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Monitoring for the management of disease risk in animal translocation programmes

Monitoring is best viewed as a component of some larger programme focused on science or conservation. The value of monitoring is determined by the extent to which it informs the parent process. Animal translocation programmes are typically designed to augment or establish viable animal populations without changing the local community in any detrimental way. Such programmes seek to minimize disease risk to local wild animals, to translocated animals, and in some cases to humans. Disease monitoring can inform translocation decisions by (1) providing information for state-dependent decisions, (2) assessing progress towards programme objectives, and (3) permitting learning in order to make better decisions in the future. Here we discuss specific decisions that can be informed by both pre-release and post-release disease monitoring programmes. We specify state variables and vital rates needed to inform these decisions. We then discuss monitoring data and analytic methods that can be used to estimate these state variables and vital rates. Our discussion is necessarily general, but hopefully provides a basis for tailoring disease monitoring approaches to specific translocation programmes.

EcoHealth

Waif gopher tortoise survival and site fidelity following translocation

Gopher tortoises ( Gopherus polyphemus ) are among the most commonly translocated reptiles. Waif tortoises are animals frequently of unknown origin that have been displaced from the wild and often held in human possession for various reasons and durations. Although there are risks associated with any translocation, waif tortoises are generally excluded from translocation projects because of heightened concerns of introducing pathogens and uncertainty about the post-release survival of these individuals. If these risks could be managed, waif tortoises could have conservation value because they can provide the needed numbers to stabilize populations. In the early 1990s, the discovery of an isolated population of gopher tortoises (≤15 individuals) near Aiken, South Carolina, USA, prioritized establishment of the Aiken Gopher Tortoise Heritage Preserve (AGTHP). Because of the population's need for augmentation and the site's isolation from other tortoise populations, the AGTHP provided the opportunity to evaluate the post-release survival of translocated waif tortoises without compromising a viable population. Since 2006, >260 waif tortoises have been introduced to the preserve. Using a Cormack-Jolly-Seber modeling framework to analyze release records and capture histories from trapping efforts in 2017 and 2018, we estimated the long-term apparent survival and site fidelity of this population composed largely of waif tortoises. We estimated annual apparent survival probabilities to be high (≥0.90) for subadult, adult male, and adult female tortoises, and these rates were similar to those reported for wild-to-wild translocated gopher tortoises and those from unmanipulated populations. Of the tortoises recaptured within the boundaries of the preserve, 75% were located within 400 m of their release location. These results suggest that waif tortoises could be an important resource in reducing the extirpation risk of isolated populations. © 2021 The Wildlife Society.

South Carolina

Captivity, reintroductions, and the rewilding of amphibian-associated bacterial communities

Many studies have noted differences in microbes associated with animals reared in captivity compared to their wild counterparts, but few studies have examined how microbes change when animals are reintroduced to the wild after captive rearing. As captive assurance populations and reintroduction programs increase, a better understanding of how microbial symbionts respond during animal translocations is critical. We examined changes in microbes associated with boreal toads ( Anaxyrus boreas ), a threatened amphibian, after reintroduction to the wild following captive rearing. Previous studies demonstrate that developmental life stage is an important factor in amphibian microbiomes. We collected 16S marker-gene sequencing datasets to investigate: (i) comparisons of the skin, mouth, and fecal bacteria of boreal toads across four developmental life stages in captivity and the wild, (ii) tadpole skin bacteria before and after reintroduction to the wild, and (iii) adult skin bacteria during reintroduction to the wild. We demonstrated that differences occur across skin, fecal, and mouth bacterial communities in captive versus wild boreal toads, and that the degree of difference depends on developmental stage. Skin bacterial communities from captive tadpoles were more similar to their wild counterparts than captive post-metamorphic individuals were to their wild counterparts. When captive-reared tadpoles were introduced to a wild site, their skin bacteria changed rapidly to resemble wild tadpoles. Similarly, the skin bacterial communities of reintroduced adult boreal toads also shifted to resemble those of wild toads. Our results indicate that a clear microbial signature of captivity in amphibians does not persist after release into natural habitat.

