Growth and development of the Tasmanian devil (Sarcophilus harrisii) at Healesville Sanctuary,Victoria, Australia

A study of the growth and development of the Tasmanian devil (Sarcophilus harrisii) was undertaken on a litter born at Healesville Sanctuary in Healesville, Victoria, Australia. Measurements of crown–rump length, head length, and head width were recorded every week from birth. Body weight was recorded weekly once the joeys were detached from the teat at 142 days of age, until 218 days of age. The growth curves revealed an initial linear increase in crown–rump lengths until approximately 60 days of age, when the gradient increased, while head length and head width showed a largely linear increase with age. The appearances of various morphological characteristics were also recorded. Zoo Biol 22:497–505, 2003. © 2003 Wiley‐Liss, Inc.     

The impact of disease on the survival and population growth rate of the Tasmanian devil

1. We investigated the impact of a recently emerged disease, Devil Facial Tumour Disease (DFTD), on the survival and population growth rate of a population of Tasmanian devils, Sarcophilus harrisii, on the Freycinet Peninsula in eastern Tasmania. 2. Cormack-Jolly-Seber and multistate mark-recapture models were employed to investigate the impact of DFTD on age- and sex-specific apparent survival and transition rates. Disease impact on population growth rate was investigated using reverse-time mark-recapture models. 3. The arrival of DFTD triggered an immediate and steady decline in apparent survival rates of adults and subadults, the rate of which was predicted well by the increase in disease prevalence in the population over time. 4. Transitions from healthy to diseased state increased with disease prevalence suggesting that the force of infection in the population is increasing and that the epidemic is not subsiding. 5. The arrival of DFTD coincided with a marked, ongoing decline in the population growth rate of the previously stable population, which to date has not been offset by population compensatory responses.     

Age‐related variation in the trophic characteristics of a marsupial carnivore,the Tasmanian devil Sarcophilus harrisii

Age‐related changes in diet have implications for competitive interactions and for predator–prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils Sarcophilus harrisii, a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δ¹³C and δ¹⁵N decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEA_B mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEA_B mode range 0.492–1.083) than devils ≥24 months old (mode range 0.092–0.240). A decrease in δ¹⁵N from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood.     

Seasonal,demographic and density‐related patterns of contact between Tasmanian devils (Sarcophilus harrisii): Implications for transmission of devil facial tumour disease

Abstract Devil facial tumour disease (DFTD), is an emerging infectious cancer thought to be spread by biting. It is causing ongoing, severe population decline of the Tasmanian devil (Sarcophilus harrisii), the largest surviving marsupial carnivore and there are concerns that DFTD may lead to extinction of the devil. Whether extinction is likely depends on contact rates and their relationship to host density. We investigated contact rates using two different datasets. The first consisted of field observations of contact and biting behaviour around prey carcasses and, the second was a 3‐year longitudinal series of injuries in a marked devil population. During feeding interactions at carcasses, contact rates were significantly positively associated with population density and subadults delivered more bites than adult males and females. Injuries from the marked devil population did not differ between adult males and females. In two of the three years, penetrating biting (resulting in injury) increased markedly during the mating season and was more frequent in adults than in subadults. Among injured devils with wounds penetrating the dermal layer, adults were more frequently bitten in the head (the location of primary tumours) in the mating season than in other seasons, and had more head bites than subadults. Our results suggest that the mating season may be the key period for disease transmission. If most penetrating bites occur during mating interactions, DFTD transmission is likely to be frequency dependent, which means that there would be no threshold host density for disease persistence, and disease‐induced extinction is possible.     

Hormonal control of birth behavior in the Tasmanian devil Sarcophilus harrisii

In a number of marsupial species, females exhibit characteristic, stereotyped parturient behavior that facilitates the passage of the neonates to the pouch. In macropodids, this parturient behavior can be induced in non-pregnant females and males by treatment with either prostaglandin F2alpha (PGF2alpha) or oxytocin (OT). This study investigated the effects of PGF2alpha and OT on behavior of Tasmanian devils. Animals tended to sit or lie down quickly, with little vocalization, after treatment with PGF2alpha or OT, while after saline, the animals remained alert, seldom sat, and frequently vocalized. Hormone treatment caused increased respiration. Urogenital and pouch grooming, a characteristic element of parturient behavior in macropodids, was seen in only one devil after hormone treatment. However, no pouch or urogenital grooming was seen in videotape of a devil giving birth, so this may not be a feature of parturient behavior in this species. Overall behavior of males and females was very similar suggesting that the behavioral effects observed may be due to direct neural action of PGF2alpha or OT, rather than an indirect response to uterine or vaginal contractions caused by the hormones. This study is the first to demonstrate that OT results in PGF2alpha secretion as PGFM levels rose after OT injection.     

Infectious disease and sickness behaviour: tumour progression affects interaction patterns and social network structure in wild Tasmanian devils

Infectious diseases, including transmissible cancers, can have a broad range of impacts on host behaviour, particularly in the latter stages of disease progression. However, the difficulty of early diagnoses makes the study of behavioural influences of disease in wild animals a challenging task. Tasmanian devils (Sarcophilus harrisii) are affected by a transmissible cancer, devil facial tumour disease (DFTD), in which tumours are externally visible as they progress. Using telemetry and mark–recapture datasets, we quantify the impacts of cancer progression on the behaviour of wild devils by assessing how interaction patterns within the social network of a population change with increasing tumour load. The progression of DFTD negatively influences devils'' likelihood of interaction within their network. Infected devils were more active within their network late in the mating season, a pattern with repercussions for DFTD transmission. Our study provides a rare opportunity to quantify and understand the behavioural feedbacks of disease in wildlife and how they may affect transmission and population dynamics in general.     

Lack of genetic diversity across diverse immune genes in an endangered mammal,the Tasmanian devil (Sarcophilus harrisii)

The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction due to the spread of devil facial tumour disease. Polymorphisms in immune genes can provide adaptive potential to resist diseases. Previous studies in diversity at immune loci in wild species have almost exclusively focused on genes of the major histocompatibility complex (MHC); however, these genes only account for a fraction of immune gene diversity. Devils lack diversity at functionally important immunity loci, including MHC and Toll‐like receptor genes. Whether there are polymorphisms at devil immune genes outside these two families is unknown. Here, we identify polymorphisms in a wide range of key immune genes, and develop assays to type single nucleotide polymorphisms (SNPs) within a subset of these genes. A total of 167 immune genes were examined, including cytokines, chemokines and natural killer cell receptors. Using genome‐level data from ten devils, SNPs within coding regions, introns and 10 kb flanking genes of interest were identified. We found low polymorphism across 167 immune genes examined bioinformatically using whole‐genome data. From this data, we developed long amplicon assays to target nine genes. These amplicons were sequenced in 29–220 devils and found to contain 78 SNPs, including eight SNPS within exons. Despite the extreme paucity of genetic diversity within these genes, signatures of balancing selection were exhibited by one chemokine gene, suggesting that remaining diversity may hold adaptive potential. The low functional diversity may leave devils highly vulnerable to infectious disease, and therefore, monitoring and preserving remaining diversity will be critical for the long‐term management of this species. Examining genetic variation in diverse immune genes should be a priority for threatened wildlife species. This study can act as a model for broad‐scale immunogenetic diversity analysis in threatened species.     

Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease

The structure of the contact network between individuals has a profound effect on the transmission of infectious disease. Using a novel technology – proximity sensing radio collars – we described the contact network in a population of Tasmanian devils. This largest surviving marsupial carnivore is threatened by a novel infectious cancer. All devils were connected in a single giant component, which would permit disease to spread throughout the network from any single infected individual. Unlike the contact networks for many human diseases, the degree distribution was not highly aggregated. Nevertheless, the empirically derived networks differed from random networks. Contact networks differed between the mating and non-mating seasons, with more extended male–female associations in the mating season and a greater frequency of female–female associations outside the mating season. Our results suggest that there is limited potential to control the disease by targeting highly connected age or sex classes.     

MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer

Tasmanian devils face extinction owing to the emergence of a contagious cancer. Devil facial tumour disease (DFTD) is a clonal cancer spread owing to a lack of major histocompatibility complex (MHC) barriers in Tasmanian devil populations. We present a comprehensive screen of MHC diversity in devils and identify 25 MHC types and 53 novel sequences, but conclude that overall levels of MHC diversity at the sequence level are low. The majority of MHC Class I variation can be explained by allelic copy number variation with two to seven sequence variants identified per individual. MHC sequences are divided into two distinct groups based on sequence similarity. DFTD cells and most devils have sequences from both groups. Twenty per cent of individuals have a restricted MHC repertoire and contain only group I or only group II sequences. Counterintuitively, we postulate that the immune system of individuals with a restricted MHC repertoire may recognize foreign MHC antigens on the surface of the DFTD cell. The implication of these results for management of DFTD and this endangered species are discussed.     

The characterization of Tasmanian devil Sarcophilius harrisii pelage fibres and their associated lipids

The Tasmanian devil (Sarcophilius harrisii) is the largest living marsupial carnivore left on Earth. In this paper we report the results of the first thorough characterization of the keratin fibres comprising the Tasmanian devil pelage. The fibre's morphology, structure, composition and surface have been investigated. The results have been compared with those of a number of other mammalian species including carnivores and herbivores. The fibres structure was found to be consistent with that expected for a keratin fibre. From the results of the bound lipid analysis it can be concluded that the Tasmanian devil is a typical mammal in which the 21‐carbon atom anteiso branched fatty acid is the predominant bound fatty acid. This is consistent with the Tasmanian devil's position in the mammalian phylogenetic tree. The amino acid analysis places the devil in line with other carnivores. The high cystine and proline content may correlate with the Tasmanian devil's diet which is rich in muscle and collagen proteins.     

Extensive population decline in the Tasmanian devil predates European settlement and devil facial tumour disease

The Tasmanian devil (Sarcophilus harrisii) was widespread in Australia during the Late Pleistocene but is now endemic to the island of Tasmania. Low genetic diversity combined with the spread of devil facial tumour disease have raised concerns for the species’ long-term survival. Here, we investigate the origin of low genetic diversity by inferring the species'' demographic history using temporal sampling with summary statistics, full-likelihood and approximate Bayesian computation methods. Our results show extensive population declines across Tasmania correlating with environmental changes around the last glacial maximum and following unstable climate related to increased ‘El Niño–Southern Oscillation’ activity.     

Transmissible cancer in Tasmanian devils: localized lineage replacement and host population response

Tasmanian devil facial tumour disease (DFTD) is a clonally transmissible cancer threatening the Tasmanian devil (Sarcophilus harrisii) with extinction. Live cancer cells are the infectious agent, transmitted to new hosts when individuals bite each other. Over the 18 years since DFTD was first observed, distinct genetic and karyotypic sublineages have evolved. In this longitudinal study, we investigate the associations between tumour karyotype, epidemic patterns and host demographic response to the disease. Reduced host population effects and low DFTD infection rates were associated with high prevalence of tetraploid tumours. Subsequent replacement by a diploid variant of DFTD coincided with a rapid increase in disease prevalence, population decline and reduced mean age of the population. Our results suggest a role for tumour genetics in DFTD transmission dynamics and epidemic outcome. Future research, for this and other highly pathogenic emerging infectious diseases, should focus on understanding the evolution of host and pathogen genotypes, their effects on susceptibility and tolerance to infection, and their implications for designing novel genetic management strategies. This study provides evidence for a rapid localized lineage replacement occurring within a transmissible cancer epidemic and highlights the possibility that distinct DFTD genetic lineages may harbour traits that influence pathogen fitness.     

Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator,the Tasmanian devil

Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top–down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low.     

Conservation Management of Tasmanian Devils in the Context of an Emerging, Extinction-threatening Disease: Devil Facial Tumor Disease

An emerging infectious facial cancer threatens Tasmanian devils with extinction. The disease is likely to occur across the range of the devil within 5 years. This urgent time frame requires management options that can be implemented immediately: the establishment of insurance populations, in captivity, wild-living on islands, and aiming for eradication in areas that can be isolated. The long-term options of the spontaneous or assisted evolution of resistance or development of a field-deliverable vaccine are unlikely to be available in time. The disease’s characteristic allograft transmission through intimate contact simplifies isolation of insurance populations and breaking transmission in suppression trials. Better knowledge of contact matrices in wild devils will help focus timing and demographic targets of removals. A metapopulation approach is needed that integrates captive and wild-living island and peninsula (disease suppression) populations to minimize the loss of genetic diversity over 50 years until either extinction and reintroduction can occur, resistance evolves or a field-deliverable vaccine is developed. Given the importance of the insurance populations and the low genetic diversity of devils, a conservative target for retention of 95% genetic diversity is recommended. Encouraging preliminary results of the first disease-suppression trial on a large peninsula show fewer late stage tumors and no apparent population decline. Limiting geographic spread or suppressing the disease on a broadscale are both unlikely to be feasible. Since the synergy of devil decline and impending fox establishment could have devastating consequences for Tasmanian wildlife, it is crucial to manage the dynamics of new and old predator species together.     

Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour

Genetic structure in host species is often used to predict disease spread. However, host and pathogen genetic variation may be incongruent. Understanding landscape factors that have either concordant or divergent influence on host and pathogen genetic structure is crucial for wildlife disease management. Devil facial tumour disease (DFTD) was first observed in 1996 and has spread throughout almost the entire Tasmanian devil geographic range, causing dramatic population declines. Whereas DFTD is predominantly spread via biting among adults, devils typically disperse as juveniles, which experience low DFTD prevalence. Thus, we predicted little association between devil and tumour population structure and that environmental factors influencing gene flow differ between devils and tumours. We employed a comparative landscape genetics framework to test the influence of environmental factors on patterns of isolation by resistance (IBR) and isolation by environment (IBE) in devils and DFTD. Although we found evidence for broad‐scale costructuring between devils and tumours, we found no relationship between host and tumour individual genetic distances. Further, the factors driving the spatial distribution of genetic variation differed for each. Devils exhibited a strong IBR pattern driven by major roads, with no evidence of IBE. By contrast, tumours showed little evidence for IBR and a weak IBE pattern with respect to elevation in one of two tumour clusters we identify herein. Our results warrant caution when inferring pathogen spread using host population genetic structure and suggest that reliance on environmental barriers to host connectivity may be ineffective for managing the spread of wildlife diseases. Our findings demonstrate the utility of comparative landscape genetics for identifying differential factors driving host dispersal and pathogen transmission.     

Isotopic niches do not follow the expectations of niche conservatism in the bird genus Cinclodes

Phenotypic traits are expected to be more similar among closely related species than among species that diverged long ago (all else being equal). This pattern, known as phylogenetic niche conservatism, also applies to traits that are important to determine the niche of species. To test this hypothesis on ecological niches, we analysed isotopic data from 254 museum study skins from 12 of the 16 species of the bird genus Cinclodes and measured stable isotope ratios for four different elements: carbon, nitrogen, hydrogen and oxygen. We find that all traits, measured individually, or as a composite measurement, lack any phylogenetic signal, which in turn suggests a high level of lability in ecological niches. We compared these metrics to the measurements of morphological traits in the same genus and found that isotopic niches are uniquely evolutionarily labile compared to other traits. Our results suggest that, in Cinclodes, the realized niche evolves much faster than expected by the constraints of phylogenetic history and poses the question of whether this is a general pattern across the tree of life     

