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Diet of the Rufous Frog Leptodactylus fuscus (Anura, Leptodactylidae) from two contrasting environments
expand article infoDiego José Santana, Vanessa Gonçalves Ferreira, Gabriel Nassif Crestani, Matheus Oliveira Neves
‡ Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil
Open Access

Abstract

The impact of urbanization on amphibians has received some attention in the conservation literature. Despite the various impacts on animal life, some species can persist along the cities structures by adjusting their natural histories. Leptodactylus fuscus is a common anuran species occurring in South America, which can commonly be found in urban environments. Herein, we compare the diet of L. fuscus between an urban and a wild environment. We collected 57 individuals of L. fuscus and analysed their diet, which differed significantly between the two sites. In the urban environment, Coleoptera were the prevalent prey items, whereas specimens from the wild site had a more diverse diet.

Key Words

anthropic changes, anthropization, Cerrado, resources, trophic ecology

Introduction

Urbanization processes lead to several changes in biological communities (Cushman 2006; Hunter 2007; McDonald et al. 2011). The impact of urbanization on amphibians has received some attention in conservation literature, particularly at broad spatial scales (Riley et al. 2005; MacGregor-Fors et al. 2013; Nicholls et al. 2017; Montezol et al. 2018). However, the few studies that have evaluated amphibians’ natural history in urban environments are local or were conducted in temperate regions (e.g. da Rosa et al. 2002; Vallan 2002; Mitchell et al. 2008). In urbanized areas, alterations to the timing and volume of water inputs (Riley et al. 2005; McDonald et al. 2011) can significantly impact amphibian populations (Barret et al. 2010). In addition, some species are capable of persisting in urban environments by adjusting certain natural history behaviors (Mitchell et al. 2008).

The majority of anurans are considered generalist predators and feed mostly on invertebrates (Rodrigues et al. 2004; López et al. 2009; Solé et al. 2009). Anuran diets are primarily influenced by predation risk, body size and condition, and prey availability (Duellman and Trueb 1986). Further, diet composition is directly influenced by habitat and seasonality (da Rosa et al. 2002). In spite of anuran colonization success along edifications (Simon et al. 2009; Threlfall et al. 2012; Scheffers and Paszkowski 2013), the urban environments have lower prey availability (Hunter 2007) as a result of lower overall biomass, abundance, or diversity (Coleman and Barclay 2013; Jaganmohan et al. 2013).

The Rufous Frog Leptodactylus fuscus (Schneider, 1799) is a common species occurring in savannas from Panama throughout South America, east of the Andes, south to southern Brazil, Bolivia, Paraguay, and northern Argentina (de Sá et al. 2014). It has nocturnal habits and lives on marshy areas all year round, and the reproduction occurs in the rainy season (Heyer et al. 1990). Previous studies have examined the diet of adults L. fuscus in Cerrado areas and found them to be generalist predators (Carvalho et al. 2008; Sugai et al. 2012; Junqueira et al. 2016). In the present work, we study the diet (frequency, volume and importance of preys) of L. fuscus between a wild and an urban site.

Material and Methods

Study area

We collected data from contrasting sites in the municipality of Campo Grande, state of Mato Grosso do Sul, Brazil (Fig. 1). The first site is a permanent pond, inserted in a savanna landscape, categorized here as a wild site (WS), located in the surroundings of the Particular Reserve of the Natural Patrimony (RPPN) Brejo Bonito (20°32'13"S, 54°45'04"W; 506 m a.s.l.). The second site (16 km west) is a temporary pond in an abandoned ground among paved streets (20°29'49"S, 54°36'24"W; 550 m a.s.l.) in the southeast area of the city of Campo Grande, categorized here as an urban site (US). Some citizens usually throw garbage and other polluted material at this site. The original vegetation that covered all the municipality territory is characterized by Cerrado phytophysiognomies. The climate in the region is classified as equatorial with two well defined seasons, a dry winter (April to August) and a wet summer (September to March). Köppen-Geiger climate classification is Aw (Kottek et al. 2006). The average annual temperature and precipitation are 22.8 °C and 1,533 mm, respectively (INMET 2005).

