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Spatial distribution of meadow jumping mice (Zapus hudsonius) in logged boreal forest of northwestern Canada
Mammalian Biology 76 (2011) 678–682
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.de/mambio
Original Investigation
Spatial distribution of meadow jumping mice (Zapus hudsonius) in logged boreal forest of northwestern Canada Thomas S. Jung ∗ , Todd Powell Yukon Department of Environment, P.O. Box 2703, Whitehorse, Yukon Y1A 2C6, Canada
a r t i c l e
i n f o
Article history: Received 3 February 2009 Accepted 5 August 2011 Keywords: Boreal forest management Edge effects Logging Meadow jumping mouse Rarity Small mammal assemblages Yukon Zapus hudsonius
a b s t r a c t Most studies of small mammal responses to habitat alterations focus on dominant species, with a resulting lack of information for rare species. Jumping mice (Order Rodentia: Dipodidae) tend to be rare in small mammal trapping studies; thus, little is known of their response to habitat alterations, such as clear-cut logging. We examined the spatial distribution of meadow jumping mice (Zapus hudsonius) captured in 3 upland habitat types (forest interior, forest edge, and logged forest) in the boreal forest of southeastern Yukon, Canada. Meadow jumping mice were the third most common rodent captured, and consistently constituted 19.7% of captures in all of the habitat types. Meadow jumping mice may not be rare in some boreal mammal assemblages. Significantly less animals were captured in the forest interior compared to the forest edge or logged forest (P < 0.05). A preference or avoidance of sharp habitat edges created by logging was not detected. Logged areas may be more preferred over unlogged areas by meadow jumping mice because they provide relatively diverse and abundant food resources and cover. To provide data more useful for biodiversity conservation, we suggest that studies of small mammals in forest ecosystems deploy a variety of trap types and sample at sufficient intensity to provide information on both dominant and rare species. © 2011 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction Several workers have investigated the impact of forest disturbances on small mammals in Nearctic boreal forest (e.g., Martell 1983; Sullivan et al. 1999; Moses and Boutin 2001; Simon et al. 2002; Pearce and Venier 2005). Most such studies, however, are only able to make comparisons among those species that are captured frequently enough to permit analyses, less is known about the impact of forest disturbances on rare species because sample sizes are too small. For example, small mammal communities in the Nearctic boreal forest tend to be dominated by red-backed voles (Myodes gapperi or M. rutilus) and North American deermice (Peromyscus maniculatus), with these species usually comprising ≥80% of captures in local assemblages (Kirkland 1990; Fisher and Wilkinson 2005). Thus, most investigations on the impact of forest disturbances on small mammal assemblages in the Nearctic boreal forest are focused on these dominant species, even though some of the rare species may (or may not) respond the strongest to habitat alterations. Clearly, if forest managers are to account for biodiversity values in managed landscapes, then a better understanding of
∗ Corresponding author. Tel.: +1 867 667 5766. E-mail addresses: [email protected], ts [email protected] (T.S. Jung).
how forest disturbances affect both common and rare species in small mammal assemblages is required. Jumping mice (Dipodidae) are typically considered rare in studies of small mammal assemblages in the North American boreal forest, comprising <1% of local communities (Krebs and Wingate 1976; Martell 1983; Sullivan et al. 1999; Simon et al. 2002; Pearce and Venier 2005). Available information for meadow jumping mice (Zapus hudsonius) suggests that initially they respond favourably to habitat modifications that remove the forest canopy, such as clearcut logging, but that as the forest regenerates they disappear (reviewed by Kirkland 1990). In their review, Fisher and Wilkinson (2005) noted that jumping mice tend to be associated with grassy areas in these disturbed areas. However, conclusions on the distribution of meadow jumping mice in managed forests tend to be based on low capture rates, and restricted to statements regarding presence or absence from trapping sites. The apparent rarity of jumping mice in boreal forest ecosystems, however, may be because they are difficult to capture in most traps used for small rodents, rather than a measure of their relative abundance in a local area (Edwards 1952; Boonstra and Hoyle 1986). McComb et al. (1991), for instance, demonstrated that pitfall traps were more efficient in capturing jumping mice than snap-traps. In an effort to provide more reliable information on the impact of logging on this apparently rare species, we used pitfall trapping to investigate their spatial distribution in a managed forest landscape
1616-5047/$ – see front matter © 2011 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2011.08.002
T.S. Jung, T. Powell / Mammalian Biology 76 (2011) 678–682
679
7m
11.3 m
vegetation plot
pitfall trap
Fig. 1. Schematic of small mammal and vegetation sampling layout used in southeastern Yukon, Canada, 2005.
in northwestern Canada. Specifically, we were interested in the distribution of meadow jumping mice among recent clearcuts (7–10 years after logging), adjacent unlogged mature boreal forest, and the abrupt ecotone between logged and unlogged forest. Material and methods Study area Our study was conducted in the northern boreal forest, about 10 km northeast of Watson Lake, Yukon, Canada (60.1◦ N, 128.7◦ W). The study area was predominately upland, with a few small ephemeral creeks and ponds. Climate was sub-arctic continental, with a mean annual temperature of −3.1 ◦ C. Mean annual precipitation was 414 mm, with about 60% falling as snow. Snowpack usually began to form by mid-October and persisted until mid-May. Forest in the study area was either recently logged (≥10 years old) or mature (≤120 years old). A sharp contrast (edge) occurred between logged stands and mature stands. Common overstory tree species included: lodgepole pine (Pinus contorta), white spruce (Picea glauca), trembling aspen (Populus tremuloides), balsam poplar (Populus balsmifera), and Alaskan birch (Betula neoalaskana). Common shrubs in the understory included Labrador tea (Ledum groenlandicum), green alder (Alnus crispa), prickly rose (Rosa acicularis), cranberry (Vaccinium vitis-idea), soapberry (Sherperdia canadensis), and willows (e.g., Salix scouleriana). Mature stands typically had a ground cover dominated by moss (e.g., Pleurozium schreberi) with some lichen (e.g., Cladina and Cladonia) and leaf litter. Downed woody debris was abundant. Herbaceous cover included common boreal species such as twinflower (Linnaea borealis), northernbastard toadflax (Geocaulon lividum), fireweed (Epilobium angustifolium), arctic lupine (Lupinus arcticus), and bunchberry (Cornus canadensis). Clearcutting was the harvest method in logged stands. Aspen, spruce and pine saplings, green alder, wild red raspberry (Rubus idaeus), and prickly rose were common in logged stands. Ground cover in logged stands was often downed woody debris and litter, with some herbaceous cover and grasses, but with much less of the moss and lichen cover found in unlogged stands. Fireweed, arctic lupine, and various grasses (Poaceae) were the dominant non-woody plants in logged stands.
