Open-access Diet of the lesser-grison, Galictis cuja (Mammalia, Carnivora): a review and new data from the Brazilian semiarid Caatinga

Dieta do furão-pequeno, Galictis cuja (Mammalia, Carnivora): uma revisão e novos dados para a Caatinga do semiárido brasileiro

Abstract

The lesser-grison (Galictis cuja) is a mustelid native to South America with an wide, but its diet remains poorly understood. The present study combines published data with new information on the diet of G. cuja from the semiarid Caatinga ecoregion, based on the analysis of the stomach contents of two road-killed specimens. Sixteen studies, conducted in Argentina, Brazil, Chile, and Uruguay, were reviewed, permitting the identification of seven dietary categories: Invertebrates, Mammals, Birds, Reptiles, Amphibians, Fish, and Plant Material. Mammals and birds were the items consumed most frequently, while amphibians and fish were the least common items. The novel items identified in the Caatinga sample included the white-eared opossum (Didelphis albiventris), white tegu eggs (Salvator merianae), and melon seeds (Cucumis melo L.). The data indicate that G. cuja has a diverse diet, with mammals present in 100% of the diets analyzed, reflecting the role of the species as a mesopredator and potential seed disperser. The lack of data from a number of different ecoregions highlights the need for further research to better understand the ecological role of the species, and to develop effective conservation strategies, given that the current knowledge on the diet of G. cuja may not best represent its ecological importance and the challenges faced by the species in impacted environments.

Keywords:
Brazilian Northeast; feeding habits; mustelid; predation

Resumo

O furão pequeno (Galictis cuja) é um mustelídeo da América do Sul com ampla distribuição, mas sua dieta ainda é pouco conhecida. Este estudo combina dados da literatura existente e fornece novas informações sobre a dieta de G. cuja na ecorregião da Caatinga, a partir da análise dos conteúdos estomacais de dois espécimes atropelados. Foram revisados 16 estudos realizados na Argentina, Brasil, Chile e Uruguai, identificando sete categorias alimentares: invertebrado, mamíferos, aves, répteis, anfíbios, peixes e material de origem vegetal. Mamíferos e aves foram os alimentos mais frequentemente consumidos, enquanto anfíbios e peixes foram menos frequentes. Para a Caatinga, foram identificados itens inéditos, como o gambá-de-orelha-branca (Didelphis albiventris), ovos de teiú (Salvator merianae) e sementes de melão (Cucumis melo L.). Os resultados indicaram que G. cuja têm uma dieta diversificada e com a presença de mamíferos em 100% das dietas analisadas, caracterizando seu papel como mesopredador e potencial dispersor de sementes. A escassez de dados em várias ecorregiões destaca a necessidade de mais pesquisas para compreender melhor o papel ecológico da espécie e traçar estratégias de conservação, uma vez que o conhecimento atual pode não refletir totalmente sua importância ecológica e os desafios que enfrenta.

Palavras-chave:
Nordeste brasileiro; hábitos alimentares; mustelídeo; predação

1. Introduction

The lesser-grison, Galictis cuja (Molina, 1782), is a poorly-known South American carnivore which belongs to the family Mustelidae (Kasper et al., 2013). While G. cuja is essentially terrestrial, it is known to be able to dig well and is a good swimmer (Ercoli et al., 2015). The species is classified as Least Concern (LC), both worldwide (IUCN, 2023) and in Brazil (ICMBio, 2023), but it is still very poorly studied. In fact, the ecological and functional features of this species are virtually unknown (Delibes et al., 2003; Poo-Muñoz et al., 2014; Tellaeche et al., 2014; Smith P., 2022). G. cuja is distributed in Argentina, Bolivia, Brazil, Chile, Paraguay, Peru, and Uruguay (Yensen and Tarifa, 2003), where it occurs in a wide variety of habitats, ranging from grassland to rainforest (Yensen and Tarifa, 2003).

