Interspecific interactions between an invasive and an imperiled reptile

doi:10.21203/rs.3.rs-2365580/v1

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Interspecific interactions between an invasive and an imperiled reptile

https://doi.org/10.21203/rs.3.rs-2365580/v1

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Invasive species are a major driver in the global decline of biodiversity. Invasive herpetofauna cause ecological harm through different mechanisms that vary in scope and severity, and Florida boasts more established nonnative herpetofauna species than any other region in the world. There, black spiny-tailed iguanas (Ctenosaura similis) are one of several large invasive reptiles known to occupy the burrows of the imperiled, native gopher tortoise (Gopherus polyphemus) and may even exclude tortoises from their burrows. To test the hypothesis that iguanas exclude tortoises from their burrows, we conducted a field study on Gasparilla Island, Florida, USA. We used a burrow scope to estimate occupancy of each species within tortoise burrows at sites with and without sustained iguana removal efforts and modelled co-occurrence patterns between the two species. We used two-species occupancy analyses to test three predictions relating to gopher tortoise burrow use. Our results support the hypothesis that gopher tortoises are excluded from their burrows by black spiny-tailed iguanas. The energetic cost to a tortoise of excavating a new burrow is unknown but may be substantial. In addition, tortoises are more vulnerable to extreme temperatures and predation while searching for a new burrow location and digging a burrow. Our results also show that sustained iguana removal is likely effective at reducing iguana occupancy of tortoise burrows. Other large invasive reptiles and perhaps even some native species typically thought of as “burrow commensals” may have similar deleterious effects on tortoise behavior.

Gopherus polyphemus

Ctenosaura similis

Occupancy modeling

Species interactions

Invasion ecology

Invasive species

Human activities have resulted in species introductions throughout history (Preston et al. 2004), but the rate of introductions has increased drastically since the era of globalization (Meyerson and Mooney 2007). Introductions may be intentional or accidental, via two main pathways. Species may be transported either as “hitchhikers” where organisms stowing away on vehicles or cargo are transported incidentally, or where the organism itself is the commodity being shipped (Hulme 2009). The global trade in exotic pets, a multi-billion-dollar industry, is a prime example of the latter pathway, particularly in the case of reptiles (Lockwood et al. 2019). Invasive species are a major driver of the global decline of biodiversity. They have been the sole cause for the extinction of 34 species and have contributed to the extinction of at least 57 others (Clavero and García-Berthou 2005). Czech and Krausman (1997) suggest that interactions with invasive species is the most frequent, and therefore most important, cause of species endangerment in the U.S., contributing to the endangerment of 305 species classified as threatened or endangered by the United States Fish and Wildlife Service.

The impact of human-facilitated introductions varies greatly among species and their recipient ecosystems (Blackburn et al. 2014). Invasive herpetofauna cause ecological harm through different mechanisms that vary in scope and severity such as competitive exclusion, predation, and pathogen introduction. For example, acoustic competition from invasive Cuban treefrogs (Osteopilus septentrionalis) alters the acoustic community structure of native treefrog calls in the southeastern United States (Tennessen et al. 2016). Cuban treefrogs prey upon native treefrogs (Wyatt and Forys 2004; Glorioso et al. 2010) and abundance of native treefrogs can increase following sustained removal of the invasive predator (Rice et al. 2011). When reared in the presence of Cuban treefrog tadpoles, tadpoles of two native species had reduced growth rates and delayed metamorphosis (Smith 2005), and Cuban treefrogs may also negatively impact native frogs through parasite spillover (Ortega et al. 2022). The introduction of cane toads (Rhinella marina) to Australia precipitated declines of native predators via lethal toxic ingestion of the toads by several varanid lizards (Burnett 1997; Doody et al. 2009) and the northern quoll (Dasyurus hallucatus) (Burnett 1997). Among reptiles, introduction of a colubrid snake (Natrix tessellata) to Lake Geneva, Switzerland led to local declines of native N. maura through competitive exclusion due to trophic overlap (Metzger et al. 2009). The introduction of brown tree snakes (Boiga irregularis) caused the decline or extinction of most of Guam’s endemic avifauna via direct predation (Savidge 1987). These are but a few examples of how invasive amphibians and reptiles negatively affect native species.

An invasive species can exclude a native species by direct competition or indirectly by altering habitat or capitalizing on shared resources. In the former scenario, the removal of the invasive species should result in an increase in abundance of native species if competition was a limiting factor for the native species. (MacDougall and Turkington 2005). Interference competition, namely interspecific territoriality, or competition for microhabitats is one such mechanism by which an invasive species may exclude a native species (Wauters et al. 2002; Gilad 2008; Muñoz-Mas et al. 2017). A better understanding of the interactions between invasive and native species may inform predictions of the relative susceptibility of ecosystems to invasion, enhance methods for removing invasive species, and facilitate predictions of the effects of their removal (Sakai et al. 2001).

