C-8 Correspondence – Victoria Bogdan Tejeda
From: Victoria Bogdan Tejeda [mailto:[email protected]] Sent: Tuesday, March 21, 2023 3:27 PM
To: CityClerk <[email protected]>
Subject: CBD Sources, 4.2
-EXTERNAL-
Attached:
USGS (2003)
USFS, Southern Sea Otter
Victoria Bogdan Tejeda (she/her)
Staff Attorney, Climate Law Institute
Center for Biological Diversity
1212 Broadway, Suite 800
Oakland, CA 94612
Ph: 510.844.7103 ext. 303
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(Enhydralutrisnereis)
5-YearReview:
Summary andEvaluation
U.S.FishandWildlifeService
VenturaFishandWildlifeOffice
Ventura,California
%-
Photocredit:LilianCarswell/Service
September15,2015
5-YEAR REVIEW
Southern Sea Otter (Enhydra lutris nereis)
I. GENERAL INFORMATION
Purpose of 5-Year Reviews
The U.S. Fish and Wildlife Service (Service) is required by section 4(c)(2) of the Endangered Species Act (Act) to conduct a status review of each listed species at least once every 5 years.
The purpose of a 5-year review is to evaluate whether or not the species’ status has changed since it was listed (or since the most recent 5-year review). Based on the 5-year review, we recommend whether the species should be removed from the list of endangered and threatened species, be changed in status from endangered to threatened, or be changed in status from threatened to endangered. Our original listing of a species as endangered or threatened is based on the existence of threats attributable to one or more of the five threat factors described in section 4(a)(l) of the Act, and we must consider these same five factors in any subsequent consideration of reclassification or delisting of a species. In the 5-year review, we consider the best available scientific and commercial data on the species and focus on new information available since the species was listed or last reviewed. If we recommend a change in listing status based on the results of the 5-year review, we must propose to do so through a separate rule-making process defined in the Act that includes public review and comment.
Species Overview
The sea otter (Enhydra lutris) is the largest member of the family Mustelidae and the smallest species of marine mammal in North America. An important predator in the nearshore marine ecosystems of the North Pacific Ocean, the sea otter is generally considered to be a “keystone” species in these communities. Sea otters exert a strong limiting influence on their prey populations, including a wide variety of nearshore marine invertebrates, and have large-scale community effects disproportionate to their abundance (Estes and Palmisano 1974, Palmisano and Estes 1977, Estes et al. 1978, Duggins 1980, Palmisano 1983, Estes and Harrold 1982).
Sea otters once ranged along the North Pacific rim from the northern Japanese islands to mid- Baja California, Mexico. Following near-extinction as a result of the fur trade during the 18th and 19th centuries, sea otters were legally protected in 1911 by the International fur Seal Treaty (Service 2003). There are three recognized subspecies of sea otters: the Russian or Asian sea otter (E. 1. lutris); the Alaskan or northern sea otter (E. 1. kenyoni); and the California or southern sea otter (E. 1. nereis). The southern sea otter has the most southerly range of the three recognized subspecies and currently occurs in only two areas of California, the mainland coastline from San Mateo County to Santa Barbara County and San Nicolas Island, Ventura County. Historically, 16,000-20,000 sea otters are believed to have resided in the area that is now California (California Department of Fish and Game (CDFG) 1976).’ The population index for 1 As of January 2013, the California Department of fish and Game was renamed the California Department of fish and Wildlife. We refer to that agency by its previous name when the document or action we are referring to was produced or undertaken prior to January 2013.
2 2014is2,944animals(U.S.GeologicalSurvey-Western EcologicalResearchCenter(USGS WERC)2014).
MethodologyUsedtoCompleteThisReview
ThisreviewwaspreparedbytheVenturaFishandWildlifeOffice(VFWO),followingthe Region$guidanceissuedinMarch2008.Weused informationfrom therecovery planforthe southernseaoiler(Service 2003), surveyinformationfromUSGS,peer-reviewedscientific publications, personal communicationswithexperts,andinformationsubmittedinresponseto ourFederalNoticeinitiatingthis5-yearreviewtoupdatethespecies’status andthreats(74FR 12878).This5-yearreviewcontainsupdatedinformationonthespecies’biologyandthreatsand anassessmentofthatinformationcomparedtowhatwasknownatthetimeoflistingorsincethe last 5-yearreview.Wefocusoncurrentthreatstothespeciesthatareattributabletothe Act’s fivelistingfactors.Thereviewsynthesizes this informationtoevaluate thelistingstatusofthe speciesandtoprovideanindicationofitsprogresstowardsrecovery.Finally,basedon this synthesisand thethreatsidentifiedinthefive-factoranalysis,werecommendaprioritized listof conservationactionstobecompletedorinitiatedwithinthenext5years.
