Advertisement

Marine Biology

, Volume 162, Issue 3, pp 493–499 | Cite as

The influence of structural complexity and reef habitat types on flight initiation distance and escape behaviors in labrid fishes

  • José de Anchieta C. C. NunesEmail author
  • Cláudio L. S. Sampaio
  • Francisco Barros
Original Paper

Abstract

Structural complexity is a key parameter for fish on reef habitats. Several studies have investigated the influence of this variable on aspects of reef fish population and community dynamics. However, there is a lack of knowledge on the influence of structural complexity on antipredator behavior. Here we studied the effect of habitat type and structural complexity on flight initiation distance (FID) and the escape behaviors of four labrid fishes (Halichoeres brasiliensis, H. penrosei, H. poeyi and Sparisoma axillare) on two different reef habitats (coral and rocky reefs). Habitat type influenced the FID of three of the studied species (H. brasiliensis, H. penrosei and S. axillare), and structural complexity negatively influenced the FID of two species (H. brasiliensis and S. axillare). The frequency of escape behaviors varied between species. All of them showed high frequency of the ‘run away’ behavior and low frequency of the ‘leave the habitat’ behavior. On coral reefs, structural complexity influenced the ‘fled to the holes’ for S. axillare only. Reef ecosystems worldwide are being modified by anthropogenic activities. Our results suggest that if such activities reduce structural complexity, then ‘seascapes of fear’ for labrid fishes will become more widespread, which could lead to negative consequences in the reef ecosystems.

Keywords

Coral Reef Reef Fish Crustose Coralline Alga Halimeda Reef Habitat 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Abraão Nunes (Grupo Nunes, BR) for helping during the field work. Lili Colman (University of Exeter, UK), Miguel Loiola (Universidade Federal da Bahia, BR) and Luciana Leite (University of Cambridge, UK) for help in the revision. Mariana Thevenin (Universidade Federal da Bahia, BR) for her help with the figures and analysis. Fraser A. Januchowski-Hartley (James Cook University, AUS) sent valuable references, and Nick Graham (James Cook University, AUS) and Daniel Blumstein (University of California, Los Angeles, EUA) exchanged ideas with the first author. We also thank CAPES for the financial support to J. A. C. C. N.

