landscape-scale features affecting small mammal assemblages on the northern great plains of north...

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Landscape-scale features affecting small mammal assemblages on the northernGreat Plains of North AmericaAuthor(s): Leanne M. Heisler , Christopher M. Somers , Troy I. Wellicome , and Ray G. PoulinSource: Journal of Mammalogy, 94(5):1059-1067. 2013.Published By: American Society of MammalogistsURL: http://www.bioone.org/doi/full/10.1644/13-MAMM-A-022.1

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Journal of Mammalogy, 94(5):1059–1067, 2013

Landscape-scale features affecting small mammal assemblages on thenorthern Great Plains of North America

LEANNE M. HEISLER, CHRISTOPHER M. SOMERS, TROY I. WELLICOME, AND RAY G. POULIN*

Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, Saskatchewan S4S 0A2, Canada (LMH,CMS)Department of Biological Sciences, University of Alberta, 11455 Saskatchewan Drive, Edmonton, Alberta T6B 2X3,Canada (TIW)Canadian Wildlife Service, Environment Canada, 4999-98th Avenue, Edmonton, Alberta T6B 2X3, Canada (TIW)Royal Saskatchewan Museum, 2340 Albert Street, Regina, Saskatchewan S4P 4W7, Canada (RGP)

* Correspondent: [email protected]

Little is known about the macrohabitat associations of rodents and shrews in prairie landscapes because of the

logistic constraints of conventional trapping. We used the remains of 60,972 small mammals in owl pellets to

assess factors affecting small mammal composition across 4.3 million hectares of the northern Great Plains of

North America. Cropland with clay soils was dominated by deer mice (Peromyscus maniculatus), whereas areas

with higher proportions of native grassland and moderately sandy soils supported communities with more

sagebrush voles (Lemmiscus curtatus). Areas with clay soils and higher annual precipitation were associated

with higher proportions of house mice (Mus musculus), meadow voles (Microtus pennsylvanicus), and shrews

(Blarina brevicauda and Sorex species), whereas drier areas with sandier soils and lower annual precipitation

were dominated by olive-backed pocket mice (Perognathus fasciatus) and northern grasshopper mice

(Onychomys leucogaster). Contrary to extrapolations of previous smaller-scale efforts, soil texture was the

primary landscape feature driving small mammal composition in our study, whereas agricultural cropland

significantly altered the composition of these assemblages. These associations demonstrate the importance of

considering macrohabitats encompassing entire populations.

Key words: agriculture, grassland, macrohabitat, owl pellet, rodent, shrew, soil

� 2013 American Society of Mammalogists

DOI: 10.1644/13-MAMM-A-022.1

Small mammals, such as mice, shrews, and voles, are vital

components of most terrestrial ecosystems (Gibbons 1988);

however, we know little about the factors affecting their

distribution and abundance over landscape spatial scales. Small

mammals influence ecosystems of the northern Great Plains by

serving as a food source for a wide variety of predators,

altering plant communities through caching or consuming

vegetation and seeds, and altering soil conditions or providing

habitat for other species through burrowing activities (Sieg

1987). Some of these influences can change species distribu-

tions by eliciting population-level responses across hundreds of

kilometers (landscape-scale—Grant and French 1980; Jaksic

and Simonetti 1987; Marti 1987). Despite their importance,

most small mammal studies have focused on small-scale

factors affecting habitat selection for specific resources, such as

food, nest sites, or refuges, within individual home ranges

(microhabitats). However, microhabitats are inherently con-

strained by the availability of the larger habitats encompassing

the home ranges of entire populations (macrohabitats—Morris

1987; Jorgensen and Demarais 1999; Mayor et al. 2009). These

landscape-scale patterns may not be apparent in studies

focusing on habitat selection within individual home ranges,

warranting a closer look at how small mammals distribute

themselves among macrohabitat types in heterogeneous

landscapes.

The scope of most previous small mammal studies has been

limited by conventional sampling techniques. Sampling small

mammal assemblages generally involves conventional trapping

methods that are relatively expensive and time consuming;

limiting these studies to small spatial or temporal scales, or

both (Hanser et al. 2011). In addition, trapping is affected by

sampling biases regardless of the type of trap or bait used. For

w w w . m a m m a l o g y . o r g

1059

http://www.mammalogy.org

example, the accuracy of the trapping session is dependent

upon weather; season; moon phase; population density; food

availability; and the age, size, and sex of the small mammals

(Wiener and Smith 1972; O’Farrell 1994), and is sensitive to

sampling effort and location (Hanser et al. 2011). Also,

trapping usually occurs in only a few distinguishable

vegetation types, limiting the results to a small subset of the

existing community (Hanser et al. 2011). These sampling

constraints have led to a lack of landscape-scale studies,

limiting the perspective of published research and effectively

inhibiting investigation of the environmental factors affecting

populations at broader spatial scales (Jorgensen 2004). To

overcome this limitation, an alternative method is needed to

sample small mammal communities across larger spatial scales.

We considered owls as another method for sampling small

mammal communities. Owls tend to focus on small mammals

while foraging and do so within a defined area (i.e., the

foraging range of the individual owl—Porder et al. 2003;

Feranec et al. 2007). Conveniently, owls regurgitate the

indigestible parts of their prey (e.g., bones) and deposit these

pellets in large quantities at their nest and roost sites (Errington

1930). The bones found within the owl pellets are usually

identifiable to species (depending on the species and the

condition of the pellet contents) and allow researchers to

quantify the animals eaten by the owls. However, similar to

conventional trapping, owl pellet sampling is not without

potential biases. In particular, owl pellets may be biased toward

species that are more available as prey based on the hunting

strategies and habitats owls use while foraging (Wooster 1936;

Glue 1970; Fulk 1976; Torre et al. 2004). Despite this

potential, some studies have found little difference in

proportional abundance and taxonomic composition between

conventional trapping results and prey assemblages inferred

from owl pellet data sets (Terry 2010). In addition, several

generalist owl species show clear functional relationships to

fluctuating prey abundances, indicating that owls consume prey

species that are the most available, and that owls are able to

switch between prey species depending on their relative

abundance (Rusch et al. 1972; Jaksic and Marti 1984; Silva

et al. 1995; Zimmerman et al. 1996; Poulin et al. 2001).

