Coral Reefs

pp 1–8 | Cite as

Influence of prior residents on settlement preferences in the anemonefish, Premnas biaculeatus

Report

Abstract

Settlement preferences play a critical role in the successful transition from pelagic larvae to benthic juveniles for many coral reef organisms. Reef fish larvae are capable of recognizing and behaviorally responding to a variety of sensory cues when assessing settlement site locations. The presence of resident conspecifics for site attached coral reef fishes could indicate a quality location, but may result in negative interactions through aggression from already-established individuals. For anemonefishes, where space on a sea anemone is limited and breeding is restricted to one adult pair, settlement preferences may depend on the number and sex of the occupants. Here we undertook both aquarium-based olfactory trials and a field experiment to determine the role resident anemonefish individuals have on sea anemone site selection in the spine cheek anemonefish, Premnas biaculeatus. We show larvae are able to identify the occupant saturation state and sex of the resident occupants based on chemical cues alone, with larvae preferring the chemical cues produced by a single male to a single female, the single fish to an empty sea anemone, and an empty sea anemone to a sea anemone containing an adult pair. These behavioral preferences were reflected in the settlement preferences of larvae when assessed in the natural environment. We hypothesize that the ability of resident fish to evict incoming larvae combined with the selective pressure on larvae to locate an ideal habitat has resulted in the larval ability to accurately identify habitat where settlement and future breeding opportunities are most likely achieved.

Keywords

Recruitment Settlement site selection Premnas biaculeatus Larvae Olfaction Sea anemone saturation state 

