Article

Article name FISH TAXONOMIC AND FUNCTIONAL DIVERSITY IN MESOHABITATS OF THE RIVER KAKADA, CAURA NATIONAL PARK, VENEZUELA
Authors

Gabriela Echevarría, Venezuelan Institute for Scientific Research (Carretera Panamericana, Km 11, Altos de Pipe, Miranda, Venezuela. 1204); e-mail: hydropsichidae@gmail.com
Nirson González, Guayana Hydrobiological Research Station, La Salle Foundation of Natural Sciences (San Félix, UD 104, Bolívar, Venezuela. 8051); e-mail: nirsongonz@gmail.com

Reference to article

Echevarría G., González N. 2018. Fish taxonomic and functional diversity in mesohabitats of the River Kakada, Caura National Park, Venezuela. Nature Conservation Research 3(Suppl.2): 21–39. http://dx.doi.org/10.24189/ncr.2018.048

Section Resarch articles
DOI http://dx.doi.org/10.24189/ncr.2018.048
Abstract

The Caura National Park encompasses the entire basin of the River Caura, one of the most biodiverse hydrographic systems of Venezuela, yet the ichthyofauna, particularly in the upper basin, has been poorly studied. In this study, the taxonomic and functional diversity of fishes in mesohabitats of the River Kakada, a main tributary of the upper River Caura in Southern Venezuela, are described. The fishes were sampled in four mesohabitat types with seines during four different occasions, representing the hydrological seasons of rising waters, high waters, falling waters and low waters. Functional diversity indices were calculated based on four traits: size, trophic guild, mouth orientation and body shape. A total of 56 fish species were registered. There were significant differences in species composition of the fish assemblages and their taxonomic diversities among mesohabitats and across hydrological seasons, and the taxonomic and functional diversities were higher in the mesohabitats with presence of riparian forest. However, there were no seasonal variations in functional composition or functional diversities. The rocky substrates had unique assemblages of habitat specialist species with a particular array of traits. On the other hand, the presence of riparian forest and more structurally complex substrates favors the coexistence of a high diversity of fishes with a variety of trait combinations, whereas the seasonal fluctuations in the water level might propitiate stochastic processes of dispersion and colonisation that generate variations in species composition and taxonomic diversity. Considering the spread of artisanal gold mines in the Caura National Park, the results of this investigation might serve as a reference for future studies that assess the impacts of the gold mining activities on the river integrity and their fish communities.

Keywords

diversity seasonal patterns, fish assemblage structure, fish traits, Guiana Shield, riverine flooded forest

