Environmental Biology of Fishes

, Volume 98, Issue 3, pp 891–904 | Cite as

Influence of temporal and spatial factors on abundance and richness of fish early stages in shallow tropical estuaries

  • Wendi Arévalo-Frías
  • Manuel Mendoza-Carranza


Accurate determination of abundance and richness of fish early stages in estuarine zones is critical to support management and protection plans; it is therefore necessary to consider all influential factors. Habitat diversity, seasonality, moon phase and diel variations, and their interactions are factors that can affect richness and abundance estimations. Appropriate spatial and temporal scales in sampling design are important to understand the assemblage dynamics of fish early stages. The objective of this research is to test how temporal and spatial scales influence the determination of abundance and richness of fish early stages based on a hierarchical sampling design considering season (dry and rainy), moon phase (new, crescent, full, and waning), day period (sunrise, midday, sunset, and night), habitat (coastal, riverine, mangrove, and Vallisneria americana beds), and their interactions. Samples were collected using a conical zooplankton net and towed horizontally for 5 min at a depth of 50 cm. A variance component analyses model showed that day period, season, and their interactions were the main factors determining variations in fish early stage abundances and richness (26.68, 10.78, and 12.82 %, respectively). The highest abundance and richness occurred at night, with significant seasonal variations related to the runoff from the Grijalva-Usumacinta basin. Abundance and richness were higher in the dry season, which were related to higher dissolved oxygen and water transparency. Presented findings can be generalized to tropical and subtropical estuaries with shallow waters.


Variance components Diel variation Moon phase Larvae Tropical estuary 



We thank those who helped us carry out the sampling: Juan Juárez, José Gaspar Calam, and Sofia Santiago, and fishermen who helped with the sampling survey: Benjamín Martínez and Gustavo Salvador. We thank Alejandro Espinoza, Juan Carlos Pérez, and Ana Laura Ibañez for early revisions of this document and for the anonymous reviewers that helped us improve this article. The second author is grateful to CONACYT for a grant that funded a sabbatical stay at the Wageningen University where this paper was finished. Thanks to the aquaculture and fisheries research group at Wageningen University for ongoing support. This project was partially financed by the International Foundation for Science and CONACYT-ECOSUR.


  1. Able KW, Grothues TM, Rowe PM, Wuenschel MJ, Vasslides JM (2011) Near-surface larval and juvenile fish in coastal habitats: comparisons between the inner shelf and an estuary in the New York Bight during summer and fall. Estuar Coasts 34(4):726–738CrossRefGoogle Scholar
  2. Álvarez CJ, Flores-Coto C (1981) Clave para indentificación de familias de larvas de peces de la laguna de Términos, Campeche, México. An cienc Mar Limnol 1:199–208Google Scholar
  3. Anderson MJ et al (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14(1):19–28PubMedCrossRefGoogle Scholar
  4. Araujo-Lima C, Silva VV, Petry P, Oliveira EC, Moura SML (2001) Diel variation of larval fish abundance in the amazon and Rio Negro. Braz J Biol 61(3):357–362PubMedCrossRefGoogle Scholar
