Robert C. Lacy

Distribution and conservation status of the orang-utan ( Pongo spp.) on Borneo and Sumatra: how many remain?

In recognition of the fact that orang-utans (Pongo spp.) are severely threatened, a meeting of orang-utan experts and conservationists, representatives of national and regional governmental and non-governmental organizations, and other stakeholders, was convened in Jakarta, Indonesia, in January 2004. Prior to this meeting we surveyed all large areas for which orang-utan population status was unknown. Compilation of all survey data produced a comprehensive picture of orang-utan distribution on both Borneo and Sumatra. These results indicate that in 2004 there were c. 6,500 P. abelii remaining on Sumatra and at least 54,000 P. pygmaeus on Borneo. Extrapolating to 2008 on the basis of forest loss on both islands suggests the estimate for Borneo could be 10% too high but that for Sumatra is probably still relatively accurate because forest loss in orang-utan habitat has been low during the conflict in Aceh, where most P. abelii occur. When those population sizes are compared to known historical sizes it is clear that the Sumatran orang-utan is in rapid decline, and unless extraordinary efforts are made soon, it could become the first great ape species to go extinct. In contrast, our results indicate there are more and larger populations of Bornean orang-utans than previously known. Although these revised estimates for Borneo are encouraging, forest loss and associated loss of orang-utans are occurring at an alarming rate, and suggest that recent reductions of Bornean orang-utan populations have been far more severe than previously supposed. Nevertheless, although orang-utans on both islands are under threat, we highlight some reasons for cautious optimism for their long-term conservation.

HIERARCHICAL ANALYSIS OF INBREEDING DEPRESSION IN PEROMYSCUS POLIONOTUS

The severity of inbreeding depression appears to vary among taxa, but few ecological or other patterns have been identified that predict accurately which taxa are most sensitive to inbreeding. To examine the causes of heterogeneity in inbreeding depression, the effects of inbreeding on reproduction, survival, and growth were measured in three replicate experimental stocks for each of three subspecies of Peromyscus polionotus mice. Inbreeding of the dam reduced the probability of breeding, the probability of producing a second litter, and litter size. Inbreeding of the litter caused depression of litter size, juvenile viability, and mass at weaning, and caused an increase in the within‐litter variance in mass. In spite of differences between the subspecies in natural population sizes, genetic variation, and mean rates of reproduction and survival, all variation observed between experimental populations in their responses to inbreeding could be attributed to random founder effects. The genetic load of deleterious alleles in each replicate was unequally partitioned among its founder pairs, and different founders contributed to the load affecting different fitness components. Thus, inbreeding depression for any one fitness component, in our experimental environment, must be due to relatively few deleterious alleles with major effects. Genetic loads so comprised would be expected to diverge among natural populations due to both random drift and selective removal of recessive deleterious alleles during population bottlenecks. The near universality of inbreeding depression would be maintained, however, if different alleles contribute to inbreeding depression of different fitness components and in different environments.

High-throughput sequencing reveals inbreeding depression in a natural population

Significance Many studies of wild populations reveal links between heterozygosity and fitness, with relatively heterozygous individuals carrying fewer parasites, living longer and being more attractive to mates. These patterns appear ubiquitous and are often highly significant, but heterozygosity usually accounts for very little of the total variation in fitness. However, most studies analyze only around 10 loci, representing a tiny fraction of the genome. We therefore used high-throughput DNA sequencing to estimate genome-wide heterozygosity based on over 10,000 loci and found it to accurately reflect inbreeding. Applied to wild harbor seals, genome-wide heterozygosity explained almost half of the variation in parasite infection. By implication, a greater proportion of fitness variation could be linked to genotype than previously thought. Proxy measures of genome-wide heterozygosity based on approximately 10 microsatellites have been used to uncover heterozygosity fitness correlations (HFCs) for a wealth of important fitness traits in natural populations. However, effect sizes are typically very small and the underlying mechanisms remain contentious, as a handful of markers usually provides little power to detect inbreeding. We therefore used restriction site associated DNA (RAD) sequencing to accurately estimate genome-wide heterozygosity, an approach transferrable to any organism. As a proof of concept, we first RAD sequenced oldfield mice (Peromyscus polionotus) from a known pedigree, finding strong concordance between the inbreeding coefficient and heterozygosity measured at 13,198 single-nucleotide polymorphisms (SNPs). When applied to a natural population of harbor seals (Phoca vitulina), a weak HFC for parasite infection based on 27 microsatellites strengthened considerably with 14,585 SNPs, the deviance explained by heterozygosity increasing almost fivefold to a remarkable 49%. These findings arguably provide the strongest evidence to date of an HFC being due to inbreeding depression in a natural population lacking a pedigree. They also suggest that under some circumstances heterozygosity may explain far more variation in fitness than previously envisaged.