Some of the most impactful invasive reptiles in Florida are the Burmese python (Python bivittatus), Argentine tegu (Salvator merianae), green iguana (Iguana iguana), and black spiny-tailed iguana (Ctenosaura similis). Each of these large reptiles has been documented to inhabit burrows of gopher tortoises (Truglio et al. 2008; Engeman et al. 2009a; Hengstebeck 2018). The gopher tortoise is a state-threatened species in Florida whose range has declined substantially mainly due to habitat loss and degradation (Diemer 1986). Burmese pythons have been observed blocking the entrance of a gopher tortoise burrow, preventing a tortoise from exiting (Bartoszek et al. 2018). Black spiny-tailed iguanas will readily enter gopher tortoise burrows and on occasion may even exclude a tortoise from its burrow (Engeman et al. 2009a). Additionally, tegus and black spiny-tailed iguanas are known predators of juvenile tortoises (Avery et al. 2009; Offner et al. 2021). However, the degree to which gopher tortoise populations are negatively affected by these invasive species is unknown.

Black spiny-tailed iguanas are highly territorial, defending their shelters, perches, and adjacent areas from members of their own species (Fitch and Hackforth-Jones 1983; Chowdhury et al. 2012). They may act aggressively towards other species of reptiles even in a non-predatory context (Engeman et al. 2009b). Invasive reptile occupancy of tortoise burrows may affect a tortoise’s ability to use its burrows and carry out normal activities (Engeman et al. 2009a; Bartoszek 2018). Also, disturbance by potential predators to a tortoise burrow is suspected, in some instances, to cause the tortoise to abandon that burrow and dig a new one (Wilson et al. 1994). Understanding interactions between introduced and native species (especially imperiled species) and their implications is essential for effective management and conservation planning. This is especially true considering climate change and resulting distributional shifts of invasive species that may lead to novel species interactions (Gilman et al. 2010; Osland et al. 2021).

However, directly observing interactions in nature can be challenging. Species co-occurrence modelling is often used to infer relationships between competing species. Negative or positive co-occurrence patterns could each be the result of numerous phenomena but examining these patterns may provide insight about how species interact, given a priori knowledge of species’ natural history, which make hypothesized interactions likely (Kass et al. 2020). Multispecies occupancy models (MSOMs) have been used to make inferences about species interactions while accounting for the influence of biotic and abiotic environmental factors as well as interspecific interactions (Richmond et al. 2010; Ladle et al. 2018; Clipp et al. 2021).

Due to the territorial and predatory nature of the iguanas and the fact that both species are diurnal and seek shelter in burrows at night, we hypothesize that iguana use of tortoise burrows may exclude tortoises from their burrows. Specifically, we predict that 1) tortoise occupancy is lower in burrows occupied by iguanas than burrows without iguanas, 2) presence of iguana side-tunnels within tortoise burrows is a proxy for iguana activity and is positively associated with iguana occupancy and negatively associated with tortoise occupancy, and 3) iguana occupancy is lower and tortoise occupancy is higher in sites with ongoing iguana removal. To test our predictions, we conducted a field study in southwest Florida at two sites where both species occur in sympatry; the sites have substantially different iguana management histories.

Study Species

Black spiny-tailed iguanas

Black spiny-tailed iguanas (Ctenosaura similis) are native from southern Mexico to Panama but are considered invasive in Florida (Avery et al. 2014). The species was first introduced to Florida on Gasparilla Island in 1979 through the exotic pet trade and they have since spread across the island. They have become established throughout southwestern Florida and there are also now populations along the southeastern coast and the Florida Keys in residential, commercial, and natural areas (Krysko et al. 2003).

Juveniles mainly feed on invertebrates and their diet shifts towards herbivory with age. However, adults will also prey on invertebrates, other lizards, small birds, small mammals, and turtle hatchlings, including the gopher tortoise (Fitch and Hackforth-Jones 1983; Avery et al. 2009; Krysko et al. 2009; García-Rosales et al. 2020; Furness 2021). Within their native range black spiny-tailed iguanas are known to burrow into earthen banks, and under rocks and logs (Burger and Gochfield 1991). In Florida they burrow around sea walls and rock piles, under houses, and will also inhabit gopher tortoise burrows. They are diurnal and seek these shelters before nightfall, emerging again in the morning. Within tortoise burrows they dig side tunnels into the wall of the main burrow excavated by the tortoise (personal observation, SLM). They are large, highly fecund lizards exceeding 30 cm SVL with clutch sizes up to 62 eggs recorded on Gasparilla Island, FL (Avery et al. 2014).

