Abstract

To characterize the diet composition of Moenkhausia bonita and its temporal and ontogenetic variations in streams in the Formoso River basin (MS). The collections were carried out in seven sampling points in two periods throughout the year (dry and rainy). The food items were analyzed according to the volumetric and occurrence frequency methods and the diet was characterized through the Food Index (IAi%). To determine ontogeny, the specimens were divided into five size classes in the dry (D1 to D5) and rainy (R1 to R5) periods. To verify the difference between the species’ diet between the size classes and the periods of the year, the Permutational Multivariate Analysis of Variance – PERMANOVA analysis was performed. Moenkhausia bonita was classified as an invertivore when it consumed basically both aquatic and terrestrial invertebrates (99.5% of the diet), with higher consumption of aquatic invertebrates. There was a significant difference in the diet of between the dry and rainy periods, and although the species basically consumed the same items in the two studied periods, the proportions were different and there was no difference in the diet between size classes. M. bonita diet is based on autochthonous resources regardless of the size class, but that there were different consumption patterns when comparing the different periods of the year. The present study provided the first information on the feeding of M. bonita in a lotic environment and diet spectrum in the developmental phases, (ontogeny) and periods of the year, enabling a better understanding of the species, the importance of invertebrates in its diet, and the need for future studies on the biology, autoecology, and behavior of this species.

Keywords
Feeding; tetra; trophic category; ontogeny

Resumo

Caracterizar a composição alimentar de Moenkhausia bonita e as variações temporais e ontogenéticas na dieta desta espécie em riachos da bacia do rio Formoso (MS). As coletas foram realizadas em sete pontos amostrais em dois períodos do ano (seco e chuvoso). Os itens alimentares foram analisados de acordo com os métodos volumétrico e de frequência de ocorrência e a dieta foi caracterizada através do Índice Alimentar (IAi%). Para determinar a ontogenia, os espécimes foram divididos em cinco classes de tamanho nos períodos seco (D1 a D5) e chuvoso (R1 a R5). Para verificar a diferença entre a dieta da espécie entre as classes de tamanho e os períodos do ano foi realizado a Análise de Variância Multivariada Permutacional – PERMANOVA. M. bonita foi classificada como invertívora ao consumir basicamente invertebrados tanto aquáticos quanto terrestres (99,5% da dieta), com consumo maior de invertebrados aquáticos. Houve diferença significativa na dieta entre os períodos seco e chuvoso, apesar da espécie consumir basicamente os mesmos itens nos dois períodos estudados, as proporções foram distintas e não houve diferença na dieta entre as classes de tamanho. A dieta de M. bonita é baseada em recursos autóctones independente da classe de tamanho, mas que houve consumo diferente entre os períodos do ano. O presente estudo forneceu as primeiras informações sobre a alimentação de M. bonita em ambiente lótico e seu espectro alimentar nas fases de desenvolvimento(ontogenia)e períodos do ano, possibilitando melhor conhecimento da espécie, a importância dos invertebrados em sua dieta e a necessidade de estudos futuros sobre a biologia, autoecologia e comportamento desta espécie.

Palavras-chave
alimentação; lambari; categoria trófica; ontogenia

Introduction

The Neotropical region has the most diverse freshwater ichthy­ofauna in the world, with about 50% of the known fauna (Reis et al. 2016REIS, R.E., ALBERT, J.S., DARIO, F.D., MINCARONE, M.M., PETRY, P. & ROCHA, L.A. 2016. Fish biodiversity and conservation in South America. J. of Fish Biol., 89:12–47.). Brazil is home to great biodiversity of fish (Buckup et al. 2007BUCKUP, P.A., MENEZES, N.A. & GHAZZI, M.S. 2007 (eds.). Catálogo das espécies de peixes de água doce do Brasil. Museu Nacional, Rio de Janeiro, 195p.; Froese et al. 2016FROESE, R., WINKER, H., GASCUEL, D., SUMAILA, U.R., & PAULY, D. 2016. Minimizing the impact of fishing. Fish and Fisheries, 17:785–802.). Most of this richness of fish inhabits inland waters, representing about two-thirds of the ichthyofauna that occurs in this region (Nelson et al. 2016NELSON, J.S., GRANDE, T.C. & WILSON, M.V.H. 2016. Fishes of the world. John Wiley & Sons 5 ed. 752p. ).

