Journal of Herpetology, Vol. 52, No. 2, 228–233, 2018 Copyright 2018 Society for the Study of Amphibians and Reptiles
Microgeographic Variation in Bog Turtle Nesting Ecology NATHAN W. BYER,1,2 SCOTT A. SMITH,3
AND
RICHARD A. SEIGEL1
1
3
Department of Biological Sciences, Towson University, Towson, Maryland USA Wildlife and Heritage Service, Maryland Department of Natural Resources, Wye Mills, Maryland USA
ABSTRACT.—Bog Turtles (Glyptemys muhlenbergii) are cryptic habitat specialists, requiring spring-fed bogs, fens, and wet meadows, and are among the most imperiled turtles in North America. Despite the sensitive conservation status of this species, data on nesting ecology remain scant. We used radiotelemetry to collect information on the nesting ecology and nest success of Bog Turtles at two sites in Maryland. We had three main objectives: 1) to determine elements of reproductive biology critical to population viability, 2) to investigate rates of nest and egg success, and 3) to compare these variables between two proximate geographic localities. We documented a total of 41 nests across both sites and study years, all between 8 and 22 June of each year. In some cases, turtles used the same nest sites between years, and nests were in moist soil, moss, sedge tussocks, and mats of vegetation. Nesting turtles were typically observed in the late afternoon and evening, between 1557 and 2222 h. Clutch sizes averaged 3.52 6 1.08 eggs across both sites and years. Nesting success was significantly different between sites, and most nests that did produce surviving hatchlings experienced at least partial depredation before hatching. We stress the importance of collecting site-specific nesting data for this species, and suggest that nest protection may be a useful tool for increasing rates of nest success at some sites.
Many reptiles appear to be imperiled and declining because of climate change, invasive species introductions, disease, and habitat alteration (Gibbons et al., 2000). Turtles are declining rapidly, with 148 of 356 species (41.6%) listed as threatened by the International Union for Conservation of Nature Red List (Rhodin et al., 2017). Life-history characteristics shared by many turtles, such as long lives, delayed sexual maturity, and low fecundity, make them vulnerable to disturbances, particularly if these disturbances cause high adult and subadult mortality (Congdon et al., 1993, 1994). In addition, some observed declines of turtle populations may be due to loss of adequate nesting habitat (Burger and Garber, 1995; Sarti et al., 1996; Spotila et al., 1996) and low nest success (Feinberg and Burke, 2003; Horne et al., 2003; Tomillo et al., 2008; Pike et al., 2015). Therefore, conservation measures for turtles and other longlived organisms must protect all life-history stages (Congdon et al., 1993, 1994). Bog Turtles (Glyptemys muhlenbergii) are among the smallest, rarest, and most imperiled North American turtles (Chase et al., 1989; Morrow et al., 2001; Ernst and Lovich, 2009). They are habitat specialists that utilize small, spring-fed bogs, fens, and wet meadows (Ernst and Lovich, 2009) that often are negatively affected by anthropogenic activities (Chase et al., 1989; Ernst and Lovich, 2009; Pittman and Dorcas, 2009). This species has also been heavily affected by the illegal pet trade (Lee and Norden, 1996). Populations in the northern part of the geographic range were listed as threatened in 1997 under the U.S. Endangered Species Act, with southern populations listed as threatened because of similarities in appearance (Klemens, 2001) Because of their habitat specialization and limited vagility, Bog Turtles differ from most other emydid turtles in that they rarely move from their aquatic habitats to nest (Arndt, 1977; Holub and Bloomer, 1977; Zappalorti et al., 2015). Bog Turtles also typically do not dig underground nest chambers as do most other emydids, instead placing eggs in uncovered vegetation, 2 Corresponding Author. Present address: Department of Forestry and Wildlife Ecology, University of Wisconsin-Madison, Madison, Wisconsin USA; E-mail:
[email protected]
DOI: 10.1670/17-120
