Abstract

The gopher frog Lithobates capito is one of the most terrestrial frogs in the southeastern United States and often inhabits gopher tortoise burrows Gopherus polyphemus outside of the breeding season. Gopher frog populations have declined, and the species is under review for listing as threatened or endangered under the U.S. Endangered Species Act. Much of our knowledge on the status of gopher frogs is based on detections of larvae at breeding wetlands, which can be challenging because of environmental variability and provides no information on the terrestrial life stages of the species. Therefore, an alternative method is called for. We recorded observations of gopher frogs during gopher tortoise surveys at four conservation lands in Florida and used line-transect distance sampling to estimate frog abundance. We also recorded burrow size, incidence of frog co-occupancy with tortoises, and distance from frog-occupied burrows to breeding wetlands. We observed 274 gopher frogs in 1,097 tortoise burrows at the four sites. The proportion of burrows occupied by gopher frogs among sites ranged from 0.17 to 0.25. Gopher frog abundance in tortoise burrows was 742 (512–1,076 95% CL) at Etoniah Creek State Forest, 465 (352–615) at Ft. White Wildlife Environmental Area, 411 (283–595) at Mike Roess Gold Head Branch State Park, and 134 (97–186) at Watermelon Pond Wildlife Environmental Area. We observed up to four frogs in a single burrow. The proportion of frogs detected in burrows occupied by a gopher tortoise ranged from 0.46 to 0.79 among sites, and overall, gopher frogs preferred burrows occupied by tortoises over unoccupied burrows (χ2 = 15.875; df = 3; P = 0.001). Gopher frogs used burrows from 7 to 43 cm in width; mean width of frog-occupied burrows did not differ from that of unoccupied burrows (F1,3 = 0.049, P = 0.825). Distance from frog-occupied tortoise burrows to the nearest breeding wetland ranged from 141 to 3,402 m. Our data on gopher frogs collected in conjunction with gopher tortoise monitoring efforts using line-transect distance sampling and burrow cameras provided novel information on frog abundance in their terrestrial habitat and required no additional effort. However, the extent to which frogs use tortoise burrows relative to other available refuges (small mammal burrows, stumps, or other structures) is unknown; thus, our estimates should be considered conservative. We suggest that terrestrial abundance estimates for gopher frogs can complement efforts to monitor breeding activity to provide a more comprehensive means of monitoring population trends in this cryptic species.

Introduction

The gopher frog Lithobates capito has declined across much of its range in the southeastern United States and is under review for listing as threatened or endangered under the U.S. Endangered Species Act (ESA 1973; Center for Biological Diversity 2012; USFWS 2015). The species breeds in seasonally inundated isolated wetlands and lives a largely fossorial existence in upland habitats during the nonbreeding season. Within uplands, gopher frogs often inhabit burrows excavated by gopher tortoises Gopherus polyphemus, where the ranges of the two species overlap (Test 1893; Carr 1940; Franz 1984; Cash et al. 2008; Roznik and Johnson 2009a). Gopher frogs also use southeastern pocket gopher Geomys pinetis, oldfield mouse Peromyscus polionotus, and Florida mouse Podomys floridanus burrows, weathered stumps, and other subterranean refuges (Carr 1940; Lee 1968; Gentry and Smith 1968; Franz 1984; Roznik and Johnson 2009a; Humphries and Sisson 2012). The decline in gopher frog populations is believed to be a result of land use change, including conversion of open pine (Pinus spp.) woodlands to urban lands and pine plantations, succession of pine woodlands to hardwood-dominated forests, and herbaceous seasonal wetlands to tree- and shrub-dominated wetlands due to fire suppression (Jensen and Richter 2005). Effects of the decline of two burrowing species, the gopher tortoise and southeastern pocket gopher (Smith et al. 2006; Parsons 2019), on gopher frog populations are unknown. However, the importance of terrestrial refuges for seasonal wetland-breeding amphibians is well-documented (Rothermel and Luhring 2005; Todd and Rothermel 2006; Roznik and Johnson 2009b; Semlitsch et al. 2009; Humphries and Sisson 2012).

Much of our knowledge of the status of gopher frogs is based on monitoring breeding activity at wetlands, including intensity of male breeding choruses and presence and abundance of egg masses and larvae (Palis 1998; Greenberg 2001; Jensen et al. 2003). These methods provide important information on annual reproductive effort but only indirect information on abundance, which may lead to false assumptions about the status of the species. Moreover, detecting breeding activity can be challenging on account of environmental variation (e.g., calling and breeding activity varies with local weather conditions, and wetlands may not fill at all in drought years). Importantly, monitoring breeding activity alone provides little information on the status of terrestrial life stages (juvenile and adult) of gopher frogs. With the exception of a few studies of terrestrial movements of gopher frogs using radiotelemetry (Blihovde 2006; Roznik and Johnson 2009a, 2009b; Humphries and Sisson 2012), we know little about gopher frogs in their terrestrial habitat. In Florida and Georgia, where the species is often associated with gopher tortoise burrows (Franz 1984; Greenberg 2001; Blihovde 2006; Roznik and Johnson 2009a) and tortoise abundance is monitored through systematic burrow surveys (Smith et al. 2009a; USFWS 2012), gopher frogs are often observed in tortoise burrows (L. Smith, Jones Center at Ichauway, personal observation). These observations offer an opportunity to concurrently monitor gopher tortoise and gopher frog populations.

