Galictis cuja (Mammalia): an update of current knowledge and geographic distribution

Galictis cuja (Mammalia): actualización sobre su conocimiento y distribución geográfica

Galictis cuja (Mammalia): an update of current knowledge and geographic distribution

Galictis cuja (Mammalia): actualización sobre su conocimiento y distribución geográfica

Daniela A. Poo-Muñoz^I; Luis E. Escobar^I,II; A. Townsend Peterson^III; Francisca Astorga^I; John F. Organ^IV; Gonzalo Medina-Vogel^I

^IFacultad de Ecología y Recursos Naturales, Universidad Andres Bello, Av. República 252, Santiago, Chile. ([e-mail]; [e-mail]; [e-mail]; corresponding author: [e-mail])

^IICenter for Global Health and Translational Science, Department of Immunology and Microbiology, State University of New York, Upstate Medical University, Syracuse, NY, USA

^IIIBiodiversity Institute, University of Kansas, 1345 Jayhawk Blvd. Lawrence 66045, Kansas, USA. ([e-mail])

^IVU.S. Fish and Wildlife Service, 300 Westgate Center Drive Hadley and Department of Environmental Conservation, Holdsworth Natural Resources Center, University of Massachusetts, Amherst, MA 01003, USA. ([e-mail])

ABSTRACT

The lesser grison (Galictis cuja) is one of the least-known mustelids in the Neotropics, despite its broad range across South America. This study aimed to explore current knowledge of the distribution of the species to identify gaps in knowledge and anticipate its full geographic distribution. Eighty-nine articles have mentioned G. cuja since 1969, but only 13 focused on the species. We generated a detailed model of the species’ potential distribution that validated previous maps, but with improved detail, supporting previous southernmost records, and providing a means of identifying priority sites for conservation and management of the species.

Keywords: Biodiversity conservation, Mustelidae, Neotropics, distribution, ecological niche modeling.

RESUMEN

El hurón menor (Galictis cuja) es uno de los mustélidos menos conocidos en el Neotrópico, a pesar de su amplia área de distribución a través de América del Sur. El objetivo de este estudio fue explorar la información actual de ocurrencias de la especie para identificar vacíos sobre su conocimiento y anticipar su distribución geográfica. Ochenta y nueve artículos han hecho referencia a G. cuja desde el año 1969, pero sólo 13 se enfocaron en la especie. Se generó un modelo detallado de la distribución potencial de la especie que validó mapas anteriores, pero con mayor detalle, apoyando previos registros australes, y proporcionando una herramienta para la identificación de sitios prioritarios para la conservación y manejo de la especie.

Palabras-clave: Conservación de biodiversidad, Mustelidae, Neotrópico, distribución, modelamiento de nicho ecológico.

The lesser grison [Galictis cuja (Molina, 1782)] is one of the least-known mustelids of South America, and its natural history and conservation status remain poorly understood (Redford & Eisenberg, 1992; Yensen & Tarifa, 2003). It is perhaps typical of a mustelid in diet, eating small mammals (Ebensperger et al., 1991; Diuk-Wasser & Cassini, 1998; Delibes et al., 2003; kraus & Rödel, 2004), and occasionally eggs, birds, reptiles, and amphibians (Yensen & Tarifa, 2003). It has a broad distribution across South America: southern Peru, western Bolivia, central and southern Chile, Paraguay, Uruguay, Argentina, and southeastern Brazil (Yensen & Tarifa, 2003; Borndholdt et al., 2013), at elevations from sea level to 4200 m (Nabte et al., 2009), and including habitats from Atlantic forest (Rocha-Mendes et al., 2010), and cold steppe in Patagonia (Prevosti & Travaini, 2005) to exotic forest plantations in Chile (Zúñiga et al., 2009). However, it appears to be rare in all habitats, as reflected in the low frequency of records (Santos et al., 2004; Kasper et al., 2007; Martínez et al., 2008; Andrade-Núñez & Aide, 2010).

The species is listed by International Union for Conservation of Nature as Least Concern (Reid & Helgen, 2008), considering its wide distribution and no apparent major threats, in spite of the minimal natural history information, imprecise known distribution, and unknown population size (Reid & Helgen, 2008; Butchart & Bird, 2010). In fact, many species with poor baseline data may be facing similar conservation threats, increasing the urgency to generate specific and updated information(see discussions in Diamond, 1987).

