Advertisement

Marine Biology

, Volume 162, Issue 12, pp 2409–2429 | Cite as

Nutritional exchange in a tropical tripartite symbiosis II: direct evidence for the transfer of nutrients from host anemone and zooxanthellae to anemonefish

  • E. Alan Verde
  • Ann Cleveland
  • Raymond W. Lee
Original Paper

Abstract

The anemone–anemonefish association is the quintessential symbol of a symbiotic mutualism from the Indo-Pacific waters. Both historical field documentation and extant scientific research advocate that these interactions are fundamental at the level of nutrient exchanges and evolutionary driving forces (natural selection) to facilitate this mutualism. Through the use of 15N and 13C stable isotope tracers, complementary laboratory- and field-based experiments were implemented in the Philippines to investigate the possibility of nutrient transmission from the host anemone, Heteractis crispa and/or endosymbiotic zooxanthellae, to two species of exosymbiotic anemonefishes (Amphiprion clarkii and A. perideraion). Mass spectrometry analyses suggest that 15N and 13C concentrations were significantly higher in tissues of the anemonefishes (intestines, liver, gills, and gonads), anemone host, and zooxanthellae compared with controls. We interpret the presence of 15N and 13C in the anemonefish tissues as direct empirical evidence for the transmission of nitrogen and/or carbon from host anemone and endosymbiotic zooxanthellae to resident anemonefish. These “translocations” and resultant recycling of elements within this classical tripartite relationship highlight the fundamental role of nutrient dynamics in this synergistic symbiosis.

Keywords

Coral Rubble Host Anemone Endosymbiotic Zooxanthella Anemonefish Species Amphiprion Clarkii 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are thankful of A. Duncanson, E. Cochrane, C. Blair, and D. Dallis for laboratory and field support and H. Calumpong and the scientific staff at Silliman University Marine Laboratory for logistical and laboratory support. This study was undertaken within the waters of Dumaguete, Philippines, and complied with all relevant local, regional, and national regulations. We thank L.R. McCloskey, N. Chadwick, and an anonymous reviewer for their time and constructive comments because it ultimately crystalized the manuscript’s arguments. Financial support was provided by the Corning School of Ocean Studies and Maine Maritime Academy.

Supplementary material

227_2015_2768_MOESM1_ESM.doc (59 kb)
Supplementary material 1 (DOC 59 kb)
227_2015_2768_MOESM2_ESM.doc (42 kb)
Supplementary material 2 (DOC 42 kb)
227_2015_2768_MOESM3_ESM.doc (76 kb)
Supplementary material 3 (DOC 76 kb)
227_2015_2768_MOESM4_ESM.doc (66 kb)
Supplementary material 4 (DOC 66 kb)
227_2015_2768_MOESM5_ESM.doc (52 kb)
Supplementary material 5 (DOC 52 kb)
227_2015_2768_MOESM6_ESM.doc (49 kb)
Supplementary material 6 (DOC 49 kb)
227_2015_2768_MOESM7_ESM.doc (48 kb)
Supplementary material 7 (DOC 48 kb)

