Refugee Species Research Articles

Continental‐scale identification and prioritisation of potential refugee species; a case study for rodents in Australia

A species is expected to be most resilient to environmental change when it occurs across a broad diversity of habitats. However, there is often no visual representation of the past (i.e. prehistoric and historical) context for a species in the range maps published by national and global authorities. Therefore, it is easy to overlook the fact that many species once occupied a broader geographic range, or greater diversity of habitats. Such oversights hinder the effective conservation of species that have become restricted to a subset of their formerly occupied habitats. Here, we quantified the shifted baseline that may underpin some of the ecological misconceptions about species, and developed a rapid assessment method to aid the identification and prioritisation of ‘potential refugee species' (i.e. species that have become restricted to a subset of their formerly occupied niche). The assessment of potential refugee status is different from, but complementary to, the International Union for Conservation of Nature (IUCN) Red List and Green Status frameworks. Our framework defines a continuum of potential refugee status, which was demonstratable in continent‐scale maps drawn from biogeographic regionalisation. Applying this framework to all native rodent species across the continent of Australia (a group that has suffered several extinctions and notable declines), we found that the risk of ecological misconceptions caused by shifted baselines (i.e. resulting from ‘shifting baseline syndrome') was prevalent. This suggests that in many cases, translocation opportunities that might be avoided because they are perceived as conservation introductions (as defined by the IUCN translocation guidelines), may in fact fall within the indigenous range, and should therefore be considered reasonable reintroductions. Ultimately, our potential refugee assessment framework will help to facilitate the undertaking of ambitious translocations that will build species' resilience to environmental change by resuming their adaptation to habitats across all formerly occupied bioregions.

Food patch selection by the largest European herbivore

AbstractThe scaling relationship between digestive system and body mass shapes foraging strategies in herbivores. The Jarman–Bell principle and the forage maturation hypothesis (FMH), two of the most important predictions formulated in herbivore foraging ecology, have been used to explain this relationship.We aimed to test these predictions for the largest European herbivore—the European bison-which is highly sexually dimorphic and recognised as a refugee species in non-optimal forest habitats. We conducted our study in the Białowieża Primeval Forest, where the European bison has been recognized as a refugee species. We estimated vegetation quality and biomass along the foraging paths of male and female European bison, and the vegetation biomass at random points in different habitats and months. We found no support for the Jarmann-Bell principle at the intraspecific level in European bison, as males and females foraged on patches of similar crude protein and fibre content. However, females selected for higher biomass. The quality of vegetation on the bison foraging patches showed a significant spatio-temporal variation. It increased from May to July and then gradually decreased. It also increased with the fertility and wetness of the habitats being the highest in wet forests. Mean biomass on European bison foraging patches (131.5 g/m2), was significantly lower than on random plots (210.5 g/m2), which supported the FMH. Our study suggests that in rich forest habitats, the abundant food resources available in summer may not constrain the metabolic rate/gut capacity ratio of either sex, potentially leading to dietary segregation. In contrast to open habitats, where vegetation maturation is less temporally variable, European bison in rich forest habitats may optimise patch selection and energy intake by tracking a habitat- and species-specific changes in the plant phenology. Understanding the relationship between European bison forage selection and forage nutritional constraints in forest habitats may be critical for conservation programmes, as European bison are better adapted to more open habitats and are recognised as refugee species in suboptimal forest habitats.

Going back for the future: Incorporating Pleistocene fossil records of saiga antelope into habitat suitability models

