Reintroduction Programs Research Articles

Life‐history traits and the fate of translocated populations

Attempts to identify predictors and mechanisms of invasion success have been weakened by poor data quality, mostly because monitoring does not begin immediately after introduction events. To overcome this issue, we used data from conservation translocations of threatened bird species. We analyzed information on >1200 translocation events of >150 bird species to investigate how life-history traits affect population establishment measured based on rates of survival and reproduction. Species position along the slow-fast life-history continuum was a key predictor of translocation success. Species with fast-paced life histories were less likely to survive (over both short- and mid-term) and more likely to breed successfully than species with slow life histories. The temporal partitioning of reproductive effort (number of clutches per year) also affected the probability of successful reproduction. Our results illustrate how conservation-motivated reintroduction programs can provide proxies for the initial stages of the invasion process, enabling empirical tests of predictions from life-history theory and informing management.

Predicting the distribution of released Oriental White Stork (Ciconia boyciana) in central Japan

AbstractThe Oriental White Stork (Ciconia boyciana) is one of the species threatened by mainly anthropogenic factor and their habitats are considered to be conserved. The first reintroduction of the species in Japan occurred in 2005. But as the species' natural wetland habitats are declining, the birds now prefer to forage in rice paddies. Thus, restoring the paddy‐dominated landscape is key for further success in the reintroduction program. In addition, a quantitative method is urgently needed to assess how much suitable habitat is available and where it is located. In this study, we identified environmental factors that affect the distribution of the Oriental White Stork and produced the first predictive spatial distribution map using 2‐year satellite tracking data of reintroduced individuals. The maximum entropy (MaxEnt) approach was used to model the species' distribution at the landscape scale (1 km × 1 km grid cells). We identified six relevant environmental variables. Our results highlight the proportion of area of rice paddies as alternative wetland habitat as the most influential variable affecting the distribution positively. Landscape diversity represented by a complex mosaic of paddies and forest is also important for the species, as total length of paddy–forest edge also had a positive effect on habitat suitability. Our predictive distribution map cannot entirely provide distribution; however, it may be valuable information when considering where should be conserved as habitat to maintain the Oriental White Stork population in Japan.

Early Observations from Monitoring a Reintroduction Program: Return of Sockeye Salmon to a Nursery Lake of Historical Importance

AbstractThe historical distribution of Sockeye Salmon Oncorhynchus nerka in the Columbia River basin has been constrained by the species’ dependence on nursery lakes for juvenile rearing. Several productive lake systems were impounded by dams during the last century leading to the extirpation of Sockeye Salmon from many nursery lakes in the region. Recent efforts to re‐establish populations in historically natal areas are exemplified by the Cle Elum Lake reintroduction program. The program is founded on outplanting adult fish from two middle Columbia River donor populations with different adaptive potentials. We used genetic stock identification methods to differentiate stock origins between Osoyoos Lake (OSO) and Lake Wenatchee (WEN) donor stocks and to evaluate the relative productivity from two brood years (2011 and 2012) of natural spawning in the novel environment. Spawning ground surveys revealed assortative mating between earlier‐spawning WEN fish that were more abundant farthest upstream and later‐spawning OSO fish that were concentrated (82%) downstream nearest the lake. Hybrids accounted for only 5% of sampled smolts and 4% of adult returns. Smolts rearing in Cle Elum Lake were significantly larger overall (OSO, 140 mm; WEN, 129 mm) than smolts in either donor population (84 mm). However, the average size of OSO smolts varied among emigration years, and relative smolt abundances favored the WEN stock (70% overall), indicative of a rearing survival advantage. In relation, the WEN stock exhibited a better average rate of replacement (0.80) in adult‐to‐adult escapement compared with the OSO stock (0.17). Continued monitoring will focus on trends in productivity and potential demographic shifts that may arise in the Cle Elum Lake population and will provide managers with information concerning limiting factors in the environment that might affect similar approaches to reintroductions in other lake systems.

Effects of life history and reproduction on recruitment time lags in reintroductions of rare plants.