ContactInformation
LeadRegionalOffice:MichaelLong,DivisionChief,EndangeredSpecies,Region8, PacificSouthwest;(916)414-6464.
LeadFieldOffice:Lilian Carswell,SouthernSeaOilerRecoveryandMarine ConservationCoordinator,andCatherineDarst,AssistantFieldSupervisor,Listingand Recovery,VenturaFishandWildlifeOffice;($05)644-1766.
FederalRegister(FR)NoticeCitationAnnouncingInitiationof ThisReview Anoticeannouncing initiationofthe5-yearreviewofthistaxonandtheopeningofa60-day periodtoreceiveinformationfromthepublicwaspublishedintheFederalRegisteronMarch25, 2009(74FR12878).Wereceivedthreesubmissionsofinformationduringthe60-day period.
ListingHistory
OriginalListing
FRNotice:42FR2965,January14,1977
EntityListed:thesubspeciesEnhydralutrisnereis
Classification:Threatened
StateListing
EnhydralutrisnereiswaslistedbytheStateofCaliforniaas“frillyprotected”in1913. 3 Associated Rulemakings
On August 11, 1987, we issued a final rule to establish and manage an experimental population of southern sea otters at San Nicolas Island, California, under the authorities and guidelines of Public Law 99-625, 100 Stat. 3500 (1986) (52 FR 29754). In 2012, we determined formally that the translocation program, which included the requirement to maintain a management or “no otter” zone in the Southern California Bight had failed; the experimental population designation was removed upon termination of the translocation program and its respective translocation and management zones by a rulemaking published in the Federal Register on December 19, 2012 (77 FR 75266).
Review History
On September 27, 1982, we requested new and relevant information on the status of the southern sea otter (47 FR 42387). The 5-year review notice generated a large volume of comments, and the comment period was extended to May 1, 1983. Among the comments received was a formal petition from the Friends of the Sea Otter to reclassify the southern sea otter as endangered. After the close of the comment period, Save Our Shellfish, the Greater Los Angeles Council of Divers, and the Pacific Legal Foundation jointly submitted a petition to delist the southern sea otter (the petition was dated February 3, 1984). The information provided with these petitions was considered in the Service’s 5-year review, which was completed in 1984 (Service 1984). The review recognized the deteriorated state of the population (no growth and possibly a decline over the previous 10 years) and additional threats, including encroachment of outer-continental-shelf oil and gas development and incidental drowning in gill and trammel set nets. It also recognized the importance of moving forward with major recovery tasks, including establishment of at least one additional population. However, it did not recommend a change in listing status. Subsequent 5-year reviews were noticed on July 7, 1987 (52 FR 25523), and November 6, 1991 (56 FR 56882). In these reviews, all then-listed species were evaluated simultaneously, with no in-depth assessment of the factors pertaining to the status of each species or its progress towards recovery.
Neither of these reviews resulted in a recommendation to change the status of the species, and no summaries were published. The current review constitutes the first species-specific 5-year review of the southern sea otter since 1984.
Species’ Recovery Priority Number at Start of 5-Year Review The recovery priority number for Enhydra tutris nereis is 9C, based on a 1 C-i 8 ranking system where 1C is the highest-ranked recovery priority and 18 is the lowest (48 FR 43098; September 21, 1983). The number “9” indicates that the taxon is a subspecies that faces a moderate level of threat and has a high potential for recovery. The letter “C” indicates conflict with economic activity.
Recovery Plan
Name of Plan: Final Revised Recovery Plan for the Southern Sea Otter (Enhydra tutris nereis)
Date Approved: February 24, 2003
4 DatesofPreviousRevisions:Thefirstrecoveryplanforthesouthernseaotterwas completedin1982.Adraft revisedrecoveryplanwasmadeavailableforpubliccomment in1991butnever finalizedbecauseofthecontroversyassociatedwithits recommendationthat,intheabsenceofinformationneededtoquantifyparticularrisks, thethresholdfordelistingshouldbeequivalenttothe lowerlimitoftheoptimum sustainablepopulationlevelundertheMarineMammalProtectionActof1972,as amended(MMPA).Asecond reviseddraft,basedonpopulationviabilityanalysisand modeledoilspillriskscenarios,wasreleasedin1996.Becauseofthenatureand magnitudeofpubliccommentsonthe1996draft,athirddraftplanwasreleasedtothe publicin2000. The2000 draftplanwasmadefinalin2003(Service2003).
