Why we need to publish a rule.This is a final rule to listArctostaphylos franciscanaas an endangered species under the Endangered Species Act. Under the Act, if a species is determined to be an endangered or threatened species we are required to promptly publish in theFederal Registerand make a determination on our proposal within one year. We were petitioned in 2010 to listA. franciscanaas an endangered or threatened species. We determined in our 12-month finding that listing was warranted, and we proposed to list the species as an endangered species in September 2001. This final rule constitutes our final determination for this species as required by the Act.
The basis for our action.Under the Endangered Species Act, we are required to determine whether a species is endangered or threatened because of any of the following factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence. We reviewed all available scientific and commercial information pertaining to these factors in our status review of the species and determined that the species was limited to one plant remaining in the wild. We proposed that the species was endangered due to threats in the five factors, as follows. The primary threat toArctostaphylos franciscanais from the present or threatened destruction, modification, or curtailment of the species' habitat or range. All original occupied habitat of the species has been lost, and its current range has been reduced to a single location that supports a singleA. franciscanaplant. Furthermore, limited suitable habitat remains available to support a viable population of the species. The remaining plant is vulnerable to overcollection or damage if visitors harvest cuttings or seeds. Sudden oak death, which is caused by the pathogenPhytophthora cinnamomi,and infections caused by otherPhytophthoraspecies are serious threats toArctostaphylos franciscanabecause only one plant occurs in the wild and the diseases are easily spread. Predation is an ongoing but lesser threat. Additional threats include climate change, altered fire regime, soil compaction from visitor use, vandalism, loss of genetic diversity, loss of pollinators, stochastic events, effects of small population size, and hybridization. In the proposed rule, we considered these threats to be significant and ongoing, but we did not find that we had sufficient informationto determine critical habitat at the time. In this final rule, we utilize public comments and peer review to inform our final determination, as required under the Act.
Peer review and public comments.In this final rule, we present and respond to peer reviewer and public comments. We obtained peer reviews from knowledgeable individuals with the scientific expertise to review our technical assumptions, analysis, adherence to regulations, and whether or not we had used the best available information. These peer reviewers generally concurred with our methods and conclusions, and they provided additional information, clarifications, and suggestions to improve this final rule. In particular, peer reviewers provided information on the physical and biological features required by the species, and on locations of remnant natural habitat that retained these features, suggesting that proposal of critical habitat would be determinable and prudent. Accordingly, a proposed rule to designate critical habitat is being published concurrently with this final rule to list the species as endangered.
It is our intent to discuss only those topics directly relevant to the listing ofArctostaphylos franciscanaunder the Act (16 U.S.C. 1531et seq.) in this final rule. For further information on the species' biology and habitat, population abundance and trend, distribution, demographic features, habitat use and conditions, threats, and conservation measures, please see the September 8, 2011, proposed listing for the species (76 FR 55623) published in theFederal Register, or the Recovery Plan for Coastal Plants of the Northern San Francisco Peninsula (Service 2003). These documents are available from the Environmental Conservation Online System (ECOS) (http://ecos.fws.gov/ecos), the Sacramento Fish and Wildlife Office Web site (http://www.fws.gov/sacramento/), or from the Federal eRulemaking Portal (http://www.regulations.gov).
In our proposed listing rule forArctostaphylos franciscana(76 FR 55623; September 8, 2011), we stated that we believed that critical habitat was not determinable at the time of the proposal due to a lack of knowledge of what physical or biological features were essential to the conservation of the species, or what other areas outside the site that is currently occupied may be essential for the conservation of the species. Subsequently, we requested information from the public during the public comment period and solicited information from peer reviewers on whether the determination of critical habitat was prudent and determinable. We also asked for information about the physical or biological features that are essential to the conservation of the species and what areas contained those features or were otherwise essential for the conservation of the species. Based on the information we received on the physical or biological features forA. franciscana,and information on areas otherwise essential for the species, we have determined that the designation of critical habitat is prudent and determinable. We are therefore proposing critical habitat elsewhere in today'sFederal Register. For more information regarding our determination to designate critical habitat please see our response to comments below and the proposed rule to designate critical habitat forA. franciscanapublished in the Proposed Rules section of today'sFederal Register.
