Dietary aspects at the population and individual level of Pimelodus argenteus, a native fish species from the southern Pantanal, Brazil

Aspectos alimentares a nível populacional e individual de Pimelodus argenteus, uma espécie de peixe nativa do Pantanal Sul, Brazil

ABSTRACT

Pantanal is highly important environmentally and economically and suffers from environmental changes and anthropization. Pimelodus argenteus is a native species from the southern Pantanal and important for artisanal fishing and feeding of riverside populations. Given the assumptions, this study aimed to characterize the diet and feeding habits of P. argenteus and verify if there is variation and individual specialization in the diet in the evaluated period. For this, the specimens were acquired from an artisanal fisherman in October 2017 in the Miranda River, southern Pantanal, Mato Grosso do Sul state, Brazil. The population's diet was variable, composed of 18 food items, and its trophic guild was determined as carnivorous/malacophagous. We observed individual variation and specialization in the diet at the individual level. The consumption of bivalves with high invasive potential and non-organic items was also observed, indicating anthropic influences. These results raise questions about the possible long-term impacts on the native and economically important species. In addition, we suggest that individual specialization may have occurred in response to competitive pressures. Finally, our results can contribute to ecological information and support conservation plans for this native species and this biome with important ecosystem functions.

Keywords
Fish, Populational diet; Individual specialization; Individual variation; Biosphere reserve; World heritage site

RESUMO

O pantanal é altamente importante do ponto de vista ambiental e econômico e sofre com as mudanças ambientais e a antropização. Pimelodus argenteus é uma espécie nativa do pantanal sul, Mato Grosso do Sul, e importante para a pesca artesanal e alimentação das populações ribeirinhas. Diante dos pressupostos, este estudo teve como objetivos caracterizar a dieta e os hábitos alimentares de P. argenteus e verificar se há variação e especialização individual na dieta no período avaliado. Para isso, os exemplares foram adquiridos de um pescador artesanal em outubro de 2017 no Rio Miranda, Pantanal sul-matogrossense. A dieta da população foi variável, composta de 18 itens alimentares, e sua guilda trófica foi determinada como carnívora/malacófaga. Observamos variação individual e especialização na dieta em nível individual. Também foi observado o consumo de bivalves com alto potencial invasivo e itens não orgânicos, indicando influências antrópicas. Esses resultados levantam questões sobre os possíveis impactos a longo prazo sobre as espécies nativas e economicamente importantes. Além disso, sugerimos que a especialização individual possa ter ocorrido em resposta a pressões competitivas. Por fim, nossos resultados podem fornecer informações ecológicas para fundamentar planos de conservação dessa espécie nativa e desse bioma com importantes funções ecossistêmicas.

Palavras-chave
Peixes, Dieta populacional; Especialização individual; Variação individual; Reserva da biosfera; Patrimônio mundial

INTRODUCTION

Pantanal is the most extensive continuous floodplain in the world (Alho et al., 2019; Pozer & Nogueira, 2004), with approximately 150,000 km² of wetlands forming a mosaic of landscapes with high richness and diversity of fauna and flora (Alho et al., 2019; Fernandes et al., 2010; Pozer & Nogueira, 2004). This mosaic of landscapes provides a wide variety of food and reproductive resources for fish (Alho, 2011), resulting in the occurrence of 386 species of fish (Gimênes Júnior & Rech, 2022). In addition, wetlands such as the Pantanal have important ecosystem functions such as maintaining microclimates, habitat for endangered species, and river flow control (Clarkson et al., 2013; Mitsch et al., 2015). Due to these characteristics, Pantanal is considered a biosphere reserve and a world heritage site by the United Nations Educational, Scientific, and Cultural Organization (Stevaux et al., 2020).