meadow jumping mice were believed to be active and not hibernating (Whitaker 1972). At each sampling site (n = 5) we established a trapping grid in each of 3 habitat types: clearcut mixedwood forest (hereafter, logged forest); adjacent mature mixedwood forest (hereafter, forest interior); and the edge habitat where the mature and logged forest met (hereafter, forest edge). Thus, the study design provided 5 replicates of each of the 3 habitat treatments. Logged and unlogged areas were >10 ha. Sampling sites were >5 km apart, and trapping grids within each sampling site (n = 3) were >300 m apart. Trapping grids were >150 m from the forest edge, with the exception of the trapping grid which was placed at the forest edge. Each trapping grid occupied approximately 500 m2 and consisted of 15 trapping stations in a 3 by 5 layout, spaced 7 m apart (Fig. 1). A single unbaited pitfall trap (5l plastic buckets that measured 21 cm diameter by 20 cm deep) was installed flush with the substrate at each trapping station. Drift fences (e.g., Williams and Braun 1983; Bury and Corn 1987) were not used in our trapping grids. Specimens were readily identified from external morphology using Nagorsen (2002). Voucher specimens were deposited at the Museum of Southwestern Biology (Albuquerque, NM, U.S.A.). Vegetation sampling Vegetation sampling and structure was assessed using 2 circular plots situated at each end of the pitfall trapping grid (Fig. 1). Stem density of live and dead trees (≥10 cm dbh and ≥2 m tall) was measured in the 0.04 ha circular plots. Species and diameter at breast height (dbh) of each tree were recorded. Canopy closure and ground cover was measured at 11.3 m from the centre of both vegetation plots, in each of the 4 cardinal directions, and an average of the 8 measures was used. Canopy closure was measured with a spherical densiometer (Lemmon 1956). Ground cover was quantified by taking digital photographs of a 1 m2 quadrat, which were later visually examined on a computer to estimate the percent cover in each quadrat (see Fig. 2 for ground cover types). To reduce observor bias in occular estimates of canopy cover and ground cover (e.g., Gotfryd and Hansell 1985; Vales and Bunnell 1988), the same observer took all of the measurements. Data analyses
Mammal trapping We used 15 pitfall trapping grids to capture small mammals (<60 g) inhabiting the forest substrate at 5 sampling sites from 3 June to 23 October 2005; a period roughly corresponding to when
We calculated a catch per unit effort (CPUE) for each trapping grid. The number of traps disturbed by American black bears (Ursus americanus) was noted, and the technique of Nelson and Clarke (1973) was used to calculate the CPUE, after accounting for the
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T.S. Jung, T. Powell / Mammalian Biology 76 (2011) 678–682
55
A
50
Forest Plots Edge Plots Logged Plots
40
B
35
B
B
30 25 A
20 A
15 A
B
A A
A
C
A
10
A
A A
A B
W e rs oa
r th e
D eb ris
W oo dy
&
oo dy
D
Li ch
eb
en
ris
s
er itt
C
& es
os se s
se H
or
Sa p & G ra ss
bs
A A A
M
ta
ils
gs lin
bs H er ru Sh
AB
Le af L
A
0
O
B
5
Fi ne
Percent Ground Cover
45
Ground Cover Type Fig. 2. Mean (±SE) percentage of ground cover types in 1 m2 quadrats in 3 habitat types (n = 5 replicates each) sampled for meadow jumping mice (Zapus hudsonius) within a managed boreal forest in southeastern Yukon, Canada. Bars with the same letter do not differ significantly in pairwise comparisons (Tukey HSD test). “Other” included bare sand, rock, tree roots and mushrooms.
number of ineffective traps. Because our study design was factorial, we used a 1-way analysis of variance (ANOVA) to test for differences in vegetation structure and meadow jumping mouse captures among habitat types, followed by multiple pairwise comparisons using Tukey’s HSD (Honestly Significant Difference) tests. Visual inspection of box-and-whisker plots indicated that the data were not normal so we applied a square root transformation to count data and an arcsine transformation to percentage data prior to analyses in order to improve homogeneity of variances and approximate normality. Contingency table analysis (log-likelihood ratio X2 tests) was used to test for differences in unreplicated data (i.e., seasonal capture rates). Systat (ver. 9) was used for all statistical analyses. We used an ˛ of P > 0.05 to denote statistical significance.
