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CFR Citation: 50 CFR Part 17

RIN ID: RIN 1018-AI28

NOTICE: RULES

ACTION: Endangered and threatened species:

DOCUMENT ACTION: Final rule.

SUBJECT CATEGORY: Endangered and Threatened Wildlife and Plants; Listing the San Miguel Island Fox, Santa Rosa Island Fox, Santa Cruz Island Fox, and Santa Catalina Island Fox as Endangered

DATES: This final rule is effective April 5, 2004.

DOCUMENT SUMMARY: We, the U.S. Fish and Wildlife Service (Service), determine endangered status pursuant to the Endangered Species Act (Act) of 1973, as amended (16 U.S.C. 1531 et seq.), for four subspecies of island fox (Urocyon littoralis): San Miguel Island fox (U. l. littoralis), Santa Rosa Island fox (U. l. santarosae), Santa Cruz Island fox (U. l. santacruzae), and Santa Catalina Island fox (U. l. catalinae). This final rule extends the Federal protection and recovery provisions of the Act to these subspecies.

SUMMARY: San Miguel Island fox et al.,

SUPPLEMENTAL INFORMATION

The island fox was first described as Vulpes littoralis by Baird in 1857 from the type locality of San Miguel Island, Santa Barbara County, California. Merriam (1888, in Hall and Kelson 1959) reclassified the island fox into the genus Urocyon and later described island foxes from Santa Catalina, San Clemente, and Santa Cruz Islands as three separate taxa (U. catalinae, U. clementae, and U. littoralis santacruzae) (Merriam 1903). Grinnell et al. (1937) revised Merriam's
classification, placing foxes from all islands under the species U. littoralis and assigning each island population a subspecific designation (U. l. catalinae on Santa Catalina Island, U. l. clementae on San Clemente Island, U. l. dickeyi on San Nicolas Island, U. l. littoralis on San Miguel Island, U. l. santacruzae on Santa Cruz Island, and U. l. santarosae on Santa Rosa Island). Recent morphological and genetic studies support the division of the U. littoralis complex into six subspecies that are each limited in range to a single island (Gilbert et al. 1990; Wayne et al. 1991; Collins 1991a, 1993; Goldstein et al. 1999). Each subspecies is reproductively isolated from the others by a minimum of 5 kilometers (3 miles) of ocean waters. The island fox is closely related to the mainland gray fox, U. cinereoargenteus, but is smaller in size and darker in coloration (Moore and Collins 1995).

The island fox is a very small canid, weighing approximately 3 to 6 pounds (1.4 to 2.7 kilograms) and standing approximately 1 foot (0.3 meter) tall. The tail is conspicuously short. Dorsal coloration is grayishwhite and black. The base of the ears and sides of the neck and limbs are cinnamonrufous in color, and the underbelly is a dull white. Island foxes display sexual size dimorphism (males being larger and heavier than females) (Moore and Collins 1995).

Island foxes inhabit the six largest islands (San Miguel, Santa Rosa, Santa Cruz, San Nicolas, Santa Catalina, and San Clemente Islands) off the coast of southern California. Genetic evidence suggests that all island foxes are descended from one colonization event (Gilbert et al. 1990), possibly from chance overwater dispersal during which foxes rafted on floating debris (Moore and Collins 1995). Fossil evidence indicates that island foxes inhabited the northern Channel Islands (San Miguel, Santa Rosa, and Santa Cruz) between 10,000 to 16,000 years ago (Orr 1968). However, island foxes are thought to have existed on the northern Channel Islands even before that time, during a period when Santa Cruz, Santa Rosa, and San Miguel were one land mass referred to as ``Santarosae,'' last known to have been united 18,000 years ago (Johnson 1978, 1983). The island fox was thought to have reached the southern Channel Islands (San Nicolas, San Clemente, and Santa Catalina) much more recently (2,200 to 3,800 years ago), most likely introduced to these islands by Native Americans as pets or semidomesticates (Collins 1991a, b). However, island fox remains recently recovered from San Nicolas Island suggest this introduction [[Page 10336]]
was earlier, approximately 5,200 years ago (Vellanoweth 1998).

Genetic evidence confirms the pattern of dispersal suggested by archeological and geological findings (Gilbert et al. 1990). The pattern of genetic relatedness supports the geological evidence of the sequence of isolation for each island, and each population, as rising sea levels separated Santarosae into the northern Channel Islands. Santa Cruz separated from the other northern Channel Islands first, about 11,500 years ago, followed by the separation of San Miguel and Santa Rosa about 9,500 years ago. Together with the fossil record, genetic evidence indicates that San Clemente was the first southern Channel Island colonized, probably by immigrants from San Miguel. Dispersal then occurred from San Clemente to San Nicolas and then Santa Catalina (Gilbert et al. 1990).

Island forms of species generally have less genetic variability than their mainland counterparts (Gill 1980), and island foxes are no exception. Mainland gray foxes are more variable both morphologically and genetically than island foxes (Wayne et al. 1991; Goldstein et al. 1999). The smaller the island size the lower the island fox population size and genetic variability seems to be. The smallest island fox populations, San Miguel and San Nicolas, show the least genetic variability, with San Nicolas having virtually no genetic variability, which is highly unusual among mammal populations. This lack of variability likely occurred as a result of a past population bottleneck (Gilbert et al. 1990; Goldstein et al. 1999); such a bottleneck occurred on San Nicolas Island in the mid1970s (Laughrin 1980).

The diminutive island fox is the largest native carnivore on the Channel Islands. The island fox is a habitat generalist, occurring in valley and foothill grasslands, southern coastal dunes, coastal bluff, coastal sage scrub, maritime cactus scrub, island chaparral, southern coastal oak woodland, southern riparian woodland, Bishop (Pinus muricata) and Torrey pine (Pinus torreyana) forests, and coastal marsh habitats. Although foxes can be found in a wide variety of habitats on the islands, they prefer areas of diverse topography and vegetation (Von Bloeker 1967; Laughrin 1977; Moore and Collins 1995). Laughrin (1973, 1980) found woodland habitats to support higher densities of island foxes due to increased food availability, while Crooks and Van Vuren (1995) found island foxes to prefer fennel grasslands and avoid ravines and scrub oak (Quercus spp.) patches.

