Characterization of wild fish diet and trophic guild in a protected area

Caracterização da dieta e guilda trófica de peixes silvestres em área protegida

Julia Kaori Kuriyama Ramos Natália Luiza da Silva Vinicius Cesar do Bonfim Bianca Yunes Fornari Bruna Caroline Kotz Kliemann Cibele Diogo Pagliarini Heleno Brandão Igor Paiva Ramos About the authors

Abstract:

Aim

We characterize the diet and trophic guild to the fish community in a protected area to contribute information about the trophic ecology.

Methods

The collection was carried out at three sampling points, in 2017 and 2018, with the help of gill nets. The collected specimens were euthanized in a 0.5% benzocaine solution. In the laboratory, all specimens' stomachs were removed, fixed in a 4% formalin solution, and preserved in 70% alcohol. Stomach contents were examined, and the food items were identified to the lowest possible taxonomic level. Food items were quantified according to the volumetric method. The characterization of the diet was presented through the percentage volume of each food item consumed. To determination of the trophic guild of each species, the predominance of a type of food resource (> 51% of the total volume) in the population's diet was considered.

Results

The species' diets were distributed in 16 food items (predominance of decapods, fish fragments, terrestrial insects, and aquatic plants), and four trophic guilds were observed (carcinophage, piscivore, terrestrial insectivore, and herbivore). Furthermore, there was the occurrence of microplastic in the diet of three species.

Conclusions

the fish community evaluated here demonstrates the wide range of resources that can make up the fish diet and demonstrates the different trophic guilds that can be observed in a protected area. As it is a conservation unit, knowing the diet and trophic guilds that make up the fish community can contribute to understanding the dynamics of food chains, the structure of the community, and the functioning of the ecosystem. Thus, this work can contribute information about the biology of the species evaluated for future work and conservation programs.

Keywords:
diet; freshwater fish; Itaipu Reservoir; Neotropical fish; Santa Helena Biological Refuge

Resumo:

Objetivo

Caracterizamos a dieta e a guilda trófica da comunidade de peixes em uma unidade de conservação para contribuir com informações sobre a ecologia trófica.

Métodos

As coletas foram realizadas em três pontos de amostragem, em 2017 e 2018, com o auxílio de redes de espera. Os espécimes foram eutanasiados em solução de benzocaína a 0,5%. Em laboratório, os estômagos foram retirados, fixados em formol 4% e preservados em álcool 70%. O conteúdo estomacal foi examinado e os itens alimentares foram identificados até o menor nível taxonômico possível e quantificados de acordo com o método volumétrico. A caracterização da dieta foi apresentada por meio do volume percentual de cada alimento consumido. Para a determinação da guilda trófica de cada espécie, foi considerada a predominância de um determinado tipo de recurso alimentar (> 51% do volume total) na dieta da população.

Resultados

A dieta das espécies foi distribuída em 16 itens alimentares (predominância de decapoda, fragmento de peixe, inseto terrestre e vegetal aquático), e quatro guildas tróficas foram observadas (carcinófago, piscívoro, insetívoro terrestre e herbívoro). Além disso, houve a ocorrência de microplástico na dieta de três espécies.

Conclusões

A comunidade de peixes aqui avaliada demonstra uma ampla gama de recursos que podem compor a dieta dos peixes e demonstra as diferentes guildas tróficas que podem ser observadas em uma área protegida. Por se tratar de uma unidade de conservação, conhecer a dieta e as guildas tróficas que compõem a comunidade de peixes pode contribuir para o entendimento da dinâmica das cadeias alimentares, da estrutura da comunidade e do funcionamento do ecossistema. Assim, este trabalho pode contribuir com informações sobre a biologia das espécies avaliadas para futuros trabalhos e programas de conservação.

Palavras-chave:
dieta; peixes de água doce; Reservatório de Itaipu; Peixes Neotropicais; Refúgio Biológico de Santa Helena

1. Introduction

Freshwater ecosystems are considered the most threatened habitats in the world (Reid et al., 2019Reid, A.J., Carlson, A.K., Creed, I.F., Eliason, E.J., Gell, P.A., Johnson, P.T.J., Kidd, K.A., MacCormack, T.J., Olden, J.D., Ormerod, S.J., Smol, J.P., Taylor, W.W., Tockner, K., Vermaire, J.C., Dudgeon, D., & Cooke, S.J., 2019. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. Camb. Philos. Soc. 94(3), 849-873. PMid:30467930. http://dx.doi.org/10.1111/brv.12480.
http://dx.doi.org/10.1111/brv.12480...
)⁠. In this case, conservation units are essential areas for protecting natural resources, guaranteeing the maintenance of the landscape and local biodiversity (Hassler, 2005Hassler, M.L., 2005. The importance of the units of conservation in Brazil. Soc. Nat. (Online), 17(33), 79-89. Retrieved in 2021, October 29, from http://www.redalyc.org/articulo.oa?id=321327187006
http://www.redalyc.org/articulo.oa?id=32...
; Henry-Silva, 2005Henry-Silva, G.G., 2005. A importância das unidades de conservação na preservação da diversidade biológica. Revista Logos, 12(12), 127-151.). The development of research on these protected areas is necessary for the protection, conservation, and management of these units (Luz & Elias, 2014Luz, A.P., & Elias, H.T., 2014. Pesquisa científica em unidades de conservação. Revista Epagri (Online), 27(1), 21-24. Retrieved in 2021, October 29, from https://publicacoes.epagri.sc.gov.br/RAC/article/download/591/494
https://publicacoes.epagri.sc.gov.br/RAC...
). Knowing which species inhabit the conservation units and their ecology makes it possible to understand the influences that conservation units have on the community (Ferreira et al., 2020Ferreira, J.D.O., Silva, M.A.S., & Bonifácio, C.M., 2020. Unidades de conservação: breves aspectos históricos e relevância. Rev. Cient. ANAP Brasil. 13(31), 45-53. http://dx.doi.org/10.17271/19843240133120202616.
http://dx.doi.org/10.17271/1984324013312...
; Henry-Silva, 2005Henry-Silva, G.G., 2005. A importância das unidades de conservação na preservação da diversidade biológica. Revista Logos, 12(12), 127-151.).