Pantanal is highly important economically for artisanal, commercial, and sport fishing (Chiaravalloti, 2019; Chiaravalloti et al., 2022; Da Silva & Simoni, 2012; Kakuru et al., 2013). Fishing practiced by the riverside population and artisanal professional fishermen generates employment and income for thousands of people (Chiaravalloti et al., 2022). However, this biome has been modified by human actions that interfere with the aquatic environment (Tomas et al., 2019). Degradation of natural habitats through fragmentation, deforestation, fires, pollution, and replacement of vegetation with pasture are some examples of these anthropic impacts (Alho et al., 2019). In addition, the introduction of non-native species (Alho et al., 2011; Gimênes Júnior & Rech, 2022) and excessive use of natural resources as predatory fishing (Bertolino et al., 2022) are reported.

Pimelodus argenteus Perugia, 1891, a fish species with economic and environmental importance, is a native to the southern Pantanal, Mato Grosso do Sul state, and presents the potential for artisanal fishing, serving as a source of income for riverside populations (Ramos Filho et al., 2010; Gimênes Júnior & Rech, 2022). Although P. argenteus is classified under conservation status as least concern (ICMBio, 2018), conservation measures for this species are necessary, and information on biology can contribute to future conservation plans. In this context, through fish feeding, it is possible to know a little about the species’ biology and evaluate the interactions between aquatic organisms and the environment (Chase & Leibold, 2003). Neotropical fishes show plasticity and trophic opportunism that allow the consumption of food items available in time and space, thus reflecting the relationships between aquatic and terrestrial environments (Abelha et al., 2001). In the case of omnivorous species, such as P. argenteus (Resende et al., 2000), foods of various origins are consumed, whether aquatic or terrestrial, organic, or non-organic (Novakowski et al., 2008).

From the perspective of evaluating the interactions of fish with the environment, considering individuals’ behavior is paramount. Studies demonstrated that individuals respond differently to environmental variations considering their requirements, aptitude, and life experience (Araújo et al., 2008, 2010; Cunha et al., 2018; Jirka & Kraft, 2017). Individuals may vary in the exploration and consumption of food items resulting in generalist populations composed of specialist individuals (Pires et al., 2011; Coblentz et al., 2017; Correa & Winemiller, 2014). According to Bolnick et al. (2003), the variation in individuals’ use of food resources indicates individual specialization and can result in greater food amplitude for the population. In this context, the population will be more resistant to trophic imbalance since, in the scarcity of a food resource, for example, few individuals will be affected (Bolnick & Ballare, 2020).

MATERIAL AND METHODS

Study area

The collections were carried out on the right bank of the Miranda River, in the Passo do Lontra, southern Pantanal, Mato Grosso do Sul state, Brazil (Fig. 1). The Pantanal wetland is in the Upper Paraguay River Basin between Mato Grosso and Mato Grosso do Sul states. The climate is tropical, with an average annual temperature of 25°C and well-defined seasons (Stevaux et al., 2020). In the southern Pantanal, the flooding period occurs between April and June; in other months, the water levels are minor (dry period; Junk & Cunha, 2005). Although rainfall is less frequent in April and June, flooding occurs between these months because of the slow drainage of the headwaters (Boin et al., 2019).

Figure 1
Study area on the Miranda River, Passo do Lontra, southern Pantanal, Mato Grosso do Sul state, Brazil.

Collection of biological material

Twenty-eight specimens of P. argenteus were acquired from an artisanal fisherman in October 2017 (SISBio authorization no. 54583-1; SISGEN certificate no. A120E5C; Ethics Committee on Animal Experimentation of Universidade Estadual Paulista “Júlio de Mesquita Filho” authorization no. 005/2019). Voucher specimens were deposited in the Fish Collection, Coleção Ictiológica de Três Lagoas (CITL), Universidade Federal do Mato Grosso do Sul, Brazil (CITL 1176).

