Advertisement

Environmental Biology of Fishes

, Volume 101, Issue 10, pp 1427–1442 | Cite as

Are vegetated areas more attractive for juvenile fish in estuaries? A comparison in a tropical estuary

  • Rayssa Soares da Silva
  • Alexandra Sofia Baptista Vicente Baeta
  • André Luiz Machado PessanhaEmail author
Article

Abstract

Seagrass beds are some of the essential nursery areas for fish, due to the great structural complexity found in these environments. Despite their importance, they are among the most threatened coastal ecosystems and their influence on fish assemblages is still poorly studied. Therefore, this study aimed to compare the composition and structure of fish assemblages found in vegetated and unvegetated areas in a tropical estuary. Samples were taken in two areas with seagrass (Halodule wrightii) and two where this vegetation is absent (tidal flats), observing variations in the hydrological regime between the dry and rainy seasons of 2014. A total of 86 species were recorded, of which 11 occurred only in vegetated areas and 31 only in the unvegetated regions. No difference was found in diversity between vegetated and unvegetated areas, but the values of abundance and biomass were higher in unvegetated areas. Thus, the environmental characteristic of unvegetated areas proved to be a major factor in determining the biomass and richness patterns. Analysis of the abiotic data set indicated that temperature and dissolved oxygen are the variables that act as environmental filters in the temporal differentiation of the structure of fish assemblages, while salinity and total dissolved solids are related to variation between seagrass beds and tidal flats. In addition, our results show that these areas are used by the species in different stages of their ontogenetic development, which may be linked to differences related to the availability of food resources and the possibility of refuge from predation.

