Caluromys Philander Research Articles

Comparative gross morphology of the digestive tract in ten Didelphidae marsupial species

Natural diets of Didelphidae species vary in the amounts of invertebrates, fruits and small vertebrates eaten. We investigated the digestive morphology of ten species of didelphid marsupials varying in food habits. The purpose was to describe and to compare the shape and relative size of the digestive tract portions among species studied and relate them to food habits. The form of the gastrointestinal tract in this family is simple, with a unilocular stomach, small intestine, large intestine and caecum. Caluromys philander was the species with highest association between digestive tract measurements and its frugivorous habits. However, although its caecum is morphologically distinct from the other species, the relative length is small when compared to the more faunivorous Metachirus nudicaudatus. Stomach length of Philander frenata is related to a more carnivorous diet, while large intestine length of Didelphis aurita is related to its omnivore diet. The digestive tract measurements of the other species appear to be related with a variable degree of morphological differentiation from a generalized form related to omnivory toward a more carnivorous diet. Great caecum relative size distinguished Metachirus nudicaudatus from the most other species and its relationship with diet is not well understood.

The rod opsin pigments from two marsupial species, the South American bare-tailed woolly opossum and the Australian fat-tailed dunnart

Rod visual pigment genes have been studied in a wide range of vertebrates including a number of mammalian species. However, no marsupials have yet been examined. To correct this omission, we have studied the rod pigments in two marsupial species, the nocturnal and frugivorous bare-tailed woolly opossum, Caluromys philander, from Central and South America, and the arhythmic and insectivorous fat-tailed dunnart, Sminthopsis crassicaudata, from Australia. Phylogenetic analysis establishes that the cloned opsin sequences are orthologues of rod opsin genes from other vertebrate species. The deduced amino acid sequences show that both possess glutamate at residue 122, a feature of rod opsins, and the corresponding gene follows the typical vertebrate rod opsin pattern of five exons separated by four introns. Compared to other vertebrates, a stretch of five residues near the C-terminus is deleted in the rod opsin of both marsupials and all eutherian mammals. From microspectrophotometric measurements, the pigments in the two species show an 8 nm difference in peak absorbance; the molecular basis for this spectral shift is discussed and two candidate substitutions are identified.

Forest Structure and Vertical Stratification of Small Mammals in a Secondary Atlantic Forest, Southeastern Brazil

This study investigated the differential capture rates of small mammals in different strata of a secondary forest, Minas Gerais State, Brazil. From March through October 1994 mammals were live-trapped at ground, understory and mid-story level. Five species of marsupials and six species of rodents were recorded. Didelphis aurita, Marmosops incanus, Metachirus nudicaudatus, and Oryzomys spp. were captured mostly on the ground, while Caluromys philander, Micoureus demerarae, Rhipidomys mastacalis and Sciurus aestuans were sampled mainly at 5-12 m height. Species richness was correlated with structural complexity of the forests surveyed. On the other hand, a relationship between species richness and habitat heterogeneity was not detected. These results suggest that local saturation of small mammal species, rather than regional species richness, is determined by the level of habitat complexity. The conservation of stratified forests, such as those found at the Parque Estadual do Rio Doce and the other sites in the Rio Doce valley, are therefore essential for the maintenance of local species diversity.

Footfall patterns and interlimb co‐ordination in opossums (Family Didelphidae): evidence for the evolution of diagonal‐sequence walking gaits in primates

Most primates typically use a diagonal‐sequence footfall pattern during walking. This footfall pattern, which is unusual for mammals, is believed to have originated in ancestral primates in association with the use of grasping extremities for movement and foraging on thin, flexible branches. This theory was tested by comparing gait parameters between the grey short‐tailed opossum Monodelphis domestica and the woolly opossum Caluromys philander, two didelphid marsupials that are strongly differentiated in grasping morphology of the extremities and in their reliance on foraging strategies involving thin branches. One hundred and thirty gait cycles were analysed quantitatively from videotapes of subjects moving quadrupedally on a runway and on poles of different diameters (7 and 28 mm). Duty factor (i.e. duration of the stance phase as a percentage of the stride period) for the forelimb and hindlimb, as well as diagonality (i.e. phase relationship between the forelimb and hindlimb cycles), were calculated for each of these symmetrical gait cycles. We found that the highly terrestrial Monodelphis, like most other non‐primate mammals, relies primarily on lateral‐sequence walking gaits on both runway and poles, and has relatively higher forelimb duty factors. Like primates, the highly arboreal Caluromys uses primarily diagonal‐sequence walking gaits on the runway and pole, with relatively higher hindlimb duty factors and diagonality. The fact that the woolly opossum, a marsupial with primate‐like feet that moves and forages mainly on thin branches, uses primarily diagonal‐sequence gaits when walking supports the view that primate gaits evolved to meet the demands of locomotion on narrow supports. This also demonstrates the functional role of a grasping foot, in association with relatively higher hindlimb duty factors, protraction, and substrate reaction forces, in the production of such walking gaits.

Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula.

The development of the scapula was studied in embryonic and postnatal specimens of Monodelphis domestica and perinatal specimens of Philander opossum, Caluromys philander, and Sminthopsis virginiae using histological sections and 3D reconstructions. Additionally, macerated skeletons of postnatal M. domestica were examined. This study focused on the detachment of the scapulocoracoid from the sternum and on the acquisition of a supraspinous fossa, a supraspinatus muscle, and a scapular spine, all these events associated with the origin of the therian shoulder girdle. In none of the specimens is there a continuity of the cartilaginous scapulocoracoid with the sternum, even though the structures are in close proximity, especially in S. virginiae. At birth, the first rib laterally presents a pronounced boss that probably contacts the humerus during certain movements. Only the acromial portion of the scapular spine, which originates from the anterior margin of the scapular blade, is preformed in cartilage. The other portion is formed by appositional bone ("Zuwachsknochen"), which expands from the perichondral ossification of the scapula into an intermuscular aponeurosis between the supra- and infraspinous muscles. This intermuscular aponeurosis inserts more or less in the middle of the lateral surface of the developing scapula. Thus, the floor of the supraspinous fossa is present from the beginning of scapular development, simultaneously with the infraspinous fossa. The homology of the therian spine with the anterior border of the sauropsid and monotreme scapula is questioned. We consider the dorsal portion (as opposed to the ventral or acromial portion) of the scapular spine a neomorphic structure of therian mammals.

Origins of primate locomotion: gait mechanics of the woolly opossum.

The locomotion of primates differs from that of other mammals in three fundamental ways. During quadrupedal walking, primates use diagonal sequence gaits, protract their arms more at forelimb touchdown, and experience lower vertical substrate reaction forces on their forelimbs relative to their hindlimbs. It is widely held that the unusual walking gaits of primates represent a basal adaptation for movement on thin, flexible branches and reflect a major change in the functional role of the forelimb. However, little data on nonprimate arboreal mammals exist to test this notion. To that end, we examined the gait mechanics of the woolly opossum (Caluromys philander), a marsupial convergent with small-bodied prosimians in ecology, behavior, and morphology. Data on the footfall sequence, relative arm protraction, and peak vertical substrate reaction forces were obtained from videotapes and force records for three adult woolly opossums walking quadrupedally on a wooden runway and a thin pole. For all steps recorded on both substrates, woolly opossums always used diagonal sequence walking gaits, protracted their arms beyond 90 degrees relative to horizontal body axis, and experienced peak vertical substrate reaction forces on forelimbs that were significantly lower than on hindlimbs. The woolly opossum is the first nonprimate mammal to show locomotor mechanics that are identical to those of primates. This case of convergence between primates and a committed fine-branch, arboreal marsupial strongly implies that the earliest primates evolved gait specializations for fine-branch locomotion, which reflect important changes in forelimb function.

Frequency of movements of small mammals among Atlantic Coastal Forest fragments in Brazil

Rates of interfragment movements were estimated for small mammals inhabiting a group of eight Atlantic Coastal Forest fragments, surrounded by grassland matrix, in order to understand the degree to which each species' population was isolated. Didelphis aurita showed the greatest movement rate (19.4% of recaptures showing interfragment movements), followed by Metachirus nudicaudatus (10.0%), Philander frenata (7.5%), Nectomys squamipes (3.6%), Micoureus demerarae (1.2%) and Akodon cursor (0.25%). Interfragment movements were not detected for Caluromys philander, Oecomys concolor and Oligoryzomys nigripes. Species can be placed along a continuum which goes from species that are represented by a single population in the whole study area, through those with metapopulations, to species that have isolated populations in each fragment. Ability to move among fragments was not related to abundance in the matrix; nevertheless, such ability helps to explain the persistence of species in fragments otherwise too small to support viable populations.

Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals.

This study is based on the examination of histological sections of specimens of different ages and of adult ossicles from macerated skulls representing a wide range of taxa and aims at addressing several issues concerning the evolution of the ear ossicles in marsupials. Three-dimensional reconstructions of the ear ossicles based on histological series were done for one or more stages of Monodelphis domestica, Caluromys philander, Sminthopsis virginiae, Trichosurus vulpecula, and Macropus rufogriseus. Several common trends were found. Portions of the ossicles that are phylogenetically older develop earlier than portions representing more recent evolutionary inventions (manubrium of the malleus, crus longum of the incus). The onset of endochondral ossification in the taxa in which this was examined followed the sequence; first malleus, then incus, and finally stapes. In M. domestica and C. philander at birth the yet precartilaginous ossicles form a supportive strut between the lower jaw and the braincase. The cartilage of Paauw develops relatively late in comparison with the ear ossicles and in close association to the tendon of the stapedial muscle. A feeble artery traverses the stapedial foramen of the stapes in the youngest stages of M. domestica, C. philander, and Sminthopsis virginiae examined. Presence of a large stapedial foramen is reconstructed in the groundplan of the Didelphidae and of Marsupialia. The stapedial foramen is absent in all adult caenolestids, dasyurids, Myrmecobius, Notoryctes, peramelids, vombatids, and phascolarctids. Pouch young of Perameles sp. and Dasyurus viverrinus show a bicrurate stapes with a sizeable stapedial foramen. Some didelphids examined to date show a double insertion of the Tensor tympani muscle. Some differences exist between M. domestica and C. philander in adult ossicle form, including the relative length of the incudal crus breve and of the stapes. Several differences exist between the malleus of didelphids and that of some phalangeriforms, the latter showing a short neck, absence of the lamina, and a ventrally directed manubrium. Hearing starts in M. domestica at an age in which the external auditory meatus has not yet fully developed, the ossicles are not fully ossified, and the middle ear space is partially filled with loose mesenchyme. The ontogenetic changes in hearing abilities in M. domestica between postnatal days 30 and 40 may be at least partially related to changes in middle ear structures.

Ontogenetic and phylogenetic transformations of the vomeronasal complex and nasal floor elements in marsupial mammals

Histological sections and three-dimensional reconstructions of section-series were used to document the anatomy of the vomeronasal complex and other aspects of the ethmoidal region in representatives of 13 families and six orders of marsupial mammals, including for the first time Microbiotheria. The changes during growth of several features were examined in ontogenetic series. Marsupials are very conservative in comparison with eutherians regarding the vomeronasal complex. All have a vomeronasal organ and a nasopalatine duct, have no nasopalatine duct cartilage, have no (or just an incipient) palatine cartilage, and the overall construction of the nasal floor is uniform across species. Most features examined show a high degree of homoplasy (e.g. presence of glandular ridges, isolated dorsal process of the paraseptal cartilage), and their systematic value is confined to low taxonomic levels. Significant ontogenetic changes occur in features usually discussed in the systematic/taxonomic literature. Amongst the didelphids examined, Caluromys philander shows several autapomorphies. It is hypothesized that the opening of the VNO into the upper end of the nasopalatine duct was present in the marsupial groundplan. Most marsupials have a large and horizontal anterior transverse lamina, the plesiomorphic condition, which becomes oblique in diprotodontians. Some features are autapomorphies of well-supported monophyletic groups of marsupials, e.g. the conspicuous internasal communication of perameliformes and the «tube-like» or ring-shaped paraseptal cartilage of vombatiformes. An outer bar joining the middle (and not the dorsal-most portion) of the paraseptal cartilage characterizes Australasian marsupials and Dromiciops, with the exclusion of perameliformes, and evolved independently in Caluromys philander.

