Review
Alignment of threat, effort, and perceived success in North American conservation translocations Typhenn A. Brichieri-Colombi and Axel Moehrenschlager ∗ Centre for Conservation Research, Calgary Zoological Society, 1300 Zoo Road, NE, Calgary, AB, T2N 0E7, Canada
Abstract: The use of conservation translocations to mitigate human effects on biodiversity is increasing, but how these efforts are allocated remains unclear. Based on a comprehensive literature review and online author survey, we sought to determine the goals of translocation efforts, whether they focus on species and regions with high threat and likelihood of perceived success, and how success might be improved. We systematically searched the ISI Web of Knowledge and Academic Search Complete databases to determine the species and regions of conservation translocations and found 1863 articles on conservation translocations in the United States, Canada, Mexico, Central America, and Caribbean published from 1974 to 2013. We questioned 330 relevant authors to determine the motivation for translocations, how translocations were evaluated, and obstacles encountered. Conservation translocations in North America were geographically widespread (in 21 countries), increased in frequency over time for all animal classes (from 1 in 1974 to 84 in 2013), and included 279 different species. Reintroductions and reinforcements were more common in the United States than in Canada and Mexico, Central America, or the Caribbean, and their prevalence was correlated with the number of species at risk at national and state or provincial levels. Translocated species had a higher threat status at state and provincial levels than globally (International Union for Conservation of Nature Red List categorization), suggesting that translocations may have been motivated by regional priorities rather than global risk. Our survey of authors was consistent with these results; most translocations were requested, supported, or funded by government agencies and downlisting species at national or state or provincial levels was the main goal. Nonetheless, downlisting was the least reported measure of success, whereas survival and reproduction of translocated individuals were the most reported. Reported barriers to success included biological factors such as animal mortality and nonbiological factors, such as financial constraints, which were less often considered in the selection of release sites. Our review thus highlights discrepancies between project goals and evaluation criteria and between risk factors considered and obstacles encountered, indicating room to further optimize translocation projects. Keywords: assisted colonization, ecological replacement, geographic distribution, reinforcement, reintroduction La Alineaci´ on de la Amenaza, el Esfuerzo y el E´ xito Percibido en las Translocaciones para Conservaci´ on en Am´erica del Norte
Resumen: El uso de las translocaciones para conservaci´on y mitigar los efectos humanos sobre la biodiversidad est´ a incrementando, pero a´ un no es claro c´ omo se asignan estos esfuerzos. Con base en una revisi´ on integral de literatura y una encuesta de autor en l´ınea buscamos determinar los objetivos de los esfuerzos de translocaci´ on, ya sea que se enfoquen en especies y regiones con una amenaza mayor y una probabilidad de ´exito percibido y c´ omo el ´exito puede mejorarse. Buscamos sistem´ aticamente las bases de datos completas de la Red de Conocimiento y B´ usqueda Acad´emica ISI para determinar las especies y regiones de las translocaciones para conservaci´ on y encontramos 1,863 art´ıculos sobre translocaciones para conservaci´ on en los Estados Unidos, Canad´ a, M´exico, Am´erica Central y el Caribe, publicados entre 1974 y 2013. Consultamos
∗ email
[email protected] Paper submitted October 15, 2015; revised manuscript accepted April 13, 2016. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
1159 Conservation Biology, Volume 30, No. 6, 1159–1172 C 2016 The Authors. Conservation Biology published by Wiley Periodicals, Inc. on behalf of Society for Conservation Biology DOI: 10.1111/cobi.12743
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North American Translocation Efforts
a 330 autores relevantes para determinar los motivos de las translocaciones, c´ omo fueron evaluadas y los obst´ aculos a los que se enfrentaron. Las translocaciones para conservaci´ on en Am´erica del Norte estaban dispersas geogr´ aficamente (en 21 pa´ıses), incrementaron su frecuencia con el tiempo para todas las clases animales (de una en 1974 a 84 en 2013) e incluyeron a 279 especies diferentes. Las reintroducciones y los refuerzos fueron m´ as comunes en los Estados Unidos que en Canad´ a, M´exico, Am´erica Central o el Caribe, y su prevalencia estuvo correlacionada con el n´ umero de especies en riesgo a nivel nacional, estatal o provincial. Las especies reubicadas ten´ıan un mayor estado de amenaza a nivel estatal y provincial que a nivel global (categor´ıas de la Lista Roja de la Uni´ on Internaci´ on para la Conservaci´ on de la Naturaleza), lo que sugiere que las reubicaciones podr´ıan haber estado motivadas por prioridades regionales en lugar del riesgo global. Nuestra encuesta a los autores fue consistente con estos resultados ya que la mayor´ıa de las reubicaciones fueron solicitadas, apoyadas o financiadas por agencias del gobierno y bajar la categor´ıa de la especie a nivel nacional, estatal o provincial era el objetivo principal. Sin embargo, bajar la categor´ıa fue la medida de ´exito menos reportada. Los obst´ aculos para el ´exito reportados incluyeron factores biol´ ogicos, como la mortalidad animal, y factores no biol´ ogicos, como las restricciones financieras, que fueron menos considerados en la selecci´ on de los sitios de liberaci´ on. Nuestra revisi´ on resalta as´ı las discrepancias entre los objetivos del proyecto y los criterios de evaluaci´ on y entre los factores de riesgo considerados y los obst´ aculos enfrentados, lo que indica que existe espacio para optimizar a´ un m´ as los proyectos de reubicaci´ on.
