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Terrestrial flight response: a new context for terrestrial activity in Sonoran mud turtles.


Animals foraging under threat of predation can either remain active or seek refuge. The risk allocation hypothesis predicts that temporal variation in risk is an important component of foraging strategy, with greatest risk aversion during brief and infrequent high risk situations, and less risk aversion during low risk situations and during chronic high risk situations (Lima and Dill, 1990; Lima and Bednekoff, 1999; Preisser et al., 2005). Tests of the risk allocation hypothesis typically involve experimental manipulations of risk or reward, often using humans as model predators in manipulations of risk. An extensive literature supports the assumption that animals respond similarly to disturbances caused by humans and risks imposed by predators (reviewed by Frid and Dill, 2002). Tests of the risk allocation hypothesis have demonstrated that animals reduce risk by reducing activity (Sih, 1986; Dill, 1987; Kiesecker and Blaustein, 1997) or by moving into less risky but less rewarding environments (Loose and Dawidowicz, 1994; Kiesecker and Blanstein, 1997; Creel et al., 2005). In addition, response to manipulations of both risk and reward are condition dependent and can vary with age, body size and reproductive status (Flinders and Magoulick, 2007; Heithaus et al., 2007).

Semi-aquatic animals often avoid risk by undergoing aquatic flight responses, acute movements from land into water following disturbances (Birt et al., 2001; Mesquita et al., 2006; Cooper et al., 2008). Under the risk allocation hypothesis, the benefit of escaping predation during an aquatic flight response outweighs the cost of suspending terrestrial activity like basking or feeding. However, the benefit of entering an aquatic refuge, or remaining hidden within one, should decrease when terrestrial predators can easily search an aquatic habitat and when the surrounding terrestrial environment is structurally complex. Under such circumstances, risk could be higher in the aquatic environment; and semi-aquatic species could reduce risk by undergoing terrestrial flight responses. Caiman (Caiman crocodilus) and two turtle species (Acanthochelys macrocephala and Kinosternon scorpiodes) were observed moving into terrestrial refuges after being disturbed in shallow water by biologists (Campos et al., 2003; Metrailler, 2006; Buskirk, 2007). These observations suggest that terrestrial flight responses could be a general strategy for risk aversion in situations where aquatic habitats are shallow and small, and focal species are effective at avoiding detection on land.

In May 2000, two members of our field crew caught 15 Sonoran mud turtles, Kinosternon sonoriense, by hand in a shallow pond (depth ca. 0.5 m, surface area ca. 100 [m.sup.2]) in the Peloncillo Mountains, New Mexico. Within minutes of release back into the pond, six turtles underwent terrestrial flight responses, moving onto land and eventually out of sight. Based on this observation, we considered our sampling method, entering and wading through the water in search of turtles, to be an experimental disturbance that could induce terrestrial flight responses in Sonoran mud turtles. We assumed that our sampling constituted a brief and infrequent high risk situation for turtles in experimental aquatic habitats, and; therefore, data on this behavior should be viewed in the context of risk allocation.

We used experimental disturbances of Sonoran mud turtles to further describe this behavior. Specifically, we asked if water depth or turtle size was correlated with the probability of undergoing terrestrial flight responses. We developed two predictions from the risk allocation hypothesis and from previous descriptions of terrestrial flight responses. First, we predicted that terrestrial flight responses were more likely in shallow (high risk) environments than in deep (low risk) environments (Metrailler, 2006). Second, we predicted that terrestrial flight responses were more likely in larger individuals (Campos et al., 2003) because larger individuals would be better able to avoid desiccation on land (Stone and Iverson, 1999) and less able to avoid detection in shallow water.



Sonoran mud turtles occur in southwestern New Mexico, Arizona and northern Mexico Iverson, 1992), sometimes reaching high abundance in intermittent aquatic habitats Stone, 2001). Sonoran mud turtles frequently move between aquatic and terrestrial habitats, including movements among pools and movements into terrestrial estivation sites (van Loben Sels et al., 1997; Stone, 2001; Ligon and Stone, 2003; Hall and Steidl, 2007). Regular and complete drying of aquatic habitats forces terrestrial estivation by all individuals in some populations (Stone, 2001; Ligon and Stone, 2003). In addition, even when water is available there is asynchronous aquatic activity in some populations, with the majority of individuals at any one time estivating on land (Stone, 2001; Ligon and Stone, 2003). Laboratory and field studies have confirmed the central role of estivation in the natural history of Sonoran mud turtles living in intermittent aquatic habitats. In the laboratory, Sonoran mud turtles from intermittent aquatic habitats can tolerate long periods (>80 d) of desiccation (Peterson and Stone, 2000; Ligon and Peterson, 2002). In the field, turtles outfitted with radio transmitters all estivated, for periods ranging from 11-34 d (Ligon and Stone, 2003).