especially grassy tussocks (Ernst and Lovich, 2009; Macey, 2015; Zappalorti et al., 2015). Such nests often are quite difficult to find, so, unsurprisingly, the few published studies conducted on the nesting ecology of Bog Turtles have had relatively small sample sizes (Arndt, 1977; Holub and Bloomer, 1977; Whitlock, 2002; Ernst and Lovich, 2009) and are limited in geographic distribution. Hence, we know relatively little about nest success in most Bog Turtle populations, a variable that is particularly important for evaluating the long-term prospects of survival for populations of Bog Turtles. In some states, 20- to 25-yr mark– recapture databases are available for analyses of adult survivorship, but these databases frequently lack any information on nest and hatchling survival rates, clutch sizes, and other elements of reproductive biology. In this study, we present data on the nesting ecology, nest success, and movements associated with nesting behavior in Bog Turtles in Maryland. Our goals were to 1) determine elements of reproductive biology critical to population viability, such as reproductive frequency and clutch sizes; 2) investigate rates of nest and egg success; and 3) compare these variables between two proximate geographic localities. MATERIALS
AND
METHODS
Study Locations.—On the basis of previous mark–recapture history and estimated numbers of females at each site, we selected two sites in Maryland for nesting studies, each with different estimated densities of Bog Turtles. The high-density site, HA411, is a small (0.2 ha) wetland situated between two roads and a stream, with 132 individual Bog Turtles captured between 1992 and 2012 (Smith, unpubl. data). The low-density site, BA030, is a much larger wetland (>1 ha) situated in a developed suburban landscape, with only 41 individual Bog Turtles captured in the past 20 yr (Smith, unpubl. data). In addition, the adult sex ratio of this site is skewed in favor of females, with approximately four females for every male (Smith, unpubl. data). Detailed descriptions of each site are given in Byer et al. (2017). Radiotelemetry and Nest Identification.—We conducted surveys in April and May 2013 and 2014 to capture female Bog Turtles. Two survey methodologies were used, as described in Byer et al. (2017). Phase II surveys involved one to three researchers
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NESTS OF BOG TURTLES opportunistically probing in shallow pools, small mammal tunnels, tussock mats, and other areas where Bog Turtles may hide in wetlands. We also used visual-encounter survey methods when appropriate. Phase III surveys, which utilized passive entry traps, were attempted in 2014 to capture turtles at BA030; however, no additional females were captured using this technique. Carapace length and width, plastron length and width, dome height, and body mass were collected from each captured female. Adult female turtles caught at each site using these surveys were outfitted with SOPR-2190 radio transmitters (Wildlife Materials, Inc., Murphysboro, Illinois USA) using standard radio attachment methodology for this species (Schubauer, 1981; Eckler et al., 1990). Radiotelemetry locations were collected twice a week from early April to late May, every day during the peak nesting season of early June to early July (Ernst and Lovich, 2009), and twice a month from late July to August. From April to July, manual palpation, a widely used technique for assessing reproductive status in turtles (although see Keller, 1998), was used every 3–5 d to detect shelled eggs in adult females and to approximate the onset of nesting. This provided an estimate of reproductive frequency, defined as the proportion of females that develop shelled eggs within a nesting season. Once shelled eggs were detected in a turtle, that turtle was tracked daily to determine its approximate nesting location. During all handling of tracked turtles and potential nesting sites, nitrile gloves were worn to avoid leaving human scent on female Bog Turtles, nests, and nesting substrates. When a gravid female was located, three pieces of flagging tape were placed in a triangle around the observed location of the female to approximate the potential nest location. A return trip was then made to the spot during the next survey period to carefully search for nests. The exact location of nests was not marked; instead, a small piece of flagging tape was tied to vegetation ~0.5 m away from the nest location. If a female was no longer gravid, the most recent telemetry locations for that individual were gently probed for nests. We supplemented nests found with radiotelemetry by conducting additional surveys of potential nest locations two to three times each week starting in mid-June. These surveys involved gently probing in sedge tussocks, mats of vegetation, and soft soil for nests, as these represent common locations for Bog Turtle nests (Ernst and Lovich, 2009; Macey, 2015; Zappalorti et al., 2015). As with nests detected using radiotelemetry, nests detected using this technique were marked with a single piece of flagging tape tied to vegetation ~0.5 m from each nest. All nests in this study were left uncaged to determine natural rates of nest success. Nest locations were recorded with a model 60 global positioning system (Garmin International, Inc., Olathe, Kansas USA; accuracy = 6 3 m, averaged for 200 s) and plotted on maps of each study site using ArcMap 10.0 (ESRI, Redlands, California USA). Nest Monitoring.