EFFECTIVENESS OF SELECTION IN REDUCING THE GENETIC LOAD IN POPULATIONS OF PEROMYSCUS POLIONOTUS DURING GENERATIONS OF INBREEDING

It has been hypothesized that natural selection reduces the “genetic load” of deleterious alleles from populations that inbreed during bottlenecks, thereby ameliorating impacts of future inbreeding. We tested the efficiency with which natural selection purges deleterious alleles from three subspecies of Peromyscus polionotus during 10 generations of laboratory inbreeding by monitoring pairing success, litter size, viability, and growth in 3604 litters produced from 3058 pairs. In P. p. subgriseus, there was no reduction across generations in inbreeding depression in any of the fitness components. Strongly deleterious recessive alleles may have been removed previously during episodes of local inbreeding in the wild, and the residual genetic load in this population was not further reduced by selection in the lab. In P. p. rhoadsi, four of seven fitness components did show a reduction of the genetic load with continued inbreeding. The average reduction in the genetic load was as expected if inbreeding depression in this population is caused by highly deleterious recessive alleles that are efficiently removed by selection. For P. p. leucocephalus a population that experiences periodic bottlenecks in the wild, the effect of further inbreeding in the laboratory was to exacerbate rather than reduce the genetic load. Recessive deleterious alleles may have been removed from this population during repeated bottlenecks in the wild; the population may be close to a threshold level of heterozygosity below which fitness declines rapidly. Thus, the effects of selection on inbreeding depression varied substantially among populations, perhaps due to different histories of inbreeding and selection.

Population viability analysis as a tool in wildlife conservation policy: With reference to Australia

Wildlife conservation policy for endangered species restoration follows a six-phase process. Population viability analysis (PVA) can play a major contributing role in four of these. PVA, as discussed here, is a technique where extinction vulnerabilities of small populations are estimated using computer simulation modeling. The benefits and limitations of using PVA in wildlife decision and policy processes are reviewed based on our direct experience. PVA permits decision makers to set time frames for management, estimate the required magnitude of restoration efforts, identify quantitative targets for species recovery, and select, implement, monitor, and evaluate management strategies. PVA is of greatest value for rare species policy and management. However, a limitation of PVA simulation models is that they are constrained by the amount of biological data available, and such data are difficult to obtain from small populations that are at immediate risk of extinction. These problems may be overcome with improved models and more data. Our experience shows benefits of PVA far outweigh its limitations, and applications of the approach are most useful when integrated with decision analysis and completed within an adaptive management philosophy. PVAs have been carried out for 14 Victorian species and less used elsewhere in Australia. Management and recovery plans are developed from these PVAs. We recommend that PVA be used to guide research programs, develop conservation strategies, and inform decision and policy making for both endangered and nonendangered species because it can significantly improve many aspects of natural resource policy and management.