References

  1. Almany G (2004) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106:275–284. doi: 10.1111/j.0030-1299.2004.13193.x CrossRefGoogle Scholar
  2. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833. doi: 10.1038/nature02691 CrossRefGoogle Scholar
  3. Bernardi G, Robertson DR, Clifton KE, Azzurro E (2000) Molecular systematics, zoogeography, and evolutionary ecology of the Atlantic genus Sparisoma. Mol Phylogenet Evol 15:292–300. doi: 10.1006/mpev.1999.0745 CrossRefGoogle Scholar
  4. Blumstein DT (2003) Flight initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857CrossRefGoogle Scholar
  5. Blumstein DT, Harcourt LL, Ross G (2003) Testing a key assumption of wildlife buffer zones: is flight initiation distance a species-specific trait? Biol Conserv 110:97–100. doi: 10.1016/S0006-3207(02)00180-5 CrossRefGoogle Scholar
  6. Blumstein DT, Fernández-Juricic E, Zollber PA, Garity SC (2005) Inter-specific variation in avian responses to human disturbance. J Appl Ecol 42(5):943–953. doi: 10.1111/j.1365-2664.2005.01071.x CrossRefGoogle Scholar
  7. Blumstein DT, Bitton A, Veiga J (2006) How does the presence of predators influence the persistence of antipredator behavior? J Theor Biol 239:460–468. doi: 10.1016/j.jtbi.2005.08.011 CrossRefGoogle Scholar
  8. Bohorquez-Herrera J, Kawano SM, Domenici P (2013) Foraging behavior delays mechanically-stimulated escape responses in fish. Integr Comp Biol 53:780–786. doi: 10.1093/icb/ict031 CrossRefGoogle Scholar
  9. 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. doi: 10.1007/s00227-005-0233-9 CrossRefGoogle Scholar
  10. Bryant D, Burke L, Mcmanus J, Spalding M (2000) Reef at risk: a map-based indicator of threats to the world’s coral reefs. World Resources Institute, Washington, DC, USA (http://www.wri.org/reefsatrisk/)
  11. Chaves LCT, Monteiro-Neto C (2009) Comparative analysis of rocky reef fish community structure in coastal islands of south-eastern Brazil. J Mar Bio Assoc UK 89:609–619. doi: 10.1017/S0025315408002695 CrossRefGoogle Scholar
  12. Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Plymouth Marine Laboratory, PRIMER-E 172 pGoogle Scholar
  13. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80. doi: 10.1016/j.jembe.2005.12.017 CrossRefGoogle Scholar
  14. Coni EOC, Nunes JACC, Sampaio CLS (2007) Halichoeres penrosei (Labridae), a sporadic cleaner wrasse. Mar Biodivers Rec 1:e82. doi: 10.1017/S1755267207008494 CrossRefGoogle Scholar
  15. Coni EOC, Nunes JACC, Ferreira CM, Maia-Nogueira R, Medeiros DV, Sampaio CLS (2010) The Spanish hogfish Bodianus rufus (Labridae) acting as cleaner of nocturnal fish in the north–east of Brazil. Mar Biodivers Rec 3:e23. doi: 10.1017/S1755267210000187 CrossRefGoogle Scholar
  16. Cooper WE Jr (2008) Visual monitoring of predators: occurrence, cost and benefit for escape. Anim Behav 76:1365–1372CrossRefGoogle Scholar
  17. Cooper WE Jr (2009) Flight initiation distance decreases during social activity in lizards (Sceloporusvirgatus). Behav Ecol Sociobiol 63:1765–1771. doi: 10.1007/s00265-009-0799-1 CrossRefGoogle Scholar
  18. Cooper WE Jr, Pérez-Mellado V, Baird T, Baird TA, Caldwell JP, Vitt LJ (2002) Effects of risk, cost, and their interaction on optimal escape by nonrefuging Bonaire whiptail lizards. Cnemidophorus murinus Behav Ecol 14:288–293. doi: 10.1093/beheco/14.2.288 CrossRefGoogle Scholar
  19. Costa OS Jr, Leão ZMAN, Nimmo M, Atrill M (2000) Nutrification impacts on coral reefs from Northern Bahia, Brazil. Hydrobiologia 440:307–316CrossRefGoogle Scholar
  20. DeLoach N, Humann P (1999) Reef fish behavior: Florida, Caribbean, Bahamas. New World Publications, Jacksonville 359pGoogle Scholar
  21. Dustan P, Doherty O, Pardede S (2013) Digital reef rugosity estimates coral reef habitat complexity. PLoS One 8(2):e57386. doi: 10.1371/journal.pone.0057386 CrossRefGoogle Scholar
  22. Feary DA, Graham NAJ, Cinner JE, Januchowski-Hartley FA (2011) The impacts of customary marine closures on fish behaviour with implications for spear fishing success and underwater visual census. Conserv Biol 25:341–349. doi: 10.1111/j.1523-1739.2010.01613.x Google Scholar
  23. Ferreira CEL, Gonçalves JEA, Coutinho R (2001) Fish community structure and habitat complexity in a tropical rocky shore. Environ Biol Fish 61:353–369. doi: 10.1023/A:1011609617330 CrossRefGoogle Scholar