Based on Nagy-Reis et al.’s (2020) review of its geographic distribution, G. cuja is known to occur in a number of different Neotropical ecoregions, including the Araucaria Moist Forest, the Atacama Desert, Atlantic Coastal Restinga, Atlantic Dry Forest, Campos Rupestres (Montane Savanna), Brazilian Cerrado Savanna, Chilean Matorral, Coastal and Interior Forests of Bahia, Pantanal, Interior Forest of Pernambuco, Serra Do Mar Coastal Forest, Southern Andean Yungas, Southern Atlantic Mangroves, Uruguayan Savanna, and Valdivian Temperate Forest. It is also found in the Caatinga (Shimabukuro et al., 2022; Ferreira et al., 2022), Alto Paraná Atlantic Forest, and in both the Dry and the Humid Chaco (Nagy-Reis et al., 2020; Smith, 2022). Despite this wide, very few or no data are available on the diet of G. cuja from most of the geographic range of the species.

Galictiscuja is considered to have a generalist diet (Sade et al., 2012), given that this species is known to feed on an ample diversity of foods, including mammals (e.g. Rocha-Mendes et al., 2010; Braga et al., 2020; Pasa et al., 2020), birds and their eggs (e.g. Diuk-Wasser and Cassini, 1998; Delibes et al., 2003; Kraus and Rödel, 2004; Galende and Raffaele, 2016), reptiles and their eggs (e.g. Ebensperger et al., 1991; Delibes et al., 2003; Braga et al., 2020), invertebrates (e.g. Zapata et al., 2005; Galende and Raffaele, 2016; Pasa et al., 2020), amphibians (e.g. Kasper et al., 2016), and plant material (e.g. Galende and Raffaele, 2016; Pasa et al., 2020; Schmitt and Favretto, 2021). In Brazil, studies of the diet of G. cuja have been conducted primarily in the southern part of the country (Schmitt and Favretto 2021, Pasa et al. 2020, Rocha-Mendes et al. 2010), while there are no published reports of its diet from the Caatinga dry forest. Given the scarcity of data on G. cuja, which also hampers the reliable assessment of its conservation status (Shimabukuro et al., 2022), a systematic review of the available information is necessary to provide a more definitive overview of the biology and feeding ecology of this species.

The semiarid Caatinga encompasses a variety of habitat types, ranging from dense dry forests with a continuous canopy to more shrubby vegetation, with sparse trees and a denser shrub layer (Fernandes and Queiroz, 2018). This biome has considerable biological diversity and endemism, including 1,400 vertebrate species, of which, 23% are endemic (Garda et al., 2018). The biome’s climate is classified as semiarid in the Köppen-Geiger system (Alvares et al., 2013), with maximum temperatures of 42ºC and greatly reduced resource availability (water and food) during the dry season (Prado, 2003). A total of 183 mammals are known to occur in the Caatinga, of which 11 are endemic species (Carmignotto and Astúa, 2017). The vast majority of these species are still poorly studied in Caatinga ecosystems (Carmignotto and Astúa, 2017; Santos, 2004; Teixeira et al., 2021).

The present study compiles data from two sources – a review of the published data on the diet of Galictis cuja from different ecoregions and new data derived from the analysis of the contents of the stomachs and intestines of two roadkilled specimens collected from the Caatinga, which provide the first record of the diet of G. cuja from this ecoregion. In addition to complementing the database on the composition of the diet of G. cuja, the present study should help to fill the knowledge gaps that exist in the natural history and feeding ecology of this poorly-known species in a region from which almost no data are available.

2. Material and Methods

2.1. Literature search

The data were compiled without any restrictions, and considered all the different ecoregions in which the species is known to occur. The references cited in the papers identified in the literature search were examined for additional sources. These data were compiled to complement the data obtained from the analysis of the contents of the stomachs and intestines of the two Galictis cuja specimens collected during the present study. The Google Scholar, Scielo, and Web of Science platforms were consulted for the literature search, which focused on papers published in indexed journals, dissertations, theses, and congress abstracts. This process was based on the following search terms – “diet, Galictis cuja” or “food, Galictis cuja” or “Galictis cuja, predation” or “diet, Lesser Grison” or “feeding, Lesser Grison” or “Lesser Grison, predation”. These search terms were applied in English, Spanish, and Portuguese, given that the distribution of G. cuja is restricted to South America.