Surveys for gopher tortoises also provide an opportunity to evaluate characteristics of tortoise burrows used by gopher frogs. Gopher tortoises excavate burrows in canopy gaps in uplands with well-drained sandy soils (Auffenberg and Franz 1982). Burrows are half-moon shaped, approximately as wide as the carapace length of the tortoise, and average about 4.5 m in length (Hansen 1963). Tortoises generally excavate and use multiple burrows, and in some populations, there may be three to four times as many burrows as tortoises (L. Smith, Jones Center at Ichauway, personal observation). Tortoise burrows are used by >360 species in addition to gopher frogs, but gopher frogs are among the few vertebrates that inhabit burrows, rather than just using burrows opportunistically (Jackson and Milstrey 1989). Mark–recapture and radio telemetry studies revealed that gopher frogs exhibit fidelity to individual gopher tortoise burrows but also use tortoise burrows as temporary refuges on breeding migrations (Franz 1984; Blihovde 2006; Roznik and Johnson 2009a).

In this study, we recorded observations of gopher frogs in gopher tortoise burrows during line-transect distance sampling (LTDS, Buckland et al. 2001) for gopher tortoises on conservation lands in Florida. These observations allowed us to estimate abundance and density for this commensal species in tortoise burrows at four sites. Line-transect distance sampling is a widely used, efficient, and statistically robust method to estimate density and abundance of wildlife species (Buckland et al. 2001; Thomas et al. 2010). The method includes counting objects observed from transects and measuring the distance from transects to each object; it assumes all objects on the line are detected but allows more distant objects to be missed, based on the fact that an observer's ability to detect objects decreases with distance from the transect (Buckland et al. 2001). Line-transect distance sampling lends itself well to surveys for gopher tortoise burrows, which are generally conspicuous objects on the landscape (Smith et al. 2009a; Stober and Smith 2010; but see Howze and Smith 2019) and occupancy of burrows by the target organism, in this case gopher frogs, can be assessed with camera systems. In addition to estimating gopher frog abundance in tortoise burrows, we examined the size (width) of burrows used by gopher frogs and the frequency of co-occupancy with tortoises. Lastly, we calculated the mean distance from frog-occupied tortoise burrows to known gopher frog breeding wetlands at the four sites. This study provides the first estimates of gopher frog abundance in tortoise burrows, and more importantly demonstrates how a survey method for estimating gopher tortoise abundance can also provide information on adult and juvenile terrestrial life stages of this otherwise cryptic anuran.

Study Sites

Surveys took place at four state conservation lands in peninsular Florida: Etoniah Creek State Forest (Putnam County; hereafter, Etoniah Creek), Ft. White Wildlife Environmental Area (Gilchrist County; Ft. White), Mike Roess Gold Head Branch State Park (Clay County; Gold Head Branch), and Watermelon Pond Wildlife Environmental Area (Alachua County; Watermelon Pond). Etoniah Creek had scrub, sandhill, and mesic pine flatwoods vegetation [see Kawula and Redner (2018) for detailed descriptions of vegetation types]. There were five confirmed gopher frog breeding wetlands on Etoniah Creek (K. Enge, Florida Fish and Wildlife Conservation Commission, unpublished data). Ft. White was dominated by sandhill vegetation with two extant gopher frog breeding wetlands; a third breeding wetland was located immediately adjacent to the site. Upland vegetation types at Gold Head Branch included sandhill and xeric scrub. There was one confirmed gopher frog breeding wetland at Gold Head Branch. Watermelon Pond had sandhill vegetation and pine plantations with a large wetland complex (Watermelon Pond). There were three confirmed gopher frog breeding wetlands on properties adjacent to Watermelon Pond, but the species had not been detected breeding in wetlands on site.

Methods

Our original intent was to survey gopher tortoise populations at the four conservation lands, so we first delineated suitable tortoise habitat based on Florida Cooperative Land Cover data (Florida Fish and Wildlife Conservation Commission 2019). We considered the following land cover types as suitable habitat: upland pine, sandhill, scrub, scrubby flatwoods, dry mesic flatwoods, and pine plantations. These land cover types were merged in ArcGIS v. 10.2 (ESRI, Redland, CA) to create a tortoise sampling area at each site. We excluded wetlands, hardwood forest, wet flatwoods, and urban land cover types from sampling areas, because they are generally not suitable tortoise habitat. Thus, surveys and estimates of density and abundance for gopher frogs in this study applied to all suitable gopher tortoise habitat at each site.

Line-transect distance sampling is the recommended method for gopher tortoise surveys (Smith et al. 2009b; USFWS 2015; Smith and Howze 2016). In a gopher tortoise survey using LTDS methods, gopher tortoises and their burrows are the search objects, and the observations of tortoises are used to estimate abundance. For this study on gopher frogs, the survey design and sampling methods (described below) were those used for gopher tortoise surveys (Smith and Howze 2016), except that we focused the analysis on tortoise burrows occupied by gopher frogs rather than tortoises. To determine the effort (total transect length) needed to obtain a sufficient sample size in the LTDS survey to generate a precise estimate (coefficient of variation <0.20; Buckland et al. 2001), we conducted preliminary surveys at randomly placed transects within the delineated sampling areas at each site (Smith et al. 2009b). We searched transects for tortoise burrows on or near the line and scoped burrows to determine whether a tortoise was present. We used these data to calculate a tortoise encounter rate (tortoise observed per kilometer searched) for each site. We then used the open source software program Distance (Distance Project 2020; Thomas et al. 2010) to create a systematic-random transect design for LTDS. In a systematic random design, transects are generated from a random starting point and are parallel and evenly spaced across the sampling area.

