DIEL AND SEASONAL ACTIVITY PATTERNS OF PYGMY RABBITS ...

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This study documented activity patterns of pygmy rabbits (Brachylagus idahoensis) in free-ranging populations at 5 sites in Nevada and California. Infrared-triggered camera systems ..... Using remote photography in wildlife ecology: a review.
Journal of Mammalogy, 90(5):1176–1183, 2009

DIEL AND SEASONAL ACTIVITY PATTERNS OF PYGMY RABBITS (BRACHYLAGUS IDAHOENSIS) EVELINE S. LARRUCEA*

AND

PETER F. BRUSSARD

Department of Biology, Program in Ecology, Evolution, and Conservation Biology, University of Nevada Reno, Reno, NV 89557, USA

Characterizing circadian activity patterns is one of the essential steps to understanding how a species interacts with its environment. This study documented activity patterns of pygmy rabbits (Brachylagus idahoensis) in free-ranging populations at 5 sites in Nevada and California. Infrared-triggered camera systems were placed within areas occupied by populations of pygmy rabbits and operated for 1 year. The number of photographs obtained per hour was used as an index of aboveground activity. Activity was analyzed for diel and seasonal patterns as well as for differences among populations. All populations showed a bimodal diel activity pattern with most activity occurring at dawn and at dusk during all seasons. Greatest activity occurred at dawn except during winter. Four of the 5 study sites showed similar levels of activity. The atypical site was located 550 m higher in elevation at a locality known for extreme weather; activity levels were twice as high at that site. Activity patterns of pygmy rabbits likely reflect a combination of predation pressures as well as metabolic energy demands. Key words: activity, Brachylagus idahoensis, California, camera, Great Basin, infrared-triggered camera, Nevada, pygmy rabbit, Trailmaster

Characterizing circadian activity patterns is one of the essential steps to understanding how a species interacts with its environment. Ecological elements including pressure from predation, foraging requirements, and thermoregulatory challenges all can influence activity patterns (Halle 2000). These patterns in turn can affect behavior, including social interactions and parental care (Alexander 1974; Clutton-Brock 1991). For a managed species, this information is crucial for understanding when foraging activities take place, when predation risk might be greatest, and also when surveys and trapping studies might be most effective. Many methods have been used to record or quantify activity patterns of small mammals. Field studies have used direct observations (Shradin 2006), live traps checked at intervals throughout the night (Drickamer 1987; Gilbert et al. 1986; O’Farell 1974), live traps equipped with digital timers (Blanchong and Smale 2000; Bruseo and Barry 1995), and radiotelemetry (Urrejola et al. 2005). However, all of these methods have shortcomings. Physical trapping can bias results by removing trapped individuals from potential activity later in the night as well as by filling traps that are no longer * Correspondent: [email protected]

E 2009 American Society of Mammalogists www.mammalogy.org

available to capture individuals (Hicks et al. 1998). This inflates capture frequencies earlier in the night relative to those later in the night. Human presence and activity in the study area while checking traps or conducting telemetry also can influence natural activity patterns (Sequin et al. 2003). Motion-based radiotelemetry can overestimate activity because it may count sedentary behaviors such as head shaking or scratching as activity (DiBitetti et al. 2006). More recently, remote camera techniques have become popular in wildlife studies (Cutler and Swann 1999). Cameras have the benefits of photo-capturing animals and not physically removing them from the population while remaining available to capture additional animals. Camera units require relatively little field maintenance, which also may allow for more natural behavior to take place (Cutler and Swann 1999). Incidental data collected from remote cameras during studies of presence and absence of large mammals recently have been used to analyze activity levels (Azlan and Sharma 2006; DiBitetti et al. 2006). In these studies the number of photos of each species captured was assumed to be correlated with relative activity level. Pygmy rabbits (Brachylagus idahoensis) are the smallest leporids in North America (Green and Flinders 1980a; Wilde 1978). They are extreme habitat specialists (Gabler 1997; Heady 1998; Heady et. al. 2001) requiring structurally dense or late-successional big sagebrush (Artemisia tridentata) 1176

