Is coexistence between non-native and native Erythrinidae species mediated by niche differentiation or environmental filtering? A case study in the upper Paraná River floodplain

Larissa S. Pereira Fábio T. Mise Luiz F. C. Tencatt Matheus T. Baumgartner Angelo A. Agostinho About the authors

ABSTRACT

The limiting similarity theory predicts that divergence in the functional traits of native and introduced species is an essential component in species establishment, as introduced species must occupy a niche that is unoccupied by resident species. On the other hand, the environmental filtering hypothesis predicts convergence between introduced and native species, as both possess traits that make them adapted to the local abiotic environment. Morphology, spatial co-occurrence, diet, feeding selectivity, and niche breadth and overlap of Erythrinidae were evaluated to detect possible mechanisms acting in the coexistence between non-native and native species. Native (Hoplias sp. B and Hoplias cf. malabaricus) and non-native (Hoplerythrinus unitaeniatus and Hoplias mbigua) species presented differences in morphological traits, spatial co-occurrence, diet, selectivity, and niche breadth and overlap. The mechanisms mediating species coexistence seem to vary according to species. The absence of spatial and feeding overlap suggests that non-native species H. unitaeniatus occupy a different niche than native species, supporting its successful establishment without eliminating the native species. However, low feeding overlap and similar morphologies between non-native and native species of Hoplias point to environmental filters; in this case, the non-native H. mbigua is able to establish due to similarities in functional traits.

Keywords:
Competition; Co-occurrence; Fish feeding; Morphology; Predation

RESUMO

Teorias sobre nicho ecológico afirmam que divergência em traços funcionais entre espécies nativas e introduzidas são essenciais ao estabelecimento da espécie introduzida, pois estas devem ocupar um nicho não utilizado pelas espécies residentes. Por outro lado, a teoria de filtros ambientais afirma a convergência entre espécies introduzidas e nativas, pois ambas possuem traços funcionais que fazem com que essas espécies estejam mais adaptadas as variáveis ambientais. Foram avaliadas a morfologia, ocorrência espacial, dieta, seletividade alimentar, sobreposição e largura de nicho em Erythrinidae para detectar possíveis mecanismos atuando na coexistência de espécies nativas e não nativas. Espécies nativas (Hoplias sp. B e Hoplias cf. malabaricus) e não nativas (Hoplerythrinus unitaeniatus e Hoplias mbigua) apresentaram diferenças em todos os atributos testados. Os mecanismos mediando a coexistência de espécies nativas e não nativas parecem variar de acordo com a espécie considerada. A ausência de sobreposição espacial e na dieta sugere que a espécie não nativa H. unitaeniatus ocupa um nicho distinto que as espécies nativas, favorecendo seu estabelecimento sem eliminar as espécies nativas, apontando para segregação de nicho. Por outro lado, morfologias similares, porém com diferentes dietas foram observadas para as espécies de Hoplias, sugerindo que as espécies coexistem devido à filtros ambientais, assim, neste caso, a espécie não nativa H. mbigua é capaz de se estabelecer no novo ambiente devido à similaridades em traços funcionais.

Palavras-chave:
Alimentação de peixes; Competição; Co-ocorrência; Morfologia; Predação

Introduction

Theories about competition and niche segregation predict that species coexistence is achieved through differences in species niches. In this case, when demand for resources exceeds supply, there will be increased competition, and tolerance of interspecific niche overlap will decline (Pianka, 1974Pianka ER. Niche overlap and diffuse competition. Proc Natl Acad Sci U S A. 1974; 71(5):2141-45., 1981Pianka ER. Competition and niche theory. In: May RM, editor. Theoretical ecology: principles and applications. Oxford: Blackwell Scientific Publications; 1981. p.167-196.). Therefore, niche differentiation will lead to a reduction in the niche overlap between potential competitors, reducing competition and allowing coexistence; in other words, there is limited similarity among coexisting species (MacArthur, 1958MacArthur RH. Population ecology of some warblers of northeastern coniferous forests. Ecology. 1958; 39(4):599-619.; Pianka, 1973Pianka ER. The structure of lizard communities. Annu Rev Ecol Syst. 1973; 4(1):53-74., 1974Pianka ER. Niche overlap and diffuse competition. Proc Natl Acad Sci U S A. 1974; 71(5):2141-45.; Schoener, 1974Schoener TW. Resource partitioning in ecological communities. Science. 1974; 185(4145):27-39.). For species coexisting in the same habitat, niche differences might involve changes in some combination of strategies for habitat use, such as feeding time, energy allocation, and defense (Winemiller et al., 2015Winemiller KO, Fitzgerald DB, Bower LM, Pianka ER. Functional traits, convergent evolution, and periodic tables of niches. Ecol Lett. 2015; 18(8):737-51.), including diet restrictions through feeding selectivity or niche retraction (Correa, Winemiller, 2014Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology. 2014; 95(1):210-24.). According to the limited similarity theory, differences in resource use are crucial in species coexistence and have likely resulted in the selection for optimal morphologies that reduce competition for resources (De León et al., 2014De León LF, Podos J, Gardezi T, Herrel A, Hendry AP. Darwin’s finches and their diet niches: The sympatric coexistence of imperfect generalists. J Evol Biol. 2014; 27(6):1093-104.).