Keywords

Seagrass Nursery Ontogenetic habitat shift Juvenile fish Estuary 

References

  1. Adams AJ, Locascio JV, Robbins BD (2004) Microhabitat use by a post-settlement stage estuarine fish: evidence from relative abundance and predation among habitats. J Exp Mar Biol Ecol 299:17–33.  https://doi.org/10.1016/j.jembe.2003.08.013 CrossRefGoogle Scholar
  2. Adams AJ, Dahlgren CP, Kellison GT et al (2006) Nursery function of tropical back-reef systems. Mar Ecol Prog Ser 318:287–301.  https://doi.org/10.3354/meps318287 CrossRefGoogle Scholar
  3. AESA – Agência Executiva de Gestão das Águas do Estado da Paraíba (2015) Climatologia da precipitação anual acumulada (mm) – ano 2010. http://site2.aesa.pb.gov.br/aesa/jsp/monitoramento/chuvas/climatologiasGraficos.jsp. Acesso 09 junho 2014
  4. Alvares CA, Stape JL, Sentelhas PC et al (2013) Köppen’s climate classification map of Brazil. Meteorol Z 22:711–728.  https://doi.org/10.1127/0941-2948/2013/0507 CrossRefGoogle Scholar
  5. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  6. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER–E Ltd., Plymouth, United KingdomGoogle Scholar
  7. Ara R, Arshad A, Musa L, Amin SMN, Kuppan P (2011) Feeding habits of larval fishes of the family Clupeidae (Actinopterygii: Clupeiformes) in the estuary of river pendas, Johor, Malaysia. J Fish Aquat Sci 6:816–821.  https://doi.org/10.3923/jfas.2011.816.821 CrossRefGoogle Scholar
  8. Araújo M.E., Teixeira J.M.C., Oliveira A.M.E. (2004) Peixes estuarinos marinhos do Nordeste brasileiro, Guia ilustrado. - Fortaleza, Edições UFC, 260 pGoogle Scholar
  9. Arrivillaga A, Blatz DM (1999) Comparision of fishes and macroinveretebrates on seagrass and bare-sand sites on Guatemala’s Atlantic coast. Bull Mar Sci 65:301–319Google Scholar
  10. Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser 206:45–58.  https://doi.org/10.3354/meps206045 CrossRefGoogle Scholar
  11. Bell JD, Pollard DA (1989) Ecology of fish assemblages and fisheries associated with seagrasses. In: McComb AJ, Larkum AWD, Shepherd SA (eds) The biology of seagrasses: an Australian perspective. Elsevier, Amsterdam, pp 565–609Google Scholar
  12. Bell JD, Westoby M (1986) Abundance of macrofauna in dense seagrass is due to habitat preference, not predation. Oecologia 68:205–209CrossRefPubMedGoogle Scholar
  13. Bertelli CM, Unsworth RKF (2014) Protecting the hand that feeds us: seagrass (Zostera marina) serves as commercial juvenile fish habitat. Mar Pollut Bull 83:425–429.  https://doi.org/10.1016/j.marpolbul.2013.08.011 CrossRefPubMedGoogle Scholar
  14. Brown A.C., McLachlan A. (1990) Ecology of sandy shores. Elsevier, Amsterdam. 328pGoogle Scholar
  15. Burfeind DD, Tibbetts IR, Udy JW (2009) Habitat preference of three common fishes for seagrass, Caulerpa taxifolia, and unvegetated substrate in Moreton Bay, Australia. Environ Biol Fish 84:317–322.  https://doi.org/10.1007/s10641-009-9444-0 CrossRefGoogle Scholar
  16. Camargo M, Isaac VJ (2003) Ictiofauna estuarina. In: Fernandes MFB (ed) Os manguezais da costa Norte brasileira, vol 1. Fundação Rio Bacanga, São Luís, pp 105–132Google Scholar
  17. Campos DMAR, Silva AF, Sales NS et al (2015) Trophic relationships among fish assemblages in a mudflat within Brazilian marine protected area. Braz J Oceanogr 63:135–146.  https://doi.org/10.1590/S1679-87592015091306302 CrossRefGoogle Scholar
  18. Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, PlymouthGoogle Scholar
  19. Connolly RM (1994) A comparison of fish assemblage from seagrass and unvegetated areas of a southern Australian estuary. Aust J Mar Freshwat Res 45:1033–1044CrossRefGoogle Scholar
  20. Contente RF, Stefanoni MF, Spach HL (2011) Feeding ecology of the Brazilian silverside Atherinella brasiliensis (Atherinopsidae) in a sub-tropical estuarine ecosystem. J Mar Biol Assoc UK 91:1197–1205.  https://doi.org/10.1017/S0025315410001116 CrossRefGoogle Scholar
  21. Contente RF, Stefanoni MF, Spach HL (2012) Feeding ecology of the American freshwater goby Ctenogobius shufeldti (Gobiidae, Perciformes) in a sub-tropical estuary. J Fish Biol 80:2357–2373.  https://doi.org/10.1111/j.1095-8649.2012.03300.x CrossRefPubMedGoogle Scholar