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growing on deep friable soils for food (Green and Flinders 1980b), protection from predators (Orr 1940), and burrow construction (Weiss and Verts 1984). Extensive degradation and fragmentation of the sagebrush habitat on which the pygmy rabbit relies recently motivated a petition to list the species throughout its entire range as threatened or endangered under the United States Endangered Species Act (Fite et al. 2003). The petition is currently under review for a 2nd time (United States Fish and Wildlife Service 2008). Researchers now are collecting information on all aspects of pygmy rabbit ecology to improve understanding of the species and to determine whether a need exists to manage for them. The majority of behavioral studies on pygmy rabbits have been conducted on a captive population in Washington State (Elias 2004; Elias et al. 2006), but captive populations do not necessarily demonstrate activity patterns similar to those of wild populations (DeCoursey 1990; Kas and Edgar 1999; Smale et al. 2003; Urrejola et al. 2005). From field observations, pygmy rabbits have been described as most active from sunrise to midmorning (Bradfield 1975), crepuscular (Janson 1946), crepuscular with some activity throughout the night (Heady 1998), and active at all times of day (Gahr 1993; Katzner 1994). There also are reports of seasonal differences, with larger home ranges used in spring and summer than during winter (Katzner and Parker 1997; Sanchez and Rachlow 2008), specific sagebrush plants used only during winter (Bradfield 1975; Katzner 1994), and rabbits using fewer (Janson 1946; Larrucea 2007) or more (Sanchez 2007) burrow systems during summer months. Our goal in this study was to document activity patterns of free-ranging pygmy rabbits using remote camera systems. Our 1st objective was to reveal diel activity patterns. We expected pygmy rabbits to have crepuscular activity patterns similar to those of other rabbit species (Mech et al. 1966; Theau and Ferron 2001). Activity patterns often are cited to be the result of predation pressures (Bakker et al. 2005), and pygmy rabbits have a similar suite of predators as do other small rabbit species (Gahr 1993; Janson 2002; Sanchez 2007). If study sites have similar predators, we would expect to see similar diel activity patterns across sites. Our 2nd objective was to determine if diel activity patterns change seasonally. Pygmy rabbits are active year-round, and energy requirements likely increase during the winter. We therefore expected to see a seasonal shift in activity times or levels. Activity levels might increase during colder seasons or shift to warmer times of the day due to higher metabolic requirements. Alternatively, activity levels might be reduced by remaining in burrows and reducing energy expenditure.

MATERIALS AND METHODS Study area.—We conducted this study at 5 sites in 4 regions of Nevada and California (Fig. 1). Three of the sites were in Nevada: Independence Valley north of Elko, Sheldon National Wildlife Refuge east of Denio, and Reese River Valley south of Austin. Two sites were located in Mono County, California:

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FIG. 1.—Diel activity patterns of pygmy rabbits (Brachylagus idahoensis) were monitored by infrared-triggered cameras in 4 regions of Nevada and California, 2004–2005. Two sites were monitored in the Mono County, California, region (region 4), 1 at Mono Lake and 1 at Bodie.

Mono Lake north of Lee Vining, and west of the historic town of Bodie. Elevation, vegetation measurements, and average temperatures and precipitation for each of the sites are provided in Table 1. Field methods.—We placed 5 active infrared-triggered Trailmaster 1550 camera units (Goodson and Associates, Inc., Lenexa, Kansas) at each study site near pygmy rabbit burrows and dense sagebrush. Camera units were composed of a single camera attached to a receiver, and a 2nd, smaller box that sent an infrared beam toward the receiver. When the infrared beam was interrupted the camera was triggered. We set the infrared beam 3 cm above ground level with a pulse delay of 1 (0.5 s) and programmed a 2-min camera delay. We narrowed the infrared lenses with electrical tape to 3 mm to increase camera precision and sensitivity. More detailed camera procedures are provided in Larrucea and Brussard (2008). Cameras were active 24 h/day and left for 1 week of data gathering. After skipping a 2nd week, we moved the cameras to 5 new locations within each site and activated them for another week. We changed the film at every camera move. New camera locations were placed 100 m from any previous location during the same month, reducing the chance that a single individual would be responsible for all data collected at multiple camera stations within a given month. Estimates of pygmy rabbit home ranges have varied from 0.21 ha in winter (Katzner and Parker 1997) to as large as 67.9 ha during spring