We used a three-observer approach for field sampling (Buckland et al. 2001; Smith et al. 2009b; Smith and Howze 2016), and collected spatial data (transect start and end points and burrow locations) using a Nomad 900B Hand Held Computer (Trimble Navigation, Ltd., Sunnyvale, CA) with a Hemisphere Crescent A101 smart GPS antenna (CSI Wireless, Calgary, AB, Canada). This system allowed submeter accuracy and real-time data collection. We calculated transect length and perpendicular distance from burrows to the transect after the fact using ArcGIS v.10.2 (ESRI). In the three-observer field approach, the primary observer searched for burrows on or within 2 m of the line while navigating with the Nomad, using ArcPad™ software (ESRI). The second and third observers surveyed the area up to approximately 5 m on either side of the line, taking care to observe all burrows between themselves and the line. We pooled observations of all three observers on each transect for analyses (Buckland et al. 2001; Smith et al. 2009b; Smith and Howze 2016).

We measured the width of all tortoise burrows (to the nearest 1 cm) 50 cm inside the opening using burrow calipers. Burrow width is roughly equal to tortoise length, which was used to describe the demographic structure of the populations (adults versus juveniles; Alford 1980). We searched all burrows with a camera equipped with a 6.4-cm-diameter head for large burrows and a 2.5-cm-diameter camera head for small burrows (Environmental Management Systems, Canton, GA). We recorded observations of gopher frogs, whether a burrow was occupied by a tortoise, or if we were unable to determine occupancy (due to obstructions within the burrow). To minimize risk of spreading pathogens, we disinfected the burrow camera head and cables using Clorox Disinfecting Wipes™ at the end of each day and between sites.

Data analyses

For this study, we used transect length sampled, perpendicular distances from all burrows to transects, and mean “cluster size” to calculate gopher frog density and abundance at each site (Buckland et al. 2001; Thomas et al. 2010). Mean cluster size was the proportion of occupied burrows (Stober et al. 2017), which we estimated in Distance (Distance Project 2020), and was the value used to convert burrow density to frog density. Burrows were our search objects; therefore, using all burrows (occupied and unoccupied) to develop the detection function increased the sample size, thus increasing the precision of our estimates (Thomas et al. 2010; Stober et al. 2017). We estimated density and abundance using the conventional distance sampling engine in Program Distance. We right-truncated data to remove the most distant observations (5%) to improve model fit (Thomas et al. 2010). The conventional distance sampling engine in Program Distance uses a semiparametric detection function modelling framework (Buckland and Turnock 1992), where a parametric key function may be paired with series adjustment terms (Thomas et al. 2010). Key functions include uniform, half-normal, hazard-rate, and negative exponential distributions. Adjustments terms can be cosine, Hermite, or simple polynomials (Thomas et al. 2010). We selected the appropriate combination of key function and adjustment terms in our analyses using Akaike's Information Criteria for model selection (Akaike 1973; Burnham and Anderson 2002).

We used the same LTDS analytical approach (described above) to estimate gopher tortoise burrow density in order to examine the relationship between burrow density and gopher frog density. We used an analysis of variance to test for differences between mean size of burrows used by gopher frogs and burrows not occupied by frogs, and a Pearson's chi-squared test to determine if frogs occurred more often in burrows with or without gopher tortoises. We ran these analyses in Program R Statistical Package (R Core Team 2013). Lastly, we calculated the straight-line distance from burrows to the nearest confirmed gopher frog breeding wetland (K. Enge, Florida Fish and Wildlife Conservation Commission, unpublished data) using ArcGIS software v.10.2.

Results

We surveyed 1,496 ha of habitat at Etoniah Creek, 328 ha at Ft. White, 1,912 ha at Gold Head Branch, and 133 ha at Watermelon Pond. Surveys occurred in September, October, and December 2014 at Ft. White, Gold Head Branch, and Watermelon Pond and in June, August, September, and November 2015 at Etoniah Creek. In total, we observed 274 gopher frogs in 1,097 gopher tortoise burrows at the four sites (Table 1; Data S1–S4, Supplemental Material). Gopher frog abundance estimates in tortoise burrows were 742 (512–1,076 95% confidence limits, CL) at Etoniah Creek, 465 (352–615) at Ft. White, 411 (283–595) at Gold Head Branch, and 134 (97–186) at Watermelon Pond. Gopher frog density was highest at Ft. White with 1.42 (1.07–1.88) frogs/ha, followed by Watermelon Pond with 1.01 (0.72–1.40), Gold Head Branch with 0.54 (0.38–0.79), and Etoniah Creek with 0.50 (0.34–0.72) frogs/ha (Table 2). Coefficients of variation for these estimates ranged from 0.14 at Ft. White to 0.19 at Etoniah Creek and Gold Head Branch (Table 2).

Table 1.

Gopher frog Lithobates capito data collected at gopher tortoise Gopherus polyphemus burrows during systematic gopher tortoise surveys using line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. SF = state forest, SP = state park, WEA = wildlife environmental area.

