A stochastic model for estimating sustainable limits to wildlife mortality in a changing world

Human-caused mortality of wildlife is a pervasive threat to biodiversity. Assessing the population-level impact of fisheries bycatch and other human-caused mortality of wildlife has typically relied upon deterministic methods. However, population declines are often accelerated by stochastic factors that are not accounted for in such conventional methods. Building on the widely applied potential biological removal (PBR) equation, we devised a new population modeling approach for estimating sustainable limits to human-caused mortality and applied it in a case study of bottlenose dolphins affected by capture in an Australian demersal otter trawl fishery. Our approach, termed sustainable anthropogenic mortality in stochastic environments (SAMSE), incorporates environmental and demographic stochasticity, including the dependency of offspring on their mothers. The SAMSE limit is the maximum number of individuals that can be removed without causing negative stochastic population growth. We calculated a PBR of 16.2 dolphins per year based on the best abundance estimate available. In contrast, the SAMSE model indicated that only 2.3–8.0 dolphins could be removed annually without causing a population decline in a stochastic environment. These results suggest that reported bycatch rates are unsustainable in the long term, unless reproductive rates are consistently higher than average. The difference between the deterministic PBR calculation and the SAMSE limits showed that deterministic approaches may underestimate the true impact of human-caused mortality of wildlife. This highlights the importance of integrating stochasticity when evaluating the impact of bycatch or other human-caused mortality on wildlife, such as hunting, lethal control measures, and wind turbine collisions. Although population viability analysis (PVA) has been used to evaluate the impact of human-caused mortality, SAMSE represents a novel PVA framework that incorporates stochasticity for estimating acceptable levels of human-caused mortality. It offers a broadly applicable, stochastic addition to the demographic toolbox to evaluate the impact of human-caused mortality on wildlife.     

Adaptive introgression as a resource for management and genetic conservation in a changing climate

Current rates of climate change require organisms to respond through migration, phenotypic plasticity, or genetic changes via adaptation. We focused on questions regarding species’ and populations’ ability to respond to climate change through adaptation. Specifically, the role adaptive introgression, movement of genetic material from the genome of 1 species into the genome of another through repeated interbreeding, may play in increasing species’ ability to respond to a changing climate. Such interspecific gene flow may mediate extinction risk or consequences of limited adaptive potential that result from standing genetic variation and mutation alone, enabling a quicker demographic recovery in response to changing environments. Despite the near dismissal of the potential benefits of hybridization by conservation practitioners, we examined a number of case studies across different taxa that suggest gene flow between sympatric or parapatric sister species or within species that exhibit strong ecotypic differentiation may represent an underutilized management option to conserve evolutionary potential in a changing environment. This will be particularly true where advanced‐generation hybrids exhibit adaptive traits outside the parental phenotypic range, a phenomenon known as transgressive segregation. The ideas presented in this essay are meant to provoke discussion regarding how we maintain evolutionary potential, the conservation value of natural hybrid zones, and consideration of their important role in adaptation to climate.     

Aligning science and policy to achieve evolutionarily enlightened conservation

There is increasing recognition among conservation scientists that long‐term conservation outcomes could be improved through better integration of evolutionary theory into management practices. Despite concerns that the importance of key concepts emerging from evolutionary theory (i.e., evolutionary principles and processes) are not being recognized by managers, there has been little effort to determine the level of integration of evolutionary theory into conservation policy and practice. We assessed conservation policy at 3 scales (international, national, and provincial) on 3 continents to quantify the degree to which key evolutionary concepts, such as genetic diversity and gene flow, are being incorporated into conservation practice. We also evaluated the availability of clear guidance within the applied evolutionary biology literature as to how managers can change their management practices to achieve better conservation outcomes. Despite widespread recognition of the importance of maintaining genetic diversity, conservation policies provide little guidance about how this can be achieved in practice and other relevant evolutionary concepts, such as inbreeding depression, are mentioned rarely. In some cases the poor integration of evolutionary concepts into management reflects a lack of decision‐support tools in the literature. Where these tools are available, such as risk‐assessment frameworks, they are not being adopted by conservation policy makers, suggesting that the availability of a strong evidence base is not the only barrier to evolutionarily enlightened management. We believe there is a clear need for more engagement by evolutionary biologists with policy makers to develop practical guidelines that will help managers make changes to conservation practice. There is also an urgent need for more research to better understand the barriers to and opportunities for incorporating evolutionary theory into conservation practice.     

