Coral Reefs

, Volume 35, Issue 2, pp 427–436 | Cite as

Cleaner wrasse influence habitat selection of young damselfish

  • D. Sun
  • K. L. Cheney
  • J. Werminghausen
  • E. C. McClure
  • M. G. Meekan
  • M. I. McCormick
  • T. H. Cribb
  • A. S. Grutter
Report

Abstract

The presence of bluestreak cleaner wrasse, Labroides dimidiatus, on coral reefs increases total abundance and biodiversity of reef fishes. The mechanism(s) that cause such shifts in population structure are unclear, but it is possible that young fish preferentially settle into microhabitats where cleaner wrasse are present. As a first step to investigate this possibility, we conducted aquarium experiments to examine whether settlement-stage and young juveniles of ambon damselfish, Pomacentrus amboinensis, selected a microhabitat near a cleaner wrasse (adult or juvenile). Both settlement-stage (0 d post-settlement) and juvenile (~5 weeks post-settlement) fish spent a greater proportion of time in a microhabitat adjacent to L. dimidiatus than in one next to a control fish (a non-cleaner wrasse, Halichoeres melanurus) or one where no fish was present. This suggests that cleaner wrasse may serve as a positive cue during microhabitat selection. We also conducted focal observations of cleaner wrasse and counts of nearby damselfishes (1 m radius) to examine whether newly settled fish obtained direct benefits, in the form of cleaning services, from being near a cleaner wrasse. Although abundant, newly settled recruits (<20 mm total length) were rarely (2 %) observed being cleaned in 20 min observations compared with larger damselfishes (58 %). Individual damselfish that were cleaned were significantly larger than the median size of the surrounding nearby non-cleaned conspecifics; this was consistent across four species. The selection by settlement-stage fish of a microhabitat adjacent to cleaner wrasse in the laboratory, despite only being rarely cleaned in the natural environment, suggests that even rare cleaning events and/or indirect benefits may drive their settlement choices. This behaviour may also explain the decreased abundance of young fishes on reefs from which cleaner wrasse had been experimentally removed. This study reinforces the potentially important role of mutualism during the processes of settlement and recruitment of young reef fishes.

Keywords

Recruitment Ectoparasites Cleaning behaviour Damselfish Mutualism 

Supplementary material

338_2015_1391_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 28 kb)

