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.
Open access