Gopher Tortoises

Gopher tortoises (Gopherus polyphemus) occur throughout the Southeastern Coastal Plain of the U.S. from Louisiana east to South Carolina and south to Florida. They occur in dry, upland habitats and require well-drained, sandy soils for burrowing and nesting, abundant herbaceous plants for forage, and open canopies that provide adequate sunlight for basking and nesting (Hipes et al. 2000). They are terrestrial turtles, reaching carapace lengths of 31 cm (Ernst et al. 1994). They mature slowly, with females becoming reproductive at 9–21 years depending on geographic location and environmental conditions (Landers et al. 1982; Godley 1989; Mushinsky et al. 1994). They have shovel-like forelimbs adapted for digging long burrows in which they live. Adult burrows average 4.5 m long and 2 m deep. Burrows typically consist of one slightly curving tunnel with a single entrance (Hansen 1963). Soil from the burrow is deposited near the burrow mouth, forming a conspicuous mound (i.e., apron) that is visible even long after a tortoise has abandoned a burrow.

Gopher tortoises spend as much as 80% of their time in their burrows, which they excavate for shelter from extreme temperatures, desiccation, fire, and predators (Hipes et al. 2000). They are diurnal, entering their burrow before nightfall and emerge to forage, thermoregulate, and carry out other activities during the day. Gopher tortoises are active year-round in southern Florida but are least active, spending the most time in their burrows, from December-February. In southern Florida, surface activity occurs between 0700–2000 h during summer months, but only between 1100–1800 h on warmer days during December-February. Activity peaks occur during the hottest hours of afternoon (1300–1600 h) throughout the year (Douglass and Layne 1978).

The number of burrows used per individual tortoise over the course of a year ranges from 1–7 and varies by sex, age class, and population. Older tortoises use more burrows than younger ones and males use more than females (McRae et al. 1981; Diemer 1992; Wilson et al. 1994). Reasons for this variation may include any combination of habitat quality, soil composition, temperature extremes at differing latitudes, breeding behavior differences, and number of disturbances to burrows, such as that of potential predators (Wilson et al. 1994).

Gopher tortoises are ecosystem engineers because their burrows provide refugia, foraging, or reproduction sites to at least 360 other species, some of which are obligate commensals (Jackson and Milstrey 1989). They are considered a keystone species, as tortoise burrow density has been shown to be a strong predictor of diversity and relative abundance of herpetofauna and small mammals (Catano and Stout 2015). Gopher tortoises are federally listed as Threatened in the western portion of their range (U.S. Fish and Wildlife Service 1987), designated as a Threatened species in Florida, and are state protected on some level in every other part of their range (Florida Fish and Wildlife Conservation Commission 2020).

Study Sites

Florida boasts more established nonnative herpetofauna species than any other region in the world. As many as 180 introduced amphibian and reptile taxa have been documented within the state, and of those, at least 63 (dominated by reptiles) are considered established (Krysko et al. 2016). In fact, Florida has three times as many established species of introduced lizards as native lizards (Hardin 2007). The magnitude of herpetofauna invasions in Florida can be attributed to several factors. Florida is a shipping hub with major ports of entry for arrival of wildlife species (both legal and illegal), thus resulting in high propagule pressure, a process known to contribute to invasion success (Lockwood et al 2005). The state has a popular captive wildlife industry, and facilities housing nonnative species (e.g., breeders, retail vendors, individual pet owners) are susceptible to escapes and sometimes intentional releases of unwanted or “seeding” animals (Fujisaki et al. 2010; Episcopio-Sturgeon and Pienaar 2019). Additionally, Florida’s mild climate and abundant rainfall results in a strong climate match for many introduced amphibians and reptiles and climate is recognized an important predictor of invasion success (Bomford et al. 2008; Engeman et al. 2011).

We conducted our study on Gasparilla Island, an 11-km barrier island off the southwest coast of Florida (Fig. 1). The island includes six distinct natural communities: mangrove swamp, beach dune, coastal strand, maritime hammock, estuarine unconsolidated substrate, and marine unconsolidated substrate (Florida Natural Areas Inventory 2010). Most of the island is private property and highly developed, containing many homes, resorts, businesses, and a golf course. We sampled tortoise burrows at two study sites on Gasparilla Island within the beach dune habitat, which we designated as our Private Property (PP) and Gasparilla Island State Park (SP) sites (Fig. 1). At PP, USDA Wildlife Services has conducted ongoing iguana removal efforts, with over 15,000 iguanas removed from an area of about 106-ha since 2008 (Avery et al. 2014; Samantha Watson, personal communication, Feb. 3, 2021; Glenn Mitchell, personal communication, July 18, 2021). On the other hand, iguana management at the SP site has been limited due to a lack of resources and high visibility by park guests to iguana removal efforts. Only ~ 600 iguanas were removed from the 51-ha area since 2012, and there are no records of removals prior to then (Karen Rogers, personal communication Dec. 2, 2021).