  5. Arévalo-Frías W, Mendoza-Carranza M (2012) Larvas y juveniles de peces en ambientes estuarinos de la Reserva de la Biosfera Pantanos de Centla y su zona costera adyacente. In: Sánchez A, Chiappa-Carrara X, Pérez B (eds) Recursos Acuáticos Costeros del Sureste: Tendencias actuales en investigación y estado del arte. vol 2. RECORECOS, CONCYTEY, UNACAR, UJAT, ECOSUR, UNAM, México, D.F., p 242–269Google Scholar
  6. Bacheler NM, Neal JW, Noble RL (2004) Reproduction of a landlocked diadromous fish population: bigmouth sleepers Gobiomorus dormitor in a reservoir in Puerto Rico. Caribb J Sci 40(2):223–231Google Scholar
  7. Baptista J, Martinho F, Dolbeth M, Viegas I, Cabral H, Pardal M (2010) Effects of freshwater flow on the fish assemblage of the Mondego estuary (Portugal): comparison between drought and non-drought years. Mar Freshw Res 61(4):490–501CrossRefGoogle Scholar
  8. Barletta M, Barletta-Bergan A (2009) Endogenous activity rhythms of larval fish assemblages in a mangrove-fringed estuary in North Brazil. Open Fish Sci J 2:15–24CrossRefGoogle Scholar
  9. Beck MW et al (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51:633–641CrossRefGoogle Scholar
  10. Beck MW et al (2003) The role of nearshore ecosystems as fish and shellfish nurseries. Issues Ecol 11:1–12Google Scholar
  11. Becker A, Coppinger C, Whitfield AK (2012) Influence of tides on assemblages and behaviour of fishes associated with shallow seagrass edges and bare sand. Mar Ecol Prog Ser 456:187–199CrossRefGoogle Scholar
  12. Breheny NB, Beckley LE, Wakefield CB (2012) Ichthyoplankton assemblages associated with pink snapper (Pagrus auratus) spawning aggregations in coastal embayments of southwestern Australia. J R Soc West Aust 95:103–114Google Scholar
  13. Capps KA et al (2011) Salinity tolerance of non-native suckermouth armoured catfish (Loricariidae: Pterygoplichthys) in south-eastern Mexico: implications for invasion and dispersal. Aquat Conserv Mar Freshwat Ecosyst 21(6):528–540CrossRefGoogle Scholar
  14. Castro LR et al (2011) Short-term variations in mesozooplankton, ichthyoplankton, and nutrients associated with semi-diurnal tides in a patagonian Gulf. Cont Shelf Res 31(3):282–292CrossRefGoogle Scholar
  15. Chew L-L, Chong VC (2011) Copepod community structure and abundance in a tropical mangrove estuary, with comparisons to coastal waters. Hydrobiologia 666(1):127–143CrossRefGoogle Scholar
  16. Chícharo L, Faria A, Morais P, Amaral A, Mendes C, Chícharo MA (2009) How to sample larval fish for taxonomical and ecophysiological studies in shallower temperate coastal ecosystems? Cah Biol Mar 50(4):311Google Scholar
  17. Colton A, Hurst T (2010) Behavioral responses to light gradients, olfactory cues, and prey in larvae of two North Pacific gadids (Gadus macrocephalus and Theragra chalcogramma). Environ Biol Fishes 88(1):39–49. doi: 10.1007/s10641-010-9616-y CrossRefGoogle Scholar
  18. da Costa AJG, da Costa KG, Pereira LCC, Sampaio MI, da Costa RM (2011) Dynamics of hydrological variables and the fish larva community in an Amazonian estuary of northern Brazil. J Coast Res:1960–1964Google Scholar
  19. da Silva PA, Reynalte-Tataje DA, Zaniboni-Filho E (2012) Identification of fish nursery areas in a free tributary of an impoundment region, upper Uruguay River, Brazil. Neotropical Ichthyol 10(2):425–438CrossRefGoogle Scholar
  20. Dai M et al (2006) Oxygen depletion in the upper reach of the Pearl River estuary during a winter drought. Mar Chem 102(1):159–169CrossRefGoogle Scholar