Using historical ecology to reassess the conservation status of coniferous forests in Central Europe

Forests cover approximately one‐third of Central Europe. Oak (Quercus) and European beech (Fagus sylvatica) are considered the natural dominants at low and middle elevations, respectively. Many coniferous forests (especially of Picea abies) occur primarily at midelevations, but these are thought to have resulted from forestry plantations planted over the past 200 years. Nature conservation and forestry policy seek to promote broadleaved trees over conifers. However, there are discrepancies between conservation guidelines (included in Natura 2000) and historical and palaeoecological data with regard to the distribution of conifers. Our aim was to bring new evidence to the debate on the conservation of conifers versus broadleaved trees at midelevations in Central Europe. We created a vegetation and land‐cover model based on pollen data for a highland area of 11,300 km² in the Czech Republic and assessed tree species composition in the forests before the onset of modern forestry based on 18th‐century archival sources. Conifers dominated the study region throughout the entire Holocene (approximately 40–60% of the area). Broadleaved trees were present in a much smaller area than envisaged by current ideas of natural vegetation. Rather than casting doubt on the principles of Central European nature conservation in general, our results highlight the necessity of detailed regional investigations and the importance of historical data in challenging established notions on the natural distribution of tree species.     

Fixism and conservation science

The field of biodiversity conservation has recently been criticized as relying on a fixist view of the living world in which existing species constitute at the same time targets of conservation efforts and static states of reference, which is in apparent disagreement with evolutionary dynamics. We reviewed the prominent role of species as conservation units and the common benchmark approach to conservation that aims to use past biodiversity as a reference to conserve current biodiversity. We found that the species approach is justified by the discrepancy between the time scales of macroevolution and human influence and that biodiversity benchmarks are based on reference processes rather than fixed reference states. Overall, we argue that the ethical and theoretical frameworks underlying conservation research are based on macroevolutionary processes, such as extinction dynamics. Current species, phylogenetic, community, and functional conservation approaches constitute short‐term responses to short‐term human effects on these reference processes, and these approaches are consistent with evolutionary principles.     

Combined effects of life-history traits and human impact on extinction risk of freshwater megafauna

Megafauna species are intrinsically vulnerable to human impact. Freshwater megafauna (i.e., freshwater animals ≥30 kg, including fishes, mammals, reptiles, and amphibians) are subject to intensive and increasing threats. Thirty-four species are listed as critically endangered on the International Union for Conservation of Nature (IUCN). Red List of Threatened Species, the assessments for which are an important basis for conservation actions but remain incomplete for 49 (24%) freshwater megafauna species. Consequently, the window of opportunity for protecting these species could be missed. Identifying the factors that predispose freshwater megafauna to extinction can help predict their extinction risk and facilitate more effective and proactive conservation actions. Thus, we collated 8 life-history traits for 206 freshwater megafauna species. We used generalized linear mixed models to examine the relationships between extinction risk based on the IUCN Red List categories and the combined effect of multiple traits, as well as the effect of human impact on these relationships for 157 classified species. The most parsimonious model included human impact and traits related to species’ recovery potential including life span, age at maturity, and fecundity. Applying the most parsimonious model to 49 unclassified species predicted that 17 of them are threatened. Accounting for model predictions together with IUCN Red List assessments, 50% of all freshwater megafauna species are considered threatened. The Amazon and Yangtze basins emerged as global diversity hotspots of threatened freshwater megafauna, in addition to existing hotspots, including the Ganges-Brahmaputra and Mekong basins and the Caspian Sea region. Assessment and monitoring of those species predicted to be threatened are needed, especially in the Amazon and Yangtze basins. Investigation of life-history traits and trends in population and distribution, regulation of overexploitation, maintaining river connectivity, implementing protected areas focusing on freshwater ecosystems, and integrated basin management are required to protect threatened freshwater megafauna in diversity hotspots.     