II.REVIEWANALYSIS
Applicationofthe1996DistinctPopulationSegment(DPS) Policy TheActdefines“species”asincludinganysubspeciesoffishorwildlifeorplants,and any distinctpopulationsegment(DP$)ofanyspeciesofvertebratewildlife.The1996Policy RegardingtheRecognitionofDistinctVertebratePopulationSegmentsundertheAct(61FR 4722;February7,1996)clarifiestheinterpretationofthephrase“distinct populationsegment” forthepurposesoflisting,delisting,andreclassifyingspecies undertheAct.
The1977listingofthesouthernseaotterwas atthesubspecieslevel(42FR2965;January14, 1977).Publishedanalysessubsequenttothe1977listingsupportthistaxonomicstatus(Wilsonet al.1991,Sanchez1992,Croninetal.1996,Larsonetal.2002a).Noportionofthesouthernsea otterpopulationhasbeendesignatedaDPS,norhaveweundertakenaformalassessmentof whetheranyportionofthesouthernseaotterpopulationshouldbedesignatedaDPS.
Seaotterpopulationsexhibitahighdegreeofspatialstructureduetothelimitedmobilityof reproductivefemales.Verylimitedmixingofadultandsub-adultfemalesbetweenhabitatareas only50kilometers(km)(31miles(mi))apart occurs,andmanyofthefactorsdrivingpopulation trends,suchasper-capitaprey availabilityandpoint-sourcepollution,can varyatsmallspatial scales(Tinkeretal.2013b).ThetranslocatedSanNicolasIslandpopulationisgeographically distinctfromthemainland population,althoughthegeographicseparationisnotexpected to precludeoccasionalexchangesofanimals(mostlikelyadultmalesorsub-adultanimalsofeither sex)betweenthe twopopulations.Populationgrowthratesandbodyconditiondiffer considerablybetweenSanNicolasIslandandthemainlandrangeduetoecologicalfactorssuch ashigherper-capitapreyabundanceattheisland(Tinkeretal.2008a)and,presumably,the absence orinsignificanceofsharkattacksasamortalityfactorthere.Despitetheseecological differences,thereiscurrentlynoexpectation(orevidence)ofgeneticormorphological discontinuitybetweenthetwopopulationsbecausethetranslocatedanimalsthatfoundedthe islandpopulationweredrawnfromthemainland population.Wewillconsidertheseandother datainanypotentialfutureconsiderationofDPSstatusforaportionofthesouthernseaotter population.
5 Information on the Species and its Status
Species’ Biology and Life History
Southern sea otters reach adult length at approximately 4-6 years of age, with females averaging 118 centimeters (cm) (46.5 inches (in)) and males averaging 127 cm (50 in). Females reach adult weight at around this same age, averaging 21 kilograms (kg) (46 pounds (ibs)), whereas males continue to gain muscle mass until approximately $ years of age, when they weigh, on average, 29 kg (64 lbs) (Tinker et al. 201 3b). Typical life spans are 12-12 years for females and 10-15 years for males (Tinker pers. comm. 2014). However, one female sea otter translocated to San Nicolas Island in 1987 as a juvenile was documented (in 2006) to have reached at least 19 years of age in the wild (USGS unpublished data).
Unlike most other marine mammals, sea otters have little subcutaneous fat. They depend on their clean, dense, water-resistant fur for insulation against the cold. Contamination of the fur by oily substances can destroy its insulating properties and lead to hypothermia and death (Costa and Kooyman 1982). Sea otters also maintain a high level of internal heat production to compensate for their lack of blubber. Consequently, their energetic requirements are high, and they consume an amount of food equivalent to 20—25 percent of their body mass per day (Costa and Kooyman 1982, Kenyon 1969, Morrison et al. 1974). Depending on factors such as habitat, sex, reproductive status, and per-capita prey availability, obtaining this quantity of food requires that sea otters spend, on average, 20—50 percent of the day foraging (Estes et al. 1986, Ralls and Siniff 1990, Staedler 2011, Tinker et al. 2008a, Yeates et a!. 2007, Tinker et al. 2013b).
Mating and pupping occur throughout the year. The gestation period lasts approximately 6 months, consisting of a phase of 2-3 months during which the embryo remains unattached to the uterine wall (delayed implantation) and an implanted phase of 4 months (Jameson and Johnson 1993). A peak period of pupping occurs from October to January, with a secondary peak in March and April (Tinker pers. comm. 2014). Females typically give birth to a single pup, with care provided solely by the female for the approximately 6 months until weaning (Riedman and Estes 1990, Jameson and Johnson 1993). Pup rearing and provisioning impose high energetic costs on females, requiring them to increase foraging effort during this period and leaving them highly susceptible to stressors they may encounter when they come into estrous after weaning, such as parasite infections or aggression by males (Tinker et al. 2013b, Thometz et a!. 2014).