Island foxes are omnivores, taking a wide variety of seasonally available plants and animals (Collins and Laughrin 1979; Collins 1980; Kovach and Dow 1981; Moore and Collins 1995; Crowell 2001). Island foxes forage opportunistically on any food items encountered within their home range. Diet is determined largely by availability, which varies by habitat and island, as well on a seasonal and annual basis. Island foxes prey on native deer mice (Peromyscus maniculatus) and harvest mice (Reithrodontomys megalotis catalinae), as well as on introduced house mice (Mus musculus) and rats (Rattus rattus and R. norvegicus). Small mammals may be especially important prey during the breeding season, because they are large, energyrich food items that adult foxes can bring back to their growing pups (Garcelon et al. 1999). In addition to small mammals, island foxes feed on ground nesting birds such as horned larks (Eremophila alpestris), Catalina quail (Callipepla californica catalinensis), and western meadowlarks (Sturnella neglecta), and a wide variety of insect prey (Moore and Collins 1995). At certain times of the year, foxes feed heavily on orthopterans (e.g., grasshoppers and crickets) (Crooks and VanVuren 1995), especially Jerusalem crickets (Stenopelmatus fuscus). Less common in the diet are amphibians, reptiles, and carrion of marine mammals (Collins and Laughrin 1979). Island foxes feed on a wide variety of native plants, including the fruits of manzanita (Arctostaphylos spp.), summer holly (Comarostaphylis spp.), toyon (Heteromeles arbutifolia), cactus (Opuntia spp.), island cherry (Prunus ilicifolia), sumac (Rhus spp.), rose (Rosa spp.), nightshade (Solanum spp.), and huckleberry (Vaccinium spp.) (Moore and Collins 1995). Fruiting shrubs do not occur on San Miguel Island, where island foxes rely more on the fruits of the lowgrowing seafig, Carpobrotus chilensis.

The island fox is a docile canid, exhibiting little fear of humans in many instances. Although primarily nocturnal, the island fox is more diurnal than the mainland gray fox (Collins and Laughrin 1979; Fausett 1993). Their more diurnal activity is thought to be a result of both the historical absence of large predators and freedom from human harassment on the islands (Laughrin 1977).

Mated island foxes maintain territories that are separate from the territories of other pairs (Crooks and Van Vuren 1996; Roemer et al. 2001a). Island fox home range size varies with sex, season, population density, landscape features, and habitat type (Laughrin 1977; Crooks and Van Vuren 1996; Thompson et al. 1998; Roemer et al. 2001a). Estimates of territory size range from 59 acres (ac) (24 hectares (ha)) in mixed habitat (Crooks and Van Vuren 1996) and 214 ac (87 ha) in grassland habitat (Roemer 1999) on Santa Cruz Island, to 190 ac (77 ha) in canyons on San Clemente Island (Thompson et al. 1998). Island fox territory configuration changes after the death and replacement of paired male foxes, but not after the death and replacement of paired females or juveniles, indicating that adult males are involved in territory formation and maintenance (Roemer et al. 2001a).

Although island foxes appear monogamous, copulations with individuals other than the mate are common and often result in offspring. Courtship activities occur from late January to early March; genetic evidence suggests that inbreeding avoidance occurs (Roemer et al. 2001a). Recent endocrine assays on fecal samples from San Miguel Island indicate that, unlike all other canids studied to date, island foxes are induced rather than spontaneous ovulators (Bauman et al. 2001), which means that female island foxes do not enter estrous unless males are present. Young are born from late April through May after a gestation period of approximately 50 days. Island foxes give birth to their young in simple dens, which are usually not excavated by the foxes themselves (Moore and Collins 1995). Rather, any available sheltered site (e.g., brush pile, rock crevice, or hollow stump) is used (Laughrin 1977). Litter size ranges from one to five pups (Moore and Collins 1995). Laughrin (1977) found an average litter of 2.17 for 24 dens on Santa Cruz Island; this estimate likely reflected the number of pups weaned rather than born. The average size of 35 litters born in captivity since 1999 is 2.3 (Coonan et al. in prep.). Both island fox parents care for the young (Garcelon et al. 1999). By 2 months of age, young foxes spend most of the day outside the den and will remain with their parents throughout the summer. Some pups disperse from their birth territories by winter, although others may stay on their natal territories into their second year (Coonan 2003a). Island foxes can mate at the end of their first year (Collins and Laughrin 1979), although most breeding involves older animals. Coonan et al. (1998) found that only 16 percent of females under the age of 2 bred over a 5 year period, in contrast to 60 percent of older females.

Due to the low reproductive output of island foxes, survival of adults is the
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most important factor influencing population growth rate (Roemer 1999; Roemer et al. 2001b, d). Compared with the gray fox, island fox populations are skewed toward older adults (Laughrin 1980; Garcelon 1988). Adult island foxes live an average of 4 to 6 years (Moore and Collins 1995), although this may be an underestimate (Coonan et al. 1998). Island foxes may live 8 to 10 years in captivity or in the wild in the absence of catastrophic mortality forces (Tim Coonan, National Park Service, in litt. 2002).

In the 1970s, island foxes were found at higher densities than any other canid species, likely due to the lack of competition and predation compared with the island foxes' mainland canid counterparts (Laughrin 1980). At the time of Laughrin's early studies, island fox populations were stable on all islands except Santa Catalina (Laughrin 1973). Predecline trapping on Santa Cruz Island in 1993 and 1994 reconfirmed that island foxes existed at high densities, with an average of 21.3 foxes per mi\2\ (8.2 foxes per km\2\) in 1994 (Roemer et al. 1994).

San Miguel, Santa Rosa, Santa Cruz, and Santa Catalina island foxes have experienced precipitous declines in the last 8 years (Coonan et al. 1998, 2000; Roemer 1999; Timm et al. 2000; Roemer et al. 2001b). The island fox population on San Nicolas Island has remained stable and the population on San Clemente appears to have experienced a gradual decline. Total island fox numbers rangewide have fallen from approximately 6,000 individuals in 1994 (Roemer et al. 1994) to fewer than 1,660 individuals in 2003 (Coonan 2003b). By 2001, island fox populations on San Miguel and Santa Cruz Islands had declined by an estimated 80 to 90 percent and were found to have a 50 percent chance of extinction over the next 5 to 10 years (Roemer 1999; Roemer et al. 2001b). During the period of decline, island fox population monitoring was not conducted on Santa Rosa Island; however, anecdotal observations and recent trapping efforts showed that a similar decline occurred for this subspecies as well (Roemer 1999; Coonan 2003a). Island fox populations on the northern Channel Islands are considered critically endangered and in need of immediate conservation action (Coonan et al. 1998; Roemer 1999; Roemer et al. 2001c). On Santa Catalina, island fox populations all but disappeared from the larger eastern portion of the island. This decline is attributed to a canine distemper outbreak that swept through the population in 1999 (Timm et al. 2000).

San Clemente and San Nicolas Islands have island fox populations estimated at approximately 595 and 614 individuals, respectively (D. Garcelon, unpublished data; Schmidt and Garcelon 2003). San Clemente Island has not experienced the sharp declines seen on other islands; however, 13 years of trapping data indicate that island fox densities have slowly declined since the early 1990s (Garcelon 1999; D. Garcelon, unpublished data). Populations of the San Nicolas Island fox appear to be stable. However, its small population size (Roemer et al. 1994), insular nature, lack of resistance to canine distemper and other diseases (Garcelon et al. 1992), high densities (Schmidt and Garcelon 2003), and low genetic variability (Wayne et al. 1991) increase the vulnerability of this subspecies (Roemer 1999). Protective measures have been put in place on these islands, such as reducing speed limits, educating island inhabitants and visitors, implementing a wildfire management plan, managing feral cat populations, administering canine distemper vaccinations, and removing all feral ungulates, to prevent further decline of these two subspecies. The statuses of these subspecies are discussed further in Issue 16 under our responses to public comments.

