Manganese Exacerbates Seasonal Health Declines in a Suicidally Breeding Mammal.

Reproductive costs must be balanced with survival to maximize lifetime reproductive rates; however, some organisms invest in a single, suicidal bout of breeding known as semelparity. The northern quoll (Dasyurus hallucatus) is an endangered marsupial in which males, but not females, are semelparous. Northern quolls living near mining sites on Groote Eylandt, Northern Territory, Australia, accumulate manganese (Mn) in their brains, testes, and hair, and elevated Mn impacts motor performance. Whether Mn is associated with other health declines is yet unknown. In the present study we show that male and female northern quolls with higher Mn accumulation had a 20% reduction in immune function and a trend toward reduced cortisol concentrations in hair. The telomere lengths of male quolls did not change pre- to postbreeding, but those with higher Mn levels had longer telomeres; in contrast, the telomeres of females shortened during the breeding season but recovered between the first year and second year of breeding. In addition, the telomeres of quolls that were recaptured declined at significantly higher rates in quolls with higher Mn between prebreeding, breeding, and/or postbreeding seasons. Future research should determine whether changes in cortisol, immune function, or telomere length affect reproductive output or survival-particularly for semelparous males. Environ Toxicol Chem 2024;43:74-86. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads.

Mammal declines across northern Australia are one of the major biodiversity loss events occurring globally. There has been no regional assessment of the implications of these species declines for genomic diversity. To address this, we conducted a species-wide assessment of genomic diversity in the northern quoll (Dasyurus hallucatus), an Endangered marsupial carnivore. We used next generation sequencing methods to genotype 10,191 single nucleotide polymorphisms (SNPs) in 352 individuals from across a 3220-km length of the continent, investigating patterns of population genomic structure and diversity, and identifying loci showing signals of putative selection. We found strong heterogeneity in the distribution of genomic diversity across the continent, characterized by (i) biogeographical barriers driving hierarchical population structure through long-term isolation, and (ii) severe reductions in diversity resulting from population declines, exacerbated by the spread of introduced toxic cane toads (Rhinella marina). These results warn of a large ongoing loss of genomic diversity and associated adaptive capacity as mammals decline across northern Australia. Encouragingly, populations of the northern quoll established on toad-free islands by translocations appear to have maintained most of the initial genomic diversity after 16 years. By mapping patterns of genomic diversity within and among populations, and investigating these patterns in the context of population declines, we can provide conservation managers with data critical to informed decision-making. This includes the identification of populations that are candidates for genetic management, the importance of remnant island and insurance/translocated populations for the conservation of genetic diversity, and the characterization of putative evolutionarily significant units.

Skull shape of a widely distributed, endangered marsupial reveals little evidence of local adaptation between fragmented populations.

The biogeographic distribution of diversity among populations of threatened mammalian species is generally investigated using population genetics. However, intraspecific phenotypic diversity is rarely assessed beyond taxonomy-focused linear measurements or qualitative descriptions. Here, we use a technique widely used in the evolutionary sciences-geometric morphometrics-to characterize shape diversity in the skull of an endangered marsupial, the northern quoll, across its 5,000 km distribution range along Northern Australia. Skull shape is a proxy for feeding, behavior, and phenotypic differentiation, allowing us to ask whether populations can be distinguished and whether patterns of variation indicate adaptability to changing environmental conditions. We analyzed skull shape in 101 individuals across four mainland populations and several islands. We assessed the contribution of population, size, sex, rainfall, temperature, and geography to skull shape variation using principal component analysis, Procrustes ANOVA, and variation partitioning analyses. The populations harbor similar amounts of broadly overlapping skull shape variation, with relatively low geographic effects. Size predicted skull shape best, coinciding with braincase size variation and differences in zygomatic arches. Size-adjusted differences in populations explained less variation with far smaller effect sizes, relating to changes in the insertion areas of masticatory muscles, as well as the upper muzzle and incisor region. Climatic and geographic variables contributed little. Strikingly, the vast majority of shape variation-76%-remained unexplained. Our results suggest a uniform intraspecific scope for shape variation, possibly due to allometric constraints or phenotypic plasticity beyond the relatively strong allometric effect. The lack of local adaptation indicates that cross-breeding between populations will not reduce local morphological skull (and probably general musculoskeletal) adaptation because none exists. However, the potential for heritable morphological variation (e.g., specialization to local diets) seems exceedingly limited. We conclude that 3D geometric morphometrics can provide a comprehensive, statistically rigorous phenomic contribution to genetic-based conservation studies.

Greater agility increases probability of survival in the endangered northern quoll.

Introduced predators combined with habitat loss and modification are threatening biodiversity worldwide, particularly the 'critical weight range' (CWR) mammals of Australia. In order to mitigate the impacts of invasive predators on native species in different landscapes, we must understand how the prey's morphology and performance determine their survival. Here, we evaluated how phenotypic traits related to escape performance predict the probability of survival for an endangered CWR mammal, the northern quoll (Dasyurus hallucatus). We measured mass, body size, body shape, body condition and age, as well as maximum sprint speed, acceleration and agility of female quolls over two consecutive years. Those with higher body condition and agility around a 135 deg corner were more likely to survive their first 21 months of life but were not more likely to survive after this period. No other morphological or performance traits affected survival. Heavier second-year individuals were more agile than first years but second years experienced higher mortality rates throughout the year. Females with higher body condition and agility around a 135 deg corner tended to have shorter limbs and feet but longer heads. Our findings suggest that higher body condition and agility are advantageous for survival in female northern quolls. These results can be used to develop predictive models of predator-prey interactions based on performance capacity and how performance is affected by habitat, aiding conservation efforts to predict and manage the impact of introduced predators on native species.

