Diet and trophic guilds of fish assemblages in two streams with different anthropic impacts in the northwest of Paraná, Brazil - PDF

doi: /S Diet and trophic guilds of fish assemblages in two streams with different anthropic impacts in the northwest of Paraná, Brazil Karine Orlandi Bonato 1, Rosilene Luciana

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doi: /S Diet and trophic guilds of fish assemblages in two streams with different anthropic impacts in the northwest of Paraná, Brazil Karine Orlandi Bonato 1, Rosilene Luciana Delariva 2 & Jislaine Cristina da Silva 3 1 Programa de Pós-Graduação em Ciências Biológicas Zoologia, Departamento de Zoologia, Universidade Federal do Paraná. Caixa Postal 19020, Curitiba, PR, Brazil. 2 Corresponding author. Centro de Ciências Biológicas e da Saúde, Universidade Estadual do Oeste do Paraná. Rua Universitária 2069, Caixa postal 711, Cascavel, PR, Brazil. 3 Programa de Pós-Graduação em Conservação e Manejo de Recursos Naturais, Centro de Ciências Biológicas e da Saúde, Universidade Estadual do Oeste do Paraná. Rua Universitária 2069, Caixa postal 711, Cascavel, PR, Brazil. ABSTRACT. In the present study, we describe the diets of the fish assemblages in two streams in the Maringá region of Paraná that are under the influence of different anthropic impacts. We also evaluate how the origin and use of food resources varies temporally and spatially and how the trophic organization of the fish assemblages differs between the two streams. Fish were collected every two months from October 2006 to October 2007 using sieves, seining and closing nets along two 50 m stretches of each stream. We used the volumetric method to analyze the stomach contents of 599 fish belonging to 15 species. We then employed ANOSIM, SIMPER, NMDS and cluster analyses (using the Bray- Curtis index) to examine how different factors (species, stream, sampling site and season) influenced the diets of the assemblages. The dietary analysis revealed a total of 21 types of items consumed, with the most common being detritus and immature Diptera. Spatial factors resulted in differences in diets between the two streams, with detritus representing the material consumed most often in the Morangueiro stream and immature Diptera being the most consumed item in the Queçaba stream. SIMPER analysis indicated a 76.33% dissimilarity between species diets during the dry and rainy seasons, with detritus, immature Diptera and testate amoebae making the greatest contributions to this differentiation. In the Morangueiro stream, three trophic guilds were found: detritivorous, detritivorous/aquatic insectivorous, and aquatic insectivorous. In Queçaba stream, six trophic guilds were present: detritivorous, benthophagous, aquatic insectivorous, terrestrial insectivorous, herbivorous and carnivorous. Autochthonous items were generally the items most consumed by species, in particularly in the Queçaba stream. In the Morangueiro stream, food items of indeterminate origin were more relevant. The differences in the diets of fish species between the two streams support the conclusion that urbanization causes the disruption of aquatic environments and trophic organization. KEY WORDS. Food resources; seasonality; spatial variation; urbanization. Research on tropical streams has intensified in recent years, particularly in southern and southeastern Brazil, highlighting several ecological aspects of these important ecosystems (CASATTI et al. 2006a, LANGEANI et al. 2007, VALÉRIO et al. 2007, GOMIERO & BRAGA 2008, FELIPE & SUAREZ 2010). Tropical streams constitute extensive water networks, though individual streams are small in size, and these waterways, exhibit a peculiar fauna that is very sensitive to the increasing degradation of the habitat (OLIVEIRA & BENNEMANN 2005, CUNICO et al. 2011). VITOUSEK et al. (1997, 2008) reported that more than half of existing freshwater is used by human populations, and approximately half of all terrestrial landscapes have been altered by human activities, resulting in a great loss of