TY - JOUR
AU - Ryerson, William, G
AB - Abstract In response to the growing number of amphibian and reptiles species in decline, many conservation managers have implemented captive breeding and headstarting programs in an effort to restore these populations. However, many of these programs suffer from low survival success, and it is often unclear as to why some individuals do not survive after reintroduction. Here I document changes to head morphology in the eastern garter snake, Thamnophis sirtalis, in response to time spent in captivity. Thamnophis raised on three diet treatments all differed in head size from wild individuals, and head size differed between the three treatments. Overall, head size was smaller in all three diet treatments than in wild snakes, potentially limiting the available prey for the captive garter snakes. Allometric patterns of growth in head size were also different for each diet treatment. Several potential implications of these changes in morphology are discussed, and what these changes may mean for other species that are part of headstarting and reintroduction programs. Introduction The current global biodiversity crisis is projected to become the sixth mass extinction in Earth’s history (Ceballos et al. 2015). Amphibian and reptile populations across the globe have been particularly hard-hit, with current estimates suggesting almost 50% of amphibians and 20% of reptiles face the threat of extinction (International Union for the Conservation of Nature [IUCN] 2017). The cause of these declines is rooted in human activities, most notably habitat loss for development and commercial harvest for food and/or the exotic pet trade (Stuart et al. 2004). In response to the rapid increases in extinction and human-induced population loss, conservation organizations and managers around the world have sought out approaches to stem the rate of decline or potentially reverse them. The strategies used to mitigate these declines focus on the augmentation of populations and strategic habitat use. In North America, the most common approach to restore declining species has been to captive breed or headstart juveniles prior to release in the wild (Seddon et al. 2014; Burke 2015). Headstarting programs consist of two major pathways: captive breeding and/or captive rearing. In a captive breeding program, adults from a population are captured and maintained in captivity. If successful breeding occurs, the juveniles are then raised in captivity until they reach a pre-determined size/age, at which point they are released into the wild. Captive rearing programs involve the collection of eggs or juveniles from the wild, raising juveniles away from potential predation and with ample food resources until they are determined to be large enough, and then subsequently released. However, while size has been typically used to determine the endpoint of a headstarting program (Burke 2015; Roe et al. 2015; Tetzlaff et al. 2019a), other performance and ecological metrics of fitness may be just as critical to the long-term success of a reintroduction program. Despite the importance of morphology, performance, and behavior to fitness, we know little about the effects of captivity on these aspects of biology. Much of our understanding comes from mammals, where changes in skull size and shape have been observed in several different groups (Wisely et al. 2002; O’Regan and Kitchener 2005; Hartstone-Rose et al. 2014; Curtis et al. 2018). The biggest implications are for carnivores, particularly those that can take advantage of consuming bone and other tough materials, which may become limited in light of changes to the skull (Hartstone-Rose et al. 2014). Our understanding of morphological changes in the reptiles is far less clear. The only example of the effects of long-term captivity on head shape and size are to be found in the American alligator (Alligator mississippiensis), farmed throughout the southeastern USA for their meat and skin. Analysis of the skulls of both captive and wild alligators found a sharp increase in the variation of skeletal elements in the captive individuals, in almost every metric measured (Drumheller et al. 2016). Drumheller et al. (2016) make the argument that corresponding increase in variation in captive alligators is likely to be the result of relaxed selection or possibly pedomorphic in nature. Along with these morphological changes, changes in performance are also observed, with captive alligators biting with higher forces than their wild counterparts (Erickson et al. 2004). How these effects manifest in other amphibians and reptiles is still unknown. Amphibians and reptiles are considered to be well-suited for these types of programs, as they considered easier to keep and breed in captivity than imperiled mammals and birds (King and Stanford 2006; Germano and Bishop 2009). There are currently multiple programs across the USA focusing on the captive breeding and headstarting of snakes as part of reintroduction programs (Kingsbury and Attum 2009). The success rate of these programs is surprisingly low, given the resources and time many organizations devote to their success. Survival of headstarts in their first year hovers around 10% in most species (Dodd and Siegel 1991), although some programs have noted slightly higher rates (King and Stanford 2006). In comparison, wild survivorship in several species of Thamnophis snakes is approximately 20% year-to-year in juvenile, and up to 60% in adults (Larsen and Gregory 1989; Bronikowski and Arnold 1999; Lind et al. 2005). There are multiple challenges that must be overcome for any individual to survive, including but not limited to finding food, avoiding predation, and overwintering successfully (Reinert and Rupert 1999). Individuals that