Decline of the Endangered Morro Bay Kangaroo Rat in California

The genus Dipodomys (family Heteromyidae) comprises 20 species of kangaroo rats, which are endemic to the arid and semiarid western United States, Mexico, and southwestern Canada (Fernandez et al. 2012; Smithsonian Institution 2014). Thirteen of these species occur in California, including 23 recognized subspecies (Hall 1981; Schmidly et al. 1993; Williams et al. 1993; Best et al. 1996), and many of these subspecies are special status taxa. Five of these are endangered pursuant to the U.S. Endangered Species Act (ESA 1973, as amended; and also state endangered or state threatened), three are state species of special concern, and nine are regarded as vulnerable (Goldingay et al. 1997). The Morro Bay kangaroo rat Dipodomys heermanni morroensis (Figure 1) is an endangered subspecies in California. It was listed as endangered pursuant to the U.S. Endangered Species Conservation Act in 1970 (U.S. Fish and Wildlife Service [USFWS] 1970), the California Endangered Species Act (1971) in 1971, and the U.S. Endangered Species Act (ESA 1973, as amended) in 1973. In addition, it was designated as fully protected pursuant to the California Fish and Game Code in 1970 (California Fish and Game Commission 1970).

The high proportion of special status kangaroo rats is attributed mostly to their abundance in relatively flat terrains with early seral or open climax plant communities (e.g., grassland, shrubland, open woodland) and in sand dune habitats (Congdon and Roest 1975; Mares 1993; Goldingay et al. 1997). In California, flat inland valley floors have been developed for urban, agricultural and industrial purposes, and coastal sand dunes for residential purposes. Loss of habitat has also occurred through plant community succession (Congdon and Roest 1975; Kelt 1988; USFWS 2011) whereby open spaces in the vegetation are filled in by native and invasive (nonnative) plant species.

The kangaroo rats share a number of important attributes that adapt them for habitats with sparse vegetation and arid environments (Mares 1993). Bipedality enables saltation and ricochetal movements for evading predators (Bartholomew and Caswell 1951; Longland and Price 1991). Enhanced hearing for predator detection is achieved via enlargement of the auditory bullae (posterior portion of skull enclosing parts of middle and inner ears; Webster and Webster 1980). Granivory enables access to foods rich in energy and metabolic water (Mares and Rosenzweig 1978; Reichman 1981) and accumulation of a buffer in seasonally productive environments because kangaroo rats typically hoard seeds in their underground burrows (Brown et al. 1979; Nikolai and Bramble 1983). In addition, kangaroo rats have anatomical and physiological adaptations for arid environments (Schmidt-Nielsen 1964), along with being nocturnal and semifossorial (Vaughan et al. 2011).

Kangaroo rats have been recognized as keystone species (e.g., Goldingay et al. 1997; Brock and Kelt 2004b; Davidson and Lightfoot 2006), including across trophic levels (e.g., Kerley et al. 1997; Valone and Schutzenhofer 2007) and through time (e.g., Ernest and Brown 2001; Hastings et al. 2007). Multiple studies elucidate their role in structuring plant communities (e.g., Davidson and Lightfoot 2007; Cosentino et al. 2013) by seed predation and caching (Brown et al. 1979; Brown and Heske 1990). In addition, kangaroo rats are ecosystem engineers that construct burrows and mounds, which are used by numerous other species (Hastings et al. 2007). Thus, kangaroo rats have multiple effects at the landscape level, some of which persist even after a population is extirpated.

The Morro Bay kangaroo rat has been studied extensively since the late 1950s, and its rapid decline has been documented. In response, multiple recovery efforts have been conducted beginning in the 1980s. Despite the research and recovery actions, no Morro Bay kangaroo rat has been captured since 1986 (Gambs and Holland 1988), and the last captive individual died at the National Zoological Park (Washington, D.C.) in 1993 (Roberts and Rall 1993). The California Department of Fish and Wildlife (California Department of Fish and Game 2000, 2005) considers the Morro Bay kangaroo rat as possibly extinct. Although there are many unpublished reports, little has been published regarding the Morro Bay kangaroo rat. Using all available information, we review the biology and conservation status from naming in 1907 to 2016, including taxonomy and genetics, soil type and burrows, history of decline, primary causes of decline, breeding in the wild and in captivity, habitat restoration, and threats, and provide conclusions and recommendations.