Results Vegetative structure and ground cover Not surprisingly, MANOVA indicated that structural characteristics and ground cover in our plots differed by habitat type (Wilk’s Lambda = 0.001, F22,4 = 7.327, P = 0.033). Univariate ANOVA and multiple pairwise comparisons revealed that the number of small trees (F2 = 18.084, P < 0.001) and trees (F2 = 33.483, P < 0.001) differed between the habitat types, with more stems in the forest than in the edge or logged habitats, as might be expected. Canopy closure was also greater in the forest than in the edge or logged habitats (F2 = 7.643, P = 0.007). All of the ground cover variables except fine woody debris and other differed by habitat type (P < 0.05; Fig. 2). Logged areas clearly were different than forest or edge habitats in both overstory and ground cover characteristics. While forest and edge habitats differed significantly in overstory characteristics (i.e., stem density of trees and canopy closure), they differed little in terms of the composition of ground cover. Herbs and mosses and lichens constituted greater percent of ground cover in forest and edge habitat than in logged areas (P < 0.05). Percent cover of shrubs and saplings, grasses and horsetails, leaf litter, and coarse woody debris were greater in logged areas than in the forest or edge habitats (P < 0.05; Fig. 2). The only distinguishing feature
of the ground cover between forest and edge plots was that the former had greater percentage of mosses and lichens (Fig. 2). Small mammals We captured 269 small rodents. Meadow jumping mice were the third most captured rodent in our pitfall trapping grids, representing 19.7% of the small rodent assemblage at our sampling sites. Other species of small rodents captured in association with meadow jumping mice included North American deermice (42.8% of captures), northern red-backed voles (29.7%), and unidentified voles (likely Microtus longicaudus, M. pennslyvanicus, M. oeconomus, and Phenacomys ungava; 7.8%). Captures of meadow jumping mice varied among two-week sampling intervals (X2 2 = 10.11, P = 0.006). No jumping mice were captured before 20 July or after 14 September; almost all of the captures (90.3%) occurred between mid-August and mid-September (Fig. 3). Meadow jumping mice were captured in all of the trapping grids except for 1 in the forest interior. The relative abundance of jumping mice, however, differed between the 3 habitat types (F2 = 6.70, P = 0.011), with numbers being highest in logged forest (Fig. 4). Pairwise comparisons revealed that jumping mice were significantly more abundant in logged forest and the forest edge than the forest interior (P ≤ 0.5, Fig. 4). The percentage of the small rodent assemblage that meadow jumping mice constituted did not differ among the habitat types within the sampling sites (F2 = 0.257, P = 0.777; Fig. 4). Discussion Small mammal assemblages Results of most studies of small mammal communities in boreal forests suggest that meadow jumping mice are a relatively rare species in local assemblages, comprising <1% of the number of individuals (e.g., Krebs and Wingate 1976; Martell 1983; Bayne and Hobson 1998; Sullivan et al. 1999; Simon et al. 2002). Meadow
T.S. Jung, T. Powell / Mammalian Biology 76 (2011) 678–682
Fig. 3. Percent of captures of meadow jumping mice (Zapus hudsonius) in pitfall traps in southeastern Yukon, Canada, by two-week sampling periods in 2005. Sampling effort was similar in all sampling intervals.
jumping mice appeared to be a relatively common species in the small mammal assemblages in our sampling sites, ranking as the third most common small rodent. Typically, small rodent communities in the North American boreal forest are dominated by Myodes and Peromyscus, with Microtus being relatively common as well, and all other species tend to be rare (e.g., <5% of the composition of
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communities; Krebs and Wingate 1976). Boonstra and Hoyle (1986) provided some weak evidence that meadow jumping mice compete with Microtus voles, and that jumping mice populations may reach high densities in years when vole populations are low. Microtus populations appeared to be relatively low in our study plots, based on pitfall trapping. Most studies, however, are based on captures in live-traps or snap-traps, which may not be efficient at capturing jumping mice (Edwards 1952; Boonstra and Hoyle 1986; McComb et al. 1991). Concurrent sampling with live-traps in adjacent sampling sites within our study area suggested that meadow jumping mice were rare, as we only caught 3, representing 0.34% of our captures in livetraps (Jung and Powell, unpublished data), compared to about 20% of the small rodent captures in our pitfall traps. It appears that pitfall traps were efficient in capturing meadow jumping mice in upland boreal forest, although our study was not designed to test trap types. McComb et al. (1991) specifically tested the efficiency of pitfall traps in capturing small mammals, including jumping mice, and found that pitfall traps caught more jumping mice then snap-traps. However, it is not clear whether Microtus are also efficiently sampled in pitfall traps, as the literature is conflicting (see: Beacham and Krebs 1980; Boonstra and Rodd 1984). Thus, we do not know whether the relative abundance of meadow jumping mice in our sample was a result of using an appropriate trap type for this species (McComb et al. 1991), or an artifact of the Microtus populations being low during our study and jumping mouse populations positively responding to decreased competition (sensu Boonstra and Hoyle 1986). The relative numerical contribution of jumping mice to small mammal assemblages in the boreal forest remains uncertain and is perhaps best assessed by using a sampling regime that reduces species-specific variation in trappability by using multiple traps types, including pitfall traps.
Percent of the Assemblage (%)
30
1.
A
25
A
A
20 15 10 5 0 7
Mean Number Captured
2. 6
A A
5 4 3
B
2 1 0 Logged Forest
Forest Edge
Forest Interior
Sampling Site Fig. 4. Mean (±SE) number (top) and percentage (bottom) of meadow jumping mice (Zapus hudsonius) captured and in 3 habitat types (n = 5 replicates each) within a managed boreal forest in southeastern Yukon, Canada. Bars with the same letter do not differ significantly in pairwise comparisons.
