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Influence of roads on the endangered Stephens' kangaroo rat (Dipodomys stephensi): are dirt and gravel roads different?
BIOLOGICAL CONSERVATION
Biological Conservation 118 (2004) 633–640 www.elsevier.com/locate/biocon
Influence of roads on the endangered StephensÕ kangaroo rat (Dipodomys stephensi): are dirt and gravel roads different? Rachel E. Brock, Douglas A. Kelt
*
Department of Wildlife, Fish, & Conservation Biology and Graduate Group in Ecology, University of California, One Shields Avenue, Davis CA 95616, USA Received 30 April 2003; received in revised form 3 October 2003; accepted 5 October 2003
Abstract Roads can have major impacts on animal distribution and movement patterns by destroying or creating habitat, and by acting as both barriers and corridors for movement. Using a combination of live trapping and spool and line tracking, we compare the relative abundance, mass, and demographic turnover of the endangered StephensÕ kangaroo rat (Dipodomys stephensi) on dirt and gravel roads in comparison with adjacent grassland habitat. D. stephensi was more active on dirt roads, and less so on gravel roads, relative to adjacent grassland habitat. Dirt roads were used extensively, and animals tended to move greater distances along dirt roads than in surrounding grasslands. In contrast, gravel roads were used much less extensively than adjacent grasslands. Animals using dirt roads were significantly lighter in mass than those on gravel roads and in adjacent grassland, suggesting greater use by juvenile animals. Dirt roads also had lower rates of recapture and higher rates of new arrivals than did adjacent habitat. These findings suggest that dirt roads provide potentially important landscape linkages for D. stephensi, whereas that gravel roads may act as movement barriers. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Dipodomys stephensi; StephensÕ kangaroo rat; Use of roads; Landscape linkage; Corridors
1. Introduction Roads are pervasive elements of most regions, and have diverse and substantial ecological effects (Forman and Alexander, 1998; Trombulak and Frissell, 2000). For animals these may include direct mortality (Ashley and Robinson, 1996; Case, 1978; Groot Bruinderink and Hazebroek, 1996), altered movement patterns (Klien, 1991), decreased reproductive output (Anthony and Isaacs, 1989), and home range shifts (Brody and Pelton, 1989; Reijnen et al., 1997). Roads may act as demographic barriers (Joly and Morand, 1997; Vos and Chardon, 1998), and they alter the physical and chemical environment of roadside habitat (Lagerwerff and Specht, 1970). Small mammals often are killed by traffic (Ashley and Robinson, 1996; Mallick et al., 1998), and may be reluctant to cross roads (Merriam et al., 1989; *
Corresponding author. Tel.: +1-530-754-9481; fax: +1-530-7524154. E-mail address: [email protected] (D.A. Kelt). 0006-3207/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2003.10.012
Oxely et al., 1974), even when the road is narrow and covered only by gravel (Oxely et al., 1974). Cotton rats (Sigmodon hispidus) and prairie voles (Microtus ochrogaster) avoid roads as narrow as 3 m (Swihart and Slade, 1984). Roads may also have positive effects, providing suitable habitat for ruderal species (Greenberg et al., 1997; Stiles and Jones, 1998), and several mammal species have been found to use roads as movement corridors (e.g., Dipodomys elator, Roberts and Packard, 1973; Rangifer tarandus, Banfield, 1974; Microtus pennsylvanicus, Getz et al., 1978; Spermophilus columbianus, Wiggett and Boag, 1989). The endangered StephensÕ kangaroo rat (Dipodomys stephensi) historically occurred only in a limited region in southern California (Grinnell, 1922). Urban development led to catastrophic habitat loss, and this species now is found in only a handful of designated reserves (U.S.F.W.S., 1997). These reserves occur in a semiurbanized matrix of lands used for grazing, agriculture, commerce, and parklands. All sites known to support
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StephensÕ kangaroo rat are relatively small in area and are bordered by, and traversed by, roads of varying size and use; these range from multi-lane asphalt roads to smaller gravel roads to dirt roads that may serve as firebreaks or as limited access routes through the reserves. This species is known to colonize dirt roadsides (OÕFarrell and Uptain, 1989), and small D. stephensi populations may occur in linear strips along disturbed roadways even when the regions surrounding the roads are unsuitable habitat (OÕFarrell, 1990). Roads may provide the flat and sparsely vegetated habitat that is preferred by this species; D. stephensi generally occupies relatively flat annual grassland (Bleich, 1973; MooreCraig, 1984; Price and Endo, 1989) with low shrub cover (Bleich, 1977; OÕFarrell and Clark, 1987; OÕFarrell and Uptain, 1987, 1989; Price et al., 1994; Price et al., 1992; Price et al., 1991). D. stephensi appears to favor intermediate seral stage plant communities that are maintained by disturbances such as fire, grazing, and agriculture (OÕFarrell, 1990). Anecdotal accounts suggest that D. stephensi may use dirt roads for dispersal (OÕFarrell, 1990; OÕFarrell and Uptain, 1989; Price et al., 1994). Radio-tracked individuals have been observed to move along dirt roads, and the longest dispersal distances recorded for D. stephensi have been between areas connected by a dirt road (Price et al., 1994). As habitat loss and fragmentation are the primary causes of decline for this species (Kramer, 1987; Price and Endo, 1989), restoring habitat and identifying ways to increase connectivity could be beneficial for the conservation of this species. Habitat connectivity may favor recovery by D. stephensi and has been promoted by some management plans (Mann and Plummer, 1995; Price and Gilpin, 1996). A spatially explicit metapopulation model for this species (Price and Gilpin, 1996) indicated that corridors connecting habitat patches should significantly increase persistence. Although no data confirm the role of connectivity for D. stephensi, the protection of corridors linking suitable habitat was a ‘‘very important’’ guideline in setting up the 17,400 ha of proposed reserves by the Riverside County Habitat Conservation Plan (Mann and Plummer, 1995). We explored the hypothesis that roads act as habitat and dispersal corridors for D. stephensi in an attempt to fill some of the gaps in our understanding of corridor use by this species. We evaluate this hypothesis by testing the following predictions: (1) Dipodomys stephensi occur with equal frequency on dirt and gravel roads and on adjacent grassland habitat; (2) Movement patterns by D. stephensi are not different on dirt and gravel roads. That is, individuals do not choose to use road habitat disproportionately over surrounding grassland habitat, and they move similar distances along roads and in adjacent grassland habitat; (3) Potential emigrants (i.e., juveniles) are equally abundant on dirt
roads and in adjacent grassland habitat; (4) Individuals on roads have a higher turnover rate (lower recaptures, greater immigration rates) than individuals in adjacent grasslands. A higher turnover rate on roads would be expected if roads are being used differentially for dispersal.
2. Methods Fieldwork was conducted at the Roy Shipley MultiSpecies Reserve in southwestern Riverside County, California (30°370 N, 117°20 W), between September 1996 and March 2000. Specifically, all field work for this study was conducted in the vicinity of Crown Valley, a gently sloped area characterized by non-native grasses and forbs and with a moderate to high density of StephensÕ kangaroo rats. The reserve has a history of agricultural disturbance and is traversed by a series of dirt and gravel roads; it was established in 1981, primarily to secure habitat for D. stephensi. Animals were captured using large Sherman live traps (model XLK, 3 3.75 12 in.) baited with millet seed (microwaved to prevent germination). Long-term work on permanent plots at the Shipley Reserve indicate that StephensÕ kangaroo rats exhibit high trappability (routinely 40–60%; Kelt, unpublished data) so in this paper we use numbers of animals trapped as estimates of local population size (e.g., number of animals on roads vs. on adjacent grassland). Individual rodents were marked using non-toxic felt tip markers or passively inducible transponders (PIT-tags) implanted under the skin. 2.1. Abundance of Stephens’ kangaroo rat in dirt, gravel, and off-road habitat D. stephensi abundance was determined with line transects in four habitat types; dirt road, gravel road, dense grassland (75–100% grass cover, average grass height 20–40 cm), and sparse grassland (<50% grass cover, average grass height 5–20 cm). Roads were sampled with traps placed along the edges of roads to avoid loss to vehicular traffic. We compared the four habitat types in both summer (July 1999) and winter (March 2000). Transects consisted of 10 traps at ca. 20 m intervals. In July 1999, five transects were sampled simultaneously for two nights at each of the four habitats (10 traps 5 transects 2 nights ¼ 100 trap-nights in each habitat). In March 2000, seven transects were sampled for three nights in each habitat (10 traps 7 transects 3 nights ¼ 210 trap-nights in each habitat). We compared relative trap success for each location and date using an analysis of variance (ANOVA) with a Tukey HSD post hoc comparison (Day and Quinn, 1989).