Our study area was within the Coronado National Forest in the Peloncillo Mountains, Hidalgo County, New Mexico. The Peloncillo Mountains (32[degrees]12'N, 108[degrees]60'W) are a north-south oriented range (110 x 20 km) along the southern border of New Mexico and Arizona, near the edge of both the Sonoran and Chihuahuan Deserts. Suitable aquatic habitats for Sonoran mud turtles in the Peloncillo Mountains included artificial stock tanks and natural canyon pools (Stone, 2001). Stock tanks were created by the construction of an earthen or concrete dam on the downstream end of the largest or most conveniently located pool within a canyon. Stock tanks were deeper, larger and more persistent than canyon pools, but both habitats had similar bank morphologies with gently sloping gravel substrates that turtles could easily move across. All aquatic habitats in the Peloncillos dried regularly. Typically, water levels were high during the wet season (Jul.-Sep.) and low during the dry season (May-Jun.). Most of our data were collected in Blackwater Canyon, a 3.75 km canyon with a stock tank, Blackwater Hole, 0.75 km from the top of the canyon (ca. 1700 m elevation; Ligon and Stone, 2003). We measured water levels in Blackwater Canyon on 30 occasions between 1994-2008, including samples during the dry season in 13 y and samples during the wet season in 13 y (Stone, 2001; Ligon and Stone, 2003). During the dry season, canyon pools were dry (n = 4) or low (total surface area < 375 [m.sup.2], n = 5) 9 of 13 y we sampled (Stone, 2001). Water levels were high in canyon pools (total surface area > 3750 [m.sup.2]) 12 of 13 y we sampled during the wet season (Stone, 2001). Blackwater Hole (maximum surface area = 375 [m.sup.2], maximum depth = 2 m), also underwent seasonal fluctuations in water levels (Stone, 2001). During the dry season, Blackwater Hole was completely dry during at least 4 y from 1994-2008 and reduced to a puddle [less than or equal to] 10 [m.sup.2] during three other years. During the wet season, Blackwater Hole was full during at least 11 y from 1994-2008.

We took advantage of these fluctuating water levels when designing our experiments. We conducted trials in two high risk habitats: shallow canyon pools and shallow stock tanks. Canyon pools were 20-150 cm maximum depth with surface areas ranging from 1-12 [m.sup.2]. Canyon pools had gravel or bedrock substrates that a turtle could not burrow into and lacked deep holes that could provide turtles with refuges from hand sampling. Trials in canyon pools were conducted in Blackwater Canyon, except for two flight response trials (see below) conducted in the nearby Cloverdale Creek drainage. Shallow stock tanks were defined as tanks that were shallow enough for effective sampling by hand. Shallow stock tanks were 20-60 cm maximum depth with surface areas ranging from 10-300 [m.sup.2]. Unlike canyon pools, stock tanks had deep substrates of silt or leaf litter that turtles could easily burrow into. In addition to Blackwater Hole, we conducted trials in two other shallow stock tanks in the Cloverdale Creek drainage, Javalina Tank and Peloncillo Tank. We also conducted experiments in a low risk habitat: deep stock tanks, defined as tanks that were too deep to be effectively sampled by hand. Deep stock tanks were 150-300 cm maximum depth with surface areas ranging from 225-2300 [m.sup.2]. Deep stock tanks included Blackwater Hole and Javalina Tank as well as Buckhorn Tank and State Line Tank.


We used two sampling methods, trapping with hoop nets and hand sampling, to capture turtles. We trapped turtles with hoop nets (variety of hoop sizes but mesh sizes of either 2.5 cm or 3.8 cm) baited with sardines (occasionally scrap meats) in deep stock tanks. We checked nets daily. We used hand sampling in canyon pools and shallow stock tanks. Once captured, mud turtles were processed immediately. New captures were marked with a unique series of notches in the marginal scutes (Cagle, 1939). For all captures, a series of shell measurements including midline carapace length (MCL) were measured to the nearest mm with dial calipers. In addition, sex was determined based upon sexually dimorphic traits and body size (MCL < 86 mm was considered juvenile unless obviously male; Stone, 2001) and locality was recorded from maps of the study area or using a GPS (Garmin eTrex Vista cX). Processing a turtle took about 2 min. We held turtles in buckets or hoop nets until all turtles captured at a given location had been processed. Depending on capture success, this could take a few minutes to over an hour. After processing, we released turtles into the water at the site of capture.


