International EcoHealth One Health Congress 2016

We provide an overview of terrestrial animal translocations carried out for conservation purposes in Britain, summarising what has been achieved in recent decades and discussing the issues raised by this approach to conservation. In the last 40 years, at least nine species have been reintroduced following extinction in Britain (or at least one country within Britain), including five birds, one mammal, one amphibian and two invertebrates. Many more species have been translocated within Britain to establish additional populations in order to improve conservation status. We discuss the guidelines and protocols used to assess translocation projects in Britain, notably the IUCN guidelines, most recently revised in 2013. We also discuss the likely use of species translocations in future and suggest that, in our increasingly fragmented landscapes, they will have an important role to play in conservation restoration, especially for animals with limited mobility. Moving species around is a complex undertaking and our understanding of the inherent risks involved, including the risks from disease, has improved significantly in recent years. Conservation translocations should be considered in the context of species recovery targets and high standards should be maintained so that disease risks and other potentially negative impacts are minimised.

     

Biosecurity for Translocations: Cirl Bunting (Emberiza cirlus), Fisher’s Estuarine Moth (Gortyna borelii lunata), Short-Haired Bumblebee (Bombus subterraneus) and Pool Frog (Pelophylax lessonae) Translocations as Case Studies

Exposure to parasites in conservation translocations increases the risks to recipient and translocated populations from disease, and therefore there has been interest in implementing biosecurity methods. Using four case examples we described how biosecurity was applied in practical translocation scenarios prior to and during a translocation and also post-release. We implemented biosecurity, including quarantine barriers, at specific points in the translocation pathway where hazards, identified by the disease risk analysis, had the potential to induce disease. Evidence that biosecurity protected translocated and recipient populations, included an absence of mortality associated with high-risk non-native parasites, a reduction in mortality associated with endemic parasites, the absence of high-risk pathogenic parasites, or associated diseases, at the destination; and the apparent absence of diseases in closely related species at the destination site. The biosecurity protocols did not alter the level or duration of translocated species confinement and therefore probably did not act as a stressor. There is a monetary cost involved in biosecurity but the epidemiological evidence suggests that conservation translocation managers should carefully consider its use. Breakdowns in quarantine have occurred in human hospitals despite considerable investment and training for health professionals, and we therefore judge that there is a need for training in the objectives and maintenance of quarantine barriers in conservation translocations. Biosecurity protocols for conservation translocations should be continually updated in response to findings from disease risk analysis and post-release disease surveillance and we recommend further studies to evaluate their effectiveness.

     

Genomic Signatures of Recent Adaptation in a Wild Bumblebee

Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.     

Evolution of population genetic structure of the British roe deer by natural and anthropogenic processes (Capreolus capreolus)

Human influence typically impacts on natural populations of conservation interest. These interactions are varied and sometimes complex, and may be negative and unintended or associated with conservation and management strategy. Understanding the details of how these interactions influence and are influenced by natural evolutionary processes is essential to the development of effective conservation strategies. In this study, we investigate a species in Britain that has experienced both negative impact through overhunting in historical times and management efforts through culls and translocations. At the same time, there are regional populations that have been less affected by human influence. We use mtDNA and nuclear microsatellite DNA markers to investigate patterns of connectivity and diversity and find multiple insular populations in Britain that probably evolved within the Holocene (when the habitat was free of ice). We identify three concurrent processes. First, surviving indigenous populations show highly provincial patterns of philopatry, maintaining and generating population structure on a small geographic scale. Second, founder populations into habitat extirpated of native populations have expanded, but remained largely insular. Third, introductions into established populations generate some admixture. We discuss the implications for the evolution of diversity of the integration of natural processes with anthropogenic influences on population size and distribution.     

