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Journal of Mammalogy, 92(2):444–451, 2011

Sex differences in the locomotor ecology of a gliding , the Malayan (Galeopterus variegatus)

GREG BYRNES,* NORMAN T.-L. LIM,CHARLENE YEONG, AND ANDREW J. SPENCE Department of Integrative Biology, University of California, Berkeley, 3060 Valley Life Sciences Building, Berkeley, CA 94720-3140, USA (GB) Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Singapore

(NT-LL) Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 Wildlife Reserves Singapore, 80 Mandai Lake Road, Singapore 729826, Singapore (CY) Structure and Motion Laboratory, Royal Veterinary College, Hawkshead Lane, North Mymms, Hertfordshire AL9 7TA, United Kingdom (AJS) * Correspondent: [email protected]

Fundamental differences could exist in the fitness-limiting resources between males and females; therefore, movement strategies might differ between the sexes. We used custom-designed -borne data loggers to record the locomotor behaviors of free-ranging Malayan (Galeopterus variegatus). Locomotor behavior, and especially gliding, make up a very small percentage of a colugo’s time budget. Furthermore, although glide distance is widely variable, most glides are much shorter than the maximum distance achievable. Males perform more glides and travel a greater distance each night than females. Females glide primarily to access foraging trees, but the greater distance traveled by males is from visiting trees to feed and transiting quickly among trees for other behaviors that include territorial defense and mate searching. This study recorded all locomotor behaviors for each animal during the sampling period and provides a starting point for the evaluation of hypotheses for the evolution of gliding and examining the differential effects of selective pressures between the sexes. The evidence suggests that ability to forage in a number of trees each night is an important aspect of the locomotor ecology of colugos and therefore could have played a role in the origins of gliding.

Key words: accelerometer, arboreal mammal, biologging, colugo, locomotion E 2011 American Society of Mammalogists DOI: 10.1644/10-MAMM-A-048.1

The locomotor behavior and performance of an animal are be tested, have been proposed for the origins of gliding flight. fundamental to all aspects of its biology. Over short time might leap or glide between trees to avoid predators intervals locomotor performance affects the ability of an (Emmons and Gentry 1983; Keith et al. 2000), increase organism to locate and capture food resources, find and locomotor or foraging efficiency (Dial 2003; Norberg 1983; compete for mates, and avoid the perils of life. Locomotor Scheibe and Robins 1998; Scheibe et al. 2006; Scholey 1986), performance ultimately plays a role in larger-scale processes, cope with a specific habitat structure (Dial et al. 2004; Dudley contributing to the patterns of diversity of life through time and DeVries 1990; Emmons and Gentry 1983), or reduce the (Nathan et al. 2008). forces associated with landing (Byrnes et al. 2008; Paskins et Selection pressures acting on locomotor repertoire can al. 2007). However, to gain insight into the selective forces result in the evolution of novel modes of locomotion. that might have shaped the ability to glide, detailed study of Although some locomotor transitions have occurred in only the locomotor behavior of free-ranging gliding animals is a few cases, such as the independent origins of flapping flight necessary. in birds, , pterosaurs, and insects, others have occurred numerous times. Gliding, for example, has evolved indepen- dently at least 30 times in and is likely to be included in the locomotor repertoire of most arboreal organisms (Dudley et al. 2007). Several hypotheses, yet to www.mammalogy.org 444 April 2011 BYRNES ET AL.—LOCOMOTOR ECOLOGY OF A GLIDING MAMMAL 445

In addition to extrinsic selective factors such as predation sexes. We also consider these data in light of previous that influence all members of a species, intrinsic factors, such hypotheses about the origins of gliding. as sex, might play a role in the locomotor behavior at the individual level. Fundamental differences between males and females in fitness-limiting resources could exist, resulting in MATERIALS AND METHODS divergent ecology (Clutton-Brock et al. 1982; Koprowski Animal protocol.—Thirteen wild colugos (G. variegatus) 1998; Koprowski and Corse 2005; Trivers 1972; Williams were captured in Singapore during the course of this study. 1980). For example, although the energetic cost of rearing Individuals of mass ,700 g (i.e., logger mass .4% body young might limit the fitness of females, male fitness often is mass), pregnant females, or those carrying young were based solely on the number of acquired mates (Gittleman and released immediately upon capture and were not used in the