survive to maturity must then locate a mate and successfully reproduce if the population restoration program is to succeed. Our limited understanding of these challenges in snakes has found that individuals can and will fail at any of these aspects of their biology, resulting in the loss of that individual from the breeding population (King and Stanford 2006). It is likely that aspects of the captive husbandry and headstarting conditions of snakes will have a strong impact on an individual’s likelihood of survival (Roe et al. 2015). Snakes present a unique opportunity to examine the effects of captive husbandry on morphology and behavior. Previous work examining the links between diet and head shape in snakes have documented extensive variation across species. In the wild, many species exhibit ontogenetic changes in head shape that are closely linked with simultaneous changes in diet. One of the best examples comes from the North American genus Nerodia, a heavy-bodied natricine snake found near water bodies throughout the continent. As juveniles, Nerodia have relatively narrow heads, and feed primarily on small fish and then transition to feeding on wide-bodied fish (e.g., Centrarchidae, the freshwater sunfishes) and frogs as adults (Muskinsky et al. 1982; Dwyer and Kaiser 1997; Vincent et al. 2007). During this transition, changes in skull morphology occur, and are hypothesized to allow for the adult snakes to more effectively capture and swallow the stockier prey items (Vincent et al. 2007; Hampton 2014). Several other natricines have converged on this morphology, allowing the adults to not only avoid direct competition with juveniles for food resources, but allow the adults to move into previously unexploited prey types as well (Dwyer and Kaiser 1997; Perkins and Eason 2019). When the diet changes are less drastic across ontogeny, juveniles are frequently observed to have relatively larger heads for their body-size (King et al. 1999; Vincent et al. 2006; Borczyk 2015). The relatively larger heads allow for juveniles to access a more diverse array of prey species, while as adults the same prey are already available to them (Vincent et al. 2006). This is particularly true for many North American colubrids, especially those that feed on small mammals, lizards, and other snakes (King et al. 1999). Similarly to wild snakes, some taxa show almost no effect of diet and captive husbandry on head morphology (Schuett et al. 2005) while others exhibit changes to almost every element of head morphology linked to captive husbandry (Bonnet et al. 2001; Smith 2014). Growth rates between wild and captive raised snakes may vary, which may be linked to foraging success and changes in feeding behavior upon release (Burghardt and Krause 1999; Roe et al. 2015; Steen et al. 2016). Similar changes are found in other behaviors, including spatial ecology (Glaudas and Alexander 2017), and the ability to locate hibernacula for overwintering (Reinert and Rupert 1999). Captively raised indigo snakes (Drymarchon couperi) exhibit changes in their tongue-flicking behavior through ontogeny (Goetz et al. 2018). Indigo snakes are generalist predators, with prey items including lizards, birds, and other snakes (Stevenson et al. 2010). In captivity, fed a mix of rodent and snake prey, juvenile indigo snakes altered their tongue-flicking behavior (Goetz et al. 2018) and feeding behavior (Wines et al. 2015). Upon release, indigo snakes were observed to feed on different prey than what is known for wild indigoes (Steen et al. 2016). These changes, even if perceived to be relatively minor changes in behavior and ecology, can have drastic implications for the survival of an individual and its contribution to the restoration of a population (Elgee and Blouin-Demers 2011).The diversity of responses, in both behavior and morphology, suggest that there is still much to learn about the responses of snakes to captivity. Ultimately, the goal of headstarting and reintroduction programs is to restore populations to stable levels. A better understanding of the long-term effects of captivity on the behavior and morphology of snakes is likely to better inform the reintroduction process, with the aim of increasing the success of these programs (Jachowski et al. 2016). This work examines the effects of captivity and diet on the head morphology of the eastern garter snake, T. sirtalis. Thamnophis sirtalis are common throughout their range in the USA, many aspects of their biology are well understood. Previous work has examined differences in head morphology and body size across this range (Krause et al. 2003), and that differences in the head morphologically are not induced plastically by temperature (Arnold and Peterson 1989). Three litters of garter snakes were raised from birth and separated into three diet treatments consisting of a mix of earthworms and fish, following protocols on the care and husbandry of garter snakes in captivity (Bartlett and Bartlett 2001; Perlowin 2005). These individuals were kept in the lab for a period of 1 year, after which they were released to the wild. During their time in captivity, they were measured for changes in head size. At the end of their stay, prior to release, I also measured head size in a wild population of garter snakes from southern New Hampshire (NH), USA. By directly comparing wild snakes with the captive-raised individuals, I can examine not only the effects of diet on these morphological parameters, but also the general effects of captivity. My hypothesis is that diet will have an impact on the head size in captive snakes, but that the overall patterns of head shape be similar to wild snakes, with the exception of more variation evident than observed in wild snakes, as evidenced by other reptiles (Drumheller