A review of native and nonnative red foxes in North America

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NATIVE AND NONNATIVE RED FOXES370

review of native and nonnative red foxes North America

Jnn E Knmler and Warrea B. Bnllard Abstract Native and nonnative red foxes (Vulpes vulpes) reportedly occur in North America,

although the origin and taxonomy of many populations often are unknown and disputed. To help elucidate the origin and taxonomy of red fox populations in North America, we conducted a literature review that focused on the historical distribution of native red foxes, known populations of nonnative red foxes, range expansions during the 1900s, taxonomic and ecological differences between native and nonnative red foxes, and impacts of nonnative red foxes on native species. Our review indicated that native red foxes are a boreal species that historically occurred in the northern regions of North America and in the southern refugia ot' montane habitats at higher elevations throughout the western United States. Nonnative red foxes, from European origin, were introduced throughout the eastern United States and in lowland areas in the Pacific coast states. From a source population in the eastern United States, red foxes expanded westward throughout the central United States and Canada during the 1900s, indicating that these red foxes were nonnative. Nonnative red foxes thrive in human-altered habitats such as urban and agricultural areas and have invaded diverse ecosystems ranging from desert to arctic tundra. Nonnative red foxes have negative impacts in many ecosystems where they now occur because they are generalist predators that attain relatively high densities. Nonnative red foxes likely replaced native red foxes throughout all northern boreal regions and may threaten remaining native populations at higher elevations in the western United States. The taxonomy of red foxes in North America needs to be re-evaluated. Although native and nonnative red foxes in North America are considered conspecifics, there are sub- stantial differences in coloration, morphology, behavior, and habitat requirements between these 2 types.

Key words distribution, native red fox, nonnative red fox, range expansion, taxonomy, Vulpes vulpes

Red foxes (Vulpes vulpes) are common preda- has been reviewed for the eastern United States tors that occur throughout much of North America. (Churcher 1959) and the Pacific Coast states Both native and nonnative red foxes reportedly (Aubry 1984, Lewis et al. 1999). Churcher (1959) occur in North America (Churcher 1959, Aubry found that native red foxes did not historically 1983, Crabtree 1993, Lewis et al. 1999), although occur in the mixed hardwood forests of the eastern the origin and taxonomy of many populations are United States. Due to the absence of native red unknown and disputed. Native red foxes reported- foxes in this region, early settlers began releasing ly are a cold-adapted species that occurs in boreal European red foxes for sport hunting in the mid- and montane habitats, whereas nonnative red foxes 1700s (Churcher 1959, Godin 1977). This popula- reportedly are a generalist species that occurs in a tion of nonnative red foxes was augmented by wider variety of habitats (hubry 1983, Crabtree other intentional releases over the next 150 years. 1993). The taxonomy and distribution of red foxes thus establishing a continuous population across

Authors address: Department of Range, Wildlife, and Fisheries Management, Texas Tech University, Box 42125, Lubbock, TX 79409, USA;e-mail for Kamler: [email protected].

Wildlife Society Bulletin 2002, 30(2):370-379 Peer refereed

Native and nonnative red foxes Kamler and Ballard 371

the eastern United States (Churcher 1959). A dis-junct population of introduced red foxes was estab-lished in a similar manner during the past 100 years along the western coast of the United States from Washington to California (Aubry 1984,Lewis et al. 1999). Red foxes introduced in this region were from the eastern United States (A~ibry1984,Lewis et al. 1999), indicating they also were descendants of European red foxes.

Red foxes, from unknown origin, expanded throughout most of the central and western United States during the past 100 years (Fichter and Williams 1967, Hoffman et al. 1969,Johnson and Sargeant 1977.Voigt 1987). Most literature sources indicated that populations in these regions were native red foxes that had recovered from low num-bers, or had expanded from adjacent regions (Fichter and Williams 1967,Johnson and Sargeant 1977. Fitzgerald et al. 1994). Thus, despite a large and continuous population of nonnative red foxes throughout the eastern United States, many biolo-gists consider red foxes in the central and western United States to be from native origin. Red foxes that expanded westward throughout the arctic tun-dra during these same periods were also consici-ered to be of native origin (Marsh 1938, MacPher-son 1964).

Clearly, a review of the origin and taxononly of red foxes in the central United States and Canada is needed. This information would be valuable to wildlife biologists, as management decisions and conservation efforts could be based on whether red foxes were native fauna or introduced preda-tors. If nonnative red foxes do occur throughout the central United States and Canada, their poten-tial to negatively affect native prey species might be great. For example, nonnative red foxes have caused severe declines or extinctions of native fauna, including threatened and endangered species, in several regions of the world (Brockie et al. 1988. Strahan 1995, Dickman 1996, Lewis et al. 1999). If negative impacts of nonnative red foxes are occurring,or could potentially occur in the cen-tral United States and Canada, control measures may be needed to prevent or lessen the damage of tlonnative red foxes on native species.

Little is known about the ecology and distribu-tion of native red foxes in the western United States because they occur in low densities at high eleva-tions, are sensitive to human activities, and have received little study (Aubry 1983, Crabtree 1993). Native red foxes often are not distinguished from

nonnative red foxes in management programs by state and provincial agencies. However, it is impor-tant that biologists distinguish between native and nonnative red foxes in their management practices. especially if populations of native red foxes are threatened and consequently need to be protected.

Our objectives were to review the: 1) historical distribution of native red foxes in North America, 2) range expansion of red foxes in the central Unit-ed States and Canada, 3) taxonomic and ecological differences between native and nonnative red foxes, and 4) actual and potential impacts of non-native red foxes on native species.

Methods We reviewed historical and more recently pub-

lished information concerning the range of native red foxes in North America. We catalogued refer-ences on a state-by-state and provitlce-by-province basis to examine the distributional changes and range expansion of red foxes during the past 100 years in the central United States and Canada. We also documented and summarized the taxo~lomic and ecological differences between native and non-native red foxes. From our review we identified impacts of nonnative red foxes on native species and ecosystems in the IJtlited States and other areas of the world. Finally,we also obtained recent infor-mation concerning livestock depredations by non-native red foxes in western states.

Results Historical distribution of native red foxes in North America

Prior to European settlement, native red foxes occurred in the boreal forests of Canada and north-ern ITnited States and in the southern refugia of montane habitats in the western United States (Churcher 1959.A~ibry1983.Crabtree 1993.Figure 1). Subspecies of native red foxes likely were derived from 2 different ancestral populatiotls (Aubry 1983) The subspecies that occur in mon-tane habitats in the weqtern United States (i.e . Vr! casc~~densis,ti zt macrour-a,and V L: necatol-) likely were derived from populations of red foxes that occurred south of the Wisconsi~lglaciers during the Pleistocene. When these glaciers retreated 10-12.000 years ago, those subspecies became restricted to the southern refugia of montane habi-tats at higher elevations (Aubry 1983). These sub-

372 Wildlife Socieg Bulletin 2002.30(2):370-379

Figure 1. Probable distribution of subspecies of native red foxes (Vulpes vulpes) in North America prior to European settlement, based on information primarily from Churcher il9593, Hall and Kelson (1959),MacPherson (19641, and Aubry (1983). Letters represent different subspecies: A = L! v. aiascensis, B = 1! v. abeitorom, C = C: L!. cdscadensis, D = L! v. necator, E = \i v. macroura, F = L! v. rigalis, and G = C: v. rubricosn. Crossed diagonal lines indicate populations of C: v. rigalis that were extirpated by 1900 dones 1964, Dekker 1973, Johnson and Sargeant 1977).

species are n~orphologicall~~ the smallest, show no clinal ~~ariations, and do not intergrade geographi- cally with the other subspecies (Aubry 1983). The subspecies that occurred throughout the boreal forests of northern North America, primarily K v. alnscensis, K v.nbietorum, K L! rigalis, and R 2:. rubricosn. likely were derived from populations of red foxes that spread south from Beringia after the Wisconsin glaciers retreated, although some south- derived populations may have integrated with north-derived populations in the extreme northern Lhited States (Aubrj 1983). These subspecies show a clinal variation with decreasing size from the northwest to the southeast portion of their range (Churcher 1957, Aubry 1983).

Based on historical records, native red foxes (Re). rigalis) extendecl south~vard from the boreal forests into the northern Great Plains (Hoffman 1877, Johnson and Sargeant 1977), as far south as central Nebraska aones 1964 Figure 1). Although there is no fossil evidence (Baird 1857), the pres- ence of red foxes in the northern Great Plains was based on historical records of red fox specimens from the region. During the Lewis and Clark expedition, 1803-1806, red foxes were reported in the northern plains near Fort Mandan in central North Dakota. Fourteen red fox pelts were sent to Wash-

ington, D.C. in 1805 after their winter encampment (Burroughs 1961). Red foxes were reported near Fort Clark in central North Dakota in 1833 by the explorer Maximilian (Bailey 1926) and were reported by Hoffman (1877) in north-central Somh Dakota. Red foxes were reportedly trapped as far nJest as the pine (P~MZIS spp.) forests in northwestern South Dakota wisher 1914). South-central Nebraska appeared to be the soutl~ern extent of red foxes in the Great Plains, as red fox specinlens were reported from eastern and south-central Nebraska from the 1820s to 1870s (Jones 1964). In general, south-central Nebraska was the historical southern limit for many mammalian boreal species in the central United States @rey 1992). A few sightings of red foxes occurred in more southern areas of the Great Plains during the 1800s, including western Kansas (Zumbaugh and Choate 1985) and southern Oklahoma (Caire et al. 1989). However, these sight- i n g ~should be used with caution because during the mid-1800s the name "common red fox" was interchanged with "grey fox" to describe C'rocyo~z cinereoarge?ztezcs, as was done during the Lewis and Clark expedition (Burroughs 1961). The tern1 "large red fox" was used to describe VuQes vulpes in these cases (Burroughs 1961). Without specimens, the occurrence of red foxes in more western and southern areas of the Great Plains cannot be confirmed.

Native red foxes in the northern Great Plains occurred at Ion7 densities and apparently were sensitive to human activities (Dekker 1973). Conse-quently, native red foxes disappeared from south- central Canada to Nebraska by the late 1800s as this area became settled (Jones 1964, Dekker 1973, Wrigley 1974, Johnson and Sargeant 1977 Figure 1).

Range expansion across tbe central United States and Canada

Red foxes began to expand sitnultaneously from the southeast and east across the central tier of states in the early 1900s (Figure 2). From the 1900s to 1920s, red foxes from populations farther east expanded into areas where they never occurred historically, including east-central Texas (Strecker 1926. Taylor and Davis 194'), eastern Oklahoma (Cross 19 17), eastern Kansas (Kellogg 191 5, Dice 1923, Lindsdale 1928), and southeastern Nebraska (Swenk 1908). This expansion continued westward into the 1930s, when red foxes expanded into eastern North Dakota (Johnson and Sargeant 1977). southern Manitoba (Bird 1961, Soper 1961). central

Native and nonnative recl foxes Kamler and Ballard 373

Figure 2. Known distribution ancl westward range expansion of nonnative red foxes (Vulpes vulpesj in central and western North America at various periods during the past century (See Results for references of individual states and provinces!. A similar and concurrent westward range expansion occurred throughout the arctic tundra (~LlacPherson1964).

Oklahoma (Blair 1939),and central Kansas moost-er 1931). In the 1950s. red foxes continued to expand westward into western Oklahoma,exclud-ing the Panhandle (Glass and Halloran 1960),west-ern Kansas (Anderson and Nelson 1958.Janes and Gier 1966,Zumbaugh and Choate 1985),western Nebraska (Jones 1964), western North Dakota ('Johnson and Sargeant 1977), and southeastern Saskatchewan (Stoudt 1971). In the 1960s red foxes expanded into west-central Texas (Packard and Bon-ers 19'0). eastern Colorado (Armstrong 1972), eastern Idaho (Fichter and Williams 1967), eastern Montana (Hoffnlann et al. 1969),and south-western Saskatchewan (Dzubin and Gollop 19'2), nr1lerethey never had been previously reported. In the 1970s,red foxes expanded into southern Alber-ta where. they had been absent since 1900 (Dekker 1973), the Oklahoma Panhandle (Hatcher 1982), western Texas (Swepston 1980), and eastern New Mexico (G. Schmitt, New Mexico Department of

Game and Fish, unpublished data). During the 1980s. red foxes expanded throughout lom7land areas in Utah and Nevada ('J. E Kamler,Texas Tech UniversiQ unpublished data) In all cases. expan-sion of red foxes in individual states and provinces occurred from east to west.

Although red foxes now occur throughout tun-dra habitats of northern North America (Hall and Kelson 1959),they did not occupy those areas his-torically (Marsh 1938,MacPherson 1964). Begin-ning in the 1910s,red foxes began expanding into the arctic tundra in northeastern Canada (MacPher-son 1964). Over the next 50 jears, this expansion progressed westward across the northern tundra (Marsh 1938, hlacpherson 1964) in concert with the range expansions farther south in the central United States. Bj the 1960s,red foxes occupied the entire Baffin Island,southern Elleslncre Island,and the mainland northwest of Hudson Bay (Marsh 1938, MacPherson 196+). Red foxes eventually became conlmon in these areas (MacPberson 1964).

Dz~etfleizcesbetuleen native and nonnative red foxes

Native and nonnatibe foxes in the western Unit-ed States differ in morphology and ecologj-. There are 3 major color phases of red foxes found throughout the world: red, silver (or black), and cross (Bailey 1936,Durrant 1952, Churcher 1959, Hall and Kelson 1959.Henrj 1996). The red color phase is typical of red foxes throughout most of the Old World (Lloyd 1975,L70igt1987) and of nonna-tive red foxes in the LTnited States (Bailey 1936. Churcher 1959, Aubry 1983). In contrast, color phases other than red are typical of native red foxes in North ,herica. Most native red foxes (Rr: necn-to?,)from the Sierra Nevada hlountains of California and Nevada exhibit the cross and silver color phas-es (Grinnell et al. 1937,Hall 1946). Similarly,most native red foxes from higher elevations in and around Yellowstone National Park exhibit the cross color phase (Crabtree 1993). The different color phases of red foxes in mountainous areas were also reported during the Lewis and Clark expeclition (1803-1806). as Lewis observed a cross phase and silver phase red fox in the higher elevations of western Montana and Oregon. respectively (Bur-roughs 1961). Of native red foxes that exhibit the red color phase, including Kzl. cascadelzsis and Yu. macrourn, most exhibit a pale red or pale yellow-ish color (Merriam 1900, Bailey 1936, Read and

374 W'ilcll~e Sociep Bulletin 2002.30(2):370-379

Gaines 1914, Fichter and Williams 1967, Aubry 198.3, Hoffmeister 1986), designated as "light" color phase by Bailey (1936). In contrast, nearly all Old World and nonnative red foxes exhibit a dark red or cherry recl color (Obbard 1987). Morphologically, nonnative red foxes in the western United States are larger than native red foxes, although some overlap in size occurs (Aubry 1983).

In the western United States, color phase appears to be somewhat reliable for distinguishing between native and nonnative red foxes. However, since overlap in color occurs, a better method for distinguishing between native and nonnative red foxes relies on elevational differences (Aubry 1983, Lewis r t al. 1999). It1 Washington.native red foxes (Vz! cns- cadensis) and nonnative foxes were restricted to high- and low-elevation areas, respectivel?; and their ranges clid not intergrade (Aubry 1983). Similarly, native (V r ! rzecator) and nonnative red foxes were separated by elevational differences in California (Le\\ is et al. 1999). Thus, locations at high elevations, sucl~ as subalpine meadows and parklands, are characteristic of native red fox habitats, whereas all othcr locations at low elevations, such as agriculture, rangeland. and urban areas, are characteristic of nonnative red fox habitats. In addition to their more restricted requirements, native red foxes occur at relatively low densities (Aubry 1983. Crabtree 199 3). which may contribute to the lack of specimens and information concerni~lg these subspecies. In contrast, nonnative red foxes occur at relatively high densities (0.5-1.0 red fox/km2 [Sargeant 1972, Voigt 19871) in many areas throughout their range.

Inzpacts of nonnative red foxes The negative effects of nonnative red foxes on

native prey populations can be significant. In Aus- tralia, nonnative red foxes. also of European origin, were introduced in the 1860s for sport and to control tlonnative rabbit ( O ~ ~ ~ c t o l a g ~ ~ s pop-czi~liculzu) ulations (Strahatl 1995. Dickman 1996). These red foxes, n7hich expanded throughout most of ALE-tralia by the 19.30~~ had severe negative impacts on native species and ecosystems. Nonnative red hxes eliminated remnant populations of some rodent and marsupial species on the mainland. and e\.idence suggested they were the primary cause in the decline or extinction of many other small and meclium-sized rodent and n~arsupial species (Stra- han 1995. I>ickman 1996). Consequently concen- trated control measures for red foxes on the mainland have resulted in the direct resurgence of 7

species of marsupials, including 5 endangered species (Strahan 1995).

In North America, the negative impacts of nonnative red foxes on nesting ducks in the prairie pothole region has been well documented (Sargeant et al. 1984, Johnson et al. 1989). Lewis et al. (1999) indicated there were 24 threatened and endangered species that were vulnerable or potentially vulnerable to nonnative red foxes in California. Consequently, nonnative red foxes are controlled in California to protect the nesting grounds of several endangered species of birds (Lewis et al. 1999). Nonnative red foxes have just recently expanded into the Great Basin region, and because of heavy predation they are already reducing populations of pheasants (Phnsinnus colchicus), (Frey et al. 2000), sage grouse (Centmcerciu zirophasiatzus), (Bun- nell et al. 2000), and nesting ducks (S. N. Frey, Utah State University unpublished data). Control measures have been initiated to reduce nonnative red fox damage in this region as well (Bunnell et al. 2000, Frey et al. 2000). Evidence suggests that nonnative red foxes could negatively impact endangered San Joaquin kit foxes (t'ulpes ~~zncrotis muti-en), (Ralls and White 1995) and possibly swift foxes (Vvelox). a species recently petitioned to be listed as threatened (Sovada et al. 1998).

Nonnative red foxes also prey on livestock. Of all United States Department of Agriculture (USDA) Wildlife Services' clients nationwide in 1998, red foxes were responsible for 1%) of sheep, 5%of lamb. 2% of goat, and 9%) of kid losses to predators (1999 Livestock Wildlife Damage Susvey Results, USDA- Wildlife Services, unpublished report). Nonnative red foxes are also a health threat to humans and pets through transmission of disease, such as rabies, distemper, parvo virus, and mange (Carey 1982, Voigt 1987, Davidson et al. 1992. Lewis et al. 1999). This threat is likely to increase as populations of nollnative red foxes continue to expand and invade more urban areas (Lewis et al. 1999).

Discussion Red foxes that expanded westward across the

central United States and Canada during the 1900s were likely nonnative, as the source of this expansion came from populations of nonnative red foxes in the eastern United States. Previous researchers have found that nonnative red foxes occurred throughout the lower elevations of Oregon. Califor- nia, and Washington, whereas native red foxes


occurred in limited areas at higher elevations in those states (Aubry 1983,Lewiset al. 1999). Similar relationships might occur among native and non-native red foxes in other mountainous western states, as red foxes now occur throughout these states at both high and low elevations (Fichter and Williams 1967, Hoffmann et al. 1969, Clark and Stromberg 1987,Fitzgerald et al. 1994). However, red foxes in these areas are usually not distin-guished as native or nonnative. For example,in Col-orado, Idaho, and Montana, native red foxes (8v. nzacmum) occur at higher elevations,although red foxes recently expanded throughout lowland areas of those states (Fichter and Williams 1967, Hoff-mann et al. 1969.Armstrong 1972,Fitzgerald et al. 1994). Fichter and Williams (1967) and Fitzgerald et al. (1994) were unsure of the taxonomy of the "new"lowland red foxes and suggested classifying them as Vz! rnacroura or Vv, rigalis. Similarly pre-vious researchers correctly classified red foxes in the mountains of western Wyoming as V 21.

nzacmura but classified red foxes in low elevations of eastern Wyoming as Kv. rigalis (Long 1965,Clark and Stromberg 1987). Our review, along with oth-ers (Aubry 1983,Crabtree 1993,Lewis et al. 1999), suggests that red foxes in lowland areas are nonna-tive red foxes that have recently expanded through-out the western United States.

Similarly, red foxes that currently occupy the northern Great Plains are usually classifled as native red foxes (Vzl rigalis, Jones et al. 1983). Although Vz! rigalis occupied portions of the northern Great Plains in pre-European times, these red foxes disap-peared completely in the late 1800s when this region was settled. Beginning in the 1930s, the northern Great Plains was occupied by expanding populations of nonnative red foxes from the east-ern United States, and these foxes were well adapt-ed to human settlement and human-induced changes to the environment. Nonnative red foxes are descendants from European stock and therefore are better adapted to human activities, urban areas, and human-induced changes to the environment (i.e.. habitat fragmentation, agriculture). For exam-ple. Dekker (1973) stated that the new populations of (nonnative) red foxes that had recently expand-ed into central Alberta were more adaptable and better able to cope with the human-dominated environment than previous populations of (native) red foxes (K 2: abeitorum) that disappeared from that area in the early 1900s. Additionally, >99% of red foxes from populations that expanded across

the central United States and southern Canada exhibited the red color phase (Obbard 1987.Voigt 1987), which was typical of nonnative red foxes from European origin.

Previously,researchers hypothesized that newly established red foxes in the northern Great Plains were native red foxes (Vz: rigalis) that had recov-ered from low populations or reoccupied parts of their former range (Johnson and Sargeant 1977, Jones et al. 1983). For example, Johnson and Sargeant (1977) suggested that reductions in coj-ote (Cavzis latrans) populations after 1915 allowed native red fox populations to recover in the north-ern Great Plains However, 20 years occurred between reduced coyote populations and the reap-pearance of red foxes (Johnson and Sargeant 1977), suggesting that they were not related events. If native red foxes reoccupied their former range in the northern Great Plains, then expansion should have occurred from the nearest source populations found in the boreal forests of Canada and northern Great Lakes region,or the montane habitats at high-er elevations in the western United States. This did not occur, as red foxes expanded across the north-ern Great Plains from east to west. Furthermore, native red foxes from western mountains. such as Vzt nzacroura,have never expanded their range, as these are cold-adapted foxes that occur in the southern refugia of high alpine meadows (Aubry 1983,Crabtree 1993). Aubry (1983) indicated that V 21. nzacroum did not occupy low elevations, and that valleys at low elevations were barriers between adjacent populations at higher elevations.

It is also unlikely that native red foxes (Kz! rigalis) from northern boreal forests have expanded their range southward throughout the central United States. Some mammalian boreal species (all small mammals) have expanded southward into the cen-tral United States during this past century (Frey 1992); however, this likely did not occur for red foxes. Range expansions of other mammalian bore-al species occurred distinctly in a north-to-south direction (Frey 1992), as expected, whereas range expansion of red foxes started in the southeastern United States and occurred in an east-to-west direc-tion. This east-to-westexpansion during the past 100 years occurred throughout south-central Canada and central United States without any north-to-south or west-to-east expansions from nearby source popula-tions of native red foxes. Furthermore,range expan-sion of red foxes continued westward throughout the western Great Plains and lowland areas of the

376 WIIdlIfeSociety Bulletin 2002,30(2):370-379

arid Southwest and Great Basin regions, which were not typical eilvironments for a boreal subspecies. Native red foxes historically did not occur in these regions, indicating that the new red foxes were not recovered populations of a boreal subspecies.

Little is known concerning the status of native red foxes in the higher elevations of the western United States. Recent evidence suggested that native red fox populations in these areas have declined since the 1800s (Aubry 1983, Crabtree 1993). Native red foxes have not been docuine~lt- ed in some areas of the western Vnited States in >50 years (Durrant 1952). Their status is now com- plicated by the relatively new occurrence of nonnative red foxes in most lowland areas of the western United States. If native red foxes still occur over much of the western United States, then their populations may now be vulnerable to inbreeding or competition with the more numerous and larger nonnative red foxes, which can thrive in hurnan- altered habitats. The California Fish and Game Commission is the only state agency that distin- guishes between native and nonnative red foxes in its management practices. Nonnative red foxes in lowland areas of California are often controlled to protect endangered bird species (Lewis et al. 1999), whereas native red foxes ( V Z Lnecntor) in the Sier- ra Nevada moulltain range are fully protected and research is being conducted to document their cur- rent numbers and distribution (Kucera 1993). Other state and provincial agencies should have similar policies, as remaining populations of native red foxes may be threatened.

Similar to more southern areas, populations of native red foxes in the northern boreal forests may also be vulnerable to expanding populations of nonnative red foxes. Red foxes expanded westward across the northern tundra during this past century. Similar to differences reported in more southern areas of North America, MacPherson (1964) stated that the"newX red foxes in the North- west Territories were quite different from previous populations of red foxes. Original populatiolls of red foxes occurred in low densities and were found only in the boreal forests in more southern areas of the region (MacPherson 1964). In contrast. the "new" red foxes occupied tundra habitats and attained densities "far in excess of those in the original population" even in the nearby boreal forests (MacPherson 1964: 140). Additionally, these new red foxes also occupied small towns, which were

not occupied by the original red fox populations (Marsh 1938. MacPherson 1964), indicating that the new red foxes were nonnatives.

In addition to changes in distribution, behavior, and density a review of red fox color morphs from Hudson's Bay Company posts over this same period showed an increase in frequency of the red color phase (Butler 1945, 1917; Swanson and Johnson 1996), which was typical of nonnative red foxes from European origin. Consequently. color morphs of native species, such as black-silver and cross, decreased throughout northern Canada (Butler 1945,1947; Swanson and Johilson 1996) and disappeared completely from some areas such as eastern Canada (Haldane 1942). Previously. researchers hypothesized several different explanations for the increasing dominance of the red color phase across Canada, including selective hunting, selective trap- ping, differential reprochictive success among color morphs, and dispersal or swamping by red-colored foxes from farther south (Haldane 1942, Butler 1945. Calhoun 1950, Swanson and Johnson 1996).

Ek hypothesize that the westward range expansion of nonnative red foxes was responsible for changes in red fox color inorphs across Canada during the past 150 years. Nonlrative red foxes expanded their range westward throughout the tundra and northern boreal forests during the same periods they expanded westward throughout the lower United States and southern Canada. The decrease. and in some areas elimination, of native red fox color morphs suggests that the more nunlerous nonnative red foxes replaced or hybridized with native red foxes throughout all or most of the northern boreal forests during this past century. If this has occurred, then subspecies of native red foxes throughout the northern boreal forests, including Kz:. nlnsce~zsis,Kzj. nbietorzlnz, K z! rigulis,and V a rz~bricosa,may be extinct.

Nonnative red foxes, a generalist predator, have caused severe declines and extinctions of native species on other continents (Strahan 1995. Dick- man 1996). In North America nonnative red foxes prey heavily on native species, iilcluding threatened and endangered species, in many areas of their range (Sargeant et al. 1984. Johnson et al. 1989. Lewis et al. 1999, Bunnell et al. 2000. Frey et al. 2000). Because nonnative red fox populations are still expanding and increasing in many areas, their negative impacts on native species may also increase. Long-tern~ effects of nonnative red foxes on prey populations in many areas are unknown.


Nonnative red foxes have the potential to cause declines and possible extinctions of native species on this continent, possibly because many of the most vulnerable species, such as ground-nesting birds, did not evolve with this particular sub-species. Cotlsequently, the recent appearance of nonnative red foxes in these ecosystems ma); lower the carrying capacity of ground-nesting bird popu-lations, with possible extirpation of some species. In areas such as the northern Great Plains,the den-sities of nonnative red fox populations (0.5 red fox/km2.Sargeant 1972) are likely higher than that of historic native red fox populations, which reportedly occurred in low numbers (Jones 1964, Johnson and Sargeant 197'). Consequently preda-tion rates of nonnative red foxes are higher than that of any native carnivore species (Johnson et al. 1989). Overall densities of red foxes increased as nonnative red foxes expanded westward across northern Canada (MacPherson 1964).also suggest-ing that nonnative red foxes occurred at higher densities than native red foxes.

Finall!; the taxonomic status of red foxes in North America is questionable. Red foxes in east-ern and southern United States are classified as V!'u ,firlzzz,although there may be no scientific basis for this subspecific designation. Because red foxes classified as Kz!fr~lz!nare likely from European ori-gin, Churcher (1959) and Hall and Kelson (1959) questioned their subspecific designation. Red foxes introduced in eastern North America by early settlers primarily came from Great Britain and France. I:' r : cl-~tcigrm,and Scandinavia. K z: i!ulpes (Churcher 1959). Thus, nonnative red foxes in North America are likely hybridized forms of reci foxes from several different Old World subspecies. These ~lonnativered foxes have now occupied nearly all of the United States and probably all of Canada. Nonnative red foxes have recently expand-ed southward into northern Mexico (Arnaud 1990), and thus may continue to expand southward throughout other areas of the New World.

Prior to 1959,red foxes in North America were classified as ITfzrlzm, a different species than Old World red foxes. I! z~zdpes.A separate species des-ignation for New World red foxes was based on dif-ferences in morphology and coloration from Old World red foxes. and this distinction was upheld by several early mammalogists (Bangs 1897, Merriam 1900, Bailey 1936). Churcher (1959) compared skull morphology and pelt coloration between red fox specimens in North America with specimens

from Europe and Asia. Churcher (1959) concluded that there were not sufficient differences between New World and Old World red foxes to designate a separate species, and subsequently New World red foxes were classified as K uulpes. However. Churcher (1959) apparently was unaware of the range expansion of nonnative red foxes in North America that had already occurred. At least 73%of the North American specimens used by Churcher (1959) were from regions where nonnative red foxes had become well established by the 1950s. Thus, many specimens that presumably represent-ed native red foxes may have been nonnative red foxes with Old World origin. Clearly, a thorough review of red fox taxonomy in North America is needed. More advanced techniques, such as genet-ic analyses, may prove usefiil for determining the taxonomy of red foxes in North America.

Acknoulledgments. We thank the personnel from state and federal agencies and universities that provided information concerning red foxes,includ-ing D. C. Backlund, R. Beach, M. J. Bodenchuk, S. Fairaizl. S. N. Fre): R. L. Gilliland,R. L. Harrison, G. A. Littauer. J. D. Perrine, J. Phelps, C. Richardson.W. K. Smith. M.A. Sovada,and S. Stivers. We also thank S. Cunningham, C. Jones, and three anonymous reviewers for helpful comments on this manu-script. C. C. Perchellet and B. Kamler helped pro-duce the figures. This is Texas Tech University,Col-lege of Agricultural Sciences and Natural Resources technical publication T-9-8'6.

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Jan E Kamler (photo) received his B.S. in biology from the Uni- versity of Kansas and his M.S. in wildlife biology from Kansas State University. He currently is a doctoral candidate in the Department of Range, Wildlife, and Fisheries Management at Texas Tech University. His research interests include the ecology and interactions of carnivores and predator-prey relationships. Warren B. Ballard received his B.S. in fish and wildlife management from New Mexico State University, his M.S. in environmental biology from Kansas State University, and his Ph.D. in wildlife science from the University of Arizona. He currently is associate professor in the Department of Range, Wildlife, and Fisheries Management at Texas Tech University. His professional interests focus on predator-prey relationships and population dynamics of carnivores and ungulates.

Special editor: Krausman hd

Documents

A review of native and nonnative red foxes in North America