  22. Cullen-Unsworth L, Unsworth R (2013) Seagrass meadows, ecosystem services, and sustainability. Environment: Science and policy for sustainable development 55:14–28.  https://doi.org/10.1080/00139157.2013.785864 CrossRefGoogle Scholar
  23. De Angelo JA, Stevens PW, Blewett DA, Switzer TS (2014) Fish assemblages of shoal- and shoreline-associated seagrass beds in eastern Gulf of Mexico estuaries. Trans Am Fish Soc 143:1037–1048.  https://doi.org/10.1080/00028487.2014.911209 CrossRefGoogle Scholar
  24. Dorenbosh M, van Riel MC, Nagelkerken I, van der Velde G (2004) The relationship of reef fish densities to the proximity of mangrove and seagrass nurseries. Estuar Coast Shelf Sci 60:37–48.  https://doi.org/10.1016/j.ecss.2003.11.018 CrossRefGoogle Scholar
  25. Dyer KR, Christie MC, Wright EW (2000) The classification of intertidal mudflats. Cont Shelf Res 20:1039–1060CrossRefGoogle Scholar
  26. Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia. III. General relationships between sediments, seagrasses, invertebrates and fishes. J Exp Mar Biol Ecol 194:107–131CrossRefGoogle Scholar
  27. Elliott M, McLusky DS (2002) The need for definitions in understanding estuaries. Estuar Coast Shelf Sci 55:815–827CrossRefGoogle Scholar
  28. Elliott M, Nedwell S, Jones NV et al (1998) Intertidal sand and mudflats & subtidal mobile sandbanks: an overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project)Google Scholar
  29. Figueiredo J.L., Menezes N.A. (1978) Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo, Museu de Zoologia da Universidade de São PauloGoogle Scholar
  30. Figueiredo J.L., Menezes N.A. (1980) Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São PauloGoogle Scholar
  31. Figueiredo J.L., Menezes N.A. (2000) Manual de peixes marinhos do sudeste do Brasil. VI. Teleostei (5). São Paulo, Museu de Zoologia da Universidade de São PauloGoogle Scholar
  32. Fukami T (2010) Community assembly dynamics in space. In: Verhoef HA, Morin PJ (eds) Community ecology: process, models, and applications. Oxford University Press, Oxford, pp 45–54Google Scholar
  33. Godefroid RS, Santos C, Hofstaetter M, Spach HL (2001) Ocurrence of larvae and juveniles of Eucinostomus argenteus, Eucinostomus gula, Menticirrhus americanus, Menticirrhus littoralis, Umbrina coroides and Micropogonias furnieri at Pontal do Sul beach, Paraná. Braz Arch Biol Technol 44:411–418.  https://doi.org/10.1590/S1516-89132001000400012 CrossRefGoogle Scholar
  34. Gray CA, Chick RC, McElligott DJ (1998) Diel changes in assemblages of fishes associated with shallow seagrass and bare sand. Estuar Coast Shelf Sci 46:849–859CrossRefGoogle Scholar
  35. Griffin JN, Jenkins SR, Gamfeldt L et al (2009) Spatial heterogeneity increases the importance of species richness for an ecosystem process. Oikos 118:1335–1342.  https://doi.org/10.1111/j.1600-0706.2009.17572.x CrossRefGoogle Scholar
  36. Guevara E, Sánchez AJ, Rosas C et al (2007) Asociación trófica de peces distribuído en vegetación acuática submergida en Laguna de Términos, sur del Golfo de México. Universidad y Ciencia 23:151–166Google Scholar
  37. Heck KL Jr, Hays G, Orth RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–136.  https://doi.org/10.3354/meps253123 CrossRefGoogle Scholar
  38. Horinouchi M (2005) A comparison of fish assemblages from seagrass beds and the adjacent bare substrata in Lake Hamana, Central Japan. Laguna 12:69–72Google Scholar
  39. Horinouchi M, Sano M (2000) Food habits of fishes in a Zostera marina bed at Aburatsubo, Central Japan. Ichthyol Res 47:163–173.  https://doi.org/10.1007/BF02684237 CrossRefGoogle Scholar
  40. Horinouchi M, Tongnunui P, Furumitsu K et al (2012) Food habits of small fishes in seagrass habitats in Trang, southern Thailand. Fish Sci 78:577–587.  https://doi.org/10.1007/s12562-012-0485-5 CrossRefGoogle Scholar
  41. Irlandi EA, Crawford MK (1997) Habitat linkages: the effect of intertidal saltmarshes and adjacent subtidal habitats on abundance, movement, and growth of an estuarine fish. Oecologia 110:222–230CrossRefPubMedGoogle Scholar
  42. Jaxion-Harm J, Saunders J, Speight MR (2012) Distribution of fish in seagrass, mangroves and coral reefs: life-stage dependente habitat use in Honduras. Rev Biol Trop 60:683–698CrossRefPubMedGoogle Scholar