Sea otters rest alone or in groups called “rafts,” which may range from 2 to 20 or more animals, with larger groups more common among males. They tend to prefer areas with surface kelp canopies but will also rest in open water (Riedman and Estes 1990). Sea otters sometimes haul out, although opportunities for hauling out vary spatially and temporally. Hauling out likely reduces thermal flux and thus overall energy requirements; as such, it may be especially important in times of nutritional stress, such as for end-lactation stage females (females that have recently weaned a pup and are entering estrous), which in areas of low per-capita prey abundance may be in poor body condition with minimal energy reserves (Tinker et a!. 2013b). 6 SpatialDistribution
Thefurtradeofthe18thand19th
centuriesreducedtherangeofsea
ottersfromabroadarcalongthe
NorthPacificRimtoanumberof
scatteredremnantcolonies.The
historicalnorthernrangelimitofthe
southernseaotterappearstohave
beenatleastasfarnorthasNewport,
Oregon(Valentineetal.200$) but
probablysouthofNeahBay,
Washington(Larsonetal.2002b).
__________
Thehistoricalsouthernrangelimit
wasPuntaAbreojos,BajaCalifornia.
Allpresent-daysouthernseaotters
descendedfromasmallgroupthat
______
survivedthefurtradenear Bixby
CreekinMontereyCounty,
California,whichnumbered
approximately50animalsin1914
_____________
(Bryant1915).
Sincereceivingprotectionunderthe
InternationalfurSealTreatyin1911,
southernseaottershavegradually
expandednorthwardandsouthwardFigure1.Currentrangeof thesouthernseaotter(USGS-WERC2014) alongthecentralCaliforniacoast.
Dataonrangeextentbyyearthroughthemid-1980saresummarizedbyLubinaandLevin (1988).At thetimeoflistingin1977,thesouthernseaotterrangespanned293linearkm(182 linearmi)ofcoastlinefromSoquelPointnearthecityofSantaCmz,SantaCruzCounty,toPt.
SanLuis,nearAvilaBeach,SanLuisObispoCounty.By2009,themainlandseaotterrange extendedabout523km(325mi), fromtheTunitasCreekmouthnearHalfMoonBay,SanMateo County,toCoalOilPoint,SantaBarbaraCounty.2Sincethattime,therangeends haveretracted, toapproximately2.5km(1.5ml)southeastofPigeonPt.inthenorthand5km(3mi)westof GaviotaStateBeachinthesouth(USGS-WERC2014).Asmall,geographicallydistinct populationresultingfromtranslocationeffortsfrom1988-1990occursatSanNicolasIsland, VenturaCounty(figure1).Southernseaottersareoccasionallyfoundwellbeyondthelimitsof theestablishedrangeandhavebeendocumentedasfarsouthasBaja California,Mexico (Schrammetal.2014).
2The rangelimitshavebeendefinedsince200$as“thepointsfarthestfrom therangecenter(to thenorthandsouth) atwhich5ormoreoffersarecountedwithina10-kmcontiguousstretchofcoastline(asmeasuredalongthe10-rn bathymetriccontour)duringthetwomostrecentspringcensuses,oratwhichthesesamecriteriaweremetinthe previousyear”(USGS-WERC2014).Thisdefinitionhasbeenadoptedtostandardizeannualreportingofrange boundariesinlightofthevariabilityofthelocationoftheterminal,mostlymale,groupsthatusuallymarktheends oftherange.
SeaOtterCensus,Spring2014
SouthernSeaOtterDistribution
—Currentextentofestablishedrange
Otterscountedoutedofrang.
1(srngle)dter
2otters
3offers
L Half MoonBay
PigeonPt
SantaCruz
MontereyBay
MontereySeaside
.
PtSur.
•3—5otters
•5—25ters
RaggedPt.
SanSimeonPt.mbria
Cayucos
MottoBay
4 i
PismoBeach
Gaviota
_________
State
IBeachSantaBarbara
PtConception
02550100Kilomisers
c1’
SanNicolasIsland
7 Sea otter abundance varies across the range, with the highest densities occurring in the center portion (Seaside to Cayucos), where sea otters have been present for the longest. Rocky, kelp- dominated areas that are occupied primarily by females, dependent pups, and territorial males generally maintain the most stable sea otter densities from year to year, whereas sandy and soft- bottom habitats (particularly those in Monterey Bay, Estero Bay, and from Pismo Beach to Pt.
