Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X1721
Acta Limnologica Brasiliensia
Original Article

Generalist populations formed by generalist individuals: a case of study on the feeding habits of a Neotropical stream fish

Populações generalistas formadas por indivíduos generalistas: um caso de estudo sobre os hábitos alimentares de um peixe de riacho Neotropical

Rafaela Carvalho Neves; Pedro Paulino Borges; Jaquelini de Oliveira Zeni; Lilian Casatti; Fabrício Barreto Teresa

Downloads: 0
Views: 1120

Abstract

Abstract:: Aim: We described the diet of the generalist stream fish Knodus chapadae and we tested if the environmental conditions are associated with population’s diet and individual specialization.

Methods: We analyzed the stomach contents of 287 individuals from 29 streams from the Brazilian savanna (Cerrado).

Results: The instream physical habitat structure, physiochemical conditions, and adjacent land use explained partially the variation in the diet of populations, but not the variation in the individual specialization. Thus, the diet changes observed at populational level were driven by changes in the average composition of the diet of individuals that, in turn, remained generalists along the environmental gradient.

Conclusions: Our results show that the trophic opportunism described for small characids was also observed in K. chapadae, whose diet shifts according to changes in environmental conditions. Furthermore, the opportunism expressed at the individual level can explain the trophic plasticity observed on the studied species.

Keywords

Characidae, diet, intraspecific variation, individual specialization, trophic niche

Resumo

Resumo:: Objetivo: Descrevemos a dieta do peixe de riacho generalista, Knodus chapadae, e testamos se as condições ambientais explicam a dieta das populações e a especialização individual.

Métodos: Para isso, analisamos o conteúdo estomacal de 287 indivíduos de 29 riachos da savana brasileira (Cerrado).

Resultados: As variáveis da estrutura interna do hábitat, condições físico-químicas e o uso do solo explicaram parcialmente a variação na dieta das populações, mas não explicaram a variação na especialização individual. Então, as mudanças na dieta observadas no nível populacional foram decorrentes da mudança na composição média da dieta dos indivíduos que, por sua vez, permaneceram generalistas ao longo do gradiente ambiental.

Conclusões: Nossos resultados mostram que o oportunismo trófico descrito para pequenos caracídeos foi encontrado também em K. chapadae, cuja dieta muda de acordo com as características ambientais. Além disso, o oportunismo expresso em nível individual pode explicar a plasticidade trófica que é observada na espécie estudada.
 

Palavras-chave

Characidae, dieta, variação intraespecífica, especialização individual, nicho trófico

Referencias

ABELL, R., THIEME, M.L., REVENGA, C., BRYER, M., KOTTELAT, M., BOGUTSKAYA, N., COAD, B., MANDRAK, N., BALDERAS, S.C., BUSSING, W., STIASSNY, M.L.J., SKELTON, P., ALLEN, G.R., UNMACK, P., NASEKA, A., NG, R., SINDORF, N., ROBERTSON, J., ARMIJO, E., HIGGINS, J.V., HEIBEL, T.J., WIKRAMANAYAKE, E., OLSON, D., LÓPEZ, H.L., REIS, R.E., LUNDBERG, J.G., SABAJ PÉREZ, M.H. and PETRY, P. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 2008, 58(5), 403-414. http://dx.doi.org/10.1641/B580507.

ANGERMEIER, P.L. and KARR, J.R. Relationships between woody debris and fish habitat in a small warmwater stream. Transactions of the American Fisheries Society, 1984, 113(6), 716-726. http://dx.doi.org/10.1577/1548-8659(1984)113<716:RBWDAF>2.0.CO;2.

ARAÚJO, M.S., BOLNICK, D.I. and LAYMAN, C.A. The ecological causes of individual specialization. Ecology Letters, 2011, 14(9), 948-958. http://dx.doi.org/10.1111/j.1461-0248.2011.01662.x. PMid:21790933.

BARBOSA, H.O., BORGES, P.P., DALA-CORTE, R.B., MARTINS, P.T.A. and TERESA, F.B. Relative importance of local and landscape variables on fish assemblages in streams of Brazilian savanna. Fisheries Management and Ecology, 2019, 26(2), 119-130. http://dx.doi.org/10.1111/fme.12331.

BARILI, E., AGOSTINHO, A.A., GOMES, L.C. and LATINI, J.D. The coexistence of fish species in streams: relationships between assemblage attributes and trophic and environmental variables. Environmental Biology of Fishes, 2011, 92(1), 41-52. http://dx.doi.org/10.1007/s10641-011-9814-2.

