Diana O. Fisher

Rarity of a top predator triggers continent-wide collapse of mammal prey: dingoes and marsupials in Australia

Top predators in terrestrial ecosystems may limit populations of smaller predators that could otherwise become over abundant and cause declines and extinctions of some prey. It is therefore possible that top predators indirectly protect many species of prey from excessive predation. This effect has been demonstrated in some small-scale studies, but it is not known how general or important it is in maintaining prey biodiversity. During the last 150 years, Australia has suffered the worlds highest rate of mammal decline and extinction, and most evidence points to introduced mid-sized predators (the red fox and the feral cat) as the cause. Here, we test the idea that the decline of Australias largest native predator, the dingo, played a role in these extinctions. Dingoes were persecuted from the beginning of European settlement in Australia and have been eliminated or made rare over large parts of the continent. We show a strong positive relationship between the survival of marsupials and the geographical overlap with high-density dingo populations. Our results suggest that the rarity of dingoes was a critical factor which allowed smaller predators to overwhelm marsupial prey, triggering extinction over much of the continent. This is evidence of a crucial role of top predators in maintaining prey biodiversity at large scales in terrestrial ecosystems and suggests that many remaining Australian mammals would benefit from the positive management of dingoes.

Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials.

Recent attempts to explain the susceptibility of vertebrates to declines worldwide have largely focused on intrinsic factors such as body size, reproductive potential, ecological specialization, geographical range and phylogenetic longevity. Here, we use a database of 145 Australian marsupial species to test the effects of both intrinsic and extrinsic factors in a multivariate comparative approach. We model five intrinsic (body size, habitat specialization, diet, reproductive rate and range size) and four extrinsic (climate and range overlap with introduced foxes, sheep and rabbits) factors. We use quantitative measures of geographical range contraction as indices of decline. We also develop a new modelling approach of phylogenetically independent contrasts combined with imputation of missing values to deal simultaneously with phylogenetic structuring and missing data. One extrinsic variable – geographical range overlap with sheep––was the only consistent predictor of declines. Habitat specialization was independently but less consistently associated with declines. This suggests that extrinsic factors largely determine interspecific variation in extinction risk among Australian marsupials, and that the intrinsic factors that are consistently associated with extinction risk in other vertebrates are less important in this group. We conclude that recent anthropogenic changes have been profound enough to affect species on a continent–wide scale, regardless of their intrinsic biology.

Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.

Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies.

The bridled nailtail wallaby, Onychogalea fraenata, is a relatively small, solitary and sexually size dimorphic macropod. We studied the mating system of free-ranging wallabies over 3 years, using microsatellite analysis of paternity, radiotelemetry and behavioural observations. Both sexes were promiscuous, and general reproductive behaviour was similar to that of larger, better-known macropods. Home range size influenced the number of associations with oestrous females, and was a significant component of male reproductive success. Female population density varied within the site, but males with home ranges that overlapped more females did not sire more offspring. Aggression between males occurred only around oestrous females and males did not establish a predetermined dominance hierarchy. Male body weight strongly influenced priority of access to oestrous females, and was related to age. The number of times that males were seen closest to an oestrous female when other males were present (priority of access) was the most important predictor of variation in the number of offspring sired. Females mated with several males within and between oestrous cycles, and may have influenced male-male competition by prolonging advertisement of approaching oestrus, expanding their home ranges at oestrus and engaging in mate chases that attracted groups of up to six males. Despite overall similarities in the mating system of this species and that of other macropods, male mating success may be less skewed in bridled nailtail wallabies than in other species, although paternity analysis of free-ranging populations of other species is required to confirm this conclusion. Copyright 1999 The Association for the Study of Animal Behaviour.

THE ECOLOGICAL BASIS OF LIFE HISTORY VARIATION IN MARSUPIALS

Our understanding of the diversity of mammalian life histories is based almost exclusively on eutherian mammals, in which the slow–fast continuum persists even after controlling for effects of body size and phylogeny. In this paper, we use modern comparative methods to test the extent to which this eutherian-based framework can be extrapolated to metatherian mammals. First, we examine the pattern of covariation among life history traits, and second, we test for correlations between variation in life history and variation in six candidate ecological variables: type of diet, extent of intraspecific competition, risk of juvenile mortality, diurnal pattern of activity, arboreality, and rainfall pattern. Even when controlling for body size and phylogeny, we observe a slow–fast continuum in metatherian mammals. Some parameters involved are different from those identified by studies of eutherians, but the underlying relationships among longevity, fecundity, and age at maturity persist. We also show that overall variation in a key life history variable, reproductive output (measured by annual reproductive rate and litter size), is significantly related to variation in type of diet, with a foliage-rich diet being associated with low fecundity. This is interesting because, although ecological correlations have been found within some eutherian subgroups, modern comparative approaches have failed to reveal robust ecological correlates of overall life history diversity in eutherians.