In aquatic protected areas, the ecological study of fish is a good tool for biomonitoring, contributing to the management and conservation of these areas (Carvalho et al., 2020Carvalho, T.L.A.B., Nascimento, A.A.D., Gonçalves, C.F.D.S., Santos, M.A.J.D., & Sales, A., 2020. Assessing the histological changes in fish gills as environmental bioindicators in Paraty and Sepetiba bays in Rio de Janeiro, Brazil. Lat. Am. J. Aquat. Res. 48(4), 590-601. http://dx.doi.org/10.3856/vol48-issue4-fulltext-2351.
http://dx.doi.org/10.3856/vol48-issue4-f...
; Chase & Leibold, 2004Chase, J.M., & Leibold, M.A., 2004. Ecological niches: linking classical and contemporary approaches. Chicago: The University of Chicago Press.). The fish are fundamental organisms in food chains, whether as consumers or food sources, maintaining the balance among the various species that make up these webs and acting as an important parameter in the trophic ecosystem characterization (Behn & Baxter, 2019Behn, K.E., & Baxter, C.V., 2019. The trophic ecology of a desert river fish assemblage: influence of season and hydrologic variability. Ecosphere 10(1), e02583. http://dx.doi.org/10.1002/ecs2.2583.
http://dx.doi.org/10.1002/ecs2.2583...
; Dias et al., 2005Dias, A.C.M.I., Castelo Branco, C.W., & Lopes, V.G., 2005. Estudo da dieta natural de peixes no reservatório de Ribeirão das Lajes, Rio de Janeiro, Brasil. Acta Sci. Biol. Sci. 27(4), 355-364. http://dx.doi.org/10.4025/actascibiolsci.v27i4.1270.
http://dx.doi.org/10.4025/actascibiolsci...
). With the study of the fish diet, it is possible to understand various aspects of the life of these animals, such as growth, reproduction, and adaptation, knowledge of the trophic organization of the ecosystem, effects of space, time variation, and biotic and abiotic factors (Esteves et al., 2021Esteves, K.E., Aranha, J.M.R., & Albrecht, M.P., 2021. Trophic ecology of stream fishes. Oecol. Aust. 25, 266-282. http://dx.doi.org/10.4257/oeco.2021.2502.04.
http://dx.doi.org/10.4257/oeco.2021.2502...
; Esteves & Aranha, 1999Esteves, K.E., & Aranha, J.M.R., 1999. Ecologia trófica de peixes de riachos. In: Caramaschi, E.P., Mazzoni, R. & Peres-Neto, P.R., eds. Ecologia de peixes de riachos. Rio de Janeiro: PPGE -UFRJ, 157-182. http://dx.doi.org/10.4257/oeco.1999.0601.05.
http://dx.doi.org/10.4257/oeco.1999.0601...
)⁠. In addition to understanding food resource sharing strategies, and how all these purposes reflect on the animals’ diet and the place where they live (Esteves et al., 2021Esteves, K.E., Aranha, J.M.R., & Albrecht, M.P., 2021. Trophic ecology of stream fishes. Oecol. Aust. 25, 266-282. http://dx.doi.org/10.4257/oeco.2021.2502.04.
http://dx.doi.org/10.4257/oeco.2021.2502...
).

Fish feeding may reflect the relationship between the aquatic environment and the surrounding areas (Carvalho et al., 2020Carvalho, T.L.A.B., Nascimento, A.A.D., Gonçalves, C.F.D.S., Santos, M.A.J.D., & Sales, A., 2020. Assessing the histological changes in fish gills as environmental bioindicators in Paraty and Sepetiba bays in Rio de Janeiro, Brazil. Lat. Am. J. Aquat. Res. 48(4), 590-601. http://dx.doi.org/10.3856/vol48-issue4-fulltext-2351.
http://dx.doi.org/10.3856/vol48-issue4-f...
), allowing evaluation to directly of the influence of river surroundings on aquatic environments (Gerking, 1994Gerking, S.D., 1994. Feeding ecology of fish. J. Anim. Ecol. 64(2), 298-299. https://doi.org/10.2307/5768.
https://doi.org/10.2307/5768...
; Silva et al., 2017Silva, J.C., Gubiani, É.A., Neves, M.P., & Delariva, R.L., 2017. Coexisting small fish species in lotic Neotropical environments: evidence of trophic niche differentiation. Aquat. Ecol. 51(2), 275-288. http://dx.doi.org/10.1007/s10452-017-9616-5.
http://dx.doi.org/10.1007/s10452-017-961...
). The forests around the rivers are transition zones between terrestrial and aquatic ecosystems, acting in processes that involve the transfer of energy and matter between these environments (Pusey & Arthington, 2003Pusey, B.J., & Arthington, A.H., 2003. Importance of the riparian zone to the conservation and management of freshwater fish: a review. Mar. Freshw. Res. 54(1), 1. http://dx.doi.org/10.1071/MF02041.
http://dx.doi.org/10.1071/MF02041...
)⁠. Also, act as an important food source for fish - trunks, branches, leaves, fruits, seeds, and invertebrates (Gonçalves et al., 2018Gonçalves, C.S., Braga, F.M.S., & Casatti, L., 2018. Trophic structure of coastal freshwater stream fishes from an Atlantic rainforest: evidence of the importance of protected and forest-covered areas to fish diet. Environ. Biol. Fishes 101(6), 933-948. http://dx.doi.org/10.1007/s10641-018-0749-8.
http://dx.doi.org/10.1007/s10641-018-074...
).

