Conservation cornerstones : capitalising on the endeavours of long-term monitoring projects

Ecological monitoring is widely used to measure change through time in ecosystems. The current extinction crisis has resulted in a wealth of monitoring programs focussed on tracking the status of threatened species, and the perceived importance of monitoring has seen it become the cornerstone of many biodiversity conservation programs. However, many monitoring programs fail to produce useful outcomes due to inherent flaws. Here we use a monitoring program from south-eastern Australia as a case study to illustrate the potential of such endeavours. The threatened carnivorous marsupial, the brush-tailed phascogale (Phascogale tapoatafa), has been monitored at various locations between 2000 and 2010. We present strong evidence for a decline in relative abundance during this period, and also describe relationships with environmental variables. These results provide insights likely to be valuable in guiding future management of the species. In the absence of the monitoring program, informed management would not be possible. While early detection of population declines is important, knowledge of the processes driving such declines is required for effective intervention. We argue that monitoring programs will be most effective as a tool for enhanced conservation management if they test specific hypotheses relating to changes in population trajectories. Greater emphasis should be placed on rigorous statistical analysis of monitoring datasets in order to capitalise on the resources devoted to monitoring activities. Many datasets are likely to exist for which careful analysis of results would have benefits for determining management directions.

Anthropogenic selection enhances cancer evolution in Tasmanian devil tumours

The Tasmanian Devil Facial Tumour Disease (DFTD) provides a unique opportunity to elucidate the long-term effects of natural and anthropogenic selection on cancer evolution. Since first observed in 1996, this transmissible cancer has caused local population declines by >90%. So far, four chromosomal DFTD variants (strains) have been described and karyotypic analyses of 253 tumours showed higher levels of tetraploidy in the oldest strain. We propose that increased ploidy in the oldest strain may have evolved in response to effects of genomic decay observed in asexually reproducing organisms. In this study, we focus on the evolutionary response of DFTD to a disease suppression trial. Tumours collected from devils subjected to the removal programme showed accelerated temporal evolution of tetraploidy compared with tumours from other populations where no increase in tetraploid tumours were observed. As ploidy significantly reduces tumour growth rate, we suggest that the disease suppression trial resulted in selection favouring slower growing tumours mediated by an increased level of tetraploidy. Our study reveals that DFTD has the capacity to rapidly respond to novel selective regimes and that disease eradication may result in novel tumour adaptations, which may further imperil the long-term survival of the world's largest carnivorous marsupial.

Telomere dynamics and homeostasis in a transmissible cancer

Devil Facial Tumour Disease (DFTD) is a unique clonal cancer that threatens the world's largest carnivorous marsupial, the Tasmanian devil (Sarcophilus harrisii) with extinction. This transmissible cancer is passed between individual devils by cell implantation during social interactions. The tumour arose in a Schwann cell of a single devil over 15 years ago and since then has expanded clonally, without showing signs of replicative senescence; in stark contrast to a somatic cell that displays a finite capacity for replication, known as the “Hayflick limit”.

From doubly labelled water to half-life; validating radio-isotopic rubidium turnover to measure metabolism in small vertebrates

The doubly labelled water method (DLW) is widely used to measure field metabolic rate (FMR), but it has some limitations. Here, we validate an innovative technique for measuring FMR by comparing the turnover of isotopic rubidium (86Rb kb) with DLW depletion and the rate of CO2 production (V·co2) measured by flow-through respirometry (FTR) for two dunnart species (Marsupialia: Dasyuridae), Sminthopsis macroura (17 g) and Sminthopsis ooldea (10 g). The rate of metabolism as assessed by V·co2 (FTR) and 86Rb kb was significantly correlated for both species (S. macroura, r2 = 0·81, P = 1·19 × 10-5; S. ooldea, r2 = 0·63, P = 3·84 × 10-4), as was V·co2 from FTR and DLW for S. macroura (r2 = 0·43, P = 0·039), but not for S. ooldea (r2 = 0·29, P = 0·168). There was no relationship between V·co2 from DLW and 86Rb kb for either species (S. macroura r2 = 0·22, P = 0·169; S. ooldea r2 = 0·21, P = 0·253). We conclude that 86Rb kb provided useful estimates of metabolic rate for dunnarts. Meta-analysis provided different linear relationships between V·co2 and 86Rb kb for endotherms and ectotherms, suggesting different proportionalities between metabolic rate and 86Rb kb for different taxa. Understanding the mechanistic basis for this correlation might provide useful insights into the cause of these taxonomic differences in the proportionality. At present, it is essential that the relationship between metabolic rate and 86Rb kb be validated for each taxon of interest. The advantages of the 86Rb technique over DLW include lower equipment requirements and technical expertise, and the longer time span over which measurements can be made. The 86Rb method might be particularly useful for estimating FMR of groups for which the assumptions of the DLW technique are compromised (e.g. amphibians, diving species and fossorial species), and groups that are practically challenging for DLW studies (e.g. insects). © 2013 British Ecological Society.