The Morro Bay kangaroo rat was originally described and named as Perodipus morroensis by Merriam (1907), with the type locality “Morro, San Luis Obispo Co., Calif.” Grinnell (1922) placed P. morroensis in Dipodomys and restricted the type locality to “the south side of Morro Bay, about four miles south of the town of Morro,” which is now the site of the communities of Baywood Park and Los Osos. On the basis of color pattern and skull characteristics, Boulware (1943) recognized Dipodomys morroensis as a subspecies of the Heermann's kangaroo rat Dipodomys heermanni, which is the currently accepted phylogenetic position. The Morro Bay kangaroo rat is the smallest of the nine subspecies of D. heermanni (Kelt 1988), with adult body mass of approximately 65 g (Roest 1984). It is diagnosed from the other eight subspecies by a combination of its smaller size, darker brown color, absent or incomplete white hip stripe, and black stripe at the tip of the rostrum (Grinnell 1922; Kelt 1988).

Dipodomys heermanni inhabits the California grassland, coastal scrub, and chaparral provinces of the Pacific Coast and San Joaquin Valley of central California (Schmidly et al. 1993) from El Dorado County to Santa Barbara County (Kelt 1988; Figure 2). The Morro Bay kangaroo rat is endemic to the vicinity of Morro Bay (specifically in and near Los Osos) in western San Luis Obispo County in coastal central California. The nearest subspecies is the Lompoc kangaroo rat D. heermanni arenae with a population 19 km to the southeast near Edna (San Luis Obispo County; Souza 1958).

The Lompoc kangaroo rat has been regarded as the closest relative of the Morro Bay kangaroo rat (USFWS 1982), in part due to geographic proximity. To test whether these two taxa are genetically distinct from each other, Matocq and Villablanca (2001) sequenced 443 nucleotides of mitochondrial DNA from the control region and cytochrome-b of 16 Morro Bay kangaroo rats and 8 Lompoc kangaroo rats. None of the eight alleles (defined by 19 polymorphic DNA positions) were shared between the two subspecies. In addition, both subspecies were monophyletic (alleles within each subspecies respectively comprised distinct portions of the phylogenetic tree of alleles). Considering the sample sizes, the lack of shared alleles, the monophyletic structure of the phylogeny, and the number of differences between the alleles, the probability that these two subspecies are genetically distinct (monophyletic) is > 95% (Takahata 1989; Takahata and Slatkin 1990).

Villablanca (2007) tested whether Morro Bay kangaroo rats are genetically distinct from the other three subspecies of D. heermanni in San Luis Obispo County, which are the subspecies with geographic ranges closest to the Morro Bay kangaroo rat. He analyzed microsatellite data from six loci from kangaroo rats collected at Morro Bay (Morro Bay kangaroo rat, n = 11, one location), at Lompoc (Lompoc kangaroo rat, n = 36, four locations), at Jolon (Jolon kangaroo rat D. heermanni jolonensis, n = 14, one location), and at the Carrizo Plain (D. heermanni swarthi, n = 10, one location). He used multilocus microsatellite data (2–35 alleles per locus, mean = 16, mode = 14) in Bayesian analyses (using BAYES-ASS+; Wilson and Rannala 2003) that assign each individual to the genetic population (location) with the highest probability of having produced its genotype. All of the genotypes in the Morro Bay sample were assigned to that genetic population (assignment probability ≥ 95%, P < 0.05). Likewise, no genotype sampled in another subspecies or location was assigned to the Morro Bay genetic population. Thus, because there was < 5% chance of gene flow into or out of the Morro Bay genetic population, the Morro Bay kangaroo rat should be regarded as genetically differentiated (Matocq and Villablanca 2001; Villablanca 2007).

The Morro Bay kangaroo rat has a small and restricted geographic range on old, stabilized sand dunes (windblown sand, late–middle Pleistocene; Wiegers 2009) underlying the communities of Baywood Park and Los Osos in the vicinity of Morro Bay. The historical geographic range comprises approximately 12.4 km² that correspond almost precisely with the distribution of Baywood Fine Sand (a soil type; Carpenter and Storie 1928), which occurs south and southeast of Morro Bay (Grinnell 1922; Stewart and Roest 1960; Congdon and Roest 1975; Figure 3). The communities of Baywood Park and Los Osos have developed on these sand dunes, some of which were farmed in the first half of the 20th century. Like the other subspecies of D. heermanni (Kelt 1988) and most kangaroo rats (Bartholomew and Caswell 1951), Morro Bay kangaroo rats construct burrows in compacted sandy soil (Roest 1973) with slopes < 15° (Gambs and Holland 1988). Individuals use and maintain multiple burrow systems, and up to 10 were used simultaneously by one individual in an outdoor enclosure (Gambs and Nelson 1989). The main burrow is approximately 1.8–3.0 m long, and with two or three chambers that contain a nest and seed caches. It has one or two main entrances and two or three side entrances that can be used for escape (Stewart and Roest 1960; Gambs and Nelson 1990). If one burrow or entrance is damaged (e.g., by off-highway vehicle, horse, or pedestrian; USFWS 1982), additional ones exist. Stewart (1958) reported a mean burrow depth of 23 cm, and Gambs and Nelson (1990) observed many burrows at depths > 70 cm and with the greatest at 90 cm. Based upon observations, the destruction of burrows by off-highway vehicles, horses, and pedestrians was highly localized and minimal rather than range-wide. Likewise, Toyoshima (1983) observed that Morro Bay kangaroo rats appeared not to be disturbed by pedestrians, horseback riding, and dogs.