Colorado

Black bears in Arkansas: Characteristics of a successful translocation

In 1958, the Arkansas Game and Fish Commission began translocating black bears ( Ursus americanus ) from Minnesota to the Interior Highlands (Ozark and Ouachita mountains) of Arkansas where bears had been extirpated early in this century. This project continued for 11 years with little public imput, during which time an estimated 254 bears were released. We estimate there are now >2,500 bears in the Interior Highlands of Arkansas, Missouri, and Oklahoma, making it one of the most successful translocations of a Carnivora. Factors that contributed to the success include use of wild-captured animals, elimination of major factors associated with extirpation, release into prime habitats within the former range, multiple release sites, release of 20–40 animals/year for eight years, and release of mostly males prior to release of mostly females. Studies on two allopatric populations demonstrate that they are now diverging in some demographic characteristics, including litter size, cub survivorship, and adult sex-ratio. Translocation of black bears to the Interior Highlands is successful in terms of numbers of animals, but it will not be truly successful until people accept black bears as part of the regional fauna. To that end, those associated with management and research of bears in Arkansas are now focussing on public education and control of nuisance bears.

Arkansas

Mortality of Siberian polecats and black-footed ferrets released onto prairie dog colonies

Black-footed ferrets ( Mustela nigripes ) likely were extirpated from the wild in 1985–1986, and their repatriation depends on captive breeding and reintroduction. Postrelease survival of animals can be affected by behavioral changes induced by captivity. We released neutered Siberian polecats ( M. eversmanii ), close relatives of ferrets, in 1989–1990 on black-tailed prairie dog ( Cynomys ludovicianus ) colonies in Colorado and Wyoming initially to test rearing and reintroduction techniques. Captive-born polecats were reared in cages or cages plus outdoor pens, released from elevated cages or into burrows, and supplementally fed or not fed. We also translocated wild-born polecats from China in 1990 and released captive-born, cage-reared black-footed ferrets in 1991, the 1st such reintroduction of black-footed ferrets. We documented mortality for 55 of 92 radiotagged animals in these studies, mostly due to predation (46 cases). Coyotes ( Canis latrans ) killed 31 ferrets and polecats. Supplementally fed polecats survived longer than nonprovisioned polecats. With a model based on deaths per distance moved, survival was highest for wild-born polecats, followed by pen-experienced, then cage-reared groups. Indexes of abundance (from spotlight surveys) for several predators were correlated with mortality rates of polecats and ferrets due to those predators. Released black-footed ferrets had lower survival rates than their ancestral population in Wyoming, and lower survival than wild-born and translocated polecats, emphasizing the influence of captivity. Captive-born polecats lost body mass more rapidly postrelease than did captive-born ferrets. Differences in hunting efficiency and prey selection provide further evidence that these polecats and ferrets are not ecological equivalents in the strict sense.

Journal of Mammalogy

Optimizing release strategies: A stepping-stone approach to reintroduction

Evaluation of alternative management strategies enables informed decisions to accelerate species recovery. For reintroductions, post-release survival to reproductive age is a key parameter influencing population growth. Here we trial a ‘stepping-stone’ method to maximize the success of captive-bred animals when the availability of more suitable wild-born release candidates is limited. Our approach makes use of relatively safe and established wild populations to prepare captive-bred individuals for eventual translocation to a final release destination, thus building resilience through establishment of multiple populations over time. We developed a novel multievent model integrating encounter history and biotelemetry data to evaluate reintroduction strategies for the critically endangered Vancouver Island marmot (Marmota vancouverensis). We compared post-release survival of 176 individuals (52 wild-born, 47 captive-bred marmots released directly to destinations, and 77 captive-bred marmots released with a stepping-stone approach). Survival estimates to prime breeding-age (PBA), were then used to quantify expected success of potential release strategies. Our analysis indicates that post-release survival varies by source population and release method, as well as age, season, year, and years since release. Conditional on an objective of maximizing survival to PBA, our results suggest that using wild-born marmots for translocations as often as possible, and stepping-stone captive-bred marmots prior to final release, will result in the best outcomes. There was a 0.86 probability that survival to PBA was greater for captive-bred marmots released as yearlings using a stepping-stone approach (survival to PBA mode = 0.13, 95% CRI = 0.05-0.30) than for captive-bred animals that were directly released to destination sites as one-year-olds (survival to PBA mode = 0.04, 95% CRI = 0.01-0.24). Consequently, the stepping-stone approach yields much higher population establishment or growth potential than previous release strategies that used captive-bred marmots. Optimizing the combination of release candidates, sites, and timing can thereby increase the effectiveness of reintroductions.