Thompson 1988; Trivers 1972). Therefore, movement strate- study. Six animals were fitted with custom-designed data Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 gies used to maximize fitness might differ between the sexes. loggers; data were retrieved from 5 individuals (3 males and 2 Fokidis and Risch (2008) found that female gliding females), and 1 data logger failed after attachment. Additional have smaller litters of relatively larger young compared to details of animal capture and handling can be found in Byrnes nongliding species, indicating increased maternal investment et al. (2008). Data were obtained from individuals with body in individual offspring. This finding suggests that sex masses between 750 g and 1.4 kg ( 5 1.1 kg) and with head– differences in locomotor ecology might be particularly body lengths ranging from 31 to 40 cm. extreme in gliders. After release at the site of capture, each animal was Evidence from radiotelemetry shows that home-range sizes observed until it glided out of sight to ensure normal behavior. differ between the sexes across a wide range of mammalian Animals immediately climbed and then rested or groomed for species, with males often having larger home ranges (Hanski several minutes before gliding 1 or more times. The horizontal et al. 2000; Harestad and Bunnel 1979). Recently, new tools to distance of these initial glides was measured using a laser examine movement patterns at a finer scale have been range-finder (Nikon ProStaff Laser 440; Nikon Inc., Melville, developed, including data-logging and transmitting devices New York). All animal capture and handling procedures that collect a variety of data on animal movement. Both time- followed guidelines approved by the American Society of depth recorders (Baird et al. 2005; Beck et al. 2003) and global Mammalogists (Gannon et al. 2007) and were approved by the positioning systems (Rose et al. 2006) have been used to University of California, Berkeley Animal Care and Use examine sex-specific differences in the foraging behavior of Committee (protocol R282-0405). free-ranging animals. Because of potential problems of using Using the data on glide lengths and durations of the global positioning systems under the forest canopy, we used observed glides recorded from the accelerometer, we derived animal-borne inertial sensors (e.g., Byrnes et al. 2008; Sato et the average horizontal velocity of the initial glide(s) for each al. 2007) to examine locomotor patterns in colugos. animal. Like any body accelerating under gravity, a gliding This study examines locomotor behavior of the Malayan animal should reach a terminal (equilibrium) velocity. Given colugo (Galeopterus variegatus). Colugos are large (.1 kg) this and the average takeoff velocity of gliding colugos gliding mammals that inhabit peninsular Southeast Asia and (Byrnes et al. 2008), we estimated the average velocity (U)of the Indonesian Archipelago (Corbet and Hill 1992; Ruggeri subsequent glides by fitting a sigmoidal curve given by the and Etterson 1998). Unlike many other gliding mammals that equation below to the observed data on glide velocity and frequently move or forage on the ground, colugos are arboreal duration (Fig. 1). The average velocity of each glide was specialists that rarely descend to the forest floor (G. Byrnes, multiplied by its duration recorded from the accelerometers to pers. obs.; Lekagul and McNeely 1988). Furthermore, they are estimate glide distance, using: almost exclusively folivorous, although they occasionally feed : ~ z 6 41 on other plant matter such as flower buds (Lim 1967; U 3:7 { t{1:75 : z ({0:165) Wischusen and Richmond 1998). Little is known about the 1 e social behavior of colugos; however, anecdotal reports of aggression between males (Wharton 1950; Wischusen et al. Accelerometry data loggers.—The custom-designed accel- 1992) suggest that males defend territories. The morphology erometry data loggers used in this study are described in detail of the vomeronasal organ suggests that scent marking also elsewhere (Byrnes et al. 2008). They included 3-axis might play an important role in the ecology of these animals accelerometers that logged to flash memory at 100 Hz and (Bhatnagar and Wible 1994), but no systematic study of can record 3-dimensional accelerations for up to 304 h at that colugo locomotor ecology has been conducted, and it remains sampling rate. Data-logger dimensions, including the battery, unclear if their unique locomotor mode affects these aspects of were 11 3 32 3 45 mm and weighed 29 g. Females carrying their ecology or even if locomotor ecology differs between the young weighing 400 g have been observed gliding (G. sexes. Therefore, our primary objective was to describe the Byrnes, pers. obs.). Thus, it is unlikely that weight of the data time budgets and patterns of locomotor behavior of the logger unduly influenced the natural behavior of an individual. Malayan colugo and to use those data to assess potential A radiofrequency telemetry tag (A2470; ATS, Isanti, Minne- differences in selective constraints on locomotion between the sota) also was incorporated into the data logger. Between dusk 446 JOURNAL OF MAMMALOGY Vol. 92, No. 2

