Prevalence of Leeches and Algae on Painted Turtles (Chrysemys picta) in Four Created Ponds in Central Ohio: Effects of Pond, Sex, and Age Class
Abstract
We examined the prevalence (% of turtles examined) of leeches (Placobdella parasitica) and algae (likely Arnoldiella sp.) on Chrysemys picta found in 4 recently created ponds in central Ohio. Chrysemys picta in ponds with fish were less likely to have leeches and more likely to have algae than those in ponds without fish. Across all ponds, males and females did not differ in leech or algal prevalence, whereas adults were more likely to have leeches than juveniles, but did not differ in algal prevalence.
The shells of freshwater turtles can be colonized by both leeches and algae. The prevalence of leeches on freshwater turtles (i.e., the proportion of turtles observed with leeches) can be quite high in some species and populations (e.g., > 50%; Saumure and Carter 1998; Ryan and Lambert 2005) but low in others (e.g., < 15%; Ernst 1971, 1976, 2011). Prevalence of algae (i.e., the proportion of turtles with algae) similarly can vary among species and populations, with some populations showing < 10% prevalence (e.g., Edgren et al. 1953; Garbary et al. 2007; Ernst 2011) and others having an algal prevalence of > 80% (e.g., Gibbons 1968; Ernst 1986) and even 100% (Belusz and Reed 1969).
We examined the prevalence of leeches (Placobdella parasitica) and algae (probably Arnoldiella (Basicladia) sp.) on Chrysemys picta from 4 recently created ponds in a restored prairie-wetland complex in central Ohio. In particular, we examined how leech and algal prevalence varied among ponds, sexes, and age classes (i.e., adults vs. juveniles).
Methods. — We conducted this study in 4 ponds on the Granville Schools Land Lab (GSLL) in Granville, Licking County, Ohio, USA (40.089°N, 82.541°W; WGS84), which were created or modified in 2014 as part of a conversion of an agricultural field to a prairie-wetland complex under the auspices of the US Fish and Wildlife Partners in Wildlife Program. Pond 1 was originally a retention pond created during the construction of the neighboring Granville Intermediate School in 2002, but its water control system was modified as part of the creation of the GSLL and wetland plants were introduced at this time. The other ponds were created through excavation, construction of soil berms, and strategically breaking field tile. In addition, aquatic plants were seeded or planted in these ponds. Pond 1 receives run-off from nearby athletic fields and several parking lots, as well as surface water from a small intermittent creek that drains an agricultural field. Pond 2 is not connected to any surface flows of water from outside the GSLL and receives water from groundwater and precipitation. Ponds 3 and 4 are connected by surface flow and are in the drainage area of surrounding active agricultural fields. Ponds 1 and 2 lack fish, whereas Ponds 3 and 4 contain fish (Lepomis spp., Micropterus salmoides), which were first observed in July 2015. Chrysemys picta and Chelydra serpentina are the only turtles in the ponds.
We used fyke nets (2.5-cm mesh, 90-cm hoop diameter, with 15-m leads) to trap turtles from 0800 to 1600 hrs approximately every 2 wks from 16 May to 6 August 2020, with 1 fyke net/pond on 16 May and 2 fyke nets/pond thereafter. We determined sex based on the presence of secondary sex characteristics (e.g., longer foreclaws in males, tail shape and length; Ernst and Lovich 2009). We recorded any turtle that we could not reliably sex as a juvenile. We individually marked turtles by notching marginals on the carapace (Cagle 1939). We recorded the presence and location of leeches and algae on each turtle; however, we did not begin recording algal presence until 30 May 2020. We include observations from only a single capture per individual. If we captured a turtle more than once, we randomly chose one capture to include in analyses. Recaptured C. picta showed no movement among ponds; thus, we can assign each turtle to a single pond.
We used chi-square tests to compare the frequency of leeches and algae among ponds (both among individual ponds and between ponds with and without fish), sexes, and age classes (i.e., adult vs. juvenile). We used JMP Pro 14 (SAS Institute, Cary, NC) and an α-value of 0.05 for statistical significance.
