Save

Spatial ecology of a small arboreal ambush predator, Trimeresurus macrops Kramer, 1977, in Northeast Thailand

In: Amphibia-Reptilia
Authors:
Colin StrineSchool of Biology, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Search for other papers by Colin Strine in
Current site
Google Scholar
PubMed
Close
,
Inês SilvaConservation Ecology Program, King Mongkut’s University of Technology Thonburi, Bangkok, Thailand

Search for other papers by Inês Silva in
Current site
Google Scholar
PubMed
Close
,
Curt H. BarnesSchool of Biology, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Search for other papers by Curt H. Barnes in
Current site
Google Scholar
PubMed
Close
,
Benjamin M. MarshallSakaerat Environmental Research Station, Nakhon Ratchasima, Thailand

Search for other papers by Benjamin M. Marshall in
Current site
Google Scholar
PubMed
Close
,
Taksin ArtchawakomSakaerat Environmental Research Station, Nakhon Ratchasima, Thailand

Search for other papers by Taksin Artchawakom in
Current site
Google Scholar
PubMed
Close
,
Jacques HillDepartment of Biological Science, University of Arkansas, Fayetteville, AR, USA

Search for other papers by Jacques Hill in
Current site
Google Scholar
PubMed
Close
, and
Pongthep SuwanwareeSchool of Biology, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Search for other papers by Pongthep Suwanwaree in
Current site
Google Scholar
PubMed
Close
View More View Less
Full Access

Abstract

The Big-Eyed Green Pit Viper (Trimeresurus macrops; Kramer, 1977) is a venomous snake species endemic to Southeast Asia. Although we have some knowledge of the systematics and toxicology of T. macrops, little is known about the spatial ecology of this species. From May 2013 to February 2014, we used radio-telemetry to determine home-range sizes of 13 adult female T. macrops inhabiting the Sakaerat Biosphere Reserve in Northeast Thailand. We found that individual home ranges for T. macrops averaged 0.175 ha, with activity areas ranging from 0.112-0.303 ha and core areas ranging from 0.023-0.052 ha. There was little overlap between conspecific tracked females, especially for the most used areas of their home ranges. We find that T. macrops ambushes more in higher humidity and expresses very little diurnal activity. They use the groundstory for ambushing, then retreat over small distances to higher refuge during the day. Future studies should focus on prey abundance, habitat selection, and survival rates.

Abstract

The Big-Eyed Green Pit Viper (Trimeresurus macrops; Kramer, 1977) is a venomous snake species endemic to Southeast Asia. Although we have some knowledge of the systematics and toxicology of T. macrops, little is known about the spatial ecology of this species. From May 2013 to February 2014, we used radio-telemetry to determine home-range sizes of 13 adult female T. macrops inhabiting the Sakaerat Biosphere Reserve in Northeast Thailand. We found that individual home ranges for T. macrops averaged 0.175 ha, with activity areas ranging from 0.112-0.303 ha and core areas ranging from 0.023-0.052 ha. There was little overlap between conspecific tracked females, especially for the most used areas of their home ranges. We find that T. macrops ambushes more in higher humidity and expresses very little diurnal activity. They use the groundstory for ambushing, then retreat over small distances to higher refuge during the day. Future studies should focus on prey abundance, habitat selection, and survival rates.

Introduction

Snakes play an important ecological role in many ecosystems, both as predators and prey for many other species (Luiselli, 2006; Wilson and Winne, 2016), and their life history is directly connected to both activity and movement patterns. Due to their lack of territorial and strong social behaviour, space use by snakes is mostly related to resource distribution and their ability to reproduce, grow, and acquire food and shelter sites (Wasko and Sasa, 2012). Nonetheless, the secretive nature and low detection rates of most snake species limits our ability to study their spatial ecology (Steen, 2010; Guillera-Arroita, 2017). Knowledge of movement patterns, activity patterns, and home ranges is vital for conservation and effective wildlife management programs (Berger-Tal et al., 2011; Fryxell, Sinclair and Caughley, 2014; Maritz et al., 2016). Members of the Trimeresurus are amongst some of the most ecologically distinct and vulnerable viper species in the world (Maritz et al., 2016).

Trimeresurus macrops, from the family Viperidae and subfamily Crotalinae, is one of the most common Green Pit Vipers in central and northern Thailand, Cambodia and Laos (Stuart, Chan-Ard and Thy, 2012). This species is arboreal and nocturnal, setting up ambush sites at dusk and moving to shelter sites near dawn (Chanhome et al., 2011). No previous studies on prey selection exist for wild T. macrops, but it is likely that it feeds opportunistically on a wide variety of prey items, such as amphibians, reptiles, and small mammals (Chanhome et al., 2011). Trimeresurus stejnegeri (Schmidt, 1925; or Trimeresurus vogeli, depending on the author) another south east Asian pit viper species of similar size and body structure, preys primarily upon amphibians, but can also eat reptiles, mammals, and insects (Creer et al., 2002).