On the other hand, species coexistence can be mediated by environmental filters, as predicted by the niche filtering hypothesis (sensuSouthwood, 1977Southwood TRE. Habitat, the templet for ecological strategies? J Anim Ecol. 1977; 46(2):336-65.). In this case, coexisting species would be more similar to one another than expected by chance due to the abiotic properties of the habitat, which would act as a filter allowing only a narrow spectrum of species to survive (Zobel, 1997Zobel M. The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends Ecol Evol. 1997; 12(7):266-69.). According to this hypothesis, habitat characteristics can be viewed as filters imposed on species gene pools to select traits suited to a particular set of environmental conditions (Diaz et al., 1998Diaz S, Cabido M, Casanoves F. Plant functional traits and environmental filters at a regional scale. J Veg Sci. 1998; 9(1):113-22.), resulting in a higher degree of biological similarity among coexisting species than would be expected by chance (Cornwell et al., 2006Cornwell WK, Schwilk DW, Ackerly DD. A trait-based test for habitat filtering: convex hull volume. Ecology. 2006; 87(6):1465-71.; Mouillot et al., 2007Mouillot D, Dumay O, Tomasini JA. Limiting similarity, niche filtering and functional diversity in coastal lagoon fish communities. Estuar Coast Shelf Sci. 2007; 71(3-4):443-56.). Considering introductions, once species have passed through dispersal and abiotic filters, that is, they were able to arrive at a site, survive and grow under the prevailing conditions, niche-based interactions will have little or no effect on these species interactions (Thompson et al., 2010Thompson K, Petchey OL, Askew AP, Dunnet NP, Beckerman AP, Willis AJ. Little evidence for limiting similarity in a long-term study of a roadside plant community. J Ecol . 2010; 98(2):480-87.).

According to the limiting similarity theory, coexisting species are dissimilar due to biotic interactions and are thus complementary, while in the environmental filtering hypothesis, the assembly is more similar due to similar environmental conditions and thus ecologically redundant (Mouillot et al., 2007Mouillot D, Dumay O, Tomasini JA. Limiting similarity, niche filtering and functional diversity in coastal lagoon fish communities. Estuar Coast Shelf Sci. 2007; 71(3-4):443-56.). The first theory would predict that the divergence in functional traits of native and introduced species is an essential component in species establishment because each niche is occupied by the best competitor species and, as species with high similarity in their biological features are likely to have the same Eltonian niche (Devictor et al., 2010Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W et al. Defining and measuring ecological specialization. J Appl Ecol. 2010; 47(1):15-25.), these species cannot co-occur and have to segregate along temporal, spatial and/or environmental gradients to coexist regionally (Mouchet et al., 2013Mouchet MA, Burns MDM, Garcia AM, Vieira JP, Mouillot D. Invariant scaling relationship between functional dissimilarity and co-occurrence in fish assemblages of the Patos Lagoon estuary (Brazil): environmental filtering consistently overshadows competitive exclusion. Oikos. 2013; 122(2):247-57.). On the other hand, the environmental filtering hypothesis predicts convergence between introduced and native species, as both possess traits that make them adapted to the local abiotic environment (Cross et al., 2015Cross EL, Green PT, Morgan JW. A plant strategy approach to understand multidecadal change in community assembly processes in Australian grassy woodlands. J Ecol. 2015; 103(5):1300-07.) (Tab. 1).

Tab. 1
Main definitions and assertions of each theory, highlighting differences between them.

In the upper Paraná River floodplain, native and introduced Erythrinidae species coexist. The native Hoplias sp. B and Hoplias cf. malabaricus (Pazza, Júlio-Jr, 2003Pazza R, Júlio-Jr HF. Occurrence of three sympatric cytotypes of Hoplias malabaricus (Pisces, Erythrinidae) in the upper Paraná river foodplain (Brazil). Cytologia (Tokyo). 2003; 68(2):159-63.; Graça, Pavanelli, 2007Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Maringá: Eduem; 2007.; Bifi, 2013Bifi AG. Revisão taxonômica das espécies do grupo Hoplias malabaricus (Bloch, 1794) (Characiformes: Erythrinidae) da bacia do rio da Prata. [PhD Thesis]. Maringá, PR: Universidade Estadual de Maringá; 2013.) currently coexist with Hoplias mbigua Azpelicueta, Benítez, Aichino, Mendez, 2015 and Hoplerythrinus unitaeniatus (Spix, Agassiz, 1829), which were introduced to this region after the flooding of the geographical barrier of the Sete Quedas Falls to create the Itaipu Reservoir (Júlio-Jr et al., 2009Júlio-Jr HF, Dei Tós C, Agostinho AA, Pavanelli CS. A massive invasion of fish species after eliminating a natural barrier in the upper rio Paraná basin. Neotrop Ichthyol. 2009; 7(4):709-18.). These are typical carnivorous fish with a preference for lentic environments, which are widely distributed in South American basins (Oyakawa, 2003Oyakawa OT. Family Erythrinidae. In: Reis RE, Kullander SO, Ferraris CJ, Jr., organizers. Check list of the freshwater fishes of South and Central America. Porto Alegre: Edipucrs; 2003. p.238-240.). Considering that interactions within the same family are stronger (Golani, Galil, 1991Golani D, Galil B. Trophic relationships of colonizing and indigenous goatfishes (Mullidae) in the eastern Mediterranean with special emphasis on decapod crustaceans. Hydrobiologia . 1991; 218(1):27-33.; Golani, 1993Golani D. The biology of the Red Sea migrant, Saurida undosquamis in the Mediterranean and comparison with the indigenous confamilial Synodus saurus (Teleostei: Synodontidae). Hydrobiologia. 1993; 271(2):109-17.) and that phylogenetic niche conservatism would predict high similarities in ecological niche use among closely related species, leading to competitive exclusion (Dammhahn et al., 2015Dammhahn M, Rakotondramanana CF, Goodman SM. Coexistence of morphologically similar bats (Vespertilionidae) on Madagascar: stable isotopes reveal fine-grained niche differentiation among cryptic species. J Trop Ecol. 2015; 31(2):153-64.), some mechanism must be acting to mediate the coexistence of these species.