Assessing fish feeding, it is also possible to organize species into trophic guilds according to the exploited food resources (Gerking, 1994Gerking, S.D., 1994. Feeding ecology of fish. J. Anim. Ecol. 64(2), 298-299. https://doi.org/10.2307/5768.
https://doi.org/10.2307/5768...
). Species that belong to the same trophic guild play trophic similarity in a community (Root, 1967Root, R.B., 1967. The niche exploitation pattern of the blue-gray gnatcatcher. Ecol. Monogr. 37(4), 317-350. http://dx.doi.org/10.2307/1942327.
http://dx.doi.org/10.2307/1942327...
). Thus, knowing the trophic guilds that make up the community can elucidate the dynamics of food chains and the structure of the community (Liu et al., 2019Liu, F., Wang, X., Wang, M., Liu, H., & Wang, J., 2019. Diet partitioning and trophic guild structure of fish assemblages in Chishui River, the last undammed tributary of the upper Yangtze River. China River Res Applic. 35(9), 1530-1539. http://dx.doi.org/10.1002/rra.3519.
http://dx.doi.org/10.1002/rra.3519...
). Therefore, when it comes to protected areas, understanding the diet and trophic guilds of the fish community is of paramount importance. This information can contribute as a monitoring tool for these sites, ensuring the protection of native species and the resources necessary for their survival and development (Hassler, 2005Hassler, M.L., 2005. The importance of the units of conservation in Brazil. Soc. Nat. (Online), 17(33), 79-89. Retrieved in 2021, October 29, from http://www.redalyc.org/articulo.oa?id=321327187006
http://www.redalyc.org/articulo.oa?id=32...
; Luz & Elias, 2014Luz, A.P., & Elias, H.T., 2014. Pesquisa científica em unidades de conservação. Revista Epagri (Online), 27(1), 21-24. Retrieved in 2021, October 29, from https://publicacoes.epagri.sc.gov.br/RAC/article/download/591/494
https://publicacoes.epagri.sc.gov.br/RAC...
). That said, we characterized the diet and trophic guild to the fish community in a conservation unit, seeking to answer the composition of the diet and trophic guild of wild fish in a conservation unit. Such a response may provide information about the trophic ecology of a poorly studied protected area.

2. Material and Methods

2.1. Study area

The Paraná River constitutes the second-largest hydrographic basin in South America (Hales & Petry, 2019Hales, J., & Petry, P., 2019. Freshwater ecorregions of the wold [online]. TNC & WWF. Retrieved in 2021, October 29, from https://www.feow.org/ecoregions/details/344
https://www.feow.org/ecoregions/details/...
)⁠. From its origin, at the confluence of the Paranaíba and Grande rivers, to the estuary of the Rio da Prata, it travels approximately 4.700 km, covering 2.8 million km2 that drain about 10% of the Brazilian territory (Agostinho et al., 2007Agostinho, A.A., Pelicice, F.M., Petry, A.C., Gomes, L.C., & Júlio Junior, H.F., 2007. Fish diversity in the Upper Paraná River Basin: habitats, fisheries, management, and conservation. Aquat. Ecosyst. Health Manage. 10(e2), 174-186. http://dx.doi.org/10.1080/14634980701341719.
http://dx.doi.org/10.1080/14634980701341...
; Agostinho & Gomes, 2005Agostinho, A.A., & Gomes, L.C., 2005. O manejo da pesca em reservatórios da Bacia do Alto Rio Paraná: avaliação e perspectivas, In: Nogueira, M.G., Henry, R., & Jorcin, A. eds. Ecologia de reservatórios: impactos potenciais, ações de manejo e sistemas em cascata. São Carlos: RiMa, 472.; Hales & Petry, 2019Hales, J., & Petry, P., 2019. Freshwater ecorregions of the wold [online]. TNC & WWF. Retrieved in 2021, October 29, from https://www.feow.org/ecoregions/details/344
https://www.feow.org/ecoregions/details/...
)⁠. The upper Paraná Basin is the most intensively dammed among the basins of South America, drains an area with large urban, industrial, and agricultural centers, and constitutes the most explored region in the country (Agostinho & Gomes, 2005Agostinho, A.A., & Gomes, L.C., 2005. O manejo da pesca em reservatórios da Bacia do Alto Rio Paraná: avaliação e perspectivas, In: Nogueira, M.G., Henry, R., & Jorcin, A. eds. Ecologia de reservatórios: impactos potenciais, ações de manejo e sistemas em cascata. São Carlos: RiMa, 472.)⁠.

The study area comprises the Refúgio Biológico de Santa Helena (RBSH) in the Paraná Hydrographic Basin III (Figure 1). The RBSH is a private environmental protection area belonging to the company Itaipu Binacional, part of the Permanent Preservation Area of Lake Itaipu. The RBSH has an area of 1.482 ha, classified as an Area of Relevant Ecological Interest, a Conservation Unit for Sustainable Use. These areas aim to conserve natural ecosystems of regional/local importance and regulate the use of these areas, allowing for research activities, environmental monitoring, inspection, and restricted visitation. The area is considered a priority for conservation by the Ministry of the Environment, as it is an integral part of the Iguaçu-Paraná Biodiversity Corridor (Santa Helena, 2010Santa Helena. Prefeitura Municipal, 2010. Plano de manejo – área de relevante interesse ecológico – Santa Helena. Revisão 2010. Santa Helena: Prefeitura Municipal.).

Figure 1
Study area with the location of sampling points in the Refúgio Biológico de Santa Helena, Itaipu Reservoir, Paraná III River Basin, Brazil.

The sampling areas comprise three points on the Paraná River, inserted in the conservation area (RBSH 01 [24°48’31.82”S; 54°21’0.24”W], RBSH 02 [24°49’39.84”S; 54°21’32.87”W] and RBSH 03 [24°51’14.54”S; 54°21’24.27”W]) (Figure 1). Details about the sampling points can be found in Table 1.

Table 1
Physiographic characteristics of the sampling points around Refúgio Biológico de Santa Helena, Itaipu Reservoir, Paraná III River Basin, Brazil, in which, RBSH = Refúgio Biológico de Santa Helena.