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2.2. Movement patterns on dirt and gravel roads We studied the effect of roads on movement patterns by applying a spool-and-line method (Berry et al., 1987; Boonstra and Crain, 1986) to D. stephensi that were trapped along the edges of both dirt and gravel roads. Spools of fine thread placed within uninflated plastic balloons were affixed to the hair on the anterior portion of each animalÕs back using commercial super glue. The mean mass of the spools was 2.4 g, or <4% of the average mass of D. stephensi. Spool-outfitted animals were released at the boundary of the dirt road and the surrounding grassland habitat. The end of the thread was fastened to the trap so that the spool unwound as the individual moved away from the trap. The unwinding 250 m spool of thread left a thread trail marking the pattern of movement. Because D. stephensi are nocturnal, spools were attached in the morning so that the test individuals would return immediately to their burrows. This allowed the animals to wear the spools for a full day inside their burrows, and to become accustomed to the spools before emerging the following night. On the following day, thread trails were located and quantified. The initial thread trail (from the trap to the burrow) was excluded from analysis. We evaluated differential use of habitats by quantifying the distribution of thread that was deposited by active kangaroo rats. For each animal, we recorded the total mass of thread deposited on vs. off the road, the total distance moved parallel to the road, and the maximum unidirectional distance traveled. The relative abundance of thread was used as an estimate of the relative activity on and off roads. If D. stephensi used roads disproportionately to surrounding grassland habitat, the mass of thread on roads should be greater than that off the roads. The total distance covered by thread trails parallel to the road was compared for thread trails on and off the road. If roads are allowing D. stephensi to move farther, the distances moved along a road should be greater than that moved parallel to the road in adjacent grassland habitat. The maximum unidirectional distance traveled also evaluates differences in distance moved on and off roads, but at a smaller spatial scale, comparing single movement trajectories rather than total distance moved. We recorded this measurement to test whether D. stephensi tend to make longer straight-line movements along roads than they do adjacent to roads. We recorded the mean of the three longest unidirectional trails both on and off the road. All trails that ran in one direction without turning more than 45° were considered to be unidirectional. If a > 45° change in direction did not persist for more than 25 cm (i.e., a compensatory movement was made such that the trail continued in the original direction), the trail was still considered to be unidirectional.
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Because data were heteroscedastic and not normally distributed, we applied non-parametric statistics. We compare thread mass, total distance, and longest unidirectional trail on and off of both dirt and gravel roads using Wilcoxon Matched Pairs tests (Siegel and Castellan, 1988). We used Mann–Whitney U tests to compare these metrics between dirt and gravel roads. 2.3. Abundance of different demographic groups on dirt roads To test whether juveniles were relatively more abundant on roads, we trapped D. stephensi on dirt roads, in grassland 10 m away from dirt roads (road adjacent), and in grassland 30–80 m away from dirt roads (grassland). Gravel roads were not included in this study because of very low capture success. All captured individuals were sexed and weighed using hand-held spring scales, and juveniles were identified by their lower mass (<55 g), relatively larger heads, and lighter color. We collected trapping data for the grassland habitat on 10 permanent 7 7 trapping arrays located 30–80 m away from roads. For dirt road and road adjacent locations, we established parallel trapping transects. Pairs of traps (i.e., one trap on the road and one trap 10 m to the side of the road) were placed 20 m apart in two parallel lines following the road. Forty-eight pairs of traps were initially placed along the parallel road transects in September. Due to trap damage from road traffic, only 44 pairs of traps were placed in subsequent trapping sessions. We trapped the parallel road transects and permanent trapping arrays in September 1998 (3 nights), and in March (1 night), May (3 nights), and July 1999 (2 nights); the number of nights trapped was dictated by constraints of the trapping permit issued by the California Department of Fish and Game and by the design of the concurrent population turnover study described below. We compared the mean mass of D. stephensi by sex, date, and trapping location (dirt road, road adjacent, and grassland) using ANOVA. 2.4. Population turnover Recapture and recruitment frequencies were compared for individuals trapped on dirt roads and in adjacent grasslands to compare demographic turnover in these habitats. Turnover was compared both over a short term (8 days) and a longer term (8 weeks). Trapping for the short-term turnover study was conducted in September 1998 using 48 paired trap stations on and adjacent to dirt roads (see above). To evaluate turnover rates over a longer term, a similar trapping effort was conducted at the beginning and end of two sequential eight-week sessions; the first of these sessions emphasized recapture rates and was run from March to May 1999, whereas the second emphasized recruitment and
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was run from May to July 1999. Recapture rate on and adjacent to roads was determined by trapping at 44 stations for a single night in March to mark a sample of D. stephensi individuals (see above). In May, the same locations were trapped for a longer period (3 nights) to compare the number of recaptured individuals relative to non-recaptured individuals. In July, trapping was conducted for an additional two nights to compare the number of new to recaptured individuals on and off roads. Duration of trapping in each census was dictated partially by constraints imposed by permitting procedures. We compared the relative numbers of recaptured animals against dispersed/missing individuals (short term study) and new recruits (longer term study) both on and adjacent to dirt roads using a 2 2 Chi square contingency table (new vs. recaptured animals road vs. adjacent grassland habitat).
ched Pairs test; Z ¼ 3:078, df ¼ 1, n ¼ 28, P < 0:005; Fig. 2(a)). In contrast, significantly more thread (by mass) was collected off than on gravel roads (Wilcoxon Matched Pairs test; Z ¼ 2:562, df ¼ 1, n ¼ 16, P < 0:01; Fig. 2(a)). Finally, the mean mass of thread collected from the dirt road was far greater than the mean mass of thread collected from the gravel road (Mann–Whitney U test; Z ¼ 4:446, df ¼ 1, n1 ¼ 28, n2 ¼ 16, P < 0:001; Fig. 2(a)), whereas there was no difference in the mean mass of thread collected in habitats adjacent to gravel vs. dirt roads (Mann–Whitney U test; Z ¼ 1:303, df ¼ 1, n1 ¼ 28, n2 ¼ 16, P > 0:5). The maximum distance covered by thread trails along the road was significantly greater on than off dirt roads (Wilcoxon Matched Pairs test; Z ¼ 3:460, df ¼ 1, n ¼ 32, P < 0:005; Fig. 2(b)). In contrast, the maximum distance moved along roads did not differ significantly on and off gravel roads (Wilcoxon Matched Pairs test; Z ¼ 1:130, df ¼ 1, n ¼ 16, P > 0:5). The mean distance
3. Results 3.1. Differential use of habitats Dirt roads and sparse grassland supported higher numbers of D. stephensi than dense grassland and gravel roads (MS ¼ 65, F3;40 ¼ 43:75, P < 0:001), but seasons were similar (MS ¼ 0:61, F1;40 ¼ 0:41, P > 0:5; Fig. 1); the interaction between habitat and season was not significant (MS ¼ 0:49, F3;40 ¼ 0:33, P > 0:5). Post-hoc comparisons indicated that all pairwise comparisons were significant (P < 0:001) except dirt roads vs. sparse grassland (P > 0:5) and dense grassland vs. gravel roads (P > 0:05). 3.2. Activity patterns in different habitats A significantly greater mass of thread was deposited on dirt roads than in adjacent habitat (Wilcoxon Mat-
Fig. 1. Mean number of Dipodomys stephensi caught at four locations (on dirt roads, in sparse grassland, in dense grassland, and on gravel roads) over two trapping censuses (July 1999 and March 2000). Error bars show one standard deviation.