Spatial distribution of jumping mice Our study yielded adequate captures to provide an initial statistical assessment of the relative abundance and distribution of meadow jumping mice in logged boreal forest. Most studies comparing small mammal populations in logged boreal forest, found a few meadow jumping mice in logged stands but very few or none in the forest interior (e.g., Martell 1983; Sullivan et al. 1999; Simon et al. 2002; Pearce and Venier 2005). For example, Sekgororoane and Dilworth (1995) did not capture any meadow jumping mice <10 m into the forest interior. We found meadow jumping mice in all of our pitfall trapping grids in the forest interior (≤150 m from the forest edge) except one, suggesting that they do spend some time in closed canopy boreal forest. Moreover, they comprised about one-fifth of the small mammal assemblage in the forest interior, similar to logged stands. Our data are insufficient to assess whether meadow jumping mice in our study incorporated the forest interior into their home ranges. Alternatively, given that most of our captures were in the late-summer or fall, perhaps animals captured in the forest interior were simply dispersing from their natal range. Additionally, several workers have commented that the meadow jumping mouse is more transitory than other small rodents (e.g., Alder et al. 1984; Hoyle and Boonstra 1986), and it may be that animals captured in the forest were simply travelling through the forest in search of more suitable habitat patches. Meadow jumping mice were more numerous in logged and forest-edge habitats than in the forest interior, confirming that they prefer open habitats, including clear-cuts. Being primarily granivores and secondarily insectivores (Quimby 1951; Whitaker 1963), jumping mice would likely find more food resources (i.e., grasses and insects) in open habitats than in closed forest with a high percentage of moss and lichen ground cover. In addition, more abundant coarse woody debris (downed logs and stumps) in the
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logged and forest-edge habitats likely provided more opportunities for jumping mice to find food (invertebrates) and cover from inclement weather and predators. We are unable, however, to distinguish whether numerical abundance equates to higher fitness in selected habitats (sensu Van Horne 1983). We failed to find any evidence of preference for forest edges by meadow jumping mice. Captures were more than 2 times greater at the forest-clearcut edge than in the forest interior, but about the same as in the logged forest. Similarity in the ground cover composition between the forest interior and forest edges is contrary to our capture of jumping mice, with similar capture rates in logged and forest edge habitats. We suggest that the increased openness of the canopy, and resulting greater percentage of grasses and horsetails (i.e., food) and coarse woody debris (i.e., shelter) in both logged and edge habitats makes those areas more suitable habitat than the forest-interior for jumping mice. In sub-boreal conifer forest in eastern Canada, the data of Sekgororoane and Dilworth (1995) suggested similar. Combined these results suggest that meadow jumping mice do not prefer or avoid forest edges, which may provide similar resources as clearcut logged forest. Conclusions Our study provides necessary information on the spatial distribution of one apparently rare small mammal in logged boreal forest. Similar data for this or other apparently rare species is often lacking. Provision of data for both dominant and rare species allows a more fulsome consideration of the impacts of logging on biodiversity. Acknowledgements We thank Riley Broadhagen, Karen Clyde, Matthias Clyde, Jason Colbert, Piia Kukka, Matt Larsen, Angela Milani, Marina Milligan, Kieran O’Donovan, Shannon Powell, and Kyle Russell for field assistance. Funding was provided by the Yukon Department of Environment. John Whitaker, Jr., kindly provided helpful comments on an earlier draft of the manuscript. References Alder, G.H., Reich, L.M., Tamarin, R.H., 1984. Demography of the meadow jumping mouse (Zapus hudsonius) in eastern Massachusetts. Am. Midl. Nat. 112, 387–391. Bayne, E.M., Hobson, K.A., 1998. The effects of habitat fragmentation by forestry and agriculture on the abundance of small mammals in the southern boreal mixedwood forest. Can. J. Zool. 76, 62–69.
Beacham, T.D., Krebs, C.J., 1980. Pitfall versus live-trap enumeration of fluctuating populations of Microtus townsendii. J. Mammal 61, 486–499. Boonstra, R., Hoyle, J.A., 1986. Rarity and coexistence of a small hibernator, Zapus hudsonius, with fluctuating populations of Microtus pennsylvanicus in the grasslands of Southern Ontario. J. Anim. Ecol. 55, 773–784. Boonstra, R., Rodd, F.H., 1984. Efficiency of pitfalls versus live traps in enumeration of populations of Microtus pennsylvanius. Can. J. Zool. 62, 758–765. Bury, R.B., Corn, P.S., 1987. Evaluation of pitfall trapping in northwestern forests: trap arrays with drift fences. J. Wildl. Manage. 51, 112–119. Edwards, R.Y., 1952. How efficient are snap traps in taking small mammals? J. Mammal 33, 497–498. Fisher, J.T., Wilkinson, L., 2005. The response of mammals to forest fire and timber harvest in the North American boreal forest. Mamm. Rev. 35, 51–81. Gotfryd, A., Hansell, R.I.C., 1985. The impact of observer bias on multivariate analyses of vegetation structure. Oikos 45, 223–234. Hoyle, J.A., Boonstra, R., 1986. Life history traits of the meadow jumping mouse, Zapus hudsonius, in southern Ontario. Can. Field-Nat. 100, 537–544. Kirkland Jr., G.L., 1990. Patterns of initial small mammal community change after clearcutting of temperate North American forests. Oikos 59, 313–320. Krebs, C.J., Wingate, I., 1976. Small mammal communities of the Kluane Region, Yukon Territory. Can. Field-Nat. 90, 379–389. Lemmon, R.E., 1956. A spherical densiometer for estimating forest overstory density. Forest Sci. 2, 314–320. Martell, A.M., 1983. Changes in small mammal communities after logging in northcentral Ontario. Can. J. Zool. 61, 970–980. McComb, W.C., Anthony, R.G., McGarigal, K., 1991. Differential vulnerability of small mammals and amphibians to two trap types and two trap baits in Pacific Northwest forests. Northwest Sci. 65, 109–115. Moses, R.A., Boutin, S., 2001. The influence of clear-cut logging and residual leave material on small mammal populations in aspen-dominated boreal mixedwoods. Can. J. Forest Res. 31, 483–495. Nagorsen, D.W., 2002. Rodents and Lagomorphs of British Columbia. University of British Columbia Press, Vancouver, British Columbia. Nelson, L., Clarke, F.W., 1973. Correction for sprung traps in catch/effort calculations of trapping results. J. Mammal 54, 295–298. Pearce, J., Venier, L., 2005. Small mammals as bioindicators of sustainable boreal forest management. Forest Ecol. Manage. 208, 153–175. Quimby, D.C., 1951. The life history and ecology of the jumping mouse, Zapus hudsonius. Ecol. Monogr. 21, 61–95. Sekgororoane, G.B., Dilworth, T.G., 1995. Relative abundance, richness, and diversity of small mammals at induced forest edges. Can. J. Zool. 73, 1432–1437. Simon, N.P.P., Stratton, C.B., Forbes, G.J., Schwab, F.E., 2002. Similarity of small mammal abundance in post-fire and clearcut forests. Forest Ecol. Manage. 165, 163–172. Sullivan, T.P., Lautenschlager, R.A., Wagner, R.G., 1999. Clearcutting and burning of northern spruce-fir forests: implications for small mammals. J. Appl. Ecol. 36, 327–344. Vales, D.J., Bunnell, F.L., 1988. Comparison of methods for estimating forest overstory cover. I. Observer effects. Can. J. Forest Res. 18, 606–609. Van Horne, B., 1983. Density as a misleading indicator of habitat quality. J. Wildl. Manage. 47, 893–901. Whitaker Jr., J.O., 1963. A study of the meadow jumping mouse, Zapus hudsonius (Zimmerman), in central New York. Ecol. Monogr. 33, 215–254. Whitaker Jr., J.O., 1972. Zapus hudsonius. Mammal. Species 11, 1–7. Williams, D.F., Braun, S.E., 1983. Comparison of pitfall and conventional traps for sampling small mammal populations. J. Wildl. Manage. 47, 841–845.
