Environmental Biology of Fishes

, Volume 100, Issue 5, pp 551–563 | Cite as

Fish diversity in tidepools: assembling effects of environmental heterogeneity

  • Luis Artur Valões BezerraEmail author
  • André Andrian Padial
  • Filipe Brasil Mariano
  • Danielle Sequeira Garcez
  • Jorge Iván Sánchez-Botero


Tidepools are considered ecosystems of high interchangeable fish biota. However, natural and anthropogenic actions that alter negatively marine ecosystems functioning (e.g., algal exploitation) are causing homogenization of fish biodiversity. Here, we describe the functional and taxonomic assembling of fishes in beach rocks of northeastern Brazil. Traits of fish species were retrieved from Fishbase and beta diversity was assessed by the dispersion of abundance, presence-absence and functional diversity in the multivariate space. We explained spatial-temporal variation in: alpha diversity, taxonomic and functional community composition; as well as temporal variation in functional, beta and gamma diversities. We found an annual stability in fish diversity and composition, and that fish biota was assembled mainly per tidepools’ depths. Substrate heterogeneity was correlated to depth, highlighting the role of local features as filters to organize the fish fauna vertically in tidepools, especially a cultivation of algae that influences the local assembling. We also highlight the uniqueness status of beach rocks in the Brazilian tropical region.


Coral reef fish Functional traits Beta diversity Community organization Gracilaria spp. Brazilian western Atlantic 



We are thankful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) by student’s scholarship for the first author, and other funding to this Project. Laboratório de Ecologia Aquática, Laboratório de Ecologia Pesqueira, Labomar (both from Universidade Federal do Ceará) to subside our samples and logistics and FUNCAP (Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico) for financial support. IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) and ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade), the federal regulatory agencies considering animal care in Brazil, support non-invasive approaches for fish census, such as the employed here. We thus declare that there is no conflict considering animal care or ethics committee.

Supplementary material

10641_2017_584_MOESM1_ESM.docx (1.3 mb)
ESM 1 (DOCX 1332 kb)