Hence, characterizing the geographic distribution of a species quantitatively and in detail is essential for guiding and planning conservation efforts (Margules & Pressey, 2000). Rigorous distribution maps can be generated from ecological niche models using fragmentary available occurrence data from specimen records, observations, or reports in the literature (Siqueira et al., 2009), appropriately set in the context of accessibility of areas to the species in question (Barve et al., 2011). Such maps can be used for identification of areas for long-term protection, and even priority sites for reintroductions (Margules & Pressey, 2000; Martínez-Meyer et al., 2006). In this contribution, we explore existing distributional knowledge of G. cuja to determine gaps, and generate a detailed map of potential and known distributional areas.

MATERIALS AND METHODS

Literature review. In January-July 2013, we used the key words "Galictis AND cuja" to find published articles on three electronic databases: Thomson Institute for Scientific Information (ISI; www.isiknowledge.com) and PubMed (http://www.ncbi.nlm.nih.gov) as they provide access to the most comprehensive databases of citations, and the Scientific Electronic Library Online (SciELO, http://www.scielo.org), for its focus on articles from South America. For the latter, we used an algorithm proposed by Curioso (2008) to improve the search. We removed articles where G. cuja was mentioned only in references but not in text, and then selected articles were classified as specific articles (i.e., articles where G. cuja was the target species of research) versus non-specific articles (i.e., articles where G. cuja was not the focus, such as baseline studies and general mammal censuses).

Potential distribution map. To establish the potential distribution of G. cuja, we generated an ecological niche model following established approaches (Peterson et al., 2011). Definition of the study area extent is crucial to accurate ecological niche models, and must be based on the dispersal ability of the species (Barve et al., 2011). Currently, no standard methodology exists that can be applied in diverse situations, but the general concept has been outlined (Barve et al., 2011). Considering current gaps of knowledge of the distribution and home range of this species, we calculated the approximate mean distance between all peripheral occurrence points and the centroid of known occurrences (Fig. 1). This distance was used to create a buffer around occurrence points, we used this area as a hypothesis of the accessible area for the species (Fig. 1).

Considering the broad known range of the species (Yensen & Tarifa, 2003; Bornholdt et al., 2013), we used climatic variables (0.16º resolution; Hijmans et al., 2005) as a source of useful environmental information for niche modeling (Peterson et al., 2011). Variables used were annual mean temperature, mean diurnal range, isothermality, temperature seasonality, maximum temperature of warmest month, minimal temperature of coldest month, temperature annual range, mean temperature of warmest quarter, mean temperature of coldest quarter, annual precipitation, precipitation of wettest month, precipitation of driest month, precipitation seasonality, precipitation of wettest quarter, and precipitation of driest quarter (Hijmans et al., 2005). We performed a principal components analysis (PCA) to reduce intervariable correlations and overall numbers of environmental variables (Peterson et al., 2011).

Occurrence data were drawn from two main sources: (i) data associated with natural history museum specimens and reported in VertNet (http://vertnet.org), Arctos (http://arctos.database.museum/home.cfm), and GBIF (http://data.gbif.org/welcome.htm); see Acknowledgments for full list of institutions; and (ii) coordinates reported in scientific articles on G. cuja occurrences that were documented with museum specimens (Prevosti & Travaini, 2005; Carrera et al., 2012; Bornholdt et al., 2013). Bornhodlt et al. (2013) did not derive from our systematic literature search, but was included because it provides an exhaustive taxonomic review of G. cuja, listing corroborated specimens. Occurrences were resampled to one per pixel on our environmental grids to avoid duplicating records.

Coordinates were divided in two groups for calibration and evaluation, based on four quadrants with similar numbers of points, using two quadrants for calibration and two for evaluation (Fig. 2). Model results were evaluated for predictive ability using a cumulative binomial test, considering proportional area predicted and numbers of evaluation points predicted correctly (Arboleda et al., 2009; Peterson et al., 2011). After evaluating models prediction, a final model was developed using all occurrences.