et al. 2016). Increased variation in morphology is likely to have an impact on performance (Erickson et al. 2004; Steen et al. 2016) ultimately leading to variation in the survival of individuals once they are released into the wild. Captive husbandry and headstarting programs will optimize their protocols in order to ensure higher success rates, and studies of captive rearing on morphology may provide insight into the current difficulties with survivorship of released individuals. Methods All animal experiments and procedures were approved by Saint Anselm College IACUC (SAC #005) and the NH Fish and Game Department. Three adult female eastern garter snakes (T. sirtalis) were captured by hand in southern and central NH during the summer months of 2017. While in captivity, each female birthed a litter, totaling 76 neonate snakes. One week after birth, the adult females were returned to the site of capture. The neonates were separated into individual Sterilite (model #1922-04) seven-quart containers. Each Sterilite container was lined with paper towels, and water provided ad libitum. Containers were kept in the Saint Anselm College animal care facility, on a 12 h light:dark cycle. Each container was heated from underneath with 3 inch wide THG heat tape (4 watts/ft of tape, THGheat.com). The heat tape was placed underneath the Sterilite container so that a 2 inch wide strip of the heat tape was directly under the container, the remaining diameter exposed to air to allow for circulation. The placement of the heat tape created a heat gradient within each cage, with a warm end at 28°C and a cool end at 25°C. The temperature at the warm end of the containers was regulated using a VE-300 thermostat (Vivarium Electronics, High Point, NC, USA). One in every 10 containers were directly monitored using the thermostats, the others had their temperatures verified daily using a Smart Sensor AR320 temperature gun (Smart Sensor, Dongguan, China). Neonates were randomly assigned to one of three diet treatments: fish, earthworm, or both. The fish diet consisted of small, live “rosy red minnows” (a commercially bred variant of the fathead minnow, Pimephales promelas). The earthworm diet was composed of earthworms (Lumbricus terrestris) that had been cut into smaller pieces as suggested by captive care manuals and others (Bartlett and Bartlett 2001; Perlowin 2005; King and Stanford 2006). Individuals assigned to the both treatment were given food items from the previous two categories. Neonates that did not feed in the first month were released to the site of their mother’s capture and are not included in this analysis. All individuals were fed twice a week for the first 6 months, then once a week for the second 6 months. The total mass of food offered was weighed prior to offering to each individual. Individuals were provided food during each feeding until they refused to eat further. The total prey mass consumed was then estimated to be the total mass offered to each individual minus the remainder that was not consumed. To ensure consistency, measurements of the body and head were done using the same methods for both the captive and wild garter snakes. Body measurements were taken once a month, mass with a digital scale (OHAUS Adventurer AR3130, OHAUS Corporation, Parsippany, NJ, USA), and snout–vent length (SVL) using a string held to the tip of the snout and the vent, while the individual was held in hand. I used a Mitutoyo digital caliper to take measurements (±0.01 mm) of head size. I assessed head size using 11 parameters of the head (Fig. 1): (1) Width at the nares, (2) width at the eyes, (3) width at the jaw joint, (4) width at the end of the head, (5) head length; (6) mandible length; (7) eye diameter; (8) height at the nares, (9) height at the eye, (10) height at the jaw joint, and (11) height at the end of the head. The measurement locations were chosen following previous measures of snake head dimensions (Vincent et al. 2004a, 2004b; Herrel et al. 2011; Penning 2017; Penning et al. 2020), as well as ease of measurement in the field. Linear measurements were chosen over landmark-based approaches (e.g., geometric morphometrics) for two reasons: (1) linear measurements can be directly compared with several over recent works on scaling of head morphology in snakes (Herrel et al. 2011; Penning 2017; Penning et al. 2020) and (2) preliminary tests of landmark-based approaches using digital images were more prone to measurement error than the linear caliper-based approach, as a result of the small head size of the individuals. After 1 year, the juvenile snakes were released to the site of their mother’s capture, in August 2018. During the summer of 2018, prior to the release of the captive raised juveniles, wild snakes were captured by hand throughout southern and central NH from the same populations that the original females had been captured. These snakes had all of their measurements taken in the field, using the same caliper and string method mentioned above. Wild snakes were marked with a red Sharpie marker behind the head to identify them as having been measured previously. Snakes were then immediately released after measurements taken and they had been marked. Fig. 1 Open in new tabDownload slide Illustration of the head measurements from a lateral view of the head (A) and a dorsal view of the head (B). All measurements were taken with digital calipers for all individuals. Fig. 1 Open in new tabDownload slide Illustration of the head measurements from a lateral view of the head (A) and a dorsal view of the head (B). All measurements were taken with digital calipers for all individuals. Measurement data were imported into R Studio (RStudio Team 2015) for analysis in R (R Core Team 2017), with figures generated