Historically, researchers have divided the geographic range of the Morro Bay kangaroo rat into eight areas (Figure 4), which are the following, along with the year of last capture in each: Hazard, 1957 (Stewart 1958); Los Osos Oaks, 1957 (Stewart 1958); Baywood Park, 1977 (Roest 1977); Extension (also known as Turri Road), 1977 (Roest 1977); Pecho, 1979 (Toyoshima 1983); Junior High/Santa Ysabel, 1984 (Villablanca 1987); Buckskin, 1985 (Villablanca 1985, 1987); and Bayview (also known as Morro Palisades), 1986 (Gambs and Holland 1988). Estimates of the population size and area of occupied habitat from 1957 to 1986 are shown in Table 1 and Figure 5. In brief, the population size and area of occupied habitat declined from approximately 8,000 individuals (Congdon and Roest 1975) on 650 ha in 1957 (Stewart and Roest 1960) to approximately 50 individuals on 12.6 ha in 1986 (Gambs and Holland 1988). Since publication of the recovery plan (USFWS 1982) that was developed under the U.S. Endangered Species Act (ESA 1973, as amended), Morro Bay kangaroo rats were captured only at Junior High/Santa Ysabel in 1984, at Buckskin in 1985, and at Bayview in 1984, 1985, and 1986 (Villablanca 1985, 1987; Gambs 1986b; Gambs and Holland 1988). Despite many searches since 1986 (reviewed by USFWS 2011), including two nearly comprehensive range-wide surveys in 1995–2002 (O'Farrell 2003 and other O'Farrell citations therein) and 2008–2012 (Villablanca 2009; Kofron and Villablanca 2010, 2011; USFWS 2012), no Morro Bay kangaroo rat has been captured since 1986.

Our range-wide search from 2008 to 2012 (Villablanca 2009; Kofron and Villablanca 2010, 2011; USFWS 2012) also included most adjacent and nearby areas with sandy soil (Figure 3). Although we captured no Morro Bay kangaroo rats, we observed potential signs (possible evidence: burrow entrances shaped like an inverted U and with a runway, tail drag marks, surface seed pit caches; Stewart 1958; Villablanca 1987; USFWS and California Department of Fish and Game 1996) at Pecho and Junior High/Santa Ysabel in 2011, which suggests that some isolated colonies may still persist. In addition, we could not obtain permission to survey on four private properties with potential habitat, including the main Buckskin property (35.312010°, −120.813642°) where a Morro Bay kangaroo rat was last captured in 1985 (Villablanca 1985, 1987). The presence or absence of the Morro Bay kangaroo rat on these four private properties cannot be determined until surveys are conducted. According to the International Union for the Conservation of Nature, a species should be considered extinct only when there is no reasonable doubt that the last individual has died (IUCN 2012). In 2016, the Morro Bay kangaroo rat may be persisting at extremely low densities in a few isolated colonies.

Trapping studies show a correlation of the presence and abundance of Morro Bay kangaroo rats with the early seral stages of coastal dune scrub (Stewart and Roest 1960; Congdon and Roest 1975; Villablanca 1987; Gambs and Holland 1988; Figure 6), which are characterized by scattered shrubs < 0.9 m tall and interspersed with annual plants and bare ground. Some characteristic plants of coastal dune scrub in the range of the Morro Bay kangaroo rat are deerweed Acmispon glaber, sandmat Cardionema ramosissimum, buckbrush Ceanothus cuneatus, thistle Cirsium occidentale, California croton Croton californicus, seacliff wild buckwheat Eriogonum parvifolium, horkelia Horkelia cuneata, and grasses (Roest 1973; Gambs and Holland 1988). Captive Morro Bay kangaroo rats ate seeds of early and midsuccessional plant species when offered as food (deerweed, thistle, California-aster Corethrogyne filaginifolia, horkelia, California spineflower Mucronea californica, black sage Salvia mellifera, mock heather Ericameria ericoides, dudleya Dudleya caespitosa, chamisso bush lupine Lupinus chamissonis, and yellow bush lupine Lupinus arboreus); stems and leaves of Dudleya sp., Lupinus sp., and brome Bromus sp.; and ants, crickets, grasshoppers, and snails. We follow Baldwin et al. (2012) for the Latin and common names of plants.

