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Exploration of structure and trophodynamics of coelobite (cavity-dwelling) communities in Red Sea coral reefs [Elektronische Ressource] / vorgelegt von Mark Wunsch


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Published 01 January 2002
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Exploration of structure and trophodynamics of coelobite (cavity-dwelling) communities in Red Sea coral reefs
Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften Dr. rer. nat.–
im Fachbereich 2 (Biologie/Chemie) der Universität Bremen
vorgelegt von
Mark Wunsch
Zentrum für Marine Tropenökologie Center for Tropical Marine Ecology Bremen 1999
Die vorliegende Arbeit wurde in der Zeit vom Juli 1996 bis Dezember 1999 am Zentrum für Marine Tropenökologie (ZMT) in Bremen angefertigt.
1. Gutachter: 2. Gutachterin:
Prof. Dr. Gotthilf Hempel PD Dr. Sigrid Schiel
ACKNOWLEDGEMENTS This research was funded by the Red Sea Program for Marine Sciences, grant no. 03F0151A and 03F0245A, of the German Federal Ministry of Education and Research (BMBF). First of all I would like to thank Prof. Dr. Gotthilf Hempel for his support and advice. He was a great and patient supervisor who overcame the worries of having a student who is interested in video techniques and likes fiddeling around with equipment. I am grateful to PD Dr. Sigrid Schiel for accepting the job of second referee. I owe special thanks to Claudio Richter for being a great colleague, supervisor and friend. He was an invaluable companion in the crypto team, constant generator of ideas and encouragement as well as a reliable dive buddy. Thank you for all the memorable days and night shifts we spent together below and above the water! He and Katharina Fabricius were fascinated by the "Swiss-cheese" structure of the reef and thus started the story about the black holes in the reef which I tried to fill out with some colours during my work. Thank you both! My warm thanks to Dr. Ahmed Abu-Hilal for his generous hospitality and support at the Marine Science Station in Aqaba. He, the staff and the students of the MSS always made me feel welcome and helped wherever they could. I thoroughly enjoyed staying with them. I am grateful to Dr. Salim A l -Moghrabi for support and fruitful discussions and to Dr. Mohammed Badran for support in the chemistry lab. Shukran! I would like to thank the Egyptian Environmental Affairs Agency (EEAA), DR General Omar Hassan for the permission to work in their beautiful coral reefs. I hope they will succeed to protect them against all pressures from tourist development and other threats. I owe special thanks to Dr. Alain de Grissac for accommodating us and facilitating work in the Ras Mohammed National Park. Essam S a a d a l l a brought in his expertise of the coral reefs in Egypt. He and Ayman Mabrouk were always enthusiastic dive buddies and became good friends. The Interuniversity Institute in Eilat provided us with a lab where we could accommodate all our gear. Special thanks to Dr. Amatzia Genin, Gitai and Ruthy Yahel for logistic support and good company. I am grateful to the Israeli Nature Reserve Authority for the permission to work in the Marine Reserve. Toda raba! I would like to thank Dr. Rob van Soest (University of Amsterdam, Netherlands) for taxonomic identification of the sponge samples. Joachim Scholz (Senckenberg Research Institute, Germany) identified bryozoans, Patricia Kott (Queensland Museum Brisbane, Australia) ascidians, Peter Schuchert (Museum of Natural History, Geneva, Switzerland) hydrozoans, Helmut Zibrowius (University of Marseille, France) ahermatypic corals, Katharina Fabricius (Australian Institute of Marine Science, Australia) soft corals, Manfred Grasshoff (Research Institute Senckenberg, Germany) gorgonians, Doug Fenner and Charles Veron (Australian Institute of Marine Science, Australia) hard corals, Lukas Hottinger (Natural History Museum, Basel, Switzerland) foraminifers, Dieter Fiege (Research Institute Senckenberg, Germany) polychaetes and Derek Keats (University of the Western Cape, South Africa) algae. H. Schuhmacher (University of Essen, Germany) identified some organisms from photographs. Thank you all for your quick replies and amusing e-mails! Wolfgang Metzler (Department of Geology, University of Bremen) engineered the electronics for t h e sophisticated cave-lightmeter and Wolfgang Fulda and the students of the University workshop built an underwater housing for it. Andrea Wieland and Gerhard Holst from the Max-Planck Institute for Marine Microbiology, Bremen provided the photodiode and wavelength filter. Thank you all! I thank Benoit Beliaeff (IFREMER, France) for discussing a statistically valuable set-up of my cave surveys. Merçi! Ard Jonker and Norbert Vischer (University of Amsterdam, Netherlands) gave advice on object image analysis and macros facilitating the analysis of my video data. Bedankt! Dieter Piepenburg (Institute for Polar Ecology, Kiel) introduced me to the secrets of the PRIMER program. Volker Koch and Boris Koch provided help with data base management and program installation. Sabine Kadler always gave logistic support and Gesche Krause drew maps. Thanks to a l l the staff at ZMT who helped in one way or another. Danke! Kirsten Schwarz joined as a dive buddy. Britta Munkes was always an enthusiastic Hiwi and a great help in the last phase. I am especially grateful to my parents for their continuous support and love. Danke, Ihr Lieben! Dear Iris, thank you sooo much for the fun, your love, help, support and patience throughout these last, always too short years!