—Nests were monitored once or twice a week from discovery to predation or hatching. Nest monitoring involved visually inspecting the nest cavity itself and, on rare occasions (no more frequently than once every week), inspecting the eggs by hand for any signs of insect predation. Care was taken to maintain the same axis and orientation of eggs during handling. If a nest or egg was predated, timing of predation was recorded. Potential predator identity was inferred on the basis of condition of egg shells whenever possible. Number of eggs was also approximated for depredated nests on the basis of
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observable egg shell fragments. When hatching occurred, the number of hatchlings and timing of emergence was noted. Nest monitoring provided two important measures of reproductive output for this species: nest success and egg survival. For the purposes of this study, nest success is defined as whether a nest had any hatchling emergence, and was calculated as the percentage of nests located at a site that had at least one successful emergence in that season. Egg survival was defined as the number of eggs laid at a given site during one study season that successfully emerged; therefore, nest success could be high (all nests produced at least one hatchling) and egg survival quite low (e.g., only one surviving hatchling per nest). Statistical Analysis.—Before comparing clutch sizes between sites and years, we used a one-way fixed-effects analysis of variance, with site as the treatment effect and female carapace length for females captured in 2013 (n = 13 for HA411, n = 12 for BA030) as the response variable, to test the null hypothesis that adult female carapace length does not differ between sites. We found no significant effect of site on carapace length for this reduced data set (F = 0.126, P = 0.726). Because of low nest counts (n = 6) at BA030 during 2013, clutch size data were pooled between years for each site. Before analyzing clutch size data, we tested this data set for normality with a Shapiro-Wilks test and for homoscedasticity with a Bartlett’s test. Data from BA030 did not violate normality (w = 0.95, P = 0.45), but data from HA411 did (w = 0.88, P = 0.014). A plot of clutch sizes for HA411 revealed that this deviation from normality was mainly because of a low frequency of two egg clutches. Bartlett’s test found no evidence of violations of homoscedasticity (Bartlett’s K2 = 0.075, P = 0.785). Given the violations of normality for this data set, a Mann-Whitney U-test was used to test the null hypothesis that the distributions of clutch sizes at each site are equal. For this study, we defined reproductive frequency as the proportion of tracked females at each site that were gravid during each study season. Reproductive frequencies for each site were compared between sites and years using a replicated 2 · 2 contingency table design, with site and year as treatments and number of gravid females to all tracked females as a response variable. We used this contingency table design to generate proportions of gravid females for each combination of site and year. We used the Cochran-Mantel-Haenszel estimator to compare sites, testing the null hypothesis that the odds ratio is equal to one (implying no difference between sites after factoring out yearly variation; Sokal and Rohlf, 1995). We used a similar procedure to test the effect of year on reproductive frequency, controlling for variation between sites. Nest success was compared between years and between sites using a similar protocol to the one outlined above. Summary statistics are presented as means 6 standard deviation unless otherwise noted, and a = 0.05 for all hypothesis tests. RESULTS Nest Locations.—We found 16 nests during 2013, 10 at HA411 and 6 at BA030. During this year, 1 nest at BA030 was located directly on top of another nest, so we documented only 15 nest locations. We found 25 nests during 2014, 13 at HA411 and 12 at BA030. During this year, 1 nest at HA411 and 2 nests at BA030 were laid directly on top of other nests, so we documented only 22 nest locations. During 2013, observed nesting at both sites occurred on 8–22 June between 1733 and 2222 h (daylight savings time [DST]). During 2014, observed nesting events occurred on 8–
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FIG. 1. Distribution of clutch sizes of Glyptemys muhlenbergii at each site in Maryland, USA.
