Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-07-06T23:43:07.932Z Has data issue: false hasContentIssue false

Reintroducing species when threats still exist: assessing the suitability of contemporary landscapes for island endemics

Published online by Cambridge University Press:  02 December 2020

Nicole Frances Angeli*
Affiliation:
Biodiversity Research and Teaching Collections, Applied Biodiversity Science Program, Department of Ecology and Conservation Biology, 2258 TAMU, Texas A&M University, College Station, Texas, 77843, USA.
Lee Austin Fitzgerald
Affiliation:
Biodiversity Research and Teaching Collections, Applied Biodiversity Science Program, Department of Ecology and Conservation Biology, 2258 TAMU, Texas A&M University, College Station, Texas, 77843, USA.
*
(Corresponding author) E-mail nicoleangeli1@gmail.com

Abstract

Reintroducing species into landscapes with persistent threats is a conservation challenge. Although historic threats may not be eliminated, they should be understood in the context of contemporary landscapes. Regenerating landscapes often contain newly emergent habitat, creating opportunities for reintroductions. The Endangered St Croix ground lizard Pholidoscelis polops was extirpated from the main island of St Croix, U.S. Virgin Islands, as a result of habitat conversion to agriculture and predation by the small Indian mongoose Herpestes auropunctatus. The species survived on two small cays and was later translocated to two islands. Since the 1950s, new land-cover types have emerged on St Croix, creating a matrix of suitable habitat throughout the island. Here we examined whether the new habitat is sufficient for a successful reintroduction of the St Croix ground lizard, utilizing three complementary approaches. Firstly, we compared a map from 1750 to the current landscape of St Croix and found statistical similarity of land-cover types. Secondly, we determined habitat suitability based on a binomial mixture population model developed as part of the programme monitoring the largest extant population of the St Croix ground lizard. We estimated the habitat to be sufficient for > 142,000 lizards to inhabit St Croix. Thirdly, we prioritized potential reintroduction sites and planned for reintroductions to take place during 2020–2023. Our case study demonstrates how changing landscapes alter the spatial configuration of threats to species, which can create opportunities for reintroduction. Presuming that areas of degraded habitat may never again be habitable could fail to consider how regenerating landscapes can support species recovery. When contemporary landscapes are taken into account, opportunities for reintroducing threatened species can emerge.

Type
Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International

Introduction

The majority of island endemics lost to invasive exotic mammals over the past 500 years have been reptiles, amphibians and birds (Sax & Gaines, Reference Sax and Gaines2008). Many endemic species were lost relatively quickly from small islands, and have often persisted only on small offshore islands and in captive colonies (Manne et al., Reference Manne, Brooks and Pimm1999). A conservation goal is to reintroduce species to the islands from which they were extirpated. Even where threats such as invasive predators continue to persist on islands, reintroduction may be possible. The Guidelines to Reintroductions and Other Conservation Translocations (IUCN, 2013, p. 4) state ‘There should generally be strong evidence that the threat(s) that caused any previous extinction have been correctly identified and removed or sufficiently reduced’. Original threats need to be addressed, but they should be understood in the present context. Often original threats such as the presence of mongooses on large islands cannot be completely eliminated with current technologies. The Guideline's phrasing ‘sufficiently reduced’ implies that large-scale restoration efforts are a prerequisite for reintroductions. However, an alternative way of addressing persistent threats is to understand them in the context of contemporary landscapes that have emerged since losses originally occurred. Extinction/extirpation takes place in a landscape context, and changes of those landscapes over time result in altered threats to biodiversity. Restoration efforts in newly developing ecosystems will thus benefit from fresh approaches and new norms (Hobbs et al., Reference Hobbs, Higgs and Harris2009). There may be opportunities for reintroductions into emergent habitats and natural refugia that were not present during historic extirpation events. This can apply to islands where landscapes are regenerating, even when some historic drivers of extinction such as invasive predators are still present.