  21. D’Alessandro EK, Sponaugle S, Serafy JE (2010) Larval ecology of a suite of snappers (family: Lutjanidae) in the Straits of Florida, western Atlantic Ocean. Mar Ecol Prog Ser 410:159–175CrossRefGoogle Scholar
  22. Day JW, Kemp WM, Yáñez-Arancibia A, Crump BC (2012) Estuarine ecology. Wiley, New YorkCrossRefGoogle Scholar
  23. Instituto Nacional de Ecología (2000) Programa de Manejo, Reserva de la Biósfera Pantanos de Centla. Secretaria de medio ambiente recursos naturales y pesca, México, DFGoogle Scholar
  24. DiBacco C, Sutton D, McConnico L (2001) Vertical migration behavior and horizontal distribution of brachyuran larvae in a low-inflow estuary: implications for bay-ocean exchange. Mar Ecol Prog Ser 217:191–206CrossRefGoogle Scholar
  25. Drolet D, Kennedy K, Barbeau MA (2013) Winter population dynamics and survival strategies of the intertidal mudflat amphipod Corophium volutator (Pallas). J Exp Mar Biol Ecol 441:126–137CrossRefGoogle Scholar
  26. Elliott M, McLusky DS (2002) The need for definitions in understanding estuaries. Estuar Coast Shelf Sci 55(6):815–827CrossRefGoogle Scholar
  27. Fahay MP (2007) Early stages of fishes in the Western North Atlantic Ocean (Davis Strait, Southern Greenland and Flemish Cap to Cape Hatteras) Two volume set. Northwestern Atlantic Fisheries Organization, DartmouthGoogle Scholar
  28. Flores-Coto C, Méndez-Vargas D (1982) Contribución al conocimiento del ictioplancton de la Laguna de Alvarado, Veracruz. An Inst Cienc Mar Limnol Univ Nac Auton Mex 9:141–160Google Scholar
  29. Garcia AM, Vieira JP, Winemiller KO, Moraes LE, Paes ET (2012) Factoring scales of spatial and temporal variation in fish abundance in a subtropical estuary. Mar Ecol Prog Ser 461:121–135CrossRefGoogle Scholar
  30. González-Ortegón E, Subida MD, Cuesta JA, Arias AM, Fernández-Delgado C, Drake P (2010) The impact of extreme turbidity events on the nursery function of a temperate European estuary with regulated freshwater inflow. Estuar Coast Shelf Sci 87(2):311–324. doi: 10.1016/j.ecss.2010.01.013 CrossRefGoogle Scholar
  31. Griffin FJ, Smith EH, Vines CA, Cherr GN (2009) Impacts of suspended sediments on fertilization, embryonic development, and early larval life stages of the pacific herring, Clupea pallasi. Biol Bull 216(2):175–187PubMedGoogle Scholar
  32. Grioche A, Harlay X, Koubbi P, Lago LF (2000) Vertical migrations of fish larvae: Eulerian and Lagrangian observations in the Eastern English Channel. J Plankton Res 22(10):1813–1828CrossRefGoogle Scholar
  33. Harris NJ, Neal JW, Perschbacher PW, Mace CE, Muñoz–Hincapié M (2011) Notes on hatchery spawning methods for bigmouth sleeper Gobiomorus dormitor. Aquacult Res 42(8):1145–1152CrossRefGoogle Scholar
  34. Hatcher BG (2006) Dynamics of marine ecosystems biological-physical interactions in the oceans. Bot Mar 49(3):272–273CrossRefGoogle Scholar
  35. Hernández-León S (2008) Natural variability of fisheries and lunar illumination: a hypothesis. Fish Fish 9(2):138–154. doi: 10.1111/j.1467-2979.2008.00272.x CrossRefGoogle Scholar
  36. Hernández-Saavedra R, Martínez-Pérez JA, Brown-Peterson NJ, Peterson MS (2004) Gonadal development and sexual dimorphism of Gobiomorus dormitor from the estuarine system of Tecolutla, Veracruz, Mexico. Gulf Caribb Res 16:95–100Google Scholar
  37. Houde ED (2008) Emerging from Hjort’s shadow. J Northwest Atl Fish Sci 41:53–70CrossRefGoogle Scholar
  38. Johnson DL, Morse WW (1994) Net extrusion of larval fish: correction factors for 0.333 mm versus 0.505 mm mesh bongo nets. NAFO Sci Counc Stud 20:85–92Google Scholar
