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First record of melanism in the critically endangered Pampa cat (Leopardus munoai), an endemic species of the Pampa grasslands

Primeiro registro de melanismo no criticamente ameaçado gato-pampeano (Leopardus munoai), uma espécie endêmica das áreas abertas do Pampa

Abstract

We report the first record of a melanistic individual of the critically endangered Pampa cat (Leopardus munoai), from July 8th, 2021, at 10:45 am (coordinates 30.096288° S; 54.941139° W) in the area of the Brazilian army, known as Campo de Instrução Barão de São Borja (CIBSB), popularly known as Saicã.

Keywords
Melanism; Uruguayan Pampas cat; Pampa

Resumo:

Este trabalho reporta o primeiro registro de melanismo do criticamente ameaçado de extinção gato-pampeano (Leopardus munoai), realizado em 8 de julho de 2021, às 10:45 da manhã. O registro foi obtido nas coordenadas 30.096288° S; 54.941139° W na área do exército brasileiro Campo de Instrução Barão de São Borja (CIBSB), popularmente conhecida como Saicã.

Palavras-chave
Melanismo; gato-palheiro-pampeano; Pampa

Introduction

Polymorphic phenotypes are common in wild cats, with records of albinism, leucism and melanism in several species of felids from Africa, South America and Asia (Eizirik et al. 2003EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453., Warrick 2010WARRICK, D.M. 2010. Inbreeding depression in captive white tigers: Methods for purifying tiger lineages. Zoos Print 15, 1–9., McBride & Giordano 2010McBRIDE, R.T. & GIORDANO, A.J. 2010. First record of a white ocelot (Leopardus pardalis). The Southwestern Naturalist. 55, 567–568., Schneider et al. 2012SCHNEIDER, A., DAVID, V.A., JOHNSON, W.E., O’BRIEN, S.J., BARSH, G.S., MAYMOND, M.M. & EIZIRIK, E. 2012. How the leopard hides its spots: ASIP mutations and melanism in wild cats. Plos One 7, e50386, Silva 2017SILVA, L.G. 2017. Ecology and evolution of melanism in big cats: Case study with black leopards and jaguars. In Big Cats. Shrivastav A. B. (Ed.). InTech Open, pp. 93–110., Cho et al. 2013CHO, Y.S., HU, L., HOU, H., LEE, H., XU, J., KWON, S., OH, S., KIM, H.M., JHO, S., KIM, S., SHIN, Y.A., KIM, B.C., KIM, H., KIM, CHANG-UK, LUO, S.J., JOHNSON, W.E., KÖPFLI, K.-P., SMIDT-KÜNTZEL, A., TURNER, J.A., MARKER, L., HARPER, C., MILLER, S.M., JACOBS, W., BERTOLA, L.D., KIM, T.H., LEE, S., ZHOU, Q., JUNG, H.J., XU, X., GADHVI, P., XU, P., XIONG, Y., LUO, Y., PAN, S., GOU, C., CHU, X., ZHANG, J., LIU, S., HE, J., CHEN, Y., YANG, L., YANG, Y., HE, J., LIU, S., WANG, J., KIM, C.H., KWAK, H., KIM, J.-S., HWANG, S., KO, J., KIM, C.-B., KIM, S., BAYARLKHAGVA, D., PAEK, W.K., KIM, S.-J., O’BRIEN, S.J., WANG, J. & BHAK, J. 2013. The tiger genome and comparative analysis with lion and snow leopard genomes. Nat. Commun. 2433, 1–7., Xu et al. 2013XU, X., DONG, G.X., HU, X.S., MIAO, L., ZHANG, X., ZHANG, D.L., YANG, H.D., ZHANG, T.Y., ZOU, Z.T., ZHANG, T.T., ZHUANG, Y., BHAK, J., CHO, Y.S., DAI, W.T., JIANG, T.J., XIE, C., LI, R. & LUO, S.J. 2013. The genetic basis of white tigers. Curr. Biol. 23, 1031–1035., Cronemberger et al. 2018CRONEMBERGER, C., PEREIRA, F.A., BACELLAR, A.E.F. & SILVA, L.G. 2018. First record of leucism in puma from Serra dos Órgãos National Park, Brazil. Cat News 68, 38–41.). Melanism can be defined as the darkening of the background coloration of the integument (fur), which is genetically controlled. So far, all felid polymorphic mutations have been associated with either the ASIP (agouti signaling protein) or MC1R genes (Eizirik et al. 2003EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453.). There are some iconic cases of melanism such as in leopards (Panthera pardus) and jaguars (Panthera onca), which are called ‘black panthers’ (Eizirik et al. 2003EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453., Schneider et al. 2012SCHNEIDER, A., DAVID, V.A., JOHNSON, W.E., O’BRIEN, S.J., BARSH, G.S., MAYMOND, M.M. & EIZIRIK, E. 2012. How the leopard hides its spots: ASIP mutations and melanism in wild cats. Plos One 7, e50386, Silva 2017, Silva et al. 2017SILVA, L.G., KAWANISHI, K., HENSCHEL, P., KITTLE, A., SANEI, A., REEBIN, A., MIQUELLE, D., STEIN, A.B., WATSON, A., KEKULE, L.B., MACHADO, R.B. & EIZIRIK, E. 2017. Mapping black panthers: Macro ecological modeling of melanism in leopards (Panthera pardus). Plos One 12, e0170378.). In Neotropical America, melanism is also frequently observed in small cats (Oliveira 1994OLIVEIRA, T.G. 1994. Neotropical Cats: Ecology and Conservation. São Luís: EDUFMA, 220 p., Eizirik et al. 2003EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453., Oliveira & Cassaro 2005OLIVEIRA, T.G. & CASSARO, C. 2005. Guia de Campo dos Felinos do Brasil. São Paulo. Instituto Pró-Carnívoros/Fundação Parque Zoológico de São Paulo/Sociedade de Zoológicos do Brasil. 80p., Silva et al. 2016SILVA, L.G., DE OLIVEIRA, T.G., KASPER, C.B., CHEREM, J.J., MORAES JR, E.A., PAVIOLO, A. & EIZIRIK, E. 2016. Biogeography of polymorphic phenotypes: Mapping and ecological modelling of coat colour variants in an elusive Neotropical cat, the jaguarundi (Puma yagouaroundi). Journal of Zoology 299, 295–303., Aximoff et al. 2021AXIMOFF, I., SALES, D., PAINKOW, E., BARQUERO, G., ROSA, C. & CARAVAGGI, A. 2021. Melanism in the Brazilian pampas cat and range extension in the Atlantic Forest, Brazil. Cat News 74, 29–32.). In some cases, as in the jaguar, it is dominant, whereas in leopards it is recessive (Eizirik et al. 2003EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453., Caro 2005CARO, T. 2005. The Adaptive Significance of Coloration in Mammals. BioScience 55, 125–136.). In this short communication, we report the first record of melanism in the Pampa cat (Leopardus munoai), an endemic species of the Pampa biome, and a small felid from the “Leopardus colocola complex”, that has recently been recognized as a full species by Nascimento et al. (2020NASCIMENTO, F.O., CHENG, J. & FEIJÓ, A. 2020. Taxonomic revision of the pampas cat Leopardus colocola complex (Carnivora: Felidae): an integrative approach Zoological Journal of the Linnean Society, XX, 1–37.).

