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Genetic tools link long-term demographic and life-history traits of anemonefish to their anemone hosts

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Abstract

The life-history traits and population dynamics of species are increasingly being attributed to the characteristics of their preferred habitats. While coral reef fish are often strongly associated with particular habitats, long-term studies establishing the demographic and life-history consequences of occupying different reef substrata are rare and no studies have monitored individuals in situ over their lifetime and determined the fate of their offspring. Here, we documented a quasi-turnover and local reproductive success for an entire population of orange clownfish (Amphiprion percula) from Kimbe Island, Papua New Guinea, by taking bi-annual samples of DNA over a 10-yr period (2003–2013). We compared demographic and life-history traits of individuals living on two host anemone species, Heteractis magnifica and Stichodactyla gigantea, including female size, adult continued presence (a proxy for relative longevity range), early post-settlement growth, the number of eggs per clutch and ‘local’ reproductive success (defined for each adult as the number of offspring returning to the natal population). Our results indicate that while the relative longevity of adults was similar on both host anemone species, females living in H. magnifica were larger than females in S. gigantea. However, despite females growing larger and producing more eggs on H. magnifica, we found that local reproductive success was significantly higher for clownfish living in S. gigantea. Life-history traits also exhibited local spatial variation, with higher local reproductive success recorded for adults living on S. gigantea on the eastern side of the island. Our findings support a ‘silver-spoon’ hypothesis that predicts individuals that are fortunate enough to recruit into good habitat and location will be rewarded with higher long-term reproductive success and will make a disproportionate contribution to population renewal.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with Image. J Biophotonics International 11:36–42

    Google Scholar 

  • Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744

    Article  CAS  PubMed  Google Scholar 

  • Almany GR, Hamilton RJ, Bode M, Matawai M, Potuku T, Saenz-Agudelo P, Planes S, Berumen ML, Rhodes KL, Thorrold SR, Russ GR, Jones GP (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23:626–630

    Article  CAS  PubMed  Google Scholar 

  • Arvedlund M, Bundgaard I, Nielsen LE (2000) Host imprinting in anemonefishes (Pisces : Pomacentridae): Does it dictate spawning site preferences? Environ Biol Fishes 58:203–213

    Article  Google Scholar 

  • Ates RML (1989) Fishes that eat sea anemones, a review. J Nat Hist 23:71–79

    Article  Google Scholar 

  • Begon M, Harper JL, Townsend CR (1996) Ecology: individuals, populations and communities. Blackwell Science, Oxford

    Book  Google Scholar 

  • Beldade R, Holbrook SJ, Schmitt RJ, Planes S, Malone D, Bernardi G (2012) Larger female fish contribute disproportionately more to self-replenishment. Proc R Soc Lond B Biol Sci 279:2116–2121

    Article  CAS  Google Scholar 

  • Berumen ML, Walsh HJ, Raventos N, Planes S, Jones GP, Starczak V, Thorrold SR (2010) Otolith geochemistry does not reflect dispersal history of clownfish larvae. Coral Reefs 29:883–891

    Article  Google Scholar 

  • Bonsall MB, Mangel M (2004) Life-history trade-offs and ecological dynamics in the evolution of longevity. Proc R Soc Lond B Biol Sci 271:1143–1150

    Article  Google Scholar 

  • Buston P (2003a) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582

    Article  Google Scholar 

  • Buston P (2003b) Social hierarchies: size and growth modification in clownfish. Nature 424:145–146

    Article  CAS  PubMed  Google Scholar 

  • Buston PM, Elith J (2011) Determinants of reproductive success in dominant pairs of clownfish: a boosted regression tree analysis. J Anim Ecol 80:528–538

    Article  PubMed  Google Scholar 

  • Chapman MR, Kramer DL (2000) Movements of fishes within and among fringing coral reefs in barbados. Environ Biol Fishes 57:11–24

    Article  Google Scholar 

  • Cockburn A (1991) An introduction to evolutionary ecology. Blackwell Scientific Publications, London

    Google Scholar 

  • De Boeck P, Bakkar M, Zwitser R, Nivard M, Hofman A, Tuerlinckx F, Partchev I (2011) The estimation of item response models with the lmer function from the lme4 package in R. J Stat Softw 39:1–28

    Article  Google Scholar 

  • Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Thorrold SR (2014) Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish. Oecologia 174:99–107

    Article  PubMed  Google Scholar 

  • Dunn DF (1981) The clownfish sea-anemones - stichodactylidae (coelenterata, actiniaria) and other sea-anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:3–113

    Article  Google Scholar 

  • Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:23–36

    Article  Google Scholar 

  • Fautin DG (1988) Sea anemones (Actiniaria and corallimorpharia) of Madang province. Science in New Guinea 14:22–29

    Google Scholar 

  • Fautin DG, Allen GR (1997) Anemonefishes and their host sea anemones: a guide for aquarists and divers. Western Australian Museum

  • Fricke HW (1979) Mating system, resource defense ans sex change in the anemonefish Amphiprion akallopisos. Z Tierphysiol Tierer 50:313–326

