THERYA NOTES 2020, Vol. 1 (1): 62-66 DOI: 10.12933/therya_notes-20-15

First records of leucism in small rodents for Argentina

Primeros registros de leucismo en pequeños roedores para Argentina

Veronica A. Beninato1*, Gustavo A. Rivero-Castro 1, Mauricio A. Pérez1, Carlos E. Borghi 1,2, and Stella M. Giannoni 1,2,3

1CIGEOBIO (Centro de Investigaciones de la Geósfera y Biósfera), CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Universidad Nacional de San Juan. Av. I. de la Roza 590 (O), CP. J5402DCS, Rivadavia, San Juan, Argentina. Email: vbeninato@unsj-cuim.edu.ar (VAB), riverogustavo90@gmail.com (GAR-C), elcodorniz81@gmail.com (MAP), cborghi@unsj-cuim.edu.ar (CEB), sgiannoni@unsj-cuim.edu.ar (SMG).

2Departamento de Biología, Facultad Ciencias Exactas, Físicas y Naturales, Universidad Nacional de San Juan. Av. I. de la Roza 590 (O), CP. J5402DCS, Rivadavia, San Juan, Argentina.

3Instituto y Museo de Ciencias Naturales, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de San Juan. Av. España 400 (N), CP. 5400, San Juan, Argentina.

* Corresponding author

Leucism appears in various groups of vertebrates, although it is rare in mammals. For Argentina, we do not know of any documented registry for small rodents. The objective of our work is to report the first cases of leucism in cricetid rodents in the Puna Desert of Argentina. Field work was carried out in the Multiple Use Provincial Reserve Don Carmelo (San Juan, Argentina), located in the Puna Desert. The animals were captured in 9 grids formed by 36 Sherman-type traps, established in plots located between 3.100 and 3.300 m, in the years 2013-2014. We recorded 6 cases of leucism in 3 species of cricetids: Eligmodontia sp. (n = 3), Abrothrix andina (n = 2), and Phyllotis xanthopygus (n = 1). This work represents the first report of cases of leucism in small mammals from Argentina. The cases in the studied population could be due to the low gene flow imposed by the high environmental severity of an extreme desert, probably related to genetic causes derived from climatic and ecological factors, as these are non-anthropized environments.

Key words: Cricetids; leucism; pigment disorder; Puna Desert; rodents.

El leucismo aparece en varios grupos de vertebrados, aunque es menos frecuente en mamíferos. Para Argentina no conocemos ningún registro documentado para roedores pequeños. El objetivo de nuestro trabajo es informar los primeros casos de leucismo en roedores cricétidos en la Puna Desértica de Argentina. El trabajo de campo se llevó a cabo en la Reserva Provincial de Uso Múltiple Don Carmelo (San Juan, Argentina), ubicada en la Puna Desértica. Los animales fueron capturados en 9 cuadrículas formadas por 36 trampas tipo Sherman, establecidas en parcelas situadas entre los 3,100 y 3,300 m, en los años 2013-2014. Registramos 6 casos de leucismo en 3 especies de cricétidos: Eligmodontia sp. (n = 3), Abrothrix andina (n = 2) y Phyllotis xanthopygus (n = 1). Este trabajo representa el primer reporte de casos de leucismo en mamíferos pequeños para Argentina. Los casos en la población estudiada podrían deberse al bajo flujo génico impuesto por la alta rigurosidad ambiental de un desierto extremo, probablemente relacionándose con causas genéticas derivadas de factores climáticos y ecológicos, al tratarse de ambientes no antropizados.

Palabras clave: Cricétidos; desorden pigmentario; leucismo; Puna Desértica; roedores.

© 2020 Asociación Mexicana de Mastozoología, www.mastozoologiamexicana.org

Genetic abnormalities that affect color expression are known as albinism, leucism, and melanism. Albinism is the condition defined by the total absence of melanin pigment in the eyes, skin and hair (Lamoreux et al. 2010). In leucism, animals have a lighter color or are stained, with pigmented eyes (Miller 2005; García-Morales et al. 2012; Liu et al. 2019). In melanism, animals are overproduced with melanin, resulting in completely black fur (Jimbow et al. 1976; Silvers 2012).

In natural populations, these pigmentation abnormalities often occur in isolated and small populations, reflecting low levels of genetic diversity (Holyoak 1978; Bensch et al. 2000; Brito and Valdivieso-Bermeo 2016; Rubio and Simonetti 2018). They have also been related to contamination in urban areas (Il’enko 1960) and radioactive contamination, as in the case of areas near Chernobyl (Møller and Mousseasu 2001).