Ontogenetic and phylogenetic transformations of the vomeronasal complex and nasal floor elements in marsupial mammals

Abstract Histological sections and three-dimensional reconstructions of section-series were used to document the anatomy of the vomeronasal complex and other aspects of the ethmoidal region in representatives of 13 families and six orders of marsupial mammals, including for the first time Microbiotheria. The changes during growth of several features were examined in ontogenetic series. Marsupials are very conservative in comparison with eutherians regarding the vomeronasal complex. All have a vomeronasal organ and a nasopalatine duct, have no nasopalatine duct cartilage, have no (or just an incipient) palatine cartilage, and the overall construction of the nasal floor is uniform across species. Most features examined show a high degree of homoplasy (e.g. presence of glandular ridges, isolated dorsal process of the paraseptal cartilage), and their systematic value is confined to low taxonomic levels. Significant ontogenetic changes occur in features usually discussed in the systematic/taxonomic literature. Amongst the didelphids examined, Caluromys philander shows several autapomorphies. It is hypothesized that the opening of the VNO into the upper end of the nasopalatine duct was present in the marsupial groundplan. Most marsupials have a large and horizontal anterior transverse lamina, the plesiomorphic condition, which becomes oblique in diprotodontians. Some features are autapomorphies of well-supported monophyletic groups of marsupials, e.g. the conspicuous internasal communication of perameliformes and the «tube-like» or ring-shaped paraseptal cartilage of vombatiformes. An outer bar joining the middle (and not the dorsal-most portion) of the paraseptal cartilage characterizes Australasian marsupials and Dromiciops , with the exclusion of perameliformes, and evolved independently in Caluromys philander .

Foraging strategies and food partitioning in the neotropical frugivorous mammals Caluromys philander and Potos flavus

AbstractThe bare‐tailed woolly opossum, Caluromys philander, and the kinkajou, Potos flavus, are two syntopic neotropical nocturnal, arboreal and frugivorous mammals. Because of close ecology but great difference in size (weight 300 vs 3000 g), they represent pertinent models to examine the influence of size on foraging strategy. These species were studied by radio‐tracking and direct observation during 22 months in a tropical forest in French Guiana. Both mammals’ foraging strategies with regard to flowers and fruits are characterized as follows: (1) numerous plant families and species are exploited; (2) most plant species are selected according to their abundance; (3) diet selectivity and diversity are similar in both mammals; (4) relative parts of flowers and fruits in the diet vary according to their year‐long availability; (5) the choice of fruiting species is not related to the morphological type, size, or nutritious quality of fruits but instead depends on easy access to the edible part; (6) the length of foraging bouts is correlated with production for the most frequently exploited tree species; (7) feeding bouts are shorter in P. flavus than in C. philander; (8) P. flavus exploits large, highly productive canopy trees, while C. philander also visits canopy trees with low production and understorey trees. In conclusion, both mammals are opportunistic flower‐ and fruit‐eaters, but the larger species (P. flavus) exploits larger, more scattered food patches, while the smaller one (C. philander) also exploits smaller, more numerous and more evenly distributed food patches.

Frugivory and taste responses to fructose and tannic acid in a prosimian primate and a didelphid marsupial

The taste responses to sweet and astringent compounds were investigated in two mammals of similar ecology, by using the classical method of the two-bottle test. The taste threshold for fructose was higher in Microcebus murinus, a prosimian primate, than in Caluromys philander, a didelphid marsupial. The profiles of suprathreshold responses resembled a dissymmetric bell-shaped curve, but the rate of consumption of sweet solutions up to maximal intake increased more rapidly in Microcebus than in Caluromys. Despite showing a photoperiod-synchronized physiology, Microcebus displayed no seasonal variation of the taste threshold and suprathreshold responses. The depressing effect of tanning acid on the ingestion of fructose solutions increased progressively with tannin concentration and was lower as fructose concentration increased. Inhibition thresholds for tannic acid were similar between the two species. The data suggest that adaptation to frugivorous diets is associated with globally similar shaping of the taste responses, even though subtle differences of palatability may account for differences of feeding selectivity.

The Influence of Moonlight on Activity of Woolly Opossums (Caluromys philander)

Activity of four radiocollared woolly opossums ( Caluromys philander ) showed an inverse relationship between moonlight and both level and duration of the activity period. However, between new moon and half-moon, both measures of activity in females remained low on average, whereas they decreased sharply in males. The influence of moonlight on activity, as well as the general activity pattern in this nocturnal marsupial, are interpreted as anti-predation adaptations. The level of activity seems to be constantly lower, and independent of moonlight intensity, in females of C. philander . Moonlight could reduce activity, not linearly but above a threshold in light intensity, for higher levels of activity reached only in males.

