The structure of fish follower-feeding associations at three oceanic islands in southwestern Atlantic

  • K. Y. InagakiEmail author
  • T. C. Mendes
  • J. P. Quimbayo
  • M. Cantor
  • I. Sazima


Structurally complex and competitive environments such as reef habitats may promote alternative behavioural feeding tactics in fishes. An understudied behavioural tactic is the follower-feeding association, in which individuals of a species follow (called “follower”) and benefit from the foraging activities of individuals of another species that disturbs the substrate (called “nuclear”). Here, we investigated the incidence of this tactic at three oceanic islands in the southwestern Atlantic by characterizing pairwise, and the emergent network of follower-feeding associations. We quantified associations among species according to their trophic categories, activity period, and group size. The incidence of follower-feeding associations was higher at islands with higher species richness, but the proportion of associations per species was higher at islands with lower species richness. Overall, mobile invertebrate-feeders, omnivores and macrocarnivores were the most common trophic categories engaged in this tactic. Most of follower-feeding associations involved diurnal species, which indicates that followers rely on visual cues to engage in this tactic. We also found that nuclear species were mainly solitary, while followers tended to aggregate in small- to medium-sized groups. Our study indicates that follower-feeding association is an opportunistic yet frequent feeding tactic at oceanic islands, which may stem from resource partitioning in such remote habitats.


Fish feeding relationships Nuclear-follower associations Commensalism Ecological interactions Brazilian province 



This study was part of the research program “Programa de Monitoramento de Longa Duração das Comunidades Recifais de Ilhas Oceânicas – PELD” (441241/2016-6, Carlos E.L. Ferreira-PI). K.Y.I. received scholarships from Coordination for the Improvement of Higher Education Personnel (CAPES)– Finance Code 001– and Brazilian National Council for Scientific and Technological Development (CNPq); T.C.M. received post-doctoral fellowship from Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; E-26/202.858/2016); J.P.Q. received post-doctoral fellowship from FAPESP (2018/21380-0); M.C. received post-doctoral fellowships from CNPq (153797/2016-9), Projeto Monitoramento de Praias (PMP/BS UFPR/UNIVALI 46/2016) and CAPES (PDE 88881.170254/2018-01); I.S. received grants from CNPq. We thank J.P. Krajewski, C. Sazima, and L. Almeida for the photographs of reef fish follower-feeding associations, and two anonymous referees for insightful suggestions. J.P.Q. thanks for the contribution of the Research Center for Marine Biodiversity of the University of São Paulo (NPBiomar).

Supplementary material

10641_2019_924_MOESM1_ESM.xlsx (29 kb)
ESM 1 (XLSX 28 kb)