    Google Scholar 

  • Gerber S, Chabrier P, Kremer A (2003) FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol Ecol N 3:479–481

    Article  CAS  Google Scholar 

  • Gibson RN (1994) Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth J Sea Re 32:191–206

    Article  Google Scholar 

  • Ginestet C (2011) ggplot2: Elegant graphics for data analysis. J R Stat Soc Ser A Stat Soc 174:245–246. doi:10.1111/j.1467-985X.2010.00676_9.x

    Article  Google Scholar 

  • Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902–908

    Article  Google Scholar 

  • Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 454–471

    Google Scholar 

  • Green BS (2008) Maternal effects in fish populations. Adv Mar Biol 54:1–105

    Article  PubMed  Google Scholar 

  • Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24:67–73

    Article  Google Scholar 

  • Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318

    Article  CAS  PubMed  Google Scholar 

  • Malloy KD, Targett TE (1991) Feeding, growth and survival of juvenile summer flounder paralichthys-dentatus - experimental-analysis of the effects of temperature and salinity. Mar Ecol Prog Ser 72:213–223

    Article  Google Scholar 

  • McMahon KW, Berumen ML, Thorrold SR (2012) Linking habitat mosaics and connectivity in a coral reef seascape. Proc Natl Acad Sci USA 109:15372–15376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell JS (2003) Mobility of Stichodactyla gigantea sea anemones and implications for resident false clown anemonefish, Amphiprion ocellaris. Environ Biol Fishes 66:85–90

    Article  Google Scholar 

  • Nedosyko AM, Young JE, Edwards JW, da Silva KB (2014) Searching for a toxic key to unlock the mystery of anemonefish and anemone symbiosis. PLoS One 9:970–976

    Article  CAS  Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83

    Article  CAS  PubMed  Google Scholar 

  • Palsboll PJ (1999) Genetic tagging: contemporary molecular ecology. Biol J Linn Soc 68:3–22

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Raventos N, Macpherson E (2001) Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Mar Biol 138:1115–1120

    Article  Google Scholar 

  • Ross RM (1978) Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Z Tierpsychol 36:71–83

    Google Scholar 

  • Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2009) Estimating connectivity in marine populations: an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios. Mol Ecol 18:1765–1776

    Article  CAS  PubMed  Google Scholar 

  • Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2015) Mothers matter: contribution to local replenishment is linked to female size, mate replacement and fecundity in a fish metapopulation. Mar Biol 162:3–14

    Article  Google Scholar 

  • Salles OC, Maynard JA, Joannides M, Barbu CM, Saenz-Agudelo P, Almany GR, Berumen ML, Thorrold SR, Jones GP, Planes S (2015) Coral reef fish populations can persist without immigration. Proc R Soc Lond B Biol Sci 282:20151311

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford 249

    Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  • van de Pol M, Bruinzeel LW, Heg D, van der Jeugd HP, Verhulst S (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J Anim Ecol 75:616–626

    Article  PubMed  Google Scholar 

  • van de Pol M, Wright J (2009) A simple method for distinguishing within- versus between- subject effects using mixed models. Anim Behav 77:753–758

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by LABEX Corail, ERC, CRISP, the GEF CRTR Connectivity Working Group, NSF, the ARC Centre of Excellence for Coral Reef Studies, TNC, Total Foundation, JCU, KAUST, and WHOI. We thank the ‘clownfish team’ that assisted in the field. N. Tolou and S. Baksay assisted with genetic analysis. Mahonia and FeBrina provided essential logistic support. We are grateful to the traditional owners of the reefs near Kimbe Island for allowing us access to their reefs. Finally, we thank J. Almany and the two anonymous reviewers for their many insightful comments and their contributions to the final draft.

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Authors and Affiliations

  1. EPHE, PSL Research University, UPVD-CNRS, USR3278 CRIOBE, 66360, Perpignan, France

    Océane C. Salles, Glenn R. Almany & Serge Planes

  2. Laboratoire d’Excellence ‘CORAIL’, Perpignan, France

    Océane C. Salles, Glenn R. Almany & Serge Planes

  3. Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile

    Pablo Saenz-Agudelo

  4. Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955, Saudi Arabia

    Michael L. Berumen

  5. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    Simon R. Thorrold

  6. ARC Centre of Excellence for Coral Reef Studies, and College of Science and Engineering, James Cook University, Townsville, QLD, 4811, Australia

    Geoffrey P. Jones

Authors
  1. Océane C. Salles
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  2. Pablo Saenz-Agudelo
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  3. Glenn R. Almany
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  4. Michael L. Berumen
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  5. Simon R. Thorrold
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  6. Geoffrey P. Jones
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  7. Serge Planes
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Corresponding author

Correspondence to Océane C. Salles.

Additional information

Communicated by Ecology Editor Dr. Alastair Harborne

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Salles, O.C., Saenz-Agudelo, P., Almany, G.R. et al. Genetic tools link long-term demographic and life-history traits of anemonefish to their anemone hosts. Coral Reefs 35, 1127–1138 (2016). https://doi.org/10.1007/s00338-016-1485-1

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  • DOI: https://doi.org/10.1007/s00338-016-1485-1

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