Human land use changes the configuration of landscape features, influencing species' distributions. Changing political and economic factors also alter prospects for landscape restoration (Wintle et al., Reference Wintle, Bekessy, Keith, van Wilgen, Cabeza and Schröder2011). In eastern North America, reduction in agricultural activities allowed regeneration of forests that sustain populations of numerous species, including the red wolf Canis rufus and red-legged salamander Plethodon shermani (Connette & Semlitsch, Reference Connette and Semlitsch2013; Karlin et al., Reference Karlin, Vaclavik, Chadwick and Meentemeyer2016). Recovery of large carnivores such as the lynx Lynx lynx, grey wolf Canis lupus lupus and wolverine Gulo gulo in Europe is largely a result of advances in the management of functional landscapes (Chapron et al., Reference Chapron, Kaczensky, Linnell, von Arx, Huber and Andrén2014). Successional forests are allowing previously overexploited animals that suffered habitat loss, such as the Puerto Rican parrot Amazona vittata and white-crowned pigeon Patagioenas leucocephala, to recover in Puerto Rico and throughout the Caribbean (Earnhardt et al., Reference Earnhardt, Vélez-Valentín, Valentin, Long, Lynch and Schowe2014; Rivera-Milán et al., Reference Rivera-Milán, Boomer and Martínez2016). Networks of suitable habitat have been modelled for the Iberian ibex Capra pyrenaica in western Iberia (Torres et al., Reference Torres, Carvalho, Serrano and Helmer2016) and for the North Island robin Petroica longipes in New Zealand (Armstrong & Davidson, Reference Armstrong and Davidson2006). These cases highlight how landscape change over time can support species reintroduction and recovery.

New ideas are emerging for the reintroduction of species to their historic ranges when threats are still perceived to be present (Stier et al., Reference Stier, Samhouri, Novak, Marshall, Ward, Holt and Levin2016). For example, the milu Elaphurus davidianus became extirpated as a result of hunting and habitat conversion for land reclamation in China in the early 20th century, but a wild population became established in 1998 from 36 animals that escaped from a nature reserve during a flooding event. Now, > 500 milu descended from those founders persist in the wild (Yang et al., Reference Yang, Song, Ma, Li, Zhang and Price2016). The Formosan clouded leopard Neofelis nebulosa, considered extinct in Taiwan, is now thought to be a candidate for reintroductions in regenerating forests with rebounding prey bases (Chiang et al., Reference Chiang, Pei, Vaughan, Li, Chen and Liu2015). A reported sighting in 2019 and other unconfirmed sightings strengthen the case for reintroductions (Everington, Reference Everington2019).

We suggest that suitable habitats and networks of refugia may exist as a result of landscape regeneration on Caribbean islands that historically lost 30–97% of native land cover to agricultural conversion. This historic land-cover change, since the 1740s, coincided with introductions of invasive species, creating multiple drivers for island extinctions (Lugo & Helmer, Reference Lugo and Helmer2004). We studied the Endangered St Croix ground lizard Pholidoscelis polops (historically known as Ameiva polops), which was extirpated from 99.97% of its historic range on the main island of St Croix (217 km2) after the 1884 introduction of the small Indian mongoose Herpestes auropunctatus. The extirpation is thought to be a result of both the conversion of 90% of the island to agricultural pastures and predation by mongooses (Henderson, Reference Henderson1992). Recent translocations (1989 and 2008) to two additional small islands without mongooses were successful (Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015). Reintroduction to the main island was not recommended historically because the presence of mongooses on St Croix was perceived to prevent population establishment (Meier et al., Reference Meier, Noble and Zwank1990). Here we explore the alternate view, suggesting that even though mongooses are still present on St Croix, regenerating landscapes in the post-agricultural period create new opportunities for the reintroduction of the St Croix ground lizard.

We predicted that areas appropriate for reintroduction exist based on similarities between the historic (1750) and re-emergent (2016) land-cover types on St Croix. We assessed the suitability of potential lizard habitat using landscape parameters (topography, land cover, elevation) developed with data collected from the largest extant population on an offshore island (Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018). We collected data on the distribution of mongooses across St Croix, and used a prioritization scheme to rank suitable reintroduction areas (Dawson et al., Reference Dawson, Oppel, Cuthbert, Holmes, Bird and Butchart2015). Our work demonstrates how changing landscapes present new opportunities for restoration in historic ranges, especially on islands, even when threats still exist on a broader landscape scale.

Study area and species

St Croix is a 218 km2 island in the Caribbean Sea and one of the U.S. Virgin Islands. It is a single land bank, erupting from the ocean where tectonic plates merged, surrounded by trenches > 1,000 m deep (Case & Holcombe, Reference Case and Holcombe1980). The island is covered by subtropical dry coastal forest, with annual rainfall of 1,250 mm in the west and 750 mm in the east (Bowden, Reference Bowden1968). Easterly trade winds blow across the island throughout the year. In addition to the main island, there are four small offshore islands, with a total area of 85 ha, off the north and south shores: Protestant Cay, Green Cay, Ruth Island and Buck Island.

