Winter and the availability of suitable overwintering conditions may be an important factor limiting the distribution, habitat use, and abundance of turtles at high latitudes (Ultsch 2006, Jackson and Ultsch 2010). Turtle species at high latitudes typically overwinter in waterbodies beneath ice. For such northern species, winter poses 2 important challenges: low oxygen availability in water and predation. Turtles overwintering in water must cope with prolonged submergence without access to atmospheric oxygen (Jackson and Ultsch 2010). Some species like painted turtles (Chrysemys picta) and common snapping turtle (Chelydra serpentina) can survive several months of submergence in anoxic water, but other species cannot (reviewed by Ultsch 2006). These so-called anoxia-intolerant species include the spiny softshell (Apalone spinifera), the northern map turtle (Graptemys geographica), and the common musk turtle (Sternotherus odoratus). Anoxia-intolerant species rely on dissolved oxygen to survive the winter months and their distribution and abundance may be limited by the availability of overwintering sites with sufficient dissolved oxygen to sustain their aerobic metabolism throughout the winter (Ultsch and Cochran 1994; Reese et al. 2001, 2003).

Overwintering turtles in regions of marked seasonality have little defense against predators such as otters (Lontra canadensis in North America and Lutra lutra in Europe), which can inflict substantial losses to turtle populations (Brooks et al. 1991; Lanszki et al. 2006; LBulté et al. in press). The local abundance of predators, as well as the availability of overwintering sites offering protection against predation, may also have a major effect on the distribution and abundance of turtles.

Although overwintering turtles reduce their activity substantially, several species remain somewhat active in winter (Taylor and Nol 1989; Greaves and Liztgus 2007; Plummer and O’Neal 2019; Robichaud et al. 2023). Studying overwintering activity can help us to understand how turtles behave to cope with the challenges associated with overwintering, such as gas exchange (e.g., Plummer and O’Neal 2019; Robichaud et al. 2023). Understanding the behavior and ecology of turtles in winter can thus offer important insights on the distribution and abundance of turtles at northern latitudes. Moreover, studying the overwintering habits of northern turtles will help identify and protect critical overwintering habitats, which is especially important considering that ice phenology is changing rapidly as a result of global warming (Huang et al. 2022).

The common musk turtle ranges as far north as Southern Ontario and Québec in Canada, making it one of the most northerly distributed turtle species in North America. At the northern edge of the range, water bodies may be covered in ice for > 4 mo every year. The common musk turtle is anoxia intolerant and can only survive for about 22 d when submerged in anoxic water at 3°C (Ultsch and Cochran 1994). However, when submerged in cold oxygen saturated water, it can survive for over 150 d (Ultsch and Cochran 1994). The overwintering habits of the common musk turtle in nature remain largely unknown. The few reports available state that musk turtles spend at least part of the winter buried in sediments (Thomas and Trautman 1937; Cagle 1942; Ernst 1986). Such observations, however, conflict with the known anoxia intolerance of common musk turtles because sediments typically have low oxygen (Ultsch and Cochran 1994). To better understand the overwintering behavior of the common musk turtle, we conducted a radiotelemetry study near the northern edge of the species’ range in eastern Ontario, Canada. Our goal was to document the habitat use and activity of common musk turtles during the winter. We also opportunistically gathered observations on winter predation as part of this study.

Methods. — This study took place from October 2022 to March 2023, in Opinicon Lake, a small mesotrophic lake in eastern Ontario (4.5590°N, 76.3280°W). In late October, we captured 9 adult common musk turtles (7 males and 2 females) while snorkeling along an approximately 150-m stretch of shoreline. A transmitter (RI-2B; Holohil System Ltd, Carp, ON, Canada) was glued to the rear side of the carapace of each turtle with epoxy (Water Weld; JB Weld, Marietta, GA, USA). The epoxy is white, which may have made the turtles more conspicuous to predators; so once the epoxy had cured, we colored it black with permanent marker to match the dark color of the carapace of musk turtles. The color remained on the epoxy all winter. We used a radio receiver (TRX-1000; Wildlife Materials, Murphysboro, IL, USA) with a Yagi antenna to locate the turtles. The turtles were relocated periodically until the lake froze; and once the ice was safe to walk on, the turtles were relocated every 5–12 d until it was no longer safe to walk on the ice again. Upon relocation, we used a 10-cm-diameter ice auger to drill a hole in the ice above the turtle. We measured water depth with a flexible measuring tape with a weight at the end, and water temperature 30 cm above the substrate using a thermal probe. We also used an ice fishing camera to record the substrate type and attempted to obtain a ‘visual’ of the turtle. Once measurements were taken, we filled the hole with snow and ice to accelerate freezing and marked the location with a wooden stick labelled with the date and turtle identification. The distances between relocations for each individual were measured using a 50-m flexible measuring tape.