San Miguel Island Fox (Urocyon littoralis littoralis)

San Miguel Island is owned by the Department of the Navy but is managed by the National Park Service as part of the Channel Islands National Park through a series of memoranda of understanding between these agencies. The first quantitative surveys for island foxes on San Miguel Island were conducted by Laughrin in the early 1970s (Laughrin 1973). Trap efficiency was high (43 percent), and Laughrin concluded that island fox populations were stable at 7 foxes per square mile (mi\2\) (2.7 foxes per square kilometer (km\2\)), although this may be an underestimate. In the late 1970s, the island foxes on San Miguel had an average density of 12 foxes per mi\2\ (4.6 foxes per km\2\), for a total estimated population of 151 to 498 individuals (Collins and Laughrin 1979). Island foxes on San Miguel Island were not surveyed again until 1993, when the NPS instituted a longterm population study, which recorded an average density of 20 foxes per mi\2\ (7.7 foxes per km\2\) on two trapping grids and estimated the total population at more than 300 foxes (Roemer et al. 1994; Coonan et al. 1998). A third trapping grid was added the following year, and yielded island fox densities higher than previously recorded (41 foxes per mi\2\ (15.8 foxes per km\2\) in one study area), resulting in an islandwide estimate of 450 adults (Coonan et al. 1998). Annual
populationmonitoring using capturemarkrecapture techniques documented a substantial decline in island fox populations on San Miguel Island between 1994 and 1999 (Coonan et al. 1998; Coonan et al. in review). During this time period, island fox populations dropped from an estimated 450 adults in 1994 (Coonan et al. 1998) to 15 foxes in 1999 (T. Coonan, unpublished data) as a result of predation by golden eagles.

In 1999, NPS captured 14 (4 males and 10 females) of the 15 remaining foxes from San Miguel Island to protect the subspecies from further losses from predation by golden eagles and to initiate a captive propagation program. The remaining island fox, a lone female, evaded capture efforts until September 2003, when she was captured and brought into captivity. Four years' captive breeding has increased the captive San Miguel Island fox population to 38 individuals.

Island foxes held in captivity are likely to be exposed to increased parasite loads due to artificial densities and unnaturally low mobility. On San Miguel Island, captive island foxes have been found to have high parasite loads of Angiocaulus spp., Spirocerca spp., and Uncinaria spp. (L. Munson, unpublished data; Sharon Patton, University of Tennessee, pers. comm. 2003). These parasites, thought to have had minor effects on the population in the past (see Coonan et al., in review), may have significant effects on individual fox health due to the facilitation of their spread and density by the captive breeding situation. For example, fox handlers have reported high incidence of rectal bleeding in the captive San Miguel population, likely due to Uncinaria (a type of hookworm). Hookworms feed on the inner lining of the small intestine and cause loss of blood or hemorrhaging to the host, sometimes to the point of severe anemia and death. The NPS is working to address this threat by developing a treatment process for hookworm in coordination with the veterinary team of the Island Fox Conservation Working Group. Captive breeding programs to facilitate recovery are planned to continue for these four island fox subspecies. Therefore, exposure to increased parasitic loads will continue to be a threat.

Until September 2001, all captive San Miguel Island foxes were held in one breeding facility, putting the subspecies in danger of extinction due to a catastrophic event such as wildfire or
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disease outbreak. The NPS moved half the captive foxes into a second breeding facility on San Miguel Island in October 2001 to minimize this risk (Coonan and Rutz 2002).

Santa Rosa Island Fox (Urocyon littoralis santarosae)

Santa Rosa Island is owned and managed by the NPS. The earliest island fox trapping study from Santa Rosa reported a trapping efficiency of 50 percent and a density of 11 foxes per mi² (4.2 foxes per km²) (Laughrin 1973). Few population data have been collected on Santa Rosa Island foxes since Laughrin's studies. Although population monitoring was not conducted on Santa Rosa Island during the period of decline, trapping data collected in 1998 and 2000, as well as anecdotal evidence, suggested that Santa Rosa experienced a decline similar to those on Santa Cruz and San Miguel Islands (Roemer 1999; Roemer et al. 2001b). During 132 trap nights in 1998, trap success was 4.8 percent, and only 9 individuals were captured (Roemer 1999). Anecdotal sightings by park and ranch staff in the late 1990s became much less frequent than in previous years (Coonan 2003a).

Believing that fewer than 100 island foxes remained on Santa Rosa Island (T. Coonan, pers. comm. 1999), the NPS captured 14 adult foxes (5 males and 9 females) to initiate captive breeding in March 2000. The last known fox in the wild on Santa Rosa Island was brought into captivity in March 2001 (Coonan and Rutz 2002). Three years' captive breeding has increased the captive population to 56 (Coonan 2003b). As with San Miguel Island, approximately half the captive foxes were moved to a second facility in October 2001 (Coonan and Rutz 2002).

Deer (Odocoileus hemionus) and elk (Cervus elaphus) are present on Santa Rosa Island and assist in supporting breeding golden eagles, the main predator of island fox. Deer numbers in 2002 fluctuated between 424 and 686 deer (Schreiner et al. 2003), while approximately 601 elk remain on the island (Nathan Vail, in litt. 2003). Numbers of deer and elk are presently at their lowest numbers since the herds were established, as the result of a negotiated settlement agreement between the NPS and the commercial hunting operation managing the herds. The presence of these ungulates on the island likely facilitates the presence of golden eagles in two ways: (1) Deer fawns provide live prey for golden eagles as evidenced by prey remains found in nests (Coonan 2003a); and (2) carcasses of deer and elk from an annual hunt and subsequent cull provide golden eagles with a food source at a time of year where food resources are usually depleted. Through a settlement between the special use permittee and the NPS, deer and elk will be removed from the island by 2011, with populations slated for decrease beginning in 2008.

Santa Cruz Island Fox (Urocyon littoralis santacruzae)

The majority (75 percent) of Santa Cruz Island is owned by The Nature Conservancy, with the remaining 25 percent owned by NPS. Santa Cruz Island is the largest of the Channel Islands and has supported the highest known densities of island fox in the past (Laughrin 1973). Laughrin (1971) estimated the island fox population of Santa Cruz Island to be approximately 3,000 individuals. Average density between 1973 and 1977 was 20.4 foxes per mi² (7.9 foxes per km²) (Laughrin 1980). Following Laughrin's studies, island fox populations on Santa Cruz Island were not surveyed again until 1993, when the average density was 21.2 foxes per mi² (8.2 foxes per km²) (Roemer et al. 1994). Since that time, the population has decreased from an estimated 1,312 in 1993 to 133 individuals in 1999 (Roemer 1999; Roemer et al. 1994, 2001b). In 1998, trapping efficiency was low (2.9 percent), and island fox density ranged from 0.0 to 6.2 foxes per mi² (0.0 to 2.4 foxes per km²), the lowest ever reported from Santa Cruz Island (Roemer 1999).

