ABSTRACT
Introduction ��������������������������������������������������������������������������������������������������������������������������������������92 Materials and Methods ��������������������������������������������������������������������������������������������������������������������93
Experimental Design �������������������������������������������������������������������������������������������������������������������93 Study Site ������������������������������������������������������������������������������������������������������������������������������������93 Experimental Organisms ������������������������������������������������������������������������������������������������������������93 Setup of the Experiment��������������������������������������������������������������������������������������������������������������94 Method of Attachment ���������������������������������������������������������������������������������������������������������������� 95 Electricity Supply ������������������������������������������������������������������������������������������������������������������������95 Data Collection Time Frame �������������������������������������������������������������������������������������������������������96 Measurements and Documentation ���������������������������������������������������������������������������������������������96 Data Selection �����������������������������������������������������������������������������������������������������������������������������96
Sponge-Infested Sample Corals ���������������������������������������������������������������������������������������������96 Uninfested Sample Corals ������������������������������������������������������������������������������������������������������97
Results ����������������������������������������������������������������������������������������������������������������������������������������������97 Sponge Extension Increase Experiment ��������������������������������������������������������������������������������������97
Acropora microphthalma Growth Rate ���������������������������������������������������������������������������������97 Relation of Sponge Extension Increase and Distance to Electrical Source ��������������������������������97 Comparison of First and Second Measurement Period Regarding Their Respective Sponge-Extension Increase ���������������������������������������������������������������������������������������99
Discussion ����������������������������������������������������������������������������������������������������������������������������������������99 First and Second Growth Period �������������������������������������������������������������������������������������������������99 Coral Growth ������������������������������������������������������������������������������������������������������������������������������99 Negative Impact of Electricity on Sponges ������������������������������������������������������������������������������� 100 Reasons for Sponge Extension Increase on Electrified Structures ������������������������������������������� 100
Conclusions ������������������������������������������������������������������������������������������������������������������������������������ 102 Acknowledgments �������������������������������������������������������������������������������������������������������������������������� 102 References �������������������������������������������������������������������������������������������������������������������������������������� 103
INTRODUCTION
Corals growing on Biorock reefs typically grow 2-6 times faster than controls and have 16-50 times higher survival after severe bleaching (Goreau and Hilbertz 2005, 2008)� Nevertheless, sponge overgrowth of some species of corals by certain sponges has occurred on some electrical coral-reef restoration projects in the Maldives and in Bali and Lombok Indonesia� This project determined the growth rates of corals and sponge overgrowth as a function of distance from the electrical field to determine whether electricity affected the sponge-coral interaction� Due to the higher levels of sponge overgrowth on some structures than on nearby natural reefs, it was initially hypothesized that sponge growth might be stimulated more than coral growth, favoring sponge overgrowth (Figures 8�1 through 8�3)�
MATERIALS AND METHODS
Experimental Design
Seven measurement sites, two on electrically connected Biorock structures and five at different distances from the electrical structures, give insight into the question whether sponges or corals gain advantages through electrical sources and how this decreases with distance from the electrical field�
Study Site
The experiment was carried out on the Karang Lestari Coral Reef Restoration project in Pemuteran, Bali, Indonesia� The village of Pemuteran (8°02′ South; 114°39′ East) faces the Bali Sea near the northwest corner of the island� Here, around 50 Biorock structures (2008 status) are located inside a village No Fishing protected area� This zone is parallel to the coastline with a total length of around 300 m� The structures are mostly 50-80 m from the shore at depths between 3 and 7 m�
Experimental Organisms
While they are hard to find in the natural reef surrounding the structures, several species of sponges, mainly red-, orange-, and pale pink-colored species seem to be a problem due to their high abundances on certain structures� They chiefly grow along the underside of the horizontal rails of a structure or fully along the vertical rails of structures, and when they reach a coral of certain species they start to overgrow the coral, whereby the coral often dies, with some species being far more susceptible to overgrowth than others� Above all, the extension of a pale pink sponge involves encroachment over living coral tissues� The most abundant species of sponge on the projects, an unidentified
pink-colored encrusting sponge, often with a whitish surface coating and fleshy red tissue, specifically attacks Acropora microphthalma, a fragile but common species on the projects� After the coral has been overgrown and killed, it eventually breaks off, and the sponge appears to weaken the dead coral skeleton�
The sponge usually occurs as a few millimeters-thick encrusting layer, but on some spots it occurs as thin, fingerlike growths up to 20 cm long along the substrata, with connected branches growing out from an encrusting base� During a six-month period, these sponge branches were noted reaching from one overgrown coral branch to another branch to another overgrown coral branch� The sponge grew together, filling the gap between the coral branches�
Setup of the Experiment
The experiment, which lasted for 88 days, was set up at the western end of the project and up to 100 m westward of it� In order to determine if the strength of the electrical field affected coral and sponge growth rates, specimens whose growth was measured were placed on top of a structuredirectly under a structure but not in physical contact with it-and at distances of 3, 10, 30, and 100 m away from a structure� Structure 22 and Fish Structure 3 were used for the experiment�
The measurement sites are named in compliance with their distance to the closest structure� Therefore, the seven measurement sites are called 3 m, 10 m, 30 m, and 100 m; and accordingly, samples under Structure 22 are called uST22 and measurement sites with samples directly on Structure 22 or Fish Structure 3 are called ST22 or Fish3�
Both structures were used for the experiment, as they showed interesting differences although located near to each other� With its simple design and its few struts, Structure 22 is one of the most successful structures of the project in building up limestone� Around the construction steel bars of diameter 1-1�2 cm, up to 4-8 cm diameter of limestone has accumulated� That structure has very little sponge growth� Fish Structure 3 is made from a construction-wire mesh with a diameter of 0�6-0�8 cm� The material itself and its many welds diminish conductivity� Additionally, the cables of this structure have to be some 15 m longer, so that there is more voltage drop� These factors give reasons for less power flow through Fish Structure 3, and so for a diameter increase has been much slower, only 2 cm� The essential point is the divergence in sponge infestation, which is highest on the structure that is receiving less power and growing more slowly� While rapidly growing Structure 22 (Figure 8�4) and its corals show only little sponge presence, slowly growing Fish Structure 3 (Figure 8�5) was almost completely covered with sponge, and sponge infestation on the corals growing on the structure is intense�
Method of Attachment
Two options of material for the coral-attaching devices were chosen: thirty 2 cm diameter and 50 cm long plastic tubes stabilized by cement pedestals, and thirty 1 cm diameter and 1 m long iron rods that simply could be hammered into the ground�
Around each measurement site mark, six iron rods were driven into the sand, and six plastic cement devices were placed� These two sorts of attaching devices were mixed-positioned, so there was no group forming, and effects of location were minimized� Although all the attaching devices were positioned as close as possible to minimize divergences in distance to the electrical source and depth, an inevitable distance was kept to prevent any contact of the samples with each other during the experimental period� In the case of uST22, an adequate distance to prevent contact to the structure was included�
All corals on the attaching devices, including those on Structure 22, are around 50 cm above the bottom� The corals on Fish Structure 3 are around 2 m above the bottom� All corals were located at depths of 3�9 to 4�4 m below the surface� The specimens were tied on with plastic cable ties�
On the five measurement sites that are not directly on the two structures, namely sites uST22, 3 m, 10 m, 30 m, and 100 m, three corals without any sponge and three sponge-infested corals were fixed onto iron rods and the same numbers onto the plastic tubes�
On Fish Structure 3 and on Structure 22, four corals without any sponge and four spongeinfested corals were fixed on to each of them�
Coral samples, after a few days of attachment at all measurement sites, appeared to be colorful and healthy-looking�
Electricity Supply
The power supply is switched on for around eight hours per day� To check that the electrolysis process is working, structures were observed to see if hydrogen
gas bubbles were rising and the anodes were clean and working normally�
During the running time of the experiment, voltage values fluctuated between 11 and 13 V� Amperes on the measured cables connected to the anodes placed around Structure 22 and Fish Structure 3 varied from 7�2 to 14�5 A, with an average of 9�6 A�
Data Collection Time Frame
Growth measurements were carried out three times� The process of data collection was repeated every time in the same chronological order� The first images of the samples were taken just after the setup of the experiment on April 17, 2008; the first repetition was right in the middle of the running period on May 30, 2008; and the last one was 88 days later on July 12, 2008� Each particular data collection was carried out after the fifth day with the measurement of the second half of the sample corals� The experiment ended on July 16, 2008�
Measurements and Documentation
To record data about sponge extension increase, photographs were taken for each coral branch infested with sponge�
A ruler was held on the same spatial level as the branch� This provides an equivalent scale for the measurement software ImageJ 1�40g with which the sponge expansion was ascertained�
Coral growth was documented by measuring height, width, and depth of each sample coral with a vernier caliper�
Data Selection
Sponge-Infested Sample Corals
Excluded Sponge Growth Values
At the collection of data, the increasing extension of sponge on all infested branches of the sample corals was measured� Sixty-six separate values were recorded�
Thirty-five of them were used for further analysis, while 31 values were excluded� The reasons for their exclusion are listed in Table 8�1
After Fish Structure 3 was knocked over by an exceptionally rough sea, samples on it were excluded from statistical interpretations� Other reasons for sample loss, like break-offs, overgrowth or bleaching are documented in Table 8�1�
Remaining Sample Distribution
How many samples on each measurement site were taken into consideration and how many samples got lost on each site is shown in Table 8�2�
Uninfested Sample Corals
Out of the 38 attached samples, the data of 27 samples could be used for further interpretations� Eleven samples had to be excluded� The exclusion of samples is attributed to three reasons� Fish Structure 3 was knocked over during exceptionally rough seas, and therefore the data of Fish Structure 3 were not used anymore for a comparison of the various measurement sites� Furthermore, two samples together with their spear qualified iron rod attaching device disappeared at measurement site 100 m� The remaining five losses are attributed to reductions of the volume of the sample coral� This reason for exclusion is caused by fish bites or somehow incurred break-offs� These are equally distributed among the measurement sites; they all have one loss because of volume reduction�
RESULTS
Sponge Extension Increase Experiment
No differences in growth, health, or sponge extension increase are found due to the use of iron rods compared to the use of plastic tubes�
Acropora microphthalma Growth Rate
Considering the total experimental time frame, a significant difference between two groups could be detected (ANOVA; P = 0�004)� There is accelerated coral growth on Structure 22, under it, and near to it, compared to the other measurement sites, which are further away� This beneficial effect seems to be the result of the electrical field around the structures and extends at least 3 m, but less than 10 m, from it�
However, it is important to note that coral growth was fairly variable between the two time intervals (Figure 8�6)� In general, the values of the second period are closer together than those of the first period� The near the structure, sites uST22 and 3 m grew faster the first 44 days than the second 44 days� The other four sites had faster growth rate in the second period than the first� The majority of individual growth values of ST22 at the first growth period rank behind those of 3 m and uST22 and ahead of those at the further measurement sites, but at the second growth period, the single values of ST22 are like those of 3 m and uST22: not very outstanding compared to the other measurement sites� Group forming could be determined in the first time interval (ANOVA; P = 0�000) but not for the second (ANOVA; P = 0�473)�
Relation of Sponge Extension Increase and Distance to Electrical Source
Sponge extension increase is higher on weak corals than on vital ones� For example, if a branch is already bleached, there is hardly any defense against the sponge anymore� So the sponge growth
rate over bleached branches is clearly higher� Average sponge growth over bleached branches was 8�4 cm, about twice as high as on healthy corals (i�e�, not bleached)� Many corals being overgrown by sponges were observed bleached, although a thermal bleaching event was not under way� It is possible that this bleaching is a stress response to allelochemicals released by the sponge� This needs to be tested�
The samples on ST22 are the strongest in contrast to the bleached samples� Three of the four lowest sponge growth rates, below 2 cm, belong to the three samples on ST22� The corals on the structure appear to be more resistant to sponge overgrowth (Figure 8�7)�
Sponges clearly grew more slowly, by about 62%, on corals on Structure 22 than they did anywhere near or far from them� Considering the total experimental time frame, a significant difference between two groups, ST22 versus all other measurement sites, could be detected (ANOVA; P = 0�004)� The role of electricity, therefore, appears to inhibit overgrowth of living corals by encrusting sponges on the electrified reef in Pemuteran, providing an advantage to the corals�
Further, it is noteworthy that as mentioned, only the samples at ST22 seem to be influenced� The two nearby sites uST22 and 3m, which showed elevated coral growth during the first measurement period, do not stand out from those farther away with regard to sponge growth� Both uST22 and 3 m have the same average of 4�2 cm, which hardly differs from the total average of 4�3 cm of the three measurement sites 10 m, 30 m, and 100 m�
Comparison of First and Second Measurement Period Regarding Their Respective Sponge-Extension Increase
The outstanding character of ST22 exists in both periods� After the first period, sponge extension increase is on average 1�5 cm slower on ST22 than on the other measurement sites, and with 1�3 cm slower increase after the second period�
However, during the second 44 days, sponge-extension increase was greater than during the first 44 days� At the second measurement on some infested branches of the samples at ST22, the sponge extension even declined� Such developments could not be registered after the third measurement�
On the other measurement sites, there is no such sponge decrease� On comparing the two measurement periods, the averages of 10 m and 30 m had gone up, respectively, 1�1 and 1�3 cm� The averages of the other three measurement sites went up only a little or not at all� They already had shown high increase values at the first period� Like the A. microphthalma, growth measurements during the first period show higher results than the during second period� Over the first period, group forming (ST22 vs� all other measurement sites) can be confirmed (ANOVA; P = 0�039)� Over the second period, it was not significant (ANOVA; P = 0�878)� The different character of ST22 can only be guessed� However, as shown in Figure 8�8, ST22 has the slowest growth values in the first and second periods�
DISCUSSION
First and Second Growth Period
The difference between growth values of samples on the structure and other measurement sites for coral growth and for sponge growth is more significant at the first period� The cause of this difference cannot be detected with certainty� Only assumptions can be made� One reason which would confirm the results of this work would be if, at the second measurement period, the power supply would have been interrupted or off for various days unobserved� Another possibility is seasonal variations in zooplankton food supply for corals and bacterial food for sponges� Higher sample numbers and more measurements to detect seasonal changes would have brought more certainty�
Coral Growth
The stimulating influence of the electricity on the growth of A. microphthalma on the structures and in the area around the structures seems to be obvious� During the first growth period, growth-rate ranking of samples is divided, with hardly any exceptions, into two groups� Samples on Structure 22, under the structure and 3 m away, grew faster than samples on the other measurement
sites farther away� Curiously, during the second growth period, there were smaller differences� For future research on coral growth acceleration, the distance and position to the anode should be taken into consideration, since at the first growth period, corals had high growth values, especially corals on measurement site 3 m, which is located in between Anode 7 and Structure 22�
Negative Impact of Electricity on Sponges
As the results of the sponge extension increase experiment show, electrical current does not offer any growth advantage for the pale pink sponge already infested on the coral A. microphthalma; in fact, it reduces sponge growth� Although the coral could not effectively reject the sponge, sponge growth was even slower on sample corals attached to the structure than on those attached to devices of the other measurement sites�
Since electricity decreased sponge growth rates, and since the structures having fast growth due to higher electrical current have few sponge problems compared to those that are growing slowly, we decided to test if increasing the current on a slow-growing, sponge-infested structure would get rid of the sponges� Fish Structure 3, which was heavily sponge-infested, was used for this experiment� The power was about doubled, and the mineral growth on the structure immediately increased� Sponge cover, which covered almost all the surface of the structure at the start, steadily decreased until only small isolated patches of sponges remained several months later� Therefore, structures that have sponge problems can get rid of them by increasing the power� The result of this attempt confirms the results of the sponge extension increase experiment�
Why sponges should grow more slowly on the structures while hard corals grow faster-and soft corals, tunicates, and bivalves also appear to-is curious� Since this is a function of being on the structure itself, and not the electrical field that stimulates corals in the vicinity of the structures, a likely explanation is the high pH generated by electrochemical reactions at the growing surface� While this makes limestone less insoluble, causing it to precipitate and grow from seawater, the silica material that makes up sponge skeletal spicules has the opposite behavior: it dissolves under high pH� Loss of the skeletal material may be the cause of reduced growth, and histological studies would be needed to clarify this�
Reasons for Sponge Extension Increase on Electrified Structures
Sponge extension on the slow-growing electric reefs is shown by close encrusting growth over the frame of the slow-growing structures, but fast-growing structures and the natural reef surrounding the structures are not affected by excessive sponge abundance� If it was only a problem of nutrition or the absence of sponge growth-controlling fish, the reef straight under and beside the structure would be impacted too�
Sponge-feeding fish seemed pretty conspicuous around the artificial reef, but a further examination of the pale pink sponge on the structures as well as on those measurement sites away from any electrical influence indicated very little physical damage or bite marks on sponges, as injuries of the pale pink tissue would have been obviously noticeable through the underlying bright red tissue beneath a pale surface layer�
The high abundance of sponges on the structures is not due to increased growth rates, since the sponge actually grows more slowly under electricity� Presumably higher recruitment and settling of sponge larvae on slow-growing structures and unhindered sponge extension on the preferred shadowed underside areas or the superior location of the three-dimensional structure-which allows filter feeders to be right in the middle of water movement, offering increased food supply-may be reasons for the very successful growth of this species�
In the following, various underlying possibilities for excessive sponge settlement will be further discussed:
According to a progress report from 2001 about the attachment of the first corals on, at this time, still-bare frames, “In order to avoid damaging healthy corals but to rescue broken-off specimens, fragments lying on reef slopes or buried in sand were selected for transplantation�” Since “large numbers of corals were found loose, often having had their bases undermined by boring worms, clams and sponges” and even “a few totally dead corals were attached because some divers involved in collection were insufficiently experienced at identifying live corals” (Hilbertz and Goreau 2001), the possibility that sponges were widely transplanted together as overgrowths with the first corals is quite likely�
Additionally, another human activity, the attempt to get rid of the recognized threat to the coral garden by scrubbing sponges off the bars of the structures, may again have caused further spreading� Even though regeneration from removed tissue is slow-and sometimes, when large parts are removed, is irreparable for some encrusting species-other sponges are rapidly regenerating� Some encrusting species even stop undisturbed tissue growth when regenerating, and patches where almost all living tissue was scraped off rocks can recover rapidly (Ayling 1983)� The futility of the attempt to free the structures from sponge cover by scrubbing them and assuming that encrusting sponge regeneration is inversely related to resistance to damage (Wulff 2006) suggests that the soft, easy-to-injure pale pink sponge can rapidly regenerate in supposedly cleaned areas� Torn fragments may rapidly reattach to the available substrata (Rützler 2), and probably all sponges are capable of regenerating viable adults from fragments (Brusca and Brusca 2003), so there is a high risk to support asexual spreading� Experiments with a sample sponge of the same genus underline the impressive survival strategies of some sponges� The cells of sponges pressed through fine cloth immediately began to reorganize themselves and reformed a functional sponge within two to three weeks (Brusca and Brusca 2003)� Additional asexual processes, such as the formation of reduction bodies with omnipotent cells that were spread during the attempt to clean the structures from sponge cover and could hatch out on numerous new spots of available substrata, may aggravate the sponge problem�
Although transplanting infested samples or scrubbing off sponges may aggravate the situation, it is probably not responsible for it, as the moment of the first attempt to clean structures was after obvious infestation and sponge spreading and did not result in large new colonization adjacent to the project�
In the first place, the spreading of the pale pink sponge at the artificial reef has very likely something to do with natural recruitment and with characteristics of the structure, including the availability of substrata, the location in the middle of water movement, or even the electrical attraction of the larvae� This needs to be directly tested�
The artificial reefs provide new suitable substrata, which allow opportunities for the dominant fastest-spreading species� Some corals may even be successful against sponge encroachment; sponge recruits will develop faster, and sponge is occupying space, preventing coral recruitment� The shaded underside of the bars is preferred by the sponge�
Furthermore, the structures may have a filter function� Standing in the movement of water, structures are offering substrata for sponge larvae or reduction bodies brought along� Particularly, strong sponge extension on more vertical structures with relatively close spacing of structural elements and slow mineral aggregation rates support the argument�
The most sponge-covered structures are constructed out of construction-wire mesh, with smaller diameter, inferior material composition, many welds, and lower electrical conductivity� The most infested of all structures inside the Karang Lestari project area is Fish 3 which is furthermore one of the structures with the longest distance to the land-based chargers and therefore has higher voltage drop because of longer cables�
Since the sponge is growing more slowly, higher sponge abundance must be due to greatly increased sponge-settlement rates, perhaps because the sponge larvae are attracted to low electrical fields� Whether they settle more or less on rapidly growing structures is unclear, as the smaller number of sponges apparent could also be due to the electrical inhibition of growth� Direct measurements of the effect of electrical fields on sponge settlement are needed�
CONCLUSIONS
Corals growing on electrified Biorock reef-restoration projects have higher growth and survival than control corals, yet on some projects in the Maldives and the Indonesian Islands of Bali and Lombok, sponge overgrowth of corals by several sponge species has been a problem, raising the question whether the sponge growth rate was accelerated more than the coral growth by the electrical current, thereby shifting the competitive advantage to the sponge� Direct measurements were made of the growth rate of a highly susceptible corals species, A. microphthalma, and of sponge overgrowth as a function of distance from the electrical field� The results showed that coral growth was stimulated in the vicinity of the Biorock structure, not only on it, but around it up to at least 3 m away from the structure, close to the anode� In contrast, sponge growth was sharply reduced, but only directly on the structure itself, and not in the vicinity, where it was much higher� Therefore, the electrical current represses sponge growth and favors coral survival over sponges on the electrified structures� The high abundance of overgrowth on A. microphthalma must, therefore, be due to much higher settlement of sponge larvae on the structure due to the attraction to the current and/or unhindered growth on seemingly preferred shadowed areas on the underside of a structure bar, wherefrom the sponge starts to attack corals attached on top of a bar�
ACKNOWLEDGMENTS
First of all, I would like to thank the two supervisors of my bachelor thesis (Coral Reef Management-The Role of Electricity on Coral overgrowth by Encrusting Sponges on a Biorock Artificial Reef Project) who supply the basis for this chapter, Dr� Thomas J� Goreau (Global Coral Reef Alliance, USA) for making the first contact to Pemuteran and for his constant support and engagement during all steps of this work, and Prof� Dr� Martin Welp (FH Eberswalde, Germany) for his support and guidance along the process of my bachelor thesis� I deeply appreciate the support of the following individuals who contributed to the achievements of the field trip and/or made the six-month stay in Pemuteran an unforgettable experience: Nara Narayana and, Rani E� Morrow-Wuigk (both in multiple ways); Pak Agung Prana; Michael Cortenbach from Bali Hai Diving Academy for placing free diving equipment at my disposal; the friendly staff of Bali Hai; Putu Yasa, Komang, and Putu from the Biorock Centre; the whole “Badini family” for being my home away from home; as well as Komang, Sandi, and Bagong� I also thank Stephanie Abel for editing grammar and style; Eric Fee for making scientific papers available to me; Dr� Carden Wallace for sample coral identification; Dr� Christine Schönberg; and Dr Nicole J� de Voogd for communication about the project� Last but not least, I thank my family and friends for their support and patience, and Melanie Adam for not only being by my side in the Bali Sea, taking the photographs, assisting in setting up and documenting the experiment, and sharing great impressions and experiences, but also for being in my life� My apologies to everyone I should have mentioned here but omitted to do so�
REFERENCES
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