Diet and trophic niche of Antarctic silverfish Pleuragramma antarcticum in the Ross Sea,Antarctica

The diet of Antarctic silverfish Pleuragramma antarcticum was evaluated by examining stomach contents of specimens collected in the Ross Sea (71°–77° S; 165°–180° E) in January to March 2008. Pleuragramma antarcticum (50–236 mm standard length, L_S) and prey items were analysed for stable‐isotopic composition of carbon and nitrogen. According to index of relative importance (I_RI), which incorporates frequency of occurrence, mass and number of prey items, the most important prey items were copepods (81%I_RI over all specimens), predominantly Metridia gerlachei and Paraeuchaeta sp., with krill and fishes having low I_RI (2·2 and 5·6%I_RI overall). According to mass of prey (M) in stomachs, however, fishes (P. antarcticum and myctophids) and krill dominated overall diet (48 and 22%M, respectively), with copepods being a relatively minor constituent of overall diet by mass (9·9%M). Piscivory by P. antarcticum occurred mainly in the extreme south‐west of the region and near the continental slope. Krill identified to species level in P. antarcticum stomachs were predominantly Euphausia superba (14·1%M) with some Euphausia crystallophorias (4·8%M). Both DistLM modelling (PRIMER‐permanova+) on stomach contents (by I_RI) and stepwise generalized linear modelling on stable isotopes showed that L_S and location were significant predictors of P. antarcticum diet. Postlarval P. antarcticum (50–89 mm L_S) consumed exclusively copepods. Juvenile P. antarcticum (90–151 mm L_S) consumed predominantly krill and copepods by mass (46 and 30%M, respectively). Small adult P. antarcticum (152–178 mm L_S) consumed krill, fishes and copepods (37, 36 and 15%M, respectively). Large adult P. antarcticum (179–236 mm L_S) consumed predominantly fishes and krill (55 and 17%M, respectively), especially in the north (near the Ross Sea slope) and in the SW Ross Sea. Amphipods were occasionally important prey items for P. antarcticum (western Ross Sea, 39%M). General concordance between stomach contents and trophic level of P. antarcticum and prey based on δ¹⁵N was demonstrated. Pleuragramma antarcticum trophic level was estimated as 3·7 (postlarval fish) and 4·1 (fish aged 3+ years).     

Catalase gene is associated with facial eczema disease resistance in sheep

Facial eczema (FE) is a hepatogenous photosensitization disease of ruminant animals, particularly in sheep which vary widely in their susceptibility to the disease. The liver damage is caused by the mycotoxin, sporidesmin. There is evidence that the toxicity of sporidesmin is due to its ability to generate 'active oxygen' species. We evaluated the catalase gene, which encodes an enzyme with antioxidant functions, as a candidate for determining the susceptibility of sheep to the disease. Two microsatellite markers, OarSHP3 and OarSHP4, which flank the sheep catalase gene, were isolated from a Yeast Artificial Chromosome (YAC) clone. These markers mapped the catalase locus by linkage to ovine chromosome 15. Eleven informative markers spaced throughout chromosome 15, inclusive of the catalase marker OarSHP4, gave no significant linkage with the disease traits when analysed in four outcross resource pedigrees. However, OarSHP3 and OarSHP4 allele frequencies showed significant differences between FE resistant and susceptible selection-lines. Comparison of sequences of catalase cDNAs from sheep of resistant and susceptible lines showed only two silent mutations. A single nucleotide polymorphisms (KP1) in exon 6 of the catalase gene also showed significant differences in allele frequencies between the selection lines. The lack of evidence for linkage in outcross pedigrees, but the significant association in the genetic lines, implies that catalase is involved in determining the susceptibility of sheep to facial eczema, and that the candidate gene's effect is probably recessive or minor.