Sal), which are typically occupied by non-territorial males and sub-adult animals of both sexes (and only rarely by adult females and pups), are more variable in abundance from year to year (Tinker et al. 2008b). This variation is driven in part by the long-distance movements and seasonal redistribution of males (Tinker et al. 200$b). The variability of counts at the southern end of the range is also related to seasonal movements: many males migrate to the range peripheries during the winter and early spring, apparently to take advantage of more abundant prey resources, but then return to the range center during the period when most breeding occurs (June to November) in search of estrous females (Jameson 1989, Rails et al. 1996, Tinker et ai. 2008b).
The home ranges of southern sea otters appear to reflect coastal bathymetry and the distribution of resources as well as reproductive strategy. The maximum home range area in Monterey Bay,
45.22 km2 (17.46 mi2), is more than twice that in Big Sur, 20.11 km2 (7.77 mi2), presumably due to the greater travel distances and ultimately prohibitive energy expenditures required to access resources distributed along a narrow coastal shelf, like that off Big Sur, rather than along a wide continental shelf, like that off Monterey (Tinker et al. 2013b). Males exhibit two distinct home range strategies that reflect their reproductive status: territorial males maintain strong site fidelity to a small home range consisting of a single center of use, whereas males that are non-territorial (or territorial only during certain parts ofthe year) move between multiple range centers over a larger total area and over a longer span of coastline (Tinker et al. 2013b). Female home range characteristics fall between those of the two groups of males (Tinker et al. 2013b). Compared to males, most female southern sea otters are more sedentary, with adult females rarely dispersing more than 20 km (12 mi) within a 1-year period (Tinker et al. 2013b), although occasionally females travel longer distances of 40-50 km (25-31 ml) (Tinker et al. 2006a). Juvenile males move further from natal groups than do juvenile females. Aggressive behavior exhibited towards the juvenile males by breeding males may be partially responsible for their more extensive travels (Ralls et al. 1996). Jameson (1998) noted that territorial males exclude juvenile and subordinate males from their territories. However, females move freely across these territories.
Abundance
The estimated historic abundance of sea otters in California is between 16,000 and 20,000 animals (CDfG 1976). According to information submitted by CDFG prior to the subspecies’ listing, the population had grown from its remnant population size of approximately 50 in 1914 (Bryant 1915) to approximately 1,760 animals in 1975 (42 FR 2965).
Data on population size have been gathered for more than 50 years. In 1982, a standardized survey technique was adopted to ensure that subsequent counts were comparable (Estes and Jameson 1988). This survey method involves shore-based censuses of approximately 60 percent of the range, with the remainder surveyed from the air. These surveys are conducted each spring. $
AsrecommendedintheFinalRevised Recovery Planforthe SouthernSeaOtter(Service2003), 3-yearrunning averagesareusedtocharacterizepopulationtrendstodampentheeffectsof anomalous countsin anygivenyear.Because thepopulationatSanNicolasIslandisnolonger consideredanexperimental population(77FR75266,December19,2012),beginningin2013 theSanNicolasIslandcountshave been addedtothoseforthemainlandrangeinordertoarrive ataCalifornia-wideindexofabundance.The3-yearrunningaveragefor 2014is2,944,which represents thecombined3-yearrunningaveragesforthemainlandpopulationandSanNicolas Island,2,881and68,respectively(USGS-WERC2014).
Whereasthetrendinabundanceforthemainlandpopulationoverthepast5yearsremains essentiallyflat,theSanNicolasIslandpopulationhasbeguntogrow rapidly, averaging approximately16percentannuallyoverthepast5years (Figure2)(USGS-WERC2014).
SouthernSeaOtterPopulationTrends
CRange-wideindexofabundance
—Mainlandallotters
——Mainlandindependents
—SanNicolasallotters
—
—SanNicolasindependents
V3000-100z
2700’
-
90 i::
1990 1992 1994 19961998 2000 2002200420062008201020122014 Year
Figure2.TrendsinabundanceofseaottersinCalifornia,basedon3-yearrunningaveragesofrawcounts.Dataare shownforallseaotters(solidline)andindependents(non-pups)only(brokenline)for:the mainlandrange(leftaxis); San NicolasIsland(rightaxis);andtheentirerangeafter2012(leftaxis),whencountswere combinedtocreateanofficial indexofabundance(USGS-WERC2014).
9 Estes et al. (2003) reported that elevated mortality (rather than reduced fecundity) appeared to be the main reason for both sluggish growth and periods of decline in southern sea otters. The 2003 recovery plan emphasized the slow rate of population growth of the southern sea otter population relative to recovering northern sea otter (E. 1. kenyoni) populations and the need to determine the causes of elevated mortality. Although rates of pupping were consistent across populations, the observed maximum population growth rates (calculated for each population as a whole) were very different (Service 2003). The maximum growth rate for the southern sea otter population along the mainland coastline has never been more than 6 percent per year since the early 1 980s, when reliable trend data first became available, although localized sub-populations have been observed to grow at much higher rates immediately after re-colonization (Lafferty and Tinker 2014). In contrast, recovering or translocated populations at Attu Island, southeast Alaska, British Columbia, and Washington state all exhibited growth rates of up to 17 or 20 percent annually during the early stages of recovery (Estes 1990, Jameson and Jeffries 1999, Jameson and Jeffries 2005).
