Differences in ecomorphology and trophic niche segregation of two sympatric heptapterids (Teleostei: Siluriformes)

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High species diversity, trophic plasticity and the broad ecological niche allow the occupation of all trophic levels in aquatic environments by fish (Motta, Norton, & Luczkovich, 1995; Wootton, 1999; Abelha, Agostinho, & Goulart, 2001), which are the main organisms used in the ecomorphological studies (Moreira & Zuanon, 2002; Ramírez, Davenport, & Mojica, 2015). Ecomorphology can be applied to describe patterns along niche breadth, using body morphology to explain the way in which organisms are using resources in the environment (Fugi, Agostinho, & Hahn, 2001; Oliveira et al., 2010; Pagotto, Goulart, Oliveira, & Yamamura, 2011; Sampaio, Pagotto, & Goulart, 2013; Prado, Goulart, & Pagotto, 2016).

Sympatric species with similar morphology, such as phylogenetic related species, are expected to present strong competitive potential (Wootton, 1999). However, the differentiation in the ecological niche as distinct use of habitats and resources allows their stable coexistence in the environment (Peres-Neto, 2004; Herder & Freyhof, 2006; Van Zwol, Neff, & Wilson, 2012). These may also be related to adaptations in morphological traits, resulting in different ways of exploring the available resources (Labropoulou & Eleftheriou, 1997; Russo, Pulcini, O’Leary, Cataudella, & Mariani, 2008; Nandi & Saikia, 2015). Thus, considering that morphology and diet are strongly correlated, the ecomorphology is an important tool to understand the exploited niche space and trophic segregation among coexisting species (Prado et al., 2016; Pease, Mendoza-Carranza, & Winemiller, 2018; Baldasso, Wolff, Neves, & Delariva, 2019).

The Heptapteridae fishes are small to medium-sized species and represent one of the largest radiations of Neotropical catfish, being endemic to this region (Bockmann & Guazzelli, 2003). Such family stands out within the Siluriformes because they occupy a wide range of habitats, from small streams to large rivers, of clear or dark waters, cold and with medium - to fast - flowing waters (Ota, Deprá, Graça, & Pavanelli, 2018). Due to similar morphology, related habits are expected for heptapterids (Bockmann & Guazzelli, 2003). The closely related species Imparfinis mirini Haseman 1991 and Cetopsorhamdia iheringi Schubart, Gomes 1959 are abundant species in streams of the Pirapó River Basin (Upper Paraná River basin) (Ota et al., 2018). Both species have an elongated body with a terminal mouth, inhabit the bottom under substrates and their diets are composed of aquatic insects (Casatti, 2002; Bonato, Delariva, & Silva, 2012; Ota et al., 2018).

Although closely related species often have similar feeding habits, niche partitioning has been inferred as a valuable mechanism to facilitate their coexistence in the Neotropical region (Prado et al., 2016; Pease et al., 2018). This mechanism involves feeding on distinct items and consequently reduction of niche overlap to avoid competitive exclusion (Schoener, 1974; Ross, 1986; Portella, Lobón‐Cerviá, Manna, Bergallo, & Mazzoni, 2017). In this context, considering that dissimilarities about morphology and habitat use can cause a small niche overlap (Hutchinson, 1959; Kokkoris, Jansen, Loreau, & Troumbis, 2002; Fowler, Lessard, & Sanders, 2014), we hypothesized that Imparfinis mirini and Cetopsorhamdia iheringi exhibit ecomorphological differences that are linked to differences in habitat use and food behavior. Thus, it is also expected a low niche overlap between these species, allowing the coexistence between them.

A total of 123 individuals were measured, but only 58 stomachs of Imparfinis mirini and 29 stomachs of Cetopsorhamdia iheringi contained food and were analyzed.

The PERMANOVA showed significant difference in ecomorphological attributes between the species (pseudo- F(1.121) = 15.18; p > 0.001). The PCA revealed the significance of the first two axes according to the Broken-Stick criterion. Together, axes 1 and 2 (Table 2) explained 38.68% and were used to characterize the morphological diversity between species (Figure 2). When analyzing the first axis of PCA, it is observed that C. iheringi is located on the negative side presenting lower values for relative area of the pectoral fin (RAPeFi), relative area of the anal fin (RAAFi), relative area of the pelvic fin (RAPFi), reason-aspect of the pectoral fin, relative length of the head (RLH) and relative length of the caudal peduncle (RLCP). Imparfinis mirini is located on the positive side presenting higher values for relative height of the mouth (RHM), relative width of the mouth (RWM) and ratio-aspect of the anal fin (RAAF).

Table 2
Eigenvalues and percentage of variation for each axis as well as the index’s loadings. The indexes that were more important for interpretation are marked in bold.