Trimeresurus macrops exhibits cryptic behaviour, sexual dimorphism, and considerable geographic variation in morphological characters (Malhotra et al., 2011; Strine et al., 2015). Although T. macrops is responsible for many human envenomations in Thailand (Hutton et al., 1990), very little information is known on the ecology of this species.

In this study, we investigated movement patterns and behaviours of T. macrops using radio-telemetry, specifically addressing the following objectives: (1) quantifying home-range sizes and (2) determine what environmental conditions affect their behaviour.

Methods

Study site

We conducted fieldwork in the core area of Sakaerat Biosphere Reserve (SBR), located in Nakhon Ratchasima Province, Thailand (14.44-14.55°N, 101.88-101.95°E). The core area of SBR is approximately 8200 ha and consists of patchy matrix of primary and secondary forest types. Within the core area, we tracked green pit vipers at the Sakaerat Environment Research Station (SERS) which includes staff offices and student dormitories, and is visited by over 17,000 school children every year. The field station represents less than 1% of the core area, and is surrounded by mixed disturbed forest with reduced canopy cover, relatively sparse vegetation and little ground cover when compared with primary forest types.

For our low disturbance study areas, outside of the main human disturbed area, we selected two water-associated areas in Dry Evergreen Forest (DEF, henceforth “forest”), a closed canopy multi-story forest dominated by robust evergreen tree species (such as Hopea adorata and H. ferria).

Data collection

We captured T. macrops through a variety of methods including actively searching for animals, and opportunistically encountering individuals in the field. After capture and prior to any measurements, we anesthetized all snakes with vaporized isoflurane, as it is less stressful for the animals and leads to more accurate measurements than traditional squeeze box methods, which require holding the snake immobile for the duration of measurement (Setser, 2007). Mass, length, and sex (cloacal probing, Schaefer, 1934) were determined for all individuals. Only adults of appropriate size were surgically implanted with 1.2 g or 1.8 g temperature-sensitive radio-transmitters (model BD-2T, Holohil Inc., Ontario, Canada), ensuring the transmitter mass was no greater than 5% of the snakes’ mass (3.4 ± 0.6%). We report only female radiotracked individuals in this paper, as we did not obtain a sufficient number of males of adequate sizes for radiotelemetry activities.

We located each individual at least once every two days between May 2013 to February 2014 which allowed investigation of two seasons; cold (November to January; ambient temperature 22.51 ± 4.18°C; ambient humidity 83.97 ± 12.61%) and dry (January to February; ambient temperature 22.78 ± 3.74°C; ambient humidity 68.88 ± 15.48%) seasons. When possible, we included both day time and night time observations. For each observation attempt (fix), we recorded if the snake was visible and noted the individual’s habitat (e.g. forest layer, perch type) and behaviour, while non-visible individuals were located using triangulation. For each relocation greater than 1 m, we collected or calculated the coordinates as Universal Transverse Mercator (UTM) using hand-held Garmin GPS units. For each snake, we determined its mean (total distance/relocations) and maximum distance moved from straight-line distances between subsequent relocations, and mean daily displacement (MDD) as the total distance moved divided by number of days tracked.

We classified forest layers as underground (< 0 m) on ground (0 m), groundstory (>0-1 m), understory (1-3 m), midstory (3-10 m), and abovestory (>10 m). When we were able to visually determine snakes were underground, including when we searched holes (in the ground, tree hollows and rocks), with headlights to confirm snake presence, they were all categorized as sheltering/resting. Principle behaviour was usually one of four categories: “ambush” (lying coiled and alert with the head raised in a ready-to-strike position), “resting” (coiled up but with its head resting on one of its coils or perch), “sheltering” (not visible but known to be underground or completely within shelter site, such as fallen logs or termite mounds), and “moving”. We identified individuals as stationary if they remained in the same shelter or perch site with only minimal body position readjustments between fixes (e.g. shifting head location from on a coil to an ambush position). We measured temperature (°C) and relative humidity (%) at ground level and ambient level (≈1.5 m above ground), both randomly from around 2-3 m from the snake’s location.

Statistical analyses

We estimated body condition using scaled mass index (SMI; Peig and Green, 2009) based on previously collected T. macrops data at SBR (Strine et al., 2015), as it can be readily compared across populations (Labocha, Schutz and Hayes, 2014). We tested the assumptions of homogeneity of variances and normality for each variable. We used a Student’s t-test to compare body condition and body length between highly disturbed (field station) and low impact (forest) study areas, a Mann-Whitney U test to compare MDD, average distance and maximum distance moved and a Wilcoxon test to compare body weights before and during tracking.