Population monitoring efforts in 2001 yielded captures of 75 individual foxes. Of these, 27 were outfitted with radio collars. The highest numbers of foxes were captured in the areas of relatively high cover. Five of the 27 radiocollared foxes died during 2001; their deaths were attributed to predation by golden eagles (David Garcelon, Institute for Wildlife Studies, pers. comm. 2001a). The Island Fox Conservation Working Group, a team of experts convened by the NPS to recommend appropriate recovery actions for the island fox, found that ``the existence of one pair of golden eagles on the island as of October 1, 2001, will warrant bringing foxes into captivity as the necessary conservative step in preserving the Santa Cruz Island fox population (Coonan 2001).'' Intensive trapping efforts to capture and relocate the remaining golden eagles in the spring and summer of 2001 resulted in three captures; however, four eagles remained on the island (B. Latta, pers. comm. 2001). Thus, the NPS and The Nature Conservancy (TNC) initiated captive breeding of island foxes on Santa Cruz Island in early 2002 (Coonan and Rutz 2003).

During 2002, 18 island foxes on Santa Cruz Island were captured and brought into captivity. One of these foxes gave birth to 5 pups, 3 of which were released back into the wild, bringing the total captive population to 20 by December 2002 (Coonan and Rutz 2003). An additional 10 pups born in 2003 brought the total captive population to 30 individuals.

Islandwide transect trapping in 2002 revealed that a minimum of 68 foxes were alive in the wild on Santa Cruz Island (D. Garcelon, unpublished data). Additional island foxes are expected to be present on the island, but the total number of island foxes in the wild is likely fewer than 100 (Schmidt and Garcelon 2003). Since December 2000, the Institute for Wildlife Studies has radiotracked 53 individual foxes. Twenty of these foxes have died; 16 of the 20 mortalities were attributed to golden eagle predation based on physical evidence at the carcass recovery site (Institute for Wildlife Studies, unpublished data).

Annual survivorship of wild island foxes on Santa Cruz Island, as determined by ongoing radiotelemetry, was 61 percent in 2001 and 70 percent in 2002. Golden eagle trapping appears to have improved annual survivorship of island foxes, as the 2001 and 2002 survivorship is significantly higher than the 39 percent survivorship recorded during the island fox population decline. However, an island fox population model indicates that survivorship needs to be at least 80 percent in order for the populations to stabilize or increase (Roemer et al. in prep.).

Santa Cruz Island is currently occupied by a large feral pig (Sus scrofa) population (estimated at approximately 3,000 to 5,000 individuals), which facilitates the colonization of the island by golden eagles. TNC and the NPS are planning to begin an islandwide pig eradication program in spring 2004, which will take years to complete (NPS 2002).

Santa Catalina Island Fox (Urocyon littoralis catalinae)

Twelve percent of Catalina Island is in private ownership, while the remaining 88 percent is owned by the Catalina Island Conservancy. Santa Catalina Island has the largest human population, a large population of domestic dogs, and the highest degree of human activity and accessibility of the Channel Islands. Island fox numbers on Santa Catalina Island have fluctuated widely over the past 30 years. In [[Page 10339]]
Laughrin's early 1970s studies, only 2 island foxes were trapped on Santa Catalina Island for a trap efficiency of 6 percent and an average estimated density of 0.3 fox per mi² (0.1 fox per km²) (Laughrin 1973). This density was 37 percent lower than any other island during this study. The reason for past low island fox numbers on Santa Catalina Island is unknown; the available food and habitats are comparable to those on the other islands. Island fox numbers on Santa Catalina Island increased slightly between 1975 and 1977, with average estimated densities of 0.77 fox per mi² (0.29 fox per km²) (Propst 1975) and 0.8 fox per mi² (0.30 fox per km²) (Laughrin 1980). During 1989 and 1990, average density estimates increased, ranging from 6.7 to 33.1 foxes per mi² (2.6 to 12.8 foxes per km²) (Garcelon et al. 1991). The Santa Catalina Island fox population increased to an estimated 1,342 foxes by 1994 (Roemer et al. 1994).

In 1999, the Santa Catalina Island fox population experienced a dramatic decline attributed to canine distemper, presumably introduced by domestic dogs, in the eastern portion of the island (Timm et al. 2000). Santa Catalina Island is separated into a large eastern side of 40,000 ac (16,190 ha) and a small western side of 8,000 ac (3,240 ha) by a narrow isthmus, which has apparently served as a barrier to the canine distemper virus. Anecdotal accounts of fox absence in the summer of 1999 resulted in renewed trapping efforts to ascertain the status of the species, and investigation of a potential diseaserelated decline. Two live foxes and one deceased fox recovered from the eastern portion of the island tested positive for canine distemper virus or had high antibody titers (a measure of concentration), constituting the first positive record of canine distemper in island foxes (Timm et al. 2000). Previous studies had found no evidence of canine distemper in Santa Catalina Island foxes (Garcelon et al. 1992). A trapping effort conducted during this time period resulted in a minimum population estimate of only 100 foxes for the year 2000 (Kohlmann et al. 2003), compared to an islandwide population estimate of 1,342 foxes reported in 1994 (Roemer et al. 1994).

Island fox trapping efforts during 2000 and 2001 resulted in capture of 137 island foxes on the western end and 37 on the eastern portion of Santa Catalina Island, and a conservative population estimate of 225 foxes islandwide (Kohlmann et al. 2003; D. Garcelon, unpublished data). Monitoring conducted in 2001 and 2002 resulted in capture of 161 individuals (67 at the east end, 94 at the west end) and a conservative population estimate of 215 foxes islandwide (119 on the west end, and 96 on the east end) (Kohlmann et al. 2003).

A captive propagation program for the Santa Catalina Island fox was initiated in 2001. The Institute for Wildlife Studies captured 16 adults (10 females and 6 males) between February and midMarch 2001 as the founder population for the captive breeding program. The pregnant females from the founder group gave birth to a total of 18 pups. Twelve of these pups died within 7 days of birth, likely due to stress to the females from capture during late pregnancy. The six remaining pups were released onto the east end of the island in the fall of 2001. Eight pups were released as part of this program in 2002, and 15 were released in 2003. During 2002, 10 additional foxes were brought into captivity from the west end to replace captive breeding stock. Early results of the captive breedingrelease program are promising. Of the 14 pups released in 2001 and 2002, 11 are known to be alive and at least 3 captive reared foxes are reproducing (Institute for Wildlife Studies, unpublished data).

In addition to the captive breeding program, the Santa Catalina Conservancy and the Institute for Wildlife Studies initiated a translocation program in 2001 to reestablish island foxes on the east side of the island. Seven of 10 juvenile island foxes were relocated from the west end to the east end in 2001, and all of the 12 foxes that were relocated in 2002 remain in the population (Institute for Wildlife Studies, unpublished data). The translocation effort has been discontinued to avoid adverse effects to the west end population, but appears to have been successful as a population augmentation mechanism for the east end. At least 6 of the translocated foxes are known to be reproducing on the east end, and at least 4 pups have been produced in the wild by translocated animals.