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TABLE 1.—Vegetation and climate characteristics at 5 study sites where aboveground activity data were collected for pygmy rabbits (Brachylagus idahoensis) in Nevada and California, 2004–2005. Average high and low temperatures for January and July as well as average annual rainfall, average annual snowfall, and range of snowpack depth are from the Western Regional Climate Center (2006). Height and cover refer to average sagebrush height and cover at each site. Site

Elevation (m)

Elko Sheldon Reese Mono Lake Bodie

1,930 1,770 1,770 1,980 2,530

Height (m) Cover (%) 1.2 1.3 1.0 1.0 0.6

60 50 55 35 40

January temperature July temperature (uC) (uC) 26.7–5.0 28.2–1.2 27.3–4.6 26.8–4.7 214.5–4.4

(Heady and Laundre 2005), and more recent studies have found annual home ranges to vary between 4.3 and 12.6 ha (Sanchez and Rachlow 2008). However, pygmy rabbits spend much of their time within 30–100 m of burrow systems (Heady and Laundre 2005; Katzner and Parker 1997; Sanchez 2007). From July 2004 through June 2005 we repeated the biweekly routine twice each month producing approximately 10 camera locations at each pygmy rabbit site per month. We continued the routine at each site for 1 year. Cameras marked each exposure with a time and date stamp, and accompanying receivers independently noted the date and time of photographs as well. All cameras were programmed to remain on standard time year-round. We downloaded the data from the receivers when we moved the cameras and compared these data to the time stamps on the developed photographs. Any photographs with discrepancies between time stamps and receivers of .5 min were removed from the analysis. Average sagebrush canopy cover and height at each site were measured using the line intercept sampling method (Bauer 1943). Along five 100-m transects, we measured the length of intercept for each plant, as well as the height of each plant touched by the transect line. Sagebrush cover was calculated by summing all intercept lengths at a site and dividing by the total transect lengths for the percent cover in the plot. All sagebrush heights at a site were summed and divided by the total number of measured plants for an average height for the plot. Data analysis.—We used every camera location from each pygmy rabbit site as an individual sample unit. There were therefore about 10 samples/month from each of the 5 sites. If film was fully exposed before the end of the week, we disregarded the data from the entire roll. We used only the 1st pygmy rabbit photograph captured in each hour; subsequent pygmy rabbit photographs during the same hour were disregarded. We divided the year into 4 biologically relevant seasons. Spring (March–May) was when the majority of young were born, and females were using natal burrows for nursing (Elias et al. 2006; Rachlow et al. 2005). Summer (June– August) included months when juveniles were active in the populations. Fall (September–November) was when temperatures were cooler and dispersal of juveniles had taken place (Estes-Zumpf and Rachlow 2009). Winter (December–February) included the coldest, harshest months when snow was often present at field sites. We compiled the photographs from

6.1–31.6 6.5–26.1 12.2–30.2 9.8–28.8 1.7–24.8

Rain (cm)

Snowfall (cm)

Snowpack (m)