Figure 1. 

Map showing the sampled areas along the municipality of Campo Grande, state of Mato Grosso do Sul, Brazil.

Data collection

We collected adult L. fuscus through nocturnal active searches by “Visual Encounter Surveys” (Crump and Scott 1994), between 19:00h and 22:00h from November 2016 to February 2017, totalizing nine hours for each site. The animals were killed with a 2% lidocaine overdose, fixed in 10% formalin, and conserved in a 70% alcohol solution. The specimens are housed in the Coleção Zoológica da Universidade Federal de Mato Grosso do Sul. We determined the sex of each individual by the presence of vocal sacs and vocal slits in males and their absence in females.

To evaluate the diet, we removed the stomachs of each specimen through a small abdominal incision and extracted their contents. We identified each prey item with a stereoscope microscope to the order level and measured the length and width of the prey with a Mitutoyo digital calliper (0.01 mm precision). Prey items in advanced stages of digestion were considered as unidentifiable.

Statistical analysis

For the diet analysis, we first identified prey to the lowest possible taxonomic level (usually order). The volume of each prey item was then calculated using an ellipsoid formula: (Griffiths and Mylotte 1987), where L = prey length and W = prey width. To determine the importance of each prey category, we calculated the relative importance index IRI = F%(N% + V%), by using the mean of the percentage of occurrence (F%), the numerical percentage (N%), and the volumetric percentage (V%), according to Pinkas (1971). For the analysis, we removed all unidentifiable items and scorpiones due to partial recovery and the inability to accurately estimate volume.

We performed a PERMANOVA analysis to test if diet composition varies between the two site types, with euclidian distance, using the prey volume, and then we executed a Principal Component Analysis (PCA) to check which prey category most contributed for the differentiation. All statistical analyses were conducted in the R software v.3.4.2 (R Core Team 2017) using the vegan package (Oksanen et al. 2015).

Results

We collected 57 individuals of Leptodactylus fuscus, 31 in the urban site (27 males and four females), and 26 in the wild site (12 males and 14 females). Among the analyzed stomachs (n = 57), only two were empty. We found 236 preys belonging to 16 categories as follow by alphabetical order: Araneae, Blattaria, Chilopoda, Coleoptera, Dermaptera, Diptera, Hymenoptera, Hemiptera, Isopoda, Isoptera, Lepidoptera, Orthoptera, Plant Material, Pulmonata, Scorpiones and unidentifiable (Table 1).

Diet composition differs between the wild and urban site types (F=7.77; df=53; P<0.001; Fig. 2). Individuals from WS consumed a larger diversity of prey types (Table 1; Fig. 3) than those from the US. Individuals from US primarily consumed coleopterans (IRI=1531.1; 70.26%) in contrast to a more diversified diet from WS individuals, composed of Lepidoptera (IRI=416.34; 34.48%), Hymenoptera (IRI=310.14; 25.68%), Diptera (IRI=48.87; 4.05%) and Coleoptera (IRI=46.91; 3.88%). The orders Isopoda, Araneae, Chilopoda and Pulmonata were recorded only in the urban population, whereas Scorpiones and Isoptera were found only in the wild population.

Figure 2. 

Principal components analysis to evaluate the differences in the diet of Leptodactylus fuscus sample in the urban and wild sites in the municipality of Campo Grande, state of Mato Grosso do Sul, Brazil. Black dots indicate individuals from the urban site, and red dots indicate individuals from the wild site. Arrows indicate the contribution in the ordination of each prey item.

Comparison of the diet of Leptodactylus fuscus between urban and wild sites in the municipality of Campo Grande, state of Mato Grosso do Sul, Brazil. V = volume, N = number, F = frequency, IRI = important relative index.

