Southeastern Naturalist M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 586 2016 SOUTHEASTERN NATURALIST 15(4):586–594 Vertebrate Use of Gopher Tortoise Burrows and Aprons Michelina C. Dziadzio1,2,* and Lora L. Smith1 Abstract - Gopher Tortoise (Gopherus polyphemus) burrows are used by more than 60 vertebrate species, but the frequency with which species use burrows and the extent to which other vertebrates use the mound of sand at the burrow entrance, called the burrow apron, has not been quantitatively assessed. Between 2 June and 9 October 2014, we monitored active and inactive adult Gopher Tortoise burrows with motion-triggered trail cameras to identify and enumerate vertebrate burrow visitors. We recorded 12,238 video clips during 2299 trap nights, of which 10,151 (83%) contained a Gopher Tortoise and 1732 (14%) contained other vertebrate species. We reduced multiple videos of a single burrow visitation to 1 observation, resulting in 929 observations of 14 vertebrate species (not including the Gopher Tortoise) using tortoise burrows and 34 species on burrow aprons. Mammals were the most commonly recorded taxa (54%), followed by birds (32%), amphibians (9%), and reptiles (5%). Active burrows were visited more frequently than inactive burrows across all taxa, and burrow aprons were used more frequently than the burrow tunnel. Although active and inactive Gopher Tortoise burrows provide refuge for some vertebrate species, active burrows may provide additional resources, such as increased prey for insectivorous species. More species were found to be present on burrow aprons than within burrows, indicating the apron may be an important microhabitat for species, including those not known to use burrows. Introduction Gopherus polyphemus (Daudin) (Gopher Tortoise) are found throughout the Coastal Plain of the southeastern United States, but habitat loss and degradation have resulted in population declines of up to 80% in the last century (Auffenberg and Franz 1982). Gopher Tortoises occurring west of the Mobile and Tombigbee Rivers are federally protected under the Endangered Species Act (USFWS 1987), and the eastern population is currently listed as a candidate species for federal protection (USFWS 2011). Gopher Tortoise population declines may impact a multitude of species because their burrows are used by more than 300 invertebrate and 60 vertebrate species as refuge from extreme weather conditions, fire, desiccation, and predators (Jackson and Milstrey 1989, Kent and Snell 1994). Consequently, the Gopher Tortoise is considered a keystone species of the Pinus palustris Mill (Longleaf Pine)–Aristida stricta Michx. (Wiregrass) ecosystem (Eisenberg 1983). In addition, the mound of sand at the burrow entrance may be used for foraging and nesting habitat by other vertebrates (DeGregorio et al. 2011, Heinrich and Richardson 1993, Kent and Snell 1994). 1Joseph W. Jones Ecological Research Center, Newton, GA 39870. 2Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602. *Corresponding author - michelina.dziadzio@gmail.com. Manuscript Editor: Max Nickerson Southeastern Naturalist 587 M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 Gopher Tortoises excavate burrows in deep, well-drained, sandy soils; the burrows average 4.6 m long and 2 m deep (Hansen 1963). Gopher Tortoise burrows can be identified by their characteristic half-moon–shaped tunnel and the mound of sand at the burrow entrance, called the burrow apron (Cox et al. 1987). Burrow width is highly correlated to the length of the tortoise occupying the burrow (Doonan and Stout 1994), and adult burrows (>23 cm in width; Alford 1980) have a 29° angle of declination (Hansen 1963). Because tortoise burrow depth increases gradually, there is a thermal gradient from the entrance to the bottom of the burrow; temperature and humidity become increasingly stable toward the burrow end, where it remains fairly constant at ~27° C throughout the year (Douglass and Layne 1978, Pike and Mitchell 2013). Other species may modify existing Gopher Tortoise burrows by excavating side channels within the burrow (Kinlaw and Grasmueck 2012), creating additional structural and thermal complexity. Species relationships to Gopher Tortoise burrows have been described as “obligate commensal” or “facultative associate”, and burrow associates have been described as frequent or occasional (Cox et al. 1987, Jackson and Milstrey 1989). While both obligate commensals and associate species use Gopher Tortoise burrows, the former, by definition, are thought to require the burrows to survive, whereas the latter are not dependent on them (Jackson and Milstrey 1989, Young and Goff 1939). Jackson and Milstrey (1989) classified species as frequent burrow associates if there were at least 10 records of the species using burrows, and suggested data on frequency of burrow use by many species were limited. Burrow use may vary by habitat, season, and