and thereafter dropped off as the cyanoacrylate glue failed naturally. Data processing and analysis.—Upon recovery of the data loggers, data were downloaded to a computer using custom software written in Matlab version 7.3 (The Mathworks Inc., Natick, Massachusetts). Each device was calibrated by rotating the device through 360u about each axis and comparing the voltage output to the known magnitude and direction of gravitational acceleration. Then the calibration was applied to the recorded voltage output of the accelerom-

eters to transform the data to units of gravitational acceleration Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 (g). We used a Matlab script to identify the timing and sequence of individual behavioral bouts. Four distinct behavioral classes were identified: rest, forage, climb, and FIG.1.—Relationship between glide duration and velocity for glide (Fig. 2). Behaviors that could not be positively identified observed glides of 5 Malayan colugos. The sigmoidal curve fit to were coded as ‘‘other’’; these behaviors made up ,5% of the these points was used to estimate the glide velocity for all unobserved overall activity. To examine differences between males and 2 glides (F3,15 5 147.97, P , 0.0001; r 5 0.99). The y-intercept females in locomotor behavior we compared differences in represents the average takeoff velocity (3.7 m/s) for colugos from glide distance, glides per night, and nightly transit distance Byrnes et al. (2008). using mixed-model regression to control for the effects of body mass and individual identity. We also compared the and dawn animals were located visually using the radiosignal shape of the frequency distributions of glides for male and each hour. The radiofrequency tag also facilitated the recovery females using a Kolmogorov–Smirnov (D) test. Time budgets of the data loggers after dropping off each animal. Data were calculated by summing the time intervals for each loggers remained on the animals for between 1 and 6 weeks behavioral class and dividing by the total observed time for

FIG.2.—Example acceleration (g) profiles for 4 distinct behaviors of Malayan colugos: a) climbing, b) foraging, c) gliding, and d) resting. Each panel shows acceleration along each of the 3 body axes. The 3 axes are defined as follows: Xb is along the craniocaudal axis, Yb is along the mediolateral axis, and Zb is along the dorsoventral axis. Note the differences in timescale for each behavior. April 2011 BYRNES ET AL.—LOCOMOTOR ECOLOGY OF A GLIDING MAMMAL 447

TABLE 1.—Transition matrix for behaviors for male and female RESULTS Malayan colugos (Galeopterus variegatus). The of transitions is A total of 430 h of data at 100 Hz was collected from the 5 read within each row. Numbers in boldface type represent transitions that are different (P , 0.05) between the 2 sexes. animals from June to August 2006 and June to August 2007 ( 5 86 h, range 5 48–154 h/animal). Animals were active Climb Forage Glide Other Rest Total primarily between sunset and sunrise (Fig. 3). During the Males sampling period a total of 267 glides was recorded. Glide Climb 0 98 123 29 25 275 duration varied between 0.64 s and 15.14 s ( 5 3.48 s, SD 5 Forage 46 0 72 5 28 151 2.10 s). Glide 173 9 1 19 6 208 Time budgets.—Malayan colugos of both sexes spent the Other 37 11 3 0 11 62 majority of each day resting, with males and females inactive