using the package ggplot2 (Wickham 2009). The raw data were first analyzed using a principal components analysis using the “prcomp” function in R. The number of principal components retained followed the Broken Stick method (Jackson 1993; Vincent et al. 2004a, 2004b) using the R package PCDimension (Wang et al. 2019). Retained principal components were subsequently analyzed in a multivariate analysis of covariance (MANCOVA) linked to univariate F-tests with the principal components as the outcome variables, the treatment (wild, earthworm, fish, both) as the predictor, and SVL as the covariate. Within significant principal components, variables with a loading greater than 0.4 (Stevens 1992) were considered substantial. Variables with a substantial loading from the principal component analysis (PCA) were included in an analysis of the allometry of head size in the captive population. First, I used a MANCOVA to test for differences in SVL, head length, and head width at day 0, with treatment as the predictor and clutch as a covariate. This MANCOVA was to account for any starting differences in my groups prior to the onset of the experiment. I used a series of generalized mixed effects models to test for differences in head size allometry using the R package lme4 (Bates et al. 2015). Each model used one of the parameters of head morphology as the dependent variable with SVL, body mass, diet treatment, clutch, time (in months), and food consumed as fixed effects and individual snake as a random effect to account for repeated measures. My mixed effects models also included interactions between diet treatment with SVL and food consumed. Initial model selection for morphology was done using a stepwise AIC procedure, with the optimal model being the simplest model within two units of the model with the lowest AIC score (Burnham and Anderson 2002). Slopes and confidence intervals were extracted from the optimal model using the “emmeans” package. Likelihood ratio tests of the optimal model compared with individual effects removed were used to determine P-values for those individual effects (Stevens et al. 2018; Ryerson 2020). Effect sizes for all of the tested mixed effects models were calculated following published methods (Stevens et al. 2018; Ryerson 2020). Briefly, the effect size is the proportional decrease in the residual variance with the variable in question compared with the null, random effects only, model as a metric of explained variance (Xu 2003). In models where diet treatment was part of the optimal model, multiple comparisons were conducted using two-sided Tukey’s contrasts with the “glht” function in the R package “multcomp” (Hothorn et al. 2008). P-value criteria for significance in all tests were adjusted to account for the multiple tests using a sequential Bonferroni correction in the R package “stats” (Holm 1979). Results Seventy-six neonatal T. sirtalis were born in the laboratory from three gravid females in August 2017. The females were released to the site of capture 1 week after the litters were born. Eight of the neonates (three from the first clutch, four from the second, and one from the third) never fed in captivity, and are not included in any further analysis, resulting in a total sample size of 68 individuals. Before the neonates had their first shed, they were randomly assigned to one of three diet treatments (number of individuals in each): fish (21), earthworm (23), or both (24). In the months of June–August 2018, I captured 86 wild T. sirtalis by hand and measured them at the site of capture. After the measurements and being marked to prevent recapture, the wild individuals were immediately released. After the collection of data from the wild population, I released the captive headstarted individuals at the site of capture of their mothers. This was to prevent potential recaptures from skewing the wild snake data. Initial PCA results yielded four axes which, when combined, explained >99.2% of the variation observed in my data (Fig. 2 and Table 1). The results of the MANCOVA found a significant difference between treatments (Wilk’s lambda<0.001, F3,154=26.28, P < 0.001) but the subsequent univariate F tests revealed only three of the four PC axes were significant following correction for multiple tests (PC 1: F3,154=767.31, P < 0.001; PC 2: F3,154=18.357, P < 0.001; PC 3: F3,154=88.042, P < 0.001). From these three axes, substantial loadings were found in six of the morphological variables (Table 2). The loadings reveal that PC 1 and 2 were indicators of length, while PC 3 was an indicator of head width. Fig. 2 Open in new tabDownload slide Results of the PCA for the wild snakes and those in the three diet treatments. PC 1 is a measure of head length and PC 3 is a measure of head width. Fig. 2 Open in new tabDownload slide Results of the PCA for the wild snakes and those in the three diet treatments. PC 1 is a measure of head length and PC 3 is a measure of head width. Table 1 Results from the PCA on head shape and diet treatment Output . PC 1 . PC 2 . PC 3 . PC 4 . PC 5 . PC 6 . PC 7 . PC 8 . PC 9 . PC 10 . Standard deviation 3.3763 0.7854 0.46503 0.17837 0.15354 0.14455 0.13076 0.12858 0.10405 0.09738 Proportion of variance 0.9221 0.0499 0.01749 0.00257 0.00191 0.00169 0.00138 0.00134 0.00088 0.00077 Cumulative proportion 0.9221 0.972 0.98947 0.99204 0.99395 0.99564 0.99702 0.99836 0.99923 1 Output . PC 1 . PC 2 . PC 3 . PC 4 . PC 5 . PC 6 . PC 7 . PC 8 . PC 9 . PC 10 . Standard deviation 3.3763 0.7854 0.46503 0.17837 0.15354 0.14455 0.13076 0.12858 0.10405 0.09738 Proportion of variance 0.9221 0.0499 0.01749 0.00257 0.00191 0.00169 0.00138 0.00134 0.00088 0.00077 Cumulative proportion 0.9221 0.972 0.98947 0.99204 0.99395 0.99564 0.99702 0.99836 0.99923 1 Open in new tab Table 