Gopher frog Lithobates capito data collected at gopher tortoise Gopherus polyphemus burrows during systematic gopher tortoise surveys using line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. SF = state forest, SP = state park, WEA = wildlife environmental area.
Gopher frog Lithobates capito data collected at gopher tortoise Gopherus polyphemus burrows during systematic gopher tortoise surveys using line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. SF = state forest, SP = state park, WEA = wildlife environmental area.
Table 2.

Gopher frog Lithobates capito density (D, frogs/ha) and abundance (N) in gopher tortoise Gopherus polyphemus burrows based on line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) using burrows as the search objects. All burrows were used to develop the detection function and burrows occupied by gopher frogs were designated as “clusters” (Thomas et al. 2010). Selection of the appropriate combination of key function (uniform, half-normal, and hazard rate) and adjustment terms (cosine or simple polynomials; Thomas et al. 2010) was accomplished using Akaike's Information Criteria for model selection (Akaike 1973; Burnham and Anderson 2002). Data were right-truncated to remove the most distant observations (5%) to improve model fit. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. Effort = total length of transect sampled. ESW = effective strip width, CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher frog) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area.

Gopher frog Lithobates capito density (D, frogs/ha) and abundance (N) in gopher tortoise Gopherus polyphemus burrows based on line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) using burrows as the search objects. All burrows were used to develop the detection function and burrows occupied by gopher frogs were designated as “clusters” (Thomas et al. 2010). Selection of the appropriate combination of key function (uniform, half-normal, and hazard rate) and adjustment terms (cosine or simple polynomials; Thomas et al. 2010) was accomplished using Akaike's Information Criteria for model selection (Akaike 1973; Burnham and Anderson 2002). Data were right-truncated to remove the most distant observations (5%) to improve model fit. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. Effort = total length of transect sampled. ESW = effective strip width, CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher frog) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area.
Gopher frog Lithobates capito density (D, frogs/ha) and abundance (N) in gopher tortoise Gopherus polyphemus burrows based on line-transect distance sampling (Buckland et al. 2001) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) using burrows as the search objects. All burrows were used to develop the detection function and burrows occupied by gopher frogs were designated as “clusters” (Thomas et al. 2010). Selection of the appropriate combination of key function (uniform, half-normal, and hazard rate) and adjustment terms (cosine or simple polynomials; Thomas et al. 2010) was accomplished using Akaike's Information Criteria for model selection (Akaike 1973; Burnham and Anderson 2002). Data were right-truncated to remove the most distant observations (5%) to improve model fit. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. Effort = total length of transect sampled. ESW = effective strip width, CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher frog) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area.

The proportion of tortoise burrows occupied by gopher frogs ranged from 0.17 at Etoniah Creek to 0.25 at Watermelon Pond (Table 1). We observed up to four frogs in a single burrow, and the average number of frogs per occupied burrow ranged from 1.1 at Etoniah Creek and Gold Head Branch to 1.5 at Watermelon Pond. The proportion of frogs detected in burrows occupied by a gopher tortoise ranged from 0.46 at Etoniah Creek to 0.79 at Watermelon Pond (Table 1). Overall, gopher frogs used burrows occupied by gopher tortoises more often than burrows without tortoises (χ2 = 15.875; df = 3; P = 0.001). At Etoniah Creek, gopher frogs were observed in burrows from 7 to 39 cm in width (mean = 29.8, SD = 6.9), as compared with 12–38 cm (mean = 26.7, SD = 5.9) at Ft. White, 13–43 cm (mean = 25.2, SD = 6.6) at Gold Head Branch, and 9–40 cm (mean = 27.0, SD = 8.5) at Watermelon Pond. Burrow width was not significantly different between frog-occupied and unoccupied burrows (F3,1 = 0.049; P = 0.825).

Distance from tortoise burrows occupied by gopher frogs to the nearest known breeding wetland ranged from 141 to 3,402 m and the average distance varied from approximately 1,000 m at Etoniah Creek to >2,200 m at Gold Head Branch (Figure 1). Burrow density estimates were 2.57 (1.95–3.39) burrows/ha at Gold Head Branch, 2.98 (2.23–3.98) burrows/ha at Etoniah Creek, 3.03 (2.40–3.84) burrows/ha at Watermelon Pond, and 5.64 (4.59–6.93) burrows/ha at Ft. White (Table 3). Gopher frog density was highest at the two sites with the highest burrow densities, Ft. White (5.64 burrows/ha, 1.42 frogs/ha) and Watermelon Pond (3.03 burrows/ha, 1.01 frogs/ha; Tables 2 and 3).

Figure 1.

Mean distance from gopher tortoise Gopherus polyphemus burrows to the nearest confirmed gopher frog Lithobates capito breeding wetland at four conservation lands in peninsular Florida in 2014–2015. Error bars depict the standard deviation. All burrows were those where gopher frogs were not detected with a camera scope; Frog burrows were those confirmed to be occupied by gopher frogs with a camera scope. Site abbreviations and sample sizes are as follows: EC = Etoniah Creek State Forest (312 unoccupied burrows, 59 occupied burrows), FW = Ft. White Wildlife Environmental Area (246 unoccupied burrows, 71 occupied burrows), GH = Mike Roess Gold Head Branch State Park (184 unoccupied burrows, 54 occupied burrows), and WP = Watermelon Pond Wildlife Environmental Area (163 unoccupied burrows, 52 occupied burrows).

Figure 1.