Arctostaphylos franciscanais a low, spreading-to-ascending, evergreen shrub in the heath family (Ericaceae) that may reach 0.6 to 0.9 meters (m) (2 to 3 feet (ft)) in height when mature (Chasseet al.2009, p. 5). Its leaves are about 1.5 to 2 centimeters (cm) (0.6 to 0.8 inches (in)) long, are isofacial (have the same type of surface on both sides), and are oblanceolate (longer than they are wide and wider towards the tip) (Eastwood 1905, p. 201; Chasseet al.2009, p. 39). Its mahogany brown fruits are about 6 to 8 millimeters (mm) (0.24 to 0.32 in) wide, while its urn-shaped flowers measure about 5 to 7 mm (0.2 to 0.28 in) long (Wallace 1993, p. 552; Service 2003, p. 57).
A closely related species,Arctostaphylos hookerissp.ravenii(Presidio or Raven's manzanita), which was federally listed as endangered on October 26, 1979 (44 FR 61909), looks similar but has a growth habit that is more prostrate, leaves that are more rounded, fruits that are smaller and less red in color, and flowers that are smaller and more spherical (Service 2003, pp. 55, 57).Arctostaphylos hookerissp.raveniihas recently undergone a taxonomic revision toA. montanassp.ravenii,and we will be referring to the listed species by this name throughout this rule (see Genetics and Taxonomy section below). Another somewhat similar appearing species, though not as closely related, isA. uva-ursi(bearberry), which can be distinguished by its lack of isofacial leaves (Chasseet al.2009, p. 39).
In the wild,Arctostaphylos franciscanais an obligate-seeding species (it reproduces primarily from seed rather than from burls) (Vasey 2010, p. 1).Arctostaphylos(manzanita) species are members of the chaparral plant community, which have a variety of triggers for seed germination including heat, smoke, and light (Keeley 1987, p. 434).Arctostaphylosspecies have germinated after being exposed to charate (ground charred wood) (Keeley 1987, pp. 435, 440), which suggests that fire or conditions that simulate fire stimulate germination of the seeds.
Based on work with other species ofArctostaphylos,the establishment of successful populations ofA. franciscanamay require the presence of a pollinator community (primarily bumblebees (Bombusspp.) but also other insects), a fruit dispersal community (primarily rodents), and a mutually beneficial soil mycorrhizal fungi community (see Historical Distribution and Habitat below) (Parker 2011, p. 1). The seeds ofArctostaphylosare dispersed primarily by rodents that consume the fruits, but also by other mammals, including coyotes (Canis latrans) and foxes (T. Parker 2011, pers. comm.; Vasey 2011a, p. 1). Seed-eating animals such as coyotes, gray foxes (Urocyon cinereoargenteus), red foxes (Vulpes vulpes), raccoons (Procyon lotor), California quail (Callipepla californica), and rodents such as the California vole (Microtus californicus) are known to occur on the Presidio of San Francisco (Presidio), a unit of the National Park System, on the San Francisco peninsula whereA. franciscanais found (National Park Service (NPS) 2012). Animals such as coyotes and foxes eat theArctostaphylosfruit and may travel long distances before depositing their scat. Any undigested fruit left in the scat can then be harvested by rodents and either eaten or buried. Parker (2010b, p. 1) found that 70 percent of the fruits buried by rodents were located deeper than 2 cm (0.78 in), which is the maximum soil depth at which seeds are typically killed by wildfire. Seed has been removed from the wild plant, and, although it has not been directly observed, California voles have been trapped near the wild plant and are likely responsible for the seed harvesting (Carlen 2012, p. 1; Estelle 2012d, p. 1).
Listed Entity Analysis
TheArctostaphylos franciscanaplants that exist in cultivation fall into three categories: (1) Cuttings and rooted specimens collected from the Laurel Hill Cemetery and transplanted to various managed botanical gardens inSan Francisco, Berkeley, and Claremont prior to 1947; (2) specimens currently propagated in greenhouses from cuttings and layers taken from the wild plant in 2010; and (3) specimens, some of which may be of unknown origin, sold in the nursery trade or transplanted into home gardens. We consider the single wild plant and plants identified in (1) and (2) above to be the listed entity under the Act. Our rationale for not including plants identified in item (3) above is outlined below.