References

  1. Agostini A, Suzuki Y, Higuchi T, Casareto BE, Nakano Y, Hidaka M, Badrun N (2009) Coral symbiotic complex: hypothesis through vitamin B12 for a new evaluation. J Coral Reef Studies 11:1–11. doi: 10.3755/galaxea.11.1 CrossRefGoogle Scholar
  2. Agostini A, Suzuki Y, Higuchi T, Casareto BE, Yoshinaga K, Nakano Y, Fujimura H (2012) Biological and chemical characteristics of the coral gastric activity. Coral Reefs 31:147–156. doi: 10.1007/s00338-011-0831-6 CrossRefGoogle Scholar
  3. Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellates association II. Mechanisms for bicarbonate uptake. J Exp Mar Biol Ecol 199:227–248. doi: 10.1016/0022-0981(95)00202-2 CrossRefGoogle Scholar
  4. Ambariyanto A, Hoegh-Guldberg O (1999) Net uptake of dissolved free amino acids by the giant clam Tridacna maxima: alternative sources of energy and nitrogen? Coral Reefs 18:91–96. doi: 10.1007/s003380050161 CrossRefGoogle Scholar
  5. Anderluh G, Sepcic K, Turk T, Macek P (2011) Cytolytic proteins from cnidarians: an overview. Acta Chim Slov 58:724–729PubMedGoogle Scholar
  6. Arnal C, Morand S (2001) Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus. Mar Biol 138:777–784. doi: 10.1007/s002270000494 CrossRefGoogle Scholar
  7. Arvedlund M, Takemura A (2005) Long-term observation in situ of the anemonefish Amphiprion clarkii (Bennett) in association with a soft coral. Coral Reefs 24:698. doi: 10.1007/s00338-005-0007-3 CrossRefGoogle Scholar
  8. Balamurugan J, Ajith Kumar TT, Kannan R, Pradeep HD (2014) Acclimation behaviour and bio-chemical changes during anemonefish (Amphiprion sebae) and sea anemone (Stichodactyla haddoni) symbiosis. Symbiosis 64:127–138. doi: 10.1007/s13199-014-0310-2 CrossRefGoogle Scholar
  9. Barneah O, Brickner I, Hooge M, Weis VM, LaJeunesse TC, Benayahu Y (2007) Three party symbiosis: acoelomorph worms, corals, and unicellular algal symbionts in Eilat (Red Sea). Mar Biol 151:1215–1223. doi: 10.1007/s00227-006-0563-2 CrossRefGoogle Scholar
  10. Benson AA, Muscatine L (1974) Wax in coral mucus: energy transfer from corals to reef fishes. Limnol Oceanogr 19:810–814. doi: 10.4319/lo.1974.19.5.0810 CrossRefGoogle Scholar
  11. Bronstein JL (2001) The costs of mutualism. Am Zool 41:825–839. doi: 10.1093/icb/41.4.825 Google Scholar
  12. Bythell JC, Wild C (2011) Biology and ecology of coral mucus release. J Exp Mar Biol Ecol 408:88–93. doi: 10.1016/j.jembe.2011.07.028 CrossRefGoogle Scholar
  13. Cleveland A (1999) Energetic costs of agonistic behavior in two herbivorous damselfishes (Stegastes). Copeia 4:857–867. doi: 10.2307/1447962 CrossRefGoogle Scholar
  14. Cleveland A, Montgomery WL (2003) Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dosopunicans and S. planifrons). Mar Biol 142:35–44. doi: 10.1007/s00227-002-0916-4 CrossRefGoogle Scholar
  15. Cleveland A, Verde EA, Lee RW (2011) Nutritional exchange in a tropical tripartite symbiosis: direct evidence for the transfer of nutrients from anemonefish to host anemone and zooxanthellae. Mar Biol 158:589–602. doi: 10.1007/s00227-010-1583-5 CrossRefGoogle Scholar
  16. Collingwood C (1868) Note on the existence of gigantic sea-anemones in the China Sea, containing within them quasi-parasitic fish. Ann Mag Nat Hist (J Nat Hist) 1:31–33. doi: 10.1080/00222936808695633 CrossRefGoogle Scholar
  17. Cook CB, Muller-Parker G, D’Elia CF (1992) Ammonium enhancement of dark carbon fixation and nitrogen limitation in symbiotic zooxanthellae: effects of feeding and starvation of the sea anemone Aiptasia pallida. Limnol Oceanogr 37:131–139. doi: 10.4319/lo.1992.37.1.0131 CrossRefGoogle Scholar
  18. Cook CB, Muller-Parker G, Orlandini CD (1994) Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanthellae symbiotic with the reef corals Madracis mirabilis and Montastrea annularis. Mar Biol 118:157–165. doi: 10.1007/BF00699230 CrossRefGoogle Scholar