burrow status (Eisenberg 1983, Hyslop et al. 2009, Kent and Snell 1994, Lips 1991, Witz et al. 1991). For example, in the northern portion of its range, Drymarchon couperi Holbrook (Eastern Indigo Snake) is thought to be a Gopher Tortoise burrow commensal, though their use of burrows varies seasonally, with peak use in winter months (Hyslop et al. 2009). Some species exhibit positive associations with “active” tortoise burrows, including Lithobates capito LeConte (Gopher Frog; Eisenberg 1983). Active burrows are those which are occupied or were recently occupied by a Gopher Tortoise. This association may be related to higher invertebrate abundance in active burrows, creating greater food availability for insectivorous species (Witz et al. 1991). Previous studies examining the use of Gopher Tortoise burrows by vertebrate associates have used funnel traps (Lips 1991) and burrow excavation (Kent and Snell 1994, Witz et al. 1991) to sample burrows. Passive sampling techniques, which allow an assessment of frequency of use and also capture activities of associate species are much less common (see Alexy et al. 2003). We monitored active and inactive Gopher Tortoise burrows with motion-triggered trail cameras to determine frequency of use of Gopher Tortoise burrows and burrow aprons by vertebrates. Field-Site Description Our study was conducted at the 11,600-ha Joseph W. Jones Ecological Research Center at Ichauway, located in Baker County, GA. The study site consisted of primarily Longleaf Pine forest with a sparse midstory. Native ground cover was Southeastern Naturalist M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 588 dominated by Wiregrass, Andropogon spp. (bluestem), and legumes (Fabaceae). Upland habitats were managed with prescribed fire on a ~2-year return interval. Gopher Tortoise density on this site was 0.71 ± 0.10 tortoises per ha; burrow density was 2.46 ± 0.24 burrows per ha (L.L. Smith, unpubl. data). Methods Between 2 June and 9 October 2014, we monitored 34 active and 20 inactive adult Gopher Tortoise burrows (i.e., tortoise burrow width >23 cm; Alford 1980) that contained an artificial or natural Gopher Tortoise nest in the burrow apron (Dziadzio et al. 2016). Burrows were classified as active if we observed signs of recent tortoise activity such as fresh scat and tortoise tracks on the burrow apron, and inactive if the apron lacked fresh scat or tortoise tracks (Auffenberg and Franz 1982). We used motion-triggered trail cameras (UWAY VH400HD, Norcross, GA) mounted on 5 cm × 5 cm × 107 cm wooden stakes within 1–2 m from the burrow entrance to identify vertebrate burrow visitors. We checked cameras daily, and videos were date and time stamped and stored on digital memory cards (SanDisk 8GB SDHC, SanDisk Corporation, Milpitas, CA). We reviewed videos to determine behavior and frequency of use of burrows and aprons by vertebrate associates. To determine temporal differences in burrow use, we considered day observations as those between 0630 h and 2029 h and night observations as those between 2030 h and 0629 h. Observations of movement (i.e., hopping, running, walking, etc.) were classified as “moving”. We classified as “stationary” animals that were motionless during the length of the video clip, and as “foraging” animals that were observed eating or carrying away plant material, or depredating natural or artificial tortoise nests in burrow aprons. Finally, the “other” category included rarely observed behaviors such as dust bathing and calling by birds, investigation of trail cameras by mammals, and behaviors that could not be determined. We considered multiple videos with a lapse time of less than 10 min to be a single event to minimize bias due to duration of time an individual spent at the burrow apron. Because we could not distinguish between species on video, we combined all mouse observations. Possible species included Peromyscus gossypinus LeConte (Cotton Mouse), Ochrotomys nuttalli Harlan (Golden Mouse), Mus musculus L. (House Mouse), and Peromyscus polionotus Wagner (Oldfield Mouse) (Smith et al. 2006). Some individual anurans and birds could not be identified to species. Results Our trail cameras recorded a total of 12,238 videos between 2 June and 9 October 2014, of which 10,151 (83%) contained a Gopher Tortoise. We reduced multiple videos of an individual to 1 event and removed Gopher Tortoise and unknown observations, resulting in 929 recorded burrow visits by vertebrate associates. Seventy video events contained more than 1 individual, 28 of which were conspecifics. We observed 14 vertebrate species using Gopher Tortoise burrows and 34 species Southeastern Naturalist 589 M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 using burrow aprons (Fig. 1). Mammals were the most commonly recorded taxa, with 504 visits by 11 species, followed by birds with 298 visits by 17 species. Trap effort varied between active (n = 