37.49 30.25 31.67 35.46 33.25

206.0 191.3 146.6 165.9 254.5

0.3–0.6 0.3–1.8 0.3–0.6 0.3–1.8 0.3–6.3

each season into 1-h time blocks. We then divided the number of photographs in each hour by the effort, defined as the number of active camera stations during that season. Active camera stations were cameras that functioned correctly and had film available for the entire week. We used the number of photographs divided by the effort as an index to the level of aboveground activity per hour within a site. The time of sunrise and sunset on the central date of every season was used as the average time of sunrise and sunset for the season. Because photoperiod changes throughout the seasons, there was an offset at the end of each season. Average maximum offset was 43 min. We analyzed daily activity patterns by dividing days into 4 periods loosely described as night, morning, day, and evening. We used Pacific Standard Time of sunrise and sunset for the central date of each season to determine the daily periods. We assigned all photographs falling within 3 h of sunrise to the morning period (a 6-h block) and all photographs falling within 3 h of sunset to the evening period. Data falling into the remaining intervals, which varied from 4 to 8 h, were used as the day and night periods. The number of photographs divided by the effort was divided by the number of hours in each time period to compensate for the different lengths of time. Differences in levels of activity among daily time periods and seasons were tested using 2-factor analysis of variance with study site as the replication factor. Differences among study sites were analyzed by grouping seasons. We used Tukey’s honestly significant difference test to evaluate variation within significant main effects. Comparisons using percent distribution of activity were performed using logittransformed data. Results were considered significant if alpha , 0.05. We tested for correlation between actual times of sunrise and sunset and the observed hour of greatest activity. We tested correlation separately for sunrise and sunset times but grouped all populations. All analyses were conducted in program JMP version 7 (Sall and Lehman 1996).

RESULTS Active camera locations (n 5 477) from the 5 study sites captured 3,247 photographs of pygmy rabbits. Of these, we used 2,670 for analyses of aboveground activity. The remaining photographs were not used because they were not the 1st pygmy rabbit photograph in any 1 h (n 5 520), the film

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was completed before the end of the week (n 5 45), or there were discrepancies between the time stamp on the photograph and the data collected from the receivers (n 5 12). We tested the temporal distribution of aboveground activity of pygmy rabbits across time of day and season at 4 study sites (Fig. 2). Winter data could not be collected at the Bodie site because of high levels of snow, and therefore we did not include that site in these analyses. Activity varied significantly with time of day (F 5 20.97, d.f. 5 3, P , 0.001) but did not vary among seasons (F 5 1.52, d.f. 5 3, P 5 0.22). There was no interaction between time of day and season (F 5 1.11, d.f. 5 9, P 5 0.37). Tukey post hoc comparisons (at P , 0.05) indicated that morning (M 5 0.480) and evening (M 5 0.346) activity levels were both significantly greater than day (M 5 0.121) and night (M 5 0.119) activity levels (P , 0.001). Morning activity levels also differed significantly from evening levels in that morning had higher levels during all seasons except winter (P 5 0.026). Observed peaks in activity period were correlated with time of sunrise (n 5 19, R2 5 0.668, P 5 0.002) and sunset (n 5 19, R2 5 0.607, P 5 0.006; Fig. 2). Sample size was 19 because we only had information on 3 seasons from the Bodie site. Activity levels also were found to vary among populations (Fig. 2). Using data from all 5 sites for spring, summer, and fall, activity varied among populations (F 5 5.82, d.f. 5 4, P 5 0.007). Results for time and season (spring, summer, and fall) including the Bodie site were similar to analyses including winter (season: F 5 0.15, d.f. 5 2, P 5 0.85; time: F 5 22.0, d.f. 5 3, P , 0.001). Tukey post hoc analyses indicated that the Bodie site (M 5 0.458) had greater overall levels of activity than all other sites (Mono: M 5 0.299; Reese: M 5 0.214; Sheldon M 5 0.211; Elko M 5 0.153, P  0.01). The Mono site also differed from the Elko site due to greater levels of activity during the day and night (P 5 0.04). Although the amount of activity varied between sites, the percent distribution of activity among time blocks was similar among populations (F 5 0.02, d.f. 5 4, P 5 0.89). Other species photographed using pygmy rabbit burrows included badgers (Taxidea taxus), black-tailed jackrabbits (Lepus californicus), least chipmunks (Tamias minimus), mountain cottontails (Sylvilagus nuttallii), ground squirrels (Spermophilus), kangaroo rats (Dipodomys), long-tailed weasels (Mustela frenata), and peromyscine mice (Peromyscus). Photo-captured predators of pygmy rabbits included bobcats (Lynx rufus), coyotes (Canis latrans), badgers, long-tailed weasels, and Cooper’s hawks (Accipiter cooperii). Additional predators observed at the sites included golden eagles (Aquila chrysaetos), northern harriers (Circus cyaneus), and red-tailed hawks (Buteo jamaicensis).