  1. Aronson RB (1983) Foraging behaviour of the West Atlantic trumpetfish, Aulostomus maculatus: use of large, herbivorous reef fishes as camouflage. Bull Mar Sci 33:166–171Google Scholar
  2. Aued AW, Smith F, Quimbayo JP et al (2018)Large-scale patterns of benthic marine communities in the Brazilian province. PLoS One 13:1–15. CrossRefGoogle Scholar
  3. Auster PJ (2008) Predation tactics of trumpetfishes in midwater. Neotrop Ichthyol 6:289–292CrossRefGoogle Scholar
  4. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  5. Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems. Blackwell Publishing, OxfordGoogle Scholar
  6. Bender MG, Leprieur F, Mouillot D, Kulbicki M, Parravicini V, Pie MR, Barneche DR, Oliveira-Santos LGR, Floeter SR (2017) Isolation drives taxonomic and functional nestedness in tropical reef fish faunas. Ecography 40:425–435. CrossRefGoogle Scholar
  7. Boccaletti S, Latora V, Moreno Y et al (2006) Complex networks: structure and dynamics. Phys Rep 424:175–308. CrossRefGoogle Scholar
  8. Bonaldo RM, Krajewski JP, Sazima C, Sazima I (2006) Foraging activity and resource use by three parrotfish species at Fernando de Noronha archipelago, tropical West Atlantic. Mar Biol 149:423–433. CrossRefGoogle Scholar
  9. Bshary R, Hohner A, Ait-el-Djoudi K, Fricke H (2006) Interspecific communicative and coordinated hunting between groupers and giant moray eels in the Red Sea. PLoS Biol 4(12):e431. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cantor M, Pires MM, Marquitti FM, Raimundo RL, Sebastián-González E, Coltri PP, Perez SI, Barneche DR, Brandt DY, Nunes K, Daura-Jorge FG (2017) Nestedness across biological scales. PLoS One 12(2):e0171691CrossRefGoogle Scholar
  11. Cantor M, Longo GO, Fontoura L, Quimbayo JP, Floeter, SR, Bender, MG (2018) Interactions networks in the tropics. In: Datiilo W, Rico-Gray V (eds) Ecological networks in the tropics. Springer, pp 141–154Google Scholar
  12. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
  13. Cornell HV, Lawton JH (1992) Species interactions, local and regional processes, and limits to the richness of ecological communities : a theoretical perspective. J Anim Ecol 61:1–12CrossRefGoogle Scholar
  14. Costa-Pereira R (2012) Small fishes follow large mammals suspending sediment. Rev Chil Hist Nat 85:361–364CrossRefGoogle Scholar
  15. Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9Google Scholar
  16. Diamant A, Shpigel M (1985) Interspecific feeding associations of groupers (Teleostei: Serranidae) with octopuses and moray eels in the Gulf of Eilat (Aqaba). Environ Biol Fish 13:153–159.
  17. Gherardi DFM, Bosence DWJ (2001) Composition and community structure of the coralline algal reefs from Atol das Rocas, South Atlantic, Brazil. Coral Reefs 19:205–219. CrossRefGoogle Scholar
  18. Gomulkiewicz R, Thompson JN, Holt RD et al (2000) Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am Nat 156:156–174. CrossRefPubMedGoogle Scholar
  19. Grossman A, Sazima C, Bellini C, Sazima I (2006) Cleaning symbiosis between hawksbill turtles and reef fishes at Fernando de Noronha archipelago, off Northeast Brazil. Chelonian Conserv Biol 5:284–288.[284:CSBHTA]2.0.CO;2 CrossRefGoogle Scholar
  20. Hixon MA (2015) Predation: piscivory and the ecology of coral reef fishes. In: Mora C (ed) ecology of fishes on coral reefs. Cambridge University Press, pp 41–52Google Scholar
  21. Hobson ES (1965)Diurnal-nocturnal activity of some inshore fishes in the Gulf of California. Copeia 3:291–302CrossRefGoogle Scholar
  22. Juanes F, Buckel JA, Scharf FS (2002) Feeding ecology of piscivorous fishes. In: Handbook of fish biology and fisheries, vol 1. Blackwell Publishing, Oxford, pp 267–283CrossRefGoogle Scholar
  23. Kikuchi RKP, Leão ZMAN (1997) Rocas (southwestern equatorial Atlantic, Brazil): an atoll built primarily by coralline algae. Proceedings of 8th international coral reef symposium. Smithsonian Tropical Research Institute, Panama, 1:731–736Google Scholar
  24. Krajewski JP (2009) How do follower reef fishes find nuclear fishes? Environ Biol Fish 86:379–387. CrossRefGoogle Scholar
  25. Krajewski JP, Floeter SR (2011) Reef fish community structure of the Fernando de Noronha archipelago (equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish 92:25–40. CrossRefGoogle Scholar
  26. Krajewski JP, Bonaldo RM, Sazima C, Sazima I (2006) Foraging activity and behaviour of two goatfish species (Perciformes: Mullidae) at Fernando de Noronha archipelago, tropical West Atlantic. Environ Biol Fish 77:1–8. CrossRefGoogle Scholar
  27. Longo GO, Floeter SR (2012) Comparison of remote video and diver’s direct observations to quantify reef fishes feeding on benthos in coral and rocky reefs. J Fish Biol 81:1773–1780. CrossRefPubMedGoogle Scholar
  28. Longo GO, Morais RA, Martins CDL et al (2015)Between-habitat variation of benthic cover, reef fish assemblage and feeding pressure on the benthos at the only atoll in South Atlantic: Rocas atoll, NE Brazil. PLoS One 10(6):e0127176. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Luiz OJ, Mendes TC, Barneche DR et al (2015) Community structure of reef fishes on a remote oceanic island (St Peter and St Paul’s archipelago, equatorial Atlantic): the relative influence of abiotic and biotic variables. Mar Freshw Res 66:739–749. CrossRefGoogle Scholar
  30. Lukoschek V, McCormick MI (2000) A review of multi-species foraging associations in fishes and their ecological significance. Proceedings of 9th international coral reef symposium. Bali, Indonesia, I:467–474Google Scholar