Red and sika deer in the British Isles,current management issues and management policy

The red deer (Cervus elaphus) is one of the most widely distributed species of deer in Europe. Due to its economic value as game species or its negative impacts on forestry, agriculture and conservation areas, most populations are currently managed, with strategies and intensity of the management varying between countries. In Britain, and less certainly in Ireland, red deer have been continuously present since the end of the last glaciation and constitute the largest population of red deer in Europe. Although they thrived in the past when forests were abundant, the current distribution of red deer in the British Isles is uneven, with the largest numbers being found in Scotland and few and more localised populations in England, Wales and the Republic of Ireland. In the British Isles, as in many other parts of Europe, there is a long history of man interacting with deer populations including local extinctions, multiple translocations and introductions of exotic species of deer. Among introduced exotic species of deer, the Japanese sika (Cervus nippon) is the one of most concern. After introduction of small numbers at multiple locations in Britain and Ireland from 1860 onwards, sika have increased in population number and range in areas with good forest cover, and where they overlap with red deer there is a risk of hybridisation. Due to recent increases in numbers and range of red and sika deer, both species pose a range of management challenges which are not easy to solve. In this review we summarise the history and status of these two species in Great Britain and Ireland, describe current management and discuss management options for the future.     

Parasitological Consequences of Overcrowding in Protected Areas

For the past several years, there has been growing interest in understanding the dynamics of parasites in ecosystems, as well as the diversity of ways in which they interfere with conservation and health preoccupations. Although it is widely recognized that many conservation practices (e.g., wildlife translocations, species removal, food supplementation) may be associated with parasite-related problems, less attention has been devoted to exploring the parasitological consequences of the overcrowding of animals in protected wildlife areas. Here, we discuss this important ecological/epidemiological problem, presenting at the same time an overview of the main questions and challenges in this field. Using empirical and theoretical examples chosen from the literature, we focus particularly on the interactions between the overcrowding of free living species and parasite population dynamics, the evolution of parasite virulence, the indirect effects on the structure of invertebrate communities, as well as the nutritional value of prey species. We argue that conservation policies should be aware more than ever of this problem, especially given the serious health risks currently posed by the spread of virulent viruses (e.g., avian influenza).     

Ecological history and latent conservation potential: large and giant tortoises as a model for taxon substitutions

Starting in the late 1970s, ecologists began unraveling the role of recently extinct large vertebrates in evolutionary ecology and ecosystem dynamics. Three decades later, practitioners are now considering the role of ecological history in conservation practice, and some have called for restoring missing ecological functions and evolutionary potential using taxon substitutes – extant, functionally similar taxa – to replace extinct species. This pro‐active approach to biodiversity conservation has proved controversial. Yet, rewilding with taxon substitutes, or ecological analogues, is now being integrated into conservation and restoration programmes around the world. Empirical evidence is emerging that illustrates how taxon substitutions can restore missing ecological functions and evolutionary potential. However, a major roadblock to a broader evaluation and application of taxon substitution is the lack of practical guidelines within which they should be conducted. While the International Union for Conservation of Nature's reintroduction guidelines are an obvious choice, they are unsuitable in their current form. We recommend necessary amendments to these guidelines to explicitly address taxon substitutions. A second impediment to empirical evaluations of rewilding with taxon substitutions is the sheer scale of some proposed projects; the majority involves large mammals over large areas. We present and discuss evidence that large and giant tortoises (family Testudinidae) are a useful model to rapidly provide empirical assessments of the use of taxon substitutes on a comparatively smaller scale. Worldwide, at least 36 species of large and giant tortoises went extinct since the late Pleistocene, leaving 32 extant species. We examine the latent conservation potential, benefits, and risks of using tortoise taxon substitutes as a strategy for restoring dysfunctional ecosystems. We highlight how, especially on islands, conservation practitioners are starting to employ extant large tortoises in ecosystems to replace extinct tortoises that once played keystone roles.     