Results. — Of the 9 radiotagged turtles, 6 died seemingly of predation during the winter. Four turtles were recovered with other dead musk turtles in what appear to be food caches (Fig. 1 A,B). Two of the presumed caches were under ice shelves overhanging the shore and contained 2 and 7 carcasses, respectively. The third cache was under a wooden dock, on the shore, and contained 8 carcasses including 2 radiotagged turtles. These two radiotagged turtles appeared to have been predated before the beginning of the tracking on the ice on 5 February because they were first located under the dock on that date. The 2 remaining turtles found dead were recovered in water after the spring thaw. One turtle may have died early during the winter because it did not move until it was recovered dead after the spring thaw. The other turtle was seemingly alive most of the winter because it regularly changed locations and was presumably depredated after its last relocation on 12 March 2023.

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Despite a high mortality rate, we were able to gather observations on the overwintering habitat and behavior of 6 individuals (Table 1). All turtles overwintered < 20 m from shore with mean depths for each turtle ranging from 0.4 to 1.9 m. The deepest turtle was found at a depth of 2.1 m. The mean temperature for each turtle ranged from 0.5° to 1.1°C (Table 1).

Table 1. Depth, temperature, and movement from 6 individual common musk turtles radiotracked between 5 February and 12 March 2023 in Opinicon Lake, Ontario, Canada.

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We made 23 attempts to obtain visuals for 7 different individuals using an ice fishing camera. Visuals were obtained for 3 turtles. Two were fully exposed and resting on the substrate (Fig. 1C) and the third was found within aquatic vegetation and only the rear end of the carapace and the transmitter antenna (Fig. 1D) was visible. One of the fully exposed turtles was found dead in the spring at the same location it was observed under the ice and may thus have been dead at the time of the observation. The other two turtles survived the winter, and one was observed moving under the ice. In all other attempts at obtaining visuals, the sediment was partially or fully covered by aquatic vegetation and the turtles could not be observed with the camera. It was thus not possible to assess whether and to what extent common musk turtles aggregate in winter, but the fact that the 9 radiotagged turtles were scattered along approximately 1 km of shoreline suggests that they do not form dense overwintering aggregations.

We obtained movement data over the winter for 5 individuals. Two turtles moved < 3 m during the winter but 3 moved regularly and covered 22, 50, and 70 m, respectively. The distance moved by these turtles between relocations ranged from 0 to 32 m (Fig. 2).

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Discussion. — Our telemetry study revealed a high (66%) rate of winter mortality over a single winter. We took precautions to minimize predation risk and do not think our methodology affected predation risk. We colored the epoxy to match the carapace of the turtles to make sure the transmitters would not make the turtles more conspicuous. We found 13 additional carcasses with, or near to, the radiotagged turtles that were recovered dead, indicating that the predators were not targeting turtles with transmitters. We also used a small-diameter (10-cm) auger and always backfilled the holes with ice and snow so that the holes were frozen shut in within a few hours.

The most likely predators capable of capturing turtles under the ice in our study area are the American mink (Mustela) and the river otter (L. canadensis), but we suspect the former is responsible for the predation we documented. We installed a trail camera near the first suspected cache site upon its discovery, and a mink was captured on camera 2, and on 4 d thereafter. River otters are much larger than American minks and have larger, and more powerful jaws (Christiansen and Wroe 2007) capable of crushing a turtle the size of a common musk turtle (G. Bulté et al. unpubl. data, in press). It is unclear whether the rate of predation we documented is normal for overwintering musk turtles in our area because we only have data from a single winter. The demography of common musk turtles at our latitude is poorly documented so it is difficult to assess whether such seemingly high rate of predation is sustainable. It is possible that predation was exceptionally high in the winter of 2022–2023 as a result of relatively warm winter temperatures. Indeed, the 2022–2023 winter in the Great Lakes and St-Lawrence region was the third warmest since 1948 with an average temperature 4.2°C above the 1961–1990 baseline (Environment Canada 2023). The warm weather resulted in thin ice conditions in the Great Lakes (North American Ice Service 2023). The ice in Opinicon Lake likely was affected by the warm weather, which may have provided more access to turtles by predators such as minks. Follow-up studies will be necessary to determine whether such rate of predation is normal, and sustainable for this population.