AbstractAimMany species have suffered anthropogenic range contraction and no longer occupy all available suitable environmental conditions. This is particularly problematic for the construction of habitat suitability models (HSMs), which assume that a species' contemporary range reflects its full species–environment relationship. HSMs therefore risk underestimating suitable environment areas, and misinforming conservation decisions. Incorporating historic (centuries‐old) records partly reduces this bias, but even these records are also subject to human disturbance. We incorporated fossil records of the critically endangered saiga antelope (Saiga tatarica, L., 1776), alongside historic and current records, into current and future habitat suitability models. Saiga has experienced drastic range contraction and may have a truncated species–environment relationship. The results allowed us to test whether its current habitat provides optimal environmental conditions, or whether saiga should be considered a refugee species.LocationNorthern Hemisphere.TaxonSaiga tatarica (Bovidae, Artiodactyla).MethodsWe collated historic and fossil saiga occurrence records from published literature, museum archives and global databases. Modern occurrence records were obtained from the International Union for Conservation of Nature Red List assessment. Four bioclimatic variables were downloaded from Worldclim.org. HSMs were generated through Maxent, using the maxnet package in R. Three HSMs were developed: present only, present historic and present fossil. Each of these models was projected onto current and two future (2070) climate change scenarios.ResultsSaiga fossil records increased the predicted suitable environment area by 783% and 1416% for current and future climate projections respectively. Our results suggest the saiga is not a refugee species but occupies only a portion of its potential environmental niche. The saiga's contemporary range is predicted environmentally suitable throughout all models and projections, and therefore in situ conservation management is recommended.Main ConclusionsThis study highlights the importance of incorporating fossil records into HSMs to better understand species–environment relationships and develop more robust conservation strategies for appropriate endangered species.

Potential changes in the extent of suitable habitats for geladas (Theropithecus gelada) in the Anthropocene

BackgroundClimate change coupled with other anthropogenic pressures may affect the extent of suitable habitat for species and thus their distributions. This is particularly true for species occupying high-altitude habitats such as the gelada (Theropithecus gelada) of the Ethiopian highlands. To explore the impact of climate change on species distributions, Species Distribution Modelling (SDM) has been extensively used. Here we model the current and future extent of sutibale habitat for geladas. Our modelling was based on 285 presence locations of geladas, covering their complete current distribution. We used different techniques to generate pseudoabsence datasets, MaxEnt model complexities, and cut-off thresholds to map the potential distribution of gelada under current and future climates (2050 and 2070). We assembled maps from these techniques to produce a final composite map. We also evaluated the change in the topographic features of gelada over the past 200 years by comparing the topography in current and historical settings.ResultsAll model runs had high performances, AUC = 0.87–0.96. Under the current climate, the suitable habitat predicted with high certainty was 90,891 km2, but it decreased remarkably under future climates, -36% by 2050 and − 52% by 2070. However, since the habitats of geladas already extend to mountaintop grasslands, no remarkable range shifts across elevation gradients were predicted under future climates.ConclusionsOur findings indicated that climate change most likely results in a loss of suitable habitat for geladas, particularly south of the Rift Valley. Currently geladas are confined to higher altitudes and steep slopes compared to historical sightings, probably qualifying geladas as refugee species. The difference in topography is potentially associated with anthropogenic pressures that drove niche truncation to higher altitudes, undermining the climatic and topographic niche our models predicted. We recommend protecting the current habitats of geladas even when they are forecasted to become climatically unsuitable in the future, in particular for the population south of the Rift Valley.

Embracing change: Invasive species and novel ecosystems

Combining ecological and socio-cultural analysis, we propose embracing the future-oriented concept of novel ecosystems. This perspective offers an alternative to the backwards-looking conservation attitude that uses metaphors of biological invasion, for example. With the case study of species whose range is shifting to include cities, we show that in a world of environmental novelty, effective conservation thinking must supplement narratives of invasive species with those about climate refugee species and novel ecosystems.

Contrasting ecological information content in whaling archives with modern cetacean surveys for conservation planning and identification of historical distribution changes.