CONVERGENT MATERNAL CARE STRATEGIES IN UNGULATES AND MACROPODS

Abstract Mammals show extensive interspecific variation in the form of maternal care. Among ungulates, there is a dichotomy between species in which offspring follow the mother (“following” strategy) versus species in which offspring remain concealed (“hiding” strategy). Here we reveal that the same dichotomy exists among macropods (kangaroos, wallabies and allies). We test three traditional adaptive explanations and one new life history hypothesis, and find very similar patterns among both ungulates and macropods. The three traditional explanations that we tested were that a “following” strategy is associated with (1) open habitat, (2) large mothers, and (3) gregariousness. Our new life-history hypothesis is that a “following strategy” is associated with delayed weaning, and thus with the “slow” end of the slow-fast mammalian life-history continuum, because offspring devote resources to locomotion rather than rapid growth. Our comparative test strongly supports the habitat structure hypothesis and provides some support for this new delayed weaning hypothesis for both ungulates and macropods. We propose that sedentary young in closed habitats benefit energetically by having milk brought to them. In open habitats, predation pressure will select against hiding. Followers will suffer slower growth to independence. Taken together, therefore, our results provide the first quantitative evidence that macropods and ungulates are convergent with respect to interspecific variation in maternal care strategy. In both clades, differences between species in the form of parental care are due to a similar interaction between habitat, social behavior, and life history. Corresponding Editor: B. Crespi

Correlates of rediscovery and the detectability of extinction in mammals

Extinction is difficult to detect, even in well-known taxa such as mammals. Species with long gaps in their sighting records, which might be considered possibly extinct, are often rediscovered. We used data on rediscovery rates of missing mammals to test whether extinction from different causes is equally detectable and to find which traits affect the probability of rediscovery. We find that species affected by habitat loss were much more likely to be misclassified as extinct or to remain missing than those affected by introduced predators and diseases, or overkill, unless they had very restricted distributions. We conclude that extinctions owing to habitat loss are most difficult to detect; hence, impacts of habitat loss on extinction have probably been overestimated, especially relative to introduced species. It is most likely that the highest rates of rediscovery will come from searching for species that have gone missing during the 20th century and have relatively large ranges threatened by habitat loss, rather than from additional effort focused on charismatic missing species.

Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk.

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.

Sperm competition drives the evolution of suicidal reproduction in mammals

Significance In some marsupial genera but in no other mammals, escalating stress hormones during the breeding season cause immune system collapse and synchronized death after mating in all males (suicidal reproduction). In this paper, we resolve the environmental drivers and adaptive mechanism of sexual selection responsible for the repeated evolution of this surprising and extreme life history strategy in mammals. The strategy of synchronized suicidal reproduction in mammals resulting in male death before offspring are born has often been attributed to altruistic or kin-selected paternal suicide to avoid food depletion. We show that rather than altruism or kin-selection, individual sexual selection leads to apparent self-sacrifice in these genera. Suicidal reproduction (semelparity) has evolved in only four genera of mammals. In these insectivorous marsupials, all males die after mating, when failure of the corticosteroid feedback mechanism elevates stress hormone levels during the mating season and causes lethal immune system collapse (die-off). We quantitatively test and resolve the evolutionary causes of this surprising and extreme life history strategy. We show that as marsupial predators in Australia, South America, and Papua New Guinea diversified into higher latitudes, seasonal predictability in abundance of their arthropod prey increased in multiple habitats. More-predictable prey peaks were associated with shorter annual breeding seasons, consistent with the suggestion that females accrue fitness benefits by timing peak energy demands of reproduction to coincide with maximum food abundance. We demonstrate that short mating seasons intensified reproductive competition between males, increasing male energy investment in copulations and reducing male postmating survival. However, predictability of annual prey cycles alone does not explain suicidal reproduction, because unlike insect abundance, peak ovulation dates in semelparous species are often synchronized to the day among years, triggered by a species-specific rate of change of photoperiod. Among species with low postmating male survival, we show that those with suicidal reproduction have shorter mating seasons and larger testes relative to body size. This indicates that lethal effort is adaptive in males because females escalate sperm competition by further shortening and synchronizing the annual mating period and mating promiscuously. We conclude that precopulatory sexual selection by females favored the evolution of suicidal reproduction in mammals.

Correlates of recent declines of rodents in northern and southern Australia : habitat structure is critical

Australia has experienced dramatic declines and extinctions of its native rodent species over the last 200 years, particularly in southern Australia. In the tropical savanna of northern Australia significant declines have occurred only in recent decades. The later onset of these declines suggests that the causes may differ from earlier declines in the south. We examine potential regional effects (northern versus southern Australia) on biological and ecological correlates of range decline in Australian rodents. We demonstrate that rodent declines have been greater in the south than in the tropical north, are strongly influenced by phylogeny, and are consistently greater for species inhabiting relatively open or sparsely vegetated habitat. Unlike in marsupials, where some species have much larger body size than rodents, body mass was not an important predictor of decline in rodents. All Australian rodent species are within the prey-size range of cats (throughout the continent) and red foxes (in the south). Contrary to the hypothesis that mammal declines are related directly to ecosystem productivity (annual rainfall), our results are consistent with the hypothesis that disturbances such as fire and grazing, which occur in non-rainforest habitats and remove cover used by rodents for shelter, nesting and foraging, increase predation risk. We agree with calls to introduce conservation management that limits the size and intensity of fires, increases fire patchiness and reduces grazing impacts at ecological scales appropriate for rodents. Controlling feral predators, even creating predator-free reserves in relatively sparsely-vegetated habitats, is urgently required to ensure the survival of rodent species, particularly in northern Australia where declines are not yet as severe as those in the south.