BERKMAN, H.E. and RABENI, C.F. Effect of siltation on stream fish communities. Environmental Biology of Fishes, 1987, 18(4), 285-294. http://dx.doi.org/10.1007/BF00004881.

BOJSEN, B.H. Diet and condition of three fish species (Characidae) of the Andean foothills in relation to deforestation. Environmental Biology of Fishes, 2005, 73(1), 61-73. http://dx.doi.org/10.1007/s10641-004-5330-y.

BOLNICK, D.I., AMARASEKARE, P., ARAÚJO, M.S., BÜRGER, R., LEVINE, J.M., NOVAK, M., RUDOLF, V.H., SCHREIBER, S.J., URBAN, M.C. and VASSEUR, D.A. Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution, 2011, 26(4), 183-192. http://dx.doi.org/10.1016/j.tree.2011.01.009. PMid:21367482.

BOLNICK, D.I., SVANBÄCK, R., FORDYCE, J.A., YANG, L.H., DAVIS, J.M., HULSEY, C.D. and FORISTER, M.L. The ecology of individuals: incidence and implications of individual specialization. American Naturalist, 2003, 161(1), 1-28. http://dx.doi.org/10.1086/343878. PMid:12650459.

BOLNICK, D.I., YANG, L.H., FORDYCE, J.A., DAVIS, J.M. and SVANBÄCK, R. Measuring individual-level resource specialization. Ecology, 2002, 83(10), 2936-2941. http://dx.doi.org/10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2.

BORGES, P.P., MARTINS, P.T.A. and FERREIRA, A.A. Uso e ocupação do solo por meio de uma série histórica na bacia do rio Santa Teresa em Goiás. Revista Brasileira de Geografia Física, 2016, 9(1), 296-304. http://dx.doi.org/10.26848/rbgf.v9.1.p296-304.

BORGES, P.P., TERESA, F.B., MARTINS, P.T.A. and NABOUT, J.C. Relative influence of direct and indirect environmental effects on sestonic chlorophyll-a concentration in Cerrado streams. Acta Limnologica Brasiliensia, 2015, 27(3), 301-310. http://dx.doi.org/10.1590/S2179-975X1815.

BRITTAIN, J.E. and EIKELAND, T.J. Invertebrate drift – A review. Hydrobiologia, 1988, 166(1), 77-93. http://dx.doi.org/10.1007/BF00017485.

BUSTAMANTE, M.M.C., NARDOTO, G.B., PINTO, A.S., RESENDE, J.C.F., TAKAHASHI, F.S.C. and VIEIRA, L.C.G. Potential impacts of climate change on biogeochemical functioning of Cerrado ecosystems. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2012, 72(3), 655-671. Supplement. http://dx.doi.org/10.1590/S1519-69842012000400005. PMid:23011296.

CARDOSO, A.C. and COUCEIRO, S.R.M. Insects in the diet of fish from Amazonian streams, in western Pará, Brazil. Marine and Freshwater Research, 2017, 68(11), 2052-2060. http://dx.doi.org/10.1071/MF16173.

CASATTI, L., DE PAULA FERREIRA, C. and CARVALHO, F.R. Grass-dominated stream sites exhibit low fish species diversity and dominance by guppies: an assessment of two tropical pasture river basins. Hydrobiologia, 2009, 632(1), 273-283. http://dx.doi.org/10.1007/s10750-009-9849-y.

CENEVIVA-BASTOS, M. and CASATTI, L. Oportunismo alimentar de Knodus moenkhausii (Teleostei, Characidae): uma espécie abundante em riachos do noroeste do Estado de São Paulo, Brasil. Iheringia. Série Zoologia, 2007, 97(1), 7-15. http://dx.doi.org/10.1590/S0073-47212007000100002.

CENEVIVA-BASTOS, M., CASATTI, L. and ROSSA-FERES, D.C. Meso and micro-habitat analysis and feeding habits of small nektonic characins (Teleostei: Characiformes) in Neotropical streams. Revista Brasileira de Zoologia, 2010, 27(2), 191-200. http://dx.doi.org/10.1590/S1984-46702010000200006.

CENEVIVA-BASTOS, M., MONTAÑA, C.G., SCHALK, C.M., CAMARGO, P.B. and CASATTI, L. Responses of aquatic food webs to the addition of structural complexity and basal resource diversity in degraded Neotropical streams. Austral Ecology, 2017, 42(8), 908-919. http://dx.doi.org/10.1111/aec.12518.

