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

Sex-specific patterns in demography of bottlenose dolphins in coastal and estuarine waters

Inherent difficulties in determining the sex of free-ranging, sexually monomorphic species (where both sexes look the same) often prevents a sex-specific approach to their study. However, accounting for sex-differences in population parameters can have important conservation and management implications, as one sex may be more susceptible to threats than the other

Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations

Genetic diversity is essential for populations to adapt to changing environments. Measures of genetic diversity are often based on selectively neutral markers, such as microsatellites. Genetic diversity to guide conservation management, however, is better reflected by adaptive markers, including genes of the major histocompatibility complex (MHC). Our aim was to assess MHC and neutral genetic diversity in two contrasting bottlenose dolphin (Tursiops aduncus) populations in Western Australia-one apparently viable population with high reproductive output (Shark Bay) and one with lower reproductive output that was forecast to decline (Bunbury). We assessed genetic variation in the two populations by sequencing the MHC class II DQB, which encompasses the functionally important peptide binding regions (PBR). Neutral genetic diversity was assessed by genotyping twenty-three microsatellite loci. We confirmed that MHC is an adaptive marker in both populations. Overall, the Shark Bay population exhibited greater MHC diversity than the Bunbury population-for example, it displayed greater MHC nucleotide diversity. In contrast, the difference in microsatellite diversity between the two populations was comparatively low. Our findings are consistent with the hypothesis that viable populations typically display greater genetic diversity than less viable populations. The results also suggest that MHC variation is more closely associated with population viability than neutral genetic variation. Although the inferences from our findings are limited, because we only compared two populations, our results add to a growing number of studies that highlight the usefulness of MHC as a potentially suitable genetic marker for animal conservation. The Shark Bay population, which carries greater adaptive genetic diversity than the Bunbury population, is thus likely more robust to natural or human-induced changes to the coastal ecosystem it inhabits

Sex-specific patterns in abundance, temporary emigration and survival of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in coastal and estuarine waters

Inherent difficulties in determining the sex of free-ranging, sexually monomorphic species often prevents a sex-specific focus on estimating abundance, movement patterns and survival rates. This study provides insights into sex-specific population parameters of Indo-Pacific bottlenose dolphins (Tursiops aduncus). Systematic, boat-based photo-identification surveys (n = 417) were conducted year-round from 2007 to 2013 in coastal and estuarine waters off Bunbury, Western Australia. Pollock's Robust Design was used to quantify population parameters for three datasets: (i) adults and juveniles combined, (ii) adult females and, (iii) adult males. For all datasets, abundance estimates varied seasonally, with general highs during summer and/or autumn, and lows during winter. Dolphins had seasonally structured temporary emigration rates with similar trends between sexes. The derived return rate (1-γ') of temporary emigrants into the study area was highest from winter to spring, indicating that dolphins had a high probability of return into the study area during spring. We suggest that the return of dolphins into the study area and increase in abundance is influenced by the breeding season (summer/autumn). Prey availability is likely a main driver responsible for the movement of dolphins out of the study area during winter. Seasonal apparent survival rates were constant and high (0.98–0.99) for all datasets. High apparent survival rates suggest there is no permanent emigration from the study area. Our sex-specific modeling approach offers a comprehensive interpretation of the population dynamics of a top predator in a coastal and estuarine environment and acts as a model for future sex-based population studies on sexually monomorphic species

Demography and genetics suggest reversal of dolphin source‐sink dynamics, with implications for conservation

The forecast for the viability of populations depends upon metapopulation dynamics: the combination of reproduction and mortality within populations, as well as dispersal between populations. This study focuses on an Indo‐Pacific bottlenose dolphin (Tursiops aduncus) population in coastal waters near Bunbury, Western Australia. Demographic modeling of this population suggested that recent reproductive output was not sufficient to offset mortality. Migrants from adjacent populations might make up this deficit, so that Bunbury would act as a “sink,” or net recipient population. We investigated historical dispersal in and out of Bunbury, using microsatellites and mitochondrial DNA of 193 dolphins across five study locations along the southwestern Australian coastline. Our results indicated limited gene flow between Bunbury and adjacent populations. The data also revealed a net‐dispersal from Bunbury to neighboring populations, with microsatellites showing that more than twice as many individuals per generation dispersed out of Bunbury than into Bunbury. Therefore, in historic times, Bunbury appears to have acted as a source population, supporting nearby populations. In combination with the prior finding that Bunbury is currently not producing surplus offspring to support adjacent populations, this potential reversal of source‐sink dynamics may have serious conservation implications for Bunbury and other populations nearby