Over 40 y ago Congdon and Roest (1975) stated that “without public ownership of occupied land and brush management, the Morro Bay kangaroo rat will become extinct.” The recovery plan (USFWS 1982), which is now 34 y of age, identified two primary causes of decline, with the basic reason being loss of habitat.

In the 5-y review, USFWS (2011) likewise identified the two primary causes of decline as loss of habitat by 1) development and 2) vegetation change in the absence of fire. Based upon our knowledge and experiences, the two primary causes of decline are 1) the direct loss of habitat by development (urban, agricultural, and industrial) and 2) the loss of habitat by plant community succession in the absence of fire, which agree with USFWS (1982, 2011).

In 2016, only pockets of habitat remain in all eight areas that were previously occupied, with optimal habitat (the early seral stages of coastal dune scrub) comprising an estimated 1% of the historical geographic range. Hazard (approximately 74 ha) and Los Osos Oaks (approximately 36.4 ha) are now mostly owned by California State Parks. Pecho (approximately 165 ha) is now mostly owned by California State Parks and California Department of Fish and Wildlife. Junior High/Santa Ysabel (approximately 14 ha) and Bayview (approximately 83 ha) are now mostly owned by California State Parks and California Department of Fish and Wildlife. However, a former private owner of Junior High/Santa Ysabel cleared and plowed much of it in the several years prior to sale in 2002 and also previously bulldozed the occupied area (approximately 0.8 ha) in 1984, which eliminated part of the population of Morro Bay kangaroo rats. The latter activity resulted in federal and state investigations with a subsequent legal settlement. All of these public lands, acquired since 1957, are now protected from development and available for habitat restoration. Buckskin is privately owned with much now developed for urban and agricultural purposes. Most of Baywood Park and the Extension are privately owned with much of both now developed for urban, agricultural, and industrial purposes. The lack of habitat restoration (e.g., by prescribed burns) on public lands and the developments on private lands have both contributed to the continued loss of habitat.

The Baywood Fine Sand in and near Los Osos previously supported a natural mosaic of coastal dune scrub, maritime chaparral, and coastal oak woodland (USFWS 1999). Historically, wildfires burned the mature vegetation, which returned it to early stages (Odion and Tyler 2002) and to habitat for the Morro Bay kangaroo rat. For example, Stewart and Roest (1960) reported Morro Bay kangaroo rats using a habitat corridor (a burned area with early seral vegetation) on a hill slope that was covered mostly with maritime chaparral, and this resulted in occupation of previously unoccupied habitat (before the fire) on the hill top. Likewise, kangaroo rats use dirt roads (and trails; F.X.V., personal observation), which may also provide important connections in the landscape (Brock and Kelt 2004a). The periodicity of wildfire in the vicinity of Morro Bay is unknown (Odion and Tyler 2002). However, fire suppression is now practiced, and it has contributed to the loss of habitat on public lands by not allowing the later stages of vegetation to be returned to the early seral stages. As young coastal dune scrub matures, the vegetation becomes taller and denser, which is less favorable for annual plants. Succession to dense, tall shrubs from early coastal dune scrub was estimated by the USFWS to require 10–15 y (USFWS 1982). The climax plant community is coastal oak woodland (USFWS 1999) and maritime chaparral.

The particular attributes of D. heermanni that adapt it for habitats with sparse vegetation and arid environments, plus the results of multiple trapping efforts (Stewart and Roest 1960; Congdon and Roest 1975; Toyoshima 1983; Villablanca 1987; Villablanca 2009), lead us to infer that the habitat becomes less favorable as succession progresses. Mature coastal dune scrub and maritime chaparral are dense, shrub-dominated plant communities with relatively few open spaces. Morro Bay kangaroo rats do not inhabit mature coastal dune scrub and maritime chaparral (and coastal oak woodland; Stewart and Roest 1960; Congdon and Roest 1975; Toyoshima 1983; Villablanca 1987; Villablanca 2009), presumably because the dense vegetation has substantially fewer annual food plants (USFWS 1982) and also negatively impacts their locomotion (Bartholomew and Caswell 1951; Rieder et al. 2010). In addition, increases in plant cover change the diversity of the small mammal community, which likely increases competition (discussed below; USFWS 1982; Gambs 1986b; Gambs and Holland 1988; Gambs and Nelson 1990). Therefore, the openness of the early seral stage vegetation is likely the most important characteristic of the habitat of the Morro Bay kangaroo rat (Stewart and Roest 1960; Villablanca 1987), along with compacted sandy soil. Stewart and Roest (1960) identified a grazed grassland (the Extension) where Morro Bay kangaroo rats occupied a harder soil. The individuals there had hair and skin in poor condition (Stewart 1958), which possibly indicated submarginal habitat.