Mean distance from gopher tortoise Gopherus polyphemus burrows to the nearest confirmed gopher frog Lithobates capito breeding wetland at four conservation lands in peninsular Florida in 2014–2015. Error bars depict the standard deviation. All burrows were those where gopher frogs were not detected with a camera scope; Frog burrows were those confirmed to be occupied by gopher frogs with a camera scope. Site abbreviations and sample sizes are as follows: EC = Etoniah Creek State Forest (312 unoccupied burrows, 59 occupied burrows), FW = Ft. White Wildlife Environmental Area (246 unoccupied burrows, 71 occupied burrows), GH = Mike Roess Gold Head Branch State Park (184 unoccupied burrows, 54 occupied burrows), and WP = Watermelon Pond Wildlife Environmental Area (163 unoccupied burrows, 52 occupied burrows).

Table 3.

Gopher tortoise Gopherus polyphemus burrow density (D, burrows/ha) and abundance (N) based on line-transect distance sampling (Buckland et al. 2004) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) with burrows as the search objects. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher tortoise burrow) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area. Effort (total transect length) and effective strip width information are presented in Table 1.

Gopher tortoise Gopherus polyphemus burrow density (D, burrows/ha) and abundance (N) based on line-transect distance sampling (Buckland et al. 2004) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) with burrows as the search objects. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher tortoise burrow) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area. Effort (total transect length) and effective strip width information are presented in Table 1.
Gopher tortoise Gopherus polyphemus burrow density (D, burrows/ha) and abundance (N) based on line-transect distance sampling (Buckland et al. 2004) at four Florida conservation lands in 2014–2015. Estimates were derived using the conventional distance sampling engine in Distance (Distance Project 2020; Thomas et al. 2010) with burrows as the search objects. Best fitted models presented here included a uniform (UN) and hazard rate (HR) distribution. CL = confidence limit, CV = coefficient of variation, P = probability of observing an object (gopher tortoise burrow) in the defined area. SF = state forest, SP = state park, WEA = wildlife environmental area. Effort (total transect length) and effective strip width information are presented in Table 1.

Discussion

In this study, we provide the first systematically derived estimates of abundance and density of gopher frogs in gopher tortoise burrows in their terrestrial habitat that we are aware of. Our data were collected in the course of gopher tortoise surveys using line-transect distance sampling, which enabled us also to detect gopher frogs using a burrow camera scope. We observed enough frogs to derive abundance estimates with reasonable precision (coefficients of variation ranged from 0.14 to 0.19; Table 2); gopher frog abundance in burrows varied among the four sites from 134 frogs at Watermelon Pond to 742 gopher frogs at Etoniah Creek. The method was efficient and offers the opportunity to monitor terrestrial gopher frog populations separately or in conjunction with gopher tortoise surveys at sites where the two species co-occur. However, estimates derived with these methods should be considered conservative (lower bound) because gopher frogs use other terrestrial refuges, such as small mammal burrows and stumps (Blihovde 2006; Roznik and Johnson 2009a; Humphries and Sisson 2012), which were not searched in our survey. Also, tortoise burrows may be missed during surveys (Howze and Smith 2019), and we possibly failed to detect all gopher frogs in burrows that were searched with the camera scope. Gopher frogs may use side channels within tortoise burrows (Kinlaw and Grasmueck 2012) or may have been located behind a tortoise in a burrow, where they could not be detected. Moreover, our surveys extended from June to December, and occupancy of tortoise burrows may vary with season (Franz 1984). Adult gopher frogs typically migrate to breeding wetlands in fall or winter, although populations in the southern part of the range may breed in summer (Jensen and Richter 2005).

Our study also provided information about the characteristics of tortoise burrows used by gopher frogs, which may aid in searches for the species. Franz (1984) captured gopher frogs most often in burrows with signs of tortoise activity, which was used as an indication of co-occupancy with a tortoise. Our data also suggest that gopher frogs preferred occupied tortoise burrows. This close association between gopher frogs and tortoises may be related to the presence of invertebrate prey specialized in decomposing tortoise scat within burrows (Jackson and Milstrey 1989). Frogs used burrows of small juvenile tortoises (7 cm in width) as well as adult tortoises (>25 cm in width), as was observed by Blihovde (2006). Our results suggest that searches for gopher frogs should target active (Auffenberg and Franz 1982) or occupied tortoise burrows of all sizes.

On average, across the four sites frogs used burrows from approximately 1,000 to 2,200 m from the nearest known breeding wetland and the maximum distance at which we detected a gopher frog was 3,400 m from a breeding wetland. This confirms that gopher frogs can move long distances into their upland habitats as has reported elsewhere (Carr 1940; Franz et al. 1988; Roznik et al. 2009a; Humphries and Sisson 2012). Interestingly, our surveys did not reveal a clear relationship between burrows occupied by frogs and distance to breeding wetlands as has been described for other pond-breeding amphibians (Semlitsch and Bodie 2003). This may have been a reflection of the scale of our surveys, which were confined to individual conservation lands. It is also likely that unidentified breeding wetlands exist outside the boundaries of our study sites. With more complete knowledge of the location of breeding wetlands, and evidence that frog abundance decreases with distance from wetlands, this distance could be used as an additional covariate in models to estimate gopher frog density and abundance (Marques and Buckland 2003). Consideration of both upland and wetland habitat is important in assessing the status of gopher frog populations and the likelihood of persistence of populations through time (Jensen et al. 2003; Jensen and Richter 2005).