The relative importance of reproduction and survival for the conservation of two dolphin populations

It has been proposed that in slow-growing vertebrate populations survival generally has a greater influence on population growth than reproduction. Despite many studies cautioning against such generalizations for conservation, wildlife management for slow-growing populations still often focuses on perturbing survival without careful evaluation as to whether those changes are likely or feasible. Here, we evaluate the relative importance of reproduction and survival for the conservation of two bottlenose dolphin (Tursiops cf aduncus) populations: a large, apparently stable population and a smaller one that is forecast to decline. We also assessed the feasibility and effectiveness of wildlife management objectives aimed at boosting either reproduction or survival. Consistent with other analytically based elasticity studies, survival had the greatest effect on population trajectories when altering vital rates by equal proportions. However, the findings of our alternative analytical approaches are in stark contrast to commonly used proportional sensitivity analyses and suggest that reproduction is considerably more important. We show that 1. in the stable population reproductive output is higher, and adult survival is lower; 2. the difference in viability between the two populations is due to the difference in reproduction; 3. reproductive rates are variable, whereas survival rates are relatively constant over time; 4. perturbations on the basis of observed, temporal variation indicate that population dynamics are much more influenced by reproduction than by adult survival; 5. for the apparently declining population, raising reproductive rates would be an effective and feasible tool to reverse the forecast population decline; increasing survival would be ineffective. Our findings highlight the importance of reproduction – even in slow-growing populations – and the need to assess the effect of natural variation in vital rates on population viability. We echo others in cautioning against generalizations based on life-history traits and recommend that population modeling for conservation should also take into account the magnitude of vital rate changes that could be attained under alternative management scenarios

The relative importance of reproduction and survival for the viability of slow-growing animal populations: lessons learned from two dolphin populations

Given limited resources and time for conservation actions, it is crucial to focus wildlife management recommendations on vital rates that have the greatest impact on population viability. It has been proposed that in slow-growing animal populations, including most marine mammals, adult survival has a greater influence on population growth than reproduction. The implication of this principle is that adult survival is more important for population viability than reproduction. Here we evaluate the relative importance of reproduction and survival for the viability of two bottlenose dolphin (Tursiopscf. aduncus) populations in Western Australia: a large, apparently stable population (Shark Bay) and a smaller one (Bunbury) that was forecast to decline. Consistent with previous studies, adult survival had the greatest effect on population trajectories when altering vital rates by equal proportions (+/− 4%). However, our alternative analytical approaches suggest that reproduction may be considerably more important. We show that (1) reproductive output is higher, and adult survival is lower in the stable population; (2) the difference in viability between the two population is best explained by the difference in reproductive rates; (3) reproductive rates are variable, whereas survival rates are relatively constant over time (12-year time period for Shark Bay);(4) perturbations based on this observed natural variation (+/− 1 SD) indicate that population dynamics are much more influenced by reproduction than by adult survival. Our findings highlight the importance of reproduction—even in slow-growing populations—and the need to assess the effect of natural variation in vital rates on population viability

Fitness and major histocompatibility complex variation in bottlenose dolphins

An individual’s fitness is determined by traits such as mate choice, reproductive output, resistance to parasites and survival to old age. The search for the genetic basis of fitness variation has until recently often relied on neutral genetic markers, including mitochondrial DNA and microsatellites. However, ecological and evolutionary processes relevant to fitness can only be inferred by non-neutral genes such as those of the major histocompatibility complex (MHC). MHC variants, including ‘supertypes’ (i.e. clusters of MHC variants which encode peptides that interact with particular types of antigens) influence many important biological traits in vertebrates. MHC variation has previously been associated with direct and indirect fitness traits, and has been shown to play an important role in mating. In this study we investigated the potential relationship between MHC variation and fitness traits in two populations of bottlenose dolphins (Tursiops cf. aduncus) in Western Australia. We used conventional Sanger and Illumina MiSeq next-gen sequencing methods to infer MHC sequence variants and supertypes. MHC variation was compared to mate choice, reproductive success, male alliance formation and survival to old age in hundreds of dolphins. We will present our findings, linking MHC variation with fitness traits, with an emphasis on the behavioural traits of mate choice and reproductive success