  24. Floeter SR, Krohling W, Gasparini JL, Ferreira CEL, Zalmon IL (2007) Reef fish community structure on coastal island of southeastern Brazil: the influence of exposure and benthic cover. Environ Biol Fish 78:147–160. doi: 10.1007/s10641-006-9084-6 CrossRefGoogle Scholar
  25. Francini-Filho RB, Moura RL (2008) Dynamics of fish assemblages on coral reefs subjected to different management regimes in the Abrolhos Bank, eastern Brazil. Aquat Conserv Mar Freshw Ecosys 18:1166–1179. doi: 10.1002/aqc.966 CrossRefGoogle Scholar
  26. Fulton CJ, Bellwood DR (2004) Wave exposure, swimming performance, and the structure of tropical and temperate reef fish assemblages. Mar Biol 144:429–437. doi: 10.1007/S00227-003-1216-3 CrossRefGoogle Scholar
  27. Fulton CJ, Belwood DR (2002) Patterns of foraging in labrid fishes. Mar Ecol Prog Ser 226:135–142. doi: 10.3354/meps226135 CrossRefGoogle Scholar
  28. Fulton CJ, Bellwood DR, Wainwright PC (2001) The relationship between swimming ability and habitat use in wrasses (Labridae). Mar Biol 139:25–33. doi: 10.1007/s002270100565 CrossRefGoogle Scholar
  29. Fulton CJ, Bellwood DR, Wainwright PC (2005) Wave energy and swimming performance shape coral reef fish assemblages. P R Soc Lond B 272:827–832. doi: 10.1098/rspb.2004.3029 CrossRefGoogle Scholar
  30. Gasparini JL, Floeter SR, Ferreira CEL, Sazima I (2005) Marine ornamental trade in Brazil. Biodivers Conserv 14:2883–2899. doi: 10.1007/s10531-004-0222-1 CrossRefGoogle Scholar
  31. Gotanda KM, Turgeon K, Kramer DL (2009) Body size and reserve protection affect flight initiation distance in parrotfishes. Behav Ecol Sociobiol 63:1563–1572. doi: 10.1007/s00265-009-0750-5 CrossRefGoogle Scholar
  32. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326. doi: 10.1007/s00338-012-0984-y CrossRefGoogle Scholar
  33. Graham NAJ, Cinner JE, Norstrom AV, Nyström M (2014) Coral reefs as novel ecosystems: embracing new futures. Curr Opin Env Sust 7:9–14. doi: 10.1016/j.cosust.2013.11.023 CrossRefGoogle Scholar
  34. Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589. doi: 10.1006/anbe.2001.1781 CrossRefGoogle Scholar
  35. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Elbert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi: 10.1126/science.1149345 CrossRefGoogle Scholar
  36. Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101. doi: 10.2307/2937124 CrossRefGoogle Scholar
  37. Hobson ES (1975) Feeding patterns among tropical fishes. Am Sci 63:382–392Google Scholar
  38. Hoegh-Guldberg O (2006) Complexities of coral reef recovery. Science 311:42–43. doi: 10.1126/science.1122951 CrossRefGoogle Scholar
  39. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory and the resilience of coral reefs to climate change. Curr Biol 17:1–6. doi: 10.1016/j.cub.2006.12.049 CrossRefGoogle Scholar
  40. Jackson JBC (2008) Ecological extinction and evolution in the brave new ocean. Proc Natl Acad Sci USA 105:11458–11465. doi: 10.1073/pnas.0802812105 CrossRefGoogle Scholar
  41. Jackson JBC (2010) The future of the oceans past. Philos Trans R Soc B 365:3765–3778. doi: 10.1098/rstb.2010.0278 CrossRefGoogle Scholar
  42. Januchowski-Hartley FA, Graham NAJ, Feary DA, Morove T, Cinner JE (2011) Fear of fishers: human predation explains behavioral changes in coral reef fishes. PLoS One 6(8):e22761. doi: 10.1371/journal.pone.0022761 CrossRefGoogle Scholar
  43. Januchowski-Hartley FA, Nash KL, Lawton RJ (2012) The influence of spear guns, dive gear, and observers on estimating fish flight initiation distance on coral reefs. Mar Ecol Prog Ser 469:113–119. doi: 10.3354/meps09971 CrossRefGoogle Scholar
  44. Januchowski-Hartley FA, Graham NAJ, Cinner JE, Russ GR (2013) Spillover of fish naïveté from marine reserves. Ecol Lett 16:191–197. doi: 10.1111/ele.12028 CrossRefGoogle Scholar
  45. Jones GP, Syms G (1998) Disturbance, habitat structure and the ecology of reef fish on coral reefs. Aust J Ecol 23:287–297. doi: 10.1111/j.1442-9993.1998.tb00733.x CrossRefGoogle Scholar
  46. Krajewski JP, Floeter SR, Jones G, Leite F (2010) Patterns of variation in behavior within and among reef fishes species on an isolated tropical island: influence of exposure and substratum. J Mar Biol Assoc UK 91:1359–1368. doi: 10.1017/S0025315410000111 CrossRefGoogle Scholar
  47. Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J3:1–7. doi: 10.2174/1874213001003030001 CrossRefGoogle Scholar