Gopher frog surveys in conjunction with regular gopher tortoise monitoring using LTDS can provide added value to these considerable efforts. As outlined, these methods provide a statistically defensible means of deriving conservative estimates of frog abundance in uplands. Recording gopher frog detections during burrow camera searches is straightforward and only requires training on how to differentiate this species from other anuran burrow associates. To maximize detections of gopher frogs in tortoise burrows, surveys should be scheduled in late spring or summer when the frogs are most likely to be in their terrestrial refuges and recording the size of frogs could provide information on population structure. Additionally, if efficient survey methods can be developed for other terrestrial refuges used by gopher frogs, such as burrows of southeastern pocket gophers Geomys pinetis, more comprehensive abundance estimates could be obtained. Regardless, data from gopher tortoise surveys alone can provide conservative estimates of gopher frog abundance in terrestrial habitats for this cryptic species.

Supplemental Material

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article.

Data S1. Microsoft Excel file of data for gopher frog Lithobates capito observations in gopher tortoise Gopherus polyphemus burrows during line-transect distance sampling at Etoniah Creek State Forest (Etoniah Creek) in Putnam County, Florida, from June, August, September, and November 2015. Data include the site name (Label), area surveyed (Area in hectares), transect identification number (Transect ID), transect length in meters (Transect Length), perpendicular distance from the transect to tortoise burrows (Perp distance), detection (1), nondetection (0) of gopher frogs (Frog), tortoise (Tortoise) and burrow width in centimeters (Burrow Width).

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S1 (30 KB XLSX).

Data S2. Microsoft Excel file of data for gopher frog Lithobates capito observations in gopher tortoise Gopherus polyphemus burrows during line-transect distance sampling at Ft. White Wildlife Environmental Area (Ft. White) in Gilchrist County, Florida, in September 2014. Data include the site name (Label), area surveyed (Area in hectares), transect identification number (Transect ID), transect length in meters (Transect Length), perpendicular distance from the transect to tortoise burrows (Perp distance), detection (1), nondetection (0) of gopher frogs (Frog), tortoise (Tortoise) and burrow width in centimeters (Burrow Width).

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S2 (21 KB XLSX).

Data S3. Microsoft Excel file of data for gopher frog Lithobates capito observations in gopher tortoise Gopherus polyphemus burrows during line-transect distance sampling at Mike Roess Gold Head Branch State Park (Gold Head Branch) in Clay County, Florida, in September and October 2014. Data include the site name (Label), area surveyed (Area in hectares), transect identification number (Transect ID), transect length in meters (Transect Length), perpendicular distance from the transect to tortoise burrows (Perp distance), detection (1), nondetection (0) of gopher frogs (Frog), tortoise (Tortoise) and burrow width in centimeters (Burrow Width).

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S3 (25 KB XLSX).

Data S4. Microsoft Excel file of data for gopher frog Lithobates capito observations in gopher tortoise Gopherus polyphemus burrows during line-transect distance sampling at Watermelon Pond Wildlife Environmental Area (Watermelon Pond) in Alachua County, Florida, in October–December 2014. Data include the site name (Label), area surveyed (Area in hectares), transect identification number (Transect ID), transect length in meters (Transect Length), perpendicular distance from the transect to tortoise burrows (Perp distance), detection (1), nondetection (0) of gopher frogs (Frog), tortoise (Tortoise) and burrow width in centimeters (Burrow Width).

Found at DOI: https://doi.org/10.3966/JFWM-20-030.S4 (26 KB XLSX).

Reference S1.Center for Biological Diversity. 2012. Petition to list 53 amphibians and reptiles in the United States as Threatened or Endangered Species under the Endangered Species Act. 454 pp.

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S5 (3.84 MB PDF).

Reference S2. Franz R. 1984. The Florida gopher frog and Florida pine snake as burrow associates of the gopher tortoise in northern Florida. Pages 16–20 in Jackson DR, Bryant RJ, editors. The gopher tortoise and its community. Proceedings of the 5th annual meeting of the Gopher Tortoise Council, Gainesville, Florida. Gainesville: Florida State Museum, University of Florida.

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S6 (2.67 MB PDF).

Reference S3. Jackson DR, Milstrey EG. 1989. The fauna of gopher tortoise burrows. Pages 86–98 in Diemer JE, Jackson DR, Landers JL, Layne JN, Wood DA, editors. Gopher tortoise relocation symposium proceedings. Tallahassee: Florida Game and Fresh Water Fish Commission Nongame Wildlife Program Technical Report 5.

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S7 (437 KB PDF).

Reference S4. Smith LL, Stober JM, Balbach HE, Meyer WD. 2009b. Gopher tortoise survey handbook. U.S. Army Corps of Engineers. ERDC/CERL TR-09-7.

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S8 (1.49 MB PDF).

Reference S5.[USFWS] U.S. Fish and Wildlife Service. 2012. Candidate conservation agreement for the gopher tortoise (Gopherus polyphemus) eastern population.

Found at DOI: https://doi.org/10.3996/JFWM-20-030.S9 (1.83 MB PDF).