Prey of the silver-headed antechinus (Antechinus argentus), a new species of Australian dasyurid marsupial

The silver-headed antechinus (Antechinus argentus) is one of Australia’s most recently described mammals, and the single known population at Kroombit Tops in south-east Queensland is threatened. Nothing is known of the species’ ecology, so during 2014 we collected faecal pellets each month (March–September) from a population at the type locality to gather baseline data on diet composition. A total of 38 faecal pellets were collected from 12 individuals (eight females, four males) and microscopic analysis of pellets identified seven invertebrate orders, with 70% combined mean composition of beetles (Coleoptera: 38%) and cockroaches (Blattodea: 32%). Other orders that featured as prey were ants, crickets/grasshoppers, butterflies/moths, spiders, and true bugs. Given that faecal pellets could only be collected from a single habitat type (Eucalyptus montivaga high-altitude open forest) and location, this is best described as a generalist insectivorous diet that is characteristic of other previously studied congeners.

Dasyurid dilemmas: problems and solutions for conserving Australia's small carnivorous marsupials

Dasyurid marsupials are distributed throughout the major terrestrial environments of Australia but since European settlement have suffered local and regional extinctions, range reductions and population declines. In this paper we examine the conservation status of small dasyurids (<500 g) and the threats they face. We also evaluate recovery procedures for threatened taxa and assess their success. Twenty-four percent of smaller dasyurids are classified as vulnerable, endangered or data deficient. Large body size and occupancy of one or two habitat types are correlated strongly with  endangerment species currently considered as 'low risk, near threatened' group closely with vulnerable and endangered species, indicating a risk of further declines. The processes contributing most to declines include habitat loss and fragmentation, altered fire regimes and predation. As of April 200 I, no Recovery Plans had been adopted by the Commonwealth Govemment for any small dasyund species. There is much information on the reproduction and development of smaller dasyurids, making them suitable for captive breeding. However, captive breeding programs have been limited. the  dibbler Paranrechinus apicalis being the only species bred systematically for reintroductions. There is a need for integration between captive breeding programs and recovery planning. as well as for more information on the population viability and metapopulation structures of small dasyurids genetic diversity of populations and inbreeding depression. We suggest a program of survey. research. management and education to Improve conservation outcomes for all small dasyurids.

Glaucodon Ballaratensis (Marsupialia, Dasyridae), a late Pliocene 'Devil' from Batesford, Victoria

The right mandible of a dasyurid from Pliocene sediments at Batesford, near Geelong, Victoria is described as a new specimen of Glaucodon ballaratensis Stirton, 1957. The new specimen is morphologically close to the holotype of Glaucodon ballaratensis. Several dental characteristics of the new specimen unknown from the holotype of Glaucodon ballaratensis are close to those of Sarcophilus moornaensis Crabb, 1982. Glaucodon ballaratensis also shares features with Dasyurus maculatus Kerr, 1792 and Sarcophilus laniarius harrisii Boitard, 1842, and hence the Batesford specimen offers additional information on the origins of these dasyurids.

Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore

Genetic diversity and population structure were investigated across the core range of Tasmanian devils (Sarcophilus laniarius; Dasyuridae), a wide-ranging marsupial carnivore restricted to the island of Tasmania. Heterozygosity (0.386-0.467) and allelic diversity (2.7-3.3) were low in all subpopulations and allelic size ranges were small and almost continuous, consistent with a founder effect. Island effects and repeated periods of low population density may also have contributed to the low variation. Within continuous habitat, gene flow appears extensive up to 50 km (high assignment rates to source or close neighbour populations; nonsignificant values of pairwise F-ST), in agreement with movement data. At larger scales (150-250 km), gene flow is reduced (significant pairwise F-ST) but there is no evidence for isolation by distance. The most substantial genetic structuring was observed for comparisons spanning unsuitable habitat, implying limited dispersal of devils between the well-connected, eastern populations and a smaller northwestern population. The genetic distinctiveness of the northwestern population was reflected in all analyses: unique alleles; multivariate analyses of gene frequency (multidimensional scaling, minimum spanning tree, nearest neighbour); high self-assignment (95%); two distinct populations for Tasmania were detected in isolation by distance and in Bayesian model-based clustering analyses. Marsupial carnivores appear to have stronger population subdivisions than their placental counterparts.

Plasma steroids and steroid-binding capacity in male semelparous dasyurid marsupials (Phascogale tapoatafa) that survive beyond the breeding season in captivity

The semelparous dasyurids display a unique life history, in that all males die within a few weeks of the completion of the breeding season. Studies of several semelparous species have revealed that the male die-off is stress-related, and accompanied by increased plasma androgen and cortisol levels and decreased corticosteroid binding capacity, resulting in suppression of immune and inflammatory responses. This study examines the endocrine profile of male brush-tailed phascogales (Phascogale tapoatafa) that survive beyond the breeding season in captivity. Plasma cortisol, corticosteroid binding globulin and albumin levels were monitored in both males and females and steroid partitioning calculated. Captive males surviving beyond the breeding season did not show the elevation in plasma cortisol and decrease in corticosteroid binding capacity reported in wild males. Plasma albumin concentrations also remained constant during the sampling period. These data indicate that captive males do not undergo the same stress response described in wild populations. (c) 2006 Elsevier Inc. All rights reserved.

Combined mitochondrial and nuclear DNA sequences resolve the interrelations of the major Australasian marsupial radiations

Australasian marsupials include three major radiations, the insectivorous/carnivorous Dasyuromorphia, the omnivorous bandicoots (Peramelemorphia), and the largely herbivorous diprotodontians. Morphologists have generally considered the bandicoots and diprotodontians to be closely related, most prominently because they are both syndactylous (with the 2nd and 3rd pedal digits being fused). Molecular studies have been unable to confirm or reject this Syndactyla hypothesis. Here we present new mitochondrial (mt) genomes from a spiny bandicoot (Echymipera rufescens) and two dasyurids, a fat-tailed dunnart (Sminthopsis crassicaudata) and a northern quoll (Dasyurus hallucatus). By comparing trees derived from pairwise base-frequency differences between taxa with standard (absolute, uncorrected) distance trees, we infer that composition bias among mt protein-coding and RNA sequences is sufficient to mislead tree reconstruction. This can explain incongruence between trees obtained from mt and nuclear data sets. However, after excluding major sources of compositional heterogeneity, both the “reduced-bias” mt and nuclear data sets clearly favor a bandicoot plus dasyuromorphian association, as well as a grouping of kangaroos and possums (Phalangeriformes) among diprotodontians. Notably, alternatives to these groupings could only be confidently rejected by combining the mt and nuclear data. Elsewhere on the tree, Dromiciops appears to be sister to the monophyletic Australasian marsupials, whereas the placement of the marsupial mole (Notoryctes) remains problematic. More generally, we contend that it is desirable to combine mt genome and nuclear sequences for inferring vertebrate phylogeny, but as separately modeled process partitions. This strategy depends on detecting and excluding (or accounting for) major sources of nonhistorical signal, such as from compositional nonstationarity.

Developmental origins of precocial forelimbs in marsupial neonates.

