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Acta Biológica Colombiana

Print version ISSN 0120-548X

Acta biol.Colomb. vol.25 no.2 Bogotá May/Aug. 2020

https://doi.org/10.15446/abc.v25n2.79721 

Nota Breve

DIURNAL FEEDING BEHAVIOUR OF CRAB-EATING RACCOON UPON A PARADOXAL FROG, WITH A REVIEW OF ITS DIET

Alimentación diurna del mapache cangrejero sobre una rana paradoxal, con una revisión de su dieta

Karoline CERON1  * 

Priscila S. CARVALHO2 

Lydia MÖCKLINGHOFF3 

Diego José SANTANA1  2 

1 Universidade Federal de Mato Grosso do Sul, Cidade Universitária, CEP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil

2 Programa de Pós-Graduação em Biologia Animal, Universidade Estadual Paulista (UNESP), 15054-000, São José do Rio Preto, São Paulo, Brazil

3 Zoologisches Forschungsmuseum Koenig, AG Tropenökologie, Prof. Dr. Schuchmann, Adenauerallee 160, 53113 Bonn, Germany


ABSTRACT

The crab-eating raccoon (Procyon cancrivorus) is considered one of the less-studied Neotropical carnivores. Observations about its behavior are difficult as it is mainly nocturnal, shy, and inconspicuous. This species is considered opportunistic, with a frugivorous-omnivorous diet. It is known to feed on fruits and invertebrates as well as small mammals and lizards. Herein, we describe a first direct observation of a crab-eating raccoon hunting for frogs during the daytime. It is also a first record of predation on a paradoxal frog (Pseudisplatensis) by P. cancrivorus. We further present a detailed literature review about its diet. We compiled a total of 14 papers published from 1986 to 2019, including eight studies that characterize the diet of P. cancrivorus. According to these studies, the diet of P. cancrivorus constitutes of 35 vegetal taxa and 96 animal taxa. Thus, the here presented record of predation on a frog by P. cancrivorus is not only the first visual description of this behavior, it also reinforces the knowledge about its generalist and opportunistic diet. It is further the first evidence of the daytime behavior for the crab-eating raccoon in the Pantanal.

Keywords: Pantanal; Procyon cancrivorus; Pseudis platensis; trophic ecology

RESUMEN

El mapache cangrejero es considerado uno de los carnívoros neotropicales menos estudiados, debido a sus hábitos nocturnos y discretos que dificultan las observaciones sobre su comportamiento. Esta especie es considerada una especie frugívora-omnívora, con hábitos oportunistas, que se alimenta desde invertebrados hasta otros mamíferos y lagartos. En este documento, proporcionamos un nuevo informe de depredación por un mapache cangrejero sobre una rana paradójica (Pseudisplatensis) y presentamos una revisión bibliográfica detallada sobre su dieta. Recopilamos un total de 14 artículos publicados de 1986 a 2019, de los cuales se utilizaron ocho estudios para caracterizar la dieta de P. cancrivorus. La dieta de P. cancrivorus estuvo constituida por 96 taxones animales y 35 vegetales. Nuestro registro de depredación sobre una rana refuerza la dieta generalista y oportunista conocida de P. cancrivorus y es además la primera evidencia de actividad diurna para el mapache cangrejero en el Pantanal y el primer informe de depredación sobre P. platensis por parte de un mamífero.

Palabras clave: Ecología trófica; Pantanal; Procyon cancrivorus; Pseudis platensis

The crab-eating raccoon (Procyon cancrivorus) is a medium-sized nocturnal carnivore widely distributed in the Neotropics, from Costa Rica to Uruguay. It inhabits forested and open areas, generally associated with limnic systems (González et al., 2010). Due to its nocturnal and inconspicuous behavior, the crab-eating raccoon is considered one of the less-studied Neotropical carnivores. The species is opportunistic, and its omnivorous diet (Paglia et al., 2012) includes fruits and invertebrates as well as small mammals and lizards (e.g., Gatti et al., 2006; Quintela et al., 2014; Dias and Bocchiglieri, 2015). In this paper, we investigate the diet of P. cancrivorus and report a predation event by P. cancrivorus upon a paradoxal frog (Pseudisplatensis) in the Southern Pantanal.