We used the software Maxent, version 3.3.3.k, to model the species’ ecological niche, based on associations between known presences and environmental conditions (Phillips et al., 2006). Specific settings were 1000 bootstrap replicates, random seed, and median of replicates (logistic) as output. Input data and model outputs were managed using ArcGIS version 9.3 (ESRI, Redlands, California, USA).

Considering that our data were of diverse provenance, an error tolerance of E = 5% was used to produce the binary map (Peterson et al., 2011). We visualized occurrences in environmental space by plotting temperature (ºC) against precipitation (mm) for presences and the broader background across the accessible area; to characterize the background, we generated 3000 random points across the study area.

RESULTS

Overall, we obtained 84 articles from SciELO, 24 from ISI, and 8 from PubMed, totaling 116 articles. Eliminating articles in which G. cuja was only mentioned in references, and removing duplicate publications, 89 articles remained. We found 13 articles (14.6%) that had G. cuja as a focus. Number and type of articles (specific or nonspecific to G. cuja) differed among countries, being Brazil producing most articles (41). Within specific articles, six articles were on diet, five on parasites or pathogens, and two documented species occurrences. The first article we found was published in 1969, followed by a gap between 1970 and 1989; then, a concentration of publications emerged between 2004 and 2013, averaging ~4 articles per year.

In our modeling exercise, the first 12 principal components (explaining >99.9% of total variance) were used as environmental variables. We found 354 occurrences of G. cuja; eliminating duplicates and resampling to pixel size of climatic layers, 201 unique occurrences remained. Model evaluation indicated significant predictive power to anticipate suitability in independent evaluation areas (p < 0.001; Fig. 2).

The final ecological niche model showed suitable areas in Ecuador (small areas in southern Guayas), Peru (southern Puno and northeastern Arequipa), eastern Brazil (fragmented, between Paraiba and Rio Grande do Sul), central and southern Bolivia (between Santa Cruz and Tarija), eastern Paraguay (between Concepcion and Itapua), Uruguay, much of Argentina (from Salta to Santa Cruz, including eastern states), and Chile (Coquimbo to Aysen; Fig. 3). Visualizations in environmental space showed broad use of precipitation and temperature combinations by the species, ranging 1.9-27.4 ºC of temperature and 83-3883 mm of precipitation (Fig. 4).

DISCUSSION

We noted a striking lack of research on G. cuja in some countries, with a total of three articles from all of Chile, Uruguay, Bolivia, Peru, and Paraguay. According to our model, Uruguay, Chile, and Argentina all hold broad distributional areas for the species, yet the species has gone unstudied (Fig. 3). Of the 89 articles, only 13 (14.6%) had G. cuja as target species, and were focused mainly on diet (Ebensperger et al., 1991; Diuk-Wasser & Cassini, 1998; Delibes et al., 2003; Kraus & Rödel, 2004; Zapata et al., 2007; Sade et al., 2012). Diet studies were based on prey identification in scat, and concentrated in the southern part of the distribution of G. cuja, where the most common prey items were rabbits (Oryctolagus cuniculus Linnaeus, 1758) and hares (Lepus europaeus Pallas, 1778), emphasizing the species’ potential role in controlling invasive species (Delibes et al., 2003; Zapata et al., 2007). Scat identification in all studies was based on morphological characteristics of feces and disposal sites (latrines, burrows), but none used additional tools (e.g., molecular typing) to confirm scat identity, a weakness because G. cuja may coexist with other terrestrial mustelids like Lyncodon patagonicus de Blainville, 1842 and Neovison vison Schreber, 1777 (Previtali et al., 1998). Another difficulty in diet studies is that G. cuja builds latrines, often with contribution of scats by several individuals (Delibes et al., 2003), impeding study of individual diets. These difficulties can be addressed by collection of fresh scats and use of camera traps and molecular analysis (Farrell et al., 2000), or via studies based on stomach contents of carcasses, considering the relatively frequent cases of road kills of the species (Pfeifer et al., 2008; Cáceres et al., 2010).

