Macropus Parma Research Articles

Fatal disseminated toxoplasmosis in captive red kangaroo (Macropus rufus) and Parma wallaby (Macropus parma): pathological and immunohistochemical investigations

Fatal disseminated toxoplasmosis in captive red kangaroo (Macropus rufus) and Parma wallaby (Macropus parma): pathological and immunohistochemical investigations

Epidemiology and isolation of viable Toxoplasma gondii strain from macropods

Wallabies and other marsupials are highly susceptible to Toxoplasma gondii. In this study, 26 macropod samples were collected (8 red kangaroos, 4 Parma wallabies, 8 red-necked wallabies, 5 albino red-necked wallabies and 1 Eastern grey kangaroo), including tissue (n = 9) and serum (n = 17) samples. According to the modified agglutination test (MAT) results (cutoff 1:25), 50% (95% Cl: 32.06–67.94%) of the macropods had T. gondii antibodies. Among them, species, survival state, and sampling date were risk factors for T. gondii susceptibility (P < 0.05). T. gondii DNA was detected in two (cases #14 and #15) of the nine cases obtained from macropod tissues. One viable T. gondii strain (TgRooCHn4) was isolated from an albino red-necked wallaby (Macropus rufogriseus, case #14) via bioassay in mice. TgRooCHn4 belongs to ToxoDB genotype #3, using the 10 multilocus PCR-RFLP markers. The ROP18 and ROP5 gene allele types of TgRooCHn4 were 2/2, which was predicted to be non-lethal to mice. The virulence of TgRooCHn4 tachyzoites was avirulent in mice. Most macropods sampled from Hernan province in 2021 and 2022 were positive with T. gondii infection. A flood occurred in July 2021 in Zhengzhou from Henan province may promote the transmission of T. gondii oocysts. To our knowledge, this is the first T. gondii strain isolated from albino red-necked wallaby. However, further investigation is required to enhance our understanding of the transmission and prevention of toxoplasmosis in sensitive zoo animals.

Camera trap detection of mycophagy among co‐occurring vertebrates

AbstractThirty camera traps were deployed for a total of 4179 trap‐nights between January and June 2020 as part of a project assessing post‐fire recovery of pademelons (Thylogale spp.) in northern New South Wales. By chance, one camera documented a site that was highly productive for the ectomycorrhizal fungal genus Amanita. This camera provided a rare opportunity to document a diversity of co‐habitating vertebrates that utilise these ectomycorrhizal fungi for food and in turn perform an important ecosystem function through the dispersal of their spores. Our camera recorded eleven vertebrate species; of these, we captured photographic evidence of Australian brush‐turkeys (Alectura lathami), a parma wallaby (Notamacropus parma), long‐nosed bandicoots (Perameles nasuta), red‐legged pademelons (Thylogale stigmatica) and red‐necked pademelons (T. thetis) feeding on fungal fruiting bodies.

Behaviour and enclosure use of captive parma wallabies (Macropus parma): an assessment of compatibility within a mixed-species exhibit.

The parma wallaby (Macropus parma) is considered to be a species of conservation concern. Collaborative breeding programs for this cryptic animal are in place in many zoos worldwide. Many zoos choose to house parma wallabies in mixed-species exhibits and a successful combination of species can greatly improve breeding prospects. However, there are potential health and welfare concerns and species compatibility requires consideration. This study investigates if a previously unreported housing of the parma wallaby and the Patagonian mara (Doliochotis patagonum), is congruous. Parma wallabies at Dudley Zoological Gardens were observed in two different housing systems; mixed-species (MS) and single species (SS) for nine days. Scan sampling of all individuals, across a range of behaviours previously reported for this species, was carried out at three 30 minute periods across the day. Differences in foraging behaviour were noted with parmas housed in the MS foraging significantly less than the SS group (p<0.01). A novel behaviour, agonistic directional urination, was also observed in the MS enclosure which was not observed within the SS group. Utilisation of the enclosure was analysed using a Spread of Participation Index (SPI); values revealed MS parmas utilised less of their enclosure, with a notable preference for areas not frequented by mara (W27=899.0, p<0.05). The MS parmas appeared to be affected by the presence of the mara, both behaviourally and in their enclosure use, this could be indicative of a negative welfare state. This study provides an indicator of species incompatibility, potentially affecting the welfare of captive parma wallabies and the future conservation of the species, and requires further investigation.

Speciation Generates Mosaic Genomes in Kangaroos.