  39. Kent J, Jenkins G, Acevedo S (2013) Temporal and spatial patterns in ichthyoplankton assemblages in bay and open coastal environments. J Fish Biol 82(2):408–429. doi: 10.1111/jfb.12008 PubMedCrossRefGoogle Scholar
  40. Krebs CJ (1999) Ecological methodology, vol 620. Benjamin/Cummings Menlo Park, CaliforniaGoogle Scholar
  41. Krumme U (2003) Tidal and diel dynamics in a nursery area: patterns in fish migration in a mangrove in North Brazil. University of BremenGoogle Scholar
  42. Lecchini D, Waqalevu VP, Holles S, Lerohellec M, Brie C, Simpson SD (2013) Vertical and horizontal distributions of coral-reef fish larvae in open water immediately prior to reef colonization. J Fish Biol 82(6):2135–2140. doi: 10.1111/jfb.12136 PubMedCrossRefGoogle Scholar
  43. Li M, Xu K, Watanabe M, Chen Z (2007) Long-term variations in dissolved silicate, nitrogen, and phosphorus flux from the Yangtze River into the East China Sea and impacts on estuarine ecosystem. Estuar Coast Shelf Sci 71(1):3–12CrossRefGoogle Scholar
  44. Liv P, Mathiassen SE, Svendsen SW (2012) Accuracy and precision of variance components in occupational posture recordings: a simulation study of different data collection strategies. BMC Med Res Methodol 12(1):58PubMedCentralPubMedCrossRefGoogle Scholar
  45. López-Sanz À, Stelzenmüller V, Maynou F, Sabatés A (2011) The influence of environmental characteristics on fish larvae spatial patterns related to a marine protected area: The Medes islands (NW Mediterranean). Estuar Coast Shelf Sci 92(4):521–533CrossRefGoogle Scholar
  46. Macossay-Cortez A, Sanchez AJ, Florido R, Huidobro L, Montalvo-Urgel H (2011) Historical and Environmental Distribution of Ichthyofauna in the Tropical Wetland of Pantanos de Centla, Southern Gulf of Mexico. Acta Ichthyol Pisc 41(3):229–245CrossRefGoogle Scholar
  47. Magalhães A, Nobre DSB, Bessa RSC, Pereira LCC, da Costa RM (2011) Seasonal and short-term variations in the copepod community of a shallow Amazon estuary (Taperaçu, Northern Brazil). J Coast Res 64:1520–1524Google Scholar
  48. Martinho F, Leitão R, Neto JM, Cabral HN, Marques JC, Pardal MA (2007) The use of nursery areas by juvenile fish in a temperate estuary, Portugal. Hydrobiologia 587(1):281–290CrossRefGoogle Scholar
  49. Matos JB, Sodré DKL, Costa KGD, Pereira LCC, Costa RMD (2011) Spatial and temporal variation in the composition and biomass of phytoplankton in an Amazonian estuary. J Coast Res SI 64:1525–1529Google Scholar
  50. Meerhoff E, Castro L, Tapia F (2013) Influence of freshwater discharges and tides on the abundance and distribution of larval and juvenile Munida gregaria in the Baker river estuary, Chilean Patagonia. Cont Shelf Res 61–62:1–11. doi: 10.1016/j.csr.2013.04.025 CrossRefGoogle Scholar
  51. Mendoza-Carranza M, Hoeinghaus DJ, Garcia AM, Romero-Rodríguez Á (2010) Aquatic food webs in mangrove and seagrass habitats of Centla Wetland, a Biosphere Reserve in Southeastern Mexico. Neotropical Ichthyol 8(1):171–178CrossRefGoogle Scholar
  52. Méthot G, Hudon C, Gagnon P, Pinel-Alloul B, Armellin A, Poirier A-MT (2012) Macroinvertebrate size-mass relationships: how specific should they be? Freshw Sci 31(3):750–764CrossRefGoogle Scholar
  53. Miller TJ (2002) Assemblages, communities, and species interactions. In: Fuimann LE, Werner RG (eds) Fishery science: the unique contributions of early life stages. Blackwell Publishing, Oxford, pp 183–205Google Scholar
