Distribution of Nonnative Red Foxes in East
Bay Oak Woodlands1
Allison L. Bidlack,2 Adina Merenlender,2 and Wayne M. Getz2
Abstract
European red foxes (Vulpes vulpes) were introduced into lowland California in the 1880s for
fur farming and hunting. The introduced foxes quickly spread throughout much of the state
and have been implicated in the decline of several federally threatened and endangered
ground-nesting bird species. Red foxes have been present in the East Bay for 25 to 30 years
and they are regularly sighted in coastal wetlands and in the Oakland and Berkeley hills. We
were interested in documenting the extent of the invasion away from human-dominated
habitats into oak woodlands in the East Bay, as foxes may negatively impact both prey
populations and native carnivores such as gray foxes. We surveyed fire roads and hiking trails
in core oak woodland sites in Contra Costa and Alameda counties for carnivore scat. All scat
samples were collected, and their locations entered into a GIS. To positively distinguish the
scat to species, DNA was extracted, amplified, and identified using Polymerase Chain
Reaction (PCR) and Restriction Fragment Length Polymorphism (RFLP) testing. Four
carnivore species were identified, including coyote, gray fox, red fox, and bobcat. Red foxes
were only detected in woodlands that were adjacent to urban or suburban development, and
were not detected in more rural sites. They may be dependent on human-dominated systems
for resources and cover, and the high numbers of coyotes present in the East Bay may be
excluding them from some areas. This research is providing managers essential information
about red fox distribution, habitat requirements, and interactions with other carnivores, which
can be used to better monitor and eventually control red fox invasions and subsequent impacts
to native species.
Keywords: Carnivore, coyote, gray fox, invasive, red fox, San Francisco Bay, Vulpes vulpes.
Introduction
Red foxes (Vulpes vulpes) are the most widespread non-domesticated carnivore in the
world, and have been enormously successful at invading many habitats (Larivière
and Pasitschniak-Arts 1996). They occur on six continents and have continued to
increase their range over the last century (Lewis and others 1993; MacPherson 1964;
Marsh 1938). Red foxes have also had tremendous impacts on native fauna in areas
where they have been introduced; in Australia their arrival is linked to the decline
and local extirpation of many native prey species (Burbidge and Manly 2002,
Burbidge and McKenzie 1989, Dickman 1996, Kinnear and others 1988, Kinnear and
others 1998).
Non-native red foxes were introduced into lowland California in the late
nineteenth century for fur farming and hunting. A localized population of these
animals in the Sacramento Valley was first described by Grinnell and others (1937),
who believed them to be distinct from the native Sierra Nevada red fox (V. v.
1
An abbreviated version of this paper was presented at the Sixth California Oak Symposium: Today's Challenges,
Tomorrow's Opportunities, October 9-12, 2006, Rohnert Park, California.
2
Graduate Student and Professors, respectively, Department of Environmental Science, Policy and Management,
University of California, Berkeley, CA 94720. e-mail: abidlack@nature.berkeley.edu; adina@nature.berkeley.edu;
getz@nature.berkeley.edu.
541
GENERAL TECHNICAL REPORT PSW-GTR-217
necator). Residents from five counties described hunting and trapping these valley
foxes beginning in about 1896 (Grinnell and others 1937). Foxes were also imported
and released in Orange County for hunting from 1905 to 1919 (Sleeper 1987).
Commercial fur farming became very popular in the mid-twentieth century, with
approximately 125 fox farms throughout California by the early 1940s (Vail 1942),
and many foxes undoubtedly escaped or were released from these farms (Lewis and
others 1993). Gray (1975) documented red foxes occupying 16 counties in Northern
California, with most sightings occurring in the Sacramento Valley. Gray (1975) also
described a population from Los Angeles County, and stated that there were
unconfirmed sightings in other Southern California localities. Most recently, Lewis
and others (1993) documented the presence of red foxes in 36 counties throughout
the state, excluding the North Coast, the Modoc Plateau, and the Mojave Desert.