2.2. Collection of biological material

The collections of the fish specimens were carried out in the years 2017 and 2018, with the help of gill nets (3, 4, 5, 6, 7, 8, 10, 12, 14 cm between knots not adjacent). The species collected were: Trachelyopterus galeatus (Linnaeus, 1766), Hoplias malabaricus (Bloch, 1794), Serrasalmus maculatus (Kner, 1858), Serrasalmus marginatus (Valenciennes, 1837), Schizodon borellii (Boulenger, 1900), and Plagioscion squamosissimus (Heckel, 1840).

The collected specimens were euthanized in a 0.5% benzocaine solution, individualized, and stored in polyethylene thermal boxes (Authorization SISBIO nº 57181 -2, CEUA-UTFPR 2016/031 and SisGen A186700). The standard length (cm) and total weight (g) of all specimens were measured, the stomachs were removed, fixed in a 4% formaldehyde solution, and preserved in 70% alcohol.

2.3. Laboratory analysis

The contents of the stomachs were examined in a stereomicroscope and microscope when needed, and the food items were identified to the lowest possible taxonomic level, using identification keys Bicudo & Bicudo (1970)Bicudo, C.E.M. & Bicudo, R.M.T., 1970. Algas de águas continentais brasileiras: chave ilustrada para identificação de gêneros. São Paulo: Fundação Brasileira para o Desenvolvimento do Ensino de Ciências. for algae, Mugnai et al. (2010)Mugnai, R., Nessimian, J., & Baptista, D., 2010. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro: para atividades técnicas, de ensino e treinamento em programas. Rio de Janeiro: Technical Books Editora. for invertebrates and Ota et al. (2018)Ota, R.R., Deprá, G.C., Graça, W.J., & Pavanelli, C.S., 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop. Ichthyol. 16(2), 1-111. http://dx.doi.org/10.1590/1982-0224-20170094.
http://dx.doi.org/10.1590/1982-0224-2017...
for fish. Food items were quantified according to the volumetric method (the displacement by each measured food item in some graduated measuring utensil) (Hyslop, 1980Hyslop, E.J., 1980. Stomach contents analysis: a review of methods and their application. J. Fish Biol. 17(4), 411-429. http://dx.doi.org/10.1111/j.1095-8649.1980.tb02775.x.
http://dx.doi.org/10.1111/j.1095-8649.19...
). In this case, used were a gridded Petri dish for smaller food items and a graduated beaker, for larger food items, as proposed by Hellawell & Abel (1971)Hellawell, J.M., & Abel, R., 1971. A rapid volumetric method for the analysis of the food of fishes. J. Fish Biol. 3(1), 29-37. http://dx.doi.org/10.1111/j.1095-8649.1971.tb05903.x.
http://dx.doi.org/10.1111/j.1095-8649.19...
.

2.4. Data analysis

A minimum of seven specimens per species was used as the criteria for the inclusion of the species in all analyses. The characterization of the diet was presented through the percentage volume of each food consumed calculated in the Excel program (Microsoft). The items were classified as autochthonous (originating from the aquatic environment), allochthonous (originating from the terrestrial environment), and undetermined (Silva et al., 2017Silva, J.C., Gubiani, É.A., Neves, M.P., & Delariva, R.L., 2017. Coexisting small fish species in lotic Neotropical environments: evidence of trophic niche differentiation. Aquat. Ecol. 51(2), 275-288. http://dx.doi.org/10.1007/s10452-017-9616-5.
http://dx.doi.org/10.1007/s10452-017-961...
). To determination of the trophic guild of each species, the predominance of a type of food resource (≥ 51% of the total volume) in the population’s diet was considered (adapted from Corrêa et al., 2011Corrêa, C.E., Albrecht, M.P., & Hahn, N.S., 2011. Patterns of niche breadth and feeding overlap of the fish fauna in the seasonal Brazilian Pantanal, Cuiabá River Basin. Neotrop. Ichthyol. 9(3), 637-646. http://dx.doi.org/10.1590/S1679-62252011000300017.
http://dx.doi.org/10.1590/S1679-62252011...
): herbivore, ≥ 51% vegetable items in the stomachs; terrestrial insectivore, ≥ 51% terrestrial insects in the stomachs; piscivore, ≥ 51% fish fragments in the stomachs and carcinophage, ≥ 51% decapods.

Specimens were deposited in the Ichthyological Collection of Federal University of Technology – Paraná State, UTFPR, Santa Helena Campus (P. squamosissimus CISH 148TB), as well as in the Ichthyological Collection of Núcleo de Pesquisa em Limnologia, Ictiologia e Aquicultura, NUPÉLIA (H. malabaricus NUP 23044, S. borellii NUP 23037, S. marginatus NUP 23028, S. maculatus NUP 23030 and T. galeatus NUP 23107).

3. Results

The stomach contents of 138 individuals belonging to six species and five families (Table 2), were analyzed. Trachelyopterus galeatus, H. malabaricus and S. maculatus are native species, and S. marginatus, S. borellii, and P. squamosissimus are non-native species (Table 2).

Table 2
Species, origin, number of stomachs analyzed (n), standard length (Sl), and weight (Wt) of the individuals sampled in the Refúgio Biológico de Santa Helena, Itaipu Reservoir, Paraná III River Basin, Brazil. Mean (ME) and Standard deviation (SD), followed by the minimum and maximum values.

The species diets were composed of allochthonous and autochthonous resources. We observed a predominance in the consumption of decapods, fish fragments, terrestrial insects, and aquatic plants (Table 3; Figure 2).

Table 3
Diet composition in the percentage of volume for Plagioscion squamosissimus (Pss), Trachelyopterus galeatus (Tg), Schizodon borellii (Sb), Hoplias malabaricus (Hm), Serrasalmus maculatus (Sm), Serrasalmus marginatus (Smr), in the Refúgio Biológico de Santa Helena, Itaipu Reservoir, Paraná III River Basin, Brazil.
Figure 2
Volume percentage (%) of food items consumed by fish species and their trophic guild in the Refúgio Biológico de Santa Helena, Itaipu Reservoir, Paraná III River Basin, Brazil. Hoplias malabaricus (Hm), Plagioscion squamosissimus (Pss), Schizodon borellii (Sb), Serrasalmus maculatus (Sm), Serrasalmus marginatus (Smr), Trachelyopterus galeatus (Tg), PISC = Piscivore, CARC = Carcinofage, HERB = Herbivore, TINS = Terrestrial insectivore.