Pigmentation abnormalities associated with albinism, such as leucism, appear in various vertebrate groups although they are less frequent in mammals (Dunlop et al. 2019). Cases were reported in fish (Mena-Valenzuela and Valdiviezo-Riveira 2016; Nugra et al. 2018; Liu et al. 2019); amphibians and reptiles (Krecsák 2008; López and Ghirardi 2011; Escoriza 2012), and birds (Comisso 2012; Chiale and Gerardo 2014; Atauchi 2015; Cadena-Ortíz et al. 2015).

In mammals, the leucism was found in various species such as bats (Artibeus fraterculus; Fernández de Córdova et al. 2017), agouti (Dasyprocta azarae and D. fuliginosa; Vilges de Olivera 2009; Mejía-Valenzuela 2019), two-furred fur sea wolf (Arctocephalus australis; Abreu et al. 2013), opossum (Didelphis albiventris; Abreu et al. 2013), squirrel (Funambulus palmarum; Samson et al. 2017), guanaco (Lama guanicoe; Puig et al. 2017), among other.

Likewise, in several genera of small rodents such as Reithrodontomys (Egoscue 1958), Otomys (Pirlot 1958), Mus musculus (Winston and Lindzey 1964), Perognathus (Egoscue and Lewis 1968), Microtus (Brewer et al. 1993; Peles et al. 1995), Myodes (Steen and Sonerud 2012), Peromyscus (Camargo et al. 2014), Akodon, Nephelomys, Transandinomys, Thomasomys and Mesomys (Brito and Valdivieso-Bermeo 2016), Akodon (Montoya- Bustamante et al. 2017), and Abrothrix (Rubio and Simonetti 2018). Currently for Argentina, we do not know of any documented record for small rodents. Thus, the objective of this work is to report the first cases of leucism in small rodents in the Argentine Puna Desert.

The study site is located in the Multiple Use Provincial Reserve Don Carmelo, at the southernmost tip of the Argentina Puna Desert. The protected area is located in the west center of Ullum department, in the province of San Juan-Argentina (31° 10’ S, 69° 46’ W; Figure 1), with an altitude that ranges from 3,000 to 3,800 m. It has an average annual temperature of 8.15 °C, an absolute maximum temperature of 26 °C, and an absolute minimum temperature of -22 °C (Andino and Borghi 2017). The vegetation consists of low xerophilous shrubs and grasses, with immature, stony or sandy soils (Martínez-Carretero 1995; Beninato et al. 2019).

The work was carried out in the 3 dominant environments of this sector of the Puna: rocky outcrop, hillside and plain, in plots located between 3,100 and 3,300 m, between the years 2013-2014. Sampling was carried out on 9 fixed grids, separated by a minimum of 500 m, made up of 36 Sherman-type traps 15 m apart (more details in Beninato et al. 2019). The captures were carried out during the 4 stations. The sampling effort was 2,592 traps nights.

From a total of 309 captured individuals, 6 individuals with leucism were registered, belonging to 3 species of cricetid rodents, thus representing 2 % of the total captured animals. There were 3 adult individuals of Eligmodontia sp. (15 %; n = 20), 1 juvenile and 1 adult individual of Abrothrix andina (2.1 %; n = 93) and 1 adult individual of Phyllotis xanthopygus (0.51 %; n = 196; Figure 2a-f; Table 1). The individuals presented small spots of white coloration on the back and / or lateral parts, with the pigmentation of the retinas and normal eyelids. The individuals of Eligmodontia sp. had spots on the back, head and sides; that of P. xanthopygus spots on the head; and that of A. andina spots on one of the ears and one of the flanks (Figure 2a-f).

Coloring patterns in wildlife are fundamental ecological adaptations for species survival because they facilitate camouflage, mimicry, sexual selection, and thermoregulation (Caro 2005; Mullen and Hoekstra 2008; Protas and Patel 2008; Hubbard et al. 2010). In individuals with pigmentation abnormalities, such as leucism, the condition is considered a disadvantage because they are more likely to be detected by predators than individuals with normal coloration (Owen and Shimmings 1992; Vignieri et al. 2010).