Red foxes have been implicated in the decline in California of several federally
threatened and endangered bird species, including the light-footed clapper rail (Rallus
longirostris levipes), the California clapper rail (R. longirostris obsoletus), the
California least tern (Sterna antillarum browni), and the western snowy plover
(Charadrius alexandrinus nivosus; U.S. Fish and Wildlife Service 1990; U.S. Fish
and Wildlife Service and U.S. Navy 1990). While depredations of bird populations
have been well-documented, less is known about red fox impacts to mammalian prey
species and native carnivores. Anecdotal evidence suggests that red foxes have
replaced gray foxes (Urocyon cinereoargenteus) in some areas (J. Patton and R.
Barrett, pers comm), and that when red fox numbers are reduced, gray fox
populations rebound (J. DiDonato, pers comm). Red foxes have also killed several
federally endangered San Joaquin kit foxes (Vulpes macrotis mutica; Clark 2001;
Ralls and White 1995), and there is concern over possible introgression between nonnative red foxes and the Sierra Nevada red fox (Perrine 2005).
Red foxes are often associated with human-dominated landscapes and may
sustain very high densities in these heterogeneous habitats (Catling and Burt 1995;
Kurki and others 1998; Larivière and Pasitschniak-Arts 1996; Oehler and Litvaitis
1996). In urban Orange County, red foxes utilize open spaces such as golf courses,
airports and cemeteries (Lewis and others 1993). In North America, predation and
competition by coyotes (Canis latrans) may also be important in shaping red fox
distributions (Harrison and others 1989; Sargeant and others 1987; Sargeant and
Allen 1989; Voigt and Earle 1983). Coyotes tend to avoid urban or developed areas
(Gosselink and others 2003; Odell and Knight 2001), and these regions might provide
a refuge from coyote predation for red foxes.
Since the mid-seventies, non-native red foxes have been present and locally
increasing in number around the San Francisco Bay (J. DiDonato, pers comm.; Lewis
and others 1993). Counties surrounding the Bay Area support a diverse mix of highand low-density housing, vineyards, oak woodlands, and grasslands, resulting in a
complex interface between human-dominated landscapes and wildlands. However,
most of the undeveloped land is under private ownership and is subject to intense
vineyard and residential development pressure. If red fox dispersal and successful
establishment is predicated on landscape conversion, these development pressures
may lead to the continued red fox invasion of northern coastal California oak
woodlands. Our objective was to evaluate the abundance of red foxes in oak
woodlands in Contra Costa and Alameda counties, in order to assess the extent of
their spread from human-dominated habitats into wildlands in the East Bay.
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Distribution of Non-Native Red Foxes in East Bay Oak Woodlands—Bidlack
Methods
We used a geographic information system (GIS) to select core oak woodland sites in
Contra Costa and Alameda counties. Using the State of California Fire and Resource
Assessment Program vegetation classification layer, along with the Bay Area Open
Space Council open space layer, we examined the land cover within a 5 km2 circle
around the centroid of each open space polygon. We defined core woodland areas as
those circles that contained 25 percent to 75 percent combined hardwood, conifer and
shrub cover, of which at least 50 percent was hardwood. These constrictions ensured
that grasslands and closed-canopy forests were not included in our site selection and
that any cover was predominantly hardwood rather than shrub or conifer. We also
eliminated properties with greater than 5 percent water, wetland, urban, or agriculture
area. This provided us with 15 oak woodland dominated properties, under a variety of
ownerships, for which we eventually obtained permission to survey 12. Six of these
properties were sufficiently large enough to conduct two survey transects, making a
total of 18 transects (fig. 1).