Species richness declines and biotic homogenisation have slowed down for NW‐European pollinators and plants

Concern about biodiversity loss has led to increased public investment in conservation. Whereas there is a widespread perception that such initiatives have been unsuccessful, there are few quantitative tests of this perception. Here, we evaluate whether rates of biodiversity change have altered in recent decades in three European countries (Great Britain, Netherlands and Belgium) for plants and flower visiting insects. We compared four 20‐year periods, comparing periods of rapid land‐use intensification and natural habitat loss (1930–1990) with a period of increased conservation investment (post‐1990). We found that extensive species richness loss and biotic homogenisation occurred before 1990, whereas these negative trends became substantially less accentuated during recent decades, being partially reversed for certain taxa (e.g. bees in Great Britain and Netherlands). These results highlight the potential to maintain or even restore current species assemblages (which despite past extinctions are still of great conservation value), at least in regions where large‐scale land‐use intensification and natural habitat loss has ceased.     

Hybridization processes in an introduced subpopulation of an endangered plant: Management strategies to guarantee the conservation of Helosciadium bermejoi (Apiaceae)

Translocations are a tool to restore populations of threatened plant species that are being widely used. However, these techniques are not without risks and require rigorous protocols to carry them out and for their subsequent monitoring. In translocation projects, hybridization with other species is one of the most important risks and may threaten the survival of the species we want to protect. Here we present the case of Helosciadium bermejoi (L. Llorens) Popper and M.F. Watson, a Critically Endangered plant from the island of Menorca (Western Mediterranean). It occurs only in one locality and has been introduced to three new locations during recent years according to its Recovery Plan (2008). Recently, intermediate forms between the endangered species and a native congener, Helosciadium nodiflorum (L.) Koch, have been detected. The aims of this study were (i) to elucidate whether these plants originated through a hybridization event and (ii) to provide information about the current conservation status of the species. Exhaustive monitoring of all subpopulations (number of patches and area of occupancy) was performed from September 2015 to June 2016, and the rDNA ITS region and cpDNA rps16-trnK intergenic spacer region were sequenced for several samples of the putative hybrid and its putative parental species. Overall, the entire population of H. bermejoi greatly increased from 2010 (last census with available data) to 2015 in terms of both number of patches and area of occupancy: from 110 to 277 patches and from 299.2 to 791.3 dm². Molecular analysis confirmed the hybrid origin of Helosciadium × clandestinum Rita, Capó and Cursach and that both H. bermejoi and H. nodiflorum (L.) Koch can act as donors of pollen or ovules. We discuss the advantages and disadvantages of translocations, as well as the great importance of monitoring them for at least the next ten years, both to know if the actions have been successful and to prevent or mitigate risks. We also present this case as an example for the importance of fast decision and coordination between environmental managers.     

Population genetics and relatedness in a critically endangered island raptor, Ridgway’s Hawk Buteo ridgwayi

Many island avian populations are of conservation interest because they have a higher risk of extinction than mainland populations. Susceptibility of island birds to extinction is primarily related to human induced change through habitat loss, persecution, and introduction of exotic species, in combination with genetic factors. We used microsatellite profiles from 11 loci to assess genetic diversity and relatedness in the critically endangered hawk Buteo ridgwayi endemic to the island of Hispaniola in the Caribbean. Using samples collected between 2005 and 2009, our results revealed a relatively high level of heterozygosity, evidence of a recent genetic bottleneck, and the occurrence of inbreeding within the population. Pair relatedness analysis found 4 of 7 sampled breeding pairs to be related similar to that of first cousin or greater. Pedigree estimates indicated that up to 18 % of potential pairings would be between individuals with relatedness values similar to that of half-sibling. We discuss our findings in the context of conservation genetic management suggesting both carefully managed translocations and the initiation of a captive population as a safeguard of the remaining genetic diversity.     