A standard set of data were extracted from each document identified during the literature search: (I) food items identified, (II) the method employed (observation, analysis of stomach contents, feces), and (III) the country. The ecoregion in which each study was conducted was identified using the geographic coordinates provided in the respective study, which were used to identify the ecoregion, based on the classification of Dinerstein et al. (2017).

2.2. The diet of Galictis cuja

The initial analysis conducted here evaluated the frequency of consumption of the different categories of dietary items in each ecoregion. For this, the number of records of consumption of each category was determined and the results were plotted on a map, showing the relative frequency of each category consumed per ecoregion. The study of Pires (2018) was not included in this analysis because it did not provide information on the ecoregion from which the dietary records were obtained. To create a map, the QGIS software version 3.22.7 was used. Then, the graphs and frequency data were generated in Excel version 2409. Finally, both information were imported into CorelDRAW where the vectorized symbols corresponding to each category were inserted.

The second analysis verified the differences in the occurrence (presence or absence) of each dietary category in the different studies. For this, a contingency analysis was applied, based on χ2, the contingency coefficient, and the respective p value. This analysis was used to show what percentage of the data fits into each food category, facilitating, in this case, the comparison between the percentages of occurrence of each food item. This analysis included only data from studies of stomach contents (13 studies), while those involving visual observations (i.e. Rocha-Mendes et al., 2010; Schmitt and Favretto, 2021; Rampinell 2022) were not considered.

The third analysis focused on the trophic niche, using Levins’ standardized index (Bsta) to measure the breadth of the feeding niche (Krebs, 1999), based on the contribution of the different categories identified in the respective analyses (considering all sampling methods) using the following Equation 1 to calculate the basic index:

B = 1 i = 1 n p i 2 (1)

where B = Levins’ index, Pi = proportion of item i in relation to the total, n = total number of items recorded.

Levins’s index was then standardized using the following Equation 2:

B s t a = B 1 n 1 (2)

where Bsta = Levins’ standardized index, B = Levins’ index (see above), n = total number of items recorded.

The value of Bsta varies from 0 to 1, with values closer to zero indicating a greater degree of specialization (fewer items included in the diet) and those closer to 1 reflecting a more generalist diet, with the more equitable exploitation of a broader range of items. The data were processed in Microsoft Excel 2019, and the similarity analysis was run in the IBM SPSS Statistics V.29.0.2.0 software. A p < 0.05 significance level was considered for all the analyses.

2.3. Study specimens

Two G. cuja specimens were analyzed here, both of which were killed in collisions with traffic. The collection of the specimens was authorized by license 40,620, emitted by the Biodiversity Information and Authorization System (SISBIO) of the Brazilian Ministry of the Environment. One specimen (G1) was found on a perimeter road of the Furna Feia National Park in the rural zone of the municipality of Mossoró (04°58.520’ S, 37°25.569’ W) on November 16th, 2021, at the end of the dry season. The second specimen (G2) was collected from the outskirts of the town of Mossoró (05°10.649’ S, 37°21.925’ W) on February 20th, 2022, during the rainy season (Figure 1). Both specimens were frozen whole at -18ºC for long-term storage prior to analysis.

Figura 1
Records of roadkilled Galictis cuja, specimen G2 collected during road monitoring in the outskirts of Mossoró.

2.4. Identification of the diet

Once defrosted, the two G. cuja specimens were first weighed on a computerized digital scale (precision of 0.2 g). The stomach and intestines were then removed for the analysis of their contents, which were processed to separate the individual components (items). These items were weighed on a precision BL-320AB digital scale (accuracy of 0.0001 g), and were examined under a Stemi 305 optical stereomicroscope (magnification of up to 40x) for the identification of the taxa, with the aid of the relevant taxonomic references. After analysis, the items were transferred to sterile containers filled with 70% alcohol.

