Population dynamics of dasyurid marsupials in dryland Australia: Variation across habitat and time

The irruptive population dynamics of rodents are a globally renowned wildlife phenomenon; however, the dynamics of other small mammals with which rodents are sympatric are poorly understood. Dryland Australia supports a high diversity of small (<200 g) arthropod‐eating marsupials (Dasyuridae). Here, we test the hypothesis that dasyurid marsupials do not exhibit the same degree of irruptive population dynamics that are shown by rodents. We addressed this question by sampling small mammal assemblages on 20 permanent trapping sites in the Simpson Desert on 20 occasions from 2007 to 2017. Sampling was stratified across three broad habitat types: sandridge, gibber plain and clay plain. We captured 478 dasyurid marsupials of nine species, ranging in mean body mass from 5.75 to 93.50 g, at a capture rate of 1.71 per 100 trap‐nights. Capture rate varied across habitat and over time and the interaction between these two effects was also significant. Capture rate was highest on clay plain (3.35 captures/100 trap‐nights), followed by gibber plain (2.16 captures/100 trap‐nights) and lowest on sand habitat (0.54 captures/100 trap‐nights). Each species had a clear preference for one of the dominant habitat types. Dasyurid assemblages responded to high rainfall pulses in November–December 2008 and January 2015; however, the largest rainfall period in 2010–2011 resulted in very low captures. Likewise, a peak in abundance occurred in April 2008 although it was not preceded by high rainfall. We conclude that, although dasyurid marsupial capture rates varied up to 34 fold during the study period, population changes are not strongly tied to rainfall. Heterothermic physiology in this family, in particular the ability to use daily torpor to save energy, may be central to the decoupling of population dynamics from rainfall‐driven primary productivity.     

Cardiovascular characteristics of two resting marsupials: An insight into the cardio-respiratory allometry of marsupials

Summary Minimum resting values for several cardiovascular and respiratory characteristics were established for two marsupial species,Trichosurus vulpecula andMacropus eugenii. Certain characteristics including heart rate, stroke volume and cardiac output varied significantly with body mass and allometric equations of the formy=aM ^b were derived to describe the relationships. The exponents of body mass,b, were generally similar to those for eutherian mammals, but in the marsupials they intercept,a, differed significantly from reported eutherian values.Although resting cardiac output in the marsupials appeared reduced in proportion to their lower resting oxygen consumption this pattern was not repeated for other variables. The stroke volume of the marsupials was 156% of eutherian levels while heart rate was less than 50% of the eutherian values.Initial data for respiratory variables also indicated comparable differences in this aspect of oxygen transport between marsupials and eutherians. Minimum respiratory rates of the marsupials were much lower than those of eutherians and tidal volumes appear larger in marsupials. The results are interpreted as suggesting that marsupials may have a large aerobic capacity.     

Identification of zoonotic Giardia genotypes in marsupials in Australia

A total of 421 fecal samples from a variety of captive and wild marsupial hosts in Western Australia, Victoria and South Australia were screened for the presence of Giardia species/genotypes using PCR and sequence analysis of a fragment of the 18S rRNA gene. Giardia spp. were identified in 13.4% (28/209) of samples from captive marsupials and 13.7% (29/212) of samples from wild marsupials. Sequence analysis at the 18S locus identified the zoonotic Giardia duodenalis Genotypes A and B in both captive and wild marsupials. Eight isolates were typed as genotype B3 and B4 at the gdh locus, although 7/8 were typed as genotype A at the 18S rRNA locus. The possible reasons for this discordance are discussed. This is the first report of genotype B and only the second report of genotype A in marsupials. As some of the genotype B isolates were identical to human-derived Giardia gdh sequences, these results suggest that marsupials in catchments may pose a public health risk and therefore warrant further investigation.     

Evaluation of PVA Models of Arboreal Marsupials: Coupling Models with Long-term Monitoring Data

This paper reports the outcomes of a novel inter-twining of long-term monitoring data and population modelling to assess the accuracy of predictions of a Population Viability Analysis (PVA) model. In particular, the relative effectiveness of different management options for reserving areas from timber harvesting was assessed for two forest-dependent arboreal marsupials, the greater glider (Petauroides volans) and Leadbeater's Possum (Gymnobelideus leadbeateri). We used data from 7 years of monitoring conducted at 161 sites to assess and modify, where appropriate, previous population models of the two species of arboreal marsupials. The results indicated that the importance of food resources for both had been underestimated in past work. Despite this, the modified models that included increased importance of food availability did not change the predicted risks of decline substantially, particularly for Leadbeater's Possum. Importantly, past conclusions about the optimal sizes of patches to reserve within the forests used wood production were robust to changes in the model. This is a valuable finding because the work we report is one of the first to empirically test the robustness of the relative predictions of a PVA model. Nevertheless, the new insights we derived from this study have implications both for: (1) the implementation of our ongoing long-term monitoring study, in particular the value of what can be termed ȁ8adaptive monitoring', and, (2) the establishment of a new silvicultural experiment designed to better create habitat for arboreal marsupials within logged and regenerated sites.     

