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Article

Drought Influences Annual Survival of Painted Turtles in Western Nebraska

by
Allyson N. Beard
† and
Larkin A. Powell
*
School of Natural Resources, University of Nebraska-Lincoln, 3310 Holdrege Street, Lincoln, NE 68583-0974, USA
*
Author to whom correspondence should be addressed.
†
Current address: School of Natural Resources, West Virginia University, 322 Percival Hall, Morgantown, WV 26506, USA.
Diversity 2023, 15(5), 597; https://0-doi-org.brum.beds.ac.uk/10.3390/d15050597
Submission received: 28 March 2023 / Revised: 15 April 2023 / Accepted: 26 April 2023 / Published: 27 April 2023
(This article belongs to the Special Issue Wildlife Population Ecology and Spatial Ecology under Global Change)
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Abstract

:
Aquatic habitats in the Great Plains of North America have increased risk of droughts under climate forecasts. Droughts have the potential to influence the population dynamics of pond turtles, and long-term studies are useful to assess the impact of climatic variation on turtles. We compiled twelve years of mark-recapture data for painted turtles (Chrysemys picta) captured in a pond in Keith County, Nebraska during 2005–2016 that included two periods of drought. We used a robust design analysis to investigate influences on population size, annual survival, temporary immigration, and capture probability. Estimates of the annual population size ranged from 92 (CI: 90–94) to 180 (CI: 175–186) but did not vary with drought conditions. Despite a relatively stable depth of water in our study pond, the probability of annual survival was reduced by 0.07 in females and 0.10 in males during drought years. Approximately one-fifth (temporary emigration probability: 0.19, CI = 0.16–0.23) of the population was outside the study pond at any given time. Our long-term research provides insights into the potential challenges to turtles in aquatic habitats undergoing prolonged changes in long-term climate conditions.

1. Introduction

Drought influences the demographics of wildlife species through impacts on reproduction [1], seasonal mortality [2], and distribution among habitat types [3]. Freshwater turtles are dependent on riverine or lacustrine habitats, which creates the potential for impacts of drought on movement, survival, and reproduction [4,5,6]. Typical responses of turtles to drought are to produce fewer eggs [7] or to move or alter the use of space [7,8,9]. In extreme situations, some pond turtles respond to drought by remaining in place in a state of estivation until sufficient rainfall returns [10].
Drought considerations, therefore, are critical to planning processes to support pond turtle species of conservation concern [11,12], and ~48% of turtle species are designated with a conservation status of threatened, endangered, or critically endangered [13]. Conservation planners in the central Great Plains recognize that the region is predicted to have increased risk of drought in current climate scenarios for the next century [14,15]. Effective planning for the management of threatened and endangered turtle species requires knowledge of drought effects in environmental systems, and long-term studies are especially valuable for this goal [16].
Our understanding of the cumulative, long-term impact of drought on turtle survival and movements is minimal as most studies on the effects of drought on pond turtles have been limited to a single drought cycle with a period of study less than five years in length (e.g., [8,17,18,19], but see 15-year study [7]). Long-term studies have greater potential to demonstrate differences in probability of survival between drought and non-drought years by increased sample size [20] and use of data across multiple drought cycles [21].
Our goal was to use a long-term, mark-recapture data set to evaluate effects of drought on the demography of a population of painted turtles (Chrysemys picta) located on the edge of the Nebraska Sandhills as drought conditions changed over 12 years. Our objectives were to: (1) estimate the annual size of the population of painted turtles at the study site, the probability of annual survival, and levels of movement away from our study site; and (2) evaluate the effect of drought conditions on these demographic parameters. We predicted that more severe drought conditions, with associated higher temperatures and lower pond water levels, would cause lower probability of annual survival and drive movements away from our study pond, which would influence local population size estimates during drought periods.