We estimated home-range size for each individual using 100% Minimum Convex Polygons (MCP) and fixed-kernel density methods (FK; Worton, 1989), enabling comparisons with previous studies. For the kernel estimates, we used the least-squares cross-validation method to select the smoothing parameter h, obtaining fixed 95% (activity range) and 50% (core area) utilization distributions for each individual (Tiebout and Cary, 1987). Although the accuracy of both MCP and kernel methods has been questioned (Row and Blouin-Demers, 2006), we have included them for comparative purposes with previous studies. All estimated home-range sizes were calculated in hectares (ha). We tested for overall differences in home-range size (MCP, 95% and 50% FK) using ANCOVA. This analysis allowed us to include the number of days each individual was tracked as a covariate, as it was positively correlated with bigger FK areas (Pearson’s r: P < 0.05).

We initially quantified spatial overlap as the MCP area shared between individuals. However, as this home range overlap includes unused areas (and as such is a poor indicator of interaction), we also assessed spatial overlap using the utilization overlap index (UDOI; Fieberg and Kochanny, 2005) of both 50% and 95% fixed-kernels. This index equals 0 for two non-overlapping home ranges and 1 for complete overlap.

We used generalized linear mixed models (GLMM) with binomial distribution to evaluate potential behaviour patterns, selecting snake ID as the random variable (to account for non-independence of locations for each individual) and principle behaviour as the binomial response variable. We considered habitat (highly disturbed versus low impact areas), forest layer and time (night versus daytime) as predictor variables. We also used GLMMs to reveal differences in microhabitat selection between habitats, using temperature and humidity at substrate as well as ambient levels for another set of predictors. Top models were selected by Akaike information criterion (AIC) corrected for small samples sizes (AICc), using R package AICcmodavg (Mazerolle, 2011). To validate each model, we used marginal R2 (mR2) and conditional R2 (cR2; Nakagawa and Schielzeth, 2013). These R2 values can be interpreted respectively as the variance explained by only fixed effects and the variance explained by both the fixed and random effects.

We analysed movement data using Geographic Information System (GIS) software (ArcGIS 10.1; ESRI, 2011) and R statistical software version 3.0.2 (R Development Team, 2013). Unless otherwise stated, all descriptive statistics are reported as means ± standard error and the significance threshold was set at α < 0.05.

Results

General observations

We report data from 13 adult female T. macrops, with a mean total body length of 64.8 ± 5.6 cm (range: 53.9-74.1 cm), mean snout to vent length (SVL) of 55.7 ± 7.5 cm (range: 46.0-67.0 cm) and 54.2 ± 11.0 g body weight (range: 39.2-81.8 g ) on the last recapture (table 1). This compares to a mean body weight of 57.5 ± 19.2 g (range: 33.49- 98.05) prior to implantation, a not significant change in body weight (Wilcoxon V= 22, P = 0.365).

Table 1.
Table 1.

Attributes of the tracked snakes. Snake ID, days tracked, telemetry fixes, date of first fix, date of final fix, biometrics for the last recapture of each study individual, and home-range estimates. Total body length (TBL), scaled mass index (SMI), 100% minimum convex polygons (MCP), 50% kernel core areas (FK50) and 95% kernel activity areas (FK95).

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

On average, we tracked snakes for 73.6 ± 26.9 days (range: 23-122, table 1), during which we recorded 13.6 ± 8.6 relocations. These movements tended to occur every 4.6 ± 1.9 days and forest snakes tended to move more frequently, but not significantly so (station: 5.1 ± 2.6 days; forest: 4.2 ± 0.8 days; Mann-Whitney U = 18.0, P = 0.731). Twenty-one days was the maximum time recorded between relocations, during which only minimal body position readjustments were observed. We were able to visually detect individuals on 564 of 819 (68.9%) observation attempts, on 3.99% of which we observed movement at the same location (movements <1 m not constituting a relocation), 24.09% sheltering, 33.33% ambushing and 38.56% resting outside.

Movement patterns of station and forest individuals did not differ significantly, either for mean distance between two subsequent relocations (ANCOVA: F 1 , 10 = 1.687, P = 0.269), MDD or daily displacement (ANCOVA: F 1 , 10 = 2.664, P = 0.298) or maximum distance between two subsequent relocations (ANCOVA: F 1 , 10 = 0.145, P = 0.712). However, mean distance moved and maximum distance moved was slightly lower for forest snakes, while MDD were lower for station snakes (fig. 1). In general, most moves were short distance and within 13.3 m of the individual’s last known location, with 43.4% of all moves within 5 m. The maximum recorded single-night move was 141.4 m, which was by a forest individual.

Figure 1.
Figure 1.

(A) Mean distances moved, (B) maximum distance moved and (C) mean displacement between two subsequent relocations for snake found in the Dry Evergreen Forest (DEF) and Field Station. Error bars represent standard errors.