Summary and Conclusions General Introduction Literature Chapter 1 The CaveCam–an endoscopic underwater videosystem for the exploration of cryptic habitats (Marine Ecology Progress Series 1998, Vol. 169: 277-282) Abstract Applications Conclusions Literature Chapter 2 The LightSheet–a new tool for surveying the morphology of underwater cavities Abstract Introduction Main Principle and System Description Procedure Accuracy Conclusions and Outlook Literature Chapter 3 Coelobite (cavity-dwelling) communities and environmental conditions in Red Sea coral reef crevices Abstract Introduction Materials and Methods Results Discussion Literature Chapter 4 Cavity-dwelling suspension feeders in coral reefs– a new link in reef trophodynamics (Marine Ecology Progress Series 1999, Vol. 188: 105-116) Abstract Introduction Material and Methods Results Discussion Literature Chapter 5 Dense populations of cavity-dwelling sponges deplete phytoplankton in Red Sea coral reefs Abstract Main Text Literature Chapter 6 An illustrated checklist of coelobite (cavity-dwelling) organisms in Red Sea coral reefs Colour Plates                                                                                                       63
 1  2  3 5 7 9 9 11 11 12 13 17 18 19 19 20 25 39 42 44 44 45 48 51 54 56 56 60 62
SUMMARY AND CONCLUSIONS The results of this work are a contribution to the understanding of the ecology of coral reef cavities and to coral reef research in general. The development of the CaveCam (Chapter 1) provided the key for a new line of coral reef research as it made available state-of-the-art endoscopic video-techniques for underwater work. Using the small handheld system and conventional SCUBA gear I was able to document the uncharted labyrinth of framework cavities interlacing coral reefs in a non-destructive way. This ‘soft’ approach obliterated earlier crude methods such as plying apart or blasting t h e framework, without compromising on the quality of the data. The accuracy of the image analysis i s ensured by ground-truthing the video records with a reference collection of selected taxa. More important, however, has the CaveCam extended the range of exploration of cryptic habitats from t h e easily accessible and rather ‘open’ overhangs, undersides of foliaceous corals, rubble, large caves, etc., to  the up to now inaccessible inner reaches of the reef framework. By yielding 1:1 close-up images of specimens up to 4 m away from the observer it is very powerful for this application. Finally, the motion pictures provide important information not only on community structure but also on the dynamics of t h e system, e.g. of ambient current flow, currents induced by active filter feeders and behaviour of vagrant organisms. I used some of these sequences along with additional material for producing a small documentary on the subject for a public TV-channel as this is a good way to convey our insights and fascination to the non-scientific public and to promote scientific work. The LightSheet (Chapter 2) proved an useful tool for determining the complex morphology of t h e highly irregular framework cavities. The volume and wall area of more or less straight tunnel cavities can be accurately determined within a <5% error margin. Accuracy decreases with increasing complexity of the cavities, where protruding ledges may obstruct part of the picture or side-arms branching off at sharp angles may be overlooked. This leads to an underestimation of the available space, and hence, to conservative estimates. The 3-D reconstructions of the cavities can be used for modelling water flow through cavities under different hydrodynamic forcing, turbulent exchange processes between water and cavity walls, etc. The analysis of the large collection of video images revealed a rich variety of mainly encrusting organisms (Chapter 3). Coralline algae predominated on the walls near the cavity entrances, while t h e gloomy and dark inner sections of the cavities were colonized by a diverse cryptofauna: filter feeders abounded, notably sponges, which covered up to more than 50% of the substrate, e.g. in the well flushed inner parts of Moses Rock, Eilat, Israel. Passive suspension feeders, such as sessile foraminifers and corals, were more patchily distributed and confined to well-flushed areas, e.g. near the cavity entrances. Light is a crucial factor determining the balance between photoautotroph and heterotroph organisms near the cavity entrance, while food supply and competition for space shape the composition of the heterotroph community further away. The metabolic activity of the coelobite community is reflected in small-scale gradients in chlorophylla and oxygen concentrations between cavities and freestream waters over the reef (Chapter 4), where stronger gradients appear to be associated with reduced flow and higher coelobite cover. Direct and indirect measurements of water replacement rates within the cavities allowed first quantitative estimates of the bulk filtering effect of the coelobite community. The conservative estimates showed that the coelobite community trapped extrinsic organic material at rates one