During 2004-2007, we conducted 16 flight response trials in the three aquatic habitats (seven trials in canyon pools, five in shallow tanks, four in deep tanks). Seven trials were conducted in six canyon pools. Two trials conducted on consecutive days in the same pool in Blackwater Canyon were considered independent because none of the same turtles were in the pool on both days. Five trials were conducted in pools in Blackwater Canyon and two were conducted in pools in the Cloverdale Creek drainage. Five trials were conducted in three shallow stock tanks. Peloncillo Tank was used once, whereas Blackwater Hole and Javalina Tank were used for trials twice, in different years. Twelve turtles (8/55 in Blackwater Hole, 4/36 in Javalina Tank) were captured during both trials in the same tank. We only used the first encounter of each turtle in our analysis (see below). Four trials were conducted in four deep stock tanks: Blackwater Hole, Javalina Tank, Buckhorn Tank and State Line Tank.

Flight response trials were divided into disturbance and observation phases. Even though we captured turtles using different methods in shallow and deep habitats, we believe that similarities in the handling process made the level of disturbance comparable in the different habitats and, therefore, made statistical comparisons valid. Regardless of capture method or type of aquatic habitat, the disturbance phase involved humans wading into the aquatic habitat, removing turtles from the water by hand, processing turtles on the shore and releasing turtles together from the shore into shallow water. The observation phase lasted for at least 20 min. If the trial was at a stock tank, 2-4 observers spread out and watched from 10-20 m distance, with at least one person watching the water's edge with binoculars. If the trial was at a canyon pool, a single observer watched from ca. 5-m distance. During the observation period, we tried to remain motionless and quiet; however, we also tried to record the mark of any turtles making terrestrial flight responses, which necessitated moving around near the edge of the water and handling responding turtles again. We tested the prediction that turtles from shallow aquatic habitats were more likely to undergo terrestrial flight responses than turtles from deep aquatic habitats using a 2 x 3 contingency table analysis.


Flight response trials produced direct observations of turtles undergoing terrestrial flight responses. However, non-responders, turtles that did not undergo terrestrial flight responses, could only be documented by inference during the flight response experiment. Multiple sampling trials involved samples at the same site on consecutive days. Multiple samples allowed direct observation of the number of non-responders.

During 1996-2007 we conducted 11 multiple sampling trials in 10 canyon pools, all within Blackwater Canyon. One pool was used in 2004 and 2007. We also conducted three multiple sampling trials in two shallow stock tanks, Blackwater Hole and Javalina Tank. All multiple samples in shallow stock tanks and three multiple samples in canyon pools were conducted in conjunction with the flight response trials. We combined data from the two types of experiment and used a t-test to compare body size (MCL) of responders and nonresponders.



Turtles underwent terrestrial flight responses in four of five trials in shallow tanks and three of seven trials in canyon pools (Table 1). Terrestrial flight responses were not observed in four trials in deep stock tanks (Table 1). Our contingency table analysis supported the prediction that terrestrial flight responses occur more often in shallow water habitats (chi square = 28.2, P < 0.001). Two of the responders from shallow stock tanks were not captured during the disturbance phase of flight response trials. In addition, six of the responders were unmarked when captured during the disturbance phase.

Terrestrial flight responses occurred rapidly with consistent directionality. In shallow stock tanks, all but one responding turtle left the water at the same side of the tank and moved away from the water in the same general direction: up the nearest and steepest slope. Responding turtles did not attempt to return to water when we disturbed them to record their identity but instead withdrew into their shells for some period before resuming the terrestrial flight response.


Multiple sampling of canyon pools revealed a high turnover in pool occupancy from one day to the next. In 11 canyon pools, a total of 17 turtles were caught on the first day of sampling. Of these, only three were recaptured in the same pool on the second day of sampling, meaning 14 of 17 turtles (82.4%) appeared to have left canyon pools between samples. We also identified four turtles that were captured on the second day of sampling but not on the first, apparently after entering a canyon pool overnight. A similar pattern was observed in shallow stock tanks, where our disturbances appeared to lead to nearly complete emigration of turtles (Table 2).