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

Home-range sizes

Home-range sizes for adult female T. macrops averaged 0.175 ± 0.097 ha over the 73.6 ± 26.9 day tracking period (range: 23-122, table 1). Although there was no significant correlation between total body length and MCP or core areas ( P > 0.050), we detected a positive correlation between body length and activity areas ( r 2 = 0.554, P < 0.050). We found no significant correlation between MCP area and number of days tracked (Spearmen’s rank S = 246.84, P = 0.284).

The overall mean percentage of MCP overlap was 41.4 ± 22.8% (fig. 2). For activity areas, however, there was little overlap among conspecifics, as UDOI averaged only 0.039 for station snakes and 0.045 for forest individuals. Core area (50% FK) overlap was even lower, with station overlap averaging 0.001, while forest was 0.005.

Behaviour and microhabitat selection

Trimeresurus macrops spent most of their time in the groundstory (48.8% of all observations), followed by understory (22.5%), on ground (13.8%), midstory (11.5%) and underground (3.1%). There was a difference in the forest layer selected during night and day (Underground, day 8.09% – night 0%; On ground, day 15.21% – night 18.22%; Groundstory, day 50.16% – night 61.78%; Understory, day 25.57% – night 19.11%; Midstory, day 0.97% – night 0.89%; fig. 3). The data’s limited size and distribution prevented robust testing of this difference.

Figure 2.
Figure 2.

Map of the study and overview of the MCPs generated for 12 of the tracked snakes. TRMA099 was located further west of both sites. Scales are UTM (m). (A) shows the Field Station location, and (B) shows the Dry Evergreen Forest (DEF) location.

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

Figure 3.
Figure 3.

The forest layer that snakes were observed using during day and night, separated into underground (<0 m), on ground (0 m), groundstory (>0-1 m), understory (1-3 m) and midstory (3-10 m).

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

Movement occurred predominantly during night time (GLMM: β = 3.409 ± 1.030, z = 3.310, P < 0.050; mR 2 = 0.454, cR 2 = 0.474), and we had only one recorded move during the day. Due to few movement observations, no environmental variables were selected as predictors by AICc.

We observed that during the day T. macrops are more likely to be resting ( β = 1.536 ± 0.234, z = 6.559, P < 0.001; mR 2 = 0.122, cR 2 = 0.356), whereas at night they were more likely to be ambushing ( β = 1.992 ± 0.242, z = 8.243, P < 0.050; mR 2 = 0.282, cR 2 = 0.387). Higher ground temperature ( β = 0.157 ± 0.042, z = 3.752, P < 0.050; mR 2 = 0.053, cR 2 = 0.435) and ground humidity ( β = 0.021 ± 0.010, z = 2.197, P < 0.050; mR 2 = 0.053, cR 2 = 0.435) were correlated to an increase in resting outside behaviour. Ambush behaviour was also associated with higher ground humidity ( β = 0.060 ± 0.011, z = 5.227, P < 0.050; mR 2 = 0.110, cR 2 = 0.327; fig. 4).

Individuals seemed to select nocturnal ambush sites more frequently in the groundstory (149 of 184 observations; fig. 5), moving to the understory for their diurnal resting sites (29.1% of observations). Both ambush and resting perch sites selected were mostly branches (178 of 217 observations), followed by thick brush patches (54.4%) and root complexes (19.4%).

Figure 4.
Figure 4.

Ambient temperature and humidity, ground temperature and humidity during one of four behaviours: ambush, moving, resting (outside, not in cover) or sheltering (under cover).

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

Figure 5.
Figure 5.

Proportion of data points where the snake was visible, and exhibiting one of four behaviours (ambush, moving, resting or sheltering), by location (Dry Evergreen Forest (DEF) and Field Station) and by forest layer.

Citation: Amphibia-Reptilia 39, 3 (2018) ; 10.1163/15685381-17000207

Sheltering behaviour, like ambush behaviour, was more frequent during the night than during the day ( β = 1.188 ± 0.284, z = 4.178, P < 0.050; mR 2 = 0.279, cR 2 = 0.562). Trimeresurus macrops selected as shelter sites hollow logs (23.5%), crevices under rocks (19.9%), and even man-made structures (8.8%; i.e. under concrete basin and porches, beneath metal doors, in dam wall). But unlike ambushing behaviour, sheltering behaviour was significantly more prevalent when the ground was colder ( β = 0.187 ± 0.045, z = 4.144, P < 0.050; mR 2 = 0.203, cR 2 = 0.580) and less humid ( β = 0.094 ± 0.013, z = 7.421, P < 0.050; mR 2 = 0.203, cR 2 = 0.580).