2. Materials and Methods

2.1. Study Area

Our study site was a 0.36 ha pond located in a privately owned pasture near Keystone, Nebraska in Keith County (Figure 1). Annual precipitation for the region ranges from 30 cm to 43 cm, and the study site is on the southwestern edge of the Sandhills region. Drought conditions are common in southwestern Nebraska during June. During 1950–2000, the region experienced 25 years of drought (drought risk = 0.49; as measured by the Palmer Drought Severity Index, PDSI, an index used to quantify drought conditions using temperature and moisture indicators; drought: PDSI < 0).
Rain and groundwater sources keep the water level of the pond relatively stable (+/−0.5 m), and the pond’s deepest area is ~2.5 m in depth. No fish have been documented in the pond during periodic seining, and northern crayfish (Orconectes virilis) and aquatic insects are abundant potential diet items. There are no known water bodies within 3 km of the pond, but the Platte River with two associated reservoirs is 5.3 km from the study site.
Our study pond hosted a super-population of painted turtles (including individuals temporarily away from the pond [22]) that varied from 113 to 223 individuals during our study period [23]. Painted turtles are widespread across much of North America [24], and the species is not threatened with extinction [25]. The environmental context of our study site provided a unique opportunity to study painted turtles, a species widespread in North America, in an environment with more limited rainfall and a landscape with sparse distribution of aquatic habitats (for comparison [5,6,26,27,28]).

2.2. Field Data Collection

We captured and marked painted turtles between 2005 and 2016 excluding 2009, with capture periods ranging from 3 to 26 days in each year during May, June, or July. Turtles were captured using basking traps and hoop nets [29,30]. We were aware that our trapping methods limited our ability to capture turtles with lengths less than ~70 mm [31], and methods were constant across the years. Turtles were removed from traps each morning (University of Nebraska-Lincoln IACUC Permits: 1074, 1568, 1993). We marked the turtles with individual marks on marginal scutes [32], and in 2014 we began to use PIT markers as a secondary method to confirm identification. We recorded the carapace length (mm), mass (g), and sex [24] of each turtle before releasing to the pond [33].

2.3. Weather and Climate Data

We acquired cloud cover data from NOAA’s National Centers for Environmental Information Local Climatological Data tool at the North Platte Regional Airport station for each day the turtles were trapped. The days that were predominately classified as broken clouds, overcast, or obscured sky between 12:00 and 19:00 were designated as cloudy days; otherwise, trap days were categorized as sunny.
We quantified drought conditions at our study site with the Palmer Hydrologic Drought Index (PHDI; National Oceanic and Atmospheric Administration). The PHDI measures hydrological impacts of drought conditions to reflect groundwater conditions, reservoir levels, and other values [34] relevant to aquatic turtles. We determined the mean PHDI in southwest Nebraska during the 12 months prior to June of each capture year [35] to quantify drought levels prior to capture events.

2.4. Analyses

We used a robust design analysis [22] using a program MARK framework [36] in the RMark package [37] to estimate the annual population size (N; we note that the model indirectly estimates N as derived from estimates of f(0), the number of individuals not captured during a closed capture period), annual survival (S), capture probability (p), recapture probability (c), and temporary emigration (γ′: the probability a marked individual will remain away from the study site during the annual time period; γ″: the probability that an individual will leave the study site). Our empirical data fitted the requirements of the robust design methods, as we had multiple capture occasions during each of successive years. The combination of closed (short periods of capture each year in which we assume no mortalities) and open (one-year gaps between successive capture events across years) population models in the robust design allows the estimation of temporary emigration in addition to estimation of population size and probability of annual survival [20].
Based on preliminary analyses [23], we simplified our analyses by setting the probability of capture (c) and recapture (p) as equal. We created 80 alternative models to describe variation in the demographic parameters. The models were combinations of null (no effect) and effects of drought and sex for annual survival, cloud cover and sex for capture probability, and drought and sex for temporary emigration. We assumed γ′ = γ″ for all models following [38].
We used a model selection framework [39] to evaluate evidence for variation of apparent survival and capture probability with Akaike’s Information Criterion corrected for a small sample (AICc). If the top-ranked model was not separated by >2.0 AICc, we were prepared to use conditional model averaging to calculate coefficients. We assessed variation in our annual estimates of population size using a linear model (PROC GLM [40]) with capture season (early summer: May, June; late summer: July, August) and PHDI during the previous year as explanatory variables.
To assess potential impacts of drought on the long-term survival of painted turtles at our study site, we developed a simulation model using PROC IML [40]. We used a range of annual drought risk from 0 to 0.6 in intervals of 0.1. For each of the seven levels of drought risk, we conducted a time series of 200 years; we modeled males and females separately and used sex-specific survival rates from our top-ranked estimation model. During each year, we generated a random number, x, from a uniform distribution between 0 and 1.0. If x was less than the drought risk, we considered the year to be a drought year; otherwise, the year was a non-drought year. We then used either drought or non-drought survival estimates and their associated level of variance to stochastically generate an annual probability of survival. Survival was generated as a beta random variable by specifying the parameter estimate and variance (from our field data) and solving for moment estimates of α and β, the beta parameters [41]. We then generated the beta random variate (annual survival) as a function of two gamma random deviates, with parameters α and β, respectively [42]. We calculated the mean annual survival, standard deviation, and 95% confidence interval across the 200 simulated years for each level of drought risk and compared the mean survival probabilities from our modeling exercise to cumulative survival curves to provide context for our results during time periods relevant to the life of a painted turtle.

