Experimental removal of introduced slider turtles offers new insight into competition with a native, threatened turtle

Study site

Our study took place at the UCD Arboretum (38.53, −121.76), a permanent waterway extending along the southern border of the UC Davis campus, Yolo County, California, USA (Fig. 1). The UCD Arboretum was formed in the 1870s when the historical north fork channel of Putah Creek was diverted into the south fork (Larkey, 1980). This waterway is 2.4 km long, ca. 4 ha in surface area, and averages 15 m wide and 1 m deep (Spinks et al., 2003). Terrestrial habitat surrounding the waterway is irrigated and landscaped with predominantly non-native vegetation (Spinks et al., 2003). A 1.5–2.5 m wide paved path encircles the entire waterway within 5–10 m of the water’s edge. This path is regularly used by pedestrians, bicyclists, and maintenance vehicles which influence turtle basking (Lambert et al., 2013; Costa, 2014). The waterway’s shoreline—including basking sites—is a combination of concrete, exposed dirt, and landscaping steel mesh which has been exposed by erosion (Lambert et al., 2013).

Turtle trapping and RES removal

Across the UCD Arboretum, we deployed baited submersible traps in optimal habitat for both RES and WPT over approximately 900 trap-days from 10 July–1 August, 2011 and again from 13–29 September, 2011. We supplemented this trapping with dip netting and opportunistic hand captures during both periods, and with a fyke net and a basking trap during the latter period. Dip netting and hand captures were targeted at RES but other trapping was not. We removed and euthanized all RES, depositing most specimens at the UC Davis School of Veterinary Medicine, the Natural History Museum of Los Angeles County, or the UC Davis Museum of Wildlife and Fish Biology. Beginning in the 1996, our group uniquely marked each captured WPT with scute notches using a handheld file or (juveniles only) nail clippers (Spinks et al., 2003). We similarly marked any new WPT during this trapping effort. We used linear regression to test whether our trapping depleted the RES population over time by regressing cumulative RES captures against trapping day for adult RES (Krebs, 1989). Using likelihood ratio tests (Crawley, 2013) to assess model fits, we compared a quadratic model, which would indicate population depletion, to a linear model, which would indicate that the RES population was not leveling off with our removal effort.

WPT body condition

To estimate changes in WPT body condition, we trapped for one week the year following RES removal, from 27 May–2 June, 2012. Due to logistical constraints we were unable to trap later in the summer at a similar time as in 2011. Differences in trapping dates may influence body condition analyses because females may be gravid and therefore heavier in the earlier 2012 sampling or because all turtles may have had more time to put on mass during the later 2011 sampling. However, these effects are likely limited. In both 2011 and 2012 we measured WPT plastron length (notch-to-notch; mm) with dial calipers and body mass (g) with Ohaus CS2000 digital pan scales (Iverson & Lewis, 2018). We used a linear mixed-effects model (function ‘lmer’, R package “lme4”; Bates et al., 2015) to test whether WPT body condition (i.e., differences in mass controlling for body length) changed after the RES removal (Cadi & Joly, 2003; Schulte-Hostedde et al., 2005; Litzgus, Bolton & Schulte-Hostedde, 2008). Our model of WPT mass controlled for plastron length and included treatment (pre- or post-removal) and sex as fixed effects and individual WPT as a random effect to control for repeated measures. This model simultaneously regresses body mass against plastron length and tests for differences in the residuals of this model between study year and sex. We used likelihood ratio tests to assess the significance (α < 0.05) of fixed effects and removed non-significant variables from our model. We obtained full model conditional R² (cR²) for fixed and random effects combined and a marginal R² (mR²) for the model’s fixed effects alone (function ‘r.squaredGLMM’, package “MuMIn”, Barton, 2018).

Basking site monitoring

We conducted binocular surveys of 24 pre-selected basking sites (Fig. 1) for 34 total days—16 days pre-removal between 18 March and 22 April 2010 (Lambert et al., 2013) and 18 days post-removal between 18 March and 22 April 2012. Following Lambert et al. (2013), we performed all surveys between 1,000 and 1,500 hr to coincide with the expected maximum turtle basking activity during this time of year. We surveyed all sites once daily in rapid succession to avoid counting the same turtle at multiple sites. Each survey was performed in under one hour, at a distance of ca. 10–100 m from turtles, and did not noticeably disturb basking turtles. MRL and S. Nielsen conducted basking surveys in 2011 and JMM and RMS conducted 2012 surveys; all surveyors were trained by GBP and HBS. During each survey we recorded the number of individuals of each species basking at each basking site as well as water temperature because we previously found that basking activity of both species increases more with warmer water temperatures than with air temperatures (Lambert et al., 2013). We also obtained air temperature data from the UC Davis Russell Ranch Weather Station which is located ca. 4 km NW of the UCD Arboretum.