Rest 25 32 3 10 0 70 Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 for 68.9% and 69.2% of the day, respectively. Foraging also Females constituted a large proportion of the daily time budget for both Climb 0 92 34 13 22 161 males (25.9 ) and females (25.7 ). In contrast, locomotor Forage 65 0 29 8 36 138 % % Glide 58 3 0 2 8 71 behaviors, including climbing and gliding, made up a very Other 20 1 4 0 3 28 small proportion of time. Males and females spent 0.6% and Rest 18 34 6 5 0 63 0.5% of the day climbing, respectively. Similarly, both males and females spent only 0.1% of time gliding. Other behaviors, each animal. Proportion of time animals exhibited each including grooming, scent marking, and defecating were behavior was compared between the sexes with Mann– indistinguishable in the accelerometry traces but made up only Whitney (W) tests. We also compared the sequence of a small portion of the daily activity budget, collectively 4.5% behavioral bouts using chi-square (x2) tests between the and 4.6% for males and females, respectively. No sex sexes. Specifically, behaviors immediately following the differences were found in the proportion of time spent climbing of a tree were compared to determine if an individual climbing (W 5 3.0, n 5 2, 3, P 5 0.083), foraging (W 5 visited a tree to forage or if they immediately glided to a 8.0, n 5 2, 3, P 5 0.564), gliding (W 5 3.0, n 5 2, 3, P 5 successive tree. To do this a transition matrix for a continuous 0.083), resting (W 5 5.0, n 5 2, 3, P 5 0.564), or engaged in ethogram (Table 1) was constructed from the acceleration other behaviors (W 5 8.0, n 5 2, 3, P 5 0.564). data. To determine the possible motivation for individual Gliding behavior.—Based on the distance of observed glides glides the transitions after animals climbed trees were from each individual colugo, the distance of all subsequent examined using a chi-square (x2) analysis. Because of the glides was estimated by fitting a line to the observed data on intermittent nature of climbing locomotion, any period of rest glide distance and duration from the accelerometry traces. ,20 min was omitted from the sequence of behaviors. Resulting estimates of glide distances from glide durations Statistical analyses were conducted using SPSS version 14 ranged from 1 m to 145 m for all animals ( 5 31.4 m, SD 5 (SPSS Inc., Chicago, Illinois). 24.7 m). Mean distances for males and females were 31.1 m (SD

FIG.3.—Activity pattern of a female Malayan colugo over 6 days. Dark bar represents nighttime hours. Each row represents 24 h. The height of the bar represents each specific behavior. In the long periods with no vertical excursion the animal is resting, the 1st level of excursion is ‘‘other’’ unidentified behaviors, the 2nd level is foraging, the 3rd level is climbs, and the highest level is glides. 448 JOURNAL OF MAMMALOGY Vol. 92, No. 2

The number of glides per night also was determined from the logged accelerometer data. The number of glides varied between 4 and 32 per night for all animals ( 5 13.5, SD 5 8.1; Fig. 4b). Males glided on average 18.2 (SD 5 8.5) times per night, whereas females glided only 8.9 (SD 5 4.3) times per night. After controlling for individual identity and body mass, we found that males glided significantly more often each night than did females (F1,17 5 5.307, P , 0.05). However, body mass was not significantly associated with the number of glides made by an individual (F3,17 5 0.511, P 5 0.49).