We also report the occurrence of microplastics in the diet of T. galeatus, S. borellii, and S. maculatus (Table 3). For T. galeatus (7 stomachs) and S. maculatus (5 stomachs) microplastics were observed only in RBSH 1. For S. borelli (3 stomachs) only in RBSH 2.

Trachelyopterus galeatus consumed mainly Coleoptera adult (29.24%), terrestrial insect (27.16%), and Hymenoptera (11.6%) being classified a terrestrial insectivore (Figure 2). Hoplias malabaricus, S. maculatus, and S. marginatus were classified as piscivores due to the high consumption of fish fragments (78.81%, 82.87%, and 72.9%, respectively) (Figure 2). Schizodon borellii mainly consumed aquatic plants (76.96%) and algae (1.84%), being classified as herbivores (Figure 2), and P. squamosissimus consumed 90.52% of decapods, so it was classified as a carcinophages (Figure 2).

4. Discussion

The fish community evaluated here consumed items of autochthonous and allochthonous origin, representing different trophic guilds. Trachelyopterus galeatus consumed Coleoptera, Hymenoptera, and other insect fragments, as observed in other studies (Garcia et al., 2018Garcia, D.A.Z., Vidotto-Magnoni, A.P., & Orsi, M.L., 2018. Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats. Aquat. Invasions 13(e4), 565-573. http://dx.doi.org/10.3391/ai.2018.13.4.13.
http://dx.doi.org/10.3391/ai.2018.13.4.1...
; Peretti & Andrian, 2004Peretti, D., & Andrian, I.F., 2004. Trophic structure of fish assemblages in five permanent lagoons of the high Paraná River floodplain, Brazil. Environ. Biol. Fishes 71(1), 95-103. http://dx.doi.org/10.1023/B:EBFI.0000043155.76741.a1.
http://dx.doi.org/10.1023/B:EBFI.0000043...
, 2008Peretti, D., & Andrian, I.F., 2008. Feeding and morphological analysis of the digestive tract of four species of fish (Astyanax altiparanae, Parauchenipterus galeatus, Serrasalmus marginatus, and Hoplias aff. malabaricus) from the Upper Paraná River floodplain, Brazil. Braz. J. Biol. 68(3), 671-679. PMid:18833491. http://dx.doi.org/10.1590/S1519-69842008000300027.
http://dx.doi.org/10.1590/S1519-69842008...
; Tonella et al., 2018Tonella, L.H., Fugi, R., Vitorino Junior, O.B., Suzuki, H.I., Gomes, L.C., & Agostinho, A.A., 2018. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817(1), 239-252. http://dx.doi.org/10.1007/s10750-017-3404-z.
http://dx.doi.org/10.1007/s10750-017-340...
). Garcia et al. (2018)Garcia, D.A.Z., Vidotto-Magnoni, A.P., & Orsi, M.L., 2018. Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats. Aquat. Invasions 13(e4), 565-573. http://dx.doi.org/10.3391/ai.2018.13.4.13.
http://dx.doi.org/10.3391/ai.2018.13.4.1...
and Tonella et al. (2018)Tonella, L.H., Fugi, R., Vitorino Junior, O.B., Suzuki, H.I., Gomes, L.C., & Agostinho, A.A., 2018. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817(1), 239-252. http://dx.doi.org/10.1007/s10750-017-3404-z.
http://dx.doi.org/10.1007/s10750-017-340...
, classified this species as omnivorous due to the consumed of plants and animals (fish and invertebrates), however, Parauchenipterus galeatus (Linnaeus, 1766) (=T. galeatus) consumed much more terrestrial insects than plants and other animals, so it was considered a terrestrial insectivore, corroborating our study. S. borellii showed a predominantly plant-based diet, corroborating other studies which classified it as a herbivore (Ferretti et al., 1996Ferretti, C.M.L., Adrian, I.F. & Torrente, G., 1996. Dieta de duas espécies de Schizodon (Characiformes, Anostomidae), na planície de inundação do Alto Rio Paraná e suas relações com aspectos morfológicos. Bol. Inst. Pesca 23, 171-186.; Pereira & Resende, 2002Pereira, R.A.C. & Resende, E.K., 2002. Peixes herbívoros da planície inundável do Rio Miranda, Pantanal, Mato grosso do Sul, Brasil. Corumbá: Embrapa-CPAP. Embrapa-CPAP. Boletim de Pesquisa, vol. 12.)⁠. However, we also report the consumption of Bivalvia, Crustacea, and detritus such as Peretti & Andrian (2004)Peretti, D., & Andrian, I.F., 2004. Trophic structure of fish assemblages in five permanent lagoons of the high Paraná River floodplain, Brazil. Environ. Biol. Fishes 71(1), 95-103. http://dx.doi.org/10.1023/B:EBFI.0000043155.76741.a1.
http://dx.doi.org/10.1023/B:EBFI.0000043...
. Thus, we observed that T. galeatus and S. borellii presented ample trophic plasticity, managing to take advantage of more available items when foraging (Gerking, 1994Gerking, S.D., 1994. Feeding ecology of fish. J. Anim. Ecol. 64(2), 298-299. https://doi.org/10.2307/5768.
https://doi.org/10.2307/5768...
).