Artice information

Received: 12.04.2018

The full text of the article
References

Abrams P. 1983. The theory of limiting similarity. Annual Review of Ecology and Systematics 14: 359–376.
Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26(1): 32–46. DOI: 10.1111/j.1442-9993.2001.01070.pp.x
Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK: Primer-EB Ltd. 214 p.
Arantes C.C., Winemiller K.O., Petrere M., Castello L., Hess L.L., Freitas C.E.C. 2018. Relationships between forest cover and fish diversity in the Amazon River floodplain. Journal of Applied Ecology 55(1): 386–395. DOI: 10.1111/1365-2664.12967
Armbruster J.W. 2002. The species of Hypostomus cochliodon group (Siluriformes: Loricariidae). Zootaxa 249(1): 1–60. DOI: 10.11646/zootaxa.249.1.1
Arrington D.A., Winemiller K.O. 2006. Habitat affinity, the seasonal flood pulse, and community assembly in the littoral zone of a Neotropical floodplain river. Journal of the North American Benthological Society 25(1): 126–141. DOI: 10.1899/0887-3593(2006)25[126:HATSFP]2.0.CO;2
Arrington D.A., Winemiller K.O., Layman C.A. 2005. Community assembly at the patch scale in a species rich tropical river. Oecologia 144(1): 157–167. DOI: 10.1007/s00442-005-0014-7
Brosse S., Grenouillet G., Gevrey M., Khazraie K., Tudesque L. 2011. Small-scale gold mining erodes fish assemblage structure in small neotropical streams. Biodiversity and Conservation 20(5): 1013–1026. DOI: 10.1007/s10531-011-0011-6
Casatti L., Castro R.M.C. 2006. Testing the ecomorphological hypothesis in a headwater riffles fish assemblage of the rio São Francisco, southeastern Brazil. Neotropical Ichthyology 4(2): 203–214. DOI: 10.1590/S1679-62252006000200006
Castello L., Hess L.L., Thapa R., McGrath D.G., Arantes C.C., Renó V.F., Isaac V.J. 2018. Fishery yields vary with land cover on the Amazon River floodplain. Fish and Fisheries 19(3): 431–440. DOI: 10.1111/faf.12261
Chao A., Jost L. 2012. Coverage-based rarefaction and extrapolation : standardizing samples by completeness rather than size. Ecology 93(12): 2533–2547. DOI: 10.1890/11-1952.1
Chao A., Gotelli N., Hsieh T.C., Sander E., Ma K.H., Colwell R.K., Ellison A. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84(1): 45–67. DOI: 10.1890/13-0133.1
Chernoff B., Machado-Allison A. 1999. Bryconops colaroja and B. colanegra, two new species from the Cuyuní and Caroní drainages of South America (Teleostei: Characiformes). Ichthyological Explorations of Freshwaters 10(4): 355–370.
Chernoff B., Machado-Allison A., Provenzano F., Willink P.W., Petry P. 2002. Bryconops imitator, a new species from the Río Caura basin of Venezuela (Teleostei: Characiformes). Ichthyological Explorations of Freshwaters 13(3): 193–202.
Chernoff B., Machado-Allison A., Willink P.W., Provenzano-Rizzi F., Petry P., García, J.V., Pereira G., Rosales J., Bevilacqua M., Díaz W. 2003. The Distribution of Fishes and Patterns of Biodiversity in the Caura River Basin, Bolívar State, Venezuela. In: B. Chernoff, A. Machado-Allison, K. Riseng, J.R. Montambault (Eds.): A Biological Assessment of the Aquatic Ecosystems of the Caura River Basin, Bolívar State, Venezuela. RAP Bulletin of Biological Assessment 28. Washington DC: Conservation International Center for Applied Biodiversity Science Department of Conservation Biology. P. 86–96.
Cilleros K., Allard L., Vigouroux R., Brosse S. 2017. Disentangling spatial and environmental determinants of fish species richness and assemblage structure in Neotropical rainforest streams. Freshwater Biology 62(10): 1–14. DOI: 10.1111/fwb.12981
Clarke K.R., Gorley R.N. 2006. PRIMER v6: User Manual/Tutorial. Plymouth UK. Primer-EB Ltd. 129 p.
Cochran-Biederman J.L., Winemiller K.O. 2010. Relationships among habitat, ecomorphology and diets of cichlids in the Bladen River, Belize. Environmental Biology of Fishes 88(2): 143–152. DOI: .1007/s10641-010-9624-y
Coleman M.J., Hynes H.B.N. 1970. The life histories of some Plecoptera and Ephemeroptera in a southern Ontario stream. Canadian Journal of Zoology 48(6): 1333–1339. DOI: 10.1139/z70-227
Díaz-Pérez W., Daza F., Sarmiento W. 2012. Composición florística, estructura y diversidad del bosque ribereño del Río Kakada, Cuenca del Río Caura, estado Bolívar, Venezuela. Revista Científica UDO Agrícola 12(2): 275–289.