Cranial Anatomy of the Earliest Marsupials and the Origin of Opossums

Background

The early evolution of living marsupials is poorly understood in part because the early offshoots of this group are known almost exclusively from jaws and teeth. Filling this gap is essential for a better understanding of the phylogenetic relationships among living marsupials, the biogeographic pathways that led to their current distribution as well as the successive evolutionary steps that led to their current diversity, habits and various specializations that distinguish them from placental mammals.

Methodology/Principal Findings

Here we report the first skull of a 55 million year old peradectid marsupial from the early Eocene of North America and exceptionally preserved skeletons of an Oligocene herpetotheriid, both representing critical groups to understand early marsupial evolution. A comprehensive phylogenetic cladistic analysis of Marsupialia including the new findings and close relatives of marsupials show that peradectids are the sister group of living opossums and herpetotheriids are the sister group of all living marsupials.

Conclusions/Significance

The results imply that North America played an important role in early Cenozoic marsupial evolutionary history and may have even been the center of origin of living marsupials and opossums. New data from the herpetotheriid postcranium support the view that the ancestral morphotype of Marsupialia was more terrestrial than opossums are. The resolution of the phylogenetic position of peradectids reveals an older calibration point for molecular estimates of divergence times among living marsupials than those currently used.     

OSSIFICATION HETEROCHRONY IN THE THERIAN POSTCRANIAL SKELETON AND THE MARSUPIAL–PLACENTAL DICHOTOMY

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.     

Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy.

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.     

Evolution of the shell coat and yolk in amniotes: a marsupial perspective

Two characters distinguish oogenesis and early development in marsupials and monotremes: (1) the shell coat that persists from the zygote to somite stages in marsupials or until hatching in monotremes; and (2) the numerous, apparently almost empty vesicles that appear in primary oocytes, increase during oogenesis in marsupials and monotremes before being shed into the cleavage cavity and are preferentially distributed to the trophoblast lineage in marsupials, but comprise the latebra in monotremes. Analysis of these unusual characters used Southern analysis of genomic DNA dot blots and histology and electron microscopy. The evidence suggests that the marsupial shell coat protein, CP4, was probably characteristic of the egg of the mammalian ancestor. Further, the vesicles, present in marsupials during oogensis and cleavage and in eutherian mammals during blastocyst formation are the residual elements of white yolk present in the larger yolky eggs of monotemes and sauropsids. By comparison with the function of the vesicle components in marsupials, it is suggested that one role for the white yolk in monotremes and the sauropsids is to provide extracellular matrix (ECM), especially hyaluronan containing stabilizing proteins, for epithelial construction. Thus, as oviparity was replaced by viviparity, egg size was reduced, the germinal cytoplasm was retained, and yellow yolk was markedly reduced or lost in marsupials and eutherians. The white yolk was retained in monotremes and marsupials where blastocyst epithelial construction requires ECM support, and its appearance is heterochronously shifted to after compaction, when blastocyst formation and expansion occurs, in eutherian mammals.     

The origin of eutherian mammals

Palaeontologically recognizable eutherians originated no later than the Early Cretaceous in warm, probably moderately seasonal climates. Immediate ancestors were small, sharing many anatomical, physiological and reproductive features with small modern marsupials. Development of characteristically eutherian features involved interactions of body size, rates of metabolism, energetic costs of reproduction, anatomical/physiological processes of development and effects of each upon rates of population growth. In contrast to eutherians, marsupials have a narrow range of basal metabolic rates (lacking high rates), and show no direct links between rate of energy expenditure and gestation period, postnatal growth rate, fecundity or reproductive potential. Biological implications of this contrast are most pronounced at small body sizes. When resources are abundant, the relatively higher growth rates and earlier maturation of small eutherians (particularly those with high rates of metabolism) can lead to rapid population growth; among most marsupials, however, both pre- and postnatal constraints apparently preclude attainment of such high rates of reproduction. Also, only eutherians among the amniotes combine intimacy of placentation with prolonged active intra-uterine morphogenesis. Once established, that combination permitted (and even favoured) increases in diversity of adaptation in such disparate aspects as elevated metabolic rate, increased pre- and postnatal growth rates, increased encephalization, greater longevity, increased gregariousness, greater karyotypic flexibility, and augmented variability in adult morphology. However, all such boosts in diversity were probably secondary and dependent upon prior innovation of trophoblastic/uterine wall immunological protection of foetal tissues during prolonged intra-uterine development. Increased metabolic rates followed thereafter, with synergisms that may have speeded evolution among early eutherians. Eutherian-style trophoblast probably originated in the Mesozoic. Dependent adaptations, variably expressed, evolved later in sundry descendant lineages. Reproductive differences between marsupials and eutherians are not biologically trivial; to the contrary, breakthroughs among eutherians assured their dominance: (1) in high intensity food habits; (2) at small body masses; and (3) in very cold climates.     