Fig. 2. Patterns of Dipodomys stephensi movement compared on and adjacent to dirt and gravel roads. Three measurements of thread trails are compared including thread abundance (by mass), total distance moved parallel to the road, and maximum unidirectional distance moved. Error bars show one standard deviation.
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moved by individuals on dirt roads was significantly greater than that moved by individuals on gravel roads (Mann–Whitney U test; Z ¼ 3:581, df ¼ 1, n1 ¼ 32, n2 ¼ 16, P < 0:001; Fig. 2(b)), whereas there was no difference in the mean parallel distances moved in habitat adjacent to gravel roads vs. habitat adjacent to dirt roads (Mann–Whitney U test; Z ¼ 0:339, df ¼ 1, n1 ¼ 32, n2 ¼ 16, P > 0:7). The longest unidirectional movement was significantly greater on dirt roads than in adjacent habitat (Wilcoxon Matched Pairs test; Z ¼ 3:622, df ¼ 1, n ¼ 17, P < 0:001; Fig. 2(c)), but there was no significant difference on and off gravel roads (Wilcoxon Matched Pairs test; Z ¼ 1:590, df ¼ 1, n ¼ 16, P > 0:1). The longest unidirectional movement was significantly greater on dirt roads than on gravel roads (Mann– Whitney U test; Z ¼ 4:296, df ¼ 1, n1 ¼ 17, n2 ¼ 16, P < 0:001) but this metric did not differ between habitat adjacent to gravel and dirt roads (Mann–Whitney U test; Z ¼ 1:261, df ¼ 1, n1 ¼ 17, n2 ¼ 16, P > 0:5). 3.3. Age distribution in different habitats The mean mass of animals differed significantly by habitat (road, 64.20 3.63 g (mean 1 SD); adjacent, 69.63 2.86 g; grassland, 67.06 2.59 g; MS ¼ 678, F2;356 ¼ 7:91, P < 0:001) and sex (males, 68.93 3.83 g, female, 65.90 3.11 g; MS ¼ 509, F1;356 ¼ 5:93, P < 0:05), but not month (MS ¼ 66, F3;356 ¼ 0:77, P > 0:5); there was no interaction between any of the three factors (all P > 0:1). Post-hoc comparisons showed that the mean mass of animals caught on dirt roads was significantly less than both the mean mass of animals caught near roads (610 m from dirt roads) and in surrounding grasslands (30–80 m from dirt roads) (Tukey HSD test; P < 0:005 and P < 0:001, respectively). However, the mean mass did not differ significantly between the nearroad captures and the grassland captures (Tukey HSD test; P > 0:8). 3.4. Population turnover in different habitats Over the short-term (8 days), there was no significant difference in the respective ratios of lost animals (i.e., those that were marked but not recaptured) on dirt roads and road adjacent grassland habitat (2 2 contingency table, X 2 ¼ 0:318, df ¼ 1, P > 0:5; Fig. 3(a)). Similarly, there was no significant difference between these habitats in the ratio of originally marked individuals to new unmarked individuals that were caught for the first time at the end of the census (2 2 contingency table, X 2 ¼ 0:038, df ¼ 1, P > 0:9). Apparent turnover was notably different when evaluated over the longer (8 week) period (Fig. 3(b) and (c)). Of the individuals captured in March, significantly fewer were recaptured on dirt roads (6 of 23 animals recap-
Fig. 3. Turnover rate of Dipodomys stephensi compared on and adjacent to dirt roads. The recapture rates and the rate of new captures on and off roads are compared for one 8-day trial in September. Recapture rate is compared between March and May and recruitment rate is compared between May and July.
tured) during the intensive trapping in May than in adjacent grassland (7 of 14 animals; 2 2 contingency table, X 2 ¼ 8:362, df ¼ 1, P < 0:005). Of the individuals captured in July, significantly more on dirt roads were new than in adjacent grasslands (i.e., they had not been previously caught in the May census) (13 of 24 animals vs. 1 of 9; 2 2 contingency table, X 2 ¼ 4:968, df ¼ 1, P < 0:05).
4. Discussion Because dirt and gravel roads are superficially similar, it might be expected that their effects on D. stephensi movement would also be similar, but this is not the case. Every analysis supports the hypothesis that D. stephensi use dirt roads extensively, but that gravel roads are used only occasionally. Many small mammal species avoid roads (Merriam et al., 1989; Oxely et al., 1974; Swihart and Slade, 1984), whereas others show an affinity for road right-of-way habitat and occur at higher densities
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in these habitats relative to surrounding areas (Adam and Geis, 1983). Dipodomys ordii are relatively abundant on gravel roads in comparison with adjacent grasslands (Stapp, 1998). In contrast to the apparent avoidance of gravel roads, these data support independent observations that both D. stephensi and D. elator will colonize and travel along dirt roads and agricultural terraces (OÕFarrell, 1990; OÕFarrell and Uptain, 1989; Price et al., 1994; Roberts and Packard, 1973). A number of factors may cause D. stephensi to use dirt and gravel roads differentially. D. stephensi is a ruderal species that is able to capitalize on habitat disturbance and flourish in sparsely vegetated areas (Jones and Stokes Associates Inc., 1983; McClenaghan, 1994; OÕFarrell, 1990; OÕFarrell and Clark, 1987; Thomas, 1975). In contrast, gravel roads may be uncomfortable to kangaroo rats, which generally favor sandy substrates (Schmidly et al., 1993). The gravel roads studied here generally were twice as wide as the dirt roads (7.5 vs. 3 m); similar width gravel and dirt roads simply were not available for comparison. While it is possible that D. stephensi simply favor narrower movement corridors, their general preference for open habitats would seem to make this an unlikely explanation. The dirt and gravel roads compared in this study also experienced different volumes of vehicular traffic; traffic even on gravel roads was not heavy, however, and occurred largely during the day when kangaroo rats were in their burrows. The high density of D. stephensi on dirt roads may reflect some advantage incurred by having a portion of oneÕs territory occupied by a road. Grassland territories traversed by dirt roads might be superior to grassland territories without road clearings because they offer advantages associated with vegetation cover (i.e. food availability and refuge) as well as with open ground (i.e. easy burrowing, foraging, movement, and dust bathing). The berms at the edges of dirt roads have high densities of D. stephensi burrow entrances (OÕFarrell and Uptain, 1987) that may indicate a preference for burrowing in the raised soil of roadsides. The high seed availability provided by weedy plants growing along gravel roads may explain why D. ordii is four times more abundant in roadside habitats than in adjacent vegetation (Stapp, 1998). Similar foraging advantages may explain D. stephensi abundance on dirt roads. Finally, the open sandy habitat characteristic of dirt roads may provide ideal conditions for dust bathing, needed by kangaroo rats to keep their pelage from becoming matted and greasy (Eisenberg, 1963). Dirt roads may also function as corridors for longer distance movements, and may provide paths for D. stephensi to disperse between territories. Movement patterns observed in the spool-and-line studies support the hypothesis that dirt roads, but not gravel roads, function as corridors for movements by D. stephensi, at least over short distances (e.g., between territories or