Modeling the effects of RES removal on turtle basking

We tested for changes in the relative basking distribution of WPT and RES (i.e., the proportion of basking turtles that were Emys − Emys / (Emys + Trachemys) across the UCD Arboretum pre- and post-RES removal using a generalized linear mixed effects model (GLMM) with a binomial family for proportion data (function ‘glmer’, R package “lme4”). A binomial GLMM accounts for binary data (two species here) and variation in sample sizes across basking sites and survey days. We modeled WPT:RES basking as a function of treatment (pre- or post-removal) and the distance of each basking site from the west end of the UCD Arboretum because turtle basking distributions were previously shown to vary west-east (Lambert et al., 2013). We accounted for repeated measures by treating survey date as a random effect (Lambert et al., 2013). To explore site-specific changes in the ratio of the two species, we also used individual binomial GLMMs for each basking site.

In addition, we modeled the absolute basking abundance of both species pre- and post-removal using Poisson GLMMs (function ‘glmer’, R package “lme4”) for count data. Our approach here was the same as with the binomial GLMM and, if an interaction between treatment and distance from the west end was significant, we used individual GLMMs for each year to test the pattern and strength of turtle basking distributions across the UCD Arboretum in each year. To test whether certain basking sites made up larger or smaller proportions of total WPT basking observations pre- or post-removal, we used contingency tables, focusing on the five most heavily-used turtle basking sites (combined for both species) pre-removal (sites P, O, E, Q, and R) and site X, the most heavily-used turtle basking site post-removal.

Trapping and RES removal

We removed and euthanized 177 RES (100.6 kg total biomass), including 28 adult males (16.3 kg), 72 adult females (79.4 kg), and 77 juveniles (4.9 kg, defined as ≤ 100 mm carapace length; Ernst & Lovich, 2009). A quadratic (rather than linear) model fit our data best (likelihood ratio test p < 0.0001, full model R² = 0.95) and showed RES captures leveling off, signifying we had removed a substantial fraction of the RES population.

We also captured, marked, and released 115 unique WPT (62.7 kg total biomass) comprising 51 males (36.1 kg), 36 females (24.1 kg), and 28 juveniles (2.5 kg, defined as ≤ 110 mm plastron length; Holland, 1991).

WPT body condition

While we trapped a larger number of WPT in each year, we trapped 25 unique adult WPT in both 2011 and 2012; we used these 25 WPT for the body condition analysis. The body condition linear model showed no interaction between treatment and sex (p = 0.92) and so we removed this interaction from the model. Sex (p = 0.009), treatment (p < 0.001), and plastron length (p < 0.0001) were significant (full model cR² = 0.95, mR² = 0.86). For a given plastron length, males were on average 61.54 g (±23.55 SD g) heavier than females. Although the 25 WPT measured before and after RES removal showed individual variation in their degree of body condition change post-removal (Fig. 2A), on average they were 39.80 g (±9.92 SD g) heavier for a given plastron length post-removal (Fig. 2B).

Basking site monitoring

We recorded 283 WPT and 645 RES observations in 2010 but only 43 WPT and 61 RES observations in 2012. Although the reduction in numbers of observed WPT was unexpected, we do not believe this reflects a decline in the WPT population. From 27 May–2 June 2012, we trapped 54 unique WPT over seven days and a Schnabel multiple capture-mark-recapture population estimate (Krebs, 1989) derived from trapping data (beginning in the mid 2000s) suggest that ca. 162 WPT (including 10 newly-marked juveniles) were present in the UCD Arboretum immediately after our post-removal surveys (J McKenzie, R Screen, and G Pauly, pers. comm., 2014); this estimate is similar to pre-removal estimates of WPT population size (ca.146 WPT, including 18 newly-marked juveniles). Given these estimates, we are confident that the WPT population was essentially unchanged during our experiment, and thus our focus on the relative basking distributions of turtles at monitored basking sites meaningfully reflects the impact of our removal experiment and not a catastrophic decline in WPT.

The basking sites most commonly used by WPT pre-removal were generally the same sites used post-removal (Figs. 3A, 3B). We recorded WPT basking at 15 of 24 basking sites pre-removal, but at only eight of 24 sites post-removal. WPT were absent from 8 sites they used pre-removal (although of these, only two were frequently used pre-removal: sites A and N) and were present at one additional site where they were not recorded pre-removal (site B). We recorded RES basking at 17 of 24 basking sites pre-removal, and only eight of 24 sites post-removal (Figs. 3A, 3B). RES were absent from nine sites they used pre-removal and were not recorded using new sites post-removal.