CHAN, E.K.W., ZHANG, Y. and DUDGEON, D. Arthropod ‘rain’ into tropical streams: the importance of intact riparian forest and influences of fish diets. Marine and Freshwater Research, 2008, 59(8), 653-660. http://dx.doi.org/10.1071/MF07191.

COSTA-PEREIRA, R., TAVARES, L.E.R., DE CAMARGO, P.B. and ARAÚJO, M.S. Seasonal population and individual niche dynamics in a tetra fish in the Pantanal wetlands. Biotropica, 2017, 49(4), 531-538. http://dx.doi.org/10.1111/btp.12434.

CUNHA, A.F., WOLFF, L.L. and HAHN, N.S. Seasonal changes at population and individual levels in the diet of juvenile catfish in a Neotropical floodplain. Journal of Freshwater Ecology, 2018, 33(1), 274-284. http://dx.doi.org/10.1080/02705060.2018.1442371.

DARIMONT, C.T., PAQUET, P.C. and REIMCHEN, T.E. Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. The Journal of Animal Ecology, 2009, 78(1), 126-133. http://dx.doi.org/10.1111/j.1365-2656.2008.01473.x. PMid:19120600.

EMLEN, J.M. The role of time and energy in food preference. American Naturalist, 1966, 100(916), 611-617. http://dx.doi.org/10.1086/282455.

FAUSCH, K.D. and NORTHCOTE, T.G. Large woody debris and salmonid habitat in a small coastal British Columbia stream. Canadian Journal of Fisheries and Aquatic Sciences, 1992, 49(4), 682-693. http://dx.doi.org/10.1139/f92-077.

FERREIRA, A., GERHARD, P. and CYRINO, J.E.P. Diet of Astyanax paranae (Characidae) in streams with different riparian land covers in the Passa-Cinco River basin, southeastern Brazil. Iheringia. Série Zoologia, 2012, 102(1), 80-87. http://dx.doi.org/10.1590/S0073-47212012000100011.

FLORES, L., LARRANAGA, A., DÍEZ, J. and ELOSEGI, A. Experimental wood addition in streams: effects on organic matter storage and breakdown. Freshwater Biology, 2011, 56(10), 2156-2167. http://dx.doi.org/10.1111/j.1365-2427.2011.02643.x.

GELWICK, F.P. and MCINTYRE, P.B. Trophic relations of stream fishes. In: F.R. HAUER and G. LAMBERTI, editors. Methods in stream ecology. 3rd ed. Cambridge: Academic Press, 2017, pp. 457-479, vol. 1: Ecosystem structure. http://dx.doi.org/10.1016/B978-0-12-416558-8.00022-6.

GOLTERMAN, H.L., CLYMO, R.S. and OHNSTAD, M.A. Methods for physical and chemical analysis of fresh water. 2nd ed. Oxford: Blackwell Scientific Publications, 1978.

GONÇALVES, C.S., BRAGA, F.M.S. and CASATTI, L. Trophic structure of coastal freshwater stream fishes from an Atlantic rainforest: evidence of the importance of protected and forest-covered areas to fish diet. Environmental Biology of Fishes, 2018, 101(6), 933-948. http://dx.doi.org/10.1007/s10641-018-0749-8.

GONSAMO, A., D’ODORICO, P. and PELLIKKA, P. Measuring fractional forest canopy element cover and openness - definitions and methodologies revisited. Oikos, 2013, 122(9), 1283-1291. http://dx.doi.org/10.1111/j.1600-0706.2013.00369.x.

HUGHES, N.F. and DILL, L.M. Position choice by drift‐feeding salmonids: model and test for Arctic grayling (Thymallus arcticus) in subarctic mountain streams, interior Alaska. Canadian Journal of Fisheries and Aquatic Sciences, 1990, 47(10), 2039-2048. http://dx.doi.org/10.1139/f90-228.

KAWAKAMI, E. and VAZZOLER, G. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Boletim do Instituto Oceanográfico, 1980, 29(2), 205-207. http://dx.doi.org/10.1590/S0373-55241980000200043.

LEAL, C.G., POMPEU, P.S., GARDNER, T.A., LEITÃO, R.P., HUGHES, R.M., KAUFMANN, P.R., ZUANON, J., DE PAULA, F.R., FERRAZ, S.F.B., THOMSON, J.R., MAC NALLY, R., FERREIRA, J. and BARLOW, J. Multi-scale assessment of human-induced changes to Amazonian instream habitats. Landscape Ecology, 2016, 31(8), 1725-1745. http://dx.doi.org/10.1007/s10980-016-0358-x.