TheArctostaphylos franciscanaplants found in botanical gardens may represent from one to six genetically distinct plants other than the single wild plant (Chasseet al.2009, p. 7; Chasse 2011a, p. 1; Chasse 2011b, p. 1; Vasey 2011b, pp. 2, 3), and cuttings from those plants may contribute genetic material to efforts to expand the number of wild plants. The botanical garden plants are not considered part of the wild population and, therefore, are not considered in the assessment of species status, although they will be considered to be listed when this final rule becomes effective (see theDATESsection above). The cuttings and layers collected from the wild plant currently propagated in greenhouses are being considered in the assessment of the species' status. These cuttings from the wild plant will be planted withA. franciscanaspecimens propagated in botanical gardens to establish additional populations of the species. We have concluded that the third category of plants, those cultivated for private or commercial uses, will not aid in the conservation or recovery of the species in the wild because some cultivated plants may be hybrids and bred for landscape use and thus offer minimal contribution to conservation.
In October 2009, an ecologist identified a plant growing in a concrete-bound median strip along Doyle Drive in the Presidio asArctostaphylos franciscana(Chasseet al.2009, pp. 3, 4; Gluesenkamp 2010, p. 7). The plant's location was directly in the footprint of a roadway improvement project designed to upgrade the seismic and structural integrity of the south access to the Golden Gate Bridge (California Department of Transportation (Caltrans)et al.2009, p. 1; Chasseet al.2009, p. 10).
Several agencies, including the Service, established a Memorandum of Agreement (MOA) and conservation plan for the species (seePrevious Federal Actionssection below) (Caltranset al.2009). The conservation partners concluded that leaving the plant undisturbed at its original site would compromise public safety and cultural resources by the potential curtailment or redesign of the roadway improvement project (Chasseet al.2009, pp. 9, 10).
The conservation plan evaluated potential translocation sites, established procedures for preparation of the new site and for the translocation itself, and called for management and monitoring (both short- and long-term) of the translocated plant, with the goal of eventually establishing self-sustaining populations of the species in the wild (Chasseet al.2009, pp. 23-27, 29-30). Following recommendations in the conservation plan, theArctostaphylos franciscanaplant was moved successfully to a new site within the Presidio in January 2010. The Presidio site was chosen after careful consideration of its appropriate soil type and the management and monitoring capabilities of the NPS and the Presidio Trust. Subsequent monitoring reports indicate the translocated plant continues to do well at its new location (Yam 2010, pp. 1, 3-14; Young 2010a, p. 1; Young 2012, p. 1).
Historical Distribution and Habitat
Known historical occurrences and collections ofArctostaphylos franciscanaare from serpentine maritime chaparral, a plant community dominated byArctostaphylosandCeanothus(California lilac) species, on the San Francisco peninsula. This area is part of a region that Willis Linn Jepson named the Franciscan Area, one of 10 areas he considered to have the highest concentration of endemic plant species in California (Jepson 1925, pp. 11-14). An endemic species is one that is native to, and restricted to, a particular geographical area. Native habitats on the San Francisco peninsula have been largely converted to urban areas of the City of San Francisco, and habitat that might have supportedA. franciscanais now mostly lost to development or habitat conversion from the introduction of nonnative plant species (Chasse 2010, p. 2; Gluesenkamp 2010, p. 7; Chasse 2011c, p. 1).
Chasse (2009, pp. 6, 7) has noted that information on the plant community that historically includedArctostaphylos franciscanais largely missing from the literature. Early records describe the species as growing “on rocky ground” (Eastwood 1905, p. 202), on “bare, stony bluff on Laurel Hill Cemetary [sic]” (Brandegee 1908), and with coast live oak (Quercus agrifolia), coast blue blossom (Ceanothus thyrsiflorus), and coyote brush (Baccharis pilularis) (Wieslander 1938).Arctostaphylos franciscanawas also observed “forming flat masses over serpentine outcroppings and humus-filled gravel and flopping down over the sides of gray and chrome rocks.Ericameria, Baccharis,Ferns, Buckwheats, and Golden Yarrow grow among it; and over it stand Toyons and Live Oaks.” Additionally,A. montanassp.raveniiwas found at nearly allA. franciscanalocations. These observations, along with the geology and climate of historical sites, indicate that the species' historical community likely consisted of a mosaic of coastal scrub, barren serpentine maritime chaparral, perennial grassland, and occasional woodlands of coast live oak and toyon shrubs and small trees (Chasse 2009, pp. 6, 7).