foraging areas). The relatively greater amount of thread left on dirt roads may indicate a preference for moving in this habitat rather than in the surrounding grassland, although the type of activities in these habitats (e.g., foraging vs. movement between foraging sites) was not evaluated. Additionally, we have no information on rate of movement through different habitats; animals may be using roads as ‘‘rapid transit’’ corridors between foraging areas, but spending relatively little time on the roads themselves. Supporting this hypothesis, individuals moved greater distances on dirt roads (both longer unidirectional movements and longer total distances parallel to the road). Thus, we suspect that dirt roads function more as ‘‘landscape linkages’’ (Hudson, 1991) than as quality habitat for StephensÕ kangaroo rat, serving primarily for rapid movements within or between areas used for foraging and social activities. In contrast to their use of dirt roads, however, D. stephensi appear to avoid traveling on gravel roads. Further work will be required to fully assess the use of roads for longer distance movements. While it in unlikely that roads could serve as corridors for movement between existing reserves (which are separated by many miles of often-unsuitable habitat; R.C.H.C.A., 1996), they might be used by dispersing animals, and specifically by juveniles. In agreement with this prediction, juveniles were relatively more abundant than adults on dirt roads. Further research should employ radiotelemetry to document juvenile dispersal distances and routes traveled. The population turnover rate potentially reveals more about the use of roads as corridors than does the relative abundance of juveniles. The relatively high turnover rate observed on dirt roads suggests that D. stephensi might be dispersing along roads. The lower rates of recapture of animals on roads, and the higher rate of new arrivals, likely reflect a greater number of transient individuals using dirt roads. Such presumptive emigration (animals not being recaptured) and immigration (new animals arriving) would be expected if individuals were using roads to move to new territories. Alternatively, animals on roads may suffer more from predation or vehiclerelated accidents. The higher immigration rates would then be the result of new residents (not necessarily dispersers) inhabiting vacated territories. Whether the higher turnover rate reflects higher mortality or dispersal could be determined by conducting morning road surveys to evaluate mortality, and by evaluating seasonal patterns in turnover rates. Additionally, if juvenile dispersal explains the high turnover, turnover rates should be lower in winter when juveniles are not dispersing. Although these results provide general support for the hypothesis that dirt roads serve to link habitats for D. stephensi, such corridors may also have negative impacts on populations (Simberloff et al., 1992; Trom-
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bulak and Frissell, 2000; but see Beier and Noss, 1998), and we emphasize four of these as they apply to this species. First, as noted above, traffic could result in increased vehicle related mortality. Second, dirt roads might also increase D. stephensi exposure to predation. If predators preferentially move along dirt roads, these could lead to elevated encounters between predator and prey. Supporting this, eastern diamondback rattlesnakes (Crotalus adamanteus) lie in wait for their prey along corridors (Mann and Plummer, 1995). The clearing provided by roads may also make D. stephensi more visible and vulnerable to predation by owls and coyotes. Third, dirt roads could facilitate invasion by exotic grasses, which in Riverside County create dense grassland habitat that is disfavored by D. stephensi (U.S.F.W.S., 1997). There is evidence from other systems that different habitat corridors (Forman, 1991; Hobbs and Hopkins, 1991), including roads (Tyser and Worley, 1992; Wein et al., 1992), facilitate exotic species invasions. Fourth, soil compaction associated with use and maintenance of dirt roads could collapse burrows and impede burrowing by D. stephensi. Provided that the potential negative effects of dirt road corridors could be adequately minimized, dirt roads or similar pathways (i.e. tractor drags) might be effectively integrated into conservation management plans as corridors to link suitable habitat fragments. However, further research is needed in two areas before dirt roads are promoted in management plans for D. stephensi. First, the scale of movement that is supported by dirt roads needs to be determined. This study was limited to 250 m by the length of the thread spools. Use of radio collars would enable an assessment of road use at larger spatial scales more relevant to dispersal. If dirt roads facilitate movement over larger scales, they could be an effective means of fostering dispersal between fragmented habitats. Second, whether dispersal between habitat patches will actually improve D. stephensi population persistence needs to be determined. As it has not been proven that D. stephensi populations are dispersal limited, it should not be assumed that connectivity will have conservation benefits. The evidence that habitat corridors will benefit D. stephensi, based on simulation modeling (Price and Gilpin, 1996), should be verified by field research before roads are promoted as movement corridors for this species.
Acknowledgements We acknowledge field assistance by Sarah Brown, Matt Forister, Paule Gros, Eddy Konno, Shauna McDonald, Marcelo Tognelli, and Gina Wesley. Comments by Debbie Elliott-Fisk, Sharon Lawlor, and two anonymous reviewers helped to improve the manuscript. This research was supported in part by a grant from the
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Southwestern Riverside County Multi-Species Reserve Management Committee (to DAK). The opinions expressed in this paper are the authors.
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Joly, P., Morand, J., 1997. Amphibian diversity and land–water ecotones. In: Bravard, J.P., Juge, R. (Eds.), Biodiversity in land–water eco-tones. In: Man and biosphere series, vol. 18. United Nations Education, Scientific and Cultural Organization, Paris, France, pp. 161–182. Jones and Stokes Associates Inc., 1983. StephensÕ kangaroo rat studies at Lake Mathews. Report to Metropolitan Water District of Southern California, CA. Klien, D.R., 1991. Caribou in the changing north. Applied Animal Behavior Science 29, 279–291. Kramer, K., 1987. Endangered and threatened wildlife and plants; determination of endangered status for StephensÕ kangaroo rat. Final Rule. Federal Register 53, 38465–38469. Lagerwerff, J.V., Specht, A.N., 1970. Contamination of roadside soil and vegetation with cadmium, nickel, lead, and zinc. Environmental Science and Technology 4, 219–229. Mallick, S.A., Hocking, G.H., Driessen, M.M., 1998. Road-kills of the eastern barred bandicoot (Perameles gunnii) in Tasmania: an index of abundance. Wildlife Research 25, 139–145. Mann, C.C., Plummer, M.L., 1995. Are wildlife corridors the right path? Science 270, 1428–1430. McClenaghan Jr., L.R., 1994. Survey for StephensÕ kangaroo rat in the Sierra, Whiskey and Zulu impact areas of Marine Corps Base, Camp Pendleton. Report to Marine Corps Base, Camp Pendleton. Merriam, G., Kozakiewicz, M., Tsuchiya, E., Hawley, K., 1989. Barriers as boundaries for metapopulations and demes of Peromyscus leucopus in farm landscapes. Landscape Ecology 2, 227–235. Moore-Craig, N.A., 1984. Distribution and habitat preference of StephensÕ kangaroo rat on the San Jacinto Wildlife Area. Senior undergraduate thesis, University of California, Riverside, CA. OÕFarrell, M.J., 1990. StephensÕ kangaroo rat: natural history, distribution, and current status. In P. J. Bryant, J. Remington (Eds.), Endangered wildlife and habitats in southern California (pp. 78–84). Memoirs of the Natural History Foundation of Orange County 3. OÕFarrell, M.J., Clark, W.A., 1987. Habitat utilization by StephensÕ kangaroo rat (Dipodomys stephensi). WESTEC Services, Inc. report to Southern California Edison Co., Rosemead, CA. OÕFarrell, M.J., Uptain, C.E., 1987. Distribution and aspects of the natural history of StephensÕ kangaroo rat (Dipodomys stephensi) on the Warner Ranch. San Diego Co., California. Wasmann Journal of Biology 45, 34–48. OÕFarrell, M.J., Uptain, C.E., 1989. Assessment of population and habitat status of the StephensÕ kangaroo rat (Dipodomys stephensi). Report to the California Department of Fish and Game, CA. Oxely, D.J., Fenton, M.B., Carmody, G.R., 1974. The effects of roads on populations of small mammals. Journal of Applied Ecology 11, 51–58. Price, M.V., Endo, P.R., 1989. Estimating the distribution and abundance of a cryptic species, Dipodomys stephensi (Rodentia; Heteromyidae) and implications for management. Conservation Biology 2, 293–301. Price, M.V., Gilpin, M., 1996. Modelers, mammalogists, and metapopulations: designing StephensÕ Kangaroo Rat reserves. In: McCullough, D.R. (Ed.), Metapopulations and wildlife conservation. Island Press, Washington, DC, pp. 217–240. Price, M.V., Goldingay, R.L., Szychowski, L.S., Waser, N.M., 1994. Managing habitat for the endangered StephensÕ kangaroo rat (Dipodomys stephensi): effects of shrub removal. American Midland Naturalist 131, 9–16. Price, M.V., Kelly, P.A., Goldingay, R.L., 1992. Distinguishing the endangered StephensÕ kangaroo rat (Dipodomys stephensi) from the