3. Results

We documented 2431 captures of 343 unique individuals (153 males, 190 females) for painted turtles that spanned 93 trap days during the 12-year study. Annual capture totals ranged from 103 individuals in 2006 during 26 capture days to 30 in 2012 during two capture days. The annual mean PHDI was 0.83 during 2005–2016 (SD = 3.45, range: −4.48–6.72), and five of 11 years (drought risk = 0.45) were classified as drought (PHDI < 0; Figure 2).
The highest-ranking robust design model (AICc = 6888.07, wAIC = 0.23) included drought and sex effects for annual survival with time- and effect-constant estimates for movement and capture probabilities. The top model was also the simplest of the highest-ranked models (Table 1) with 16 parameters (k). Annual survival estimates declined ~7–10% during drought conditions for females (Snon-drought = 0.934, SE = 0.011, 95% CI: 0.908–0.953; Sdrought = 0.863, SE = 0.022, CI: 0.813–0.901) and males (Snon-drought = 0.897, SE = 0.018, CI: 0.857–0.927; Sdrought = 0.796, SE = 0.030, CI: 0.730–0.849; Figure 3). The probability for temporary emigration (γ: the probability of an individual being away from the pond in a given year) was 0.190 (SE = 0.019, CI = 0.155–0.231).
Two competing models had ΔAICc < 2.0 from the top model (Table 1). The second-ranked model (AICc = 6889.52, ΔAICc = 1.45, wAIC = 0.11) provided weak evidence for a negative drought effect on temporary emigration (γdrought = 0.168, SE = 0.034, CI: 0.111–0.246; γdrought = 0.199, SE = 0.023, CI: 0.158–0.247). The third-ranked model (AICc = 6890.02, ΔAICc = 1.95, wAIC = 0.09) included very weak evidence for sex-specific estimates for temporary emigration (γmale = 0.198, SE = 0.034, CI: 0.140–0.272; γfemale: 0.186, SE = 0.023, CI: 0.145–0.237). The top 11 models (cumulative wAIC = 0.82) included sex- and drought-specific estimates of annual survival.
The daily probability of capture was 0.188 (SE = 0.003, 95% CI: 0.180–0.195) and the top four models (cumulative wAIC = 0.52) included constant estimates for capture probability across time and weather conditions. The null model with constant parameter estimates (no effects) was ranked fourth to last (k = 14, AICc = 7104.88, ΔAICc = 216.81, wAIC = 0.0), and the most general model (k = 20, AICc = 6895.49, ΔAICc = 7.42, wAIC = 0.01) with all effects had very little support.
In-pond population size ranged from 92 (CI: 90–94) to 181 (CI: 175–186; in-pond density range: 256–503 turtles/ha). However, population size did not vary with the previous year’s drought conditions (F1,10 = 0.09, p = 0.77) or month (May/June vs. July/August) of capture (F1,10 = 1.00, p = 0.34).
The simulated mean annual survival for females ranged from 0.93 (SD = 0.01) with no drought risk to 0.89 (SD = 0.04) with a drought risk of 0.6 (the level of drought risk observed during our study period). Simulated mean annual survival for males ranged from 0.90 (SD = 0.02) with no drought risk to 0.84 (SD = 0.06) with a drought risk of 0.6. Mean annual survival for females and males dropped approximately 0.01 for a yearly increase in drought risk of 0.1 (Figure 4A). The cumulative impact of relatively small changes in mean annual survival is represented by a comparison of 20-year survival estimates (mean annual S = 0.93: 20-year survival = 0.23; 0.91: 20-year survival = 0.15; 0.89: 20-year survival = 0.10; 0.87: 20-year survival = 0.06; Figure 4B).

