons, but most of the other dolphin fisheries are nonselective, and fishery management ignores a possible difference in effects of removing different component of the population It is well known that contribution of members to reproduction differs by age and sex I have pointed out that loss of a mother will adversely affect survival and production of her offspring either suckling or weaned (Section 12572) There are other factors in the case of the short-finned pilot whale Each pod must have accumulated memory and a behavioral pattern based on past experience, which is their culture Females live longer, and older females are likely to have an important role as carriers of the culture If such older females are killed in small-type whaling, the remaining members of the pod will be affected by loss of culture A drive fishery, on the other hand, removes whole pods and wipes out all the culture contained in the pod This process reduces the cultural diversity in a population and damages the adaptability of the population to a changing or fluctuating environment I doubt if the current technology of managing fishery resources is successfully applicable to such highly social species as short-finned pilot whales and some primates

After publication of the Japanese version, Kanaji et al (2011) analyzed the abundance of northern-form pilot whales off Japan using sighting data covering the period of 1984-2006 This study is new in its attempt to estimate annual abundance and its trend over the period and differs from past abundance estimates that combined data of several years to increase sample size and reach a single estimate Their method included a multiplication of school density by mean school size to calculate density of individual whales However, they identified two problems in their data due to observer difference between cruises: (1) a large annual fluctuation in school size that had an annual declining trend and (2) uncertainty in classifying primary and secondary sightings In order to overcome these problems Kanaji et al (2011) used two methods One was to use a single common mean school size calculated from all the primary sightings as recorded by observers, and the other was to estimate annual mean school size based on regression of mean school size on year using the same data as given earlier They also felt that some of the secondary sightings could have been erroneously classified as primary sighting In order to correct this bias the authors applied the ratio of primary to secondary sightings obtained elsewhere Thus they obtained four sets of estimates of abundance and annual trend Because these correction procedures were made by combining all the data for 1984-2006, each estimate was not independent in a strict sense

Each of the four abundance series was represented by eight estimates for the years 1985-1988, 1991, 1992, 1997, and

dance estimates was 32 in total None of the members of the pairs were statistically different (CV of each estimate ranged between 049 and 080) The fluctuation must, at least in part, be due to limited opportunity of encountering schools of the species and limited sighting effort

Kanaji et al (2011) noted a trend common to the four series of abundance estimates: (1) high abundance figures for 1985 (6287-8646), (2) low figures for 1986-1988 (1086-1690), (3)  a weak upward trend from 1991 to 2006 (2415-3971) In  my view, the high figures for 1985 are likely reliable because they are close to the previous estimate of 5344 (IWC 1992) obtained by combining the data for 1982-1988 (Table  313) The smaller figures for the later years (19862006) may reflect a declining trend

Kanaji et al (2011) indicated that the annual catch since 1982, when exploitation resumed, exceeded the safe take level calculated by applying PBR to the annual abundance estimate and suggested that whaling contributed to the apparent decline The parameters used for the PBR calculation were Rmax = 4%, Fr = 05 and Nmin as the 20th percentile as suggested by Wade (1998)

The total reported catch by the small-type whalers during 1982 through 1988 was 645 (Table 43), and it is still unconfirmed whether such a small take alone could explain the observed apparent declining trend