Origin of, and conservation units in, the Irish red squirrel (Sciurus vulgaris) population

Knowledge of genetic relationships among wildlife populations is fundamental to their conservation, particularly where translocations are concerned. This study involved a survey of mitochondrial DNA variation in the Irish red squirrel population. Our main aims were: (1) to determine whether the Irish red squirrel population is distinct from that found in Britain, given known translocations that took place from Britain in the 1800’s; and (2) whether inclusion of Irish data into a reanalysis of European red squirrel data could reveal patterns of postglacial spread in Ireland. We found evidence that the current Irish red squirrel population may be a mixture of native and translocated stock, and relationships between Irish and European haplotypes supported a number of colonisation events of the island. Although only one haplotype was common to both Ireland and Britain, it is probable that the most common haplotypes in Ireland are British introductions that have since become extinct in Britain. There was a significant regional genetic structure in Ireland (P < 0.001), as well as between all Irish and British regions. Although it is likely that the red squirrel will not be fundamental in tracing the colonisation of Ireland by mammals, the data demonstrated that individual regions within Ireland, as well as the Irish population as a whole, are distinct both from the British population and from each other and, therefore, these populations should be treated as separate Management Units (MU) in conservation strategies.     

Use of remote sensing to measure change in the extent of habitat for the critically endangered Jerdon's Courser Rhinoptilus bitorquatus in India

Jerdon's Courser Rhinoptilus bitorquatus is one of the most endangered and least understood birds in the world. It is endemic to scrub habitats in southeast India which have been lost and degraded because of human land use. We used satellite images from 1991 and 2000 and two methods for classifying land cover to quantify loss of Jerdon's Courser habitat. The scrub habitats on which this species depends decreased in area by 11–15% during this short period (9.6 years), predominantly as a result of scrub clearance and conversion to agriculture. The remaining scrub patches were smaller and further from human settlements in 2000 than in 1991, implying that much of the scrub loss had occurred close to human population centres. We discuss the implications of our results for the conservation of Jerdon's Courser and the use of remote sensing methods in conservation.     

Temporal genetic dynamics of reintroduced and translocated populations of the endangered golden lion tamarin (<Emphasis Type="Italic">Leontopithecus rosalia</Emphasis>)

Reintroductions—captive-born animals introduced into the species’ original distribution area—and translocations—free-living animals transferred to another location within the historical distribution area—are important conservation strategies for endangered species. Genetic analyses of 239 individuals from unmanaged, translocated and reintroduced populations of Leontopithecus rosalia were performed using 14 microsatellites. These samples were collected during two periods: (a) 1996–1997 (historic), when individuals were translocated and reintroduced into forest fragments in the lowland Atlantic Forest, and (b) 2007–09 (recent). We hypothesized that effective population size and genetic diversity would increase over time and that these management strategies would affect the resulting population genetic structure. We found trends indicating that the effective population size at the translocation site increased while that at the reintroduction sites diminished over time. The inbreeding coefficient of the translocated population diminished over time (from 0.38 to 0.03) and was much lower than that of the native (0.29) and reintroduced (0.13) recent populations. We observed a greater genetic admixture among the reintroduced sites on the historic sampling, as well as a strong genetic structure at the translocation site. In the recent sampling, the population structuring became more site-related suggesting low or inconsistent gene flow between sampling sites. This research highlights how conservation management decisions have an important influence on the genetic outcome of translocations and reintroductions. Future conservation planning should consider population genetic monitoring before and after management measures and maintain population connectivity thereafter to avoid the negative effects of a population size reduction.     