Combining data from canyon pools and shallow tanks, non-responders (n = 17, MCL mean [+ or -] SE = 88.6 [+ or -] 9.60 mm) were significantly smaller than responders (n = 23, MCL = 112.7 [+ or -] 4.06 mm, t = 2.54, P = 0.015). Almost half of non-responders (7/17) were juveniles, whereas all but one responder (22/23) were adults (Fig. 1).


Sonoran mud turtles underwent terrestrial flight responses when disturbed in shallow aquatic habitats. Consistent with one of the core predictions of the risk allocation hypothesis (Lima and Dill, 1990; Lima and Bednekoff, 1999), flight responses were more likely from shallow habitats than deep habitats, suggesting that shallow aquatic habitats were risky and that terrestrial habitats were refuges. We also found that terrestrial flight responses were more likely in larger turtles, suggesting that there may be important ontogenetic changes in habitat use and the factors affecting survival in Sonoran mud turtles.

Terrestrial flight responses appeared to be stereotypical responses to disturbance. The responses occurred quickly, with most turtles moving up the nearest, steepest slope and some turtles moving past plainly visible humans. This behavior is unlikely to be the result of turtles becoming trap shy over the course of our study. Although most responding turtles had been previously marked, unmarked turtles underwent flight responses six times out of 33 observations (18%). Furthermore, the initial observation in May 2000 involved turtles that had minimal previous contact with investigators. In addition, because two of the responders from shallow stock tanks were not captured during the disturbance phase, it appears that disturbance without capture and handling is a sufficient stimulus to invoke a terrestrial flight response.


The aquatic habitats where we observed terrestrial flight responses offered few refuges from predation. These habitats were shallow and small (Table 1), could be sampled by hand from shore and lacked crevices where mud turtles could escape hand sampling. Freshwater turtles in shallow aquatic habitats are vulnerable to a variety of predators (Minckley, 1966; Iverson et al., 1991). During 1994-2008, we found 51 turtle shells in the study area, many with signs of predation (Stone, 2001). These data, coupled with the occurrence of several potential predators in the study area, including coati (Nasua narica), coyote (Canis latrans) and black bear (Ursus americanus), suggest that Sonoran mud turtles are susceptible to predation in the shallow aquatic habitats where we observed terrestrial flight responses (Stone, 2001).

In contrast, the surrounding terrestrial habitat in our study area offered more area with more refuges, away from where predators were most likely to search. Although we did not follow turtles undergoing terrestrial flight responses as they moved away from the water, we assumed they selected terrestrial refuges similar to those selected when turtles were entering terrestrial estivation (Ligon and Stone, 2003; Hall and Steidl, 2007). Based on radiotelemetry data, turtles estivated in shallow forms under soil or vegetation, or in crevices under boulders (Ligon and Stone, 2003; Hall and Steidl, 2007). Estivation sites were located up to 79 m from the canyon bed (Ligon and Stone, 2003). The sheer number of suitable estivation sites within this distance from the canyon bed makes detection of Sonoran mud turtles in terrestrial refuges unlikely.

Terrestrial flight responses occurred more frequently in larger individuals, both in our study and in the Campos et al. (2003) study of caiman (Caiman crocodilus). There are two possible reasons for this pattern. First, rates of water loss are inversely proportional to body size (Schmidt-Nielsen, 1984; Stone and Iverson, 1999; Lehmann et al., 2000). Thus, a physiological constraint, desiccation, might prevent small individuals from using terrestrial habitats as refuges from predation. Second, larger individuals are often easier to detect or preferentially selected by predators (Kotler et al., 1988; De Robertis, 2002; Flinders and Magoulick, 2007). This appears to be true in the shallow aquatic habitats in our study area, where the opportunities for concealment likely increase as body size decreases. Thus, an ecological constraint, predation risk, might limit large turtles from using shallow aquatic habitats for feeding, hydration and mating.