The three species of piscivores evaluated here (H. malabaricus, S. marginatus, and S. maculatus) mainly consumed fish fragments but also consumed plants, insects, decapods, and Bivalvia, as observed in other studies (Bozza & Hahn, 2010Bozza, A.N., & Hahn, N.S., 2010. Uso de recursos alimentares por peixes imaturos e adultos de espécies piscívoras em uma planície de inundação neotropical. Biota Neotrop. 10(3), 217-226. http://dx.doi.org/10.1590/S1676-06032010000300025.
http://dx.doi.org/10.1590/S1676-06032010...
; Garcia et al., 2018Garcia, D.A.Z., Vidotto-Magnoni, A.P., & Orsi, M.L., 2018. Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats. Aquat. Invasions 13(e4), 565-573. http://dx.doi.org/10.3391/ai.2018.13.4.13.
http://dx.doi.org/10.3391/ai.2018.13.4.1...
; Peretti & Andrian, 2004Peretti, D., & Andrian, I.F., 2004. Trophic structure of fish assemblages in five permanent lagoons of the high Paraná River floodplain, Brazil. Environ. Biol. Fishes 71(1), 95-103. http://dx.doi.org/10.1023/B:EBFI.0000043155.76741.a1.
http://dx.doi.org/10.1023/B:EBFI.0000043...
, 2008Peretti, D., & Andrian, I.F., 2008. Feeding and morphological analysis of the digestive tract of four species of fish (Astyanax altiparanae, Parauchenipterus galeatus, Serrasalmus marginatus, and Hoplias aff. malabaricus) from the Upper Paraná River floodplain, Brazil. Braz. J. Biol. 68(3), 671-679. PMid:18833491. http://dx.doi.org/10.1590/S1519-69842008000300027.
http://dx.doi.org/10.1590/S1519-69842008...
; Santana-Porto & Andrian, 2009Santana-Porto, E.A., & Andrian, I.F., 2009. Trophic organization the ichthyofauna of two semilentic environments in a flood plain on the Upper Paraná River, Brazil. Acta Limnol. Bras. 21, 359-366.; Tonella et al., 2018Tonella, L.H., Fugi, R., Vitorino Junior, O.B., Suzuki, H.I., Gomes, L.C., & Agostinho, A.A., 2018. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817(1), 239-252. http://dx.doi.org/10.1007/s10750-017-3404-z.
http://dx.doi.org/10.1007/s10750-017-340...
). Considering that plants were found in small quantities, we inferred that the consumption of these items was an accidental act due to the predatory behavior of these species (Behr & Signor, 2008Behr, E.R., & Signor, C.A., 2008. Distribuição e alimentação de duas espécies simpátricas de piranhas Serrasalmus maculatus e Pygocentrus nattereri (Characidae, Serrasalminae) do rio Ibicuí, Rio Grande do Sul, Brasil. Iheringia Ser. Zool. 98(4), 501-507. http://dx.doi.org/10.1590/S0073-47212008000400014.
http://dx.doi.org/10.1590/S0073-47212008...
; Costa et al., 2005Costa, A.C., Salvador Junior, L.F., Domingos, F.F.T., & Fonseca, M.L., 2005. Alimentação da pirambeba Serrasalmus spilopleura Kner, 1858 (Characidae; Serrasalminae) em um reservatório do Sudeste brasileiro. Acta Sci. Biol. Sci. 27(4), 365-369. http://dx.doi.org/10.4025/actascibiolsci.v27i4.1331.
http://dx.doi.org/10.4025/actascibiolsci...
; Garcia et al., 2018Garcia, D.A.Z., Vidotto-Magnoni, A.P., & Orsi, M.L., 2018. Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats. Aquat. Invasions 13(e4), 565-573. http://dx.doi.org/10.3391/ai.2018.13.4.13.
http://dx.doi.org/10.3391/ai.2018.13.4.1...
; Moraes & Bárbola, 1995Moraes, M.F.P., & Bárbola, I.F., 1995. Hábito alimentar e morfologia do tubo digestivo de Haplias malabaricus (Osteichthyes, Elythrinidae) da Lagoa Dourada, Ponta Grossa, Paraná, Brasil. Acta Biol. Parana. 24, 1-23. http://dx.doi.org/10.5380/abpr.v24i0.700.
http://dx.doi.org/10.5380/abpr.v24i0.700...
; Peretti & Andrian, 2008Peretti, D., & Andrian, I.F., 2008. Feeding and morphological analysis of the digestive tract of four species of fish (Astyanax altiparanae, Parauchenipterus galeatus, Serrasalmus marginatus, and Hoplias aff. malabaricus) from the Upper Paraná River floodplain, Brazil. Braz. J. Biol. 68(3), 671-679. PMid:18833491. http://dx.doi.org/10.1590/S1519-69842008000300027.
http://dx.doi.org/10.1590/S1519-69842008...
)⁠.

