Overwintering in the Nest by Hatchling Map Turtles (Graptemys Geographica)

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Overwintering in the nest by hatchling map turtles (Graptemys geographica)

Roy D. Nagle, Clayton L. Lutz, and Andrew L. Pyle

Abstract: We monitored 75 natural nests of Graptemys geographica (Lesueur, 1817) in central Pennsylvania to determine the tactics and patterns of hatchling emergence. Following incubation, all hatchlings in 95% of nests delayed emergence from their natal nest cavities throughout autumn and winter until the following spring. Nests were constructed in a variety of substrates ranging from loose sand or coal to hard-packed clay mixed with gravel. Time from egg deposition to natural hatchling emergence averaged 333 days. During winter, hatchlings tolerated subzero temperatures as low as –8 °C, which are lethal to hatchlings of some sympatric species. Emergence occurred from 10 April to 25 May, and most hatchlings were found during morning following rain. There was an interactive effect of minimum daily air temperature and rainfall level 1 day prior to emergence on the number of hatchlings emerging each day. One half of all hatchlings found dead were contained in nests in which autumn emergence had apparently occurred. We speculate that autumn emergence by hatchlings of some turtle species may be an adaptive response to nest conditions likely to provide poor environments for successful overwintering.

Résumé : Nous avons suivi 75 nids naturels de Graptemys geographica (Lesueur, 1817) dans le centre de la Pennsyl- vanie afin de déterminer les stratégies et les patterns d’émergence des nouveau-nés. Après l’incubation, dans 95 % des nids, tous les nouveau-nés retardent leur émergence de la cavité du nid natal pendant l’automne et l’hiver jusqu’au printemps suivant. Les nids sont construits dans une variété de substrats, allant de sable ou de charbon non consolidé à de la glaise compacte mêlée de gravier. Le temps entre la ponte des oeufs et l’émergence naturelle des petits est en moyenne de 333 jours. En hiver, les petits supportent le gel jusqu’à –8 °C, des températures létales pour les nouveau- nés de quelques autres espèces sympatriques. L’émergence a eu lieu du 10 avril au 25 mai et la plupart des petits ont été retrouvés le matin après une pluie. Ilyauneffetinteractif entre la température minimale journalière de l’air et la quantité de précipitations la veille de l’émergence, d’une part, et le nombre de petits qui émergent chaque jour, d’autre part. La moitié de tous les nouveau-nés trouvés morts proviennent de nids où il s’est apparemment produit une émer- gence d’automne. Nous posons l’hypothèse que l’émergence à l’automne des nouveau-nés chez certaines espèces de tortues peut être une réaction adaptative à des conditions dans le nid qui vont vraisemblablement fournir un mauvais environnement pour survivre à l’hiver. [Traduit par la Rédaction] Nagle et al. 1218

Introduction of some species hatch during late summer or autumn yet remain in nests throughout winter, delaying emergence and Turtles exhibit remarkable abilities to cope with adverse dispersal until the following spring. As a result, some hatch- conditions and commonly do so through prolonged periods lings spend 6–8 months in the nest post hatch, whereas their of inactivity. At early developmental stages, for example, incubation period is approximately 2 months (Tinkle et al. embryos of some species enter extended diapause in 1981; Christens and Bider 1987; Gibbons and Nelson 1978; response to chilling (Ewert 1979, 1985), whereas in other Lindeman 1991; Jackson 1994; Costanzo et al. 1995; DePari species embryos complete development but wait to hatch 1996; Tucker 1999). By utilizing the “proven sanctuary” af- coincidently with favorable conditions, such as the onset of forded by the nest, such a strategy may reduce uncertainties the wet season in Australia’s wet-dry tropics (Doody et al. associated with the fluctuating or declining resource levels 2001). In yet other species, offspring complete development of late autumn (Gibbons and Nelson 1978) or the vulnerabil- and hatch from their eggs but delay emergence and migration ity of hatchlings to predators during a period of low growth from terrestrial nests. potential (Wilbur 1975). Delayed emergence is the phenomenon in which hatchling Among North American turtles, hatchlings of five species turtles remain in or near their natal nest cavities for extended of the family Emydidae and two species of the family Kino- periods following hatching. At northern latitudes, neonates sternidae are reported to delay emergence from nests

Received 16 February 2004. Accepted 12 July 2004. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 7 October 2004. R.D. Nagle,1 C.L. Lutz,2 and A.L. Pyle.3 Environmental Science and Studies, Juniata College, Huntingdon, PA 16652, USA. 1Corresponding author (e-mail: [email protected]). 2Present address: Nongame Branch, Arizona Game and Fish Department, Phoenix, AZ 85023, USA. 3Present address: Programa Restauración de Tortugas Marinas, 1203-1100, Tibás, San José, Costa Rica.

