Janzen,
Fredric
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Joint estimation of growth and survival from mark–recapture data to improve estimates of senescence in wild populations: Reply
Becoming creatures of habit: among‐ and within‐individual variation in nesting behavior shifts with age
The quantification of repeatability has enabled behavioral and evolutionary ecologists to assess the heritable potential of traits. For behavioral traits that vary across life, age-related variation should be accounted for to prevent biasing the microevolutionary estimate of interest. Moreover, to gain a mechanistic understanding of ontogenetic variation in behavior, among- and withinin- individual variance should be quantified across life. We leveraged a 30-year study of painted turtles (Chrysemys picta) to assess how age contributes to variation in the repeatability of nesting behaviors. We found that four components of nesting behavior were repeatable, and that accounting for age increased the repeatability estimate for maternal choice of canopy cover over nests. We detected canalization (diminished within-individual variance with age) of canopy cover choice in a reduced dataset despite no shift in repeatability. Additionally, random regression analysis revealed that females became more divergent from each other in their choice of canopy cover with age. Thus, properly modeling age-related variance should more precisely estimate heritable potential, and assessing among- and within-individual variance components in addition to repeatability will offer a more mechanistic understanding of behavioral variation across age.
Risk-sensitive maternal investment: an evaluation of parent–offspring conflict over nest site choice in the wild
Parents increase their fitness by investing resources to offspring. However, such investment is costly for parents, leading to tradeoffs, which should shift towards heavier investment to reproduction as females age and future reproductive opportunities decrease. Nests of aquatic turtles laid farther from water have higher survival than those laid closer to shore because nest predators often forage along environmental edges. However, the predation risk of adult females increases farther from water because water is used as refuge from terrestrial predators. Thus, females may balance investment in current offspring vs. maternal survival and future offspring. To test if investment varies depending upon perceived risk, we exposed 30 painted turtles (Chrysemys picta) to simulated predation by capturing and handling them shortly after females chose a nest site. We then released females, which fled to water, and allowed them to return to land and nest undisturbed. We compared the distance to water of nests laid before and after simulated predation. Unexpectedly, females did not vary distance to water in response to simulated predation. Regardless, nest sites chosen after simulated predation were more likely to be depredated than those chosen before simulated predation, suggesting females altered nest-site choice in ways we did not quantify. In addition, although older turtles nested almost twice as far from water as younger turtles, we found no evidence that age influenced maternal response to simulated predation. Our findings suggest perceived risk of mothers to predation influences nest-site choice and subsequently reduces offspring survival in C. picta. In addition, we provide a rare assessment of how plastic maternal investment might vary across reproductive life.
Joint estimation of growth and survival from mark‐recapture data to improve estimates of senescence in wild populations
Understanding age-dependent patterns of survival is fundamental to predicting population dynamics, understanding selective pressures, and estimating rates of senescence. However, quantifying age- specific survival in wild populations poses significant logistical and statistical challenges. Recent work has helped to alleviate these constraints by demonstrating that age specific survival can be estimated using mark recapture data even when age is unknown for all or some individuals. However, previous approaches do not incorporate auxiliary information that can improve age estimates of individuals. We introduce a survival estimator that combines a von Bertalanffy growth model, age-specific hazard functions, and a Cormack-Jolly-Seber mark-recapture model into a single hierarchical framework. This approach allows us to obtain information about age and its uncertainty based on size and growth for individuals of unknown age when estimating age-specific survival. Using both simulated and real-world data for two painted turtle (Chrysemys picta) populations, we demonstrate that this additional information substantially reduces the bias of age-specific hazard rates, which allows for the testing of hypotheses related to aging. Estimating patterns of senescence is just one practical application of jointly estimating survival and growth; other applications include obtaining better estimates of the timing of recruitment and improved understanding of life history trade-offs between growth and survival.
Age Predicts Risky Investment Better Than Residual Reproductive Value
Life-history theory predicts that investment in reproduction should increase as future reproductive potential (i.e., residual reproductive value [RRV]) decreases. Researchers have thus intuitively used age as a proxy for RRV and assume that RRV decreases with age when interpreting age-specific investment. Yet age is an imperfect proxy for RRV and may even be a poor correlate in some systems. We used a 31-year study of the nesting ecology of painted turtles (Chrysemys picta) to assess how age and RRV compare in explaining variation in a risky investment behavior. We predicted that RRV would be a better predictor of risky investment than age because RRV accounts for variation in future reproductive potential across life. We found that RRV was high in early life, slowly decreased until midlife, and then steadily decreased to terminal reproduction. However, age predicted risky behavior better than RRV. This finding suggests that stronger correlates of age (e.g., size) may be more responsible for this behavior in turtles. This study highlights that researchers should not assume that age-specific investment is driven by RRV and that future work should quantify RRV to more directly test this key element of life-history theory.