  43. Jenkins GP, Hamer PA (2001) Spatial variation in the use of seagrass and unvegetated habitats by post-settlement king George whiting (Percoidei: Sillaginidae) in relation to meiofaunal distribution and macrophyte structure. Mar Ecol Prog Ser 224:219–229.  https://doi.org/10.3354/meps224219 CrossRefGoogle Scholar
  44. Jenkins GP, Wheatley MJ (1998) The influence of habitat structure on nearshore fish assemblages in a southern Australian embayment: comparison of shallow seagrass, reef-algal and unvegetated sand habitats, with emphasis on their importance to recruitment. J Exp Mar Biol Ecol 221:147–172.  https://doi.org/10.1016/S0022-0981(97)00121-4 CrossRefGoogle Scholar
  45. Jernakoff P, Brearley A, Nielsen J (1996) Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceanogr Mar Biol 34:109–162Google Scholar
  46. Kerschner BA, Peterson MS, Gilmore, RG (1985) Ecotopic and ontogenetic trophic variation in mojarras (Pisces: Gerreidae). Estuaries 8(3):311–322Google Scholar
  47. Kimirei IA, Nagelkerken I, Griffioen B et al (2011) Ontogenetic habitat use by mangrove/seagrass-associated coral reef fishes shows flexibility in time and space. Estuar Coast Shelf S 92:47–58.  https://doi.org/10.1016/j.ecss.2010.12.016 CrossRefGoogle Scholar
  48. Laborel-Deguen F (1963) Nota preliminar sobre a ecologia das pradarias das fanerógamas marinhas nas costas dos Estados de Pernambuco e da Paraíba. Trabalhos do Instituto de Biologia Marítima e Oceanografia 3(4):39–50Google Scholar
  49. Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257:229–253CrossRefPubMedGoogle Scholar
  50. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24CrossRefGoogle Scholar
  51. Lubbers L, Boynton WR, Kemp WM (1990) Variations in structure of estuarine fish communities in relation to abundance of submersed vascular plants. Mar Ecol Prog Ser 65:1–14CrossRefGoogle Scholar
  52. Magalhães KM, Borges JCG, Pitanga ME (2015) Halophila baillonis Ascherson: first population dynamics data for the southern hemisphere. An Acad Bras Cienc 87:861–865CrossRefPubMedGoogle Scholar
  53. Magurran AE (2004) Measuring biological diversity. Blackwell Science, OxfordGoogle Scholar
  54. Magurran AE, Khachonpisitsak S, Ahmad AB (2011) Biological diversity of fish communities: pattern and process. J Fish Biol 79:1393–1412CrossRefPubMedGoogle Scholar
  55. Matias MG, Underwood AJ, Hochuli DF, Coleman RA (2010) Independent effects of patch size and structural complexity on diversity of benthic macroinvertebrates. Ecology 91:1908–1915.  https://doi.org/10.1890/09-1083.1 CrossRefPubMedGoogle Scholar
  56. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community dada: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  57. Menezes N.A., Figueiredo J.L. (1980) Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São PauloGoogle Scholar
  58. Menezes N.A., Figueiredo J.L. (1985) Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São PauloGoogle Scholar
  59. Micheli F, Peterson CH (1999) Estuarine vegetated habitats as corridors for predator movements. Conserv Biol 13:869–881CrossRefGoogle Scholar
  60. Nakamura Y, Horinouchi M, Nakai T, Sano M (2003) Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyol Res 50:15–22.  https://doi.org/10.1007/s102280300002 CrossRefGoogle Scholar
  61. Nakamura Y, Kawasaki H, Sano M (2007) Experimental analysis of recruitment patterns of coral reef fishes in seagrass beds: effects of substrate type, shape, and rigidity. Estuar Coast Shelf Sci 71:559–568.  https://doi.org/10.1016/j.ecss.2006.09.005 CrossRefGoogle Scholar
  62. Nelson JS (2006) Fishes of the world. 4th edition. John Wiley & Sons, Inc, New Jersey. 601pGoogle Scholar
  63. Nobrega RRA, Nishida AK (2003) Aspectos socioeconômicos e percepção ambiental dos catadores de caranguejo-uçá Ucides cordatus cordatus (L. 1763) (Decapoda, Brachyura) do estuário do Rio Mamanguape, Nordeste do Brasil. Interciência 28:36–43Google Scholar
  64. Oliveira REMCC, Pessanha ALM (2014) Fish assemblage along a morphodynamic continuum onthree tropical beaches. Neotrop Ichthyol 12:165–175.  https://doi.org/10.1590/S1679-62252014000100018
  65. Orth RJ, Heck KL Jr, van Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7:339–350CrossRefGoogle Scholar