DISCUSSION Diel activity.—Pygmy rabbits in Nevada and California were active above ground at all times of day, but the greatest activity in every sampled region occurred in a bimodal, crepuscular pattern (Fig. 2). The distinct peaks in activity were correlated

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with changes in photoperiod with peaks closer together during winter and farther apart during summer. A bimodal crepuscular activity pattern is observed in many other lagomorph species (Mech et al. 1966; Theau and Ferron 2001) and often is assumed to be the result of predation risk (Bakker et al. 2005; Lima and Dill 1990). Predation also is the most common cause of death in free-ranging pygmy rabbits (Gahr 1993; Sanchez 2007). Predators of pygmy rabbits include mammals such as badgers, weasels, coyotes, and bobcats as well as a suite of avian predators including hawks, eagles, and owls (Dobler and Dixon 1990; Green 1978; Wilde 1978). Diurnal activity might be limited by avian predators such as hawks and eagles, whereas nocturnal activity might be limited by owls, coyotes, and bobcats. Another possibility is that both diurnal and nocturnal species are active during crepuscular periods, increasing potential risk from predation during these times (Halle 2000). However, because prey commonly reduce activity in response to stimuli that suggest greater predation (Lima 1998) and because pygmy rabbits were potentially active at all times of day, we suggest that threat of predation is likely higher during day and night hours leading to the observed crepuscular pattern. Furthermore, the same suite of potential predators was photocaptured and sighted at each of our study sites, suggesting that predation may be driving similar activity patterns. Nonetheless, pygmy rabbits were photographed at all times of day, which demonstrates that they are not strictly crepuscular. Additional factors such as forage availability, available light, and individual behavior also can influence activity patterns (Halle 2000). Because sagebrush is continuously available, forage availability is unlikely to influence activity patterns of pygmy rabbits. Variation in moonlight influences activity patterns in small mammals (Daly et al. 1992; Griffin et al. 2005; Lima 1998). Nights with more light are more dangerous and therefore correspond with reduced activity of prey species. We did not have daily weather data for our study sites and therefore did not evaluate potential influence of moonlight on activity of pygmy rabbits. In the northern hemisphere, differences in light intensity between full and new moon are greatest during the winter (Janiczek and DeYoung 1987), and snow cover in winter also provides greater reflectance as well as a substrate against which prey species would be more visible. However, we did not observe lower levels of nocturnal activity during the winter season. Finally, different individuals, for example males and females, might be responsible for different peaks in activity. However, our methods did not distinguish among specific individuals, and we could not examine this question. For this study we considered only aboveground movement as activity, but pygmy rabbits dig burrows and probably have some underground activity as well. However, pygmy rabbit burrows are simple structures usually having only 1 main tunnel with 2–4 entrances (Elias 2004; Grinnell et al. 1930). Therefore, burrows probably serve more as refuges than as locations for extensive activity. Seasonal activity.—A 2nd major environmental cycle that affects activity in mammals is season (Daan and Aschoff

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FIG. 2.—Temporal activity patterns for pygmy rabbits (Brachylagus idahoensis) at 5 sites in Nevada and California, 2004–2005. In panel A, the number of photographs captured per hour divided by the effort (number of active camera stations) was used as an index to aboveground activity for each of the 4 seasons. The letters below the x-axis correspond to the average time of sunrise and sunset for each season. In panel B, we show the distribution of activity (as a percent of the total) during morning, day, evening, and night for each season. Winter data were not collected at the Bodie site.