The state of Mato Grosso do Sul is drained by the Middle Paraguay River and Upper Paraná River basins, where 358 fishes species have been recorded, 257 species of which are recorded in the Paraguay River basin, (Froehlich et al. 2017FROEHLICH, O., CAVALLARO, M., SABINO, J., SÚAREZ, Y.R. & VILELA, M.J.A. 2017. Checklist da ictiofauna do Estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zoologia., 107 (supl.) doi:10.1590/16784766e2017151
https://doi.org/10.1590/16784766e2017151... ). The Formoso River basin is a sub-basin of the Miranda River, inserted entirely within the municipality of Bonito, a place that presents tourist trend due to its scenic beauty (Teruya-Júnior 2011TERUYA-JUNIOR, H. 2011. Diagnóstico Ambiental da Bacia Hidrográfica do Rio Formoso, MS. Campo Grande. [Dissertação de mestrado em Tecnologias Ambientais] Campo Grande: Universidade Federal de Mato Grosso do Sul.). This region is a reference for ecotourism in the country since most of the tourist attractions are linked to water resources (Lelis et al. 2015LELIS, L.R.M., PINTO, A.L., SILVA, P.V., PIROLI, E.L., MEDEIROS, R.B. & GOMES, W.M. 2015. Qualidade das águas superficiais da bacia hidrográfica do rio Formoso, Bonito – MS. Revista Formação, 22(2):279–302. http://dx.doi.org/10.33081/formacao.v2i22.3151
https://doi.org/10.33081/formacao.v2i22.... ). Few studies have been conducted on the ichthyofauna in the Formoso River basin, such as the composition and structure of the ichthyofauna in streams comparing conservation gradients (Casatti et al. 2010CASATTI, L., ROMERO, R.M., TERESA, F.B., SABINO, J. & LANGEANI, F. 2010. Fish community structure along a conservation gradient in Bodoquena Plateau streams, Central West of Brazil. Acta Limnol. Brasil., 22(1):50–59. doi: 10.4322/actalb.02201007
https://doi.org/10.4322/actalb.02201007... ), the weight-length relationship in stream fishes (Severo-Neto et al. 2018SEVERO-NETO, F., LOPES, D., FERREIRA, A., MARTÍNEZ, B. & ROQUE, F. 2018. Length–weight relations of fishes (Actinopterygii) from karst streams in the Bodoquena Plateau, western Brazil. Acta Ichthyologica Et Piscatoria, [S.L.] 48(4):419–422. http://dx.doi.org/10.3750/AIEP/02500
https://doi.org/10.3750/AIEP/02500... ) and studies of the ecological interactions of fishes with habitat characteristics (Nunes et al. 2020NUNES, L.T., MORAIS, R.A., LONGO, G.O., SABINO, J. & FLOETER, S.R. 2020. Habitat and community structure modulate fish interactions in a neotropical clearwater river. Neotrop. Ichthy, [S.L.], 18(1):1–20. http://dx.doi.org/10.1590/1982-0224-2019-0127
https://doi.org/10.1590/1982-0224-2019-0... ).

Eight species of Moenkhausia are known in the state of Mato Grosso do Sul (Froehlich et al. 2017FROEHLICH, O., CAVALLARO, M., SABINO, J., SÚAREZ, Y.R. & VILELA, M.J.A. 2017. Checklist da ictiofauna do Estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zoologia., 107 (supl.) doi:10.1590/16784766e2017151
https://doi.org/10.1590/16784766e2017151... ). Moenkhausia bonita is a small characid species that have been described in the Baía Bonita River, a tributary of the Formoso River (area of this study) (Benine et al. 2004BENINE, R.C., CASTRO, R.M.C. & SABINO, J. 2004. Moenkhausia bonita: a new small characin fish from the rio Paraguay basin, southwestern Brazil. (Characiformes: Characidae). Copeia., 2004(1):68–73. doi:10.2307/1448639.
https://doi.org/10.2307/1448639.... ). This species occurs mainly near the water surface, swimming in schools of 10 to 30 individuals (Benine et al. 2004BENINE, R.C., CASTRO, R.M.C. & SABINO, J. 2004. Moenkhausia bonita: a new small characin fish from the rio Paraguay basin, southwestern Brazil. (Characiformes: Characidae). Copeia., 2004(1):68–73. doi:10.2307/1448639.
https://doi.org/10.2307/1448639.... ). It is a widely distributed species in the Paraguay River basin but has been recorded in other basins, like La Plata River and Amazon region (Froehlich et al. 2017FROEHLICH, O., CAVALLARO, M., SABINO, J., SÚAREZ, Y.R. & VILELA, M.J.A. 2017. Checklist da ictiofauna do Estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zoologia., 107 (supl.) doi:10.1590/16784766e2017151
https://doi.org/10.1590/16784766e2017151... ; Vanegas-Ríos et al. 2019VANEGAS-RIOS, J.A., BRITZKE, R. & MIRANDE, J.M. 2019. Geographic variation of Moenkhausia bonita (Characiformes: Characidae) in the rio de la Plata basin, with distributional comments on M. intermedia. Neotrop. Ichthyol., 17(1):e170123. https://doi.org/10.1590/1982-0224-20170123
https://doi.org/10.1590/1982-0224-201701... ; Fricke et al. 2020FRICKE, R., ESCHMEYER, W.N. & FONG, J.D. 2020. Espécies por Família / Subfamília., Disponível em: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp
http://researcharchive.calacademy.org/re... ). Moenkhausia bonita isn’t registered on the Red List of endangered species of the Ministry of the Environment (PORTARIA MMA 148/2022) and is classified as Least Concern (LC) according to the International Union for Conservation of Nature (IUCN, 2019).

