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Structure and composition of ichthyofauna associated with cage fish farming and compared to a control area after severe drought in a Neotropical reservoir

Abstract

In 2014, an atypical drought in Southeast Brazil drastically reduced the water level in several reservoirs. We investigated the effects of this drought and the subsequent flood period on the attributes of ichthyofauna in an aquaculture and in a control area. Fish were collected bimonthly between 2014 and 2015 (drought) and 2016 (wet), using gill nets in the two sample areas in the Ilha Solteira reservoir, Upper Paraná River basin, Brazil. We compared ichthyofauna attributes between the drought and wet seasons in each area and between areas within each season. In the aquaculture area, the assemblages showed similar characteristics between the seasons. By contrast, the control area varied between seasons, with greater species richness, Shannon diversity, species evenness, and less β diversity in the wet season. Comparisons between areas in each season showed higher abundance in the fish farm within the drought season. Changes in structure and composition in the control area are possibly associated with new areas and resources made available by the flooding of marginal areas during the wet season. We inferred that the effect of the flood on the aquaculture community was attenuated by the continuous habitat structure such as shelters and food provided by the enterprise.

Keywords:
Diversity; Ilha Solteira reservoir; Invasive species; Upper Paraná River; Water crisis

Resumo

Em 2014 um evento de seca atípica no sudeste brasileiro diminuiu drasticamente o nível da água em diversos reservatórios. Nós investigamos os efeitos dessa seca, e seu subsequente período de cheia sobre atributos da ictiofauna em uma área aquícola e uma área controle. Os peixes foram coletados bimestralmente entre 2014 a 2015 (seca) e 2016 (cheia), usando redes de espera nas duas áreas amostrais no reservatório de Ilha Solteira, bacia do alto rio Paraná, Brasil. Comparamos atributos da ictiofauna entre os períodos de seca e cheia em cada área e entre as áreas dentro de cada período. Na área aquícola, verificou-se similaridade das assembleias entre os períodos. Em contraste, a área controle apresentou variação entre os períodos, com maior riqueza, diversidade Shannon, equitabilidade e menor diversidade β no período de cheia. Comparações entre áreas em cada período, mostraram maior abundância na piscicultura no período de seca. As mudanças na estrutura e composição na área controle possivelmente está associada as novas áreas e recursos disponibilizados pela inundação de áreas marginais no período de cheia. Infere-se que o efeito da cheia na comunidade da área aquícola foi atenuado pela continua estrutura de habitat, como abrigos e ração fornecidos pelo empreendimento.

Palavras-chave:
Alto rio Paraná; Crise hídrica; Diversidade; Espécies invasoras; Reservatório de Ilha Solteira

INTRODUCTION

The construction of reservoirs causes changes in the physical, chemical, geomorphological, and hydrological conditions of rivers, transforming lotic ecosystems into lentic ones (Agostinho et al., 2007Agostinho AA, Pelicice FM, Petry AC, Gomes LC, Júlio Jr. HF. Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquat Ecosyst Health Manag. 2007; 10(2):174–86. https://doi.org/10.1080/14634980701341719
https://doi.org/10.1080/1463498070134171...
, 2016Agostinho AA, Gomes LC, Santos NCL, Ortega JCG, Pelicice FM. Fish assemblages in neotropical reservoirs: colonization patterns, impacts and management. Fish Res. 2016; 173(1):26–36. https://doi.org/10.1016/j.fishres.2015.04.006
https://doi.org/10.1016/j.fishres.2015.0...
). These changes in environmental conditions tend to modify native species richness and abundance, decreasing community resistance and facilitating introduction or invasion by non-native fish species (Pelicice et al., 2014Pelicice FM, Vitule JRS, Lima Junior DP, Orsi ML, Agostinho AA. A serious new threat to Brazilian freshwater ecosystems: The naturalization of nonnative fish by decree. Conserv Lett. 2014; 7(1):55–60. https://doi.org/10.1111/conl.12029
https://doi.org/10.1111/conl.12029...
; Ruaro et al., 2020Ruaro R, Tramonte RP, Buosi PRB, Manetta GI, Benedito E. Trends in studies of nonnative populations: Invasions in the Upper Paraná River Floodplain. Wetlands. 2020; 40:113–24. https://doi.org/10.1007/s13157-019-01161-y
https://doi.org/10.1007/s13157-019-01161...
). Reservoirs are present in the main river basins in Brazil, and the principal purpose is the production of electricity, however, among ours the use multiple, the aquaculture activities have drawn the attention of researchers about their possible effects on the structure of ichthyofauna (Daga et al., 2015Daga VS, Skóra F, Padial AA, Abilhoa V, Gubiani ÉA, Vitule JRS. Homogenization dynamics of the fish assemblages in Neotropical reservoirs: comparing the roles of introduced species and their vectors. Hydrobiologia. 2015; 746:327–47. https://doi.org/10.1007/s10750-014-2032-0
https://doi.org/10.1007/s10750-014-2032-...
; Agostinho et al., 2016Agostinho AA, Gomes LC, Santos NCL, Ortega JCG, Pelicice FM. Fish assemblages in neotropical reservoirs: colonization patterns, impacts and management. Fish Res. 2016; 173(1):26–36. https://doi.org/10.1016/j.fishres.2015.04.006
https://doi.org/10.1016/j.fishres.2015.0...
; Nobile et al., 2020Nobile AB, Cunico AM, Vitule JRS, Queiroz J, Vidotto-Magnoni AP, Garcia DAZ et al.Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac. 2020; 12(3):1495–517. https://doi.org/10.1111/raq.12393
https://doi.org/10.1111/raq.12393...
). A trend toward the replacement of extractive fisheries by aquaculture has been conducted under the argument of the decrease of natural fish stocks and the increase in demand for fish consumption (FAO, 2016Food and Agriculture Organization of the United Nations (FAO). The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. Rome. 2016. Available from: http://www.fao.org/3/a-i5555e.pdf
http://www.fao.org/3/a-i5555e.pdf...
). In Brazil, aquaculture can occupy 1% of the surface of a reservoir, but there are concerns about this regulation due to its potential effects on ecosystems (Nobile et al., 2020Nobile AB, Cunico AM, Vitule JRS, Queiroz J, Vidotto-Magnoni AP, Garcia DAZ et al.Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac. 2020; 12(3):1495–517. https://doi.org/10.1111/raq.12393
https://doi.org/10.1111/raq.12393...
). In 2020, there was a 4.3% increase in production from Brazilian fish farming compared to 2019, which recorded 551.9 thousand tons of fish. Oreochromis niloticus (Linnaeus, 1758) was the most cultivated species, with 62.3% of the total fish produced or 343.6 thousand tons (IBGE, 2020Instituto Brasileiro de Geografia e Estatística (IBGE). Produção da pecuária municipal 2019. Prod Pec Munic. 2020; 47:1–08. Available from: https://biblioteca.ibge.gov.br/visualizacao/periodicos/84/ppm_2019_v47_br_informativo.pdf
https://biblioteca.ibge.gov.br/visualiza...
).