Palabras Clave: colonizaci´on asistida, distribuci´on geogr´afica, refuerzo, reintroducci´on, remplazo ecol´ogico
Introduction Conservation translocations are the intentional humanmitigated movement of organisms from one area for free-release into another for conservation purposes (IUCN/SSC 2013) and are increasingly used to mitigate human effects on biodiversity (Seddon et al. 2007; Bajomi et al. 2010). Historic translocations were frequently sporadic trial-and-error attempts that yielded a valuable foundation for subsequent refinements. Recent exponential increases in conservation translocations have been associated with improved planning and practice; release decisions are now more frequently embedded within decision-theory or adaptive-management frameworks, assisted by elaborate release-site selection or preparation, and executed using increasingly sophisticated selection, preparation, training, and support techniques for released individuals (Moehrenschlager & Lloyd 2016). Yet, conservation translocations can be risky (Seddon et al. 2010; Sainsbury & Vaughan-Higgins 2012), expensive (Bowkett 2009; Weise et al. 2014), and timeconsuming (Lewis et al. 2012), suggesting that translocation efforts should be allocated where there is greatest need and highest likelihood for success. Conservation translocations are of 4 types: reintroduction, reinforcement, assisted colonization, and ecological replacement. Reintroduction, “the intentional movement and release of an organism inside its indigenous range from which it has disappeared” (IUCN/SSC 2013), has received considerable attention in the literature (Armstrong & Seddon 2007; Godefroid et al. 2011). Reinforcement is “the intentional movement and release of an organism into an existing population of conspecifics”; assisted colonization is “the intentional movement and release of an organism outside its indigenous range to avoid extinction of populations of the focal species”; and ecological
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replacement is “the intentional movement and release of an organism outside its indigenous range to perform a specific ecological function” (IUCN/SSC 2013). Conservation translocations are different from other translocations because their overall objective is a measurable conservation benefit at a population, species, or ecosystem level (IUCN/SSC 2013). Nonetheless, motivating factors are likely complex and generally unpublished. Similarly, metrics for conservation translocation success are variable and not standardized (Seddon 1999; Robert et al. 2015), but assessments of conservation translocation success remain critical for refinement of this intensive species management option. Recent reviews of conservation translocations focus primarily on reintroductions and examine issues of taxonomic bias (Seddon et al. 2005; Bajomi et al. 2010), genetics and disease (Deredec & Courchamp 2007; Laikre et al. 2010), captive breeding (Letty et al. 2007; Jule et al. 2008), and evaluations of translocation success (Griffith et al. 1989; Fischer & Lindenmayer 2000; Godefroid et al. 2011). Many have identified a need to develop vigorous experimental approaches, clear definitions, and measurement tools for project goals (e.g., Seddon et al. 2007) and a more systematic approach to evaluation (e.g., Moehrenschlager et al. 2013). Yet, translocations are difficult to evaluate. The ultimate goal of reintroductions is to attain long-term persistence without human intervention (Seddon 1999). However, translocations are often evaluated based on the survival and reproduction of translocated individuals or on an increase in population size, even though these criteria do not necessarily imply a selfsustaining population (Wolf et al. 1998). Consequently, perceived success is also used to evaluate translocations (Soorae 2008, 2010, 2011, 2013). Previous reviews show that for conservation translocations, habitat quality, location of release, total number of released individuals, and