British Columbia

Survival of captive-raised light-footed Ridgway’s rails is influenced by release date and time in wild

Captive breeding and translocation programs are an increasingly common conservation tool and management strategy used for some of the rarest and most endangered species in the world. These programs come at a high cost, and many translocation programs fail to monitor animals after release. Light-footed Ridgway’s rails ( Rallus obsoletus levipes ) are federally endangered marsh birds endemic to coastal wetlands of southern California and northern Mexico. Juvenile captive-raised light-footed Ridgway’s rails have been released into marshes within their U.S. range for >20 yr, but little effort has been devoted to post-release tracking of their movement and survival. We used satellite GPS transmitters to track survival of 46 juvenile captive-released and 42 juvenile wild-caught light-footed Ridgway’s rails from 2020–2022. Our results suggest that juvenile captive-released rails had lower initial daily survival probability (0.979) compared with that of juvenile wild-caught rails (0.994). Survival probability of captive-released rails increased with time in the wild, matching that of wild birds at about 100 d post-release. Survival of captive-released birds was most influenced by the date birds were released (releases in early summer had the highest survival). Our study emphasizes the importance of post-release monitoring as part of any captive breeding and translocation program and provides important insight into management strategies that may improve captive-released rail survival in the wild.

California

Captive propagation, introduction, and translocation programs for wildlife vertebrates

Captive propagation, introduction, and translocation (relocation) programs for many animals have been undertaken by federal, state, and private agencies for more than 20 years. These programs help aid the recovery of endangered and threatened species, reestablish lost species, augment declining populations, increase recreational opportunities, reduce nuisance species, and introduce non-native species. Davidson and Nettles (1992) discuss translocation as a component of successful early restorations of game species including wild turkey ( Meleagris gallopavo ) and white-tailed deer ( Odocoileus virginianus ), and recovery of endangered species such as the peregrine falcon (Falco peregrinus). Despite some successes, the total number of translocations that occur yearly is unknown, as is the success and effects of these programs, because there is rarely appreciable monitoring after release (Griffith et al. 1989; Gogan 1990). This report focuses on trends in the use of translocation programs and disease transmission following translocation of wildlife vertebrates other than fish. In the absence of a national data base on wildlife translocations, a search for publications with information on translocations was performed by using Wildlife Review and the U.S. Fish and Wildlife Reference Service CD-ROM data bases for the 20-year period, 1971-91. In addition, personnel from multiple federal, state, and private agencies that conduct propagation and translocation programs were contacted for supplemental information and literature. Increasing numbers of books (Neilsen and Brown 1988), journals (Ullrey 1993), and meetings (Junge 1992; Wolff and Seal 1992) discuss wildlife translocations and many contain information on the effects of translocations on animals and their environment.

Book chapter

Identifying factors linked with persistence of reintroduced populations: Lessons learned from 25 years of amphibian translocations