Echevarría G., González N. 2017. Co-occurrence patterns of fish communities in littorals of three floodplain lakes of the Orinoco River, Venezuela. Journal of Threatened Taxa 9(6): 10249–10260. DOI: 10.11609/jott.2710.9.6.10249-10260
Echevarría G., González N. 2018. Fish trait diversity in littorals of two floodplain lakes of the highly biodiverse Caura River, Venezuela. Ecology of Freshwater Fish 27(1): 158–169. DOI: .1111/eff.12333
Echevarría G., Gonzalez N., Mass F. 2011. Aspectos reproductivos de la comunidad de peces de la cuenca alta del río Caura , Venezuela. Ciencia 19(1): 25–40.
Echevarría G., Rodríguez J.P., Machado-Allison A. 2017. Seasonal fluctuations in taxonomic and functional diversity in assemblages of catfishes in the Venezuelan Arauca River Floodplain. Studies on Neotropical Fauna and Environment 53(1): 38–53. DOI: 10.1080/01650521.2017.1387426
Fitzgerald D.B., Winemiller K.O., Sabaj Pérez M.H., Sousa L.M. 2017. Seasonal changes in the assembly mechanisms structuring tropical fish communities. Ecology 98(1): 21–31. DOI: 10.1002/ecy.1616
Froese R., Pauly D. (Eds.). 2018. FishBase. World Wide Web electronic publication. Available from www.fishbase.org
Funk V.A., Kelloff C.L. 2009. Introduction. In: R.P. Vari, C.J. Ferraris, A. Radosavljevic, V.A. Funk (Eds.): Checklist of Freshwater Fishes of the Guiana Shield. Bulletin of the Biological Society of Washington 17: 1–8.
Géry J. 1977. Characoids of the world. Neptune City: T.F.H. Publications, Inc. Ltd. 672 p.
González N., Vispo C. 2004. Ecología trófica de algunos peces importantes en lagunas de inundacion del bajo río Caura, Estado Bolívar, Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales “2003": 147–183.
González N., Echevarría G., Daza F., Mass F. 2012a. List Illustrated list of additions to the ichthyofauna of the Caura River, Venezuela. Check List 8(1): 43–52. DOI: 10.15560/8.1.043
González N., Lasso C., Rosales J. 2012b. Estructura trófica de las comunidades de peces durante un ciclo hidrológico en dos lagunas inundables de la cuenca del bajo Río Orinoco. Memoria de la fundacion La Salle de Ciencias Naturales 173: 39–70.
Hsieh T.C., Ma K.H., Chao A. 2016. iNEXT: interpolation and Extrapolation for species diversity. R package version 2.0.12. Available from http://chao.stat.nthu.edu.tw/blog/software-download/
Gotelli N.J. 2000. Null Model Analysis of Species Co-Occurrence Patterns. Ecology 81(9): 2606–2621. DOI: 10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
Jost L. 2006. Entropy and diversity. Oikos 113(2): 363–375. DOI: 10.1111/j.2006.0030-1299.14714.x
Junk W., Bayley P., Sparks E. 1989. The Flood Pulse Concept in River - Floodplain Systems. In: P. Dodge (Ed.): Proceedings of the International Large Rivers Simposium. Canadian Special Publications in Fish and Aquatic Science 106. Ontario. P. 110–127.
Keddy P. 1992. Assembly and response rules: two goals for predictive community ecology. Journal of Vegetation Science 3(2): 157–164. DOI: 10.2307/3235676
Kembel S.W., Cowan P.D., Helmus M.R., Cornwell W.K., Morlon H., Ackerly D.D., Blomberg S.P., Webb C.O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11): 1463–1464. DOI: 10.1093/bioinformatics/btq166
Kullander S., Royero R., Taphorn D.C. 1992. Two new species of Geophagus (Teleostei: Cichlidae) from the Río Orinoco drainage in Venezuela. Ichthyological Exploration of Freshwaters 3(4): 359–375.
Laliberté E., Legendre P. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1): 299–305. DOI: 10.1890/08-2244.1
Laliberté A.E., Shipley B., Laliberté M.E. 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. 27 p.
Lasso C., Provenzano F. 1997. Chaetostoma vasquezi, nueva especie de corroncho del Escudo de Guayana, estado Bolívar, Venezuela (Siluroidei: Loricariidae) descripción y consideraciones biogeográficas. Memorias de la Sociedad de Ciencias Naturales La Salle 57(147): 53–65.
Lasso C., Machado-Allison A. 2000. Sinopsis de las especies de peces de la familia Cichlidae presentes en la cuenca del río Orinoco: claves, diagnosis, aspectos bio-ecológicos e ilustraciones. Caracas: Universidad Central de Venezuela, Facultad de Ciencias, Instituto de Zoología Tropical, Museo de Biología. 171 p.
López-Fernández H., Taphorn D.C., Kullander S.O. 2006. Two New Species of Guianacara from the Guiana Shield of Eastern Venezuela (Perciformes: Cichlidae). Copeia 2006(3): 384–395. DOI: 10.1643/0045-8511(2006)2006[384:TNSOGF]2.0.CO;2