Urban environment Wild environment
Prey category V% N% F% IRI V% N% F% IRI
Araneae 0.87 4.65 5.43 30 - - - -
Blattaria 0.17 0.58 1.09 0.81 2.93 1.56 2.44 10.96
Chilopoda - 0.58 1.09 0.63 - - - -
Coleoptera 26.36 34.88 25.00 1531.11 1.72 4.69 7.32 46.91
Dermaptera 4.67 4.65 6.52 60.78 2.32 3.13 4.88 26.54
Diptera 0.27 1.16 1.09 1.56 0.64 9.38 4.88 48.87
Hemiptera 1.18 6.98 9.78 79.76 0.89 3.13 2.44 9.79
Hymenoptera 11.31 21.51 10.87 356.73 0.43 25.00 12.2 310.14
Isopoda 1.36 4.07 2.17 11.8 - - - -
Isoptera - - - - 0.47 3.13 2.44 8.78
Lepidoptera 4.66 2.33 3.26 22.79 27.05 15.63 9.76 416.34
Not Identified 40.21 11.05 20.65 1058.5 46.3 20.31 34.15 2274.62
Orthoptera 1.18 2.33 4.35 15.23 0.28 1.56 2.44 4.5
Pulmonata 4.16 0.58 1.09 5.16 - - - -
Scorpiones - - - - - 4.69 4.88 22.87
Vegetal 3.62 4.65 7.61 62.9 16.95 7.81 12.2 301.94
Figure 3. 

Diet of Leptodactylus fuscus in the urban and wild sites in the municipality of Campo Grande, state of Mato Grosso do Sul, Brazil. Bars represent Index of Relative Importance (IRI) (Pinkas 1971). Note the distinctness of the items consumed and their importance to the diet of studied species.

Discussion

In this study, we report differences in the diet composition of L. fuscus between urban and wild sites. Differences between urban and wild environments have been reported for other vertebrates such as birds (Zalewski 1994; Grzedzicka et al. 2013; Chenchouni 2016), snakes (Capizzi et al. 2008), lizards (Balakrishna et al. 2016), and salamanders (Barrett et al. 2012). For anurans, a recent study that evaluated the trophic ecology of anuran assemblages in northeast Argentina found out significant differences in the diet composition of all species along increasingly human-altered environments (López et al. 2015). Balakrishna et al. (2016) also found differences from natural and urban environments for the lizard Psammophilus dorsalis (Gray, 1831). The authors reported that individuals from a natural environment had a greater diversity of prey in their stomach contents (Balakrishna et al. 2016).

All previous diet studies of L. fuscus reported different prey as the most important in the species diet. We also highlight that each study was conducted in different ecoregions. Firstly, a population from a Cerrado area was studied, and the most important prey item was Coleoptera (Carvalho et al. 2008). Then, a population from the Pantanal floodplain presented Orthoptera as the most important prey item (Sugai et al. 2012). We also highlighted that both areas mentioned are characterized as wild environments. The third known study on L. fuscus diet (Junqueira et al. 2016) was performed in the Atlantic Forest ecoregion. However, the area where the individuals were collected is inserted in a fragmented landscape with pastures and crops. The study did not analyze the importance of prey items. However, they show that coleopterans and ants were the most consumed items (Junqueira et al. 2016). Besides, each of our studies found a different most important prey; they therefore support the idea that L. fuscus, as most anurans, is a generalist species (Carvalho et al. 2008; Sugai et al. 2012; Junqueira et al. 2016). Our diet results from the wild environment also support the belief that L. fuscus is a generalist predator, with a wild range of invertebrate orders (Fig. 3).

The changes from urban to wild environments provide a gradient in the composition of insect communities (McIntyre et al. 2001; McKinney 2008; Raupp et al. 2010). Some insects are positively phototropic (Sivinski 1998), and the urban illumination can attract specific insect orders, contributing to the difference in the insect’s community composition. In the same way, the different availability of arthropods between environments, as shown in previous studies (e.g. McIntyre et al. 2001; McKinney 2008; Raupp et al. 2010), allied to the generalist diet of L. fuscus, which is influenced by arthropods availability in environment, can lead to the significant differences found in the diet of the animals from both sites.