Notes

Acknowledgements

Special thanks to BM Devine for assistance with field work, the staff at Mahonia na Dari Research Station for field support and the staff at James Cook University’s Aquarium Facility for logistical support. This research was funded by the American Australian Association and the Alfred P. Sloan Foundation. This research was conducted under ethics approval number A1477 and followed all guidelines for the country in which it took place. Datasets used in this study are available online from the Zenodo repository.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. Arvedlund M, Nielsen LE (1996) Do the anemonfish Amphiprion ocellaris (Pisces: Pomacentridae) imprint themselves to their host sea anemone Heteractis magnifica (Anthozoa: Actinidae)? Ethology 102:197–211CrossRefGoogle Scholar
  2. 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
  3. Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160CrossRefGoogle Scholar
  4. Allen GR (1972) The anemonefishes: their classification and biology. TFH Publ Inc., Neptune CityGoogle Scholar
  5. Bay LK, Jones GP, McComrick MI (2001) Habitat selection and aggression as determinants of spatial segregation among damselfish on a coral reef. Coral Reefs 20:289–298CrossRefGoogle Scholar
  6. Ben-Tzvi O, Tchernov D, Kiflawi M (2010) Role of coral derived chemical cues in microhabitat selection by settling Chromis viridis. Mar Ecol Prog Ser 409:181–187CrossRefGoogle Scholar
  7. Bonin MC, Srinivasan M, Almany GR, Jones GR (2009) Interactive effects of interspecific competition and microhabitat on early post-settlement survival in a coral reef fish. Coral Reefs 28:265–274CrossRefGoogle Scholar
  8. Booth DJ (1992) Larval settlement patterns and preferences by domino damselfish, Dascyllus albisella Gill. J Exp Mar Biol Ecol 155:85–104CrossRefGoogle Scholar
  9. Booth DJ (1995) Juvenile groups in a coral-reef damselfish: density-dependent effects on individual fitness and population demography. Ecology 76:91–106CrossRefGoogle Scholar
  10. Buston P (2002a) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582CrossRefGoogle Scholar
  11. Buston PM (2002b) Group structure of the clown anemonefish Amphiprion percula (PhD dissertation. Cornell University, Ithaca, NYGoogle Scholar
  12. Buston PM (2003) Mortality is associated with social rank in the clown anemonefish (Amphiprion percula). Mar Biol 143:811–815CrossRefGoogle Scholar
  13. Buston PM, Elith J (2011) Determinants of reproductive success in dominant pairs of clownfish: a boosted regression tree analysis. J Animal Ecol 80:528–538CrossRefGoogle Scholar
  14. Coker DJ, Pratchett MS, Munday PL (2012) Influence of coral bleaching, coral mortality and conspecific aggression on movement and distribution of coral-dwelling fish. J Exp Mar Biol Ecol 414–415:62–68CrossRefGoogle Scholar
  15. Dixson DL, Abrego D, Hay ME (2014a) Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892–897CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Thorrold SR (2014b) Experimental evaluation of imprinting and the role innate preferences plays in habitat selection in a coral reef fish. Oecologia 174:99–107CrossRefPubMedGoogle Scholar
  17. Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Srinivasan M, Syms C, Thorrold SR (2008) Coral reef fish smell leaves to find island homes. Proc R Soc B 275:2831–2839CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75CrossRefPubMedGoogle Scholar
  19. Dixson et al (2012) Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species. Anim Behav 84:45–51CrossRefGoogle Scholar
  20. Døving KB, Stabell OB, Östlund-Nilsson S, Fisher R (2006) Fidelity and homing in tropical coral reef cardinalfish: are they using olfactory cues? Chem Senses 31:265–272CrossRefPubMedGoogle Scholar
  21. Dunn DF (1981) The clownfish sea anemones. Trans Am Philos Soc 71:1–115CrossRefGoogle Scholar
  22. Elliott JK, Elliott JM, Mariscal RN (1995) Host selection, location and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377–389CrossRefGoogle Scholar
  23. Fautin DG (1985) Competition by anemone fishes for host actinians. In: Proceedings of 5th internal coral reef congress, vol 5, pp 373–377Google Scholar
  24. Fautin DG (1986) Why do anemonefishes inhabit only some host actinians? Environ Biol Fish 15:171–180CrossRefGoogle Scholar
  25. Fautin DG, Allen GR (1992) Field guild to anemonefishes and their host sea anemones. Western Australian Museum Publ, PerthGoogle Scholar
  26. Fishelson L (1998) Behavior, socio-ecology and sexuality in damselfishes (Pomacentridae) Ital. J Zool Suppl 67:387–398Google Scholar
  27. Fricke H, Fricke S (1977) monogamy and sex change by aggressive dominance in coral reef fish. Nature 266:830–832CrossRefPubMedGoogle Scholar
  28. Fricke HW (1979) Mating system, resource defense and sex change in the anemonefish Amphiprion akallopisos. Z Tierpsychol 50:313–326CrossRefGoogle Scholar
  29. Gardiner NM, Jones GP (2005) Habitat specialization and overlap in a guild of coral reef cardinalfishes (Apogonidae). Mar Ecol Prog Ser 305:163–175CrossRefGoogle Scholar