Targeted gene flow and rapid adaptation in an endangered marsupial

Targeted gene flow is an emerging conservation strategy. It involves translocating individuals with favorable genes to areas where they will have a conservation benefit. The applications for targeted gene flow are wide-ranging but include preadapting native species to the arrival of invasive species. The endangered carnivorous marsupial, the northern quoll (Dasyurus hallucatus), has declined rapidly since the introduction of the cane toad (Rhinella marina), which fatally poisons quolls that attack them. There are, however, a few remaining toad-invaded quoll populations in which the quolls survive because they know not to eat cane toads. It is this toad-smart behavior we hope to promote through targeted gene flow. For targeted gene flow to be feasible, however, toad-smart behavior must have a genetic basis. To assess this, we used a common garden experiment, comparing offspring from toad-exposed and toad-naïve parents raised in identical environments, to determine whether toad-smart behavior is heritable. Offspring from toad-exposed populations were substantially less likely to eat toads than those with toad-naïve parents. Hybrid offspring showed similar responses to quolls with 2 toad-exposed parents, indicating the trait may be dominant. Together, these results suggest a heritable trait and rapid adaptive response in a small number of toad-exposed populations. Although questions remain about outbreeding depression, our results are encouraging for targeted gene flow. It should be possible to introduce toad-smart behavior into soon to be affected quoll populations.     

Male Mutation Bias and Possible Long‐Term Effects of Human Activities

Abstract: The ability of a population to adapt to changing environments depends critically on the amount and kind of genetic variability it possesses. Mutations are an important source of new genetic variability and may lead to new adaptations, especially if the population size is large. Mutation rates are extremely variable between and within species, and males usually have higher mutation rates as a result of elevated rates of male germ cell division. This male bias affects the overall mutation rate. We examined the factors that influence male mutation bias, and focused on the effects of classical life‐history parameters, such as the average age at reproduction and elevated rates of sperm production in response to sexual selection and sperm competition. We argue that human‐induced changes in age at reproduction or in sexual selection will affect male mutation biases and hence overall mutation rates. Depending on the effective population size, these changes are likely to influence the long‐term persistence of a population.     

A Comparison of Linear Demographic Models and Fraction of Lifetime Egg Production for Assessing Sustainability in Sharks

Conventional methods for management of data‐rich fisheries maintain sustainable populations by assuring that lifetime reproduction is adequate for individuals to replace themselves and accounting for density‐dependent recruitment. Fishing is not allowed to reduce relative lifetime reproduction, the fraction of current egg production relative to unfished egg production (FLEP), below a sustainable level. Because most shark fisheries are data poor, other representations of persistence status have been used, including linear demographic models, which incorporate life‐history characteristics in age‐structured models with no density dependence. We tested how well measures of sustainability from 3 linear demographic methods (rebound potential, stochastic growth rate, and potential population increase) reflect actual population persistence by comparing values of these measures with FLEP for 26 shark species. We also calculated the value of fishing mortality (F) that would allow all 26 species to maintain an accepted precautionary threshold for sharks of FLEP = 60%, expressing F as a fraction of natural mortality (M). Values of stochastic growth rate and potential population growth did not covary in rank order with FLEP (p = 0.057 and p = 0.077, respectively) and neither was significantly correlated with FLEP. Ordinal ranking of rebound potential positively covaried with FLEP (p = 0.00013), but the relative rankings of some species were substantially out of order. Adopting a sustainable limit of F = 0.16M would maintain all 26 species above the precautionary minimum value of FLEP (60%). We concluded that shark‐fishery and conservation policies should rely on calculation of replacement (i.e., FLEP), and that sharks should be fished at a precautionary level that would protect all stocks (i.e., F< 0.16M). Comparación entre Modelos Demográficos Lineales y la Fracción de Producción de Huevos a lo Largo de la Vida para Estudiar la Sustentabilidad en Tiburones Resumen