  19. D’Ambra I, Graham WM, Carmichael RH, Hernandez FJ Jr (2015) Fish rely on scyphozoan hosts as a primary food source: evidence from stable isotope analysis. Mar Biol 162:247–252. doi: 10.1007/s00227-014-2569-5 CrossRefGoogle Scholar
  20. Daumas R, Galois R, Thomassin BA (1981) Biochemical composition of soft and hard coral mucus on a New Caledonian lagoonal reef. In: Proceedings of the 4th international coral reef symposium, Manila, Philippines vol 2, pp 59–67Google Scholar
  21. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol R 76:229–261. doi: 10.1128/MMBR.05014-11 CrossRefGoogle Scholar
  22. De Crespigny CC (1869) Notes on the friendship existing between the malacopterygian fish Premnas biaculeatus and the Actinia crassicornis. J Zool 37:248–249Google Scholar
  23. DeFreese DE, Clark KB (1991) Transepidermal uptake of dissolved free amino acids from seawater by three sacoglossan opisthobranchs. J Mollus Stud 57:65–74. doi: 10.1093/mollus/57.Supplement_Part_4.65 CrossRefGoogle Scholar
  24. Eibl-Eibesfeldt I (1960) Beobachtungen und Versuche an Anemonenfishchen (Amphiprion) der Malediven und der Nicobaren. Z Tierpsychol 17(1):1–10CrossRefGoogle Scholar
  25. Elliot DG (2000) Integumentary system. In: Ostrander GK (ed) The laboratory fish. Academic Press, San Diego, pp 95–108, 271–306Google Scholar
  26. Elliott J (1992) The role of sea anemones as refuges and feeding habitats for the temperate fish Oxylebius pictus. Environ Biol Fish 35:381–400. doi: 10.1007/BF00004991 CrossRefGoogle Scholar
  27. Fautin DG (1991) The anemonefish symbiosis: What is known and what is not. Symbiosis 10:23–46Google Scholar
  28. Fautin DG, Allen GR (1997) Field guide to anemonefish and their host sea anemones. Western Australian Museum, PerthGoogle Scholar
  29. Fautin DG, Guo C-C, Hwang J-S (1995) Costs and benefits of the symbiosis between the anemoneshrimp Periclimenes brevicarpalis and its host Entacmaea quadricolor. Mar Ecol Prog Ser 129:77–84. doi: 10.3354/meps129077 CrossRefGoogle Scholar
  30. Ferguson JC (1982) A comparative study of the net metabolic benefits derived from the uptake and release of free amino acids by marine invertebrates. Biol Bull 162:1–17CrossRefGoogle Scholar
  31. Fiore CL, Jarett JK, Olson NK, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18:455–463. doi: 10.1016/j.tim/2010.07.001 CrossRefGoogle Scholar
  32. Fitzgerald LM, Szmant AM (1997) Biosynthesis of ‘essential’ amino acids by scleractinian corals. Biochem J 322:213–221. doi: 10.1042/bj3220213 CrossRefGoogle Scholar
  33. Frazao B, Vasconcelos V, Antunes A (2012) Sea anemone (Cnidaria, Anthozoa, Actinaria) toxins: an overview. Mar Drugs 10:1812–1851. doi: 10.3390/md10081812 CrossRefGoogle Scholar
  34. Furla P, Benazet-Tambutte S, Jaubert J, Allemand D (1998a) Diffusional permeability of dissolved inorganic carbon through the isolated oral epithelial layers of the sea anemone, Anemonia viridis. J Exp Mar Biol Ecol 221:71–88. doi: 10.1016/S0022-0981(97)00116-0 CrossRefGoogle Scholar
  35. Furla P, Benazet-Tambutte S, Jaubert J, Allemand D (1998b) Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am J Physiol Regul Integr Comp Physiol 274:R303–R310CrossRefGoogle Scholar
  36. Furla P, Galgani I, Durand I, Allemand D (2000a) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  37. Furla P, Orsenigo MN, Allemand D (2000b) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon absorption for endosymbiotic photosynthesis. Am J Physiol Regul Integr Comp Physiol 278:R870–R881CrossRefGoogle Scholar
  38. Galetto MJ, Bellwood DR (1994) Digestion of algae by Stegastes nigricans and Amphiprion akindynos (Pisces: Pomacentridae), with an evaluation of methods used in digestability studies. J Fish Biol 44:415–428. doi: 10.1111/j.1095-8649.1994.tb01222.x CrossRefGoogle Scholar
  39. Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 1992:902–908. doi: 10.2307/1446171 CrossRefGoogle Scholar