Reintroductions are important components of conservation and recovery programs for rare plant species, but their long-term success rates are poorly understood. Previous reviews of plant reintroductions focused on short-term (e.g., ≤3 years) survival and flowering of founder individuals rather than on benchmarks of intergenerational persistence, such as seedling recruitment. However, short-term metrics may obscure outcomes because the unique demographic properties of reintroductions, including small size and unstable stage structure, could create lags in population growth. We used time-to-event analysis on a database of unusually well-monitored and long-term (4-28 years) reintroductions of 27 rare plant species to test whether life-history traits and population characteristics of reintroductions create time-lagged responses in seedling recruitment (i.e., recruitment time lags [RTLs]), an important benchmark of success and indicator of persistence in reintroduced populations. Recruitment time lags were highly variable among reintroductions, ranging from <1 to 17 years after installation. Recruitment patterns matched predictions from life-history theory with short-lived species (fast species) exhibiting consistently shorter and less variable RTLs than long-lived species (slow species). Long RTLs occurred in long-lived herbs, especially in grasslands, whereas short RTLs occurred in short-lived subtropical woody plants and annual herbs. Across plant life histories, as reproductive adult abundance increased, RTLs decreased. Highly variable RTLs were observed in species with multiple reintroduction events, suggesting local processes are just as important as life-history strategy in determining reintroduction outcomes. Time lags in restoration outcomes highlight the need to scale success benchmarks in reintroduction monitoring programs with plant life-history strategies and the unique demographic properties of restored populations. Drawing conclusions on the long-term success of plant reintroduction programs is premature given that demographic processes in species with slow life-histories take decades to unfold.

Founding in action: genetic assessment of new populations from the same reintroduction program

Founding in action: genetic assessment of new populations from the same reintroduction program

Functional-trait ecology of the plateau pika Ochotona curzoniae in the Qinghai-Tibetan Plateau ecosystem.

Understanding a species' functional traits allows for a directed and productive perspective on the role a species plays in nature, and thus its relative importance to conservation planning. The functional-trait ecology of the plateau pika Ochotona curzoniae is examined to better understand the resilience and sustainability of the high alpine grasslands of the Qinghai-Tibetan Plateau (QTP). The key functional traits of plateau pikas are their abundance and behavior of digging extensive burrow systems. Plateau pikas have been poisoned over a significant part of their original geographic distribution across the QTP, allowing comparison of ecological communities with and without pikas. Nearly all mammalian and avian carnivores, most of which are obligate predators on pikas, have been lost in regions where pikas have been poisoned. Most endemic birds on the QTP nest in pika burrows; when pikas are poisoned, burrows collapse, and these birds are greatly reduced in number. Due to the biopedturbation resulting from their burrows, regional plant species richness is higher in areas with pikas than without. The presence of pika burrows allows higher rates of infiltration during heavy monsoon rains compared to poisoned areas, possibly mitigating runoff and the potential for serious downslope erosion and flooding. Thus, the functional traits of plateau pikas enhance native biodiversity and other important ecosystem functions; these traits are irreplaceable. As plateau pikas are not natural colonizers, active re-introduction programs are needed to restore pikas to areas from which they have been poisoned to restore the important functional ecological traits of pikas.

Habitat preferences of reintroduced banteng (Bos javanicus) into the Salakphra Wildlife Sanctuary, Thailand

Abstract ContextLarge forest-dwelling mammals are highly sensitive to habitat structure. Thus, understanding the responses of reintroduced banteng (Bos javanicus d’Alton 1823) to their habitat is important for ensuring the sustainability of a reintroduction program. AimsThe aim of the present study was to evaluate the habitat preferences of banteng after reintroduction into the Salakphra Wildlife Sanctuary in Thailand on the basis of fieldwork conducted between January 2015 and November 2017. MethodsSeven banteng individuals bred at the Khao Nampu Nature and Wildlife Education Center were systematically reintroduced into the Salakphra Wildlife Sanctuary in 2015 (four individuals) and 2016 (three individuals). The banteng individuals were tracked via radio-collars and camera-traps. The maximum-entropy method (MaxEnt) and multiple logistic regressions (MLR) were used to identify habitat preferences. Kernel-density estimates (KDE) and a minimum convex polygon (MCP) were used to estimate the area of the habitat used. Key resultsIn total, 407 radio-signal locations showed that the MaxEnt habitat-preference models classified the banteng as associated with distance from villages and salt licks (regularised training gain of &amp;gt;1.0). Multiple logistic regressions form 32 camera-trap locations classified the banteng as associated with low elevations far from villages, guard stations and roads in a flat area (no aspect). The two methods for estimating habitat use provided similar results and showed that the reintroduced banteng used a wider range of habitat in the dry than in the wet season. ConclusionsThe results from the present study suggest that the reintroduced banteng individuals prefer low elevations and flat areas without human activity. ImplicationsThese findings are important for possible translocations elsewhere.