Translocations: Providing Outcomes for Wildlife, Resource Managers, Scientists, and the Human Community

The World Conservation Union (1987) defines a translocation as a release of animals with the intention of establishing, reestablishing, or augmenting an existing population. Despite frequent use as a tool for the management of threatened and endangered wildlife, the full benefits of translocations often go unrealized. In this article, I demonstrate how translocations can achieve outputs for conservation management, conservation science, and the wider human community, using North Island (NI) Saddleback or Tieke ( Philesturnus rufusater ) as an illustrative example. From a conservation management perspective, NI Saddleback have been salvaged from a relic population of less than 500 birds on 484-ha Hen Island to a metapopulation of approximately 6,000 birds on 13 offshore islands and at two mainland New Zealand sites. These translocations have reduced the risk of global extinction for this species and helped restore the ecosystems involved. All these translocations have occurred in the past 42 years from known source populations and with known numbers of birds released. The resulting replicated serial population bottlenecks provide numerous scientific opportunities for conservation and biological research. Although the first Saddleback translocations were to reserves closed to the public, subsequent translocations have been to open reserves, providing the wider human community with an opportunity to see and be actively involved in the management of a threatened endemic species. This has raised the profile of both NI Saddleback and other species and has provided wider community conservation benefits. These three outputs illustrate the value of translocations for resource management and conservation science and for increasing community interest, participation, and investment in biological conservation.     

Cryptic genetic divergence within threatened species of <Emphasis Type="Italic">Acropora</Emphasis> coral from the Indian and Pacific Oceans

Most hard corals have broad distributions, and historically this was attributed to their capability for extensive dispersal leading to high evolutionary and demographic inter-dependence among regions. More recently there has been a paradigm shift in the understanding of coral dispersal, driven largely by genetic evidence, which has put greater emphasis on self-recruitment and larval retention. There is now a growing body of evidence that morphologically cryptic species exist within many recognized ‘species’ of stony corals. Here, we characterise levels of genetic divergence within and between five species of Acropora sampled from disparate populations spanning the Indo-Pacific Oceans. We find that strong regional genetic differentiation corresponding to the separation of the Indian and Pacific Ocean basins is a consistent pattern in three of the five species examined. Furthermore, the extent of allopatric divergence within species is similar to that observed between species, implying negligible contemporary gene flow between regions in four of the five species examined. This is consistent with the presence of numerous morphologically cryptic allopatric subspecies or incipient Acropora species. If this is confirmed, the conservation status of several species, which are already demonstrably threatened, would require re-evaluation so that risks including silent extinctions and inappropriate translocations are properly managed.     

Balanced translocations in mental retardation

Over the past few decades, the knowledge on genetic defects causing mental retardation has dramatically increased. In this review, we discuss the importance of balanced chromosomal translocations in the identification of genes responsible for mental retardation. We present a database-search guided overview of balanced translocations identified in patients with mental retardation. We divide those in four categories: (1) balanced translocations that helped to identify a causative gene within a contiguous gene syndrome, (2) balanced translocations that led to the identification of a mental retardation gene confirmed by independent methods, (3) balanced translocations disrupting candidate genes that have not been confirmed by independent methods and (4) balanced translocations not reported to disrupt protein coding sequences. It can safely be concluded that balanced translocations have been instrumental in the identification of multiple genes that are involved in mental retardation. In addition, many more candidate genes were identified with a suspected but (as yet?) unconfirmed role in mental retardation. Some balanced translocations do not disrupt a protein coding gene and it can be speculated that in the light of recent findings concerning ncRNA’s and ultra-conserved regions, such findings are worth further investigation as these potentially may lead us to the discovery of novel disease mechanisms.     

Stepping into the past to conserve the future: Archived skin swabs from extant and extirpated populations inform genetic management of an endangered amphibian