Table 1. North American turtles that typically delay nest emergence, and locations where they were sampled. Family Species Location Reference(s) Emydidae Chrysemys picta (Schneider, 1783) Idaho Lindeman 1991 Michigan Wilbur 1975; Tinkle et al. 1981 Minnesota Woolverton 1963 Nebraska Costanzo et al. 1995 New Jersey DePari 1996 Quebec Christens and Bider 1987 Deirochelys reticularia (Latr., 1801) South Carolina Congdon et al. 1983; Buhlmann and Coffman 2001 Graptemys geographica (Lesueur, 1817) Indiana Baker et al. 2003 Terrapene ornata (Agassiz, 1857) Nebraska Costanzo et al. 1995 Trachemys scripta (Schoepff, 1792) Florida Jackson 1994 Illinois Tucker 1999 South Carolina Gibbons and Nelson 1978 Kinosternidae Kinosternon flavescens (Agassiz, 1857) Iowa Christiansen and Gallaway 1984 Nebraska Iverson 1991 K. subrubrum (Lacépede, 1788) South Carolina Gibbons and Nelson 1978

(Table 1). One factor common among such species is the abil- Materials and methods ity of females to produce multiple clutches during a given reproductive season. Owing to the lengthy egg-laying season, We located turtle nests from May 2000 through July 2002 hatching occurs over a broad temporal range and may include by searching terrestrial areas for nesting females along a periods highly unfavorable for growth and survival of hatch- portion of the Juniata River in Huntingdon County, Pennsyl- ling turtles (Gibbons and Nelson 1978). By delaying nest vania. The Juniata River is the second largest tributary of the emergence until spring, hatchlings are more likely to enter en- Susquehanna River and local discharge rates vary annually vironments favorable to the acquisition and allocation of re- from >10 000 ft3/s (1 ft3/s = 28.316 85 dm3/s) during April sources. Delayed emergence has also been suggested as a to <1000 ft3/s during August and September (Pluto and Bellis proximate response to impenetrable nest soil conditions 1986; Durlin and Schaffstall 2001). The area is near the (Cagle 1944; Hartweg 1944; DePari 1996), although the pro- western range limit of G. geographica in the central part of pensities of some turtle species to delay emergence across the state, where the larger rivers of Pennsylvania’s ridge and broad latitudinal and longitudinal ranges and among a variety valley region give rise to the Allegheny Front. Sympatric of substrates appear to counter a general interpretation of the species at the site include Chelydra serpentina (L., 1758), “nest integrity” hypothesis (Table 1). Clemmys insculpta (LeConte, 1830), and Sternotherus A more complete understanding of the adaptive signifi- odoratus (Latr., 1801). cance of delayed emergence by hatchling turtles requires Observed G. geographica nests were protected from pred- data on the relative costs and benefits, as well as the pres- ators using cylindrical 2.5 cm×5cmwire-mesh cages mea- ence and magnitude of geographic variation within and suring ~75 cm diameter × 25 cm high. We rotated cages into among species whose hatchlings overwinter in the nest. Fur- the soil to bury their edges and hold them in place. Thermis- thermore, documenting temporal aspects of delayed emer- tor probes from calibrated HOBO® temperature data loggers gence can elucidate important aspects of natural history and (Onset Computer, Pocasset, Massachusetts) were placed in a provide valuable information for wildlife managers and sample of nests each year to monitor thermal environments land-use planners. associated with incubation, overwintering, and hatchling Map turtles (Graptemys geographica) are a highly aquatic emergence. Protected nests were monitored at least twice emydid turtle endemic to the rivers and lakes of eastern and weekly throughout July and August for external signs of re- central North America (Ernst et al. 1994). They are noted for duced viability (erosion, subterranean predation, etc.) and frequent communal basking (Newman 1906; Flaherty and for hatchling emergence. Samples of nests were dug and in- Bider 1984; Pluto and Bellis 1986), extreme sexual size di- spected during September, October, and the following April morphism (Gordon and MacCulloch 1980; Gibbons and and May to determine hatching success and hatchling emer- Lovich 1990), and a molluscivorous diet (Newman 1906; gence strategies. Vogt 1980). In Pennsylvania, isolated populations of G. geo- During the first year of our study, nests were monitored graphica occur in the Delaware and Susquehanna river sys- daily during spring to determine patterns of hatchling emer- tems (Ernst et al. 1994). Only a few studies have described gence. In late March 2001, we buried rings of 15 cm high selected aspects of reproduction in G. geographica (Newman aluminum flashing to a depth of about 5 cm inside the pro- 1906; Gordon and McCullough 1980; Vogt 1980) and only tective wire cages to restrain hatchlings as they emerged one other study has examined aspects of early life stages from nests. Cages were examined 1–3 times per day from (Baker et al. 2003). In this report we describe delayed nest 1 April to 25 May for the presence or absence of emergence emergence by hatchling G. geographica in central Pennsyl- holes and hatchlings. Emergence was defined as synchro- vania and present winter nest temperatures and the phen- nous when all hatchlings emerged on the same day. During ology and timing of emergence. the period of nest inspections, we recorded levels of rainfall

