Use of zygodactylous grasp by Caluromys philander (Didelphimorphia: Didelphidae)

The present report aims to quantify the use of zygodactylous (opposability of digits II to III) grasping in relation to positional modes and support size and orientation, in the highly arboreal, walking/climbing woolly opossum, Caluromys philander. For this purpose, four captive adult C. philander were intensively video-recorded and their positional behavior, hand grasp, and support size and orientation use were analyzed frame-by-frame. Overall, C. philander used a zygodactylous grasp in 81.3±1.2% of bouts. In terms of support features, this grasp was particularly common on (a) supports that could be wholly and partly held by the animals’ hand and (b) vertical supports in particular. In a comparable manner, zygodactyly dominated during above-support positional modes, but was significantly less used during bridging and suspension. The results show that zygodactyly provided an above-support secure and steady grasp on relatively unstable arboreal supports, by aligning the hand with the main axis of the support. This very likely assisted in controlling over the applied torques during cautious quadrupedal and climbing activities with extended hand contact that characterizes the locomotor strategy of C. philander. These observations need to be further tested by more detailed kinetic studies and on a larger sample of arboreal didelphids.     

Male influence on oestrous cycles in female woolly opossum (Caluromys philander)

Plasma progesterone concentrations and the occurrence of oestrous cycles were studied in isolated woolly opossums subsequently subjected to male influences during a 40-day period. Pairing (N = 48) or exposure to male urine (N = 15) resulted in all females exhibiting oestrous during the stimulation phase, providing evidence that the activation of ovarian activity in the woolly opossum involves pheromonal cues from males. The latency of occurrence of oestrous in stimulated females depended upon their sexual state before male stimulation. In anoestrous females, the mean latency was 20.7 +/- 0.9 days (N = 35), a value which agrees with the duration of the follicular phase. In females which first entered oestrous before male stimulation, the latency of induced oestrous was inversely correlated to the date of occurrence of the previous oestrous. The inter-oestrous interval was normal (38.1 +/- 1 days, N = 5) when females were in oestrous at the beginning of male stimulation. In contrast, the inter-oestrous interval was significantly shortened (28.7 +/- 2 days, N = 7) or lengthened (51.1 +/- 1.7 days, N = 16) depending on whether females were in the luteal or follicular phases at the beginning of male stimulation. During pairing several females became pregnant and gave birth 24 +/- 0.9 days (N = 13) after copulation. In the woolly opossum, the response to male influences involves mechanisms similar to those observed in eutherians and results in enhancement and synchronization of oestrous cycles in females. Pheromonal interactions could play an important role in synchronizing oestrous cycles in wild females during the dry season, a period when animals regroup to feed on spatially localized food resources.     

Variations of chromosomal structures in Caluromys philander (Didelphimorphia: Didelphidae) from the Amazon region

Caluromys is considered to be one of the most ancient genera of extant marsupials and is positioned among the basal taxa of the family Didelphidae. At least two species occur in Brazil, C. philander and C. lanatus, both of which have 2n = 14 chromosomes. For the first time, we present evidence of an intrapopulation polymorphism of the sexual chromosome pair in C. philander females from the Central Amazon region. Detailed cytogenetic results of animals from three localities on the Amazon region were analyzed using classical cytogenetics (NOR, C-Band and G-Band) and molecular techniques (18S rDNA and telomere probes). Similar to other conspecific individuals, the diploid number of these animals is 2n = 14, and their fundamental number is 24, with NOR present on the 6th autosomal pair. The X chromosome presented variation detectable by G banding, suggesting a pericentric inversion.     

Plasma concentrations of progesterone and testosterone in captive woolly opossums (Caluromys philander)

Plasma testosterone and progesterone concentrations were measured in captive woolly opossums, a didelphid marsupial originating from neotropical forests in French Guyana. Although not exposed to cyclic environmental conditions as in the field, both sexes exhibited spontaneous circannual changes in sexual hormones. Males showed synchronous variations in plasma testosterone characterized by significant elevated concentrations during April and September (8.6 +/- 1 ng/ml, N = 5) and lower levels from May to July (3.6 +/- 0.4 ng/ml). In females, synchronous periods of 2-3 successive oestrous cycles occurred. Between these periods, females remained acyclic. The oestrous cycle, determined by urogenital smears, lasted 28-45 days (n = 14) and included a 20-day spontaneous luteal phase in which progesterone concentrations reached 30-40 ng/ml plasma. Even though testosterone concentrations in paired males increased significantly in response to oestrous periods of the paired females, spontaneous circannual rhythms of sexual activity were not well synchronized between the sexes in captivity. When compared to field data, sexual activity of captive animals followed a pattern similar to that in wild animals, without any changes in males but with a delay of 3 months in females.     