Assessment of Browse Availability and Suitability for Black Rhino’s Re-Introduction in Northern Gonarezhou National Park, Southeastern Zimbabwe

Wildlife reintroduction regulations require feasibility assessment to inform planning. The study aims to contribute to the existing knowledge on northern Gonarezhou National Park (GNP), southeastern Zimbabwe, prior to the black rhino re-introduction project. The study objective was to assess browse availability and suitability for black rhino re-introduction in northern GNP. We stratified the study area into two strata, i.e. north and south of Runde River in GNP. A total of 96 sample plots measuring 20 m × 30 m (i.e., 48 plots in each study stratum) were randomly placed across the study strata, between March and April 2011. Woody plant variables recorded are: shrub height, shrub canopy diameters, evidence of browsing on woody plants, number of shrubs and woody species. Principal browse frequency of occurrence and proportional quality of woody species were categorized and analyzed in combination with knowledge on the woody species’ value to black rhino diet. Preferred woody species were determined using browse suitability/electivity index. A total of 3201 woody plants were recorded across the study strata. Woody species diversity and black rhino’s browse suitability/electivity value significantly (p = 0.001) differed across the study strata. However, there were no significant differences in shrub density, shrub canopy volume and density of browsed plants. Common principal forages were recorded and included: knob thorn Acacia (Acacia nigrescens), small-leaved sickle-bush (Dichrostachys cineria) and tamboti (Spirostachys africana). The study suggested that black rhino’s browse suitability, preferred browse woody species, woody species diversity and proportional browse availability, as selected attributes are favorably more pronounced in the northern side of the Runde River in GNP, suggesting it is more suitable as a sanctuary for the black rhino re-introduction programme. It was recommended that black rhinos could be re-introduced in the northern GNP area provided other important factors such as law enforcement are taken into consideration.

Managing Populations, Diseases, and Landowner Perceptions of Prairie Dogs for Black-Footed Ferret Reintroduction

The black-footed ferret (Mustela nigripes) is one of the rarest mammal species in North America. Captive breeding has prevented extinction of this species, but successful reintroduction of ferrets into their native grassland habitat is a complex endeavor. As specialist predators, ferrets depend almost exclusively on prairie dogs (Cynomys spp.) for both food and shelter, so successful black-footed ferret reintroduction hinges on maintaining large colonies of prairie dogs. However, prairie dogs are also considered agricultural pests and are often subjected to eradication programs. These eradication programs hamper efforts to reintroduce ferrets and disrupt the valuable ecosystem services prairie dogs provide in their role as both keystone and foundation species. Even when agreements are reached to maintain prairie dog colonies, plague (Yersinia pestis), which infects both prairie dogs and ferrets, can threaten the success of a ferret reintroduction program. We describe the research on the complex ecological relationships and socio-environmental challenges of reintroducing endangered black-footed ferrets, with a focus on the most abundant prairie dog species, the black-tailed prairie dog (Cynomys ludovicianus).

Isolation and Characterization of 32 Microsatellite Markers in Hermann's Tortoise, Testudo hermanni (Testudinidae)

We used 454-sequencing to identify and characterize 32 microsatellite loci for the Western Hermann's tortoise (Testudo hermanni hermanni) for which primer sequences, characteristics, and multiplexes are provided. These markers have been tested for one continental (Var) and one insular (Corsica) French population as well as for the Eastern Hermann's tortoise (Testudo hermanni boettgeri). For these 3 populations, 24 loci were polymorphic. These microsatellite markers will be particularly useful to assess the genetic diversity and characteristics of the different Hermann's tortoise populations and will have direct applications for its protection, notably with respect to reintroduction and conservation programs.