Laboratory analyses

All specimens had their standard length (cm) and total mass (g) measured using an ichthyometer (0.1 cm) and analytical balance (0.01 g), respectively. Subsequently, the stomachs were removed, fixed in a 4% formalin solution, and preserved in 70% alcohol. Stomach contents were examined under an optical stereomicroscope, and food items were identified to the lowest possible taxonomic level (Bicudo & Bicudo, 1970; Mugnai et al., 2010). The food items were quantified according to the gravimetric method (Hyslop, 1980) using the mass of each food item obtained on a precision analytical balance (0.0001 g). In the case of small items, a percentage was assigned concerning the total mass of stomach contents. The food item earthworm, when found, was removed from the analysis because it corresponded to the bait used by the fishermen.

Data analysis

For data analysis, the mass values of the food items were subjected to an adjustment to the mass of the consuming fish to minimize the effect of fish size on the amounts of food consumed. For this, Eq. 1 was adapted from Ahlbeck et al., (2012):

$$\mathrm{AIW}=\mathrm{WI}/\mathrm{WF}$$ (1)

Where: AIW: the weight of the food item consumed adjusted for fish weight; WI: the weight of the food item; WF: the weight of the fish.

Then, a matrix with the adjusted mass consumption data (decimal numbers) was used for all the analyses.

Food items consumed by the population and individuals were identified using bar graphs representing the percentage of consumption. The trophic guild of the population was determined considering the predominance of a type of food resource (≥ 51% of the total volume) in the population’s diet (adapted from Corrêa et al., 2011).

Diet variation between individuals was verified using an inter-individual variation index (E). The calculation of E is according to Eq. 2 (Araújo et al. 2008):

$$\mathrm{E}=1-{\mathrm{w}}_{\mathrm{ij}}$$ (2)

Where: w_ij: the measure of the niche pairwise overlap between individual i and j.

Values of E index closer to 0 indicate identical individual diets, and values closer to 1 indicate inter-individual dietary variation (Araújo et al., 2008).

Individual specialization (V) was measured using the Eq. 3, proposed by Bolnick et al. (2007):

$$\text{V =1 - IS}$$ (3)

Where: IS: the average of individual PSi values (proportional similarity index). PSi was calculated by comparing the distribution of the individual’s diet with that of the population (Bolnick et al., 2002; Schoener, 1968). High values of V close to 1 indicate that individuals’ diets are more specialized (Bolnick et al., 2007).

The E and Psi indices, presented descriptively, were calculated by the Eindex and Psicalc functions, respectively, using the RInSP package in the RStudio programming environment (RStudio Team, 2022).

RESULTS

The stomach contents of 28 individuals were analyzed, and the population’s diet consisted of 18 food items of different origins. Aquatic and terrestrial insects, fish, mollusks, algae, plants, and detritus comprise the diet of P. argenteus (Fig. 2). The non-native freshwater mussel Limnoperna fortunei (Dunker 1857) (Bivalvia) was the leading food consumed, followed by detritus and terrestrial insects (Fig. 2; Kliemann et al., 2024). The consumption percentage of 54% of L. fortunei characterizes this population as carnivorous/malacophagous (Fig. 2; Kliemann et al., 2024). Synthetic items were also observed in the stomach contents of four individuals, such as dishwashing sponges, plastics, plastic monofilament thread, and bubble gum.

Figure 2
Percentage mass of the diet composition of the population level of Pimelodus argenteus sampled in October 2017 in the Miranda River, Passo do Lontra, southern Pantanal, Mato Grosso do Sul state, Brazil.

When evaluating feeding individually, we observed that the consumption of food items varied between individuals, with some individuals consuming only L. fortunei and terrestrial insects and other individuals consuming aquatic insects, algae, and detritus (Fig. 3). However, we observed that L. fortunei and terrestrial insects were consumed by most individuals. In addition, index E (0.73) and V (0.62) showed an inter-individual variation and individual specialization in the diet, respectively.

