Marmosa paraguayana (Tate, 1931)

Russell A. Mittermeier & Don E. Wilson, 2015, Didelphidae, Handbook of the Mammals of the World – Volume 5 Monotremes and Marsupials, Barcelona: Lynx Edicions, pp. 129-186 : 143

24.

South-eastern Woolly Mouse Opossum

Marmosa paraguayana

French: Opossum du Paraguay / German: Stdostliche Zwergbeutelratte / Spanish: Marmosa lanuda meridional

Other common names: Long-furred Woolly Mouse Opossum, Tate's Woolly Mouse Opossum

Taxonomy. Marmosa cinerea paraguayana Tate, 1931 ,

“ Villa Rica ,” Guaira, Paraguay.

This species is monotypic.

Distribution. E Brazil, from S Bahia S to Rio Grande do Sul, to N Argentina (Misiones), and E Paraguay.

Descriptive notes. Head-body 12-20 cm, tail 15-26 cm; weight 56-230 g. Dorsal fur of the South-eastern Woolly Mouse Opossum is uniformly grayish, with no or very little brownish tinge. Fur on head transitions to buffy to orange between eyes and up to nose. Eye-rings around black eyes are not very marked, do not reach base of ears, and barely reach nose. Tail length is c.125% of head—body length, and tail has fur on proximal 30 mm or more. Naked part of tail is brown, with white on distal one-third or mottled white on distal end. Ventral fur is buffy to orange, in a narrow median stripe from cheeks and chin to inguinal region, flanked by gray-based hairs. Furis long, soft, and woolly. Feet are pale brown to pinkish, and ears are round and brownish-pink. Females lack a pouch and have eleven mammae, five on each side and a medial mamma. There is no sexual dimorphism in skull size and shape. The South-eastern Woolly Mouse Opossum has a 2n = 14, FN = 24 karyotype, with all biarmed autosomes and acrocentric X-chromosome and Y-chromosome; a FN = 20 has also been reported.

Habitat. Primary and secondary forests, both in continuous areas and fragmented landscape. The South-eastern Woolly Mouse Opossum is able to move between fragments across the surrounding matrix, although this rarely happens. It also occurs in exotic Eucalyptus (Myrtaceae) plantations when a native understory is preserved. In southern Brazil, highest capture rates of South-eastern Woolly Mouse Opossums were in the most deforested areas and areas without a developed understory.

Food and Feeding. Diet of the South-eastern Woolly Mouse Opossum is well studied compared with that of most other species of opossums. In the Atlantic Forest of south-eastern Brazil, arthropods were present in more than 80% of the fecal samples analyzed, followed by fruits in 40% of feces. Arthropods constituted 80% of total volume, and fruits the remaining 20%. In subsequent studies in forest fragments in south-eastern Brazil, arthropods were recorded in 100% of fecal samples analyzed, and seeds were present in 58% of them. Arthropods most frequently consumed included Coleoptera, Hymenoptera (ants), Lepidoptera larvae, Orthoptera, Arachnida, Hemiptera, Blattodea, and Isopoda, along with seeds of Piper (Piperaceae) , Cecropia (Urticaceae) , and Passiflora (Passifloraceae) . In another Atlantic Forest site, five species of Araceae were consumed and most probably dispersed ( Philodendron corcovadense, P. appendiculatum, P. exymium, P. crassinervium, and Anthurium harrisii). In the Atlantic Forest of southern Brazil, its diet also included birds and Opiliones, in addition to the most frequently consumed Blattodea, Hymenoptera, and Orthoptera; seeds of Cecropia and Piper were also frequently recovered. In the cerrado, 90% of feces contained arthropods, including Coleoptera, Arachnida, Orthoptera, Hymenoptera, and Hemiptera, and 45% contained fruit seeds of Tapirira (Anacardiaceae) , Clidemia and Miconia (both Melastomataceae ), Myrcia (Myrtaceae) , and Amaioua and Psychotria (both Rubiaceae ). Feathers and flowers were also retrieved in fecal samples. Even didelphid remains were found in feces of young South-eastern Woolly Mouse Opossums. In a cerrado area in south-eastern Brazil, the South-eastern Woolly Mouse Opossum showed seasonal shifts in dietary composition; there was a wider trophic niche for the whole population in the dry season than in the wet season as individual food preferences shifted. South-eastern Woolly Mouse Opossums are also important dispersers of several seeds of riparian forest species in the Brazilian cerrado. Nutritional contents of preferred diets, determined with cafeteria experiments in captivity where individuals were free to choose food items, resulted in 2-3 g of proteins, 8-1 g of carbohydrates, 0-63 g oflipids, and 2-8% offibers per 100 g of dry matter.