The second most frequent topic was pathogens and parasites (Ferriolli & Barretto, 1969; Barros et al., 1990; Vieira et al., 2012; Zabott et al., 2012; Megid et al., 2013). Most of these articles were based on necropsy findings (Barros et al., 1990; Vieira et al., 2012; Zabott et al., 2012; Megid et al., 2013). One of the organisms studied was the zoonotic giant kidney worm Dioctophyma renale (Barros et al., 1990; Zabott et al., 2012), which appears to be hosted in South America by native species G. cuja and G. vittata, and eventually by the exotic N. vison (Measures, 2001). Also, a domestic dog strain of Canine Distemper virus (CDV) was detected in one individual (Megid et al., 2013). These finding could be of conservation concern because CDV has been related with high mortality rates in mustelids, and can be transmitted by free-ranging dogs, an increasing issue in some South American countries (Acosta-Jamett et al., 2011; Megid et al., 2013). We did not find specific studies on threats to G. cuja, such as land use change, human encroachment, or invasive species. No articles concerning the species’ abundance or populations were found.

Previous range maps of G. cuja may be underestimating the species distributional potential in some areas. As an example, previous estimates of the species’ distributional area in Chile were 252,300 km² (Cofré & Marquet, 1999), while our model estimated >310,000 km². We reviewed three previous distribution maps for G. cuja. The smallest was from IUCN (Reid & Helgen, 2008), while Prevosti & Travaini (2005) and Yensen & Tarifa (2003) presented broader distribution maps, the former including occurrences in southern South America, based on skin and skeletal remains. Our map anticipated the potential for these southern occurrences, validating the southern range limit of the species proposed by Prevosti & Travaini (2005; Fig. 3).

Finally, to improve G. cuja conservation, further research should address movement patterns, phylogeography, and emerging threats such as effects of invasive species, to understand critical aspects of its ecology that are not presently well understood. Exploration of these topics would offer a robust baseline by which to identify and monitor current status of and emerging threats for the species.

Acknowledgements. Occurrence data were obtained from Administracion de Parques Nacionales, Argentina; Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Argentina; American Museum of Natural History, USA; Los Angeles County Museum of Natural History, USA; Louisiana State University Museum of Natural Science, USA; Michigan State University Museum, USA; Museum of Vertebrate Zoology, USA; University of Michigan Museum of Zoology, USA; Field Museum of Natural History, USA; Yale University Peabody Museum, USA; and Royal Belgian Institute of Natural Sciences, Belgium. Universidad Andres Bello provided an Initiation Grant (DI-04-11/I) and a Regular Grant (DI-49-11/R); Ministerio del Medio Ambiente de Chile provided a grant from the Fondo de Proteccion Ambiental (RMI-001-2012).

Received 17 February 2014.

Accepted 23 July 2014.