In South America, so far there are few records of leucism in small rodents and all have been associated with anthropogenic effects. In Ecuador, leucism was recorded in an anthropized environment of the Cordillera in the genera Akodon, Nephelomys, Transandinomys, Thomasomys and Mesomys (Brito and Valdivieso-Bermeo 2016) and in a valley near Quito (Reithrodontomys mexicanus; Ramírez-Jaramillo et al. 2019). In Colombia, leucism was found in specimens of Akodon affinis (Montoya- Bustamante et al. 2017) which was associated with possible inbreeding effects due to discontinuous distribution and habitat fragmentation in the Andes. In Chile, the presence of specimens with leucism in Abrothrix hirta and A. olivacea was associated with a possible decrease in genetic diversity due to the effect of human disturbances (Rubio and Simonetti 2018). For the genus Eligmodontia so far there is no documentation of any pigment disorder, while for Phyllotis andium there is a record of albinism in the coastal desert of Perú (Ramírez and Arana 2005). With respect to Argentina, total melanism, another pigmentary disorder, had previously only been registered in two species of small mammals (Scapteromys tumidus and Oligoryzomys flavescens) from the Paraná Delta (Massoia 1978).

The cases of leucism reported in this work for P. xanthopygus, A. andina and Eligmodontia sp. in the Argentina Puna Desert, could have an origin in low genetic variability, as has been suggested for other vertebrates (Owen and Shimmings 1992; Bensch et al. 2000), and other small mammals (Brito and Valdivieso-Bermeo 2016; Rubio and Simonetti 2018). The Argentina Puna Desert presents extreme climatic conditions, with scarce vegetation cover, except in the rocky outcrops, which appear as patchy and scarce environments (Beninato et al. 2019), in addition to the presence of air and land predators. Beninato et al. (2019) found that P. xanthopygus and A. andina, restricted their distribution almost exclusively to the rocky areas and Eligmodontia sp. to the plains. The cases of leucism in the studied population could be due to the low gene flow imposed by the high environmental rigor.

This work represents the first report of cases of leucism in small rodents for Argentina. In this case, the presence of leucism is probably related to the effect of natural ecological factors in these extreme non-anthropic environments. However, genetic studies are required to advance the causality that this type of condition is generating in the wild fauna of the small mammal of the arid end of the Argentina Puna Desert.

Acknowledgements

We thank A. Curatola for his hospitality and for allowing us to use the facilities of the Don Carmelo Multiple Use Provincial Reserve. We want to thank T. Gonzalez for providing the map and L. Cella for english revision. This research was partially funded by the CICITCA E / 920 grant (Carlos E. Borghi, UNSJ, Argentina).

Literature cited

Abreu, M. S., R. Machado, F. Barbieri, N. S. Freitas, and L. R. Olivera. 2013. Anomalus color in Neotropical mammals: a review with new records for Didelphis sp. (Didelphidae, Didelphimorphia) and Arctocephalus australis (Otariidae, Carnivora). Brazilian Journal of Biology 73:85–194.

Andino, N., and C. E. Borghi. 2017. Occurrence of Ctenomys mendocinus in a high-altitude cold desert: effect on density, biomass, and fitness of sagebrush plants. Arctic, Antarctic, and Alpine Research 49:53–60.

Atauchi, P. J. 2015. Leucismo en el rascón plomizo (Pardirallus sanguinolentus: Rallidae) en el Humedal de Lucre-Huacarpay, al sur de los Andes de Perú. The Biologist 13:157–60.

Beninato, V. A., C. E. Borghi, C. F. de los Ríos, and S. M. Giannoni. 2019. Diversidad de un ensamble de micromamíferos en la Puna Desértica de San Juan (Argentina). Mastozoología Neotropical 26:31–48.

Bensch, S., H. Bengt, D. Hasselquist, and B. Nielsen. 2000. Partial albinism in an semi-isolated population of great reed warblers. Hereditas 133:167–170.

Brito, J., and K. Valdivieso-Bermeo. 2016. First records of leucism in eight species of small mammals (Mammalia: Rodentia). Therya 7:483489.

Brewer, S. R., M. F. Lucas, J. A. Mugnano, J. D. Peles, and G. W. Barrett. 1993. Inheritance of albinism in the meadow vole (Microtus pennsylvanicus). American Midland Naturalist 130:393–396.

Cadena-Ortiz, H. F., D. Bahamonde-Vinueza, D. F. Cisneros Heredia, and G. Buitrón-Jurado. 2015. Alteraciones de coloración en el plumaje de aves silvestres del Ecuador. Avances en Ciencias e Ingenierías 7:75–90.

Camargo, I., E. Rios, C. Cornejo-Latorre, and S. T. Álvarez- Castañeda. 2014. First record of leucism in the genus Peromyscus (Mammalia: Rodentia). Western North American Naturalist 74:366369.

Caro, T. 2005. The adaptative significance of coloration in mammals. BioScience 55:125136.

Chiale, M. C., and P. L. Gerardo. 2014. A case of partial leucism in the American Barn Owl (Tyto furcata) (Temminck, 1827), from Buenos Aires province, Argentina. Sociedade Brasileira de Ornitologia. Ararajuba 22:307310.