Acknowledgments

This study was funded by the Florida Fish and Wildlife Conservation Commission (Contract #13161). We greatly appreciate logistical support provided by staff with the Florida Fish and Wildlife Conservation Commission, Florida Park Service, Florida Forest Service. We especially thank tortoise survey field crew members J. Heemeyer, M. Dziadzio, R. Holton, N. Schwartz, J. Folkerts, and K. Hengstebeck. Burrow scoping was permitted under Florida Scientific Collection Permits #03241410 and #0403201520. Three anonymous reviewers and the Associate Editor provided comments that improved an earlier version of this manuscript.

Any use of trade, product, website, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

References

Akaike
H.
1973
.
Information theory and an extension of the maximum likelihood principle
.
Pages
267
281
in
Petrov
BN,
Csaki
F,
editors.
2nd international symposium on information theory
.
Budapest
:
Akademia Kiado
.
Alford
RA.
Population structure of Gopherus polyphemus in northern Florida
.
Journal of Herpetology
.
14
:
177
82
.
Auffenberg
W,
Franz
R.
1982
.
The status and distribution of the gopher tortoise (Gopherus polyphemus)
.
Wildlife Research Report 12:95–126.
Blihovde
WB.
2006
.
Terrestrial movements and upland habitat use of gopher frogs in central Florida
.
Southeastern Naturalist
5
:
265
276
.
Buckland
ST,
Anderson
DR,
Burnham
KP,
Laake
JL,
Borchers
DL,
Thomas
L.
2001
.
Introduction to distance sampling: estimating abundance of biological populations
.
Oxford, UK
:
Oxford University Press
.
Buckland
ST,
Anderson
DR,
Burnham
KP,
Laake
JL,
Borchers
DL,
Thomas
L.
2004
.
Advanced distance sampling
.
Oxford, UK
:
Oxford University Press
.
Buckland
ST,
Turnock
BJ.
1992
.
A robust line transect method
.
Biometrics
48
:
901
909
.
Burnham
KP,
Anderson
DR.
2002
.
Model selection and multimodel inference: a practical information-theoretic approach. 2nd edition
.
Springer
:
New York
.
Carr
AF.
1940
.
Contribution to the herpetology of Florida
.
University of Florida Bulletin, Biological Science Series
3
:
1
118
.
Cash
WB,
Jensen
JB,
Stevenson
DJ.
2008
.
Pages
102
104
in
Jensen
JB,
Camp
CD,
Gibbons
W,
Elliott
MJ,
editors.
Amphibians and reptiles of Georgia
.
Athens
:
University of Georgia Press
.
Center for Biological Diversity.
2012
.
Petition to list 53 amphibians and reptiles in the United States as Threatened or Endangered Species under the Endangered Species Act.
454
pp (see Supplemental Material, Reference S1).
Distance Project.
2020
.
Distance, version 7.3
.
Available: http://distancesampling.org/Distance/ (April 2021).
Florida Fish and Wildlife Conservation Commission.
2019
.
Cooperative land cover, version 3.4, Florida Fish and Wildlife Conservation Commission, Tallahassee, FL
.
Franz
R.
1984
.
The Florida gopher frog and Florida pine snake as burrow associates of the gopher tortoise in northern Florida
.
Pages
16
20
in
DR,
Jackson
Bryant
RJ,
editors.
The gopher tortoise and its community. Proceedings of the 5th annual meeting of the Gopher Tortoise Council, Gainesville, Florida
.
Gainesville
:
Florida State Museum, University of Florida
(see Supplemental Material, Reference S2).
Franz
R,
Dodd
CK
Jr,
Jones
C.
1988
.
Rana areolata aesopus (Florida gopher frog). Movement
.
Herpetological Review
19
:
33
.
Gentry
JB,
Smith
MH.
1968
.
Food habits and burrow associates of Peromyscus polionotus
.
Journal of Mammalogy
49
:
562
565
.
Greenberg
CH.
2001
.
Spatio-temporal dynamics of pond use and recruitment in Florida gopher frogs (Rana capito aesopus)
.
Journal of Herpetology
35
:
74
85
.
Hansen
KL.
1963
.
The burrow of the gopher tortoise
.
Quarterly Journal of the Florida Academy of Sciences
26
:
353
360
.
Howze
JM,
Smith
LL.
2019
.
Detection of gopher tortoise burrows before and after a prescribed fire: implications for surveys
.
Journal of Fish and Wildlife Management
10
:
62
68
.
Humphries
WJ,
Sisson
MA.
2012
.
Long distance migrations, landscape use, and vulnerability to prescribed fire of the gopher frog (Lithobates capito)
.
Journal of Herpetology
46
:
665
670
.
Jackson
DR,
Milstrey
EG.
1989
.
The fauna of gopher tortoise burrows
.
Pages
86
98
in
Diemer
JE,
DR,
Jackson
Landers
JL,
JN,
Layne
Wood
DA,
editors.
Gopher tortoise relocation symposium proceedings
.
Tallahassee
:
Florida Game and Fresh Water Fish Commission Nongame Wildlife Program Technical Report 5
(see Supplemental Material, Reference S3).
Jensen
JB,
Bailey
MA,
Blankenship
EL,
Camp
CD.
2003
.
The relationship between breeding by the gopher frog, Rana capito (Amphibia: Ranidae) and rainfall
.
The American Midland Naturalist
150
:
185
190
.
Jensen
JB,
Richter
SC.
2005
.