Among the aquaculture industry activities in artificial reservoirs in Brazil, cage fish farming systems stand out. In these systems, there is a continuous input of organic matter and energy in the form of feed, up to 18% of which can be introduced into the aquatic ecosystem in the form of unconsumed feed remains (Montanhini-Neto, Ostrensky, 2015Montanhini-Neto R, Ostrensky A. Nutrient load estimation in the waste of Nile tilapia Oreochromis niloticus (L.) reared in cages in tropical climate conditions. Aquac Res. 2015; 46(6):1309–22. https://doi.org/10.1111/are.12280
https://doi.org/10.1111/are.12280...
). The introduction of this matter and of allochthonous energy devoid of this activity contributes locally to changes in the structure of the fish fauna. Such changes have been reported in relation to fish species abundance and richness around the fish farming activity. For abundance, generally, the fish farm increases the wild species abundance (Barrett et al., 2019Barrett LT, Swearer SE, Dempster T. Impacts of marine and freshwater aquaculture on wildlife: a global meta-analysis. Rev Aquac. 2019; 11(4):1022–44. https://doi.org/10.1111/raq.12277
https://doi.org/10.1111/raq.12277...
), however, patterns of the effect of fish farm on the species richness are still unclear. In some studies, an increase in species richness was observed (Barrett et al., 2019Barrett LT, Swearer SE, Dempster T. Impacts of marine and freshwater aquaculture on wildlife: a global meta-analysis. Rev Aquac. 2019; 11(4):1022–44. https://doi.org/10.1111/raq.12277
https://doi.org/10.1111/raq.12277...
; Pereira et al., 2019Pereira LS, Demétrio JA, Cunico AM, Latini JD, Gomes LC, Agostinho AA. Cage aquaculture in Neotropical waters promotes attraction and aggregation of fish. Aquac Res. 2019; 50(10):2896–906. https://doi.org/10.1111/are.14244
https://doi.org/10.1111/are.14244...
) and in others, a reduction (Nobile et al., 2018Nobile AB, Zanatta AS, Brandão H, Zica EOP, Lima FP, Freitas-Souza D et al. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture. 2018; 495:780–85. https://doi.org/10.1016/j.aquaculture.2018.06.053
https://doi.org/10.1016/j.aquaculture.20...
). Fish farming can also act as a source of introduction of non-native species (Britton, Orsi, 2012Britton JR, Orsi ML. Non-native fish in aquaculture and sport fishing in Brazil: economic benefits versus risks to fish diversity in the upper River Paraná basin. Rev Fish Biol Fisher. 2012; 22(3):555–65. http://dx.doi.org/10.1007/s11160-012-9254-x
http://dx.doi.org/10.1007/s11160-012-925...
; Ortega et al., 2015Ortega JCG, Júlio Jr. HF, Gomes LC, Agostinho AA. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia. 2015; 746:147–58. https://doi.org/10.1007/s10750-014-2025-z
https://doi.org/10.1007/s10750-014-2025-...
; Ruaro et al., 2020Ruaro R, Tramonte RP, Buosi PRB, Manetta GI, Benedito E. Trends in studies of nonnative populations: Invasions in the Upper Paraná River Floodplain. Wetlands. 2020; 40:113–24. https://doi.org/10.1007/s13157-019-01161-y
https://doi.org/10.1007/s13157-019-01161...
) and favor generalist species (Ramos et al., 2013Ramos IP, Brandão H, Zanatta AS, Zica ÉOP, Silva RJ, Rezende-Ayroza DMM et al. Interference of cage fish farm on diet, condition factor and numeric abundance on wild fish in a Neotropical reservoir. Aquaculture. 2013; 414–415:56–62. https://doi.org/10.1016/j.aquaculture.2013.07.013
https://doi.org/10.1016/j.aquaculture.20...
; Nobile et al., 2018Nobile AB, Zanatta AS, Brandão H, Zica EOP, Lima FP, Freitas-Souza D et al. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture. 2018; 495:780–85. https://doi.org/10.1016/j.aquaculture.2018.06.053
https://doi.org/10.1016/j.aquaculture.20...
), contributing to fish faunal homogenization processes (Pelicice et al., 2014Pelicice FM, Vitule JRS, Lima Junior DP, Orsi ML, Agostinho AA. A serious new threat to Brazilian freshwater ecosystems: The naturalization of nonnative fish by decree. Conserv Lett. 2014; 7(1):55–60. https://doi.org/10.1111/conl.12029
https://doi.org/10.1111/conl.12029...
; Daga et al., 2015Daga VS, Skóra F, Padial AA, Abilhoa V, Gubiani ÉA, Vitule JRS. Homogenization dynamics of the fish assemblages in Neotropical reservoirs: comparing the roles of introduced species and their vectors. Hydrobiologia. 2015; 746:327–47. https://doi.org/10.1007/s10750-014-2032-0
https://doi.org/10.1007/s10750-014-2032-...
; Bezerra et al., 2019Bezerra LAV, Freitas MO, Daga VS, Occhi TVT, Faria L, Costa APL et al. A network meta-analysis of threats to South American fish biodiversity. Fish Fish. 2019; 20(4):620–39. https://doi.org/10.1111/faf.12365
https://doi.org/10.1111/faf.12365...
).