Many species are restricted to a marginal or suboptimal fraction of their historical range due to anthropogenic impacts, making it hard to interpret their ecological preferences from modern-day data alone. However, inferring past ecological states is limited by the availability of robust data and biases in historical archives, posing a challenge for policy makers . To highlight how historical records can be used to understand the ecological requirements of threatened species and inform conservation, we investigated sperm whale (Physeter macrocephalus) distribution in the Western Indian Ocean. We assessed differences in information content and habitat suitability predictions based on whale occurrence data from Yankee whaling logs (1792-1912) and from modern cetacean surveys (1995-2020). We built maximum entropy habitat suitability models containing static (bathymetry-derived) variables to compare models comprising historical-only and modern-only data. Using both historical and modern habitat suitability predictions we assessed marine protected area (MPA) placement by contrasting suitability in- and outside MPAs. The historical model predicted high habitat suitability in shelf and coastal regions near continents and islands, whereas the modern model predicted a less coastal distribution with high habitat suitability more restricted to areas of steep topography. The proportion of high habitat suitability inside versus outside MPAs was higher when applying the historical predictions than the modern predictions, suggesting that different marine spatial planning optimums can be reached from either data sources. Moreover, differences in relative habitat suitability predictions between eras were consistent with the historical depletion of sperm whales from coastal regions, which were easily accessed and targeted by whalers, resulting in a modern distribution limited more to steep continental margins and remote oceanic ridges. The use of historical data can provide important new insights and, through cautious interpretation, inform conservation planning and policy, for example, by identifying refugee species and regions of anticipated population recovery.

Whither the science in wildlife management?

Whither the science in wildlife management?

Functional limb anatomy in a refugee species: The endangered Patagonian huemul deer (Hippocamelus bisulcus).

Early naturalists already considered huemul rare, refuged and a stocky, short-legged mountain deer, 163years before declared endangered (1972). Anatomically, huemul do not overlap with rock-climbers previously considered analogous, as corroborated in this paper by including additional huemul cases. Assertions that population declines are caused principally via livestock infections remain unfounded. Instead, osteopathology in multiple populations across 1,000km, affecting 57% among dead and 86% among live specimens, may relate to micronutrient deficiencies. Historically classified a mountain deer, widespread osteopathology, micronutrient deficiencies and lack of recovery qualify huemul as a refugee species. Recovery strategies thus must include repopulating historical distribution sites.

European bison conservation must move beyond entrenched debates – response to Kerley et al. (2020)

European bison conservation must move beyond entrenched debates – response to Kerley <i>et al.</i> (2020)

European bison conservation cannot afford to ignore alternative hypotheses: a commentary on Perzanowski et al. (2019)

European bison conservation cannot afford to ignore alternative hypotheses: a commentary on Perzanowski <i>et al</i>. (2019)

The Protected Area Paradox and refugee species: The giant panda and baselines shifted towards conserving species in marginal habitats

AbstractParadoxically, despite the growth in protected areas globally, many species remain threatened and continue to decline. Attempts to conserve species in suboptimal habitats (i.e., as refugee species) may in part explain this Protected Area Paradox. Refugee species yield poor conservation outcomes as they suffer lower densities and fitness. We suggest that the giant panda may serve as an iconic example, reflecting the contraction and shift in the giant panda's range, diet and habitat use over the past 3,500 years, coinciding with increasing human pressure, and now maintained by conservation efforts, this due to shifted baselines. The global bias of protected area location to less productive habitats indicates that this problem may be widespread. We urgently need efforts to identify victims of refugee species status to allow improved conservation management globally, reducing the paradoxical outcomes of our conservation efforts.

Habitat selection and genetic diversity of a reintroduced ‘refugee species’

AbstractA ‘refugee’ species is one with a current distribution that has been restricted to a subset of their former niche by threatening processes. Conservation opportunities for such species can be limited by a poor understanding of habitat requirements, where habitat models are based on current distributions and not the innate capacity of the animal to survive where threats are managed. We examined patterns of habitat selection by a putative refugee species, the threatened New Holland mouse Pseudomys novaehollandiae, following reintroduction into historic habitat (habitat that corresponds to a currently unoccupied component of its former niche). Current New Holland mouse populations exist predominantly in coastal heath habitat of select vegetation and fire history, and these environmental conditions differ greatly to those found across the species historical distribution. Using a novel, non‐invasive method of detection for the species, we investigated patterns of habitat selection following reintroduction into historic habitat, where the species primary threat of exotic predators has been removed. We also assessed the changes in genetic diversity measures across three stages of the reintroduction process (before, during and after) using microsatellite markers, to reflect on past efforts in maintaining genetic diversity. We found that historic habitat can still support New Holland mouse populations and identified more diverse potential habitat for the species. We also identified loss of alleles and an increased inbreeding coefficient at the captive breeding stage, but these findings were not statistically significant. This study expands on our limited understanding of habitat requirements and the fundamental niche of the New Holland mouse, highlighting new potential conservation opportunities.