Growth of Pouch Young in the Bare-Tailed Woolly Opossum, Caluromys philander

Growth of pouch young from birth to first exit from pouch was recorded in female bare-tailed woolly opossums, Caluromys philander , a didelphid marsupial from French Guiana. An age-predicting curve was assessed for its use in determining the age of pouch young from length of body in free-living individuals. Increase in body mass of sucklings during pouch life indicates the level of maternal investment during lactation; reproductive effort appears to be low during the first 40 days of pouch life, then increasing to a higher rate in the last 40 days. Maternal investment during lactation is discussed in light of variations in energetic cost during lactation.

Use of space by the woolly opossum Caluromys philander (Marsupialia, Didelphidae) in French Guiana

Use of space by a woolly opossum (Caluromys philander) population in a primary forest of French Guiana was examined by trapping and radio tracking during 27 months over a period of 3.5 years. Mean home-range size was about 3 ha. Home ranges widely overlapped between both males and females. Use of space was more evenly distributed during the season of fruit scarcity than during the season of fruit abundance. The location of the core area within the home range was correlated with the location of feeding sites. A high dispersal rate was observed in both young and adults. Space-use patterns were influenced to some extent by factors relating to the environment (food availability) and the individual (energy needs of females related to maternal investment). Nevertheless, ranging behaviour varied greatly among individuals. Space-use patterns appear to be highly opportunistic in this species and may explain why C. philander has colonized a vast range of habitats over a wide geographical area.

Optimal litter size: Does it cost more to raise a large litter in Caluromys philander?

Food intake of lactating Caluromys philander, a didelphid marsupial, was recorded from parturition until weaning of the pouch young. Variation in the average caloric value of daily food intake throughout lactation, in relation to litter size, showed no significant differences, but females increased food intake during late lactation, prior to weaning. Food intake was positively correlated with total litter mass at weaning. Moreover, there were significant differences in body mass and body length of offspring at first pouch exit (3 months) and at weaning (4 months): young born in small litters (1–3) were bigger than those born in large litters (6–7). Reproductive success is discussed on the assumption that pouch-young survival depends on food resources.

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.

Feeding and Reproduction of Three Didelphid Marsupials in Two Neotropical Forests (French Guiana)

The reproductive patterns of three didelphid marsupial species (Caluromys philander, Didelphis marsupialis and Philander opossum) were studied in secondary and mature forest in French Guiana in relation to food supply and seasonal variation. Both forests exhibited a period of low fruit availability which was longer and more acute in the mature forest. Nevertheless, survival rate of pouch young was higher for C. philander and P. opossum in the mature forest. It was correlated with high nectar availability during the season of fruit scarcity, and with lower population density compared to the secondary forest site. Conversely, D. marsupialis had a more seasonal breeding pattern, with low mortality of pouch young on both sites, and thus appeared less directly dependent on environmental conditions. Annual variations in body weight were compared for the three species on both study areas. Influence of parturition dates, age and body weight of the female upon litter size and pouch young survival is discussed.

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.

Dynamique de Population chez Trois Marsupiaux Didelphides de Guyane

Five species of Didelphid marsupials were trapped live, marked, and released in a secondary forest in French Guiana during a 26mo field study. Data on body weight, body length, dental stage, and reproductive state of females were collected. A total of 851 individuals, including 372 pouch-young, were monitored in 2273 captures. This abundance of data we made led us to a comparative analysis of the population dynamics of three species: Didelphis marsupialis, Philander opossum, and Caluromys philander, which represented 94 percent of the whole captures. Some data on the two other species, Marmosa murina and M. cinerea, were added for comparison. These sympatric Didelphids are nocturnal, with a basically frugivorous and insectivorous diet. The three main species have high densities, high reproductive rates, short life-spans, and rapid population turnover. There are some differences in these parameters, mainly between the arboreal species, C. philander, and both terrestrial species, D. marsupialis and P. opossum. Although all have few social interactions and show a lack of territoriality, C. philander appear to have a longer life-span, a lower reproductive rate and a more sedentary population. M. cinerea were very rare in this area, whereas M. murina show large density variation. LA FAMILLE DES DIDELPHIDES est l'une des deux dernieres familles de Marsupiaux vivant encore sur le continent americain. Elle rassemble pres de 80 especes en 12 genres diffe les conditions particulierement favorables dont nous avons beneficie en Guyane ont permis d'aborder cet aspect de l'adaptation de ces animaux a leur milieu.