Monodelphis domestica (Wagner, 1842)

Astúa, D., 2015, Didelphidae, Handbook of the Mammals of the World – Volume 5 Monotremes and Marsupials, Barcelona: Lynx Edicions, pp. 129-186 : 151-152

39.

Gray Short-tailed Opossum

Monodelphis domestica

French: Opossum a queue courte / German: Graue Spitzmausbeutelratte / Spanish: Colicorto gris

Other common names: Brazilian Bare-tailed Opossum, Brazilian Gray Short-tailed Opossum, Gray Opossum, Gray-faced Opossum, Laboratory Opossum, Plain Bare Tail, Short Bare-tailed Opossum, Short-tailed Opossum

Taxonomy. Dudelphys domestica Wagner, 1842 ,

“ Cuyaba,” Mato Grosso, Brazil.

The species has been treated as monotypic, but recent phylogenetic analyses based on mtDNA sequences show that itis in fact composed of two clades representing two evolutionary units, one from the cerrado and the Pantanal and one from the caatinga. Formal definition and description of these two taxa are pending. Monotypic.

Distribution. E Bolivia, N Argentina (Formosa), N & C Paraguay, and C & NE Brazil.

Descriptive notes. Head-body 12:3-17.9 cm, tail 4:6.9-6 cm; weight 58-110 g. The Gray Short-tailed Opossum is now widely used as a laboratory animal. More than 80,000 individuals have been produced from a single colony of 2000 individuals and used either directly or as founders of additional colonies. As a consequence, there are measurements and weights in the literature that differ from those of wild individuals; some captive males have been reported to have a head-body length of up to 20 cm and weigh up to 150 g. The Gray Short-tailed Opossum is clearly distinct from almost all other species in the genus because its dorsal fur is uniformly grayish to gray-brown, and paler with yellowish tinges on cheeks and body sides. Head is the same color as dorsum and does not have a mid-rostral stripe or eye-rings. Tail length is ¢.50-55% of head-body length, tail has fur on proximal 10 mm or more, and naked rest oftail is dark brown dorsally and paler ventrally and at tip. Ventralfur is pale, gray-based, gray to buff with an orange tinge up to chin and no contrast with sides of body or dorsum. Fur is short, dense, and smooth. Feet are pinkish or whitish, and ears are small, uniformly colored grayish, and appear naked. Females lack a pouch, and 13 mammae are present, six on each side and a medial mamma. Throat gland is present in males and has a well-documented role in reproductive behavior. The Gray Short-tailed Opossum has a 2n = 18 karyotype, with a variable FN, with a small acrocentric X-chromosome and a minute acrocentric Y-chromosome (sometimes described as submetacentric, metacentric, or dotlike). Variation in FN ranges from FN = 20 in specimens from Goias, Brazil, FN = 22 in Pernambuco and Bahia, FN = 24 in Bolivia, FN = 28 in Goias, and FN = 30 in Espirito Santo, Brazil, and unspecified Brazilian localities. Males are larger than females; females stop growing when they reach sexual maturity, whereas males continue to grow. Skull size is sexually dimorphic. The Gray Short-tailed Opossum is the only opossum that has had its whole genome sequenced and published.

Habitat. Usually a wide variety of xeric habitats. Distribution of the Gray Short-tailed Opossum coincides with the South American diagonal of open and drier habitats that occurs from the Brazilian caatinga, through the cerrado, and into the Chaco of northern Argentina (including eastern Bolivia and northern Paraguay), but also in Pantanal, Campos, and Amazonian localities. Gray Short-tailed Opossums are therefore usually associated with more open vegetation. In the caatinga, they are found in most habitats, including low thorn scrub, high thorn scrub, cultivated and abandoned fields, and granitic outcrops. In the cerrado, they have been found in gallery forests, semi-deciduous forests, cerrado sensu stricto, wet grasslands, and rocky cerrado. In the Paraguayan Chaco, Gray Short-tailed Opossums occur in cerrado woodland, subhumid forest, cerrado scrub, and Chaco woodland. Nevertheless, they seem to avoid open pastures and even grasslands, preferring some level of vegetative cover.

Food and Feeding. Gray Short-tailed Opossums feed mainly on invertebrates, mostly insects, but their diet may also include small vertebrates and fruits. Seeds of Cipocereus minensis ( Cactaceae ) and carrion were found in its feces in an area of montane savanna in Brazil. Captive individuals were offered and readily attacked, killed, and ate a variety of small vertebrates, including snakes and lizards that were up to 75% of their own weight. Consumption of a rodent of the genus Calomys weighing about one-third of the opossum’s weight has been observed directly in the field. Gray Short-tailed Opossums catch small ants and flying insects with their forepaws. They even prey on scorpions, first pinning the scorpion to the ground, biting off the last tail segments before eating it. Nutritional contents of their preferred diets were determined with cafeteria experiments in captivity where individuals were free to choose food items according to their needs. They consumed 4-4 g of proteins, 2 g of carbohydrates, 0-88 g of lipids, and 1% offibers per 100 g of dry matter. Colonies of the Gray Short-tailed Opossum bred as laboratory individuals have been maintained successfully for generations with commercial fox food pellets, sometimes supplemented with mealworms and fruit.

