The Impact of Dispersal Assessment Methods on the Resulting Management Interpretations of Endangered Species Stewardship
Date
2023-12
Authors
Sirsi, Shashwat
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Abstract
Taxonomic biases in conservation research were observed two decades ago, with an over-representation of bird and mammal studies relative to reptiles and amphibians. However, changing this bias has been slow and societal preferences, methodological limitations, and a relative lack of funding opportunities likely contribute to a continuing slow redress of the issue. Consequently, knowledge gaps limit management decisions for many taxonomic groups. At the same time, advances in telemetry and genetic approaches have begun to mitigate some of methodological limitations inherent for some groups (e.g., reptile and amphibian studies). For instance, improvements to global satellite networks, device miniaturization and new deployment methods have enabled an increased use of GPS enabled and satellite telemeters in determining fine scale and/or long-term movement data for smaller bodied reptiles. Similarly, an increased access to genetic markers, the advent of high throughput techniques, and new analytical approaches to analyze high throughput data have resulted in an increased application of genetic methods for taxa that are too small for animal-borne devices and with capture rates/heterogeneity that are intractable for direct field-based study methods. We sought to apply relatively recent, high-resolution direct (i.e., telemetry) and indirect (i.e., genetic) methods to address knowledge gaps in one freshwater reptile and one endemic amphibian species and therein provide context for their management. We used GPS enabled telemetry to estimate and identify proximate cues of movement in Rio Grande Cooters (Pseudemys gorzugi). Similarly, we used ~20,000 genome-wide markers to determine the evolutionary status and population genetic structure of Houston Toads (Bufo [=Anaxyrus] houstonensis). Based on findings from these studies, we conducted a meta-analytical comparison among direct and indirect approaches in amphibian, reptile, bird, and mammalian dispersal studies to determine the relative efficiency of each.
Rio Grande Cooters (Pseudemys gorzugi) occupy the Rio Grande watershed and have among the smallest distributions of all North American freshwater turtles. Anthropogenic dewatering is considered to have caused range contractions and population declines. Consequently, the species has been petitioned for listing as an endangered or threatened species under the United States Endangered Species Act. However, these riverine turtles are among the most poorly documented in all North American turtle species. Notable among prior studies, a range-wide assessment of genetic connectivity that supported panmictic population structure, indicating long-range movements between populations by individuals of this long-lived species. Long-range movements were at odds with site-level Capture-Mark-Recapture and radio telemetry data, which indicated extremely sedentary behavior (Pierce et al. 2016). We sought to address this discrepancy and facilitate management recommendations by determining the extent of movement and potential associations with extrinsic cues using high-resolution telemetry data. We conducted a GPS-enabled telemetry study from August 2015 to May 2017 on the Devils River in Texas, USA. We included CMR data from 2011, 2014, and 2015-2018 to estimate population size in conjunction with our movement ecology study. We obtained GPS telemetry data from 5 female and 3 male turtles, which is a small number of animals relative to ~30 freshwater turtles tagged in recent GPS and conventional VHF telemetry studies. However, by means of our tagged animals, we sampled the underlying distribution of movement distances more frequently and over a longer duration relative to previous studies, increasing the chance of observing dispersal distances that were longer. Positional fixes were realized at up to ~ 6 times the resolution and 1.1 to 4 times the duration observed in previous semi-aquatic and freshwater turtle GPS telemetry studies. Similarly, the number of relocations from our study were 1.1 to nearly 5 times greater than conventional VHF freshwater turtle telemetry studies. Maximum net displacement observed in our study was two orders of magnitude larger than previous estimates for the species. We attribute this to the higher sampling frequency and duration of our GPS telemetry data in comparison to the relatively sparse data used in previous estimates. We speculate that seasonality (i.e., day of year) and increases in streamflow facilitate switches from slower, localized movement to transiting/exploratory modes in tagged turtles. Individual heterogeneity was observed in the linear extent of transitory and exploratory movements and thus linear extent of home ranges. These transitory and exploratory movements led us to maintain our population estimate of 726 to 1219 individual P. gorzugi as representative of the entire Devils River. Additionally, the extent of long-range movements observed over the two-year telemetry study suggest that movements made over the lifetime (i.e., lifetime tracks) of this long-lived species could explain previously observed panmictic genetic structure. With an increase in sampling resolution for our direct, telemetry study, we found support for the dispersal implicit in previous genetic data and therein, the recommended range-wide scale for management efforts. Future efforts to reestablish natural flow regimes in the Rio Grande basin could potentially be the most effective approach in recovery efforts for this range-restricted chelonian.