The seasonal differences observed were in sheltering and ambush behaviour. The cold season saw an increase in sheltering behaviour ( β = 2.729 ± 0.685, z = 3.984, P < 0.050; mR 2 = 0.279, cR 2 = 0.562). Whereas the dry season was linked to increased ambush activity ( β = 1.538 ± 0.494, z = 3.114, P < 0.050; mR 2 = 0.282, cR 2 = 0.387).

Discussion

We provide the first detailed study on the spatial ecology of T. macrops and one of the most in depth for the Trimeresurus group, especially in Southeast Asia.

Our results confirmed T. macrops as a highly nocturnal ambush predator. Activity pattern was largely sedentary with very short moves between relocations, similar to other ambush-hunting vipers such as Bothrops asper (Garman, 1883; Wasko and Sasa, 2009). Individuals tended to choose higher perch sites, or low shelter sites, for their daytime resting sites, likely to avoid predation, and then moved short distances into more exposed areas during the night for their nocturnal ambush sites. Mostly, they chose thin branches in the groundstory (68 out of 184 ambush observations) and although we observed one instance of diurnal ambush behaviour, it was likely an atypical observation. More successful predations, or higher prey abundance, may also have led to higher inactivity periods and reduced ambush observations in highly disturbed areas, as home-range size may be correlated to prey abundance (Hoss et al., 2010).

Higher humidity led to increased ambush opportunities, as hygrophillic prey, items, such as amphibians, are likely to be more active and abundant during higher humidity. Increased predation opportunity corresponding to higher humidity was one hypothesis presented by Daltry et al. (1998) in a study on the Southeast Asian Malayan pit viper Calloselasma rhodostoma (Kuhl, 1824). Other Trimeresrusus species are known to consume amphibians frequently compared to other mammalian or reptilian prey (Creer et al., 2002). Movement, aside from <1m small scale shifts from shelter to ambush sites, was rare and mostly limited to night-time and cooler temperatures. Although the ambient temperature reached a maximum of 39.4°C, we only observed movement below 31.2°C, and even that instance was with a snake basking in full sun within 3 m of a human settlement. And while the lowest temperature recorded was 12.8°C, we did not observe any movement below 23.2°C. These results agree with other studies on viper species indicating that these temperatures may be below optimal (Shine et al., 2003; Tsai and Tu, 2005), perhaps indicating a physiological limitation. Alternatively, prey density may vary by temperature and therefore influence T. macrops activity. We did observe less ambush behaviour at the lower temperatures, but without data on prey availability it is difficult to decipher whether the reduced ambushing is connected to fewer prey items or reduced metabolism at these temperatures.

During the cold season, snakes were under cover for long periods of time; selecting hollow logs, crevices under rocks and even man-made structures as shelters. This low activity in the cold season was likely primarily driven by the lower temperatures that were associated with sheltering behaviour. In contrast, during the dry season T. macrops did not face such low minimum temperatures. The slight increase in temperatures, perhaps to above a physiological threshold, may have enabled them to ambush more frequently, despite the lower mean humidity of the dry season. Ambushing behaviour during the dry season likely strengthened the overall connection between ambushing and humidity, as T. macrops may have needed to exploit the most humid periods in an otherwise dry season.

Unlike another ambush cryptic pit viper (i.e. Bothrops asper; Wasko and Sasa, 2009), T. macrops did not avoid heavily disturbed areas with reduced canopy and ground cover. This difference could be related to the higher intensity of movements made by B. asper or its terrestrial nature (Sasa et al., 2009). Greater movements could elevate a snake’s risk of predation (Bonnet et al., 1999). So when compared to a terrestrial viper with a larger home range, the limited and arboreal movements of T. macrops may aid in the use of disturbed habitats by reducing their exposure to mainly terrestrial anthropogenic disturbance or threats. However, field station individuals tended to use man-made structures over their more typical perch sites (e.g. branches, vegetation complexes). High usage of man-made structures would suggest that remaining off the ground would not necessarily reduce the exposure to humans. Alternatively, T. macrops may be encouraged into disturbed areas by higher prey availability. There is evidence showing that B. asper do modify their macro and micro-habitat selection, as well as their time spent ambushing in response to prey availability, although in their case being drawn to swamp areas (Wasko and Sasa, 2012). Our results begin to support this, as we found snakes in less disturbed areas more frequently in ambush position, potentially suggesting greater effort ambushing is required to acquire sufficient prey.

Body size did not influence home range sizes in T. macrops, even though it has been shown to have an effect on home ranges of other snake species (Whitaker and Shine, 2003; Roth, 2005; Hyslop et al., 2014; Bauder et al., 2006). Individuals within the field station exhibited larger home ranges on average, which may suggest an effect of human disturbance on space use; however, there was no discernible pattern. These results are likely due to individual variation and the small sample size available for analysis. However, proximity to human settlements likely has the same effect as edges: facilitating thermoregulation since they provide access to open sunny areas which increased body temperature, and shaded areas that decreased body temperatures (Carfagno and Weatherhead, 2008).

