Historical museum collections and contemporary population studies implicate roads and introduced predatory bullfrogs in the decline of western pond turtles

Abstract

The western pond turtle (WPT), recently separated into two paripatrically distributed species (Emys pallida and Emys marmorata), is experiencing significant reductions in its range and population size. In addition to habitat loss, two potential causes of decline are female-biased road mortality and high juvenile mortality from non-native predatory bullfrogs (Rana catesbeiana). However, quantitative analyses of these threats have never been conducted for either species of WPT. We used a combination of historical museum samples and published and unpublished field studies shared with us through personal communications with WPT field researchers (B. Shaffer, P. Scott, R. Fisher, C. Brown, R. Dagit, L. Patterson, T. Engstrom, 2019, personal communications) to quantify the effect of roads and bullfrogs on WPT populations along the west coast of the United States. Both species of WPT shift toward increasingly male biased museum collections over the last century, a trend consistent with increasing, female-biased road mortality. Recent WPT population studies revealed that road density and proximity were significantly associated with increasingly male-biased sex ratios, further suggesting female-biased road mortality. The mean body size of museum collections of E. marmorata, but not E. pallida, has increased over the last 100 years, consistent with reduced recruitment and aging populations that could be driven by invasive predators. Contemporary WPT population sites that co-occur with bullfrogs had significantly greater average body sizes than population sites without bullfrogs, suggesting strong bullfrog predation on small WPT hatchlings and juveniles. Overall, our findings indicate that both species of WPT face demographic challenges which would have been difficult to document without the use of both historical data from natural history collections and contemporary demographic field data. Although correlational, our analyses suggest that female-biased road mortality and predation on small turtles by non-native bullfrogs are occurring, and that conservation strategies reducing both may be important for WPT recovery.

Reference Genome of the Northwestern Pond Turtle,Actinemys marmorata

“…We captured an adult male northwestern pond turtle using baited hoop nets in Putah Creek in Solano County, CA (38.517263°N, 121.751965°W) on 16 July 2020 (CDFW permit# SC-11197 to BDT) ( Figure 1 ). Distinguishing A. marmorata from A. pallida can be difficult; we identified the captured individual based on the geographic location of the collection site and the presence of enlarged, triangular inguinal scutes ( Figure 1 ), which are found in 89% of northwestern pond turtles, but are reduced or absent in 94% of southwestern pond turtles ( Seeliger 1945 ; Nicholson et al 2020 ). BDT collected 0.8 mL of fresh whole blood from the subcarapacial sinus, briefly stored it in a Vacutainer tube with EDTA, and delivered it to the UC Davis Genome Center within 30 min of collection.…”

“…The US Fish and Wildlife Service announced in 2015 that protection under the Endangered Species Act (ESA 1973, as amended) may be warranted, and its listing status is currently under review ( USFWS 2015 ). Important causes of decline include predation on hatchling turtles, particularly by non-native American bullfrogs ( Rana catesbeiana ), and largemouth bass ( Micropterus salmoides ), pathogens—including a newly described pathogenic shell fungus—and habitat alteration ( Woodburn et al 2019 ; Nicholson et al 2020 ; Manzo et al 2021 ).…”

Impacts of a Non-indigenous Ecosystem Engineer, the American Beaver (Castor canadensis), in a Biodiversity Hotspot

“…Other predominant invasives include American bullfrog (Lithobates catesbeianus), red swamp crayfish (Procambarus clarkii), African clawed frog (Xenopus laevis), and Emydid turtles [e.g., red-eared slider (Trachemys scripta elegans) and others in the pet trade], with bullfrog and red swamp crayfish being two of the worst and most common invaders (Kats and Ferrer, 2003). Introduced bullfrog prey upon on a variety of native species, and the larger an individual grows the large the prey item it can consume (Rosen and Schwalbe, 1995;Casper and Hendricks, 2005;Maret et al, 2006;Nicholson et al, 2020). The presence of invasive centrarchid fish species has been shown to increase the abundance and spread of bullfrog in systems where they cooccur, as the non-native fish consume native macroinvertebrates that would otherwise prey on larval bullfrog (Adams et al, 2003).…”

Geospatial assessment of freshwater invasive species to inform turtle conservation and management

“…Santori et al (2018) used community science data to assess the mortality of the eastern long‐necked turtle, Chelodina longicollis , associated with roads. Nicholson et al (2020) used museum data to assess the effects of roads and invasive bullfrogs on western pond turtle populations. Ryberg et al (2017) integrated habitat modelling with data on land use change to assess the conservation status of the western chicken turtle ( Deirochelys reticularia miaria ).…”