For each night of sampling the total horizontal distance Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 traveled was calculated by summing the glide distances for that night. This nightly transit distance ranged from 94 m to 1,410 m ( 5 409.5 m, SD 5 308.5 m) for all animals (Fig. 4c). The mean distance traveled per night by males was 542.7 m (SD 5 267.1 m). Females traveled a shorter distance each night ( 5 359.0 m, SD 5 105.9 m). After controlling for both body mass and individual identity, we found that sex was a significant predictor of nightly transit distance (F1,17 5 13.925, P , 0.005). Furthermore, after we accounted for the effects of sex, body mass also was significantly associated with nightly transit distance (F3,17 5 6.858, P 5 0.018), with larger animals traveling longer distances each night. Sequence of behaviors.—A transition matrix (Table 1) was constructed for the 5 behavioral classes: climb, forage, glide, other, and rest. Colugos normally (83%) climbed the landing tree shortly after gliding to it. We examined frequencies in the transition from climb to either forage or glide and subse- quently explored sex differences in these frequencies. Overall, colugos transitioned to foraging 190 times and to gliding 157 times (44% and 36%, respectively) after climbing from a total of 436 transitions. Males exhibited climb-to-forage transitions 98 times and climb-to-glide transitions 123 times (36% and 45%, respectively) from a total of 275 transitions. In females climb-to-forage transitions were observed 92 times and climb- to-glide transitions 34 times (57% and 21%, respectively) from a total of 161 transitions. Males glided multiple times in succession without foraging significantly more often than did 2 females (x 16 5 26.63, P , 0.001).