References

  1. Almany GR (2003) Priority effects in coral reef fish communities. Ecology 84:1920–1935CrossRefGoogle Scholar
  2. Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25:19–22CrossRefGoogle Scholar
  3. 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
  4. Bshary R, Würth M (2001) Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation. Proc R Soc Lond B Biol Sci 268:1495–1501CrossRefGoogle Scholar
  5. Bshary R, Oliveira RF, Oliveira TS, Canário AV (2007) Do cleaning organisms reduce the stress response of client reef fish? Front Zool 4:21CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chambers JM (1992) Linear models. In: Chambers JM, Hastie TJ (eds) Statistical models in S. Wadsworth & Brooks/Cole, Pacific Grove, CA, pp 95–144Google Scholar
  7. Cheney KL, Bshary R, Grutter AS (2008) Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations. Behav Ecol 19:1063–1067CrossRefGoogle Scholar
  8. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ (2009) Blue and yellow signal cleaning behavior in coral reef fishes. Curr Biol 19:1283–1287CrossRefPubMedGoogle Scholar
  9. Clague GE, Cheney KL, Goldizen AW, McCormick MI, Waldie PA, Grutter AS (2011) Long-term cleaner fish presence affects growth of a coral reef fish. Biol Lett 6:863–865CrossRefGoogle Scholar
  10. 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 Bio Ecol 414–415:62–68CrossRefGoogle Scholar
  11. Côté IM, Arnal C, Reynolds JD (1998) Variation in posing behaviour among fish species visiting cleaning stations. J Fish Biol 53:256–266CrossRefGoogle Scholar
  12. Dufour V, Galzin R (1993) Colonisation patterns of reef fish larvae to the lagoon at Moorea Island, French Polynesia. Mar Ecol Prog Ser 192:143–152CrossRefGoogle Scholar
  13. Gorlick DL, Atkins PD, Losey GS (1987) Effect of cleaning by Labroides dimidiatus (Labridae) on an ectoparasite population infecting Pomacentrus vaiuli (Pomacentridae) at Enewetak Atoll. Copeia 1:41–45CrossRefGoogle Scholar
  14. Green AL (1998) Spatio-temporal patterns of recruitment of labroid fishes (Pisces: Labridae and Scaridae) to damselfish territories. Environ Biol Fishes 51:235–244CrossRefGoogle Scholar
  15. Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30CrossRefGoogle Scholar
  16. Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58CrossRefGoogle Scholar
  17. Grutter AS (1996) Parasite removal rates by the cleaner wrasse, Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70CrossRefGoogle Scholar
  18. Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673CrossRefGoogle Scholar
  19. Grutter AS (2004) Cleaner fish use tactile dancing behaviour as a preconflict management strategy. Curr Biol 14:1080–1083CrossRefPubMedGoogle Scholar
  20. Grutter AS, Poulin R (1998) Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Mar Ecol Prog Ser 164:263–271CrossRefGoogle Scholar
  21. Grutter AS, Lester RJG (2002) Cleaner fish Labroides dimidiatus reduce ‘temporary’ parasitic corallanid isopods on the coral reef fish Hemigymnus melapterus. Mar Ecol Prog Ser 234:247–255CrossRefGoogle Scholar
  22. Grutter AS, Murphy J, Choat H (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67CrossRefPubMedGoogle Scholar
  23. Grutter AS, Glover S, Bshary R (2005) Does client size affect cleaner fish choice of client? An empirical test using client fish models. J Fish Biol 66:1748–1752CrossRefGoogle Scholar
  24. Grutter AS, Cribb TH, McCallum H, Pickering JL, McCormick MI (2010) Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis. Coral Reefs 29:31–40CrossRefGoogle Scholar
  25. Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, McCormick MI (2011) Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol 25:586–594CrossRefGoogle Scholar
  26. Heinlein JM, Stier AC, Steele MA (2010) Predators reduce abundance and species richness of coral reef fish recruits via non-selective predation. Coral Reefs 29:527–532CrossRefGoogle Scholar
  27. Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval-juvenile transition of a coral reef fish. Oecologia 139:23–29CrossRefPubMedGoogle Scholar
  28. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  29. Kerrigan BA (1996) Temporal patterns in size and condition at settlement in two tropical reef fishes (Pomacentridae: Pomacentrus amboinensis and P. nagasakiensis). Mar Ecol Prog Ser 135:27–41CrossRefGoogle Scholar
  30. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513CrossRefGoogle Scholar
  31. Lecchini D, Planes S, Galzin R (2005) Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav Ecol Sociobiol 58:18–26CrossRefGoogle Scholar
  32. Lecchini D, Planes S, Galzin R (2007) The influence of habitat characteristics and conspecifics on attraction and survival of coral reef fish juveniles. J Exp Mar Bio Ecol 341:85–90CrossRefGoogle Scholar
  33. Lecchini D, Peyrusse K, Lanyon RG, Lecellier G (2014) Importance of visual cues of conspecifics and predators during the habitat selection of coral reef fish larvae. Ethology 337:345–351Google Scholar
  34. Leis JM (2006) Are larvae of demersal fishes plankton or nekton? Adv Mar Biol 51:59–141Google Scholar
  35. Leis JM, Carson-Ewart BM (2002) In situ settlement behaviour of damselfish (Pomacentridae) larvae. J Fish Biol 61:325–346CrossRefGoogle Scholar
  36. Losey GS, Mahon JL, Danilowicz BS (1995) Innate recognition by host fish of their cleaning symbiont. Ethology 100:277–283CrossRefGoogle Scholar
  37. McCormick MI, Makey L, Dufour V (2002) Comparative study of metamorphosis in tropical reef fishes. Mar Biol 141:841–853CrossRefGoogle Scholar
  38. McCormick MI, Moore JAY, Munday PL (2010) Influence of habitat degradation on fish replenishment. Coral Reefs 29:537–546CrossRefGoogle Scholar
  39. Meekan MG, Milicich MJ, Doherty PJ (1993) Larval production drives temporal patterns of larval supply and recruitment of a coral reef damselfish. Mar Ecol Prog Ser 93:217–225CrossRefGoogle Scholar
  40. Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar Biol 139:373–381CrossRefGoogle Scholar
  41. Mitchell MD, McCormick MI, Chivers DP, Ferrari MCO (2013) Generalization of learned predator recognition in coral reef ecosystems: how cautious are damselfish? Funct Ecol 27:299–304CrossRefGoogle Scholar
  42. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  43. Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. Crawford House Publishing, Bathurst, NSWGoogle Scholar
  44. Robertson DR (1974) A study of the biology and reproductive biology of the labrid fish, Labroides dimidiatus, at Heron Island, Great Barrier Reef. Ph.D. thesis, The University of Queensland, pp 174Google Scholar
  45. Simpson SD, Jeffs A, Montgomery JC, McCauley R, Meekan MG (2008) Nocturnal relocation of adult and juvenile coral reef fishes in response to reef noise. Coral Reefs 27:97–104CrossRefGoogle Scholar
  46. Soares MC, Oliveira R, Ros AFH, Grutter AS, Bshary R (2011) Tactile stimulation lowers stress in fish. Nat Commun 2:534CrossRefPubMedGoogle Scholar
  47. Stummer LE, Weller JA, Johnson ML, Côté IM (2004) Size and stripes: how fish clients recognize cleaners. Anim Behav 68:145–150CrossRefGoogle Scholar
  48. Sun D, Blomberg SP, Cribb TH, McCormick MI, Grutter AS (2012) The effects of parasites on the early life stages of a damselfish. Coral Reefs 31:1065–1075CrossRefGoogle Scholar
  49. Sun D, Cheney KL, Werminghausen J, Meekan MG, McCormick MI, Cribb TH, Grutter AS (2015) Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs. Biol Lett 11 [DOI: 10.1098/rsbl.2015.0456]
  50. Sweatman H (1985) The influence of adults of some coral reef fishes on larval recruitment. Ecol Monogr 55:469–485CrossRefGoogle Scholar
  51. Tolimieri N (1995) Effects of microhabitat characteristics on the settlement and recruitment of a coral reef fish at two spatial scales. Oecologia 102:52–63CrossRefGoogle Scholar
  52. Vail AL, McCormick MI (2011) Metamorphosing reef fishes avoid predator scent when choosing a home. Biol Lett 7:921–924CrossRefPubMedPubMedCentralGoogle Scholar
  53. Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS (2011) Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities. PLoS One 6:e21201CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • D. Sun
    • 1
  • K. L. Cheney
    • 1
  • J. Werminghausen
    • 1
  • E. C. McClure
    • 1
    • 2
  • M. G. Meekan
    • 3
  • M. I. McCormick
    • 2
  • T. H. Cribb
    • 1
  • A. S. Grutter
    • 1
  1. 1.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  2. 2.ARC Centre of Excellence for Coral Reef Studies and College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia
  3. 3.Australian Institute of Marine ScienceThe UWA Oceans Institute (M096)CrawleyAustralia

Personalised recommendations