Pacific kangaroo rat (Dipodomys agilis). Bulletin Southern California Academy of Sciences 91, 126–136. Price, M.V., Kelly, P.A., Goldingay, R.L., 1994. Distances moved by StephensÕ kangaroo rat (Dipodomys stephensi Merriam) and implications for conservation. Journal of Mammalogy 75, 929– 939. Price, M.V., Longland, W.S., Goldingay, R.L., 1991. Niche relationships of Dipodomys agilis and D. stephensi: two sympatric kangaroo rats of similar size. American Midland Naturalist 126, 172–186. Reijnen, R., Foppen, R., Veenbaas, G., 1997. Disturbance by traffic of breeding birds: evaluation of the effect and considerations in planning and managing road corridors. Biodiversity and Conservation 6, 567–581. R.C.H.C.A. (Riverside County Habitat Conservation Agency) 1996. Habitat conservation plan for the StephensÕ kangaroo rat in western Riverside County, California (Vol. 1). Habitat conservation plan. Riverside County Habitat Conservation Agency, Riverside, CA. Roberts, J.D., Packard, R.L., 1973. Comments on movement, home range and ecology of the Texas kangaroo rat, Dipodomys elator Merriam. Journal of Mammalogy 54, 957–962. Schmidly, D.J., Wilkins, K.T., Derrm, J.N., 1993. Biogeography. In: H. H. Genoways, J. H. Brown (Eds.), Biology of the Heteromyidae (pp. 319–356). Special publication No. 10, The American Society of Mammalogists, Shippensburg University, Shippensburg, PA. Siegel, S., Castellan, N.J., 1988. Nonparametric statistics for the behavioral sciences, second ed. McGraw-Hill, New York. Simberloff, D., Farr, J.A., Cox, J., Mehlman, D.W., 1992. Movement corridors: conservation bargains or poor investments? Conservation Biology 6, 493, 504. Stapp, P., 1998. Foraging by kangaroo rats under predation risk in native and roadside prairie vegetation. Poster presented 78th Annual meeting of the American Society of Mammalogists, Blackburg, VA. Stiles, J.H., Jones, R.H., 1998. Distribution of the red imported fire ant, Solenopsis invicata, in road and powerline habitats. Landscape Ecology 335, 335–346. Swihart, R.K., Slade, N.A., 1984. Road crossing in Sigmodon hispidus and Microtus ochrogaster. Journal of Mammalogy 65, 357–360. Thomas, J.R., 1975. Distribution, population densities, and home range requirements of the StephensÕ kangaroo rat (Dipodomys stephensi). M.A. thesis, California State Polytechnic University, Pomona, CA. Trombulak, S.C., Frissell, C.A., 2000. Review of ecological effects of roads on terrestrial and aquatic communities. Conservation Biology 14, 18–30. Tyser, R.W., Worley, C.A., 1992. Alien flora in grasslands adjacent to road and trail corridors in Glacier National Park, Montana (USA). Conservation Biology 6, 253–262. U.S.F.W.S. (United States Fish and Wildlife Service) 1997. Recovery plan for the StephensÕ kangaroo rat (Dipodomys stephensi). Portland, OR. Vos, C., Chardon, J.P., 1998. Effects of habitat fragmentation and road density on the distribution patterns on the moor frog Rana arvalis. Journal of Applied Ecology 35, 44–56. Wein, R.W., Wein, G., Bahret, S., Cody, W.J., 1992. Northward invading non-native vascular plant species in and adjacent to Wood Buffalo National Park, Canada. Canadian Field Naturalist 106, 216–224. Wiggett, D.R., Boag, D.A., 1989. Movements of inter-colony natal dispersers in the Columbian ground squirrel. Canadian Journal of Zoology 67, 1447–1452.
Biological Conservation 118 (2004) 633–640 www.elsevier.com/locate/biocon
Influence of roads on the endangered StephensÕ kangaroo rat (Dipodomys stephensi): are dirt and gravel roads different? Rachel E. Brock, Douglas A. Kelt
*
Department of Wildlife, Fish, & Conservation Biology and Graduate Group in Ecology, University of California, One Shields Avenue, Davis CA 95616, USA Received 30 April 2003; received in revised form 3 October 2003; accepted 5 October 2003
Abstract Roads can have major impacts on animal distribution and movement patterns by destroying or creating habitat, and by acting as both barriers and corridors for movement. Using a combination of live trapping and spool and line tracking, we compare the relative abundance, mass, and demographic turnover of the endangered StephensÕ kangaroo rat (Dipodomys stephensi) on dirt and gravel roads in comparison with adjacent grassland habitat. D. stephensi was more active on dirt roads, and less so on gravel roads, relative to adjacent grassland habitat. Dirt roads were used extensively, and animals tended to move greater distances along dirt roads than in surrounding grasslands. In contrast, gravel roads were used much less extensively than adjacent grasslands. Animals using dirt roads were significantly lighter in mass than those on gravel roads and in adjacent grassland, suggesting greater use by juvenile animals. Dirt roads also had lower rates of recapture and higher rates of new arrivals than did adjacent habitat. These findings suggest that dirt roads provide potentially important landscape linkages for D. stephensi, whereas that gravel roads may act as movement barriers. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Dipodomys stephensi; StephensÕ kangaroo rat; Use of roads; Landscape linkage; Corridors
1. Introduction Roads are pervasive elements of most regions, and have diverse and substantial ecological effects (Forman and Alexander, 1998; Trombulak and Frissell, 2000). For animals these may include direct mortality (Ashley and Robinson, 1996; Case, 1978; Groot Bruinderink and Hazebroek, 1996), altered movement patterns (Klien, 1991), decreased reproductive output (Anthony and Isaacs, 1989), and home range shifts (Brody and Pelton, 1989; Reijnen et al., 1997). Roads may act as demographic barriers (Joly and Morand, 1997; Vos and Chardon, 1998), and they alter the physical and chemical environment of roadside habitat (Lagerwerff and Specht, 1970). Small mammals often are killed by traffic (Ashley and Robinson, 1996; Mallick et al., 1998), and may be reluctant to cross roads (Merriam et al., 1989; *
Corresponding author. Tel.: +1-530-754-9481; fax: +1-530-7524154. E-mail address: [email protected] (D.A. Kelt). 0006-3207/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2003.10.012
Oxely et al., 1974), even when the road is narrow and covered only by gravel (Oxely et al., 1974). Cotton rats (Sigmodon hispidus) and prairie voles (Microtus ochrogaster) avoid roads as narrow as 3 m (Swihart and Slade, 1984). Roads may also have positive effects, providing suitable habitat for ruderal species (Greenberg et al., 1997; Stiles and Jones, 1998), and several mammal species have been found to use roads as movement corridors (e.g., Dipodomys elator, Roberts and Packard, 1973; Rangifer tarandus, Banfield, 1974; Microtus pennsylvanicus, Getz et al., 1978; Spermophilus columbianus, Wiggett and Boag, 1989). The endangered StephensÕ kangaroo rat (Dipodomys stephensi) historically occurred only in a limited region in southern California (Grinnell, 1922). Urban development led to catastrophic habitat loss, and this species now is found in only a handful of designated reserves (U.S.F.W.S., 1997). These reserves occur in a semiurbanized matrix of lands used for grazing, agriculture, commerce, and parklands. All sites known to support