Marsupial mammals are born in an embryonic state, as compared with their eutherian counterparts, yet certain features are accelerated. The most conspicuous of these features are the precocial forelimbs, which the newborns use to climb unaided from the opening of the birth canal to the teat. The developmental mechanisms that produce this acceleration are unknown. Here we show that heterochronic and heterotopic changes early in limb development contribute to forelimb acceleration. Using Tbx5 and Tbx4 as fore- and hindlimb field markers, respectively, we have found that, compared with mouse, both limb fields arise notably early during opossum development. Patterning of the forelimb buds is also accelerated, as Shh expression appears early relative to the outgrowth of the bud itself. In addition, the forelimb fields and forelimb myocyte allocation are increased in size and number, respectively, and migration of the spinal nerves into the forelimb bud has been modified. This shift in the extent of the forelimb field is accompanied by shifts in Hox gene expression along the anterior-posterior axis. Furthermore, we found that both fore- and hindlimb fields arise gradually during gastrulation and extension of the embryonic axis, in contrast to the appearance of the limb fields in their entirety in all other known cases. Our results show a surprising evolutionary flexibility in the early limb development program of amniotes and rule out the induction of the limb fields by mature structures such as the somites or mesonephros.

Comparison of life-history characteristics of island and mainland populations of the swamp antechinus

The reproductive ecology of the swamp antechinus Antechinus minimus, a small dasyurid (Dasyuridae) marsupial with obligate male semelparity, was investigated in populations inhabiting the mainland coast and on a nearby offshore island in south-eastern Australia. The size and sex ratios of litters, individual body mass and size, timing of births and female longevity were determined from live-trapped animals. The island population had significantly smaller litter sizes and greater adult body mass in comparison with the mainland population. This is consistent with features of the ‘island syndrome’, which predicts directional selection for these traits in high-density populations with reduced extrinsic mortality. However, inter-annual variability in litter sizes in the island population suggests that litter size is more responsive to fluctuating local conditions, such as population density, which is likely to affect food availability, rather than directional genetic changes. In contrast with other antechinus species, biased sex ratios were not evident. In addition, large variations of the timing of births were estimated at both sites and these appear to be related to seasonal conditions such as autumn rainfall and female body mass before mating.

High muscle mitochondrial volume and aerobic capacity in a small marsupial (Sminthopsis crassicaudata) reveals flexible links between energy-use levels in mammals

We investigated the muscle structure-function relationships that underlie the aerobic capacity of an insectivorous, small (~15?g) marsupial, Sminthopsis crassicaudata (Family: Dasyuridae), to obtain further insight into energy use patterns in marsupials relative to those in placentals, their sister clade within the Theria (advanced mammals). Disparate hopping marsupials (Suborder Macropodiformes), a kangaroo (Macropus rufus) and a rat-kangaroo (Bettongia penicillata), show aerobic capabilities as high as those of 'athletic' placentals. Equivalent muscle mitochondrial volumes and cardiovascular features support these capabilities. We examined S. crassicaudata to determine whether highly developed aerobic capabilities occur elsewhere in marsupials, rather than being restricted to the more recently evolved Macropodiformes. This was the case. Treadmill-trained S. crassicaudata attained a maximal aerobic metabolic rate (VO2,max or MMR) of 272ml O2min-1kg -1 (N=8), similar to that reported for a small (?20g), 'athletic' placental, Apodemus sylvaticus, 264ml O2min -1kg-1. Hopping marsupials have comparable aerobic levels when body mass variation is considered. Sminthopsis crassicaudata has a basal metabolic rate (BMR) about 75% of placental values but it has a notably large factorial aerobic scope (fAS) of 13, elevated fAS also features in hopping marsupials. The VO2,max of S. crassicaudata was supported by an elevated total muscle mitochondrial volume, which was largely achieved through high muscle mitochondrial volume densities, Vv(mt,f), the mean value being 14.0±1.33%. These data were considered in relation to energy use levels in mammals, particularly field metabolic rate (FMR). BMR is consistently lower in marsupials, but this is balanced by a high fAS, such that marsupial MMR matches that of placentals. However, FMR shows different mass relationships in the two clades, with the FMR of small (<, 125 g) marsupials, such as S. crassicaudata, being higher than that in comparably sized placentals, with the reverse applying for larger marsupials. The flexibility of energy output in marsupials provides explanations for this pattern. Overall, our data refute widely held notions of mechanistically closely linked relationships between body mass, BMR, FMR and MMR in mammals generally.