The main island has been mapped since 1750, but only one land-cover map from 1750 still exists (Hopkins, Reference Hopkins1989). The acreage of plantations increased island-wide during 1742–1754 (Westergaard, Reference Westergaard1938), transitioning from cotton to sugar cane during 1754–1800 (Tyson, Reference Tyson1992). Mongooses were introduced to control rats Rattus rattus and Rattus norvegicus in sugar cane fields in 1884. By 1917, nearly 90% of native forests and woodlands had been cleared for agriculture or logged (Ward et al., Reference Ward, Rodriguez, Morgan and Zimmerman2000). Sugar cane cultivation virtually ceased by the late 1950s (Atkinson & Marín-Spiotta, Reference Atkinson and Marín-Spiotta2015). Since then, secondary subtropical forests have developed on St Croix, with naturalized tree species and novel assemblages colonizing former agricultural lands (Atkinson & Marín-Spiotta, Reference Atkinson and Marín-Spiotta2015).

The St Croix ground lizard is a small diurnal ectotherm that uses a variety of vegetation cover as habitat. It forages in leaf litter for small invertebrate prey (Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015). The earliest records of the species’ loss are from the 1930s. It was completely extirpated from the eastern end of St Croix by 1920, and the last individuals were observed in Frederiksted on the western end of St Croix in 1969 (Dodd, Reference Dodd1978). Fortunately, two populations persisted on Protestant Cay (2.6 ha; 150 m offshore) and Green Cay (4.3 ha; 400 m offshore) because mongooses were absent there (Dodd, Reference Dodd1980; Thomas & Joglar, Reference Thomas and Joglar1996).

Two successful introductions indicate St Croix ground lizards are relatively easy to establish in new areas. A population was established on Ruth Island (9.7 ha; 430 m offshore), a dredge-spoil island, with only nine founders from Protestant Cay in 1989. A translocation of 57 founders from Green Cay to Buck Island (69 ha; 2.6 km offshore) in 2008 was successful (Treglia & Fitzgerald, Reference Treglia, Fitzgerald and Soorae2011; Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015). An estimated total of c. 3,000 individuals now occur on these four islands, with > 2,000 on Buck Island. Green Cay, Protestant Cay and Ruth Island each harbour 100–400 individuals (Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015; Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018). All of these islands are small (total area 85 ha), leaving the lizard populations vulnerable to stochastic events such as hurricanes, predator invasion and habitat degradation.

Methods

Analysing landscape change

We compiled data on protected areas, the predicted distribution of mongooses and land-cover types, and predicted the carrying capacity for lizards in each 30 m2 cell in a grid covering the entire island of St Croix. We digitized the land-cover map from 1750 (Hopkins, Reference Hopkins1989) using the Georeferencer plugin tool in QGIS 2.14.0 (Open Source Geospatial Foundation, Beaverton, USA). Maps from 1950 showed that at that time 97% of land was urban or agricultural pasture (Ward et al., Reference Ward, Rodriguez, Morgan and Zimmerman2000). We obtained land-cover data for 2016 from Landsat 2016 (Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018). Because the maps from 1750 and 2016 showed landscapes with a heterogeneous mix of land-cover types that were not dominated by agriculture and urban development such as in 1950, we compared the area occupied by different land-cover types in 1750 and 2016 using a paired Welch's t test.

Estimating lizard carrying capacity

We created a map layer for St Croix ground lizard carrying capacity using the results of a mechanistic binomial mixture model developed for Buck Island (Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018), which accounted for latent abundance and low detection of the species. In that model, we found significant associations of lizard abundance with areas identified by operative temperature models as optimal for the species’ thermoregulation (see model description in Supplementary Material 1, and description of the full modelling process in Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018 and Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015). We scored the final data set for mean lizard abundance per grid cell as: 1–6 lizards = not suitable, 7–12 lizards = potentially suitable, 13–20 lizards = suitable, and 21–25 = most suitable (Supplementary Fig. 1). These estimates were summed to obtain an estimate of lizard habitat A across all areas (Table 1) for the presently dispersing population and the future population (Supplementary Fig. 2).

Table 1 A ranked list of the proposed areas for potential reintroduction of the St Croix ground lizard Pholidoscelis polops, based on combined scores of habitat suitability, mongoose presence, and mongoose control measures.

1 Per cent of the total habitat in the categories: potentially suitable, suitable, most suitable.

2 Carrying capacity was estimated from the model, and summed to obtain an estimate for the entire area.

Prioritizing suitable sites for reintroduction

We considered protected areas on both public and private land for reintroduction. We prioritized potential reintroduction areas by considering the total area of the site and suitable habitat for St Croix ground lizards in the site. We also gave higher priority to sites where the threat of predation by mongooses was mitigated through management. Mongoose management was in place at some sites (e.g. Sandy Point); at other sites there was capacity for land managers to control mongoose populations.