1532 trap nights, i.e., a 24-hr period) and inactive (n = 767 trap nights) burrows. We calculated observations per 100 trap nights for both burrow-activity classes and found a difference in frequency of use by vertebrates between active and inactive burrows and aprons (Fig. 1). Active burrows were visited more frequently than inactive burrows by all taxa, and several species were observed exclusively at active burrows, including the Gopher Frog, Thryothorus ludovicianus Latham (Carolina Wren), and Colinus virginianus L. (Northern Bobwhite) (Fig. 1). We also observed several species exclusively at inactive burrows (e.g., Sciurus niger L. [Fox Squirrel] and Mephitis mephitis Schreber [Striped Skunk]), but these observations were based on only a few individuals captured by trail cameras (Fig. 1). Several species, including Peucaea aestivalis M.H.K. Lichtenstein (Bachman’s Sparrow), Aspidoscelis sexlineata L. (Six-lined Racerunner), and the “mouse” group, were observed at both burrow categories but most frequently at active burrows (Fig. 1). We recorded 708 individual events of 34 species using Gopher Tortoise burrow aprons. The highest species diversity observed on burrow aprons was among birds (n = 17 species). Bachman’s Sparrow was the most common bird recorded, observed at 11.6% of all trap nights (Fig. 1). Behaviors were different between species, but similar within taxa (Table 1). The most frequently observed behavior Figure 1. Vertebrate observations at active and inactive Gopherus polyphemus (Gopher Tortoise) burrows and aprons between 2 June to 9 October 2014 at Ichauway, Baker County, GA. Observations for each species were calculated for 100 trap nights at each burrow type because of unequal trap effort at active (n = 1532 trap nights) and inactive burrows (n = 767 trap nights). Southeastern Naturalist M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 590 Table 1. Observations of vertebrates at Gopher Tortoise (Gopherus polyphemus) burrows and aprons from 2 June to 9 October 2014 at Ichauway, Baker County, GA. Behaviors were classified as “moving” (M), which referred to movement behavior (i.e., hopping, walking, running, and entering or exiting the burrow); “stationary” (S) when an animal remained still through the duration of the video; “foraging” (F) when an animal was observed actively foraging on the burrow apron; or “other” (O), which included rarely observed and unknown behaviors. Behavior (% of observations) Common name Species M S F O Mammals (total) 75 9 15 1 Coyote Canis latrans Say 67 0 0 33 Eastern ChipmunkA Tamias striatus L. 100 0 0 0 Eastern Cottontail Sylvilagus floridanus J.A. Allen 57 42 2 0 Hispid Cotton Rat Sigmodon hispidus Say and Ord 86 14 0 0 Mouse spp. Mouse spp. 89 8 3 0 Nine-Banded ArmadilloB Dasypus novemcinctus L. 62 1 37 1 Raccoon Procyon lotor L. 51 0 40 9 Sherman's Fox Squirrel Sciurus niger shermani Moore 100 0 0 0 Striped Skunk Mephitis mephitis Schreber 100 0 0 0 Virginia Opossum Didelphis virginiana Kerr 83 0 17 0 White-tailed DeerA Odocoileus virginianus Zimmermann 67 8 25 0 Birds (Total) 64 11 20 5 Bachman’s Sparrow Peucaea aestivalis Lichenstein 63 8 22 6 Bird spp. Bird spp. 69 13 16 3 Blue GrosbeakA Passerina caerulea L. 0 0 100 0 Blue JayA Cyanocitta cristata L. 0 0 100 0 Brown ThrasherA Toxostoma rufum L. 100 0 0 0 Carolina Wren Thryothorus ludovicianus Latham 89 6 6 0 Common Ground-DoveA Columbina passerina L. 100 0 0 0 Crow sp.A Corvus sp. 50 50 0 0 Eastern BluebirdA Sialia sialis L. 0 0 0 100 Florida Burrowing Owl Athene cunicularia floridana Ridgway 0 43 57 0 Great Crested FlycatcherA Myiarchus crinitus L. 20 40 0 40 Indigo BuntingA Passerina cyanea L. 100 0 0 0 Mourning DoveA Zenaida macroura L. 81 10 10 0 Northern Bobwhite Colinus virginianus L. 88 12 0 0 Northern MockingbirdA Mimus polyglottos L. 67 8 17 8 Pine WarblerA Setophaga pinus Wilson 100 0 0 0 Tufted TitmouseA Baeolophus bicolor L. 0 0 100 0 Wood ThrushA Hylocichla mustelina Gmelin 0 100 0 0 Amphibians (total) 29 71 0 0 Anuran spp. Anuran spp. 29 71 0 0 Eastern Spadefoot Toad Scaphiopus holbrookii Harlan 67 33 0 0 Gopher Frog Lithobates capito LeConte 6 94 0 0 Southern Toad Anaxyrus terrestris Bonnaterre 52 48 0 0 Reptiles (total) 89 0 7 4 Black Racer Coluber constrictor L. 100 0 0 0 Eastern Coachwhip Coluber flagellum Shaw 82 0 0 18 Eastern Hog-Nosed Snake Heterodon platyrhynos Latreille 50 0 50 0 Six-Lined Racerunner Aspidoscelis sexlineata L. 94 0 6 0 ASpecies not previously described using tortoise burrows or burrow aprons. BNon-native species. Southeastern Naturalist 591 M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 classification was moving among mammals (75%), birds (64%), and reptiles (89%) and stationary among amphibians (71%). Birds spent the most time foraging on the burrow apron (20%), followed by mammals (15%). Other observed behaviors included birds dust bathing (n = 5), collecting vegetation (n = 8), and calling (n = 