Leucism is the lack or reduction in pigmentation in the most or parts of the body, but not in the eyes and body extremities. It is extremely rare in primates and has never been reported for Callithrix, a genus endemic to Brazil. We searched for individuals of Callithrix jacchus and C. penicillata with pigmentation anomalies in a systematic survey of three protected areas in the Atlantic Forest, within museum collections in Brazil, and opportunistically during field studies. Since 2008, we have recorded 8 individuals with leucism in small urban and periurban forest patches. Four were from native populations of C. penicillata in Cerrado savannahs and of C. jacchus in the Caatinga xeric scrubland, and 4 were from populations of hybrids between C. jacchus and C. penicillata in invaded areas in the coastal Atlantic Forest. We found no pigmentation abnormalities in museum specimens. We hypothesize that the observed leucism may be linked to inbreeding within the native range, but to hybridization within the invaded range, and discuss the likely ecological consequences to leucistic individuals.

Keywords:
Atlantic Forest, Savannah, Leucism, Hybridization, Inbreeding
1.
Abreu MSL, Machado R, Barbieri F, Freitas NS, Oliveira LR (2013). Anomalous colour in Neotropical mammals: a review with new records for Didelphis sp. (Didelphidae, Didelphimorphia) and Arctocephalus australis (Otariidae, Carnivora). Brazilian Journal of Biology 73: 185–194.
2.
Alexandrino ER, Apolinario da Luz DT, Maggiorini EV, Ferraz KMPMB (2012). Nest stolen: the first observation of nest predation by an invasive exotic marmoset (Callithrix penicillata) in an agricultural mosaic. Biota Neotropica 12: 211–215.
3.
Arntzen JW, Wallis GP (1991). Restricted gene flow in a moving hybrid zone of the newts Triturus cristatus and T. marmoratus in western France. Evolution 45: 805–826.
4.
Arntzen JW, Wielstra B, Wallis GP (2014). The modality of nine Triturus newt hybrid zones, assessed with nuclear, mitochondrial and morphological data. Biological Journal of the Linnean Society 113: 604–622.
5.
Aximoff IA, Carvalho S (2016). Gymnodactylus darwinii (Darwin’s gecko) predation. Herpetological Review 47: 298–299.
6.
Aximoff IA, Vaz SM (2016). Bugio-ruivo (Primates, Atelidae) em campos de altitude e com anomalia na coloração no Parque Nacional do Itatiaia, Sudeste do Brasil. Oecologia Australis 20: 122–127.
7.
Aximoff IA, Soares HM, Pissinatti A, Bueno C (2016). Registros de Callithrix aurita (Primates, Callitrichidae) e seus híbridos no Parque Nacional do Itatiaia. Oecologia Australis 20: 520–525.
8.
Bandeira CM (1994). Parque Nacional da Tijuca. São Paulo, Books do Brasil Editora Ltda.
9.
Begotti RA, Landesmann LF (2008). Predação de ninhos por um grupo híbrido de sagüis (Callithrix jacchus/penicillata) introduzidos em área urbana: implicações para a estrutura da comunidade. Neotropical Primates 15: 28–29.
10.
Bensch S, Hansson B, Hasselquist D, Nielsen B (2000). Partial albinism in a semi-isolated population of great reed warblers. Hereditas 133: 167–170.
11.
Berube M, Aguilar A (1998). A new hybrid between a blue whale, Balaenoptera musculus, and a fin whale, B. physalus: frequency and implications of hybridization. Marine Mammal Science 14: 82–98.
12.
Bicca-Marques JC, Silva VM, Gomes DF (2006). Ordem Primates. In Mamíferos do Brasil (Reis NR, Peracchi AL, Pedro WA, Lima IP, eds.), pp 101–148. London, Sociedade Brasileira de Zoologia.
13.
Bridge H, von dem Hagen EA, Davies G, Chambers C, Gouws A, Hoffmann M, Morland AB (2014). Changes in brain morphology in albinism reflect reduced visual acuity. Cortex 56: 64–72.
14.