Insights from Population Genomics to Enhance and Sustain Biological Control of Insect Pests
Biological control—the use of organisms (e.g., nematodes, arthropods, bacteria, fungi, viruses) for the suppression of insect pest species—is a well-established, ecologically sound and economically profitable tactic for crop protection. This approach has served as a sustainable solution for many insect pest problems for over a century in North America. However, all pest management tactics have associated risks. Specifically, the ecological non-target effects of biological control have been examined in numerous systems. In contrast, the need to understand the short- and long-term evolutionary consequences of human-mediated manipulation of biological control organisms for importation, augmentation and conservation biological control has only recently been acknowledged. Particularly, population genomics presents exceptional opportunities to study adaptive evolution and invasiveness of pests and biological control organisms. Population genomics also provides insights into (1) long-term biological consequences of releases, (2) the ecological success and sustainability of this pest management tactic and (3) non-target effects on native species, populations and ecosystems. Recent advances in genomic sequencing technology and model-based statistical methods to analyze population-scale genomic data provide a much needed impetus for biological control programs to benefit by incorporating a consideration of evolutionary consequences. Here, we review current technology and methods in population genomics and their applications to biological control and include basic guidelines for biological control researchers for implementing genomic technology and statistical modeling.
Sex and Incubation Temperature Independently Affect Embryonic Development and Offspring Size in a Turtle with Temperature-Dependent Sex Determination
Developmental environments can have lasting effects on an individual’s phenotype. In many reptiles, for example, egg incubation temperature permanently determines offspring sex (temperature-dependent sex determination, TSD) and also influences a suite of morphological, physiological, and behavioral traits. Thus, the contributions of sex and incubation temperature to phenotypic variation are difficult to identify because these factors are confounded under TSD. We used chemical manipulations to experimentally decouple gonadal sex and incubation temperature in a turtle with TSD (Chrysemys picta) to examine their relative and interactive effects on variation in incubation duration and offspring size. We show that warm incubation temperature accelerates development as expected and that exogenous estradiol treatment to eggs further shortens incubation duration across all incubation temperatures. Moreover, estradiol unexpectedly induced male development, resulting in male offspring hatching sooner than female offspring. Variation in offspring size was also influenced by incubation temperature and gonadal sex, but interactions between these two variables were relatively small or nonsignificant. The fitness consequences of these effects are unknown, but we provide preliminary results from our attempts at examining the long-term and sex-specific effects of incubation temperature. Manipulative experimental approaches, combined with longer-term experiments that track individuals through reproduction, will provide novel insights into the adaptive significance of developmental plasticity in long-lived organisms.
Modeling Onset of Hourly Nesting Activity in a Freshwater Turtle Using Abiotic Variables and Physiological Capacity
Nesting is an essential, yet variable, reproductive behavior in most oviparous organisms. Although many factors conceivably influence nesting behaviors, it is unclear which factors strongly influence terrestrial nest timing in aquatic nonavian reptiles. As climate is changing rapidly, understanding the relative influences of biotic and abiotic factors on nesting behaviors may yield important information on future changes in daily and seasonal nesting activity. We collected hourly data to examine the significance of local weather conditions to the timing of within-season nesting activity in a large population of Painted Turtles (Chrysemys picta). We quantified nesting activity as the ratio of females who nested to all females who could nest in each hour, adjusting the size of the denominator to include the time required to shell a subsequent egg clutch. We then used zero-inflated models to identify potential weather predictors of presence/absence of nesting activity and strength of nesting responses (i.e., the fraction of turtles nesting that could nest). Higher temperatures and rainfall predicted stronger nesting responses, whereas lower temperatures and no rainfall predicted the absence of nesting activity, indicating that both temperature and rainfall are important cues in within-season nesting phenology. Our study enhances our understanding of abiotic influences on the terrestrial nesting behavior of aquatic organisms.
Nest Temperatures Predict Nest Emergence of Painted Turtle (Chrysemys picta) Offspring
Environmental conditions during embryonic development affect morphology, behavior, and survival in turtles. Nest temperature also could affect posthatching traits of offspring, such as emergence behaviors. We monitored thermal conditions in painted turtle (Chrysemys picta) nests along the Mississippi River in Illinois to examine their influence on offspring survival and nest emergence. We recorded hourly temperatures within nest cavities during embryonic development in summer 2016 (n = 34) and after hatching through the following January (n = 15–20). Hatching success and posthatching survival appeared to be largely unaffected by thermal conditions recorded in nests. Emergence of neonates from nests was observed from 19 March through 12 May 2017. Onset of offspring emergence occurred later in the spring for nests with greater exposure to subzero temperatures in winter. For nearly all nests with live offspring, siblings did not emerge en masse, but instead departed the nest across multiple days. Nests with higher mean temperatures during incubation exhibited earlier mean emergence dates in spring, yet emergence duration was positively correlated with thermal maxima experienced in nests in fall and winter. Thus, thermal environments in nests at different times of year apparently elicited variation in spring emergence timing of C. picta hatchlings.
What Have Long-Term Field Studies Taught Us About Population Dynamics?
Long-term studies have been crucial to the advancement of population biology, especially our understanding of population dynamics. We argue that this progress arises from three key characteristics of long-term research. First, long-term data are necessary to observe the heterogeneity that drives most population processes. Second, long-term studies often inherently lead to novel insights. Finally, long-term field studies can serve as model systems for population biology, allowing for theory and methods to be tested under well-characterized conditions. We illustrate these ideas in three long-term field systems that have made outsized contributions to our understanding of population ecology, evolution, and conservation biology. We then highlight three emerging areas to which long-term field studies are well positioned to contribute in the future: ecological forecasting, genomics, and macrosystems ecology. Overcoming the obstacles associated with maintaining long-term studies requires continued emphasis on recognizing the benefits of such studies to ensure that long-term research continues to have a substantial impact on elucidating population biology.