Editorial Type: ARTICLES
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Online Publication Date: 09 Dec 2022

Climate-Mediated Recruitment Failure in a Turtle Population and Its Bearing on Northern Limits of Distribution

Article Category: Research Article
Page Range: 181 – 186
DOI: 10.2744/CCB-1554.1
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Abstract

The eruption of Mount Pinatubo in the Philippines in June 1991 reduced global temperatures over the following 2 yrs. The greatest suppression (apart from Antarctica) was centered in the northern Great Plains of North America, directly over my long-term turtle study site. Temperatures at that site in 1992 and 1993 were the coldest in at least 50 yrs. Normal annual hatchling recruitment of yellow mud turtles (Kinosternon flavescens) in the spring following incubation at that site averaged 375; however, only 3 hatchlings emerged in 1993 (1992 incubation cohort), and none emerged in 1994 (1993 incubation cohort). The depressed temperatures apparently prolonged incubation times to such an extent in 1992 and 1993 that hatching was nearly impossible before winter mortality. The result was a gap in the age class structure that was still evident 26 yrs later. This site is at the northern range limit of this species, and this event suggests that incubation temperatures (i.e., summer season length) may be responsible for that limit.

Keywords: Kinosternon flavescens ; yellow mud turtle; Nebraska; Sandhills; Pinatubo eruption; northern limit

The impact of climate on reproductive success of organisms is undeniable and is expected to increase given global climate predictions (e.g., Patrício et al. 2021). For turtles, climate is known to impact at least nesting phenology (Janzen et al. 2018; Hedrick et al. 2021), nest success (Pike and Stiner 2007a, 2007b), reproductive output (Tomillo et al. 2009; Rollinson et al. 2012; Hedrick et al. 2017), sex ratios (Schwanz et al. 2010; Valenzuela et al. 2019), growth (Richard et al. 2014; Bjorndal et al. 2016), and survival (Converse et al. 2005; Blechschmidt et al. 2020). These impacts are expected to only increase as the rate of climate change continues to climb due to human activities. However, climate changes not related to humans can also occur, as in the case of geological (e.g., earthquakes and volcanoes) or astronomical (e.g., sun cycles and asteroid impacts) events. I have been monitoring a population of yellow mud turtles (YMTs) (Kinosternon flavescens) in the Sandhills of western Nebraska since 1981. Here I report on the catastrophic recruitment failure of the population over 2 yrs as a result of the global cooling induced by the eruption of Mount Pinatubo in June 1991.

METHODS

I monitored the population of YMTs at Gimlet Lake (lat 41°45.24′N, long 102°26.12′W), a shallow lake and associated wetlands on the Crescent Lake National Wildlife Refuge, Garden County, Nebraska (for study site description, see Iverson 1991; Iverson and Smith 1993) during most years from 1981 through 2018. At this site, YMTs typically overwinter terrestrially buried in upland sandhills adjacent to wetlands, then emerge in April and May and migrate to the water. Most females then return to the same sandhill to nest in June (Iverson 1990, 1991; Iverson et al 2009; see also Christiansen et al. 1985; Tuma 2006), although some do not reproduce every year (Iverson 1990). Median date of females moving to nest over 18 yrs (4984 records) was 17 June (range, 9–27 June; J.B. Iverson, unpubl. data; the subject of a separate article).

Of the eggs produced each year at this site, only about 19%–20% survive to hatching, primarily due to high rates of depredation by snakes and rodents (Iverson 1991). Surviving eggs hatch in the fall. Laboratory incubations at 27°C–28°C lasted 89–125 d and averaged 103 d in 4 studies (Lardie 1975, 1979; Christiansen et al. 1984; Thornton and Smith 1996) and at 30°C lasted 87–128 d, averaging 105 d (Ewert 1985). On hatching, neonates dig downward as much as 66 cm or more (i.e., well below the frost line; Costanzo et al. 1995) and brumate there. The following spring, hatchlings dig upward, emerge from the sandhill, and migrate to Gimlet Lake and associated wetlands (Iverson et al. 2009). Drift fences (1100 m total) constructed along the base of the sandhills allowed the capture during April–June of the entire hatchling cohort resulting from the eggs laid the previous year and all nesting females between late May and early July. I monitored the spring emergence of hatchlings (and other age classes) at the fences during 12 yrs (1983, 1986, 1988, 1990, 1993, 1994, 1998, 1999, 2000, 2006, 2007, and 2018).