Besides to aquaculture activities, qualitative and quantitative environmental factors can influence the structure of the fish fauna in reservoirs, such as depth, width, flow, shelter, and resources, associated with climatological/hydrological changes (Agostinho et al., 2007Agostinho AA, Pelicice FM, Petry AC, Gomes LC, Júlio Jr. HF. Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquat Ecosyst Health Manag. 2007; 10(2):174–86. https://doi.org/10.1080/14634980701341719
https://doi.org/10.1080/1463498070134171...
; Bond et al., 2008Bond NR, Lake PS, Arthington AH. The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia. 2008; 600:3–16. https://doi.org/10.1007/s10750-008-9326-z
https://doi.org/10.1007/s10750-008-9326-...
; Rolls et al., 2016Rolls RJ, Heino J, Chessman BC. Unravelling the joint effects of flow regime, climatic variability and dispersal mode on beta diversity of riverine communities. Freshw Biol. 2016; 61(8):1350–64. https://doi.org/10.1111/fwb.12793
https://doi.org/10.1111/fwb.12793...
). In Neotropical reservoirs, inter annual or seasonal effects of drastic reduction or rise in the water level in a hydroelectric reservoir are usually avoided or minimized by operation and management in the dam (Gunkel et al., 2018Gunkel G, Selge F, Keitel J, Lima D, Calado S, Sobral M et al. Water management and aquatic ecosystem services of a tropical reservoir (Itaparica, São Francisco, Brazil). Reg Environ Change. 2018; 18:1913–25. https://doi.org/10.1007/s10113-018-1324-8
https://doi.org/10.1007/s10113-018-1324-...
). However, events such as atypical floods and droughts strongly affect habitat and aquatic biota structures in these environments (Lytle, Poff, 2004Lytle DA, Poff NL. Adaptation to natural flow regimes. Trends Ecol Evol. 2004; 19(2):94–100. https://doi.org/10.1016/j.tree.2003.10.002
https://doi.org/10.1016/j.tree.2003.10.0...
). Periods of lower water level can favor the dominance of a few species, decreasing fish species richness and diversity (Chessman, 2013Chessman BC. Identifying species at risk from climate change: Traits predict the drought vulnerability of freshwater fishes. Biol Conserv. 2013; 160:40–49. https://doi.org/10.1016/j.biocon.2012.12.032
https://doi.org/10.1016/j.biocon.2012.12...
; Freitas et al., 2013Freitas CEC, Siqueira-Souza FK, Humston R, Hurd LE. An initial assessment of drought sensitivity in Amazonian fish communities. Hydrobiologia. 2013; 705:159–71. https://doi.org/10.1007/s10750-012-1394-4
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). Periods of higher water levels allow expansion of the flooded area and greater availability of habitats (Miranda, 2001Miranda LE. A review of guidance and criteria for managing reservoirs and associated riverine environments to benefit fish and fisheries. Marmulla G., editor. Dam, fish and fisheries: Opportunities, challenges and conflict resolution. FAO Fisheries Technical Paper; No. 419. Rome: FAO; 2001. p.91–137. p.91–137. Available from: http://www.fao.org/3/Y2785E/y2785e04.htm
http://www.fao.org/3/Y2785E/y2785e04.htm...
). This incorporation of new habitats and resources can attract non-resident species, with a consequent increase in species richness and local diversity (Lowe-Mcconnell, 1999Lowe-Mcconnell RH. Estudos ecológicos de comunidades de peixes tropicais. São Paulo: Edusp; 1999.; Agostinho et al., 2001Agostinho AA, Gomes LC, Zalewski M. The importance of floodplains for the dynamics of fish communities of the upper river Paraná. Ecohydrol Hydrobiol. 2001; 1(1-2):209–17. Available from: http://repositorio.uem.br:8080/jspui/bitstream/1/5283/1/197.pdf
http://repositorio.uem.br:8080/jspui/bit...
, 2016Agostinho AA, Gomes LC, Santos NCL, Ortega JCG, Pelicice FM. Fish assemblages in neotropical reservoirs: colonization patterns, impacts and management. Fish Res. 2016; 173(1):26–36. https://doi.org/10.1016/j.fishres.2015.04.006
https://doi.org/10.1016/j.fishres.2015.0...
). However, some studies that investigated the similarity among fish assemblage under hydrological effects showed an increase in β diversity during seasons with a lower water level as a result of an increase in species replacement due to greater habitat fragmentation or less connectivity when compared to flooding seasons (Thomaz et al., 2007Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia. 2007; 579:1–13. https://doi.org/10.1007/s10750-006-0285-y
https://doi.org/10.1007/s10750-006-0285-...
; Rolls et al., 2016Rolls RJ, Heino J, Chessman BC. Unravelling the joint effects of flow regime, climatic variability and dispersal mode on beta diversity of riverine communities. Freshw Biol. 2016; 61(8):1350–64. https://doi.org/10.1111/fwb.12793
https://doi.org/10.1111/fwb.12793...
).

An atypical drought recorded during the years 2014 to 2015 in Southeast Brazil caused numerous consequences for urban and rural supply and electricity generation (Coelho, 2016Coelho CAS, Cardoso DHF, Firpo MAF. Precipitation diagnostics of an exceptionally dry event in São Paulo, Brazil. Theor Appl Climatol. 2016; 125:769–84. https://doi.org/10.1007/s00704-015-1540-9
https://doi.org/10.1007/s00704-015-1540-...
; Hunt et al., 2018Hunt JD, Stilpen D, Freitas MAV. A review of the causes, impacts and solutions for electricity supply crises in Brazil. Renew Sust Energ Rev. 2018; 88:208–22. https://doi.org/10.1016/j.rser.2018.02.030
https://doi.org/10.1016/j.rser.2018.02.0...
). In addition, losses for artisanal fisheries and aquaculture were recorded (Galvão, Bermann, 2015Galvão J, Bermann C. Crise hídrica e energia: conflitos no uso múltiplo das águas. Estud av. 2015; 29(84):43–68. https://doi.org/10.1590/S0103-40142015000200004
https://doi.org/10.1590/S0103-4014201500...
). The few information on the effects of events of droughts and floods in freshwater aquaculture areas refers to productivity and on cultivated fish (Ahmed, Diana, 2016Ahmed N, Diana JS. Does climate change matter for freshwater aquaculture in Bangladesh?. Reg Environ Change. 2016; 16(6):1659–69. https://doi.org/10.1007/s10113-015-0899-6
https://doi.org/10.1007/s10113-015-0899-...
; Ahmed et al., 2019Ahmed N, Thompson S, Glaser M. Global aquaculture productivity, environmental sustainability, and climate change adaptability. Environ Manage. 2019; 63(2):159–72. https://doi.org/10.1007/s00267-018-1117-3
https://doi.org/10.1007/s00267-018-1117-...
). The scientific production on atypical hydrological events in the aquatic biota in areas close to fish cage systems has not been explored and elucidated. However, the expected of increasing the severity of droughts and aridification in many parts of the world (Park et al., 2018Park C-E, Jeong S-J, Joshi M, Osborn TJ, Ho C-H, Piao S et al. Keeping global warming within 1.5°C constrains emergence of aridification. Nat Clim Change. 2018; 8:70–74. https://doi.org/10.1038/s41558-017-0034-4
https://doi.org/10.1038/s41558-017-0034-...
) and the expansion of the cage farms placed in reservoirs in Brazil (Nobile et al., 2020Nobile AB, Cunico AM, Vitule JRS, Queiroz J, Vidotto-Magnoni AP, Garcia DAZ et al.Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac. 2020; 12(3):1495–517. https://doi.org/10.1111/raq.12393
https://doi.org/10.1111/raq.12393...
), alert to the necessity and relevance of research in these terms for wildlife management under future extreme hydrological events.

Here we aimed to investigate the structure and composition of the ichthyofauna in an aquaculture area (cage fish farming system) under the effect of an atypical hydrological event due to a severe drought that occurred between 2014 and 2015 and the subsequent rainy season (2016). We hypothesized that the change in the water level has a reduced effect on the ichthyofauna in the aquaculture area compared to the area without this activity. More specifically, we predict that the effects of the flood on the ichthyofauna are attenuate in the fish farming area, that is, little or no change in the abundance, richness, diversity, evenness, β diversity, and composition of the ichthyofauna between the drought and wet season. Considering that cage fish farming can locally influence fish species abundance by the attraction and aggregation of fish near the cages (Nobile et al., 2018Nobile AB, Zanatta AS, Brandão H, Zica EOP, Lima FP, Freitas-Souza D et al. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture. 2018; 495:780–85. https://doi.org/10.1016/j.aquaculture.2018.06.053
https://doi.org/10.1016/j.aquaculture.20...
; Barrett et al., 2019Barrett LT, Swearer SE, Dempster T. Impacts of marine and freshwater aquaculture on wildlife: a global meta-analysis. Rev Aquac. 2019; 11(4):1022–44. https://doi.org/10.1111/raq.12277
https://doi.org/10.1111/raq.12277...
; Pereira et al., 2019Pereira LS, Demétrio JA, Cunico AM, Latini JD, Gomes LC, Agostinho AA. Cage aquaculture in Neotropical waters promotes attraction and aggregation of fish. Aquac Res. 2019; 50(10):2896–906. https://doi.org/10.1111/are.14244
https://doi.org/10.1111/are.14244...
), we also hypothesized that the fish farming area promoted changes in the structure of the ichthyofauna. Thereby, we expected variation in taxonomic attributes between areas, with higher abundance in aquaculture area for both seasons.