Behavior and maintenance of the woolly opossum (Caluromys) in captivity

Circadian activity, general behavior, dietary requirements, and reproductive activity were recorded in a small laboratory colony (four females, six males) of two species of the woolly opossum (Caluromys lanatus and C derbianus) over a period of 3 years. The two species were indiscernable in all aspects of their behavior. Both were completely nocturnal and rarely active during daylight hours. General behavior was apparently related to many variables, particularly individual temperament and cage size. Even docile individuals were more excitable when housed in small cages. Although the woolly opossum is reported to prefer a meat diet, the opossums in this study remained healthy on a meat-egg-fruit diet, and showed a special liking for fruit, especially bananas. Vaginal smears indicated that females of the colony were cyclic, but all attempts to breed them were unsuccessful. Sexual behavior included pre-mount, pelvic-thrust displays on the part of the male, with complete repulsion by all females.     

Hallucal grasping behavior in Caluromys (Didelphimorphia: Didelphidae): Implications for primate pedal grasping

A key feature in primate evolution is a foot with a divergent opposable hallucal metatarsal bearing a large peroneal process. Extant primates are characterized by a powerful hallucal grasp—an either “euprimate” or “plesiadapoid-euprimate” ancestor acquisition—that facilitates the exploitation of fine branches, an ability that increased the fitness of ancestral euprimates. In this context, the didelphid marsupial Caluromys has been used as the extant analog to this primate morphotype stage due to some morphological, ecological, and behavioral features. However, the extent to which and the positional and support contexts in which Caluromys uses powerful hallucal grasping are not known. This renders analogies to any mode of “euprimate” or “stem primate” grasping poorly substantiated. The present paper quantifies locomotor and postural behavior, support use, and associated frequencies of hallucal grasping in captive Caluromys philander via analysis of video recordings. During locomotion, Caluromys primarily used diagonal sequence walk, clamber, and climb, whereas stand, foot-hang, and bipedal stand were the dominant postures. Small, fine, horizontal, and moderately inclined branches were frequently used. Overall rates of “apparently powerful hallucal grasps” were high, but were exceptionally high during clamber, climb, foot-hang, and bipedal stand. Additionally, an “apparently powerful hallucal grasp” was very common upon fine, small, steep, and vertical branches. The extensive use of such powerful hallucal grasping provided stability and safety that enabled Caluromys to proficiently utilize fine branches of various orientations. The ability to negotiate such unstable supports, further reflected in foot anatomy, provides evidence that the morphobehavioral complex of Caluromys can serve as an extant analog to the plesiadapoid-euprimate ancestor, represented as a terminal branch feeder with effective hallucal grasping.     

Phylogenetic and biogeographic relationships of the mouse opossum Thylamys (Didelphimorphia,Didelphidae) in southern South America

Nucleotide sequence data from the mitochondrial cytochrome b gene were used to evaluate the phylogenetic relationships among mouse opossum species of the genus Thylamys. Based on approximately 1000 bp in five of the six species of the genus and including different localities for some of the species, we concluded that T. macrura from the subtropical forests of eastern Paraguay is the most primitive taxon. Subsequent radiation of the genus is explained mainly via founder effect speciation. This evolutionary scenario would account for the speciation of T. pusilla, T. venusta, T. pallidior, and T. elegans in the Chaco, southern Bolivia and northern Argentina, the Andean Altiplano, the Coastal Desert of Chile, and coastal Perú, respectively. Calibration of a molecular clock set the Pleistocene as the period for the differentiation of Thylamys species. The molecular results confirm the strong genetic connection between populations that inhabit the "pre-cordillera" of northern Chile (T. pallidior) and the canyons that run through the Atacama Desert to the lowlands in northern Chile. Our results confirm the occurrence of two Thylamys species in Chile, T. pallidior and T. elegans, within and south to the Atacama Desert, respectively.     

Water conservation in the South American desert mouse opossum, Thylamys pusilla (Didelphimorphia, Didelphidae).

The aim of this paper was to analyze the renal performance of the insectivorous desert mouse opossum, Thylamys pusilla, a marsupial that inhabits temperate drylands of the Neotropics. We measured the urine concentrating ability of this marsupial in the field and under three different experimental conditions in the laboratory. (1) Ad libitum treatment: animals were fed ad lib. on apples, sausages and cat food; (2) restriction treatment: foods high in nitrogen were supplied ad lib., while only apple, a food with high water to nitrogen load, was restricted, and (3) fasting: 2 days of food deprivation. Osmolarity values recorded in the field were similar to those obtained under the restriction treatment. The maximum urinary concentration found (9015 mOsm/l) is the highest reported for a marsupial and more in keeping with similarly sized desert rodents. Similar urine concentrations in T. pusilla and desert rodents suggest that xeric environments, rather than phylogeny, play a major role in water conservation. The kidney of T. pusilla possesses a long papilla and shows high renal indices (M/C: 9.37; RMT: 11.76). Our results question the idea that urine concentration is not high in desert-dwelling insectivores. Although their dietary water intake is potentially high, this may not always be sufficient to eliminate the nitrogenous waste resulting from insectivory. Thus, T. pusilla uses its ability to conserve water to overcome periods of food shortage and high nitrogen load.     