Most turtles were initially aged confidently (as the number of winters post-hatching) as hatchlings or small juveniles based on the number of abdominal scute annuli and their size class cohort (Iverson 1991). However, 54 of the 1472 turtles captured in 2018 exhibited 10–20 annuli when first captured, and their initial ages were estimated only from counts of abdominal scute annuli. Hence, those estimates are believed to be accurate within 1–3 yrs based on initial comparisons with known age turtles with similar numbers of scute annuli. Four turtles exhibited more than 20 annuli in 1981–1982 when first captured (Hedrick and Iverson 2017); hence, their age estimates are minima.

Weather data were recorded at a NOAA weather station just north of Gimlet Lake, between 120 and 1000 m from the ends of the drift fences and were available since 1970. Degree-days (DD) were calculated as the difference in actual daily maximum temperature and 15.6°C (60°F), but only for days that reached above 15.6°C. Hence, a day with a maximum temperature of 25.6°C would accumulate 10 DD. This threshold reflects the general activity of YMTs at this site (J.B. Iverson, unpubl. data). Unfortunately, long-term data on soil temperatures are not available for this site.

RESULTS AND DISCUSSION

The mean of all daily maximum and minimum temperatures for April–September from 1970 to 2020 at my field site averaged 17.21°C, varied annually from 14.42°C (1993) to 20.07°C (2012), and increased by about 0.4°C per decade (Fig. 1; see also Hedrick et al. 2021). April–September 1993 was the coldest summer of the period (14.42°C), followed by the summers of 1982 (15.76°C) and 1992 (15.77°C). The record-cold summers of 1992 and 1993 have been linked to the eruption of Mount Pinatubo on 15 June 1991 and the effects of the atmospheric aerosols generated by that eruption (Hanson et al. 1996; Parker et al. 1996; Kirchner et al. 1999). The greatest summer temperature suppressions in North America during both those years were centered over the northern Great Plains (Fig. 3b in Hanson et al. 1996), including my study site.

Figure 1.Figure 1.Figure 1.
Figure 1. Temporal trend in the annual average of the mean daily maximum and minimum temperatures (°C) from April through September at Gimlet Lake in the Nebraska Sandhills from 1970 to 2020. Temperature = 0.0416(Year) – 65.703 (r2 = 0.39; p < 0.0001).

Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 2; 10.2744/CCB-1554.1

Figure 3.Figure 3.Figure 3.
Figure 3. Lack of significant relationship between the number of hatchling yellow mud turtles that emerged in the spring and the median date of nesting females in the previous summer (r2 = 0.224; p = 0.28).

Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 2; 10.2744/CCB-1554.1

The hatchling cohort varied from 0 to 712 per year over the 12 yrs when I monitored the spring emergence period (Table 1) but averaged 376 for the 10 yrs excluding 1993 and 1994. For 7 of those years, I had also monitored the fences during the entire nesting season in the previous summer and counted the total number of gravid females (determined by X-radiographs) that nested (Table 1). Although I expected that the number of hatchlings each year would be correlated with the number of females that nested the previous year (e.g., Tomillo et al. 2009), there was no such relationship (Fig. 2). In addition, I expected that spring hatchling numbers might reflect how late in the season females nested in the previous year. Although there was a trend for fewer hatchlings following years of late nesting (Fig. 3), the relationship was not significant given the small sample size. Instead, the size of the hatchling cohort was positively correlated with July–September mean temperatures (Fig. 4) and July–August mean temperature during the previous year (r2 = 0.439; p = 0.021), suggesting that low summer temperatures reduce the number of embryos that complete development before winter and die.

Table 1. Number of yellow mud turtles encountered at our fences for years when we monitored the spring emergence. Number of hatchlings refers to number captured in the spring of the year following nesting. Number of hatchlings in 1983 reflects most but not all of the initial fence, and numbers for 1986 and 1988 do not include a new section of the fence first installed in 1990; values in parentheses are extrapolations to captures at the total length of all fences using long-term relative capture numbers at each fence. Number of females in 1982 was similarly estimated. Asterisk indicates the exclusion of hatchling data from 1993 to 1994 (Pinatubo impact years).
Table 1.
Figure 2.Figure 2.Figure 2.
Figure 2. Lack of relationship between the number of hatchling yellow mud turtles that emerged in the spring and the number of females that nested in the previous summer (r2 = 0.081; p = 0.54).

Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 2; 10.2744/CCB-1554.1

Figure 4.Figure 4.Figure 4.
Figure 4. Relationship between mean temperature (°C) during July, August, and September and the size of the hatchling cohort of yellow mud turtles captured at our fences the following spring. Number = 92.835(Temperature) – 1532.7 (r2 = 0.426; p = 0.021).

Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 2; 10.2744/CCB-1554.1

This conclusion was supported by the fates of 4 YMT nests (22 total eggs) deposited between 16 and 28 June 1993, protected with hardware cloth, and excavated on 16 October 1993. Several eggs were desiccated or rotten, and all viable eggs contained near full-term embryos unlikely to hatch before winter given that daily mean air temperatures during the remainder of October averaged only 18.1°C maximum (range, –3.9°C–22.8°C) and –4.2°C minimum (range, –17.2°C–6.1°C).

The long-term impact of the 1993–1994 recruitment failure is evident from the complete age class distribution (by sex) of my 2018 sample (Fig. 5). My data suggest that the variability among age class sizes reflects the size of the original hatchling cohort, which is related to warmth of the previous summer. For example, the low recruitment in 1993 and 1994 and the high recruitment in 1998 (see Table 1) are reflected in the 26-, 25-, and 21-yr age classes, respectively.

Figure 5.Figure 5.Figure 5.
Figure 5. Age class distribution for all captured yellow mud turtles (Kinosternon flavescens) in 2018 (n = 1472). Ages for some individuals were estimated (estimated males, n = 25, and estimated females, n = 29) because they were not first captured as juveniles that could be aged precisely. Also, ages for all individuals older than 50 yrs of age (n = 4 females) are minimum estimates. All other males, females, and juveniles were initially aged as small juveniles (see text). Sexed turtles were at least 85-mm maximum carapace length. Note the gaps at age 25 yrs (3 hatchlings in 1993), 26 yrs (no hatchlings in 1994), and 36 yrs (an estimated 52 hatchlings in 1983) and the peak at age 21 yrs (from 725 hatchlings in 1998).

Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 21, 2; 10.2744/CCB-1554.1

CONCLUSIONS

The eruption of Mount Pinatubo in 1991 decreased global temperatures for the next 2 yrs, with extreme impact on the northern Great Plains, where my field site is located (Hanson et al. 1996). Because hatchling recruitment of YMTs at that site is positively correlated with summer temperatures during incubation the previous year, the record-low temperatures in 1992 and 1993 resulted in virtually no recruitment in 1993 and 1994. Surprisingly, hatchling recruitment had little relationship with the number of nesting females or the timing of nesting in the previous year.

The temperature effects described here suggest that incubation temperatures may limit the northern range of this turtle, as previously proposed by Iverson (1991) for this population and by Bobyn and Brooks (1994) and Brooks (2007) for turtles at their northern distribution limits in Ontario, Canada. This conclusion is supported by the fact that YMT populations in the Nebraska Sandhills (the northern range limit) have a relict distribution associated locally with wetlands with elevated sandhills generally facing south (Iverson et al. 1983), that is, the warmest available sites for brumation, nesting, and incubation. Elevated sandhills face southwest and southeast at Gimlet Lake and support most of the resident subpopulations.

Although cooler summers (mean July–September temperatures < 18.1°C) have resulted in little or no hatchling recruitment of YMTs at my field site, the changing climate produces increasingly warmer summers on average (Fig. 1), which will likely continue. Hence, annual hatchling recruitment is expected to increase with time, and the distribution of YMTs is expected to expand northward at 26 to 57 km per decade (Butler et al. 2016). Fortunately, the combination of this climate change effect and the long life of this turtle (Hedrick and Iverson 2017) minimized the negative impact of the 2 yrs of recruitment failure demonstrated here.

Only 1 other instance of the impact of the eruption of Mount Pinatubo on recruitment in a freshwater turtle has been reported. Greaves and Litzgus (2009) noted a reduction in the size of the 12- to 14-yr-old age cohort in Glyptemys insculpta in Ontario as a result of the lower ambient temperatures following that eruption. However, the extent of that reduction was not quantified. The effects of the Pinatubo eruption on reproduction have also been reported for Arctic birds (negative; Ganter and Boyd 2000) and polar bears (positive; Stirling et al. 1999).