  40. Gohar HAF (1934) Partnership between fish and anemones. Nature 134:291CrossRefGoogle Scholar
  41. Gohar HAF (1948) Commensalism between fish and anemone (with a description of the eggs of Amphiprion bicinctus Rüppell). Publs Mar Biol Stn Ghardaqa 6:35–44Google Scholar
  42. Goiran C, Shine R (2014) Reaction of a sea snake (Hydrophis major) to contact with a sea anemone. Coral Reefs 33:793. doi: 10.1007/s00338-014-1161-2 CrossRefGoogle Scholar
  43. Goiran C, Al-Moghrabi S, Allemand D, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellates association I. photosynthetic performances of symbionts and dependence on sea water bicarbonate. J Exp Mar Biol Ecol 199:207–225. doi: 10.1016/0022-0981(95)00201-4 CrossRefGoogle Scholar
  44. Goiran C, Dubey S, Shine R (2013) Effects of season, sex and body size on the feeding ecology of turtle-headed sea snake (Emydocephalus annulatus) on Indo-Pacific inshore coral reefs. Coral Reefs 32:527–538. doi: 10.1007/s00338-012-1008-7 CrossRefGoogle Scholar
  45. Goldshmid R, Holzman R, Weihs D, Genin A (2004) Aeration of corals by sleep-swimming fish. Limnol Oceangr 49(5):1832–1839. doi: 10.4319/lo.2004.49.5.1832 CrossRefGoogle Scholar
  46. Gomme J (1982) Epidermal nutrient absorption in marine invertebrates: a comparative analysis. Am Zool 22:691–708. http://www.jstor.org/stable/3882589 CrossRefGoogle Scholar
  47. Gorlick DL (1980) Ingestion of host fish surface mucus by the Hawaiian cleaning wrasse, Labroides phthirophagus (Labridae), and its effect on host species preference. Copeia 1980:863–868. doi: 10.2307/1444466 CrossRefGoogle Scholar
  48. Hattori A (2000) Social and mating systems of the protandrous anemonefish Amphiprion perideraion under the influence of a larger congener. Austral Ecol 25:187–192. doi: 10.1046/j.1442-9993.2000.01035.x CrossRefGoogle Scholar
  49. Herndl GJ, Velimirov B (1986) Role of bacteria in the gastral cavity of anthozoa. Actes de Colloques 3:407–414. http://archimer.ifremer.fr/doc/1984/acte-989.pdf
  50. Herre AWCT (1936) Some habits of Amphiprion in relation to sea anemones. Copeia 1936:167–168. doi: 10.2307/1435828 CrossRefGoogle Scholar
  51. Hill R, Scott A (2012) The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish. Coral Reefs 31:273–284. doi: 10.1007/s00338-011-0848-x CrossRefGoogle Scholar
  52. Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actinaria): benefits of hosting anemonefish. Coral Reefs 24:67–73. doi: 10.1007/s00338-004-0432-8 CrossRefGoogle Scholar
  53. Koenig O (1960) Verhaltensuntersuchungen an Anemonenenfishen. Pyramide 8(2):52–56Google Scholar
  54. Kopp C, Domart-Coulon I, Escrig S, Humbel BM, Hignette M, Meibom A (2015) Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. mBio 6(1):2–14. doi: 10.1128/mBio.02299-14 CrossRefGoogle Scholar
  55. Lesser MP, Falcon LI, Rodriguez-Roman A, Enriquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152. doi: 10.3354/meps07008 CrossRefGoogle Scholar
  56. Liberman T, Genin A, Loya Y (1995) Effects on growth and reproduction of the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus. Mar Biol 121:741–746. doi: 10.1007/BF00349310 CrossRefGoogle Scholar
  57. Madduppa HH, Juterzenka KV, Syakir M, Kochzius M (2014) Socio-economy of marine ornamental fishery and its impact on the population structure of the clown anemonefish Amphiprion ocellaris and its host anemones in Spermonde Archipelago, Indonesia. Ocean Coast Manage 100:41–50. doi: 10.1016/j.ocecoaman.2014.07.013 CrossRefGoogle Scholar
  58. Mariscal RN (1970) The nature of the symbiosis between Indo-Pacific anemone fishes and sea anemones. Mar Biol 6:58–65. doi: 10.1007/BF00352608 CrossRefGoogle Scholar
  59. Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328. doi: 10.1007/BF00942117 CrossRefGoogle Scholar
  60. McCormick MI (2003) Consumption of coral propagules after mass spawning enhances larval quality of damselfish through maternal effects. Oecologia 136:37–45. doi: 10.1007/s00442-003-1247-y CrossRefGoogle Scholar