Considering the limiting similarity theory, there should exist a mechanism that determines differences in the use of resources, such as space and food. On the other hand, according to the environmental filtering hypothesis, persistence in a particular environment would lead to similar traits among these species, and, consequently, similar resource use. Therefore, the objective of this study was to identify whether such mechanisms are acting as mediators of species coexistence in Erythrinidae in the upper Paraná River floodplain and the mechanism that most contributes to it, based on morphological and ecological traits. If species coexistence is mediated by niche differentiation, niche segregation, in terms of space and food, between native and introduced species with a larger divergence in ecological traits would be expected, while if species coexistence is mediated by environmental filtering, we would expect that species would be more similar in ecological traits.

Material and Methods

Sampling. The upper Paraná River floodplain (22°-22°50’ S and 53°15’-53°40’ W) is located in the lower third of the upper Paraná River and is the only remnant of the upper Paraná River with lotic waters within Brazil. This area is characterized by high biodiversity and endemic fauna, which are highly threatened due to hydrological alterations and species invasions (Agostinho et al., 2005Agostinho AA, Thomaz SM, Gomes LC. Conservation of the biodiversity of Brazil’s inland waters. Conserv Biol. 2005; 19(3):646-52.).

Sampling was performed as part of the PELD project (Long Term Research Project - Site 6 - CNPq) in different environments of the floodplain, totaling 36 sampling stations (fig. 1 of Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio-Jr HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná river floodplain. Hydrobiologia . 2008; 607(1):187-98.). These environments included connected and non-connected lakes, channels, and the main river channel. Fish species were captured quarterly from March 2007 to June 2013 using seine and gill nets of different mesh sizes (2.4 to 16 cm between opposite knots). The gill nets were deployed for a 24-hour period and checked at 8:00 AM, 4:00 PM, and 10:00 PM. All sampled fish were identified, measured, anaesthetized (Benzocaine), and euthanized. The Erythrinidae species were eviscerated, having their stomachs removed and preserved in 10% formalin for later analysis. Species were identified according to Graça, Pavanelli (2007Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Maringá: Eduem; 2007.), except the species of Hoplias, which were identified according to Bifi (2013Bifi AG. Revisão taxonômica das espécies do grupo Hoplias malabaricus (Bloch, 1794) (Characiformes: Erythrinidae) da bacia do rio da Prata. [PhD Thesis]. Maringá, PR: Universidade Estadual de Maringá; 2013.). Only adult Erythrinidae were used for the analyses. The adults were selected by the standard length at first gonadal maturation (L50), which corresponds to the length at which 50% of the individuals are able to reproduce; for H. unitaeniatus, the L50 is 165 mm for females and 140 mm for males, and for Hoplias species, it is 164 mm and 152 mm for females and males, respectively (Suzuki et al., 2004Suzuki HI, Vazzoler AEAM, Marques EE, Lizama MAP, Inada P. Reproductive ecology os the fish assemblages. In: Thomaz SM, Agostinho AA, Hahn NS. The upper Paraná river and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers; 2004. p.271-291.).

Voucher specimens were deposited in the Fish Collection of Nupélia (Núcleo de Pesquisa em Limnologia, Ictiologia e Aquicultura - UEM/Maringá). H. mbigua: NUP 9953, 7589, 3456, 7584, 7582, 7590, 9725, 7592, 10437, 4253, 269; Hoplias sp. B: NUP 10439, 12260, 12285, 10438, 10226, 10225, 3040, 6399; H. cf. malabaricus: NUP 11415, 12257, 265, 9698, 11200, 11132, 7286, 3458, 12291, 1140; H. unitaeniatus: NUP 11289, 4160, 9710, 10599, 8635, 8857.

Morphological analysis. The fish used for morphological analyses were obtained from the Fish Collection of Nupélia and from samples. A total of 90 individuals were measured, with 28 H. mbigua, 21 Hoplias sp. B, 18 Hoplias cf. malabaricus, and 23 H. unitaeniatus. The standard length ranges of the species were as follows: H. mbigua - 170.78 to 287 mm, Hoplias sp. B - 160.5 to 347 mm, H. cf. malabaricus - 175 to 255 mm, and H. unitaeniatus - 140 to 248 mm.

Morphological linear measures related to trunk, fins, and head were taken with the aid of a digital caliper (approximation of 0.01 mm); measures greater than 130 mm were taken with a ruler. Measurements of fins and eye areas were obtained from the outline drawings of the structures on plastic sheets, which were subsequently scanned to calculate the internal area using the software AutoCAD (Autodesk, 2013Autodesk. AutoCAD: graphic computation. 2013.).