Results: Leeches. — We observed leeches on 67% of turtles (44 of 66 captures). We found leeches most often on the carapace, plastron, and inguinal pockets, and at lower frequencies on other areas of exposed skin (Table 1). Leech prevalence differed among ponds, with Pond 4 having the lowest prevalence and Pond 1 having the highest (Table 2; χ23 = 16.52, p = 0.0009). Turtles from ponds with fish had leeches less frequently than did turtles from ponds without fish (Table 2; χ21 = 6.08, p = 0.014). Adult C. picta were more likely to have leeches than were juveniles (Table 2; χ21 = 4.53, p = 0.033). Males and females did not differ in leech prevalence (Table 2; χ21 = 0.39, p = 0.53).
Results: Algae. — We observed algae on 43% of turtles (26 of 61 captures). We observed algae most commonly on the carapace, especially the posterior half, only rarely on the plastron, and never on exposed skin (Table 1). Ponds 3 and 4 had higher algal prevalence than did Ponds 1 and 2, with Pond 2 having the lowest prevalence (Table 2; χ23 = 15.58, p = 0.0014). Turtles from ponds with fish had a higher prevalence of algae than did turtles from ponds without fish (Table 2; χ21 = 14.95, p = 0.0001). Adult and juvenile turtles were equally likely to have algae (Table 2; χ21 = 0.53, p = 0.47). Males and females did not differ in algal prevalence (Table 2; χ21 = 2.37, p = 0.12).
Discussion: Leeches. — The overall prevalence of leeches on C. picta in our study was 67%, which is among the highest frequencies observed for C. picta. Placobdella parasitica occurred on 32% of C. picta from a stretch of the Qu'Appelle River in Saskatchewan (MacCulloch 1981). Leeches were found on 26% of C. picta from a pool on the upper Mississippi River in Illinois (Ziglar and Anderson 2002). In Pennsylvania, 11% of C. picta from a pond and surrounding marsh had leeches (Ernst 1971). However, in our study leech prevalence varied from 86% in Pond 1 to 22% in Pond 4 (see further discussion below). This variation in leech prevalence among ponds within < 1 km of each other strongly suggests that the characteristics of the pond or wetland may drive variation in leech prevalence among populations and may explain variation in leech prevalence among studies.
The frequency of C. picta with leeches varied among ponds at the GSLL and in particular was lower for C. picta from ponds with fish than those without fish. The effects of fish on leech prevalence in C. picta at GSLL may be a function of the fish (mostly Lepomis spp.) consuming leeches (e.g., Dineen 1953; Etnier 1971), thereby potentially reducing their overall abundance in the ponds (e.g., Young and Spelling 1986; Spelling and Young 1987; Koperski 2006). Sunfish may also reduce leeches on turtles through a cleaning symbiosis (Dawson 2010). In addition, factors other than the presence of fish may help explain the difference of leech prevalence among ponds. The prevalence of leeches may vary among ponds as a result of differences in the opportunity for aerial basking because basking and raising body or shell temperature may cause leeches to abandon turtles (Selman et al. 2008). However, this explanation is very unlikely in our study because Pond 1, the pond with the highest leech prevalence, is also the only pond at the GSLL with numerous basking structures (e.g., logs, downed trees that were added during the restoration) and the highest frequency of aerial basking (G.R.S., J.E.R., W.O.S., and L.E.S., unpubl. data, 2020; see Ryan and Lambert 2005 and Readel et al. 2008 for similar observations in other turtles). The presence of submerged vegetation in the ponds may also help explain variation in leech prevalence. For example, comparing the 2 ponds with fish (Ponds 3 and 4), Pond 3 has more extensive beds of aquatic vegetation than does Pond 4 (S. Chandler and G.R. Smith, unpubl. data, 2019). The higher prevalence of leeches in Pond 3 compared with Pond 4 (χ21 = 7.34, p = 0.007) may therefore be a consequence of the presence of vegetation, which can be associated with higher abundances of leeches (Pardue and Webb 1985), perhaps by providing refuge from fish predation (e.g., Gotceitas 1990; but see Young and Spelling 1986). However, vegetation did not appear to affect leech prevalence in a turtle assemblage in Illinois (Readel et al. 2008). It is also possible that variation in water characteristics and chemistry (e.g., turbidity, fertilizer load) might affect leech prevalence (e.g., Readel et al. 2008). More detailed study is needed to explain such variation in leech prevalence on freshwater turtles among ponds and aquatic habitats.