Leptodactylus fuscus is a common and abundant species, inhabiting many environments (Uetanabaro et al. 2008). Although it is a species of generalist habits (Carvalho et al. 2008; Sugai et al. 2012; Pimenta et al. 2014; Junqueira et al. 2016), the urbanization probably affects its diet composition. However, a study with a more appropriated design would response more precisely how the urbanization process alters the biological traits of the frog. We recommend in a further experiment, at least, sample three ponds of each environment type, as well as repeat the experiment by two years minimum.

Acknowledgements

We are grateful to two anonymous reviewers for their critical revision. To Vinícius de Avelar São Pedro for his revision and comments in a previous version of the manuscript. To the Use Animal Ethics Committee of the Federal University of Mato Grosso do Sul for their approval of the project that predated this experiment (protocol 810/2016). The collection license was provided by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio 49080-1). We thank “Dona” Marina e “Seu” João for the study permits in the area of Santa Fé Farm in “Projeto Brejo Bonito”. VGF and MON thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their scholarship (financial code 001). DJS thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for his research fellowship (311492/2017-7).

References

  • Balakrishna S, Batabyal A, Thaker M (2016) Dining in the city: dietary shifts in Indian Rock Agamas across an urban-rural landscape. Journal of Herpetology 50: 423–428. https://doi.org/10.1670/14-073
  • Barrett K, Samoray ST, Helms BS, Guyer C (2012) Southern two-lined salamander diets in urban and forested streams in western Georgia. Southeastern Naturalist 11: 287–296. https://doi.org/10.1656/058.011.0210
  • Carvalho CB, Freitas EB, Faria RG, Batista RC, Batista CC, Coelho WA, Bocchiglieri WA (2008) Natural history of Leptodactylus mystacinus and Leptodactylus fuscus (Anura: Leptodactylidae) in the Cerrado of Central Brazil. Biota Neotropica 8: 105–115. http://dx.doi.org/10.1590/S1676-06032008000300010
  • Chenchouni H (2016) Variation in White Stork (Ciconia ciconia) diet along a climatic gradient and across rural-to-urban landscapes in North Africa. International Journal of Biometeorology 61: 549–564. https://doi.org/10.1007/s00484-016-1232-x
  • Coleman JL, Barclay RM (2013) Prey availability and foraging activity of grassland bats in relation to urbanization. Journal of Mammalogy 94(5): 1111–1122. https://doi.org/10.1644/12-MAMM-A-217.1
  • Crump ML, Scott NJJ (1994) Visual encounter surveys. In: Heyer WR, Donnelly MA, Mcdiarmid RW, Hayek LC, Foster MS (Eds) Measuring and monitoring biological diversity: standard methods for amphibian. Smithsonian Institution Press, Washington, 84–92.
  • da Rosa I, Canavero A, Maneyro R, Naya DE, Camargo A (2002) Diet of four sympatric anuran species in a temperate environment. Boletín de la Sociedad de Biología de Uruguay 13: 12–20.
  • de Sá RO, Grant T, Camargo A, Heyer WR, Ponssa ML, Stanley E (2014) Systematics of the neotropical genus Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae): phylogeny, the relevance of non-molecular evidence, and species accounts. South American Journal of Herpetology 9: S1–S100. https://doi.org/10.2994/SAJH-D-13-00022.1
  • Grzedzicka E, Krzysztof KUS, Nabielec J (2013) The effect of urbanization on the diet composition of the Tawny owl (Strix aluco L.). Polish Journal of Ecology 61: 391–400.
  • Heyer WR, Rand AS, Cruz CAG, Peixoto OL, Nelson CE (1990) Frogs of Boracéia. Arquivos de Zoologia 31(4): 231–410.
