Metachirus nudicaudatus (E. Geoffroy Saint-Hilaire, 1803)

Astúa, D., 2015, Didelphidae, Handbook of the Mammals of the World – Volume 5 Monotremes and Marsupials, Barcelona: Lynx Edicions, pp. 129-186 : 157

48.

Brown Four-eyed Opossum

Metachirus nudicaudatus

French: Opossum quatre-yeux / German: Nacktschwanzbeutelratte / Spanish: Filandro pardo

Taxonomy. Didelphis nudicaudata E. Geoffroy Saint-Hilaire, 1803 ,

“ Cayenne,” French Guiana.

Molecular phylogenetic studies show significant divergences among specimens of this species from different regions, providing strong evidence that it contains more than one species. Five subspecies recognized.

Subspecies and Distribution.

M.n.nudicaudatusE.GeoffroySaint-Hilaire,1803—Venezuela(SoftheOrinocoRiverandtheOrinocoDelta),theGuianas,andNBrazil.

M.n.colombianusJ.A.Allen,1900—SMexico(Chiapas),CentralAmerica,N&WColombia,WVenezuela(MaracaiboLake,Andes,andWLlanos),andNWEcuador.

M.n.modestusThomas,1923—SBrazil,E&CParaguay,andNArgentina(MisionesandFormosa).

M.n.myosurosTemminck,1824—EBrazil(PernambucoStoSantaCatarina).

M. n. tschudiiJ. A. Allen, 1900 — upper Amazon Basin of E & SE Colombia, W Brazil, E Peru, and N & E Bolivia.

Descriptive notes. Head-body 24.5-28 cm, tail 28-36.9 cm; weight 284-480 g. The Brown Four-eyed Opossum is very distinctive. Its dorsal fur varies from reddishor yellowish-brown to gray-brown, finely streaked with buff on hair tips. Dorsal fur is darker along midline and rump, and darker fur extends onto outer surfaces of limbs. Broad reddish-brown to dark brown eye-rings extend from nose to ears, merging on top of head. Dark, broad stripe of the same color also runs from tip of muzzle to top of head, merging with eye-rings, enclosing conspicuous buff to yellowish-white spot above each eye that gives the Brown Four-eyed Opossum its common name. Cheeks are also buff to yellowish-white. Tail length is ¢.130% of head-body length, and tail is naked from base, varying from uniformly brownish to darker above and paler below. Ventral fur is brown to yellowish-white; fur overall is short, dense, and soft; and ears are dark brown and naked. The Brown Four-eyed Opossum is the largest opossum in which females lack a pouch. They have nine mammae, four on each side, and an additional medial mamma. The Brown Four-eyed Opossum is also the largest opossum with a 2n = 14, FN = 20 karyotype, with four biarmed and one acrocentric autosome pairs, and acrocentric X-chromosome and Y-chromosome. Skull size and shape are sexually dimorphic.

Habitat. Variety of forest habitats, usually mature evergreen lowland and lower montane forests from sea level to elevations exceeding 2100 m, and occasionally deciduous or dense secondary forest. The Brown Four-eyed Opossum also has been recorded in orchards and yards near and within human settlements.

Food and Feeding. The Brown Four-eyed Opossum is considered highly insectivorous. In a restinga (sandy soil forest) in south-eastern Brazil, its diet is mainly composed of ants, termites, cockroaches, and beetles, which are present in 70-90% ofall feces examined, as well as seeds of Cactaceae and Solanaceae . In Atlantic Forest sites in southern Brazil, its diet also includesfruits of Arecaceae and Bromeliaceae , along with invertebrates. Birds, small mammals, skinks (Mabuya), and ground lizards (Tropidurus) were also consumed. In Atlantic Forest sites in south-eastern Brazil, its diet included Coleoptera, Hymenoptera, Arachnida, Hemiptera, Isoptera, and seeds of Cecropia . In a cerrado site, seeds of Clidemia and Miconia (both Melastomataceae ) were recovered in almost one-third of the feces analyzed, in addition to the usual invertebrate prey. Brown Four-eyed Opossums can be considered important dispersers of several seeds of riparian forest species in the Brazilian cerrado. In Chiapas, Mexico, feces contained avian eggshell remains, Coleoptera, Hymenoptera, Homoptera, feathers, and reptilian scales. Diet seem to be influenced by resource availability because low occurrence of fruits in restinga (10-5%) and Atlantic Forest (7%) sites contrasts with higher levels of fruit consumption (more than 45%) in cerrado sites. Nutritional contents of preferred diets, determined with cafeteria experiments in captivity where individuals were free to choose food items according to their needs, resulted in 8-7 g of proteins, 12-9 g of carbohydrates, 1-9 g oflipids, and 2% offibers per 100 g of dry matter.

Breeding. Dens of Brown Four-eyed Opossums are found under roots of trees, sometimes with entrance tunnels, and at bases of palm trees, or in hollow logs at a maximum of I m high. Nests have also been found on the ground, usually well hidden in litter and undetectable from above. Other nestsites include ground hollows, rocky crevices, and underfallen palm fronds. Nests are spherical, built with leaves and twigs, and their entrances are closed with leaves. Although Brown Four-eyed Opossums are ground dwelling and sometimes are reported as lacking a prehensiletail, a specimen was videotaped carrying leaves with its tail in Colombia. Sexual maturity is reached at c.10 months (subadult females with pouch young were captured in Peru). Gestation is long compared with other opossum species, at least 21 days, with records of 20-28 days in captive specimens. Newborn young remain attached to teats for 75-80 days, after which they are left in the nest for the first time. They spend 30-45 days in the nest until they are totally weaned. They disperse at c.130 days of age. In south-eastern Brazil, mean littersize is five young (varying from one to nine young), but an average litter size of 7-6 young (varying from four to nine young) has been recorded. Litters of nine young were also found in Amazonian Peru, and litters of 6-9 young were recorded in Brazilian Amazonia. Female Brown Four-eyed Opossums with young were captured in February, April, June, November, and December in one Atlantic Forest site in south-eastern Brazil, and lactating females in April, June, and October. They were caught in August-April in another Atlantic Forest site, April in Paraguay, and February, June, and October in Peru. In Brazilian Amazonia, they seem to breed all year long because reproductively active females were captured in February-September. Lactating females were found in April in Colombia, April-May in Venezuela, and September in Peru.