MATERIAL AND METHODS

Study area. The Ilha Solteira reservoir is an accumulation reservoir formed in 1978 by the Paraná River in the region of the Upper Paraná River, Brazil. It has an average depth of 17.6 m, a maximum volume of 21.06 x 109 m3, a basin area of 1,195 km2, and a residence time of 46.7 days (Garcia et al., 2015Garcia F, Kimpara JM, Valenti WC, Ambrosio LA. Emergy assessment of tilapia cage farming in a hydroelectric reservoir. Ecol Eng. 2015; 68:72–79. https://doi.org/10.1016/j.ecoleng.2014.03.076
https://doi.org/10.1016/j.ecoleng.2014.0...
). The sample areas were: one under the influence of a cage fish farming system (fish farm; 20°02’30.54”S 50°55’59.65”W) and one in a location approximately 10 km upstream with similar physiographic characteristics, free from the influence of cage fish farming systems (control; 20°00’13.71”S 50°51’58.94”W) (Fig. 1). Both areas have an average depth of 9 meters, similar elevation (335–350 m) and their margins with agricultural and livestock activities. In 2014 and 2015, there was a significant rainfall deficit in several regions of Brazil, and the state of São Paulo experienced one of the largest droughts ever recorded (Coelho et al., 2016Coelho CAS, Cardoso DHF, Firpo MAF. Precipitation diagnostics of an exceptionally dry event in São Paulo, Brazil. Theor Appl Climatol. 2016; 125:769–84. https://doi.org/10.1007/s00704-015-1540-9
https://doi.org/10.1007/s00704-015-1540-...
), with historical decreases in water flow, volume (Hunt et al., 2018Hunt JD, Stilpen D, Freitas MAV. A review of the causes, impacts and solutions for electricity supply crises in Brazil. Renew Sust Energ Rev. 2018; 88:208–22. https://doi.org/10.1016/j.rser.2018.02.030
https://doi.org/10.1016/j.rser.2018.02.0...
), and quota of the Ilha Solteira reservoir (ONS, 2018Operador Nacional de Sistema Elétrico (ONS). Histórico da Operação. 2018. Available from: http://ons.org.br/paginas/resultados-da-operacao/historico-da-operacao
http://ons.org.br/paginas/resultados-da-...
; Fig. 2).

FIGURE 1 |
Map of South America showing the Ilha Solteira reservoir, with an indication of the sample areas (black circles). Adapted from Kliemann et al., (2018)Kliemann BCK, Delariva RL, Amorim JPA, Ribeiro CS, Silva B, Silveira RV et al. Dietary changes and histophysiological responses of a wild fish (Geophagus cf. proximus) under the influence of tilapia cage farm. Fish Res. 2018; 204:337–47. https://doi.org/10.1016/j.fishres.2018.03.011
https://doi.org/10.1016/j.fishres.2018.0...
.

FIGURE 2 |
Historical series of the variation in quota (m) between 1999 and 2019 in the Ilha Solteira reservoir, Upper Paraná River, São Paulo, Brazil. The dots indicate the sampling period.

Collection of biological material. Samples were collected bimonthly during the drought (quota below 323 m; December/2014 to October/2015) and wet (quota above 323 m; February to December/2016) seasons, using gill nets of different sizes (3, 4, 5, 6, 7, 8, 10, 12, and 14 cm between non-adjacent knots), set close to the margin or cages (up to 30 m from margin) in the fish farm and control areas between 5:00 p.m. and 6:00 a.m. The collected specimens were identified (Britski et al., 1999Britski HA, Silimon KZS, Lopes BS. Peixes do Pantanal - Manual de identificação. Brasília: Embrapa; 1999.; Graça, Pavanelli, 2007Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Maringá: EDUEM; 2007.; Ota et al., 2018Ota RR, Deprá GDC, Graça WJD, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol. 2018; 16(2):e170094. https://doi.org/10.1590/1982-0224-20170094
https://doi.org/10.1590/1982-0224-201700...
), and specimens from all species collected were deposited in the fish collection of the Departamento de Zoologia e Botânica, Universidade Estadual Paulista “Julio de Mesquita Filho”, São José do Rio Preto (DZSJRP), São Paulo, Brazil (Tab. S1).

Limnological data. Water temperature was measured in situ using a multiparameter probe (HORIBA U53) and water transparency was determined by a Secchi disk. Water samples were collected to determine total nitrogen (N) (Mackereth et al., 1978Mackereth FJH, Heron J, Talling JF. Water analysis: Some revised methods of water analysis for limnologists. Ambleside, Cumbria: Freshwater Biological Association; 1978.) and total phosphorus (P) (Golterman et al., 1978Golterman HL, Clymo RS, Ohnstad MAM. Methods for physical and chemical analysis of freshwaters. Oxford: Blackwell Scientific Publication; 1978. p.172–78.). All measurements were determined in surface, middle and bottom depth. The quota data were obtained from the Reservoir Monitoring System available on the website of the National Water Agency (ANA, 2017Agência Nacional das Águas (ANA). SAR - Sistema de Acompanhamento de Reservatórios. Version Mar-2017 [Internet]. Brasília; 2017. Available from: http://sar.ana.gov.br
http://sar.ana.gov.br...
). The reservoir water flow and rainfall data were obtained from the weather station at the Laboratory of Hydraulics and Irrigation of the Universidade Estadual Paulista (UNESP), Ilha Solteira, São Paulo, Brazil. The limnological characteristics of the fish farm and control in each season are shown in Tab. S1.

Data analysis. To verify the sufficiency of samples for ichthyofauna data, we generated rarefaction curves with interpolation and extrapolation (Chao et al., 2014Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr. 2014; 84(1):45–67. https://doi.org/10.1890/13-0133.1
https://doi.org/10.1890/13-0133.1...
) and 95% confidence intervals. To do that, we used species abundance data from the seasons within each area and individuals as the sampling unit.

To assess the effects of flooding on ichthyofauna attributes after the drought, we calculated total abundance, species richness, Shannon diversity index, and Pielou evenness (Magurran, 2004Magurran AE. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.) for each collection in each sample area (collections were used as replicas of “season” (levels: drought and wet) and “area” (levels: control and fish farm). To compare each attribute between the seasons in each area and between the areas in each season, we tested the assumptions of normality and homoscedasticity through a graphical inspection of residuals and Levene’s test, respectively. Subsequently, we compared the groups (areas and seasons) using two-way ANOVA, and in case of observed differences between the groups, we applied the least-squares means for paired comparisons.