1 Results from the PCA on head shape and diet treatment Output . PC 1 . PC 2 . PC 3 . PC 4 . PC 5 . PC 6 . PC 7 . PC 8 . PC 9 . PC 10 . Standard deviation 3.3763 0.7854 0.46503 0.17837 0.15354 0.14455 0.13076 0.12858 0.10405 0.09738 Proportion of variance 0.9221 0.0499 0.01749 0.00257 0.00191 0.00169 0.00138 0.00134 0.00088 0.00077 Cumulative proportion 0.9221 0.972 0.98947 0.99204 0.99395 0.99564 0.99702 0.99836 0.99923 1 Output . PC 1 . PC 2 . PC 3 . PC 4 . PC 5 . PC 6 . PC 7 . PC 8 . PC 9 . PC 10 . Standard deviation 3.3763 0.7854 0.46503 0.17837 0.15354 0.14455 0.13076 0.12858 0.10405 0.09738 Proportion of variance 0.9221 0.0499 0.01749 0.00257 0.00191 0.00169 0.00138 0.00134 0.00088 0.00077 Cumulative proportion 0.9221 0.972 0.98947 0.99204 0.99395 0.99564 0.99702 0.99836 0.99923 1 Open in new tab Table 2 Loadings from the significant PC axes Variable . PC 1 . PC 2 . PC 3 . Head length −0.754 −0.619 −0.213 Jaw length −0.643 0.761 0.061 Height at nares −0.019 −0.049 0.1 Height at eye −0.028 −0.022 0.088 Height at jaw joint 0.029 0.003 −0.078 Height at postorbital scale −0.017 −0.006 0.033 Width at nares −0.067 −0.07 0.454 Width at eye −0.048 −0.069 0.444 Width at braincase −0.055 −0.138 0.569 Width at neck −0.07 −0.067 0.446 Variable . PC 1 . PC 2 . PC 3 . Head length −0.754 −0.619 −0.213 Jaw length −0.643 0.761 0.061 Height at nares −0.019 −0.049 0.1 Height at eye −0.028 −0.022 0.088 Height at jaw joint 0.029 0.003 −0.078 Height at postorbital scale −0.017 −0.006 0.033 Width at nares −0.067 −0.07 0.454 Width at eye −0.048 −0.069 0.444 Width at braincase −0.055 −0.138 0.569 Width at neck −0.07 −0.067 0.446 Substantial loadings are indicated by bold font. Open in new tab Table 2 Loadings from the significant PC axes Variable . PC 1 . PC 2 . PC 3 . Head length −0.754 −0.619 −0.213 Jaw length −0.643 0.761 0.061 Height at nares −0.019 −0.049 0.1 Height at eye −0.028 −0.022 0.088 Height at jaw joint 0.029 0.003 −0.078 Height at postorbital scale −0.017 −0.006 0.033 Width at nares −0.067 −0.07 0.454 Width at eye −0.048 −0.069 0.444 Width at braincase −0.055 −0.138 0.569 Width at neck −0.07 −0.067 0.446 Variable . PC 1 . PC 2 . PC 3 . Head length −0.754 −0.619 −0.213 Jaw length −0.643 0.761 0.061 Height at nares −0.019 −0.049 0.1 Height at eye −0.028 −0.022 0.088 Height at jaw joint 0.029 0.003 −0.078 Height at postorbital scale −0.017 −0.006 0.033 Width at nares −0.067 −0.07 0.454 Width at eye −0.048 −0.069 0.444 Width at braincase −0.055 −0.138 0.569 Width at neck −0.07 −0.067 0.446 Substantial loadings are indicated by bold font. Open in new tab Wild snakes have larger heads, both in length and width than any of the captive treatments from the MANOVA results (Table 3). Snakes in the earthworm treatment had the shortest heads of any treatment, but equal in width to the both treatment. Snakes in the fish treatment had the narrowest heads of any treatment, but equal in length to the both treatment. The results from the day 0 MANCOVA found no differences in any of the measurement variables as predicted by treatment or clutch, so any differences at the end of the experiment are due to differences in growth patterns. Table 3 Head measurements from the diet treatments and the wild T. sirtalis sampled . . . Captive diet treatment . Morphological variable . Wild . Both . Fish . Earthworm . Head length 14.23±0.02a 10.23±1.26b 11.23±1.26b 8.23±1.31c Jaw length 12.91±0.09a 9.91±0.27b 10.91±0.25b 6.91±0.19c Width—nares 2.74±0.12a 2.25±0.21b 2.04±0.2b 2.24±0.19b Width—eyes 4.63±0.1a 4.23±0.19b 3.93±0.21c 4.23±0.16b Width—braincase 6.63±0.08a 6.23±0.19b 5.73±0.21c 6.23±0.2b Width—neck 5.97±0.09a 5.47±0.17b 5.07±0.17c 5.49±0.12b . . . Captive diet treatment . Morphological variable . Wild . Both . Fish . Earthworm . Head length 14.23±0.02a 10.23±1.26b 11.23±1.26b 8.23±1.31c Jaw length 12.91±0.09a 9.91±0.27b 10.91±0.25b 6.91±0.19c Width—nares 2.74±0.12a 2.25±0.21b 2.04±0.2b 2.24±0.19b Width—eyes 4.63±0.1a 4.23±0.19b 3.93±0.21c 4.23±0.16b Width—braincase 6.63±0.08a 6.23±0.19b 5.73±0.21c 6.23±0.2b Width—neck 5.97±0.09a 5.47±0.17b 5.07±0.17c 5.49±0.12b All measurements are in millimeters (mm). Significantly different groupings from the MANOVAs are indicated by the superscript letters. Open in new tab Table 3 Head measurements from the diet treatments and the wild T. sirtalis sampled . . . Captive diet treatment . Morphological variable . Wild . Both . Fish . Earthworm . Head length 14.23±0.02a 10.23±1.26b 11.23±1.26b 8.23±1.31c Jaw length 12.91±0.09a 9.91±0.27b 10.91±0.25b 6.91±0.19c Width—nares 2.74±0.12a 2.25±0.21b 2.04±0.2b 2.24±0.19b Width—eyes 4.63±0.1a 4.23±0.19b 3.93±0.21c 4.23±0.16b Width—braincase 6.63±0.08a 6.23±0.19b 5.73±0.21c 6.23±0.2b Width—neck 5.97±0.09a 5.47±0.17b 5.07±0.17c 5.49±0.12b . . . Captive diet treatment . Morphological variable . Wild . Both . Fish . Earthworm . Head length 14.23±0.02a 10.23±1.26b 11.23±1.26b 8.23±1.31c Jaw length 12.91±0.09a 9.91±0.27b 10.91±0.25b 6.91±0.19c Width—nares 2.74±0.12a 2.25±0.21b 2.04±0.2b 2.24±0.19b Width—eyes 4.63±0.1a 4.23±0.19b 3.93±0.21c 4.23±0.16b Width—braincase 6.63±0.08a 6.23±0.19b 5.73±0.21c 6.23±0.2b Width—neck 5.97±0.09a 5.47±0.17b 5.07±0.17c 5.49±0.12b All measurements are in millimeters (mm). Significantly different groupings from the MANOVAs are indicated by the superscript letters. Open in new tab Model selection for the allometric analysis of head size in the captive snakes resulted in an optimal model including time, SVL, and treatment as predictors for every parameter of head size (Table 4). There is a significant interaction between time and treatment for head length, jaw length, width at the nares, and width at the braincase. The Tukey’s two-way multiple comparisons test revealed differences in diet treatment for every measurement of head size (Table 5). The earthworm treatment differed in allometry from the other treatments in measures of head length, while in measures of width the fish treatment differed. Slope estimates from the mixed effects model show that while all individuals may have started from the same point, individuals in the earthworm treatment showed slower growth in metrics of head length while the fish treatment showed slower growth in metrics of head width (Fig. 3). Fig. 3 Open in new tabDownload slide Slope estimates from the mixed effects model on the patterns of allometry in the three diet treatments. Error bars represent standard error for each slope estimate. Fig. 3 Open in new tabDownload slide Slope estimates from the mixed effects model on the patterns of allometry in the three diet treatments. Error bars represent standard error for each slope estimate. Table 4 Model output from each optimal model as selected by AIC Dependent variable . Predictor . Estimate . Standard error . t-Value . Ω2 . P-value . Head length Time 0.734 0.055 3.105 0.46 0.002 SVL 0.502 0.038 2.9812 0.45 0.003 Treatment 0.692 0.032 3.619 0.72 <0.001 Time * Treatment 0.411 0.082 2.6619 0.29 0.008 Jaw length Time 0.721 0.021 2.8905 0.33 0.004 SVL 0.773 0.075 2.8186 0.45 0.005 Treatment 0.674 0.039 3.782 0.58 <0.001 Time * Treatment 0.581 0.043 2.7587 0.3 0.006 Width—nares Time 0.613 0.078 2.5515 0.48 0.011 SVL 0.519 0.051 2.7072 0.35 0.007 Treatment 0.812 0.029 3.3086 0.44 0.001 Time * Treatment 0.434 0.07 2.5206 0.31 0.012 Width—eyes Time 0.636 0.069 2.8905 0.47 0.004 SVL 0.821 0.049 2.8905 0.47 0.004 Treatment 0.858 0.039 3.3086 0.64 0.001 Width—braincase Time 0.584 0.072 2.8905 0.51 0.004 SVL 0.723 0.04 2.8186 0.49 0.005 Treatment 0.897 0.057 3.911 0.6 <0.001 Time * Treatment 0.44 0.068 2.5849 0.27 0.01 Width—neck Time 0.473 0.058 2.6619 0.26 0.008 SVL 0.663 0.044 2.7587 0.32 0.006 Treatment 0.847 0.052 2.9812 0.44 0.003 Dependent variable . Predictor . Estimate . Standard error . t-Value . Ω2 . P-value . Head length Time 0.734 0.055 3.105 0.46 0.002 SVL 0.502 0.038 2.9812 0.45 0.003 Treatment 0.692 0.032 3.619 0.72 <0.001 Time * Treatment 0.411 0.082 2.6619 0.29 0.008 Jaw length Time 0.721 0.021 2.8905 0.33 0.004 SVL 0.773 0.075 2.8186 0.45 0.005 Treatment 0.674 0.039 3.782 0.58 <0.001 Time * Treatment 0.581 0.043 2.7587 0.3 0.006 Width—nares Time 0.613 0.078 2.5515 0.48 0.011 SVL 0.519 0.051 2.7072 0.35 0.007 Treatment 0.812 0.029 3.3086 0.44 0.001 Time * Treatment 0.434 0.07 2.5206 0.31 0.012 Width—eyes Time 0.636 0.069 2.8905 0.47 0.004 SVL 0.821 0.049 2.8905 0.47 0.004 Treatment 0.858 0.039 3.3086 0.64 0.001 Width—braincase Time 0.584 0.072 2.8905 0.51 0.004 SVL 0.723 0.04 2.8186 0.49 0.005 Treatment 0.897 0.057 3.911 0.6 <0.001 Time * Treatment 0.44 0.068 2.5849 0.27 0.01 Width—neck Time 0.473 0.058 2.6619 0.26 0.008 SVL 0.663 0.044 2.7587 0.32 0.006 Treatment 0.847 0.052 2.9812 0.44 0.003 Open in new tab Table 4 Model output from each optimal model as selected by AIC Dependent variable . Predictor . Estimate . Standard error . t-Value . Ω2 . P-value . Head length Time 0.734 0.055 3.105 0.46 0.002 SVL 0.502 0.038 2.9812 0.45 0.003 Treatment 0.692 0.032 3.619 0.72 <0.001 Time * Treatment 0.411 0.082 2.6619 0.29 0.008 Jaw length Time 0.721 0.021 2.8905 0.33 0.004 SVL 0.773 0.075 2.8186 0.45 0.005 Treatment 0.674 0.039 3.782 0.58 <0.001 Time * Treatment 0.581 0.043 2.7587 0.3 0.006 Width—nares Time 0.613 0.078 2.5515 0.48 0.011 SVL 0.519 0.051 2.7072 0.35 0.007 Treatment 0.812 0.029 3.3086 0.44 0.001 Time * Treatment 0.434 0.07 2.5206 0.31 0.012 Width—eyes Time 0.636 0.069 2.8905 0.47 0.004 SVL 0.821 0.049 2.8905 0.47 0.004 Treatment 0.858 0.039 3.3086 0.64 0.001 Width—braincase Time 0.584 0.072 2.8905 0.51 0.004 SVL 0.723 0.04 2.8186 0.49 0.005 Treatment 0.897 0.057 3.911 0.6 <0.001 Time * Treatment 0.44 0.068 2.5849 0.27 0.01 Width—neck Time 0.473 0.058 2.6619 0.26 0.008 SVL 0.663 0.044 2.7587 0.32 0.006 Treatment 0.847 0.052 2.9812 0.44 0.003 Dependent variable . Predictor . Estimate . Standard error . t-Value . Ω2 . P-value . Head length Time 0.734 0.055 3.105 0.46 0.002 SVL 0.502 0.038 2.9812 0.45 0.003 Treatment 0.692 0.032 3.619 0.72 <0.001 Time * Treatment 0.411 0.082 2.6619 0.29 0.008 Jaw length Time 0.721 0.021 2.8905 0.33 0.004 SVL 0.773 0.075 2.8186 0.45 0.005 Treatment 0.674 0.039 3.782 0.58 <0.001 Time * Treatment 0.581 0.043 2.7587 0.3 0.006 Width—nares Time 0.613 0.078 2.5515 0.48 0.011 SVL 0.519 0.051 2.7072 0.35 0.007 Treatment 0.812 0.029 3.3086 0.44 0.001 Time * Treatment 0.434 0.07 2.5206 0.31 0.012 Width—eyes Time 0.636 0.069 2.8905 0.47 0.004 SVL 0.821 0.049 2.8905 0.47 0.004 Treatment 0.858 0.039 3.3086 0.64 0.001 Width—braincase Time 0.584 0.072 2.8905 0.51 0.004 SVL 0.723 0.04 2.8186 0.49 0.005 Treatment 0.897 0.057 3.911 0.6 <0.001 Time * Treatment 0.44 0.068 2.5849 0.27 0.01 Width—neck Time 0.473 0.058 2.6619 0.26 0.008 SVL 0.663 0.044 2.7587 0.32 0.006 Treatment 0.847 0.052 2.9812 0.44 0.003 Open in new tab Table 5 Results from the two-way Tukey’s multiple comparisons test Response variable . Comparison . Estimate . z-value . P-value . Head length B–E 2.564 3.09 0.001 B–F 1.311 1.751 0.04 E–F −2.914 3.187 <0.001 Jaw length B–E 2.251 2.753 0.003 B–F 0.874 1.036 0.15 E–F −2.318 2.879 0.002 Width—nares B–E 0.344 0.524 0.3 B–F 2.182 2.547 0.006 E–F 2.205 2.611 0.005 Width—eyes B–E 0.318 1.838 0.33 B–F 2.202 2.663 0.004 E–F 2.246 2.748 0.003 Width—braincase B–E 1.613 1.927 0.027 B–F 2.612 3.092 0.001 E–F 3.036 3.331 <0.001 Width—neck B–E 1.282 1.706 0.044 B–F 2.208 2.579 0.005 E–F 2.299 2.762 0.003 Response variable . Comparison . Estimate . z-value . P-value . Head length B–E 2.564 3.09 0.001 B–F 1.311 1.751 0.04 E–F −2.914 3.187 <0.001 Jaw length B–E 2.251 2.753 0.003 B–F 0.874 1.036 0.15 E–F −2.318 2.879 0.002 Width—nares