Individuals are solitary in the wild (Gambs and Holland 1988) but with some degree of home range overlap, particularly by males, whose ranges overlap with the homes ranges of multiple females (Villablanca 1987). Home range was reported to be 0.08 ha in 1957 (Stewart 1958) and, then later after substantial population decline and habitat reduction, 0.24 ha in 1984–1985 (Villablanca 1987) and 0.23 ha in 1984–1986 (Gambs and Holland 1988). Trapping records indicate year-round activity, with juveniles captured from March to November (Roest 1984). Captive-bred individuals attained sexual maturity at approximately 42 d, and gestation averaged 32 d (Roest 1991). Litter size ranged from 1–4 pups (Stewart and Roest 1960; Roest 1991). Maximum longevity in the wild is probably 2–3 y (USFWS 1982).

Captive breeding of Jolon kangaroo rats and Lompoc kangaroo rats as surrogates commenced in 1976 and 1983, respectively, at California Polytechnic State University (San Luis Obispo). Captive breeding of Morro Bay kangaroo rats commenced there in 1984 with seven females and three males taken from the wild over 3 y (Roest 1991): eight individuals from Bayview, one from Junior High/Santa Ysabel, and one from Buckskin (Roberts and Rall 1993). Because of their solitary nature, individuals were aggressive when paired, which was problematic for establishing a long-term captive colony (Roest 1991; Rathbun et al. 1990; Roberts and Rall 1993). Paired individuals fought except when females were in estrus, and one individual was even killed during a pairing (Roest 1991). From 1984 to 1987, three females and two males reproduced, which resulted in 23 offspring (Roest 1991), and four other individuals died from unknown causes. By January 1989, the wild-caught individuals were of advanced age (≥ 5 y of age; maximum lifespan reported for captive Dipodomys is 8 y; Egoscue et al. 1970) and the lab-born individuals were younger (1.5–4.5 y of age). At this time the captive colony (n = 21; 12 females, 9 males) was transferred to USFWS (Piedras Blancas Research Station, San Simeon, San Luis Obispo County; Roest 1989; Rathbun et al. 1990). By November 1990, approximately 2 y later, 14 of these individuals had died, with no additional viable offspring (Rathbun et al. 1990). The seven remaining individuals (three females, four males; at this point 40–53 mo of age) were subsequently transferred to the National Zoological Park for a final attempt at a captive breeding program (Roberts and Rall 1993; USFWS 1999), but no additional reproduction occurred. The last of the captive individuals died in 1993 (Thompson et al. 1995). In preparation for future attempts, captive breeding of Lompoc kangaroo rats as a surrogate commenced in 1993 at the University of California Berkeley (Alameda County) and continued until 1998 (Yoerg and Shier 2000). We point out that the work reported by Roest (1991) was conducted primarily by undergraduate students, whereas the work reported by Rathbun et al. (1990), Roberts and Ralls (1993), and Yoerg and Shier (2000) was conducted by professional biologists and graduate students. The latter group was more qualified, and this detail has strongly influenced our point of view: that is, a successful captive breeding program for the endangered Morro Bay kangaroo rat can be achieved, if the Morro Bay kangaroo rat still exists.

A team of government agencies (California Conservation Corps, California Department of Corrections, California Department of Fish and Game, California Department of Forestry, California Polytechnic State University, California State Parks, and USFWS) conducted habitat restoration at Pecho from 1983 to 1986 (Gambs and Holland 1988; USFWS 1999), commencing 4 y after the last capture of Morro Bay kangaroo rats in this area in 1979 (Toyoshima 1983). Workers manually removed invasive iceplant Mesembryanthemum sp. (approximately 23 m³) by digging, removed brush by cutting from two plots (1 ha each), and conducted controlled burns on three plots (2 ha, 5 ha, 10 ha). Four Morro Bay kangaroo rats from the captive colony were introduced into an outdoor enclosure (aviary wire, 46 m wide × 46 m long × 1.5 m high × 0.9 m below the soil surface) at Pecho South in 1988. The enclosure was on a plot previously treated with a controlled burn in 1984. Three individuals disappeared during 1988 and 1989, and one escaped by burrowing (subsequently recaptured in 1988; Gambs and Nelson 1990; USFWS 1999). Despite the extensive recovery and survey efforts (e.g., Gambs 1989; Morro Group 1996; USFWS 2012), no Morro Bay kangaroo rat has been captured at Pecho subsequent to the habitat restoration.