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.de/mambio
Original Investigation
Spatial distribution of meadow jumping mice (Zapus hudsonius) in logged boreal forest of northwestern Canada Thomas S. Jung ∗ , Todd Powell Yukon Department of Environment, P.O. Box 2703, Whitehorse, Yukon Y1A 2C6, Canada
a r t i c l e
i n f o
Article history: Received 3 February 2009 Accepted 5 August 2011 Keywords: Boreal forest management Edge effects Logging Meadow jumping mouse Rarity Small mammal assemblages Yukon Zapus hudsonius
a b s t r a c t Most studies of small mammal responses to habitat alterations focus on dominant species, with a resulting lack of information for rare species. Jumping mice (Order Rodentia: Dipodidae) tend to be rare in small mammal trapping studies; thus, little is known of their response to habitat alterations, such as clear-cut logging. We examined the spatial distribution of meadow jumping mice (Zapus hudsonius) captured in 3 upland habitat types (forest interior, forest edge, and logged forest) in the boreal forest of southeastern Yukon, Canada. Meadow jumping mice were the third most common rodent captured, and consistently constituted 19.7% of captures in all of the habitat types. Meadow jumping mice may not be rare in some boreal mammal assemblages. Significantly less animals were captured in the forest interior compared to the forest edge or logged forest (P < 0.05). A preference or avoidance of sharp habitat edges created by logging was not detected. Logged areas may be more preferred over unlogged areas by meadow jumping mice because they provide relatively diverse and abundant food resources and cover. To provide data more useful for biodiversity conservation, we suggest that studies of small mammals in forest ecosystems deploy a variety of trap types and sample at sufficient intensity to provide information on both dominant and rare species. © 2011 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction Several workers have investigated the impact of forest disturbances on small mammals in Nearctic boreal forest (e.g., Martell 1983; Sullivan et al. 1999; Moses and Boutin 2001; Simon et al. 2002; Pearce and Venier 2005). Most such studies, however, are only able to make comparisons among those species that are captured frequently enough to permit analyses, less is known about the impact of forest disturbances on rare species because sample sizes are too small. For example, small mammal communities in the Nearctic boreal forest tend to be dominated by red-backed voles (Myodes gapperi or M. rutilus) and North American deermice (Peromyscus maniculatus), with these species usually comprising ≥80% of captures in local assemblages (Kirkland 1990; Fisher and Wilkinson 2005). Thus, most investigations on the impact of forest disturbances on small mammal assemblages in the Nearctic boreal forest are focused on these dominant species, even though some of the rare species may (or may not) respond the strongest to habitat alterations. Clearly, if forest managers are to account for biodiversity values in managed landscapes, then a better understanding of
∗ Corresponding author. Tel.: +1 867 667 5766. E-mail addresses: [email protected], ts [email protected] (T.S. Jung).
how forest disturbances affect both common and rare species in small mammal assemblages is required. Jumping mice (Dipodidae) are typically considered rare in studies of small mammal assemblages in the North American boreal forest, comprising <1% of local communities (Krebs and Wingate 1976; Martell 1983; Sullivan et al. 1999; Simon et al. 2002; Pearce and Venier 2005). Available information for meadow jumping mice (Zapus hudsonius) suggests that initially they respond favourably to habitat modifications that remove the forest canopy, such as clearcut logging, but that as the forest regenerates they disappear (reviewed by Kirkland 1990). In their review, Fisher and Wilkinson (2005) noted that jumping mice tend to be associated with grassy areas in these disturbed areas. However, conclusions on the distribution of meadow jumping mice in managed forests tend to be based on low capture rates, and restricted to statements regarding presence or absence from trapping sites. The apparent rarity of jumping mice in boreal forest ecosystems, however, may be because they are difficult to capture in most traps used for small rodents, rather than a measure of their relative abundance in a local area (Edwards 1952; Boonstra and Hoyle 1986). McComb et al. (1991), for instance, demonstrated that pitfall traps were more efficient in capturing jumping mice than snap-traps. In an effort to provide more reliable information on the impact of logging on this apparently rare species, we used pitfall trapping to investigate their spatial distribution in a managed forest landscape
1616-5047/$ – see front matter © 2011 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2011.08.002
T.S. Jung, T. Powell / Mammalian Biology 76 (2011) 678–682
679
7m
11.3 m
vegetation plot
pitfall trap
Fig. 1. Schematic of small mammal and vegetation sampling layout used in southeastern Yukon, Canada, 2005.
in northwestern Canada. Specifically, we were interested in the distribution of meadow jumping mice among recent clearcuts (7–10 years after logging), adjacent unlogged mature boreal forest, and the abrupt ecotone between logged and unlogged forest. Material and methods Study area Our study was conducted in the northern boreal forest, about 10 km northeast of Watson Lake, Yukon, Canada (60.1◦ N, 128.7◦ W). The study area was predominately upland, with a few small ephemeral creeks and ponds. Climate was sub-arctic continental, with a mean annual temperature of −3.1 ◦ C. Mean annual precipitation was 414 mm, with about 60% falling as snow. Snowpack usually began to form by mid-October and persisted until mid-May. Forest in the study area was either recently logged (≥10 years old) or mature (≤120 years old). A sharp contrast (edge) occurred between logged stands and mature stands. Common overstory tree species included: lodgepole pine (Pinus contorta), white spruce (Picea glauca), trembling aspen (Populus tremuloides), balsam poplar (Populus balsmifera), and Alaskan birch (Betula neoalaskana). Common shrubs in the understory included Labrador tea (Ledum groenlandicum), green alder (Alnus crispa), prickly rose (Rosa acicularis), cranberry (Vaccinium vitis-idea), soapberry (Sherperdia canadensis), and willows (e.g., Salix scouleriana). Mature stands typically had a ground cover dominated by moss (e.g., Pleurozium schreberi) with some lichen (e.g., Cladina and Cladonia) and leaf litter. Downed woody debris was abundant. Herbaceous cover included common boreal species such as twinflower (Linnaea borealis), northernbastard toadflax (Geocaulon lividum), fireweed (Epilobium angustifolium), arctic lupine (Lupinus arcticus), and bunchberry (Cornus canadensis). Clearcutting was the harvest method in logged stands. Aspen, spruce and pine saplings, green alder, wild red raspberry (Rubus idaeus), and prickly rose were common in logged stands. Ground cover in logged stands was often downed woody debris and litter, with some herbaceous cover and grasses, but with much less of the moss and lichen cover found in unlogged stands. Fireweed, arctic lupine, and various grasses (Poaceae) were the dominant non-woody plants in logged stands.