Table 2. Body sizes of 350 hatchling Graptemys geographica captured in natural nests following overwintering. Plastron length (mm) Carapace length (mm) Height (mm) Width (mm) Mass (g) 27.5, 0.08 (22.9–30.2) 30.2, 0.08 (25.2–33.3) 15.2, 0.04 (13.0–16.8) 27.9, 0.10 (21.3–31.8) 6.39, 0.05 (4.23–8.20) Note: Values are as follows: mean, 1 SE (min.–max.).

(nearest 0.025 mm) using a RainWise® rain gauge connected The total number of live hatchlings marked and released to a HOBO event logger and ambient air temperature in was 350 (Table 2), whereas the total number of fully devel- shade using a HOBO temperature data logger (Onset Com- oped hatchlings found dead in nests was 20. Clutch size av- puter). On 26–30 May, all remaining nests were excavated eraged 10.6 eggs (n = 49, min. = 6, max. = 15, SE = 0.29). and numbers of dead eggs, embryos, and hatchlings (alive or Mean distance from the soil surface to the bottom of the nest dead) were recorded. cavity was 13.6 cm (n = 46, min. = 10.5, max. = 16.0, SE = During the second year, nests were monitored throughout 0.22). Nest depth exhibited a significant, positive relation- fall and early spring (as above), but instead of monitoring ship to clutch size (r = 0.41; F[1,28] = 5.55; P = 0.026). the timing of emergence within this sample, nests were exca- During the first year of study (2000–2001), observations vated and inspected on 10 April 2002 to assess embryo and suggested that all hatchlings in monitored nests overwintered hatchling survivorship. In addition, 35 hatchlings in four within their terrestrial natal nest cavities. During the second nests were weighed prior to and following overwintering to year, some hatchlings from four nests (all in gravel-soil sub- determine changes in body mass. Hatchlings were weighed strates) emerged during late autumn of 2001–2002. The four on 31 August 2001 and 10 April 2002, encompassing a pe- nests had been intact on 18 October 2001 but showed de- riod of 302 days. graded nest plugs and emergence holes upon the first spring Nests were categorized as totally successful when all nest inspection conducted on 31 March 2002, within a few hatchlings emerged, partially successful when at least one days after snow melt. One of the nests contained only egg- hatchling emerged, or failed if no hatchlings emerged. Dis- shell fragments within an intact nest cavity and was there- tances from the soil surface to the bottoms of nest cavities fore categorized as totally successful. Totals of 10 dead were measured with a ruler. Clutch sizes were determined hatchlings and 5 live hatchlings were found among the re- when no emergence holes were present and eggs and hatch- maining three nests. In another group of nests, within the lings could be clearly enumerated. Hatchlings were mea- sample of hatchlings weighed prior to and following sured with calipers, weighed using an electronic balance, overwintering, individuals lost, on average, 14.7% of their individually marked by notching marginal scutes (Cagle body mass (min. = 0.5, max. = 22.0, SE = 0.75). 