The differentiation in the diet of a fish species may be due to spatial, temporal, ontogenetic, individual variations, and according to feeding tactics (Abelha et al. 2001ABELHA, M.C.F., AGOSTINHO, A.A. & GOULART, E., 2001. Plasticidade trófica em peixes de água doce. Acta Sci Biol Sci., 23(2):425–434. https://doi.org/10.4025/actascibiolsci.v23i0.2696
https://doi.org/10.4025/actascibiolsci.v... ). In tropical regions, subject to wide seasonal variations in water level, seasonality is one of the main factors influencing changes in fish diet, since it causes qualitative and quantitative changes in the availability of food items in aquatic ecosystems (Junk et al. 1989JUNK, W., BAYLEY, P.B. & SPARKS, R.E. 1989. The Flood Pulse Concept in River –Floodplain Systems. In: Proceedings of the International Large River Symposium (LARS). Ontario: Canada Department of Fisheries and Oceans, 110–127.; Junk et al. 2021JUNK, W.J., CUNHA, N., THOMAZ, S.M., AGOSTINHO, A.A., FERREIRA, F.A., SOUZA-FILHO, E.E., STEVAUX, J.C., SILVA, J.C.B., ROCHA, P.C., & KAWAKITA, K. 2021. Macrohabitat classification of wetlands as a powerful tool for management and protection: the example of the Parana River floodplain, Brazil. Ecohydrol Hydrobiol, 21:411–424.). Seasonal changes in fish diet are especially related to the entry of allochthonous resources into the aquatic environment (Quirino et al. 2017QUIRINO, B.A., CARNIATTO, N., GUGLIELMETTI, R. & FUGI, R. 2017. Changes in diet and niche breadth of a small fish species in response to the flood pulse in a Neotropical floodplain lake. Limnologica, 62:126–131. https://doi.org/10.1016/j.limno.2016.10.005.
https://doi.org/10.1016/j.limno.2016.10.... ). Ontogenetic variation is an important factor to be verified in the diet of fish, usually accompanied by morphological changes throughout the development of individuals (Hahn et al. 2000HAHN, N.S., PAVANELLI, C.S. & OKADA, E.K. 2000. Dental development and ontogenetic diet shifts of Roeboides paranensis Pignalberi (Osteichthyes, Characinae) in pools of the Upper Rio Paraná floodplain (state of Paraná, Brazil). Rev Bras Biol 60:93–99.; Bozza and Hahn 2010BOZZA, A. & HAHN, N.S. 2010. Uso de recursos alimentares por peixes imaturos e adultos de espécies piscívoras em uma planície de inundação neotropical. Biota Neotrop, 10:217–226.; Alves et al. 2021ALVES, G.H.Z., FIGUEIREDO, B.R.S., MANETTA, G.I. & BENEDITO, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências, 93(4):e20190868.). Feeding tactics can change as fish grow, due to physical limitations regarding prey and food selectivity (Wainwrigth and Richard, 1995WAINWRIGTH, P.C. & RICHARD, B.A. 1995. Predicting patterns of prey use from morphology of fishes. Environ. Biol. Fishes, 44:97–113. doi:10.1007/bf00005909.
https://doi.org/10.1007/bf00005909... ; Arim et al. 2010ARIM, M., ABADES, S.B., LAUFER, G., LOUREIRO, M. & MARQUET, P. 2010. Food web structure and body size trophic position and resourc acquisition. Oikos., 119(1):147–153. https://doi.org/10.1111/j.1600-0706.2009.17768.x
https://doi.org/10.1111/j.1600-0706.2009... ; Bozza and Hahn 2010BOZZA, A. & HAHN, N.S. 2010. Uso de recursos alimentares por peixes imaturos e adultos de espécies piscívoras em uma planície de inundação neotropical. Biota Neotrop, 10:217–226.; Keppeler et al. 2015KEPPELER, F.W., LANÉS, L.E.K., ROLON, A.S., STENERT, C., LEHMANN, P., REICHARD, M. & MALTCHIK, L. 2015. The morphology-diet relationship and its role in the coexistence of two species of annual fishes. Ecology of Freshwater Fish, 24:77–90. doi:10.1111/eff.12127.
https://doi.org/10.1111/eff.12127... ; Alves et al. 2021ALVES, G.H.Z., FIGUEIREDO, B.R.S., MANETTA, G.I. & BENEDITO, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências, 93(4):e20190868.). Dietary ontogenetic changes can reduce intraspecific competition and allow species to successfully establish themselves in environments (Alves et al. 2021ALVES, G.H.Z., FIGUEIREDO, B.R.S., MANETTA, G.I. & BENEDITO, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências, 93(4):e20190868.). Understanding the relationships between fish fauna and the environment is essential to assist in methods of conservation and environmental restoration (Ferreira & Casatti 2006FERREIRA, C.P. & CASATTI, L. 2006. Influência da estrutura do hábitat sobre a ictiofauna de um riacho em uma micro-bacia de pastagem, São Paulo, Brasil. Revista Brasileira de Zoologia., 23:642–651. doi:10.1590/S0101-81752006000300006
https://doi.org/10.1590/S0101-8175200600... ; Dias et al. 2022DIAS, R.M., PELÁEZ, O., LOPES, T.M., OLIVEIRA, A.G., ANGULO-VALENCIA, M.A. & AGOSTINHO A.A. 2022. Importance of protection strategies in the conservation of the flagship species “dourado” Salminus brasiliensis (Characiformes: Bryconidae). Neotrop Ichthyol, 20(4):e220046. https://doi.org/10.1590/1982-0224-2022-0046
https://doi.org/10.1590/1982-0224-2022-0... ). The studies on the trophic ecology of fish are of paramount importance to know both individual and community processes, being important aspects for the conservation of species (Nunn et al. 2012NUNN, A.D., TEWSON, L.H. & COWX, I.G. 2012. A ecologia de forrageamento de peixes larvais e juvenis. Reviews in Fish Biology and Fisheries, 22(2):377–408. doi: 10.1007/s11160-011-9240-8
https://doi.org/10.1007/s11160-011-9240-... ; Tonella et al. 2019TONELLA, L.H., DIAS, R.M., VITORINO, O.B., FUGI, R. & AGOSTINHO, A.A. 2019. Conservation status and bio-ecology of Brycon orbignyanus (Characiformes: Bryconidae), an endemic fish species from the Paraná River basin (Brazil) threatened with extinction. Neotropical Ichthyology 17(3). https://doi.org/10.1590/1982-0224-20190030
https://doi.org/10.1590/1982-0224-201900... ). Thus, this study aimed to characterize the diet of M. bonita in streams of the Formoso River basin and to verify possible changes in the diet of the species by periods (dry and rainy) and highlight the origin (allochthonous or autochthonous) of the food items most consumed by the species in the respective evaluated periods and to identify ontogenetic diet variations of the species.