  1. Adjeroud M, Kayal M, Penin L (2015) In: Rossi S, Bramanti L, Gori A, del Valle C (eds) Marine animal forests: the ecology of benthic biodiversity hotspots. Springer International Publishing, Cham, pp 1–21Google Scholar
  2. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi: 10.1111/j.1461-0248.2006.00926.x CrossRefPubMedGoogle Scholar
  3. Anderson MJ, Crist TO, Chase JM et al (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28. doi: 10.1111/j.1461-0248.2010.01552.x CrossRefPubMedGoogle Scholar
  4. Andrades R, Macieira RM, Reis-Filho JA et al (2016) Trapped in their own “home”: unexpected records of intertidal fish desiccation during low tides. J Appl Ichthyol:1–3. doi: 10.1111/jai.13074
  5. Arakaki S, Tokeshi M (2006) Short-term dynamics of tidepool fish community: diel and seasonal variation. Environ Biol Fish 76:221–235. doi: 10.1007/s10641-006-9024-5 CrossRefGoogle Scholar
  6. Arakaki S, Tsuchiya M, Tokeshi M (2014) Testing latitudinal patterns of tidepool fish assemblages: local substrate characteristics affect regional-scale trends. Hydrobiologia 733:45–62. doi: 10.1007/s10750-013-1768-2 CrossRefGoogle Scholar
  7. Baker DGL, Eddy TD, McIver R et al (2016) Comparative analysis of different survey methods for monitoring fish assemblages in coastal habitats. PeerJ 4:1–21. doi: 10.7717/peerj.1832 CrossRefGoogle Scholar
  8. Barbier E, Hacker SD (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193CrossRefGoogle Scholar
  9. Barrett CJ, Johnson ML, Hull SL (2015) Diet as a mechanism of coexistence between intertidal fish species of the U.K. Hydrobiologia 768:125–135. doi: 10.1007/s10750-015-2537-1 CrossRefGoogle Scholar
  10. Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. doi: 10.1111/j.1466-8238.2009.00490.x CrossRefGoogle Scholar
  11. Bizzarro JJ, Yoklavich MM, Wakefield WW (2016) Diet composition and foraging ecology of U.S. Pacific Coast groundfishes with applications for fisheries management. Environ Biol Fishes. doi: 10.1007/s10641-016-0529-2 Google Scholar
  12. Blanchet FG, Legendre P, Borcard D (2008) forward selection of explanatory variables. Ecology 89:2623–2632. doi: 10.1890/07-0986.1
  13. Bloch CP, Klingbeil BT (2016) Anthropogenic factors and habitat complexity influence biodiversity but wave exposure drives species turnover of a subtropical rocky inter-tidal metacommunity. Mar Ecol 37:64–76. doi: 10.1111/maec.12250 CrossRefGoogle Scholar
  14. Boettiger C, Lang DT, Wainwright PC (2012) Rfishbase: exploring, manipulating and visualizing FishBase data from R. J Fish Biol 81:2030–2039. doi: 10.1111/j.1095-8649.2012.03464.x CrossRefPubMedGoogle Scholar
  15. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. doi: 10.1016/S0304-3800(01)00501-4 CrossRefGoogle Scholar
  16. Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540. doi: 10.1111/j.1654-1103.2005.tb02393.x CrossRefGoogle Scholar
  17. Bozec YM, Kulbicki M, Laloë F et al (2011) Factors affecting the detection distances of reef fish: implications for visual counts. Mar Biol 158:969–981. doi: 10.1007/s00227-011-1623-9 CrossRefGoogle Scholar
  18. Bueno LS, Bertoncini AA, Koenig CC et al (2016) Evidence for spawning aggregations of the endangered Atlantic goliath grouper Epinephelus Itajara in southern Brazil. J Fish Biol 89:876–889. doi: 10.1111/jfb.13028 CrossRefPubMedGoogle Scholar
  19. Bush A, Harwood T, Hoskins AJ et al (2016) Current uses of Beta-diversity in biodiversity conservation: a response to Socolar et al. Trends Ecol Evol 31:337–338. doi: 10.1016/j.tree.2016.02.020 CrossRefPubMedGoogle Scholar
  20. Carr MH, Anderson TW, Hixon M (2002) Biodiversity, population regulation, and the stability of coral-reef fish communities. Proc Natl Acad Sci U S A 99:11241–11245. doi: 10.1073/pnas.162653499 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Castellanos-Galindo GA, Giraldo A, Rubio EA (2005) Community structure of an assemblage of tidepool fishes on a tropical eastern Pacific rocky shore, Colombia. J Fish Biol 67:392–408. doi: 10.1111/j.0022-1112.2005.00735.x CrossRefGoogle Scholar
  22. Chargulaf CA, Townsend KA, Tibbetts IR (2011) Community structure of soft sediment pool fishes in Moreton Bay, Australia. J Fish Biol 78:479–494. doi: 10.1111/j.1095-8649.2010.02866.x CrossRefPubMedGoogle Scholar
  23. Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science (80- ) 328:1388–1391. doi: 10.1126/science.1187820