Large mammals of the Palaeo-Agulhas Plain showed resilience to extreme climate change but vulnerability to modern human impacts

Recent evidence indicates that the now submerged continental shelf, the Palaeo-Agulhas Plain (PAP), formed a novel ecosystem during periods of low sea level. This landscape provided nutrient-rich forage and habitats to a variety of large mammals. This is in contrast to the modern faunal assemblage found in the present-day Cape Floristic Region, which is dominated by landscapes with nutrient-poor soils and unpalatable plants. We used archaeological and paleontological records for the region to reconstruct past large mammal communities. We build on this approach by using modern knowledge of ecosystems and ecosystem processes to help us understand how systems functioned in the past. We reconstruct species communities for the PAP of the last 300 ka and investigate potential gaps in the record using Hutchinson's weight ratio theory. We then compare the results to modern occurrences of mammals on the Cape South and West Coasts and the Serengeti (a comparable migratory system) using general linear models. Both sea-level and sampling effort influenced species richness in both the South and West coast regions during the last seven marine isotope stages. In the South coast we observed a decrease in species richness during intermediate sea levels which indicates patterns of use by early humans and habitat availability. Large mammals showed an extraordinary resilience to extreme habitat loss and survived as refugee species during high sea levels and low habitat availability. However the combination of habitat loss and modern human weapons were the cause of severe extinction rates during the last 400 years.

Historical data on European bison management in Bia\u0142owie\u017ca Primeval Forest can contribute to a better contemporary conservation of the species

Many mammal species have been extensively impacted by human interventions in the past. It was especially important for endangered or key species such as European bison Bison bonasus, which has a long history of human interventions and is currently a refugee species confined by anthropogenic activities to suboptimal forest habitats. Using archival information (1795–1915) on bison population dynamics and management practices in Eastern Poland’s Białowieża Primeval Forest (BPF) in three periods (1795–1860, 1861–1888, 1889–1915) differing in management goals, we identify the main factors affecting bison numbers and discuss implications of this knowledge for modern conservation of the species. Mean annual increase rate of bison population varied between 3.03% in the first, − 3.04% in the second, and 2.69% in the third period. The most important drivers of European bison population dynamics were the increasing supplementary feeding and anthropogenic offtake (annual number of individuals hunted, live-captured and poached), along with opening of the forest by different traditional activities. Although this management was solely directed at hunting goals, relatively low intensity of animal removal and counteracting effect of supplementary feeding secured the survival of the species. However, management practices applied in all three periods acted against natural selection and increased animal dependence on human support. Collected historical data presents a unique long-term assessment of management practices and their effectiveness and allows to draw conclusions for the current management of the species. Historical management was not based on evidence. The general principles of traditional bison management were adapted by the twentieth-century management of reinstated population. To avoid repeating the same mistakes, the contemporary management model needs revaluation and changes to conform to up-to-date knowledge on the species habitat selection and forage requirements. Continuation of traditional management practices will sustain species refugee status.

Demographic drivers of a refugee species: large-scale experiments guide strategies for reintroductions of hirola.

Effective reintroduction strategies require accurate estimates of vital rates and the factors that influence them. The hirola (Beatragus hunteri) is the rarest antelope on Earth, with a global population size of <500 individuals restricted to the Kenya-Somali border. We estimated vital rates of hirola populations exposed to varying levels of predation and rangeland quality from 2012 to 2015, and then built population matrices to estimate the finite rate of population change (λ) and demographic sensitivities. Mean survival for all age classes and population growth was highest in the low-predation-high-rangeland-quality setting (λ=1.08±0.03 [mean ± SE]), and lowest in the high-predation-low-rangeland-quality setting (λ=0.70±0.22). Retrospective demographic analyses revealed that increased fecundity (the number of female calves born to adult females annually) and female calf survival were responsible for higher population growth where large carnivores were absent. In contrast, variation in adult female survival was the primary contributor to differences in population growth attributable to rangeland quality. Our analyses suggest that hirola demography is driven by a combination of top-down (predation) and bottom-up (rangeland quality) forces, with populations in the contemporary geographic range impacted both by declining rangeland quality and predation. To enhance the chances of successful reintroductions, conservationists can consider rangeland restoration to boost both the survival and fecundity of adult females within the hirola's historical range.