Similarly, Houston Toads (Bufo [=Anaxyrus] houstonensis) are an appropriate amphibian analog, given their small geographic range and endangered status. Morphological similarity-based classification of North American toads placed B. houstonensis in the Bufo americanus (American Toad) species group along with ten other species. The Houston toad is endemic to Southeast-Central Texas, USA and in situ populations currently face a high risk of extinction. Land-use changes have predominantly driven decline in B. houstonensis with population supplementation efforts predominant among efforts to reduce its current extinction risk. Direct, field-based methods (i.e., Capture-Mark-Recapture and telemetry) have sought to determine spatial requirements for individuals (i.e., home ranges from radio telemetry) and population connectivity (i.e., multi-year CMR studies). However, small-body size and critically low abundance of Houston Toads have limited the ability of telemetry and CMR approaches to direct management approaches at the appropriate spatial scale for the species. Further, there has been historic uncertainty regarding the taxonomic status and age of B. houstonensis relative to B. americanus. Additionally, there are few genetic assessments to potentially inform population supplementation efforts. We generated thousands of genome-wide nuclear DNA markers from Houston Toads sampled over multiple years to provide insights into the evolutionary status and population genetic structure of Houston Toads. This range-wide assessment sought to provide an appropriate spatial scale for management efforts and thereby address a knowledge gap that persisted despite direct, field-based attempts. We examined phylogenetic relationships and divergence times among constituents of the B. americanus group and B. nebulifer, a sympatric Middle American species. An increased density of nuclear markers used in phylogenetic analyses supported a Late Cretaceous divergence between Nearctic and Middle American representatives that is substantially older than previous estimates of their divergence. Our results necessitate a subsequent re-examination of the origin of Family Bufonidae to potentially reassess global patterns of bufonid biogeography. Age estimates of our Nearctic toad taxa also support a plausible historical context (i.e., Pleistocene glaciation) for the secondary contact between historically proximal populations of American and Houston toads that was indicated in phylogenetic topologies. Genome scans detected a predominant signature of diversifying selection in protein coding genes which may be attributed to novel genetic variation introduced by erstwhile fragmentation and reexpansion in populations of representative toad taxa. Admixture analysis ascertained reproductive isolation between B. americanus and B. houstonensis while ABBA-BABA tests corroborated ancient gene flow, indicative of secondary contact, between the two taxa. Similarly, a minimum of three MUs (i.e., genomic clusters) were identified within B. houstonensis with a county-wide/regional spatial scale for population supplementation and protection/restoration of dispersal corridors. Additionally, observed genetic differentiation within B. houstonensis appeared consistent with the role of Pleistocene refugia in shaping contemporary genetic structure. Further, the increased resolution afforded by this genome-wide study enabled inference at a deeper timescale. We found support across analyses for the influence of historic processes on population connectivity and ancient gene flow between and within populations of Nearctic toad taxa. Our data also direct Houston Toad population supplementation and habitat restoration measures at broader spatial scales relative to previous studies. Our study strengthens the need and ability for B. houstonensis conservation while re-affirming the evolutionary novelty of an endangered relict.
It is well recognized that a clear understanding animal movement or dispersal is critical for the biodiversity conservation and management, particularly in the face of human-induced processes such as land-use and climate change. Knowledge gaps in animal dispersal and biased application of data types are among potential reasons for ineffective implementation of legislative measures for habitat protection. Underlying differences in the temporal scale, variability, and sample size attainable by dispersal study types and differences in the uptake of dispersal data types may lead to systematic errors in management implementation. We observed the greater efficiency of genetic data in providing an appropriate spatial scale for management relative to direct, field-based methods in both herpetofaunal case studies pursued in this dissertation. To assess whether such variation in efficiency among study types was inherent in existing dispersal literature and therein, the management implications of such potential patterns, we applied a metanalytical approach. A systematic metadata comparison was conducted between and among two traditional field (i.e., Capture-Mark-Recapture and telemetry) methods and genetic studies in amphibian, reptilian, avian, and mammalian taxa to assess the relative efficiency of each method in dispersal inference. We calculated dispersal scores for each study type based on magnitude, variability, and sample size associated with direct and indirect dispersal speeds. Indirect dispersal speeds were three to six orders of magnitude lower than direct dispersal speeds, but variability of indirect dispersal estimates was twofold to five orders of magnitude lower than variability of direct estimates while sample sizes from genetic studies were ≥ one order of magnitude larger than direct studies. As a result, dispersal scores for genetic studies were consistently ~1 order of magnitude greater than direct study types across representative orders. We suggest that large sample sizes and low variability, as above, of such dispersal estimates are tenable indicators of an increased probability of detecting long-distance dispersal and precision of dispersal estimates. Genetic methods potentially serve as a powerful alternative when measuring dispersal by direct methods is intractable at broad scales or when the morphology and underlying abundance of the study organism is not amenable to direct, field-based methods. Further, dispersal indices from genetic data can be complementary to direct dispersal information and when combined, can provide a relatively more holistic perspective on species dispersal (Comte and Olden 2018; Lowe and Allendorf 2010; Nathan et al. 2003). Given the limitations associated with indirect indices of genetic connectivity, we recommend the use of direct indices of genetic connectivity such as individual assignment tests for broad-scale habitat identification. We recognize the need for direct methods to elucidate demographic dependence, resource selection, and dispersal mechanisms in combination with genetic indices for efficient broad-scale management decisions. We emphasize the need to bridge gaps in the knowledge and application of genetic data type, particularly for rapid assessments of data deficient taxonomic groups with limited funding opportunities.
Description
Keywords
turtles, Devils River, Rio Grande Watershed, GPS telemetry, movements, home range, phylogenetics, ddRADseq, Bufo [=Anaxyrus] houstonensis, endangered, historic gene flow, biodiversity conservation, wildlife management, critical habitat designation, knowledge gap, genetic connectivity
Citation
Sirsi, S. (2023). The impact of dispersal assessment methods on the resulting management interpretations of endangered species stewardship (Unpublished dissertation). Texas State University, San Marcos, Texas.