biodiversity. In recent years, the rapid radial expansion of urban centers over tropical streams, coupled with the heavy consumption of their resources and the subsequent disposal of materials in them, has contributed to their degradation. In particular, this has led to a reduction in the complexity of different habitats that make up aquatic ecosystems and landscapes (HELMS & FEMINELLA 2005, MCKINNEY 2006, CASATTI et al. 2009, DI GIULIO et al. 2009). Studies performed by CUNICO et al. (2006, 2011) showed that urbanization leads to changes in the diversity and species composition of tropical stream fish assemblages due to the loss of forested areas, reductions in water quality because of domestic and industrial sewage, and alterations of water flow and available substrates. Changes in water quality or habitat conditions usually result in differences in the availability of food resources. Fish generally display high trophic plasticity (ABELHA et al. 2001) and temporal and spatial variations in their diets (ZEUG & WINEMILLER 2008, DEKAR et al. 2009). However, in impacted environments, these patterns can be altered, and changes, such 2012 Sociedade Brasileira de Zoologia All rights reserved. 28 K. O. Bonato et al. as increases in generalist species and reduced numbers of trophic guilds, can occur (CASATTI et al. 2009, ALEXANDRE et al. 2010, ESTEVES & ALEXANDRE 2011). Evaluation of the feeding habits of fish in streams under the influence of different human impacts represents a key tool for assessing the biotic integrity of these streams and managing such environments. It also provides a consistent approach for understanding interactive processes within aquatic communities. Variations in the trophic organization of assemblages can be considered to be indicators of changes in the quality and complexity of a habitat (KARR 1981, JARAMILLO & CARAMASCHI 2008). In this context, a number of studies have been undertaken to examine the urban streams in the state of Paraná. However, these studies have mainly focused on the influence of urbanization on the species composition and richness of fish assemblages (CUNICO et al. 2006, VIEIRA & SHIBATTA 2007, CUNICO et al. 2009, GUBIANI et al. 2010, CUNICO et al. 2011). Only OLIVEIRA & BENNEMANN (2005) have evaluated the diet of sampled species in the Londrina Municipality region. Therefore, we aimed to describe the diet of the fish assemblages in two streams under the influence of different anthropic impacts in the region of Maringá, Paraná to evaluate how the origin and use of food resources varied temporally and spatially in these assemblages and whether the trophic organization of assemblages differed between the two streams. MATERIAL AND METHODS We studied two third order streams, Morangueiro and Queçaba, which are indirect and direct tributaries, respectively, of the Pirapó River. This river is a source of public water supplies for Maringá and is located in the northern region of the state of Paraná. It rises in the municipality of Apucarana and runs for a length of 168 km until reaching its mouth at the Paranapanema River. Morangueiro stream rises and runs for approximately 40% of its course through the urban perimeter of Maringá, with the remainder of the stream running through agricultural areas. Queçaba stream runs through agricultural areas, small recreation centers, and fish farms. Four sampling sites were established: two in each stream, with one at the headwater and another near the mouth (Fig. 1). Qualitative characteristics of the sampling sites are described in Table I. Fish were sampled every two months from October 2006 to October 2007 at each of the four sampling sites using sieves (65 cm in diameter, 3 mm mesh size) and seining and closing nets (0.5 cm between opposite nodes). The sieves were used at the margins and on the substrate of the river beds, with sampling being performed for an initial period of 15 minutes and, after an interval of 20 minutes, for another five minutes to catch additional specimens, representing a total collection effort