B–E 0.344 0.524 0.3 B–F 2.182 2.547 0.006 E–F 2.205 2.611 0.005 Width—eyes B–E 0.318 1.838 0.33 B–F 2.202 2.663 0.004 E–F 2.246 2.748 0.003 Width—braincase B–E 1.613 1.927 0.027 B–F 2.612 3.092 0.001 E–F 3.036 3.331 <0.001 Width—neck B–E 1.282 1.706 0.044 B–F 2.208 2.579 0.005 E–F 2.299 2.762 0.003 E, earthworm treatment; F, fish, and B, both. Hypothesized difference for all comparisons is 0. Bolded values indicate significant differences after correcting for multiple tests. Open in new tab Table 5 Results from the two-way Tukey’s multiple comparisons test Response variable . Comparison . Estimate . z-value . P-value . Head length B–E 2.564 3.09 0.001 B–F 1.311 1.751 0.04 E–F −2.914 3.187 <0.001 Jaw length B–E 2.251 2.753 0.003 B–F 0.874 1.036 0.15 E–F −2.318 2.879 0.002 Width—nares B–E 0.344 0.524 0.3 B–F 2.182 2.547 0.006 E–F 2.205 2.611 0.005 Width—eyes B–E 0.318 1.838 0.33 B–F 2.202 2.663 0.004 E–F 2.246 2.748 0.003 Width—braincase B–E 1.613 1.927 0.027 B–F 2.612 3.092 0.001 E–F 3.036 3.331 <0.001 Width—neck B–E 1.282 1.706 0.044 B–F 2.208 2.579 0.005 E–F 2.299 2.762 0.003 Response variable . Comparison . Estimate . z-value . P-value . Head length B–E 2.564 3.09 0.001 B–F 1.311 1.751 0.04 E–F −2.914 3.187 <0.001 Jaw length B–E 2.251 2.753 0.003 B–F 0.874 1.036 0.15 E–F −2.318 2.879 0.002 Width—nares B–E 0.344 0.524 0.3 B–F 2.182 2.547 0.006 E–F 2.205 2.611 0.005 Width—eyes B–E 0.318 1.838 0.33 B–F 2.202 2.663 0.004 E–F 2.246 2.748 0.003 Width—braincase B–E 1.613 1.927 0.027 B–F 2.612 3.092 0.001 E–F 3.036 3.331 <0.001 Width—neck B–E 1.282 1.706 0.044 B–F 2.208 2.579 0.005 E–F 2.299 2.762 0.003 E, earthworm treatment; F, fish, and B, both. Hypothesized difference for all comparisons is 0. Bolded values indicate significant differences after correcting for multiple tests. Open in new tab Discussion Here I document changes in head size and allometry as a result of rearing captive diet in the garter snake, T. sirtalis. Through their first year of life, I found effects of both diet as well as the captive environment resulting in differences in head size. Using diet recommendations following captive care instructions (Bartlett and Bartlett 2001; Perlowin 2005), I found that diet in captivity had a significant effect on the head size of juvenile garter snakes. When individuals were fed a diet of strictly small minnows, a strikingly narrow head resulted, without significant changes to the length of the head in comparison to the individuals in the both treatment. Similarly, individuals that were fed a diet of earthworm pieces resulted in a head size different than those in the fish treatment. On the earthworm diet, head width did not differ from the both treatment but the head was significantly shorter than those in the both and fish treatment. While differences in head morphology have been noted in different populations (Krause et al. 2003), it is unclear how these differences arose. Tests on the temperature effects on the head size of T. sirtalis found no changes in either size or allometry in different temperature regimes (Arnold and Peterson 1989), in contrast to the effects of diet observed in my data, suggesting that head size may only respond to certain environmental conditions. The underlying cause of the changes from diet is likely the result of functional demands on the swallowing of individual food items. Feeder fish, particularly the small minnows common in pet stores, are long-bodied, narrow in shape. The earthworm diet had pieces of earthworm that were shorter in length than the fish treatment, but each individual piece was wider. Individuals in the both treatment faced with a diet of varying shape, most closely matched the patterns observed in the wild population. It is likely that the different functional demands of swallowing the different food types induced phenotypic changes in the head skeleton, either plastically or permanently. Experimental manipulation of diet has previously been shown to induce changes in head and body morphology in snakes. In the gaboon viper, Bitis gabonica, individuals in a high-food treatment (as a measure of total prey mass) grew substantially larger than the individuals with a lower total prey mass, not only in metrics of whole body size, but also in key elements of the feeding apparatus, including jaw length, head width, and fang length (Bonnet et al. 2001) while another viper, Crotalus viridis, saw changes in head length and width when fed large mice compared with a force-fed prepared diet (Smith 2014). Nerodia, mentioned above, have also been found to show plasticity in terms of both body size and dimensions of head shape when fed fish of differing size and shape (Queral-Regil and King 1998). Individuals fed larger fish had larger heads in terms of length and width, but it was unclear how much of the difference in the morphology was in response to individual prey size versus total prey mass. Similar patterns were also observed in the tiger snake, Notechis scutatus, raised in captivity from two distinct populations, an island and mainland population (Aubret et al. 2004). The island population, a recent arrival to that location, exhibited stronger effects of diet manipulation than the mainland population. This suggests that while there are significant impacts of the environment on the morphology, there are also genetic underpinnings which may enhance or inhibit these environmental effects. These findings of phenotypic plasticity, both in this study and the ones just mention contradict the work on several other species, including Vipera berus (Forsman 1996) and the Boa constrictor (Schuett et al. 2005). The variation in responses to diet manipulation suggests that life history, ecological (sexual size dimorphism, mating, etc.), and genetic factors will