Microhabitat suitability as a tool to improve the success rate of a translocation or reintroduction, case‐study of the bullhead (Cottus perifretum) in Flanders, Belgium

Microhabitat suitability models are useful tools to enhance the reintroduction success of fish. Since 2008, a translocation and reintroduction program has been carried out in Flanders to prevent substantial loss of genetic variability in the Cottus perifretum (bullhead) population, and to meet the goals set by the Habitat Directive. To this end, habitat suitability of potential headstreams was assessed on a macrohabitat and microhabitat scale prior to the reintroduction. On a macrohabitat scale, water quality, habitat structure, food availability, and fish community were screened. Based on microhabitat models for bullhead in the summer period, microhabitat suitability was assessed in headstreams where macrohabitat characteristics showed a high potential for success. Both macro‐ and microhabitat assessment showed that reintroduction of bullheads in the Nellebeek, Bruelbeek, and Mollendaalbeek would most likely lead to self‐sustaining populations. For the Sint‐Annabeek, the microhabitat suitability model, considering depth and stream velocity, estimates that 7.5–9.5% of the headstream is suitable for bullhead. However, when substratum is taken into account, the microhabitat suitability index shows that only 4.3–5.8% of the brook is suitable. The current habitat quality and quantity in the Sint‐Annabeek is estimated to support a mean total population of 812 bullheads. However, the microhabitat suitability can be substantially improved by the artificial deposition of medium‐sized gravel (5–50 mm) and large gravel (50–100 mm). By doing so, the mean estimated population size could increase up to 1,330 individuals. Our results show that habitat improvement is necessary prior to the reintroduction of bullheads in the Sint‐Annabeek.

The resistance of Eimeria spp. to toltrazuril in black grouse (Lyrurus tetrix) kept in an aviary

The black grouse is a critically endangered species in Europe. Aviary breeding and re-introduction programs have contributed to the reinstatement of black grouse populations. Parasitic diseases can influence the species' behavior, choice of habitats, and survival rates. Protozoa of the genus Eimeria are the most prevalent parasites in black grouse. The aim of this study was to evaluate the effectiveness of toltrazuril (TOL) against Eimeria spp. in black grouse kept in an aviary. Eimeria spp. oocysts (mean OPG for all birds = 7,047.84; SD = 5,625.05) were detected in feces samples in a routine parasitological examination. Parasitic infections were treated with toltrazuril Baycox 2.5% (Bayer, Leverkusen, Germany) at 1ml/1 l H2O administered per os with drinking water twice a day for 2 d, 12h/24h. High oocysts counts persisted upon the second parasitic examination. Therefore, the birds were divided into 3 groups in 3 existing aviaries. Toltrazuril was administered according to the same protocol, and its uptake with drinking water was monitored. A parasitological examination conducted 5d later revealed the presence of parasites, and the TOL dose was increased to 3ml/1 l H2O. When oocysts were detected in a successive exam, the TOL dose was further increased to 5ml/1 l H2O. The increase in TOL dose did not eliminate parasites, therefore, the treatment was discontinued. The fecal egg count reduction test (FECRT) revealed that 1ml of TOL reduced fecal oocysts counts (OPG) by 0.02%, the second application of the same TOL dose reduced OPG by 0%, 3ml of TOL reduced OPG by 0%, and 5ml of TOL reduced OPG by 65.7%. The applied doses of TOL did not induce significant differences in the fecal oocysts counts of any of the identified species of coccidia. The results indicate that the coccidia species infecting black grouse have natural resistance to TOL.

An estimation of number of birds to be consecutively released in the reintroduction of Japanese Crested Ibises (Nipponia nippon)

The Japanese captive population of Crested Ibis (Nipponia nippon) has rapidly increased, and reintroduction programs were initiated on Sado Island in 2008. The Japanese captive population, however, was founded by only 5 individuals originating from the Chinese captive population. Because efforts were directed toward preserving genetic diversity in the captive population, it was appropriate to consider genetic diversity in the reintroduced population to evaluate its potential to survive in the wild, where environmental changes are more significant than in captivity. The purpose of this study was to determine the number of individuals to release in the future to preserve genetic diversity of the reintroduced population. We simulated the probability that the reintroduced population after 50 years would retain a rare allele existing in the captive population, based on demographic parameters obtained from either the Japanese captive or reintroduced populations, or Chinese wild populations. As a result, the 10–15 individuals currently released in the annual reintroduction would be the number needed to be released each year over 50 years to retain the rare allele with a frequency in the captive population of 0.05 with a >90% probability. Therefore, the current reintroduction program seems reasonable and should be continued.