We searched for studies in the Web of Science (<https://webofknowledge.com/>) and Scopus (<https://www.scopus.com>) databases, using the keywords 'Procyon cancrivorus' AND 'Diet*' OR 'feed*' OR 'trophic ecology* up to 2019. Besides, we gather all data from direct searches of references in Google Scholar (https://scholar.google.com.br/). Among these compiled references, we selected only studies presenting absolute data on the diet of P. cancrivorus.

We compiled a total of 14 papers published from 1986 to 2019, with eight publications characterizing the diet of P. cancrivorus. Seven studies were performed in Brazil, distributed in Northeast, Southeast, and South, and only one study was performed in Venezuela with multiples localities. These studies accessed P. cancrivorus diet, analyzing fecal samples and stomach content. According to these studies, the diet incorporates 96 animal taxa and 35 vegetal taxa (Supplementary material. Aratus sp. (Brachyura: Decapoda) and Syagrus romanzoffiana (Arecaceae) were reported to be the animal and plant most abundant in the diet of P. cancrivorus. Coleoptera and Orthoptera were the items most frequent among six of the eight studies compiled.

Besides this information from existing literature, were here report a direct observation on P. cancrivorus foraging in a freshwater lake at Fazenda Barranco Alto Lodge in the Southern Pantanal, municipality of Aquidauana, Mato Grosso do Sul (19°34'S, 56°8' W, 114 m.a.s.l). The observation occurred by chance during fieldwork on 4 Jun 2011 from 07:10 am to 07:19 am. An adult P. cancrivorus was observed while it was catching anurans in a lagoon. The species was foraging among aquatic macrophytes, moving its hands quickly back and forth to feel possible catch underneath the water plants. It was hunting exclusively haptic and did not try to move the plants to the side to visualize possible prey in the water. In this manner, the raccoon captured and ate six anurans during nine minutes of observation. Only one of these anurans preyed by P. cancrivorus could be identified as the paradoxal frog (Pseudis platensis) (Fig. 1), an aquatic diurnal/nocturnal hylid that occurs in permanent and semi-permanent ponds (Dixon et al., 1995). Paradoxal frog could be identified by its medium size (greater than Lysapsus limmelum, another aquatic hylid) and by the coloration of its thigh, with thick dark lines (Garda et al., 2010) (Fig.1c). This is the first visual record of P. cancrivorus feeding upon an anuran and the first report of predation upon P. platensis by a mammal.

Figure 1 (a-c) An adult crab-eating racoon (Procyon cancrivorus) searching and preying an adult paradoxal frog (Pseudis platensis) in a lagoon in Pantanal, Mato Grosso do Sul, Brazil. (Photos: Lydia Möcklinghoff) 

Despite the wide distribution of P. cancrivorus, dietary studies were concentrated in Brazil, mainly in Protected Areas (e.g., Santos and Hartz, 1999; Gatti et al., 2016). The elevate abundance of Aratus sp. (n = 114) can be related to the mangrove environment where this species is common (Novaes, 2002). Syagrus romanzoffiana is a common palm in a semideciduous forest in South Brazil and frequently is reported in dietary studies of mammals like squirrels, tapirs, peccary, brown-nosed coatis and maned wolfs (e.g., Bueno and Motta-Junior, 2004; Keuroghlian and Eaton, 2008; Giombini et al., 2009). Fruits are produced throughout the year, showing ovoid shape (ca. 2.5 cm diameter), with a soft exocarp and woody endocarp (Galetti et al., 1992). The elevated frequency of Coleoptera and Orthoptera in P. cancrivorus diet is related to wide distribution and the great abundance of these orders in the environment, which facilitate their visualization and capture (Rafael et al., 2012).