order of magnitude higher than epi-reefal communities. Thus this newly discovered trophic pathway channels pelagic production into the coral reef. However, due to the lack of quantitative community data, spatio-temporal resolution of chlorophyllato treat the cavities as ‘black boxes’. and oxygen, at that time we still had It is only after the quantitative high-resolution analysis of filter-feeder cover, water exchange as well as chlorophyllaand oxygen concentrations that we can provide circumstantial evidence, that coelobite filter feeders are indeedcausingthe oberserved phytoplankton depletions (Richter, & Badran Wunsch Chapter 5). Time-series data show strong variations in the magnitude of chlorophylladepletions in a given set of cavities, depending mostly on the ambient flow conditions. Concomitant nutrient analyses indicated that remineralization of the largely extrinsic organic matter taken up by the coelobite filter feeders may fuel close to 20% of the gross metabolism of the entire reef. If validated by independent studies in other areas, this would indeed alter the way we perceive coral reefs. Examples of the latter are provided in Chapter 6, a checklist of coelobite organisms in the Red S e a , which is a tribute to the many friends out in the field who helped me in this work and were interested in field identification.
Coral reefs are the most diverse ecosystems in the sea and the largest biological structures on earth. The profusion and dazzling beauty of life on the surface of a coral reef holds one’s attention so completely, that it takes considerable experience to realize that its bulk volume is largely empty (Ginsburg 1983): crevices, caves, cracks and holes of all shapes and sizes interlace the coral reef framework, giving rise to a complex three-dimensional labyrinth. Growth and the various kinds of erosion of the reef framework are the sculpturing forces shaping the carbonate rock, enlarging t h e available surface for settlement by a factor 2 or more (Jackson et al. 1971, Logan et al. 1984). The dark and sheltered nature of framework cavities provides a particular setting to which the reef flora and fauna have to adapt. Growth of algae and animals is constrained by low light and food availability. The sheltered nature of the cavities, on the other hand, is likely to provide protection from predation and physical damage. These factors gain in importance in cavities which are narrow and extend deep into the reef framework, fostering the development of a specialized cavity-dwelling or coelobite’ community (Ginsburg & Schroeder 1973). There has been a considerable interest in marine underwater caves dating back to the 1950’s and 1960’s when Laborel (1958) and Riedl (1966) investigated large Mediterranean caves and already identified important factors for the composition of the sessile cave communities, namely light and water exchange. The first studies of coral reef caves and tunnels investigated by divers in Madagascar (Vasseur 1974), Grand Cayman (Logan 1981), Belize (Macintyre et al. 1982) and Bermuda (Logan et al. 1984) followed in the 1970’s and 1980’s. All of these studies were carried out in caves measuring several meters to tens of meters in length and several meters in diameter, which, although not uncommon, are by no means typical for temperate or tropical rock bottoms. Smaller-scale studies were carried out on cryptic communities living on the undersides of foliaceous corals (Buss & Jackson 1979, Jackson & Winston 1982) and in coral rubble (Choi & Ginsburg 1983, Meesters et al. 1991, Gischler & Ginsburg 1996), which are easily accessible to divers. The small cavities in the meter to decimeter range, by contrast, have been scientifically neglected, due to the lack of appropriate techniques for their study. Their ubiquitous occurrence, however, puts them in favour of being an integral, perhaps even essential element of the reef ecosystem (Ginsburg 1983, Kobluk 1988) and may hold the key to one of the enigmas which has puzzled reef scientists for decades: the depletion of phytoplankton over coral reefs (Richter 1998). Phytoplankton depletions were first observed by Glynn (1973) over a reef in the Caribbean and subsequently over reefs in other parts of the world (Legendre et al. 1988, Ayukai 1995, Fabricius & Dommisse in press) including the Red Sea (Fabricius et al. 1998, Yahel et al. 1998). Depletions occurred in spite of the small size of the phytoplankton and the apparently low cover (Yahel et a l . 