Comisso, E. 2012. Caso de leucismo en caburé grande (Glaucidium nana). Ecoregistros 2:13.

Dunlop, J., D. Peacock, H. Moore, and M. Cowan. 2019. Albinism in Dasyurus species-a collation of historical and modern records. Australian Mammalogy 42:114118.

Escoriza, D. 2012. Description of a case of albinism in a tadpole of Discoglossus pictus pictus (Anura: Discoglossidae) in Sicily. Herpetology Notes 5:311–312.

Egoscue, H. J. 1958. Albinism in the western harvest mouse. Journal of Mammalogy 39:306.

Egoscue, H. J., and T. J. Lewis. 1968. An albino long-tailed pocket mouse from Utah. Journal of Mammalogy 49:319.

Fernández de Córdova, C. J. F., C. H. Nivelo-Villavicencio, and P. X. A. Webster. 2017. Primer reporte de leucismo para Artibeus fraterculus (Chiroptera: Phyllostomidae) en Ecuador. Revista Biodiversidad Neotropical 7:114118.

García-Morales, R., D. T. Duran, E. S. A. Gómez, C. E. Moreno, and M. S. Akmentis. 2012. Registro de leucismo en Sturnira ludovici y Artibeus jamaicensis (Phyllostomidae) en México. Chiroptera Neotropical 18:11011105.

Hafner, M., and D. Hafner. 1987. Geographic distribution of two Costa Rican species of Orthogeomys, with comments on dorsal pelage marking in the Geomyidae. The Southwestern Naturalist 32:511.

Holyoak, D. T. 1978. Variable albinism of the flight feathers as an adaptation of recognition of individual birds in some Polynesian populations of Acrocephalus warblers. Ardea 66:112–117.

Hubbard, J. K., J. A. C. Uy, M. E. Hauber, H. E. Hoekstra, and R. J. Safran. 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends in Genetics 26:231239.

Il’enko, A. I. 1960. On the occurrence of albinism among house sparrows in Moscow. Protection of Nature 2:7274.

Jimbow, K., W. C. Quevedo, T. B. Fitzpatrick, and G. Szabo. 1976. Some aspects of melanin biology: 1950–1975. The Journal of Investigative Dermatology 67:72–89.

Krecsák, L. 2008. Albinism and leucism among European Viperinae: a review. Russian Journal of Herpetology 15:97102.

Lamoreux, M. L., V. Delmas, L. Laure, and D. C. Bennett. 2010. The color of mice. A model genetic network. Wiley-Blackwell. Texas, U.S.A.

Liu, Z., H. Wen, F. Hailer, F. Dong, Z. Yang, T. Liu, and J. Zhou. 2019. Pseudogenization of Mc1r gene associated with transcriptional changes related to melanogenesis explains leucistic phenotypes in Oreonectes cavefish (Cypriniformes, Nemacheilidae). Journal of Zoological Systematics and Evolutionary Research 57:900909.

López, J. A., and R. Ghirardi. 2011. First record of albinism in Rhinella fernandezae (Gellardo, 1957). Belgian Journal of Zoology 141:5961.

Martínez-Carretero, E. 1995. La Puna argentina: delimitación general y división en distritos florísticos. Boletín de la Sociedad Argentina de Botánica 31:27–40.

Massoia, E. 1978. El melanismo total del pelaje en tres mamíferos del Delta del Paraná (Carnivora y Rodentia). Revista de Investigaciones Agropecuarias INTA 14:1–6.

Mejía-Valenzuela, E. G. 2019. First record of leucism in the Dasyprocta fuliginosa (Dasyproctidae, Rodentia) in Ecuador. Biota Colombiana 20:128133.

Mena-Valenzuela, P., and J. Valdiviezo-Rivera. 2016. Leucismo en Astroblepus ubidiai (Pellegrin 1931) (Siluriformes: Astroblepidae), de la provincia de Imbabura, Ecuador. Biota Colombiana 17:131135.

Miller, J. D. 2005. All about albinism. Missouri Conservationist 66:5–7.

Møller, A. P., and T. A. Mousseau. 2001. Albinism and phenotype of Barn Swallows. Evolution 55:2097–2104.

Montoya-Bustamante, S., N. Zapata-Mesa, and O. E. Murillo-García. 2017. Leucism in Akodon affinis (Allen, 1912) (Rodentia: Cricetidae). Therya 8:269–272.

Mullen, L. M., and H. E. Hoekstra. 2008. Natural selection along an environmental gradient: a classic cline in mouse pigmentation. Evolution: International Journal of Organic Evolution 62:1555–1570.