Conservation translocations are increasingly used to help recover imperiled species. However, success of establishing populations remains low, especially for amphibians. Identifying factors associated with translocation success can help increase efficiency and efficacy of recovery efforts. Since the 1990s, several captive and semi-captive facilities have produced Chiricahua Leopard Frogs ( Rana chiricahuensis ) to establish or augment wild populations in Arizona and New Mexico, USA. During this same time, personnel associated with several programs surveyed translocation and non-translocation sites for presence of amphibians. We used 25 years (1995–2019) of survey and translocation data for the federally threatened Chiricahua Leopard Frog to identify factors linked with population persistence. Our dataset included approximately 40,642 egg masses or animals translocated in 314 events to 115 distinct sites and > 5800 visual encounter surveys from 641 sites; 120 of these sites were also surveyed with environmental DNA methods in 2018. We used a hierarchical dynamic occupancy model that accounted for imperfect detection to identify patch- and landscape-level attributes associated with site occupancy, and then used predictions from that model to evaluate factors associated with population persistence at translocation sites. Across all sites, extinction probability for Chiricahua Leopard Frogs was higher in lotic (stream) than lentic (pond) habitats and when Western Tiger Salamanders ( Ambystoma mavortium ) were present. Restoration of sites specifically for frog conservation reduced extinction probability. Colonization of unoccupied sites increased moderately with increasing numbers of translocation sites within 2 km, indicating a benefit of translocation efforts beyond sites where frogs were stocked. At translocation sites, persistence was greater in lentic than lotic habitats and was negatively correlated with the proportion of years tiger salamanders were present. Increasing numbers of translocation events, especially of late-stage larvae, increased persistence. There was little difference in population persistence based on whether stock was from captive, semi-captive, or wild sources, but translocations during the dry season (January— July) succeeded more than those after the typical arrival of summer rains (August— December). Based on the number of years translocation sites were predicted to be occupied, 2 or more translocations produced, on average, a > 4-yr increase in predicted occupancy compared to sites without translocations. While translocations have increased the number of populations across the landscape, continued management of water availability and threats such as invasive predators and disease remain critical to recovery of the Chiricahua Leopard Frog.

Arizona, New Mexico

Guidelines for the field evaluation of desert tortoise health and disease

Field evaluation of free-ranging wildlife requires the systematic documentation of a variety of environmental conditions and individual parameters of health and disease, particularly in the case of rare or endangered species. In addition, defined criteria are needed for the humane salvage of ill or dying animals. The purpose of this paper is to describe, in detail, the preparation, procedures, and protocols we developed and tested for the field evaluation of wild desert tortoises ( Gopherus agassizii ). These guidelines describe: preparations for the field, including developing familiarity with tortoise behavior and ecology, and preparation of standardized data sheets; journal notes to document background data on weather conditions, temperature, rainfall, locality, and historic and recent human activities; procedures to prevent the spread of disease and parasites; data sheets for live tortoises to record tortoise identification, location, sex, body measurements and activity; health profile forms for documenting and grading physical abnormalities of tortoise posture and movements, general condition (e.g., lethargy, cachexia), external parasites, and clinical abnormalities associated with shell and upper respiratory diseases; permanent photographic records for the retrospective analysis of progression and regression of upper respiratory and eye diseases, analysis of shell lesions and evaluation of growth and age; and indications and methods for salvaging ill or dying tortoises for necropsy evaluation. These guidelines, tested on 5,000 to 20,000 tortoises over a 10 to 27 yr period, were designed to maximize acquisition of data for demographic, ecological, health and disease research projects; to reduce handling and stress of individual animals; to avoid spread of infectious disease; to promote high quality and consistent data sets; and to reduce the duration and number of field trips. The field methods are adapted for desert tortoise life cycle, behavior, anatomy, physiology, and pertinent disease; however the model is applicable to other species of reptiles. Comprehensive databases of clinical signs of disease and health are crucial to research endeavors and essential to decisions on captive release, epidemiology of disease, translocation of wild tortoises, breeding programs, and euthanasia.

Journal of Wildlife Diseases

Release of captive-reared or translocated endangered birds: What do we need to know?

Attempts to evaluate the success of endangered-species reintroduction programs are frustrated by a lack of reliable information on releases of either endangered or nonendangered species. Although many programs have attempted to establish or augment wild populations with captive-reared or wild-caught birds (Williams 1977), there are few published accounts that allow quantitative statements on the success of releases and the role played by animals subjected to different rearing and release protocols (Berger 1978, Kear and Berger 1980). This makes it difficult to assess accurately the status of these species, or to evaluate the influence of various management actions.