1998) or total absence of epibenthic suspension feeders (Lazar, pers. com.), raising speculation on possible non-biological causes (Ayukai 1995). A ship accident set the stage for this investigation: a sailing boat with a damaged rudder had run into the fringing reef just south of the Interuniversity Institute (IUI) in Eilat, Israel, breaking up part of the reef crest. Claudio Richter (Center for Tropical Marine Ecology in Bremen, Germany) and Katharina Fabricius (Australian Institute of Marine Science in Townsville, Australia), who were guiding a student excursion to the Red Sea at that time, inspected the site and found the exposed framework riddled with cavities. Most striking was their discovery that the cavity walls were virtually carpeted with suspension feeders. Obviously, only centimeters under the rather inconspicuous outer surface of the reef the framework harboured an entirely different community. Was this coelobite community responsible for the unexplained depletions? This question became one of the central issues of Project B of the Red Sea Program for Marine Science, an Egyptian-German-Israeli-Palestinian project on pelagic-benthic coupling in coral reefs, funded by the German Ministry for Education, Science, Research and Technology (BMBF) and later part of t h e additional project between the ZMT and the Marine Science Station in Aqaba, Jordan. However, first attempts to tackle the question were frustrated by the absence of reproducible depletions. More important, however, was the lack of appropriate methodology at that time to explore and quantify the coelobite community enclosed within the coral rock: the challenge was how to obtain this crucial information without deliberately destroying the reef? The problem called for a
new tool facilitating the non-destructive exploration of this secluded habitat. The efforts resulted in the development of the CaveCam, an underwater endoscopic videosystem, which is the subject of t h e first paper (Wunsch & Richter 1998). This methodological break-through laid the foundation for the subsequent work of this cumulative dissertation. The CaveCam has proven very successful and reliable and is becoming a standard instrument for coelobite investigations, enjoying widespread attention, it is in use e.g. in the Caribbean (Bak, Scheffers, pers. com.). Interchangeable lenses, close-up and scaling accessories make it a versatile instrument for quantitatively mapping coelobite communities, but also for measuring currents in spatially confined habitats. The next challenge was to get a handle on the complex 3-dimensional morphology of the cavities to obtain first order estimates of cavity volume, wall area, roughness, etc. Based on CaveCam technology, I developed an optical method for assessing these critical parameters. The resulting LightSheet forms the basis of the second paper (Wunsch, submitted). This system allows to document cave morphology in great detail. The desired parameters are calculated from the contours of a successive series of light rings projected onto the cavity walls. The cave is then reconstructed in 3-D from the resulting sections by means of digital image analysis. With the CaveCam and LightSheet at hand the central questions could be tackled: are all cavities densely populated by coelobites? How diverse are these hidden communities and which are t h e dominant taxa? Which environmental factors govern their distribution? And finally: how significant is their share in the overall coral reef community? In order to find answers, I systematically investigated coral reef cavities in Egypt, Jordan and Israel and measured environmental factors like water exchange and light intensity and collected reference samples for taxonomic identification. After this wet part a long time of analyzing thousands of video-images with self-written software macros followed. Results were statistically tested and finally answers for most of the initial questions were found. These are presented in Chapter 3. The fourth paper analyses the role of coral reef cavities on the phytoplankton flowing across t h e reef (Richter & Wunsch 1999). Surveys were carried out on the reefs in Sinai and Eilat. They provided the first account on the subject and revealed significant depletions by coral reef cavities treated as “black boxes” (Chapter 4). The fifth paper is a synthesis of the results, linking community data to the observed depletions of phytoplankton and regeneration of nutrients in coral reef cavities. This paper derives partly from investigations carried out within the Aqaba project and the Red Sea Program, covering a variety of different locations (Chapter 5). In situ combination best proved to be the objects of themacro photography and consecutive sampling for ground-truthing of the video data and to build up a reference collection. This is the only practical way to address the organisms in the field and to convey the laboriously acquired knowledge to a wider ‘non-taxonomist’ public – be it scientific or private. This work resulted in a checklist of cryptic organisms which is featured in Chapter 6.
LITERATURE CITED Ayukai T (1995) Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs 14:141-147 Buss LW, Jackson JBC (1979) Competetive networks: nontransitive competitive relationships in cryptic coral reef environments. The American Naturalist 113:224-234 Choi DR, Ginsburg RN (1983) Distribution of coelobites (cavity-dwellers) in coral rubble across t h e Florida reef tract. Coral Reefs 2:165-172 Fabricius KE, Dommisse M (in press) Depletion of suspended pariculate matter over coastal reef communities dominated by zooxanthellate soft corals. Mar Ecol Prog Ser Fabricius KE, Yahel G, Genin A (1998) In situ depletion of phytoplankton by an azooxanthellate soft coral. Limnol Oceanogr 43:354-356