Water temperatures were warmer in 2010 (17.0 C ± 1.71 SD) than in 2012 (15.4 C ± 2.12 SD; two-tailed t-test, p < 0.0001). However, maximum daily air temperatures (averaged across all days of each survey period) were not different between years (2010, 19.2 C ± 4.13 SD; 2012, 18.8 C ± 5.25 SD; two-tailed t-test, p = 0.74). Furthermore, in the two weeks prior to our surveys, maximum daily air temperatures were marginally significantly warmer in 2012 (18.6 C ± 4.04 SD) than in 2010 (16.07 C ± 3.34 SD; two-tailed t-test, p = 0.08). Air temperatures were also warmer in the winter (beginning of December to end of February) preceding the post-removal survey than the winter preceding the pre-removal survey (2009–2010, 13.4 C ± 3.35 SD; 2011–2012, 15.5 C ± 2.83 SD; two-tailed t-test, p < 0.0001). Colder water temperatures may thus have contributed to the lower overall turtle basking we observed in 2012, but this effect might have been modulated by warmer air temperatures prior to our 2012 surveys.

Effects of RES removal on turtle basking

The interaction between removal treatment and distance from the west end of the UCD Arboretum was not significant (p = 0.18) and was removed from the model. Both treatment (p < 0.0001) and distance from the west end (p < 0.0001) were retained (cR² = 0.31, mR² = 0.31).

The non-significant interaction indicates the removal did not change the ratio basking turtles that were WPT across the UCD Arboretum. Both pre- and post-removal, the basking distribution of turtles was WPT-biased in the west end and RES-biased in the east end (Fig. 4). However, the proportion of basking individuals that were WPT increased from 30.5% pre-removal to 41.3% post-removal (p < 0.0001; Tukey’s post-hoc test, function ‘glht’, package “multcomp”). Individual binomial GLMMs for each basking site showed removal treatment effects on the WPT:RES basking ratio for site Q (p = 0.002, 9% WPT to 55% WPT; Fig. 3) and a marginal effect for site O (p = 0.09, 30% WPT to 75% WPT; Fig. 3). All other individual basking sites showed no differences (all p > 0.1).

Pre-removal, the WPT basking distribution declined from west to east, and post-removal WPT basking had a relatively flat distribution (Fig. 5). We detected a shift in the absolute basking distribution of WPT with a significant interaction between removal treatment and distance from the west end (Poisson GLMM, p = 0.012, cR² = 0.23, mR² = 0.06). Individual GLMMs for each year indicated that distance from the west end was significantly associated with WPT basking abundance in the pre-removal year (p < 0.012, cR² = 0.27, mR² = 0.03) but not in the post-removal year (p = 0.55).

WPT predominantly used the same basking sites post-removal but showed a more even distribution across basking sites, with more basking activity at two center-east sites (Q and X) compared to before the RES removal (Figs. 3A, 3B). Contingency table analyses showed that sites Q (p = 0.01) and X (p = 0.001) encompassed larger proportions of total WPT basking observations post-removal than pre-removal (Figs. 3A, 3B). All other sites made up similar proportions pre- and post-removal (all p > 0.1), though some sites had generally low basking activity (Figs. 3A, 3B), possibly limiting our power to detect shifts.

Our experimental removal of RES was associated with flatter observed distribution of WPT. Even so, if more eastern sites that were dominated by RES pre-removal (e.g., sites O, P, Q, and R) are also preferred WPT basking locations, then WPT should have increased basking at these sites post-removal. We did not see this shift.

After removal, remaining RES were sparse throughout much of the UCD Arboretum and concentrated in the east end (Figs. 3A, 5). For RES, a Poisson GLMM indicated a significant interaction between treatment and distance to the west end (p < 0.0001, cR² = 0.30, mR² = 0.16). Individual GLMMs for each year showed a positive relationship between RES basking and the distance to the west end pre-removal (p < 0.0001, cR² = 0.27, mR² = 0.02) and post-removal (p < 0.0001, cR² = 0.14, mR² = 0.14). The distance of each basking site from the west end explained substantially more of the variation in RES basking abundance post-removal than pre-removal, indicating that remaining RES concentrated in the east end more strongly after we removed most of the RES population (Figs. 3A, 5). Contingency table analyses indicated that sites E, O, P, and R (Fig. 3) comprised lower proportions of total RES basking observations after the removal and site X (Fig. 3) comprised a higher proportion (all p < 0.05). Site Q made up similar proportions of total RES observations in both years (p = 0.14).

The RES remaining post-removal abandoned several basking sites that they previously used heavily (particularly sites O and P; Fig. 3) and shifted towards the east end of the UCD Arboretum (e.g., site X). This result suggests that RES prefer habitat at this end of the waterway and that, prior to our experiment, RES densities were high enough for intraspecific competition to force many RES into less preferred areas of the waterway. Our previous work showed that RES basking activity was highest at sites with shallow slopes, deeper water adjacent to the site, a steel mesh (rather than concrete or dirt) substrate, and high human activity (Lambert et al., 2013). Post-removal, RES basking activity was highest at the two sites (V and X) that maximized this combination of variables based on 2010 surveys (Fig. 4B from Lambert et al., 2013).

