Philip J. Seddon

Reversing defaunation: Restoring species in a changing world

The rate of biodiversity loss is not slowing despite global commitments, and the depletion of animal species can reduce the stability of ecological communities. Despite this continued loss, some substantial progress in reversing defaunation is being achieved through the intentional movement of animals to restore populations. We review the full spectrum of conservation translocations, from reinforcement and reintroduction to controversial conservation introductions that seek to restore populations outside their indigenous range or to introduce ecological replacements for extinct forms. We place the popular, but misunderstood, concept of rewilding within this framework and consider the future role of new technical developments such as de-extinction.

Persistence without intervention: assessing success in wildlife reintroductions.

Wildlife reintroductions proceed from a seductively simple assumption: by releasing individuals of a species into a suitable habitat it is possible to restore natural biodiversity. Not surprisingly, therefore, the release of animals to re-establish populations of endangered or threatened species is becoming increasingly common. By 1998 the World Conservation Union (IUCN)/Species Survival Commission’s Reintroduction Specialist Group (RSG) had current projects listed for over 200 animal species. The RSG issued a set of reintroduction guidelines in 1998, in which it defines reintroduction as: ‘… an attempt to establish a species in an area which was once part of its historical range …’1xGuidelines for Re-introductions. IUCN. See all References1. The definition goes on to state that ‘re-establishment … is a synonym, but implies that the reintroduction has been successful’1xGuidelines for Re-introductions. IUCN. See all References1. This raises a fundamental question common to all reintroduction attempts: by what criteria should we assess success – or should we even try?There is no general agreement on what constitutes a successful reintroduction, although a variety of definitions of success have been discussed. These definitions include: breeding by the first wild-born generation2xSarrazin, F. and Barbault, B. Trends Ecol. Evol. 1996; 11: 474–478Abstract | Full Text PDF | PubMed | Scopus (240)See all References2; a three-year breeding population with recruitment exceeding adult death rate2xSarrazin, F. and Barbault, B. Trends Ecol. Evol. 1996; 11: 474–478Abstract | Full Text PDF | PubMed | Scopus (240)See all References2; an unsupported wild population of at least 500 individuals3xBeck, B.B. et al. : 265–286CrossrefSee all References3; or the establishment of a self-sustaining population4xGriffith, B. et al. Science. 1989; 245: 477–480Crossref | PubMedSee all References4. An immediate problem is that variation in life history traits between target species will limit the general usefulness of any one criterion.The 7th World Conference on Breeding Endangered Species, held in Cincinnati in May 1999, aimed to link zoos and field conservation through an ambitious series of working groups addressing a range of current issues. One group considered the post-release phase of reintroductions, where a key topic was how best to assess success.A major problem with defining a reintroduction as a success or a failure is that, by any criteria, this definition is limited in time. If the aim is to establish a self-sustaining population, then a given project can be said to have achieved its aim (i.e. be successful) only at the time at which the assessment was made. Self-sustainability does not necessarily mean long-term persistence. A review of the changing status of reintroduction attempts over a five-year period found that four out of 74 projects (5%) categorized as successful in 1987, had declining populations by 1993 (Ref. 5xWolf, C.M. et al. Conserv. Biol. 1996; 10: 1142–1154Crossref | Scopus (375)See all ReferencesRef. 5). The danger of classifying a reintroduction as successful is that it implies an end-point beyond which further effort, in the form of new releases or monitoring, might be deemed unnecessary. Population viability analyses estimate extinction probabilities over periods of hundreds of years, thus ‘failure’ of apparently ‘successful’ projects after only five years is of concern. Demographic stochasticity affecting small populations, and environmental variation acting on larger populations6xMay, R.M. Symp. Zool. Soc. London. 1991; 62: 145–163See all References6, will mean that a reintroduction can be considered successful only at a given point in time. In addition, new threats might arise. A recent example is given by the re-establishment of Arabian oryx in the Sultanate of Oman, considered to be one of the reintroduction success stories6xMay, R.M. Symp. Zool. Soc. London. 1991; 62: 145–163See all References6. Almost two decades after the first releases of oryx, an epidemic of poaching over a three-year period rendered the free-ranging oryx population no longer viable7xGorman, M. Nature. 1999; 398: 190Crossref | Scopus (6)See all References7.The consensus of the Cincinnati group was that the end-point categorization of a reintroduction as a success was misleading and potentially deleterious. Although the goal of any reintroduction might be reasonably stated as establishment of a self-sustaining population, this is not a criterion for success. Instead, we could consider any reintroduction as comprising a sequence of three objectives: the survival of the release generation; breeding by the release generation and their offspring; and persistence of the re-established population, perhaps assessed through extinction probability modelling. Long-term post-release monitoring is essential to track these demographic parameters. However, this does not mean that once animals have been released, programme managers become impartial observers; but what level of post-release intervention is acceptable?Reintroductions have been viewed as a means to restore free-living populations in as natural a state as possible. Consequently, it has been stated that releases should not take place until certain conditions have been fulfilled, for example, restoration of habitat and removal of the causes of initial population declines1xGuidelines for Re-introductions. IUCN. See all References1. It is important, however, to consider the potential benefits that might be gained by releasing animals. Released animals might increase natural biodiversity, fulfil a role as keystone components of an ecosystem, and/or create the public and political support necessary to undertake habitat restoration or to put species protection measures in place. It can be beneficial, or even necessary, to release individuals before all formal pre-release criteria have been met.This implies that some form of post-release management could be required. It would be ideal to release a group of animals that survive, breed and thereby establish a self-sustaining population with a high probability of persistence in the long-term – all without post-release support. However, it is evident, particularly when releasing captive-bred animals, that it is unreasonable to expect survival and persistence without some degree of post-release care. Fragmentation of suitable habitat will exacerbate matters and, in the case of highly endangered flagship or keystone species, high intensity post-release intervention (e.g. supplementary feeding, veterinary care or predator control) is clearly warranted, even over the long-term. This re-emphasizes the importance of post-release monitoring, not only to evaluate the current status of the re-established population, but also to regularly assess the degree of intervention necessary to achieve population persistence. The ultimate objective of any reintroduction is population persistence without intervention, but this is a state, not a result, and is assessable only through long-term, post-release monitoring.