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the source population of translocated individuals (wild vs. captive) are influential factors (Griffith et al. 1989; Wolf et al. 1998; Fischer & Lindenmayer 2000). We combined a comprehensive literature review of animal conservation translocations in North America with an online survey of relevant authors to examine how well the allocation of translocation efforts reflects conservation need and likelihood of success. Focusing on North America, the region with the largest number of conservation translocations after Oceania (Fischer & Lindenmayer 2000; Seddon et al. 2014), we examined the geographic and taxonomic distributions of conservation translocations at a state or provincial and country scale and explored motivations and outcome evaluations. Specifically, we used the literature review to examine the prevalence of conservation translocations, what species are being moved, and where translocations are conducted and to explore how increased conservation translocation activity relates to local and international threat status (proxy for conservation need). We then surveyed authors to examine perceived translocation success within the context of alignment with project goals. By combining a literature review with an author survey, we sought to provide a broad perspective on conservation translocation efforts in North America that would allow us to identify areas for improvement and future research.
Methods Literature Review We used systematic review techniques (Collaboration for Environmental Evidence 2013) to examine the published literature on conservation translocations. Although recognizing that no data set is ever complete given the continual increase in publications (Mabe & Amin 2001), we collected as many papers on conservation translocations as possible by using inclusive search terms in 2 literature search engines: Thomson Reuters Web of Science and Academic Search Complete. In both search engines, we scanned all papers from the earliest available record to December 2013. Some papers may have been missed by our search, and the published literature may not reflect all conservation translocations, but the literature we searched is likely a good and representative proxy. We divided search terms into 3 categories: terms related to conservation translocations, motive, and geographic area (Supporting Information). We used or to join search terms within categories and and to relate search terms between categories. We considered Central America and the Caribbean (CAC) part of North America and thus included relevant geographic search terms for the entire study area. All hits reported by the 2 search engines were imported into Endnote X6 (Thompson Reuters, New York 2012) referencing software. Then, we manually screened
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them to verify relevance to North American conservation translocations. We eliminated articles from the study if they were not relevant to conservation translocations based on their title or abstract or upon further examination of the paper. We also excluded the 295 articles for which we could not obtain abstracts or the full text to verify relevance. We then imported all relevant articles into a database (Microsoft Access 2013) and collected further information from each: article type (peer-reviewed journal, book, magazine, newspaper, newsletter, report, or conference proceeding), species’ source and release locations (at the level of country, province, or state and exact location), source of release population (captive or wild), and type of paper (review, animal release study, proposal, theoretical or experimental study, or monitoring study). We classified articles into the 4 types of conservation translocations: reintroductions, reinforcements, assisted colonizations, and ecological replacements. The use of established definitions for conservation translocations is important to minimize confusion in the literature (Dalrymple & Moehrenschlager 2013). We therefore used the definitions in the International Union for Conservation of Nature (IUCN) Species Survival Commission (SSC) (2013) guidelines for reintroductions and other conservation translocations. Given the alternate definitions of conservation-translocation terms sometimes used in the literature, there may be differences between how we classified a translocation and the terms authors used in their papers. To examine the geographic distribution of conservation translocations across North America, we mapped the number of species for which a reintroduction or reinforcement was performed in each province or state in Canada, the United States, and Mexico. Mapping in CAC was done at the country level. For all articles, we attempted to identify the exact location of release. If the exact location was not available, we used the province or state level for grouping in Canada, the United States, and Mexico and country level for grouping in CAC. If the location of a release was a protected area spanning several states (e.g., Yellowstone National Park) and no additional information on the release location was provided, we associated the reintroduction or reinforcement with the state or province in which the largest area of the protected area was located (e.g., wolves [Canis lupus] reintroduced to Yellowstone National Park were mapped in Wyoming). This procedure was pertinent for 10% of articles. We then used Pearson’s correlation to explore geographic overlap between the number of reintroductions and reinforcements in each state or province in the United States, Mexico, and Canada and for each country in CAC. We did not map or perform these tests for assisted colonizations and ecological replacements because of the limited sample size for these types of translocations in our database.