Capacity to control mongooses was assessed based on reports from staff engaged in the trapping of mongooses to protect nesting marine turtles (Angeli, Reference Angeli2017). We also took into account the threat of predation at individual sites based on the distribution of mongooses on St Croix. Mongooses are not evenly distributed across St Croix; their population density varies. We used a species distribution model created by Gould (Reference Gould2007) to visualize overlap between priority reintroduction areas and mongoose presence. Mongooses were absent from 7.96 km2 (3.65%) of St Croix, most notably in the south of the island where the carrying capacity of St Croix ground lizards was thus predicted to be greater.

Results

Landscape change

In 1750, 42% of St Croix was forested, < 11% was devoted to pasture or agriculture and < 5% was urban. According to the historic map, the remaining 42% consisted of woodland, shrubland, and edge forest. The 2016 map showed 32% pasture and agriculture, 31% forest cover and 12% urban areas. Succession of fallow fields to shrubland, woodland and edge forest comprised the remaining 25% of land cover in 2016. We found no statistical differences in land-cover area between the 1750 and 2016 maps (Fig. 1; t = 0.013, df = 4.26, P = 0.989). The model of mongoose occurrence on St Croix showed numerous areas where mongooses are predicted to be absent that overlapped with priority areas for reintroduction of the St Croix ground lizard (Hoagland et al., Reference Hoagland, Horst, Kilpatrick and Woods1989; Gould et al., Reference Gould2007; Fig. 2).

Fig. 1 Historic and recent land cover in St Croix, U.S. Virgin Islands. (a) The historic map from 1750 was created by J. Cronenberg and J. von Jaegersber (reproduced with permission of Copenhagen Archives). (b) This map was digitized to show historic land-cover types. Landscape transformation and introduction of mongooses led to the extirpation of the now Endangered St Croix ground lizard Pholidoscelis polops. (c) Land-cover classifications of 2016, matched to the digitized historic land-cover types. Establishment of protected areas, land spared from agriculture, and suburban development resulted in emergent land-cover types, which now include potential habitats for the St Croix ground lizard.

Fig. 2 Suitable habitat for the St Croix ground lizard on St Croix, U.S. Virgin Islands. We used a predictive habitat suitability model, with suitability categories based on threats, land-cover types and ongoing conservation efforts.

Lizard carrying capacity

The models estimated that St Croix could potentially support 142,421 lizards across 1,169 ha. We identified 19 protected areas, with 2.4−100% suitable habitat (Table 1, Fig. 2). Population models estimated 21,469 St Croix ground lizards could be supported in protected areas on St Croix, based on a mean of 8.2 ± SD 4.1 (range 0.0–24.0) lizards per 30 m2 grid cell. Based on the model results and ranking of potential sites, we prioritized reintroduction sites that contained suitable lizard habitat and reduced threat from mongooses (Fig. 3). Eight of the 30 protected areas with lizard habitat already have some mongoose control measures in place, specifically trapping to reduce mongoose density. Mongoose-proof barriers do not currently exist on St Croix, but could be constructed at some sites with < 3 km of fencing. We included this information in the ranking should managers decide to build barriers.

Fig. 3 The St Croix ground lizard occurs in four extant populations, on (a) Green Cay, (b) Buck Island, (c) Protestant Cay and (d) Ruth Island. We propose three reintroduction sites on St Croix, at (e) Sandy Point, (f) Altoona Lagoon and (g) Southgate Coastal Preserve. Area of habitat is shown for each site; they are not drawn to scale. The inset map indicates where each site is located on St Croix.

The three most suitable reintroduction sites are: (1) The Sandy Point National Wildlife Refuge, which is located on the south-west end of St Croix and contains 43.4 ha of suitable habitat. The mongoose population in the Refuge has been monitored and reduced through trapping. Lizard reintroductions can occur without fencing, but a 2.9 km mongoose exclusion fence proposed to benefit nesting marine turtles would also reduce mongoose predation on the St Croix ground lizard in this area. (2) Altoona Lagoon, which is managed by the Government of the Virgin Islands, with 6.8 ha of habitat. Our model showed the entire area as suitable habitat for the St Croix ground lizard. The site is protected and is equal in size to Protestant Cay and Green Cay combined, where the lizards persisted after extirpation from St Croix. A wetland adjacent to coastal forest and beach is an important area for migratory birds. This would be a good site to study effects of mongoose control on St Croix ground lizard density. (3) The Southgate Coastal Reserve, which contains 19.3 ha of suitable habitat and is managed by the St Croix Environmental Association. Southgate has a large salt pond supporting birds, and a beach used by nesting marine turtles on the north shore of St Croix. A birding trail is used for environmental education, and outreach activities for the St Croix ground lizard could be included. The reserve is currently fenced with stainless steel chain link, which can potentially be modified to exclude mongooses if deemed necessary.