Taxonomic bias in reintroduction projects

Taxonomic bias has been documented in general science and conservation research publications. We examined whether taxonomic bias is similarly severe in actual conservation programmes as indicated by the focus of species reintroduction projects worldwide. We compiled a database of reintroduction projects worldwide, yielding a total of 699 species of plants and animals that are the focus of recent, current or planned reintroductions. Using IUCN (World Conservation Union) data for total numbers of known species worldwide, we found that vertebrate projects were over-represented with respect to their prevalence in nature. Within vertebrates, mammals and, to a lesser extent, birds, were over-represented, whereas fish were under-represented. This over-representation extended to two mammal orders, artiodactylids and carnivores, and to four bird orders, anseriforms, falconiforms, gruiforms and galliforms. For neither mammals nor birds was reintroduction project bias related to any differences between orders in vulnerability to threat. Bird species that are the focus of reintroduction efforts are more likely to be categorised as ‘Threatened’ than expected on the basis of the distribution of all known species over all threat categories, however, nearly half of all bird species being reintroduced are classified as ‘Least Concern’. The selection of candidates for reintroduction programmes is likely to consider national priorities, availability of funding and local community support, over global conservation status, While a focus on charismatic species may serve to garner public support for conservation efforts, it may also divert scarce conservation resources away from taxa more in need of attention.

Invasive mammal eradication on islands results in substantial conservation gains.

Significance Global conservation actions to prevent or slow extinctions and protect biodiversity are costly. However, few conservation actions have been evaluated for their efficacy globally, hampering the prioritization of conservation actions. Islands are key areas for biodiversity conservation because they are home to more than 15% of terrestrial species and more than one-third of critically endangered species; nearly two-thirds of recent extinctions were of island species. This research quantifies the benefits to native island fauna of removing invasive mammals from islands. Our results highlight the importance of this conservation measure for protecting the worlds most threatened species. More than US

Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans

21 billion is spent annually on biodiversity conservation. Despite their importance for preventing or slowing extinctions and preserving biodiversity, conservation interventions are rarely assessed systematically for their global impact. Islands house a disproportionately higher amount of biodiversity compared with mainlands, much of which is highly threatened with extinction. Indeed, island species make up nearly two-thirds of recent extinctions. Islands therefore are critical targets of conservation. We used an extensive literature and database review paired with expert interviews to estimate the global benefits of an increasingly used conservation action to stem biodiversity loss: eradication of invasive mammals on islands. We found 236 native terrestrial insular faunal species (596 populations) that benefitted through positive demographic and/or distributional responses from 251 eradications of invasive mammals on 181 islands. Seven native species (eight populations) were negatively impacted by invasive mammal eradication. Four threatened species had their International Union for the Conservation of Nature (IUCN) Red List extinction-risk categories reduced as a direct result of invasive mammal eradication, and no species moved to a higher extinction-risk category. We predict that 107 highly threatened birds, mammals, and reptiles on the IUCN Red List—6% of all these highly threatened species—likely have benefitted from invasive mammal eradications on islands. Because monitoring of eradication outcomes is sporadic and limited, the impacts of global eradications are likely greater than we report here. Our results highlight the importance of invasive mammal eradication on islands for protecting the worlds most imperiled fauna.