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To determine whether the number of translocations was proportional to the number of listed species and thus whether translocations reflect conservation need, we determined the international threat status of all species translocated in our database and the total number of species listed as imperiled within each jurisdiction. Species were deemed internationally threatened if listed as vulnerable, endangered, critically endangered, extinct in the wild, or extinct on the 2014 IUCN Red List (IUCN 2015). Using Pearson’s correlation, we examined the correlation between the total number of internationally threatened species present and the number of internationally threatened species translocated within each country. In Canada and the United States, we determined the provincial- or state-level threat status of translocated species and the total number of species listed within each province or state. We used the Species At Risk Act (2015) (SARA) to determine species’ provincial threat designation for all translocations in Canada and the U.S. Endangered Species list (US Fish & Wildlife Service 2015) to determine species’ state threat designation for all translocations in the United States. We simplified U.S. threat designations to general threat status. For example, we considered species listed as endangered and experimental nonessential populations as simply endangered. We then computed a Pearson correlation between the number of species involved in reintroductions (regardless of success, hereafter reintroduction species) or reinforcements (hereafter reinforcement species) and the number of species at risk in each state or province. We were unable to determine the national status of species in Canada and the United States because, for most species, threat status varies across jurisdictions. For example, northern leopard frogs (Rana pipiens) in Canada are listed as endangered in British Columbia, of special concern in the Northwest Territories, Alberta, Saskatchewan, and parts of Manitoba, and not at risk in the rest of Canada under SARA. Online Survey To better understand the motivations and outcomes of conservation translocations, we invited authors of the studies we reviewed to participate in an online survey (Survey Monkey 2013). We selected 330 authors from our review database to participate in the survey. They were the contact authors for articles published from 2000 to 2013. We used this period because contact information from before 2000 was likely inaccurate (total 1301 articles). We then eliminated articles that did not have an email address for any author (836 articles remaining). We narrowed our selection to articles that either described an actual translocation (e.g., authors specifically said they translocated x number of individuals) or focused on monitoring a translocated population and provided details on the translocation process
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North American Translocation Efforts
(379 articles). Because one author may have published several papers, we removed duplicates from our list of authors (leaving 330 authors). Only one author per paper was contacted. The purpose of the survey was disclosed to authors upon initial contact, and author’s participation was voluntary. Although participants did not sign a consent form, consent was obtained by virtue of survey completion in accordance with the University of St Andrews guidelines for online surveys and questionnaires (Hearn 2016). Our 15-question survey asked authors about criteria underlying their choice of species and release locations, as well as their monitoring strategies, translocation evaluation, and obstacles to translocations (Supporting Information). Authors could choose multiple responses from a choice of answers and were asked to explain their answers in a comments box. If the translocation involved more than one species, authors were asked to complete separate surveys on each species. We asked authors to self-evaluate success of their conservation translocations as highly successful, successful, partially successful, failure, on-going, or do not know, which are the same terms used in the Reintroduction Specialist Group’s Global Reintroduction Perspectives books (Soorae 2008, 2010, 2011, 2013). We did not provide a definition for each level of success. No uniformly agreed-upon measures of success exist for conservation translocations, and commonly used definitions vary in scale, from an individual level (survival of released individuals and their successful breeding and contribution to future generations), to the population level (long-term persistence of a reestablished population), to the species level (downlisting) (Seddon 1999; Moehrenschlager et al. 2013). Even when success is defined as the establishment of a self-sustaining population (e.g. in Griffith et al. 1989; Fischer & Lindenmayer 