Discussion

Two successful conservation introductions showed the St Croix ground lizard can be established on small offshore cays where mongooses have been eradicated, such as on Buck Island. However, all four existing populations are vulnerable. Continued recovery of this Endangered endemic species depends on reintroducing it to the main island of St Croix. The short-term risk of reintroduction to the survival of the extant populations is low, because the new population on Buck Island has > 2,000 individuals and can serve as source of individuals for reintroductions. Two successful translocations of the St Croix ground lizard to Ruth Island and Buck Island indicate that once established, populations grow rapidly and disperse into unoccupied available habitat (Fitzgerald et al., Reference Fitzgerald, Treglia, Angeli, Hibbitts, Leavitt and Subalusky2015). On Buck Island, the newly established population expanded rapidly, with a marked dispersal front emanating from the point of introduction (Angeli et al., Reference Angeli, Lundgren, Pollock, Hillis-Starr and Fitzgerald2018). This indicates high potential for dispersal on mainland St Croix once founder populations are established.

Lindenmayer et al. (Reference Lindenmayer, Fischer, Felton, Crane, Michael and Macgregor2008, p. 134) suggested, ‘novel ecosystems present major challenges to traditional thinking in conservation ecology, such as the focus on species extinctions as the usual response to landscape transformation.’ Understanding the landscape of threats and using that knowledge to adjust conservation actions can present positive opportunities for restoration of species and rewilding ecosystems (Jordan, Reference Jordan, Gobster and Hull2000). We examined land-cover change on St Croix spanning 250 years and documented landscape transformations that led to extirpation of the St Croix ground lizard. The primary factors in this extirpation were deforestation, land conversion for agriculture, and introduction of mongooses. In recent decades land has been spared from agriculture, protected areas have been established, and invasive species including mongooses are increasingly managed. This recent transformation of land use in St Croix has facilitated emergence of land cover that includes suitable habitat for the St Croix ground lizard. Using a prioritization scheme, we identified potential reintroduction sites that could increase the area occupied by the St Croix ground lizard by 180%. In previous studies, a predictive approach using demographic data demonstrated that sufficiently low levels of threats could allow reintroductions of the Iberian ibex in western Iberia, and the North Island robin and North Island saddleback Philesturnus rufusater in New Zealand (Armstrong & Davidson, Reference Armstrong and Davidson2006; Parlato & Armstrong, Reference Parlato and Armstrong2012; Torres et al., Reference Torres, Carvalho, Serrano and Helmer2016). Our approach differs in that we evaluated suitability across emergent contemporary landscapes, to determine areas best suited for reintroduction.

Although threat abatement is important for protecting endemic species on islands, and mongoose control on St Croix should be a priority, total eradication of invasive predators on relatively large, human-inhabited islands may not be feasible. Our approach relies on re-emergence of habitat and refugia that will allow the St Croix ground lizards to persist, despite continued presence of mongooses. The decline of the St Croix ground lizard, spanning 95 years, provides some evidence that anthropogenic landscapes created refugia where populations escaped predation. The last stronghold for the species in the 1960s was along the waterfront in the busy town of Frederiksted (Dodd, Reference Dodd1978). St Croix was stripped of native vegetation cover, and mongooses devastated native fauna. In comparison with the pre-extinction landscape, present-day St Croix contains similar amounts of suitable habitat in protected and in urbanized areas.

Reintroduction experiments such as the one we have proposed can be carried out with careful implementation and monitoring, and species recovery can be tracked with frameworks such as the IUCN Green List (Akçakaya et al., Reference Akçakaya, Bennet, Brooks, Grace, Heath and Hedges2018). In 2019 we met with ecologists and personnel from U.S. Virgin Islands resource agencies, the U.S. Fish & Wildlife Service and U.S. National Park Service to finalize decisions about the reintroductions. The group planned for reintroductions during 2020–2023 using the prioritization outlined here.

There is a long-term risk associated with not learning how to repatriate endemic species. Small, isolated wildlife populations will remain vulnerable to sea level rise and anthropogenic disturbance. In such conditions, they could increasingly be perceived as only able to persist in refuge locations outside their core range. Taking contemporary landscapes and regeneration of suitable habitat into account could provide new opportunities for reintroducing threatened species to areas from which they were originally extirpated.

Acknowledgements

LFA and NFA received funding from USA National Science Foundation DGE 0654377. NFA received funding from a Smithsonian Institution Predoctoral Fellowship, National Park Service PMIS 154945, and FWS R4 I&M project #67942, program #66785. We thank staff of the U.S. Fish & Wildlife Service Caribbean Ecological Services Office & Caribbean Refuges Complex, St Croix Environmental Association, and Buck Island Reef National Monument staff for their support. Claudia Lombard, Jan Paul Zegarra, Zandy Hillis-Starr, Ian Lundgren, Clayton Pollock, Jennifer Valiulis, Kristen Kelbe, Orris Scribner, Michael Pede, Buzz Hoagland, Kirstina Barry, Michael Evans, Fitzgerald Lab, and Caribbean Partners for Amphibian and Reptile Conservation provided support. Mickey Parker prepared the figures for publication.