  • Hunter P (2007) The human impact on biological diversity. How species adapt to urban challenges sheds light on evolution and provides clues about conservation. EMBO Reports 8: 316–318. https://doi.org/10.1038/sj.embor.7400951
  • INMET [Instituto Nacional de Meteorologia] (2005) Parâmetros meteorológicos de Campo Grande. http://www.inmet.gov.br [Accessed in March 01, 2017]
  • Jaganmohan M, Vailshery LS, Nagendra H (2013) Patterns of insect abundance and distribution in urban domestic gardens in Bangalore, India. Diversity 5(4): 767–778. https://doi.org/10.3390/d5040767
  • López JA, Scarabotti PA, Medrano MC, Ghirardi R (2009) Is the red spotted green frog Hypsiboas punctatus (Anura: Hylidae) selecting its preys? The importance of prey availability. Revista de Biología Tropical 57: 847–857. https://doi.org/10.15517/rbt.v57i3.5497
  • MacGregor-Fors I, Ordoñez OH, Ortega-Álvarez R (2013) Urban croaking: diversity and distribution of anurans in a neotropical city. Urban Ecosystems 16(2): 389–396. https://doi.org/10.1007/s11252-012-0267-y
  • McDonald RI, Green P, Balk D, Fekete BM, Revenga C, Todd M, Montgomery M (2011) Urban growth, climate change, and freshwater availability. Proceedings of the National Academy of Sciences 108: 6312–6317. https://doi.org/10.1073/pnas.1011615108
  • Mitchell JC, Jung Brown RE, Bartholomew B (2008) Urban herpetology. Society for the Study of Amphibians and Reptiles, Salt Lake City.
  • Montezol M, Cassel M, Silva D, Ferreira A, Mehanna M (2018) Gametogenesis and reproductive dynamics of Rhinella schneideri (Anura: Bufonidae): Influence of environmental and anthropogenic factors. Acta Zoologica 99(1): 93–104. https://doi.org/10.1111/azo.12195
  • Nicholls B, Manne LL, Veit RR (2017) Changes in distribution and abundance of anuran species of Staten Island, NY, over the last century. Northeastern Naturalist 24(1): 65–81. https://doi.org/10.1656/045.024.0106
  • Pimenta BVS, Costa D, Murta-Fonseca R, Pezutti T (2014) Anfíbios: Alvorada de Minas, Conceição do Mato Dentro, Dom Joaquim: Minas Gerais. Belo Horizonte, 196pp.
  • Pinkas L (1971) Bluefin tuna food habits. In: Pinkas L, Oliphant MS, Iverson IK (Eds) Food habits of Albacore, Bluefin Tuna, and Bonito in California waters. Department of Fish and Game, Los Angeles, 47–63.
  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R–project.org/.
  • Riley SP, Busteed GT, Kats LB, Vandergon TL, Lee LF, Dagit RG, Kerby AL, Fisher RN, Sauvajot RM (2005) Effects of urbanization on the distribution and abundance of amphibians and invasive species in southern California streams. Conservation Biology 19: 1894–1907. https://doi.org/10.1111/j.1523-1739.2005.00295.x
  • Rodrigues DJ, Uetanabaro M, Prado CPA (2004) Seasonal and ontogenetic variation in diet composition of Leptodactylus podicipinus (Anura, Leptodactylidae) in the southern Pantanal, Brazil. Revista Española de Herpetologia 18: 19–28. https://dialnet.unirioja.es/servlet/articulo?codigo=1393184
  • Simon JA, Snodgrass JW, Casey RE, Sparling DW (2009) Spatial correlates of amphibian use of constructed wetlands in an urban landscape. Landscape Ecology 24(3): 361–373. https://doi.org/10.1007/s10980-008-9311-y
  • Threlfall CG, Law B, Banks PB (2012) Influence of landscape structure and human modifications on insect biomass and bat foraging activity in an urban landscape. PLoS One 7(6): e38800. https://doi.org/10.1371/journal.pone.0038800
  • Uetanabaro M, Prado CPA, Rodrigues DJ, Gordo M, Campos Z (2008) Guia de campo dos anuros do Pantanal e planaltos de entorno. Editora UFMS, Campo Grande, 196 pp.
  • Vallan D (2002) Effects of anthropogenic environmental changes on amphibian diversity in the rain forests of eastern Madagascar. Journal of Tropical Ecology 18: 725–742. https://doi.org/10.1017/S026646740200247X