Lead Exposure in the Critically Endangered Bearded Vulture (Gypaetus barbatus) Population in Southern Africa

Lead poisoning is an important threat to some raptor species, and the primary source of lead is through the ingestion of carcasses that have been shot with lead, which makes scavengers such as vultures particularly vulnerable. We examined the concentrations of lead in blood and bone tissue samples collected throughout the range of the Bearded Vulture (Gypaetus barbatus) in southern Africa. This population is regionally critically endangered and it is not known to what extent lead poisoning may be a threat. Blood lead levels (0.62 ± 0.81 μg dL−1) from six live birds tested in 2017 indicated background levels of exposure to lead. Similarly, five live birds tested in 2009 using a less sensitive method all had blood lead levels <3 μg dL−1. Bone lead levels (11.79 ± 8.34 μg g−1) from eight birds that had died indicated lead exposure and accumulation over time, suggesting that lead may have contributed to their deaths. These levels of lead may be detrimental to the survival and fecundity of this small and declining population. Recommendations to address this threat include banning hunting and culling with lead ammunition, which is the most likely source of this pollutant. Such actions may reduce the population's susceptibility to other threats, which may be compounded by high lead levels, and help ensure the success of planned reintroduction programs.

Comparing the bacterial communities of wild and captive golden mantella frogs: Implications for amphibian conservation.

Bacterial communities are frequently found in symbiotic associations with most animal species. The characteristically moist amphibian skin provides a good environment for the growth of some species of bacteria; among these a few can act as a first line defense mechanism against infections. Amphibians in the wild have relatively high exposure to bacteria through environmental transmission and through interactions with different conspecifics, whilst in captivity animals interact with fewer individuals, as well as experiencing a less complex environment through which to obtain their bacterial community. Here we compared the skin microbiota of captive and wild Mantella aurantiaca to investigate whether the captive environment was affecting individuals’ skin associated bacteria. This could have survivorship implications if captive animals had a different skin microbial community in comparison to wild counterparts and they were to be used in a reintroduction program. The microbial community were characterized through 16S rRNA amplicon sequencing methodology. Analyses showed that captive individuals had significantly lower diversity of bacterial species and lower relative abundant microbiota when compared to wild populations; this could result in captive frogs released back to the wild probably has greater susceptibility to infections due to inadequate skin microbiota.

Conservation genomics illuminates the adaptive uniqueness of North American gray wolves

The resolution of conservation genetic analyses has been limited until recently due to technological and computational challenges associated with genotyping multiple loci at once. In this review, we focus on how the development of high-throughput genotyping methods have enabled conservation genomics studies of wolves in North America. The gray wolf (Canis lupus) historically had a Holarctic distribution across widely varying environments, yet during the early twentieth century many populations declined due to direct persecution and other anthropogenic disturbances. First, we discuss genetic substructure and adaptive uniqueness among genetically and environmentally defined wolf ecotypes. Second, we focus on the new conservation implications revealed by studies having increased genomic resolution of the dynamics of reintroduced and re-established wolves, specifically Mexican and Pacific Northwest wolves. Mexican wolves, a distinct subspecies of North American wolf that inhabit a small area within the southwestern U.S. and Mexico, remain endangered despite decades since a reintroduction program began. How biologists and management agencies use scientific data to define the historical range of Mexican wolves will be critical to future reintroduction efforts. In the Pacific Northwest, admixture occurs between the distinct and declining coastal wolf ecotype and the more abundant reintroduced interior wolves. If coastal wolves obtain protection, then the Pacific Northwest wolves may also warrant protection. Therefore, more precise policies are needed for the management of admixed populations when one source is protected. We recommend that future conservation efforts should provide full protection for distinct ecotypes, support scientifically rigorous definitions of historical range to inform restoration, and enhance the legal status of admixed populations.