Gambs and Holland (1988) identified the following as potential predators: common kingsnakes Lampropeltis getula, gopher snakes Pituophis melanoleucus, western rattlesnakes Crotalus viridis, barn owls Tyto alba, great-horned owls Bubo virginianus, long-tailed weasels Mustela frenata, American badgers Taxidea taxus, bobcats Lynx rufus, domestic cats, coyotes Canis latrans, gray foxes Urocyon cinereoargenteus, and domestic dogs. Multiple reports document the severe problem of domestic cat predation on native wildlife (e.g., Van Heezik 2010; Dauphine and Cooper 2011; Loss et al. 2013); however, no data exist for the predation rate of domestic cats on Morro Bay kangaroo rats. In this regard, the systematic review and quantitative analysis by Loss et al. (2013) is especially relevant. They determined that predation by domestic cats is probably the leading anthropogenic cause of mammal mortalities in the United States. Therefore, predation by domestic cats is likely a major threat, and we suspect it has contributed to the decline of the Morro Bay kangaroo rat due to the increased residential development (the source of domestic cats) in and near the habitat. Dogs likely never posed a threat because dogs are mostly diurnal (Berman and Dunbar 1983) whereas kangaroo rats are nocturnal. Our assessment of dogs is contrary to Gambs and Holland (1988) and USFWS (1999), neither of which stated their reasoning.

The habitat of the Morro Bay kangaroo rat has become increasingly fragmented by development since at least the early 1970s (Congdon and Roest 1975), resulting in loss of connectivity across the landscape and isolation of colonies (USFWS 1982, 1999). Habitat fragmentation reduces or eliminates gene flow, which potentially reduces genetic diversity. The resultant inbreeding can have deleterious effects on individuals, including reduced vigor, low fecundity, and sterility (Lande 1988). Although genetic diversity in Morro Bay kangaroo rats has not been evaluated across colonies, genetic exchange between colonies is predicted to decrease as the landscape becomes fragmented. However, rare dispersals can maintain gene flow and genetic diversity (Slatkin 1985). Matocq and Villablanca (2001) reported low genetic diversity in a 443-nucleotide fragment of mitochondrial DNA of the Morro Bay kangaroo rat, and because half of their samples were dried museum specimens collected in 1918 they were able to conclude that the lack of genetic diversity predates the rapid population decline since 1957. This result suggests the Morro Bay kangaroo rat has a history of low genetic diversity and that an episode of inbreeding or a small population (or possibly both) occurred sometime in the past, or that low genetic diversity is a long-term pattern. Likewise, Villablanca (2007) found the Morro Bay kangaroo rat to have significantly lower microsatellite diversity (mean number of alleles per locus, P = 0.02; expected heterozygosity, P = 0.01) than any of the other subspecies sampled. If this historical and low genetic diversity has resulted in genetically homogenous colonies, then genetic exchange between isolated colonies by dispersing individuals is less likely to result in genetic rescue. In addition, habitat fragmentation makes it unlikely that areas from which the Morro Bay kangaroo rat has been extirpated will be repopulated by dispersal from any persisting colonies (USFWS 1982), which eliminates potential for a demographic rescue. Therefore, we determine that habitat fragmentation, population fragmentation, reduced genetic diversity, and inbreeding are threats, and they have likely contributed to the decline of the Morro Bay kangaroo rat.

Interference competition may occur between burrowing rodents that destroy each other's burrows. California ground squirrels Spermophilus beecheyi moved into restored habitat for the Morro Bay kangaroo rat at Pecho, which Gambs (1989) and Gambs and Nelson (1990) considered a serious threat. Likewise, Botta's pocket gophers Thomomys bottae were in and near the outdoor enclosure for captive Morro Bay kangaroo rats at Pecho, which Gambs and Nelson (1989) also considered a serious threat. However, Fitch (1948) observed D. heermanni using burrows of California ground squirrels and also “probable” gopher burrows, which suggests the interactions may not always be competitive or unfavorable for D. heermanni. California ground squirrels and Botta's pocket gophers have limited and patchy distributions in and near Los Osos and are likely not a range-wide threat to the Morro Bay kangaroo rat.