1939), and released directly into the river near their nest lo- Dates and times of emergence were recorded for 42 hatch- cation. lings from nine nests during the spring of 2001. Hatchlings Statistics were analyzed using SAS for Windows (SAS In- emerged over a span of 45 days, with the earliest emergence stitute Inc., Cary, North Carolina). We used random-effects occurring on 10 April and the latest on 25 May. The mean ANOVA to examine relationships of rainfall and minimum number of days from nest construction until hatchling emer- and maximum daily temperatures to numbers of hatchlings gence was 333 (SE = 4.3) and ranged from 289–346 (Fig. 1). emerging each day. We also examined the effects of these All hatchlings emerged synchronously from four nests. variables 1 day prior to emergence and their interactions on Emergence in five other nests was asynchronous, with the numbers of hatchlings that emerged. Levels of significance number of days over which hatchlings emerged ranging from were set at α = 0.05. 2–31. Most hatchlings were found early in the day following a Results day or night with rain. Although most emergence appeared to occur during morning hours (and actual emergence was Survivorship and hatchling emergence strategies were observed only during morning, n = 5), our data do not rule monitored in a total of 75 G. geographica natural nests. out the possibility of nighttime emergence. Twenty-seven of Nesting was observed from 3 June to 14 July 2000 and from 42 hatchlings (64%) were present inside protective cages 2 June to 2 July 2001. Habitats used for nesting consisted of when nests were inspected for the first time during morning relatively open-canopy, sparsely vegetated, disturbed sites hours (0800–1100). Eight hatchlings (19%) were discovered such as areas along highways containing fill materials and during the second daily nest inspection conducted during spill piles of coal slag. Nests were constructed in a wide va- morning hours (0900–1200). Three hatchlings (7%) were riety of substrates including limestone gravel overlaying or discovered during the second daily nest inspection in early mixed with soil (n = 40), coal slag (n = 10), shale (n = 6), afternoon (1200–1300). Rainfall occurred on 15 days during soils ranging from predominantly sand (n = 2) to mostly the 45-day span over which hatchlings emerged, and 32 of clay (n = 5), and various combinations of the aforemen- 42 hatchlings (76%) emerged <30 h after rain. tioned substrate types (n = 12). Of 36 nests constructed and Minimum temperatures recorded in three nests during the monitored during 2000–2001, 14 (39%) were totally suc- night prior to actual emergence were 14.5, 15.2, and cessful, 15 (42%) were partially successful, and seven (19%) 15.6 °C. As individual factors, none of minimum daily air failed entirely. Of 39 nests constructed and monitored during temperature, maximum daily air temperature, level of rain 2001–2002, 13 (33%) were totally successful, 24 (62%) on the day of emergence, or level of rain on the day prior to were partially successful, and two (5%) failed. emergence was associated with the number of hatchlings

Fig. 1. Number of days from nest construction and egg deposi- Fig. 2. Temperature profile of a G. geographica nest from tion until emergence for hatchling Graptemys geographica. 1 December 2001 to 28 February 2002. Minimum temperature was –8.4 °C, recorded on 2 January. The nest contained five hatchlings, all of which survived the winter.