To calculate and compare β diversity between seasons in each area and between areas in each season, we used the PERMDISP analysis based on the Jaccard dissimilarity index using community presence/absence data. This method yielded a measure of overall total β-diversity (if based on presence/absence data) and community structural variation (if based on abundance data) (Anderson et al., 2006Anderson MJ, Ellingsen KE, Mcardle BH. Multivariate dispersion as a measure of beta diversity. Ecol Lett. 2006; 9(6):683–93. https://doi.org/10.1111/j.1461-0248.2006.00926.x
https://doi.org/10.1111/j.1461-0248.2006...
). Also, to test whether the ichthyofauna structure differs between seasons in each area, we applied one-way PERMANOVA based on Bray-Curtis dissimilarity (Anderson et al., 2006Anderson MJ, Ellingsen KE, Mcardle BH. Multivariate dispersion as a measure of beta diversity. Ecol Lett. 2006; 9(6):683–93. https://doi.org/10.1111/j.1461-0248.2006.00926.x
https://doi.org/10.1111/j.1461-0248.2006...
; Anderson, 2017Anderson MJ. Permutational Multivariate Analysis of Variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL, editors. Wiley StatsRef: Statistics Reference Online. John Wiley & Sons, Ltd.; 2017. p.1–15. https://doi.org/10.1002/9781118445112.stat07841
https://doi.org/10.1002/9781118445112.st...
), using a community abundance data matrix as dependent variable and area and season as independent variables. To unravel the reason for rejecting the null hypothesis of PERMANOVA (i.e., location in the multivariate space or dispersion effects or both), the PERMDISP was then performed on the same Bray-Curtis matrix to test for differences in the multivariate dispersion (Anderson et al., 2006Anderson MJ, Ellingsen KE, Mcardle BH. Multivariate dispersion as a measure of beta diversity. Ecol Lett. 2006; 9(6):683–93. https://doi.org/10.1111/j.1461-0248.2006.00926.x
https://doi.org/10.1111/j.1461-0248.2006...
; Anderson, 2017Anderson MJ. Permutational Multivariate Analysis of Variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL, editors. Wiley StatsRef: Statistics Reference Online. John Wiley & Sons, Ltd.; 2017. p.1–15. https://doi.org/10.1002/9781118445112.stat07841
https://doi.org/10.1002/9781118445112.st...
). Because of the variation in the structure of the ichthyofauna, we applied the SIMPER overall pool analysis to verify the percentage of dissimilarity of fish communities and the species that most contributed to the differences (Clarke, Ainsworth, 1993Clarke KR, Ainsworth M. A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser. 1993; 92:205–19. Available from: http://www.int-res.com/articles/meps/92/m092p205.pdf
http://www.int-res.com/articles/meps/92/...
). Furthermore, we applied a redundancy analysis (RDA) to verify the relationship of the species abundance data matrix with the limnological variables matrix. For this analysis, species abundance data were transformed by Hellinger distance, and ANOVA was performed to test the significance of each limnological variable for the entire model.

Statistical analyses were performed using the R software (R Development Core Team, 2019R Development Core Team. R: The R project for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2019. Available from: https://www.r-project.org/
https://www.r-project.org/...
). Sample sufficiency analyses were performed with the aid of the “iNEXT” package and the iNEXT function (Hsieh et al., 2016Hsieh TC, Ma KH, Chao A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol. 2016; 7(12):1451–56. https://doi.org/10.1111/2041-210X.12613
https://doi.org/10.1111/2041-210X.12613...
). Species richness, Shannon index, and Pielou evenness were calculated by the “vegan” package using the diversity function (Oksanen et al., 201Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D et al. Vegan: Community Ecology Package. R Package Version 2.5-2; 2018. Available from: https://cran.r-project.org/package=vegan
https://cran.r-project.org/package=vegan...
8). Two-way ANOVA, PERMDISP, one-way PERMANOVA, SIMPER, and RDA were performed with the aid of the “vegan” package, respectively using the aov, betadisper, adonis, simper, and RDA functions (Oksanen et al., 201Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D et al. Vegan: Community Ecology Package. R Package Version 2.5-2; 2018. Available from: https://cran.r-project.org/package=vegan
https://cran.r-project.org/package=vegan...
8). The homoscedasticity of the models was verified by the “car” package using the leveneTest function (Fox, Weisberg, 2011Fox J, Weisberg S. An {R} companion to applied regression. Thousand Oaks: Sage; 2011. Available from: https://toc.library.ethz.ch/objects/pdf03/z01_978-1-5443-3647-3_01.pdf
https://toc.library.ethz.ch/objects/pdf0...
). The paired comparisons of the models were performed with the “emmeans” package using the emmeans function (Lenth et al., 2018Lenth R, Love J, Herve M, Miguez F, Riebl H, Singmann H. Emmeans: Estimated marginal means, aka least-squares means. R package. 2018; 1(1). Available from: https://cran.r-project.org/package=emmeans
https://cran.r-project.org/package=emmea...
). The graphs were prepared using the emmeans function (Lenth et al., 2018Lenth R, Love J, Herve M, Miguez F, Riebl H, Singmann H. Emmeans: Estimated marginal means, aka least-squares means. R package. 2018; 1(1). Available from: https://cran.r-project.org/package=emmeans
https://cran.r-project.org/package=emmea...
) and the “ggplot2” package (Wickham et al., 2016Wickham H, Chang W, Henry L, Pedersen TL, Takahashi K, Wilke C, Woo K, Yutani H, Dunnington D. ggplot2: Elegant graphics for data analysis.Version 2.1 [Internet]. New York: Springer-Verlag; 2016. Available from: https://ggplot2.tidyverse.org
https://ggplot2.tidyverse.org...
). The level of statistical significance was set at α = 0.05.

RESULTS

We sampled 978 specimens in the control area (Drought: 473; Wet: 505), comprising a total of 25 species (Drought: 20; Wet: 21), and 1,452 in the fish farm area (Drought: 888; Wet: 564) with 24 species (Drought: 15; Wet: 24). Species accumulation curves show that sufficiency of samples was reached, following similar stabilization patterns in both seasons for the sample areas evaluated (Fig. S2).

Most species were shared between seasons and evaluated areas; however, there was variation in their abundance. Schizodon intermedius Garavello & Britski, 1990, Heterotilapia buttikoferi (Hubrecht, 1881), and Megalancistrus paranus (Peters, 1881) were exclusive to the control area, while Hoplosternum littorale (Hancock, 1828) and Leporinus lacustris Amaral Campos, 1945 were exclusive to the fish farm area. The non-native species Geophagus sveni Lucinda, Lucena & Assis, 2010 and Plagioscion squamosissimus (Heckel, 1840) were the most abundant in the drought and wet seasons in the fish farm area and the drought season in the control area, while G. sveni and Serrasalmus maculatus Kner, 1858 were the most abundant species in the wet season in the control area (Tab. 1).

