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From cooperation to combat: adverse effect of thermal stress in a symbiotic coral-crustacean community

  • Behavioral ecology - Original research
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Abstract

Although mutualisms are ubiquitous in nature, our understanding of the potential impacts of climate change on these important ecological interactions is deficient. Here, we report on a thermal stress-related shift from cooperation to antagonism between members of a mutualistic coral-dwelling community. Increased mortality of coral-defending crustacean symbionts Trapezia cymodoce (coral crab) and Alpheus lottini (snapping shrimp) was observed in response to experimentally elevated temperatures and reduced coral-host (Pocillopora damicornis) condition. However, strong differential numerical effects occurred among crustaceans as a function of species and sex, with shrimp (75 %), and female crabs (55 %), exhibiting the fastest and greatest declines in numbers. These declines were due to forceful eviction from the coral-host by male crabs. Furthermore, surviving female crabs were impacted by a dramatic decline (85 %) in egg production, which could have deleterious consequences for population sustainability. Our results suggest that elevated temperature switches the fundamental nature of this interaction from cooperation to competition, leading to asymmetrical effects on species and/or sexes. Our study illustrates the importance of evaluating not only individual responses to climate change, but also potentially fragile interactions within and among susceptible species.

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References

  • Abele LG (1976) Comparative species richness in fluctuating and constant environments—coral-associated decapod crustaceans. Science 192:461–463

    Article  CAS  PubMed  Google Scholar 

  • Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593

    Article  Google Scholar 

  • Bascompte J, Stouffer DB (2009) The assembly and disassembly of ecological networks. Philos Trans R Soc B-Biol Sci 364:1781–1787

    Article  Google Scholar 

  • Bonin MC, Srinivasan M, Almany GR, Jones GP (2009) Interactive effects of interspecific competition and microhabitat on early post-settlement survival in a coral reef fish. Coral Reefs 28:265–274

    Article  Google Scholar 

  • Brawley SH, Adey WH (1982) Coralliophila abbreviata: a significant corallivore! Bull Mar Sci 32:595–599

    Google Scholar 

  • Briand F, Yodzis P (1982) The phylogenetic distribution of obligate mutualism—evidence of limiting similarity and global instability. Oikos 39:273–275

    Article  Google Scholar 

  • Briffa M, Dallaway D (2007) Inter-sexual contests in the hermit crab Pagurus bernhardus: females fight harder but males win more encounters. Behav Ecol Sociobiol 61:1781–1787

    Article  Google Scholar 

  • Bronstein J, Dieckmann U, Ferrière R (2004) Coevolutionary dynamics and the conservation of mutualisms. In: Ferrière R, Dieckmann U, Couvet D (eds) Evolutionary conservation biology. Cambridge University Press, Cambridge, pp 305–325

    Chapter  Google Scholar 

  • Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309

    Article  CAS  Google Scholar 

  • Castro P (1976) Brachyuran crabs symbiotic with scleractinian corals: a review of their biology. Micronesica 12:99–110

    Google Scholar 

  • Castro P (1978) Movements between coral colonies in Trapezia ferruginea (Crustacea Brachyura), an obligate symbiont of scleractinian corals. Mar Biol 46:237–245

    Article  Google Scholar 

  • Castro P (1988) Animal symbioses in coral-reef communities—a review. Symbiosis 5:161–184

    Google Scholar 

  • Connell JH (1961) Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecol Monogr 31:61–104

    Article  Google Scholar 

  • Elton CS (1927) Animal ecology. The University of Chicago Press, Chicago (Reprint)

    Google Scholar 

  • Feary DA, McCormick MI, Jones GP (2009) Growth of reef fishes in response to live coral cover. J Exp Mar Biol Ecol 373:45–49

    Article  Google Scholar 

  • Fukami T (2001) Sequence effects of disturbance on community structure. Oikos 92:215–224

    Article  Google Scholar 

  • Glynn PW (1976) Some physical and biological determinants of coral community structure in the Eastern Pacific. Ecol Monogr 46:431–456

    Article  Google Scholar 

  • Glynn PW (1980) Defense by symbiotic Crustacea of host corals elicited by chemical cues from predators. Oecologia 47:287–290

    Article  Google Scholar 

  • Glynn PW (1983a) Crustacean symbionts and the defense of corals: co-evolution on the reef? University of Chicago Press, Chicago

    Google Scholar 

  • Glynn PW (1983b) Increased survivorship in corals harboring crustacean symbionts. Mar Biol Lett 4:105–111

    Google Scholar 

  • Glynn PW (1991) Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol Evol 6:175–179

    Article  CAS  PubMed  Google Scholar 

  • Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191

    Article  Google Scholar 

  • Glynn PW, Perez M, Gilchrist SL (1985) Lipid decline in stressed corals and their crustacean symbionts. Biol Bull 168:276–284

    Article  CAS  Google Scholar 

  • Harley CDG, et al. (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241

    Article  PubMed  Google Scholar 

  • Huber ME (1987) Aggressive behavior of Trapezia intermedia Miers and Trapezia digitalis Latreille (Brachyura, Xanthidae). J Crustac Biol 7:238–248