Material and Methods

Study area

The study was carried out in seven points sampled in the streams of the Formoso River basin (MS). The Formoso River basin is located mostly in a limestone region and is situated in the sub-basin of the Miranda River, one of the six sub-basins of the Upper Paraguay basin (Mato Grosso do Sul 2004). The main river names the basin and extends a drainage area of about 136,000 hectares and is within the Serra da Bodoquena (Teruya-Júnior et al. 2009TERUYA-JUNIOR, H., LASTORIA, G., CORRÊA, L.C., MOREIRA, E.S., TORRES, T.G. & FILHO, A.C.P. 2009. Análise Multitemporal da Bacia do Rio Formoso, 1989 – 2005. Anais XIV Simpósio Brasileiro de Sensoriamento Remoto, Natal, Brasil, INPE, 6329–6336.).

The Formoso River basin has an area of 1,334 km², located in the central region of the municipality of Bonito, in the state of Mato Grosso do Sul and is 100 km long (Duarte et al. 2005DUARTE, G., MEDINA JÚNIOR, P.B., PINTO. 2005. Caracterização do perfil sócio-econômico-cultural e sua relação com o grau de consciência e interação ambiental dos visitantes no Balneário Municipal de Bonito, Mato Grosso do Sul. In: Evaldo Luiz Gaeta Espíndola; Edson Wedland. (Org.). Trajetórias e perspectivas de um curso multidisciplinar. São Carlos: RIMA, v. 4, p. 264–276.). The Formoso River is characterized by clear waters, a sandy-clay riverbed, thick litter and dense riparian forest that in some stretches is about 500 m wide from the riverbed (Reys et al. 2005REYS, P., GALETTI, M., MORELLATO, L.P.C. & SABINO, J., 2005. Fenologia reprodutiva e disponibilidade de frutos de espécies arbóreas em mata ciliar do rio Formoso, Mato Grosso do Sul, Bio. Neotrop., 5(2). https://doi.org/10.1590/S1676-06032005000300021
https://doi.org/10.1590/S1676-0603200500... ). According to the Köppen classification, the climate of the region is sub-hot tropical, with hot and rainy periods occurring on average between October to April and dry seasons predominating from May to September, with average annual temperatures between 22 °C and 26 °C.

Collecting the fish

The fish were collected at two times of the year (January/rainy and October/dry 2016) in the seven points sampled in the streams of the Formoso River basin (coordinate 21°02'01"S 56°28'31"W), (coordinate 21°06'34"S 56°28'24"W), (coordinate 21°04'22"S 56°28'26"W), (coordinate 21°04'08"S 56°25'59"W), (coordinate 21°06'24"S 56° 33'42"W) (coordinate 21°02'55"S 56°18'10"W) and (coordinate 21°02'14"S 56°18'39"W) (Figure 1). The fish were sampled using seine net (5 mm mesh) and sieves. The specimens were anesthetized with Eugenol (clove oil; 70 mg/L) and then euthanized and fixed in 10% formalin solution and preserved 70% ethanol. Voucher specimens were deposited in the Zoological Collection (ZUFMS) of Universidade Federal do Mato Grosso do Sul (ZUFMS-PIS06693).

Figure 1.
Map showing the location of the study area and the seven points sampled in the streams of the Formoso River basin, Mato Grosso do Sul, Brazil.

Diet analysis

In the laboratory, the biometry of the individuals of M. bonita were measured standard length (SL-mm), and the total weight (g) were taken. The individuals were dissected and the stomachs were removed. Stomach content was analyzed under a stereomicroscope and the food items were identified to the lowest possible taxonomic level with the support of specialized literature (McCafferty 1981MCCAFFERTY, W.P. 1981. Aquatic entomology: the fishermen’s and ecologists. Illustrated guide to insects and their relatives. Boston: Jones and Bartlett Publishers.; Mugnai et al. 2010MUGNAI, R., NESSIMIAN, J.L., & BAPTISTA, D.F. 2010. Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro. Rio de Janeiro: Technical Books.). The items were analyzed according to the frequency of occurrence and volumetric methods (Hyslop, 1980HYSLOP, E.J. 1980. Stomach contents analysis – a review of methods and their applications. J. Fish Biol., 17(4):411–429. http://dx.doi.org/10.1111/j.1095-8649.1980.tb02775.x
https://doi.org/10.1111/j.1095-8649.1980... ). The volume of the items was obtained by compressing the material with a glass slide on a millimeter plate to a known height (1 mm), and the result was converted to milliliters (1 mm³ = 0.001 ml) (Hellawell & Abel 1971HELLAWELL, J. & ABEL, R. 1971. A rapid volumetric method for the analysis of the food of fishes. Journal of Fish Biology, 3:29–37. doi:10.1111/j.10958649.1971.tb05903.x
https://doi.org/10.1111/j.10958649.1971.... ).