Polymorphic microsatellite markers for the gliding marsupials Petaurus australis and Petaurus breviceps

Habitat destruction is causing population decline of many hollow dependent species such as gliding marsupials of the Family Petauridae. Three petaurid species are now listed in some Australian states as either threatened, rare or vulnerable, precipitating a need for information on their basic biology and population structure. We isolated and characterized three polymorphic microsatellite loci from the yellow‐bellied glider (Petaurus australis) and six polymorphic microsatellite loci from the sugar glider (P. breviceps). Per‐locus heterozygosities range from 42%–92%, and cross‐species amplification studies show that between five and seven loci are polymorphic in the two target species as well as a related species P. norfolcensis.     

A First Look at Estimating Body Size in Dentally Conservative Marsupials

The relationship between body size and tooth size has been documented for recent primates and insectivores and resulting predictive equations used to estimate body size in fossil species. This relationship is an important one, as body size is related to a host of physiological and ecological factors. In this study, the relationship between body size and molar size in recent dentally conservative marsupials is examined and body size in Cretaceous marsupials is estimated. Body weight information and basic length, width, and area measurements were taken from the molars of individuals from 22 species of Didelphidae and Dasyuridae. Least squares regression analysis shows that, as in previous studies on eutherians, the first molar is generally the most highly correlated with body size. In fact, there is a strong relationship between body size and tooth size throughout the molar series, suggesting that a fairly accurate body size estimate could be obtained from molars other than the first molar. The inclusion of species that are morphologically divergent from the average morphotype may affect the analysis. Body mass estimated in Cretaceous marsupials indicates a range of sizes similar to that seen in Recent dentally primitive marsupials.     

Molecular Systematics of Marsupials Based on the rRNA 12S Mitochondrial Gene: The Phylogeny of Didelphimorphia and of the Living Fossil Microbiotheriid Dromiciops gliroides Thomas

Nucleotide sequence data from the mitochondrial 12S rRNA gene were used to evaluate the phylogenetic relationships among the major groups of didelphimorph and paucituberculatan marsupials from South America, the microbiotheriid Dromiciops gliroides, and representatives of four orders of Australasian marsupials. Based on approximately 800 bp in 18 genera, we conclude that the didelphids constitute a monophyletic group with large-sized forms differentiated from small opossums, while Caluromys constitutes the sister taxon to didelphids. The peramelid Isoodon was recovered as the sister taxon to the paucituberculatans Caenolestes and Rhyncholestes, although it is in an uncertain phylogenetic position within the marsupial tree. Dromiciops was recovered as a well-differentiated lineage from South American opossums within the Australidelphian radiation of metatherians that include dasyurid, diprotodontian, and notoryctemorph marsupials.     

Patterns of co-occurrence among arboreal marsupials in the forests of central Victoria,southeastern Australia

Abstract Patterns of co-occurrence were examined among the suite of species of arboreal marsupials that inhabit the montane ash forests of the Central Highlands of Victoria, southeastern Australia. The data used in our analyses were counts of different species of arboreal marsupials derived from stagwatching surveys of 152 sites throughout the Central Highlands region. Our work investigated both the number of species that tend to occur together, as well as identity of the taxa in such associations. A total of eight different species of arboreal marsupials were recorded from field surveys of montane ash forests: Leadbeater's Possum (Gymnobelideus leadbeateri), Sugar Glider (Petaurus breviceps), Yellow-bellied Glider (Petaurus australis), Greater Glider (Petauroides volans), Mountain Brushtail Possum (Trichosurus caninus), Feathertail Glider (Acrobates pygmaeus), Common Ringtail Possum (Pseudocheirusperegrinus), and Eastern Pygmy Possum (Cercartetus nanus). Large assemblages of taxa were rare and no sites supported the full array of species of arboreal marsupials– the maximum number of species recorded on a given 3 ha site was five. The results of our analyses indicated that if any one species of arboreal marsupials was present at a site, then on average 1. 5 other taxa will co-inhabit that site. The exception was the Common Ringtail Possum. When this species was detected, few other arboreal marsupial taxa tended to be recorded with it. Principal Co-ordinates Analysis showed that although combinations of animals comprised of either Mountain Brushtail Possum, Leadbeater's Possum, or Greater Glider were often recorded, there were no strong patterns in the identities of co-occurring taxa. This finding, together with the result that most taxa in these forests typically co-occurred with one or two other species, indicates that none of the arboreal marsupials inhabiting the montane ash forests of the Central Highlands of Victoria would be a good surrogate for (or ‘indicator’ of), the presence of the suite of other species in the assemblage.     

Reproduction in males of the feathertail glider Acrobates pygmaeus (Marsupialia)

Between 1984 and 1986, reproductive tracts were collected from 17 male Acrobates pygmaeus (Shaw) from south-eastern Australia and the anatomy of these tracts is described. The prostate is heart-shaped and the arrangement of its three segments, anterior, central and posterior, is different to the patterns described for other marsupials. The testes are large in proportion to the body size but their structure and that of the remainder of the tract is typical of other marsupials. The sperm morphology is similar to that of the Phalangeridae and Burramyidae.
Seasonal cycles were found in the sizes of testes and prostates. Increases in testes sizes, starting in April or May, were associated with increases in seminiferous tubule diameter and Leydig cell size. The weight of the prostate increased rapidly to a short peak in June when the testes also reached maximum weight. The first births occurred approximately one month later in this population. Following this peak, both the testes and the prostate decreased in size and had returned to the original weights by January. The beginning of this period when the testes and prostate were small coincided with the cessation of births in the population and was marked by an interruption in spermatogenesis.
Males born early in a breeding season mature before the start of the next breeding season, but males born at the end of a breeding season may not mature until the second season after their birth, at which time they are approximately 18 months of age.     

Diversity and Evolution of the Marsupial Mandibular Angular Process

A medial inflection of the mandibular angular process is present in most marsupials. The few living marsupials that lack this trait either are very specialized forms (e.g., Tarsipes) or show a medial inflection at some point in development that is lost in later ontogenetic stages (cf. Dactylopsila and Phascolarctos). A medially inflected angular process is not present in any known extant or extinct placental (including all Cretaceous taxa that preserve the back of the dentary bone). Some extant placentals with enlarged auditory bullae evolved a medial flange of the angular process as a strategy to increase gape, but this is not homologous to the marsupial condition. We conclude that the medially inflected angular process is a shared derived trait of extant and extinct marsupials. The significant diversity in the form of the medially inflected mandibular angular process in marsupials, documented here for 53 taxa, shows a general relation to dietary adaptations. Herbivores (with well-developed masseter and medial pterygoid muscles) tend to have a shelf-like angular process, while small, insectivorous marsupials generally have a rod-like angular process. A close connection between the angular process and the ectotympanic is maintained during early postnatal development in all marsupials examined, a relation not seen in the placentals examined. A previous hypothesis suggested that the angular process plays a role in hearing in pouch-young Monodelphis. Data on the maturation of the auditory system does not support this hypothesis. Currently there are no data on differences in muscular anatomy or mastication between marsupials and placentals that could serve as a causal explanation for the difference in adult form of the angular process between the two groups.     

Rearrangements of mitochondrial transfer RNA genes in marsupials

Summary The nucleotide sequences of the mitochondrial origin of light-strand replication and the five tRNA genes surrounding it were determined for three marsupials. The region was found to be rearranged, leaving only the tRNA^Tyr gene at the same position as in placental mammals andXenopus. Distribution of the same rearranged genotype among two marsupial families indicates that the events causing the rearrangements took place in an early marsupial ancestor. The putative mitochondrial light-strand origin of replication in marsupials contains a hairpin structure similar to other vertebrate origins and, in addition, extensive flanking sequences that are not found in other vertebrates. Sequence comparisons among the marsupials as well as placentals indicate that the tRNA^Tyr gene has been evolving under more constraints than the other tRNA genes.Deceased July 21, 1991     

A comparative study of lymph node mast cell populations in five marsupial species.