1), and mammals investigating trail cameras (n = 3). There was a difference in the temporal pattern of burrow visits among taxa. Mammals (n = 448) and amphibians (n = 61) were most frequently observed at night, between 2030 and 0629 h, whereas birds (n = 269) and reptiles (n = 45) were most commonly observed during the day, between 0630 and 2029 h (Fig. 2). Nocturnal bird observations were the result of Athene cunicularia floridana Ridgway (Florida Burrowing Owl; n = 14) foraging on a burrow apron between 2300 and 0516 h, and passerines at burrow aprons up to 2 hours before dawn, from 0435 to 0629 h (n = 15). Discussion This study provides novel information about the frequency with which vertebrate taxa used tortoise burrows and burrow aprons. Many studies have examined vertebrates using tortoise burrows (e.g., Alexy et al. 2003, Jackson and Milstrey 1989, Kent and Snell 1994, Lips 1991, Witz et al. 1991), but data documenting use of burrow aprons are much more limited. Mammals were the most commonly observed taxa, with more than 500 visits by at a total of at least 11 species, followed by birds, with nearly 300 visits by 17 species. We found birds used burrow aprons Figure 2. Vertebrate observations at Gopher Tortoise (Gopherus polyphemus) burrows and aprons monitored using motion sensor cameras between 2 June to 9 October 2014 at Ichauway, Baker County, GA. Day observations were between 0630 h and 2029 h and night observations were between 2030 h and 0629 h. Southeastern Naturalist M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 592 as foraging sites, including species not previously known to be associated with tortoise burrows, such as Zenaida macroura L. (Mourning Dove) and Mimus polyglottos L. (Northern Mockingbird). Bachman’s Sparrows have been documented occasionally using Gopher Tortoise burrows as a refuge (Pittman 1960, Stevenson 2013), but Gopher Tortoise burrows may also benefit Bachman’s Sparrows in other ways. Bachman’s Sparrows are strictly ground-foragers (Allaire and Fisher 1975), and their abundance appears to be positively correlated with percent bare ground and negatively correlated with increases in understory density and height (Cox and Jones 2009). The open sand at burrow aprons may be important to Bachman’s Sparrows, especially in areas of marginal habitat where fire suppression has resulted in a dense understory and midstory. Overall, active Gopher Tortoise burrows and burrow aprons were used more frequently than inactive burrows, suggesting active burrows provide additional resources for associate species. We did not examine if burrow occupancy by a tortoise impacted vertebrate associate use, but previous research suggests there is no effect (Kent and Snell 1994, Witz et al. 1991). Active burrows may contain more tortoise scat than inactive burrows, which could have cascading effects on burrow use by associates (Kent and Snell 1994, Lips 1991). The presence of scat may attract coprophagous invertebrates (Young and Goff 1939), which may increase the abundance of insectivorous predators, potentially leading to an increase in abundance of carnivorous predators (Lips 1991). Use of trail cameras to record burrow visits may have biased our data against observations of small species, including lizards and toads, because their movements may not have triggered the cameras. Also, our study took place during the tortoise nesting season, from June through October, and burrow use by other vertebrate species may differ in late fall, winter, and spring. It is also likely that we observed more mesomammals than would naturally occur during the sampling period because they are the primary predators of Gopher Tortoise nests (Dziadzio et al. 2016, Landers et al. 1980). Despite these limitations, trail cameras were a useful tool to examine use of Gopher Tortoise burrows and aprons without altering the behavior of most species. Acknowledgments We are grateful to the Warnell School of Forestry and Natural Resources, the Joseph W. Jones Ecological Research Center, and the Gopher Tortoise Council for financial support. We also thank G. Morris, B. O’Hanlon, and B. Schlimm for assistance with species identification and J. Howze for providing helpful suggestions on an earlier draft of the manuscript. Literature Cited Alexy, J.K., K.J. Brunjes, J.W. Gassett, and K.V. Miller. 2003. Continuous remote monitoring of Gopher Tortoise burrow use. Wildlife Society Bulletin 31:1240–1243. Alford, R.A. 1980. Population structure of Gopherus polyphemus in northern Florida. Journal of Herpetology 14:177–182. Allaire, P.N., and C.D. Fisher. 1975. Feeding ecology of three resident sympatric sparrows in eastern Texas. The Auk 92:260–269. Southeastern Naturalist 593 M.C. Dziadzio and L.L. Smith 2016 Vol. 15, No. 4 Auffenberg, W., and R. Franz. 1982. The status and distribution of the Gopher Tortoise (Gopherus polyphemus). 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