emerging each day (all P-values >0.05). However, the inter- action of minimum daily air temperature and level of rainfall later Cahn (1937), hypothesized that partially developed em- 1 day prior to emergence on number of hatchlings was sig- bryos within eggs could overwinter and then subsequently complete development during the following spring. Since nificant (F[3,44] = 5.60, P = 0.022). The greatest numbers of hatchlings emerged at air temperatures of ~12 °C or higher those early reports, however, additional field studies have following ~0.5 cm or more of rain, although five hatchlings indicated that partially developed embryos and unpipped emerged on days when air temperature fell below 5 °C. In- eggs are unable to tolerate the rigors of winter in shallow, ternal nest temperatures lag behind changes in ambient air terrestrial nests (MacCulloch and Secoy 1983; Storey et al. temperature and the relationship between the two is influ- 1988; St. Clair and Gregory 1990; Lindeman 1991; Congdon enced by factors such as terrain, ground temperature and et al. 2000; Nagle et al. 2000). Thus, turtle embryos at cover, insolation, and time of day (Costanzo et al. 1995; northern latitudes that fail to complete development before Nagle et al. 2000; Doody et al. 2001). Thus, following peri- winter appear to inevitably die in their nests. Those that do ods of warmer temperatures and soaking rains, a few hatch- complete development may either emerge from nests and lings appeared to emerge shortly after cold fronts had moved move to wetlands prior to the onset of cold winter tempera- in, entering into environments colder than their nests. tures or hibernate terrestrially until the beginning of the next Temperatures during winter were recorded in 10 nests year’s activity season. (2000–2001, n = 7; 2001–2002, n = 3). Minimum tempera- Hatchling G. geographica in central Pennsylvania exhib- tures in nests ranged from –2.4 to –8.4 °C. A total of 10 ited an overwhelming propensity to delay nest emergence. hatchlings in two nests were exposed to temperatures below Likewise, hatchlings in 19 of 20 nests from a recent study in –6 °C on five consecutive nights (see Fig. 2 for the tempera- northern Indiana were found to overwinter (Baker et al. ture profile of one of the nests). Despite relatively low 2003). Other studies have reported indirect evidence, such as subzero temperatures, however, no mortality was observed observations of hatchlings entering wetlands during early among 41 fully developed hatchlings when nests with tem- spring in Iowa (Christiansen and Gallaway 1984) and Min- perature loggers were examined in spring. Thus, within the nesota (Pappas et al. 2000), suggesting that hatchlings may sample of nests equipped with temperature probes, no hatch- overwinter terrestrially (although not necessarily within ling mortality could be attributed to freezing. nests). Similar indirect evidence was reported for 24 hatchlings in Illinois (McCallum 2003) and for a single G. geo- Discussion graphica hatchling in a Wisconsin study that reported no overwintering among sympatric hatchling G. pseudogeogra- The first published account of spring emergence in hatch- phica (Gray, 1831) and G. ouachitensis Cagle, 1953 (Vogt ling G. geographica was given by Newman (1906), who at- 1980). Combined with our results, evidence from areas tributed the pattern to incomplete embryo development across the species’ range indicates that delayed emergence during the previous summer and fall. Newman (1906), and may be a common strategy for G. geographica.