Experimental Design

We delineated beach dune habitat within our study sites visually using the World Imagery layer in ArcGIS® Online by Esri (Source: Esri, Maxar, Earthstar Geographics, and the GIS User Community). Although gopher tortoises can occur in coastal strand, we excluded this habitat because of low tortoise burrow density and the difficultly of confidently locating all burrows due to dense vegetation (Lau and Dodd 2015). We generated 200 random points spaced at least 10 m apart within the beach dune at each study site and selected the burrow closest to each random point. We selected the closest burrow by walking to each random point using an ArcGIS® Survey123 map (Esri), staking a long PVC tube in the ground at the point, and walking outwards from there in a gradually expanding spiral until the first burrow was found within ~ 10 m of the point, marking each burrow with a metal ID tag and stake. We discarded points farther than ~ 10 m from a burrow, or where the closest burrow was already marked from another PVC point. We measured burrow widths by inserting calipers 50 cm into the burrow or as deep as possible to compare burrow size-class distributions between sites. Burrow width is strongly correlated with tortoise carapace length (CL) of the resident tortoise (Alford 1980; Martin and Layne 1987) and CL is associated with age in gopher tortoises (Landers et al. 1982). During pilot surveys, we noted iguanas and tortoises in burrows that appeared inactive (e.g., having an entrance filled with debris, no tracks on the burrow apron). Therefore, we considered tortoise burrows with an entrance open enough such that a tortoise could enter without modification as potentially occupied and included them in our surveys regardless of apparent activity status.

We determined the occupancy of tortoise burrows by tortoises and iguanas by inspecting them with a burrow camera (Environmental Management Systems, Canton, Georgia, USA). The camera kit consisted of a 7.6 m scope with a 5 cm diameter camera-head and a “juvenile” camera with a 3.6 m scope with a 2.5 cm camera-head. The camera feed was displayed on a color monitor housed in a watertight Pelican™ case. We scoped burrows from January to March 2022, between sunrise and noon to maximize the likelihood that tortoises and iguanas were inside the burrows. In an occupancy modeling framework, site occupancy is assumed to be constant between surveys, so repeat surveys were conducted back-to-back such that animals would not change locations between burrow surveys on a given day (i.e., we inserted the scope as far as we could down the burrow and any side-tunnels, pulled out the scope, and scoped it again). We treated each pair of surveys at a burrow as a “season” where occupancy in a burrow is assumed to be constant between the two consecutive surveys. Two surveys per season is considered appropriate when detection probability of a species is high (ρ > 0.6) (MacKenzie et al. 2018).

Iguanas frequently dug side-tunnels in the tortoise burrow at angles that were impossible to scope with a standard burrow scope. To help address this, we attached the string of a dive reel to the camera to make it more maneuverable. We positioned the head of the scope in front of a side tunnel and by pulling the string we could lift the head of the scope or turn it to the side to enter a side tunnel that otherwise could not be scoped due to the angle. We recorded the occupancy state of the tortoise burrow as neither (0), only iguana (1), only tortoise (2), or both (3) for each survey, and we recorded the presence of iguana side-tunnels. Iguanas frequently excavated side-tunnels off the main tortoise burrow (Fig. 2) and we fully scoped as many as possible. Most side-tunnels had obvious crest-shaped marks along their roof, and many had obvious iguana tail drags and/or claw marks on their floor.

We surveyed burrows at the PP site for three seasons with two surveys per season and at the SP site for one season, also with two surveys per season. The third season at PP and the single season at SP overlapped in time. Surveys at the PP site in Season 1 occurred from Jan. 3–18, Season 2 from Jan. 19 to Feb. 9, and Season 3 from Mar. 7–22. Burrow surveys for the single season at the SP site occurred Mar. 10–20.

Analysis

We used MSOMs to examine species co-occurrence patterns between black spiny-tailed iguanas and gopher tortoises to test our predictions relating to gopher tortoise burrow use given knowledge of their natural histories. We modelled co-occurrence patterns between the two species while accounting for imperfect detection (MacKenzie et al. 2018; Richmond et al. 2010; Waddle et al. 2010). We interpreted the results of our models using 95% confidence intervals. We included the detection data input and PRESENCE output for each model in Online Resource 2.