Pollution, habitat loss, fishing, and climate change as critical threats to penguins

Animal populations are increasingly challenged by anthropogenic environmental changes. Species, populations and individuals vary in their ability to cope with exposure to human proximity. However, little is known about what drives habituation or sensitization in wild populations. Via behavioural observations and heart rate telemetry during experimental disturbance, we determined the habituation potential of yellow-eyed penguins, Megadyptes antipodes , a key species for nature-based tourism in southern New Zealand. Individual birds differed significantly in both their initial stress response and habituation potential. While some birds did not habituate, or even appeared to be sensitized by frequent disturbance, others habituated. Individual variation in habituation potential depended on previous experience with humans, sex and character (i.e. timid, calm or aggressive). Birds that were exposed to research that involved frequent interactions at the nest site, including blood sampling, several years prior to our experiments were less likely to habituate. Overall, females were more flexible than males in their stress response pattern, and calm individuals appeared to adapt more readily than aggressive birds. Character, classified during penguin–researcher interactions at the nest site, was independent of sex, age or previous experience, and was consistent over two seasons. Initial heart rate response to human approach, also similar between seasons, varied with sex and character of an individual. Yellow-eyed penguins may habituate to short and consistent approaches, but appear unsuitable for unregulated tourist visits at nest sites. Individual differences in habituation potential to human disturbance can have fitness consequences and may lead to contemporary evolutionary change in the composition of breeding populations.

Reintroducing resurrected species: selecting DeExtinction candidates

Cumulative human impacts across the worlds oceans are considerable. We therefore examined a single model taxonomic group, the penguins (Spheniscidae), to explore how marine species and communities might be at risk of decline or extinction in the southern hemisphere. We sought to determine the most important threats to penguins and to suggest means to mitigate these threats. Our review has relevance to other taxonomic groups in the southern hemisphere and in northern latitudes, where human impacts are greater. Our review was based on an expert assessment and literature review of all 18 penguin species; 49 scientists contributed to the process. For each penguin species, we considered their range and distribution, population trends, and main anthropogenic threats over the past approximately 250 years. These threats were harvesting adults for oil, skin, and feathers and as bait for crab and rock lobster fisheries; harvesting of eggs; terrestrial habitat degradation; marine pollution; fisheries bycatch and resource competition; environmental variability and climate change; and toxic algal poisoning and disease. Habitat loss, pollution, and fishing, all factors humans can readily mitigate, remain the primary threats for penguin species. Their future resilience to further climate change impacts will almost certainly depend on addressing current threats to existing habitat degradation on land and at sea. We suggest protection of breeding habitat, linked to the designation of appropriately scaled marine reserves, including in the High Seas, will be critical for the future conservation of penguins. However, large-scale conservation zones are not always practical or politically feasible and other ecosystem-based management methods that include spatial zoning, bycatch mitigation, and robust harvest control must be developed to maintain marine biodiversity and ensure that ecosystem functioning is maintained across a variety of scales.

Conservation short cut, or long and winding road? A critique of umbrella species criteria

Technological advances have raised the controversial prospect of resurrecting extinct species. Species DeExtinction should involve more than the production of biological orphans to be scrutinized in the laboratory or zoo. If DeExtinction is to realize its stated goals of deep ecological enrichment, then resurrected animals must be translocated (i.e., released within suitable habitat). Therefore, DeExtinction is a conservation translocation issue and the selection of potential DeExtinction candidates must consider the feasibility and risks associated with reintroduction. The International Union for the Conservation of Nature (IUCN) Guidelines on Reintroductions and Other Conservation Translocations provide a framework for DeExtinction candidate selection. We translate these Guidelines into ten questions to be addressed early on in the selection process to eliminate unsuitable reintroduction candidates. We apply these questions to the thylacine, Yangtze River Dolphin, and Xerces blue butterfly.