Isolation and characterization of microsatellite loci in the woolly mouse opossum,Micoureus paraguayanus (Marsupialia: Didelphimorphia)

Five microsatellite loci were isolated and characterized within the woolly mouse opossum (Micoureus paraguayanus), a Neotropical marsupial, using an enrichment cloning procedure. Between four and seven alleles were detected per locus, with expected heterozygosity ranging from 0.358 to 0.560. These microsatellites should provide useful markers in a variety of genetic analyses to examine parentage, inbreeding, population structure and population dynamics in fragmented forest habitats.     

Carpal ontogeny in Monodelphis domestica and Caluromys philander (Marsupialia)

Carpal bones have experienced numerous changes during marsupial evolution, even though their diversity and development remain poorly studied. The aim of this work was to document adult form and the pattern of mesenchymal tissue condensation and formation of chondrification and ossification centers in the hand of two marsupials. Two fundamental questions were asked: whether the loss of embryonic precursors was associated with the loss of adult elements, or whether there were developmental signs of ancestral mammalian elements that have been fused or lost in marsupial taxa. We were also interested to find out whether there is sexual dimorphismus in the carpals, as has been reported for some didelphids. Histological sections, cleared and stained specimens and macerated skeletons representing an ontogenetic series of Monodelphis domestica were used to document carpal development. Comparisons were made with perinatal stages of Caluromys philander and with adult specimens of other marsupials. A prenatal M. domestica in the 13th day after conception has a cell condensation that because of its position is homologized with a centrale, which is at birth already lost or fused. Neonatal M. domestica and C. philander have the number and arrangement of their adult carpal anatomy. Trapezium and trapezoid start ossification later than most other carpals, while pisiform and prepollex are the last to do so. Adult males of M. domestica have relatively larger and more robust pisiforms, compared to other carpals, than females. This sexual dimorphism develops relatively late as it was not recorded in male specimens around 160 days old. An extra sesamoid bone located just distal to the radius and proximo-palmar to the scaphoid was recorded in specimens of C. philander, C. derbianus and Didelphis virginiana.     

Delineating geographic boundaries of the woolly mouse opossums, Micoureusdemerarae and Micoureus paraguayanus (Didelphimorphia: Didelphidae)

This paper reports on molecular classification of the woolly mouse opossum, Micoureus spp., in the southeastern Atlantic Forest in Brazil, a hotspot of critically threatened biodiversity. Phylogenetic analysis and character-based diagnosis were done using DNA sequences from the mitochondrial cytochrome b gene and cytochrome c oxidase subunit I genes, and exon 6 of the nuclear dentine matrix protein 1 gene (DMP1). Although the nuclear DMP1 gene showed insufficient genetic variation for species diagnosis, the mtDNA analyses resulted in the robust grouping of samples of the M. paraguayanus/M. demerarae complex into three clades with distinct DNA sequence diagnostics for the species units in this study. The results support the species status of M. paraguayanus (Tate in Am Mus Novit 493: 1–13, 1931), which has a geographic distribution in the Atlantic Forest from the North and Northeast of Minas Gerais state in Brazil, going south along the coastal region of Brazil, to Paraguay and Argentina. Evidence of the boundary for this species and the provided diagnostics should facilitate and improve accuracy of studies that have been done in critical threatened fragments of the Atlantic Forest, especially in Minas Gerais and Bahia states, Brazil.     

Reproduction ofDidelphis marsupialis (Didelphimorphia: Didelphidae) in the Venezuelan Andes

The reproductive cycle of the common opossumDidelphis marsupialis Linnaeus, 1758, inhabiting an agricultural area in the Venezuelan Andes was studied by live-trapping for 18 months (from July 1998 to December 1999). Trap success was slightly higher in the less humid months. Most females captured breed during the least rainy period, with two different birth peaks: January-March and April-June, a minor reproductive event occurs from August to October. Reproductive activity ofD. marsupialis appears closely associated with precipitation.     