To address prediction 1, that tortoise occupancy would be lower given the presence of iguanas, we conducted a single-season two-species occupancy analysis in Program Presence (version 2.13.18) using data from the third season at the PP site and the one season at SP that overlapped temporally, estimating detection and occupancy probabilities of iguanas and detection and marginal occupancy probabilities of tortoises (Rota et al. 2016). This model allowed detection probability to be different for each species. We assumed that this detection probability was fixed and the same for both surveys of a burrow. We did not allow detection probability of tortoises to differ conditional on the presence or absence of iguanas because the presence of an iguana would not affect our ability to detect a tortoise with the burrow scope. We also conducted a model with the same parameterizations except with tortoise occupancy conditional upon the presence of iguanas. We compared the two models using ΔAIC to determine if the model including iguana occupancy as a predictor of tortoise occupancy was more parsimonious (see: “Conditional and marginal occupancy models” in Results.

To address prediction 2, that presence of iguana side-tunnels within tortoise burrows is positively associated with iguana occupancy and negatively associated with tortoise occupancy, we used these same data to conduct a single-season two-species analyses estimating the effects of binary covariate of iguana side-tunnel presence within burrows (present or absent, see “Iguana side-tunnel model” in Results. We did the same to address prediction 3, that iguana occupancy is lower and tortoise occupancy is higher in sites with ongoing iguana removal, but instead including the binary site covariate of site management (PP or SP, see “Private property management model” in Results). We also conducted a multi-season analysis using the three seasons of data from the PP, but the data were insufficient to provide clear results. We included this analysis in Online Resource 3.

We identified a total of 173 gopher tortoise burrows (PP site = 116, SP site = 57) for scoping to determine occupancy of tortoises and iguanas. We surveyed all 116 tortoise burrows during each of the three seasons at our PP site, and all 57 burrows at SP in the single season we sampled there. We were able to completely scope almost all tortoise burrows at least once during each season, except for one burrow in season 2 and three burrows in season 3 at PP, and five burrows in the one season we surveyed at SP.

Almost all iguanas were encountered at the end of their side-tunnels, sometimes partially buried or with only the tail visible (Fig. 3). We did not observe any instances where an iguana side-tunnel led to a secondary opening at the surface. We detected iguana side-tunnels in 87 of the 116 burrows we scoped at the PP site and 39 of the 57 burrows at SP. In total we were able to fully scope 69.5% of all iguana side tunnels that we observed across both sites. We were not able to completely examine the other iguana side tunnels due to sharp-angled turns or multiple forks. The number of iguana side-tunnels per burrow ranged from one to four, including splits where one side-tunnel became two or more. One side-tunnel was most common; 56 (48.3%) and 32 (56.1%) of the burrows with side-tunnels at PP and SP, respectively, had a single side-tunnel. Two side-tunnels were detected in 20 (17.2%) burrows at the PP site and 7 (12.5%) at SP. We never detected more than two iguana side-tunnels in a tortoise burrow at SP, but at our PP site nine (7.8%) burrows had three iguana side-tunnels and two (1.7%) had four side-tunnels.

At our PP site, the number of empty tortoise burrows (i.e., neither tortoise nor iguana detected) ranged from 67.2% (season 1) to 74.1% (season 2). At the SP site, where we only sampled one season, 54.4% of burrows were unoccupied. During that same period 69.5% (season 3) of tortoise burrows were empty at the PP site. We rarely observed instances of burrow co-occupancy and if a burrow was occupied it was almost always by a single tortoise or single iguana (Table 1). We observed multiple iguanas in a burrow on only one occasion, in which two iguanas occupied separate side-tunnels within a burrow at SP. We never observed more than one tortoise in a burrow. We found that PP had a greater proportion of wider tortoise burrows and SP had a greater proportion of narrower tortoise burrows (Fig. 4). Three burrows at the State Park could not be properly measured due to vegetation or partial collapse upon returning for measurements (Online Resource 1).

Table 1

Seasonal detections of black spiny-tailed iguanas (*Ctenosaura similis*) and gopher tortoises (*Gopherus polyphemus*) during burrow surveys from January to March, 2022 on Gasparilla Island, Florida, USA
Site-Season	Neither	Iguana Only	Tortoise Only	Both	Total
PP-season 1	78	17	19	2	116
PP-season 2	86	15	14	1	116
PP-season 3	81	12	22	1	116
SP-season 3	31	21	4	1	57

Occupancy Analyses

Naïve occupancy (not accounting for imperfect detection) was 0.24 for iguanas and 0.16 for tortoises across both sites using data from the third season at PP and the one season at SP. Estimated probability of detection was ρ = 0.89 (95% CI 0.79–0.95) for iguanas and 1.0 for tortoises. Detection probability for tortoises was estimated at effectively 1.0, which is atypical for wildlife surveys, but to be expected in the case of surveying gopher tortoises with a burrow scope. The tortoises are generally nearly the diameter of the burrow and could only be missed if they were farther back in the burrow than could be reached with the scope, and very few tortoise burrows could not be scoped entirely at our sites.