Arctostaphylos franciscanais considered to be endemic to the San Francisco peninsula, and historically occurred in areas with serpentine soils, bedrock outcrops, greenstone, and mixed Franciscan rock, typically growing in mixed populations withA. montanassp.ravenii(Service 2003, pp. 95, 96; Chasseet al.2009, p. 6). The Doyle DriveA. franciscanasite was comprised of disturbed soil over serpentinite (Chasseet al.2009, p. 3). Serpentine soil restricts the growth of many plants due to its high nickel and magnesium concentrations, and thus tends to support unique plant communities (Brooks 1987, pp. 19, 53; Service 2003, p. 16) because relatively few plant species can tolerate such soil conditions. These conditions generally result in semibarren soil and a lack of competing plants, which benefits serpentine-tolerant plants (Bakker 1984, p. 79) such asA. franciscana.
The coastal upland habitat ofArctostaphylos franciscanais influenced by cool, humid conditions and frequent summer fog. Summer fog is important to upland coastal vegetation and partly determines the distribution of coastal species (Johnstone and Dawson 2010, p. 4533). Besides serpentine soil and cool air temperatures (Parker 2010c, p. 1), summer fog is one of the primary habitat requirements forA. franciscana(Vasey 2010, p. 1). Summer fog results from two phenomena upwelling of cold coastal ocean water and temperature inversion of hot air flowing toward the ocean over a cool humid marine air layer below (Johnstone and Dawson 2010, p. 4533; Vasey 2010, p. 1). Fog reduces sunlight and air temperature, and raises humidity. Summer fog provides a source of water for plants, includingArctostaphylosspecies, by condensing in the plant canopy and falling directly as water to the soilwhere it is taken up by the plant's roots or directly by leaves (Johnstone and Dawson 2010, p. 4533; Vasey 2010, p. 1).
Historically, the maritime serpentine chaparral plant community, of whichArctostaphylos franciscanais a part, may have been present in the southeastern portion of the San Francisco area (for example, Potrero Hill and Bayview Hill), but the cumulative effects of burning by native Americans, grazing during the Spanish/Mexican period, and later more grazing and firewood gathering during the U.S. military period may have converted the maritime chaparral to grassland or depauperate coastal scrub (Chasse 2010, p. 2). Prior to 1947,A. franciscanawas known from three locations: the Masonic and Laurel Hill Cemeteries in San Francisco's Richmond District, and Mount Davidson in south-central San Francisco (Service 2003, pp. 16, 62, 95; Chasseet al.2009, p. 4). Unconfirmed sightings were also noted at a possible fourth location near Laguna and Haight Streets (Chasse 2012, p. 1). By 1947, the Masonic and Laurel Hill Cemetery sites were removed and the grounds were destroyed in preparation for commercial and urban development (Chasseet al.2009, p. 7). The Mount Davidson and Laguna and Haight Streets locations were lost to urbanization as well. Until October 2009,A. franciscanahad not been recorded in the wild since 1947 (Chasseet al.2009, pp. 3, 7), although no systematic surveys are known to have taken place to search for potential remaining individuals (Chasse 2010, p. 1).
Cultivated Arctostaphylos franciscana
Between 1930 and 1947, prior to the loss of the wild plants, botanists collected cuttings and rooted specimens from confirmed wildArctostaphylos franciscanaplants, possibly representing between one and six distinct genotypes, and propagated them in botanical gardens (Chasseet al.2009, p. 7; Chasse 2011a, p. 1; Chasse 2011b, p. 1; Service 2003, p. 96; Vasey 2011b, p. 2). The number of distinct genotypes depends on whether the botanical garden specimens were started from cuttings of the same individual (which would mean multiple plants have identical genotypes (genetic constitutions)), or whether each specimen originated from a separate plant (in which case they would have different genotypes) (Chasse 2011a, p. 1; Chasse 2011b, p. 1; Vasey 2011b, pp. 2, 3).