Mud turtles in general are adapted to intermittent aquatic habitats and use terrestrial habitats in a variety of contexts other than nesting. Many mud turtles, including those in our study area, occur in habitats where water is absent for long periods, resulting in forced estivation of entire populations (Semmler, 1979; Ligon and Stone, 2003). In addition, even when water is available, Sonoran mud turtles in our study area exhibit asynchronous aquatic activity, with the majority of individuals absent from aquatic habitats at a given time (Stone, 2001). Asynchronous aquatic activity can perhaps be explained using the same theoretical framework we used to explain terrestrial flight responses. Assuming that aquatic activity is risky when water levels are low, any turtle that has satisfied its aquatic resource requirements and can tolerate the physiological challenges of terrestrial estivation should be risk averse and inactive in terrestrial habitat. The large percentage of our study population that is consistently absent from aquatic habitats (Stone, 2001) may represent turtles that were risk averse at the time of our samples. Conversely, turtles that were captured in aquatic habitats were not risk averse, presumably because they had not satisfied their aquatic resource requirements. Our experimental disturbances appeared to be sufficient to make many of these turtles risk averse, invoking terrestrial flight responses.

Terrestrial flight responses have been reported in three turtle species and one crocodilian (this study; Campos et al., 2003; Metrailler, 2006; Buskirk, 2007). This behavior might be a general strategy for risk aversion in species that utilize shallow aquatic habitats yet have the capacity for terrestrial activity.

Acknowledgments.--We thank K. Brock, N. Calder, M. Cameron, J. Congdon, M. Curtis, R. Hites, M. Jordan, D. Ligon, T. Russell, J. Scheer, R. Spencer, Z. Stone and S. Thomas for assistance with data collection, C. Painter and J. Palumbo for advice about data interpretation, C. Weaver for translating a paper from French, and D. Ligon and C. Perry for recording the initial observation of a terrestrial flight response. We thank J. Congdon, L. Fitzgerald, J. Iverson, M. Jordan, D. Ligon and P. Rosen for reviewing an earlier version of the manuscript. We thank the Gault, Hadley and McDonald families for providing access to their private property or encouraging our activities on their Forest Service leases. Partial funding was provided by the University of Central Oklahoma Office of Research and Grants. This research was conducted under permits issued by the New Mexico Department of Game and Fish (2905) and the U. S. Forest Service (SUP0080-01) and under an IACUC protocol from the University of Central Oklahoma.




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Department of Biology, University of Central Oklahoma, Edmond 73034

(1) Corresponding author: e-mail:

(2) Current address: Department of Biology, Utah State University, Logan 84321
TABLE 1.--Frequency of terrestrial flight responses in Sonoran mud
turtles from three types of aquatic habitat in the Peloncillo
Mountains. The number of trials for each treatment is given in the
first column. The next five columns are means [+ or -] SE (range)

                     Maximum              Surface area
Habitat             depth (cm)            ([m.sup.2])

Canyon pool     44 [+ or -] 18         6.6 [+ or -] 1.6
  (n = 7)         (20-150)               (1-12)
Shallow tank    42 [+ or -] 7          149 [+ or -] 58
  (n = 5)         (20-60)                (10-300)
Deep tank       225 [+ or -] 32        825 [+ or -] 493
  (n = 4)         (200-300)              (225-2300)

                    Individuals               Flight
Habitat               captured              responses

Canyon pool     1.9 [+ or -] 0.4       0.71 [+ or -] 0.42
  (n = 7)         (1-3)                  (0-3)
Shallow tank    19.2 [+ or -] 6.5      4.4 [+ or -] 1.7
  (n = 5)         (5-40)                 (0-10)
Deep tank       22.5 [+ or -] 16.4     0
  (n = 4)         (1-71)

Habitat              responding

Canyon pool     0.33 [+ or -] 0.18
  (n = 7)         (0-1)
Shallow tank    0.22 [+ or -] 0.08
  (n = 5)         (0-0.43)
Deep tank       0
  (n = 4)

TABLE 2.--Overnight changes in capture frequency of Sonoran mud
turtles from shallow stock tanks  in the Peloncillo Mountains. Non-
responders were turtles captured on multiple days in the same tank

Habitat            Date      Captures 1st clay     Captures 2nd day

Javalina Tank      May-06             9                    3
Blackwater Hole    May-06            14                   10
Blackwater Hole    Jul-07            40                    3
Total                                63                   16

Habitat             Captures 3rd day      Non-Responder

Javalina Tank              --                   1
Blackwater Hole            1                    3
Blackwater Hole            6                    8
Total                      7                   12
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Author:Stone, Paul A.; Stone, Marie E.B.; Stanila, Brian D.; Locey, Kenneth J.
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1USA
Date:Jan 1, 2011
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