20 June between 1557 and 2112 h (DST). Nesting attempts were typically observed at or near sunset. Reproductive Frequency.—Reproductive frequencies varied for each site during 2013, with 8 of 10 (80%) females showing signs of shelled eggs at BA030 and all 11 females showing signs of shelled eggs at HA411. During 2014, reproductive frequencies were similar to those observed in 2013, with 9 of 11 (82%) females at BA030 showing signs of shelled eggs and all 14 females at HA411 showing signs of shelled eggs. Differences in reproductive frequencies between sites were not significant (Mantel-Haenszel v2 = 2.9391, df =1, P = 0.086), although low sample size may have reduced power for this comparison. Clutch Sizes.—We excluded three nests before analyzing clutch sizes. At BA030, one nest from 2013 was depredated before accurate clutch size estimates could be determined. At HA411, two nests from 2014 were excluded: one had a very large clutch size (six eggs) that could have been the result of multiple clutches in a single nest cavity, and a second nest was depredated before accurate clutch size estimates could be determined. Therefore, the final sample sizes for each site were 17 at BA030 (5 in 2013, 12 in 2014) and 21 at HA411 (8 in 2013, 13 in 2014). During 2013, the average clutch sizes were 3.60 6 1.14 eggs at BA030 and 2.62 6 1.51 eggs at HA411. During 2014, the average clutch sizes were 3.42 6 1.31 eggs at BA030 and 3.62 6 0.87 eggs at HA411, for a study-wide average of 3.52 6 1.08 eggs. A Mann-Whitney U-test did not find any difference in the distributions of clutch sizes at both sites, pooled between years (W = 200.5, P = 0.51; Fig. 1). Nest and Egg Success.—Nest success varied significantly between sites (Mantel-Haenszel v2 = 6.265, df = 1, P = 0.012), but did not vary significantly between years (Mantel-Haenszel v2 = 0.2448, df = 1, P = 0.6208). Nest success rates were 50% in 2013 and 30.8% in 2014 at HA411, and far fewer eggs successfully hatched at HA411 in 2014 (5 of 47, or 10.6%) compared with 2013 (13 of 28, or 46.4%; Table 1). This was mainly because of greater small mammal predation during the 2014 field season (Table 1). At BA030 during 2013 and 2014, both nest and egg success were zero (0 of 60 eggs and 0 of 18 nests; Table 1).
Mammalian and insect predation were the primary causes of nest failure at BA030 and HA411 during both study years, with most mammalian predation appearing to be because of small mammals, especially shrews, voles, or mice (Table 1). Although exact species are uncertain, most identification of probable small mammal predation was based on small teeth marks in egg shells. In addition to predation, nest failure could also be attributed to presumed egg inviability, as 5–15% of eggs laid at each site each year did not hatch within the study period. Although eggs that did not hatch were not taken from the field for controlled incubation in this study, there has been only one possible case of embryonic diapause or overwintering in this species (Ernst and Lovich, 2009; Lovich et al., 2014), although hatchlings have occasionally been found with an egg tooth in late April/early May (Smith, pers. obs.). Therefore, eggs that did not hatch by November in each study year were presumed to be inviable. Two eggs laid at BA030 during 2014 contained partially developed hatchlings that attempted to pip eggs in the late afternoon, but hatchlings in both cases died by the next morning, with no signs of depredation. DISCUSSION Comparisons with Other Studies.—The nesting ecology of our two populations appeared to align relatively closely with the few other published accounts for Bog Turtles, although there were some exceptions. Ernst and Lovich (2009) described the nesting season of Bog Turtles in Maryland as extending from 7 June to 6 July; however, we found that nesting typically lasted only from 8 June to 22 June, with little variation in the timing of nesting between sites or years. Reproductive frequencies also varied very little between years, and seemed to support the contention of Holub and Bloomer (1977) that Bog Turtles may have a reproductive frequency of