Finally, the effects of summer temperature are also complicated by the fact that YMTs exhibit temperature-dependent sex determination, with the production of all females at high constant temperatures and mostly males at low constant temperatures (Ewert et al. 1994). This pattern suggests that female YMTs are produced in most years, even after relatively cool summers. For example, the sex ratio (males/total) of 55 emerging hatchlings captured between 9 May and 6 June 1990 from near our field site was only 29% male (M.A. Ewert, pers. comm., October 1990), following a year with cooler-than-average temperatures (Table 1; long-term sex ratio of 4237 adults captured at fences in the spring was 40% male). Furthermore, I found no relationship between the sex ratio (males/total) of individual age cohorts with n ≥ 10 captured in 2018 (see Fig. 5) and July–September temperatures during the year in which that cohort was incubating (n = 17; r2 = 0.009; p = 0.72). This result is perhaps not surprising given the general difficulty in predicting sex ratios from air temperatures (Leivesley et al. 2022).

The minimal impact on this turtle population of a 2-yr recruitment failure emphasizes the adaptive significance of the typical (though not universal) turtle life-history strategy of late maturity and long life (Congdon et al. 2022), even in a species like this, in which only a single small clutch (mean = 6.5 eggs; Iverson 1991) is produced in a year and ∼ 25% of females currently forgo reproduction in any given year (Iverson 1990).

Acknowledgments

I would like to thank the staff of Crescent Lake National Wildlife Refuge for permitting my fieldwork since 1981, in particular Refuge Biologist Marlin French, who facilitated our work there for the past 25 yrs. The field assistance of many Earlham students was essential for this work. Funding was provided by Earlham College, the Joseph Moore Museum of Natural History, and the National Science Foundation (IOS-1257857 to F.J. Janzen and D.A. Warner). Annual permits were provided by the Nebraska Game and Parks Commission. Most of this work was done before the advent of the Earlham College Institutional Animal Care and Use Committee but was approved by that committee beginning in 2014 (20140516-2JI). For the entire project, I abided by the ethical guidelines published by the SSAR Guidelines for the Use of Live Amphibians and Reptiles in Field Research. The constructive comments of Geoff Smith and 2 anonymous reviewers on an early draft of the article were much appreciated.

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Copyright: © 2022 Chelonian Research Foundation 2022
Figure 1.
Figure 1.

Temporal trend in the annual average of the mean daily maximum and minimum temperatures (°C) from April through September at Gimlet Lake in the Nebraska Sandhills from 1970 to 2020. Temperature = 0.0416(Year) – 65.703 (r2 = 0.39; p < 0.0001).

Figure 3.
Figure 3.

Lack of significant relationship between the number of hatchling yellow mud turtles that emerged in the spring and the median date of nesting females in the previous summer (r2 = 0.224; p = 0.28).

Figure 2.
Figure 2.

Lack of relationship between the number of hatchling yellow mud turtles that emerged in the spring and the number of females that nested in the previous summer (r2 = 0.081; p = 0.54).

Figure 4.
Figure 4.

Relationship between mean temperature (°C) during July, August, and September and the size of the hatchling cohort of yellow mud turtles captured at our fences the following spring. Number = 92.835(Temperature) – 1532.7 (r2 = 0.426; p = 0.021).

Figure 5.
Figure 5.

Age class distribution for all captured yellow mud turtles (Kinosternon flavescens) in 2018 (n = 1472). Ages for some individuals were estimated (estimated males, n = 25, and estimated females, n = 29) because they were not first captured as juveniles that could be aged precisely. Also, ages for all individuals older than 50 yrs of age (n = 4 females) are minimum estimates. All other males, females, and juveniles were initially aged as small juveniles (see text). Sexed turtles were at least 85-mm maximum carapace length. Note the gaps at age 25 yrs (3 hatchlings in 1993), 26 yrs (no hatchlings in 1994), and 36 yrs (an estimated 52 hatchlings in 1983) and the peak at age 21 yrs (from 725 hatchlings in 1998).

Contributor Notes

Handling Editor: Peter V. Lindeman

Received: 02 Jul 2022
Accepted: 19 Aug 2022
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