• Acosta-Jamett, G.; Chalmers, W. S. K.; Cunningham, A. A.; Cleaveland, S.; Handel, I. G. & Bronsvoort, B. M. de C. 2011. Urban domestic dog populations as a source of canine distemper virus for wild carnivores in the Coquimbo region of Chile. Veterinary Microbiology 152:247-257.
• Andrade-Núńez, M. J. & Aide, A. T. 2010. Effects of habitat and landscape characteristics on medium and large mammal species richness and composition in northern Uruguay. Zoologia 27:909-917.
• Arboleda, S.; Jaramillo-O, N. & Peterson, A. T. 2009. Mapping environmental dimensions of dengue fever transmission risk in the Aburrá Valley, Colombia. International Journal of Environmental Research and Public Health 6:3040-3055.
• Barros, D. M.; Lorini, M. L. & Persson, V. G. 1990. Dioctophymosis in the Little Grison (Galictis cuja). Journal of Wildlife Diseases 26:538-539.
• Barve, N.; Barve, V.; Jiménez-Valverde, A.; Lira-Noriega, A.; Maher, S.P.; Peterson, A. T.; Soberón, J. & Villalobos, F. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222:1810-1819.
• Bornholdt, R.; Helgen, K.; Koepfli, K. P.; Oliveira, L.; Lucherini, M. & Eizirik, E. 2013. Taxonomic revision of the genus Galictis (Carnivora: Mustelidae): Species delimitation, morphological diagnosis, and refined mapping of geographical distribution. Zoological Journal of the Linnean Society 167:449-472.
• Butchart , S. H. M. & Bird, J. P. 2010. Data deficient birds on the IUCN Red List: What dont we know and why does it matter? Biological Conservation 143:239-247.
• Cáceres, N. C.; Hannibal, W.; Freitas, D. R.; Silva, E. L.; Roman, C. & Casella, J. 2010. Mammal occurrence and roadkill in two adjacent ecoregions (Atlantic forest and Cerrado) in south-western Brazil. Zoologia 27:709-717.
• Carrera, M.; Nabte, M. J. & Udrizar-Sauthier, D. E. 2012. Distribución geográfica, historia natural y conservación del hurón menor Galictis cuja (Carnivora: Mustelidae) en la Patagonia Central, Argentina. Revista Mexicana de Biodiversidad 83:1252-1257.
• Cofré, H. & Marquet, P. A. 1999. Conservation status, rarity, and geographic priorities for conservation of Chilean mammals: An assessment. Biological Conservation 88:53-68.
• Curioso, W. H. 2008. Una estrategia simple para mejorar la búsqueda de artículos indexados en SciELO. Revista Médica de Chile 136:812-814.
• Delibes, M.; Travaini, A.; Zapata, S. C. & Palomares, F. 2003. Alien mammals and the trophic position of the lesser grison (Galictis cuja) in Argentinean Patagonia. Canadian Journal of Zoology 81:157-162.
• Diamond, J. 1987. Extant unless proven extinct? Or, extinct unless proven extant? Conservation Biology 1:77-79.
• Diuk-Wasser, M. A. & Cassini, M. H. 1998. A study on the diet of minor grisons and a preliminary analysis of their role in the control of rabbits in Patagonia. Studies on Neotropical Fauna and Environment 33:3-6.
• Ebensperger, L. A.; Mella, J. E. & Simonetti, J. A. 1991. Trophic-niche relationships among Galictis cuja, Dusicyon culpaeus, and Tyto alba in central Chile. Journal of Mammalogy 72:820-823.
• Farrell, L. E.; Roman, J. & Sunquist, M. E. 2000. Dietary separation of sympatric carnivores identified by molecular analysis of scats. Molecular Ecology 9:1583-1590.
• Ferriolli, F. & Barretto, M. P. 1969. Disease reservoirs and wild vectors of Trypanosoma cruzi. Natural infection of the ferret Galictis cuja furax (Thomas, 1907) caused by T. cruzi. Revista do Instituto de Medicina Tropical de São Paulo 11:264-273.
• Hijmans, R. J.; Cameron, S. E.; Parra, J. L.; Jones, P. G. & Jarvis, A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965-1978.
• Kasper, C. B.; Mazim, F. D.; Soares, J. B. G.; de Oliveira, T. G. & Fabián, M. E. 2007. Composição e abundância relativa dos mamíferos de médio e grande porte no Parque Estadual do Turvo, Rio Grande do Sul, Brasil. Revista Brasileira de Zoología 24:1087-1100.
• Kraus, C. & Rödel, H. 2004. Where have all the cavies gone? Causes and consequences of predation by the minor grison on a wild cavy population. Oikos 105:489-500.
• Margules, C. R. & Pressey, R. L. 2000. Systematic conservation planning. Nature 405:243-253.