Previous Federal Action

We published an updated candidate Notice of Review (NOR) for animals on December 30, 1982 (47 FR 58454). This notice included all six subspecies of island fox in a list of category 2 candidate species. We maintained all six subspecies of island fox as category 2 candidates in subsequent notices: September 18, 1985 (50 FR 37958), January 6, 1989 (54 FR 554), November 21, 1991 (56 FR 58804) and November 15, 1994 (59 FR 58982). As announced in a notice published in the February 28, 1996, Federal Register (61 FR 7596), we discontinued the designation of category 2 candidates. Thus, all six subspecies of island fox were not included in the 1996 and subsequent NORs until our October 30, 2001 (66 FR 54808), NOR in which the San Miguel, Santa Rosa, Santa Cruz, and Santa Catalina Island foxes were included as candidate species. Candidate species are those species being considered for listing by the Secretary but which are not yet the subject of a proposed listing rule (50 CFR 424.02(b).

On June 1, 2000, we received a petition from the Center for Biological Diversity (Center) in Tucson, Arizona, and the Institute for Wildlife Studies in Arcata, California, requesting that we add four subspecies of island fox, the San Miguel Island fox, Santa Rosa Island fox, Santa Cruz Island fox, and Santa Catalina Island fox, to the list of endangered species pursuant to the Act. Due to a lack of funding, we initially did not issue a 90day finding in response to the petition. In response to our lack of action on the petition, the Center sent us a 60day notice of intent to sue on December 4, 2000. In the October 30, 2001, NOR, however, the island foxes were included as candidate species for which listing was warranted but precluded by higher priority listing actions (66 FR 54808); as noted in the NOR, the Service considered that the island foxes, and all other candidate species, as having been subject to a positive 90day finding and a warrantedbut precluded 12month finding (66 FR 54814). We proposed to list the four subspecies of island fox on December 10, 2001 (66 FR 63654). The proposed rule satisfied a measure in the settlement agreement with the Center (Center for Biological Diversity, et al. v. Norton, Civ. No. 01 2063 (JR) (D.D.C.)), entered by the Court on October 2, 2001.

On April 22, 2003, the Center filed suit against the Service for failure to finalize the listing and for failure to publish a final determination regarding critical habitat. (Center for Biological Diversity v. Williams, et al. No. CV032729 AHM). In a settlement of that lawsuit, the Service agreed to submit the final listing determination to the Federal Register on or by March 1, 2004, and if prudent, submit a proposed rule to designate critical habitat to the Federal Register on or by October 1, 2004, and a final determination regarding critical habitat on or by November 1, 2005.

Summary of Comments and Responses

In the December 10, 2001, proposed rule (66 FR 63654), we requested all interested parties to submit factual
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reports or information that might contribute to development of a final rule. A 60day comment period closed on February 8, 2002. We contacted appropriate Federal agencies, State agencies, county and city governments, scientific organizations, and other interested parties and requested comments, and notified affected landowners of the proposed listing. We published public notices of the proposed rule, which invited general public comment, in the Santa Barbara News Press and Ventura County Star on December 15, 2001. We requested peer review in compliance with our policy, published in the Federal Register on July 1, 1994 (59 FR 34270). We did not receive any requests for a public hearing, and no public meeting was held.

During the public comment period, we received written comments from 11 individuals, businesses, and organizations. In all, one commenter opposed the listing and two supported continued protection of the subspecies proposed for listing. The remaining eight commenters stated neither opposition nor support for the ruling, but provided additional information on the causes of decline and threats to the island fox. Issues raised by the commenters, and our response to each, are summarized below.

Issue 1: Several commenters stated that the rule lists the introduction of nonnative herbivores as the primary cause of the fox decline. One commenter further pointed out that, if nonnative herbivores were the cause of decline, the fox population on Santa Rosa Island should have been decimated in the 1870s, when more than 100,000 head of sheep (Ovis aries) were present. Several commenters noted that foxes flourished for over 130 years with extensive grazing by cattle (Bos taurus) and sheep, and for close to 70 years with the added presence of pigs, elk, and deer.

Our response: Although the degradation of habitat that occurred due to the introduction of nonnative herbivores is the first threat presented in the rule (under Factor A), this threat was not identified as the primary cause of the island fox decline. The Service concluded that the primary cause of decline for island foxes is from predation by golden eagles on Santa Cruz, San Miguel, and Santa Rosa Islands and canine distemper on Santa Catalina Island. However, the introduction of nonnative mammals to the northern Channel Islands has facilitated declines of island foxes in two ways: (1) By typeconverting woodland and scrub habitats to open grasslands comprised of nonnative annual grasses, it greatly reduces the amount of cover available to island foxes and (2) feral pigs and deer provide an unnatural prey base for golden eagles, which has facilitated the colonization of the northern Channel Islands by golden eagles. Removing nonnative animals is essential to break the link that attracts golden eagles to the northern islands, where they also prey on island foxes.

Issue 2: Several commenters pointed out that the rapid decline in fox populations over the last 6 years occurred concurrently with the removal of nonnative species, including pigs and cattle, and the reduction of deer and elk. The commenters proposed that the removal of nonnative species caused the decline of the island foxes.

Our response: Declines of island foxes only occurred concurrently with the removal of nonnative species on Santa Rosa Island. On San Miguel Island, no nonnative species removal programs occurred during the period of decline, and on Santa Cruz Island, 9,000 sheep were removed after island fox numbers had declined. An analysis of the best available data regarding the island fox population declines (Coonan et al. 2000; Roemer et al. 2001b and 2002; Coonan 2003) has not revealed a causal link between the removal of cattle on Santa Rosa Island and the decline. The removal of cattle from Santa Rosa Island may have negatively affected foxes, as the cattle fed on the nonnative annual grasses and kept them in check. Although island foxes may have been negatively affected by the proliferation of nonnative annual grasses following the removal of cattle (Roemer and Wayne 2003), we do not believe that this was the cause of decline. As described in the rule, predation by golden eagles is the primary cause of decline on the three northern Channel Islands. We are not aware of any data that show that the decline of island foxes is due to the removal of nonnative herbivores. In addition, island foxes existed on the islands for thousands of years without the presence of deer, elk, pigs, and cattle. Therefore, it seems unlikely that removing nonnative species would cause a decline in island foxes.

Issue 3: Two commenters recommended that objective research be conducted prior to the removal of deer and elk on Santa Rosa Island to study the impacts of removing nonnative animals. Another commenter asked if the Service or NPS had conducted any research to find out if pigs and cattle have a positive impact on fox populations.

Our response: We are not aware of any studies that have been or are planned to be conducted on these subjects. Funding for research has been focused on those areas identified as being most crucial for the recovery of the island fox. On Santa Cruz, Santa Rosa, and San Miguel islands, financial resources have gone into removing the primary threat, golden eagles, and constructing and operating captive breeding facilities. Because island foxes existed on all islands for thousands of years without the presence of deer, elk, pigs, and cattle, the Service concludes that removing these species should not affect the longterm conservation of island foxes once the ecosystem has been restored to more natural conditions.