Brito J, Valdivieso-Bermeo K (2016). First records of leucism in eight species of small mammals (Mammalia: Rodentia). Therya 7: 483–489.
15.
Bruno SF, Bard VT (2016). Exóticos invasores: Bioinvasores selvagens introduzidos no estado do Rio de Janeiro e suas implicações. Niterói, Eduff – Editora da Universidade Federal Fluminense.
16.
Bufalo FS, Galetti M, Culot L (2016). Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic Forest of South America. International Journal of Primatology 37: 333–349.
17.
Caro T (2005). The adaptive significance of coloration in mammals. Bioscience 55: 125–136.
18.
Coimbra-Filho AF, da Cruz Rocha N (1978). Acérca de disfunção pigmentar em Leontopithecus rosalia chrysomelas (Kuhl, 1820), seu tratamento e recuperação (Callitrichidae, Primates). Revista Brasileira de Biologia 38: 165–170.
19.
Cunha AA, Vieira MV (2004). Present and past primate community of the Tijuca Forest, Rio de Janeiro, Brazil. Neotropical Primates 12: 153–154.
20.
Cunha AA, Vieira MV, Grelle CE (2006). Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic forest fragment: the capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca forest, Rio de Janeiro. Urban Ecosystems 9: 351–359.
21.
Espinal M, Mora JM, Ruedas LA, López LI, Marineros L (2016). A case of albinism in the Central American spider monkey, Ateles geoffroyi, in Honduras. Mastozoología neotropical 23: 63–69.
22.
Faria DS (1986). Tamanho, composição de um grupo social e a área de vivência (home-range) do sagüi Callithrix jacchus penicillata na mata ciliar do córrego Capetinga, Brasília, DF. In A Primatologia no Brasil (Mello MT, ed.), vol 2, pp 87–105. Brasília, Sociedade Brasileira de Primatologia.
23.
Fertl D, Rosel P (2002). Albinism. In Encyclopedia of Marine Mammals (Perrin WF, Würsig B, Thewissen JGM, eds.), pp 16–18. San Diego, Academic Press.
24.
Fortes VB, Bicca-Marques JC (2008). Abnormal pelage color in an isolated population of Alouatta guariba clamitans Cabrera, 1940, in South Brazil. International Journal of Primatology29: 717–722.
25.
Galetti M, Bovendorp RS, Fadini RF, Gussoni COA, Rodrigues M, Alvarez AD, Guimarães Jr PR, Alves K (2009). Hyperabundant mesopredators and bird extinction in an Atlantic forest island. Zoologia 26: 288–298.
26.
Hofreiter M, Schöneberg T (2010). The genetic and evolutionary basis of colour variation in vertebrates. Cellular and Molecular Life Sciences67: 2591–2603.
27.
Kehas AJ, Theoharides K, Gilbert J (2005). Effect of sunlight intensity and albinism on the covering response of the Caribbean sea urchin Tripneustes ventricosus. Journal of Marine Biology 146: 1111–1117.
28.
Leite G, Duarte MH, Young RJ (2011). Human-marmoset interactions in a city park. Applied Animal Behaviour Science 132: 187–192.
29.
Lynch M (1991). The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622–629.
30.
Miller JD (2005). All about albinism. Missouri Conservationist 66: 4–7.
31.
Mittermeier RA, Rylands AB, Wilson DE (eds.) (2013). Handbook of the Mammals of the World, vol 3. Barcelona, Lynx Editions.
32.
Modesto TC, Bergallo HG (2008). Ambientes diferentes, diferentes gastos do tempo entre atividades: o caso de dois grupos mistos do exótico Callithrix spp. na Ilha Grande, Brasil. Neotropical Biology and Conservation 3: 112–118.
33.
Moller AP, Mousseau TA (2001) Albinism and phenotype of barn swallows (Hirundo rustica) from Chernobyl. Evolution 55: 2097–2104.
34.
Nkosi V, Twala G (2002). White buffalo killed by lion. Ecological Journal (Johannesburg)4: 241.
35.