meadow jumping mice were believed to be active and not hibernating (Whitaker 1972). At each sampling site (n = 5) we established a trapping grid in each of 3 habitat types: clearcut mixedwood forest (hereafter, logged forest); adjacent mature mixedwood forest (hereafter, forest interior); and the edge habitat where the mature and logged forest met (hereafter, forest edge). Thus, the study design provided 5 replicates of each of the 3 habitat treatments. Logged and unlogged areas were >10 ha. Sampling sites were >5 km apart, and trapping grids within each sampling site (n = 3) were >300 m apart. Trapping grids were >150 m from the forest edge, with the exception of the trapping grid which was placed at the forest edge. Each trapping grid occupied approximately 500 m2 and consisted of 15 trapping stations in a 3 by 5 layout, spaced 7 m apart (Fig. 1). A single unbaited pitfall trap (5l plastic buckets that measured 21 cm diameter by 20 cm deep) was installed flush with the substrate at each trapping station. Drift fences (e.g., Williams and Braun 1983; Bury and Corn 1987) were not used in our trapping grids. Specimens were readily identified from external morphology using Nagorsen (2002). Voucher specimens were deposited at the Museum of Southwestern Biology (Albuquerque, NM, U.S.A.). Vegetation sampling Vegetation sampling and structure was assessed using 2 circular plots situated at each end of the pitfall trapping grid (Fig. 1). Stem density of live and dead trees (≥10 cm dbh and ≥2 m tall) was measured in the 0.04 ha circular plots. Species and diameter at breast height (dbh) of each tree were recorded. Canopy closure and ground cover was measured at 11.3 m from the centre of both vegetation plots, in each of the 4 cardinal directions, and an average of the 8 measures was used. Canopy closure was measured with a spherical densiometer (Lemmon 1956). Ground cover was quantified by taking digital photographs of a 1 m2 quadrat, which were later visually examined on a computer to estimate the percent cover in each quadrat (see Fig. 2 for ground cover types). To reduce observor bias in occular estimates of canopy cover and ground cover (e.g., Gotfryd and Hansell 1985; Vales and Bunnell 1988), the same observer took all of the measurements. Data analyses
Mammal trapping We used 15 pitfall trapping grids to capture small mammals (<60 g) inhabiting the forest substrate at 5 sampling sites from 3 June to 23 October 2005; a period roughly corresponding to when
We calculated a catch per unit effort (CPUE) for each trapping grid. The number of traps disturbed by American black bears (Ursus americanus) was noted, and the technique of Nelson and Clarke (1973) was used to calculate the CPUE, after accounting for the
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Ground Cover Type Fig. 2. Mean (±SE) percentage of ground cover types in 1 m2 quadrats in 3 habitat types (n = 5 replicates each) sampled for meadow jumping mice (Zapus hudsonius) within a managed boreal forest in southeastern Yukon, Canada. Bars with the same letter do not differ significantly in pairwise comparisons (Tukey HSD test). “Other” included bare sand, rock, tree roots and mushrooms.
number of ineffective traps. Because our study design was factorial, we used a 1-way analysis of variance (ANOVA) to test for differences in vegetation structure and meadow jumping mouse captures among habitat types, followed by multiple pairwise comparisons using Tukey’s HSD (Honestly Significant Difference) tests. Visual inspection of box-and-whisker plots indicated that the data were not normal so we applied a square root transformation to count data and an arcsine transformation to percentage data prior to analyses in order to improve homogeneity of variances and approximate normality. Contingency table analysis (log-likelihood ratio X2 tests) was used to test for differences in unreplicated data (i.e., seasonal capture rates). Systat (ver. 9) was used for all statistical analyses. We used an ˛ of P > 0.05 to denote statistical significance.