The Service, the NPS, and the Island Fox Conservation Working Group have identified a concern with the timing of eradication of pigs from Santa Cruz Island. Pig carcasses will be left to decompose on the island, rather than being transported to the mainland. If golden eagles remain on the island, the widespread availability of pig carcasses may increase golden eagle numbers and impede capture efforts by making bait less attractive. In addition, once pigs have been removed or their numbers substantially decreased, lingering golden eagles may switch to island foxes remaining in the wild. The Service, NPS, and TNC are working to develop measures to decrease the probability of the negative effects of pig removal on island foxes. Although the removal of pigs may have shortterm negative effects on island foxes, this action is essential to deter golden eagles from colonizing the islands, and will facilitate the longterm recovery of the island fox.

Issue 4: One commenter noted that after burros (Equus asinus) were removed from San Miguel Island, vegetation piled up, making the island impossible to penetrate. The conversion of onceopen hunting grounds to impenetrable forest may have affected the ability of foxes to find food.

Our response: No impenetrable forests currently exist on San Miguel Island. When the San Miguel Island fox began to decline, the NPS conducted a study to determine if food availability was the cause of decline. They concluded that the availability of food was not the cause of decline (Coonan et al. 1998; Crowell 2001). Numbers of alligator lizards (Gerrhonotus multicarinatus), mice, and seafigs, important components of the San Miguel Island fox diet, did not decrease during the period of decline. In addition, the decrease in fox numbers was not [[Page 10341]]
accompanied by declines in adult fox weight, making lack of food unlikely as a cause of decline.

Issue 5: One commenter stated that the removal of greater than 35,000 sheep and 3,000 cattle on Santa Cruz Island resulted in an explosion of fennel (Foeniculum vulgare), which now forms ``miles of impenetrable fennelforests.'' The commenter poses that the loss of the island foxes' open hunting habitat caused the population crash. Another commenter speculated that foxes needed the more open habitat that grazing animals provided on all islands, and the removal of those animals led to the decline.

Our response: Nonnative fennel covers approximately 10 percent of Santa Cruz Island (Breton and Klinger 1994). The densest stands of fennel are concentrated in approximately 1,800 ac (730 ha) (in the isthmus area; an additional 1,600 acres in the central valley on Santa Cruz Island are dominated by fennel (NPS 2002). The best available data do not support the conclusion that island foxes find the fennel to be impenetrable. In a recent study to determine distribution and abundance of island foxes on Santa Cruz Island, most foxes were found in the central valley and isthmus area. Of the 82 foxes trapped during the study, 22 were trapped in the thick fennel stands on the isthmus (Dennis et al. 2001). The high percentage of island foxes found in these stands may be due to the fact that the fennel provides foxes with cover from aerial predation by golden eagles. Crooks and Van Vuren (1995) found more foxes in the fennel grasslands than in ravines and patches of scrub oak on the isthmus. As with San Miguel Island, no available data support the idea that island foxes were limited by food availability. Although island foxes (predecline) could be found in all vegetative community types occurring on the island, they appear to prefer vegetative communities that provide some cover. As described above, for most of the island foxes' evolutionary history, nonnative herbivores were not present on the islands. Because island foxes existed for thousands of years in the more dense vegetation with increased cover that occurred on the island before the introduction of nonnative herbivores, removing these species should not affect the longterm conservation of island foxes once the other threats to its continued existence have been removed.

Issue 6: One commenter pointed out that the decrease in the fox population coincided with increased trapping and fox studies by the NPS and other scientists, and that it is possible that humans played a role in the population decline.

Our response: The best available data do not support a causal link between the increased trapping and studies by scientists. In fact, no trapping of island foxes occurred during declines on Santa Catalina and Santa Rosa islands. Surveys that include capture and handling of island foxes are conducted biannually on San Nicolas Island, which has had stable or increasing island fox numbers for approximately a decade. Between 2000 and 2003 (following the decline on Santa Catalina Island), the Catalina Island Conservancy increased capture and handling of island foxes. During this time period, the size of the island fox population has increased.

Issue 7: One commenter asked about the sizes of the fox populations on the Channel Islands prior to the influence of Europeans.

Our response: We have no data on fox numbers on the Channel Islands prior to the influence of Europeans. We do know from the fossil record that foxes existed on the islands; however, this information cannot be used to determine numbers.

Issue 8: One commenter stated that government efforts to rescue island foxes will fail because the foxes are being managed as a ``climax'' species.

Our response: We are not sure what the commenter meant by managing foxes as a ``climax'' species. Island foxes are found in all habitats on the island, including native habitats such as oak woodlands. Our management for island foxes has focused on addressing the primary causes of decline (golden eagles on the northern Channel Islands and canine distemper on Santa Catalina Island) and on captive propagation of island foxes to bolster numbers.

Issue 9: Two commenters disputed the conclusion that the presence of deer on Santa Rosa Island is a threat to the fox, as the deer ``likely'' compete for flowering and fruiting branches of native shrubs. One commenter stated that no scientific evidence is cited to support this assertion.

Our response: Competition between deer and island foxes has not been studied on Santa Rosa Island. In the presence of a healthy island fox population, competition for food resources with deer may occur. Deer have been shown to have a significant browsing effect that reduces the amount of flowering and seed production on the Santa Rosa Island manzanita (Arctostaphylos confertiflora) on some study plots (Schreiner et al. 2003).

Issue 10: Three commenters pointed out that Santa Rosa Island foxes may have been supported in large part by carrion available from the 300 to 400 feral pigs shot annually, as well as from the normal death of piglets. In addition, carrion from cattle, elk, and deer would have been available to island foxes. The decline of island foxes on Santa Rosa Island corresponded with the removal of pigs from the island.

Our response: Island foxes are omnivorous and do feed upon carrion, when available. No studies of food availability were conducted on Santa Rosa Island during the period of decline; however, environmental conditions should have been similar to those on San Miguel Island, where food availability was ruled out as a cause of decline (Coonan et al. 1998; Crowell 2001). Although the decline of island foxes on Santa Rosa Island occurred after pig removal, the best available data concerning island fox declines do not implicate feral pig removal as the cause of the declines (Coonan et al. 2000; Roemer et al. 2001b and 2002; Coonan 2003). We believe that removing pigs has had a net beneficial effect on island foxes, by removing the food source that supports their main predator, the golden eagle thereby discouraging golden eagles from staying on the islands.

Issue 11: One commenter pointed out that there is some disagreement on which habitats island foxes prefer, and that scrub and woodland habitat exist on Santa Rosa Island, yet no foxes remain.