Modern collections of this plant at East Bay Regional Park District's Botanical Garden at Tilden Regional Park, San Francisco Botanical Garden (formerly known as Strybing Arboretum), Rancho Santa Ana Botanic Garden, Claremont, and University of California (UC) Berkeley Botanical Garden include some of the original specimens from Laurel Hill, as well as specimens propagated vegetatively after the species was thought to be extinct in the wild (Chasseet al.2009, pp. 6-8). Accession records for the botanical garden specimens indicate that some specimens collected and planted prior to 1947 did not survive and others are duplicates of original collections, leaving possibly only two specimens confirmed to have been original plants transplanted from Laurel Hill (Chasse 2011b, p. 1; Smisko 2012, p. 1). Further genetic work will verify whether plants with differing morphological features prove to be additionalArctostaphylos franciscanaindividuals. Although some of the botanical garden specimens may have different genotypes, which is generally the result of sexual reproduction (sprouting from seed) rather than clonal reproduction (vegetative reproduction from cuttings or plant parts other than seeds), all of the botanical garden specimens are considered to beA. franciscanauntil further genetic work can be conducted. The number of existing distinct genotypes cannot currently be determined because a suitable genetic sampling technique has not yet been developed (Chasse 2011a, p. 1).
Under the conservation plan for the relocated wild plant, cuttings and rooted specimens from the wild plant are also being cultivated. Cuttings from the plant, both nonrooted stems and layering stems (stems that have rooted at their leaf nodes), were taken for vegetative propagation prior to translocation of theArctostaphylos franciscanaplant in January 2010 (Chasseet al.2009, pp. 10-16, 40-42, Young 2010a, p. 1). This material was distributed to seven locations, including UC Berkeley Botanic Garden, Regional Parks Botanic Garden, UC Santa Cruz Botanical Garden, San Francisco Botanical Garden, Cal Flora Nursery, Presidio Nursery, and the Presidio Trust Forester (Young 2011, p. 1 of attachment 2). As of February 2012, 351 clones continue to survive at these locations (Young 2012, p. 1). A total of 1,346A. franciscanaseeds were collected from the plant in 2009, before it was transplanted; an estimated 2,100 seeds were collected in July and August 2010; and 19 seeds were collected in 2011 (Frey 2010, p. 1; Young 2010a, p. 1; Young 2012, p. 1). The numbers of seeds collected are estimates based on weight of seed collected (Laskowski 2012, p. 1). No attempts have yet been made to germinateA. franciscanaseeds (Young 2012, p. 1). Two rootedA. franciscanacuttings were outplanted to managed sites at the UC Santa Cruz Arboretum in January 2011 (Kriegar 2011, unpaginated). The conservation plan calls for eventual propagation of seeds (including any seeds collected from the soil around the plant's original location), and for genetic testing of resulting plants. Seeds fertilized in the wild could result from cross-pollination from another individualArctostaphylos franciscanaor a closely related species to produce a genetically unique individual (Chasseet al.2009, p. 13). Additionally, because the roots of mostArctostaphylosindividuals establish a mutually beneficial association with mycorrhizal fungi in the soil, the conservation plan establishes means by which the soil for propagating cuttings and seeds should be inoculated with spores from such fungi (Chasseet al.2009, p. 9). Propagation ofA. franciscanaseed and inoculation of seeds and cuttings by mycorrhizal fungi have not yet occurred. Soil surrounding the wild plant has been examined for presence of a seedbank, but noA. franciscanaseeds have been found (Young 2011, p. 1; Young 2012, p. 1).