Moving animals on a landscape through translocations and reintroductions is an important management tool used in the recovery of endangered species, particularly for the maintenance of population genetic diversity and structure. Management of imperiled amphibian species rely heavily on translocations and reintroductions, especially for species that have been brought to the brink of extinction by habitat loss, introduced species, and disease. One striking example of amphibian declines and associated management efforts is in California's Sequoia and Kings Canyon National Parks with the mountain yellow‐legged frog species complex (Rana sierrae/muscosa). Mountain yellow‐legged frogs have been extirpated from more than 93% of their historic range, and limited knowledge of their population genetics has made long‐term conservation planning difficult. To address this, we used 598 archived skin swabs from both extant and extirpated populations across 48 lake basins to generate a robust Illumina‐based nuclear amplicon data set. We found that samples grouped into three main genetic clusters, concordant with watershed boundaries. We also found evidence for historical gene flow across watershed boundaries with a north‐to‐south axis of migration. Finally, our results indicate that genetic diversity is not significantly different between populations with different disease histories. Our study offers specific management recommendations for imperiled mountain yellow‐legged frogs and, more broadly, provides a population genetic framework for leveraging minimally invasive samples for the conservation of threatened species.     

Trends in lizard translocations in New Zealand between 1988 and 2013

There is growing concern about mitigation-driven translocations that move animals from anthropogenic threats at donor sites because of their failure rate and lack of application of scientific principles and best practice. We reviewed all known lizard translocations in New Zealand between 1988 and 2013 and identified 85 translocations of 30 lizard taxa to 46 release sites. Most translocations (62%) were motivated by conservation goals for the species or the release site, and one-third were mitigation-driven translocations, typically motivated by habitat loss due to development. Mitigation-driven translocations began in 2003, and since that time have equalled the number of conservation-motivated translocations. Conservation-motivated translocations usually released lizards on islands without mammalian predators, whereas mitigation-driven translocations usually relocated lizards to mainland sites with introduced predators. Long-term monitoring has been sparse and often rudimentary. Eight lizard translocations have recorded population growth, including one mitigation-driven translocation that was into a fenced reserve. Research on commonly used management techniques to mitigate human-related impacts is recommended to establish whether these techniques benefit lizards in the long term.     

An abundance–occupancy time-lag during the decline of an arctiid tiger moth

The positive interspecific abundance–occupancy relationship is one of the most general patterns in ecology. Positive intra specific relationships should also exist within species over time, and so a species should occupy more sites in years when it is more abundant. However, positive intraspecific relationships are not as ubiquitous as their interspecific counterparts. It has been hypothesized that low levels of temporal variation and time-lags between changes of abundance and occupancy within species make positive intraspecific relationships difficult to detect. We analyse 31 years of U.K.-wide data on the decline of an arctiid moth, Arctia caja , which provides the first empirical demonstration of an abundance–occupancy time-lag for any species. Such time-lags are probably common and we discuss their impact on the intraspecific abundance–occupancy relationship and their implications for conservation management. In A. caja , the time-lag indicates that the decline of the species is probably not driven by habitat loss.     

Dispersal and gene flow in the rare, parasitic Large Blue butterfly Maculinea arion

Dispersal is crucial for gene flow and often determines the long‐term stability of meta‐populations, particularly in rare species with specialized life cycles. Such species are often foci of conservation efforts because they suffer disproportionally from degradation and fragmentation of their habitat. However, detailed knowledge of effective gene flow through dispersal is often missing, so that conservation strategies have to be based on mark–recapture observations that are suspected to be poor predictors of long‐distance dispersal. These constraints have been especially severe in the study of butterfly populations, where microsatellite markers have been difficult to develop. We used eight microsatellite markers to analyse genetic population structure of the Large Blue butterfly Maculinea arion in Sweden. During recent decades, this species has become an icon of insect conservation after massive decline throughout Europe and extinction in Britain followed by reintroduction of a seed population from the Swedish island of Öland. We find that populations are highly structured genetically, but that gene flow occurs over distances 15 times longer than the maximum distance recorded from mark–recapture studies, which can only be explained by maximum dispersal distances at least twice as large as previously accepted. However, we also find evidence that gaps between sites with suitable habitat exceeding ～20 km induce genetic erosion that can be detected from bottleneck analyses. Although further work is needed, our results suggest that M. arion can maintain fully functional metapopulations when they consist of optimal habitat patches that are no further apart than ～10 km.