Together, these features of generalist owl diet suggest that

pellet composition should be a good reflection of the small

mammal assemblage in the foraging range of the owl. How-

ever, few studies have capitalized on widely distributed owls to

examine small mammal communities over large spatial scales.

Here, we use great horned (Bubo virginianus) and burrowing

owl (Athene cunicularia) pellets to examine factors that

influence small mammal composition across the northern Great

Plains of North America. This vast region of the Great Plains in

western Canada is a heterogeneous landscape characterized by

climatic, soil, and land-use variation that has the potential to

affect small mammal species composition (Coupland 1950).

Burrowing and great horned owls are dietary generalist species

that are widespread across the Great Plains; they consume a

variety of small mammal species, and their pellets provide an

excellent opportunity to examine the landscape-scale compo-

sition of prairie small mammal assemblages and their macro-

habitat associations. Our objectives were to identify the

environmental factors primarily responsible for small mammal

composition across the landscape, as well as those potentially

responsible for differences in composition between heavily

cultivated regions and predominately native grassland regions.

MATERIALS AND METHODS

Study area.—We collected owl pellets from across the

mixed-grass prairie and aspen parkland of western Canada

(Fig. 1). This region is covered in boulder clay soil deposits of

FIG. 1.—Pellet collection sites for burrowing owls (white circles) and great horned owls (black circles) on the mixed-grass prairie (dark gray)

and aspen parkland (light gray) of the northern Great Plains of North America. The black circles outlined in white are reference points (right:

Calgary, Alberta, Canada; left: Regina, Saskatchewan, Canada). Cross-hatching represents regions where owl pellet samples were used to

determine similarity in small mammal composition between predominately native grassland (southeastern Alberta) on the left and a heavily

cultivated region (Regina Plain) on the right.

1060 Vol. 94, No. 5JOURNAL OF MAMMALOGY

varying texture, and experiences a continental climate of

extreme variation in temperature and precipitation, with a short

annual growing period of 3–5 months (Coupland 1950). Grain

farming and livestock ranching have heavily affected the

region since the late 1800s. Nearly 70% of the mixed-grass

prairie has been converted to agriculture (Samson et al. 2004),

severely altering the vegetative land cover and homogenizing

the landscape in some regions. Variation in climate, soil

characteristics, and land use across the whole region enables

examination of small mammal communities in a diverse

landscape, as well as a closer examination of regions

dominated by single land-use features. For instance, one part

of the study area (Regina Plain of southern Saskatchewan) is a

heavily cultivated landscape, whereas another part

(southeastern Alberta) remains predominantly native

grassland. These regions also differ in soil and climate

characteristics; the Regina Plain is dominated by heavy clay

soils and receives an average of 40% more precipitation than

southeastern Alberta.

Owl pellet data.—We collected pellets from nest and roost

locations of burrowing owls over a 15-year period (1997–

2011) and of great horned owls primarily in 2007 and 2008

(Fig. 1); these pellets are now stored in the collections at the

Royal Saskatchewan Museum. These pellets were collected as

part of ongoing field studies on owls, during which researchers

and birdbanders made a focused effort to collect all pellets

from each nest and associated roost. Burrowing owl pellets

were collected an average 5 times during the breeding season

of each year (April–July) from 1,181 nests, whereas great

horned owl pellets were collected primarily during a single

visit from 258 nests. We used a 10% sodium hydroxide

solution to dissolve fur in the pellets and provide clean bones

and teeth for identification. Prey species were identified via

unique skeletal and dental traits using a reference collection

when necessary. The abundance of each small mammal species

was determined for each nest based on the number of

individual craniomandibular elements present (i.e., minimum

number of individuals).

The resulting data set included 60,972 small mammal

individuals, from which a total 19 species of rodents and

shrews were identified (Table 1). Seven species of Sorex were

identified in the owl pellets; however, we could not reliably

identify a large number (nearly 1,500) of these individuals by

specific dental or skeletal traits. The vast majority of Sorexshrews were most likely S. haydeni and S. cinereus, but to

reduce error in the data set all specimens of Sorex and Blarinabrevicauda were consolidated into a single group referred to

collectively as ‘‘shrews.’’ We included only remains of the 6

most abundant rodent species and shrews (Sorex species and B.brevicauda) in statistical analyses, which represented 99.7% of

all small mammals identified (Table 1). The remaining species

were not included in these analyses because combined they

made up less than 0.01% of the diet of both owl species, the

statistical results for which were overwhelmed by the more

abundant species in the data set. Collections were pooled by

nest per year, and are referred to hereafter as a sample.

The same 6 species and shrews comprised the majority of

prey items in the pellets of both owl species, indicating that the

diets of the 2 owls were generally similar. However, after the

top 3 prey species, the order of importance was somewhat

different; correlation analyses using Spearman’s rho showed a

moderately positive correlation between the rank abundances

of the top 6 small mammal species (Table 1; rho ¼ 0.61, P ¼0.17). Thus, both owls are likely generalist predators exhibiting

functional responses to changing prey densities (Terry 2010),

but we did not pool pellet data across owl species for analyses.