4. Discussion

4.1. Population Size

Our study pond was relatively small but supported a robust population of painted turtles (density: 256–502 turtles/ha). The pond receives direct and indirect nutrients from cattle in the surrounding pasture. Although our anecdotal observations suggest a relatively rich source of food, [43] reported that growth of painted turtles was reduced during drought years. Densities of painted turtles in other studies ranged widely from 22 turtles/ha in New York (3 ha pond) to 827 turtles/ha in a 5.7 ha marsh in Michigan [26,44,45,46,47].
We found variability in population size among the years (Figure 2). Although we found a reduction in annual survival of ~10% during drought years (Figure 3), the variation in population size was not related to drought conditions. We suspect that short-term dynamics of movement into and away from the pond are responsible for fluctuations in population size, but we found only weak evidence that temporary immigration (γ) was influenced by drought conditions.

4.2. Survival

Painted turtles are long-lived, and [48] estimated a maximum life expectancy in Illinois and Wisconsin of ~20–40 years. The annual survival rates we estimated are predicted to result in similar dynamics (Figure 3B). Annual survival in painted turtles varies among studies [45,49], and males typically have lower annual survival than females [46] (but see [47,48]). We note that the inference for our survival estimates is limited to individuals with lengths greater than ~70 mm due to our trapping methods [31,47].
We provide strong evidence for an effect of drought on annual survival of painted turtles. Although emigration has been previously documented to reduce population levels by 80% for painted turtles in a lake that dried completely for two consecutive years, the assessment of drought impact on mortality for that case was anecdotal [18]. Pond turtles (Actinemys marmorata) had reduced survival during a drought in which a pond completely dried [50], but we believe we are the first to demonstrate an impact of drought on the probability of survival in a pond system that remains intact during periods of drought. Our study was not designed to determine the mechanism for the reduction in probability of survival. However, reduction in the rates of growth of painted turtles, documented by [43] in our study pond, suggests that competition for food resources may become stronger during drought conditions [51,52].

4.3. Movement

Our study design allowed the use of the robust design analysis, which provided the opportunity to estimate temporary emigration away from our study site. Annual observations suggested that a relatively substantial proportion of previously trapped turtles were not captured despite adequate sampling pressure each year. The level of temporary emigration suggests that approximately one-fifth of the super-population using our study pond was away from the pond in a given year. Such high levels of temporary emigration were surprising given the distance to other permanent water sources, which suggests painted turtles are capable of navigating and exploring the surrounding semi-arid uplands to reach distant bodies of water. Emigrating painted turtles in Virginia traveled a mean distance of 2.4 km with a maximum emigration distance of 3.3 km [5]. We have occasionally sampled in the closest ponds, yet we have never captured any painted turtles at those locations. The destination of the individuals leaving our study site remains a mystery at present.
Painted turtles in other aquatic systems have been documented with higher rates of movement between study ponds [5,6,26] in landscapes with more aquatic resources. Emigration is also common for pond turtles when a water resource dries completely [5,6,7,53]. The lower level of temporary emigration we observed in our system is likely the result of limited destinations away from our study site. Although we found only weak evidence to suggest that drought affected movements away from our study pond, it is possible that turtles responded to short-term opportunities when rains provided for temporary connections to other water bodies through intermediate stopping sites in road ditches or drainage ditches in pastures and fields.