  48. Loiola M, Oliveira MD, Kikuchi RKP (2013) Tolerance of Brazilian brain coral Mussismilia braziliensis to sediment and organic matter inputs. Mar Pollut Bull 77:55–62. doi: 10.1016/j.marpolbul.2013.10.033 CrossRefGoogle Scholar
  49. Luckhurst BE, Luckhurst K (1978) Analysis of influence of substrate variables on coral reef fish communities. Mar Biol 49:317–324. doi: 10.1007/BF00455026 CrossRefGoogle Scholar
  50. Maia-Nogueira R, Medeiros DV, Jardim A, Nunes JACC, Sampaio CLS (2010) Banded butterflyfish Chaetodon striatus (Chaetodontidae) cleaning the green turtle, Chelonia mydas (Cheloniidae). Mar Biodivers Rec 3:e116. doi: 10.1017/S1755267210001041 CrossRefGoogle Scholar
  51. Martha M, Jones KMM (2002) Behavioural overlap in six Caribbean labrid species: intra- and interspecific similarities. Environ Biol Fish 65:71–81. doi: 10.1023/A:1019675323053 CrossRefGoogle Scholar
  52. Miranda RJ, Cruz ICS, Leão ZMAN (2013) Coral bleaching in the Caramuanas reef (Todosos Santos Bay, Brazil) during the 2010 El Niño event. Lat Am J Aquat Res 41:351–360. doi: 10.3856/vol41-issue2-fulltext-14 CrossRefGoogle Scholar
  53. Nunes JACC, Medeiros DV, Reis-Filho JA, Sampaio CLS, Barros F (2010) Reef fishes captured by recreational spearfishing on reefs of Bahia State, northeast Brazil. Biota Neotrop 12:179–185. http://www.biotaneotropica.org.br/v12n1/pt/abstract?article+bn02012012012
  54. Nunes JACC, Sampaio CLS, Barros F (2013) How wave exposure, group size and habitat complexity influence foraging and population densities in fishes of the genus Halichoeres (Perciformes: Labridae) on tropical rocky shores. Mar Biol 160:2383–2394. doi: 10.1007/s00227-013-2233-5 CrossRefGoogle Scholar
  55. Polunin NVC, Roberts CM (1993) Greater biomass and value of target coral reef fishes in two small Caribbean marine reserves. Mar Ecol Prog Ser 100:167CrossRefGoogle Scholar
  56. R Core Team (2012) 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/
  57. Rocha LA (2004) Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia 4:770–782. doi: 10.1643/CG-04-106 CrossRefGoogle Scholar
  58. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. P R Soc B 272:573–579. doi: 10.1098/2004.3005 CrossRefGoogle Scholar
  59. Rocha LA, Pinheiro TH, Gasparini JL (2010) Description of Halichoeres rubrovirens, a new species of wrasse (Labridae: Perciformes) from the Trindade and Martin Vaz Island group, southeastern Brazil, with a preliminary mtDNA molecular phylogeny of New World Halichoeres. Zootaxa 2422:22–30Google Scholar
  60. Runyan AM, Blumstein DT (2004) Do individual differences influence flight initiation distance? J Wild Manag 68:1124–1129. doi:10.2193/0022-541X(2004)068[1124:DIDIFI]2.0.CO;2CrossRefGoogle Scholar
  61. Sampaio CLS, Nottingham MC (2008) Guia para identificação de peixes ornamentais volume I: espécies marinhas. IBAMA, Brasília, p 205Google Scholar
  62. Sazima I, Moura RL, Gasparini JL (1998) The wrasse Halichoeres cyanocephalus (Labridae) as a specialized cleaner fish. Bull Mar Sci 63:605–610Google Scholar
  63. Sazima C, Bonaldo RM, Krajewski JP, Sazima I (2005) The Noronha wrasse: a jack-of-all-trades follower. Aqua J Ichthyol Aquat Biol 9:97–108Google Scholar
  64. Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173. doi: 10.1016/j.biocon.2008.06.026 CrossRefGoogle Scholar
  65. Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B 272:2627–2634. doi: 10.1098/rspb.2005.3251 CrossRefGoogle Scholar
  66. Streelman JT, Alfaro M, Westneat MW, Bellwood DR, Karl SA (2002) Evolutionary history of the parrotfishes: biogeography, ecomorphology, and comparative diversity. Evolution 56:961–971. doi: 10.1111/j.0014-3820.2002.tb01408.x CrossRefGoogle Scholar
  67. Wirsing AJ, Heithaus MR, Frid A, Dill LM (2008) Seascapes of fear: evaluating sublethal predator effects experienced and generated by marine mammals. Mar Mam Sci 24:1–15. doi: 10.1111/j.1748-7692.2007.00167.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • José de Anchieta C. C. Nunes
    • 1
    • 2
    Email author
  • Cláudio L. S. Sampaio
    • 3
  • Francisco Barros
    • 1
  1. 1.Programa de Pós-Graduacão em Ecologia e Biomonitoramento, Laboratório de Ecologia BentônicaUniversidade Federal da BahiaSalvadorBrazil
  2. 2.ECUS, Institute of EducationScience and Socio-Environmental UtilitySalvadorBrazil
  3. 3.Departamento de Engenharia de Pesca, Unidade de Ensino PenedoUniversidade Federal de AlagoasMaceióBrazil

Personalised recommendations