Earlier studies on P. cancrivorus diet show an elevated number of aquatic preys (e.g., Aratus sp.), confirming that this species forages next to water (Trolle, 2003). In these analyses, on the diet of P. cancrivorus, anurans were identified only to the family level, with Bufonidae, Hylidae, and Leptodactylidae being cited. Thus, our record of P. cancrivorus preying on P. platensis was the first one to analyze the preyed anuran to species level.

Paradoxal frog has diurnal and nocturnal habits, vocalizing on the water surface, among macrophytes (Dixon et al., 1995). Information on P. platensis natural history is scarce, with the majority being related to the diet of its giant tadpoles and on parasites (e.g., Emerson, 1988; Arias et al., 2002; Campião et al., 2010; Ceron et al., 2017; Landgref Filho et al., 2019). Reports of animals preying on adults of P. platensis include five bird species, another frog species, snakes, fishes, and caimans (Landgref-Filho et al., 2019). Until now it was not known that also mammals hunt for this frog species. Our observation shows that the ability of the crab-eating raccoon to catch frogs in the water without visual reference, as recorded here, is possible due to the well-developed tactile abilities, using their forepaws skilfully, and other sensory skills of the species (Nowak and Walker, 1999). This tactile way of hunting might be especially of interest when hunting in the dark as P. cancrivorus is known to be mainly nocturnal, such as its congeners Procyon lotor (Greenwood, 1982). However, the observations here presented of diurnal foraging activity of P. cancrivorus are rare, also shows that the animal hunts in a tactile and not visual way during daytime and that this hunting strategy enables the animal to hunt in water with limited visibility and catch the frogs under the floating vegetation.

Few studies have reported diurnal habits to P. cancrivorus (Brooks, 1993; Carrillo and Vaughan, 1993; Gómez et al., 2005). For the Pantanal, this is even the first evidence of a crab-eating raccoon being active during the daytime. Several factors may affect on activity times of raccoons, such as the hunting success in the previous night and individual fitness (Gehrt and Fritzell, 1998). Due to the difficulty to observe predatory events in nature, these records are an important source, as they directly contribute to the knowledge of a species' natural history. Our observation reinforces the known generalist and opportunistic diet of P. cancrivorus, gives new insides about the hunting strategy of this mammal species, and it is the first record of predation on P. platensis by a mammal.

ACKNOWLEDGMENT

KC is grateful to Fundect (Fundação de Apoio ao Desenvolvimento de Ensino, Ciência e Tecnologia do Mato Grosso do Sul) for her scholarship (# 71/700.146/2017). PSC thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES) - Finance Code 001. DJS is grateful to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for his research fellowship (311492/2017-7). LM is grateful for her scholarship at the Studienstiftung des Deutschen Volkes Foundation, Bonn, Germany; the National Institute of Science and Technology for Wetland Research INAU/INCT/UFMT, Cuiaba, Brazil, and the Brazilian Science without Borders Program (SISBO Research Permit No. 5331241).

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Associate Editor: Sonia Gallina Tessaro.

Citation/Citar este artículo como: Ceron K, Carvalho PS, Möcklinghoff L, Santana DJ. Diurnal feeding behaviour of crab-eating raccoon upon a paradoxal frog, with a review of its diet. Acta biol. Colomb. 2020;25(2):359-367. DOI: http://dx.doi.org/10.15446/abc.v25n2.79721

CONFLICT OF INTEREST The authors declare that there is no conflict of interest.

SUPPLEMENTARY MATERIAL

Table. Items reported in the diet of the crab eating racoon (Procyon cancrivorus) reported in the literature between 1986 and 2019. NI = not identified. 

Received: May 16, 2019; Revised: July 05, 2019; Accepted: August 15, 2019

* For correspondence: adenomera@gmail.com

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