The Risks of Assisted Colonization

Conservation planners often seek short cuts when making decisions about land use by directing management towards one or a few species that will benefit the wider ecosystem. The umbrella species concept is one such pro- posed short cut. An umbrella species comprises a population of individuals of a particular species whose resource re- quirements and habitat needs encompass the sufficient home ranges and resource needs of viable populations of co-occurring species. We examined the 17 published criteria available to identify a potential umbrella species and recommend that conservation managers wishing to apply this concept could focus on only seven criteria: well-known biology; large home range size; high probability of pop- ulation persistence; co-occurrence of species of conserva- tion interest; management needs that are beneficial to co-occurring species; sensitivity to human disturbance; and ease of monitoring. We note however, that rigorous assessment of candidate umbrella species requires such detailed knowledge of candidate and co-occurring species that it seems less of a short cut than planners may wish.

EFFECTS OF HATCHING ORDER, SIBLING ASYMMETRIES, AND NEST SITE ON SURVIVAL ANALYSIS OF JACKASS PENGUIN CHICKS

There is a growing debate over whether species should be translocated outside their historic ranges to deal with extinction risks as habitats shift due to climate change. This idea of taking preemptive action to avert predicted extinction risks has been given emphasis by the recent International Union for Conservation of Nature (IUCN) assessment of species susceptibility to climate-change impacts (Foden et al. 2008), prompting suggestions that “more aggressive measures, such as so-called ‘assisted migration’” be considered (Marris 2008). Hoegh-Guldberg et al. (2008) provide a decision framework for identifying scenarios in which what they term “assisted colonization” (AC) is justified. We see problems with the impact of these articles, despite their conservative approach. First, there are current international translocation guidelines (IUCN 1998) that provide a strong rationale against the early adoption of AC as a conservation tool. The Reintroduction Specialist Group (RSG) was created in 1988 to address the proliferation of ill-conceived translocations that had been taking place, including many releases of species outside historic ranges (Stanley Price & Soorae 2003). The RSG formulated the guidelines for translocation planning to ensure that conservation benefits accrue. “Benign introduction” (BI)—the translocation of species to suitable habitat outside their historic range as a conservation measure—was considered appropriate only when there was no habitat left within the original species range (IUCN 1998). Although AC appears to fall within the definition of BI, the two differ in that AC aims proactively to establish species outside their historic range to preempt predicted climate-driven changes in habitat suitability. Calls to take proactive conservation measures need to consider that there are currently huge uncertainties involved, not only in climatechange predictions and consequent species responses (Araújo et al. 2005; Hulme 2005; Sekercioglu et al. 2008) but also in our understanding of the habitat requirements of species (Stamps & Swaisgood 2007) and the effects of translocations on ecosystem function (Armstrong & Seddon 2008). At a recent conference (First International Wildlife Reintroduction Conference, Lincoln Park Zoo, Chicago, Illinois,April2008, http://www. reintroduction.org/), RSG members discussed climate-change implications for translocations, acknowledging the need for the integration of reintroduction biology and restoration ecology, and the updating of translocation guidelines to consider issues such as the mitigation of climate-driven habitat change and overcoming barriers to natural dispersal of species. Given current uncertainty, however, there is substantial risk that prematurely embracing the undeniably sexy AC concept will initiate a new era of ill-conceived species translocations. Philip J. Seddon,∗ Doug P. Armstrong,† Pritpal Soorae,‡ Frederic Launay,§ Sally Walker,∗∗ Carlos R. Ruiz-Miranda,†† Sanjay Molur,∗∗ Heather Koldewey,‡‡ and Devra G. Kleiman§§ ∗RSG Bird Section Chair, Department of Zoology, University of Otago, Dunedin, New Zealand, email philip.seddon@stonebow. otago.ac.nz †RSG Australasia Chair, Massey University, Palmerston North, New Zealand ‡RSG Programme Officer, Environment Agency, Abu Dhabi, United Arab Emirates §RSG Chair, Environment Agency, Abu Dhabi, United Arab Emirates ∗∗RSG South Asia co-Chair, Zoo Outreach, Coimbatore, India ††RSG Meso-South America Chair, Environmental Sciences Laboratory, Universidade Estadual do Norte Fluminense, Rio de Janeiro, Brazil ‡‡RSG Fish Section Chair, Zoological Society of London, London, United Kingdom §§RSG North America Chair, Zoo-Logic, Chevy Chase, MD 20815, U.S.A.