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Getting a head in hard soils: Convergent skull evolution and divergent allometric patterns explain shape variation in a highly diverse genus of pocket gophers (Thomomys)
Background
High morphological diversity can occur in closely related animals when selection favors morphologies that are subject to intrinsic biological constraints. A good example is subterranean rodents of the genus
Thomomys
, one of the most taxonomically and morphologically diverse mammalian genera. Highly procumbent, tooth-digging rodent skull shapes are often geometric consequences of increased body size. Indeed, larger-bodied
Thomomys
species tend to inhabit harder soils. We used geometric morphometric analyses to investigate the interplay between soil hardness (the main extrinsic selection pressure on fossorial mammals) and allometry (i.e. shape change due to size change; generally considered the main intrinsic factor) on crania and humeri in this fast-evolving mammalian clade.
Results
Larger
Thomomys
species/subspecies tend to have more procumbent cranial shapes with some exceptions, including a small-bodied species inhabiting hard soils. Counter to earlier suggestions, cranial shape within
Thomomys
does not follow a genus-wide allometric pattern as even regional subpopulations differ in allometric slopes. In contrast, humeral shape varies less with body size and with soil hardness. Soft-soil taxa have larger humeral muscle attachment sites but retain an orthodont (non-procumbent) cranial morphology. In intermediate soils, two pairs of sister taxa diverge through differential modifications on either the humerus or the cranium. In the hardest soils, both humeral and cranial morphology are derived through large muscle attachment sites and a high degree of procumbency.
Conclusions
Our results show that conflict between morphological function and intrinsic allometric patterning can quickly and differentially alter the rodent skeleton, especially the skull. In addition, we found a new case of convergent evolution of incisor procumbency among large-, medium-, and small-sized species inhabiting hard soils. This occurs through different combinations of allometric and non-allometric changes, contributing to shape diversity within the genus. The strong influence of allometry on cranial shape appears to confirm suggestions that developmental change underlies mammalian cranial shape divergences, but this requires confirmation from ontogenetic studies. Our findings illustrate how a variety of intrinsic processes, resulting in species-level convergence, could sustain a genus-level range across a variety of extrinsic environments. This might represent a mechanism for observations of genus-level niche conservation despite species extinctions in mammals.
Journal Article
Gophers
Gophers rely on their sense of touch to find their way in dark tunnels. They use their whiskers to feel what is in front of them and their tails to feel what is behind them. These interesting facts and more can be found in Gophers, an Animals in My Backyard book.
Book
Fire Management Effects on Long-Term Gopher Tortoise Population Dynamics
Long-term datasets are required to understand the response of long-lived organisms (e.g., gopher tortoises [Gopherus polyphemus]) to management actions, such as prescribed burns. Our objective was to estimate the effects of prescribed burning on gopher tortoise population dynamics over decadal time frames at Fort Stewart Army Reserve, southeastern Georgia, USA. We captured and marked adult tortoises from 1994–2020. In addition, since the early 1990s, managers at Fort Stewart collected spatial records of prescribed burns; thus, we could compare demography of the population to prescribed burning. We used a Bayesian hierarchical model (open population Jolly-Seber model) to estimate population parameters (emigration and survival, immigration and recruitment, and adult abundance) and their relationships with years since burn. We observed opposing responses to years since burn at 2 sites: abundance and the probability of staying (survival plus not emigrating) increased within 1 site when it had been more recently burned (F zones), but abundance and probability of staying in a second site increased when it had been longer since the site was burned (E zones). Some of these effects were weak but indicative of different responses to burning between the sites. Although the sites experienced similar burning regimes, they differed substantially in other habitat features: the F zones had almost twice the tree cover and lower soil sand composition, indicating that tortoise population responses to burning depend on habitat context. We inferred that the primary mechanism for demographic responses to years since burn was likely emigrating adults, which indicates the need for more detailed movement data. Our results demonstrate that gopher tortoise population responses to prescribed burning are complex, context dependent, and primarily influenced by tortoise movements. Therefore, prescribed burn plans may best accommodate spatially dynamic tortoise populations when they create spatial heterogeneity in burn ages within the range of typical tortoise movements.