Moving in complex environments: a biomechanical analysis of locomotion on inclined and narrow substrates.

Characterisation of an organism's performance in different habitats provides insight into the conditions that allow it to survive and reproduce. In recent years, the northern quoll (Dasyurus hallucatus) - a medium-sized semi-arboreal marsupial native to northern Australia - has undergone significant population declines within open forest, woodland and riparian habitats, but less so in rocky areas. To help understand this decline, we quantified the biomechanical performance of wild northern quolls as they ran up inclined narrow (13 mm pole) and inclined wide (90 mm platform) substrates. We predicted that quolls may possess biomechanical adaptations to increase stability on narrow surfaces, which are more common in rocky habitats. Our results showed that quolls have some biomechanical characteristics consistent with a stability advantage on narrow surfaces. This includes the coupled use of limb pairs, as indicated via a decrease in footfall time, and an ability to produce corrective torques to counteract the toppling moments commonly encountered during gait on narrow surfaces. However, speed was constrained on narrow surfaces, and quolls did not adopt diagonal sequence gaits, unlike true arboreal specialists such as primates. In comparison with key predators, such as cats and dogs, northern quolls appear inferior in terrestrial environments but have a stability advantage at higher speeds on narrow supports. This may partially explain the heterogeneous declines in northern quoll populations among various habitats on mainland Australia.

Manganese contamination affects the motor performance of wild northern quolls (Dasyurus hallucatus).

Neuromotor deficits are an important sign of manganese (Mn) toxicity in humans and laboratory animals. However, the impacts of Mn exposure on the motor function of wild animals remains largely unknown. Here, we assessed the impact of chronic exposure to Mn from active mining operations on Groote Eylandt, Australia on the motor function of the semi-arboreal northern quoll (Dasyurus hallucatus), an endangered species. The three motor tests conducted-maximum sprint speed on a straight run, manoeuvrability around a corner, and motor control on a balance beam-showed that elevated Mn body burden did not diminish performance of these traits. However, quolls with higher Mn body burden approached a corner at a significantly narrower range of speeds, due to a significantly lower maximum approach speed. Slower speeds approaching a turn may reduce success at catching prey and avoiding predators. Given that maximum sprint speed on a straight run was not affected by Mn body burden, but maximum speed entering a corner was, slower speeds approaching a turn may reflect compensation for otherwise impaired performance in the turn.

Sex-specific thermal sensitivities of performance and activity in the asian house gecko, Hemidactylus frenatus.

Studies of sexual selection primarily focus on morphological traits such as body size and secondary trait dimorphism, with less attention been given to the functional differences between the sexes and even more so their thermal performance capacities. Each sex may benefit from possessing different thermal performance capacities that would allow them to maximise their fitness relative to their different reproductive roles; especially when performances are closely related to reproductive success. Here, we examine sexual divergence in thermal sensitivities of performance across three populations of the Asian house gecko (Hemidactylus frenatus) over an extensive latitudinal cline. Using analyses of the thermal sensitivity of routine activity, bite force and sprint speed, we explored whether: (i) males and females differed in their optimal temperatures for performance, (ii) the sexes differed in their thermal sensitivities of performance, and (iii) the degree of sexual divergence in thermal sensitivity varied among the populations. Because male H. frenatus are highly aggressive and frequently engage in combat to gain territories and mating opportunities, we expected males would be active over a wider range of temperatures than females and this would favour broad thermal sensitivity curves for males. In addition, we expected a greater divergence between the sexes in thermal sensitivities for the temperate populations that experience greater daily and seasonal thermal variation. We found that males were more active, and had greater bite forces and faster sprint speeds than females, independent of body size. In addition, we found differences between the sexes in thermal sensitivities for the tropical population; female H. frenatus were less active and possessed lower sprint speeds at higher temperatures than males. Although H. frenatus from the most variable thermal environments also displayed the broadest thermal performance range, it was the more stable tropical population that exhibited the greatest divergence between the sexes in thermal sensitivity of performance. The divergence in thermal physiology that we detected between the sexes of H. frenatus is consistent with the idea that males will derive mating and territorial advantages for maintaining function over a broader range of temperatures.

Manganese accumulates in the brain of northern quolls (Dasyurus hallucatus) living near an active mine.

Mining is fundamental to the Australian economy, yet little is known about how potential contaminants bioaccumulate and affect wildlife living near active mining sites. Here, we show using air sampling that fine manganese dust within the respirable size range is found at levels exceeding international recommendations even 20 km from manganese extraction, processing, and storage facilities on Groote Eylandt, Northern Territory. Endangered northern quolls (Dasyurus hallucatus) living near mining sites were found to have elevated manganese concentrations within their hair, testes, and in two brain regions-the neocortex and cerebellum, which are responsible for sensory perception and motor function, respectively. Accumulation in these organs has been associated with adverse reproductive and neurological effects in other species and could affect the long-term population viability of northern quolls.