However, recent data and analyses indicate that the emphasis on differential rates of population growth may be misplaced. First, a variety of evidence in recent years supports the conclusion that sea otters throughout much of the central portion of the range (between Seaside and Cayucos) are at or very near carrying capacity of the local environment, which explains the lack of growth in these areas (i.e., additional population growth in this portion of the range is limited by available food resources) (Tinker et al. 2006b, Tinker et al. 2008a, Tinker et al. 2013b, Thometz et al. 2014, Lafferty and Tinker 2014). Second, radio-tagging studies report age- and sex-specific rates of survival and reproduction that are comparable for southern sea otters and northern sea otters, at least when status with respect to carrying capacity is controlled for (Monson et al. 2000, Tinker et al. 2006b). finally, recent modeling analyses indicate that the spatial configuration of available habitat (the long narrow strip of coastal shelf characteristic of California versus the bays, islands, and complex matrices of inland channels characteristic of the habitat in British Columbia and Alaska), combined with the high degree of spatial structure in sea otter populations (due to limited mobility of reproductive females), will result in greatly different expected population growth rates over the long term and may account in large part for the differences in trends between the southern sea otter and northern sea otter populations (Tinker pers. comm. 2013). The same demographic processes frmax, dispersal, rate of range expansion and local equilibrium abundance) that explain the observed rate of recovery in Southeast Alaska are also consistent with the observed rate of recovery in California over the past 75 years (Tinker pers. comm. 2014).
Monitoring of stranding rates and causes of death allows for the detection of new or unexpected sources of mortality that may cause deviations from expected population growth. An effort to document all southern sea otter strandings (live and dead sea otters that wash ashore) has been underway since 196$. While nearly all stranded sea otters are found dead, a small proportion is retrieved alive and is included in the stranding database. Relative mortality (measured by dividing the number of carcasses retrieved in a given year by the number of sea otters counted in the mainland spring count for that same year) indicates that mortality was roughly constant at about 5 percent during the period when the population was growing (from about 1985-1995) but somewhat higher during periods of apparent decline (the early 1980s and from 1996-1999) (Figure 3). Whereas the decline during the early 1 9$Os has been attributed to gill net mortality 10 tEstes1990),thecauseof
the declineduringthelateRelativeNo.ofSeaOtterStrandings 1990shasnotbeen1983-2014
determined(Esteseta!.
2003).Anunusuallyhigh
_____________________________________
numberofstranded12
southernseaotterswas.
10•
recoveredin2003,x8
promptingdeclarationofan.‘6
Unusual MortalityEvent4
undertheMMPAforthe2
periodfromN/lay23to0-IIIIIIIII
October1,2003.CoNt-\c‘b
IntoxicationbydomoicacidNN NNci,fl.
producedbybloomsofthe
____________________________________________________
algaPseudonitzschiaFigure3.Strandingsofsouthernseaoffersrelativetothespringcount,1983- australisappearstohave2014.Theentryfor2011ismissingbecausethespringsurveywasnotcompleted beenanimportantthatyear.Source:USGSunpublisheddata.
contributor(Jessupetal.2004),butnoonecausewasidentifiedasbeing responsible.Relative mortalityhasexceededeven2003levelsinrecentyears.These increasesinrelativemortality appearto beduelargelytoanacceleratingincreaseinsharkbitemortality,particularlyinthe northernandsouthernportionsoftherange(northofSeasideand,mostmarkedly,from Estero BaytoPointConception)(Tinkeretal.2015).Rangewide,theestimatedprobabilitythata strandedseaotterwillbeshark-bittenhasincreasedthreefold,from19percentin1990to61 percentin2013;inthesouthernportionofthe rangethisprobabilityhasincreasedeightfold, from8percentin1990to6$percentin2013(seeTinkeretal.2015fortheassociated95-percent confidencebounds).Whitesharkbitesnowaccountfor morethan50percentofrecovered carcasses.These shark bitesarenon-consumptiveandprobablyserveaninvestigatoryfunction.
Thereasonsfortheincreaseinsharkbitesinareasoftheseaotterrangenotpreviously subjectto highratesofshark-relatedmortalityarenotwellunderstood,buttheymayreflectgrowingwhite shark(Carcharodoncarcharias)numbersand/or changesinwhite sharkbehaviorand distributionassociatedwithincreasingpopulationsofnorthernelephantseals(Mirounga angustirostris)andCaliforniasealions(Zalophuscalifornianus)alongtheCalifornia coastline (Tinkeretal.2015).