of 20 minutes. A seining net installed at the downstream end of the sampled stretch was hauled upstream of the 50 m length of the stream delimited at each site. After being captured, fish were anesthetized with benzocaine (250 mg/l) and fixed in a 10% formalin solution. In the laboratory, specimens were separated and identified according to GRAÇA & PAVANELLI (2007) and preserved in 70% alcohol. Each collected specimen was weighed on an analytical scale, measured for standard and total lengths in cm, and then eviscerated. For the analysis of stomach contents, we used only species for with n 5. Using optical and stereoscopic microscopes, food items were identified to the lowest possible taxonomic level using the identification keys provided by BICUDO & BICUDO (1970) for algae and MUGNAI et al. (2010) for invertebrates. The items were quantified using graduated test tubes and a glass counting plate (HELLAWELL & ABEL 1971) according to the volumetric method, Table I. Physical characteristics of the sampling sites sampled in the the Morangueiro (sites 1 and 2) and Queçaba (sites 3 and 4) streams, Pirapó River Basin, Maringá, Paraná State. Sites Coordinates ,5 S, ,5 W ,41 S, ,25 W ,41 S, ,19 W ,6 S, ,8 W Width (m) Depth (m) Predominant substrate Riparian vegetation Observations Rocky Approximately 5 m of arboreal vegetation; shrubby, with exotic and fruit trees Sandy stretches with pebbles Few stretches with pebbles, mostly muddy Rocky, pebbles, sandy and muddy Arboreal vegetation at left margin and grasses and shrubs at right margin Arboreal vegetation for approximately 30 m Arboreal and shrubby vegetation for approximately 20 m Erosion at the margins Located in an urban area Solid waste at the margins and in the river Some pools reach a 1 m depth Preserved area on the right margin, surrounding of the left margin with cultivars Surrounded with pasture and cultivars Pools up to 0.5 m Surrounding with pasture and cultivars Pools up to 0.6 m Diet and trophic guilds of fish assemblages in two streams with different anthropic impacts 29 Figure 1. Sampling sites for the Queçaba and Morangueiro streams in the state of Paraná, Brazil. where the total volume of a food item consumed by a population is given as a percentage of the total volume of all stomach contents (HYSLOP 1980). Items with a low volumetric representation were categorized as other aquatic invertebrates (Acarina, Cladocera, Copepoda, Rotifera, Gastropoda, and Oligochaeta), algae (diatoms and filamentous) or detritus (including all types of organic and inorganic material from the bottom). To examine the influence of urbanization on fish diets, we focused on four factors: species, stream (Morangueiro and Queçaba), site (sites 1, 2, 3 and 4), and season (either rainy Oct-Dec 2006, Feb-Oct 2007) or dry (Apr/Jun/Aug 2007), es- 30 K. O. Bonato et al. tablished based on rainfall data obtained from the Climatological Station of the Universidade Estadual de Maringá. To analyze how the diet of the fish was related to these factors, we used the statistical package PRIMER-E v. 6.0 (CLARKE & GORLEY 2001). Similarity matrices between samples were constructed using the Bray-Curtis index (LEGENDRE & LEGENDRE 1998), and data were standardized (as a percentage) to minimize the discrepancy between samples. After obtaining these matrices, we performed a one-way analysis of similarity (ANOSIM) to evaluate which of the factors significantly influenced which food items were consumed (global R 0 and p 0.05). A posteriori, we performed a cluster ordination (dendrogram) using the UPGMA method with complete linkage to detect whether the samples were grouped according to the different factors (LEGENDRE & LEGENDRE 1998, CLARKE & GORLEY 2001). We then performed non-metric multidimensional scaling (NMDS) to examine the dispersion of the samples on a multidimensional scale (represented by a twodimensional graph) indicating the badness-of-fit, or stress, of its representation. Finally, we used discriminant (similarity percentage) analysis to demonstrate the dissimilarities between