Gambs (1986b) reported Morro Bay kangaroo rats as denser in the early stages of coastal dune scrub, and other species of small mammals as less dense or absent. As coastal dune scrub progressively matures, the small-mammal community changes and the result is an increase in its diversity, which likely places Morro Bay kangaroo rats in competition with other species of rodents (USFWS 1982; Gambs and Holland 1988; Gambs and Nelson 1990). Exploitative competition for seed resources occurs among desert granivores (e.g., Brown and Munger 1985), and there appears to be a lack of species-specific preference for particular seed types, which together suggest that extreme competition occurs in diverse granivore communities (Kelrick et al. 1986). In addition, spatial and temporal partitioning of the habitat occurs among desert granivores, and the kangaroo rats generally forage farthest from cover (e.g., Brown et al. 1979; Longland and Price 1991). Thus, the negative effect of competition on Morro Bay kangaroo rats is generally expected to increase with progressive changes in vegetation because less open space will be available to solely exploit, proportionally more of the remaining open space will be near cover, and more species will be foraging near cover. Therefore, competition with other rodents has been inferred to increase with plant community succession (USFWS 1982; Gambs and Holland 1988; Gambs and Nelson 1990) and has likely contributed to the decline of the Morro Bay kangaroo rat.

The USFWS (2011) identified invasive plant species, in particular perennial veldt grass Ehrharta calycina, as a new threat to the Morro Bay kangaroo rat. This exotic species now occurs throughout the geographic range of the Morro Bay kangaroo rat, and it comprises dense stands at Junior High/Santa Ysabel, Pecho, Hazard, and Buckskin. We consider perennial veldt grass a threat because at high density it eliminates open spaces.

The USFWS (2011) identified stochastic events as a threat to the Morro Bay kangaroo rat. Species with small populations are vulnerable to extinction by stochastic events (Shaffer 1981; Ricklefs 2008). This means that environmental or demographic chance or randomness can cause the population size to fluctuate, and in small populations the fluctuations are more likely to include zero. Therefore, stochastic events are a threat, and we suspect they have contributed to the decline of the Morro Bay kangaroo rat, although we cannot provide evidence.

The USFWS (2011) identified climate change as a new threat. The year 2015 was the warmest since record-keeping began in 1880, and most of the warming has occurred in the past 35 y, with 15 of the 16 warmest years occurring since 2001 (Brown et al. 2016). In particular, California is becoming hotter and drier. The 3-y period from 2012 to 2014 was the hottest and driest in California in the past 100 y (Mann and Gleick 2015), and it was the most severe drought in California in the past 1,200 y (Griffin and Anchukaitis 2014). Species with small geographic ranges are more vulnerable to climate change (e.g., Foden et al. 2013), and of particular concern are associated extreme weather events (e.g., severe drought, harsh winter) that could also affect the food plants. Therefore, climate change is likely a threat to the Morro Bay kangaroo rat, especially because the subspecies may be persisting in small and isolated colonies.

The Morro Bay kangaroo rat inhabits predominantly early and midseral stages of coastal dune scrub on sandy soil in and near Los Osos in the vicinity of Morro Bay. In 2016, only pockets of this habitat remain, with optimal habitat (early seral stages of coastal dune scrub) comprising an estimated 1% of the historical geographic range. In consideration of the vast loss and fragmentation of its habitat, along with the continuing and pervasive threats, the Morro Bay kangaroo rat is clearly conservation-reliant (sensu Scott et al. 2010). We believe that without urgent human intervention, the Morro Bay kangaroo rat will soon become extinct if it is not already. Using controlled fire to restore the mature vegetation to early stages would likely benefit the Morro Bay kangaroo rat (e.g., Stewart and Roest 1960; Quinn 1979; Fellers 1994; Sauvajot 1995; Potter et al. 2010; Borchert and Borchert 2013), if it still exists. In addition, this benefit could potentially extend to other co-occurring species including the federally endangered Indian Knob mountainbalm Eriodictyon altissimum (USFWS 1994; Keil 1997; USFWS 1998, 2013b), the federally threatened Morro manzanita Arctostaphylos morroensis (USFWS 1994, 1998, 2013a; Wells 1962; Odion and Tyler 2002), and the federally endangered Morro shoulderband snail Helminthoglypta walkeriana (USFWS 1994, 1998, 2006). However, a proposed prescribed burn was denied by the USFWS in 2013 because of the likely mortality of an unknown number of Morro shoulderband snails and the uncertainty of other effects. This illustrates the challenge and difficulty of managing a landscape with multiple species that are listed (legally protected) under the U.S. Endangered Species Act (ESA 1973, as amended).