Our response: The proposed rule states that the island fox is a habitat generalist, occurring in all habitats found on the islands. Some authors have indicated that island foxes prefer areas of diverse topography and vegetation (Von Bloeker 1967; Laughrin 1977; Moore and Collins 1995). Laughrin (1973, 1980) found woodland habitats to support higher densities of island fox due to increased food availability, while Crooks and Van Vuren (1995) found island foxes to prefer fennel grasslands and avoid ravines and scrub oak patches. Because of the generalist nature of the island fox, studies conducted at different times under variable environmental conditions may produce different results. Scrub and woodland habitat only comprise about 5 percent of Santa Rosa Island; the majority of the island is covered by nonnative annual grasslands (Clark et al. 1990). Although some habitats providing cover do remain on Santa Rosa Island, these habitats have not protected island foxes from golden eagle predation, as no island foxes currently exist in the wild on the island.

Issue 12: Several commenters stated that the island fox decline on Santa
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Rosa Island coincided with NPS assumption of the ranch. These commenters recommended further investigation of NPS management as a cause of decline.

Our response: The best available data concerning the island fox decline on Santa Rosa Island points to the golden eagle as the cause of decline (Roemer 1999; Roemer et al. 2001b, 2002; Coonan 2003b; Coonan et al. in review; Institute for Wildlife Studies unpublished data). We are aware of no information that indicates that NPS management was responsible for the presence of golden eagles on the island. We are also not aware of other data supporting NPS management as a cause of decline. See responses to issues 2, 5 and 6.

Issue 13: Two commenters doubted the importance of golden eagle predation in the island fox declines. One only rarely observed golden eagles on the Santa Rosa Island, while another asked if there have been sightings of numerous successful hunting attempts by golden eagles on island foxes.

Our response: Direct observations of golden eagles on the northern Channel Islands have been rare, even by teams of biologists working on golden eagle removal. However, golden eagles commonly leave behind evidence of island fox carcasses that leaves little doubt as to their involvement. Specific evidence found at numerous fox carcasses implicating golden eagle predation includes plucking spots, golden eagle feathers, talon holes, and carcasses typically left by eagles (evisceration, degloving of limbs (i.e., pulling flesh away from bone as in removing a glove), damage to fragile bones). In addition, numerous island fox bones have been found in golden eagle nests on Santa Cruz and Santa Rosa islands (Latta 2001; B. Latta, pers. comm. 2003), indicating that golden eagles were present on the island before 2000 and preyed upon island foxes.

Issue 14: One commenter stated that golden eagles had been regular visitors to the islands for years and that island foxes had dealt with aerial predators for eons. Also, due to the more nocturnal nature of foxes, they would not be visible when golden eagles were foraging.

Our response: The behavior of the island fox suggests an evolutionary history lacking in predation. As described in the proposed rule, the only known predator of island foxes was the redtailed hawk (Buteo jamaicensis), which preyed only occasionally on young island foxes (Laughrin 1973; Moore and Collins 1995). Although island foxes are primarily nocturnal, they exhibit more diurnal behavior than mainland gray foxes and can commonly be seen during the daytime. Evidence of golden eagle predation at island fox carcass sites, as well as the remains of island foxes found in a nest on Santa Rosa Island, indicate that golden eagles are finding and preying upon island foxes.

Issue 15: One commenter was skeptical that introducing bald eagles (Haliaeetus leucocephalus) would assist the island fox situation.

Our response: We acknowledge that the effectiveness of bald eagles in assisting with island fox recovery is uncertain. Restoring bald eagles to the northern Channel Islands may deter future golden eagles from becoming resident and attempting to nest on the islands, especially if the majority of the prey base for the golden eagle is removed. Bald and golden eagles are fairly equally matched in interspecific antagonistic interactions; in most cases, the territory holder will have the advantage (B. Latta, pers. comm. 2001). If bald eagles successfully breed and create territories, they may be able to discourage future colonization by nonterritorial golden eagles. However, our recovery actions for the island fox do not hinge upon the success of bald eagle reintroduction. Removing golden eagles and conditions attracting them to the islands is the singlemost important recovery action for the Santa Cruz, Santa Rosa, and San Miguel island fox and will be implemented regardless of the status of bald eagles on the islands. Unlike golden eagles, which forage on land, bald eagles are primarily marine feeders, and coexisted with island foxes in the past. Remains from an historic bald eagle nest indicate that island foxes constituted less than 0.5 percent of faunal elements found, and these remains were speculated to be scavenged rather than hunted (Collins et al. 2003; Paul Collins, Santa Barbara Museum of Natural History, pers. comm. 2003).

Issue 16: Two commenters questioned why the proposed listing rule did not include the San Clemente Island fox and the San Nicolas Island fox subspecies, as these populations also have threats to their continued existence. San Nicolas Island foxes have unusually low genetic variability, increasing their susceptibility to disease. One commenter presented information concerning threats to the San Clemente Island fox from the management program for the San Clemente loggerhead shrike (Lanius ludovicianus mearnsi). Another commenter disputed the characterization contained in the proposed rule that the decline of the San Clemente Island fox population was ``slow,'' pointing out that the decline, if continued over time, would probably lead to extinction in the next 100 years.

Our response: We limited our analysis in the proposed rule to the four subspecies on which we were petitioned. The petition included substantial information concerning the threats to these four subspecies. We did not receive a petition for the San Clemente and San Nicolas island subspecies. In addition, because we determined that listing was not needed, we did not make these subspecies candidates in the October 2001 NOR. We will continue to monitor the San Nicolas Island fox and San Clemente Island fox to determine if they warrant listing.

Issue 17: Three commenters stated that the entire island fox species should be listed, as with precipitous declines on 4 of 6 islands where it occurs, it meets the definition of endangered: ``any species which is in danger of extinction throughout all or a significant portion of its range.''

Our response: The Endangered Species Act allows for listing of species, subspecies, or distinct population segments. Because island foxes have subspecific status on each island where they occur, this taxonomic level is the appropriate level upon which to evaluate our listing decisions. As discussed previously, the island foxes on San Clemente Island and San Nicolas Island do not warrant listing under the ESA.

Peer Review

In accordance with our July 1, 1994, Interagency Cooperative Policy for Peer Review in Endangered Species Act Activities (59 FR 34270), we solicited review from five experts in the fields of ecology, conservation, genetics, taxonomy, pathology, and management. Four of these have direct experience with island foxes, while the fifth is a wellknown mammalogist. The purpose of such a review is to ensure that listing decisions are based on scientifically sound data, assumptions, and analyses, including input from appropriate experts. Three reviewers sent us letters during the public comment period supporting the listing of the four island fox subspecies. All three provided corrections on minor factual issues, interpretation of data, and citations. One recommended that the entire island fox species be listed, while another recommended further scrutiny and monitoring for the San Clemente Island fox. Their information has been incorporated, as appropriate. [[Page 10343]]

Summary of Factors Affecting the Species

Section 4 of the Endangered Species Act and its implementing regulations (50 CFR part 424) issued to implement the listing provisions of the Act establish procedures for adding species to the Federal Lists. A species may be determined to be an endangered or threatened species due to one or more of the five factors described in section 4(a)(1) of the Act. These factors and their application to the four island fox subspecies are as follows:

A. The present or threatened destruction, modification, or curtailment of its habitat or range. Habitat on all islands occupied by island foxes has been altered by a history of livestock grazing, cultivation, and other disturbance. A century and a half of grazing by nonnative herbivores, including sheep, goats (Capra hircus), rabbits (Oryctolagus cuniculus), deer, elk, cattle, pigs, and horses (Equus caballus) resulted in substantial impacts to the soils, topography, and vegetation of the islands (Coblentz 1980; Johnson 1980; O'Malley 1994; Peart et al. 1994). Damage to native island plants and their habitats on the northern Channel Islands by introduced stock and game animals is discussed in our 1997 listing of 13 endemic island plants as endangered or threatened (62 FR 40954).