Author contributions

Study design, fieldwork, writing: both authors; analysis: NFA.

Conflicts of interest

None.

Ethical standards

This research was carried out under U.S. Virgin Islands permit (STX 019-13), USFWS permit (TE98000A-0) and Texas A&M University permit IACUC (2013-0011), and otherwise complied with the Oryx guidelines on ethical standards.

Data availability

Geospatial data layers are available at figshare.com/projects/Repatriation_St_Croix_ground_lizard/28461. Code is available at github.com/nangeli1/repatriation.

Footnotes

*

Current address: Division of Fish and Wildlife, Government of U.S. Virgin Islands, St Croix, USA

Supplementary material for this article is available at doi.org/10.1017/S0030605319001091

References

Akçakaya, H.R., Bennet, E.L., Brooks, T.M., Grace, M.K., Heath, A., Hedges, S. et al. (2018) Quantifying species recovery and conservation successes to develop an IUCN Green List of Species. Conservation Biology, 32, 11281138.Google Scholar
Angeli, N.F. (2017) Identifying mechanisms of persistence for ground lizards (Reptilia: Ameiva) in the Caribbean informed by habitat, physiology, and predation. PhD thesis, Texas A&M University, College Station, USA.Google Scholar
Angeli, N.F., Lundgren, I., Pollock, C., Hillis-Starr, Z. & Fitzgerald, L.A. (2018) Dispersal and population state of an Endangered island lizard following conservation translocation. Ecological Applications, 28, 336347.CrossRefGoogle ScholarPubMed
Armstrong, D.P. & Davidson, R.S. (2006) Developing population models for guiding reintroductions of extirpated bird species back to the New Zealand mainland. New Zealand Journal of Ecology, 30, 7385.Google Scholar
Atkinson, E. & Marín-Spiotta, E. (2015) Land use legacy effects on structure and composition of subtropical dry forest in St. Croix, U.S. Virgin Islands. Forest Ecology and Management, 33, 270280.CrossRefGoogle Scholar
Bowden, M. (1968) Water balance of a dry island. Geography Publications at Dartmouth, 6, 189.Google Scholar
Case, J.E. & Holcombe, T.L. (1980) Geologic-Tectonic Map of the Caribbean Region, 1100. U.S. Geological Survey Miscellaneous Investigations Series Map I-1100, scale 1: 2,500,000. Prepared in cooperation with the United States Naval Oceanographic Office and the United States Naval Ocean Research and Development Activity, John C. Stennis Space Center, Hancock County, USA.Google Scholar
Chapron, G., Kaczensky, P., Linnell, J.D., von Arx, M., Huber, D., Andrén, H. et al. (2014) Recovery of large carnivores in Europe's modern human-dominated landscapes. Science, 346, 15171519.CrossRefGoogle ScholarPubMed
Chiang, P.J., Pei, K.J.C., Vaughan, M.R., Li, C.F., Chen, M.T., Liu, J.N. et al. (2015) Is the clouded leopard Neofelis nebulosa extinct in Taiwan, and could it be reintroduced? An assessment of prey and habitat. Oryx, 49, 261269.CrossRefGoogle Scholar
Connette, G.M. & Semlitsch, R.D. (2013) Life history as a predictor of salamander recovery rate from timber harvest in southern Appalachian forests, USA. Conservation Biology, 27, 13991409.CrossRefGoogle ScholarPubMed
Dawson, J., Oppel, S., Cuthbert, R.J., Holmes, N., Bird, J.P., Butchart, S.H. et al. (2015) Prioritizing islands for the eradication of invasive vertebrates in the United Kingdom Overseas Territories. Conservation Biology, 29, 143153.Google ScholarPubMed
Dodd, C.K. (1978) Island lizard in danger. National Parks Conservation Magazine, 52, 1011.Google Scholar
Dodd, C. K. (1980) Ameiva polops Cope, St. Croix ground lizard. In Catalogue of American Amphibians and Reptiles No. 240. Society for the Study of Amphibians and Reptiles, Granville, USA.Google Scholar
Earnhardt, J., Vélez-Valentín, J., Valentin, R., Long, S., Lynch, C. & Schowe, K. (2014) The Puerto Rican parrot reintroduction program: sustainable management of the aviary population. Zoo Biology, 33, 8998.CrossRefGoogle ScholarPubMed
Everington, K. (2019) Taiwanese scholars reluctant to declare Formosan clouded leopard extinct. Taiwan News, 25 February 2019, taiwannews.com/tw/en/3645555 [accessed 20 February 2020].Google Scholar
Fiske, I.J. & Chandler, R.B. (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software, 43, 123.Google Scholar
Fitzgerald, L.A., Treglia, M., Angeli, N.F., Hibbitts, T., Leavitt, D., Subalusky, A. et al. (2015) Determinants of successful establishment and post-translocation dispersal of a new population of the Critically Endangered St. Croix ground lizard (Ameiva polops). Restoration Ecology, 23, 776786.CrossRefGoogle Scholar
Gesch, D. (2007) The national elevation dataset. In Digital Elevation Model Technologies and Applications: The DEM Users Manual. 2nd edition (ed. Maune, D.), pp. 99118. American Society for Photogrammetry and Remote Sensing, Bethesda, USA.Google Scholar
Gould, W.A. (2007) The Puerto Rico Gap Analysis Project. USDA Forest Service, International Institute of Tropical Forestry. General Technical Report IITF-GTR-39, San Juan, Puerto Rico.Google Scholar
Henderson, R.W. (1992) Consequences of predator introductions and habitat destruction on amphibians and reptiles in the post-Columbus West Indies. Caribbean Journal of Science, 28, 110.Google Scholar
Hoagland, D.B., Horst, G.R. & Kilpatrick, C.W. (1989) Biogeography and population biology of the mongooses in the West Indies. In Biogeography of the West Indies (ed. Woods, C.A.), pp. 611634. Sandhill Crane Press, Gainesville, USA.Google Scholar