A simulation study of the impacts of population subdivision on the mountain brushtail possum Trichosurus caninus Ogilby (Phalangeridae: Marsupialia), in south-eastern Australia. II. Loss of genetic variation within and between subpopulations

Abstract The subdivision of populations that results from habitat fragmentation can impact the amount and pattern of genetic variation in metapopulations of organisms. Subdivision can lead to a loss of heterozygosity, and increased inbreeding within subpopulations is one factor that may contribute to an extinction vortex. However, a number of genetic models have also shown that, under some conditions, subdivision of populations can protect heterozygosity and allelic diversity, and that small subpopulations can become adapted to inbreeding. In this study we further investigated the relationships between habitat fragmentation, population subdivision, and various measures of genetic variability. VORTEX, a computer program for Population Viability Analysis (PVA), was used to simulate the impacts of fragmentation and subdivision on the genetic variation within and between subpopulations of the mountain brushtail possum Trichosurus caninus Ogilby, a forest-dependent species of arboreal marsupial that inhabits wet sclerophyll forests and rainforests in eastern Australia. For this study and a related investigation of the demographic stability of populations of T. caninus, hypothetical populations of 100, 200 and 400 animals were partitioned into one to 10 subpopulations that were, in turn, linked by varying rates of migration between subpopulations. Our application of PVA allowed an examination of the effects on population dynamics of demographic fluctuations, genetic drift, and interactions between demographic and genetic processes. The results of our analysis showed that both gene diversity (heterozygosity) and allelic diversity of subpopulations and metapopulations were lost rapidly when a population was subdivided. The increased levels of demographic stochasticity that resulted from population subdivision caused a decrease in the effective population sizes of the metapopulations that were modelled as well as the ensemble of subpopulations in each case. This, in turn, resulted in more rapid losses of genetic variation than would occur in the absence of demographic fluctuations. The extinction of some subpopulations further accelerated the loss of gene diversity and alleles. In addition, the genetic and demographic instability of small, fragmented populations diminished the effectiveness of selection against recessive lethal alleles. Migration among subpopulations partly reversed the impacts of population subdivision. However, even high rates of migration did not eliminate demographic fluctuations or prevent subpopulation extinction. Therefore, although gene flow largely prevented genetic divergence between subpopulations, migration did not prevent subdivided populations from losing genetic variation more rapidly than single populations of the same total size. The dynamics of small, fragmented populations were shown to be critically dependent on the interactions between demographic and genetic processes. Thus, our findings are in striking contrast to the predictions made by several previous models of genetic changes in metapopulations that exclude consideration of the impacts of demographic stochasticity. These results demonstrated the value of PVA simulation models in revealing some of the consequences of fragmentation that have previously been overlooked. Our investigation has indicated that populations of forest-dependent taxa and other species that depend on habitats undergoing rapid change due to human activities may have to be relatively large and continuous to avoid significant losses of genetic variation.

Unsustainable harvest of dugongs in Torres Strait and Cape York (Australia) waters: two case studies using population viability analysis

A significant proportion of the world’s remaining dugongs (Dugong dugon) occur off northern Australia where they face various anthropogenic impacts. Here, we investigate the viability of two dugong meta-populations under varying regimes of indigenous hunting. We construct population viability analyses (PVAs) using the computer package VORTEX and published estimates of population sizes and hunting rates. In Torres Strait between Cape York and New Guinea, our models predict severe and imminent reductions in dugong numbers. Our ‘optimistic’ and ‘pessimistic’ models suggest median times for quasi-extinction of 123 and 42 years, respectively. Extinction probabilities are also high for eastern Cape York Peninsula. We demonstrate the inadequacy of reserves when harvest rates in neighbouring areas are high, identify the maximum harvest rates for meta-population stability and emphasise the urgent need for indigenous community involvement in management to establish sustainable rates of dugong harvest in these regions.

Metapopulation Viability of Leadbeater's Possum, Gymnobelideus Leadbeateri, in Fragmented Old‐Growth Forests