A total of 19 ecomorphological indices were calculated from the linear morphometric measurements and the areas to represent the occupation of trophic and spatial niches by species. The use of indices aims to eliminate the effect of individual size, allowing comparisons related only to body shape and its structures (Winemiller, 1991Winemiller KO. Ecomorphological diversification in lowland freshwater fish assemblages from five biotic regions. Ecol Monogr . 1991; 61(4):343-65.). The following indices were used: compression index (CI), depression index (DI), relative height of body (RHB), compression index of caudal peduncle (CIPd), relative length of caudal peduncle (RLPd), relative height of caudal peduncle (RHPd), relative width of caudal peduncle (RWPd), relative length of head (RLHd), relative height of head (RHHd), relative width of head (RWHd), eye position (EP), relative area of eye (RAE), relative height of dorsal fin (RHD), relative area of dorsal fin (RAD), aspect ratio of caudal fin (ARC), relative height of anal fin (RHA), aspect ratio of anal fin (ARA), aspect ratio of pectoral fin (ARPt), and aspect ratio of pelvic fin (ARPv). More details about the linear and area measures involved in the calculation of morphological proportions, as well as their respective ecological explanations, can be found in Oliveira et al. (2010Oliveira EF, Goulart E, Breda L, Minte-Vera CV, Paiva LRS, Vismara MR. Ecomorphological patterns of the fish assemblage in a tropical floodplain: effects of trophic, spatial and phylogenetic structures. Neotrop Ichthyol . 2010; 8(3):569-86.).

To highlight the interspecific morphological patterns, a principal components analysis (PCA) was conducted using the ecomorphological indices. The selection of the axes for interpretation was carried out according to the broken-stick model (Jackson, 1993Jackson DA. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology. 1993; 74(8):2204-14.), which creates a null distribution of eigenvalues for comparison with the observed values. After the selection of the axes by the broken-stick model, an analysis of variance (ANOVA) was applied, using the axis scores (dependent variable) to identify possible significant morphological segregation among species (categorical variable). Finally, only the selected axes that presented significant results in the ANOVA were retained for interpretation.

Spatial co-occurrence analysis. Null models for species co-occurrence were used to assess whether spatial segregation could be a major driver of species co-existence. Null models are pattern-generating models based on randomized ecological data (Gotelli, McCabe, 2002Gotelli NJ, McCabe DJ. Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology. 2002; 83(8):2091-96.). This technique allows the comparison of an observed co-occurrence pattern against randomized occurrence data, which represents co-occurrence expected by chance, with no ecological relationship between species. The metric chosen was the C-score (Stone, Roberts, 1990Stone L, Roberts A. The checkerboard score and species distributions. Oecologia. 1990; 85(1):74-79.), which represents the average number of checkerboard units in the species matrix. Checkerboard units indicate samples in which species A is present and species B is absent and vice versa (Stone, Roberts, 1990Stone L, Roberts A. The checkerboard score and species distributions. Oecologia. 1990; 85(1):74-79.). The observed C-score was compared with C-scores generated by 10,000 randomizations using an algorithm that keeps the row and column sums fixed (“sim 9”; Gotelli, 2000Gotelli NJ. Null model analysis of species co-occurrence patterns. Ecology. 2000; 81(9):2606-21.). Statistical differences between the observed and simulated C-scores suggest different patterns of species co-occurrence. Significant negative values mean that species are co-occurring more often than expected by chance, suggesting an aggregation pattern (Stone, Roberts 1992Stone L, Roberts A. Competitive exclusion, or species aggregation? - An aid in deciding. Oecologia . 1992; 91(3):419-24.), while significant positive values indicate less species co-occurring than expected by chance, suggesting a segregation pattern (Gotelli, McCabe, 2002Gotelli NJ, McCabe DJ. Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology. 2002; 83(8):2091-96.). In addition, the total and relative number of occurrences was evaluated for each pair of species to assess which species contributed the most to the observed pattern.

Dietary analysis. To avoid diet variations caused by seasonal changes in the floodplain (dry and flood periods) (Power et al., 1995Power ME, Sun A, Parker G, Dietrich WE, Wootton JT. Hydraulic food-chain models. Bioscience. 1995; 45(3):159-67.; Abelha et al., 2001Abelha MCF, Agostinho AA, Goulart E. Plasticidade trófica em peixes de água doce. Acta Sci Biol Sci. 2001; 23(2):425-34.; Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio-Jr HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná river floodplain. Hydrobiologia . 2008; 607(1):187-98.), diet analyses were performed only for dry periods with river levels below 450 cm for the Baía and Paraná Rivers and 275 cm for the Ivinhema River (Suzuki et al., 2009Suzuki HI, Agostinho AA, Bailly D, Gimenes MF, Júlio-Jr HF, Gomes LC. Inter-annual variations in the abundance of young-of-the-year of migratory fishes in the upper Paraná river floodplain: relations with hydrographic attributes. Braz J Biol . 2009; 69(2):649-60.). This is due to the greatest number of captures occurring in dry periods and because intense and prolonged floods are likely to narrow the niches of these species (Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio-Jr HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná river floodplain. Hydrobiologia . 2008; 607(1):187-98.), causing the underestimation of niche breadth. The stomach contents were analyzed under stereoscopic microscopes using the volumetric method described by Hyslop (1980Hyslop EJ. Stomach contents analysis-a review of methods and their application. J Fish Biol . 1980; 17(4):411-29.) and the contents were identified to the lowest feasible taxonomic level (species, genus, family, or order for fish and usually order for invertebrates). Fish prey was identified according to Graça, Pavanelli (2007Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Maringá: Eduem; 2007.) and Ottoni, Costa (2009Ottoni FP, Costa WJEM. Description of a new species of Laetacara Kullander, 1986 from central Brazil and re-description of Laetacara dorsigera (Heckel, 1840) (Labroidei: Cichlidae: Cichlasomatinae). Vertebr Zool. 2009; 59(1):41-48.), measured, and counted. The contribution of each item to the total stomach contents was evaluated as the percentage of the total number of items in all stomach contents (Baker et al., 2014Baker R, Buckland A, Sheaves M. Fish gut content analysis: robust measures of diet composition. Fish Fish. 2014; 15(1):170-77.). Partially digested unidentified material and arthropod fragments of unknown origin were excluded from the total. To facilitate statistical analyses, the 45 food types found within the stomach contents were grouped into 36 broad categories. Insects were grouped into only one group, and mollusks and frogs were excluded from the analysis, as they occurred only twice and once, respectively.