When evaluating the dietary composition of C. iheringi and I. mirini, it is observed that both species consumed predominantly aquatic food resources and Trichoptera larvae, Ephemeroptera nymph and Chironomidae larvae occurred in most of the analyzed stomachs (Figure 3A and B). However, some preferences were observed. Out of 11 food resources recorded in the diet of C. iheringi, Simuliidae larvae was highly consumed (22.6% of volume and 27.6% of occurrence) and it was an exclusive food resource to this species. Although the allochthonous feeding resources were less representative (Figure 3C and D), terrestrial Coleoptera larvae were the second most consumed by C. iheringi (21.84% of volume and 27.6% of occurrence), followed by the Trichoptera larvae (18, 2% of volume and 41.4% of occurrence). Out of 17 feeding resources consumed by of I. mirini, Trichoptera larvae dominated the diet, composing 54.9% of total volume and occurring in 76.8% of the analyzed stomachs, followed by Ephemeroptera nymph (9.9 % of the volume and 30.3% of occurrence), and Annelida (8.6% of the volume and 5.2% of occurrence). This latter and six other resources were consumed exclusively by I. mirini (Figure 3A and 3B).

Figure 2.
Ordination diagram of the first two PCA axes for the 22 ecomorphological attributes of Heptapteridae: (●) Cetopsorhamdia iheringi and (□) Imparfinis mirini. RHM = Relative height of the mouth, RWM = Relative width of the mouth, RAAF = Ratio-aspect of the anal fin, RLH = Relative length of the head, RACF = Ratio-aspect of the caudal fin, RAPeF = Reason-aspect of the pectoral fin, RAAFi = Relative area of the anal fin, RAPFi = Relative area of the pelvic fin and, RAPeFi = Relative area of the pectoral fin. Total variation explained by axes 1 and 2 = 37%.

Figure 3.
Composition and contribution of autochthonous (Auto) and allochthonous (Allo) items in the diet of Cetopsorhamdia iheringi (Ci) and Imparfinis mirini (Im), captured in April and May 2017, in streams of the Pirapó River Basin. A and C = % volume, B and D= % occurrence. An= Annelida; Ce= Ceratopogonidae; Ch= Chironomidae larvae; CoA= adult Coleoptera; CoLA= aquatic Coleoptera larvae; CoLT= terrestrial Coleoptera larvae; DiA= adult Diptera; DiP= Diptera pupae; Ep= Ephemeroptera; Hi= Hirudinea; Is= Isoptera; Od= Odonata; Pl= plants; Se= sediment; Si= Simuliidae; TrA= adult Trichoptera; TrL= Trichoptera larvae; TrP= Trichoptera pupae;Si= Simuliidae; CoLT= terrestrial Coleoptera larvae; TrL= Trichoptera larvae; Ep= Ephemeroptera; Ch= Chironomidae larvae; Se= sediment; Pl= plants; Ce= Ceratopogonidae; TrP= Trichoptera pupae; CoA= adult Coleoptera; CoLA= aquatic Coleoptera larvae; An= Annelida; Is= Isoptera; TrA= adult Trichoptera; Hi= Hirudinea; DiP= Diptera pupae; DiA= adult Diptera; Od= Odonata.

PERMANOVA also showed a significant difference in diet composition between the two species (pseudo-F(1.83) = 4.31; p < 0.05) (Figure 4) and ordination analysis evidenced separation between the species, mainly on axis 1: C. iheringi located on the negative values and I. mirini located in the positive values. Together, axes 1 and 2 explained 30.2% of the variation (Figure 4). The niche overlap was considered intermediate (0.54).

Figure 4.
Ordination diagram of the first two PCoA axes (32.7%) for the diet of two species of Heptapteridae: (●) Cetopsorhamdia iheringi and (□) Imparfinis mirini. Axis 1 explained 30.3% of data variation.

The results showed that despite Imparfinis mirini and Cetopsorhamdia iheringi are phylogenetically close and occupy the same stratum in the environment and are considered insectivorous species, they present differences in morphology and the use of food resources. Also, there is a low overlap, indicating low competition for food resources. Ecomorphological differences, mainly related to foraging, swimming, and habitat occupation favor the coexistence between these species. Correlations between diet and ecomorphology in fish are constantly observed (Neves, Delariva, & Wolff, 2015; Pease et al., 2018; Baldasso et al., 2019), which supports the idea that morphology acts as one of the mechanisms responsible for the variation of diet. In fact, sympatric species tend to differ in feeding preferences, segregating resources to avoid competitive exclusion (Hardin, 1960; Schoener, 1974).