Hobbs, R.J., Higgs, E. & Harris, J.A. (2009) Novel ecosystems: implications for conservation and restoration. Trends in Ecology and Evolution, 24, 599605.CrossRefGoogle ScholarPubMed
Hopkins, D. (1989) An extraordinary eighteenth-century map of the Danish sugar-plantation island St. Croix. Imago Mundi, 41, 4458.Google Scholar
Horst, G.R., Hoagland, D.B. & Kilpatrick, C.W. (2001) The mongooses in the West Indies: the biogeography and population biology of an introduced species. In Biogeography of the West Indies: Patterns and Perspectives, 2nd edition (eds Woods, C.A. & Sergile, F.E.), pp. 409424. CRC Press, Boca Raton, USA.CrossRefGoogle Scholar
IUCN/SSC (2013) Guidelines for Reintroductions and Other Conservation Translocations. Version 1.0. IUCN Species Survival Commission, Gland, Switzerland.Google Scholar
Jordan, W.R. (2000) Restoration, community, and wilderness. In Restoring Nature: Perspectives from the Social Sciences and Humanities (eds Gobster, P.H. & Hull, R.B.), pp. 2136. Island Press, Washington, DC, USA.Google Scholar
Karlin, M., Vaclavik, T., Chadwick, J. & Meentemeyer, R. (2016) Habitat use by adult red wolves, Canis rufus, in an agricultural landscape, North Carolina, USA. Mammal Study, 41, 8795.Google Scholar
Lindenmayer, D.B., Fischer, J., Felton, A., Crane, M., Michael, D., Macgregor, C. et al. (2008) Novel ecosystems resulting from landscape transformation create dilemmas for modern conservation practice. Conservation Letters, 1, 129135.CrossRefGoogle Scholar
Lugo, A.E. & Helmer, E. (2004) Emerging forests on abandoned land: Puerto Rico's new forests. Forest Ecology and Management, 190, 145161.CrossRefGoogle Scholar
Manne, L.L., Brooks, T.M. & Pimm, S.L. (1999) Relative risk of extinction of passerine birds on continents and islands. Nature, 399, 258261.CrossRefGoogle Scholar
Meier, A.J., Noble, R.E. & Zwank, P.J. (1990) Criteria for the introduction of the St. Croix ground lizard. New York State Museum Bulletin, 471, 154156.Google Scholar
Ostendorf, B., Boardman, W.S. & Taggart, D.A. (2016) Islands as refuges for threatened species: multispecies translocation and evidence of species interactions four decades on. Australian Mammalogy, 38, 204212.CrossRefGoogle Scholar
Parlato, E.H. & Armstrong, D.P. (2012) An integrated approach for predicting fates of reintroductions with demographic data from multiple populations. Conservation Biology, 26, 97106.CrossRefGoogle ScholarPubMed
Rivera-Milán, F.F., Boomer, G.S. & Martínez, A.J. (2016) Sustainability assessment of plain pigeons and white-crowned pigeons illegally hunted in Puerto Rico. The Condor, 118, 300308.Google Scholar
Sax, D.F. & Gaines, S.D. (2008) Species invasions and extinction: the future of native biodiversity on islands. Proceedings of the National Academy of Sciences of the United States of America, 105, 1149011497.CrossRefGoogle ScholarPubMed
Stier, A.C., Samhouri, J.F., Novak, M., Marshall, K.N., Ward, E.J., Holt, R.D. & Levin, P.S. (2016) Ecosystem context and historical contingency in apex predator recoveries. Science Advances, 2, e1501769.CrossRefGoogle ScholarPubMed
Thomas, R. & Joglar, R. (1996) The herpetology of Puerto Rico. Annals of the New York Academy of Sciences, 776, 181196.CrossRefGoogle Scholar
Torres, R.T., Carvalho, J., Serrano, E. & Helmer, W. (2016) Favourableness and connectivity of a Western Iberian landscape for the reintroduction of the iconic Iberian ibex Capra pyrenaica. Oryx, 51, 709717.Google Scholar
Treglia, M.L. & Fitzgerald, L.A. (2011) Translocation of the St. Croix ground lizard to Buck Island Reef National Monument, St. Croix, U.S. Virgin Islands. In Global Re-introduction Perspectives: 2011. More Case Studies from around the Globe (ed. Soorae, P.S.), pp. 109115. IUCN/SSC Re-introduction Specialist Group, Gland, Switzerland and Environment Agency-Abu Dhabi, Abu Dhabi, United Arab Emirates.Google Scholar
Tyson, G.F. (1992) On the periphery of the peripheries: the cotton plantations of St. Croix, Danish West Indies, 1735–1815. The Journal of Caribbean History, 26, 136.Google Scholar
Ward, S., Rodriguez, A. & Morgan, R. (2000) Estate Thomas experimental forest: past, present, and future. In Proceedings of the 5th Annual Caribbean Urban Forestry Conference (ed. Zimmerman, T.W.), pp. 105114. St. Thomas, U.S. Virgin Islands, USA.Google Scholar
Westergaard, W. (1938) A St. Croix Map of 1766: with a note on its significance in West Indian Plantation Economy. The Journal of Negro History, 23, 216228.Google Scholar
Wolf, C.M., Garland, T. & Griffith, B. (1998) Predictors of avian and mammalian translocation success: reanalysis with phylogenetically independent contrasts. Biological Conservation, 86, 243255.CrossRefGoogle Scholar
Wintle, B.A., Bekessy, S.A., Keith, D.A., van Wilgen, B.W., Cabeza, M., Schröder, B. et al. (2011) Ecological-economic optimization of biodiversity conservation under climate change. Nature Climate Change, 1, 355359.CrossRefGoogle Scholar
Yang, D., Song, Y., Ma, J., Li, P., Zhang, H., Price, M.R.S. et al. (2016) Stepping-stones and dispersal flow: establishment of a meta-population of milu (Elaphurus davidianus) through natural re-wilding. Scientific Reports, 6, 27297.CrossRefGoogle ScholarPubMed
Figure 0