For each species, differences in diet among the different river systems of the floodplain (Baía, Ivinhema, and Paraná) were tested through a permutational multivariate analysis of variance (PERMANOVA). As no significant differences among the river systems were found for any of the analyzed species, which means that the species present consistent diets regardless of the river system, the subsequent analysis did not consider different river systems. Differences between the diets of each species were obtained using post hoc PERMANOVA pairwise comparisons. The significance level adopted was 0.05; therefore, the probability for pseudo-F is higher than that for observed F. The pseudo-F value indicates the probability of rejecting the null hypothesis by quantifying the size of the difference among the analyzed samples (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E. UK: Plymouth; 2008.). The original matrix (the volume of each item in the stomach of each captured fish) was transformed into a dissimilarity matrix using the Bray-Curtis distance (Bray, Curtis, 1957Bray JR, Curtis JT. An ordination of the upland forest community of southern Wisconsin. Ecol Monogr. 1957; 27(4):325-49.).

Niche breadth was calculated for each species using Levins’ measure (Krebs, 1999Krebs CJ. Ecological methodology. San Francisco: Benjamin Cummings; 1999.), which measures the uniformity of the distribution of items among various food resources. It is given as B = 1/(∑nn= 1 pi 2), where B=niche breadth, pi=the proportion of food item i, and n=number of stomachs. Possible differences in niche breadth (dependent variable) among species (categorical variable) were tested by an analysis of variance (ANOVA) followed by Tukey’s HSD test. Niche overlap among species pairs was quantified using Pianka’s (1973Pianka ER. The structure of lizard communities. Annu Rev Ecol Syst. 1973; 4(1):53-74.) index,

where O represents the overlap between a species pair, and pij and pik represent the proportion of the i th resource used by the species. This index ranges from 1 to 0, where 1 means complete overlap and 0 no overlap. The significance of the observed mean overlap among species was determined by comparisons against a null model of expected niche overlap when resources are randomly consumed. Simulated diets were generated by a randomization in which the diet breadths were maintained, zero values were reshuffled, and all items had the same probability of being consumed (Gotelli, Graves, 1996Gotelli NJ, Graves GR. Null models in ecology. Washington (DC): Smithsonian Institution Press; 1996.).

To determine whether prey size has an influence on species diet rather than taxonomic composition, we performed a feeding selectivity analysis by size range. The data used for the calculations were based on the relative numerical composition of the prey items in the stomach contents of the species and in the environment. For the analysis, the selectivity index E i proposed by Vanderploeg, Scavia (1979Vanderploeg HA, Scavia D. Two electivity indices for feeding with special reference to zooplankton grazing. J Fish Res Board Can. 1979; 36(4):362-65.) was used: Ei = (Wi - n -1) (Wi + n -1)-1, where n is the number of prey types available, and Wi = ripi -1 ∑(ripi -1)-1 ripi -1 ∑(ripi -1)-1, where r i is the percentage of prey item i in the diet of the fish, and p i is the percentage of prey item i in the environment. Ei varies from -1 to 1. Negative values indicate avoidance of the prey, positive values indicate active selection, and null values indicate predation by chance. This index assumes that the gut samples and habitat samples accurately reflect the relative abundance of prey consumed and in the environment, respectively (Kohler, Ney, 1982Kohler CC, Ney JJ. A comparison of methods for quantitative analysis of feeding selection of fishes. Environ Biol Fishes. 1982; 7(4):363-68.), in this case, the prey size classes. Prey sizes not found in the gut contents during the study were omitted from the analysis, as they were deemed inaccessible to the studied species (Cantanhêde et al., 2009Cantanhêde G, Fugi R, Hahn NS. Variation in prey selection of a piscivorous fish after the impoundment of a Neotropical reservoir: prey size and type. J Fish Biol. 2009; 75(1):75-86.). The data of prey in the stomachs of each individual and in the environment were arbitrarily grouped into eleven classes at 20 mm intervals: 10-29, 30-49, 50-69, 70-89, 90-109, 110-129, 130-149, 150-169, 170-189, 190-209, and 210-230. Environmental data were obtained in the same samples described above, in which each sampled fish was identified and counted as described in the sampling methods.

Due to the great divergence in diet and morphological traits among species, especially those that are non-native (H. unitaeniatus and H. mbigua), the results are presented by species and not by status (non-native or native). The selectivity test was conducted only for species that mostly prey on fish due to the lack of information on other organisms. Consequently, it was only conducted for Hoplias species, as the diet of H. unitaeniatus presented a low representation of fish.

The analyses were carried out in R software (R Development Core Team, 2015R Development Core Team. R: a language and environment for statistical computing [Computer software manual - Internet]. Vienna: R Foundation for Statistical Computing; 2015. Available from: https://www.r-project.org/
https://www.r-project.org/...
): null models for species co-occurrence using the package ‘EcoSimR’ (Gotelli, Entsminger, 2010Gotelli N, Entsminger GL. EcoSim: null models software for ecology. Bull Ecol Soc Am. 2010; 81(2):125-27.). PERMANOVA using the package ‘vegan’ (Oksanen et al., 2015Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al. Vegan: community ecology package. R package Version 2.3-0 [Internet]. 2015. Available from: https://cran.r-project.org/web/packages/vegan/
https://cran.r-project.org/web/packages/...
) and Levins’ measure with the package ‘spaa’ (Zhang, 2016Zhang J. spaa: species association analysis. [Internet]. 2016. Available from: https://cran.r-project.org/package=spaa
https://cran.r-project.org/package=spaa...
). The PERMANOVA pairwise comparison was carried out using the statistical software Primer-E + PERMANOVA (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E. UK: Plymouth; 2008.). Pianka’s niche overlap and randomizations were performed in EcoSim 7.71 (Gotelli, Entsminger, 2010Gotelli N, Entsminger GL. EcoSim: null models software for ecology. Bull Ecol Soc Am. 2010; 81(2):125-27.). Graphics were generated in the software Statistica 10 (StatSoft Inc, 2011StatSoft, Inc. STATISTICA:data analysis software system. 2011.).