Home-range sizes for T. macrops were also significantly smaller when compared with other pit vipers: Crotalus viridis Rafinesque, 1818 had an MCP home range of 8.0 ha (Macartney, 1985), C. horridus Linnaeus, 1758 had 27.4 ha (Reinert and Zappalorti, 1988), Bothrops asper had 5.95 ha (Wasko and Sasa, 2009), and even the smallest viper, Bitis schneideri (Boettger, 1886), had a home range of 0.10 ha for adult females (Maritz and Alexander, 2012). That may be somewhat explained by the contrasting terrestrial and arboreal behaviour; having movements expressed largely two-dimensionally compared to T. macrops’ three.

However, MCP does not take into account the number of occurrences (i.e. highly versus rarely used areas) or allows areas outside of the polygon to be included in the activity area. It also significantly overestimates the area used by an individual (Reed and Douglas, 2002), causing bias for small sample sizes (Nilsen, Pedersen and Linnell, 2008). Trimeresurus macrops in this study remained in the same areas for long periods of time with little to no movement, so both MCP and kernel estimates included large areas of unused space. Kernel methods usually produce larger estimates than polygons, as their probabilistic contours may extend beyond the polygon boundaries. As such, and taking into consideration their foraging strategy, small home ranges and low frequency of movement, we believe both methods are not a biologically meaningful estimate of spatial use for T. macrops. Recent research has also suggested that this method is not an accurate measure for home range size in reptiles due to their sedentary nature (Row and Blouin-Demers, 2006). Our average tracking period of two months may have also failed to capture the full extent of the snakes’ home ranges. Despite the tropical climate, snakes in these areas can still express seasonal variation in activity (Brown, Shine and Madsen, 2002). Longer-term tracking would need to be undertaken to fully elucidate any seasonal movement patterns. However, transmitter battery life constraints and the ethical dilemma of multiple transmitter surgeries of individuals would need to be addressed for tracking individual vipers longer.

Home-range overlap was not significant, core area overlap especially was very limited. We observed 42 instances of proximity between tracked snakes (within less than 5 m of each other), although the individuals did not interact directly.

As any reliable conclusions on spatial ecology require large sample sizes (Kernohan, Gitzen and Millspaugh, 2001), our results can only provide preliminary data on this species. In light of the patchy data concerning some vipers (Maritz et al., 2016), this limited insight into the lives of T. macrops presents a valuable start in elucidating their habitat requirements and activity patterns.

Their persistence and continued use of human-disturbed areas indicates a high tolerance for human presence. Further studies on habitat utilization and selection for both male and female T. macrops are necessary, and how this selection relates to prey availability between highly disturbed areas and low impact forested areas also requires more investigation.

Acknowledgements

We thank Suranaree University of Technology (SUT) for funding this study. The Royal Thai Forestry Department generously provided permissions to work within the protected area. All methods were carried out under the guidelines of the Animal Use and Ethics Committee of SUT. The Thailand Institute of Scientific and Technological Research (TISTR) and Sakaerat Environmental Research Station (SERS) provided permission and technical support throughout the project. Additional thanks must go to the many volunteers who made this project possible, as well as to the SERS staff who assisted on a daily basis.

References

  • Bauder, J.M., Breininger, D.R., Bolt, M.R., Legare, M.L., Jenkins, C.L., Rothermel, B.B., McGarigal, K. (2016): Seasonal variation in Eastern Indigo snake (Drymarchon couperi) movement patterns and space use in Peninsular Florida at multiple temporal scales. Herpetologica 72: 214-226.

    • Search Google Scholar
    • Export Citation
  • Berger-Tal, O., Polak, T., Oron, A., Lubin, Y., Kotler, B.P., Saltz, D. (2011): Integrating animal behavior and conservation biology: a conceptual framework. Behav. Ecol. 22: 236-239.

    • Search Google Scholar
    • Export Citation
  • Bonnet, X., Naulleau, G., Shine, R. (1999): The dangers of leaving home: dispersal and mortality in snakes. Biol. Conserv. 89: 39-50.

  • Brown, G.P., Shine, R., Madsen, T. (2002): Responses of three sympatric snake species to tropical seasonality in northern Australia. J. Trop. Ecol. 18: 549-568.

    • Search Google Scholar
    • Export Citation
  • Carfagno, G.L., Weatherhead, P.J. (2008): Energetics and space use: intraspecific and interspecific comparisons of movements and home ranges of two Colubrid snakes. J. Anim. Ecol. 77: 416-424.

    • Search Google Scholar
    • Export Citation
  • Chanhome, L., Cox, M.J., Vasaruchapong, T., Chaiyabutr, N., Sitprija, V. (2011): Characterization of venomous snakes of Thailand. Asian Biomed. 5: 311-328.