The Auk

Can captive populations function as sources of genetic variation for reintroductions into the wild? A case study of the Arabian oryx from the Phoenix Zoo and the Shaumari Wildlife Reserve, Jordan

The Arabian oryx ( Oryx leucoryx ) historically ranged across the Arabian Peninsula and neighboring countries until its extirpation in 1972. In 1963&ndash;1964 a captive breeding program for this species was started at the Phoenix Zoo (PHX); it ultimately consisted of 11 animals that became known as the &lsquo;World Herd&rsquo;. In 1978 &ndash; 1979 a wild population was established at the Shaumari Wildlife Reserve (SWR), Jordan, with eight descendants from the World Herd and three individuals from Qatar. We described the mtDNA and nuclear genetic diversity and structure of PHX and SWR. We also determined the long-term demographic and genetic viability of these populations under different reciprocal translocation scenarios. PHX displayed a greater number of mtDNA haplotypes ( n = 4) than SWR ( n = 2). Additionally, PHX and SWR presented nuclear genetic diversities of N &macr; A N&macr;A = 2.88 vs. 2.75, H &macr; O H&macr;O = 0.469 vs. 0.387, and H &macr; E H&macr;E = 0.501 vs. 0.421, respectively. Although these populations showed no signs of inbreeding ( F &macr; IS F&macr;IS &asymp; 0), they were highly differentiated ( G &prime; &prime; ST GST&prime;&prime; = 0.580; P < 0.001). Migration between PHX and SWR ( Nm = 1, 4, and 8 individuals/generation) increased their genetic diversity in the short-term and substantially reduced the probability of extinction in PHX during 25 generations. Under such scenarios, maximum genetic diversities were achieved in the first generations before the effects of genetic drift became predominant. Although captive populations can function as sources of genetic variation for reintroduction programs, we recommend promoting mutual and continuous gene flow with wild populations to ensure the long-term survival of this species.

Conservation Genetics

Translocation as a species conservation tool: Status and strategy

Surveys of recent (1973 to 1986) intentional releases of native birds and mammals to the wild in Australia, Canada, Hawaii, New Zealand, and the United States were conducted to document current activities, identify factors associated with success, and suggest guidelines for enhancing future work. Nearly 700 translocations were conducted each year. Native game species constituted 90 percent of translocations and were more successful (86 percent) than were translocations of threatened, endangered, or sensitive species (46 percent). Knowledge of habitat quality, location of release area within the species range, number of animals released, program length, and reproductive traits allowed correct classification of 81 percent of observed translocations as successful or not.

Science

Pit tag application in native freshwater mussels: Case studies across small, medium, and large rivers

Since their first use in the mid-1980s, external passive integrated transponder (PIT) tags have facilitated innovative investigations into multiple biological traits of animals. For native freshwater mussels, PIT tags are frequently used in capture-mark-recapture applications because they allow repeated, noninvasive sampling, are easy to apply, have high retention rates, and have negligible short-term effects on growth and survival. Because of these traits, resource managers and scientists are using PIT-tagged animals to estimate survival and movement of mussels associated with restoration efforts. However, consistency is limited in how PIT tags are affixed, monitored, and reported. Thus, our objectives were to (1) share our collective experiences in PIT tagging mussels across three case studies in small, medium, and large rivers and (2) propose guidelines for tagging and reporting data from PIT tag studies with native freshwater mussels to facilitate comparisons across future studies. The number of studies that have marked mussels with PIT tags has increased over the past 10 years. The ability to detect mussels using PIT tags has substantially advanced research in three areas of mussel ecology: (1) estimating vital rates (e.g., growth and survival), (2) tracking movements and behaviors of captively propagated, wild, and translocated individuals, and (3) improving our understanding of life history traits, such as reproductive timing. Each case study offers insights on tagging methods, tag loss, tag retention, and monitoring frequency across multiple species that range in conservation status from common to rare. We conclude with best-practice guidelines for placing PIT tags on freshwater mussels and a list of variables that could be reported in future studies to facilitate cross-system comparisons.