Plagioscion squamosissimus diet was composed mainly of shrimp and classified as carcinophages. According to Garcia, et al. (2018)Garcia, D.A.Z., Vidotto-Magnoni, A.P., & Orsi, M.L., 2018. Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats. Aquat. Invasions 13(e4), 565-573. http://dx.doi.org/10.3391/ai.2018.13.4.13.
http://dx.doi.org/10.3391/ai.2018.13.4.1...
, P. squamosissimus was considered a specialist in shrimp in a lentic environment. In addition, there are reports of environmental and ontogenetic variation in the diet with the consumption of fish and other aquatic invertebrates (Bozza & Hahn, 2010Bozza, A.N., & Hahn, N.S., 2010. Uso de recursos alimentares por peixes imaturos e adultos de espécies piscívoras em uma planície de inundação neotropical. Biota Neotrop. 10(3), 217-226. http://dx.doi.org/10.1590/S1676-06032010000300025.
http://dx.doi.org/10.1590/S1676-06032010...
; Neves et al., 2015Neves, M.P., Delariva, R.L., Guimarães, A.T.B., & Sanches, P.V., 2015. Carnivory during Ontogeny of the Plagioscion squamosissimus: a successful non-native fish in a lentic environment of the Upper Paraná River Basin. PLoS One 10(11), 1-15. PMid:26524336. http://dx.doi.org/10.1371/journal.pone.0141651.
http://dx.doi.org/10.1371/journal.pone.0...
), demonstrating that feeding can change according to energy requirements and availability resources (Bennemann et al., 2006Bennemann, S.T., Capra, L.G., Galves, W., & Shibatta, O.A., 2006. Dinâmica trófica de Plagioscion squamosissimus (Perciformes, Sciaenidae) em trechos de influência da represa Capivara (rios Paranapanema e Tibagi). Iheringia Ser. Zool. 96(1), 115-119. http://dx.doi.org/10.1590/S0073-47212006000100020.
http://dx.doi.org/10.1590/S0073-47212006...
; Cardoso et al., 2019Cardoso, D.C., Dehart, P., Freitas, C.E.D.C., & Siqueira-Souza, F.K., 2019. Diet and ecomorphology of predator fish species of the Amazonian floodplain lake. Biota Neotrop. 19(3), e20180678. http://dx.doi.org/10.1590/1676-0611-bn-2018-0678.
http://dx.doi.org/10.1590/1676-0611-bn-2...
). Opportunistic behavior is reported for some Neotropical fish that can take advantage of the most abundant food source in time and space, consuming resources according to their availability and preferences (Abelha et al., 2001Abelha, M.F.C., Agostinho, A.A., & Goulart, E., 2001. Plasticidade trófica em peixes de água doce. Acta Scientiarum 23(e2), 425-434. https://doi.org/10.1007/s12562-010-0271-1.
https://doi.org/10.1007/s12562-010-0271-...
; Dias et al., 2017Dias, R.M., Ortega, J.C.G., Gomes, L.C., & Agostinho, A.A., 2017. Relações tróficas em assembleia de peixes em lagoas de planície de inundação Neotropical: seletividade e sobreposição alimentar mediada pela disponibilidade de recursos alimentares. Iheringia Ser. Zool. 107, 1-11. https://doi.org/10.1590/1678-4766E2017035.
https://doi.org/10.1590/1678-4766E201703...
; Gerking, 1994Gerking, S.D., 1994. Feeding ecology of fish. J. Anim. Ecol. 64(2), 298-299. https://doi.org/10.2307/5768.
https://doi.org/10.2307/5768...
; Pereira et al., 2016Pereira, L.S., Agostinho, A.A., & Delariva, R.L., 2016. Effects of river damming in Neotropical piscivorous and omnivorous fish: Feeding, body condition, and abundances. Neotrop. Ichthyol. 14(1), 267-278. http://dx.doi.org/10.1590/1982-0224-20150044.
http://dx.doi.org/10.1590/1982-0224-2015...
).

The consumption of items from various sources and the trophic guilds classified in this work demonstrate that the fish community evaluated belongs to different trophic levels. Each trophic level plays a role in maintaining the ecosystem (Díaz & Cabido, 2001Díaz, S., & Cabido, M., 2001. Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol. Evol. 16(11), 646-655. http://dx.doi.org/10.1016/S0169-5347(01)02283-2.
http://dx.doi.org/10.1016/S0169-5347(01)...
), essential for the maintenance of conservation units. The carnivorous fish that are represented here as terrestrial insectivores, piscivores, and carcinophages, have a functional role in the population control of invertebrates and vertebrates (Manna et al., 2013Manna, L.R., Rezende, C.F., & Mazzoni, R., 2013. Diversidade funcional de peixes de riacho: como as assembleias podem estar organizadas? Oecol. Aust. 17(3), 402-410. http://dx.doi.org/10.4257/oeco.2013.1703.08.
http://dx.doi.org/10.4257/oeco.2013.1703...
)⁠. Carnivorous fishes promote long-term selective pressure and helping to increase species diversity (Townsend et al., 2011Townsend, C.R., Begon, M., & Harper J.L., 2011. Fundamentos em ecologia. Porto Alegre: Artmed, 3 ed.). Herbivorous fish, represented here by S. borellii, contribute to the entry of nutrients into the food chain in that area, cycling nutrients from plants, such as nitrogen and phosphorus (Hulot et al., 2000Hulot, F.D., Lacroix, G., Lescher-Moutoué, F., & Loreau, M., 2000. Functional diversity governs ecosystem response to nutrient enrichment. Nature 405(6784), 340-344. PMid:10830961. http://dx.doi.org/10.1038/35012591.
http://dx.doi.org/10.1038/35012591...
; Manna et al., 2013Manna, L.R., Rezende, C.F., & Mazzoni, R., 2013. Diversidade funcional de peixes de riacho: como as assembleias podem estar organizadas? Oecol. Aust. 17(3), 402-410. http://dx.doi.org/10.4257/oeco.2013.1703.08.
http://dx.doi.org/10.4257/oeco.2013.1703...
).