HabitatorEcosystem
Seaotterhabitatistypicallydefinedbythe40m(131ft)depthcontour(RiedmanandEstes 1990,Laidreeta!.2001). ThetotalnearshoreareainCalifornia(tothe40-mdepthcontour)is 7,569km2(2,922mi2),ofwhich27percentisrockyhabitat,51percentissandyhabitat,and22 percentismixedhabitat(Laidreetal.2001).Dependingonlocalbathymetry,mostseaottersin Californiaresidewithin2km(1.2ml)ofshore.Southernseaottersforageinbothrocky and soft-sedimentcommunitiesinwaterdepthsgenerally25m(82ft)orless,althoughsomeanimals utilizedeeperwaters. Seaottersoccasionallymakedivesofupto100m(328ft),but thevast majorityoffeedingdives(about95percent)occurinwaterslessthan40m(131ft)indepth (Tinkereta!.2006a).Divedepthanddivepatternvarybysex(malestendtomakedivesgreater 11 than 25 m ($2 fi) more frequently than females), geographic location, and diet specialization (Tinker et al. 2006a, Tinker et aL 2007), as well as age and reproductive status (Tinker et al. 2013b).
The density of southern sea otters within most of the population’s range is most likely related to substrate type. Rocky habitats that are topographically heterogeneous and support kelp forests are likely to support the greatest diversity and abundance of sea otter food resources, which include abalone, rock crabs, sea urchins, kelp crabs, clams, turban snails, mussels, octopus, barnacles, scallops, sea stars, and chitons. Rocky bottom habitats support an average equilibrium density of 4.65-5.62 individuals per km2 (12.05-14.56 individuals per mi2), whereas areas with sandy bottoms and areas of mixed habitat support average equilibrium densities of 0.84-1.32 and
0.44-1.16 individuals per km2 (and 2.18-3.42 and 1.14-3.01 individuals per mi2), respectively (Laidre et al. 2001). Based on these densities and the area consisting of these benthic habitat types, Laidre et al. (2001) estimated the carrying capacity of California as approximately 16,000 animals. The high densities of sea otters observed in Elkhom Slough over recent years (USGS WERC 2014) suggest that estuaries may serve as particularly valuable habitat.
Sea otters’ mobility, forelimb dexterity, and ability to crush large invertebrates, either with their teeth or with rocks, enable them to prey on most invertebrates. The best refuges for invertebrates from predation by sea otters appear to be deep holes and crevices in rocky areas or deep water (e.g., Lowry and Pearse 1973, Hines and Pearse 1982). Shallow water may also provide refuge for invertebrates; southern sea otters failed to find an “unusually dense concentration of Pismo clams (that occupied a very narrow band of habitat in the high intertidal (zone)) ... for several years” (CDFG 1999). The energetic inefficiency of consuming small prey items may protect invertebrates of small size, although specialists preying on small items appear to be able to compensate for low energetic return with increased efficiency (Tinker et al. 2006a, Tinker et al. 2007). Because of their ability to eat large quantities of marine invertebrates, sea otters play a significant role in nearshore marine ecosystems, enhancing not only kelp forests (Estes and Palmisano 1974, Palmisano and Estes 1977, Estes et al. 1978, Duggins 1980, Palmisano 1983, Estes and Harrold 1982) but also seagrass beds (Hughes et al. 2013).
Changes in Taxonomic Classification or Nomenclature
All sea otters of the subspecies E. 1. nereis are descended from a single remnant population.
Southern sea otters are geographically isolated from the other two recognized subspecies of sea otters, E. 1. lutris and E. 1. kenyoni, and have been shown to be distinct from these subspecies in studies of cranial morphology (Wilson et al. 1991) and variation at the molecular level (Sanchez 1992, Cronin et al. 1996, Larson et al. 2002a). No changes in the taxonomic classification of the southern sea otter have been proposed in the published literature since the time of listing.
Genetics
Genetic variation in the southern sea otter is among the lowest observed for any mammal (Aguilar et al. 2002) and is generally most similar to that seen in other species that have undergone known bottlenecks or persistent population declines, such as the northern elephant seal (Mirounga anguistirostris) and Mediterranean monk seal (Monachus monachus) (Larson et 12 a!.2002a,Aguilaretal.200$).Thelossofgeneticvariationinseaotterpopulationsisconsistent withthebottleneckcausedbythedocumentedfurtrade(Larsonetal.2002b,Larsonetal.2012) butmayhavebegunearlier(upto550yearsago),possiblyasaresultofintensivehuntingby nativepeople(Aguilareta!.200$).