Individual-based species accumulation curves were used to

identify the minimum number of identified small mammal

remains within which species richness approached an asymp-

tote; we used this value as the sample size needed to include a

site for statistical analyses (Gotelli and Colwell 2001). This

assessment was based on the sample size at which information

content (species richness) reached an asymptote (Gotelli and

TABLE 1.—Total abundances and relative abundances of small mammal species found within burrowing owl (BUOW) and great horned owl

(GHOW) pellets, respectively. Species in boldface type were included in the multivariate regression tree analyses and comparison between a

heavily cultivated region (Regina Plain) and a predominantly native grassland region (southeastern Alberta). All Sorex and Blarina species were

combined into a single group (SHREW) for the analyses.

Species

abundance (BUOW)

Species

abundance (GHOW)

Species relative

abundance (BUOW)

Species relative

abundance (GHOW)

Deer mouse (Peromyscus maniculatus) 26,199 10,648 58% 68%

Meadow vole (Microtus pennsylvanicus) 9,189 2,291 20% 15%

Sagebrush vole (Lemmiscus curtatus) 5,738 705 13% 5%

Shrews (Sorex and Blarina)a 1,726 301 4% 2%

Olive-backed pocket mouse (Perognathus fasciatus) 915 799 2% 5%

House mouse (Mus musculus) 838 115 2% 1%

Northern grasshopper mouse (Onychomys leucogaster) 607 736 1% 5%

Western jumping mouse (Zapus princeps) 32 19 , 0.1% , 0.1%

Ord’s kangaroo rat (Dipodomys ordii) 9 19 , 0.1% , 0.1%

Southern red-backed vole (Myodes gapperi) 5 45 , 0.1% , 0.1%

Prairie vole (Microtus ochrogaster) 2 30 , 0.1% , 0.1%

Western harvest mouse (Reithrodontomys megalotis) 2 0 , 0.1% 0%

Meadow jumping mouse (Zapus hudsonius) 2 0 , 0.1% 0%

a This category includes Blarina brevicauda, Sorex arcticus, Sorex cinereus, Sorex haydeni, Sorex hoyi, Sorex monticolus, and Sorex palustris.

October 2013 1061HEISLER ET AL.—SMALL MAMMAL MACROHABITAT ASSOCIATIONS

Colwell 2001). Burrowing owl samples with fewer than 30

individual mammals and great horned owl samples containing

fewer than 20 individual mammals were excluded from our

analyses, which left 397 burrowing owl nests (557 samples;

some nests were sampled in multiple years) with an average

size of 59 (6 31 SD) individuals and 171 great horned owl

nests (171 samples) with an average of 88 (6 83 SD)

individuals to be included in statistical analyses. These samples

were then standardized for sampling effort by dividing the

abundance of each small mammal species by the total number

of individuals of all species for statistical analyses.

Environmental data.—Soil characteristics (i.e., percentage

of sand and clay in the soil, soil texture, and soil order), spatial

variation in climate (i.e., average annual precipitation,

temperature, and snow depth), and land-use type were

included in all analyses of small mammal composition (Table

2). Land cover from vectorized, raster thematic data collected

in approximately 2000 was provided by Geobase Canada

(Centre for Topographic Information 2010). To avoid using

outdated data for nests visited recently, we replaced land use

within a 4-km radius of each nest visited between 2004 and

2011 with ground-truthed land-use data collected the year these

nests were visited. Soil variables, which were compiled from

existing soil survey maps, were obtained from Agriculture and

Agri-Food Canada (Soil Landscapes of Canada Working

Group 2010). Annual averages of temperature, rainfall, and

snow depth from 1997 to 2011 were taken from the national

summaries of climate averages and extremes from

Environment Canada (Toronto, Ontario, Canada). We used

geographic information systems to create circular buffers with

2,500-m and 5,000-m radii from each pellet collection site for

burrowing owl and great horned owl samples, respectively.

These radii represent the typical foraging distances from nest

sites of each owl species (Baumgartner 1939; Schoener 1968;

Rusch et al. 1972). Within foraging-range buffers, average

environmental conditions between 1997 and 2011 were

determined for each pellet collection site. This approach

provided a data set containing annual small mammal

composition and associated environmental conditions for

each owl nest.

Statistical analysis.—Multivariate regression tree (MVRT)

analyses were used to identify the broadscale environmental

factors influencing small mammal composition (De’Ath 2002;

Larsen and Speckman 2004). This method is suitable for

complex data sets such as owl pellets because it relies on few

statistical assumptions, tolerates colinearity and higher-order

interactions among predictor variables, and can analyze large

data sets with multiple response variables efficiently (De’Ath

2002; Larsen and Speckman 2004). The hierarchy of branches

represents the environmental variables in decreasing order of

influence on the composition of small mammal assemblages

across the study region. Each branch is characterized by a

threshold value chosen to maximize homogeneity within the

resulting nodes (De’Ath 2002). The terminal nodes represent

small mammal assemblages characterized by the environmental

factors used to separate the small mammal species data into

homogeneous groups. Cross-validation relative error identifies

the optimal tree size by determining the predictive accuracy of

the tree, and the amount of variation in small mammal species

composition unexplained by the tree is quantified by the

relative error. Trees with the smallest cross-validation relative

error tend to be overly optimistic in their predictive capacity

because they include redundant or irrelevant branching. Thus,

final models were chosen from models above or below the

minimum cross-validation relative error plus 1 standard error

(SE) threshold (De’Ath 2002). Principal component analysis

was used to determine the homogeneity of samples

representing each small mammal assemblage identified with

MVRT analysis (De’Ath 2002). The Dufrene–Legendre index

was used to identify individual species that were associated

with specific environmental conditions based on the relative

TABLE 2.—Means (6 SD) of average continuous environmental variables associated with burrowing owl (BUOW) and great horned owl

(GHOW) pellet samples, as well as for the heavily cultivated (Regina Plain) and predominately native grassland (southeastern Alberta) regions.