  54. Novelo-Retana A (2006) Plantas acuáticas de la Reserva de la Biosfera Pantanos de Centla, DFGoogle Scholar
  55. Ohman MD (2012) Estimation of mortality for stage-structured zooplankton populations: what is to be done? J Mar Syst 93:4–10CrossRefGoogle Scholar
  56. Ooi AL, Chong VC (2011) Larval fish assemblages in a tropical mangrove estuary and adjacent coastal waters: Offshore–inshore flux of marine and estuarine species. Cont Shelf Res 31(15):1599–1610. doi: 10.1016/j.csr.2011.06.016 CrossRefGoogle Scholar
  57. Pepin P, Helbig JA (2012) Sampling variability of ichthyoplankton surveys—exploring the roles of scale and resolution on uncertainty. Fish Res 117:137–145CrossRefGoogle Scholar
  58. Ponce Vélez MG (1991) Mareas. In: de la Lanza-Espino G (ed) Oceanografía de mares mexicanos. AGT, México, pp 63–66Google Scholar
  59. Powles H, Markle DF (1984) Identification of larvae. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall Jr AW, Richardson SL (eds) Ontogeny and Systematics of Fishes. Am Soc Ichthyol Herpetol Spec Publ 1(760):31–33Google Scholar
  60. Primo AL, Azeiteiro UM, Marques SC, Pardal MÂ (2011a) Impact of climate variability on ichthyoplankton communities: an example of a small temperate estuary. Estuar Coast Shelf Sci 91(4):484–491CrossRefGoogle Scholar
  61. Primo AL, Azeiteiro UM, Marques SC, Ré P, Pardal MÂ (2011b) Seasonal, lunar and tidal control of ichthyoplankton dynamics at the interface between a temperate estuary and adjacent coastal waters (western Portugal). Sci Mar 76(2):237–246CrossRefGoogle Scholar
  62. Ramos S, Cowen RK, Paris C, Ré P, Bordalo AA (2006a) Environmental forcing and larval fish assemblage dynamics in the Lima River estuary (northwest Portugal). J Plankton Res 28(3):275–286CrossRefGoogle Scholar
  63. Ramos S, Cowen RK, Ré P, Bordalo AA (2006b) Temporal and spatial distributions of larval fish assemblages in the Lima estuary (Portugal). Estuar Coast Shelf Sci 66(1):303–314CrossRefGoogle Scholar
  64. Ramos JAA, Barletta M, Dantas DV, Lima ARA, Costa MF (2011) Influence of moon phase on fish assemblages in estuarine mangrove tidal creeks. J Fish Biol 78(1):344–354PubMedCrossRefGoogle Scholar
  65. Reyier EA, Shenker JM (2007) Ichthyoplankton community structure in a shallow subtropical estuary of the Florida Atlantic coast. Bull Mar Sci 80(2):267–293Google Scholar
  66. Richards WJ (2005) Early stages of Atlantic fishes: an identification guide for the western central north Atlantic, Two Volume Set, vol 1. CRC PressGoogle Scholar
  67. Salcedo MA, Sánchez AJ, de la Lanza-Espino G, Kampichler C, Florido R (2012) Condición ecológica del humedal tropical Pantanos de Centla. In: Sánchez AJ, Chiappa-Carrara X, Pérez B (eds) Recursos Acuáticos Costeros del Sureste: Tendencias actuales en investigación y estado del arte. vol 2. RECORECOS, CONCYTEY, UNACAR, UJAT, ECOSUR, UNAM, México, D.F., p 112–136Google Scholar
  68. Sánchez AJ, Florido R, A. M-C, Cruz-Ascencio M, Montalvo-Urgel H, Garrido-Mora A (2012) Distribución de macroinvertebrados acuáticos y peces en cuatro hábitats en Pantanos de Centla, sur del golfo de México. In: Sánchez AJ, Chiappa-Carrara X, Pérez B (eds) Recursos Acuáticos Costeros del Sureste: Tendencias actuales en investigación y estado del arte. vol 2. RECORECOS, CONCYTEY, UNACAR, UJAT, ECOSUR, UNAM., México, D.F., p 416–443Google Scholar
  69. Sanvicente-Añorve L, Flores-Coto C, Chiappa-Carrara X (2000) Temporal and spatial scales of ichthyoplankton distribution in the Southern Gulf of Mexico. Estuar Coast Shelf Sci 51(4):463–475CrossRefGoogle Scholar