Data analysis

The food items were grouped according to the following food categories: terrestrial invertebrate, aquatic invertebrate, plant, and other (filamentous algae and fish scale) and according to origin of food items (autochthonous, allochthonous and indeterminate). To characterize the diet the Food Index (IAi%) was calculated Fi is the relative frequency of occurrence of item i (%) and Vi is the relative volume of item i (total%) (Kawakami & Vazzoler 1980KAWAKAMI, E. & VAZZOLER, G. 1980. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol. Inst. Oceanogr., 29(2):205–207. http://dx.doi.org/10.1590/S0373-55241980000200043
https://doi.org/10.1590/S0373-5524198000... ).

To assess ontogenetic variations in diet, individuals were grouped into five size classes (mm) in the dry (D1 to D5) (D1 = 15,3 – 20,3); (D2 = 20,4 – 25,4); (D3 = 25,5 – 30,5); (D4 = 30,6 – 35,6) and (D5 = 35,7 – 40,7) and rainy (R1 to R5) (R1 = 14,6 – 19,6); (R2 = 19,2 – 24,7); (R3 = 24,8 – 29,8); (R4 = 29,9 – 34,9) and (R5 = 35,0 – 40,0) periods. The groups were separated every five millimeters from the smallest individual for each period. To verify whether the diet of M. bonita showed differences in relation to size classes and sampling periods, we performed Permutational Multivariate Analysis of Variance – PERMANOVA (Anderson et al. 2008).

Results

The stomach contents of 240 specimens of M. bonita were analyzed during the dry (97) and rainy (143) periods. The diet of M. bonita was characterized as invertivorous as it basically consumed both aquatic and terrestrial invertebrates, despite the higher consumption of aquatic invertebrates in both periods (Figure 2). In the diet of M. bonita, were identified 30 food items consumed by the species, 27 food items were found in the dry, and 26 in the rainy period (Table 1). The main food items eaten in the dry period were fragments of aquatic insects, Formicidae and larvae, and pupae of Diptera. In the rainy period, the species mainly consumed Formicidae and Aquatic Insect fragments. Resources autochthonous origin were the most consumed in both periods (dry and rainy). The interaction term between period and size classes was not significant. Significant differences were identified in the diet of the species between the periods considered (pseudo-F = 5.02; p = 0.02). However, the diet of M. bonita did not show ontogenetic variations, which indicates that the species feeds on the same food resources throughout development. The aquatic and terrestrial invertebrates food categories were the most consumed in most size classes (Figure 3). The main food items consumed in the different size classes were aquatic insect fragments, Formicidae, Diptera larvae, and pupae.

Figure 2.
Food categories (IAi%) consumed by Moenkhausia bonita in the dry and rainy periods in streams of the Formoso River basin, Mato Grosso do Sul, Brazil.

Figure 3.
Food categories (IAi%) consumed by Moenkhausia bonita in different size classes (A) in the dry (D1 to D5) and (B) rainy (R1 to R5) in streams of the Formoso river basin, Mato Grosso do Sul, Brazil.