Journal Article
Waif Gopher Tortoise Survival and Site Fidelity Following Translocation
Gopher tortoises (Gopherus polyphemus) are among the most commonly translocated reptiles. Waif tortoises are animals frequently of unknown origin that have been displaced from the wild and often held in human possession for various reasons and durations. Although there are risks associated with any translocation, waif tortoises are generally excluded from translocation projects because of heightened concerns of introducing pathogens and uncertainty about the post-release survival of these individuals. If these risks could be managed, waif tortoises could have conservation value because they can provide the needed numbers to stabilize populations. In the early 1990s, the discovery of an isolated population of gopher tortoises (≤15 individuals) near Aiken, South Carolina, USA, prioritized establishment of the Aiken Gopher Tortoise Heritage Preserve (AGTHP). Because of the population’s need for augmentation and the site’s isolation from other tortoise populations, the AGTHP provided the opportunity to evaluate the post-release survival of translocated waif tortoises without compromising a viable population. Since 2006, >260 waif tortoises have been introduced to the preserve. Using a Cormack-Jolly-Seber modeling framework to analyze release records and capture histories from trapping efforts in 2017 and 2018, we estimated the long-term apparent survival and site fidelity of this population composed largely of waif tortoises. We estimated annual apparent survival probabilities to be high (≥0.90) for subadult, adult male, and adult female tortoises, and these rates were similar to those reported for wild-to-wild translocated gopher tortoises and those from unmanipulated populations. Of the tortoises recaptured within the boundaries of the preserve, 75% were located within 400m of their release location. These results suggest that waif tortoises could be an important resource in reducing the extirpation risk of isolated populations.
Journal Article
Survival of Immature Gopher Tortoises Recruited into a Translocated Population
Population manipulations such as translocation and head-starting are increasingly used as recovery tools for chelonians. But evaluating success of individual projects can require decades of monitoring to detect population trends in these long-lived species. Furthermore, there are often few benchmarks from stable, unmanipulated populations against which to compare demographic rates, particularly for the immature stages. We used 8 years of mark-recapture data to estimate apparent survival of immature gopher tortoises (Gopherus polyphemus) recruited into an introduced population of gopher tortoises first established on St. Catherines Island, Georgia, USA, in 1987. During 2006–2013, we conducted targeted trapping of immature gopher tortoises and compared survival of the hatchling, juvenile and subadult stages among treatments: individuals released shortly after hatching from eggs obtained from gravid female founders (direct releases), individuals reared in captivity for 6–9 months following hatching (head-starts), and individuals first encountered as free-ranging, wild-recruited offspring (wild recruits). Among the candidate models we examined, the best fit model included additive effects of tortoise stage and treatment; however, overlapping 95% credible intervals among treatments (CrI) suggested that survival did not vary significantly among treatments. Annual apparent survival increased over the immature period, highlighting the importance of calculating separate estimates for the different immature stages. Across all treatments, the additive model estimated annual apparent survival probability to be 0.37 (CrI=0.25–0.48) for hatchlings, 0.71 (CrI=0.61–0.81) for juveniles, and 0.83 (CrI=0.74–0.94) for subadults. Our study, in combination with previous monitoring efforts at St. Catherines Island, provides strong evidence that the translocation and subsequent population augmentation efforts have been successful in establishing a robust population of gopher tortoises. Additionally, our results provide estimates of demographic rates for life stages that are poorly understood but critical to understanding population dynamics of this imperiled species.
Journal Article
Accounting for spatial heterogeneity in visual obstruction in line-transect distance sampling of gopher tortoises
Line-transect distance sampling (LTDS) surveys are commonly used to estimate abundance of animals or objects. In terrestrial LTDS surveys of gopher tortoise (Gopherus polyphemus) burrows, the presence of ground-level vegetation substantially decreases detection of burrows of all sizes, but no field or analytical methods exist to control for spatially heterogeneous vegetation obstruction as a source of variation in detection. We propose the addition of a simple measurement of groundlevel vegetation that serves as a covariate for the detection function. We present a Bayesian hierarchical model in which covariates burrow width and nearby vegetation height help to account for detection bias and improve precision of estimated density. We investigate the performance of this covariate by simulation and by using real LTDS data collected before and after application of prescribed fire. We collected data in 2018 at the Jones Center at Ichauway in Newton, Georgia, USA. Across all simulations, our model including both covariates produced the most accurate density point estimates of any of the models tested. For our case study, our Bayesian model with vegetation covariates tended to produce similar estimates of density before and after burns. Our study indicates that any level of spatial variation in vegetation obstruction decreases detection of burrows and may lead to underestimation in population size (≤68%) and proportion of individuals with small burrow sizes (≤32%) when not considered during analysis. Our work is extensible to other terrestrial sampling efforts where systematic measurement of a spatially distributed obstructing feature is feasible during the LTDS survey.