López-Fernández H., Arbour J., Willis S., Watkins C., Honeycutt R.L., Winemiller K.O. 2014. Morphology and efficiency of a specialized foraging behavior, sediment sifting, in neotropical cichlid fishes. PLoS ONE 9(3): e89832. DOI: 10.1371/journal.pone.0089832
Lujan N.K., Winemiller K.O., Armbruster J.W. 2012. Trophic diversity in the evolution and community assembly of loricariid catfishes. BMC Evolutionary Biology 12(1): 124. DOI: 10.1186/1471-2148-12-124
Machado-Allison A., Kullander S.O., Lasso C.A. 1989. Description of a new Apistogramma species (Teleostei-Cichlidae) from the Morichal River Slong in Venezuela. Acta Biologica Venezuelica 12(3–4): 131–139.
Machado-Allison A., Chernoff B., Buckup P.A. 1996. Bryconops humeralis y B. vibex, dos nuevas especies del genero Bryconops Kner (1858) para Venezuela. Acta Biologica Venezuelica 16(2): 43–58.
Machado-Allison A., Chernoff B., Provenzano F.R., Willink P.W., Marcano A., Petry P., Sidlaukas B., Jones T. 2003. Inventory, Relative Abundance and Importance of Fishes in the Caura River Basin, Bolívar State, Venezuela. In: B. Chernoff, A. Machado-Allison, K. Riseng, J. Montambault (Eds.): A Biological Assessment of the Aquatic Ecosystems of the Caura River Basin, Bolívar State, Venezuela. Washington DC.: Conservation International Center for Applied Biodiversity Science Department of Conservation Biology. P. 64–74.
Mago-Leccia F. 1994. Electric fishes of the continental waters of America. Vol. 29. Caracas: Fundación para el Desarrollo de las Ciencias Físicas, Matemáticas y Naturales. 226 p.
Mason N.W.H., Mouillot D., Lee W.G., Wilson J.B. 2005. Functional richness, functional and functional evenness divergence: the primary of functional components diversity. Oikos 111(1): 112–118. DOI: 10.1111/j.0030-1299.2005.13886.x
Mason N.W.H., Lanoiselée C., Mouillot D., Wilson J.B., Argillier C. 2008. Does niche overlap control relative abundance in French lacustrine fish communities? A new method incorporating functional traits. Journal of Animal Ecology 77(4): 661–669. DOI: 10.1111/j.1365-2656.2008.01379.x
Ministerio del Poder Popular para el Ambiente. 2007. Análisis ecológico social y ordenamiento territorial de la región del río Caura. Base técnica. Caracas: Ministerio para el poder popular para el Ambiente. Despacho de la Viceministra de ordenación y administración ambiental. 241 p.
Mouillot D., Graham N., Villéger S., Mason N.W.H., Bellwood D.R. 2013. A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28(3): 167–177. DOI: 10.1016/j.tree.2012.10.004
Nijssen H., Isbrücker I.J. 1982. Corydoras boehlkei, a new catfish from the Río Caura system in Venezuela (Pisces, Siluriformes, Callichthyidae). Proceedings of the Academy of Natural Science of Philadelphia 134: 139–142.
Oyakawa O.T., Mattox G.M.T. 2009. Revision of the Neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotropical Ichthyology 7(2): 117–140. DOI: 10.1590/S1679-62252009000200001
Pease A.A., González-Díaz A.A., Rodiles-Hernández R., Winemiller K.O. 2012. Functional diversity and trait-environment relationships of stream fish assemblages in a large tropical catchment. Freshwater Biology 57(5): 1060–1075. DOI: 10.1111/j.1365-2427.2012.02768.x
Poff N. 1997. Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. Journal of the North American Benthological Society 16(2): 391–409. DOI: 10.2307/1468026
Presidencia de la República Bolivariana de Venezuela. 2016. Decreto No 2.231, mediante el cual se autoriza la creación de una Empresa del Estado, bajo la forma de Compañía Anónima, que se denominará Compañía Anónima Militar de Industrias Mineras, Petrolíferas y de Gas (CAMIMPEG). Caracas. Gaceta Oficial 40.845. P. 426327-426330.
Presidencia de la República Bolivariana de Venezuela. 2017. Decreto No. 2.767. Creación del Parque Nacional Caura. Caracas. Gaceta Oficial 41.118. P. 434.575-434.578.
R Development Core Team. 2012. R: A language and environment for statistical computing. Vienna, Austria. Available from http://www.R-project.org/
Ribeiro M.D., Teresa F.B., Casatti L. 2016. Use of functional traits to assess changes in stream fish assemblages across a habitat gradient. Neotropical Ichthyology 14(1): e140185. DOI: 10.1590/1982-0224-20140185