Overwintering in the nest may facilitate the entry of tur- Fig. 3. Partially excavated G. geographica nest photographed tles into habitats when conditions are optimal for growth, during November 2001. Note the vertical orientation and over- survival, or dispersal. In central Pennsylvania, G. geogra- lapping arrangement that is also characteristic of overwintering phica hatch during August and early September, when rivers hatchling painted turtles (Chrysemys picta). are at their lowest annual levels (Pluto and Bellis 1986; Durlin and Schaffstall 2001). In contrast, at the time of hatchling emergence during April and May, water discharge levels are typically one order of magnitude higher (Durlin and Schaffstall 2001). Similarly, Australian Carettochelys insculpta Ramsay, 1886 delay emergence and exit nests coincidently with high river levels (Doody et al. 2001). One likely benefit of high river levels for hatchling turtles is the ability to rapidly move long distances downstream. Hatch- ling G. geographica sometimes move as much as 4000– 5000 m downriver during their first year (Pluto and Bellis 1988). Increased dispersal may increase opportunities for hatchlings to locate productive feeding and basking areas. High water levels may also contribute to high levels of food availability through bank erosion, floodplain inundation, and food mobility. Other, more indirect benefits could include a reduced chance of predation owing to increased water tur- bidity or to increased dispersion and thus low hatchling den- sities (Doody et al. 2001). Both rainfall and thermal cues have been implicated in prompting the emergence of hatchling turtles (Bustard 1967; Mrosovsky 1968; Alho and Padua 1982; DePari 1996; Tucker 1999; Doody et al. 2001). At our study site, the ma- jority of hatchling G. geographica emerged within 30 h after rain. Rain may facilitate emergence by softening nest substrates and likely reduces hatchling desiccation during sub- sequent migration to wetlands. Our results suggest that rain prompts the emergence of hatchling G. geographica, al- extensive supercooling capacity combined with a well- though hatchlings may require a period of ~12–24 h follow- developed resistance to inoculative freezing (Baker et al. ing a substantial rain to dig their way out of the nest. We 2003). This pattern contrasts with that of sympatric C. ser- also found that hatchlings emerged at nest temperatures of pentina hatchlings, which emerge from their nests during au- approximately 15 °C. In other turtle species, temperature tumn (Congdon et al. 1987, 1999) and freeze and die when thresholds appear to be similarly important for hatchling exposed to temperatures near –2 °C for ~24 h (Costanzo et emergence, although nest temperature gradients and diel al. 1995; Packard et al. 1999). In our study, all G. geo- changes in temperature may serve as more specific timing graphica hatchlings in nests in which winter temperatures cues (Tucker 1999; Doody et al. 2001). were recorded survived temperatures below –2.4 °C, and Several aspects of overwintering of hatchling G. geogra- some hatchlings survived brief periods of exposure to tem- phica were similar to those of the turtle Chrysemys picta. peratures below –8 °C (Fig. 2). In accordance with the labo- For example, both the minimum and maximum numbers of ratory results of Baker et al. (2003), we observed a total of days from egg deposition until hatchling emergence for 10 hatchlings in two natural nests survive temperatures be- Pennsylvania G. geographica (289–346, Fig. 1) were similar low –6 °C on five consecutive nights. To our knowledge, no to values reported for C. picta from New Jersey (288–346; turtle species other than C. picta has been shown to tolerate DePari 1996) and Idaho (292–348; Lindeman 1991). Also such low temperatures in nature. like C. picta, G. geographica neonates overwintered within The ability of hatchlings to tolerate subzero temperatures their shallow, terrestrial nest cavities and aligned themselves may contribute to the northerly distribution of G. geogra- in stereotypical arrangements (Fig. 3). Such behaviors in- phica. The remarkable ability of hatchling C. picta to toler- volved an overlapping, symmetrical organization and vertical ate subzero temperatures (to –11 °C in natural nests: orientation (Breitenbach et al. 1984; Packard et al. 1989; Woolverton 1963; Costanzo et al. 1995; Packard 1997; Nagle et al. 2000). Although the adaptive significance of Packard et al. 1997) has been suggested as a factor promot- these behaviors remains poorly understood, one postulated ing the species’ extreme northern distribution (Paukstis et al. benefit is increased resistance to ice inoculation (Costanzo et 1989; St. Clair and Gregory 1990). The range of G. geo- al. 2000; Nagle et al. 2000). graphica extends into southern Quebec and northern Ver- Our field data corroborate previous findings that hatchling mont (Gordon and McCullough 1980; Ernst et al. 1994), G. geographica exhibit a physiological tolerance for rela- making it the most northerly distributed Graptemys species tively low subzero temperatures (Baker et al. 2003). Hatchling and ranking it among the most northerly distributed turtles G. geographica tolerate subfreezing temperatures through an of North America. In comparison, hatchlings of two other,