  24. Christensen MS, Winterbottom R (1981) A correction factor for, and its application to, visual censuses of littoral fish. South African J Zool 16:73–79. doi: 10.1080/02541858.1981.11447736 CrossRefGoogle Scholar
  25. Cowen RK (2006) Scaling of Connectivity in Marine Populations. Science (80- ) 311:522–527. doi: 10.1126/science.1122039
  26. Cox TE, Baumgartner E, Philippoff J, Boyle KS (2011) Spatial and vertical patterns in the tidepool fish assemblage on the island of O′ahu. Environ Biol Fish 90:329–342. doi: 10.1007/s10641-010-9744-4 CrossRefGoogle Scholar
  27. Crabtree RE, Dean JM (1982) The structure of two South Carolina estuarine tide pool fish assemblages. Estuaries 5:2. doi: 10.2307/1352211 CrossRefGoogle Scholar
  28. Cunha EA, Carvalho RAA, Monteiro-Neto C et al (2008) Comparative analysis of tidepool fish species composition on tropical coastal rocky reefs at state of Ceará, Brazil. Iheringia Série Zool 98:379–390. doi: 10.1590/S0073-47212008000300013 CrossRefGoogle Scholar
  29. Davis J (2000) Spatial and seasonal patterns of habitat partitioning in a guild of southern California tidepool fishes. Mar Ecol Prog Ser 196:253–268. doi: 10.3354/meps196253 CrossRefGoogle Scholar
  30. Dethier MN (1984) Disturbance and recovery in intertidal pools: maintenance of mosaic patterns. Ecol Monogr 54:99–118. doi: 10.2307/1942457 CrossRefGoogle Scholar
  31. Eschmeyer WN, Fricke R (2011) Species of fishes by family/subfamily. In: Cat. Fishes Electron. version.
  32. Ferreira CEL, Luiz OJ, Floeter SR et al (2015) First record of invasive lionfish (Pterois Volitans) for the Brazilian coast. PLoS One 10:1–5. doi: 10.1371/journal.pone.0123002 Google Scholar
  33. Freitas JEP, Lotufo TMC (2015) Reef fish assemblage and zoogeographic affinities of a scarcely known region of the western equatorial Atlantic. J Mar Biol Assoc United Kingdom 95:623–633. doi: 10.1017/S0025315414001404 CrossRefGoogle Scholar
  34. Froese R, Pauly D (2012) FishBase. World Wide Web electronic publication. In: version (01/2012).
  35. Gibson RN (1972) The vertical distribution and feeding relationships of intertidal fish on the Atlantic coast of France. J Anim Ecol 41:189–207. doi: 10.2307/3512 CrossRefGoogle Scholar
  36. Gibson RN, Yoshiyama RM (1999) Intertidal fish communities. Intertidal fishes life two worlds:264–296Google Scholar
  37. Godinho WO, Lotufo TMC (2010) Local v. Microhabitat influences on the fish fauna of tidal pools in north-East Brazil. J Fish Biol 76:487–501. doi: 10.1111/j.1095-8649.2009.02501.x CrossRefPubMedGoogle Scholar
  38. Grieve B, Curchitser E, Rykaczewski R (2016) Range expansion of the invasive lionfish in the Northwest Atlantic with climate change. Mar Ecol Prog Ser 546:225–237. doi: 10.3354/meps11638 CrossRefGoogle Scholar
  39. Griffiths SP (2003) Rockpool ichthyofaunas of temperate Australia: species composition, residency and biogeographic patterns. Estuar Coast Shelf Sci 58:173–186. doi: 10.1016/S0272-7714(03)00073-8 CrossRefGoogle Scholar
  40. Gutterres Giordano R, Neves dos Santos L (2014) Comparative analysis of free and scuba diving for benthopelagic and cryptic fish species associated with rocky reefs. Lat Am J Aquat Res 42:301–306. doi: 10.3856/vol42-issue2-fulltext-2 CrossRefGoogle Scholar
  41. Halpern B, Floeter S (2008) Functional diversity responses to changing species richness in reef fish communities. Mar Ecol Prog Ser 364:147–156. doi: 10.3354/meps07553 CrossRefGoogle Scholar
  42. Heino J, Melo AS, Siqueira T et al (2015) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw Biol 60:845–869. doi: 10.1111/fwb.12533 CrossRefGoogle Scholar
  43. Hilomen-Garcia G, Reyes RD, Garcia CMH (2003) Tolerance and growth of juvenile seahorse Hippocampus Kuda exposed to various salinities. J Appl Ichthyol 19:94–98CrossRefGoogle Scholar
  44. Human P, DeLoach N (2002) Reef Fish Identification. Florida Caribbean Bahamas, 3rd edn. New World Publications, Inc. Jacksonville, Fl. Printed by Star Standard Industries Pte LTD, SingaporeGoogle Scholar
  45. Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  46. Jones KMM, Fitzgerald DG, Sale PF (2002) Comparative ecology of marine fish communities. In: Handbook of Fish Biology and Fisheries. Wiley Online Library, pp 341–358Google Scholar
