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Environmental Biology of Fishes

, Volume 87, Issue 4, pp 333–347 | Cite as

Assemblage and interaction structure of the anemonefish-anemone mutualism across the Manado region of Sulawesi, Indonesia

  • Francesco Ricciardi
  • Massimo Boyer
  • Jeff Ollerton
Article

Abstract

The Manado area (Indonesia–North Sulawesi), a marine high diversity hot-spot, hosts 7 species of anemonefish (family Pomacentridae, subfamily Amphiprioniae) living in symbiosis with 9 species of sea anemones (family Stichodactylidae and Actiniidae). This high biological diversity −27% and 80%, respectively, of the total known diversity of anemonefish and sea anemones—allows us to test different hypotheses focused on the obligate mutualism between anemonefish and sea anemones. In the Manado area, species richness of anemones and anemonefish across several sites was not correlated, but all anemones contained at least one fish individual, and there was a strong positive correlation between the numbers of individual anemonefish and anemones. As expected, each fish species had a preferred anemone host; also a partial niche overlap (Pianka’s Index) was often detected. The analysis of unique species composition suggests that competition is not an important factor determining the presence or absence of particular combinations of either anemonefish or host anemones (no evidence of competitive exclusion). The NODF algorithm showed that, at both a regional and local scale, the interaction between anemonefish and host anemones is not significantly nested, as a result of a combination of local conditions with competition, forcing species that regionally are more generalist to become more specialist.

Keywords

Coral reef fish Anemone Symbiosis Mutualism Interaction structure Nestedness Habitat use Niche differentiation Anemonefish 

Notes

Acknowledgments

We wish to acknowledge the faculty of Fisheries and Marine Sciences of the Sam Ratulangi University, Manado, and in particular Prof. Siegfried Berhimpon, for the precious cooperation in making this work possible. During data collection we have been assisted by a team of volunteers, participating to the Darwineide program, promoted by the Civic Aquarium of Milan, Italy. The experiment complied with the current laws of Indonesia and with local regulations active in Bunaken National Marine Park. The authors thank the referees and the editor for their helpful comments.