MF ¼moderately fine, M ¼ moderate, VF ¼ very fine, VE ¼ vertisolic, CH ¼ chernozemic, SZ ¼ solonetzic.

Environmental condition Unit

Canadian prairies

Regina Plain Southeastern AlbertaBUOW GHOW

Native grass % 31 (6 30) 17 (6 18) 20 (6 10) 70 (6 22)

Ripariana % 6 (6 7) 3 (6 4) 10 (6 5) 6 (6 9)

Trees and shrubs % 0 (6 1) 1 (6 3) 0 (6 0) 0 (6 0)

Tame grass % 10 (6 9) 10 (6 10) 14 (6 8) 9 (6 10)

Human developmentb % 2 (6 9) 1 (6 2) 1 (6 1) 1 (6 2)

Cropland % 50 (6 31) 67 (6 24) 55 (6 17) 13 (6 21)

Sand % 26 (6 19) 33 (6 17) 6 (6 8) 43 (6 14)

Clay % 43 (6 20) 36 (6 15) 70 (6 12) 23 (6 6)

Soil texture Cc MF M VF MF

Soil order C VE CH VE SZ

Average annual precipitation mm 260 (6 160) 241 (6 98) 340 (6 91) 205 (6 96)

Average annual snow depth cm 58 (6 47) 64 (6 42) 83 (6 25) 41 (6 40)

Temperature 8C 3.16 (6 1.26) 2.15 (6 1.46) 4.16 (6 1.24) 3.38 (6 2.05)

a Refers to surface area of permanent water bodies only (i.e., lakes, reservoirs, rivers, and streams).b Human development refers to roads, railways, buildings, paved surfaces, urban areas, industrial sites, farmsteads, excavation pits, and dumping sites.c Categorical variable.


abundance and relative frequency of occurrence within small

mammal assemblages (Dufrene and Legendre 1997).

We used MVRT analysis to identify overall landscape

patterns in small mammal composition across the entire study

area. We analyzed pellet samples from burrowing owls and

great horned owls separately to account for differential

sampling effort between the 2 pellet data sets. We used the

chi-square test to determine similarities in composition of small

mammal assemblages between a heavily cultivated region

(Regina Plain) and a predominately native grassland region

(southeastern Alberta—Everitt 1977). MVRT analyses of the

burrowing owl samples from these 2 regions identified which

environmental variables affected small mammal species

composition. There were too few great horned owl samples

in either region to conduct this analysis, so only burrowing owl

samples were used.

We used ArcMap 10.0 for all data preparation (ESRI 2011);

all statistical computations were conducted in R Project for

Statistical Computing 2.14.1 (R Development Core Team

2011), using vegan 2.0–5 (Oksanen et al. 2012), mvpart 1.6-0

(Therneau et al. 2012), and MVPARTwrap 0.1–9 packages

(Ouellette and Legendre 2012).

RESULTS

Overall landscape patterns in small mammal speciescomposition.—The proportion of cropland and the percentage

of sand in the soil had the greatest influence on small mammal

species composition in the MVRT of all burrowing owl pellet

samples, in which foraging ranges were composed of 1,962 ha

(Fig. 2). The model explained 47% of the variation in small

mammal species composition and predicted the relative

abundance of all 6 individual species plus shrews based on 4

of the 12 environmental variables considered. The relative

abundance of deer mice (Peromyscus maniculatus) in

assemblages increased with the proportion of cropland,

whereas the relative abundance of sagebrush voles

(Lemmiscus curtatus) showed the opposite trend, particularly

in regions with moderately sandy soils (Fig. 3). Meadow voles

(Microtus pennsylvanicus), house mice (Mus musculus), olive-

backed pocket mice (Perognathus fasciatus), northern

grasshopper mice (Onychomys leucogaster), and shrews (B.brevicauda and Sorex species) were associated with soil orders

characteristic of grassland environments (chernozemic or

solonetzic soils). These species were split further into 2 small

mammal assemblages along a gradient of precipitation. In

regions receiving an average annual precipitation higher than

439 cm, the average relative abundances of meadow voles,

house mice, and shrews were 29%, 4%, and 4% higher,

respectively. In the same regions characterized by soils made

up of more than 40% sand, the average relative abundances of

northern grasshopper mice and olive-backed pocket mice were

5% and 2% higher, respectively.

Soil characteristics had the greatest influence on small

mammal species composition across the landscape in the

MVRT of all great horned owl pellet samples from foraging

ranges comprising 7,850 ha (Fig. 4). This is similar to the

results of the burrowing owl pellet samples, where soil

characteristics occur at 4 of the 6 branches of the resulting

MVRT. Soil texture and soil order explained 35% of the

variation in small mammal species composition and predicted

the relative abundances of 5 individual species (all except

house mice) and shrews. Deer mice and meadow voles were

FIG. 2.—Small mammal assemblages predicted by multivariate

regression tree analysis of small mammal relative abundances from

burrowing owl pellet samples and landscape-scale environmental

variables averaged within the owl foraging range. The hierarchy of

nodes represents the environmental variables in decreasing order of

influence on small mammal composition across the study region (Crop

¼ proportion of cropland, Sand ¼ proportion of sand, CH ¼chernozemic soil order, SZ ¼ solonetzic soil order, RG ¼ regosolic

soil order, VE ¼ vertisolic soil order, Prec ¼ average annual

precipitation). Bar plots represent mean relative abundances of species

occurring in each small mammal assemblage (from left to right: black

¼ deer mouse, dark gray¼meadow vole, light gray¼ sagebrush vole,

black ¼ Sorex and Blarina as a collective group, dark gray ¼ olive-

backed pocket mouse, light gray ¼ house mouse, black ¼ northern

grasshopper mouse). Asterisks (*; P , 0.05) represent indicator

species that occur in high frequency and abundance with specific

environmental conditions, identified using the Dufrene–Legendre

index.