Breeding. In south-eastern Brazil, South-eastern Woolly Mouse Opossums make nests preferentially in spiny palms ( Astrocaryum aculeatissimum , Arecaceae ), where the petiole is attached to the trunk, probably because dead leaves naturally collect there. These dens were located at heights of c.4-5 m. Additional dens were also found at c.10 m tree cavities and hollows, palms, and tangled lianas. Other nests were found in bromeliads, termite nests, and tree hollows. The South-eastern Woolly Mouse Opossum also used artificial nest boxes in an Atlantic Forest reserve. Males and females used nest boxes (which are thus used as dens and nests), but only a single female out of ten found in these nest boxes had lactating young; this female had ten young. In south-eastern Brazil, females reach sexual maturity at ¢.6 months of age, and breeding is highly seasonal. Reproductive females have been found only in the wet season in October—May, and their presence was directly related to rainfall in that month. One or two litters, depending on the year, were recorded. Litter sizes varied from six to eleven (the number of mammae) young. Their mating system is probably promiscuous, as inferred by structure of their territorial behavior. As in some other species in the genus, female South-eastern Woolly Mouse Opossums retrieve detached young when they call out with a distinct chirp.

Activity patterns. South-eastern Woolly Mouse Opossums are nocturnal, with an activity peak right after sunset and a gradual decrease in activity into the night.

Movements, Home range and Social organization. The South-eastern Woolly Mouse Opossum is highly arboreal, as revealed by its morphology, locomotion, and capture data in several communities. They move relatively faster than larger species of opossums on horizontal supports and jump easily across gaps, leaping long distances. Nevertheless, they may use both canopy and understory, depending on the site and its vegetation structures, and they may occasionally forage on the ground. In almost all studies of small mammal communities where the South-eastern Woolly Mouse Opossum occurs, it was captured exclusively or almost exclusively in arboreal traps, and more frequently in traps 3-12 m above ground level. Individuals tracked with spooland-line revealed that ground activity was infrequent and that all nests and dens were located above the ground. In some sites, canopy was preferred, and in others, the lower stratum was more used. Differences in use of the vertical component of the habitat were also seen; females explored the vertical axis of the forest more than males did. Use of the ground was apparently influenced by habitat characteristics, including arboreal cover and ground vegetation. Not only can South-eastern Woolly Mouse Opossums occasionally forage on the ground, but they can even use the ground level, if necessary, to move between forested fragments separated by low vegetation. Although such events were rare, individual Southern Woolly Mouse Opossums were recorded covering distances of ¢.300 m and even consuming fruits present exclusively in the matrix. In fact, their perceptual range, or the maximum distance at which a landscape element can be detected, is 100 m, based on abilities of individuals released in a grass matrix to detect and head for forest fragments from which they had been removed. Estimates of distances traveled by South-eastern Woolly Mouse Opossums using trapping grids were 300-350 m but varied more widely, 34-1140 m, when estimates were based on radio-telemetry data. Likewise, home ranges estimates were, depending on the study, 0-1-2-5 ha, 0-2-1-8 ha, and 0-8-1-7 ha—all from the same area in south-eastern Brazil using trapping grids. Much larger home ranges were, however, estimated using radio-telemetry in the same or nearby area: 5-4-24-2 ha for males and 0-3-10-7 ha for females. As in several opossum species, male South-eastern Woolly Mouse Opossums have much larger home ranges than females, and home ranges of males frequently overlap those of several females and even those of other males. Density in southern Brazil is 110 ind/km?, In south-eastern Brazil, densities were 75-275 ind/km? in one study and 60-371 ind/km?, with an average of 175 ind/km?, in another study.