  31. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  32. Montoya JM, Raffaelli D (2010) Climate change, biotic interactions and ecosystem services. Philos Trans R Soc B 365:2013–2018. CrossRefGoogle Scholar
  33. Morais RA, Brown J, Bedard S, Ferreira CEL, Floeter SR, Quimbayo JP, Rocha LA, Sazima I (2017a) Mob rulers and part-time cleaners: two reef fish associations at the isolated Ascension Island. J Mar Biol Assoc UK 97(4):1–13. CrossRefGoogle Scholar
  34. Morais RA, Ferreira CEL, Floeter SR (2017b) Spatial patterns of fish standing biomass across Brazilian reefs, southwestern Atlantic. J Fish Biol 91:1642–1667CrossRefGoogle Scholar
  35. Mouillot D, Villeger S, Parravicini V, Kulbicki M, Arias-González JE, Bender M, Chabanet P, Floeter SR, Friedlander A, Vigliola L, Bellwood DR (2014) Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc Natl Acad Sci 111(38):13757–13762. CrossRefPubMedGoogle Scholar
  36. Nash JC (2014) On best practice optimization methods in R. J Stat Softw 60:1–14CrossRefGoogle Scholar
  37. Nash JC, Varadhan R (2011) Unifying optimization algorithms to aid software system. J Stat Softw 43:1–14CrossRefGoogle Scholar
  38. Pereira, P. H. C., Feitosa, J. L. L., Chaves, L. C. T., and Araújo, M. E. (2012) Reef fish foraging associations: “nuclear-follower” behavior or an ephemeral interaction? In ‘proceedings of the 12th international coral reef symposium, Cairns, July 2012’. (Ed. D. Yellowlees and T. P. Hughes.) (ARC Centre of excellence for coral reef studies James Cook University, Townsville, AustraliaGoogle Scholar
  39. Pinheiro HT, Bernardi G, Simon T et al (2017) Island biogeography of marine organisms. Nature 549:82–85. CrossRefPubMedGoogle Scholar
  40. Pinheiro HT, Rocha LA, Macieira RM et al (2018)South-Western Atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity Centre in the Atlantic Ocean. Divers Distrib 24:951–965. CrossRefGoogle Scholar
  41. Quimbayo JP, Zapata FA, Floeter SR, Bessudo S, Sazima I (2014) Reef fish foraging associations at Malpelo Island, Colombia (tropical eastern Pacific). Bol Invest Mar Cost 43:183–193Google Scholar
  42. Quimbayo JP, Dias MS, Kulbicki M, Mendes TC, Lamb RW, Johnson AF, Aburto-Oropeza O, Alvarado JJ, Bocos AA, Ferreira CEL, Garcia E, Luiz OJ, Mascareñas-Osorio I, Pinheiro HT, Rodriguez-Zaragoza F, Salas E, Zapata FA, Floeter SR (2019) Determinants of reef fish assemblages in tropical oceanic islands. Ecography 42:77–87. CrossRefGoogle Scholar
  43. Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086. CrossRefGoogle Scholar
  44. Sale PF (1977) Maintenance of high diversity in coral reef fish communities. Am Nat 111:337–359CrossRefGoogle Scholar
  45. Sazima C (2006) Associações alimentares em peixes recifais, com destaque em espécies nucleares e seguidoras. Dissertation, Universidade Estadual Paulista “Julio de Mesquita Filho”Google Scholar
  46. Sazima C, Bonaldo RM, Krajewski JP, Sazima I (2005) The Noronha wrasse: a “jack-of-all-trades” follower. Aqua J Ichthyol Aquat Biol 9:97–108. CrossRefGoogle Scholar
  47. Sazima C, Krajewski JP, Bonaldo RM, Sazima I (2007)Nuclear-follower foraging associations of reef fishes and other animals at an oceanic archipelago. Environ Biol Fish 80:351–361. CrossRefGoogle Scholar
  48. Strand S (1988) Following behavior: interspecific foraging associations among Gulf of California reef fishes. Copeia 1988:351–357. CrossRefGoogle Scholar
  49. Teresa FB, Sazima C, Sazima I, Floeter SR (2014) Predictive factors of species composition of follower fishes in nuclear-follower feeding associations: a snapshot study. Neotrop Ichthyol 12:913–920. CrossRefGoogle Scholar
  50. Ternes MLF, Giglio VJ, Mendes TC, Pereira PHC (2018) Follower fish of the goldspotted eel Myrichthys ocellatus with a review on anguilliform fish as nuclear species. Helgol Mar Res 1–8.
  51. Whittaker RJ, Triantis KA, Ladle RJ (2008) A general dynamic theory of oceanic island biogeography. J Biogeogr 35:977–994. CrossRefGoogle Scholar
  52. Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21(12):1–20CrossRefGoogle Scholar
  53. Wilson SK, Fisher R, Pratchett MS et al (2008) Exploitation and habitat degradation as agents of change within coral reef fish communities. Glob Chang Biol 14:2796–2809. CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratório de Ecologia Marinha, Departamento de Oceanografia e LimnologiaUniversidade Federal do Rio Grande do NorteNatalBrazil
  2. 2.Departamento de EcologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Reef System Ecology and Conservation Lab, Departamento de Biologia MarinhaUniversidade Federal FluminenseNiteróiBrazil
  4. 4.Instituto do MarUniversidade Federal de São PauloSantosBrazil
  5. 5.Centro de Biologia MarinhaUniversidade de São PauloSão SebastiãoBrazil
  6. 6.Departamento de Ecologia e Zoologia, Centro de Ciências BiológicasUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  7. 7.Centro de Estudos do MarUniversidade Federal do ParanáPontal do ParanáBrazil
  8. 8.Max Planck Institute of Animal BehaviorRadolfzell am BodenseeGermany
  9. 9.School of Animal, Plant and Environmental SciencesUniversity of the WitswatersrandJohannesburgSouth Africa
  10. 10.Museu de ZoologiaUniversidade Estadual de CampinasCampinasBrazil
  11. 11.Grupo de Pesquisa de História Natural de VertebradosUniversidade Estadual de CampinasCampinasBrazil

Personalised recommendations