FIG. 3.—Mean relative abundance of deer mice (gray line) and

sagebrush voles (black line) as the proportion of cropland increases

and the percentage of sand in the soil (gray bars) decreases within owl

foraging ranges.


split into separate small mammal species assemblages based on

soil texture and soil order. In particular, average deer mouse

relative abundance was 43% higher in regions where soils

contained more than 28% clay, whereas meadow vole relative

abundance was an average 9% higher in the same regions

characterized by solonetzic soils. The remaining species were

an average 12% more abundant in regions where soils

contained less than 18% clay (average species relative

abundance: sagebrush voles¼ 3%, shrews¼ 2%, olive-backed

pocket mouse ¼ 26%, northern grasshopper mouse ¼ 17%).

However, northern grasshopper mice and olive-backed pocket

mice were almost 9 times more abundant than sagebrush voles

and shrews in these regions. These results corroborate the

relationship between soil texture and small mammal species

composition exhibited in the previous MVRT of burrowing

owl samples.

Agricultural influence on small mammal speciescomposition.—Small mammal assemblages in the heavily

cultivated Regina Plain differed significantly from those in

the predominately native grassland region of southeastern

Alberta (v2¼ 3,864.3, P , 0.05; Table 3). Deer mice made up

41% of the assemblage in the heavily cultivated region (Regina

Plain), but only 16% of the assemblage in the predominantly

native grassland region (southeastern Alberta). In contrast,

sagebrush voles made up only 1% of the assemblage in the

heavily cultivated region but up to 21% of the assemblage in

the predominately native grassland. To confirm that differences

in soil and climate between the 2 regions did not confound

these results, another chi-square test comparing the

composition of small mammal assemblages from samples

with owl foraging ranges composed of � 90% cropland or

native grassland across the entire sampled region showed

almost identical results (data not shown; v2 ¼ 2,717.8, P ,

0.05). These results also are similar to the relationship

identified in the 1st split of the MVRT of all burrowing owl

samples where deer mice and sagebrush voles were inversely

associated with cropland. Thus, it appears that land use may be

largely responsible for shifts in assemblage composition

between these 2 regions, despite the differences in soil and

weather characteristics.

The proportion of cropland in the MVRT analysis of pellet

samples from the predominantly native grassland region had

the greatest influence on small mammal species composition,

further identifying this land-use type as a dominant factor

affecting assemblages. Thirty-seven percent of the variation in

small mammal species composition and the predicted distri-

butions of 4 species were explained by the proportion of



great horned owl pellet samples and landscape-scale environmental



influence on small mammal composition across the study region (Clay

¼ proportion of clay, CH ¼ chernozemic soil order, SZ ¼ solonetzic

soil order, RG¼ regosolic soil order, VE¼ vertisolic soil order). Bar

plots represent mean relative abundances of species occurring in each

small mammal assemblage (from left to right: black ¼ deer mouse,

dark gray¼meadow vole, light gray¼ sagebrush vole, black¼ Sorexand Blarina as a collective group, dark gray ¼ olive-backed pocket

mouse, light gray ¼ house mouse, black ¼ northern grasshopper

mouse). Asterisks (*; P , 0.05) represent indicator species that occur

in high frequency and abundance with specific environmental

conditions, identified using the Dufrene–Legendre index.

TABLE 3.—Chi-square analyses comparing the abundances of species within burrowing owl pellets from a heavily cultivated region (Regina

Plain) and a predominately native grassland region (southeastern Alberta) to identify differences in small mammal composition. Observed species

abundances were used to calculate expected abundances and adjusted residuals for comparison of small mammal composition and species

abundances between regions, respectively. Taxon acronyms represent species (DM¼ deer mouse, MV¼meadow vole, SBV¼ sagebrush vole,

SHREW ¼ Sorex and Blarina as a collective group, OBPM ¼ olive-backed pocket mouse, HM ¼ house mouse, NGM ¼ northern grasshopper

mouse). NS ¼ not significant.

Taxon

Regina Plain Southeastern Alberta

Observed Expected Adjusted residuals P Observed Expected Adjusted residuals Marginal row totals Pa

DM 5,492 4,223 42.39 , 0.001 2,004 3,237 �42.39 7,496 , 0.001

MV 1,992 1,929 2.50 0.05 1,431 1,494 �2.50 3,423 0.05

SBV 153 1,491 �57.96 , 0.001 2,493 1,155 57.96 2,646 , 0.001

SHREW 218 275 �5.29 , 0.001 270 213 5.29 488 , 0.001

OBPM 71 70 0.104 . 0.05 54 55 �0.104 125 NS

HM 264 161 12.39 , 0.001 22 125 �12.39 286 , 0.001

NGM 23 64 �7.74 , 0.001 90 49 7.74 113 , 0.001

Marginal column totals 8,213 6,364

a a ¼ 0.05.


cropland and average annual snow cover (Fig. 5). Average

relative abundances of deer mice and northern grasshopper

mice were 25% and 2% higher in regions with greater than 6%

cropland, respectively. In contrast, average relative abundances

of sagebrush voles and meadow voles exhibited a correspond-

ing decrease by 17% and 9%, respectively. Interestingly, the

MVRT analysis of pellet samples from the heavily cultivated

region explained less than 1% of the variation in small

mammal species composition and had no predictive value.