3. Results

A total of 15 studies of the diet of G. cuja were identified in the literature search, of which, 11 were written in English, one in Spanish, and three in Portuguese. The earliest study was published in 1991, and the most recent, in 2022. The present study brings the total number of studies to 16. These studies were conducted at 27 different sites in eight ecoregions. Some studies present sampling sites in more than one ecoregion (i.e. Diuk-Wasser and Cassini, 1998; Delibes et al., 2003; Rocha-Mendes et al. 2010; Galende and Raffaele, 2016;) Four of these sites were located on the Patagonian Steppe, three each in the Serra do Mar Coastal Forest and Uruguayan Savanna, and two each in the Auraucaria Moist Forest, Valdivian Temperate Forest, Alto Paraná Atlantic Forest, and Chilean Matorral, with the present study providing the first data from the Caatinga. Eight of the 16 studies were conducted in Brazil, four in Argentina, three in Chile and one in Uruguay (Table 1). The dietary items identified in these studies were allocated to seven different categories: Invertebrates, Mammalia, Aves, Reptilia, Amphibia, Pisces, and Plant Material. When an item could not be identified unequivocally, it was designated as Unidentified (UI).

Table 1
Findings of the literature search of the data published on the diet of Galictis cuja per ecoregion, locality, and types of food ingested.

Figure 2 provides an overview of the data compiled in the present study, showing the distribution of the sites investigated in the different ecoregions of South America, and the number of records of the different items recorded in the diet of the local G. cuja. A total of seven categories were recorded in the Uruguayan Savanna, for example, where mammals accounted for 43.8% of the records, while birds, reptiles, and invertebrates each accounted for 12.5%, and plant material, amphibians, and fish for 6.3%, in each case. In the Patagonian Steppe, mammals accounted for 62.2% of the records and invertebrates, for 13.3%, while birds and reptiles each provided 8.9% of the records, and plant material, 6.7%. In the Alto Paraná Atlantic Forest, half (50.0%) of the records were of invertebrates, while mammals and birds each provided 25.0%. Most (70.0%) of the records from the Valdivian Temperate Forest were of mammals, with 13.0% being provided by birds, and 7.0% by reptiles. In the Auraucaria Moist Forest, by contrast, plant material was the principal category, providing 40.0% of the dietary records, followed by mammals, birds, and invertebrates, which each provided 20.0%. Mammals were the principal prey in the Chilean Matorral, however, with 63.0% of the records, while birds and plant material each provided 13.0%, and reptiles and invertebrates, 6.0% each. In the present study, in the Caatinga, plant material and reptiles each provided a third (33.3%) of the records, with mammals and invertebrates providing the rest of the records (16.7% each). The studies in the Serra do Mar Coastal Forest recorded only reptilian prey (100.0% of the records), however (Figure 2).

Figure 2
Distribution of the Galictis cuja sites reported here and in the 15 studies published between 1991 and 2022 identified in the literature search. The graphics show the relative frequencies of the items of dietary different categories recorded in each ecoregion: Patagonian Steppe, Serra do Mar Coastal Forests, Uruguayan Savanna, Auraucaria Moist Forest, Valdivian Temperate Forest, Alto Paraná Atlantic, Chilean Matorral, and Caatinga.

The analysis of the records shows that the composition of the items consumed varied significantly among the 13 studies for which quantitative data were available (N = 91; df = 6; χ2 = 41.03; C = 0.56; p < 0.05). Mammals (100.0%), birds (92.3%, 12 studies), and invertebrates (76.9%, 10 studies) were the most widespread items, while amphibians (15.3%, 2 studies) and fish (7.6%, 1 study) were the least common. The contribution of these two groups – common (mammals, birds, and invertebrates) and rare (amphibians and fish) – was significantly different (p < 0.05). By contrast, reptiles (61.5%, 8 studies) and plant material (53.8%, 7 studies) were intermediate in their occurrence, and were not significantly different from the other categories (p > 0.05).