  70. Sanvicente-Añorve L, Sánchez-Ramírez M, Ocaña-Luna A, Flores-Coto C, Ordóñez-López U (2011) Metacommunity structure of estuarine fish larvae: the role of regional and local processes. J Plankton Res 33(1):179–194CrossRefGoogle Scholar
  71. Satterthwaite FE (1946) An approximate distribution of estimates of variance components. Biom Bull 2(6):110–114CrossRefGoogle Scholar
  72. Searle SR, Casella G, McCulloch CE (2009) Variance components. Wiley, New JerseyGoogle Scholar
  73. Shuiwang D, Shen Z, Hongyu H (2000) Transport of dissolved inorganic nitrogen from the major rivers to estuaries in China. Nutr Cycl Agroecosyst 57(1):13–22CrossRefGoogle Scholar
  74. Smith PE, Richardson SL (1977) Standard techniques for pelagic fish egg and larva surveys,Google Scholar
  75. Sommer U, Lewandowska A (2011) Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Global Change Biol 17(1):154–162CrossRefGoogle Scholar
  76. Specziár A, György Á, Erős T (2013) Within-lake distribution patterns of fish assemblages: the relative roles of spatial, temporal and random environmental factors in assessing fish assemblages using gillnets in a large and shallow temperate lake. J Fish Biol 82:840–855PubMedCrossRefGoogle Scholar
  77. Suthers IM, Bowling L, Kobayashi T, Rissik D (2009) Sampling methods for plankton. In: Suthers IM, Rissik D (eds) Plankton: a guide to their ecology and monitoring for water quality. CSIRO PUBLISHING, Australia, pp 73–114Google Scholar
  78. Takemura A, Rahman MS, Park YJ (2010) External and internal controls of lunar–related reproductive rhythms in fishes. J Fish Biol 76(1):7–26PubMedCrossRefGoogle Scholar
  79. Thom BG (1967) Mangrove ecology and deltaic geomorphology: Tabasco, Mexico. J Ecol 55(2):301–343CrossRefGoogle Scholar
  80. Toledo A (2003) Ríos, costas y mares. Hacia un análisis integrado de las regiones hidrológicas de México. INE-Semarnat, MéxicoGoogle Scholar
  81. Wakida-Kusonoki AT, Riuz-Carus R, Amador-del-Angel E (2007) Amazon Sailfin Carfish Pterygoplichthys pardalis (Castelnau, 1955) (Loricaridae), Another Exotic Species Established in Southeastern Mexico. Southwest Nat 52(1):4Google Scholar
  82. Wantiez L, Hebert P, Juncker M (2007) Nocturnal and lunar input patterns of pre-settlement coral reef fish in Wallis lagoon (Central South Pacific): implications for sampling strategies. Aquat Living Resour 20(02):171–174CrossRefGoogle Scholar
  83. Winston JE (2012) Dispersal in marine organisms without a pelagic larval phase. Integr Comp Biol 52(4):447–457PubMedCrossRefGoogle Scholar
  84. Wolff N, Grober-Dunsmore R, Rogers CS, Beets J (1999) Management implications of fish trap effectiveness in adjacent coral reef and gorgonian habitats. Environ Biol Fish 55(1–2):81–90CrossRefGoogle Scholar
  85. Ysebaert T, Herman PMJ (2002) Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Mar Ecol Prog Ser 244:105–124CrossRefGoogle Scholar
  86. Zar JH (2010) Biostatistical analysis. Prentice-Hall, New JerseyGoogle Scholar
  87. Zavala-García F, Flores-Coto C (2005) Marco de soporte para muestreo de plancton y neuston en áreas someras y canales. Cienc Mar 9(25):21–24Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Wendi Arévalo-Frías
    • 1
  • Manuel Mendoza-Carranza
    • 1
    • 2
  1. 1.Sustainable Management of Basin and Coastal ZonesEl Colegio de la Frontera SurVillahermosaMexico
  2. 2.Aquaculture and Fisheries GroupWageningen UniversityWageningenThe Netherlands

Personalised recommendations