Surveys for red fox were performed using a detection dog trained to locate the
scats of all canids and felids, excluding domestic dog. Scat sniffing dogs have proven
to be both remarkably efficient and precise in their searching. In prior research,
detection dogs have correctly identified 100 percent of target carnivore scats in a
matrix of sympatric species (Smith and others 2001, 2003) and have detected the
Figure 1—Location map of survey transects in the East Bay. BDM1 and BDM2,
Black Diamond Mines Regional Park; BR1 and BR2, Briones Regional Park; CAR,
Carnegie State Vehicular Recreation Area; CLAY, Clayton Land Bank; GDC1 and
GDC2, Garin/Dry Creek Regional Park; MT1 and MT2, Morgan Territory Regional
Park; OHL, Ohlone Wilderness; PLR1 and PLR2, Pleasanton Ridge Regional Park;
RV, Round Valley Regional Park; SR, Sky Ranch; SUN1 and SUN2, Sunol Regional
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GENERAL TECHNICAL REPORT PSW-GTR-217
Wilderness; and VAR, Vargas Land Bank. Sunburst symbol represents sites where
red foxes were found. Dark gray color represents urban areas, light gray is oak
woodlands.
presence of target species regardless of species density or vegetation type (Smith and
others 2005). In a controlled test, our dog detected 100 percent of scats placed within
10 m of the centerline of a transect along an unpaved road, and 98 percent of scats
within 20 m (Reed and Bidlack 2006). A pilot survey indicated that in these oak
woodland systems, most canid scats are deposited along trails, with surveying and
collection off-trail extremely difficult and inefficient (Bidlack Unpublished data).
Therefore, surveys were conducted along fire roads, and hiking and game trails.
Transect start points and direction were chosen randomly within the site, which
means that the land cover around the transect may differ slightly from that around the
centroid of the site. Each transect was 2-km long, and all transects were separated by
at least 2.5 km to increase independence of sampling (red fox home ranges vary
widely, but average 5 square km [Larivière and Pasitschniak-Arts 1996]). Due to
time and financial constraints, each transect was surveyed only once.
Collected scats were individually bagged and given an identification number and
a GPS location and subsequently stored at -800 C. Scats were later identified to
species using molecular genetic methods. DNA was extracted from each scat using a
small sub-sample (~500 g) that was removed from the outer surface or end of each
feces and used in a QIAamp DNA stool kit (Qiagen). Polymerase chain reaction
(PCR) was then used to amplify a 196 base pair segment of the mitochondrial
cytochrome b gene. Restriction fragment length polymorphism (RFLP) analysis
using three restriction enzymes (HpaII, DdeI and HpyCh4V) to cut this fragment was
used to separate coyote, gray fox, red fox, and bobcat scats (for protocols see Bidlack
and others 2006).
Results and Discussion
Eighteen 2-km transects were surveyed during the summer of 2005. We collected a
total of 383 scats, with a mean of 21.3 scats found per transect, and with a range of 5
to 48. There was a mean of 12.48 (± 8.83 s.d.) scats located per km. Using molecular
methods we identified 353 scats (92 percent) to species. Coyote scat was the most
prevalent at 222 (62 percent), followed by gray fox at 93 (26 percent), bobcat at 35
(10 percent), and red fox at three (1 percent). Coyotes were detected at all sites, while
bobcats and gray fox were detected at 11 and 7 sites, respectively. Red fox scats were
found at only two sites, Vargas Plateau and Garin/Dry Creek, both in Alameda
County (fig. 1).