Breeding. Female Gray Short-tailed Opossums make a variety of nests. In the wild, nests have been found in crevices of rocks, made of varied material such as leaves, bark, grasses, snakeskin, paper, cloth, and plastic remains. Captive individuals build nests from paper strips that vary from simple circular unwoven nests to fully woven and globular nests with walls, roof, and entrance tunnel, as reported for several other species of opossums. Nesting behavior usually increases the day before parturition, and even in captive individuals, construction of woven nests is more frequent on sunny days compared with cloudy days, which may be a temperature-related strategy to increase isolation of the nest. Although species of this genus are said to have semi-prehensile tails, they use their tails to drag material for nest construction, just like many other opossum genera. Materials for the nest are gathered with forepaws and then pushed under the belly to be carried with the tail. Both sexes build nests, but those of females are more woven and complex. Estimated sexual maturity in the caatinga was 5-7 months; observed littersizes in a single population were 6-11 young, with an average of 8-4 young/litter. Data from a longer and geographically broader study shows a greater range, 2-16 embryos (not pouch young), yet with a similar average, 7-9 embryos, and a median of eight embryos. Three females were collected in March in the caatinga; one had a litter of eleven young and each of the other two had nine young. In the Pantanal, litter sizes were 7-11 young. There is contrasting information on the breeding season in the wild. A one-year study with a caatinga population of Gray Shorttailed Opossums concluded that it breeds throughout the year because reproductively active females were recorded in eight out of ten months. During this time, some females produced two litters at most, with 7-8 weeks being the shortest time recorded between pregnancies in the same area. A study of more than 1000 museum specimens collected overfive years from seven different localities in the caatinga determined that the breeding season as a whole started in summer (December, sometimes November) and ended in winter (July), with the breeding season coinciding with the wet season. This is similar to breeding in several other species of opossum and more expected in species living in highly seasonal habitats. In fact, a population of Gray Short-tailed Opossums in the Brazilian Pantanal also showed a seasonal breeding pattern, with a breeding season in September—-May, and specimens recently collected in March in another caatinga locality included three females with pouch young. In the caatinga, presence of reproductively active females did not correlate with actual monthly rainfall but with the normal mean of rainfall, thus indicating that the breeding season is triggered by changes in photoperiod and not by immediate environmental conditions (actual rainfall), which is usually highly variable and unpredictable. As in the caatinga, breeding in a cerrado patch in Paraguay was also seasonal, occurring during the wet season. Unlike some other small species of opossums, despite the sexual dimorphism found, the Gray Short-tailed Opossum is iteroparous and breeds several times during its lifetime. In addition to breeding data from field studies, however, the Gray Shorttailed Opossum is unique among opossums in that its breeding biology has been well studied in captivity because it is now a widely used laboratory animal. Females bred and raised in the laboratory confirmed expected sexual maturity calculated from field data; maturity was usually attained at 5-6 months. Contrary to what is reported for most species of opossums, the Gray Short-tailed Opossum does not have a regular estrous cycle. Initially, an ovarian cycle of 32 days was noted, but further research showed that in fact there is no periodicity in ovulation or a spontaneous estrus. It is presence of new, unfamiliar males that triggers estrus, which is induced through pheromones from these new males. Puberty is only reached with stimulus of male pheromones, but solitary post-lactating females can have a spontaneous estrus even in the absence of male pheromones. Estrus-inducing pheromones seem to be more present in urine than feces or suprasternal gland secretions, and males use a variety of scent marking behaviors. Females actively investigate scent marks. Anestrous females typically display aggressive behavior toward new males, including hissing, open-mouth displays, and attacks that may occasionally result in death of the male. After 3-5 days, females start being receptive, and males and females engage in courtship, including sniffing cloacal opening, chases, and rump dragging, which is then followed by full estrus and mating. Courtship involves a series of clicking vocalizations by males when meeting females, which constitute a submissive communication. The male then follows the female, with genital sniffing, sometimes grabbing her at her hindquarters for further genital investigation. If she is receptive, reciprocal sniffing and reciprocal biting ensue. Finally, the male grabs the female’s ankles with his hindfeet and uses his forefeet to grasp her at waist level, usually biting the back of her neck. Mating lasts c.5 minutes, with the couple usually lying on their right side. Females will mate with multiple males during one estrus. Behavioral estrous lasts 1-1-5 days and ends with ovulation. Following ejaculation, little or no post-copulatory behavior occurs except for quick self-grooming of the genital area, and both sexes respond with typical open-mouthed threats if approached after copulation. Gestation in captivity lasts c.14 days. Neonates measure c.10 mm crown-rump length and weigh c.0-1 g. Young remain attached to teats for c.14 days and are weaned at eight weeks. Fur starts growing at 18-21 days of age, and eyes open at 28-35 days. Females do not retrieve newborns that have failed to attach to a nipple but will respond to distress calls and retrieve older young that get detached. Litter sizes vary with age, with younger females producing much smallerlitters than fully-grown females. A litter may consist of up to 16 young, but only those that reach nipples survive, and there are only 13 mammae. Mostlitters in captive colonies are 7-8 young. Captive females remain reproductively active until 18-24 months and males until 24-30 months. Longevity in captivity is 36-42 months, with a record of 49 months.