Even after the removal of nonnative grazers on some islands, habitat recovery is slow (Hochberg et al. 1979) and threatened by the spread of nonnative plants that became established during the ranching era. These exotic species continue to invade and modify island fox habitat, resulting in lower diversity of vegetation and habitat structure, and reduced food availability. The replacement of native shrub communities by nonnative annual grasslands has reduced protective cover for island foxes, making them more vulnerable to predation (Roemer 1999; Coonan et al. in review). Annual grasslands also offer fewer food resources to foxes, and the seeds of nonnative annual grasses can become lodged in the eyes of island foxes, causing occasional damage or temporary blindness (Laughrin 1977).

In summary, the habitat of island foxes on all islands has been subject to substantial humaninduced changes over the past 150 years. Although these changes have resulted in some adverse effects to island foxes described above, they are unlikely to have directly caused the observed declines. However, the habitat changes indirectly contributed to the effects of other factors (e.g., predation) by reducing the amount of vegetative cover available to island foxes.

B. Overutilization for commercial, recreational, scientific, or educational purposes. Although island foxes were used in the past for pelts and ceremonial uses by Native Americans (Collins 1991b), island foxes are not currently known to be exploited for commercial, recreational, scientific, or educational purposes.

C. Disease or predation. Predation. Recent island fox declines on San Miguel, Santa Cruz, and Santa Rosa islands have been attributed to predation by golden eagles (Roemer 1999; Roemer et al. 2001b, 2002; Coonan et al. in review). Roemer (1999) linked 19 of 21 documented island fox mortalities on Santa Cruz Island between April 1994 and July 1997 to golden eagles. Most (90 percent) of these mortalities occurred in 18 months between April 1994 and September 1995. On San Miguel Island, 5 of 7 mortalities of radiocollared foxes were attributed to golden eagle predation between 1998 and 1999 (Roemer et al. 2001b; Coonan et al. in review). No mortality data exist from Santa Rosa Island, but due to its location between Santa Cruz and San Miguel islands, island foxes on Santa Rosa Island likely experienced similar predation pressures from golden eagles.

As island foxes did not evolve with the presence of a large avian predator, they are likely not vigilant towards avian predators, and thus provide an easy target for golden eagles (Roemer et al. 2001b). Golden eagle predation continues to be the leading cause of mortality of island foxes on Santa Cruz Island. In 3 years of islandwide radio tracking on the island, 16 of 20 island fox mortalities were attributed to golden eagle predation (Institute for Wildlife Studies, unpublished data). Annual survivorship of Santa Cruz Island foxes, as estimated from radiotelemetry, was 61 percent in 2001 and 70 percent in 2002 (Coonan 2003b). This level of survivorship is below the 80 percent required for an increasing island fox population (Roemer et al. in prep.).

The current level of golden eagle activity on the northern Channel Islands is unprecedented (Roemer et al. 2002). Golden eagles were known to occasionally visit the islands but never to establish residence (Diamond and Jones 1980; Jones and Collins, in prep.). The first known active golden eagle nest on the Channel Islands was located on Santa Cruz Island in 1999 (Latta 2001), but golden eagles were likely established on the island as early as 1994 (Roemer et al. 2001b). Island fox remains, along with the remains of feral piglets, common ravens (Corvus corax), Brandt's cormorants (Phalacrocorax pencillatus), and western gulls (Larus occidentalis), were found in the nest. In September 1999, surveys by the Santa Cruz Predatory Bird Research Group (SCPBRG) identified 12 resident golden eagles, including possibly 5 breeding pairs on Santa Cruz Island.

At the time we published the proposed rule, golden eagles breeding on Santa Cruz Island were thought to ``commute'' to Santa Rosa and San Miguel Islands to feed. On Santa Rosa and San Miguel Islands, eagles find fewer alternative prey species to island foxes (e.g., no feral pigs on Santa Rosa and San Miguel islands as occur on Santa Cruz Island) and foxes have less cover from vegetation to hide them from avian predators (Roemer 1999). However, since the proposed rule was published, we have obtained information that two breeding pairs appeared to have successfully bred on Santa Rosa Island during the period when island fox numbers were declining (Latta 2003). Remains of island foxes, deer fawns, and numerous birds were found during an excavation of one of the nests on Santa Rosa Island, indicating that golden eagles were breeding on the island before island foxes were taken into captivity in 1999 and 2000.

Before golden eagles started using the northern Channel Islands in the 1990s, the only known predator of island foxes was the redtailed hawk (Buteo jamaicensis), which preyed only occasionally on young island foxes (Laughrin 1973; Moore and Collins 1995). The docile and inquisitive nature of the island fox (Laughrin 1977) suggests an evolutionary history lacking predation (Carlquist 1974).

The recent colonization of the northern Channel Islands by golden eagles is likely a combination of two factors: (1) Introduction of exotic mammals on the northern Channel Islands, resulting in a historically unprecedented prey base, and (2) the extirpation of bald eagles from the islands as a result of dichlorodiphenyltrichloroethane (DDT) poisoning. Historically, the small population of vertebrate island fauna would have provided little prey for golden eagles, which rely on a diet of small terrestrial vertebrates. Before the ranching era on the Channel Islands, transient golden eagles landing on the islands would have found little prey to encourage them to establish permanent residence. Furthermore, nesting bald eagles would have discouraged foraging golden eagles from establishing residence by aggressively defending
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their already established territories. Bald eagles are represented in the prehistoric fossil record of the northern Channel Islands (Guthrie 1993) and bred there until 1960, when nest failures, as a result of DDT contamination, extirpated them from the northern Channel Islands (Kiff 1980). The northern Channel Islands (Anacapa, Santa Cruz, Santa Rosa, and San Miguel) likely supported more than 14 pairs of bald eagles before their decline (Kiff 1980).

Roemer et al. (2001b) modeled timeenergy budgets and predation rates of golden eagles on Santa Cruz Island to determine if the precipitous decline in island foxes could be attributed to predation alone. They concluded that the island fox declines on the northern Channel Islands are a consequence of hyperpredation, defined as when the availability of one prey species, that can sustain high predation rates, leads to the extinction of another prey species that becomes an alternate food resource for a shared predator (Courchamp et al. 1999). In this case, the large feral pig population provided sufficient prey base for the golden eagle t

FOR FURTHER INFORMATION CONTACT Field Supervisor, U.S. Fish and Wildlife Service, Ventura Fish and Wildlife Office, at the address above (telephone 805/6441766; facsimile 805/6443958).