TABLE 1 |
Taxonomic order of the sampled species and their abundance during the drought and wet seasons in the control area and fish farm area at the Ilha Solteira reservoir, Upper Paraná River, SP, Brazil. C = Characiformes, P = Perciformes, Ci = Cichliformes, and S = Siluriformes. Voucher specimens of DZSJRP.

Comparisons between the sampling seasons within each area (Fish farm: drought vs. wet; Control: drought vs. wet) showed no changes in total abundance (Fig. 3A); however, species richness was higher during the wet season in both areas (Control: t = 3, p < 0.01; Fish farm: t = 2.24, p = 0.03; Fig. 3B). The Shannon index and Pielou evenness were higher in the wet season only in the control area (Shannon: t = 3.83, p < 0.01; Pielou: t = 2.14, p = 0.04; Figs. 3C,D). Comparisons between areas within each season (Drought: fish farm vs. control; Wet: fish farm vs. control) showed differences only total abundance within drought season, with the higher value in fish farm (t = 3.21, p < 0.01; Fig. 3A).

FIGURE 3 |
Box plots (minimum and maximum value = vertical line ends, standard error = box, and mean = horizontal line) of the ichthyofauna attributes in the control area and fish farm area, in the drought and wet seasons at the Ilha Solteira reservoir, Upper Paraná River, SP, Brazil. A. Total abundance; B. Species richness; C. Shannon index; D. Pielou evenness. Asterisks indicates significant upper value between seasons within each area. Hash indicates significant upper value between areas within each season.

The β diversity differed between seasons only in the control area, it was higher values in the drought season (PERMDISP, p = 0.03; Fig. 4). The ichthyofauna structure also showed differences between seasons only for the control area (PERMANOVA, R2 = 0.31; F = 4.66; p = 0.03) by a shift in the assemblage structure, and not by variation around the mean composition within groups (PERMDISP, p > 0.05), with a percentage of dissimilarity (SIMPER) of 62.29% and a high contribution of non-native and invasive species in the basin, G. sveni and P. squamosissimus, and only one native species (S. maculatus) (Tab. 2). In addition, for the control area, the “quota” variable was the only one that was significantly associated with the composition of the ichthyofauna (RDA-ANOVA; F = 5.17; p < 0.01), explaining 25.8% (adjusted R2) of the variation in the dataset. The abundance of P. squamosissimus and S. maculatus were strongly influenced by the model and negatively and positively related to the increase in the quota, respectively (Fig. 5). The limnological variables did not have significant correlations with the composition of the ichthyofauna in the fish farm area.

TABLE 2 |
Contribution of species to the percentage of dissimilarity (SIMPER) of the ichthyofauna in the control area considering abundance data for the drought and wet seasons at the Ilha Solteira reservoir, Upper Paraná River, SP, Brazil.

FIGURE 4 |
Beta diversity (PERMDISP) in the drought and wet seasons in the control and fish farm areas at the Ilha Solteira reservoir, Upper Paraná River, São Paulo, Brazil. Average distances of centroids with presence/absence of data. Asterisks indicates significant upper value between seasons within each area.

FIGURE 5 |
Redundancy analysis (RDA). Relation of ichthyofauna to the significant environmental variable (quota) in the drought and wet seasons in an area without the influence of fish farming (Control) at the Ilha Solteira reservoir, Upper Paraná River, São Paulo, Brazil. Ala = Acestrorhynchus lacustris, Acr = Astronotus crassipinnis, Cke = Cichla kelberi, Cpi = Cichla piquiti, Cbr = Cyphocharax gillii, Cgi = Crenicichla britskii, Gsv = Geophagus sveni, Hma = Hoplias aff. malabaricus, Mac = Megalancistrus parananus, Mli = Metynnis lippincottianus, Oni = Oreochromis niloticus, Ppl = Pimelodus platicirris, Ppi = Pinirampus pirinampu, Psq = Plagioscion squamosissimus, Pam = Pterygoplichthys ambrosettii, Rvu = Rhaphiodon vulpinus, Rde = Roeboides descalvadensis, Spa = Satanoperca pappaterra, Sin = Steindachnerina insculpta, Sit = Schizodon intermedius, Sna = Schizodon nasutus, Sma = Serrasalmus maculatus, Smg = Serrasalmus marginatus, Hbu = Heterotilapia buttikoferi, and Tne = Triportheus nematurus.

DISCUSSION

Ichthyofauna responses to water level changes were different in the fish farm and control areas. Our results indicate that in the fish farm area, the change in water level did not influence the structure and composition of the ichthyofauna. Furthermore, in the control area, the wet season showed greater mean values of the species richness, Shannon diversity, evenness, and lower β diversity, and these results corroborating our hypothesis. Our analysis showed that the greatest difference observed in the structure of the ichthyofauna between the seasons in the control area is possibly associated with the variation in the quota. Such a pattern is also shown by other studies (Baumgartner et al., 2017Baumgartner MT, Baumgartner G, Gomes LC. The effects of rapid water level changes on fish assemblages: the case of a spillway gate collapse in a Neotropical reservoir. River Res Appl. 2017; 33(4):548–57. https://doi.org/10.1002/rra.3110
https://doi.org/10.1002/rra.3110...
, 2020Baumgartner MT, Piana PA, Baumgartner G, Gomes LC. Storage or run-of-river reservoirs: exploring the ecological effects of dam operation on stability and species interactions of fish assemblages. Environ Manage. 2020; 65:220–31. https://doi.org/10.1007/s00267-019-01243-x
https://doi.org/10.1007/s00267-019-01243...
; Lima et al., 2017Lima FT, Reynalte-Tataje DA, Zaniboni-Filho E. Effects of reservoirs water level variations on fish recruitment. Neotrop Ichthyol. 2017; 15(3):e160084. https://doi.org/10.1590/1982-0224-20160084
https://doi.org/10.1590/1982-0224-201600...
), so we consider that the overall patterns and the possible explanations for spatial and seasonal variabilities described here will not change severely.