3.1. Diet of the Caatinga specimens

Most of the items found in the digestive tracts of the two G. cuja specimens analyzed in the present study were relatively well-preserved, which permitted their reliable identification. While the digestive tracts of both specimens contained some plant material, all the prey items were unique to each individual.

The identification of the white-eared opossum, Didelphis albiventris (Didelphidae), was possible from the coloration of the pelage and the hind legs, which were found whole. The eggshells of white tegu, Salvator merianae (Teiidae) found in the intestine of specimen G1 (see Table 2) were more brownish in color than those found in the stomach, which reflects the more advanced stage of digestion in this posterior portion of the digestive tract. These eggs were soft and elliptical in shape, and were approximately 4 cm long. The tick was in perfect condition, and was identified as Amblyomma parvum (Appendix 1). By contrast, the specimen of Tropidurus sp. (Tropiduridae) was fragmented and chewed up, and it was only possible to identify the taxon from the jaw and pieces of skin from the head that still had scales attached to them. The melon (Cucumis melo L.) seeds were whole and yellowish in color and were associated with some melon pulp, which indicates the direct consumption of the fruit and the potential for seed dispersal.

Table 2
Details of the Galictis cuja specimens collected from the Caatinga ecoregion and analyzed in the present study, and the items found in their digestive tracts.

The analysis of the trophic niche of G.cuja revealed a diet of intermediate diversity, with a Levins’ index (B) of 2.774, which indicates a variety of dietary categories with a certain predominance of some items. When standardized by the total number of items consumed (Bsta), the index was 0.296.

4. Discussion

Despite the very ample geographic distribution of G. cuja in South America (Yensen and Tarifa, 2003), the available data on the diet of the species are still incipient, and far from complete. To begin with, data are only available from four countries – Argentina, Brazil, Chile, and Uruguay. This general lack of data may hamper the interpretation of the ecological role of G. cuja, in particular, by underestimating the relevance of the species in some regions or overlooking specific ecological pressures, which may represent threats to its survival in certain environments (Roemer et al., 2009; Wright et al., 2022; Llorca et al., 2024).

The data compiled in the present study, from two complementary sources, revealed that G. cuja exploits a high diversity of food categories (Table 1), which indicates that the species has a broad feeding niche, irrespective of the ecoregion. Despite this, mammalian prey was predominant in the G. cuja diet throughout its geographic range, while the negligible contribution of amphibians and fish may be related to differences in the availability of these resources in the environment, especially on a seasonal basis (Sidorovich, 2000), or to foraging preferences of the grisons (Pedó et al., 2006). The records of frugivory and the presence of seeds in some samples indicates opportunistic foraging behavior, as postulated in some previous studies, such as those of Galende and Raffaele (2016) and Schmitt and Favretto (2021). Similar opportunistic foraging behavior has been observed in other mustelids, such as the common weasel (Mustela nivalis) and the stoat, Mustela erminea (Remonti et al., 2007), as well as species of the genera Martes and Meles (Newman et al., 2011).

While mammals and reptiles are common prey of G. cuja, neither D. albiventris nor Tropidurus have been recorded previously. The mean body weight of D. albiventris is 829 g (Faria et al., 2019), which is consistent with the findings of Zapata et al. (2005), who report that adult G. cuja take prey of up to 3 kg, including adult hares. The two previous records of the predation of S. merianae (Braga et al., 2020; Rampinell., 2022) referred to the adult animal, rather than the eggs, as observed here, although other studies have also recorded the ingestion of reptile eggs (Delibes et al., 2003; Galende and Raffaele, 2016), which may thus be an important nutritional resource for G. cuja. The presence of leaf fragments in the ingesta of specimen G1 was likely associated with the predation of the S. merianae eggs, which are typically buried under the leaf litter to keep them moist (Schaumburg et al., 2016). This further reinforces the hypothesis of Braga et al. (2020), who concluded that G. cuja may habitually dig to search for nests and burrows during its foraging activities.