DISCUSSION

Using owls to sample small mammal assemblages enabled

us to conduct a landscape-scale study of a size that would have

been inconceivable with traditional sampling methods. All

sampling methods have inherent biases, and do not provide a

perfect spatial representation of small mammal communities

(Torre et al. 2004). For example, traps can be species- and size-

selective (O’Farrell et al. 1994), whereas owls may be selective

through nonrandom habitat and prey choices (Yom-Tov and

Wool 1997). However, despite the differences in habitat use,

body size, and foraging strategies of the 2 owl species we used,

the overall small mammal species composition of great horned

and burrowing owl diets were similar. Also, land-use and soil

characteristics were important predictors in the MVRT

analyses using pellets from both owl species. The similarity

in diet composition across such a large landscape area suggests

that both owls are generalist predators, and the similarity in

results of the MVRT analyses suggests the relative abundance

of small mammals within pellet samples is reflective of their

relative abundance in the environment. Thus, owl pellets

should be considered a useful method of small mammal

sampling (Terry 2010). Also, the efficiency of collecting pellet

samples and the potential for acquiring data sets encompassing

large geographic areas and long time periods compared to

traditional trapping methods (Hanser et al. 2011) suggest that

owl pellets should be considered an alternative method for

future large-scale small mammal studies.

Species–habitat associations at spatial scales that encompass

the distributions of entire populations (macrohabitat) provide

important insight into the factors affecting small mammal

composition. Most microhabitat studies sample areas less than

2 ha and focus on a few vegetation types at most (Bowman et

al. 2000; Jorgensen 2004). Although some of these studies

found explicit relationships between resource distribution and

local species abundance, they were less successful in

determining how species distribute themselves across land-

scapes (Jorgensen 2004). Our study sampled small mammals

from more than 4 million hectares irrespective of vegetation

type, making this a truly landscape-scale study of small

mammal species composition. Our results were similar to

several multiscale studies that suggest that small mammals

have greater affiliations with macrohabitats than other spatial

scales, potentially due to species distributing themselves

according to microhabitat abundance within macrohabitats

(Morris 1987; Jorgensen and Demarais 1999; Stevens and

Tello 2009). Thus, including macrohabitat associations in

studies of small mammal composition markedly enhances our

perspective on the importance of both scale and important

habitat features beyond that gained from studies focused solely

on microhabitat selection.

Agriculture has changed the native grassland ecosystem

from one with a diverse assemblage of small mammals to a

system completely dominated by deer mice. Approximately

60% of the mixed-grass prairie in North America was

cultivated for agricultural purposes (Henwood 2010); in many

areas this proportion reaches more than 90% of the land area

(Poulin et al. 2005). Conversion of native grassland to cropland

homogenizes vegetative structure and alters resource availabil-

ity across the landscape, redistributing resources in a way that

appears to benefit some species while imposing a cost on

others. In particular, the high relative abundances of deer mice

in agricultural areas are likely due to high seed productivity

and the use of ephemeral burrows for nesting and reproduction

in cropland (Witmer et al. 2007; White et al. 2012).

Conversely, the inverse relationship that sagebrush voles have

with the prevalence of cropland is likely due to cultivation

eliminating many resources this species depends on, such as

vegetative structure for food and shelter, as well as a lack of a

stable underground environment for extensive burrowing

activities (Witmer et al. 2007). The overall result is that the

conversion of native grassland to cropland has significantly

altered small mammal assemblages and populations across the

northern Great Plains of North America. The ecological

consequences of altering the dynamics of such a key species



burrowing owl pellet samples of the predominately native grassland

region (southeastern Alberta) and landscape-scale environmental



influence on small mammal composition across the study region

(CROP ¼ proportion of cropland, SNOW ¼ average annual snow

cover). Bar plots represent mean relative abundances of species

occurring in each small mammal assemblage (from left to right: black

¼ deer mouse, dark gray¼meadow vole, light gray¼ sagebrush vole,

black ¼ Sorex and Blarina as a collective group, dark gray ¼ olive-

backed pocket mouse, light gray ¼ house mouse, black ¼ northern

grasshopper mouse). Asterisks (*; P , 0.05) represent indicator

species that occur in high frequency and abundance with specific

environmental conditions, identified using the Dufrene–Legendre

index.


group to predator–prey dynamics and disease or parasite

transmission among animals and humans should be the focus

for future large-scale studies.

Previous studies of grassland small mammal assemblages

have concluded that precipitation is a dominant contributing

factor to small mammal species composition (Grant and Birney

1979; Reed et al. 2006); however, our findings suggest that soil

characteristics may have been overlooked as a potential driving

force at the landscape scale. Microhabitat studies show that

precipitation is responsible for the variation in resource

distribution that species use to partition microhabitats, thereby

allowing coexistence across the landscape (Price 1978; Reed et

al. 2006). In our study only a weak relationship existed between

precipitation and small mammal species composition, whereas

soil texture and soil order were dominant environmental factors

determining small mammal species composition. Soil charac-

teristics have been considered in some microhabitat studies, but

few found associations between small mammal density and the

edaphic features measured (Feldhamer 1979; Stevens and Tello

2009). The lack of evidence for soil characteristics, such as

texture and order, as a determining factor for small mammal

abundance at microhabitat scales may stem from the fact that

these species are associating with habitats characterized by

differing edaphic characteristics at the macrohabitat level.

The importance of soil texture as a predictor of small mammal

species composition is likely due to its indirect influence on

primary productivity and vegetative structure. Several small

mammal microhabitat studies suggest that litter-dwelling

herbivorous and insectivorous species associate with consistent

vegetative structure for food, shelter, and predator avoidance,

whereas granivorous species associate with heterogeneous

structure for easier access to seeds (Wrigley et al. 1979; Reed

et al. 2006). Fine-textured clay maintains soil moisture and

nutrient availability closer to the soil surface for more consistent,

natural vegetative cover. In contrast, sandy soils drain moisture

and nutrients away from the soil surface, leaving them

unavailable for most plant growth except forbs and shrubs.

Thus, large areas with sandy soils often exhibit heterogeneous

vegetative structure and cover (Epstein et al. 1997; Lane et al.

1998; Hook and Burke 2000). These concepts are consistent

with the patterns observed in our study; olive-backed pocket

mice (i.e., granivore) were associated with coarse-textured soils

more so than were voles or shrews (i.e., litter-dwelling species).