Should we remove RES to benefit declining native turtles?

A recent summary of research goals for effective conservation of WPT (Thomson, Wright & Shaffer, 2016) identified the need for a clearer quantitative understanding of the impact of introduced RES. Controlling invasive species is a substantial commitment that rarely eliminates the entire population, particularly in situations with continual introductions (Kikillus, Hare & Hartley, 2012; Gaeta et al., 2015; García-Díaz et al., 2017). Removing 177 RES from the UCD Arboretum was an intensive effort requiring >2,000 person-hours of field work across 40 days. A similar level of effort would conservatively cost the California Department of Fish and Wildlife $26,000–$31,000 in Scientific Aid hourly wages (L Patterson, pers. comm., 2019). While our study suggests that removing RES does influence native turtle basking ecology and feeding, the potential benefits with respect to short-term basking-site usage appear quantitatively modest. However, the substantial increase in WPT body condition during the year following the RES removal suggests that removing RES meaningfully increased resource availability for WPT. Whether these returns justify the effort may well depend on several variables, including RES abundance / density, attitudes of local human residents to introduced RES, disease risk (Héritier et al., 2017), other potential axes of competition (e.g., nesting sites), and additional aspects of ecosystem health.

Our results also provide evidence that RES introductions may affect native turtles simply by inflating turtle densities in general (regardless of species identity). Therefore, removing RES may not necessarily relieve native turtles from a dominant competitor but, rather, may relieve ecological or behavioral pressures associated with high turtle densities and could conceivably result in unexpected responses by native species. One such unexpected response here was the substantial decrease in overall WPT basking observations after we removed over half of the turtle community, a result that suggests a change in WPT behavior and habitat use that our experimental design, with fixed monitoring sites, failed to capture. Unlike many other freshwater turtles, WPT are aggressive baskers—threatening, biting, pushing, and ramming other turtles from basking sites—and prefer to bask alone or in low numbers (Bury & Wolfheim, 1973). Reduced turtle densities post-removal may thus have allowed WPT to occupy other basking habitats in lower numbers as is their preference. Additionally, higher WPT body condition post-removal was likely influenced by there simply being fewer turtles overall competing for food in the UCD Arboretum. Improved body condition may also be the result of WPT adopting preferred basking behaviors, thereby improving digestive efficiency and mass gain. Future studies, including dietary research, that include unmanipulated control sites, pre-removal surveys that span multiple years and account for year-to-year variation, as well as a design that tracks the behavior of native turtles pre- and post-RES removal (e.g., using GPS-enabled radio transmitters) may better elucidate these unexpected outcomes on native turtles. Overall, our analyses suggest WPT responded to RES removal in a manner consistent with interspecific competition for food but inconsistent with strong interspecific competition for basking habitats, implying that removing RES may well be an important management strategy in some situations.

Alternatively, the direct management of basking habitat may be a more generally tractable conservation activity for WPT (Spinks et al., 2003; Thomson, Wright & Shaffer, 2016). In human-modified waterways, removal of floating basking sites for flood control and aesthetics (Spinks et al., 2003) could exacerbate competition for basking sites. Emerging research suggests that experimentally-added floating logs are preferred by WPT compared to bank-side basking sites and are more heavily used by WPT than RES, especially when they are isolated from human activities (Cossman et al., unpublished data). Adding artificial basking sites that favor WPT, alone or in combination with RES population reduction, is a simple, comparatively inexpensive manipulation that should be explored in future field experiments.

Study limitations

The primary limitations of our study center on interpreting our basking results. We expected to observe fewer basking RES in the second year of study due to our intense removal effort but did not expect a concomitant decline in WPT observations. It is possible that water temperature, other environmental variation, or unforeseen consequences of our manipulation resulted in reduced overall turtle basking activity, or (more likely to us) radical shifts in basking to new and unmonitored locations, after the RES removal. Unfortunately, we cannot confidently identify which factor(s) resulted in fewer WPT basking observations. Although we studied both basking and feeding, we also recognize that our experiment did not address other potentially important axes of competition that are important for the continued recruitment and persistence of WPT populations. While we employed a before-after comparative design, the use of unmanipulated control sites would have improved our ability to make stronger inferences in this study. We do not believe that the lower number of WPT basking observations confounds our results because our analyses of relative basking distribution differences between species and years can accommodate sample size differences. Additionally, our analyses found that residual RES shifted their basking in intuitive ways (i.e., towards sites with preferred characteristics), increasing confidence in our results. While field experiments offer more biological realism than experiments in captivity, that added complexity may also yield unexpected results, such as changing a focal species’ behaviors or habitat use.