The Optimal Timing of Reintroducing Captive Populations Into the Wild

We examine a conservation problem in which the recovery of an endangered species depends on a captive breeding and reintroduction program. The model is applied to the case of the black-footed ferret (Mustela nigripes), an endangered species in North America reliant on captive breeding for survival. The timing of reintroduction is an important concern in these programs as there is a tradeoff between the duration (and therefore the cost) of the captive breeding program and the period the population spends in recovery and in the wild. In this paper, we develop a stylized bioeconomic model to determine the optimal reintroduction time, in which the objective is to minimize the cost of reintroduction while providing a viably-sized population in the wild. Our control variable is the timing of reintroduction, which departs from a large body of work in bioeconomics that focuses on adjustable controls that directly affect the target population. Generally, we find it is optimal to reintroduce ferrets early in a reintroduction program, although this result is contingent on species interactions and provisioning services.

Habitat Suitability of Release Site for Javan Gibbon (Hylobates moloch) in Mount Malabar Protected Forests, West Java

The javan gibbon reintroduction program requires assessment of suitable habitat within release sites to assure the survival of released gibbons. We studied habitat suitability for javan gibbon beginning in April 2017, extending to June 2017 in the Mount Malabar Protected Forest (MMPF), West Java. The objectives of this study were to analyze the habitat suitability of the release site for javan gibbon in MMPF. Analysis of Geographical Information System (GIS) and Principal Component Analysis (PCA) approach were used to obtain habitat suitability values. Habitat suitability variables measured are elevation, Normalized Differential Vegetation Index (NDVI), Bareness Soil Index (BSI), distance from the road, farming, settlement, and open field. We found suitability valued areas consisting of high suitability covered 2,009.23 ha (22.31%), moderate suitability covered 2,497.46 ha (27.73%), and low suitability covered 4.499,65 ha (49.96%), from a total area ± 8.894,47 ha in MMPF.

Haemoproteus paraortalidum n. sp. in captive Black-fronted Piping-guans Aburria jacutinga (Galliformes, Cracidae): High prevalence in a population reintroduced into the wild

Haemosporidian parasites of the genus Haemoproteus are widespread and can cause disease and even mortality in birds under natural and captive conditions. The Black-fronted Piping-guan (Aburria jacutinga) is an endangered Neotropical bird of the Cracidae (Galliformes) going through a reintroduction program to avoid extinction. We used microscopic examination and partial cytochrome b DNA sequencing to describe a new Haemoproteus species infecting Black-fronted Piping-guans bred and raised in captivity that were reintroduced into the Atlantic rainforest. Haemoproteus (Parahaemoproteus) paraortalidum n. sp. was detected in the blood of 19 out of 29 examined birds. The new species is distinguished from other haemoproteids due to the shape of gametocytes, which have pointed ends in young stages, and due to the presence of vacuole-like unstained spaces in macrogametocytes and numerous volutin granules both in macro- and microgametocytes. Illustrations of the new species are provided. Phylogenetic inference positioned this parasite in the Parahaemoproteus subgenus clade together with the other two Haemoproteus genetic lineages detected in cracids up to date. We discuss possible implications of the reintroduction of birds infected with haemosporidian parasites into the wild. Treatment of Haemoproteus infections remains insufficiently studied, but should be considered for infected birds before reintroduction to improve host reproductive and survival rates after release.

To mix or not to mix the sources of relocated plants? The case of the endangered Iris lortetii

Active management of endangered species is required for the persistence of many rare species. Species translocation, a common practice used to mitigate the negative effects of small population sizes, entails risks of outbreeding depression due to dilution of local adaptations, and therefore must be weighed against the costs of a hands-off conservation approach. Iris lortetii is an endangered rhizomatous plant, growing in a small number of isolated populations in northern Israel. We implemented a quasi-in-situ reintroduction program by planting 234 rhizomes from diverse origins in five new sites. All new sites were selected to be as similar as possible to those of the largest natural population. We recorded plant survival and flowering in the field after four years. Flowering plants were artificially crossed either with plants from the same population of origin (within population) or with plants from different origin (between populations). We found no differences in survival between populations of origin and only some indication of local adaptations in the form of increased flowering of the local population. Nonetheless, seed set was significantly higher (a 73% increase) in crosses between populations of origin, compared to within-population crosses, suggesting low genetic diversity within the natural populations. The ability to combine active conservation with rigid testing of theoretical hypothesis, while avoiding all risk to natural populations, highlights the value of the quasi-in-situ approach for restoration. Our results indicate that, in the case of Iris lortetii, active relocation of genotypes, seeds or pollen can enhance the survival of natural populations over time.