the groupings and the contribution of different food items (LEGENDRE & LEGENDRE 1998, CLARKE & GORLEY 2001). To determine trophic guilds for the species analyzed from each stream, we used the data collected regarding food item volumes to generate a similarity matrix using PRIMER-E v. 6.0 software. We then performed a cluster analysis using the Bray- Curtis index. For classification into guilds, we only used groupings of species with a similarity greater than 55%. To examine the origin of the food items, they were classified as autochthonous, allochthonous or indeterminate. We only used the factors species, stream, site and season, and we followed the same methodology as described earlier using PRIMER software, but with overlapping clusters (circles) delimiting groups. ated use of food resources between species with a stress of 0.14 (Fig. 2). This was also supported by SIMPER analysis. Based on these results, we were able to determine which items contributed most to the formation of the following groups (i.e., to the similarity within species): Astyanax bockmanni Vari & Castro, 2007 (Characidae), Bryconamericus stramineus Eigenmann, 1908 (Characidae), Characidium aff. zebra Eigenmann, 1909 (Crenuchidae), Imparfinis mirini Haseman, 1911 (Heptapteridae), Pimelodella gracilis (Valenciennes, 1835) (Heptapteridae), Rhamdia quelen (Quoy & Gaimard, 1824) (Heptapteridae) and Rineloricaria sp. (Loricariidae) consumed immature Diptera ( 60%); Gymnotus inaequelabiatus (Valenciennes, 1839) (Gymnotidae) consumed Ephemeroptera (56.1%) and immature Diptera (39.8%); Astyanax altiparanae Garutti & Britski, 2000 (Characidae) consumed Coleoptera (45.6%) and Hymenoptera (40.8%); Piabina argentea Reinhardt, 1867 (Characidae) consumed immature Diptera (37.9%) and vegetal fragments (31.1%); Astyanax aff. paranae Eigenmann, 1914 (Characidae) consumed vegetal fragments (55.8%) and immature Diptera (30.1%); Corydoras aeneus (Gill, 1858) consumed testate amoebae (50.3%) and detritus (27.8%); and Hypostomus ancistroides (Ihering, 1905) (Loricariidae), Hypostomus cf. strigaticeps (Regan, 1908) (Loricariidae), and Poecilia reticulata Peters, 1859 (Poecilidae) consumed detritus ( 75%). RESULTS Diet analysis and spatial and temporal variation We collected 1,393 individuals belonging to 23 species. Among these fish, the diets of 15 species were described based on analysis of the stomach contents of 599 individuals (Tab. II). The species consumed 21 types of food items. Of these items, 12 were categorized as autochthonous, eight as allochthonous, and one was considered indeterminate (Tab. III). The most consumed types of items were immature Diptera (28% of the total resources consumed), which were consumed by all species, and detritus (20% of the total resources consumed), which was consumed by 93% of the species. The other items, consumed in lower proportions, were Ephemeroptera (8%), vegetal fragments (7%) and fragments of terrestrial insects (6%). ANOSIM demonstrated the influence of the factor species (Global R = 0.377, p = 0.001). In the NMDS analysis, we observed the formation of groupings based on the differenti- Figure 2. Two-dimensional plot of the fifteen species analyzed showing the ordination resulting from the NMDS. ABO = Astyanax bockmanni; AAL = Astyanax altiparanae; APA = Astyanax aff. paranae; BST = Bryconamericus stramineus; CAE = Corydoras aeneus; CZE = Characidium aff. zebra; GIN = Gymnotus inaequilabiatus; HAN = Hypostomus ancistroides; HST = Hypostomus cf. strigaticeps; IMI = Imparfinis mirini; PAR = Piabina argentea; PGR = Pimelodella gracilis; PRE = Poecilia reticulata; RIN = Rineloricaria sp.; RQU = Rhamdia quelen. The factors stream (Global R = 0.09, p = 0.001) and site (Global R = 0.106, p = 0.001) were significant in the differentiation of diet between species. For the Morangueiro and Queçaba streams, the most consumed items were detritus (68.0%) and immature Diptera (39.6%), respectively. At site 4, Diet and trophic guilds of fish assemblages in two streams with different anthropic impacts 31 Table