    Article  Google Scholar 

  • Huber ME, Coles SL (1986) Resource utilization and competition among the 5 Hawaiian species of Trapezia (Crustacea, Brachyura). Mar Ecol Prog Ser 30:21–31

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2000) Supply-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249

    Article  Google Scholar 

  • Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Hyatt GW, Salmon M (1978) Combat in the fiddler crabs Uca pugilator and U. pugnax: a qualitative analysis. Behaviour 65:182–211

    Article  Google Scholar 

  • Ives AR (1995) Predicting the response of populations to environmental-change. Ecology 76:926–941

    Article  Google Scholar 

  • Ives AR, Gilchrist G (1993) Climate change and ecological interactions. In: Kareiva P, Kingsolver J, Huey R (eds) Biotic interactions and global change. Sinauer, Sunderland, pp 120–146

    Google Scholar 

  • Karplus I (1987) The association between gobiid fishes and burrowing alpheid shrimps. Oceanogr Mar Biol Annu Rev 25:507–562

    Google Scholar 

  • Kiers E, Palmer T, Ives A, Bruno J, Bronstein J (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474

    Article  Google Scholar 

  • Knudsen JW (1967) Trapezia and Tetralia (Decapoda, Brachyura, Xanthidae) as obligate ectoparasites of pocilloporid and acroporid corals. Pac Sci 21:51–57

    Google Scholar 

  • LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc R Soc B-Biol Sci 276:4139–4148

    Article  Google Scholar 

  • Lassig BR (1977) Communication and coexistence in a coral community. Mar Biol 42:85–92

    Article  Google Scholar 

  • Lough JM (1999) Sea surface temperatures along the Great Barrier Reef: a contribution to the study of coral bleaching. Great Barrier Reef Marine Park Authority research report no. 57. Great Barrier Reef Marine Park Authority, Townsville

  • Lough JM (2007) Climate and climate change on the Great Barrier Reef. In: Johnson JE, Marshall PA (ed) Climate change and the Great Barrier Reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority, Townsville, pp 15–50

  • Lubchenco J, et al. (1991) The sustainable biosphere initiative: an ecological research agenda: a report from the Ecological Society of America. Ecology 72:371–412

    Article  Google Scholar 

  • Marin IN, Anker A, Britayev TA, Palmer AR (2005) Symbiosis between the alpheid ahrimp, Athanas ornithorhynchus Banner and Banner, 1973 (Crustacea: Decapoda), and the brittle star, Macrophiothrix longipeda (Lamarck, 1816) (Echinodermata: Ophiuroidea). Zool Stud 44:234–241

    Google Scholar 

  • Marvier M, Kareiva P, Neubert MG (2004) Habitat destruction, fragmentation, and disturbance promote invasion by habitat generalists in a multispecies metapopulation. Risk Anal 24:869–878

    Article  PubMed  Google Scholar 

  • May RM (1976) Models for two interacting populations. In: May RM (ed) Theoretical ecology: principles and applications. Saunders, Philadelphia, pp 47–71

    Google Scholar 

  • Maynard-Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • McKeon CS, Stier AC, McIlroy SE, Bolker BM (2012) Multiple defender effects: synergistic coral defense by mutualist crustaceans. Oecologia 169:1095–1103

    Article  PubMed  Google Scholar 

  • Miller TJ, Crowder LB, Rice JA, Marschall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45:1657–1670

    Article  Google Scholar 

  • Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442:259–264

    Article  CAS  PubMed  Google Scholar 

  • Munday PL, Leis JM, Lough JM, Paris CB, Kingsford MJ, Berumen ML, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395

    Article  Google Scholar 

  • Norman CP, Jones MB (1993) Reproductive ecology of the velvet swimming crab, Necora puber (Brachyura: Portunidae), at Plymouth. J Mar Biol Assoc UK 73:379–389

    Article  Google Scholar 

  • Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320

    Article  Google Scholar 

  • Parker GA (1974) Assessment strategy and evolution of fighting behavior. J Theor Biol 47:223–243

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Patton WK (1974) Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In: Vernberg WB (ed) Symbiosis in the sea. University of South Carolina Press, Columbia, pp 219–243

    Google Scholar 

  • Pollock FJ, Katz SM, Bourne DG, Willis BL (2012) Cymo melanodactylus crabs slow progression of white syndrome lesions on corals. Coral Reefs 32:43–48

    Google Scholar 

  • Pratchett MS (2001) Influence of coral symbionts on feeding preferences of crown-of-thorns starfish Acanthaster planci in the western Pacific. Mar Ecol Prog Ser 214:111–119

    Article  Google Scholar 

  • Rausher MD, Fowler NL (1979) Intersexual aggression and nectar defense in Chauliognathus distinguendus (Coleoptera, Cantharidae). Biotropica 11:96–100

    Article  Google Scholar 

  • Robertson R (1970) Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pacif Sci 24:43–54