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References

  1. Allen GR (1991) Damselfish of the world. Aquarium Systems, MelleGoogle Scholar
  2. Almeida-Neto M, Guimaraes P, Guimaraes PR, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239CrossRefGoogle Scholar
  3. Arvedlund M, McCormick MI, Fautin DG, Bildsoe M (1999) Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae). Mar Ecol Prog Ser 188:207–218CrossRefGoogle Scholar
  4. Atmar W, Patterson BD (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96:373–382CrossRefGoogle Scholar
  5. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387CrossRefPubMedGoogle Scholar
  6. Bshary R (2003) The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. J Anim Ecol 72:169–176CrossRefGoogle Scholar
  7. Buston PM (2003) Size and growth modification in clownfish. Nature 24:145–146CrossRefGoogle Scholar
  8. Buston PM, Cant MA (2006) A new perspective on size hierarchies in nature: pattern, causes, and consequences. Oecologia 149:362–372CrossRefPubMedGoogle Scholar
  9. Dunn DF (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:1–115CrossRefGoogle Scholar
  10. Dupont YL, Hansen DM, Olesen JM (2003) Structure of a plant-pollinator network in the high altitude sub-alpine desert of Tenerife, Canary Islands. Ecography 26:301–310CrossRefGoogle Scholar
  11. Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:23–36CrossRefGoogle Scholar
  12. Elliott JK, Lougheed SC, Bateman B, McPhee LK, Boag PT (1999) Molecular phylogenetic evidence for the evolution of specialization in anemonefishes. Proc Roy Soc Lond B 266:677–685CrossRefGoogle Scholar
  13. Fautin DG (1991) The anemonefish symbiosis—what is known and what is not. Symbiosis 10:23–46Google Scholar
  14. Fautin DG, Allen GR (1997) Anemonefishes and their host sea anemones, Revisedth edn. Western Australian Museum, PerthGoogle Scholar
  15. Floeter SR, Vázquez DP, Grutter AS (2007) The macroecology of marine cleaning mutualisms. J Anim Ecol 76:105–111CrossRefPubMedGoogle Scholar
  16. Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902–908CrossRefGoogle Scholar
  17. Gotelli NJ, Entsminger GL (2001) EcoSim: null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. http://garyentsminger.com/ecosim.htm
  18. Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21:1512–1513CrossRefGoogle Scholar
  19. Hattori A (1995) Coexistence of 2 anemonefishes, Amphiprion clarkii and A. perideraion, which utilize the same host sea-anemone. Environ Biol Fish 42:345–353CrossRefGoogle Scholar
  20. Hattori A (2002) Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. J Anim Ecol 71:824–831CrossRefGoogle Scholar
  21. Hattori A, Yamamura N (1995) Co-exixtence of subadult males and females as alternative tectics of breeding post acquisition in a monogamous and protandrous anemonefish. Evol Ecol 9:292–303CrossRefGoogle Scholar
  22. Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24:67–73CrossRefGoogle Scholar
  23. Jang-Liaw N-H, Tang KL, Hui C-F, Shao K-T (2002) Molecular phylogeny of 48 species of damselfishes (Perciformes: Pomacentridae) using 12S mtDNAsequences. Mol Phylogenet Evol 25:445–454CrossRefPubMedGoogle Scholar
  24. Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318CrossRefPubMedGoogle Scholar
  25. Kobayashi M, Hattori A (2006) Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones. Ichthyol Res 53:1–6CrossRefGoogle Scholar
  26. Lester RJG, Sewell KB (1989) Checklist of parasites from Heron Island, Great Barrier Reef. Aust J Zool 37:101–128CrossRefGoogle Scholar
  27. MacArthur RH, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  28. Manly B, McDonald L, Thomas D (1993) Resource selection by animals. Statistical design and analysis for field studies. Chapman and Hall, LondonGoogle Scholar
  29. Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc Roy Soc Lond B 271:2605–2611CrossRefGoogle Scholar
  30. Mitchell JS, Dill LM (2005) Why is group size correlated with the size of the host sea anemone in the false clown anemonefish? Can J Zool 83:372–376CrossRefGoogle Scholar
  31. Munday PL, Buston PM, Warner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21:89–95CrossRefPubMedGoogle Scholar
  32. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world, vol. 25. Coral Reefs. Elsevier, Amsterdam, pp 75–87Google Scholar
  33. Ollerton J (2006) “Biological Barter”: patterns of specialization compared across different mutualisms. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 411–435Google Scholar
  34. Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland asclepiads in South Africa. Annals Bot 92:807–834CrossRefGoogle Scholar
  35. Ollerton J, McCollin D, Fautin DG, Allen GR (2007) Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts. Proc R Soc B 274:591–598CrossRefPubMedGoogle Scholar
  36. Parmentier E, Vandewalle P (2005) Further insight on carapid-holothuroid relationships. Mar Biol 146:455–465CrossRefGoogle Scholar
  37. Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74CrossRefGoogle Scholar
  38. Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530:513–520CrossRefGoogle Scholar
  39. Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthella content and tissue regeneration. Mar Freshw Behav Physiol 38:43–51CrossRefGoogle Scholar
  40. Randall JE, Lobel PS, Kennedy CW (2005) Comparative ecology of the gobies Nes longus and Ctenogobius saepepallens, both symbiotic with the snapping shrimp Alpheus floridanus. Environ Biol Fish 74:119–127CrossRefGoogle Scholar
  41. Richardson DL (1999) Correlates of environmental variables with patterns in the distribution and abundance of two anemonefishes (Pomacentridae: Amphiprion) on an eastern Australian sub-tropical reef system. Environ Biol Fish 55:255–263CrossRefGoogle Scholar
  42. 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 154:547–556CrossRefGoogle Scholar
  43. Sale PF, Douglas WA, Doherty PJ (1984) Choice of microhabitats by coral reef fishes at settlements. Coral Reefs 3:91–100CrossRefGoogle Scholar
  44. Santini S, Polacco G (2006) Finding Nemo: molecular phylogeny and evolution of the unusual lifestyle of anemonefish. Gene 385:19–27CrossRefPubMedGoogle Scholar
  45. Schmitt RJ, Holbrook SJ (2003) Mutualism can mediate competition and promote coexistence. Ecol Lett 6:898–902CrossRefGoogle Scholar
  46. 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 24:564–573CrossRefGoogle Scholar
  47. Srinivasan UT, Dunne JA, Harte J, Martinez ND (2007) Response of complex food webs to realistic extinction sequences. Ecology 88:671–682CrossRefPubMedGoogle Scholar
  48. Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85:74–79CrossRefGoogle Scholar
  49. Tomascik T, Mah AJ, Nontji A, Moosa MK (1997) Fringing reef of Central Indonesia. In: The ecology of Indonesian Seas. Periplus Edition, Hong KongGoogle Scholar
  50. Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant-pollinator interactions. Ecology 85:1251–1257CrossRefGoogle Scholar
  51. Vázquez DP, Chacoff NP, Cagnolo L (2009) Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90:2039–2046CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Francesco Ricciardi
    • 1
  • Massimo Boyer
    • 2
  • Jeff Ollerton
    • 3
  1. 1.Department of BiologyUniversity of PadovaPadovaItaly
  2. 2.DiSMaR. Dipartimento di Scienze del MareUniversità Politecnica delle MarcheAnconaItaly
  3. 3.Landscape and Biodiversity Research Group, School of Science and TechnologyUniversity of NorthamptonNorthamptonUK

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