Results

Morphological analysis. The ordination (PCA; Fig. 1) revealed three significant axes according to the broken-stick criteria (Table 2), but the ANOVA applied to the PCA scores did not present significant values for the second axis (F3,85=1.52, p=0.21), so it was not retained for interpretation. In the first PCA axis, differences between H. unitaeniatus and the Hoplias species were highlighted. Individuals of H. unitaeniatus had more negative scores, being characterized by higher values in the aspect ratio of the caudal, anal, pectoral, and pelvic fins. On the other hand, Hoplias specimens had positive scores, indicating larger areas of the dorsal fin and eyes, less depressed bodies, and more dorsal eyes than H. unitaeniatus. The third PCA axis separated the three species of Hoplias. Specimens of H. mbigua were characterized by larger dorsal and anal fins, a larger caudal peduncle, and a higher ratio for the pectoral fin than the other two species of Hoplias. It was not possible to make a clear distinction between the native species, Hoplias sp. B and H. cf. malabaricus, but both species had longer and deeper heads and more compressed bodies and caudal peduncles than H. mbigua. In general, native species (Hoplias sp. B and H. cf. malabaricus) presented similar morphologies, while non-native species (H. unitaeniatus and H. mbigua) were morphologically distinct from each other and from the native species.

Fig. 1
Distribution of scores of non-native (H. mbigua and H. unitaeniatus) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species on axes 1 and 3 of the principal components analysis (PCA 1 and PCA 3) applied to the correlation matrix (Pearson) formed by 19 ecomorphological indices.

Tab. 2
Pearson’s correlation coefficients (r) obtained among the ecomorphological indices for axes 1 and 3 of the principal components analysis (PCA) applied to the correlation matrix formed by 19 indices describing non-native (H. mbigu a and H. unitaeniatu s) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species. At the lower level, the eigenvalues predicted by the broken-stick model and the proportions of the accumulated and explained variability are described. The indices with higher correlation values (in bold) were selected for interpretation.

Spatial co-occurrence analysis. The species co-occurrence pattern had significant positive values for the entire floodplain (C-score=2982, p<0.001), indicating spatial segregation. The same pattern was observed when considering the Baía (C-score=423.17, p<0.001) and Ivinhema systems (C-score=453.50, p<0.001). However, for the Paraná system, a random pattern was observed (C-score=124, p>0.05). Considering each of the species (Table 3), H. unitaeniatus had the lowest number of total occurrences, although, when found, the overlap with Hoplias species was high. This species was encountered more often in those samples in which Hoplias sp. B was also present. Hoplias mbigua and Hoplias sp. B, which were the most frequent species, had more intense spatial overlap, and both were rarely encountered with H. unitaeniatus. For H. cf. malabaricus, the spatial overlap occurred evenly with H. mbigua and Hoplias sp. B. However, this was the Hoplias species that most spatially overlapped with H. unitaeniatus.

Tab. 3
Co-occurrence in terms of number and proportion (in parentheses) of each pair of Erythrinidae species in the upper Paraná River floodplain. Valid comparisons can be made only between the rows of a single column.

Dietary analysis. Species of Hoplias had diets dominated by fish, with some participation of insects, crustaceans, and plants, while H. unitaeniatus had a diet dominated by aquatic insects (mainly Ephemeroptera), which represented more than 50% of its diet (Table 4). Significant differences in species diets were observed (PERMANOVA: pseudo-F218=1.98, p=0.001), and all species revealed significant differences in diet in the pairwise comparison (Table 5). All three Hoplias species consumed individuals of the same genus (Hoplias spp.). The non-native, H. mbigua consumed mainly Pimelodus spp. A great participation of Hoplosternum littorale and Gymnotus spp. was observed in the diets of the natives Hoplias sp. B and H. cf. malabaricus, respectively (Table 4).

Tab. 4
Diet composition (in volume percentage - %V) of non-native (H. mbigu a and H. unitaeniatu s) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species in the upper Paraná River floodplain. Bold values indicate the food resources with the highest %V for each species. ne=number of empty stomachs (excluded from the analyses). na=number of analyzed stomachs. *Minimum and maximum size of analyzed individuals (mm).

Tab. 5
PERMANOVA (t - pairwise comparison) post hoc test results applied to species diet and Pianka’s niche overlap (O) between non-native (H. mbigu a and H. unitaeniatu s) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species in the upper Paraná River floodplain. *Considered significant.

Differences in niche breadth among species were observed (ANOVA, F3,15=11.82, p<0.001). The non-native H. unitaeniatus presented a narrower niche breadth than Hoplias sp. B (Tukey’s HSD: p=0.02 and p=0.001, respectively), presenting similar niche breadth to that of H. cf. malabaricus (Tukey’s HSD: p=0.99). The non-native H. mbigua presented a niche breadth that was distinct from that of H. cf. malabaricus (Tukey’s HSD: p=0.02); however it had a similar niche breadth to that of Hoplias sp. B (Tukey’s HSD: p=0.37) (Fig. 2). Niche overlap among species was greater than expected under a null model of random consumption of resources (p=0.01). The lowest overlap found was between H. unitaeniatus and H. mbigua, and the greatest overlap was between H. mbigua and Hoplias sp. B (Table 4).