• Martínez, O.; Rechberger, J.; Vedia-Kennedy, J. & Mesili, T. 2008. Mamíferos medianos y grandes de la Serranía del Aguaragüe, Tarija (Bolivia). Mastozoologia Neotropical 15:335-348.
• Martínez-Meyer, E.; Peterson, A. T.; Servin, J. I. & Kiff, L. F. 2006. Ecological niche modelling and prioritizing areas for species reintroductions. Oryx 40:411-418.
• Measures, L. N. 2001. Dioctophymatosis. In: Samuel, W. M. ; Pybus, M. J. & Kocan, A. A. eds. Parasitic Diseases of Wild Mammals Iowa,University Press. p. 357-364.
• Megid, J.; Teixeira, C. R.; Cortez, A.; Heinemann, M. B.; Antunes, J. M. A. P.; Fornazari, F.; Rassy, F. B. & Richtzenhain, L. J. 2013. Canine Distemper Virus infection in a lesser grison (Galictis cuja): First report and virus phylogeny. Pesquisa Veterinária Brasileira 33:247-250.
• Nabte, M. J.; Saba, S. L. & Monjeau, A. 2009. Mamíferos terrestres de la Península de Valdés: Lista sistemática comentada. Mastozoologia Neotropical 16:109-120.
• Peterson, A. T.; Soberón, J.; Pearson, R. G.; Anderson, R. P.; Martinez-Meyer, E.; Nakamura, M. & Araújo, M. B. 2011. Ecological Niches and Geographic Distributions New Jersey, Princeton University Press. 328p.
• Pfeifer, I.; Kindel, A. & Pfeifer, A. V. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. European Journal of Wildlife Research 54:689-699.
• Phillips, S. J.; Anderson, R. P. & Schapire, R. E. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190:231-259.
• Previtali, A.; Cassini, M. H. & Macdonald, D. W. 1998. Habitat use and diet of the American Mink (Mustela vison) in Argentinian Patagonia. Journal of Zoology 246:482-486.
• Prevosti, F. J. & Travaini, A. 2005. New records of Galictis cuja (Molina, 1782) (Carnivora, Mustelidae) in southern Patagonia. Mammalian Biology 70:317-320.
• Redford, K. & Eisenberg, J. 1992. Order Carnivora. In: Redford, K. & Eisenberg, J. eds. Mammals of the Neotropics. The Southern Cone: Chile, Argentina, Uruguay, Paraguay Illinois, The University of Chicago Press. p. 144-252.
• Reid, F. & Helgen, K. 2008. Galictis cuja, IUCN Red List of Threatened Species. Version 2013.1 Available at: <www.iucnredlist.org>. Accessed on: 11 November 2013.
• Rocha-Mendes, F.; Mikich, S. B.; Quadros, J. & Wagner, A. P. 2010. Feeding ecology of carnivores (Mammalia, Carnivora) in Atlantic Forest remnants, southern Brazil. Biota Neotropica 10:21-20.
• Sade, S.; Rau, J. R. & Orellana, J. I. 2012. Dieta del quique (Galictis cuja, Molina 1782) en un remanente de bosque Valdiviano fragmentado del sur de Chile. Gayana 76:112-116.
• Santos, M. F. M. dos; Pellanda, M.; Tomazzoni, A. C.; Hasenack, H. & Hartz, S. M. 2004. Mamíferos carnívoros e sua relação com a diversidade de hábitats no Parque Nacional dos Aparados da Serra, Sul do Brasil. Iheringia, Serie Zoologia 94:235-245.
• Siqueira, M. F. D.; Durigan, G.; de Marco Júnior, P. & Peterson, A. T. 2009. Something from nothing: Using landscape similarity and ecological niche modeling to find rare plant species. Journal for Nature Conservation 17:25-32.
• Vieira, F.; Muniz-Pereira, L. C.; de Souza Lima, S.; Moraes Neto, A. H. A.; Goncalves, P. R. & Luque, J. L. 2012. Crenosoma brasiliense sp. n. (Nematoda: Metastrongyloidea) parasitic in lesser grison, Galictis cuja (Molina, 1782) (Carnivora, Mustelidae) from Brazil, with a key to species of Crenosoma Molin, 1861. Folia Parasitologica 59:187-194.
• Yensen, E. & Tarifa, T. 2003. Galictis cuja. Mammalian Species 728:1-8.
• Zabott, M. V.; Pinto, S. B.; Viott, A. M.; Tostes, R. A.; Bittencourt, L. H. F. B.; Konell, A. L. & Gruchouskei, L. 2012. Ocorrência de Dioctophyma renale em Galictis cuja. Pesquisa Veterinária Brasileira 32:786-788.
• Zapata, S. C.; Travaini, A.; Delibes, M. & Martínez-Peck, R. 2007. Annual food habits of the lesser grison (Galictis cuja) at the southern limit of its range. Mammalia 69:85-88.
• Zúńiga, A.; Muńoz-Pedreros, A. & Fierro, A. 2009. Uso de hábitat de cuatro carnívoros terrestres en el sur de Chile. Gayana 73:200-210.

Publication Dates

• Publication in this collection
  13 Nov 2014
• Date of issue
  Sept 2014

History

• Accepted
  23 July 2014
• Received
  17 Feb 2014