Here, three non-native species were analyzed (S. marginatus (piscivores), P. squamosissimus (carcinophages), and S. borellii (herbivores)). Although trophic guilds contribute to population control of some species or nutrient cycling, non-native species can compete for food resources with native species (Gallardo et al., 2016Gallardo, B., Clavero, M., Sánchez, M.I., & Vilà, M., 2016. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22(1), 151-163. PMid:26212892. http://dx.doi.org/10.1111/gcb.13004.
http://dx.doi.org/10.1111/gcb.13004...
). Soon after their introduction, non-native species have a competitive advantage over native species due to the absence of natural predators in the invaded environment, which can lead to their establishment and population increase (Britton, 2019Britton, J.R., 2019. Empirical predictions of the trophic consequences of non-native freshwater fishes: a synthesis of approaches and invasion impacts. Turk. J. Fish. Aquat. Sci. 19(6), 529-539. http://dx.doi.org/10.4194/1303-2712-v19_6_09.
http://dx.doi.org/10.4194/1303-2712-v19_...
; De La Torre Zavala et al., 2018De La Torre Zavala, A.M., Arce, E., Luna-Figueroa, J., & Córdoba-Aguilar, A., 2018. Native fish, Cichlasoma istlanum, hide for longer, move and eat less in the presence of a non-native fish, Amatitlania nigrofasciata. Environ. Biol. Fishes 101(6), 1077-1082. http://dx.doi.org/10.1007/s10641-018-0761-z.
http://dx.doi.org/10.1007/s10641-018-076...
) and decrease the population of native species (Gallardo et al., 2016Gallardo, B., Clavero, M., Sánchez, M.I., & Vilà, M., 2016. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22(1), 151-163. PMid:26212892. http://dx.doi.org/10.1111/gcb.13004.
http://dx.doi.org/10.1111/gcb.13004...
; Levis et al., 2013Levis, C., Ramos, T.P.A., & Lima, S.M.Q., 2013. A disputa desigual entre peixes nativos e exóticos do semiárido. Natal: EDUFRN.). Agostinho et al. (2003)Agostinho, C.S., Hahn, N.S., & Marques, E.E., 2003. Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the Upper Paraná River Floodplain. Braz. J. Biol. 63(2), 177-182. PMid:14509839. http://dx.doi.org/10.1590/S1519-69842003000200002.
http://dx.doi.org/10.1590/S1519-69842003...
⁠, has shown this impact with an experiment between the non-native piranha (S. marginatus) and native (Serrasalmus spilopleura Kner, 1958 (= S. maculatus) species in the upper Paraná River, where there was competition. The authors noted that due the greater advantage of the non-native species, the population of native piranhas decreased (Agostinho et al., 2003Agostinho, C.S., Hahn, N.S., & Marques, E.E., 2003. Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the Upper Paraná River Floodplain. Braz. J. Biol. 63(2), 177-182. PMid:14509839. http://dx.doi.org/10.1590/S1519-69842003000200002.
http://dx.doi.org/10.1590/S1519-69842003...
).

Another relevant aspect was the occurrence of microplastics in the diet of some species in the RBSH 1 and RBSH 2. This record is worrying since the conservation unit is located close to the urban area, demonstrating the current problem of plastic contamination in freshwater biota, associated with urbanization (Azevedo-Santos et al., 2019Azevedo-Santos, V.M., Gonçalves, G.R.L., Manoel, P.S., Andrade, M.C., Lima, F.P., & Pelicice, F.M., 2019. Plastic ingestion by fish: a global assessment. Environ. Pollut. 255(Pt 1), 112994. PMid:31541837. http://dx.doi.org/10.1016/j.envpol.2019.112994.
http://dx.doi.org/10.1016/j.envpol.2019....
; Pinheiro et al., 2017Pinheiro, C., Oliveira, U., & Vieira, M., 2017. Occurrence and impacts of microplastics in freshwater fish. J. Aquac. Mar. Biol. 5(6), 00138. https://doi.org/10.15406/jamb.2017.05.00138.
https://doi.org/10.15406/jamb.2017.05.00...
; Silva-Cavalcanti et al., 2017Silva-Cavalcanti, J.S., Silva, J.D.B., França, E.J., Araújo, M.C.B., & Gusmão, F., 2017. Microplastics ingestion by a common tropical freshwater fishing resource. Environ. Pollut. 221, 218-226. PMid:27914860. http://dx.doi.org/10.1016/j.envpol.2016.11.068.
http://dx.doi.org/10.1016/j.envpol.2016....
). The consumption of microplastics by fish promotes several negative physiological effects (Fu et al., 2020Fu, Z., Chen, G., Wang, W., & Wang, J., 2020. Microplastic pollution research methodologies, abundance, characteristics and risk assessments for aquatic biota in China. Environ. Pollut. 266(Pt 3), e115098. PMid:32629309. http://dx.doi.org/10.1016/j.envpol.2020.115098.
http://dx.doi.org/10.1016/j.envpol.2020....
; Lönnstedt & Eklöv, 2016Lönnstedt, O.M., & Eklöv, P., 2016. Environmentally relevant concentrations of microplastic particles influence larval fish ecology. Science 352(6290), 1213-1216. PMid:27257256. http://dx.doi.org/10.1126/science.aad8828.
http://dx.doi.org/10.1126/science.aad882...
), and due to their characteristics, they can reach fish of all levels of development (Azevedo-Santos et al., 2019Azevedo-Santos, V.M., Gonçalves, G.R.L., Manoel, P.S., Andrade, M.C., Lima, F.P., & Pelicice, F.M., 2019. Plastic ingestion by fish: a global assessment. Environ. Pollut. 255(Pt 1), 112994. PMid:31541837. http://dx.doi.org/10.1016/j.envpol.2019.112994.
http://dx.doi.org/10.1016/j.envpol.2019....
).

As it is a conservation unit, knowing the trophic guilds that make up the fish community can contribute to understanding the dynamics of food chains, the structure of the community, and the functioning of the ecosystem. In addition, the occurrence of microplastics reported here raises the issue about the contamination of conservation units in aquatic environments, since there is no way to contain the effluents coming from urban areas, for example. Finally, this work can contribute information about the biology of the species evaluated for future work and conservation programs.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES- Finance Code 001) and was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (process 402670/2016-7 financial support; process 52196/2019-0 scholarship of the 1st author J.K.K.R.; process 52654/2019-0 scholarship of the 3rd author V.C.B.; process CNPq 140754/2019-9 scholarship of the 6th author C.D.P.; process 303311/2018-5 productivity scholarship of the last author I.P.R.) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process 2018/01117-2 of the 5th author B.C.K.K). We would like to thank the people from the Faculdade de Engenharia de Ilha Solteira (FEIS), Universidade Estadual Paulista (UNESP) and Universidade Tecnológica do Paraná (UTFPR) for the use of laboratory facilities and logistics. Specially the Laboratório de Ecologia de Peixe (Pirá/UNESP) and Grupos de Estudos em Ictiologia Neotropical (GEIN/UTFPR).

  • Cite as: Ramos, J.K.K et al. Characterization of wild fish diet and trophic guild in a pro-tected area. Acta Limnologica Brasiliensia, 2022, vol. 34, e15.

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Publication Dates

  • Publication in this collection
    03 June 2022
  • Date of issue
    2022

History

  • Received
    20 Jan 2022
  • Accepted
    13 May 2022
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