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1982). We found that crepuscular patterns, as well as relative levels of activity, remained similar in all pygmy rabbit populations throughout the 4 seasons. The only seasonal effect observed was in the timing of greatest activity. In spring, summer, and fall, greatest activity occurred in the morning, whereas in winter, the difference between morning and evening activity was not apparent. Pygmy rabbits can live in areas with no free water and obtain all needed moisture from vegetation. One possibility is that pygmy rabbits are taking advantage of available moisture from dew in the mornings during the warmer and drier seasons. Additionally, dawn is generally the coldest time of day, and although this might provide a thermal benefit during warmer months, it is likely to be the opposite in winter. Pygmy rabbits are small mammals with a high surface to volume ratio, which means that they are susceptible to temperature extremes. Pygmy rabbits also have higher energy requirements relative to body size than do other lagomorphs (Shipley et al. 2006). Therefore, a shift of activity to dusk compared to dawn during winter might be a result of rabbits taking advantage of the warmer of the 2 main activity periods (Katzner and Parker 1997). For the same reason one also might expect to see greater diurnal activity during winter. However, pygmy rabbits demonstrate a unique behavior that also highlights an important limitation of remote cameras. Cameras operated well for the vast majority of the year, even during extreme heat and cold. Light snow sometimes triggered cameras, but with enough exposures, cameras still remained able to capture pygmy rabbits throughout a week. With a limited snowpack, cameras could be moved onto the surface of the snow or snow could be removed from around the unit, and pygmy rabbits were photographed frequently in snow depths up to about 30 cm. However, at greater snow depths, keeping cameras free of snow was challenging, and pygmy rabbits also created tunnels under the snow to gain access to sagebrush. These subnivian tunnels allowed them to remain under cover and presumably decreased their predation risk. Thus, during the coldest winter months when pygmy rabbits have greater energy requirements due to cold temperatures, they may satisfy these requirements by foraging under the snow; and, unfortunately, activity under the snow could not be recorded by our camera systems. Population differences.—All 5 of the sites we tested showed similar distributions of activity throughout the day. Four of the sites also showed similar levels of activity, but the index to aboveground activity was nearly twice as high at the Bodie site relative to the other 4 sites (Fig. 2). The Bodie site was 550 m higher in elevation than any of the other sites, and the area is well known for its harsh conditions (Table 1; DeLyser 1999). Decreased ambient temperatures might require increased activity as has been noted for white-tailed jackrabbits (Lepus townsendii—Rogowitz 1997). Pygmy rabbits in Bodie might have greater energy demands because of their harsher environment and, therefore, might need to forage more frequently to meet those demands. A difference in population density of pygmy rabbits between Bodie and the other sites also might account for the

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observed difference in activity levels. Greater numbers of pygmy rabbits might lead to a larger number of photo-captures and a perceived greater level of activity. However, we do not believe that this was the case. Population densities vary within pygmy rabbit populations throughout the year due to births and a high mortality rate (Janson 1946; Sanchez 2007; Weiss and Verts 1984). Population densities are likely higher during summer and fall than during winter and spring. Within each of our 5 study sites we found no differences in activity levels among seasons, indicating that cameras were not sensitive to changes in population densities. Rather, individual camera stations most likely photographed only 1 or 2 individuals in the vicinity of their burrows during each 2-week period. Furthermore, we corrected for any differences in sampling effort by dividing the number of photographs obtained by the number of cameras placed into each population. These considerations further support a true difference in activity levels at the Bodie site. Knowledge of activity patterns of pygmy rabbits can be useful to both management and future behavioral studies by allowing for more efficient surveys. Survey times can be planned during main periods of activity, increasing the chances of sighting a pygmy rabbit and providing conclusive evidence of current occupancy at a site. Trapping efforts also can benefit. Traps can be set during times of peak activity and then checked and closed during less-active times, resulting in animals spending less time in traps. Although this study provides much information about activity patterns in free-ranging pygmy rabbit populations, many interesting questions remain. Our methods did not distinguish among individual pygmy rabbits, and different sexes or specific individuals might be responsible for activity observed during different times or different seasons. Additionally, all of our study sites had similar predator species. Regions with different or fewer predators might elicit different activity patterns. Finally, the potential relationship between population densities and activity levels deserves further study.

ACKNOWLEDGMENTS Funding for pygmy rabbit research was provided by the Nevada Biodiversity Initiative and the University of Nevada Graduate Student Association.

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Submitted 27 August 2008. Accepted 5 March 2009. Associate Editor was Janet L. Rachlow.