Conditional And Marginal Occupancy Models:

To test our first prediction, that tortoise occupancy would be lower given the presence of iguanas, we first used AIC values to compare the fit of the conditional and marginal occupancy models to the data. The conditional and marginal occupancy models were similarly parsimonious, though the conditional model had a slightly lower AIC (ΔAIC = 1.59). In the conditional occupancy model, the probability of iguana occupancy was ΨIg = 0.24 (95% CI 0.18–0.31). The probability of tortoise occupancy given iguana absence was ΨTort|Ig.Ab = 0.19 (95% CI 0.13–0.27) and the probability of tortoise occupancy given iguana presence was ΨTort|Ig.Pr = 0.07 (95% CI 0.02–0.20; Fig. 5). The mean estimates support our prediction of lower tortoise occupancy in the presence of iguanas. Still, there is moderate uncertainty associated with these estimates due to the limited number of observations of burrow co-occupancy. There were only three instances of species co-occupancy in the single season data set, and limited co-occupancy would be expected if tortoises avoid burrows containing iguanas.

Iguana Side-tunnel Model:

Iguana occupancy was positively associated with the presence of iguana side-tunnels (prediction 2). The probability of iguana occupancy given the presence of iguana side-tunnels was ΨIg.T = 0.30 (95% CI 0.22–0.38) and the probability of iguana occupancy given the absence of iguana side-tunnels was ΨIg.NT = 0.10 (95% CI 0.04–0.22). The occupancy probability of tortoises was lower in burrows with side tunnels (ΨTort.T = 0.12 [95% CI 0.07–0.19]), than without side-tunnels (ΨTort.NT = 0.26 [95% CI 0.16–0.40; Fig. 5]). The connection between iguana side-tunnels and iguana occupancy is obvious in hindsight but we did not anticipate that iguanas would be observed almost exclusively within side-tunnels, so we included that parameter for reference. However, the estimate of tortoise occupancy given the presence of iguana side-tunnels is more informative, indicating that tortoises may avoid using burrows with higher levels of iguana disturbance, though there is some uncertainty in this estimate.

Private Property Management Model:

The probability of iguana occupancy was lower where iguanas are actively managed (prediction 3) by USDA (ΨIg.PP = 0.13 [95% CI 0.08–0.21]), whereas the probability of iguana occupancy within our SP site without consistent iguana removal was ΨIg.SP = 0.46 (95% CI 0.34–0.59; Fig. 5) indicating that iguana occupancy was negatively associated with iguana management at the PP site. In contrast, the probability of tortoise occupancy was higher at the managed site (ΨTort.PP = 0.11 [95% CI 0.03–0.30]), compared to the SP site (ΨTort.SP = 0.05 [95% CI 0.02–0.17; Fig. 5]). The difference between ΨIg.PP and ΨIg.SP was clear, but the difference between ΨTort.PP and ΨTort.SP is less certain given overlapping confidence intervals.

Our results show that mean tortoise occupancy is lower in burrows occupied by iguanas or in burrows with iguana side-tunnels, and that tortoise occupancy is higher in areas actively managed to remove iguanas. In total, these results suggest an overall negative effect of iguana presence on tortoise occupancy. Nevertheless, our occupancy estimates have moderate uncertainty due to limited number of detections. The SP site had a higher proportion of small (i.e., juvenile) burrows (Fig. 4). Across their range, the average number of burrows used per individual tortoise varies by population, and disturbances by potential predators may cause juvenile tortoises abandon an active burrow to dig a new one. Differences in the number of these disturbances may help explain the variation in average number of burrows used by juvenile tortoises among populations (Wilson et al. 1994). This is in line with our findings of the SP site having a greater proportion of smaller burrows with higher iguana occupancy and lower tortoise occupancy than PP (we found 11.4 burrows/tortoise at SP and 5.0 burrows/tortoise at PP). This also supports the hypothesis that iguana presence excludes tortoises from their burrows, with iguana disturbance causing tortoises, especially juveniles, to abandon their current burrows and dig new ones. Across their range, coastal dunes populations of gopher tortoises are poorly studied, but our finding at SP of 11.4 burrows per tortoise is considerably higher than we have seen in the literature (McRae et al. 1981; Diemer 1992, Wilson et al. 1994), and more than double what we found at PP.