II. Taxonomic position and number of stomachs analyzed for the fish species from the sampled streams. The list of species recorded and their taxonomic positions are consistent with REIS et al. (2003) and GRAÇA & PAVANELLI (2007). Species Species code Voucher specimens N analyzed stomachs Characiformes Characidae Astyanax altiparanae Garutti & Britski, 2000 AAL 5290, Astyanax bockmanni Vari & Castro, 2007 ABO Astyanax aff. paranae Eigenmann, 1914 APA Bryconamericus stramineus Eigenmann, 1908 BST Piabina argentea Reinhardt, 1867 PAR 5291, Crenuchidae Characidium aff. zebra Eigenmann, 1909 CZE Cyprinodontiformes Poecilidae Poecilia reticulata Peters, 1859 PRE Gymnotiformes Gymnotidae Gymnotus inaequilabiatus (Valenciennes, 1839) GIN Siluriformes Callichthyidae Corydoras aeneus (Gill, 1858) CAE 5293, Heptapteridae Imparfinis mirini Haseman, 1911 IMI Pimelodella gracilis (Valenciennes, 1835) PGR Rhamdia quelen (Quoy & Gaimard, 1824) RQU Loricariidae Hypostomus ancistroides (Ihering, 1905) HAN ND 66 Hypostomus cf. strigaticeps (Regan, 1908) HST Rineloricaria sp. RIN 5299, Total Number 599 there was a predominance of immature Diptera (43.4%) and a more contribution from other resources, such as vegetal fragments (9.3%), Ephemeroptera (8.1%) and Hymenoptera (6.9%). At the sites 1, 2 and 3 detritus was the most consumed item based on results obtained from the SIMPER analysis. This analysis also showed that for the factor season (Global R = 0.027, p = 0.001), there was a dissimilarity of 76.3% between the dry and rainy seasons. In the dry season, the predominant food item category for all species was detritus (73%), while in the rainy season, the most consumed items were immature Diptera (49%). Trophic classification Based on the volume of consumed items in each stream, the species were grouped into trophic guilds, with the grouping analysis corroborating our conclusion that the species within the assemblages formed distinct groups (Figs 3 and 4). For the Morangueiro stream, three trophic guilds were established: detritivorous/aquatic insectivorous, comprised of P. reticulata and C. aeneus, both of which consumed detritus along with aquatic insects; detritivorous, including only H. ancistroides, which predominantly consumed detritus; and aquatic insectivorous, consisting of the majority (10 out of 15) of species studied (B. stramineus, A. bockmanni, P. gracilis, I. mirini, C. aff. zebra, Rineloricaria sp., R. quelen, P. argentea, A. aff. paranae and A. altiparanae), all of which consumed a higher proportion of aquatic insects. In the Queçaba stream, six trophic guilds were formed: aquatic insectivorous, comprised of seven of the 15 species studied (P. gracilis, B. stramineus, P. argentea, G. inaequelabiatus, C. aff. zebra, I. mirini and A. bockmanni), which mainly consumed aquatic insects; carnivorous, including only R. quelen, which consumed both fish and aquatic insects; herbivorous, consisting of A. aff. paranae, for which the diet was based on vegetal 32 K. O. Bonato et al. 3 4 Figures 3-4. Similarity dendrogram based on the diet composition of the fifteen species of fish analyzed in (3) Morangueiro and (4) Queçaba streams, PR, Brazil. Table III. Food items consumed by the studied species and the origin of the food items. Values are based on data indicating the volume percentage of the item consumed. Asterisk indicates values less than 0.1%. The most significant values for each species are shown in bold. Food items AAL ABO APA BST CZE CAE GIN HAN HST IMI PAR PGR PRE RQU RIN Autochthonous Algae * * 2.1 * 0.3 Testate amoebae * 51.6 * * Conchostraca * 0.6 * 6.0 * * 0.8 * * Immature Coleoptera * Immature Diptera Ephemeroptera Immature Lepidoptera * Odonata nymph Trichoptera * Aquatic insects fragments Other aquatic invertebrates * Fish * * Allochthonous Vegetal fragments Arachinida Coleoptera Adult Diptera Hemiptera Hymenoptera * Orthoptera Terrestrial insects fragments Indeterminate Detritus * Diet and trophic guilds of fish assemblages in two streams wit
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