The Pampa cat or grassland Pampas cat, also known as Uruguayan or Muñoa’s Pampas cat, is a small felid that measures between 70 and 96 centimeters in length, and weighs an average of 3.5 kg; however, its basic ecological needs are virtually unknown. Its distribution to the north of its range would be restricted by the forest massif of the Atlantic Forest, to the south and southwest by the Prata and Paraná Rivers, respectively, and to the east by the Atlantic Ocean (Nascimento et al. 2020NASCIMENTO, F.O., CHENG, J. & FEIJÓ, A. 2020. Taxonomic revision of the pampas cat Leopardus colocola complex (Carnivora: Felidae): an integrative approach Zoological Journal of the Linnean Society, XX, 1–37.). Thus, the species’ range is restricted to the extreme south of Brazil (Pampa biome), Uruguay and a small strip of the Corrientes fields in the extreme northeast of Argentina. The part of the Pampa biome that spreads into the Brazilian territory measures approximately 178,000 km2, which corresponds to 2.07% of the country as a whole, and is restricted to the state of Rio Grande do Sul. By making up 63% of the territory of the state, it is the dominant landscape (IBGE 2004IBGE - Instituto Brasileiro de Geografia e Estatística. 2004. Mapa da vegetação do Brasil e Mapa de Biomas do Brasil. Retrieved from https://ww2.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm#sub_download.
https://ww2.ibge.gov.br/home/presidencia...
, Overbeck et al. 2007OVERBECK, G.E., MÜLLER, S.C., FIDELIS, A., PFADENHAUER, J., PILLAR, V.D., BLANCO, C., BOLDRINI II BOTH R. & FORNECK E. 2007. Brazil’s neglected biome: The South Brazilian Campos. Perspect Plant Ecol Evol Syst 9:101–116.). As a species, L. munoai is of high conservation concern (see Tirelli et al. 2021TIRELLI, F.P., TRIGO, T.C., QUEIROLO, D., KASPER, C.B., BOU, N., PETERS, F., MAZIM, F.D., MARTÍNEZ-LANFRANCO, J.A., GONZALEZ, E.M., ESPINOSA, C., FAVARINI, M., SILVA, L.G., MACDONALD, D.W., LUCHERINI, M. & EIZIRIK, E. 2021. High extinction risk and limited habitat connectivity of Muñoa’s pampas cat, an endemic felid of the Uruguayan Savanna ecoregion. Journal for Nature Conservation 62 (2021) 126009.) and is going to be classified as Critically Endangered CR by the Brazilian authorities; however, this status has not been made official yet, and it is currently still classified under Leopardus colocola (as L.c. munoai) as Vulnerable (Queirolo et al. 2013QUEIROLO, D., DE ALMEIDA, L.B., BEISIEGEL, B.M. & DE OLIVEIRA, T.G. 2013. Avaliação do risco de extinção do gato-palheiro Leopardus colocolo (Molina, 1782) no Brasil. Biodiversidade Brasileira 3, 91–98. https://doi.org/10.37002/biobrasil.v%25vi%25i.375
https://doi.org/10.37002/biobrasil.v%25v...
, ICMBio unp. data). In this paper our intent is to report a new color morph identified for the Pampa cat (Leopardus munoai).