The greater mean values of the species richness in both areas during the wet season may be a result of the flooding of marginal areas, as observed in other studies (e.g., Agostinho et al., 2001Agostinho AA, Gomes LC, Zalewski M. The importance of floodplains for the dynamics of fish communities of the upper river Paraná. Ecohydrol Hydrobiol. 2001; 1(1-2):209–17. Available from: http://repositorio.uem.br:8080/jspui/bitstream/1/5283/1/197.pdf
http://repositorio.uem.br:8080/jspui/bit...
, 2007Agostinho AA, Pelicice FM, Petry AC, Gomes LC, Júlio Jr. HF. Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquat Ecosyst Health Manag. 2007; 10(2):174–86. https://doi.org/10.1080/14634980701341719
https://doi.org/10.1080/1463498070134171...
; Fernandes et al., 2009Fernandes R, Agostinho AA, Ferreira EA, Pavanelli CS, Suzuki HI, Lima DP et al. Effects of the hydrological regime on the ichthyofauna of riverine environments of the Upper Paraná River floodplain. Braz J Biol. 2009; 69(2):669–80. https://doi.org/10.1590/S1519-69842009000300021
https://doi.org/10.1590/S1519-6984200900...
). The flooding of these areas, providing stable habitat and resources, such as greater availability of shelter and food, contributes to the increase in local species richness and diversity due to the attraction of species and population recovery (Lowe-Mcconnell, 1999Lowe-Mcconnell RH. Estudos ecológicos de comunidades de peixes tropicais. São Paulo: Edusp; 1999.; Bond et al., 2008Bond NR, Lake PS, Arthington AH. The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia. 2008; 600:3–16. https://doi.org/10.1007/s10750-008-9326-z
https://doi.org/10.1007/s10750-008-9326-...
). This increase in local diversity as a result of flooding in the control area is supported by higher mean values of the Shannon diversity and Pielou evenness. The increase in these indices indicates a decrease in the abundance of dominant species and a better quantitative distribution of rare species (Magurran, 2004Magurran AE. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.). Conversely, the similarity in Shannon and Pielou indices between the seasons in the fish farm area can be explained by the tendency of dominance by a few species such as G. sveni and P. squamosissimus in areas close to fish farms. These species are non-native, generalist, and less susceptible to environmental variations (Moretto et al., 2008Moretto EM, Marciano FT, Velludo MR, Fenerich-Verani N, Espíndola ELG, Rocha O. The recent occurrence, establishment and potential impact of Geophagus proximus (Cichlidae: Perciformes) in the Tietê River reservoirs: an Amazonian fish species introduced in the Paraná Basin (Brazil). Biodivers Conserv. 2008; 17(12):3013–25. https://doi.org/10.1007/s10531-008-9413-5
https://doi.org/10.1007/s10531-008-9413-...
; Queiroz-Sousa et al., 2018Queiroz-Sousa J, Brambilla EM, Garcia-Ayala JR, Travassos FA, Daga VS, Padial AA et al. Biology, ecology and biogeography of the South American silver croaker, an important Neotropical fish species in South America. Rev Fish Biol Fisher. 2018; 28:693–714. https://doi.org/10.1007/s11160-018-9526-1
https://doi.org/10.1007/s11160-018-9526-...
).

Our results showed that the effect of flooding on the structure (PERMANOVA) and β diversity of the fish fauna in control area was not observed in the fish farm area. The continuous habitat structure provided by the enterprise in the arrangement of shelters (cages), feed, and attracted prey (e.g., invertebrates and small fish) is used directly by wild fish species (Pereira et al., 2019Pereira LS, Demétrio JA, Cunico AM, Latini JD, Gomes LC, Agostinho AA. Cage aquaculture in Neotropical waters promotes attraction and aggregation of fish. Aquac Res. 2019; 50(10):2896–906. https://doi.org/10.1111/are.14244
https://doi.org/10.1111/are.14244...
; Nobile et al., 2020Nobile AB, Cunico AM, Vitule JRS, Queiroz J, Vidotto-Magnoni AP, Garcia DAZ et al.Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac. 2020; 12(3):1495–517. https://doi.org/10.1111/raq.12393
https://doi.org/10.1111/raq.12393...
), including the dominant species in our study (Kliemann et al., 2022Kliemann BCK, Delariva RL, Manoel LO, Silva APS, Veríssimo-Silveira R, Ramos IP. Do cage fish farms promote interference in the trophic niche of wild fish in neotropical reservoir?. Fish Res. 2022; 248:106198. https://doi.org/10.1016/j.fishres.2021.106198
https://doi.org/10.1016/j.fishres.2021.1...
). This reduces the seasonal effect of the availability of natural resources on the community (Nobile et al., 2018Nobile AB, Zanatta AS, Brandão H, Zica EOP, Lima FP, Freitas-Souza D et al. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture. 2018; 495:780–85. https://doi.org/10.1016/j.aquaculture.2018.06.053
https://doi.org/10.1016/j.aquaculture.20...
). Thus, the fish assemblage aggregates and persists in areas surrounding fish farms and tend to be dominated by non-native and generalist species (Daga et al., 2015Daga VS, Skóra F, Padial AA, Abilhoa V, Gubiani ÉA, Vitule JRS. Homogenization dynamics of the fish assemblages in Neotropical reservoirs: comparing the roles of introduced species and their vectors. Hydrobiologia. 2015; 746:327–47. https://doi.org/10.1007/s10750-014-2032-0
https://doi.org/10.1007/s10750-014-2032-...
; Pereira et al., 2019Pereira LS, Demétrio JA, Cunico AM, Latini JD, Gomes LC, Agostinho AA. Cage aquaculture in Neotropical waters promotes attraction and aggregation of fish. Aquac Res. 2019; 50(10):2896–906. https://doi.org/10.1111/are.14244
https://doi.org/10.1111/are.14244...
), contributing to greater biotic homogenization in fish farming areas.

Variation in assemblage structure is usually a response to the reordering of species abundance (Avolio et al., 2015Avolio ML, La Pierre KJ, Houseman GR, Koerner SE, Grman E, Isbell F et al. A framework for quantifying the magnitude and variability of community responses to global change drivers. Ecosphere. 2015; 6(12):1–14. https://doi.org/10.1890/ES15-00317.1
https://doi.org/10.1890/ES15-00317.1...
). Hence, the change in the structure of the ichthyofauna between seasons in the control area may have occurred due to the increase in the abundance of some species due to the environmental conditions of the wet season. The presence of habitats for natural recolonization when the water level rises is one of the main factors for the recovery of native populations after drought impacts (Bond et al., 2008Bond NR, Lake PS, Arthington AH. The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia. 2008; 600:3–16. https://doi.org/10.1007/s10750-008-9326-z
https://doi.org/10.1007/s10750-008-9326-...
). The rise in water levels enables, for example, the intense growth of aquatic macrophytes (Gomes et al., 2012Gomes LC, Bulla CK, Agostinho AA, Vasconcelos LP, Miranda LE. Fish assemblage dynamics in a Neotropical floodplain relative to aquatic macrophytes and the homogenizing effect of a flood pulse. Hydrobiologia. 2012; 685:97–107. https://doi.org/10.1007/s10750-011-0870-6
https://doi.org/10.1007/s10750-011-0870-...
), which are used by specialist species as feeding habitat or a site for laying eggs on the roots and parental care of the offspring (e.g., S. maculatus) (Sazima, Zamprogno, 1985Sazima I, Zamprogno C. Use of water hyacinths as shelter, foraging place, and transport by young piranhas, Serrasalmus spilopleura. Environ Biol Fish. 1985; 12:237–40. https://doi.org/10.1007/BF00005154
https://doi.org/10.1007/BF00005154...
; Silveira Prudente et al., 2015da Silveira Prudente B, Ferreira MAP, Rocha RM, Montag LFA. Reproductive biology of the piranha Serrasalmus gouldingi (Fink and Machado-Allison 1992) (Characiformes: Serrasalmidae) in “drowned” rivers of the Eastern Amazon. Environ Biol Fish. 2015; 98:11–22. https://doi.org/10.1007/s10641-014-0232-0
https://doi.org/10.1007/s10641-014-0232-...
). Thus, such interaction also contributes to explaining the increase in abundance and contribution of the native species S. maculatus by the SIMPER analysis in the control area, and its positive relation to the increase in the quota level.