Using fossil records to inform reintroduction of the kakapo as a refugee species

Many threatened species persist only as relict populations occupying a fraction of their former distribution, in habitats which may not be optimal for supporting viable populations. Following population growth of one such species, the kakapo (Strigops habroptilus), conservation managers are faced with the challenge of identifying suitable locations for reintroduction. Areas which support habitat conditions typical of those occupied by kakapo in the past have the greatest potential to support future populations. We collated occurrences of kakapo from recent fossil records, then used MaxEnt to model the past distribution of kakapo across New Zealand, and contemporary areas suitable for reintroductions based on extant habitat and present-day climate. We validated our models against three independent data sets of the most recent relict populations. Our models suggest that kakapo once occurred in mountain beech and Hall's totara or broadleaf forests with moderate to high precipitation and milder winters. Areas predicted to be environmentally suitable for kakapo in contemporary New Zealand include the west coast of the South Island, the west and north-east of the North Island and the southern side of Lake Taupo. Assuming that known threats of introduced predators can be managed, our study suggests that suitable kakapo habitat persists in New Zealand, and here we offer insight into locations for future population establishment. Given the finite carrying capacity of offshore islands, this is an important first step which will enable kakapo managers to prioritise focal areas and also highlights the benefits and potential pitfalls of using these modelling approaches for refugee species.

Diet and habitat of the saiga antelope during the late Quaternary using stable carbon and nitrogen isotope ratios

Saiga antelope (Saiga tatarica) is one of the typical late Pleistocene species of the cold and arid mammoth steppe that covered a large area of northern hemisphere. The species is currently endangered and persists only in small areas of Central Asian steppe and desert ecosystems. The investigation of the ecology of the Pleistocene saiga using stable isotope ratios (δ13C, δ15N) aimed to decipher how different their diet and habitat were from those observed nowadays in relict populations. Up to 76 samples of bone collagen of ancient saiga from Western Europe, Siberia and Eastern Beringia were analysed and compared with 52 samples of hair and bone collagen of modern specimens from Kazahkstan, Russia and Mongolia. The δ13C values of the ancient saiga do not exhibit a clear trend over time. They cover the same range of values as the modern ones, from a C3-dominated to a C3-C4-dominated mixed diet (including probably Chenopodiaceae). In contrast, the δ15N values of fossil saigas are more variable and lower on average than the extant ones. The lowest δ15N values of ancient saiga are found around the Last Glacial Maximum, reflecting the influence of the cold conditions at that time. On the other hand, fossil saiga occupying the same regions as the historical and modern populations exhibit high δ15N values similar to the modern ones, confirming ecological continuity over time. Modern saiga is thus occupying just one of its potential diverse habitats they used in the past. Therefore, the extant saiga is not a refugee species confined to a suboptimal habitat. During the late Pleistocene, the saiga occupied a separate niche compared with the other ungulates of the mammoth steppe. However, this species could also adapt to a lichen-dominated diet normally seen in reindeer, leading to an isotopic overlap between the two species in south-western France and Alaska around the Last Glacial Maximum. This adaptation allowed a geographical expansion that does not correspond to a habitat-tracking episode. Hence, the realized niche currently observed for the saiga is reduced compared with their potential capacity for adaptation, a crucially important factor for the conservation of this endangered species.

Resource selection and landscape change reveal mechanisms suppressing population recovery for the world's most endangered antelope