Genetics and Taxonomy
At one timeArctostaphylos franciscanaandA. montanassp.raveniiwere considered to be subspecies ofA. hookeri(Hooker's manzanita). However, recent taxonomic revisions have establishedA. montanassp.raveniiandA. franciscanaas separate species. These revisions have been based primarily on genetic comparisons, including the fact thatA. franciscanais diploid whileA. montanassp.raveniiis tetraploid (having four sets of chromosomes, 26 chromosome pairs) (Service 2003, p. 95; Parkeret al.2007, pp. 149, 150; Chasseet al.2009, p. 6). The identification of the wild plant asA. franciscanahas since been confirmed with 95 percent confidence based on morphological characteristics (Chasseet al.2009, pp. 3, 4; Vasey and Parker 2010, pp. 1, 5). Additional tests indicate that the plant is diploid, consistent withA. franciscana(Vasey and Parker 2010, p. 6). Molecular genetic data also indicate that the plant isA. franciscana(Parker 2010a). Based on the best available scientific information, we consider the individual found along Doyle Drive in October 2009 to beA. franciscana(Vasey and Parker 2010, pp. 1, 5-7).
Previous Federal Actions
Arctostaphylos franciscanawas originally proposed for listing as an endangered species under the Act in 1976 (41 FR 24524; June 16, 1976). In 1980, it was included in the list of Category 1 candidates for listing as one of the taxa retaining a high priority for addition to the list, subject to confirmation of extant wild populations. At that time, the species was thought to be extinct in the wild, although it was known to be extant in cultivation (45 FR 82479; December 15, 1980). It was included as a species of concern in the Recovery Plan for Coastal Plants of the Northern San Francisco Peninsula (Service 2003, pp. 95-96).
On December 23, 2009, we received a petition dated December 14, 2009, from Wild Equity Institute, Center for Biological Diversity, and California Native Plant Society requesting thatArctostaphylos franciscanabe listed as endangered on an emergency basis under the Act and that critical habitat be designated. Included in the petition was supporting information regarding the species' taxonomy and ecology, historical and current distribution, present status, and actual and potential causes of decline. On January 26, 2010, we acknowledged the receipt of the petition in a letter to Wild Equity Institute. In that letter, we responded that we had reviewed the information presented in the petition and determined that issuing an emergency rule to temporarily list the species, under section 4(b)(7) of the Act, was not warranted. Our rationale for this determination was that, although only a single plant of this species remained in the wild, the individual had recently been transplanted to a new location on Federal land. Additionally, a conservation plan (Chasseet al.2009, pp. 1-44) and associated MOA (cited herein as Caltranset al.2009) signed by five Federal and State wildlife and land management agencies (conservation partners) successfully addressed the concerns raised by the petition to the extent that none of those concerns constituted an “emergency posing a significant risk to the well-being of the species” (50 CFR 424.20(a)). The Federal agencies participating in the MOA are the NPS and the Service. The State of California is represented by Caltrans and the California Department of Fish and Game (CDFG). The Presidio Trust, a wholly owned government corporation that jointly manages the Presidio with NPS, also participates (71 FR 10608; March 2, 2006).
The transplanted plant is considered to be the single remaining plant in the wild, despite having been transplanted to the Presidio. The original habitat of the plant was threatened by the ongoing redevelopment of Doyle Drive, but that threat was removed by moving the plant to a new location (translocation). Potential immediate threats in the new location, including the danger that the plant might not survive the move and transplantation, were addressed by provisions in the conservation plan for collecting and propagating rooted clones, seeds, and cuttings from the original plant prior to translocation. The conservation plan provides for the long-term propagation, and eventual reestablishment in wild populations, of all remaining genetic lines, including those from the surviving wild plant and from the individuals located in two botanical gardens, which were collected from historically confirmed locations. It also includes long-term monitoring provisions. While these provisions do not remove the need for further review of the species' status, they appear to be effective for protecting the species in the short term.
We published a 90-day finding in theFederal Registeron August 10, 2010 (75 FR 48294), in which we found that the petition presented substantial scientific or commercial information indicating that listing this species may be warranted. On June 14, 2011, Wild Equity Institute filed a complaint that alleged that, given our 90-day finding, the Service had failed to make the required 12-month finding on the petition in a timely manner. On September 8, 2011, we published a combined 12-month finding and proposed rule in theFederal Registerin which we determined that listingArctostaphylos franciscanawas warranted, and, as a result, we proposed to list the species as endangered (76 FR 55623). We also stated that we did not find critical habitat to be determinable at that time, and requested information and comments on whether designation of critical habitat for the species was prudent and determinable.