Riseng K., Sparks J. 2003. A Limnological Analysis of the Caura River Basin, Bolívar State, Venezuela. RAP Bulletin of Biological Assessment 28. In: B. Chernoff, A. Machado-Allison, K. Riseng, J. Montambault (Eds.): A Biological Assessment of the Aquatic Ecosystems of the Caura River Basin, Bolívar State, Venezuela. Washington DC.: Conservation International Center for Applied Biodiversity Science Department of Conservation Biology. P. 44–48.
Rodríguez M., Lewis W.M. Jr. 1997. Structure of fish assemblages along environmental gradients in floodplain lakes of the Orinoco River. Ecological Monographs 67(1): 109–128. DOI: 10.1890/0012-9615(1997)067[0109:SOFAAE]2.0.CO;2
Rodrigues-Filho C.A.S., Gurgel-Lourenço R.C., Lima S.M.Q., de Oliveira E.F., Sánchez-Botero J.I. 2017. What governs the functional diversity patterns of fishes in the headwater streams of the humid forest enclaves: environmental conditions, taxonomic diversity or biotic interactions? Environmental Biology of Fishes 100(9): 1023–1032. DOI: 10.1007/s10641-017-0603-4
Southwood T. 1977. Habitat, the templet for ecological strategies? Journal of Animal Ecology 46: 337–365.
Taphorn D. 1992. The characiform fishes of the Apure River drainage. Biollania 4: 1–537.
Teresa F.B., Casatti L. 2012. Influence of forest cover and mesohabitat types on functional and taxonomic diversity of fish communities in Neotropical lowland streams. Ecology of Freshwater Fish 21(3): 433–442. DOI: 10.1111/j.1600-0633.2012.00562.x
Thorp J., Thoms M., Delong M. 2008. The Riverine Ecosystem Synthesis. London, UK: Elsevier. 233 p.
Townsend C.R. 1989. The patch dynamics concept of stream community ecology. Journal of the North American Benthological Society 8(1): 36–50. DOI: 10.2307/1467400
Townsend C., Hildrew A. 1994. Species traits in relation to a habitat templet for river systems. Freshwater Biology 31(3): 265–275. DOI: 10.1111/j.1365-2427.1994.tb01740.x
Vari R.P. 1989. Systematics of the Neotropical characiform genus Psectrogaster Eigenmann and Eigenmann (Pisces: Characiformes). Smithsonian Contributions to Zoology 481: 1–43. DOI: 10.5479/si.00810282.481
Vari R.P. 1983. Phylogenetic relationships of the families Curimatidae, Prochilodontidae, Anostomidae, and Chilodontidae (Pisces, Characiformes). Smithsonian Contributions to Zoology 378: 1–60. DOI: 10.5479/si.00810282.378
Vari R.P., Ferraris C.J. 2009. Fishes of the Guiana Shield. In: R.P. Vari, C.J. Ferraris, A. Radosavljevic, V.A. Funk (Eds.): Checklist of Freshwater Fishes of the Guiana Shield. Bulletin of the Biological Society of Washington 17: 9–20.
Vari R.P., Ferraris C.J. 2013. Two New Species of the Catfish Genus Tatia (Siluriformes: Auchenipteridae) from the Guiana Shield and a Reevaluation of the Limits of the Genus. Copeia 2013(3): 396–402. DOI: 10.1643/CI-12-115
Villéger S., Mason N.W.H., Mouillot D. 2008. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89(8): 290–301. DOI: 10.1890/07-1206.1
Villéger S., Brosse S. Mouchet M., Mouillot D., Vanni M.J. 2017. Functional ecology of fish: current approaches and future challenges. Aquatic Sciences 79(4): 783–801. DOI: 10.1007/s00027-017-0546-z
Vispo C., Lasso C.A., Lasso-Alcalá Ó.M., González N. 2003. Geographical and temporal variation in fish communities of the floodplain lakes of the lower Caura drainage in the Venezuelan Guayana. Scientia Guaianae 12: 297–327.
Weiher E., Keddy P. 2004. Assembly rules as general constraints on community composition. In: E. Weiher, P. Keddy (Eds.): Ecological Assembly Rules. Perspectives, Advances, Retreats. Cambridge, UK: Cambridge University Press. P. 251–271.
Willink P.W., Chernoff B., Machado-Allison A., Provenzano F., Petry P. 2003. Aphyocharax yekwanae, a new species of bloodfin tetra (Teleostei: Characiformes: Characidae) from the Guyana Shield of Venezuela. Ichthyoplogical Explorations of Freshwaters 14(1): 1–8.
Willis S.C., Winemiller K.O., Lopez-Fernandez H. 2005. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia 142(2): 284–295. DOI: 10.1007/s00442-004-1723-z
Winemiller K.O. 1991. Ecomorphological diversification in lowland freshwater fish assemblages from five biotic regions. Ecological Monographs 61(4): 343–365. DOI: 10.2307/2937046
Winemiller K.O., Flecker A.S., Hoeinghaus D.J. 2010. Patch dynamics and environmental heterogeneity in lotic ecosystems. Journal of the North American Benthological Society 29(1): 84–99. DOI: 10.1899/08-048.1