Status and Conservation. Classified as Least Concern on The IUCN Red List. The South-eastern Woolly Mouse Opossum has a wide distribution, occurs in several protected areas, and is tolerant of habitat modification. Nevertheless, there is habitat loss due to agriculture and urbanization in much of its distribution. This is probably one of the few species of opossums with enough demographic data, obtained from a series of long-term population studies in south-eastern Brazil, to allow population viability analyses. These analyses indicate that several of these populations will not be viable over the next 100 years with the present movement of migrants across fragments and that levels of connectivity and number of migrants per generation necessary to maintain that metapopulation for 100 years are much higher than those actually observed.

Bibliography. Argot (2001, 2002, 2003), Astua (2010), Astua et al. (2003), Barros et al. (2008), Brito (2009, 2012), Brito & Fernandez (2000, 2002), Brito & da Fonseca (2006, 2007), Brito & Grelle (2004), Caceres et al. (2002), Cantor et al. (2013), Carvalho, Fernandez & Nessimian (2005), Carvalho, Pinheiro et al. (1999), Casella (2011), Casella & Caceres (2006), Cooper et al. (2010), Creighton & Gardner (2007b), Delciellos & Vieira (2006, 2007, 2009a, 2009b), Dias etal. (2010), Emmons & Feer (1997), da Fonseca & Kierulff (1989), Forero-Medina & Vieira (2009), Gardner (2005), Gardner & Creighton (2007b), Goulart et al. (2006), Graipel et al. (2006), Grelle (2003), Gutiérrez et al. (2010), Hershkovitz (1992a), Leite, Costa & Stallings (1996), Leite, Stallings & Costa (1994), Lessa & Costa (2010), Lessa et al. (2013), Lira et al. (2007), Loretto & Vieira (2011), Martinelli & Nogueira (1997), Miles et al. (1981), Moraes & Chiarello (2005a, 2005b), Oliveira-Santos et al. (2008), Paresque et al. (2004), Passamani (1995, 2000), Passamani & Fernandez (2011b), Patton & Costa (2003), Pereira et al. (2008), Pinheiro et al. (2002), Pires & Fernandez (1999), Pires, Fernandez & de Freitas (1999), Pires, Lira et al. (2002), Pires, Martins, Araujo et al. (2013), Pires, Martins, Cruz et al. (2010), Prevedello, Forero-Medina & Vieira (2010), Prevedello, Rodrigues & Monteiro-Filho (2009), Quental et al. (2001), Quintal et al. (2011), Redford & Eisenberg (1992), de la Sancha (2014), de la Sancha et al. (2012), Smith (2009b), Stallings (1988), Svartman & Vianna-Morgante (1999), Talamoni & Dias (1999), Tate (1933), Vieira & Izar (1999), Vieira & Monteiro-Filho (2003), Voss et al. (2014).

Figures

65. Pygmy Opossum (Chacodelphys formosa), 66. Agricola’s Opossum (Cryptonanus agricola), 67. Chacoan Mouse Opossum (Cryptonanus chacoensis), 68. Guaiba Mouse Opossum (Cryptonanus guahybae), 69. Unduavi Mouse Opossum (Cryptonanus unduaviensis), 70. . Emilie’s. 9 Opossum.. Gracilinanus. (null), 71. Aceramarca Opossum (Gracilinanus aceramarcae), 72. Agile Opossum (Gracilinanus agilis), 73. Wood Sprite Opossum (Gracilinanus dryas), 74. Northern Gracile Opossum (Gracilinanus marica), 75. Brazilian Gracile Opossum (Gracilinanus microtarsus)

Distribution. E Brazil, from S Bahia S to Rio Grande do Sul, to N Argentina (Misiones), and E Paraguay.