Fig. 2
Mean variation (vertical lines) in diet breadth (boxes) from non-native (H. mbigua and H. unitaeniatus) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species in the upper Paraná River floodplain based on 36 food categories.

The selectivity test showed that the three species of Hoplias positively selected small-sized prey, especially those in the interval between 30 and 49 mm, which was one of the most abundant class ranges available in the environment, and avoided prey larger than 150 mm, despite their abundance. Hoplias cf. malabaricus avoided prey between 10 and 29 mm, the most abundant class range in the environment; this species positively selected prey of 50 to 69 mm (Fig. 3A and 3B). Specimens of Hoplias sp. B presented positive selectivity for prey between 90 and 109 mm, while H. cf. malabaricus negatively selected this interval.

Fig. 3
A- Relative composition of prey species sizes in the diets of non-native (H. mbigua) and native (Hoplias sp. B and H. cf. malabaricus) Erythrinidae species in the upper Paraná River floodplain and relative abundance in the environment during the sampling period in the upper Paraná River floodplain. B - Feeding selectivity (E i) of H. mbigua (non-native), Hoplias sp. B and H. cf. malabaricus (native) for different prey size classes (mm). The non-native H. unitaeniatus is not present due to the low representation of fish in its diet.

Discussion

Comparing with other species of the fish assemblage, the Erythrinidae species presents a similar morphology and ecological aspects due to phylogenetic conservatism (Gross et al., 2013Gross N, Börger L, Duncan RP, Hulme PE. Functional differences between alien and native species: do biotic interactions determine the functional structure of highly invaded grasslands? Funct Ecol. 2013; 27(5):1262-72.). In this sense, non-native species should present adaptations that enable their establishment through niche segregation and/or environmental filtering, as they would have to survive under different abiotic conditions and interspecific interactions. Analyzing at a fine scale, the native and non-native species could be discriminated to a certain level based on morphological traits. This was observed in the native species (Hoplias sp. B and H. cf. malabaricus), as they presented similar morphologies, highlighted by the overlapping scores observed in the PCA, while the two non-native species (H. unitaeniatus and H. mbigua) presented morphologies that were distinct from each other and from the native species. Considering H. unitaeniatus, the morphological differences might lead to niche differentiation, and they should be more important for the coexistence of natives and this introduced species than environmental filtering, especially when considering that all native species presented significant differences in spatial distribution patterns and in their diets compared with such species. The segregation pattern observed allows for the occupation of different microhabitats among these species. This suggests that, at different levels, the species do not occupy the same microhabitat, a fact that would decrease any potential competition that could exclude any of them. The only exception was in the Paraná system, but this could be attributed to the fact that this is the system with the lowest abundances of fish (Fernandes et al., 2009Fernandes R, Agostinho AA, Ferreira EA, Pavanelli CS, Suzuki HI, Lima DP, Gomes LC. 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.), decreasing any potential competition even further.

Considering diets, the non-native H. unitaeniatus presented a narrow niche breadth, with a diet dominated by insects (mainly Ephemeroptera) and small contributions of fish, and showed extremely low values of diet overlap with the native species. The low participation of fish in the diet of this species, allowing it to be classified as insectivorous, goes against previous observations of this species that classified it as a piscivore in the same studied area (Hahn et al., 2002Hahn NS, Fugi R, Peretti D, Russo MR, Loureiro-Crippa VE. Estrutura trófica da ictiofauna da planície de inundação do alto rio Paraná. In: Núcleo de Pesquisas em Limnologia, Ictiologia e Aqüicultura (NUPÉLIA). A planície de inundação do alto rio Paraná. Relatório Anual 2002 [Internet]. 2002 [updated 2003 Aug 18]. Available from: Available from: http://www.peld.uem.br/Relat2002/pdf/comp_biotico_estruturaTrofica.pdf
http://www.peld.uem.br/Relat2002/pdf/com...
). The low niche overlap is one of the mechanisms facilitating coexistence among this non-native species and the native Erythrinidae, as it suggests reduced competition if spatial and feeding resources were limited. Increased ecological interactions with native species could lead to such temporal differences; however, any explanations on this subject would be based on speculation, and further studies are needed to draw more consistent conclusions. Nevertheless, the low captures of H. unitaeniatus must be noted, as this was the species with the lowest number of captures during the study period (326 individuals).

The non-native species H. mbigua was distinguished from the native species by the width and height of the head. The higher values presented by the native species are an indication that they are able to ingest larger prey than the non-native H. mbigua. Still, the native species presented a greater dorsal area and lower eyes than the non-native H. mbigua, implying that the native species occupy more benthic positions in the water column. The differences in the diets of the native species (Hoplias sp. B and H. cf. malabaricus) compared to the non-native H. mbigua can be explained spatially. Despite their segregated occurrences, when occurring in the same microhabitat, differences in ecomorphological attributes suggest different foraging locations. The fact that the native species have similar morphologies but different diets suggests that dietary differences between these species are caused by other factors besides morphology. The preference for smaller prey might be associated with gape size, prey handling time, risk of predation, and energy gain (Nilsson, Bronmark, 2000Nilsson PA, Brönmark C. Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos . 2000; 88(3):539-46.). Moreover, larger prey species possess greater escape capacities and are more difficult to handle than smaller prey (Baras et al., 2010Baras E, Hafsaridewi R, Slembrouck J et al. Why is cannibalism so rare among cultured larvae and juveniles of Pangasius djambal? Morphological, behavioural and energetic answers. Aquaculture. 2010; 305(1-4):42-51.). This distinction in prey size preference among these species may occur to reduce potential competition caused mainly, but not exclusively, by morphological similarities.