  47. Jordaan A, Crocker J, Chen Y (2011) Linkages among physical and biological properties in tidepools on the Maine coast. Environ Biol Fish 92:13–23. doi: 10.1007/s10641-011-9812-4 CrossRefGoogle Scholar
  48. Kolasa J, Manne LL, Pandit SN (2012) Species-area relationships arise from interaction of habitat heterogeneity and species pool. Hydrobiologia 685:135–144. doi: 10.1007/s10750-011-0846-6 CrossRefGoogle Scholar
  49. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. doi: 10.1890/08-2244.1 CrossRefPubMedGoogle Scholar
  50. Leitão RP, Zuanon J, Villéger S et al (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proc R Soc B Biol Sci 283:1–9. doi: 10.1098/rspb.2016.0084 CrossRefGoogle Scholar
  51. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257. doi: 10.1038/nature08251 CrossRefPubMedGoogle Scholar
  52. Lobato CMC, Soares BE, Begot TOR, Montag LFA (2016) Tidal pools as habitat for juveniles of the goliath grouper Epinephelus Itajara (Lichtenstein 1822) in the Amazonian coastal zone, Brazil. Nat Conserv 14:20–23. doi: 10.1016/j.ncon.2015.12.001 CrossRefGoogle Scholar
  53. Lucrezi S, van der Walt MF (2016) Beachgoers’ perceptions of sandy beach conditions: demographic and attitudinal influences, and the implications for beach ecosystem management. J Coast Conserv 20:81–96. doi: 10.1007/s11852-015-0419-3 CrossRefGoogle Scholar
  54. Machado FS, Macieira RM, Zuluaga Gómez MA et al (2015) Checklist of tidepool fishes from Jericoacoara National Park, southwestern Atlantic, with additional ecological information. Biota Neotrop 15:1–9. doi: 10.1590/1676-06032015011114 CrossRefGoogle Scholar
  55. Macieira RM, Joyeux JC (2011) Distribution patterns of tidepool fishes on a tropical flat reef. Fish Bull 109:305–315Google Scholar
  56. Macieira RM, Simon T, Pimentel CR, Joyeux JC (2014) Isolation and speciation of tidepool fishes as a consequence of Quaternary Sea-level fluctuations. Environ Biol Fish 98:385–393. doi: 10.1007/s10641-014-0269-0 CrossRefGoogle Scholar
  57. Martin KL (1995) Time and tide wait for no fish: intertidal fishes out of water. Environ Biol Fish 44:165–181. doi: 10.1007/BF00005914 CrossRefGoogle Scholar
  58. Menezes NA, Buckup PA, Figueiredo JL, Moura RL (2003) Catálogo das Espécies de Peixes Marinhos do Brasil. Museu de Zoologia USP, São PauloGoogle Scholar
  59. Messmer V, Jones G, Munday P, Holbrook S (2011) Habitat biodiversity as a determinant of fish community structure on coral reefs. Ecology 92:2285–2298CrossRefPubMedGoogle Scholar
  60. Metcalfe K, Vaz S, Engelhard GH et al (2015) Evaluating conservation and fisheries management strategies by linking spatial prioritization software and ecosystem and fisheries modelling tools. J Appl Ecol 52:665–674. doi: 10.1111/1365-2664.12404 CrossRefGoogle Scholar
  61. Methratta ET (2004) Top-down and bottom-up factors in tidepool communities. J Exp Mar Bio Ecol 299:77–96. doi: 10.1016/j.jembe.2003.09.004 CrossRefGoogle Scholar
  62. Mittelbach GG, Schemske DW (2015) Ecological and evolutionary perspectives on community assembly. Trends Ecol Evol 30:241–247. doi: 10.1016/j.tree.2015.02.008 CrossRefPubMedGoogle Scholar
  63. Mora C, Chittaro PM, Sale PF et al (2003) Patterns and processes in reef fish diversity. Nature 421:933–936. doi: 10.1038/nature01421.1 CrossRefPubMedGoogle Scholar
  64. Moring JR (1986) Seasonal presence of tidepool fish species in a rocky intertidal zone of northern California, USA. Hydrobiologia 134:21–27. doi: 10.1007/BF00008696 CrossRefGoogle Scholar
  65. Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876. doi: 10.1111/j.1365-2435.2010.01695.x CrossRefGoogle Scholar
  66. Nelson JS (2006) Fishes of the world, 4th edn. John Wiley & Sons, Hoboken (New Jersey)Google Scholar
  67. Oksanen J, Blanchet FG, Kindt R, et al. (2015) vegan: Community Ecology Package.Google Scholar
  68. Oliveira RRS, Macieira RM, Giarrizzo T (2016) Ontogenetic shifts in fishes between vegetated and unvegetated tidepools: assessing the effect of physical structure on fish habitat selection. J Fish Biol 89:959–976. doi: 10.1111/jfb.13013 CrossRefPubMedGoogle Scholar
  69. Pereira PHC, Moraes RL, dos Santos MVB et al (2014) The influence of multiple factors upon reef fish abundance and species richness in a tropical coral complex. Ichthyol Res 61:375–384. doi: 10.1007/s10228-014-0409-8 CrossRefGoogle Scholar
  70. Pinheiro J, Bates D, DebRoy S, et al. (2013) nlme: Linear and Nonlinear Mixed Effects Models. R Packag. version 3.1–113 R package:1–86.Google Scholar