Paglia AP, da Fonseca GA, Rylands AB, Herrmann G, Aguiar LM, Chiarello AG, et al. (2012). Lista anotada dos mamíferos do Brasil (Annotated Checklist of Brazilian Mammals), 2ª Edição. Occasional Papers in Conservation Biology, No. 6. Arlington, Conservation International.
36.
Pereira DG, Oliveira MEA, Ruiz-Miranda CR (2008). Interações entre calitriquídeos exóticos e nativos no Parque Nacional da Serra dos Órgãos – RJ. Espaço e Geografia11: 67–94.
37.
Rodrigues AP, Felfili JM, Vale MM (2016). Value of an urban fragment for the conservation of Cerrado in the federal district of Brazil. Oecologia Australis 20: 109–118.
38.
Romero V, Racines-Márquez CE, Brito J (2018). A short review and worldwide list of wild albino rodents with the first report of albinism in Coendou rufescens (Rodentia: Erethizontidae). Mammalia 82: 509–515.
39.
Rosa CA, Curi NHA, Puertas F, Passamani M (2017). Alien terrestrial mammals in Brazil: current status and management. Biological Invasions 19: 2101–2123.
40.
Rothe H (1999). Adaptation to natural food resources by semi-free common marmosets (Callithrix jacchus): preliminary results. Neotropical Primates 7: 54–57.
41.
Ruiz-Miranda CR, Affonso AG, Morais MM, Verona CE, Martin A, Beck B (2006). Behavioral and ecological interactions between reintroduced golden lion tamarins (Leontopithecus rosalia, Linnaeus, 1766) and introduced marmosets (Callithrix spp., Linnaeus, 1758) in Brazil’s Atlantic Coast Forest fragments. Brazilian Archives of Biology and Technology 49: 99–109.
42.
Rylands AB, Coimbra-Filho AF, Mittermeier RA (2009). The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and callimico (Callimico) (Callitrichidae, Primates). In The Smallest Anthropoids (Ford SM, Porter LM, Davis LC, eds.), pp 25–61. New York, Springer.
43.
Rylands AB, Fonseca GAB, Leite YLR, Mittermeier RA (1996). Primates of the Atlantic Forest: origin, distributions, endemism, and communities. In Adaptive Radiations of Neotropical Primates (Norconk MA, Rosenberger AL, Garber PA, eds.), pp 21–51. New York, Plenum Press.
44.
Sazima I, Di-Bernardo M (1991). Albinismo em serpentes neotropicais. Memórias do Instituto Butantan 53: 167–173.
45.
Slavík O, Horký P, Maciak M (2015). Ostracism of an albino individual by a group of pigmented catfish. PLoS One 10: e0128279.
46.
Stevenson MF, Rylands AB (1988). The marmosets, genus Callithrix. In Ecology and Behavior of Neotropical Primates(Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca GAB, eds.), vol 2, pp 131–222. Washington, World Wildlife Fund.
47.
Talamoni S, Viana PIM, Costa CG, Palú L, Oliveira RB, Pessôa LM (2017). Occurrence of leucism in Eira barbara (Carnivora, Mustelidae) in Brazil. Biota Neotropica 17: e20170328.
48.
Vivo M (1991). Taxonomia de Callithrix Erxleben, 1977 (Callitrichidae Primates). Belo Horizonte, Fundação Biodiversitas.
49.
Yazdi P (2002). A possible hybrid between the dusky dolphin (Lagenorhynchus obscurus) and the southern right whale dolphin (Lissodelphis peronii). Aquatic Mammals 28: 211–217.
50.
Zaluar MT (2015). Comportamento e utilização do habitat de grupos de Callithrix sp. (Primates, Callitrichidae) no Instituto de Pesquisas do Jardim Botânico do Rio de Janeiro. Mastozoología Neotropical 22: 201–210.
51.
Zaluar MT, Loguercio MFC, Rangel CH, Rocha-Barbosa O, Youlatos D (2014). Comportamento locomotor e postural de Callithrix jacchus(Linnaeus, 1758). In A Primatologia no Brasil (Passos FC, Miranda JMD, eds.), vol 13, pp 290–301. Brasília, Sociedade Brasileira de Primatologia.
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