Nugra, F., F. Anaguano-Yancha, C. Arízaga, E. Zárate, and J. Brito. 2018. Leucismo en el pez Lebiasina bimaculata (Characiformes: Lebiasinidae) en Guayas, Ecuador. Biota Colombiana 19:133139.

Owen, M., and P. Shimmings. 1992. The occurrence and performance of leucistic Barnacle Geese Branta leucopsis. Ibis 134:22–26.

Peles, J. D., M. F. Lucas, and G.W. Barrett. 1995. Population dynamics of agouti and albino meadow voles in high-quality, grassland habitats. Journal of Mammalogy 76:1013–1019.

Pirlot, P. L. 1958. Albinism among wild African rodents. Journal of Mammalogy 39:1376–1377.

Protas, M. E., and N. H. Patel. 2008. Evolution of coloration patterns. Annual Review of Cell and Developmental Biology 24:425-446.

Puig, S., F. Videla, M. I. Rosi, V. P. Seitz, J. Moreni, M. Pérez, R., F. Tobares Maldonado, and S. Martín. 2017. Primeros registros de guanacos albinos en las montañas de la precordillera andina austral (Mendoza, Argentina). Multequina 16:7786.

Ramírez, O. E., and M. Arana. 2005. Albinism in the Andean leaf-eared mouse, Phyllotis andium (Rodentia, Cricetidae). Mastozoología Neotropical 12:269–270.

Ramírez-Jaramillo, S. M., P. Bejarano-Muñoz, A. Caiza, M. Novillo, and P. Moreno-Cárdenas. 2019. Leucismo en Reithrodontomys mexicanus soederstroemi (Rodentia: Cricetidae), Quito, Ecuador. Acta Zoológica Mexicana 35:1-4.

Rubio, A. V., and J. A. Simonetti. 2018. Partial and complete leucism in two Abrothrix species (Rodentia: Cricetidae) from central Chile. Mammalia 83:100102.

Samson, A., B. Ramakrishnan, and S. Bargavi. 2017. Leucism in the three-striped palm squirrel (Funambulus palmarum) at Gudalur Forest Division, Tamil Nadu, Southern India. Therya 8:261–262.

Silvers, W. K. (ed.). 2012. The Coat Colors of mice: a Model for Mammalian Gene Action and Interaction. Springer Science and Business Media. New York, U.S.A.

Steen, R., and G. A. Sonerud. 2012. A bank vole (Myodes glareolus) with complete leucism captured by a Eurasian kestrel (Falco tinnunculus) in Norway. Annales Zoologici Fennici 49:306–308.

Vignieri, S. N., J. G. Larson, and H. E. Hoekstra. 2010. The selective advantage of crypsis in mice. Evolution 64:2153–2158.

Vilges de Olivera, S. 2009. Albinismo parcial em cutia Dasyprocta azarae (Rodentia, Dasyproctidae), no sul do Brasil. Biotermas 22:243–246.

Winston, H. D., and G. Lindzey. 1964. Albinism and water escape performance in the mouse. Science 144:189–191.

Associated editor: Cristian Kraker-Castañeda

Submitted: April 22, 2020; Reviewed: June 29, 2020.

Accepted: July 11, 2020; Published on line: July 20, 2020.

Figure 1. Location of the study area located in the Argentina Puna Desert, province of San Juan, Argentina. a) South America (in gray Argentina); b) San Juan; c) Don Carmelo Multiple Use Reserve, d) Study sites.

Table 1. Cases of leucism in 3 species of small rodents in the Argentina Puna Desert, province of San Juan Argentina.

Species

Latitude

Longitude

Altitude

Environment

Sex

Season

Photography

Eligmodontia sp.

30°57’26.8”

69°5’15.8”

3.115

Plain

Female

Spring

a

Eligmodontia sp.

30°56’26.2”

69°5’12.7”

3.096

Plain

Male

Winter

b

Eligmodontia sp.

30°56’26.3”

69°5’12.1”

3.120

Hillside

Male

Winter

c

Phyllotis xanthopygus

30°57’2.4”

69°4’50.04”

3.096

Rock

Male

Autumn

d

Abrothrix andina

30°57’0.0”

69°4’50.7”

3.165

Rock

-

Summer

e

Abrothrix andina

30°56’56.8”

69°4’48.2”

3.175

Rock

-

Summer

f

Figure 2. Leucism in 3 species of small rodents in the Argentina Puna Desert, province of San Juan Argentina. Eligmodontia sp. (a, b, c), Phyllotis xanthopygus (d) and Abrothrix andina (e, f). Photography: V. A. Beninato.