The iconic Australasian kangaroos and wallabies represent a successful marsupial radiation. However, the evolutionary relationship within the two genera, Macropus and Wallabia, is controversial: mitochondrial and nuclear genes, and morphological data have produced conflicting scenarios regarding the phylogenetic relationships, which in turn impact the classification and taxonomy. We sequenced and analyzed the genomes of 11 kangaroos to investigate the evolutionary cause of the observed phylogenetic conflict. A multilocus coalescent analysis using ∼14,900 genome fragments, each 10 kb long, significantly resolved the species relationships between and among the sister-genera Macropus and Wallabia. The phylogenomic approach reconstructed the swamp wallaby (Wallabia) as nested inside Macropus, making this genus paraphyletic. However, the phylogenomic analyses indicate multiple conflicting phylogenetic signals in the swamp wallaby genome. This is interpreted as at least one introgression event between the ancestor of the genus Wallabia and a now extinct ghost lineage outside the genus Macropus. Additional phylogenetic signals must therefore be caused by incomplete lineage sorting and/or introgression, but available statistical methods cannot convincingly disentangle the two processes. In addition, the relationships inside the Macropus subgenus M. (Notamacropus) represent a hard polytomy. Thus, the relationships between tammar, red-necked, agile, and parma wallabies remain unresolvable even with whole-genome data. Even if most methods resolve bifurcating trees from genomic data, hard polytomies, incomplete lineage sorting, and introgression complicate the interpretation of the phylogeny and thus taxonomy.

Zoo foraging ecology: development and assessment of a welfare tool for captive animals

AbstractForaging ecology and food patch studies are commonly used to elucidate the environmental perceptions of wild, free-ranging animals. Their application to captive animals, however, especially those in zoos, is still in its infancy. To illustrate some specific applications of zoo foraging ecology, we provide a study that evaluated: (i) whether patch use and giving-up densities (GUDs) can reveal areas of preference within an exhibit for zoo species; (ii) if food patches provide an effective form of behavioural enrichment; and (iii) if visitor interest and behaviour is affected by food patch presence. A combination of behavioural observations, and experimental food patches and giving-up densities were used to address these objectives in Parma wallabies (Macropus parma) and Patagonian cavies (Dolichotis patagonum) at Lincoln Park Zoo, Chicago, Illinois USA. GUDs revealed distinct areas of preference and aversion within the exhibit for cavies, but not so for the wallabies. For both species, presence of food patches increased foraging behaviours, decreased inactive behaviours, and increased within-exhibit movement, demonstrating that food patches serve as an effective behavioural enrichment technique. The use of food patches also revealed striking differences between individuals, particularly for the pair of cavies. There were encouraging trends toward increased visitor number and stay-time when food patches were present in each exhibit, but the effect was not statistically significant. These results suggest that utilising patch use, GUDs, and foraging theory in zoo populations may enhance animal welfare, and can inform improvements to exhibit design directly from the animal's perspective. We conclude with a broader discussion of zoo foraging ecology as an emerging field, with suggestions for future avenues of research.

A Retrospective and Prospective Study of Megaesophagus in the Parma Wallaby (Macropus parma) at the San Diego Zoo, California, USA

At the San Diego Zoo (California, USA), 22 cases of megaesophagus were diagnosed in the parma wallaby (Macropus parma); a prevalence of 21.1%. Parma wallabies often have no clinical signs until severe and chronic dilation of the esophagus is present. Clinical signs of advanced disease include weight loss, swelling of the cervical region, regurgitation without reswallowing of ingesta, short flight distance, depression, collapse, dyspnea, and sudden death. Retrospective and prospective studies at the San Diego Zoo and a multi-institutional survey in the United States were used to try to determine the cause of megaesophagus. The retrospective study did not identify an etiology. The prospective study revealed megaesophagus and severely delayed esophageal transit time in eight of eight animals. Myasthenia gravis, lead toxicosis, toxoplasmosis, and thyroid disease were eliminated as possible causes. Of 286 living and dead parma wallabies surveyed at other institutions, three cases of esophageal diverticulum and one case of megaesophagus were reported. The cause of megaesophagus in parma wallabies was not determined.

Neosporosis in a Captive Parma Wallaby (Macropus parma)

Infection with Neospora caninum has been diagnosed in a variety of animal species; however, reports in marsupials are rare. A captive Parma wallaby (Macropus parma) died suddenly and was subjected to necropsy examination. The main finding was necrotizing myocarditis associated with protozoan parasites. The protozoa were identified as N. caninum by use of immunohistochemistry and partial gene sequence analysis. Neospora and Toxoplasma should be considered a possible cause of disease in captive marsupials. Further work is required to determine whether marsupials are an accidental or terminal host of this protozoan in order to better understand the host-parasite relationship.

Successful Treatment of Chronic Periapical Osteomyelitis in a Parma Wallaby (Macropus parma) Using Comprehensive Endodontic Therapy with Apicoectomy

Although necrobacillosis remains a common condition of captive macropods, there have been limited reports of successful treatment modalities by which it can be treated. Comprehensive endodontic therapy with apicoectomy has been used reliably in human and domestic animal dentistry. This report describes a case of periapical osteomyelitis involving a mandibular incisor in a Parma wallaby (Macropus parma) that was successfully treated using these techniques in conjunction with low-level laser therapy at 810 nm, which was used for decontamination of the pulp cavity, anti-inflammatory, and biostimulatory effects.

Esophageal Diverticula in Parma Wallabies (Macropus parma)

Four adult, wild caught Parma wallabies (Macropus parma) presented with intermittent, postprandial, midcervical swellings. Esophageal diverticula were discovered in the four animals. One of two wallabies was managed successfully with surgery. A third animal died of other causes. The fourth animal died with possible complications from the diverticulum. This is the first published report of esophageal diverticula in macropods.

Methods and Prospects for Using Molecular Data in Captive Breeding Programs: An Empirical Example Using Parma Wallabies (Macropus parma)

Zoo and aquarium breeding programs rely on accurate pedigrees to manage the genetics and demographics of captive populations. Breeding recommendations are often encumbered, however, by unknown parentage. If an individual has any amount of unknown ancestry, the relationships between that individual and all other individuals in a population are ambiguous, and breeding recommendations cannot be tailored to maximize genetic diversity and minimize inbreeding. In those situations, breeding program management might be improved by the incorporation of molecular data. We developed microsatellite markers for the parma wallaby (Macropus parma) and investigated how genetic data might be used to improve the management of the captive population. The parma wallaby is a small marsupial found in fragmented forests near the coast of New South Wales, Australia. Because the species is of conservation concern, the captive population in North America is managed by recurring breeding recommendations. The effectiveness of the population's management is hampered, however, because over half of the individuals have some amount of unknown ancestry. We used microsatellite data to resolve unknown parentage, described how molecular estimates of relatedness might inform future breeding recommendations, and used computer simulations to investigate how molecular estimates of relatedness among founders might contribute to the genetic management of the population. Our results indicated that microsatellite appraisals of parentage were useful with respect to clarifying pedigrees but that molecular assessments of founder relatedness provided very marginal benefits with regard to the preservation of genetic diversity and the avoidance of inbreeding.

A Re-Description of Progamotaenia Ewersi (Schmidt, 1975) (Cestoda: Anoplocephalidae) from Wallabies and Kangaroos (Macropodidae) with the Description of a New Species, Progamotaenia Ualabati N. SP.

A new species of anoplocephalid cestode, Progamotaenia ualabati n. sp., is described from the small intestines of the wallabies Wallabia bicolor (Desmarest, 1804) and Macropus parma Waterhouse, 1845. It most closely resembles P. ewersi (Schmidt, 1975) in having an ovoid cirrus sac which does not extend into the medulla, but differs in strobilar width, the length of the distal vagina, the asymmetry ratio of the female genitalia and the shape of the egg. Progamotaenia ewersi is redescribed from the type host, M. agilis (Gould, 1842). Specimens from this host species differ from those found in M. fuliginosus (Desmarest, 1817) and M. giganteus Shaw, 1790 in scolex size and from specimens from M. parryi Bennett, 1835 in the size of the seminal receptacle. Specimens are also reported from Macropus rufogriseus (Desmarest, 1817), M. irma (Jourdan, 1837), W. bicolor, Petrogale assimilis Ramsay, 1877, Pet. penicillata (Gray, 1825) and from captive M. rufus (Desmarest, 1822) and M. parma. However, insufficient material is available for detailed morphological comparisons. Specimens currently identified as P. ewersi from M. robustus Gould, 1841 represent an undescribed species.

Seroprevalence of Retrovirus in North American Captive Macropodidae

Laboratory records of serology results from captive macropodidae sampled between 1997 and 2005 were reviewed to assess the seroprevalence of retrovirus exposure. Serum samples from 269 individuals (136 males, 133 females) representing 10 species of macropods housed in 31 North American captive collections were analyzed for retrovirus antibody using an indirect immunofluorescent assay. The prevalence of positive antibody titers comparing male versus female, between species, between age groups, and among animals with identified parentage was examined by nonparametric statistical analyses. Median age of animals at time of sample collection was 36 mo (range 2-201 mo). Total percentage seropositive was 20.4%. Serum antibody was detected in 31 of 47 (66.0%) tammar wallaby (Macropus eugenii), nine of 24 (37.5%) yellow-footed rock wallaby (Petrogale xanthopus), four of 11 (36.4%) swamp wallaby (Wallabia bicolor), 10 of 80 (12.5%) red-necked wallaby (Macropus rufogriseus), and one of 54 (1.9%) parma wallaby (Macropus parma). No individuals of western gray kangaroo (n=3) (Macropus fuliginosus), eastern gray kangaroo (n=19) (Macropus giganteus), common wallaroo (n=6) (Macropus robustus), red kangaroo (n=11) (Macropus rufus), or Matschie's tree kangaroo (n=14) (Dendrolagus matschiei) were positive for retrovirus antibody. These results demonstrate that five species of captive macropods have a history of exposure to retrovirus, with the highest percentage seropositive and highest statistical correlation in M. eugenii (pair-wise Fisher's exact test, alpha = 0.05). Additionally, one wild-caught M. eugenii was confirmed seropositive during quarantine period, indicating that retrovirus exposure may exist in wild populations.

Association of parma wallabies (Macropus parma) with sedge swamps in Gibraltar Range National Park.

Parma wallabies (Macropus parma) have a patchy distribution on the coast and ranges of central and northern New South Wales from Goulburn northward to the Queensland border. In Gibraltar Range National Park they are found in dry sclerophyll forest with a heath understorey, a departure from their apparent preference for wet forest types. Distance to swamp was by far the best correlate of M. parma distribution.

Perturbed growth and development in marsupial young after reciprocal cross-fostering between species

Cross-fostering of marsupial young between species can potentially facilitate propagation of endangered or rare marsupial species by artificially increasing the number of progeny produced. The present study compares the growth and development of normal and cross-fostered tammar and parma wallabies. Tammars cross-fostered into the pouches of parmas grew at a similar rate to naturally reared tammar young and had developmental milestones at a similar age. However, parma young cross-fostered between the day of birth and 15 days post-partum into tammars that were carrying young of equivalent developmental stages did not grow normally and were lost from the pouch. Parma young cross-fostered at 30 days survived, but had significantly reduced growth rates and their developmental milestones were delayed compared with normally reared parma young. Thus, growth can be affected by cross-fostering, even between species like tammars and parmas that are of similar size and have similar lactation lengths. The results of the present study suggest that maternal milk regulates the timing of development of each species and a mis-match in the time that each young receives critical milk components can have a marked effect on their growth and development.

Antibodies to the Ross River Virus in Captive Marsupials in Urban Areas of Eastern New South Wales, Australia

Serum samples collected from 224 tammar wallabies (Macropus eugenii) in two captive populations in urban areas in eastern New South Wales Australia, between December 1999 and May 2004, were tested for antibodies to Ross River virus (RRV). In one population in northwest Sydney, 21 animals (11%) tested positive, and in another population in Newcastle, New South Wales, thirteen (33%) of the animals were positive. Antibodies were detected in four of 11 wallaroos (Macropus robustus) (36%) but not in parma wallabies (Macropus parma) (n=5), koalas (Phascolarctos cinereus) (n=12) and southern hairy-nosed wombats (Lasiorhinus latifrons) (n=2) from the Sydney area. These data support the possible role of marsupials as urban amplifying hosts for RRV.

The temporal organisation of the feeding behaviour of four species of wallaby: examining chronobiological and homeostatic influences

We studied the temporal distribution of feeding events of tammar wallabies, parma wallabies, brush-tailed rock-wallabies and swamp wallabies by infrared video-recording of captive animals maintained in a 12 : 12 light : dark cycle with constant temperature, and by radio-microphone surveillance of free-ranging animals on Kawau Island, New Zealand. Analyses of mean time spent feeding per 20-min period for tammar and parma wallabies showed significant circadian variation in both captive and free-ranging animals but not in captive or free-ranging brush-tailed rock wallabies or swamp wallabies. While there was no significant difference in the extent of circadian variation of feeding rate between tammar and parma wallabies there were significant differences according to the type of food being fed. Thus, circadian variation in feeding rate was greater in both species when standing sward was fed. None of the survivorship curves of the interfeed intervals of either captive or free-ranging animals showed a discontinuity suggestive of organisation of feed events into meals. There were bicrepuscular peaks of feed-event density in both captive and free-ranging tammar and parma wallabies. There was a similar bicrepuscular distribution of feed-event density in free-ranging brush-tailed rock-wallabies but a more uniform temporal distribution of this parameter in captive specimens. There was a more uniform circadian distribution of feed-event density in a single captive and a single free-ranging swamp wallaby. Thus the circadian incidence of the feeding events of tammar and parma wallabies were more resistant to changes in the incidence of stochastic environmental variables such as predation whereas those of bush-tailed rock-wallabies and swamp wallabies were more susceptible to changes in these stimuli.

Predator scent induces differing responses in two sympatric macropodids

When prey species encounter the scent of a predator they must make a decision on how to respond. This may be either to ignore, flee, hide or alarm call. While many species are able to derive detailed information from the chemical cues associated with predator scent, for some the decision to respond is often made without being able to identify the actual location and intentions of the predator. Depending on the sociality and ecology of the species, it may pay to flee or to engage in predator inspection where knowledge is impure. We tested for this in two sympatric marsupial macropodids, the parma wallaby (Macropus parma) and the red-necked pademelon (Thylogale thetis), as little is known of how these species detect and respond to olfactory cues of predation risk. We observed that, when presented with a synthetic predator scent mimicking dog urine, the social forager, T. thetis, tended to spend more time close to the predator odour, while the solitary forager, M. parma, exhibited an aversive response. The results suggest that social and ecological constraints on the sensory modalities used in predator detection may influence how macropodids respond to olfactory predator cues.

Evolution in the suite of semiochemicals secreted by the sternal gland of Australian marsupials

The nature and distribution of the components, and evolution of the suite of compounds, secreted by the sternal gland of marsupials were studied. Individuals from nine families (18 species) of marsupials and from the echidna were sampled over an 18-month period. The assay system used gas chromatography/mass spectrometry and utilised thermal desorption with cryofocusing. Parsimony analysis, constrained by an assumed phylogeny, was used to examine the evolution of the suite of compounds detected. Large interspecies variation in secretion composition was observed with acetic acid, short-chain (C6–C10) aldehydes, long-chain (&gt;C15) hydrocarbons and 1,1-bis-(p-tolyl)-ethane being constituents of the secretion of most species. The suite of compounds, however, varied from three compounds in the yellow-bellied and feathertail gliders to 41 in the koala. The most complex suites of compounds were found in the brown antechinus, red kangaroo, tammar wallaby and koala. Radical differences were observed between the secretions of related species (for example, brown antechinus and mulgara, tammar and parma wallabies, wombat and koala). Compounds appeared and disappeared repeatedly across the phylogeny. No compound constituted a synapomorphy for the Australian marsupials and only one compound was considered a synapomorphy for the Diprotodontia.

Temporal aspects of feeding events in tammar (Macropus eugenii) and parma (Macropus parma) wallabies. I. Food acquisition and oral processing

We studied parameters that influence the efficiency of food acquisition and oral processing in the tammar wallaby (a grazer) and the parma wallaby (a grazer/browser), both in captivity and under free range on Kawau Island, New Zealand.In captivity, both species spent less time feeding per gram of dry matter intake when browsing than when grazing, and there were no significant differences between the species with respect to the rates of feeding per gram of dry matter intake of a given food. However, under free-ranging conditions, tammar wallabies spent longer feeding than did parma wallabies, so it was likely that tammar wallabies spent more time grazing than browsing. Differences in the relationships between feeding event and inter-feed interval duration in captive and free-ranging wallabies indicated that feeding behaviour was influenced by different factors in the two situations.Microtemporal analysis of the chewing sounds of free-ranging tammar and parma wallabies showed that the interval between the first and second sounds in a 'run' of chewing sounds was longer than that between subsequent intervals, indicating that there was a time cost associated with food aquisition. However, as there were no significant differences between the two wallaby species, either in the mean duration of 'runs' of chewing sounds within feeding events or in the mean duration of whole feeding events, this cost was similar for grazing and browsing. Chewing characteristics differed from those of larger (eutherian) herbivores in that the numbers of chews in a run were not randomly distributed, both species having a preponderance of runs with seven chews. Whilst, the intervals between the second and subsequent chewing sounds in a run did not vary in a periodic manner, such as would occur in batch processing of food, they were more prolonged in runs with more chewing sounds and were significantly longer in tammar wallabies than in parma wallabies. Thus, the slower rate of oral processing of grass was likely due to a generally slower rate of chewing when grazing than when browsing.