    • Search Google Scholar
    • Export Citation
  • Creer, S., Chou, W.H., Malhotra, A., Thorpe, R.S. (2002): Offshore insular variation in the diet of the Taiwanese bamboo viper Trimeresurus stejnegeri (Schmidt). Zool. Sci. 19: 907-913.

    • Search Google Scholar
    • Export Citation
  • Daltry, J.C., Ross, T., Thorpe, R.S., Wüster, W. (1998): Evidence that humidity influences snake activity patterns: a field study of the Malayan pit viper Calloselasma rhodostoma. Ecography 21: 25-34.

    • Search Google Scholar
    • Export Citation
  • ESRI (2011): ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands, CA.

  • Fieberg, J., Kochanny, C.O. (2005): Quantifying home-range overlap: the importance of the utilization distribution. J. Wildl. Manage. 69: 1346-1359.

    • Search Google Scholar
    • Export Citation
  • Fryxell, J.M., Sinclair, A.R., Caughley, G. (2014): Wildlife Ecology, Conservation, and Management. John Wiley & Sons, New York.

  • Guillera-Arroita, G. (2017): Modelling of species distributions, range dynamics and communities under imperfect detection: advances, challenges and opportunities. Ecography 40: 281-295.

    • Search Google Scholar
    • Export Citation
  • Hoss, S.K., Guyer, C., Smith, L.L., Schuett, G.W. (2010): Multiscale influences of landscape composition and configuration on the spatial ecology of eastern diamond-backed rattlesnakes (Crotalus adamanteus). J. Herpetol. 44: 110-123.

    • Search Google Scholar
    • Export Citation
  • Hutton, R.A., Looareesuwan, S., Ho, M., Silamut, K., Chanthavanich, P., Karbwang, J., Supanaranond, W., Vejcho, S., Viravan, C., Phillips, R.E., Warrell, D.A. (1990): Arboreal green pit vipers (genus Trimeresurus) of South-East Asia: bites by T. albolabris and T. macrops in Thailand and a review of the literature. Trans. R. Soc. Trop. Med. Hyg. 84: 866-874.

    • Search Google Scholar
    • Export Citation
  • Hyslop, N.L., Meyers, J.M., Cooper, R.J., Norton, T.M. (2009): Survival of radio-implanted Drymarchon couperi (eastern indigo snake) in relation to body size and sex. Herpetologica 65: 199-206.

    • Search Google Scholar
    • Export Citation
  • Hyslop, N.L., Meyers, J.M., Cooper, R.J., Stevenson, D.J. (2014): Effects of body size and sex of Drymarchon couperi (eastern indigo snake) on habitat use, movements, and home range size in Georgia. J. Wildl. Manage. 78: 101-111.

    • Search Google Scholar
    • Export Citation
  • Kernohan, B.J., Gitzen, R.A., Millspaugh, J.J. (2001): Analysis of animal space use and movements. In: Radiotracking and Animal Populations, p. 126-166. Millspaugh, J.J., Marzluff, J.M., Eds, Academic Press, San Diego.

    • Search Google Scholar
    • Export Citation
  • Labocha, M.K., Schutz, H., Hayes, J.P. (2014): Which body condition index is best? Oikos 123: 111-119.

  • Luiselli, L. (2006): Resource partitioning and interspecific competition in snakes: the search for general geographical and guild patterns. Oikos 114: 193-211.

    • Search Google Scholar
    • Export Citation
  • Macartney, J.M. (1985): The ecology of the northern Pacific rattlesnake, Crotalus viridis oreganus, in British Columbia. M.Sc. Thesis, Department of Biology, University of Victoria, British Columbia, Canada. Available at http://ecoreserves.bc.ca/wp-content/uploads/1985/06/maccartney_1985_rattlesnake_ecology_thesis.pdf.

  • Malhotra, A., Thorpe, R.S., Mrinalini, Stuart, B.L. (2011): Two new species of pitviper of the genus Cryptelytrops Cope 1860 (Squamata: Viperidae: Crotalinae) from Southeast Asia. Zootaxa 2757: 1-23.

    • Search Google Scholar
    • Export Citation
  • Maritz, B., Alexander, G.J. (2012): Dwarfs on the move: spatial ecology of the world’s smallest viper, Bitis schneideri. Copeia 1: 115-120.

    • Search Google Scholar
    • Export Citation
  • Maritz, B., Penner, J., Martins, M., Crnobrnja-Isailović, J., Spear, S., Alencar, L.R.V., Sigala-Rodriguez, J., Messenger, K., Clark, R.W., Soorae, P., Luiselli, L., Jenkins, C., Greene, H.W. (2016): Identifying global priorities for the conservation of vipers. Biol. Conserv. 204: 94-102.

    • Search Google Scholar
    • Export Citation
  • Mazerolle, M.J. (2011): AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.00.