Discussion

We classified Moenkhausia bonita as invertivorous in the streams of the Formoso River basin, by consuming basically aquatic and terrestrial insects, with a tendency to consume higher proportions of autochthonous invertebrates. In lake environments, the insects were also the main items consumed by M. bonita (Carniatto et al. 2014CARNIATTO, N., FUGI, R. THOMAZ, S.M. & CUNHA, E.R. 2014. The invasive submerged macrophyte Hydrilla verticillata as a foraging habitat for small-sized fish. Nat Conservação, 12:30–35. doi: 10.4322/natcon.2014.006
https://doi.org/10.4322/natcon.2014.006... ; Carniatto et al. 2016CARNIATTO, N., FUGI, R. & THOMAZ, S.M. 2016. Highly segregated trophic niche of two congeneric fish species in Neotropical floodplain lakes. J. Fish Biol., 90(3):1118–1125. http://dx.doi.org/10.1111/jfb.13236
https://doi.org/10.1111/jfb.13236... ; Quirino et al. 2018QUIRINO, B.A., CARNIATTO, N., THOMAZ, S.M. & FUGI, R. 2018. Small fish diet in connected and isolated lakes in a Neotropical floodplain. Ecol. Fresh. Fish., 28(1):97–109.) where Chironomidae pupae were the most consumed item in most lakes. Others species of Moenkhausia showed a diet based on terrestrial and aquatic insects, such as M. dichroura (Toffoli et al. 2010TOFFOLI, R.M., HAHN, N.S., ALVES, G.H.Z. & NOVAKOWSKI, G.C. 2010. Uso do alimento por duas espécies simpátricas de Moenkhausia (Characiformes, Characidae) em um riacho da Região Centro-Oeste do Brasil. Iheringia, Série. Zoologia, 100(3):201–206.http://dx.doi.org/10.1590/s0073-47212010000300003
https://doi.org/10.1590/s0073-4721201000... ), M. sanctafilomenae (Crippa et al. 2009CRIPPA, V.E.L., HAHN, N.S. & FUGI, A.R. 2009. Food resource used by small-sized fish in macrophyte patches in ponds of the upper Paraná river floodplain. Revista Acta Scient., 31(2):119–125. http://dx.doi.org/10.4025/actascibiolsci.v31i2.3266
https://doi.org/10.4025/actascibiolsci.v... ; Toffoli et al. 2010TOFFOLI, R.M., HAHN, N.S., ALVES, G.H.Z. & NOVAKOWSKI, G.C. 2010. Uso do alimento por duas espécies simpátricas de Moenkhausia (Characiformes, Characidae) em um riacho da Região Centro-Oeste do Brasil. Iheringia, Série. Zoologia, 100(3):201–206.http://dx.doi.org/10.1590/s0073-47212010000300003
https://doi.org/10.1590/s0073-4721201000... ), and M. intermedia (Crippa et al. 2009CRIPPA, V.E.L., HAHN, N.S. & FUGI, A.R. 2009. Food resource used by small-sized fish in macrophyte patches in ponds of the upper Paraná river floodplain. Revista Acta Scient., 31(2):119–125. http://dx.doi.org/10.4025/actascibiolsci.v31i2.3266
https://doi.org/10.4025/actascibiolsci.v... ; Vidotto-Magnoni et al. 2009VIDOTTO-MAGNONI, A.P. & CARVALHO, E.D. 2009. Population biology of dominant fish species of the Santa Bárbara river, a tributary of the Nova Avanhandava reservoir (low Tietê river, São Paulo State, Brazil). ACTA SCIENTIARUM. BIOLOGICAL SCIENCES (ONLINE), v. 31, p. 55–63. doi:10.4025/actascibiolsci.v31i1.650
https://doi.org/10.4025/actascibiolsci.v... ). Several authors emphasize the importance of the insectivorous diet, considering it as an adaptive advantage since the nutritional value of insects is more relevant than other food items present in the environment (Lowe-Mcconnell 1987LOWE-MCCONNELL, R.H. 1987. Ecological studies in tropical fish Communities. Cambridge Uruv. Press, Cambridge, XIII+., 382 p., Gandini et al. 2012GANDINI, C.V., BORATTO, I.A., FAGUNDES, D.C. & POMPEU, P.S. 2012. Estudo da alimentação dos peixes no rio Grande à jusante da usina hidrelétrica de Itutinga, Minas Gerais, Brasil. Iheringia, Série Zoologia, 102(1):56–61. http://dx.doi.org/10.1590/S007347212012000100008
https://doi.org/10.1590/S007347212012000... ).

In relation to the periods sampled, although the specimens consumed basically the same items, the proportions were unequal, presenting a significant difference in diet according to the two periods sampled. In both periods aquatic invertebrates (mainly fragments of aquatic insects, larvae, and pupae of Diptera) were more consumed. Larvae and pupae of Diptera have different locomotion and dispersal techniques (Backenbury 2000BACKENBURY, J. 2000. Locomotory modes in the larva and pupa of Chironomusplumosus (Diptera, Chironomidae). Journal of Insect Physiology, 46(12):1517–1527. https://doi.org/10.1016/S0022-1910(00)00079-2
https://doi.org/10.1016/S0022-1910(00)00... ), which often favors the capture of aquatic forms of this insect group by fish (Quirino et al. 2018QUIRINO, B.A., CARNIATTO, N., THOMAZ, S.M. & FUGI, R. 2018. Small fish diet in connected and isolated lakes in a Neotropical floodplain. Ecol. Fresh. Fish., 28(1):97–109.). In the rainy season, there was a higher increment of terrestrial invertebrates (mainly Formicidae). Some studies with tetras of the genus Astyanax (Borba et al. 2008BORBA, C.S., FUGI, R., AGOSTINHO, A.A. & NOVAKOWSKI, G.C. 2008. Dieta de Astyanax asuncionensis (Characiformes, Characidae) em riachos da bacia do rio Cuiabá, estado do Mato Grosso. Acta Sci Biol Sci., 30(1):39–45. doi:10.4025/actascibiolsci.v30i1.1442.
https://doi.org/10.4025/actascibiolsci.v... ; Ferreira et al. 2012aFERREIRA, A., GERHARD, P. & CYPRINO, J.E.P. 2012a. Diet of Astyanax paranae (Characidae) in streas whth diferente riparian land covers in the Passa-Cinco River basin, southeastern Brazil. Iheringia, Série Zoologia, 102:80–87.) report an expressive consumption by Formicidae. We assume that the ingestion of this item was possible due to its availability and abundance in the sampled sites and periods. The abundance of Formicidae in the diet of fishes species may be related to the action of rain and wind, which would result in the fall of individuals from the riparian vegetation (Toffoli et al. 2010TOFFOLI, R.M., HAHN, N.S., ALVES, G.H.Z. & NOVAKOWSKI, G.C. 2010. Uso do alimento por duas espécies simpátricas de Moenkhausia (Characiformes, Characidae) em um riacho da Região Centro-Oeste do Brasil. Iheringia, Série. Zoologia, 100(3):201–206.http://dx.doi.org/10.1590/s0073-47212010000300003
https://doi.org/10.1590/s0073-4721201000... ). With the onset of rainfall, there is increase in water velocity, which provides increase in water volume in the terrestrial environment, which contributes to a greater transport of items into the aquatic environment (Payne 1986PAYNE, A.I. 1986. The ecology of tropical lakes and rivers. John Wiley & Sons., 301pp.).