Materials and Methods

Camera trapping is being conducted in a public area belonging to the Brazilian army, known as Campo de Instrução Barão de São Borja (CIBSB), or popularly known as Saicã (Fig. 1), which covers 51,000 hectares, and is located between the municipalities of Rosario do Sul and Cacequi, in the state of Rio Grande do Sul, southernmost Brazil. The area comprises mostly native fields, with forest formations along water courses, adjacent to agriculture. In 2021, we deployed 6–9 camera traps spaced at ca. 500 m (400–600 m) from each other that focused on native fields that have been free from agriculture for at least 40 years. We followed well established camera-trapping protocols (as those described by de Oliveira et al. 2018DE OLIVEIRA, T.G., MICHALSKI, F., BOTELHO, A., MICHALSKI, L., CALOURO, A. & DESBIEZ, A. 2018. How rare is rare? Quantifying and assessing the rarity of the bush dog Speothos venaticus across the Amazon and other biomes. Oryx. 52, 98–107. https://doi.org/10.1017/S0030605316000624.
https://doi.org/https://doi.org/10.1017/...
, 2020DE OLIVEIRA, T.G., LIMA, B.C., FOX-ROSALES, L., PEREIRA, R.S., PONTES-ARAÚJO, E. & DE SOUSA, A.L. (2020). A refined population and conservation assessment of the elusive and endangered northern tiger cat (Leopardus tigrinus) in its key worldwide conservation area in Brazil. GECCO 22: e00927. https://doi.org/10.1016/j.gecco.2020.e00927.
https://doi.org/https://doi.org/10.1016/...
).

Figure 1.
Location where the melanistic male specimen was recorded.

Species identification was confirmed based on the concave head profile shown by both L. munoai and its sister species from the Cerrado, Leopardus braccatus. This is a diagnostic feature for identification of both species during camera-trapping (T.G. de Oliveira, pers. obs., F.D. Mazim pers. obs.). The ears are more pointed than the spotted species of Leopardus, which would also set it apart from a melanistic Geoffroy’s cat, aside the bulkier body of the latter (T.G. de Oliveira, pers. obs., F.D. Mazim pers. obs.). Body shape and proportions are also used to distinguish them among the species (Oliveira & Cassaro 2005OLIVEIRA, T.G. & CASSARO, C. 2005. Guia de Campo dos Felinos do Brasil. São Paulo. Instituto Pró-Carnívoros/Fundação Parque Zoológico de São Paulo/Sociedade de Zoológicos do Brasil. 80p.). Additionally, the researchers (TGO, FDM) have a vast experience with camera-trapping of small Neotropical felids (>5,000 records identified), live-trapping (>200 individuals caught) as well as experience with several specimens of all Brazilian small cats in captivity.