5. Conclusions

Our study confirms that drought conditions can impact the annual probability of survival in painted turtles in a pond with water levels that remain relatively constant during drier conditions. Although approximately one-fifth of the population had temporarily emigrated away from the study site each year, we found that drought conditions were not responsible for temporary movements. Similarly, the large variation in population size we saw over time was not correlated with drought conditions.
The northern Great Plains will be at higher risk for drought conditions in the future, and our local study of a large population of turtles over 12 years with a range of drought conditions has potential to inform how pond turtles may respond to warmer, drier periods in the future. We provide insights into the cumulative effects of reduced survival during drought conditions, and we encourage conservationists working with species of concern to use similar modeling exercises in their planning processes.

Author Contributions

Conceptualization, L.A.P.; methodology, L.A.P.; formal analysis, A.N.B. and L.A.P.; investigation, L.A.P.; resources, L.A.P.; data curation, L.A.P.; writing—original draft preparation, A.N.B.; writing—review and editing, A.N.B. and L.A.P.; visualization, A.N.B. and L.A.P.; supervision, L.A.P.; project administration, L.A.P.; funding acquisition, L.A.P. All authors have read and agreed to the published version of the manuscript.

Funding

This project was funded by Hatch Funds from the University of Nebraska-Lincoln’s Agricultural Research Division, University of Nebraska-Lincoln’s Undergraduate Creative Activities and Research Experience program, and the National Science Foundation (award number DUE-0531920).

Institutional Review Board Statement

This research conducted under University of Nebraska-Lincoln’s Institutional Animal Care and Use Committee Permits: 1074, 1568, 1993.

Data Availability Statement

The data used in this paper are available under Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) license through the UNL Data Repository at the following URL: https://0-doi-org.brum.beds.ac.uk/10.32873/unl.dr.20230303.

Acknowledgments

The long-term project was funded by Hatch Funds from the University of Nebraska-Lincoln’s Agricultural Research Division, University of Nebraska-Lincoln’s Undergraduate Creative Activities and Research Experience program, and the National Science Foundation (award number DUE-0531920). We are grateful to the staff of the Cedar Point Biological Station who provided logistical support during our research. A small army of student researchers including K. Powell and T. Powell volunteered their time to capture and measure turtles during the study. D. Tyre and D. Ferraro provided statistical assistance and logistical logical insights. Four anonymous reviewers provided useful comments that improved our manuscript.

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationship that could have appeared to influence the work reported in this paper.