Even with differences in diet composition with the native species, the non-native H. mbigua, presented higher values of diet overlap with the native species. This degree of overlap might be related to the opportunistic behavior of these species, given their capacity to change their diet composition according to prey availability or due to biotic interactions, such as competition and predation (Pompeu, Godinho, 2001Pompeu PS, Godinho AL. Mudança na dieta da traíra Hoplias malabaricus (Bloch) (Erythrinidae, Characiformes) em lagoas da bacia do rio Doce devido à introdução de peixes piscívoros. Rev Bras Zool. 2001; 18(4):1219-25.; Carvalho et al., 2002Carvalho LN, Fernandes CHV, Moreira VSS. Alimentação de Hoplias malabaricus (Bloch, 1794) (Osteichthyes, Erythrinidae) no rio Vermelho, Pantanal Sul Mato-Grossense. Rev Bras Zoociências. 2002; 4(2):227-36.). In fact, H. mbigua, as other species of Hoplias, presented high feeding plasticity, defined by a varied diet composed of crustaceans, insects, and plants, in addition to a frog (Trachycephalus typhonius -Strictar-Pereira, Oda, 2012Strictar-Pereira L, Oda FH. Trachycephalus typhonius (amazon milk frog): predation. Herpetol Bull. 2012; 122:38-39.). Additionally, H. mbigua was morphologically distinct in terms of attributes related to swimming and feeding, such as having a larger area of the dorsal fin, which allows this species to achieve higher speeds and perform more stable movements (Gosline, 1971Gosline WA. Functional morphology and classification of teleostean fishes. Honolulu: University Press of Hawaii; 1971.) than the native species (Hoplias sp. B and H. cf. malabaricus). This fact is reflected in its diet, as this was the only species to consume individuals of Serrasalmus marginatus and Acestrorhynchus lacustris, species that present high swimming capacity (Breda et al., 2005Breda L, Oliveira EF, Goulart E. Ecomorfologia de locomoção de peixes com enfoque para espécies neotropicais. Acta Sci Biol Sci . 2005; 27(4):371-81.; Teixeira, Bennemann, 2007Teixeira I, Bennemann ST. Ecomorfologia refletindo a dieta dos peixes em um reservatório no sul do Brasil. Biota Neotrop. 2007; 7(2):67-76.), considering that both species are predators that capture their prey through active swimming. Hoplias species are sedentary, territorial, and solitary predators, inhabiting macrophyte-covered areas and using ambush feeding strategies (Almeida et al., 1997Almeida VLL, Hahn NS, Vazzoler AEAM. Feeding patterns in five predatory fishes of the high Parana river floodplain (PR, Brazil). Ecol Freshw Fish. 1997; 6(3):123-33.; Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio-Jr HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná river floodplain. Hydrobiologia . 2008; 607(1):187-98.; Petry et al., 2010Petry AC, Gomes LC, Piana PA, Agostinho AA. The role of the predatory trahira (Pisces: Erythrinidae) in structuring fish assemblages in lakes of a Neotropical floodplain. Hydrobiologia . 2010; 651(1):115-26.). The great participation of congeneric species (Hoplias spp.) in the H. mbigua diet may be related to this high degree of territorialism; this species presented a large overlap with the native species, and the consumption of congeneric species is noted as a possible mechanism that could facilitate its establishment in the floodplain (Strictar-Pereira et al., 2015Strictar-Pereira L, Agostinho AA, Gomes LC. Eating the competitor: a mechanism of invasion. Hydrobiologia . 2015; 746(1):223-31.). In addition to the tendency for competition, due to their morphological similarities, the two species possess similar abundances in the floodplain, with the presence of the non-native species not eliminating or even reducing the abundance of the native species (Hauser, Benedito, 2012Hauser M, Benedito E. Species of the Hoplias aff. malabaricus complex (Characiformes: Erythrinidae): an investigation of coexistence in a Neotropical floodplain. Zoologia (Curitiba). 2012; 29(1):59-69.).

Considering only the limiting similarity theory and the environmental filtering hypothesis, it can be concluded that different mechanisms act in mediating the coexistence of native and non-native Erythrinidae species. For non-native H. unitaeniatus, which presented an extremely different diet and morphology from the native species, niche partitioning (limiting similarity) seems to be the major mechanism mediating species coexistence. On the other hand, for the non-native H. mbigua, which presented similar morphology to that of the native species, environmental filtering seems to be mediating the coexistence among species. These observations emphasize that different mechanisms can be acting in allowing species establishment, persistence and interactions with native species, even for closely related species and similar periods of introduction. This highlights that species introductions are unpredictable, as several simultaneous factors can be acting in mediating species establishment and interactions with other species.

Acknowledgments

The authors thank two anonymous reviewers who greatly improved the manuscript quality, all members of the Fish Collection of Nupélia for fish identification, and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) for financial support.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    11 May 2016
  • Accepted
    03 May 2017
Sociedade Brasileira de Ictiologia Universidade Estadual de Maringá, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura/Coleção Ictiologia, Av. Colombo, 5790, 87020-900 Maringá, PR, Brasil, Tel.: (55 44)3011 4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br