Co-occurrence patterns of fish species in two aquatic habitats of the Arauca River floodplain, Venezuela

Abstract

The study of co-occurrence patterns has been extensively applied to propose assembly rules for community organization. Recently, a new interest has grown in the effect of gradients on these patterns and to analyze them through new approximations such as co-occurrence networks, through which keystone species can be identified. Neotropical floodplains represent interesting systems to study such patterns, because of their spatial heterogeneity, temporal variability and their high fish species richness. With this in mind, our goal was to study the co-occurrence patterns of fish in a segment of the Arauca River’s floodplain and the influence of the spatial and temporal variability on them. One stream and one floodplain lake were sampled with gill nets during 2014 – 2015 across a hydrological cycle and 5 matrices for each 5 sampled months in each water body were prepared to explore the co-occurrence patterns in each water body across months and 2 for the entire period, through a probabilistic pair-wise analysis of species co-occurrence that identified aggregated and segregated species pairs. With the observed cooccurrences × water body × month, the species weighted degrees and betweenness were calculated, and co-occurrence networks were constructed. The networks structures, in terms of the degrees of every species, were compared spatially and temporally through a generalized linear model. The stream showed the highest numbers of aggregated species pairs, and in general showed the most complex networks in terms of nodes, edges and degrees. The habitat type and the hydrological phases significantly influenced the structure of the fish co-occurrence networks. Two species, Loricariichthys brunneus and Pygocentrus cariba were identified as the core of the fish communities of the floodplain and as keystone species because they contribute to the connection of the networks by having a series of links with less frequent species.

References

  1. Adlte, A. and K.O. Winemiller. 1996. Trophic ecology and ecomorphology of fish assemblages in coastal lakes of Benin, West Africa. Ecoscience 4:6–23.

    Google Scholar 

  2. Amestoy, P., A. Azzalini, T. Badics, G. Benison, A. Bowmanm, W. Bohm and K. Briggs. 2015. Package “ igraph .” CRAN.

  3. Araújo, M.B., A. Rozenfeld, C. Rahbek and PA. Marquet. 2011. Using species co-occurrence networks to assess the impacts of climate change. Ecography 34:897–908.

    Article  Google Scholar 

  4. Arrington, D.A. and K.O. Winemiller. 2003. Diel changeover in sandbank fish assemblages in a Neotropical floodplain river. J. Fish Biol. 63:442–459.

    Article  Google Scholar 

  5. Arrington, D. A. and K. O. Winemiller. 2006. Habitat affinity, the seasonal flood pulse, and community assembly in the littoral zone of a Neotropical floodplain river. J. North Ameri. Benthol. Soc. 25:126–141.

    Article  Google Scholar 

  6. Arrington, D.A., K.O. Winemiller and C.A. Layman. 2005. Community assembly at the patch scale in a species rich tropical river. Oecologia 144:157–67.

    Article  PubMed  Google Scholar 

  7. Barbarino, A. and K.O. Winemiller. 2003. Dietary segregation among large catfishes of the Apure and Arauca Rivers, Venezuela. J. Fish Biol. 63:410–427.

    Article  Google Scholar 

  8. Barrat, A., M, Barthélemy, R. Pastor-Satorras and A. Vespigniani. 2004. The architecture of complex weighted networks. PNAS 101:3747–3752.

    Article  CAS  PubMed  Google Scholar 

  9. Bell, G. 2005. The co-distribution of species in relation to the neutral theory of community ecology. Ecology 86:1757–1770.

    Article  Google Scholar 

  10. Benedito-Cecilio, E. and Â.A. Agostinho. 1999. Determination of patterns of icthyofauna co-occurrence in the Paraná River basin, area of influence of the Itaipu reservoir. Interciencia 24:360–365.

    Google Scholar 

  11. Blasina, G., J. Molina, A. Lopez Cazorla and J. D. Astarloa. 2016. Relationship between ecomorphology and trophic segregation in four closely related sympatric fish species (Teleostei, Sciaenidae). Comptes Rendus Biologies 339:498–506.

    Article  PubMed  Google Scholar 

  12. Cecilio, E.B., A.A. Agostinho and C.S. Pavanelli. 1997. Colonizacao ictiofaunística do reservatório de Itaipu e áreas adjacentes. Rev. Bras. Zool. 14:1–14.

    Article  Google Scholar 

  13. Céréghino, R., F. Santoul, A. Compin, J. Figuerola and S. Mastrorillo. 2005. Co-occurrence patterns of some small-bodied freshwater fishes in southwestern France: implications for fish conservation and environmental management. Ambio 34:440–444.

    Article  PubMed  Google Scholar 

  14. Connor, E.F. and D. Simberloff. 1979. The assembly of species communities: chance or competition? Ecology 60:1132–1140.