  61. Meyer JL, Schultz ET (1985) Tissue condition and growth rate of corals associated with schooling fish. Limnol Oceanogr 30:157–166. doi: 10.4319/lo.1985.30.1.0157 CrossRefGoogle Scholar
  62. Meyer JL, Schultz ET, Helfman GS (1983) Fish schools: an asset to corals. Science 220:1047–1049. doi: 10.1126/science.220.4601.1047 CrossRefGoogle Scholar
  63. Moser J (1931) Beobachtungen über die Symbiose von Amphiprion percula mit Aktinien. Sber Ges naturf Freunde Berl 1931(2):160–167Google Scholar
  64. Moyer JT, Bell LJ (1976) Reproductive behavior of the anemonefish Amphiprion clarkii at Miyake-Jima, Japan. Jpn J Ichthyol 23:23–32Google Scholar
  65. Naumann MS, Mayr C, Struck U, Wild C (2010) Coral mucus stable isotope composition and labeling: experimental evidence for mucus uptake by epizoic acoelomorph worms. Mar Biol 157:2521–2531. doi: 10.1007/s00338-010-0612-7 CrossRefGoogle Scholar
  66. Nedosyko AM, Young JE, Edwards JW, Burke da Silva K (2014) Searching for a toxic key to unlock the mystery of anemonefish and anemone symbiosis. PLoS ONE 9:e98449. doi: 10.1371/journal.pone.0098449 CrossRefGoogle Scholar
  67. Olsen KR (2000) Circulatory System. In: Ostrander GK (ed) The laboratory fish. Academic Press, San Diego, pp 161–171CrossRefGoogle Scholar
  68. Palincsar EE, Jones WR, Palincsar JS, Glogowski MA, Mastro JL (1989) Bacterial aggregates within the epidermis of the sea anemone Aiptasia pallida. Biol Bull 177:130–140. doi: 10.2307/1541840 CrossRefGoogle Scholar
  69. Piniak GA, Lipschultz F (2004) Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals. Mar Biol 145:1085–1096. doi: 10.1007/s00227-004-1410-y CrossRefGoogle Scholar
  70. Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136. doi: 10.3354/meps262125 CrossRefGoogle Scholar
  71. Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530(531):513–520. doi: 10.1007/s10750-004-2688-y Google Scholar
  72. Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthellae content and tissue regeneration. Mar Fresh Beh Phys 38:43–51. doi: 10.1080/10236240500057929 CrossRefGoogle Scholar
  73. Pratchett MS, Gust N, Goby G, Klanten SO (2001) Consumption of coral propagules represents a significant trophic link between corals and reef fish. Coral Reefs 20:13–17. doi: 10.1007/s003380000113 CrossRefGoogle Scholar
  74. Raina J-B, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501. doi: 10.1128/AEM.02567-08 CrossRefGoogle Scholar
  75. Randall JE, Fautin DG (2002) Fishes other than anemonefishes that associate with sea anemones. Coral Reefs 21:188–190. doi: 10.1007/s00338-002-0234-9 Google Scholar
  76. Rinkevich B, Wolodarsky Z, Loya Y (1991) Coral-crab association: a compact domain of a multilevel trophic system. Hydrobiologia 216–217:279–284. doi: 10.1007/BF00026475 CrossRefGoogle Scholar
  77. Roberts JM, Davies PS, Fixter LM, Preston T (1999) Primary site and initial products of ammonium assimilation in the symbiotic sea anemone Anemonia viridis. Mar Biol 135:223–236. doi: 10.1007/s002270050620 CrossRefGoogle Scholar
  78. Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284. doi: 10.1126/science.1067728 CrossRefGoogle Scholar
  79. Robertson DR (1984) Cohabitation of competing territorial damselfishes on a Caribbean coral reef. Ecology 65:1121–1135. doi: 10.2307/1938320 CrossRefGoogle Scholar
  80. Roopin M, Chadwick NE (2009) Benefits to host sea anemones from ammonia contributions of resident anemonefish. J Exp Mar Biol Ecol 370:27–34. doi: 10.1016/j.jembe.2008.11.006 CrossRefGoogle Scholar
  81. Roopin M, Henry RP, Chadwick NE (2008) Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol 154:547–556. doi: 10.1007/s00227-008-0948-5 CrossRefGoogle Scholar
  82. Roopin M, Thornhill DJ, Santos SR, Chadwick NE (2011) Ammonia flux, physiological parameters, and Symbiodinium diversity in the anemonefish symbiosis on Red Sea coral reefs. Symbiosis 53:63–74. doi: 10.1007/s13199-011-0110-x CrossRefGoogle Scholar