2000), considerable subjectivity remains unless self-sustaining is defined based on standardized demographic metrics on a species-specific basis. Moreover, measures of success need to reflect the initial goal of the study, and each project must be assessed individually. We therefore refrained from imposing a fixed definition of success and used perceived success instead. The order of questions in our survey aimed to capture the alignment between motivations, methods, evaluation criteria, and perceived success by requiring authors to reflect on the former elements of their study before selfevaluating the success of their translocation. Ultimately, we categorized survey responses as successful projects (self-evaluated as highly successful and successful), partially successful, and failures. To assess alignment between translocation goals and evaluation criteria, for each level of success we first crosstabulated responses on motivating factors and measures of success, excluding goals and success levels with sample sizes less than 5 to avoid misrepresentation in the data. We also cross-tabulated factors influencing release site
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selection and reported obstacles to success to examine the effectiveness of translocation strategies. We grouped factors into important factors if considered highly important or important, and unimportant factors if listed as of minor importance, unimportant, or not considered by survey participants. We used Spearman’s rank correlations to examine the alignment between threat, efforts, and perceived success and examined the relationships between each species’ IUCN Red List status (ranked from 1, not assessed, to 6, critically endangered) and the number of released individuals; the number of released individuals or number of years releases occurred and translocation success for each taxon; and each species’ IUCN Red List status and translocation success (ranked from 1, failure, to 4, highly successful).
Results Literature Review Our search of the 2 databases yielded 35,742 articles (including duplicates), 18,110 from the ISI Web of Knowledge database from 1955 to December 2013 and 17,632 from the Academic Search Complete database from 1904 to December 2013. We deemed 1863 articles relevant to conservation translocations. These articles came from 512 different sources: peer-reviewed journals (47% of all sources), magazines (20%), conference proceedings (14%), books (9%), reports (5%), newsletters (4%), and newspaper articles (1%). The number of articles discussing conservation translocations increased over 40 years for all taxa (Fig. 1). Articles on reintroductions dominated the literature (1304 articles on 139 species), followed by articles on reinforcements (498 on 129 species). We found 29 articles on assisted colonizations: 19 theoretical papers and 10 describing the release of 6 species, all in the United States. Released species included fringed darter (Etheostoma crossopterum) in Illinois, gopher tortoise (Gopherus polyphemus) in Georgia, wood frog (Rana sylvatica) in Illinois, Wild Turkey (Meleagris gaallopavo) in South Dakota and Minnesota, ornate box turtle (Terrapene ornata ornata) in Iowa, and white sands pupfish (Cyprinodon tularosa) in New Mexico (the latter 2 were experimental releases). We also found 2 articles on ecological replacements pertaining to 2 species: the potential release of Greater Prairie-Chicken (Tympanuchus cupido) to replace the extinct Heath Hen (Tympanuchus cupido cupido) in Massachusetts and the release of the Yellow-crowned Night Heron (Nyctanassa violacea) in Bermuda to replace the endemic Bermuda Night Heron (Nyctanassa carcinocatactes). Although these assisted colonizations and ecological replacements are of interest due to their novelty and increasing prevalence, we
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focused primarily on the larger sample of reintroduction and reinforcement translocations. Publications covered considerable taxonomic breadth. Conservation translocations were undertaken or considered for 279 different species (Supporting Information). We found more publications on mammals and birds (1283) than on herpetofauna, invertebrates, and fish (416). Articles were published on 71 different species of birds, 58 species of mammals, 55 species of fish, 52 species of herpetofauna, and 43 species of invertebrates. Geographically, reintroductions and reinforcements were more frequent and widely distributed in the United States than in Canada, Mexico, and CAC (Fig. 2). One hundred forty-two articles on 62 species were published in the Mexico and CAC, 136 articles on 40 species were published in Canada, and 1339 articles were published in the United States on 215 species. Moreover, there was spatial overlap between the number of reintroductions and reinforcements in the United States at state-level resolution (r = 0.549, p