Freshwater Mollusk Biology and Conservation

Island of misfit tortoises: Waif gopher tortoise health assessment following translocation

Translocation, the intentional movement of animals from one location to another, is a common management practice for the gopher tortoise ( Gopherus polyphemus ). Although the inadvertent spread of pathogens is a concern with any translocation effort, waif tortoises—individuals that have been collected illegally, injured and rehabilitated or have unknown origins—are generally excluded from translocation efforts due to heightened concerns of introducing pathogens and subsequent disease to naïve populations. However, repurposing these long-lived animals for species recovery is desirable when feasible, and introducing waif tortoises may bolster small populations facing extirpation. The objective of this study was to assess the health of waif tortoises experimentally released at an isolated preserve in Aiken County, SC, USA. Our assessments included visual examination, screening for 14 pathogens using conventional or quantitative polymerase chain reaction (qPCR) and haematological evaluation. Of the 143 individuals assessed in 2017 and 2018, most individuals (76%; n = 109 of 143) had no overt clinical evidence of disease and, when observed, clinical findings were mild. In both years, we detected two known tortoise pathogens, Mycoplasma agassizii and Mycoplasma testudineum , at a prevalence of 10.2–13.9% and 0.0–0.8%, respectively. Additionally, we found emydid Mycoplasma , a bacterium commonly found in box turtles ( Terrapene spp . ), in a single tortoise that showed no clinical evidence of infection. The presence of nasal discharge was an important, but imperfect, predictor of Mycoplasma spp. infection in translocated tortoises. Hemogram data were comparable with wild populations. Our study is the first comprehensive effort to assess pathogen prevalence and hemogram data of waif gopher tortoises following translocation. Although caution is warranted and pathogen screening necessary, waif tortoises may be an important resource for establishing or augmenting isolated populations when potential health risks can be managed.

Conservation Physiology

Translocation and early post-release demography of endangered Laysan teal

In an attempt to reduce the high extinction risk inherent to small island populations, we translocated wild Laysan teal Anas laysanensis to a portion of its presumed prehistoric range. Most avian translocations lack the strategic post-release monitoring needed to assess early population establishment or failure. Therefore, we monitored the survival and reproduction of all founders, and their first-generation offspring using radio telemetry for 2 years after the first release. Forty-two Laysan teal were sourced directly from the only extant population on Laysan Island and transported 2 days by ship to Midway Atoll. All birds survived the translocation with nutritional and veterinary support, and spent between 4 and 14 days in captivity. Post-release survival of 42 founders was 0.857 (95% CI 0.86-0.99) during 2004-2006 or annualized 0.92 (95% CI 0.83-0.98). Seventeen of 18 founding hens attempted nesting in the first two breeding seasons. Fledgling success was 0.57 (95% CI 0.55-0.60) in 2005 and 0.63 (95% CI 0.62-0.64) in 2006. The effective founding female population (Ne) was 13. We applied these initial demographic rates to model population growth. The nascent population size increased to >100 after only 2 years post-release (?? = 1.73). If this growth rate continues, the size of the Midway population could surpass the source population before 2010. ?? 2008 The Authors. Journal compilation ?? 2008 The Zoological Society of London.

Animal Conservation

Trading off hatching success and cost in the captive breeding of Whooping Cranes

Captive breeding is an increasingly used conservation strategy for species with a high risk of extinction in the wild, but managing a captive breeding programme can be challenging if there is a deficiency in knowledge about the species’ breeding biology. A knowledge gap can make it difficult to evaluate different management options. For avian species, egg hatching success is a key demographic parameter, and data-logging egg technology can provide important information on optimal species-specific incubation conditions, which can help inform captive breeding practises and identify efficient captive management options. In the context of a captive breeding programme for endangered Whooping Cranes Grus americana , we investigated associations between hatching success and incubation conditions, including environmental parameters (temperature, relative humidity and egg turning rate), and incubation type (artificial incubation; foster incubation by Sandhill Cranes, Grus canadensis ; and Whooping Crane incubation). Finally, we considered both cost and breeding output in an analysis of incubation practises. We found that daily mean temperatures were negatively associated with hatching success, and that hatching success was highest with incubation under Sandhill Cranes. However, incubation by artificial incubators, rather than Sandhill Cranes, provided a trade-off between cost and breeding output that is likely to be acceptable to many captive programme managers. We encourage other captive breeding programmes to use innovations that help to increase potential release numbers for conservation translocations by considering biological and financial constraints.

Animal Conservation