Results Vegetative structure and ground cover Not surprisingly, MANOVA indicated that structural characteristics and ground cover in our plots differed by habitat type (Wilk’s Lambda = 0.001, F22,4 = 7.327, P = 0.033). Univariate ANOVA and multiple pairwise comparisons revealed that the number of small trees (F2 = 18.084, P < 0.001) and trees (F2 = 33.483, P < 0.001) differed between the habitat types, with more stems in the forest than in the edge or logged habitats, as might be expected. Canopy closure was also greater in the forest than in the edge or logged habitats (F2 = 7.643, P = 0.007). All of the ground cover variables except fine woody debris and other differed by habitat type (P < 0.05; Fig. 2). Logged areas clearly were different than forest or edge habitats in both overstory and ground cover characteristics. While forest and edge habitats differed significantly in overstory characteristics (i.e., stem density of trees and canopy closure), they differed little in terms of the composition of ground cover. Herbs and mosses and lichens constituted greater percent of ground cover in forest and edge habitat than in logged areas (P < 0.05). Percent cover of shrubs and saplings, grasses and horsetails, leaf litter, and coarse woody debris were greater in logged areas than in the forest or edge habitats (P < 0.05; Fig. 2). The only distinguishing feature
of the ground cover between forest and edge plots was that the former had greater percentage of mosses and lichens (Fig. 2). Small mammals We captured 269 small rodents. Meadow jumping mice were the third most captured rodent in our pitfall trapping grids, representing 19.7% of the small rodent assemblage at our sampling sites. Other species of small rodents captured in association with meadow jumping mice included North American deermice (42.8% of captures), northern red-backed voles (29.7%), and unidentified voles (likely Microtus longicaudus, M. pennslyvanicus, M. oeconomus, and Phenacomys ungava; 7.8%). Captures of meadow jumping mice varied among two-week sampling intervals (X2 2 = 10.11, P = 0.006). No jumping mice were captured before 20 July or after 14 September; almost all of the captures (90.3%) occurred between mid-August and mid-September (Fig. 3). Meadow jumping mice were captured in all of the trapping grids except for 1 in the forest interior. The relative abundance of jumping mice, however, differed between the 3 habitat types (F2 = 6.70, P = 0.011), with numbers being highest in logged forest (Fig. 4). Pairwise comparisons revealed that jumping mice were significantly more abundant in logged forest and the forest edge than the forest interior (P ≤ 0.5, Fig. 4). The percentage of the small rodent assemblage that meadow jumping mice constituted did not differ among the habitat types within the sampling sites (F2 = 0.257, P = 0.777; Fig. 4). Discussion Small mammal assemblages Results of most studies of small mammal communities in boreal forests suggest that meadow jumping mice are a relatively rare species in local assemblages, comprising <1% of the number of individuals (e.g., Krebs and Wingate 1976; Martell 1983; Bayne and Hobson 1998; Sullivan et al. 1999; Simon et al. 2002). Meadow
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Fig. 3. Percent of captures of meadow jumping mice (Zapus hudsonius) in pitfall traps in southeastern Yukon, Canada, by two-week sampling periods in 2005. Sampling effort was similar in all sampling intervals.
jumping mice appeared to be a relatively common species in the small mammal assemblages in our sampling sites, ranking as the third most common small rodent. Typically, small rodent communities in the North American boreal forest are dominated by Myodes and Peromyscus, with Microtus being relatively common as well, and all other species tend to be rare (e.g., <5% of the composition of
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communities; Krebs and Wingate 1976). Boonstra and Hoyle (1986) provided some weak evidence that meadow jumping mice compete with Microtus voles, and that jumping mice populations may reach high densities in years when vole populations are low. Microtus populations appeared to be relatively low in our study plots, based on pitfall trapping. Most studies, however, are based on captures in live-traps or snap-traps, which may not be efficient at capturing jumping mice (Edwards 1952; Boonstra and Hoyle 1986; McComb et al. 1991). Concurrent sampling with live-traps in adjacent sampling sites within our study area suggested that meadow jumping mice were rare, as we only caught 3, representing 0.34% of our captures in livetraps (Jung and Powell, unpublished data), compared to about 20% of the small rodent captures in our pitfall traps. It appears that pitfall traps were efficient in capturing meadow jumping mice in upland boreal forest, although our study was not designed to test trap types. McComb et al. (1991) specifically tested the efficiency of pitfall traps in capturing small mammals, including jumping mice, and found that pitfall traps caught more jumping mice then snap-traps. However, it is not clear whether Microtus are also efficiently sampled in pitfall traps, as the literature is conflicting (see: Beacham and Krebs 1980; Boonstra and Rodd 1984). Thus, we do not know whether the relative abundance of meadow jumping mice in our sample was a result of using an appropriate trap type for this species (McComb et al. 1991), or an artifact of the Microtus populations being low during our study and jumping mouse populations positively responding to decreased competition (sensu Boonstra and Hoyle 1986). The relative numerical contribution of jumping mice to small mammal assemblages in the boreal forest remains uncertain and is perhaps best assessed by using a sampling regime that reduces species-specific variation in trappability by using multiple traps types, including pitfall traps.
Percent of the Assemblage (%)
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Sampling Site Fig. 4. Mean (±SE) number (top) and percentage (bottom) of meadow jumping mice (Zapus hudsonius) captured and in 3 habitat types (n = 5 replicates each) within a managed boreal forest in southeastern Yukon, Canada. Bars with the same letter do not differ significantly in pairwise comparisons.
Spatial distribution of jumping mice Our study yielded adequate captures to provide an initial statistical assessment of the relative abundance and distribution of meadow jumping mice in logged boreal forest. Most studies comparing small mammal populations in logged boreal forest, found a few meadow jumping mice in logged stands but very few or none in the forest interior (e.g., Martell 1983; Sullivan et al. 1999; Simon et al. 2002; Pearce and Venier 2005). For example, Sekgororoane and Dilworth (1995) did not capture any meadow jumping mice <10 m into the forest interior. We found meadow jumping mice in all of our pitfall trapping grids in the forest interior (≤150 m from the forest edge) except one, suggesting that they do spend some time in closed canopy boreal forest. Moreover, they comprised about one-fifth of the small mammal assemblage in the forest interior, similar to logged stands. Our data are insufficient to assess whether meadow jumping mice in our study incorporated the forest interior into their home ranges. Alternatively, given that most of our captures were in the late-summer or fall, perhaps animals captured in the forest interior were simply dispersing from their natal range. Additionally, several workers have commented that the meadow jumping mouse is more transitory than other small rodents (e.g., Alder et al. 1984; Hoyle and Boonstra 1986), and it may be that animals captured in the forest were simply travelling through the forest in search of more suitable habitat patches. Meadow jumping mice were more numerous in logged and forest-edge habitats than in the forest interior, confirming that they prefer open habitats, including clear-cuts. Being primarily granivores and secondarily insectivores (Quimby 1951; Whitaker 1963), jumping mice would likely find more food resources (i.e., grasses and insects) in open habitats than in closed forest with a high percentage of moss and lichen ground cover. In addition, more abundant coarse woody debris (downed logs and stumps) in the
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logged and forest-edge habitats likely provided more opportunities for jumping mice to find food (invertebrates) and cover from inclement weather and predators. We are unable, however, to distinguish whether numerical abundance equates to higher fitness in selected habitats (sensu Van Horne 1983). We failed to find any evidence of preference for forest edges by meadow jumping mice. Captures were more than 2 times greater at the forest-clearcut edge than in the forest interior, but about the same as in the logged forest. Similarity in the ground cover composition between the forest interior and forest edges is contrary to our capture of jumping mice, with similar capture rates in logged and forest edge habitats. We suggest that the increased openness of the canopy, and resulting greater percentage of grasses and horsetails (i.e., food) and coarse woody debris (i.e., shelter) in both logged and edge habitats makes those areas more suitable habitat than the forest-interior for jumping mice. In sub-boreal conifer forest in eastern Canada, the data of Sekgororoane and Dilworth (1995) suggested similar. Combined these results suggest that meadow jumping mice do not prefer or avoid forest edges, which may provide similar resources as clearcut logged forest. Conclusions Our study provides necessary information on the spatial distribution of one apparently rare small mammal in logged boreal forest. Similar data for this or other apparently rare species is often lacking. Provision of data for both dominant and rare species allows a more fulsome consideration of the impacts of logging on biodiversity. Acknowledgements We thank Riley Broadhagen, Karen Clyde, Matthias Clyde, Jason Colbert, Piia Kukka, Matt Larsen, Angela Milani, Marina Milligan, Kieran O’Donovan, Shannon Powell, and Kyle Russell for field assistance. Funding was provided by the Yukon Department of Environment. John Whitaker, Jr., kindly provided helpful comments on an earlier draft of the manuscript. References Alder, G.H., Reich, L.M., Tamarin, R.H., 1984. Demography of the meadow jumping mouse (Zapus hudsonius) in eastern Massachusetts. Am. Midl. Nat. 112, 387–391. Bayne, E.M., Hobson, K.A., 1998. The effects of habitat fragmentation by forestry and agriculture on the abundance of small mammals in the southern boreal mixedwood forest. Can. J. Zool. 76, 62–69.