Most of the species that inhabit gopher tortoise burrows are often referred to as “burrow commensals.” However, by definition, a commensal relationship is one in which one species is benefitted and the other is neither benefitted nor harmed. Of the hundreds of native species documented to occupy gopher tortoise burrows, some are known predators of small tortoises, such as the eastern indigo snake (Drymarchon couperi) (Vetter 1970, Stevenson et al. 2010), and the eastern coachwhip (Masticophis flagellum) (Douglass and Winegarner 1977). There are numerous anecdotal reports of predation on tortoises by a variety of suspected predators, but quantitative estimates of these interactions are lacking (Wilson 1991). We propose that these and other large native species frequently referred to as “burrow commensals,” may disturb tortoises and cause them to abandon active burrows, like the black spiny-tailed iguanas did at our sites. Little is known about exactly how these species interact, especially inside burrows (Pike and Grosse 2006). However, Melanson (2021) reported burrow “blocking” and “charging” behaviors by gopher tortoises towards eastern cottontails (Sylvilagus floridanus). Gapsarilla Island State Park staff reported a similar observation of a “stand-off” as a black spiny-tailed iguana approached a tortoise which blocked the burrow entrance (Fig. 6). The iguana eventually left without entering the burrow. In the following days, both species were seen using the burrow, and eventually only the iguana was seen at the burrow (park staff, personal communication).

The precise mechanism by which tortoises avoid or are excluded by iguanas is still unclear. However, we know that gopher tortoises have acute olfactory senses and that chemical cues from conspecifics can elicit avoidance responses (Kelley et al. 2022). Furthermore, gopher tortoises have the largest otolith of any extant tetrapod, making them highly sensitive to seismic vibrations produced by potential predators near or in their burrow (Bramble and Hutchinson 2014; see also Radzio and O’Connor 2017). It is unknown if the tortoises recognize these species as predators, or are simply agitated by their activity within the tortoise burrow. We suspect that a combination of nuisance interactions inside of or near burrows as well as failed predation attempts (in the case of juvenile tortoises) or acts of aggression by iguanas may drive tortoises to leave a burrow and excavate a new one.

Management Implications

Typically, if a land manager observes numerous juvenile tortoise burrows in an area, they may assume there are many juvenile tortoises in the area and a high level of recruitment in the population (Alford 1980). In contrast, our findings suggest that in areas where black spiny-tailed iguanas or other large invasive reptiles also occur (see below), this may instead be the result of tortoises, especially juveniles, digging extra burrows as a response to disturbance from the iguanas. Therefore, we urge land managers to use methods other than just counting burrows and applying a standard tortoise/burrow correction factor from the literature to estimate the population size of their resident tortoises, especially for small burrows.

We rarely observed instances of multiple iguanas occupying a burrow simultaneously, so it may be advisable for iguana trappers to cease trapping at a burrow once an iguana has been captured and move the trap to another burrow. That said, our data do not allow us to estimate how long it may take for another iguana to begin use of a newly vacant tortoise burrow. Also, our observations pertain to overnight burrow use during the winter season and burrow activity by iguanas may differ during the day and at other times of the year. Simultaneous use of a tortoise burrow by multiple iguanas has been documented during the daytime (McKercher 2001; Engeman et al. 2009a; Personal Observation), but this may be a result of iguanas fleeing from approaching humans and may be less frequent otherwise. It is also important to note that we observed many iguanas in burrows which appeared from the surface to be inactive, with the entrance filled with debris and lacking any ground sign. Therefore, iguana trapping efforts should not a priori exclude burrows in this condition.

Although our study was observational in nature, our data also support the idea that the ongoing iguana removal effort by USDA at our PP site has reduced the iguana density and iguana occupancy of tortoise burrows. Thus, we urge land managers to remove invasive black spiny-tailed iguanas, especially where they co-occur with imperiled gopher tortoises. Our findings support the notion the tortoises inhabiting Gasparilla Island State Park (our SP site) would benefit from the initiation of sustained iguana removal plan and the same can be said for other areas in Florida with both species co-occur. Additionally, other large invasive reptiles known to use tortoise burrows such as green iguanas, Argentine tegus, and Burmese pythons likely have similar effects on tortoise activity and effort should be allocated for their removal as well. Argentine tegus are especially concerning as they are less climactically restricted than iguanas and pythons, which are climatically constrained to southern Florida (Krysko et al. 2003; Krysko et al. 2007; Pyron et al. 2008). Argentine tegus already have a latitudinally wider established range in the U.S. than green iguanas or Burmese pythons that includes multiple locations in Florida (Pernas et al. 2012; Krysko et al. 2019; Offner et al. 2021; EDDMapS 2022) and a site in southeastern Georgia (Haro et al. 2020). Moreover, species distribution models predict that the entire range of the gopher tortoise in the U.S. is climatically suitable for colonization by Argentine tegus (Jarnevich et al. 2018; Goetz et al. 2021).