Figure 3
Percentage mass of the diet composition of individuals of Pimelodus argenteus from the Miranda River, Passo do Lontra, southern Pantanal, Mato Grosso do Sul state, Brazil. Each bar represents the food items consumed by an individual.

DISCUSSION

The specimens of P. argenteus analyzed in the present study consumed food items from various sources, such as aquatic and terrestrial insects, fish, mollusks, algae, plants, and detritus. In addition, we observed the main consumption of the non-native freshwater mussel L. fortunei, which characterizes this population as carnivorous/malacophagous. When evaluating feeding individually, the individuals presented differences in the consumption of food items, corroborating the inter-individual variation and individual specialization in the diet observed by the E and V indices, respectively.

The population of P. argenteus consumed a wide variety of food items of animal and plant origin, corroborating the trophic opportunism and generalist diet observed in another study in southern Pantanal/Miranda River (Resende et al., 2000). Resende et al. (2000) reported the consumption of aquatic and terrestrial invertebrates and plants and the degree of digestion of these items, which indicated a benthic foraging strategy. Here, we observed a high percentage of detritus and terrestrial insect consumption, confirming the benthic foraging of P. argenteus.

Despite a diet with a wide variety of food resources, P. argenteus consumed much L. fortunei (Bivalvia) compared to other food items. Studies show that the fish’s diet reflects the availability of food in the environment (Kliemann et al., 2019; Neves et al., 2020) since fish are trophic opportunists (Chase & Leibold, 2003; Gerking, 1994; Pires et al., 2011). In addition, the energy cost in the search, capture, handling time, and digestion determines the cost-benefit ratio during foraging (Gerking, 1994; Pires et al., 2011; Schoener, 1971). Thus, we suggest that the high availability and ease of capturing Limnoperna fortunei in the study area justify its high consumption. Limnoperna fortunei, known as golden mussel, was recorded in 2003 in Passo do Lontra (study area) on floating platforms made of wood and plastic gallons (De Oliveira et al., 2004).

The high availability of L. fortunei in Brazilian aquatic ecosystems is directly related to its use as a food resource by wild ichthyofauna. According to Cataldo (2015), after the introduction of L. fortunei, the diet of several fish species changed. Omnivorous species varied from a low-quality diet based on plants and few animals to a high-energy diet dominated by these mollusks (Boltovskoy et al., 2006; Garcia & Protogino, 2005; Ferriz et al., 2000). Several researchers evaluated the predatory ability of L. fortunei by fish and reported the main predators: Pterodoras granulosus (Valenciennes 1821) (wild fish; Ferriz et al., 2000), Rhinodoras dorbignyi (Kner 1855), Brochiloricaria chauliodon (Isbrücker 1979) (wild fish; Garcia & Protogino, 2005), Megaleporinus obtusidens (Valenciennes 1837) (wild and cultivated fish; Garcia & Protogino, 2005; Rosa et al., 2014; de Melo Rosa et al., 2019), Leporinus friderici (Bloch 1794), Piaractus mesopotamicus (Holmberg 1887), Pimelodus maculatus Lacepède 1803, and Geophagus sveni Lucinda, Lucena & Assis 2010 (syn. Geophagus proximus (Castelnau 1855) (wild fish; Rosa et al., 2014). Specifically, in P. maculatus, golden mussels were found in large numbers and intact in their stomachs (Rosa et al., 2014; ICMBio, 2018), corroborating the observations reported in this study.

At the population level, we observed trophic generalism of the P. argenteus, but, at the individual level, we observed a variation and specialization in the diet of individuals. Generalist populations composed of specialist individuals were previously observed in fish studies (Araújo et al., 2010; Cunha et al., 2018; Paz Cardozo et al., 2021). Researchers observed a broad population diet with items of animal and plant origins (Cunha et al., 2018; Neves et al., 2020). However, at the individual level, they observed specialists consuming subsets of the population’s diet and varying food items consumed among themselves (Cunha et al., 2018; Neves et al., 2020). This diet variation among individuals is paramount for population stability, reducing risks when some food resources are scarce (Bolnick & Ballare, 2020).