Results and Discussion

After an effort of 1,080 trap-nights, a melanistic male Muñoa’s Pampas cat was photo-trapped on July 8th, 2021, at 10:45 am (coordinates 30.096288° S; 54.941139° W) on the edge of a swamp, locally known as Laguna, which, in the 1970s, was intensively used to irrigate rice fields; a practice that no longer occurs within the limits of the CIBSB (Fig. 2). Another individual, with a plain, standard coat had been recorded earlier in the same area (May 27th 2021).

Figure 2.
Melanistic male Pampa cat (Leopardus munoai) caught by camera-trap in the Pampa grasslands of Saicã (southernmost Brazil).

This is the first report of a melanistic L. munoai individual. However, melanism in the Pampas cat species complex (i.e., Leopardus colocola complex) has been recorded, mostly in the Pampas cats (Leopardus braccatus) found in the savannas of northern and central-western Brazil (Aximoff et al. 2021AXIMOFF, I., SALES, D., PAINKOW, E., BARQUERO, G., ROSA, C. & CARAVAGGI, A. 2021. Melanism in the Brazilian pampas cat and range extension in the Atlantic Forest, Brazil. Cat News 74, 29–32., T. de Oliveira pers. com.). In some sites, such as Mirador State Park in the savannas of Maranhão state, melanistic individuals can comprise up to > 90% of all records (T. de Oliveira pers. com.). However, we still cannot confirm whether melanism is a common event for L. munoai; but, based on records of road-killed individuals (N = 28, F. Mazim pers. obs.), it does not seem to be so. There is still a lot to be learned about this endemic felid of the Pampas.

Acknowledgments

Our deepest gratitude to the Brazilian Army’s Comando Maior do Sul, for the logistic support and permission to access their Saicã site. This study was supported by Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS) – Funding code:19/2551–0001842–8.

Data Availability

All data are available in the paper.

REFERENCES

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  • DE OLIVEIRA, T.G., LIMA, B.C., FOX-ROSALES, L., PEREIRA, R.S., PONTES-ARAÚJO, E. & DE SOUSA, A.L. (2020). A refined population and conservation assessment of the elusive and endangered northern tiger cat (Leopardus tigrinus) in its key worldwide conservation area in Brazil. GECCO 22: e00927. https://doi.org/10.1016/j.gecco.2020.e00927.
    » https://doi.org/https://doi.org/10.1016/j.gecco.2020.e00927
  • DE OLIVEIRA, T.G., MICHALSKI, F., BOTELHO, A., MICHALSKI, L., CALOURO, A. & DESBIEZ, A. 2018. How rare is rare? Quantifying and assessing the rarity of the bush dog Speothos venaticus across the Amazon and other biomes. Oryx. 52, 98–107. https://doi.org/10.1017/S0030605316000624.
    » https://doi.org/https://doi.org/10.1017/S0030605316000624
  • EIZIRIK, E., YUHKI, N., JOHNSON, W.E., RAYMOND, M., HANNAH, S.S. & O’BRIEN, S.J. 2003. Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448–453.
  • IBGE - Instituto Brasileiro de Geografia e Estatística. 2004. Mapa da vegetação do Brasil e Mapa de Biomas do Brasil. Retrieved from https://ww2.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm#sub_download
    » https://ww2.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm#sub_download
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  • TIRELLI, F.P., TRIGO, T.C., QUEIROLO, D., KASPER, C.B., BOU, N., PETERS, F., MAZIM, F.D., MARTÍNEZ-LANFRANCO, J.A., GONZALEZ, E.M., ESPINOSA, C., FAVARINI, M., SILVA, L.G., MACDONALD, D.W., LUCHERINI, M. & EIZIRIK, E. 2021. High extinction risk and limited habitat connectivity of Muñoa’s pampas cat, an endemic felid of the Uruguayan Savanna ecoregion. Journal for Nature Conservation 62 (2021) 126009.
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Edited by

Associate Editor Diego Astúa

Publication Dates

  • Publication in this collection
    28 July 2023
  • Date of issue
    2023

History

  • Received
    16 Dec 2022
  • Accepted
    26 June 2023
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