In an attempt to explain the preference of fish for a particular resource, some factors may be directly related, such as abundance and nutritional quality, as well as their morphology and behavior. However, when we observe the diet of benthic fish, these factors in the predator-prey relationship are not clear, since the heterogeneity and complexity of habitat in the benthic region can act as a physical barrier during the foraging of benthic, preventing many preys from being consumed by fish (Hill & Grossman, 1987; Gillette, 2012, Guglielmetti, Silva, Higuti, & Fugi, 2019).’ Several studies have shown that fish belonging to benthic invertivorous guild have a very specific diet and that the use of a determinate resource is mainly attributed to trophic morphology and predation foraging (Rolla, Esteves, & Silva, 2009; Brejão, Gerhard, & Zuanon, 2013; Neves et al., 2015). In our study, morphological characteristics such as head, mouth, and fins sizes allowed both species to feed on benthic organisms, while the terminal mouth and the laterally compressed body possibly allowed the expansion of the consumption of other resources available in the environment (Pease et al., 2018), as the allochthonous items present in the diet of both species such as terrestrial Coleoptera larvae, plants, adult Coleoptera, Isoptera, adult Trichoptera, and adult Diptera.

Despite the similarities, our results showed differences in morphology between the species that are probably related to different feeding preferences. The indices that influenced Cetopsorhamdia iheringi dispersal in ordination are associated with fish that prefer benthic and high water flow regions, presenting slow swimming and movement stability (Watson & Balon, 1984; Breda et al., 2005). In addition, the smaller head length indicates that C. iheringi feeds on smaller prey (Pouilly, Lino, Bretenoux, & Rosales, 2003; Oliveira et al., 2010), as is the case of Simuliidae larvae that attach to the substrates or plant surfaces (Kiel, 2001) and was found in abundance and exclusivity in their diet. However, the indices that influenced the dispersion of Imparfinis mirini in the ordination are associated with fish that have faster progressive and retrograde movements (Breda et al., 2005) and consequently act more efficiently in the exploration of complex structurally habitats (Prado et al., 2016). In addition, I. mirini presented a greater length and width of the mouth, suggesting that species with these characteristics feed on relatively large prey (Gatz Jr., 1979; Winemiller, 1991), such as Trichoptera larvae consumption, item of great abundance in the diet this species. This high abundance in the diet can be explained because this aquatic larvae has low mobility, which makes its escape capacity lower and the larvae became more vulnerable to predation (Tófoli, Alves, Higuti, Cunico, & Hahn, 2013). In addition, since it is a relatively large invertebrate, it makes the larvae more visible to the predator (Tófoli et al., 2013).

The niche overlap value indicates a low potential for competitive interaction (Zaret & Rand, 1971). Although we have not measured food availability in this study, several studies point out that diet divergences may reduce competition when resources are limited (Hutchinson, 1957; Colloca, Carpentieri, Balestri, & Ardizzone, 2010; Guo et al., 2014; Carniatto, Fugi, & Thomaz, 2017). Besides, it should be considered that the variety and abundance of resources consumed by the species must be mediated by their morphological characteristics (Prado et al., 2016), where one species is able to explore resources that other is not (Casatti, 2002; Freitas, Montag, & Barthem, 2017; Pagotto et al., 2011). In this case, a strong competitive potential would not be expected between C. iheringi and I. mirini, since both species occupy different morphological niches.

Another important ecological factor that can promote coexistence between species is the preference for some resources (Novakowski, Fugi, & Hahn, 2004; Tófoli et al., 2013; Walker, Kluender, Inebnit, & Adams, 2013; Bison et al., 2015). The differential use of resources, even partially, is an essential component of the trophic interactions within a community (Schoener, 1974; Portella et al., 2017; Gračan, Zavodnik, Krstinić, Dragičević, & Lazar, 2016). Trophic varieties observed in species analyzed here highlight interspecific differences in the use of food items. This specialization in different resources probably allows segregation of the niche (Prado et al., 2016; Portella et al., 2017). Trichoptera was the most abundant item in I. mirini diet and the third most abundant in C. iheringi diet, which reflects the great abundance of these invertebrates in the Pirapó basin streams (Guglielmetti et al., 2019) and makes them easily predated mainly by I. mirini, which forages the substrate since it uses the head barbs to find and capture the prey (Casatti & Castro, 2006). This feature may also explain the large number of unique items found in I. mirini diet. On the other hand, the high abundance of terrestrial Coleoptera suggests that C. iheringi uses both benthic and pelagic region, consuming drifting resources (Guglielmetti et al., 2019). Thus, the prey origin and the different use of fine-scale habitat contribute to the trophic segregation between these species (Barros, Zuanon, & Deus, 2017; Richardson, Lyons, Roby, Cushing, & Lerczak, 2018).

In short, our results showed ecomorphological differences between the sympatric species, and that such variations may be determinant in diet differences. Although both species are insectivorous, they present particular preferences, resulting in the low trophic overlap. The ecomorphological and diet relationship of species enable us to understand how they perform their ecological niches (Peres-Neto, 1999; Severo-Neto, Teresa, & Froehlich, 2015). Thus, these factors seem to be essential to coexistence between these species in these environments. Studying the ecology of these species provides subsidies for the management and conservation of these ecosystems that are under constant anthropogenic effects.

We are grateful to the Universidade Estadual de Maringá (UEM) for the infrastructure and logistic support. Rosemara Fugi for contributions in the manuscript and Larissa Strictar Pereira for corrections of the English language of the manuscript.