Some studies associate the high variation and individual specialization with dry periods in response to increased intraspecific competition (Araújo et al., 2010; Cobain et al., 2019; Kovalenko et al., 2012). In this context, individuals add new resources to their diet to reduce intraspecific competition (Araújo et al., 2010; Svanback & Bolnick, 2005, 2007). Thus, individuals tend to vary in the use of resources, which is lower due to the contraction of ecosystems and less ecological opportunity (Cachera et al., 2017; Paz Cardozo et al., 2021). In the case of floodplains, the contraction of the ecosystem in the dry period is very evident compared to periods of flooding, in which the wetlands are connected to the river channels (Stevaux et al., 2020). Here, although we observed the consumption of L. fortunei and terrestrial insects by most individuals, other food items were also consumed, indicating variation among individuals. Moreover, we observed an inter-individual variation (E). Likewise, we suggest that in the scenario of less food availability (dry period, October), the individuals share the most abundant food item L. fortunei, and terrestrial insects. However, other food items (less abundant; see Fig. 2) are also consumed to supply energy demands and decrease intraspecific competition.

Another relevant aspect observed in our results was the occurrence of synthetic food items, such as plastic, bubble gum, and dishwashing sponges. The ingestion of synthetic materials indicates anthropic influence on the Miranda River, as suggested by Camargo et al. (2022), De Faria et al. (2021), and Marchini (2003). Pantanal is going through a series of environmental impacts that degrade the environment and interfere with the aquatic environment (Tomas et al., 2019). The microplastics in fish from the southern Pantanal have been reported to be associated with water contamination by industrial and urban pollutants and tourism, and fishing residues (Camargo et al., 2022; De Faria et al., 2021). Plastics and toxins in aquatic organisms concern researchers globally since adverse physiological effects are associated with the consumption of microplastics by fish (Fu et al., 2020; Lönnstedt & Eklöv, 2016). Due to the small size of the microplastics, they can be consumed by fish of all sizes and thus reach all levels of development (Azevedo-Santos et al., 2019). In this context, we emphasize the importance of studies with aquatic organisms to obtain data on the contamination of plastic waste in aquatic environments.

CONCLUSION

Research on a population of native fish in the southern Pantanal, Mato Grosso do Sul state revealed their generalist diet and carnivorous/malacophagous feeding habits. The study found that the primary food item for P. argenteus is a non-native bivalve species with high invasive potential, alongside synthetic materials like plastic, dishwashing sponges, and bubble gum in their stomachs. These findings suggest significant anthropic influences on the fish, raising concerns about long-term impacts on this economically important species. Additionally, the study confirms anthropic impacts on the Pantanal biome. Individual specialization in diet was observed during the dry period, possibly due to competitive pressures. Future research comparing flood and dry periods could provide insights into behavioral adaptations to seasonal food availability. Overall, these findings are valuable ecological information for conservation efforts in the Pantanal biome and the preservation of P. argenteus.

ACKNOWLEDGMENTS

The authors would like to thank the Universidade Estadual Paulista “Júlio de Mesquita Filho”, Faculdade de Engenharia de Ilha Solteira, Laboratório de Ictiologia Neotropical, for the logistical support and facilities provided during this work.

• FUNDING
  Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  Finance Code 001
  Conselho Nacional de Desenvolvimento Científico e Tecnológico
  Grant No.: PIBIC 47816; 303311/2018-5

DATA AVAILABILITY STATEMENT

Supplementary data are available at https://zenodo.org/records/12584903

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Edited by

• Section editor:
  Raniere Garcez C. Sousa https://orcid.org/0000-0002-5620-389X

Publication Dates

• Publication in this collection
  22 Aug 2025
• Date of issue
  2024

History

• Received
  07 Oct 2023
• Accepted
  06 July 2024