contribute to the possibility of induced changes in head morphology. In this experiment, each diet treatment resulted in different linear aspects of head size, but none of the treatments were similar in size to the wild snakes that were sampled. For individuals of the same size, wild snakes had larger heads than their captive counterparts, but were similar in size to the both treatment. Unlike the aforementioned work on diet manipulation and head size in snakes, this is the first work to directly compare the diet treatments of individuals in captivity to individuals from the same wild population. There are clear differences between the wild Thamnophis sampled in this study and the captive-raised individuals, and it remains unclear what the underlying differences may be. There are, however, several hypotheses that may shed light on the mechanism of the observed changes. The first is that while manipulations of diet in captivity result in changes to head size, I was still unable to properly alter the diet to reflect the true diversity of prey sizes and shapes that are consumed in the wild, having instead been unable to induce the same changes in head size that would occur in the wild (Smith 2014). The second hypothesis is that my manipulation of diet had a minimal impact on the morphology of the head in snakes, but that changes to the other aspects of morphology (e.g., size and condition) are washing out changes in head morphology, and that my comparisons between the captive and wild individuals are skewed by changes in body morphology that both populations undergo in their first year of growth and that these changes may perpetuate through adulthood (Madsen and Shine 2000). There exists the possibility that in the wild snakes grow more slowly in terms of SVL and body mass, and the plasticity that results from captivity is more strongly represented by those metrics, while the head size is significantly less plastic. The faster growing body size would result in the appearance of a head size and shape that is retaining juvenile characteristics. The effects of changes in head size as a result of a diet in captivity are long-reaching. Snakes are classically considered “gape-limited” predators, in which the maximum size of ingestible prey is determined by maximum gape size (Madsen and Shine 2000; Vincent et al. 2006; Elgee and Blouin-Demers 2011). While snakes have evolved several different pathways for the capture and subjugation of prey (venom and constriction), in almost all species prey are swallowed whole with minimal processing. The obvious implication of a smaller head size in snakes is a potential constraint on the food resources available to the individual. Snakes with relatively small heads for their body size would not be able to consume larger prey. The smaller relative head size would also suggest that snakes would have to catch and consume prey more frequently, to provide the appropriate caloric and nutritional needs from a smaller prey base (Elgee and Blouin-Demers 2011). Lost feeding opportunities would be even more detrimental to the individual, and may increase the likelihood of starvation for individuals that had been bred in captivity and released into the wild. When assessing the likelihood of success for a headstarting or reintroduction, metrics including survival (both short- and long-term) and reproduction are the commonly used (Burke 2015). However, the difficulties of predicting survival suggest that we seek a broader understanding of captive rearing programs and the effects they have on individuals. In recent years, more and more studies suggest that there are a myriad of factors that may have a direct impact on an individual’s survival in the wild, including the time spent in captivity (Tetzlaff et al. 2019a), habitat enrichment (Tetzlaff et al. 2019b), and soft releases with supplemental feedings (Roe et al. 2015), beyond the usual metrics of body size and age. Accounting for species-specific behaviors is also paramount for improving the success of reintroduction programs. Snakes are well-known for the use of hibernacula to overwinter in temperate and colder climates (Greene 1997). Native populations of snakes will retreat to the same hibernacula repeatedly over the course of their lives, while snakes that have been translocated show considerable difficulty in locating these hibernacula (Reinert and Rupert 1999). Those unable to find the hibernacula succumb to winter conditions or become easy prey themselves (Reinert and Rupert 1999). In order to better predict and ultimately improve survival and reproduction in the wild, captive breeding and headstarting programs should include assessments of morphology, physiology, and performance (Jachowski et al. 2016). By including these newer metrics into headstarting and captive rearing protocols, it is possible to raise the numbers of individuals that succeed when released into the wild. Ultimately, increasing the likelihood of a reintroduction program succeeding is the goal, and incorporating more information into these programs should help their success. From the symposium “Applied Functional Biology: linking ecological morphology to conservation and management” presented at the annual meeting of the Society for Integrative and Comparative Biology January 3–7, 2020 at Austin, Texas. References Arnold SJ , Peterson CR. 1989 . 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TI - Captivity Affects Head Morphology and Allometry in Headstarted Garter Snakes, Thamnophis sirtalis
JO - Integrative and Comparative Biology
DO - 10.1093/icb/icaa020
DA - 2020-08-01
UR - https://www.deepdyve.com/lp/oxford-university-press/captivity-affects-head-morphology-and-allometry-in-headstarted-garter-Y0fRT6BiT2
SP - 476
EP - 486
VL - 60
IS - 2
DP - DeepDyve
ER -