Activity patterns. Unlike several other species in the genus that have been reported to have diurnal activity, the Gray Short-tailed Opossum is apparently mostly nocturnal or crepuscular, with most activity during the first 1-3 hours after dusk and additional shorter active periods during the night.

Movements, Home range and Social organization. The Gray Short-tailed Opossum is ground dwelling, always captured in traps set at ground level. Nevertheless,it is worth noting that captured and released individuals have been seen fleeing and climbing trees up to 3 m. Gray Short-tailed Opossums are solitary and highly intolerant of other individuals, with social interactions limited to the mating period. Home ranges in the caatinga have been estimated at 0-12 ha for males and 0-18 ha for females, and density is estimated at 400 ind/km?. In a cerrado patch in Paraguay, average maximum distance traveled was 46-5 m.

Status and Conservation. Classified as Least Concern on The IUCN Red List. The Gray Short-tailed Opossum is widely distributed and has a presumably large overall population. It occurs in several protected areas, and it is quite tolerant of habitat modification.

Bibliography. Alho et al. (1986), Anderson (1997), de Andreazzi et al. (2011), Aragona & Marinho-Filho (2009), Astua (2010), Astua et al. (2003), Baggott & Moore (1990), Bergallo & Cerqueira (1994), Bonvicino, Lemos & Weksler (2005), Bonvicino, Lindbergh & Maroja (2002), Breed et al. (2003), Caceres et al. (2010), Caramaschi et al. (2011), Carvalho, Oliveira, Langguth et al. (2011), Carvalho, Oliveira, Nunes & Mattevi (2002), Cerqueira & Bergallo (1993), Christian (1983), Clark & Smith (1993), Crisp et al. (1989), Das et al. (2012), Dooley et al. (2012), Fadem (1985, 1987), Fadem & Cole (1985), Fadem & Corbett (1997), Fadem & Rayve (1985), Fadem & Schwartz (1986), Frost & Masterton (1994), Gardner (2005), Geise et al. (2010), Grant et al. (2013), Graves & Renfree (2013), Hamrick (2001), Harder & Jackson (2010), Harder, Hsu & Garton (1996), Harder, Jackson & Koester (2008), Herrera (2010), Holmes (1992b), Hume (1999a), Ivanco et al. (1996), Keyte & Smith (2009), Kimble (1997), Lammers (2007, 2009a, 2009b), Lammers & Biknevicius (2004), Lammers & German (2002), Lammers et al. (2006), Lemelin et al. (2003), Lima etal. (2012), Macrini (2004), Macrini et al. (2007), Mares et al. (1989), Maunz & German (1996, 1997), McNab (2005), Melo & Sponchiado (2012), Mikkelsen et al. (2007), Moore (1992), Neto & dos Santos (2012), van Nievelt & Smith (1997, 2005), Owen (2013), Palma & Yates (1996), Parchman et al. (2003), Paresque et al. (2004), Patton & Costa (2003), Pavan et al. (2012), Pereira & Geise (2007), Pereira et al. (2008), Pine (1979), Pine & Handley (2007), Reimer & Baumann (1995), Samollow (2006, 2008), Santori, Asta & Cerqueira (2004), Santori, Lessa & Astua (2012), Santos-Filho et al. (2008), Smith, K.K. (1994), Smith, K.K. & van Nievelt (1997), Smith, P (2008a), Solari (2010), Streilein (1982a, 1982b, 1982¢c, 1982d), Svartman (2009), Thompson et al. (2003), Trupin & Fadem (1982), Unger (1982), VandeBerg (1990), VandeBerg & Robinson (1997), Wilkinson et al. (2010).

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 Bolivia, N Argentina (Formosa), N & C Paraguay, and C & NE Brazil.