DISCUSSION We examined the locomotor behavior of free-ranging

FIG.4.—Distribution of a) glide lengths for Malayan colugos, b) colugos using 3-dimensional accelerometry. We observed numbers of glides per night for individual colugos, and c) total transit glides covering distances ranging over 100-fold (approximate- distance per night for individual colugos. Dark bars represent males ly 1 m to 150 m), consistent with previously reported (n 5 3) and light bars represent females (n 5 2). In b) and c) an distributions of glide lengths for other large gliders, including animal-night refers to a single night for a single individual, the sum of the Philippine flying (Cynocephalus volans—Wischu- which equals the total number of nights sampled for all individuals. sen 1990) and giant flying squirrels (Petaurista—Ando and Shiraishi 1993; Scholey 1986), suggesting that colugos glide 5 24.4 m) and 32.3 m (SD 5 25.8 m), respectively (Fig. 4a). under similar circumstances to other large gliders. Further, by Mean glide distance did not differ between the sexes (F1,264 5 collecting a continuous record of all behaviors we observed 0.062, P 5 0.84) or vary with body mass (F3,264 5 0.901, P 5 the natural variation of locomotion and determined funda- 0.49). In addition, the cumulative frequency distributions for mental differences between the sexes in locomotor behavior. males and females did not significantly differ in shape (D 5 Time budgets constructed from the accelerometry data 0.086, n 5 71, 196, P 5 0.82). revealed, most notably, that animals spent very little time April 2011 BYRNES ET AL.—LOCOMOTOR ECOLOGY OF A GLIDING MAMMAL 449 engaging in locomotor behaviors, consistent with data from visited trees. This suggests a fundamental difference between other gliding folivores and exudivores. For example, the the sexes in the motivation to glide. Males often glide to trees greater glider (Petauroides volans) spends approximately 6% just as transit points, climbing only to immediately glide again of daily time in locomotor activities (Comport et al. 1996). (45%), suggesting they are engaging in other activities that Similarly, the yellow-bellied glider (Petaurus australis) could include searching for mates and chasing other males. spends minimal time climbing (3%) and gliding (0.3%— These quantitative data support previous, limited observations Goldingay 1989). Furthermore, colugos spend most of their on the mating system of colugos (Wharton 1950; Wischusen et active period foraging, consistent with other gliders (Comport al. 1992) that have suggested that males likely hold and defend et al. 1996; Goldingay 1989). However, we found no territories. More important, it suggests that males and females differences in the time budgets between the sexes. To our use different locomotor strategies to increase fitness. knowledge, this is the 1st study to examine sex differences in Despite possible differences between the sexes in the Downloaded from https://academic.oup.com/jmammal/article/92/2/444/869618 by guest on 29 September 2021 the time budgets of a gliding animal. motivation to glide, both sexes visited on average 5 foraging Because using data loggers ensured that we recorded every trees each night. Furthermore, they each foraged for glide during the sampling period for each individual, we were equivalent periods of time. This suggests that males and able to examine differences in the gliding behavior between females forage in the same ways, possibly visiting multiple the sexes. Colugos are sexually dimorphic in body size, with trees to feed on a variety of forage. However, females females in this study being on average 30% larger than males. concentrate their active time on foraging and acquiring Biomechanics theory (Norberg 1990) suggests that as a result resources, and males appear to expend resources on additional of smaller body size, males will have improved locomotor activities that can include searching for mates or defending performance. However, the average length of glides did not territories. differ between males and females. Thus, the biomechanical In addition to identifying differences in the locomotor effects of body size alone do not play a large role in the ecology between the sexes, we observed similarities in selection of glide paths in colugos. Consistent with this, locomotor behavior between the sexes that also can provide Byrnes et al. (2008) showed that during gliding colugos insights into the origins of gliding. Although not directly generate more force than required to offset body weight, related to each of the hypotheses for the evolution of gliding, suggesting that predictions of glide performance based solely our data are most consistent with the foraging efficiency on steady-state aerodynamics should be evaluated with hypothesis (Goldingay 2000). Despite traveling long distances caution. In addition, female southern flying squirrels (Glau- each night, colugos spend only minutes each day moving comys volans) have longer limbs (Robins et al. 2000) and between foraging patches. Time itself can be a valuable lower wing loading (Fokidis and Risch 2008) than males. If currency that shapes behavior (Dunbar 1992; Dunbar and colugos exhibit similar differences in body shape, the negative Dunbar 1988), and by gliding, colugos, like other gliders effects of body size on performance also could be offset. (Comport et al. 1996; Goldingay 1989; Scheibe et al. 2006), Male colugos glided approximately twice as often each minimize time spent for locomotion. In turn, time spent night as did females. Furthermore, average nightly transit acquiring resources and the rate at which resources can be distance was greater in males than females. In addition, larger acquired could be maximized (Charnov 1976). animals of both sexes traveled greater distances each night. In contrast, our data and observations do not support the Reproductive success in males is likely a consequence of notion that gliding is used commonly as a means of escape access to mates, and increased movement (both number of from predators. The strong temporal relationship between glides and total distance) per night might increase encounters locomotor and foraging behaviors and reliance on crypsis to with females. However, increased gliding also might elevate avoid predators (G. Byrnes, pers. obs.; Lim 2007) both risks, including injury or contact with predators. The major suggest that gliding is not used to flee from predators. predator of the closely related is However, Byrnes et al. (2008) reported that colugos landed believed to be the (Pithecophaga jefferyi), on the ground in only 4 of 222 glides; therefore, the arboreal with the lemur making up more than half of the eagle’s diet lifestyle of these animals alone intrinsically could reduce (Kennedy 1985). Colugos appear to avoid predation mainly by encounter rates with terrestrial predators (Emmons and crypsis (G. Byrnes, pers. obs.; Lim 2007), so gliding more Gentry 1983). frequently might significantly increase predation risk, partic- Specific predictions can be made to test each of the ularly by aerial predators. proposed hypotheses for the evolution of gliding, as discussed To gain a more complete understanding of the locomotor in Paskins et al. (2007). Animal-borne data loggers allow for ecology of an organism the internal state of the individual that the collection of the types and quantity of data required to test determines why it moves also must be accounted for (Nathan these predictions. Therefore, combining a framework of et al. 2008). From observation of the animal’s sequence of predictions with the long-term collection of both behavioral discrete behaviors we revealed that females glide primarily to and biomechanical data in a natural context can contribute to visit foraging trees, with females immediately climbing to the our understanding of not only the natural history of gliding canopy and foraging in 60% of trees visited. Conversely, mammals but also the selective forces that have influenced the males immediately climbed and began foraging in just 36% of evolution of gliding. 450 JOURNAL OF MAMMALOGY Vol. 92, No. 2

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