Regardless of the specific mechanism, examination of our data

suggests that soil texture plays a role as a natural macrohabitat

feature responsible for variance in small mammal species

composition across the prairie landscape.

ACKNOWLEDGMENTS

We thank everyone involved in collecting owl pellets from across the

Canadian prairies, particularly H. Trefry, G. Holroyd, and A. Froese for

collecting and allowing use of their pellet samples for this study. We

also thank T. Schowalter for identifying the majority of individual small

mammals collected. Thanks to J. Piwowar for sharing his expertise

regarding ArcGIS 10. LMH was supported by Mathematics of

Information Technology and Complex Systems—Accelerate intern-

ships, Friends of the Royal Saskatchewan Museum, and the University

of Regina. Additional financial and logistic support provided by

Environment Canada—Interdepartmental Recovery Fund, Canadian

Museum of Nature, Agriculture and Agri-Food Canada—Prairie Farm

Rehabilitation Administration, and Grasslands National Park.

LITERATURE CITED

BAUMGARTNER, F. M. 1939. Territory and population in the great

horned owl. Auk 56:274–282.

BOWMAN, J., G. FORBES, AND T. DILWORTH. 2000. The spatial scale of

variability in small-mammal populations. Ecography 23:328–334.

CENTRE FOR TOPOGRAPHIC INFORMATION. 2010. Land cover, circa

2000—vector. Government of Canada, Sherbrooke, Ontario,

Canada.

COUPLAND, R. T. 1950. Ecology of mixed prairie in Canada.

Ecological Monographs 20:271–315.

DE’ATH, G. 2002. Multivariate regression trees: a new technique for

modeling species–environment relationships. Ecology 83:1105–

1117.

DUFRENE, M., AND P. LEGENDRE. 1997. Species assemblages and

indicator species: the need for a flexible asymmetrical approach.

Ecological Monographs 67:345–366.

EPSTEIN, H. E., W. K. LAUENROTH, AND I. C. BURKE. 1997. Effects of

temperature and soil texture on ANPP in the U.S. Great Plains.

Ecology 78:2628–2631.

ERRINGTON, P. L. 1930. The pellet analysis method of raptor food

habits study. Condor 32:292–296.

ESRI. 2011. ArcGIS. Release 10.0. Environmental System Research

Institute, Inc., Redlands, California.

EVERITT, B. S. 1977. The analysis of contingency tables. Chapman and

Hall, London, United Kingdom.

FELDHAMER, G. A. 1979. Vegetative and edaphic factors affecting

abundance and distribution of small mammals in southeast Oregon.

Great Basin Naturalist 39:207–218.

FERANEC, R. S., E. A. HADLY, AND A. PAYTAN. 2007. Determining

landscape use of Holocene mammals using strontium isotopes.

Oecologia 153:943–950.

FULK, G. W. 1976. Owl predation and rodent mortality: a case study.

Mammalia 40:423–427.

GIBBONS, J. W. 1988. The management of amphibians, reptiles, and

small mammals in North America: need for an environmental

attitude adjustment. United States Forest Service Rocky Mountain

Forest Range Experimental Station, Technical Report RM-166:4–

10.

GLUE, D. E. 1970. Avian predator pellet analysis and the mammal-

ogist. Mammal Review 1:53–62.

GOTELLI, N. J., AND R. K. COLWELL. 2001. Quantifying biodiversity:

procedures and pitfalls in the measurement and comparison of

species richness. Ecological Letters 4:379–391.

GRANT, W. E., AND E. C. BIRNEY. 1979. Small mammal community

structure in North American grasslands. Journal of Mammalogy

60:23–36.

GRANT, W. E., AND N. R. FRENCH. 1980. Evaluation of the role of small

mammals in grassland ecosystems: a modelling approach. Ecolog-

ical Modelling 8:15–37.

HANSER, S. E., ET AL. 2011. Occurrence of small mammals: deer mice

and the challenge of trapping across large spatial extents. Pp. 337–

356 in Sagebrush ecosystem conservation and management:

ecoregional assessment tools and models for the Wyoming basins

(S. E. Hanser, M. Leu, S. T. Knick, and C. L. Aldridge, eds.). Allen

Press, Lawrence, Kansas.


HENWOOD, W. D. 2010. Toward a strategy for the conservation and

protection of the world’s temperate grasslands. Great Plains

Research 20:121–134.

HOOK, P. B., AND I. C. BURKE. 2000. Biogeochemistry in a shortgrass

landscape: control by topography, soil texture, and microclimate.

Ecology 81:2686–2703.

JAKSIC, F. M., AND C. D. MARTI. 1984. Comparative food habits of

Bubo owls in Mediterranean-type ecosystems. Condor 86:288–296.

JAKSIC, F. M., AND J. A. SIMONETTI. 1987. Predator/prey relationships

among terrestrial vertebrates: an exhaustive review of studies

conducted in southern South America. Revista Chilena de Historia

Natural 60:221–244.

JORGENSEN, E. E. 2004. Small mammal use of microhabitat reviewed.

Journal of Mammalogy 85:531–539.

JORGENSEN, E. E., AND S. DEMARAIS. 1999. Spatial scale dependence in

rodent habitat use. Journal of Mammalogy 80:421–429.

LANE, D. R., D. P. COFFIN, AND W. K. LAUENROTH. 1998. Effects of soil

texture and precipitation on above-ground net primary productivity

and vegetation structure across the central grassland region of the

United States. Journal of Vegetation Science 9:239–250.

LARSEN, D. R., AND P. L. SPECKMAN. 2004. Multivariate regression

trees for analysis of abundance data. Biometrics 60:543–549.