Summary Understanding how bottom‐up and top‐down forces affect resource selection can inform restoration efforts. With a global population size of &lt;500 individuals, the hirola Beatragus hunteri is the world's most endangered antelope, with a declining population since the 1970s. While the underlying mechanisms are unclear, some combination of habitat loss and predation are thought to be responsible for low abundances of contemporary populations. Efforts to conserve hirola are hindered by a lack of understanding as to why population density remains low, despite eradication of the viral disease, rinderpest. To elucidate factors underlying chronically low numbers, we examined resource selection and landscape change within the hirola's native range. Because hirola are grazers, we hypothesized that the availability of open areas would be linked both to forage and safety from predators. We quantified: (i) changes in tree cover across the hirola's historical range in eastern Kenya over the past 27 years; (ii) how tree cover has influenced resource selection by hirola; and (iii) interactions between tree cover and predation. Between 1985 and 2012, tree cover increased by 251% across the historical range of hirola. Tree encroachment was associated with a 98% decline of hirola and elephant Loxodonta africana populations, a 74% decline in cattle Bos indicus, an increase in browsing livestock by 327%, and a reduction in rainfall. Although hirola avoided tree cover, we found no evidence that predation on hirola increased with increasing tree cover. Synthesis and applications. Hirola may qualify as a refugee species, in which contemporary populations are restricted to suboptimal habitat and exhibit low survival, reproduction or both. The extinction of hirola would be the first of a mammalian genus on the African continent in modern history. We conclude that contemporary low numbers of hirola are due at least partly to habitat loss via tree encroachment, triggered by some combination of elephant extirpation, overgrazing, drought and perhaps fire suppression. We recommend a combination of rangeland restoration efforts (including conservation of elephants, manual clearing of trees, and grass seeding), increased enforcement of an existing protected area (Arawale National Reserve), and reintroductions to enhance recovery for this endangered species. These efforts will rely on enhanced support from the international conservation community and the cooperation of pastoralist communities with which the hirola coexist.

Anthropogenic areas as incidental substitutes for original habitat.

One speaks of ecological substitutes when an introduced species performs, to some extent, the ecosystem function of an extirpated native species. We suggest that a similar case exists for habitats. Species evolve within ecosystems, but habitats can be destroyed or modified by natural and human-made causes. Sometimes habitat alteration forces animals to move to or remain in a suboptimal habitat type. In that case, the habitat is considered a refuge, and the species is called a refugee. Typically refugee species have lower population growth rates than in their original habitats. Human action may lead to the unintended generation of artificial or semiartificial habitat types that functionally resemble the essential features of the original habitat and thus allow a population growth rate of the same magnitude or higher than in the original habitat. We call such areas substitution habitats and define them as human-made habitats within the focal species range that by chance are partial substitutes for the species' original habitat. We call species occupying a substitution habitat adopted species. These are 2 new terms in conservation biology. Examples of substitution habitats are dams for European otters, wheat and rice fields for many steppeland and aquatic birds, and urban areas for storks, falcons, and swifts. Although substitution habitats can bring about increased resilience against the agents of global change, the conservation of original habitat types remains a conservation priority.

European bison as a refugee species? Evidence from isotopic data on Early Holocene bison and other large herbivores in northern Europe.

According to the refugee species concept, increasing replacement of open steppe by forest cover after the last glacial period and human pressure had together forced European bison (Bison bonasus)—the largest extant terrestrial mammal of Europe—into forests as a refuge habitat. The consequent decreased fitness and population density led to the gradual extinction of the species. Understanding the pre-refugee ecology of the species may help its conservation management and ensure its long time survival. In view of this, we investigated the abundance of stable isotopes (δ13C and δ15N) in radiocarbon dated skeletal remains of European bison and other large herbivores—aurochs (Bos primigenius), moose (Alces alces), and reindeer (Rangifer tarandus)—from the Early Holocene of northern Europe to reconstruct their dietary habits and pattern of habitat use in conditions of low human influence. Carbon and nitrogen isotopic compositions in collagen of the ungulate species in northern central Europe during the Early Holocene showed significant differences in the habitat use and the diet of these herbivores. The values of the δ13C and δ15N isotopes reflected the use of open habitats by bison, with their diet intermediate between that of aurochs (grazer) and of moose (browser). Our results show that, despite the partial overlap in carbon and nitrogen isotopic values of some species, Early Holocene large ungulates avoided competition by selection of different habitats or different food sources within similar environments. Although Early Holocene bison and Late Pleistocene steppe bison utilized open habitats, their diets were significantly different, as reflected by their δ15N values. Additional isotopic analyses show that modern populations of European bison utilize much more forested habitats than Early Holocene bison, which supports the refugee status of the species.