Rana capito, gopher frog
.
Pages
536
538
in
Lannoo
MJ,
editor.
Amphibian declines: the conservation status of United States species
.
Berkeley
:
University of California Press
.
Kawula
R,
Redner
J.
2018
.
Florida land cover classification system
.
Tallahassee
:
Center for Spatial Analysis, Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission
.
Kinlaw
A,
Grasmueck
M.
2012
.
Evidence for and geomorphologic consequences of a reptilian ecosystem engineer: the burrowing cascade initiated by the gopher tortoise
.
Geomorphology157:108–121.
Lee
DS.
1968
.
Herpetofauna associated with central Florida mammals
.
Herpetologica
24
:
83
84
.
Marques
FFC,
Buckland
ST.
2003
.
Incorporating covariates into standard line transect analysis
.
Biometrics
59
:
924
935
.
Palis
JG.
1998
.
Breeding biology of the gopher frog, Rana capito, in western Florida
.
Journal of Herpetology
32
:
217
223
.
Parsons
E.
2019
.
Determining habitat requirements and landscape factors for the decline of the southeastern pocket gopher (Geomys pinetis). Master's thesis
.
Auburn, Alabama
:
Auburn University
.
R Core Team.
2013
.
R: a language and environment for statistical computing. Vienna: Foundation for Statistical Computing. Available;
Rothermel
BB,
Luhring
TM.
2005
.
Burrow availability and desiccation risk of mole salamanders (Ambystoma talpoideum) in harvested versus unharvested forest stands
.
Journal of Herpetology
39
:
619
626
.
Roznik
EA,
Johnson
SA.
2009
a.
Burrow use and survival of newly metamorphosed gopher frogs (Rana capito)
.
Journal of Herpetology
43
:
431
437
.
Roznik
EA,
Johnson
SA.
2009
b.
Canopy closure and emigration by juvenile gopher frogs
.
The Journal of Wildlife Management
73
:
260
268
.
Semlitsch
RD,
Bodie
JR.
2003
.
Biological criteria for buffer zones around wetlands and riparian habitats for amphibians and reptiles
.
Conservation Biology
17
:
1219
1228
.
Semlitsch
RD,
Todd
BD,
Blomquist
SM,
Calhoun
AJ,
Gibbons
JW,
Gibbs
JP,
Graeter
GJ,
Harper
EB,
Hocking
DJ,
Hunter
ML
Jr,
Patrick
DA.
2009
.
Effects of timber harvest on amphibian populations: understanding mechanisms from forest experiments
.
BioScience
59
:
853
862
.
Smith
LL,
Elliott
M,
Linehan
J,
Jensen
J,
Stober
J.
2009
a.
An evaluation of distance sampling for large-scale gopher tortoise surveys in Georgia, USA
.
Applied Herpetology
6
:
355
368
.
Smith
LL,
Howze
JM.
2016
.
Gopher tortoise line transect distance sampling workbook
.
Newton, Georgia
:
Joseph Jones Ecological Research Center
.
Smith
LL,
Stober
JM,
Balbach
HE,
Meyer
WD.
2009
b.
Gopher tortoise survey handbook. U.S. Army Corps of Engineers. ERDC/CERL TR-09-7
(see Supplemental Material, Reference S4).
Smith
LL,
Tuberville
TD,
Seigel
RA.
2006
.
Workshop on the ecology, status, and management of the gopher tortoise (Gopherus polyphemus), Joseph W. Jones Ecological Research Center, 16–17 January 2003: final results and recommendations
.
Chelonian Conservation and Biology
5
:
326
330
.
Stober
JM,
Prieto-Gonzalez
R,
Smith
LL,
Marques
TA,
Thomas
L.
2017
.
Techniques for estimating the size of low-density gopher tortoise populations
.
Journal of Fish and Wildlife Management
8
:
377
386
.
Stober
JM,
Smith
LL.
2010
.
Total counts versus line transects for estimating abundance of small gopher tortoise populations
.
Journal of Wildlife Management
74
:
1595
1600
.
Test
FC.
1893
.
The “gopher frog.”
Science
22
:
75
.
Thomas
L,
Buckland
ST,
Rexstad
EA,
Laake
S,
Strindberg
JL,
Hedley
JR,
Bishop
B,
Marques
TA,
Burnham
KP.
2010
.
Distance software: design and analysis of distance sampling surveys for estimating population size
.
Journal of Applied Ecology
47
:
5
14
.
Todd
BD,
Rothermel
BB.
2006
.
Assessing quality of clearcut habitats for amphibians: effects on abundances versus vital rates in the southern toad (Bufo terrestris)
.
Biological Conservation
133
:
178
185
.
[ESA] U.S. Endangered Species Act of 1973, as amended, Pub. L. No. 93-205, 87 Stat. 884 (Dec. 28, 1973)
.
[USFWS] U.S. Fish and Wildlife Service.
2012
.
Candidate conservation agreement for the gopher tortoise (Gopherus polyphemus) eastern population
(see Supplemental Material, Reference S5).
[USFWS] U.S. Fish and Wildlife Service.
2015
.
Endangered and Threatened wildlife and plants; 90-day findings on 31 Petitions
.
Federal Register
80
(126)
:
37568
37579
.

The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Author notes

Citation: Smith LL, Howze JM, Staiger JS, Sievers ER, Burr D, Enge KM. 2021. Added value: gopher tortoise surveys provide estimates of gopher frog abundance in tortoise burrows. Journal of Fish and Wildlife Management 12(1):3–11; e1944-687X. https://doi.org/10.3996/JFWM-20-030

Supplementary data