  15. Diamond, J. 1975. Assembly rules. In: M. Cody and J. Diamond (eds.), Ecology and Evolution of Communities. Harvard University Press, Cambridge, Mass. pp. 342–444.

    Google Scholar 

  16. Erős, T., P. Takács, A. Specziár, D. Schmera and P. Sály. 2016. Effect of landscape context on fish metacommunity structuring in stream networks. Freshwater Biol. 62:1–14.

    Google Scholar 

  17. Eschmeyer, W.N., R. Fricke and R. van der Laan (eds). 2016. Catalog Of Fishes: Genera, Species, References. (http://researcharchive. calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Electronic version accessed in 2017.

  18. Fernandes, I.M., R. Henriques-Silva, J. Penha, J. Zuanon and P.R. Peres-Neto. 2013. Spatiotemporal dynamics in a seasonal metacommunity structure is predictable: the case of floodplain-fish communities. Ecography 37:464–475.

    Google Scholar 

  19. Flecker, A.S. 1992. Fish trophic guilds and the structure of a tropical stream: Weak direct vs. strong indirect effects. Ecology 73:927–940.

    Article  Google Scholar 

  20. Girvan, M. and M.E.J. Newman. 2002. Community structure in social and biological networks. PNAS USA 99:7821–7826.

    Article  CAS  PubMed  Google Scholar 

  21. Gotelli, N.J. and G. Graves. 1996. Null Models in Ecology. Smithsonian Institution Press, Washington and London, pp. 358.

    Google Scholar 

  22. Gotelli, N.J. 2000. Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621.

    Google Scholar 

  23. Gotelli, N.J., N.J. Buckley and J.A. Wiens. 1997. Co-occurrence of Australian land birds: Diamond’s assembly rules revisited. Oikos 80:311–324.

    Article  Google Scholar 

  24. Gotelli, N.J. and D.J. McCabe. 2002. Species co-occurrence: A meta-analysis of J. M. Diamond’s assembly rules model. Ecology 83:2091.

    Google Scholar 

  25. Griffith, D.M., J.A. Veech and C.J. Marsh. 2016. cooccur: Probabilistic species co-occurrence analysis in R. J. Stat.Softw. 69:1–17.

    Article  Google Scholar 

  26. Hoeinghaus, D.J., K.O. Winemiller and J.S. Birnbaum. 2006. Local and regional determinants of stream fish assemblage structure: inferences based on taxonomic vs. functional groups. J. Biogeogr. 34:1–15.

    Article  Google Scholar 

  27. Horner-Devine, M.C., J.M. Silver, M.A. Leibold, B.J.M. Bohannan, R.K. Colwell, J.A. Fuhrman, J.L. Green, C.R. Kuske, J.B.H. Martiny, G. Muyzer, L. Ovreås, A.-L. Reysenbach and V.H. Smith. 2007. A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88:1345–53.

    Article  PubMed  Google Scholar 

  28. Hubbell, S. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  29. Jackson, A.T., A. Adite, K.A. Roach and K.O. Winemiller. 2013. Fish assemblages of an African river floodplain: a test of alternative models of community structure. Ecol. Freshw. Fish 22:295–306.

    Article  Google Scholar 

  30. Jackson, D., P.R. Peres-Neto and J.D. Olden. 2001. What controls who is where in freshwater fish communities — the roles of biotic, abiotic, and spatial factors. Can. J. Fish. Aquat. Sci. 58:157–170.

    Google Scholar 

  31. Jackson, D., K.M. Somers and H.H. Harvey. 1992. Null models and fish communities: evidence of nonrandom patterns. Amer. Nat. 139:930–951.

    Article  Google Scholar 

  32. Jordán, F., T.A. Okey, B. Bauer and S. Libralato. 2008. Identifying important species: Linking structure and function in ecological networks. Ecol. Model. 216:75–80.

    Article  Google Scholar 

  33. Junk, W., P. Bayley and E. Sparks. 1989. The Flood Pulse Concept in River — Floodplain Systems. In: P. Dodge, (ed.), Proceedings of the International Large Rivers Symposium. Canadian Special Publications in Fish and Aquatic Science, pp. 110–127.

    Google Scholar 

  34. Keddy, P. and E. Weiher. 2004. Introduction: The scope and goals of research on assembly rules. In: E. Weiher and P. Keddy (eds.). Ecological Assembly Rules. Perspectives, Advances, Retreats. Cambridge University Press, Cambridge, UK. pp. 1–20.

    Google Scholar 

  35. Layman, C.A. and K.O. Winemiller. 2005. Patterns of habitat segregation among large fishes in a Venezuelan floodplain river. Neotrop. Ichthyol. 3:103–109.

    Article  Google Scholar 

  36. Lewis, W., S. Hamilton, M.A., Lasi, M. Rodriguez and F.J. Saunders. 2000. Ecological Determinism on the Orinoco Floodplain. BioScience 50:681–692.