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StephensÕ kangaroo rat are relatively small in area and are bordered by, and traversed by, roads of varying size and use; these range from multi-lane asphalt roads to smaller gravel roads to dirt roads that may serve as firebreaks or as limited access routes through the reserves. This species is known to colonize dirt roadsides (OÕFarrell and Uptain, 1989), and small D. stephensi populations may occur in linear strips along disturbed roadways even when the regions surrounding the roads are unsuitable habitat (OÕFarrell, 1990). Roads may provide the flat and sparsely vegetated habitat that is preferred by this species; D. stephensi generally occupies relatively flat annual grassland (Bleich, 1973; MooreCraig, 1984; Price and Endo, 1989) with low shrub cover (Bleich, 1977; OÕFarrell and Clark, 1987; OÕFarrell and Uptain, 1987, 1989; Price et al., 1994; Price et al., 1992; Price et al., 1991). D. stephensi appears to favor intermediate seral stage plant communities that are maintained by disturbances such as fire, grazing, and agriculture (OÕFarrell, 1990). Anecdotal accounts suggest that D. stephensi may use dirt roads for dispersal (OÕFarrell, 1990; OÕFarrell and Uptain, 1989; Price et al., 1994). Radio-tracked individuals have been observed to move along dirt roads, and the longest dispersal distances recorded for D. stephensi have been between areas connected by a dirt road (Price et al., 1994). As habitat loss and fragmentation are the primary causes of decline for this species (Kramer, 1987; Price and Endo, 1989), restoring habitat and identifying ways to increase connectivity could be beneficial for the conservation of this species. Habitat connectivity may favor recovery by D. stephensi and has been promoted by some management plans (Mann and Plummer, 1995; Price and Gilpin, 1996). A spatially explicit metapopulation model for this species (Price and Gilpin, 1996) indicated that corridors connecting habitat patches should significantly increase persistence. Although no data confirm the role of connectivity for D. stephensi, the protection of corridors linking suitable habitat was a ‘‘very important’’ guideline in setting up the 17,400 ha of proposed reserves by the Riverside County Habitat Conservation Plan (Mann and Plummer, 1995). We explored the hypothesis that roads act as habitat and dispersal corridors for D. stephensi in an attempt to fill some of the gaps in our understanding of corridor use by this species. We evaluate this hypothesis by testing the following predictions: (1) Dipodomys stephensi occur with equal frequency on dirt and gravel roads and on adjacent grassland habitat; (2) Movement patterns by D. stephensi are not different on dirt and gravel roads. That is, individuals do not choose to use road habitat disproportionately over surrounding grassland habitat, and they move similar distances along roads and in adjacent grassland habitat; (3) Potential emigrants (i.e., juveniles) are equally abundant on dirt
roads and in adjacent grassland habitat; (4) Individuals on roads have a higher turnover rate (lower recaptures, greater immigration rates) than individuals in adjacent grasslands. A higher turnover rate on roads would be expected if roads are being used differentially for dispersal.
2. Methods Fieldwork was conducted at the Roy Shipley MultiSpecies Reserve in southwestern Riverside County, California (30°370 N, 117°20 W), between September 1996 and March 2000. Specifically, all field work for this study was conducted in the vicinity of Crown Valley, a gently sloped area characterized by non-native grasses and forbs and with a moderate to high density of StephensÕ kangaroo rats. The reserve has a history of agricultural disturbance and is traversed by a series of dirt and gravel roads; it was established in 1981, primarily to secure habitat for D. stephensi. Animals were captured using large Sherman live traps (model XLK, 3 3.75 12 in.) baited with millet seed (microwaved to prevent germination). Long-term work on permanent plots at the Shipley Reserve indicate that StephensÕ kangaroo rats exhibit high trappability (routinely 40–60%; Kelt, unpublished data) so in this paper we use numbers of animals trapped as estimates of local population size (e.g., number of animals on roads vs. on adjacent grassland). Individual rodents were marked using non-toxic felt tip markers or passively inducible transponders (PIT-tags) implanted under the skin. 2.1. Abundance of Stephens’ kangaroo rat in dirt, gravel, and off-road habitat D. stephensi abundance was determined with line transects in four habitat types; dirt road, gravel road, dense grassland (75–100% grass cover, average grass height 20–40 cm), and sparse grassland (<50% grass cover, average grass height 5–20 cm). Roads were sampled with traps placed along the edges of roads to avoid loss to vehicular traffic. We compared the four habitat types in both summer (July 1999) and winter (March 2000). Transects consisted of 10 traps at ca. 20 m intervals. In July 1999, five transects were sampled simultaneously for two nights at each of the four habitats (10 traps 5 transects 2 nights ¼ 100 trap-nights in each habitat). In March 2000, seven transects were sampled for three nights in each habitat (10 traps 7 transects 3 nights ¼ 210 trap-nights in each habitat). We compared relative trap success for each location and date using an analysis of variance (ANOVA) with a Tukey HSD post hoc comparison (Day and Quinn, 1989).
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2.2. Movement patterns on dirt and gravel roads We studied the effect of roads on movement patterns by applying a spool-and-line method (Berry et al., 1987; Boonstra and Crain, 1986) to D. stephensi that were trapped along the edges of both dirt and gravel roads. Spools of fine thread placed within uninflated plastic balloons were affixed to the hair on the anterior portion of each animalÕs back using commercial super glue. The mean mass of the spools was 2.4 g, or <4% of the average mass of D. stephensi. Spool-outfitted animals were released at the boundary of the dirt road and the surrounding grassland habitat. The end of the thread was fastened to the trap so that the spool unwound as the individual moved away from the trap. The unwinding 250 m spool of thread left a thread trail marking the pattern of movement. Because D. stephensi are nocturnal, spools were attached in the morning so that the test individuals would return immediately to their burrows. This allowed the animals to wear the spools for a full day inside their burrows, and to become accustomed to the spools before emerging the following night. On the following day, thread trails were located and quantified. The initial thread trail (from the trap to the burrow) was excluded from analysis. We evaluated differential use of habitats by quantifying the distribution of thread that was deposited by active kangaroo rats. For each animal, we recorded the total mass of thread deposited on vs. off the road, the total distance moved parallel to the road, and the maximum unidirectional distance traveled. The relative abundance of thread was used as an estimate of the relative activity on and off roads. If D. stephensi used roads disproportionately to surrounding grassland habitat, the mass of thread on roads should be greater than that off the roads. The total distance covered by thread trails parallel to the road was compared for thread trails on and off the road. If roads are allowing D. stephensi to move farther, the distances moved along a road should be greater than that moved parallel to the road in adjacent grassland habitat. The maximum unidirectional distance traveled also evaluates differences in distance moved on and off roads, but at a smaller spatial scale, comparing single movement trajectories rather than total distance moved. We recorded this measurement to test whether D. stephensi tend to make longer straight-line movements along roads than they do adjacent to roads. We recorded the mean of the three longest unidirectional trails both on and off the road. All trails that ran in one direction without turning more than 45° were considered to be unidirectional. If a > 45° change in direction did not persist for more than 25 cm (i.e., a compensatory movement was made such that the trail continued in the original direction), the trail was still considered to be unidirectional.