The limited evidence of frugivory found up to now in G. cuja (Tables 1 and 2) may be related to the fact that most fruit is digested rapidly, and is thus rarely discernible in stomach contents or feces (Schmitt and Favretto, 2021). The presence of three intact seeds in the intestine of specimen G2 is also consistent with the role of G. cuja as a potential seed disperser, as observed in many other carnivores (e.g. Cazetta and Galetti, 2009; Cossíos, 2010; Quintela et al., 2014), including other mustelids (Zhou et al., 2008; Tsuji et al., 2011). Large plantations of C. melo L. are found in the rural zone of Mossoró, which is a major producer of melon in the Brazilian state of Rio Grande do Norte (Oliveira et al., 2007). The association between wild animals and commercial fruit plantations has been documented previously in both the study region (Davi et al., 2019) and in other semiarid environments (Mellink et al., 2016; Riojas-López et al., 2018; Silva and Azevedo, 2020). Freitas et al. (2017) also recorded the crab-eating fox (Cerdocyon thous) feeding on watermelon in the Caatinga. It seems likely that large-scale plantations of fruit with a high water content, such as melons, which are produced for export (Brasil, 2024), in the Caatinga, may represent an extremely important source of nutrients and water for many local vertebrate populations, in particular during the dry season. Given this, it would be essential to better understand the consequences of the presence of these animals in agricultural environments, in search of water and nutrients, which has the potential to provoke conflicts with farmers (see Spagnoletti et al., 2017; Zhong et al., 2023).

Ticks (Ixodida) had not been recorded previously in the ingesta or feces of G. cuja (Table 1), and these invertebrates are an unlikely item in the diet of a mustelid. As only a single individual was found, it seems likely that this was a case of accidental ingestion, probably during self-grooming, which is the principal route of ingestion of parasites by birds and mammals (Johnson et al., 2010). Alternatively, the tick may have been ingested unintentionally during the predation of an animal to which it was attached.

While Levins’ index (B = 2.774) indicated a diverse diet, the standardized index (Bsta = 0.295) revealed that, despite the diversity of items consumed, G. cuja prefers certain items, which predominate in its diet. Overall, the data highlight the role of G. cuja as a mesopredator, which feeds on an ample variety of vertebrate prey. The exploitation of certain specific types of item may be influenced by a range of ecological and environmental factors, such as the variation in the local and seasonal availability of prey (Azevedo et al., 2006), as well as interspecific competition (Smith et al., 2023). Based on the findings of the present study, it seems likely that G. cuja exploits the most abundant prey (e.g. Tropidurus sp.) or resource (e.g. C. melo L.) available within its home range, or items that provide most nutrients, such as mammals, including D. albiventris (Kohl et al., 2015; Gómez-Ortiz et al., 2011).

While only a very limited sample was analyzed in the present study, all the specimens identified in the digestive tracts of the two lesser-grison specimens analyzed here, with the exception of S. merianae, represented novel items in the diet of G. cuja, providing new insights into the feeding ecology of the species. While G. cuja is considered to be a dietary generalist in most studies, the results of the present study have revealed a marked preference for mammalian prey. In addition to the novel taxa (D. albiventris, Tropidurus sp., A. parvum, and C. melo L.) recorded here, the ingestion of intact melon seeds indicates that G. cuja may play an ecological role as a seed disperser, which reinforces the need for further data on the feeding ecology of the species from new areas within its geographic distribution. This reinforces the need for more extensive and systematic research to better understand the feeding ecology of G. cuja, and the development of more effective strategies for the conservation of the species.

Acknowledgements

We would like to thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for authorizing the collection of specimens through license number 40,620. We are also grateful to the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing a doctoral scholarship to S. Cabral (88887.702593/2022-00). A. Queiros (88887.921508/2023-00), J. Lima (88887.687023/2022-00) and R. Santos (88887.825921/2023-00) are grateful to the Brazilian Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their graduate scholarships. The authors also would like to thank the editor and reviewers for their constructive feedback.

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Publication Dates

  • Publication in this collection
    31 Jan 2025
  • Date of issue
    2024

History

  • Received
    03 May 2024
  • Accepted
    01 Nov 2024
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