  83. Ross RM (1978) Behavior of the anemonefish Amphiprion melanopus on Guam. Copeia 1:103–107. doi: 10.2307/1443829 CrossRefGoogle Scholar
  84. Schuett CS, Doepke H, Grathoff A, Gedde M (2007) Bacterial aggregates in the tentacles of the sea anemone Metridium senile. Helgoland Mar Res 61:211–216. doi: 10.1007/s10152-007-0069-4 CrossRefGoogle Scholar
  85. Scott A, Francisco B (2006) Observations on the feeding behavior of resident anemonefish during host sea anemone spawning. Coral Reefs 25:451. doi: 10.1007/s00338-006-0126-5 CrossRefGoogle Scholar
  86. Shick JM (1991) A functional biology of sea anemones. Chapman & Hall, LondonCrossRefGoogle Scholar
  87. Shuman CS, Hodgson G, Ambrose RF (2005) Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines. Coral Reefs 24:564–573. doi: 10.1007/s00338-005-0027-z CrossRefGoogle Scholar
  88. Simon-Blecher N, Chemedanov A, Eden N, Achituv Y (1999) Pit structure and trophic relationship of the coral pit crab Cryptochirus coralliodytes. Mar Biol 134:711–717. doi: 10.1007/s002270050587 CrossRefGoogle Scholar
  89. Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. WH Freeman and Co, New YorkGoogle Scholar
  90. Steele RD (1975) Stages in the life history of a symbiotic zooxanthellae in pellets extruded by its host Aiptasia tagetes (Duch. and Mich.)(Coelenterata, Anthozoa). Biol Bull 149:590–600. doi: 10.2307/1540389 CrossRefGoogle Scholar
  91. Steele RD (1976) Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae in Aiptasia tagetes (Coelenterata, Anthozoa). J Zool 179:387–405. doi: 10.1111/j.1469-7998.1976.tb02302.x CrossRefGoogle Scholar
  92. Stewart HL, Holbrook SJ, Schmitt RJ, Brooks AJ (2006) Symbiotic crabs maintain coral health by clearing sediments. Coral Reefs 25:609–615. doi: 10.1007/s00338-006-0132-7 CrossRefGoogle Scholar
  93. Szczebak JT, Henry RP, Al-Horani FA, Chadwick NE (2013) Anemonefish oxygenate their anemone hosts at night. J Exp Biol 216:970–976. doi: 10.1242/jeb.075648 CrossRefGoogle Scholar
  94. Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pages C (2012) Autotrophic carbon in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393. doi: 10.1242/jeb.065201 CrossRefGoogle Scholar
  95. Valdivia N, Stotz W (2006) Feeding behavior of the porcellanid crab Allopetrolisthes spinifrons, symbiont of the sea anemone Phymactis papillosa. J Crustacean Biol 26:308–315. doi: 10.1651/C-2607.1 CrossRefGoogle Scholar
  96. Verwey J (1930) Coral reef studies I. The symbiosis between damselfishes and sea anemones in Batavia Bay. Treubia 12:305–366Google Scholar
  97. Weis VM (1991) The induction of carbonic anhydrase in symbiotic sea anemone Aiptasia pulchella. Biol Bull 180:496–504. doi: 10.2307/1542351 CrossRefGoogle Scholar
  98. Weis VM (1993) Effect of dissolved inorganic carbon concentration on the photosynthesis of the symbiotic sea anemone Aiptasia pulchella Carlgren: role of carbonic anhydrase. J Exp Mar Biol Ecol 174:209–225. doi: 10.1016/0022-0981(93)90018-J CrossRefGoogle Scholar
  99. Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202. doi: 10.1007/BF00391958 CrossRefGoogle Scholar
  100. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376. doi: 10.1016/j.tree.2004.03.004 CrossRefGoogle Scholar
  101. Whitehead LF, Douglas AE (2003) Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to animal host. J Exp Biol 206:3149–3157. doi: 10.1242/jeb.00539 CrossRefGoogle Scholar
  102. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70. doi: 10.1038/nature02344 CrossRefGoogle Scholar
  103. Zar JH (2009) Biostatitical Analysis, 5th edn. Pearson, LondonGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Corning School of Ocean StudiesMaine Maritime AcademyCastineUSA
  2. 2.School of Biological SciencesWashington State UniversityPullmanUSA

Personalised recommendations