Beacham, T.D., Krebs, C.J., 1980. Pitfall versus live-trap enumeration of fluctuating populations of Microtus townsendii. J. Mammal 61, 486–499. Boonstra, R., Hoyle, J.A., 1986. Rarity and coexistence of a small hibernator, Zapus hudsonius, with fluctuating populations of Microtus pennsylvanicus in the grasslands of Southern Ontario. J. Anim. Ecol. 55, 773–784. Boonstra, R., Rodd, F.H., 1984. Efficiency of pitfalls versus live traps in enumeration of populations of Microtus pennsylvanius. Can. J. Zool. 62, 758–765. Bury, R.B., Corn, P.S., 1987. Evaluation of pitfall trapping in northwestern forests: trap arrays with drift fences. J. Wildl. Manage. 51, 112–119. Edwards, R.Y., 1952. How efficient are snap traps in taking small mammals? J. Mammal 33, 497–498. Fisher, J.T., Wilkinson, L., 2005. The response of mammals to forest fire and timber harvest in the North American boreal forest. Mamm. Rev. 35, 51–81. Gotfryd, A., Hansell, R.I.C., 1985. The impact of observer bias on multivariate analyses of vegetation structure. Oikos 45, 223–234. Hoyle, J.A., Boonstra, R., 1986. Life history traits of the meadow jumping mouse, Zapus hudsonius, in southern Ontario. Can. Field-Nat. 100, 537–544. Kirkland Jr., G.L., 1990. Patterns of initial small mammal community change after clearcutting of temperate North American forests. Oikos 59, 313–320. Krebs, C.J., Wingate, I., 1976. Small mammal communities of the Kluane Region, Yukon Territory. Can. Field-Nat. 90, 379–389. Lemmon, R.E., 1956. A spherical densiometer for estimating forest overstory density. Forest Sci. 2, 314–320. Martell, A.M., 1983. Changes in small mammal communities after logging in northcentral Ontario. Can. J. Zool. 61, 970–980. McComb, W.C., Anthony, R.G., McGarigal, K., 1991. Differential vulnerability of small mammals and amphibians to two trap types and two trap baits in Pacific Northwest forests. Northwest Sci. 65, 109–115. Moses, R.A., Boutin, S., 2001. The influence of clear-cut logging and residual leave material on small mammal populations in aspen-dominated boreal mixedwoods. Can. J. Forest Res. 31, 483–495. Nagorsen, D.W., 2002. Rodents and Lagomorphs of British Columbia. University of British Columbia Press, Vancouver, British Columbia. Nelson, L., Clarke, F.W., 1973. Correction for sprung traps in catch/effort calculations of trapping results. J. Mammal 54, 295–298. Pearce, J., Venier, L., 2005. Small mammals as bioindicators of sustainable boreal forest management. Forest Ecol. Manage. 208, 153–175. Quimby, D.C., 1951. The life history and ecology of the jumping mouse, Zapus hudsonius. Ecol. Monogr. 21, 61–95. Sekgororoane, G.B., Dilworth, T.G., 1995. Relative abundance, richness, and diversity of small mammals at induced forest edges. Can. J. Zool. 73, 1432–1437. Simon, N.P.P., Stratton, C.B., Forbes, G.J., Schwab, F.E., 2002. Similarity of small mammal abundance in post-fire and clearcut forests. Forest Ecol. Manage. 165, 163–172. Sullivan, T.P., Lautenschlager, R.A., Wagner, R.G., 1999. Clearcutting and burning of northern spruce-fir forests: implications for small mammals. J. Appl. Ecol. 36, 327–344. Vales, D.J., Bunnell, F.L., 1988. Comparison of methods for estimating forest overstory cover. I. Observer effects. Can. J. Forest Res. 18, 606–609. Van Horne, B., 1983. Density as a misleading indicator of habitat quality. J. Wildl. Manage. 47, 893–901. Whitaker Jr., J.O., 1963. A study of the meadow jumping mouse, Zapus hudsonius (Zimmerman), in central New York. Ecol. Monogr. 33, 215–254. Whitaker Jr., J.O., 1972. Zapus hudsonius. Mammal. Species 11, 1–7. Williams, D.F., Braun, S.E., 1983. Comparison of pitfall and conventional traps for sampling small mammal populations. J. Wildl. Manage. 47, 841–845.