Leeches were found most often on the carapace, plastron, and inguinal pockets. Leeches were also found at lower frequencies on other areas of exposed skin, such as the legs, tail, and head/neck region. Similar distributions of leeches on C. picta have been found by Ernst (1971), MacCulloch (1981), and Siddall and Gaffney (2004). McCoy et al. (2007) also found that leeches were found more often on posterior portions of C. picta than the anterior. However, leeches attached most frequently to the tail and head of C. picta, with fewer on the carapace and plastron (Readel et al. 2008).
Leech prevalence did not differ between male and female C. picta in our ponds. Our result is similar to that of Readel et al. (2008), who found that there was no difference in leech prevalence between males and females from 5 species of freshwater turtles combined.
Adult C. picta had a higher prevalence of leeches than juveniles in our ponds. This is consistent with MacCulloch (1981), who found that > 30% of adult C. picta had leeches, but only 4% of juveniles. Adult turtles (5 species pooled) were more likely to have leeches than were juveniles (Readel et al. 2008). It is not clear why adults would have a greater likelihood of having a leech, but it may be due to the greater surface area of adult turtles providing a larger target and more attachment sites for leeches than are available on smaller juveniles (see also Readel et al. 2008).
Discussion: Algae. — We observed algae on 43% of C. picta in the ponds at GSLL, which is at the lower end of the range observed in previous studies of C. picta (69% in Pennsylvania [Ernst et al. 2012]; 100% in Michigan [Belusz and Reed 1969]; > 75% in summer in Michigan [Gibbons 1968]; 58% in Illinois [Ziglar and Anderson 2002]). However, < 10% of C. picta from a museum collection had algae (Edgren et al. 1953) and none of 14 C. picta had algae in southwestern Nova Scotia (Garbary et al. 2007).
Algal prevalence ranged from 11% in Pond 2 to 73% in Pond 3. Algae were much more prevalent on C. picta in ponds with fish than those in ponds without fish. Variation in algal prevalence, both among studies and among the ponds in our study, may reflect environmental conditions in the ponds or wetlands in which the turtles occur. Access to basking sites and aerial basking may limit algal infestation on C. picta (Edgren et al. 1953); however, Pond 1, which had the greatest number of basking structures and frequency of aerial basking (G.R.S., J.E.R., W.O.S., and L.E.S., pers. obs.) had a similar algal prevalence to the other fishless pond (Pond 2; χ21 = 0.86, p = 0.65). Other possible explanations include differences in nutrient loads, turbidity, or other aspects of water chemistry that might affect primary productivity. We encourage additional studies that try to examine how water quality and the presence of fish might affect algal prevalence on turtles.
Algae were most commonly found on the carapace, especially the posterior half, whereas algae were only rarely observed on the plastron, and never observed on exposed skin. These observations are consistent with previous observations of algae on C. picta, which have found the highest prevalence on the carapace, especially among the marginal and costal scutes (Edgren et al. 1953; Moski 1957; Proctor 1958). The increased occurrence on the posterior carapace may result from algal colonization of freshwater turtles often proceeding from the posterior edge of the carapace forward (Hulse 1976).
Male and female C. picta did not differ in algal prevalence. Ziglar and Anderson (2002) also found no difference in algal prevalence in male and female C. picta in Illinois. We also found no difference in algal prevalence between adults and juveniles. We know of no other similar comparisons in C. picta, but in some populations of Emydoidea blandingii juveniles had more algae than did adults (Garbary et al. 2007).
Conclusions. — Our results suggest that leech and algal prevalence varies among C. picta occurring in different ponds, even though the ponds are < 1 km apart. Our results suggest that fish may be a potential factor in determining leech prevalence, and especially algal prevalence. We found no difference between the sexes in leech or algal prevalence. Adults had higher leech prevalence than did juveniles, perhaps because of surface area available for colonization by leeches, but there was no difference in algal prevalence. In addition, specific parts of turtles appear prone to occupation by leeches and algae. The significance of leech and algae attachment on freshwater turtles at the population level is unclear. Given the variation in leech and algal prevalence that we observed among ponds and that has been found among studies, the impacts of these epibionts deserve further study.
Contributor Notes
4 Present address: Department of Biology, Missouri State University, Springfield, Missouri 65897 USA
Handling Editor: Peter V. Lindeman