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Figure 1. Aerial photo of landscape for the study site with absence of nearby open water. Inset map of Nebraska counties shows Keith County highlighted with location of aerial photo shown in white rectangle. Study pond is outlined by yellow rectangle.
Figure 1. Aerial photo of landscape for the study site with absence of nearby open water. Inset map of Nebraska counties shows Keith County highlighted with location of aerial photo shown in white rectangle. Study pond is outlined by yellow rectangle.
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Figure 2. Annual population size estimates (with 95% confidence intervals) for painted turtles in a pond near Keystone, Nebraska during 2005 to 2016. Years included in gray shading were classified as drought years (Palmer Hydrologic Drought Index < 0).
Figure 2. Annual population size estimates (with 95% confidence intervals) for painted turtles in a pond near Keystone, Nebraska during 2005 to 2016. Years included in gray shading were classified as drought years (Palmer Hydrologic Drought Index < 0).
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Figure 3. Annual survival probabilities (with 95% confidence intervals) of male and female painted turtles during drought and non-drought conditions near Keystone, Nebraska during 2005–2016. Drought conditions determined as Palmer Hydrologic Drought Index < 0.
Figure 3. Annual survival probabilities (with 95% confidence intervals) of male and female painted turtles during drought and non-drought conditions near Keystone, Nebraska during 2005–2016. Drought conditions determined as Palmer Hydrologic Drought Index < 0.
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Figure 4. Simulated survival of male and female painted turtles from empirical estimates during a range of modeled drought conditions near Keystone, Nebraska during 2005–2016: (A) mean annual survival (with 95% confidence intervals) from 200 replicate simulations given annual drought risk scenarios ranging from 0 to 0.6, and (B) cumulative probability of survival over 40 years given annual probabilities of survival ranging from 0.87 to 0.93 to provide context for the mean annual survival predications in panel (A) (the vertical dotted line provides example of differences in cumulative survival over 20 years).
Figure 4. Simulated survival of male and female painted turtles from empirical estimates during a range of modeled drought conditions near Keystone, Nebraska during 2005–2016: (A) mean annual survival (with 95% confidence intervals) from 200 replicate simulations given annual drought risk scenarios ranging from 0 to 0.6, and (B) cumulative probability of survival over 40 years given annual probabilities of survival ranging from 0.87 to 0.93 to provide context for the mean annual survival predications in panel (A) (the vertical dotted line provides example of differences in cumulative survival over 20 years).
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Table
Table 1. Comparison of alternative models considered in the robust design analyses for painted turtles (Chrysemys picta) in a pond near Keystone, Nebraska during 2005–2016, ranked by AICc. Notation for model structure describes S (annual survival), p (capture probability), and γ (annual probability of temporary emigration). All models indirectly estimated population size (N) as year-specific, and all models used γ″ = γ′ (annual probabilities of leaving the study site and staying away from the study site, respectively) and p = c (occasion-specific probability of capture, p, and recapture, c). Survival and movement parameters in some models varied by drought status and sex, while capture probability varied by sex and cloud conditions in some models). Constant parameters are noted by (.). We show the 16 highest-ranked models as a set with 90% of the wAIC from the 80, and sixty-four models are not shown.
Table 1. Comparison of alternative models considered in the robust design analyses for painted turtles (Chrysemys picta) in a pond near Keystone, Nebraska during 2005–2016, ranked by AICc. Notation for model structure describes S (annual survival), p (capture probability), and γ (annual probability of temporary emigration). All models indirectly estimated population size (N) as year-specific, and all models used γ″ = γ′ (annual probabilities of leaving the study site and staying away from the study site, respectively) and p = c (occasion-specific probability of capture, p, and recapture, c). Survival and movement parameters in some models varied by drought status and sex, while capture probability varied by sex and cloud conditions in some models). Constant parameters are noted by (.). We show the 16 highest-ranked models as a set with 90% of the wAIC from the 80, and sixty-four models are not shown.
RankModelkAICcΔAICcwAIC
1S (drought + sex) γ (.) p (.)166888.0700.23
2S (drought + sex) γ (drought) p (.)176889.521.450.11
3S (drought + sex) γ (sex) p (.)176890.021.950.09
4S (drought + sex) γ (.) p (sex)176890.092.020.09
5S (drought + sex) γ (.) p (cloudy)176890.102.030.09
6S (drought + sex) γ (sex + drought) p (.)186891.503.430.04
7S (drought + sex) γ (drought) p (cloudy)186891.553.480.04
8S (drought + sex) γ (drought) p (sex)186891.593.520.04
9S (drought + sex) γ (sex) p (cloudy)186892.053.980.03
10S (drought + sex) γ (sex) p (sex)186892.074.000.03
11S (drought + sex) γ (.) p (cloudy + sex)186892.164.100.03
12S (drought) γ (.) p (.)156893.034.960.02
13S (drought + sex) γ (sex + drought) p (cloudy)196893.485.410.02
14S (drought + sex) γ (sex + drought) p (sex)196893.505.440.02
15S (drought + sex) γ (drought) p (cloudy + sex)196893.575.500.02
16S (drought + sex) γ (sex) p (cloudy + sex)196894.055.980.01
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Beard, A.N.; Powell, L.A. Drought Influences Annual Survival of Painted Turtles in Western Nebraska. Diversity 2023, 15, 597. https://0-doi-org.brum.beds.ac.uk/10.3390/d15050597

AMA Style

Beard AN, Powell LA. Drought Influences Annual Survival of Painted Turtles in Western Nebraska. Diversity. 2023; 15(5):597. https://0-doi-org.brum.beds.ac.uk/10.3390/d15050597

Chicago/Turabian Style

Beard, Allyson N., and Larkin A. Powell. 2023. "Drought Influences Annual Survival of Painted Turtles in Western Nebraska" Diversity 15, no. 5: 597. https://0-doi-org.brum.beds.ac.uk/10.3390/d15050597

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