  66. Pessanha ALM, Araújo FG (2003) Spatial, temporal and diel variation of fish assemblages at two sandy beaches in the Sepetiba Bay, Rio de Janeiro, Brazil. Estuar Coast Shelf Sci 57:817–828.  https://doi.org/10.1016/S0272-7714(02)00411-0 CrossRefGoogle Scholar
  67. Potter IC, Beckley LE, Whitfield AK, Lenanton RCJ (1990) Comparisons between the roles played by estuaries in the life cycles of fishes in temperate Western Australia and southern Africa. Environ Biol Fish 28:143–178CrossRefGoogle Scholar
  68. Rozas LP, Minello TJ (1997) Estimating densities of small fishes and decapod crustaceans in shallow estuarine habitats: a review of sampling design with focus on gear selection. Estuaries 20:199–213CrossRefGoogle Scholar
  69. Rozas LP, Zimmerman RJ (2000) Small-scale patterns of nekton use among marsh and adjacent shallow nonvegetated areas of the Galveston Bay estuary, Texas (USA). Mar Ecol Prog Ser 193:217–239.  https://doi.org/10.3354/meps193217 CrossRefGoogle Scholar
  70. Ruiz GM, Hines AH, Posey MH (1993) Shallow water as a refuge habitat for fish and crustaceans in unvegetated estuaries: an example from Chesapeake Bay. Mar Ecol Prog Ser 99:1–16CrossRefGoogle Scholar
  71. Scharf FS, Manderson JP, Fabrizio MC (2006) The effects of seafloor habitat complexity on survival of juvenile fishes: species-specific interactions with structural refuge. J Exp Mar Biol Ecol 335:167–176.  https://doi.org/10.1016/j.jembe.2006.03.018 CrossRefGoogle Scholar
  72. Silva MA, Araújo FG, Azevedo MCC, Mendoça P (2003) Distribuição espacial e temporal de Cetengraulis edentulus (Cuvier) (Actinopterygii, Engraulidae) na Baía de Sepetiba, Rio de Janeiro, Brasil. Rev Bras Zool 20:577–581CrossRefGoogle Scholar
  73. Silva KG, Paludo D, Oliveira EMA, Lima RP, Soavinski RJ (2011) Distribution and occurrence of manatee (Trichechus manatus) in the Mamanguape River estuary, Paraíba, Brazil. Nat Resour 1:5–14Google Scholar
  74. Smith KA, Sinerchia M (2004) Timing of recruitment events, residence periods and post-settlement growth of juvenile fish in a seagrass nursery area, South-Eastern Australia. Environ Biol Fish 71:73–84.  https://doi.org/10.1023/B:EBFI.0000043154.96933.de CrossRefGoogle Scholar
  75. Sogard SM (1989) Variability in growth rates of juvenile fishes in different estuarine habitats. Mar Ecol Prog Ser 85:35–53CrossRefGoogle Scholar
  76. Triola MF (2005) Introdução à estatística. 9. ed. LTC, Rio de JaneiroGoogle Scholar
  77. Unsworth RKF, Bell JJ, Smith DJ (2007) Tidal fish connectivity of reef and sea grass habitats in the indo-Pacific. J Mar Biol Assoc UK 87:1287–1296.  https://doi.org/10.1017/S002531540705638X CrossRefGoogle Scholar
  78. Watt-Pringle P, Strydom NA (2003) Habitat use by larval fishes in a temperate south African surf zone. Estuar Coast Shelf Sci 58:765:774–765:774.  https://doi.org/10.1016/S0272-7714(03)00183-5 CrossRefGoogle Scholar
  79. Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69:1352–1366.  https://doi.org/10.2307/1941633 CrossRefGoogle Scholar
  80. Wetzel RG, Linkens GE (1991) Limnological analysis. 2ed. Springer Verlag, New YorkGoogle Scholar
  81. Wuenschel MJ, Jugovich AR, Hare JA (2005) Metabolic response of juvenile gray snapper (Lutjanus griseus) to temperature and salinity: physiological cost of different environments. J Exp Mar Biol Ecol 321:145–154CrossRefGoogle Scholar
  82. Wyda JC, Deegan LA, Hughes JE, Weaver MJ (2002) The response of fishes to submerged aquatic vegetation complexity in two ecoregions of the mid-Atlantic bight: Buzzards Bay and Chesapeake Bay. Estuaries 25:86–100.  https://doi.org/10.1007/BF02696052 CrossRefGoogle Scholar
  83. Xavier JHA, Cordeiro CAMM, Tenório GD et al (2012) Fish assemblage of the Mamanguape environmental protection area, NE Brazil: abundance, composition and micro-habitat availability along the mangrove-reef gradient. Neotrop Ichthyol 10:109–122CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Ecologia e Conservação (PPGEC)Universidade Estadual da Paraíba (UEPB)ParaíbaBrazil
  2. 2.Marine and Environmental Sciences Centre (MARE), Faculty of Sciences and TechnologyUniversity of CoimbraCoimbraPortugal

Personalised recommendations