Journal Article
Contrasting Patterns of Demography and Population Viability Among Gopher Tortoise Populations in Alabama
Population viability analyses are useful tools to predict abundance and extinction risk for imperiled species. In southeastern North America, the federally threatened gopher tortoise (Gopherus polyphemus) is a keystone species in the diverse and imperiled longleaf pine (Pinus palustris) ecosystem, and researchers have suggested that tortoise populations are declining and characterized by high extinction risk. We report results from a 30-year demographic study of gopher tortoises in southern Alabama (1991–2020), where 3 populations have been stable and 3 others have declined. To better understand the demographic vital rates associated with stable and declining tortoise populations, we used a multi-state hierarchical markrecapture model to estimate sex- and stage-specific patterns of demographic vital rates at each population. We then built a predictive population model to project population dynamics and evaluate extinction risk in a population viability context. Population structure did not change significantly in stable populations, but juveniles became less abundant in declining populations over 30 years. Apparent survival varied by age, sex, and site; adults had higher survival than juveniles, but female survival was substantially lower in declining populations than in stable ones. Using simulations, we predicted that stable populations with high female survival would persist over the next 100 years but sites with lower female survival would decline, become male-biased, and be at high risk of extirpation. Stable populations were most sensitive to changes in apparent survival of adult females. Because local populations varied greatly in vital rates, our analysis improves upon previous demographic models for northern populations of gopher tortoises by accounting for population-level variation in demographic patterns and, counter to previous model predictions, suggests that small tortoise populations can persist when habitat is managed effectively.
Journal Article
Post-Release Movement and Survivorship of Head-Started Gopher Tortoises
Gopher tortoise (Gopherus polyphemus) populations are declining throughout their range and recovery requires management intervention to alleviate losses. Population augmentation strategies may prove useful in recovery of depleted populations once threats are mitigated. We head-started and soft-released hatchlings produced from robust donor populations and evaluated their post-release survivorship and movement for the first year following their release. During 2014 and 2015, we head-started and released 145 tortoises, of which we radio-tracked a subset of 41 individuals, from 2 cohorts at 2 release areas within Yuchi Wildlife Management Area in Burke County, Georgia, USA. Movement and mortality of gopher tortoises was highest in the first month after release but declined soon after. Estimated annual survivorship of our first cohort was 60.6%. Annual survivorship of our second cohort was low (7.1%) at the southeast release area but much higher (75.0%) at the northwest release area because of spatial variation in predation. Although survivorship was variable, site fidelity remained high throughout the study and no tortoise moved >122.0 m from its release location. Initial results suggest that head-starting could prove effective as a population recovery tool, but that release strategy and predator mitigation, especially within the first month, are critical to success.
Journal Article
Genetic support for discrete conservation units of the fossorial rodent Geomys pinetis
Knowledge of the population genetic structure and diversity of at-risk species is essential to accurately evaluate population viability and define units for conservation and management. The southeastern pocket gopher (Geomys pinetis) is a fossorial rodent native to the imperiled longleaf pine savannas of the southeastern United States. Its recent decline has made it a species of ‘high conservation concern’ by state agencies. Previous phylogenetic analyses suggested two distinct lineages within the species occurring east (G. p. pinetis) and west (G. p. mobilensis) of the Apalachicola-Chattahoochee-Flint River (ACF) Basin, a phylogeographic break for many species. However, little is known about the genetic substructure within each region. We examined neutral and putatively adaptive variation in 9373 single nucleotide polymorphisms (SNPs) to assess the extent of genetic structure across the species' geographic range. We confirmed significant genetic divergence of populations east–west of the ACF Basin, predating the Last Glacial Maximum, supporting the presence of two evolutionary independent lineages. Our results indicate additional strong genetic substructuring within each lineage and possible non-neutral variation across latitudes. Given the high degree of genetic differentiation and lack of evidence for secondary contact among populations within the ACF Basin, we recommend that G. pinetis be managed as two conservation units corresponding to distinct lineages representing G. pinetis and G. mobiliensis.
Journal Article