  71. Pool TK, Cucherousset J, Boulêtreau S et al (2016) Increased taxonomic and functional similarity does not increase the trophic similarity of communities. Glob Ecol Biogeogr 25:46–54. doi: 10.1111/geb.12384 CrossRefGoogle Scholar
  72. Pusack TJ, Benkwitt CE, Cure K, Kindinger TL (2016) Invasive red lionfish (Pterois volitans) grow faster in the Atlantic Ocean than in their native Pacific range. Environ Biol Fish 99:571–579. doi: 10.1007/s10641-016-0499-4 CrossRefGoogle Scholar
  73. R Core Team (2015) R: A Language and Environment for Statistical Computing.Google Scholar
  74. Rangel CA, Chaves LCT, Monteiro-Neto C (2007) Baseline assessment of the reef fish assemblage from Cagarras archipelago, Rio de Janeiro, southeastern Brazil. Brazilian J Oceanogr 55:7–17. doi: 10.1590/S1679-87592007000100002 CrossRefGoogle Scholar
  75. Ritter AF (2008) Habitat variation influences movement rates and population structure of an intertidal fish. Oecologia 157:429–439. doi: 10.1007/s00442-008-1086-y CrossRefPubMedGoogle Scholar
  76. Rosindell J, Hubbell SP, Etienne RS (2011) The unified neutral theory of biodiversity and biogeography at age ten. Trends Ecol Evol 26:340–348. doi: 10.1016/j.tree.2011.03.024 CrossRefPubMedGoogle Scholar
  77. Sabino J (1999) Comportamento de peixes em riachos: métodos de estudo para uma abordagem naturalística. Oecologia Aust 6:183–208. doi: 10.4257/oeco.1999.0601.06 CrossRefGoogle Scholar
  78. Sale PF (1980) Assemblages of fish on patch reefs - predictable or unpredictable? Environ Biol Fish 5:243–249. doi: 10.1007/BF00005358 CrossRefGoogle Scholar
  79. Shanksa AL, Pfisterb CA (2009) Annual recruitment of three species of tide-pool fishes is driven by variation in springtime coastal hydrodynamics. Limnol Oceanogr 54:1481–1487. doi: 10.4319/lo.2009.54.5.1481 CrossRefGoogle Scholar
  80. Shulman MJ (1985) Variability in recruitment of coral reef fishes. J Exp Mar Bio Ecol 89:205–219. doi: 10.1016/0022-0981(85)90127-3 CrossRefGoogle Scholar
  81. Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) Sparse data necessitate explicit treatment of Beta-diversity: a reply to bush et al. Trends Ecol Evol 31:338–339. doi: 10.1016/j.tree.2016.02.019 CrossRefPubMedGoogle Scholar
  82. Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. doi: 10.1890/07-1206.1 CrossRefPubMedGoogle Scholar
  83. Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522. doi: 10.1890/09-1310.1 CrossRefPubMedGoogle Scholar
  84. Vitule JRS, Costa, APLda, Frehse FA, et al. (2016) Comments on “Fish biodiversity and conservation in South America by Reis et al. (2016)”. J Fish Biol. doi: 10.1111/jfb.13239
  85. Watson JL, Huntington BE (2016) Assessing the performance of a cost-effective video lander for estimating relative abundance and diversity of nearshore fish assemblages. J Exp Mar Bio Ecol 483:104–111. doi: 10.1016/j.jembe.2016.07.007 CrossRefGoogle Scholar
  86. White GE, Brown C (2013) Site fidelity and homing behaviour in intertidal fishes. Mar Biol 160:1365–1372. doi: 10.1007/s00227-013-2188-6 CrossRefGoogle Scholar
  87. Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338. doi: 10.2307/1943563 CrossRefGoogle Scholar
  88. Witman JD, Lamb RW, Byrnes JEK (2015) Towards an integration of scale and complexity in marine ecology. Ecol Monogr 85:475–504. doi: 10.1890/14-2265.1 CrossRefGoogle Scholar
  89. Zuur AF, Ieno EN, Walker NJ, et al. (2009) Mixed Effects Models and Extensions in Ecology with R.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Luis Artur Valões Bezerra
    • 1
    Email author
  • André Andrian Padial
    • 1
  • Filipe Brasil Mariano
    • 2
    • 3
  • Danielle Sequeira Garcez
    • 2
    • 4
  • Jorge Iván Sánchez-Botero
    • 2
    • 4
  1. 1.Laboratório de Análise e Síntese em Biodiversidade, Programa de Pós-Graduação em Ecologia e ConservaçãoUniversidade Federal do Paraná (UFPR)CuritibaBrazil
  2. 2.Laboratório de Ecologia Pesqueira, Instituto de Ciências do Mar – LabomarUniversidade Federal do CearáFortalezaBrazil
  3. 3.Laboratório de Ecologia Aquática, Departamento de BiologiaUniversidade Federal do CearáFortalezaBrazil
  4. 4.Programa de Pós-Graduação em Ciências Marinhas Tropicais, Instituto de Ciências do Mar – LabomarUniversidade Federal do CearáFortalezaBrazil

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