LEGENDRE, P. and LEGENDRE, L. Numerical ecology. 3rd ed. Amsterdam: Elsevier, 2012.

LIANG, D., YANG, S., PAGANI-NÚÑEZ, E., HE, C., LIU, Y., GOODALE, E., LIAO, W.B. and HU, J. How to become a generalist species? Individual niche variation across habitat transformation gradients. Frontiers in Ecology and Evolution, 2020, 8, 597450. http://dx.doi.org/10.3389/fevo.2020.597450.

LORION, C.M. and KENNEDY, B.P. Riparian forest buffers mitigate the effects of deforestation on fish assemblages in tropical headwater streams. Ecological Applications, 2009, 19(2), 468-479. http://dx.doi.org/10.1890/08-0050.1. PMid:19323203.

LOWE‐MCCONNELL, R.H. Ecological studies in tropical fish communities. Cambridge: Cambridge University Press, 1987. http://dx.doi.org/10.1017/CBO9780511721892.

MANNA, L.R., VILLÉGER, S., REZENDE, C.F. and MAZZONI, R. High intraspecific variability in morphology and diet in tropical stream fish communities. Ecology Freshwater Fish, 2019, 28(1), 41-52. http://dx.doi.org/10.1111/eff.12425.

MAZZONI, R., FENERICH-VERANI, N. and CARAMASCHI, E.P. Electrofishing as a sampling technique for coastal stream fish populations and communities in the Southeast of Brazil. Revista brasileira de biologia, 2000, 60(2), 205-216. http://dx.doi.org/10.1590/S0034-71082000000200003. PMid:10959103.

MENNINGER, H.L. and PALMER, M.A. Herbs and grasses as an allochthonous resource in open-canopy headwater streams. Freshwater Biology, 2007, 52(9), 1689-1699. http://dx.doi.org/10.1111/j.1365-2427.2007.01797.x.

MORTILLARO, J.M., POUILLY, M., WACH, M., FREITAS, C.E.C., ABRIL, G. and MEZIANE, T. Trophic opportunism of central Amazon floodplain fish. Freshwater Biology, 2015, 60(8), 1659-1670. http://dx.doi.org/10.1111/fwb.12598.

MUGNAI, R., NESSIMIAN, J.L. and BAPTISTA, D.F. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro: para atividades técnicas, de ensino e treinamento em programas de avaliação da qualidade ecológica dos ecossistemas lóticos. Rio de Janeiro: Technical Books Editora, 2010.

MURRAY, I.W. and WOLF, B.O. Desert tortoise (Gopherus agassizii) dietary specialization decreases across a precipitation gradient. PLoS One, 2013, 8(6), e66505. http://dx.doi.org/10.1371/journal.pone.0066505. PMid:23840495.

NAIMI, B., HAMM, N.A.S., GROEN, T.A., SKIDMORE, A.K. and TOXOPEUS, A.G. Where is positional uncertainty a problem for species distribution modelling? Ecography, 2014, 37(2), 191-203. http://dx.doi.org/10.1111/j.1600-0587.2013.00205.x.

NAVARRO, J., GRÉMILLET, D., RAMIREZ, F.J., AFÁN, I., BOUTEN, W. and FORERO, M.G. Shifting individual habitat specialization of a successful predator living in anthropogenic landscapes. Marine Ecology Progress Series, 2017, 578, 243-251. http://dx.doi.org/10.3354/meps12124.

OKSANEN, J., BLANCHET, F.G., FRIENDLY, M., KINDT, R., LEGENDRE, P., McGLINN, D., MINCHIN, P.R., O’HARA, R.B., SIMPSON, G.L., SOLYMOS, P., STEVENS, M.H.H., SZOECS, E. and WAGNER, H. vegan: Community ecology package. R package version 2.5-7. Vienna, Austria: R Foundation for Statistical Computing, 2020.

QUEVEDO, M., SVANBÄCK, R. and EKLÖV, P. Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology, 2009, 90(8), 2263-2274. http://dx.doi.org/10.1890/07-1580.1. PMid:19739388.

R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing [online]. Vienna, Austria: R Foundation for Statistical Computing, 2018 [viewed 16 Mar. 2021]. Available from: https://www.R-project.org/

REZENDE, C.F. and MAZZONI, R. Aspectos da alimentação de Bryconamericus microcephalus (Characiformes, Tetragonopterinae) no Córrego Andorinha, Ilha Grande–RJ. Biota Neotropica, 2003, 3(1), 1-6. http://dx.doi.org/10.1590/S1676-06032003000100012.