Our data indicate gopher tortoises are excluded from their burrows by black spiny-tailed iguanas, likely abandoning their burrows and excavating new ones because of iguana disturbance. However, the mechanism by which this is occurring and the ultimate impacts on the tortoise population are uncertain. The daily energy expenditure of gopher tortoises has been studied (Jodice et al. 2006), but we found no reports specifically on the energetic cost of burrow excavation, which we suspect could be substantial given the size of the tortoise as compared to the length of their burrows. It has been reported in a popular coffee-table book that gopher tortoises may dig a new burrow in one or two days (Ashton and Ashton 2004), but we found no documentation of this in the primary literature. Studies emphasize the energetic cost of missed foraging and thermoregulatory opportunities when tortoises retreat into their burrows as a predator avoidance response, as well as the increased vulnerability to predation while basking outside the burrow (Wilson 1991; Radzio and O’Connor 2017). The energetic cost and exposure to predators is certainly even higher during the search for a new locations and the excavation additional burrows. Besides the energetic cost and increased exposure to predation, tortoises would also be more vulnerable to temperatures and desiccation until their new burrow is complete. Additionally, as both true islands and habitat islands resulting from habitat fragmentation are considered sub-optimal habitats for gopher tortoises from which they cannot easily disperse (Mushinsky and McCoy 1994), displacement by iguanas in these areas with limited space and resources could lead to increased intraspecific competition among tortoises and stress marginal populations even further (Blonder et al. 2021).

Across their range in the Southeast, gopher tortoises continue to face numerous threats. Habitat loss, fragmentation, and degradation (e.g., fire suppression) are among the most pronounced (Diemer 1986; Mushinsky and Gibson 1991; Basiotis 2007). Additional threats include climate change, disease, vehicle induced mortality, and occasionally poaching (Gibbs and Shriver 2002; Mushinsky et al. 2006; Diemer et al. 2010; McCoy et al. 2011; Blonder et al. 2021). Considering this, novel, deleterious interactions with black spiny-tailed iguanas and other invasive reptiles including Argentine tegus, green iguanas, and Burmese pythons, become even more important to the remaining populations. The nature and impact of these interactions should be investigated further and considered in conservation planning for the imperiled gopher tortoise.

Data Availability

All data generated or analysed during this study are included in this published article [and its supplementary information files].

Funding

This research was funded by the United States Department of Agriculture, Wildlife Services (#AP20WSNWRC00C036) and the University of Florida’s Department of Wildlife Ecology and Conservation.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author Contributions

Bryan Kluever, Sean McKnight, Steve Johnson and Darryl MacKenzie conceived and designed the study. Material preparation and data collection were performed by Sean McKnight, data analysis was performed by Sean McKnight, Darryl MacKenzie, Steve Johnson, and Miguel Acevedo. The first draft of the manuscript was written by Sean McKnight and Steve Johnson and all authors contributed to revisions of the manuscript. All authors read and approved the final manuscript.

Acknowledgements

We thank John Humphrey for advice on study design interpretation of results, Glenn Mitchell for assistance in the field, Gasparilla Island State Park Staff for sharing their observations, the Florida Fish and Wildlife Conservation Commission (permit #LSSC-20-00006), Florida Department of Environmental Protection (permit #12172114), United States Department of Agriculture (QA-3410), and University of Florida IACUC (protocol #202111338). We also thank the reviewers for their consideration of our work.

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ESM1.pdf
ESM 1. Table of gopher tortoise burrow widths
ESM2.pdf
ESM 2. Program PRESENCE outputs for each model
ESM3.pdf
ESM 3. Analysis of Multi-season occupancy model
ESM4.pdf
ESM 4. Presence/absence and site covariate data used for single season occupancy models

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Interspecific interactions between an invasive and an imperiled reptile

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Abstract

Figures

Introduction

Methods

Study Species

Black spiny-tailed iguanas

Gopher Tortoises

Study Sites

Experimental Design

Analysis

Results

Occupancy Analyses

Conditional And Marginal Occupancy Models:

Iguana Side-tunnel Model:

Private Property Management Model:

Discussion

Management Implications

Conclusions

Declarations

References

Supplementary Files

Status:

Version 1