Table 1 A ranked list of the proposed areas for potential reintroduction of the St Croix ground lizard Pholidoscelis polops, based on combined scores of habitat suitability, mongoose presence, and mongoose control measures.

Figure 1

Fig. 1 Historic and recent land cover in St Croix, U.S. Virgin Islands. (a) The historic map from 1750 was created by J. Cronenberg and J. von Jaegersber (reproduced with permission of Copenhagen Archives). (b) This map was digitized to show historic land-cover types. Landscape transformation and introduction of mongooses led to the extirpation of the now Endangered St Croix ground lizard Pholidoscelis polops. (c) Land-cover classifications of 2016, matched to the digitized historic land-cover types. Establishment of protected areas, land spared from agriculture, and suburban development resulted in emergent land-cover types, which now include potential habitats for the St Croix ground lizard.

Figure 2

Fig. 2 Suitable habitat for the St Croix ground lizard on St Croix, U.S. Virgin Islands. We used a predictive habitat suitability model, with suitability categories based on threats, land-cover types and ongoing conservation efforts.

Figure 3

Fig. 3 The St Croix ground lizard occurs in four extant populations, on (a) Green Cay, (b) Buck Island, (c) Protestant Cay and (d) Ruth Island. We propose three reintroduction sites on St Croix, at (e) Sandy Point, (f) Altoona Lagoon and (g) Southgate Coastal Preserve. Area of habitat is shown for each site; they are not drawn to scale. The inset map indicates where each site is located on St Croix.

Supplementary material: PDF

Angeli and Fitzgerald supplementary material

Angeli and Fitzgerald supplementary material

Download Angeli and Fitzgerald supplementary material(PDF)
PDF 325.1 KB