Risk assessment to determine the probability of persistence of populations has an increasingly important role in the development of conservation and resource use strategies. We used the computer program VORTEX to estimate the viability of populations of Leadbeaters possum, Gymnobelideus leadbeateri, an endangered species of forest-de- pendent marsupial inhabiting timber production areas in southeastern Australia. The study simulated population dynamics and genetic variability in metapopulations occupying small numbers of habitat patches of varying size. The impacts of different rates of migration between subpopulations were also examined. Computer simulations with subpopulations of 20 or fewer G. leadbeateri were characterized by very rapid rates of extinction, and most metapopulations typically failed to persist for longer than 50 yr. Increasing either the rate of migration or the number of small subpopulations exacerbated the demographic instability of metapopulations when subpopulations contained 10%) loss in expected heterozygosity over 100 yr even at the highest rates of migration among five subpopulations of 40 animals. Our analyses predicted that while demographic stability might occur in metapopulations of 200 G. leadbeateri, considerably more individuals than this might be required to avoid a sig- nificant decline in genetic variability over 100 yr. Thus, genetic and demographic stability in G. leadbeateri occurred at different metapopulation sizes. Metapopulation structures used in our investigation were hypothetical. However, our results might emulate the dynamics of some populations of arboreal marsupials over the next century within substantial areas of wood production forests in the Central Highlands of Victoria. In many of these areas, there are now only a few and typically very small remaining patches of old-growth forest that will provide suitable habitat for G. leadbeateri in the long term. Thus, over the next 100 yr, the species might be lost from extensive parts of its present range within montane ash forests that are utilized for timber production. Our study also indicated that there might be metapopulation structures in which the addition of subpopulations and moderate migration could have a negative effect on subpopulation persistence. These findings highlight the importance of understanding the size, number, and isolation of subpopulations that are targeted for management.

Methods and Prospects for Using Molecular Data in Captive Breeding Programs: An Empirical Example Using Parma Wallabies (Macropus parma)

Zoo and aquarium breeding programs rely on accurate pedigrees to manage the genetics and demographics of captive populations. Breeding recommendations are often encumbered, however, by unknown parentage. If an individual has any amount of unknown ancestry, the relationships between that individual and all other individuals in a population are ambiguous, and breeding recommendations cannot be tailored to maximize genetic diversity and minimize inbreeding. In those situations, breeding program management might be improved by the incorporation of molecular data. We developed microsatellite markers for the parma wallaby (Macropus parma) and investigated how genetic data might be used to improve the management of the captive population. The parma wallaby is a small marsupial found in fragmented forests near the coast of New South Wales, Australia. Because the species is of conservation concern, the captive population in North America is managed by recurring breeding recommendations. The effectiveness of the populations management is hampered, however, because over half of the individuals have some amount of unknown ancestry. We used microsatellite data to resolve unknown parentage, described how molecular estimates of relatedness might inform future breeding recommendations, and used computer simulations to investigate how molecular estimates of relatedness among founders might contribute to the genetic management of the population. Our results indicated that microsatellite appraisals of parentage were useful with respect to clarifying pedigrees but that molecular assessments of founder relatedness provided very marginal benefits with regard to the preservation of genetic diversity and the avoidance of inbreeding.

When do we need more data? A primer on calculating the value of information for applied ecologists

Summary Applied ecologists continually advocate further research, under the assumption that obtaining more information will lead to better decisions. Value of information (VoI) analysis can be used to quantify how additional information may improve management outcomes: despite its potential, this method is still underused in environmental decision-making. We provide a primer on how to calculate the VoI and assess whether reducing uncertainty will change a decision. Our aim is to facilitate the application of VoI by managers who are not familiar with decision-analytic principles and notation, by increasing the technical accessibility of the tool. Calculating the VoI requires explicit formulation of management objectives and actions. Uncertainty must be clearly structured and its effects on management outcomes evaluated. We present two measures of the VoI. The expected value of perfect information is a calculation of the expected improvement in management outcomes that would result from access to perfect knowledge. The expected value of sample information calculates the improvement in outcomes expected by collecting a given sample of new data. We guide readers through the calculation of VoI using two case studies: (i) testing for disease when managing a frog species and (ii) learning about demographic rates for the reintroduction of an endangered turtle. We illustrate the use of Bayesian updating to incorporate new information. The VoI depends on our current knowledge, the quality of the information collected and the expected outcomes of the available management actions. Collecting information can require significant investments of resources; VoI analysis assists managers in deciding whether these investments are justified.