The replacement of species in the control area showed susceptibility to water changes, which is strengthened by the variation in β diversity between the seasons in this area, a fact that was not observed in the fish farm area. In the control area, the decline in β diversity during the wet season was expected, given that β diversity in aquatic ecosystems is generally greater in drought periods (Thomaz et al., 2007Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia. 2007; 579:1–13. https://doi.org/10.1007/s10750-006-0285-y
https://doi.org/10.1007/s10750-006-0285-...
). With the decrease of water levels, the progressive loss of the littoral zone and its associated vegetation can modify or to fragment habitats (Paller, 1997Paller MH. Recovery of a reservoir fish community from drawdown related impacts, N Am J Fish Manag. 1997; 17(3):726–33. https://doi.org/10.1577/1548-8675(1997)017%3C0726:ROARFC%3E2.3.CO;2
https://doi.org/10.1577/1548-8675(1997)0...
; Gomes et al., 2012Gomes LC, Bulla CK, Agostinho AA, Vasconcelos LP, Miranda LE. Fish assemblage dynamics in a Neotropical floodplain relative to aquatic macrophytes and the homogenizing effect of a flood pulse. Hydrobiologia. 2012; 685:97–107. https://doi.org/10.1007/s10750-011-0870-6
https://doi.org/10.1007/s10750-011-0870-...
), which may result in more dissimilar assemblages, showing a tendency towards an increase in β diversity (Anderson et al., 2011Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett. 2011; 14(1):19–28. https://doi.org/10.1111/j.1461-0248.2010.01552.x
https://doi.org/10.1111/j.1461-0248.2010...
). Subsequently, with the prolonged rise in the water level and, as a consequence, more homogeneous habitats, the similarity between communities increases (Thomaz et al., 2007Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia. 2007; 579:1–13. https://doi.org/10.1007/s10750-006-0285-y
https://doi.org/10.1007/s10750-006-0285-...
).

Contrary to our expectation, there were few differences in community structure between the control and fish farm areas in each season. The greatest abundance in the fish farm area was predicted as the effect of attraction and increased densities in areas surrounding fish farms (Barrett et al., 2019Barrett LT, Swearer SE, Dempster T. Impacts of marine and freshwater aquaculture on wildlife: a global meta-analysis. Rev Aquac. 2019; 11(4):1022–44. https://doi.org/10.1111/raq.12277
https://doi.org/10.1111/raq.12277...
). This effect is mainly due to the increased abundance of opportunistic species around fish farms that contribute to differences between these areas and “natural” places (Nobile et al., 2018Nobile AB, Zanatta AS, Brandão H, Zica EOP, Lima FP, Freitas-Souza D et al. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture. 2018; 495:780–85. https://doi.org/10.1016/j.aquaculture.2018.06.053
https://doi.org/10.1016/j.aquaculture.20...
). Nevertheless, the similarity between the areas in the other ichthyofauna attributes is possibly related to the sharing of many non-native and generalist species, a common aspect in Neotropical reservoirs (Ortega et al., 2015Ortega JCG, Júlio Jr. HF, Gomes LC, Agostinho AA. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia. 2015; 746:147–58. https://doi.org/10.1007/s10750-014-2025-z
https://doi.org/10.1007/s10750-014-2025-...
; Queiroz-Sousa et al., 2018Queiroz-Sousa J, Brambilla EM, Garcia-Ayala JR, Travassos FA, Daga VS, Padial AA et al. Biology, ecology and biogeography of the South American silver croaker, an important Neotropical fish species in South America. Rev Fish Biol Fisher. 2018; 28:693–714. https://doi.org/10.1007/s11160-018-9526-1
https://doi.org/10.1007/s11160-018-9526-...
). Generalists dominate immediately after or during disturbances (Freitas et al., 2013Freitas CEC, Siqueira-Souza FK, Humston R, Hurd LE. An initial assessment of drought sensitivity in Amazonian fish communities. Hydrobiologia. 2013; 705:159–71. https://doi.org/10.1007/s10750-012-1394-4
https://doi.org/10.1007/s10750-012-1394-...
), as many specialist species require medium- to long-term flooding to recover (Beesley et al., 2014Beesley LS, Gwinn DC, Price A, King AJ, Gawne B, Koehn JD et al. Juvenile fish response to wetland inundation: How antecedent conditions can inform environmental flow policies for native fish. J Appl Ecol. 2014; 51(6):1613–21. https://doi.org/10.1111/1365-2664.12342
https://doi.org/10.1111/1365-2664.12342...
), decreasing the spatial effect on diversity patterns expected between the fish farm and control areas.

We concluded that cage fish farming can interfere in ichthyofauna responses to water changes, with similarity in the structure traits and taxonomic compositional between the drought and wet seasons. The smallest change in the structure of the ichthyofauna in the aquaculture area (fish farm), even after extreme water changes, shows that this farming system contributes to the maintenance of non-native and dominant species such G. sveni and P. squamosissimus. Likewise, a good understanding of the quota regimes required for the conservation of native fish in regulated environments is essential and particularly useful for assemblage recovery after drought events, as recorded for the control area. We assess taxonomic aspects of the fish assemblages, and variations due to impacts of water regimes or fish farming may also occur on functional and genetic aspects. Thus, future studies on the effects of fish farming, focusing on drought and flooding periods, will be extremely relevant to the fields of aquaculture and ecology.

ACKNOWLEDGEMENTS

This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES, Finance Code 001), and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, process 443103/2014–3) and by the fellowship granted to IPR (CNPq, process 303311/2018–5 and FUNDUNESP/PROPE UNESP, grant number 0305/001/14–PROPe/CDC). We would like to thank the staff at the Laboratory of Fish Ecology (Pirá/UNESP), Laboratory of Neotropical Ichthyology (LINEO/UNESP), Laboratory of Aquatic Ecology (UNESP), Laboratory of Animal Physiology Studies (LEFISA/UNESP), for helping with field collection, and Prof. Francisco Langeani Neto for the identification of the fish species (IBILCE/UNESP). We also thank Puro Peixe cage farm for its partnership in the development of this work.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Orlandi-Neto A, Amorim RV, Delariva RL, Camargo AFM, Veríssimo-Silveira R, Ramos IP. Structure and composition of ichthyofauna associated with cage fish farming and compared to a control area after severe drought in a Neotropical reservoir. Neotrop Ichthyol. 2022; 20(3):e210141. https://doi.org/10.1590/1982-0224-2021-0141

Edited-by

Paulo Pompeu

Publication Dates

  • Publication in this collection
    14 Oct 2022
  • Date of issue
    2022

History

  • Received
    23 Sept 2021
  • Accepted
    04 July 2022
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br