MARTI, C. D. 1987. Predator–prey interactions: a selective review of

North American research results. Revista Chilena de Historia

Natural 60:203–219.

MAYOR, S. J., D. C. SCHNEIDER, J. A. SCHAEFER, AND S. P. MAHONEY.

2009. Habitat selection at multiple scales. Ecoscience 16:238–247.

MORRIS, D. W. 1987. Ecological scale and habitat use. Ecology

68:362–369.

O’FARRELL, M. J., ET AL. 1994. Use of a mesh live trap for small

mammals: are results from Sherman live traps deceptive? Journal of

Mammalogy 75:692–699.

OKSANEN, J., ET AL. 2012. Vegan: community ecology package. R

package version 2.0–5. http://CRAN.R-project.org/package¼vegan.

Accessed 11 January 2012.

OUELLETTE, M.-H., AND P. LEGENDRE. 2012. MVPARTwrap: additional

functionalities for package mvpart. R package version 0.1–9. http://

CRAN.R-project.org/package¼MVPARTwrap. Accessed 11 Janu-

ary 2012.

PORDER, S., A. PAYTAN, AND E. A. HADLY. 2003. Mapping the origin of

faunal assemblages using strontium isotopes. Paleobiology 29:197–

204.

POULIN, R. G., L. D. TODD, K. M. DOHMS, AND T. I. WELLICOME. 2005.

Factors associated with nest- and roost-burrow selection by

burrowing owls (Athene cunicularia) on the Canadian prairies.

Canadian Journal of Zoology 83:1373–1380.

POULIN, R. G., T. I. WELLICOME, AND L. D. TODD. 2001. Synchronous

and delayed numerical responses of a predatory bird community to

a vole outbreak on the Canadian prairies. Journal of Raptor

Research 35:288–295.

PRICE, M. V. 1978. The role of microhabitat in structuring desert

rodent communities. Ecology 59:910–921.

R DEVELOPMENT CORE TEAM. 2011. R: a language and environment for

statistical computing. R Foundation for Statistical Computing,

Vienna, Austria.

REED, A. W., G. A. KAUFMAN, AND D. W. KAUFMAN. 2006. Species

richness–productivity relationships for small mammals along a

desert–grassland continuum: differential responses of functional

groups. Journal of Mammalogy 87:777–783.

RUSCH, D. H., E. C. MESLOW, P. D. DOERR, AND L. B. KEITH. 1972.

Response of great horned owl populations to changing prey

densities. Journal of Wildlife Management 36:282–296.

SAMSON, F. B., F. L. KNOPF, AND W. R. OSTLIE. 2004. Great Plains

ecosystem: past, present, and future. Wildlife Society Bulletin 32:6–15.

SCHOENER, T. W. 1968. Sizes of feeding territories among birds.

Ecology 49:123–141.

SIEG, C. H. 1987. Small mammals: pests or vital components of the

ecosystem. Pp. 88–92, 8th Wildlife Damage Control Workshop,

April 26-30, 1987, Rapid City, South Dakota. University of

Nebraska Digital Commons, http://digitalcommons.unl.edu/

gpwdcwp/97/.

SILVA, S. I., I. LAZO, E. SILVA-ARANQUIZ, F. M. JAKSIC, P. L. MESERVE,

AND J. R. GUTIERREZ. 1995. Numerical and functional response of

burrowing owls to long-term fluctuations in Chile. Journal of

Raptor Research 29:250–255.

SOIL LANDSCAPES OF CANADA WORKING GROUP. 2010. Soil landscapes of

Canada digital map and database at 1:1 million scale. Version 3.2.

Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.

STEVENS, R. C., AND J. S. TELLO. 2009. Micro- and macrohabitat

associations in Mojave Desert rodent communities. Journal of

Mammalogy 90:388–403.

TERRY, R. C. 2010. On raptors and rodents: testing the ecological

fidelity and spatiotemporal resolution of cave death assemblages.

Paleobiology 36:137–160.

THERNEAU, T. M., B. ATKINSON, B. RIPLEY, J. OKSANEN, AND G. DE’ATH.

2012. Mvpart: multivariate partitioning. R package version 1.6-0.

http://CRAN.R-project.org/package¼mvpart. Accessed 11 January

2012.

TORRE, I., A. ARRIZABALAGA, AND C. FLAQUER. 2004. Three methods for

assessing richness and composition of small mammal communities.


WHITE, A. J., R. G. POULIN, B. WISSEL, J. L. DOUCETTE, AND C. SOMERS.

2012. Agricultural land use alters trophic status and population

density of deer mice (Peromyscus maniculatus) on the North

American Great Plains. Canadian Journal of Zoology 90:868–874.

WIENER, J. G., AND M. H. SMITH. 1972. Relative efficiencies of four

small mammal traps. Journal of Mammalogy 53:868–873.

WITMER, G., R. SAYLER, D. HUGGINS, AND J. CAPELLI. 2007. Ecology

and management of rodents in no-till agriculture in Washington,

USA. Integrative Zoology 2:154–164.

WOOSTER, L. D. 1936. The contents of owl pellets as indicators of

habitat preferences of small mammals. Transactions of the Kansas

Academy of Science 39:395–397.

WRIGLEY, R. E., J. E. DUBOIS, AND H. W. R. COUPLAND. 1979. Habitat,

abundance, and distribution of six species of shrews in Manitoba.


YOM-TOV, Y., AND D. WOOL. 1997. Do the contents of barn owl pellets

accurately represent the proportion of prey species in the field?

Condor 99:972–976.

ZIMMERMAN, G., P. STAPP, AND B. VAN HORNE. 1996. Seasonal variation

in the diet of great horned owls (Bubo virginianus) on shortgrass

prairie. American Midland Naturalist 136:149–156.

Submitted 21 January 2013. Accepted 30 April 2013.

Associate Editor was Winston P. Smith.


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