Activity patterns. The Brown Four-eyed Opossum is nocturnal. An individual radiotracked in south-eastern Brazil was active exclusively at night, with activity peaks between 20:00 h and 23:00 h; activity diminished considerably after 02:00 h. A study using live-traps equipped with clocks that recorded capture times in south-eastern Brazil confirmed a strictly nocturnal habit, with individuals starting their activities c¢.2 hours after sunset and a major activity peak from 20:00 h to 22:00 h.

Movements, Home range and Social organization. The Brown Four-eyed Opossum is exclusively ground dwelling and well adapted for running. In fact, it seems to be the most specialized ground-dwelling opossum, even considered by some authors to be a cursorial species because it moves by high-speed leaps, with several muscular and skeletal adaptations to support this classification. Only one of 19 individuals tracked with spool-and-line in south-eastern Brazil had a single above-ground movement, out of 3200 m of line recorded. In studies in which traps are set at different heights, the Brown Four-eyed Opossum is consistently and exclusively captured in ground traps, although there is a single report of a study in which traps were set on the ground and in the understory, and an individual was captured in a trap set in the understory, but not on the ground. Likewise, the Brown Four-eyed Opossum performed poorly on experimental tests of locomotion on horizontal and vertical supports, and it was the only tested didelphid that refused to jump to across gaps. Home range estimates based on trapping grids were 0-74-16 ha, but an estimate for a female based on radiotelemetry was 8-4 ha. In a restinga forest, Brown Four-eyed Opossums usually moved 40-200 m between captures, with occasional movements of up to 300 m, but radiotelemetry estimates indicate that they can move on average 549-9 m/night. Estimates using spool-and-line devices in the Atlantic Forest of south-eastern Brazil indicated a mean distance between successive captures of 20-100 m, with maximal recorded distances traveled amounting to 253 m in one study and reaching 100-1500 m in another. Density estimates for the Brown Four-eyed Opossum in south-eastern Brazil are 50-600 ind/km? in an Atlantic Forestsite and 22 ind/km?®in a restinga forest.

Status and Conservation. Classified as Least Concern on The IUCN Red List. The Brown Four-eyed Opossum has a wide distribution, occurs in several protected areas, and presumably has a large population. Nevertheless,it is in need of taxonomic revision and very likely includes several species under what is now understood to be the Brown Four-eyed Opossum. Conservation status will need to be reassessed if distinct forms are elevated to full species.

Bibliography. Abdala et al. (2006), Adler et al. (2012), Argot (2001, 2002, 2003), Astua (2010), Astua et al. (2003), Beisiegel (2006), Bergallo (1994), Caceres (2004, 2005), Carvalho et al. (1999), Cerqueira et al. (1993), Costa (2003), Crouzeilles et al. (2010), Cunha & Vieira (2002), Delciellos & Vieira (2006, 2007, 2009a, 2009b), Delgado et al. (2014), Diaz (2014), Diaz & Flores (2008), Emmons & Feer (1997), Ferreira (2011), Fleck & Harder (1995), Gardner (2005), Gardner & Dagosto (2007), Gentile & Cerqueira (1995), Gentile et al. (2004), Grand (1983), Grelle (2003), Handley (1976), Herrera (2010), Hershkovitz (1992a), Julien-Laferriere (1991), Lambert et al. (2005), Lessa & Costa (2010), Lessa et al. (2013), Loretto et al. (2005), Macedo et al. (2007), McNab (1982, 2005), Medellin et al. (1992), Mendel & Vieira (2003), Miles et al. (1981), Miranda et al. (2009), Moraes (2004), de Muizon & Argot (2003), Nogueira, Martinelli et al. (1999), Palma & Yates (1996), Paresque et al. (2004), Passamani (2000), Patton & Costa (2003), Patton et al. (2000), Pereira et al. (2008), Reig et al. (1977), Santori, Astla & Cerqueira (1995, 2004), Santori, Lessa & Astua (2012), Santos-Filho et al. (2008), Santos et al. (2004), da Silva (2005), Smith (2008e), Svartman (2009), Svartman & Vianna-Morgante (1999), Szalay (1994), Vieira (2006), Voss & Jansa (2009), Yunis et al. (1973).

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)

Subspecies and Distribution. M.n.nudicaudatusE.GeoffroySaint-Hilaire,1803—Venezuela(SoftheOrinocoRiverandtheOrinocoDelta),theGuianas,andNBrazil. M.n.colombianusJ.A.Allen,1900—SMexico(Chiapas),CentralAmerica,N&WColombia,WVenezuela(MaracaiboLake,Andes,andWLlanos),andNWEcuador. M.n.modestusThomas,1923—SBrazil,E&CParaguay,andNArgentina(MisionesandFormosa). M.n.myosurosTemminck,1824—EBrazil(PernambucoStoSantaCatarina). M. n. tschudiiJ. A. Allen, 1900 — upper Amazon Basin of E & SE Colombia, W Brazil, E Peru, and N & E Bolivia.