  30. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hattori A (1994) Inter-group moment and mate acquisition tactics of the protandrous anemonefish, Amphiprion clarkii, on a coral reef, Okinawa Jpn. J Ichthyol 41:159–165Google Scholar
  32. Hattori A (1995) Coexistence of two anemonefishes, Amphiprion clarkii and Amphiprion perideraion which utilize the same host sea anemone. Environ Biol Fish 42:345–353CrossRefGoogle Scholar
  33. Johnston NK, Dixson DL (2017) Anemonefishes rely on visual and chemical cues to correctly identify conspecifics. Coral Reefs 36:903–912.  https://doi.org/10.1007/s00338-017-1582-9 CrossRefGoogle Scholar
  34. Kingsford MJ, Leis J, Shanks A, Lindeman K, Morgan S, Pineda J (2002) Sensory environments, larval abilities and local self recruitment. Bull Mar Sci 70:309–340Google Scholar
  35. Lecchini D, Planes S, Galzin R (2005a) Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav Ecol Sociobiol 58:18–26CrossRefGoogle Scholar
  36. Lecchini D, Shima J, Banaigs B, Galzin R (2005b) Larval sensory abilities and mechanisms of habiat selection of a coral reef fish during settlement. Oecologia 143:326–334CrossRefPubMedGoogle Scholar
  37. Lecchini D, Osenberg CW, Shima JS, St Mary CM, Galzin R (2007) Ontogenetic changes in habitat selection during settlement in a coral reef fish: ecological determinants and sensory mechanisms. Coral Reefs 26:423–432CrossRefGoogle Scholar
  38. Leis JM (1991) The pelagic stages of reef fishes: the larval biology of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, CA, pp 183–230CrossRefGoogle Scholar
  39. Leis JM, Siebeck U, Dixson DL (2011) How nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integra Comp Biol 51:826–843CrossRefGoogle Scholar
  40. Munday PL, Dixson DL, Donelson JM, Pratchett MS, Devitsina G, Døving K (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci 106:1848–1852CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ochi H (1985) Temporal patterns of breeding and larval settlement in a temperte population of tropical anemonefish, Amphiprion clarkii. Jpn J Ichthyol 32:248–257Google Scholar
  42. Ochi H (1986) Growth of the anemonefish Amphiprion clarkii in temperate waters, with special reference to the influence of settling time on the growth of 0-year olds. Mar Biol 92:223–229CrossRefGoogle Scholar
  43. Ochi H (1989) Acquisition of breeding space by non-breeders in the anemonefish Amphiprion clarkii. Jpn J Icthyol 32:248–256Google Scholar
  44. Pereira PCH, Munday PL (2016) Coral colony size and structure as determinants of habitat use and fitness of coral-dwelling fishes. Mar Ecol Prog Ser 553:163–172CrossRefGoogle Scholar
  45. Robertson DR (1996) Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77:885–899CrossRefGoogle Scholar
  46. Sale PF (2004) Connectivity, recruitment variation, and the structure of reef fish communities. Integr Comp Biol 44:390–399CrossRefPubMedGoogle Scholar
  47. Sale PF, Doulas WA, Doherty PJ (1984) Choice of microhabitats by coral reef fishes at settlement. Coral Reefs 3:91–99CrossRefGoogle Scholar
  48. Schmitt RJ, Holbrook SJ (1999) Mortality of juvenile damselfish: implications for assessing processes that determine abundance. Ecology 80:35–50CrossRefGoogle Scholar
  49. Scott A, Dixson DL (2016) Reef fishes can recognize bleached habitat during settlement: sea anemone bleaching alters anemonefish host selection. Proc R Soc B 283:20152694CrossRefPubMedPubMedCentralGoogle Scholar
  50. Scott A, Rushworth KJW, Dalton SJ, Smith SDA (2016) Subtropical anemonefish Amphiprion latezonatus recorded in two new additional sea anemone species. Mar Biodiv 46:327–328CrossRefGoogle Scholar
  51. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910CrossRefPubMedGoogle Scholar
  52. Srinivasan M, Jones GP, Caley MJ (1999) Experimental evaluation of the roles of habitat selection and interspecific competition in determining patterns of host use by two anemonefishes. Mar Ecol Prog Ser 186:283–292CrossRefGoogle Scholar
  53. Sweatman HPA (1983) Influence of conspecifics on choice of settlement sites by larvae of two pomacentrid fishes (Dascyllus aruanus and Dascyllus reticulatus) on coral reefs. Mar Biol 75:225–229CrossRefGoogle Scholar
  54. Sweatman HPA (1988) Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J Exp Mar Biol Ecol 124:163–174CrossRefGoogle Scholar
  55. Tupper M, Boutilier RG (1995) Effects of conspecific density on settlement, growth and post-settlement survival of a temperate reef fish. J Exp Mar Biol Ecol 191:209–222CrossRefGoogle Scholar
  56. Webster MS, Hixon MA (2000) Mechanisms and individual consequences of intraspecific competition in a coral-reef fish. Mar Ecol Prog Ser 196:187–194CrossRefGoogle Scholar
  57. Wilson SK, Burgess SC, Cheal AJ, Emslie M, Fisher R, Miller I, Polunin NVC, Sweatman HPA (2008) Habitat utilization by coral reef fish: implications for specialists vs generalists in a changing environment. J Anim Ecol 77:220–228CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Marine Science and PolicyUniversity of DelawareLewesUSA
  2. 2.Marine Biology and Aquaculture, College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  3. 3.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

Personalised recommendations