Regarding size variations, there was no difference in diet among size classes, with aquatic invertebrates being the main food category in most classes for both periods, except for Classes D1 and R5 where the consumption of terrestrial invertebrates was slightly higher. In a study on ontogenetic variations in the diet of Astyanax janeiroensis, the authors pointed out that the smallest individuals consumed greater proportions of items of animal origin and the larger ones had a diet based on items of plant origin (Mazzoni et al. 2010MAZZONI, R., NERY, L. & IGLESIAS, R.I. 2010. Ecology and ontogeny of feeding habit of Astyanax janeiroensis (Osteichthyes, Characidae) from a coastal stream from Southeast Brazil. Biota Neotrop., 10(3):53–60.). In the process of fish development, it is common for larvae and juveniles to include larger prey items in their diet, modifying their diet (Makrakis et al. 2005MAKRAKIS, M.C., NAKATANI, K., BIALETZKI, A., SANCHES, P.V., BAUMGARTNER, G. & GOMES, L.C. 2005. Ontogenetic shifts in digestive tract morphology and diet of fish larvae of the Itaipu Reservoir, Brazil. Environ. Biol. Fishes, 72:99–107.doi:10.1007/s10641-004-6596-9.
https://doi.org/10.1007/s10641-004-6596-... ; Nunn et al. 2007NUNN, A.D., HARVEY, J.P. & COWX, I.G. 2007. The food and feeding relationships of larval and 0+ year juvenile fishes in lowland rivers and connected waterbodies. I. Ontogenetic shifts and interspecific diet similarity. J. Fish Biol., 70(3):726–742. https://doi.org/10.1111/j.1095-8649.2007.01334.x
https://doi.org/10.1111/j.1095-8649.2007... ), that is, as the fish increase in size, they consume wider variety of prey items becoming generalists (Winemiller 1989WINEMILLER, K.O. 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environ. Biol. Fishes, 26:177–199. doi:10.1007/BF00004815
https://doi.org/10.1007/BF00004815... ; Sánchez-Hernández et al. 2012SÁNCHEZ-HERNÁNDEZ, J., SERVIA, M.J., VIEIRA-LANERO, R. & COBO, F. 2012. Ontogenetic Dietary Shifts in a Predatory Freshwater Fish Species: The Brown Trout as an Example of a Dynamic Fish Species. In: Turker, H. (Ed.) New Advances and Contributions to Fish Biology. InTech, 271–298.; Keppeler et al. 2015KEPPELER, F.W., LANÉS, L.E.K., ROLON, A.S., STENERT, C., LEHMANN, P., REICHARD, M. & MALTCHIK, L. 2015. The morphology-diet relationship and its role in the coexistence of two species of annual fishes. Ecology of Freshwater Fish, 24:77–90. doi:10.1111/eff.12127.
https://doi.org/10.1111/eff.12127... ). Morphological changes are factors that instigate fish to seek food resources of various sizes and appropriate nutritional proportions for each developmental stage (Winemiller 1989WINEMILLER, K.O. 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environ. Biol. Fishes, 26:177–199. doi:10.1007/BF00004815
https://doi.org/10.1007/BF00004815... ; Ortiz & Arim 2016ORTIZ, E. & ARIM, M. 2016. Hypotheses and trends on how body size affects trophic interactions in a guild of South American killifishes. Austr. Ecol., 41(8):976–982. doi:10.1111/aec.12389
https://doi.org/10.1111/aec.12389... ). Consumption of small food items by smaller fish individuals is generally associated with mouth opening and position and number of teeth (Dala-Corte et al. 2016DALA-CORTE, R.B., SILVA, E.R. DA & FIALHO, C.B. 2016. Diet-morphology relationship in the stream-dwelling characid Deuterodon stigmaturus (Gomes, 1947) (Characiformes: Characidae) is partially conditioned by ontogenetic development. Neotropical Ichthyology, 14(2). doi:10.1590/1982-0224-20150178
https://doi.org/10.1590/1982-0224-201501... ; Bonato et al. 2017BONATO, K.O., BURRESS, E.D., & FIALHO, C.B. 2017. Dietary differentiation in relation to mouth and tooth morphology of a neotropical characid fish Community. Zoologischer Anzeiger, 267:31–40. doi:10.1016/j.jcz.2017.01.003.
https://doi.org/10.1016/j.jcz.2017.01.00... ). In the literature, smaller individuals of characids have a diet based on small aquatic organisms such as microcrustaceans and insect larvae, showing ontogenetic variations in their diets (Araújo et al. 2005ARAÚJO, F.G., ANDRADE, C.C., SANTOS, R.N., SANTOS, A.F.G.N. & SANTOS, L. N. 2005. Spatial and seasonal changes in the diet of Oligosarcus hepsetus (Characiformes: Characidae) in a Brazilian reservoir. Braz J Biol. 65:1–8.; Mazzoni et al. 2010MAZZONI, R., NERY, L. & IGLESIAS, R.I. 2010. Ecology and ontogeny of feeding habit of Astyanax janeiroensis (Osteichthyes, Characidae) from a coastal stream from Southeast Brazil. Biota Neotrop., 10(3):53–60.; Lampert et al. 2022LAMPERT, V.R., DIAS, T.S., TONDATO-CARVALHO, K.K., & FIALHO, C.B. 2022. The effects of season and ontogeny in the diet of Piabarchus stramineus (Eigenmann 1908) (Characidae: Stevardiinae) from southern Brazil. Acta Limnologica Brasiliensia, 34.). Unlike these studies, we did not find ontogenetic differences in the diet of M. bonita. The fact that this species does not