We recommend that searches continue for the Morro Bay kangaroo rat, in particular at Pecho South and Junior High/Santa Ysabel, where we observed potential signs of the Morro Bay kangaroo rat in 2011. However, rather than traditional trapping methods such as we used during our 2008–2012 search (e.g., USFWS 2012), we recommend 1) using scent-detection dogs (Brehme et al. 2010; Duggan et al. 2011) trained on the Lompoc kangaroo rat and 2) using cameras and bait stations at sites with potential signs of the Morro Bay kangaroo rat. These methods may be more effective at detecting a small, nocturnal burrowing rodent that is possibly persisting at extremely low densities in a few isolated colonies. In addition, restoring the mature vegetation to early stages of coastal dune scrub, along with removing the densest stands of perennial veldt grass, may enable any persisting Morro Bay kangaroo rats to increase in numbers. Therefore, we recommend 3) that habitat restoration be conducted by prescribed burns and other means, in particular at Pecho South and Junior High/Santa Ysabel. Also, we recommend 4) that efforts continue toward gaining permission to survey on the four private properties with potential habitat: the main Buckskin property (26.3 ha) and the property immediately northwest (35.318454°, −120.815472°; 16.0 ha); one property (35.320744°, −120.819658°; 5.7 ha) south of Junior High/Santa Ysabel; and one property (35.315682°, −120.839664°; 21.9 ha) in Baywood Park. The status of the Morro Bay kangaroo rat on these four private properties cannot be determined until surveys are conducted. In addition, if any Morro Bay kangaroo rats are found, we recommend 5) that some be used to establish a captive breeding program at a zoo in California as a safeguard against extinction in the wild (McCleery et al. 2014). The breeding efforts from 1976 to 1993 were the first attempted with D. heermanni, and several relevant studies with this species have since been published, including on mating behavior (Thompson et al. 1995; Yoerg 1999; Shier and Randall 2004), reproduction and captive breeding (Roest 1991; Yoerg and Shier 1997), and husbandry (Thompson et al. 1995). In particular, Yoerg and Shier (2000) demonstrated that D. heermanni can be bred successfully in captivity. Some recent captive breeding programs for endangered mammals have achieved substantial success, for example for the federally endangered black-footed ferret Mustela nigripes (USFWS 1967; Santymire et al. 2014), and many International Union for the Conservation of Nature Red List species classified as extinct in the wild are currently maintained by captive breeding for subsequent reintroductions (Gusset and Dick 2012). Further, we recommend 6) that USFWS recognize the Morro Bay kangaroo rat as conservation-reliant, with integration of this concept in natural resource and landscape management in the Baywood Fine Sand ecosystem. Conserving the Morro Bay kangaroo rat and its habitat will help to conserve multiple other animal and plant species also in the ecosystem, and particularly those associated with the early and midseral stages of coastal dune scrub. Finally, and with the highest priority, we recommend 7) that USFWS and the relevant state agencies (California State Parks, and California Department of Fish and Wildlife) develop and implement a comprehensive management plan for the multiple listed species in the Baywood Fine Sand ecosystem, which includes the Morro Bay kangaroo rat. We believe that without urgent human intervention, the Morro Bay kangaroo rat will soon become extinct if it is not already.

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We thank the following persons for their assistance: Lisa Andreano, Vince Cicero, and Michael Walgren of California State Parks; Scott Osborn and Robert Stafford of the California Department of Fish and Wildlife; and Carl Benz, Angela Chapman, Douglass Cooper, Chris Dellith, Christopher Diel, Danielle Dillard, Roger Gambs, William Miller, Chad Mitcham, Michaela Koenig, David Pereksta, Roger Root, Martin Ruane, Michael Stiles, William Tietje, Juliana Trunzo, Julie Vanderwier, Kirk Waln, and Christina Williams. We thank the following landowners for permission to search on their private properties: Barry Branin, William Lee, Natasha Lilly, Theodore Lilly, Marla Morrissey, El Morro Church of the Nazarene, Larry O'Brian, Charles Piccuta, Jeena Piccuta, Jeannie Rocha, Mabel Silva, Tony Silva, and John Tonini. Without the contributions of all these persons, this project could not have been accomplished. Finally, we acknowledge the Associate Editor and the three reviewers for their efforts and services that have substantially improved this paper.

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