Our study indicates that red foxes have not been particularly successful in
invading core oak woodlands in the East Bay. This may be the result of several
factors, one of which is the amount and pattern of development. Most previous
research in other regions suggests that red foxes are closely associated with disturbed
or heterogeneous habitats. In Australia, red foxes only occur in forested patches close
to areas that have been cultivated, heavily grazed, burned, logged, or converted to
residential development (Catling and Burt 1995). In Europe, red foxes are most
abundant in landscapes including 20 to 30 percent agricultural land (Kurki and others
1998). Urban areas may provide reliable sources of food, water, and cover for foxes;
in fact, local residents provided red foxes with supplemental food at every site
studied in Orange County (Lewis and others 1993). The two sites in which red fox
544
Distribution of Non-Native Red Foxes in East Bay Oak Woodlands—Bidlack
scats were found in our study were both near developed areas. Vargas Plateau is a
working cattle ranch, and Garin/Dry Creek Park directly abuts a dense residential
neighborhood, unlike all the other sites (some of which are adjacent to low-density
suburban developments). Another recent survey for foxes conducted in grasslands
(<25 percent canopy cover) in eastern Alameda and Contra Costa counties indicates
that red foxes may persist only near permanent water sources such as reservoirs and
canals (Clark and others 2003; Smith and others 2006). This study surveyed 17 sites
in these two counties and detected red foxes at only three sites, again confirming that
this species has on the whole not been successful in invading wildlands in Northern
California (Clark and others 2003; Smith and others 2006). Red foxes may not be
able to persist in wildlands far from developed areas, though they may survive in the
same types of habitats close to human development. This pattern has been observed
in other human-associated species (for example, domestic cats, cowbirds; Hejl and
others 2002; Maestas and others 2003; Morrison and Hahn 2002; Odell and Knight
2001). If red fox occupancy patterns reflect a reliance on human development, then
conserving large patches of undeveloped oak woodland habitat in the East Bay may
help buffer these habitats against invasion by red fox.
The high numbers of coyotes in the East Bay may also be excluding red foxes
from some areas, or keeping their abundance low. Coyotes are known to kill red
foxes (Sargeant and Allen 1989), and red foxes will avoid areas with high densities of
coyotes (Harrison and others 1989; Sargeant and others 1987; Voigt and Earle 1983).
We found coyote scats on all of our transects, indicating that they are ubiquitous in
oak woodlands in the Bay Area. We found no relationship between coyote abundance
and distance of the transect from developed areas. However, we found coyote scats
on the same transects with red fox scats. Currently, the relationship between these
two species is still unclear, and it is impossible to differentiate between coyote
presence and lack of development as impediments to red fox spread into core
woodlands. Similarly, we remain uncertain concerning the interaction between gray
and red foxes in these sites, in view of the fact that we found gray fox scats at both of
the sites that also supported red fox.
Recently, presence/absence surveys have come under criticism for a general lack
of detection rate estimates, leading to biased approximations of habitat occupancy
(MacKenzie and others 2006, and papers cited therein). However, surveys performed
by scat detection dogs are likely to detect more species and more samples per species,
especially for rare taxa, than other non-invasive survey methods such as searching by
humans, track plates, remote cameras, and hair snares (Harrison and others 2002;
Smith and others 2001). We made the assumption that all species were defecating on
roads and trails, and that there would be no detection bias by the dog among the
target species. Our findings concerning red fox occurrence are corroborated by the
results of Smith and others (2006), who surveyed some of the same properties (Black
Diamond Mines, Round Valley, Carnegie State Recreation Area) using a scatdetection dog, with negative results. Nevertheless, our surveys may be an
underestimate of species presence, given that transects were only surveyed once.
Our preliminary data suggest that in the East Bay red foxes have successfully
established populations only in core oak woodlands adjacent to human development.
Further research is needed to better quantify the habitat correlates of red fox as well
as to tease apart the relationships among the three canid species in the area. In this
way we may gain insight into the drivers of the red fox invasion, and the possible
impact of future development on the spread of this exotic species.
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GENERAL TECHNICAL REPORT PSW-GTR-217
Acknowledgments
We thank the East Bay Regional Park District, the Muir Heritage Land Trust, and
California State Parks for permission to survey their properties. We are also grateful
to Dr. Per Palsbøll for generously allowing us to use his genetics laboratory. This
work was supported by an American Society of Mammalogists Grant-in-aid of
Research to ALB.
References
Bidlack, A.L.; Reed, S.E.; Palsbøll, P.J.; Getz, W.M. 2007. Characterization of a western
North American carnivore community using PCR-RFLP of cytochrome b obtained
from fecal samples. Conservation Genetics 8: 1511-1513.
Burbidge, A.A.; McKenzie, N.L. 1989. Patterns in the modern decline of Western
Australia’s vertebrate fauna: causes and conservation implications. Biological
Conservation 50: 143-198.
Burbidge, A.A.; Manly, B.F. 2002. Mammal extinctions on Australian islands: causes and
conservation implications. Journal of Biogeography 29: 465-473.
Catling, P.C.; Burt, R.J. 1995. Why are red foxes absent from some eucalypt forests in
eastern New South Wales? Wildlife Research 22: 535-546.
Clark, H.O. 2001. Endangered San Joaquin kit fox and non-native red fox: interspecific
competitive interactions. Fresno, CA: California State University; 84 p. M.S. thesis.
Clark, H.O.; Smith, D.A.; Cypher, B.L.; Kelly, P.A. 2003. Detection dog surveys for San
Joaquin kit foxes in the northern range. Fresno, California: Endangered Species
Recovery Program. 37 p. Contract number 4600013447.
Dickman, C.R. 1996. Impact of exotic generalist predators on the native fauna of
Australia. Wildlife Biology 2: 185-195.
Gosselink, T.E.; Van Deelen, T.R.; Warner, R.E.; Joselyn, M.G. 2003. Temporal habitat
partitioning and spatial use of coyotes and red foxes in east-central Illinois. Journal
of Wildlife Management 67: 90-103.
Gray, R.L. 1975. Sacramento Valley red fox survey. Non-game wildlife investigation
progress report. Sacramento: California Department of Fish and Game. 6 p.
Grinnell, J.; Dixon, J.S.; Linsdale, J.M. 1937. Furbearing mammals of California.
Berkeley: University of California Press; 777 p.
Harrison, D.J.; Bissonette, J.A.; Sherburne, J.A. 1989. Spatial relationships between coyotes
and red foxes in eastern Maine. Journal of Wildlife Management 53: 181-185.
Harrison, R.L.; Barr D.J.; Dragoo, J.W. 2002. A comparison of population survey
techniques for swift foxes (Vulpes velox) in New Mexico. American Midland
Naturalist 148:320-337.
Hejl, S.J.; Mack, D.E.; Young, J.S.; Bednarz, J.C.; Hutto, R.L. 2002. Birds and changing
landscape patterns in conifer forests of the north-central Rocky Mountains. Studies
in Avian Biology 25:113-129.
Kinnear, J.E.; Onus, M.L.; Bromilow, R.N. 1988. Fox control and rock wallaby population
dynamics. Australian Wildlife Research 15: 435-477.
Kinnear, J.E.; Onus, M.L.; Sumner, N.R. 1998. Fox control and rock wallaby dynamics II. An update. Wildlife Research 25: 81-88.
546
Distribution of Non-Native Red Foxes in East Bay Oak Woodlands—Bidlack
Kurki, E.G.; Nikula, A.; Helle, P.; Linden, H. 1998. Abundances of red fox and pine
marten in relation to the composition of boreal forest landscapes. Journal of Animal
Ecology 67: 874-886.
Lariviere, S.; Pasitschniak-Arts, M. 1996. Vulpes vulpes. Mammalian Species 1-11.
Lewis, J.C.; Sallee, K.L.; Golightly Jr., R.T. 1993. Introduced red fox in California. NonGame Bird and Mammal Section Report 93-10. Sacramento: California Department of
Fish and Game. 70 p.
MacKenzie, D.I.; Nichols, J.D.; Royle, J.A.; Pollock, K.H.; Bailey, L.L; Hines, J.E. 2006.
Occupancy Estimation and Modeling: inferring patterns and dynamics of species
occurrence. Oxford: Elsevier, Inc.; 324 p.
MacPherson, A.H. 1964. A northward range extension of the red fox in the eastern
Canadian arctic. Journal of Mammalogy 45: 138-140.
Maestas, J.D.; Knight, R.L.; Gilgert, W.C. 2003. Biodiversity across a rural land-use
gradient. Conservation Biology 17: 1425-1434.
Marsh, D.B. 1938. The influx of the red fox and its colour phases into the barren lands.
Canadian Field-Naturalist 52: 60-61.
Morrison, M.L.; Hahn, D.C. 2002. Geographic variation in cowbird distribution,
abundance and parasitism. Studies in Avian Biology 25:65-72.
Odell, E.A.; Knight, R.L. 2001. Songbird and medium-sized mammal communities
associated with exurban development in Pitkin County, Colorado. Conservation
Biology 15: 1143-1150.
Oehler, J.D.; Litvaitis, J.A. 1996. The role of spatial scale in understanding responses of
medium-sized carnivores to forest fragmentation. Canadian Journal of Zoology 74:
2070-2079.
Perrine, J.D. 2005. Ecology of red fox (Vulpes vulpes) in the Lassen Peak region of
California, U.S.A. Berkeley, CA: University of California. Ph.D. dissertation.
Ralls, K.; White, P.J. 1995. Predation on San Joaquin kit foxes by larger canids. Journal of
Mammalogy 76: 723-729.
Reed, S.E.; Bidlack, A.L. 2006. Optimizing field surveys using wildlife detection dogs.
Unpublished draft.
Sargeant, A.B.; Allen, S.H.; Hastings, J.O. 1987. Spatial relations between sympatric
coyotes and red foxes in North Dakota. Journal of Wildlife Management 51: 285-293.
Sargeant, A.B.; Allen, S.H. 1989. Observed interactions between coyotes and red foxes.
Journal of Mammalogy 70: 631-633.
Sleeper, J. 1987. Bears to briquets: a history of Irvine Park 1897-1997. Trabuco Canyon,
CA: California Classics; 32 p.
Smith, D.A.; Ralls, K.; Davenport, B.; Adams, B.; Maldonado, J.E. 2001. Canine assistants
for conservationists. Science 291: 435.
Smith, D.A.; Ralls, K.; Hurt, A.; Adams, B.; Parker, M.; Davenport, B.; Smith, M.C.;
Maldonado, J.E. 2003. Detection and accuracy rates of dogs trained to find scats of
San Joaquin kit foxes (Vulpes macrotis mutica). Animal Conservation 6: 339-346.
Smith, D.A.; Ralls, K.; Cypher, B.L.; Maldonado, J.E. 2005. Assessment of scat-detection
dog surveys to determine kit fox distribution. Wildlife Society Bulletin 33: 897-904.
Smith D.A.; Ralls, K.; Cypher, B.L.; Clark, H.O.; Kelly, P.A.; Williams, D.F.; Maldonado,
J.E. 2006. Relative abundance of endangered San Joaquin kit foxes (Vulpes macrotis
mutica) based on scat-detection dog surveys. Southwestern Naturalist 51: 210-219.
547
GENERAL TECHNICAL REPORT PSW-GTR-217
U.S. Fish and Wildlife Service. 1990. Predator management plan and environmental
assessment, San Francisco Bay National Wildlife Refuge. Draft report. Newark, CA.
26 p.
U.S. Fish and Wildlife Service; U.S. Navy. 1990. Endangered species management and
protection plan, Naval Weapons Station - Seal Beach and Seal Beach National
Wildlife Refuge. Final Environmental Impact Statement. Portland, OR. 591 p.
Vail, E.L. 1942. Fox ranching in southern California. California Fish and Game 28: 87-88.
Voigt, D.R.; Earle, B.D. 1983. Avoidance of coyotes by red fox families. Journal of Wildlife
Management 47: 852-857.
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