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Because data were heteroscedastic and not normally distributed, we applied non-parametric statistics. We compare thread mass, total distance, and longest unidirectional trail on and off of both dirt and gravel roads using Wilcoxon Matched Pairs tests (Siegel and Castellan, 1988). We used Mann–Whitney U tests to compare these metrics between dirt and gravel roads. 2.3. Abundance of different demographic groups on dirt roads To test whether juveniles were relatively more abundant on roads, we trapped D. stephensi on dirt roads, in grassland 10 m away from dirt roads (road adjacent), and in grassland 30–80 m away from dirt roads (grassland). Gravel roads were not included in this study because of very low capture success. All captured individuals were sexed and weighed using hand-held spring scales, and juveniles were identified by their lower mass (<55 g), relatively larger heads, and lighter color. We collected trapping data for the grassland habitat on 10 permanent 7 7 trapping arrays located 30–80 m away from roads. For dirt road and road adjacent locations, we established parallel trapping transects. Pairs of traps (i.e., one trap on the road and one trap 10 m to the side of the road) were placed 20 m apart in two parallel lines following the road. Forty-eight pairs of traps were initially placed along the parallel road transects in September. Due to trap damage from road traffic, only 44 pairs of traps were placed in subsequent trapping sessions. We trapped the parallel road transects and permanent trapping arrays in September 1998 (3 nights), and in March (1 night), May (3 nights), and July 1999 (2 nights); the number of nights trapped was dictated by constraints of the trapping permit issued by the California Department of Fish and Game and by the design of the concurrent population turnover study described below. We compared the mean mass of D. stephensi by sex, date, and trapping location (dirt road, road adjacent, and grassland) using ANOVA. 2.4. Population turnover Recapture and recruitment frequencies were compared for individuals trapped on dirt roads and in adjacent grasslands to compare demographic turnover in these habitats. Turnover was compared both over a short term (8 days) and a longer term (8 weeks). Trapping for the short-term turnover study was conducted in September 1998 using 48 paired trap stations on and adjacent to dirt roads (see above). To evaluate turnover rates over a longer term, a similar trapping effort was conducted at the beginning and end of two sequential eight-week sessions; the first of these sessions emphasized recapture rates and was run from March to May 1999, whereas the second emphasized recruitment and
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was run from May to July 1999. Recapture rate on and adjacent to roads was determined by trapping at 44 stations for a single night in March to mark a sample of D. stephensi individuals (see above). In May, the same locations were trapped for a longer period (3 nights) to compare the number of recaptured individuals relative to non-recaptured individuals. In July, trapping was conducted for an additional two nights to compare the number of new to recaptured individuals on and off roads. Duration of trapping in each census was dictated partially by constraints imposed by permitting procedures. We compared the relative numbers of recaptured animals against dispersed/missing individuals (short term study) and new recruits (longer term study) both on and adjacent to dirt roads using a 2 2 Chi square contingency table (new vs. recaptured animals road vs. adjacent grassland habitat).
ched Pairs test; Z ¼ 3:078, df ¼ 1, n ¼ 28, P < 0:005; Fig. 2(a)). In contrast, significantly more thread (by mass) was collected off than on gravel roads (Wilcoxon Matched Pairs test; Z ¼ 2:562, df ¼ 1, n ¼ 16, P < 0:01; Fig. 2(a)). Finally, the mean mass of thread collected from the dirt road was far greater than the mean mass of thread collected from the gravel road (Mann–Whitney U test; Z ¼ 4:446, df ¼ 1, n1 ¼ 28, n2 ¼ 16, P < 0:001; Fig. 2(a)), whereas there was no difference in the mean mass of thread collected in habitats adjacent to gravel vs. dirt roads (Mann–Whitney U test; Z ¼ 1:303, df ¼ 1, n1 ¼ 28, n2 ¼ 16, P > 0:5). The maximum distance covered by thread trails along the road was significantly greater on than off dirt roads (Wilcoxon Matched Pairs test; Z ¼ 3:460, df ¼ 1, n ¼ 32, P < 0:005; Fig. 2(b)). In contrast, the maximum distance moved along roads did not differ significantly on and off gravel roads (Wilcoxon Matched Pairs test; Z ¼ 1:130, df ¼ 1, n ¼ 16, P > 0:5). The mean distance
3. Results 3.1. Differential use of habitats Dirt roads and sparse grassland supported higher numbers of D. stephensi than dense grassland and gravel roads (MS ¼ 65, F3;40 ¼ 43:75, P < 0:001), but seasons were similar (MS ¼ 0:61, F1;40 ¼ 0:41, P > 0:5; Fig. 1); the interaction between habitat and season was not significant (MS ¼ 0:49, F3;40 ¼ 0:33, P > 0:5). Post-hoc comparisons indicated that all pairwise comparisons were significant (P < 0:001) except dirt roads vs. sparse grassland (P > 0:5) and dense grassland vs. gravel roads (P > 0:05). 3.2. Activity patterns in different habitats A significantly greater mass of thread was deposited on dirt roads than in adjacent habitat (Wilcoxon Mat-
Fig. 1. Mean number of Dipodomys stephensi caught at four locations (on dirt roads, in sparse grassland, in dense grassland, and on gravel roads) over two trapping censuses (July 1999 and March 2000). Error bars show one standard deviation.
Fig. 2. Patterns of Dipodomys stephensi movement compared on and adjacent to dirt and gravel roads. Three measurements of thread trails are compared including thread abundance (by mass), total distance moved parallel to the road, and maximum unidirectional distance moved. Error bars show one standard deviation.
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moved by individuals on dirt roads was significantly greater than that moved by individuals on gravel roads (Mann–Whitney U test; Z ¼ 3:581, df ¼ 1, n1 ¼ 32, n2 ¼ 16, P < 0:001; Fig. 2(b)), whereas there was no difference in the mean parallel distances moved in habitat adjacent to gravel roads vs. habitat adjacent to dirt roads (Mann–Whitney U test; Z ¼ 0:339, df ¼ 1, n1 ¼ 32, n2 ¼ 16, P > 0:7). The longest unidirectional movement was significantly greater on dirt roads than in adjacent habitat (Wilcoxon Matched Pairs test; Z ¼ 3:622, df ¼ 1, n ¼ 17, P < 0:001; Fig. 2(c)), but there was no significant difference on and off gravel roads (Wilcoxon Matched Pairs test; Z ¼ 1:590, df ¼ 1, n ¼ 16, P > 0:1). The longest unidirectional movement was significantly greater on dirt roads than on gravel roads (Mann– Whitney U test; Z ¼ 4:296, df ¼ 1, n1 ¼ 17, n2 ¼ 16, P < 0:001) but this metric did not differ between habitat adjacent to gravel and dirt roads (Mann–Whitney U test; Z ¼ 1:261, df ¼ 1, n1 ¼ 17, n2 ¼ 16, P > 0:5). 3.3. Age distribution in different habitats The mean mass of animals differed significantly by habitat (road, 64.20 3.63 g (mean 1 SD); adjacent, 69.63 2.86 g; grassland, 67.06 2.59 g; MS ¼ 678, F2;356 ¼ 7:91, P < 0:001) and sex (males, 68.93 3.83 g, female, 65.90 3.11 g; MS ¼ 509, F1;356 ¼ 5:93, P < 0:05), but not month (MS ¼ 66, F3;356 ¼ 0:77, P > 0:5); there was no interaction between any of the three factors (all P > 0:1). Post-hoc comparisons showed that the mean mass of animals caught on dirt roads was significantly less than both the mean mass of animals caught near roads (610 m from dirt roads) and in surrounding grasslands (30–80 m from dirt roads) (Tukey HSD test; P < 0:005 and P < 0:001, respectively). However, the mean mass did not differ significantly between the nearroad captures and the grassland captures (Tukey HSD test; P > 0:8). 3.4. Population turnover in different habitats Over the short-term (8 days), there was no significant difference in the respective ratios of lost animals (i.e., those that were marked but not recaptured) on dirt roads and road adjacent grassland habitat (2 2 contingency table, X 2 ¼ 0:318, df ¼ 1, P > 0:5; Fig. 3(a)). Similarly, there was no significant difference between these habitats in the ratio of originally marked individuals to new unmarked individuals that were caught for the first time at the end of the census (2 2 contingency table, X 2 ¼ 0:038, df ¼ 1, P > 0:9). Apparent turnover was notably different when evaluated over the longer (8 week) period (Fig. 3(b) and (c)). Of the individuals captured in March, significantly fewer were recaptured on dirt roads (6 of 23 animals recap-
Fig. 3. Turnover rate of Dipodomys stephensi compared on and adjacent to dirt roads. The recapture rates and the rate of new captures on and off roads are compared for one 8-day trial in September. Recapture rate is compared between March and May and recruitment rate is compared between May and July.
tured) during the intensive trapping in May than in adjacent grassland (7 of 14 animals; 2 2 contingency table, X 2 ¼ 8:362, df ¼ 1, P < 0:005). Of the individuals captured in July, significantly more on dirt roads were new than in adjacent grasslands (i.e., they had not been previously caught in the May census) (13 of 24 animals vs. 1 of 9; 2 2 contingency table, X 2 ¼ 4:968, df ¼ 1, P < 0:05).