    Article  Google Scholar 

  37. Lowe-McConnell, R.H. 1975. Fish Communities in Tropical Freshwaters. Their Distribution, Ecology and Evolution. Longman Inc., New York.

    Google Scholar 

  38. MacArthur, R. H. and E. O Wilson. 1967. Theory of Island Biogeography. Princeton University Press, Princeton.

    Google Scholar 

  39. Mokross, K., T.B. Ryder, M.C. Côrtes, J.D. Wolfe and P.C. Stouffer. 2014. Decay of interspecific avian flock networks along a disturbance gradient in Amazonia. Proc. Royal Soc. B: Biol. Sci. 281:01–10.

    Article  Google Scholar 

  40. Montana, C.G., C. Layman and K.O. Winemiller. 2015. Species-area relationship within benthic habitat patches of a tropical floodplain river: An experimental test. Austral Ecol. 40:331–336.

    Article  Google Scholar 

  41. Morueta-Holme, N., B. Blonder, B. Sandel, B.J. Mcgill, R.K. Peet, J.E. Ott, C. Violle, B. J. Enquist, P.M. Jorgensen and J.C. Svenning. 2016. A network approach for inferring species associations from co-occurrence data. Ecography 39:1–12.

    Article  Google Scholar 

  42. Mouchet, M.A., M.D.M. Burns, A M. Garcia, J.P Vieira and D. Mouillot. 2013. Invariant scaling relationship between functional dissimilarity and co-occurrence in fish assemblages of the Patos Lagoon estuary (Brazil): Environmental filtering consistently overshadows competitive exclusion. Oikos 122:247–257.

    Article  Google Scholar 

  43. Mouillot, D., O Dumay and J.A. Tomasini. 2007. Limiting similarity, niche filtering and functional diversity in coastal lagoon fish communities. Estuarine, Coastal and Shelf Science 71:443–156.

    Article  Google Scholar 

  44. Opsahl, T. 2015. tnet. V. 3.0.14. Software for Analysis of Weighted, Two-Mode, and Longitudinal Networks. CRAN. Available at http://toreopsahl.com. United Kingdom.

  45. Opsahl, T., F.Agneessens, and Skvoretz, J. 2010. Node centrality in weighted networks: Generalizing degree and shortest paths. Social Networks 32: 245–251.

    Article  Google Scholar 

  46. Opsahl, T. and P. Panzarasa. 2009. Clustering in weighted networks. Social Networks 31: 155–163. doi:10.1016/j.socnet.2009.02.002

    Article  Google Scholar 

  47. Pease, A., J.M. Taylor, K.O. Winemiller and R.S. King. 2015. Ecoregional, catchment, and reach-scale environmental factors shape functional-trait structure of stream fish assemblages. Hydrobiologia 753:265–283.

    Article  Google Scholar 

  48. Peres-Neto, PR. 2004. Patterns in the co-occurrence of fish species in streams: the role of site suitability, morphology and phylogeny versus species interactions. Oecologia 140:352–60.

    Article  PubMed  Google Scholar 

  49. Petry, A.C., A.A. Agostinho and L. C. Gomes. 2003a. Fish assemblages of tropical floodplain lagoons: exploring the role of connectivity in a dry year. Neotrop. Ichthyol. 1:111–119.

    Article  Google Scholar 

  50. Petty, P., PB. Bayley and D.F. Markle. 2003b. Relationships between fish assemblages , macrophytes and environmental gradients in the Amazon River floodplain. J. Fish Biol. 63:547–579.

    Article  Google Scholar 

  51. Power, M.E. and W.E. Dietrich. 2002. Food webs in river networks. Ecol.Res. 17:451–471.

    Article  Google Scholar 

  52. Proulx, S.R., D.E.L. Promislow and P.C. Phillips. 2005. Network thinking in ecology and evolution. Trends Ecol. Evol. 20:345–353.

    Article  Google Scholar 

  53. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  54. Reis, R.E., J.S. Albert, F. Di Dario, M.M.M. Mincarone, P.L. Petty and L.R. Rocha. 2016. Fish Biodiversity and Conservation in South America. J. Fish Biol. 89:12–17.

    Article  CAS  PubMed  Google Scholar 

  55. Rodríguez, M. and W. Lewis. 1994. Regulation and stability in fish assemblages of Neotropical floodplain lakes. Oecologia 99:166–180.

    Article  PubMed  Google Scholar 

  56. Sampaio, A.L.A., J.P.A. Pagotto and E. Goulart. 2013. Relationships between morphology, diet and spatial distribution: testing the effects of intra and interspecific morphological variations on the patterns of resource use in two Neotropical Cichlids. Neotrop. Ichthyol. 11:351–360.