present a significant difference between the size classes may be due mainly to the greater consumption of aquatic invertebrates in all stages of developmen generally smaller individuals consume this resource, that making necessary, further studies on the biology, ecology, and behavior of this species. Riparian forests have vast importance in regulating energy flow and nutrient cycling (Vannote et al. 1980VANNOTE, R.L., MINSHALL, G.W., CUMMINS K.W., SEDELL, J.R. & CUSHING, C.E. 1980. The river continuum concept. Canadian J. of Fisheries and Aquatic Sci., 37:130–137.). The maintenance of aquatic biodiversity is extremely dependent on the ecological functions performed by forests, mainly in providing abundant terrestrial food of animal and plant origin that falls into the water (Barrela & Petrere Junior 2001BARRELA, W. & PETRERE-JUNIOR, M., 2001. A biodiversidade da ictiofauna dos rios Tietê e Paranapanema e sua relação com a floresta Atlântica. In: Fundação Tropical de Pesquisas e Tecnologia. Bases de Dados Tropicais.). Gregory et al. 1991GREGORY, S.V., SWANSON, F.J., MCKEE, W.A. & CUMMINS, K.W. 1991. An ecosystem perspective of riparian zones. BioScience, 41(8):540–551. doi:10.2307/1311607
https://doi.org/10.2307/1311607... ; Bretschko & Waidbcher 2001BRETSCHKO, G. & WAIDBACHER, H. 2001. Riparian ecotones, invertebrates and fish: life cycle timing and trophic base. Ecohydrology & Hydrobiology., 1(0.1):57–64.; Sabino & Deus e Silva 2004SABINO, J. & DEUS E SILVA, C.P. 2004. História natural de peixes da estação ecológica Juréia-Itatins. In: MARQUES, O.A.V. & DULEBA, W. (Ed.) Estação Ecológica Juréia-Itatins: ambiente físico, flora e fauna. Ribeirão Preto: HOLOS, 230–242., emphasize the influence of the riparian forest even when fish feed on autochthonous items because the primary source of these food resources has an allochthonous origin, considered the base of the trophic chain in streams. The Formoso River basin is a region with high agricultural and cattle ranching exploitation and with this we have been observing the decline of forest areas, reduction of permanent preservation areas, and increase of urban areas and ecotourism (Teruya-Júnior 2011TERUYA-JUNIOR, H. 2011. Diagnóstico Ambiental da Bacia Hidrográfica do Rio Formoso, MS. Campo Grande. [Dissertação de mestrado em Tecnologias Ambientais] Campo Grande: Universidade Federal de Mato Grosso do Sul.). Riparian forests can act as an effective barrier against sedimentation and provide resources for stream fauna (Ferreira et al. 2012bFERREIRA, A., PAULA, F.R., GERHARD, P., KASHIWAQUI, E.A.L., CYRINO, J.E.P. & MARTINELLI, L.A. 2012b. Riparian coverage affects diets of characids in neotropical streams. Ecology of Freshwater Fish, 21:12–22. doi:10.1111/j.1600-0633.2011.00518.x
https://doi.org/10.1111/j.1600-0633.2011... ), besides hindering the carriage of agrochemicals into the water bodies, particularly in streams that pass through basins subjected to intense agricultural and livestock activity (Sweeney et al. 2004SWEENEY, B.W., BOTT, T.L., JACKSON, J.K., KAPLAN, L.A., NEWBOLD, J.D., STANDLEY, L.J., HESSION, W.C. & HORWITZ, R.J. 2004. Riparian Deforestation, Stream Narrowing, and Loss of Stream Ecosystem Services. Proceedings of the National Academy of Sciences, 101:14132–14137. https://doi.org/10.1073/pnas.0405895101.
https://doi.org/10.1073/pnas.0405895101... , Martinelli & Filoso 2007MARTINELLI, L.A. & FILOSO, S. 2007. Polluting effects of Brazil’s sugar-ethanol industry. Nature, 445(7126):364.).

Taking into account that the streams sampled along the Formoso River basin have forested riparian zones in different degrees of preservation, we can infer that the invertivorous diet of M. bonita is favored by food resources coming directly and indirectly from these environments. The results found in this first study with the species in a lotic environment reinforce the importance of resources of autochthonous origin in the food composition of the species. Emphasizing the importance of aquatic invertebrates, mainly immature forms of aquatic insects, which were verified in the diet of M. bonita. These resources were important for both times and for all size classes.

Acknowledgements

To the projects of Hydrological Monitoring of the Formoso River and the urban streams of Bonito/MS and the Integrated Monitoring System of the waters of the Hydrographic Basin of the Formoso River; to the Neotropica Foundation of Brazil; to NUPAQ-MS/UFGD for the availability of the laboratory and equipment for analyzing the contents and Drº. Francisco de Paula Severo da Costa Neto and Drª. Karina Keyla Tondato de Carvalho for the availability of the UFMS laboratories, for the explanations about the biology of the species studied and for the discussions.

Data Availability

Supporting data are available at https://doi.org/10.48331/scielodata.BGIQSN.

References

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