ROCHA, F.C.D., CASATTI, L., CARVALHO, F.R. and SILVA, A.M.D. Fish assemblages in stream stretches occupied by cattail (Typhaceae, Angiospermae) stands in Southeast Brazil. Neotropical Ichthyology, 2009, 7(2), 241-250. http://dx.doi.org/10.1590/S1679-62252009000200016.

ROUGHGARDEN, J. Evolution of niche width. American Naturalist, 1972, 106(952), 683-718. http://dx.doi.org/10.1086/282807.

SCHOENER, T.W. Theory of feeding strategies. Annual Review of Ecology and Systematics, 1971, 2(1), 369-404. http://dx.doi.org/10.1146/annurev.es.02.110171.002101.

SMITH, J.A., BAUMGARTNER, L.J., SUTHERS, I.M. and TAYLOR, M.D. Generalist niche, specialist strategy: the diet of an Australian percichthyid. Journal of Fish Biology, 2011, 78(4), 1183-1199. http://dx.doi.org/10.1111/j.1095-8649.2011.02926.x. PMid:21463314.

STRAHLER, A.N. Quantitative analysis of watershed geomorphology. Transactions - American Geophysical Union, 1957, 38(6), 913-920. http://dx.doi.org/10.1029/TR038i006p00913.

SVANBÄCK, R. and BOLNICK, D.I. Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evolutionary Ecology Research, 2005, 7, 993-1012.

SVANBÄCK, R. and BOLNICK, D.I. Intraspecific competition drives increased resource use diversity within a natural population. Proceedings. Biological Sciences, 2007, 274(1611), 839-844. http://dx.doi.org/10.1098/rspb.2006.0198. PMid:17251094.

SVANBÄCK, R. and PERSSON, L. Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. Journal of Animal Ecology, 2004, 73(5), 973-982. http://dx.doi.org/10.1111/j.0021-8790.2004.00868.x.

TERESA, F.B., SOUZA, L.S., SILVA, D.M.A., BARBOSA, H.O., LIMA, J.D. and NABOUT, J.C. Environmental constraints structuring fish assemblages in riffles: evidences from a tropical stream. Neotropical Ichthyology, 2016, 14(3), e150185. http://dx.doi.org/10.1590/1982-0224-20150185.

TONIN, A.M., GONÇALVES JUNIOR, J.F., BAMBI, P., COUCEIRO, S.R.M., FEITOZA, L.A.M., FONTANA, L.E., HAMADA, N., HEPP, L.U., LEZAN-KOWALCZUK, V.G., LEITE, G.F.M., LEMES-SILVA, A.L., LISBOA, L.K., LOUREIRO, R.C., MARTINS, R.T., MEDEIROS, A.O., MORAIS, P.B., MORETTO, Y., OLIVERIA, P.C.A., PEREIRA, E.B., FERREIRA, L.P., PÉREZ, J., PETRUCIO, M.M., REIS, D.F., S REZENDE, R., ROQUE, N., SANTOS, L.E.P., SIEGLOCH, A.E., TONELLO, G. and BOYERO, L. Plant litter dynamics in the forest-stream interface: precipitation is a major control across tropical biomes. Scientific Reports, 2017, 7(1), 10799. http://dx.doi.org/10.1038/s41598-017-10576-8. PMid:28883445.

XIA, Y., LI, Y., ZHU, S., LI, J., LI, S. and LI, X. Individual dietary specialization reduces intraspecific competition, rather than feeding activity, in black amur bream (Megalobrama terminalis). Scientific Reports, 2020, 10(1), 17961. http://dx.doi.org/10.1038/s41598-020-74997-8. PMid:33087846.

ZACCARELLI, N., BOLNICK, D.I. and MANCINELLI, G. RInSp: an r package for the analysis of individual specialization in resource use. Methods in Ecology and Evolution, 2013, 4(11), 1018-1023. http://dx.doi.org/10.1111/2041-210X.12079.

ZENI, J.O. and CASATTI, L. The influence of habitat homogenization on the trophic structure of fish fauna in tropical streams. Hydrobiologia, 2014, 726, 259-270. http://dx.doi.org/10.1007/s10750-013-1772-6.
 


Submitted date:
16/03/2021

Accepted date:
23/08/2021

Publication date:
21/09/2021

6149ef4aa95395269e621bb2 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections