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BEHA GENETIC CHARACTERISTICS OF RED FOXES IN NORTHEASTERN OREGON BALD GREGORY AGREEN Owl Ridge NRC, 22116 45th Avenue SE, Bothell, WA 98021 USA; [email protected]

CA BENJAMIN NSACKS Mammalian Ecology and Conservation Unit, 248 CCAH, Veterinary Genetics Laboratory, University of FIRST California Davis, One Shields Avenue, Davis, CA 95618 USA RA LEONARD JERICKSON Oregon Department of Fish and Wildlife, 107 20th Street, La Grande, OR 97850 USA

RAPT KEITH BAUBRY US Forest Service, Pacific Northwest Research Station, 3625 93rd Avenue SW, Olympia, WA 98512 USA

NORTHWESTERN NATURALIST 98:73–81 AUTUMN 2017

GENETIC CHARACTERISTICS OF RED FOXES IN NORTHEASTERN OREGON

GREGORY AGREEN Owl Ridge NRC, 22116 45th Avenue SE, Bothell, WA 98021 USA; [email protected]

BENJAMIN NSACKS Mammalian Ecology and Conservation Unit, 248 CCAH, Veterinary Genetics Laboratory, University of California Davis, One Shields Avenue, Davis, CA 95618 USA

LEONARD JERICKSON Oregon Department of Fish and Wildlife, 107 20th Street, La Grande, OR 97850 USA

KEITH BAUBRY US Forest Service, Pacific Northwest Research Station, 3625 93rd Avenue SW, Olympia, WA 98512 USA

ABSTRACT—The Rocky Mountain Red Fox (Vulpes vulpes macroura), once common in the Blue Mountains ecoregion of northeastern Oregon, was considered rare in eastern Oregon by the 1930s and thought to be extirpated by the 1960s, when putatively new Red Fox populations began to appear. Although the new foxes were long presumed to be nonnative (originating from fur-farms or deliberate release), they were often phenotypically similar to native Red Foxes, suggesting the alternative possibility that they arose from range expansions, either by small numbers of remnant native foxes at higher elevations or by Rocky Mountain Red Foxes to the east. In this study, we used mitochondrial DNA to investigate the origins of extant Red Fox populations in northeastern Oregon. Our findings show that both native and nonnative sources contributed to the Red Fox populations currently occupying this region. In particular, Red Foxes in montane habitats of their former range in northeastern Oregon reflect predominantly native ancestry, whereas those in more lowland habitats outside the boundaries of their former range represent a mix of native and nonnative ancestry. Recognizing the existence of foxes with native ancestry in northeastern Oregon may shape management decisions regarding this species, especially in respect to control versus conservation.

Key words: cytochrome b, D-loop, haplotype, mitochondrial DNA, northeastern Oregon, recolonization, Rocky Mountain Red Fox, Vulpes vulpes macroura

Since European colonization, Red Fox (Vulpes generations of captive breeding and selection, vulpes) populations in North America have were derived primarily from a small number of expanded both from habitat alteration (Lloyd wild-caught individuals from southeastern Can- 1980; Nowak 1991) and anthropogenic translo- ada and Alaska (Statham and others 2012). From cations (Long 2003). Farmland development has a conservation standpoint, Red Foxes that created open-field habitats favored by this originated from translocations represent inva- species, while foxes have been translocated sive nonnative species that could threaten the across the continent either for sport (hound genetic integrity of native conspecifics through hunting) or to bolster fur trapping (Wilcomb hybridization (Krueger and May 1991) or com- 1948; Mace 1970; Aubry 1984). New Red Fox petition (MacDonald and others 1989; Simberloff populations have also been established by fur- 1997; Lockwood and others 2007). However, all farm escapees (Ashbrook 1923; Witmer and wild Red Fox populations exhibit variable Lewis 2001). Fur-farm foxes, which reflect many morphological characteristics, both between

73 74 NORTHWESTERN NATURALIST 98(2) and within standard color-phases (red, cross, publication, native foxes had disappeared from and silver); consequently, distinguishing native Oregon, and that the ‘‘foxes today are descen- from nonnative Red Foxes based on coat color is dants of eastern stock transplanted in the Will- very difficult, although subtle differences in red- amette Valley’’. Although Wilcomb (1948) did phase pelage color between the groups do occur describe several instances of nonnative fox (Bailey 1936). Conservation efforts to control translocations into the Willamette Valley be- nonnative Red Foxes might have led to the tween 1900 and 1924, which is likely the basis for unintentional removal of native foxes, which is Mace’s conclusions, Verts and Carraway (1998) of special concern where the native fox may be could find no evidence to support Mace’s naturally rare or endangered. Thus, understand- contention that the original foxes were extirpat- ing the genetic affinities and origins of Red Fox ed state-wide. populations in northeastern Oregon will be Mace (1970) also identified (on a range map) essential for the conservation and recovery of small pockets of presumably nonnative Red Fox native foxes in this region. occurrence in northeastern Oregon, especially in In western North America, native foxes the irrigated farmland of northern Malheur generally inhabit mountainous regions, where County on the Oregon-Idaho border. These foxes habitat conditions at high elevations are believed first appeared in fur-harvest records from to closely parallel the colder environmental Oregon in 1964, and by the late 1980s .100 conditions that existed in the southern refugium foxes were being harvested annually (Verts and during the last glacial maximum where the Carraway 1998). Because Red Foxes in the mountain foxes evolved (Aubry and others Willamette Valley would have to travel approx- 2009). Three montane subspecies are currently imately 150 km to get across the Cascade Range, recognized: the Rocky Mountain (V. v. macroura), and then cross approximately 350 km of very Sierra Nevada (V. v. necator), and Cascade (V. v. dry and largely unforested habitat to reach the cascadensis) Red Foxes (Aubry 1983; Perrine and Blue Mountains, they were an unlikely source others 2007). Mountain Red Foxes tend to be for these new populations. rare. The northern Malheur County irrigated farm- The Rocky Mountain Red Fox is native to the ing district is the Oregon extension of an Blue Mountains ecoregion of northeastern Ore- expansive Snake River Plains farming area that gon and southwestern Washington (Bailey 1936). bisects southern Idaho. Red Foxes began ap- Between 1825 and 1857, 1597 Red Fox pelts were pearing in the Idaho portion of the Snake River traded at Fort Nez Perce, located on the Walla Plain about 1960 (Fichter and Williams 1967). Walla River (Cowan 1938). Based on trade The lack of previous records from these low- patterns, Cowan (1938) and Stern (1993) con- elevation (700 to 1600 m) farming areas, coupled cluded that the majority of these foxes would with known occurrences of fox-fur farms in the have come from the general vicinity of the fort, region (Fichter and Williams 1967), suggested which in this case would likely have been the that nonnative Red Foxes became established in Blue Mountains of northeastern Oregon and southern Idaho in the early 1960s, eventually southeastern Washington. In 1914, Dice (1919) progressing downriver to Oregon by the late investigated the fauna of southeastern Washing- 1960s (the 1st record was in 1967) and early ton and reported that Red Fox were ‘‘commonly 1970s. However, Fichter and Williams (1967) found on the ridges of the Blue Mountains’’.By described a fox with red-phase pelage charac- the 1930s, however, 2 decades of intensive fox teristics more similar to native mountain foxes trapping during an inflated fur market (Bailey (yellow, buff, or tawny), and as a result 1936), along with the intensive predator-reduc- tentatively classified these foxes as V. v. macro- tion programs initiated by the Bureau of ura, with possible admixture with fur-farm Biological Survey (DeCalesta 1976), had greatly escapees. reduced their number, although Bailey (1936) Red Foxes began appearing elsewhere in stated ‘‘their extermination. . .has not been ac- northeastern Oregon in the mid-1990s (Verts complished’’. No Red Foxes were reported in and Carraway 1998), and by 2010 populations harvest records from southeastern Washington were well established in 8 counties (and in between 1938 and 1980 (Aubry 1984), and Mace adjacent Walla Walla County, Washington), (1970) concluded that by the date of his including the original mountainous range de- AUTUMN 2017 GREEN AND OTHERS:GENETIC CHARACTERISTICS OF RED FOXES 75 scribed by Bailey (1936) as well as farmlands in the hypothesis that Red Foxes were largely both the Snake River Plain and Columbia River native: (1) haplotypes are all or mostly native; Plateau. and (2) multiple native haplotypes occur in the The possible origins of extant Red Fox population. populations in northeastern Oregon include expansion by foxes in the Snake River Plain into METHODS similar farmland habitat in northeastern Oregon, Study Area fox-farm escapees (including a known release of foxes from a fur farm near Hermiston in 1987; M The northeastern portion of Oregon where Kirsch, Oregon Department of Fish and Wildlife, genetic samples were collected included 3 pers. comm.), down-slope expansion by mem- ecoregions: the Blue Mountains, Columbia Pla- bers of a small, persistent native population in teau, and Snake River Plain (USEPA 2003; Fig. the Wallowa Mountains, immigration from 1). The Blue Mountains ecoregion includes the native populations in the mountains of central Blue, Wallowa, and Ochoco Mountains, with Idaho, or some combination of the above. elevations in mountainous areas ranging from Because fur-farm releases had been documented 2100 to 2900 m, and in basin areas ranging from in northeastern Oregon, and Red Foxes currently 750 to 900 m (Franklin and Dyrness 1973). occupy lowland portions of that region they did Forested areas are dominated by Ponderosa Pine not occupy historically, the Oregon Department (Pinus ponderosa) and Douglas-fir (Pseudotsuga of Fish and Wildlife concluded that all Red Foxes menziesii), with Western Juniper (Juniperus occi- in that area had nonnative origins and repre- dentalis) at lower elevations and Western Larch sented an invasive species (ODFW 2006). How- (Larix occidentalis), spruce (Picea spp.), and fir ever, red-phase foxes examined near La Grande (Abies spp.) at higher elevations (Clarke and in 2011 were of a tawny-yellowish color more Bryce 1997; Thorson and others 2003). The characteristic of mountain foxes (Bailey 1936) sediment-filled basins of the Blue Mountains than the reddish-yellow coloration of Eastern or include the Wallowa, Grande Ronde, and Baker Alaskan foxes, suggesting that native genotypes Valleys. The Wallowa and Grande Ronde Valleys may be present. Because management and are characterized by Bluebunch Wheatgrass conservation activities for native versus nonna- (Pseudoroegneria spicata) and fescue (Festuca tive wildlife in Oregon vary substantially, spp.) grasslands, while the Baker Valley is drier, determining the genetic affinities of Red Fox and more characterized by shrub-steppe domi- populations in northeastern Oregon is essential nated by Big Sagebrush (Artemisia tridentata; for ensuring that management objectives are Thorson and others 2003). Much of the basin appropriate for these populations. The mitochondrial DNA (mtDNA) of Red areas have been converted to irrigated cropland Foxes, which represents their maternal lineages, and pasture. has been extensively studied and catalogued The arid Columbia Plateau includes a large, throughout the world in both wild and captive sandy Pleistocene lake basin (Lake Condon) populations, providing the most convenient immediately adjacent to the Columbia River, starting point to understand population origins and a foothill region between the lake basin and (for example, Aubry and others 2009; Statham the Blue Mountains. The flat (100 to 200 m and others 2012, 2014). We therefore used elevation) lake basin is dominated by shrub- mtDNA analyses to investigate the genetic steppe including Big Sagebrush, rabbitbrush affinities of northeastern Oregon Red Fox pop- (Chrysothamnus spp.), Western Needle-and- ulations and test the hypotheses that these Thread (Stipa comata), and introduced Cheat- populations originated from fur farms or arose grass (Bromus tectorum; Clarke and Bryce 1997). from range expansions by nearby native popu- Much of this area has been converted to irrigated lations (such as Wallowa Mountains or Idaho). cropland to produce potatoes, onions, and Although a comprehensive understanding of alfalfa. The foothills region is dominated by Red Fox ancestry, allowing for admixture, will bunchgrasses (wheatgrass and fescue) with the ultimately require a more extensive sample and deeper-soiled areas converted to dryland wheat. nuclear genetic analyses, 2 clear predictions Much of the stream bottomland has been associated with mtDNA would strongly support converted to improved pasture and alfalfa fields. 76 NORTHWESTERN NATURALIST 98(2)

FIGURE 1. Location of the study area (red dashed line) and the 3 ecoregions (Columbia Plateau, Blue Mountains, Snake River Plain) within the study area. The original Rocky Mountain Red Fox range in northeastern Oregon as described by Bailey (1936) is shown in shaded hatch.

The Snake River Plain includes the Treasure Oregon in 2000. All hair and scat samples Valley, surrounded by alkaline foothills (Thorson collected in the field were fixed in 95% ethanol, and others 2003). Treasure Valley was formerly whereas most carcass samples were initially shrub-steppe, but an extensive network of frozen and later transferred to 95% ethanol irrigation canals has transformed the valley into before being sent to the University of California, irrigated pastureland and cropland. Crops in- Davis for analysis. clude wheat, sugar beets, potatoes, onions, and alfalfa. The adjacent rangeland foothills are Laboratory Analyses dominated by Big Sagebrush, Bluebunch Wheat- We conducted DNA extraction, polymerase grass, and Cheatgrass, and used primarily for chain reaction (PCR) amplification, sequencing, cattle grazing. and genotyping at the Mammalian Ecology and Conservation Unit in the Veterinary Genetics Genetic Field Data Collection Laboratory at the University of California, Genetic material was obtained from scats and Davis. DNA was extracted from tissue samples hair samples collected at den sites, and from hair using a DNeasy Blood and Tissue kit (Qiagen, and tissue collected from Red Fox carcasses CA), and from scats using a QIAmp DNA Stool (roadkills, predator management, fur harvest). kit (Qiagen, CA). DNA was extracted from hair All samples were collected between 2011 and samples by first digesting the follicles as 2013, plus 1 sample collected near Heppner, suggested by Pfeiffer and others (2004), followed AUTUMN 2017 GREEN AND OTHERS:GENETIC CHARACTERISTICS OF RED FOXES 77 by purification using a modified phenol-chloro- TABLE 1. Cytochrome b/D-loop haplotypes from form method (Sambrook and Russell 2001). Red Fox DNA samples collected in northeastern Primers, PCR chemistry, cycling conditions, Oregon (2000–2013). and sequencing for the mtDNA D-loop and Ecoregion Haplotype cytochrome b loci were as reported previously (Cytochrome Blue Columbia Snake (Perrine and others 2007; Aubry and others b/D-loop) Mountains Plateau River Plain Total 2009). A-19a 35 10 1 46 A-37a 3003 Data analysis A-43a 0202 A-82a 0011 Attributions of haplotypes as native were G-38b 2406 based on the analysis of historical museum Total 40 16 2 58 specimens from throughout the historical range a native b of the Red Fox in North America by Aubry and nonnative others (2009). In particular, cytochrome b haplo- types A, A3, A4, and A6 were found in the Dakota (Aubry and others 2009; Sacks and native range of the Rocky Mountains Red Fox. others 2010; Statham and others 2012). The attribution of nonnative Red Fox haplotypes The remaining 6 samples were haplotype G- were based both on samples directly from fur 38, a common fur-farm haplotype with an farms and nonnative populations derived from Alaskan or north-Canadian origin (for example, fur farms (Statham and others 2012; Sacks and Sacks and others 2011; Statham and others 2012). others 2016). In particular, the most prevalent Four of these nonnative samples were obtained nonnative haplotypes were G and N, ultimately at relatively low elevations (,775 m) in the from Alaska, as well as E and F, derived from Columbia Plateau, and likely originated from a southeastern Canada. To better assess minimum 1987 fur-farm release near Stanfield, Oregon (M numbers of independent native matrilines, we Kirsch, Oregon Department of Fish and Wildlife, combined the cytochrome b and D-loop frag- pers. comm.). The presence of both cytochrome b ments into a single concatenated haplotype, haplotype A and G within the same general which we denoted as X-Y, where X represents vicinity in the Columbia Plateau also suggests the cytochrome b fragment and Y represents the mixed ancestry involving both native and D-loop fragment; the concatenated haplotypes nonnative populations. The remaining 2 nonna- provided greater resolution than the cytochrome tive haplotypes were found in the Blue Moun- b fragment alone, enabling us to infer indepen- tains; 1 fox with haplotype G-38 was captured at dent native and nonnative matrilines (for exam- approximately 1250 m elevation upslope from ple, Sacks and others 2010, 2016). Walla Walla, and the other was sampled near Baker City, Oregon, at 1120 m elevation. Inter- estingly, both samples collected in the Snake RESULTS River Plain ecoregion near Ontario, Oregon, Of the 58 samples from which Red Fox were native haplotypes (A-19 and A-82) at mtDNA was successfully extracted, 46 (79%) elevations of only 680 and 720 m. were of the cytochrome b/D-loop haplotype Within the Blue Mountains ecoregion, 95% combination A-19 (Table 1), the most common (38/40) of the foxes we sampled had native haplotype in native populations from the Rocky haplotypes, whereas in lowland ecoregions Mountains, Sierra Nevada, and the Cascade (Columbia Plateau and Snake River Plain), 14/ Range of Oregon (Aubry and others 2009). Other 18 (78%) samples contained native haplotypes native haplotypes that we detected included A- (Table 1, Fig. 1). Over 97% (38/39) of the fox 37 (n ¼ 3), A-43 (n ¼ 2), and A-82 (n ¼ 1; Table 1). samples we collected within the original range To date, haplotypes A-43 and A-82 have been described by Bailey (1936; Fig. 2) exhibited found only in Rocky Mountain Red Fox popu- native haplotypes, whereas 78% (14/18) of the lations (Aubry and others 2009; Sacks and others samples collected within the Columbia Plateau 2010; Statham and others 2012), and A-37 is a and Snake River Plains ecoregions, which are relatively rare haplotype that was found previ- both outside the range of Red Foxes described ously in the Rocky Mountains and central South by Bailey (1936), contained native haplotypes. 78 NORTHWESTERN NATURALIST 98(2)

FIGURE 2. Locations where Red Fox genetic samples were collected based on cytochrome b haplotypes. Blue- filled circles indicate haplotype A samples (native) and red-filled diamonds indicate haplotype G samples (nonnative). The pie charts show the distribution of native and nonnative haplotypes for each ecoregion (see Table 1). The shaded hatch represents the original Rocky Mountain Red Fox range as described by Bailey (1936).

DISCUSSION distribution of our samples suggests that both scenarios are possible. Three foxes (all haplotype Our results suggest that extant Red Foxes A-19) that were trapped at .1100 m elevation within the original range in northeastern Oregon near the mouth of the Lostine River in Wallowa described by Bailey (1936) can be generally County could represent animals that originated characterized as native Rocky Mountain Red in the Wallowa Valley, but could also be high- Foxes reestablishing their former range. Al- elevation foxes that migrated downslope for the though mtDNA analysis does not measure the winter (although downslope migration of mon- level of genetic diversity within an individual (a tane foxes has not been firmly established . fox that is genetically 90% nonnative can still anywhere). carry a native haplotype), the fact that over 97% The presence of both native (A) and nonnative of the foxes within the original range exhibited a (G) cytochrome b haplotypes in close proximity native haplotype is compelling. Further, 90% to each other in the lower-elevation Columbia (35/39) of the samples collected within Bailey’s Plateau (Umatilla and Morrow counties) suggest original range were haplotype A-19, which Sacks mixed ancestry in that region. The presence of and others (2010) also found in a museum nonnative foxes on the Columbia Plateau is not specimen collected in 1924 from the Wallowa surprising, given the 1987 release of foxes from a Mountains. fur farm in Umatilla County and the increase in It is unclear from this analysis whether these Red Fox reports soon afterward. However, the foxes originated from native populations in high prevalence of native haplotypes on the Idaho, perhaps dispersing into Oregon via the Columbia Plateau was not expected, given that Snake River Plain, or a remnant population Rocky Mountain Red Foxes and other mountain persisting in the higher elevations of the Wallo- fox subspecies typically occur at much higher wa Mountains (Magoun and others 2013). The elevations. Aubry (1984) suggested that physio- AUTUMN 2017 GREEN AND OTHERS:GENETIC CHARACTERISTICS OF RED FOXES 79 logical and behavioral limitations may restrict questions that must be investigated before clear montane Red Foxes to higher elevations, and management actions can be recommended. In non-native Red Foxes to the lowlands. However, the aggregate, the occurrence of nonnative Fichter and Williams (1967) speculated that mtDNA haplotypes documented in the present downslope movements by Rocky Mountain study clearly indicates the presence of some Red Foxes may explain the expansion of Red nonnative ancestry in these populations. How- Foxes into the Snake River Plain during the ever, these data provide no direct information on 1960s, and Statham and others (2012) suggested the quantity of nonnative nuclear genetic ad- that native Red Foxes in the Willamette Valley of mixture. Moreover, an individual fox carrying a western Oregon may have originated from nonnative mtDNA haplotype cannot be as- downslope movements by mountain foxes oc- sumed to be ‘‘nonnative’’ on that basis alone. cupying high-elevation habitats in the Cascade For example, if a product of multiple generations Range. Statham and others (2012) noted, how- of backcrossing, an individual could reflect ever, that their findings do not exclude the .99% native genes and still carry a nonnative possibility that the presence of native Red Fox mtDNA haplotype (for example, Sacks and haplotypes in the Willamette Valley was human- others 2011). We are currently using nuclear mediated in one way or another, and the same is genetic markers to investigate the potential for true of our results in lowland ecoregions that genetic exchange between high-elevation Wallo- were outside the range of Rocky Mountain Red wa Mountain fox populations and those inhab- Foxes historically. iting the Wallowa, Grande Ronde, and Baker If native Red Foxes occupied these lowland Valleys to gain a better understanding of the areas naturally, it may be that new opportuni- ties for expanding their range into previously extent of nonnative introgression into native unoccupied low-elevation habitats were created populations. Ultimately, these and additional by the extensive ecological changes that oc- nuclear genetic results will be necessary to assess curred on the Columbia Plateau and Snake the potential threat of nonnative introgression. River Plain during the past 100 y. Large-scale Moreover, although a cross-sectional under- irrigation projects on the Columbia Plateau and standing of nuclear admixture is essential in Snake River Plain, beginning with the Recla- quantifying the magnitude of introgression to mation Enabling Act of 1905, resulted in the date, continued genetic monitoring will be conversion of hundreds of thousands of acres of necessary to determine the risk of eventual shrub-steppe, a habitat largely avoided by genetic swamping versus, for example, a limited native Red Foxes (Bailey 1936), to irrigated pulse or zone of introgression. pasture and cropland (especially alfalfa hay- fields) that now provide improved habitat for ACKNOWLEDGMENTS Red Fox prey (Bailey 1931, 1936; Grinnell and We would like to thank the following people for others 1937; Aubry 1983, 1984; Perrine 2005) assisting in collecting DNA samples: E Miguez, T such as Belding’s Ground Squirrels (Urocitellus Reynolds, J Akenson, S Rhea, G Ward, M Kirsch, H beldingi), Yellow-bellied Marmots (Marmota fla- Hayden, E Crain, M Hanson, K Mitchell, C Nowak, H viventris), Montane Voles (Microtus montanus), Petty, H Reynolds, R Torland, M Henderson, and W and Northern Pocket Gophers (Thomomys tal- Van Dyke. R Anderson, B Gibson, S Cherry, V Coggins, poides), all of which can reach pest levels M Henjum, G Ward, D Kerley, H Bryant, and J Akins (Dalquest 1948; Sullins and Verts 1978; Thomp- provided historical perspective on the recent expansion son 1979; Verts and Carraway 1998). These of Red Foxes in northeastern Oregon, or assisted our pastures and croplands may provide suitable understanding of mountain Red Foxes in general. We greatly appreciate the project support and manuscript surrogates for the mountain-meadow habitats reviews provided by T Hiller, J Perrine, and R Morgan. in which native Red Foxes typically forage We thank M Statham and Z Lounsberry for (Bailey 1931, 1936; Grinnell and others 1937; supervising and training the following interns, who Aubry 1983, 1984). assisted with laboratory procedures: M Holtz, N Our findings provide a 1st pass at essential Goddard, S Aamoth, and T Kalani. M Repaci baseline information for the management and prepared the graphics. The project was generously conservation of Red Foxes in northeastern supported by the Oregon Department of Fish and Oregon, but also raise many new research Wildlife, Owl Ridge NRC, and Oregon Wildlife. 80 NORTHWESTERN NATURALIST 98(2)

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