In order to determine whether different subpopulations of mast cells exist, mast cells of mandibular and axillary lymph nodes from five species (Didelphis aurita, Metachirus nudicaudatus, Philander opossum, Marmosops incanus and Gracilinanus agilis) of South American marsupials were studied. Our results showed that mast cells present in the connective tissue of the capsule and septa (CTMC) were similar to those described for eutherian mammals. However, a population of mast cells that was present in the lymphatic sinuses and bathed by the lymph, plus in direct contact with granulocytes, lymphocytes, macrophages, and reticular cells, were morphologically and histochemically different from the CTMC. In the five species studied, these cellular types, called lymphatic-sinus mast cells (LSMC), had a lower concentration of intragranular heparin and, in four of the five species, the cytoplasmic granules appeared to be larger than those in CTMC. Although LSMC have been rarely described in eutherian mammals, it was verified, in this study, that LSMC are nevertheless present in lymphatic sinuses of the five metatherian species studied. These observations suggest that the presence of LSMC may be a characteristic of the marsupials and important in the immune response and adaptive success of the Didelphidae.     

J. P. Hill and Katherine Watson's studies of the neural crest in marsupials

In the early part of the 20th century, J. P. Hill and K. P. Watson embarked on a comprehensive study of the development of the brain in Australian marsupials. Their work included series from three major groups: dasyurids, peramelids, and diprotodonts, covering early primitive streak through brain closure and folding stages. While the major part of the work was on the development of the brain, in the course of this work they documented that cellular proliferations from the neural plate provided much of the mesenchyme of the branchial arches. These proliferations are now known to be the neural crest. However, except for a very brief note, published shortly after Hill's death, this work was never published. In this study, I present Hill and Watson's work on the development of the early neural plate and the neural crest in marsupials. I compare their findings with published work on the South American marsupial, Monodelphis domestica and demonstrate that patterns reported in Monodelphis are general for marsupials. Further, using their data I demonstrate that in dasyurids, which are ultra-altricial at birth, the neural crest migrates early and in massive quantities, even relative to other marsupials. Finally, I discuss the historical context and speculate on reasons for why this work was unpublished. I find little support for ideas that Hill blocked publication because of loyalty to the germ layer theory. Instead, it appears primarily to have been a very large project that was simply orphaned as Watson and Hill pursued other activities.     

Klossiella (Apicomplexa, Klossiellidae) in petaurid and macropodid marsupials in Australia

Six new species of Klossiella are described in the kidneys of Australian marsupials: Klossiella rufogrisei in Bennett's Wallaby, Macropus rufogriseus; Klossiella rufi in the Red Kangaroo, Macropus rufus; Klossiella thylogale in the Red-Bellied or Tasmanian Pademelon, Thylogale billardierii; Klossiella beveridgei in the Spectacled Hare-Wallaby, Lagorchestes conspicillatus; Klossiella bettongiae in the Tasmanian Bettong, Bettongia gaimardi; and Klossiella schoinobatis in the petaurid Greater Glider, Petauroides volans. It is concluded that the genus Klossiella has radiated widely among Australian marsupials, and that since it is present in American marsupials, it may have an ancient association with the subclass.     

The external ear morphology and presence of tragi in Australian marsupials

Multiple studies have described the anatomy and function of the external ear (pinna) of bats, and other placental mammals, however, studies of marsupial pinna are largely absent. In bats, the tragus appears to be especially important for locating and capturing insect prey. In this study, we aimed to investigate the pinnae of Australian marsupials, with a focus on the presence/absence of tragi and how they may relate to diet. We investigated 23 Australian marsupial species with varying diets. The pinnae measurements (scapha width, scapha length) and tragi (where present) were measured. The interaural distance and body length were also recorded for each individual. Results indicated that all nectarivorous, carnivorous, and insectivorous species had tragi with the exception of the insectivorous striped possum (Dactylopsila trivirgata), numbat (Myrmecobius fasciatus), and nectarivorous sugar glider (Petaurus breviceps). No herbivorous or omnivorous species had tragi. Based on the findings in this study, and those conducted on placental mammals, we suggest marsupials use tragi in a similar way to placentals to locate and target insectivorous prey. The Tasmanian devil (Sarcophilus harrisii) displayed the largest interaural distance that likely aids in better localization and origin of noise associated with prey detection. In contrast, the smallest interaural distance was exhibited by a macropod. Previous studies have suggested the hearing of macropods is especially adapted to detect warnings of predators made by conspecifics. While the data in this study demonstrate a diversity in pinnae among marsupials, including presence and absence of tragi, it suggests that there is a correlation between pinna structure and diet choice among marsupials. A future study should investigate a larger number of individuals and species and include marsupials from Papua New Guinea, and Central and South America as a comparison.