Mitochondrial genetic variability of Didelphis albiventris (Didelphimorphia, Didelphidae) in Brazilian localities

Didelphis albiventris is a well-known and common marsupial. Due to its high adaptability, this very widespread generalist species occurs under various environmental conditions, this even including protected regions and disturbed urban areas. We studied a 653 bp fragment of cytochrome oxidase c (COI) from 93 biological samples from seven Brazilian localities, with linear distances ranging between 58 and about 1800 km to analyze the effects of geographic distances on variability and genetic differentiation. The haplotype network presented nine haplotypes and two genetic clusters compatible with the two most distant geographic areas of the states of Minas Gerais, in the southeast, and Rio Grande do Sul, in the extreme south. As each cluster was characterized by low nucleotide and high haplotype diversities, their populations were obviously composed of closely related haplotypes. Surprisingly, moderate to high F(ST) differentiation values and a very weak phylogeographic signal characterizes interpopulation comparisons within Minas Gerais interdemes, these being correlated with the presence of privative haplotypes. On a large rgeographic scale, a comparison between demes from Minas Gerais and Rio Grande do Sul presented high F(ST) values and a robust phylogeographic pattern. This unexpected scenario implies that mtDNA gene flow was insufficient to maintain population cohesion, reflected by the observed high differentiation.     

The diversification of the genus Monodelphis and the chronology of Didelphidae (Didelphimorphia)

To evaluate the monophyletic status of the genus Monodelphis, and its species complexes, we used a 9.3‐kb multimarker alignment to build a phylogenetic tree based on the largest taxon sampling for this didelphid genus to date. Furthermore, using a Bayesian framework and six calibration points, we inferred the divergence times for the major Monodelphis lineages and their current geographical distribution to perform an ancestral state reconstruction for geographical areas. Our results indicate the monophyletic nature of Monodelphis and suggest ‘kunsi’ as a new species complex that includes Monodelphis kunsi and an undescribed species. Monodelphis is further subdivided into three clades showing a common vicariance pattern, with each major clade consisting of a northern South American lineage joined with an Atlantic Forest lineage. This geographic consistency suggests a vicariant event that might have been related to a warm period at the Oligocene/Miocene border, according to our time results. © 2015 The Linnean Society of London     

First evidence of gregarious denning in opossums (Didelphimorphia,Didelphidae), with notes on their social behaviour

The Didelphidae are considered solitary opossums with few social interactions, usually limited to mating-related or mother–pouch young interactions. Anecdotal reports suggest that additional interactions occur, including den sharing by a few individuals, usually siblings. Here, we report novel observations that indicate opossums are more social than previously thought. These include nest sharing by males and females of Marmosa paraguayana, Gracilinanus microtarsus and Marmosops incanus prior to the onset of the breeding season and without signs of sexual activity; this is taken to indicate early pair-bonding matching and cooperative nest building. We also recorded den sharing among recently weaned siblings of Didelphis aurita and Caluromys philander. In addition, we observed 13 individuals of Didelphis albiventris representing three age classes resting without agonistic interactions in a communal den. These are the first reports of gregarious behaviour involving so many individuals, which are either unrelated or represent siblings from at least two litters, already weaned, sharing the same den with three adults. Sociality in opossums is probably more complex than previously established, and field experimental designs combining the use of artificial nests with camera traps or telemetry may help to gauge the frequency and extent of these phenomena.     

Diet of the gracile mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae) in a neotropical savanna: intraspecific variation and resource selection

Investigation of the effect of endogenous and exogenous factors on the diet of animals is necessary for a better understanding of their feeding habits. This approach can provide relevant information on the autoecology of a species and its ecological interactions. We investigated the composition and intraspecific variation in the diet of the marsupial Gracilinanus agilis in areas of dry woodland forests (i.e., cerradão) in the Cerrado of Central Brazil, taking into consideration the availability of prey (arthropods) in the environment. We found insects, spiders, birds, and fruits in the scats of G. agilis. Insects (orders Hymenoptera, Isoptera, Hemiptera, and Coleoptera) and fruits were the most frequently consumed resources. Males fed more heavily on insects than females did, whereas during the warm–wet season (October to April), the reproductive females fed on insects more than the nonreproductive females did. On the other hand, the consumption of fruits and vertebrates did not vary between seasons, sexes, or according to female reproductive condition. Moreover, reproductive females fed more frequently on ants and beetles than nonreproductive females did. We also detected both positive (for Isoptera and Hemiptera) and negative (for Hymenoptera) selection of insects during the cool–dry season, whereas in the warm–wet season, these resources were consumed according to their availability in the environment. Our study revealed that G. agilis is an insectivore–omnivore species, but fruits also are a relevant part of its diet. This marsupial seemed to select their prey qualitatively according to its energy demands and nutritional requirements.