    Google Scholar 

  • Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592

    Article  PubMed  Google Scholar 

  • Siebeck UE, Marshall NJ, Kluter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

    Article  Google Scholar 

  • Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246

    Article  Google Scholar 

  • Stella JS (2012) Evidence of corallivory by the keyhole limpet Diodora galeata. Coral Reefs 31:579

    Google Scholar 

  • Stella JS, Jones GP, Pratchett MS (2010) Variation in the structure of epifaunal invertebrate assemblages among coral hosts. Coral Reefs 29:957–973

    Article  Google Scholar 

  • Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011a) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol Annu Rev 49:43–116

    Google Scholar 

  • Stella JS, Munday PL, Jones GP (2011b) Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce. Coral Reefs 30:719–727

    Article  Google Scholar 

  • Stewart HL, Holbrook SJ, Schmitt RJ, Brooks AJ (2006) Symbiotic crabs maintain coral health by clearing sediments. Coral Reefs 25:609–615

    Article  Google Scholar 

  • Stier AC, McKeon CS, Osenberg CW, Shima JS (2010) Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs 29:1019–1022

    Article  Google Scholar 

  • Stimson J (1990) Stimulation of fat-body production in the polyps of the coral Pocillopora damicornis by the presence of mutualistic crabs of the genus Trapezia. Mar Biol 106:211–218

    Article  Google Scholar 

  • Taylor HH, Leelapiyanart N (2001) Oxygen uptake by embryos and ovigerous females of two intertidal crabs, Heterozius rotundifrons (Belliidae) and Cyclograpsus lavauxi (Grapsidae): scaling and the metabolic costs of development. J Exp Biol 204:1083–1097

    CAS  PubMed  Google Scholar 

  • Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Townsend Peterson A, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

    Article  CAS  PubMed  Google Scholar 

  • Trench RK (1979) The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 30:485–531

    Article  CAS  Google Scholar 

  • Tsuchiya M (1999) Effect of mass coral bleaching on the community structure of small animals associated with the hermatypic coral Pocillopora damicornis. Galaxea. JCRS 1:65–72

    Article  Google Scholar 

  • Tsuchiya M, Yonaha C (1992) Community organization of associates of the coral Pocillopora damicornis: effects of colony size and interactions among the obligate symbionts. Galaxea 11:29–56

    Google Scholar 

  • Tsuchiya M, Nakamura H, Nishihira M, Licuanan W, Yonaha C, Wang Z, Zhu D (1989) Effect of suspended particles on the community structure of small animals associated with the hermatypic coral Pocillopora damicornis and some population traits of its obligate symbionts in Okinawa, Japan. Galaxea 8:159–177

    Google Scholar 

  • Tsuchiya M, Yamauchi Y, Moretzsohn F, Tsukiji M (1992) Species composition and some population traits of obligate symbiotic xanthid crabs, Trapezia and Tetralia, associated with bleached corals. Proc 10th Intl Coral Reef Symp 1:56–63

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • Vannini M (1985) A shrimp that speaks crab-ese. J Crustac Biol 5:160–167

    Article  Google Scholar 

  • Walther GR (2010) Community and ecosystem responses to recent climate change. Philos Trans R Soc B-Biol Sci 365:2019–2024

    Article  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17:R661–R672

    Article  CAS  PubMed  Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Williams ST, Knowlton N (2001) Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Mol Biol Evol 18:1484–1493

    Article  CAS  PubMed  Google Scholar 

  • Wootton JT (1994) Predicting direct and indirect effects—an integrated approach using experiments and path-analysis. Ecology 75:151–165

    Article  Google Scholar 

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Acknowledgments

We thank the Yugilbar Foundation and Lizard Island Research Station—A facility of the Australian Museum and the Great Barrier Reef Marine Park Authority Science for Management Award for funding this study; Lyle Vail and Anne Hoggett for generosity of time lent to assist with logistics; Fernanda de Faria, Ben Gordon, Tom Bridge, Daniel Twikler and Tanya Lamb for invaluable field assistance and anonymous reviewers for their valuable comments. This study was also financially supported by the ARC Centre of Excellence for Coral Reef Studies. This research was conducted under animal ethics approval from James Cook University and a research permit from the Great Barrier Reef Marine Park Authority.

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  1. School of Marine and Tropical Biology, James Cook University, Townsville, QLD, 4811, Australia

    J. S. Stella, P. L. Munday & G. P. Jones

  2. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia

    J. S. Stella, P. L. Munday, S. P. W. Walker, M. S. Pratchett & G. P. Jones

  3. Climate Adaptation Flagship, CSIRO, Hobart, TAS, 7001, Australia

    J. S. Stella

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  1. J. S. Stella
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Correspondence to J. S. Stella.

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Communicated by Geoffrey C Trussell.

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Stella, J.S., Munday, P.L., Walker, S.P.W. et al. From cooperation to combat: adverse effect of thermal stress in a symbiotic coral-crustacean community. Oecologia 174, 1187–1195 (2014). https://doi.org/10.1007/s00442-013-2858-6

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