  • Nakagawa, S., Schielzeth, H. (2013): A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecol. Evol. 4: 133-142.

    • Search Google Scholar
    • Export Citation
  • Nilsen, E.B., Pedersen, S., Linnell, J.D. (2008): Can minimum convex polygon home ranges be used to draw biologically meaningful conclusions? Ecol. Res. 23: 635-639.

    • Search Google Scholar
    • Export Citation
  • Peig, J., Green, A.J. (2009): New Sistrurus catenatus catenatus perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891.

    • Search Google Scholar
    • Export Citation
  • R Development Core Team (2013): R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.

    • Search Google Scholar
    • Export Citation
  • Reed, R.N., Douglas, M.E. (2002): Ecology of the Grand Canyon rattlesnake (Crotalus viridis abyssus) in the Little Colorado River Canyon, Arizona. Southwest Naturalist 47: 30-39.

    • Search Google Scholar
    • Export Citation
  • Reinert, H.K., Zappalorti, R.T. (1988): Timber rattlesnakes (Crotalus horridus) of the Pine Barrens: their movement patterns and habitat preference. Copeia 4: 964-978.

    • Search Google Scholar
    • Export Citation
  • Roth, E.D. (2005): Spatial ecology of a cottonmouth (Agkistrodon piscivorus) population in east Texas. J. Herpetol. 39: 308-312.

  • Row, J.R., Blouin-Demers, G. (2006): Kernels are not accurate estimators of home-range size for herpetofauna. Copeia 4: 797-802.

  • Sasa, M., Wasko, D.K., Lamar, W.W. (2009): Natural history of the terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. Toxicon 54: 904-922.

    • Search Google Scholar
    • Export Citation
  • Schaefer, W.H. (1934): Diagnosis of sex in snakes. Copeia 4: 181.

  • Setser, K. (2007): Use of anesthesia increases precision of snake measurements. Herpetol. Rev. 38: 409-411.

  • Shine, R. (1987): Intraspecific variation in thermoregulation, movements and habitat use by Australian Blacksnakes, Pseudechis porphyriachus (Elapidae). J. Herpetol. 21: 165-177.

    • Search Google Scholar
    • Export Citation
  • Shine, R., Sun, L., Fitzgerald, M., Kearney, M. (2003): A radiotelemetric study of movements and thermal biology of insular Chinese pit-vipers (Gloydius shedaoensis, Viperidae). Oikos 100: 342-352.

    • Search Google Scholar
    • Export Citation
  • Steen, D.A. (2010): Snakes in the grass: secretive natural histories defy both conventional and progressive statistics. Herpetol. Conserv. Biol. 5: 183-188.

    • Search Google Scholar
    • Export Citation
  • Strine, C., Barnes, C., Crane, M., Silva, I., Suwanwaree, P., Nadolski, B., Hill, J. (2015): Sexual dimorphism of tropical green pit viper Trimeresurus (Cryptelytrops) macrops in Northeast Thailand. Amphibia-Reptilia 36: 327-338.

    • Search Google Scholar
    • Export Citation
  • Stuart, B., Chan-Ard, T., Thy, N. (2012): Cryptelytrops macrops. The IUCN Red List of Threatened Species. Version 2014.3. Available at www.iucnredlist.org. Accessed on 09 January 2015.

  • Tiebout III, H.M., Cary, J.R. (1987): Dynamic spatial ecology of the water snake, Nerodia sipedon. Copeia 1: 1-18.

  • Tsai, T.S., Tu, M.C. (2005): Postprandial thermophily of Chinese green tree vipers, Trimeresurus s. stejnegeri: interfering factors on snake temperature selection in a thigmothermal gradient. J. Therm. Biol. 30: 423-430.

    • Search Google Scholar
    • Export Citation
  • Wasko, D.K., Sasa, M. (2009): Activity patterns of a Neotropical ambush predator: spatial ecology of the Fer-de-lance (Bothrops asper, Serpentes: Viperidae) in Costa Rica. Biotropica 41: 241-249.

    • Search Google Scholar
    • Export Citation
  • Wasko, D.K., Sasa, M. (2012): Food resources influence spatial ecology, habitat selection, and foraging behavior in an ambush-hunting snake (Viperidae: Bothrops asper): an experimental study. Zoology 115: 179-187.

    • Search Google Scholar
    • Export Citation
  • Whitaker, P.B., Shine, R. (2003): A radiotelemetric study of movements and shelter-site selection by free-ranging brownsnakes (Pseudonaja textilis, Elapidae). Herpetol. Monogr. 17: 130-144.

    • Search Google Scholar
    • Export Citation
  • Worton, B.J. (1989): Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70: 164-168.

Footnotes

Associate Editor: Sylvain Ursenbacher.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 531 20 0
Full Text Views 353 94 5
PDF Views & Downloads 157 127 6