© 2004 NRC Canada 1216 Can. J. Zool. Vol. 82, 2004 more southerly distributed Graptemys spp. are reported to Acknowledgments emerge during autumn (Vogt 1980), and hatchlings of these species may exhibit more limited cold tolerance than hatch- Partial funding was provided by the Pennsylvania Depart- ling G. geographica. ment of Transportation (PennDOT). Hatchlings were col- One potential cost of remaining in shallow terrestrial nest lected under a scientific permit issued by the Pennsylvania cavities throughout winter is death from exposure to subzero Fish and Boat Commission and animal care was conducted temperatures (Christens and Bider 1987; Packard et al. 1989; within the guidelines of the Canadian Council on Animal St. Clair and Gregory 1990; Packard 1997; Packard et al. Care. Previous versions of the manuscript were improved by 1997; Nagle et al. 2000). In our study, one half of all G. geo- comments from J. Congdon, M. Finkler, J. Hosler, and K. graphica hatchlings found dead were contained in three Noiseaux. We also thank D. Davis of PennDOT for logistical nests in which autumn emergence had occurred. This result support, V. Eilenberger, T. Enedy, and B. Ingram for field as- suggests that breaching the integrity of the nest cavity may sistance, and J. Lakso, P. Martin, and C. Yohn of Juniata expose hatchlings to deleterious winter conditions such as College for their continued support of the study. J. Schmid ice and cold ambient temperatures. Moreover, the presence and A. Shiels of the Pennsylvania Fish and Boat Commis- of emergence holes and degraded nest plugs during winter sion and T. Pluto of the US Army Corps of Engineers pro- may reduce successful cold tolerance mechanisms by in- vided helpful comments and insights. creasing hatchling contact with soil and water. Because increased hydration levels of both nest soil and hatchling References tissues reduce the ability of hatchlings to resist freezing (Costanzo et al. 1995, 1998; see also Packard and Packard Alho, C.J.R., and Padua, L.F.M. 1982. Reproductive parameters 2003, who argue that only water-saturated substrates present and nesting behaviour of the Amazon turtle Podocnemis expansa a high risk of freezing), it would likely be advantageous un- (Testudinata: Pelomedusidae) in Brazil. Can. J. Zool. 60(1): 97– der such circumstances for all hatchlings to exit the nest. We 103. hypothesize that fall emergence of G. geographica and other Baker, P.J., Costanzo, J.P., Iverson, J.B., and Lee, R.E. 2003. Ad- hatchlings may sometimes be a proximate response to de- aptations to terrestrial overwintering of hatchling northern map graded nests that provide poor structural or physical condi- turtles, Graptemys geographica. J. Comp. Physiol. B, 173: 643– tions for overwintering. 651. The average time from egg deposition to hatchling emer- Breitenbach, G.L., Congdon, J.D., and van Loben Sels, R.C. 1984. Winter temperatures of Chrysemys picta nests in Michigan: ef- gence for Pennsylvania G. geographica was approximately fects on hatchling survival. Herpetologica, 40: 76–81. 11 months, with about 9 of those months following hatch. Buhlmann, K.A., and Coffman, G. 2001. Fire ant predation of tur- The loss of 15% of body mass, on average, during over- tle nests and implications for the strategy of delayed emergence. wintering may be partially or wholly attributable to lipid ca- J. Elisha Mitchell Sci. Soc. 117: 94–100. tabolism (Congdon and Gibbons 1990). Because energy Bustard, H.R. 1967. Mechanism of nocturnal emergence from the exchange for individual eggs and hatchlings is limited to nest in green turtle hatchlings. Nature (Lond.), 214: 317. water, gases, and occasionally materials in the nest soil Cagle, F.R. 1939. A system of marking turtles for future recogni- (Packard et al. 2001; Costanzo et al. 2003), extended periods tion. Copeia, 1939: 170–173. spent in the nest require hatchlings to have high levels of en- Cagle, F.R. 1944. Activity and winter changes of hatchling Pseu- ergy reserves (Congdon 1989; Congdon and Gibbons 1990; demys. Copeia, 1944: 105–109. Nagle et al. 1998). In general, species whose hatchlings de- Cahn, A.R. 1937. The turtles of Illinois. Ill. Biol. Monogr. 16:1– lay emergence from the nest allocate higher amounts of en- 218. ergy storage lipids, such as triacylglycerol, to eggs compared Christens, E., and Bider, J.R. 1987. Nesting activity and hatching with species whose hatchlings exhibit early emergence success of the painted turtle (Chrysemys picta marginata)in (Congdon and Gibbons 1985, 1990; Rowe et al. 1995; Nagle southwestern Quebec. Herpetologica, 43: 55–65. et al. 1998, 2003). Although patterns of lipid storage and uti- Christiansen, J.L., and Gallaway, B.J. 1984. Raccoon removal, lization in G. geographica eggs and hatchlings have not been nesting success, and hatchling emergence in Iowa turtles with investigated, we predict that compared with other turtle spe- special reference to Kinosternon flavescens (Kinosternidae). cies, they contain high amounts of energy storage lipids. Southwest. Nat. 29: 343–348. In conclusion, the remarkable strategy of delayed nest Congdon, J.D. 1989. Proximate and evolutionary constraints on energy relations of reptiles. Physiol. Zool. 62: 356–373. emergence by hatchling turtles involves organized, stereo- Congdon, J.D., and Gibbons, J.W. 1985. Egg components and re- typical behaviors associated with successful overwintering. productive characteristics of turtles: relationships to body size. Proximate factors associated with the timing of emergence Herpetologica, 41: 194–205. include rainfall and thermal cues. 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