Based on our observations, common musk turtles appear to preferentially overwinter in shallow water (< 2 m) with abundant aquatic vegetation. Although we were unable to observe most turtles, our limited but direct observations suggest that common musk turtles do not bury in the sediments as suggested by others (Cagle 1942; Ernst et al. 1986), but rather hide in aquatic vegetation (Fig. 1D). This behavior is consistent with the limited tolerance for anoxia documented in common musk turtles (Ultsch and Cochran 1994), and with the fact that some individuals moved regularly throughout the winter potentially in response to changing oxygen levels. If musk turtles must remain fully exposed to permit extrapulmonary gas exchange, aquatic vegetation may provide a hiding place with relatively high dissolved oxygen because aquatic plants can photosynthesize even under the ice (Spencer and Wetzel 1993).

The average water temperature recorded 30 cm above the substrate at turtle locations was 0.9°C. Other temperate turtles have also been reported to overwinter in water around 1°C (Greaves and Litzgus 2007; Rollinson et al. 2008; Edge et al. 2009; Robichaud et al. 2023). Selecting cold temperature during the winter may be a means to behaviorally reduce metabolism and thus the demand for oxygen at a time when dissolved oxygen may become limited. Moreover, the concentration of dissolved oxygen increases with decreasing temperature. Selecting low temperature in the winter may be particularly important for the common musk turtle because this species is the second-least-tolerant species to anoxia among North American turtle species studied to date (Ultsch 2006). Unfortunately, we were unable to measure dissolved oxygen as part of this study to determine whether it plays a role in overwintering habitat selection.

Some radiotagged turtles travelled considerable distances under the ice indicating that, at least in our study population, some individuals are active in winter. Several species of freshwater turtles have been reported to be somewhat active in winter (Taylor and Nol 1989; Greaves and Liztgus 2007; Plummer and O’Neal 2019; Robichaud et al. 2023), but few studies have measured the distance travelled by turtles under the ice. Greaves and Litzgus (2007) reported that wood turtles (Glyptemys insculpta) travelled up to 10 m between relocations (7–12 d apart) and Edge et al. (2009) reported that Blanding turtles (Emydoidea blandingii) moved < 1 m under the ice between relocations (interval unspecified). In contrast, 3 of 5 common musk turtles from which we obtained movement data, moved > 10 m between relocations (5–12 d apart). The greatest distance travelled between two relocations was 32.5 m over 7 d. This individual moved regularly and traveled 70 m between 5 February and 12 March (35 d). The common musk turtle thus appears to remain particularly active in winter compared with co-occurring species studied to date. The reason for winter activity remains unclear but may help ventilate the skin and promote gas exchange (Plummer and O’Neil 2019). Other functions such as courtship and mating cannot be excluded.

Based on our observations, the common musk turtles in Opinicon Lake have a different overwintering strategy from that of the northern map turtle occurring in the same lake. Both species are considered anoxia intolerant in winter (Ultsch 2006) and may thus be expected to seek similar overwintering habitats and behaviors. However, in Opinicon Lake, hundreds of northern map turtles overwinter gathered together in a shallow and rocky area with limited aquatic vegetation (Feng et al. 2020; Robichaud et al. 2023). The propensity of northern map turtles to form large overwintering aggregations may indicate that overwintering habitats with sufficient dissolved oxygen are limited (Graham and Graham 1992). In contrast, musk turtles did not appear to form large aggregations and overwintered in vegetated areas with softer substrate. Differences in size, and thus in metabolism, as well as differences adaptations for extrapulmonary gas exchange, may explain some of these differences between these species. Although a large adult common musk turtles in our study population weighs about the same as a large adult male northern map turtle, adult female northern map turtles can weigh 10 times as much as a common musk turtle. In absolute terms, northern map turtles thus have higher demands for oxygen. Moreover, the common musk turtle appears to be better adapted for aquatic respiration than the northern map turtle because they have a relatively large cutaneous surface area for their size, a relatively thin integument (Stone et al. 1992), and possess a heavily vascularized buccopharyngeal area that appears to facilitate gas exchange (Heiss et al. 2010). The common musk turtle may thus be less limited than the northern map turtle in its choice of overwintering sites, which could explain why they do not seem to form larger aggregations. Overwintering aggregations in common musk turtles may, however, occur in other regions (see Thomas and Trautman 1937).

Our study spanned a single tacking season, and our sample size was small. Our findings should therefore be viewed as preliminary. We showed that the common musk turtle, an anoxia-intolerant species, spends the winter concealed in aquatic vegetation at water temperatures around 1°C and remains active in winter, moving relatively long distances under the ice. Moreover, we showed that common musk turtles can be especially vulnerable to predation in winter, which raises concerns about effects of lake ice loss (Huang et al. 2022) on the abundance and distribution of northern turtles.