    Article  Google Scholar 

  57. Scarabotti, P., J. López and M. Pouilly. 2011. Flood pulse and the dynamics of fish assemblage structure from Neotropical floodplain lakes. Ecol. Freshw. Fish 20:605–618.

    Article  Google Scholar 

  58. Stone, L. and A. Roberts. 1992. Competitive exclusion, or species aggregation? An aid in deciding. Oecologia 91:419–424.

    Article  Google Scholar 

  59. Strange, E., P. Moyle and T. Foin. 1992. Interactions between stochastic and deterministic processes in stream fish community assembly. Environ. Biol. Fishes 36:1–15.

    Article  Google Scholar 

  60. Taphorn, D C. and C. Lylestrom. 1985. Revista UNELLEZ de Ciencia y Tecnologia 3:55–85.

  61. Team, R.D.C. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  62. Thorp, J.H., M.C. Thorns and M.D. Delong. 2006. The riverine ecosystem synthesis: biocomplexity in river networks across space and time. River Res. App. 22:123–147.

    Article  Google Scholar 

  63. Thorp, J., M. Thorns and M. Delong. 2008. Ecological implications of the Riverine Ecosystem Synthesis: Some proposed biocomplexity tenets. In: J. Thorp et al. (ed.). The Riverine Ecosystem Synthesis. Elsevier, London, UK. Chapter 6. pp. 103–131.

  64. Townsend, C. 1989. The patch dynamics concept of stream community ecology. J. North Amer. Benthol. Soc. 8:36–50.

    Article  Google Scholar 

  65. Ulrich, W. and N.J. Gotelli. 2013. Pattern detection in null model analysis. Oikos 122:2–18.

    Article  Google Scholar 

  66. Veech, J. 2006. A probability-based analysis of temporal and spatial co-occurrence in grassland birds. J. Biogeogr. 33:2145–2153.

    Article  Google Scholar 

  67. Veech, J. 2013. A probabilistic model for analyzing species co-occurrence. Global Ecol. Biogeogr. 22:252–260.

    Article  Google Scholar 

  68. Veech, J. 2014. The pairwise approach to analyzing species co-occurrence. J. Biogeogr. 41:1029–1035.

    Article  Google Scholar 

  69. Weiher, E. and P. Keddy. 2004. Assembly rules as general constraints on community composition. In: E. Weiher and P. Keddy (eds.), Ecological Assembly Rules. Perspectives, Advances, Retreats. Cambridge University Press, Cambridge, UK. pp. 251–271

    Google Scholar 

  70. Widder, S., K. Besemer, G.A. Singerb, S. Ceolae, E. Bertuzzof, C. Quinceg, W.T. Sloang, A. Rinaldof and T.J. Battin. 2014. Fluvial network organization imprints on microbial co-occurrence networks. Proc. Nat. Acad. Sci. USA 111:12799–12804.

    Article  CAS  PubMed  Google Scholar 

  71. Williams, R.J., A. Howe and K.S. Hofmockel. 2014. Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Frontiers Microbiol. 5:1–10.

    Article  Google Scholar 

  72. Winemiller, K.O. 1990. Spatial and temporal variation in tropical fish trophic networks. Ecol. Monogr. 60:331–367.

    Article  Google Scholar 

  73. Winemiller, K.O. 1996. Dynamic diversity in fish assemblages of tropical rivers. In: M. L. Cody and J. A. Smallwood (eds.). Long-Term Studies of Vertebrate Communities. Academic Press, London. pp. 99–134.

    Google Scholar 

  74. Wisz, M.S., J. Pottier, W.D. Kissling, L. Pellissier, J. Lenoir, C.F. Damgaard, C.F. Dormann, M.C. Forchhammer, J.-A. Grytnes, A. Guisan, R.K. Heikkinen, T.T. Høye, I. Kühn, M. Luoto, L. Maiorano, M.-C. Nilsson, S. Normand, E. Öckinger, N.M. Schmidt, M. Termansen, A. Timmermann, D.A. Wardle, P. Aastrup and J.-C. Svenning. 2013. The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modeling. Biol. Rev. 88:15–30.

    Article  PubMed  Google Scholar 

  75. Zaret, T.M. and S. Rand. 1971. Competition in tropical stream fishes: Support for the competitive exclusion principle. Ecology 52:336–342.

    Article  Google Scholar 

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Echevarría, G., Rodríguez, J.P. Co-occurrence patterns of fish species in two aquatic habitats of the Arauca River floodplain, Venezuela. COMMUNITY ECOLOGY 18, 137–148 (2017). https://doi.org/10.1556/168.2017.18.2.3

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Keywords

  • Assembly rules
  • Co-occurrence networks
  • Fish community structure
  • Freshwater fish ecology
  • Seasonal environments