4. Discussion Because dirt and gravel roads are superficially similar, it might be expected that their effects on D. stephensi movement would also be similar, but this is not the case. Every analysis supports the hypothesis that D. stephensi use dirt roads extensively, but that gravel roads are used only occasionally. Many small mammal species avoid roads (Merriam et al., 1989; Oxely et al., 1974; Swihart and Slade, 1984), whereas others show an affinity for road right-of-way habitat and occur at higher densities
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in these habitats relative to surrounding areas (Adam and Geis, 1983). Dipodomys ordii are relatively abundant on gravel roads in comparison with adjacent grasslands (Stapp, 1998). In contrast to the apparent avoidance of gravel roads, these data support independent observations that both D. stephensi and D. elator will colonize and travel along dirt roads and agricultural terraces (OÕFarrell, 1990; OÕFarrell and Uptain, 1989; Price et al., 1994; Roberts and Packard, 1973). A number of factors may cause D. stephensi to use dirt and gravel roads differentially. D. stephensi is a ruderal species that is able to capitalize on habitat disturbance and flourish in sparsely vegetated areas (Jones and Stokes Associates Inc., 1983; McClenaghan, 1994; OÕFarrell, 1990; OÕFarrell and Clark, 1987; Thomas, 1975). In contrast, gravel roads may be uncomfortable to kangaroo rats, which generally favor sandy substrates (Schmidly et al., 1993). The gravel roads studied here generally were twice as wide as the dirt roads (7.5 vs. 3 m); similar width gravel and dirt roads simply were not available for comparison. While it is possible that D. stephensi simply favor narrower movement corridors, their general preference for open habitats would seem to make this an unlikely explanation. The dirt and gravel roads compared in this study also experienced different volumes of vehicular traffic; traffic even on gravel roads was not heavy, however, and occurred largely during the day when kangaroo rats were in their burrows. The high density of D. stephensi on dirt roads may reflect some advantage incurred by having a portion of oneÕs territory occupied by a road. Grassland territories traversed by dirt roads might be superior to grassland territories without road clearings because they offer advantages associated with vegetation cover (i.e. food availability and refuge) as well as with open ground (i.e. easy burrowing, foraging, movement, and dust bathing). The berms at the edges of dirt roads have high densities of D. stephensi burrow entrances (OÕFarrell and Uptain, 1987) that may indicate a preference for burrowing in the raised soil of roadsides. The high seed availability provided by weedy plants growing along gravel roads may explain why D. ordii is four times more abundant in roadside habitats than in adjacent vegetation (Stapp, 1998). Similar foraging advantages may explain D. stephensi abundance on dirt roads. Finally, the open sandy habitat characteristic of dirt roads may provide ideal conditions for dust bathing, needed by kangaroo rats to keep their pelage from becoming matted and greasy (Eisenberg, 1963). Dirt roads may also function as corridors for longer distance movements, and may provide paths for D. stephensi to disperse between territories. Movement patterns observed in the spool-and-line studies support the hypothesis that dirt roads, but not gravel roads, function as corridors for movements by D. stephensi, at least over short distances (e.g., between territories or
foraging areas). The relatively greater amount of thread left on dirt roads may indicate a preference for moving in this habitat rather than in the surrounding grassland, although the type of activities in these habitats (e.g., foraging vs. movement between foraging sites) was not evaluated. Additionally, we have no information on rate of movement through different habitats; animals may be using roads as ‘‘rapid transit’’ corridors between foraging areas, but spending relatively little time on the roads themselves. Supporting this hypothesis, individuals moved greater distances on dirt roads (both longer unidirectional movements and longer total distances parallel to the road). Thus, we suspect that dirt roads function more as ‘‘landscape linkages’’ (Hudson, 1991) than as quality habitat for StephensÕ kangaroo rat, serving primarily for rapid movements within or between areas used for foraging and social activities. In contrast to their use of dirt roads, however, D. stephensi appear to avoid traveling on gravel roads. Further work will be required to fully assess the use of roads for longer distance movements. While it in unlikely that roads could serve as corridors for movement between existing reserves (which are separated by many miles of often-unsuitable habitat; R.C.H.C.A., 1996), they might be used by dispersing animals, and specifically by juveniles. In agreement with this prediction, juveniles were relatively more abundant than adults on dirt roads. Further research should employ radiotelemetry to document juvenile dispersal distances and routes traveled. The population turnover rate potentially reveals more about the use of roads as corridors than does the relative abundance of juveniles. The relatively high turnover rate observed on dirt roads suggests that D. stephensi might be dispersing along roads. The lower rates of recapture of animals on roads, and the higher rate of new arrivals, likely reflect a greater number of transient individuals using dirt roads. Such presumptive emigration (animals not being recaptured) and immigration (new animals arriving) would be expected if individuals were using roads to move to new territories. Alternatively, animals on roads may suffer more from predation or vehiclerelated accidents. The higher immigration rates would then be the result of new residents (not necessarily dispersers) inhabiting vacated territories. Whether the higher turnover rate reflects higher mortality or dispersal could be determined by conducting morning road surveys to evaluate mortality, and by evaluating seasonal patterns in turnover rates. Additionally, if juvenile dispersal explains the high turnover, turnover rates should be lower in winter when juveniles are not dispersing. Although these results provide general support for the hypothesis that dirt roads serve to link habitats for D. stephensi, such corridors may also have negative impacts on populations (Simberloff et al., 1992; Trom-
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bulak and Frissell, 2000; but see Beier and Noss, 1998), and we emphasize four of these as they apply to this species. First, as noted above, traffic could result in increased vehicle related mortality. Second, dirt roads might also increase D. stephensi exposure to predation. If predators preferentially move along dirt roads, these could lead to elevated encounters between predator and prey. Supporting this, eastern diamondback rattlesnakes (Crotalus adamanteus) lie in wait for their prey along corridors (Mann and Plummer, 1995). The clearing provided by roads may also make D. stephensi more visible and vulnerable to predation by owls and coyotes. Third, dirt roads could facilitate invasion by exotic grasses, which in Riverside County create dense grassland habitat that is disfavored by D. stephensi (U.S.F.W.S., 1997). There is evidence from other systems that different habitat corridors (Forman, 1991; Hobbs and Hopkins, 1991), including roads (Tyser and Worley, 1992; Wein et al., 1992), facilitate exotic species invasions. Fourth, soil compaction associated with use and maintenance of dirt roads could collapse burrows and impede burrowing by D. stephensi. Provided that the potential negative effects of dirt road corridors could be adequately minimized, dirt roads or similar pathways (i.e. tractor drags) might be effectively integrated into conservation management plans as corridors to link suitable habitat fragments. However, further research is needed in two areas before dirt roads are promoted in management plans for D. stephensi. First, the scale of movement that is supported by dirt roads needs to be determined. This study was limited to 250 m by the length of the thread spools. Use of radio collars would enable an assessment of road use at larger spatial scales more relevant to dispersal. If dirt roads facilitate movement over larger scales, they could be an effective means of fostering dispersal between fragmented habitats. Second, whether dispersal between habitat patches will actually improve D. stephensi population persistence needs to be determined. As it has not been proven that D. stephensi populations are dispersal limited, it should not be assumed that connectivity will have conservation benefits. The evidence that habitat corridors will benefit D. stephensi, based on simulation modeling (Price and Gilpin, 1996), should be verified by field research before roads are promoted as movement corridors for this species.
Acknowledgements We acknowledge field assistance by Sarah Brown, Matt Forister, Paule Gros, Eddy Konno, Shauna McDonald, Marcelo Tognelli, and Gina Wesley. Comments by Debbie Elliott-Fisk, Sharon Lawlor, and two anonymous reviewers helped to improve the manuscript. This research was supported in part by a grant from the
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Southwestern Riverside County Multi-Species Reserve Management Committee (to DAK). The opinions expressed in this paper are the authors.
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