Species-SpecificResearchand/orGrant-Supported Activities Extensive researchhasbeenundertakenbyarangeoffederal,state,non-governmental,and academicentities sincethe listingofthesouthernseaotter.Becausethisbodyofworkisvast,we donotprovideafullaccountofit here.However, muchofthe important literatureisreferenced throughoutthisdocument.Inwhatfollows,weprovideasummaryofrecentService-supported federal,state,andotherresearchandactivities directedtowardssouthernseaotterrecovery. federal:ThroughtheScienceSupport Partnership program,inwhichUSGS fundsaredirected topriority Service-researchneeds, the ServiceandUSGSenteredintoamulti-yearcollaborative effortfrom2001-2004toinvestigatethemortalityofsouthernseaotters.Fundingwasdedicated intheamountof$315,000forthisresearch.USGS’sprimaryreportonseaotter mortalitywas publishedinMarine MammalScience (Estesetal.2003).Another$23,500wasawardedin2005 tostudymovementandforagingpatternsofseaottersatSanNicolasIsland.Thisstudy(Tinker etal.2008a)contributedtoourunderstandingoffoodlimitationinthemainlandrange.Forthe pastseveral years, the Servicehasallocatedfundingtosupportrecovery-relatedresearch undertakenbyUSGS.
FY200$-$100K:Partial supportfor“InvestigatingtheConsequencesofCoastal ContaminationandAnthropogenicStressorsforSeaOtter Recovery.”Thepurposeofthis 3-yearstudywastodeterminetheimpactofcontaminantsandpathogensonseaottersin food-limitedareas.
FY 2009-$65K:Partialsupportfor“InvestigatingtheConsequencesofCoastal ContaminationandAnthropogenicStressorsfor SeaOtterRecovery” FY2010-$30K:Partialsupportfor“InvestigatingtheConsequencesofCoastal ContaminationandAnthropogenicStressorsforSeaOtter Recovery” FY2011-$42K:Partialsupportfor“Territoriality,reproductivesuccess,anddispersalin southernseaotters.”Thepurposeofthisresearchwastocharacterizepatternsofmale territoriality,tomeasurethedegreeofpolygamy,toexaminethefactorsaffectingmale reproductivesuccessinsouthernseaotters,andtodescribethepatternsandpredictorsof longdistance dispersal,allofwhicharerelevanttodeterminingequilibriumabundanceof agivenhabitatand therateofre-colonizationofnewhabitat.
FY2012-$42K:Partialsupportformonitoringofseaottermovementsandhabitatuseat thesouthernendoftherange.Thisresearchwaspartofa largerstudyfundedbythe BureauofOceanEnergyandManagement(BOEM).
13 FY 2013 - $3 1.5K: Partial support for “Factors limiting sea otter recovery and range expansion into Santa Barbara Channel.” This research was part of a larger study funded by BOEM.
FY 2014 - $5 OK: Partial support for “Patterns and consequences of shark bite mortality in southern sea otters” ($3 OK) and “Southern sea otter recovery and ecosystem health in Elkhorn Slough” ($20K)
FY 2015 - $30.5K: Partial support for “Southern sea otter recovery and ecosystem health in Elkhom Slough”
State: The Service has also awarded funds under section 6 of the Act and recovery funds for research and assistance related to sea otter recovery conducted by CDFW.
FY 2001 - $40K (Oil Spill Prevention and Response): Section 6 grant for personnel and programs to support recovery of the southern sea otter, including monitoring existing and translocated populations
FY 2002 - $46.2K: Section 6 grant to refine and report, in peer-reviewed literature, the aerial survey methodologies being developed and the influence of differing viewing conditions; to continue to assist with twice-yearly otter population counts; and to continue to retrieve, and conduct postmortem examination of otter carcasses to determine cause of death
FY 2006 - $5 6.5K: Section 6 grant for work in 2007 and 2002 to assist the Service with recovery of the southern sea otter. CDfW stated that they would participate in implementation of the Southern Sea Otter Recovery Plan, primarily by continuing to determine the cause for the high mortality rate of prime-age adults and the extent of the contribution of anthropogenic activities to this rate.
FY 2010 - $20K: CDFW necropsy services in support of the USGS-led study, “Investigating the Consequences of Coastal Contamination and Anthropogenic $tressors for Sea Otter Recovery”
FY 2011 - $30K: CDFW aerial surveys as part of southern sea otter rangewide counts FY 2012 - $1 6.5K: Histopathology contract with University of Illinois to address CDFW necropsy case backlog
FY 2015 - $4.5K: Histopathology contract with University of Illinois to address CDFW necropsy case backlog
Other: The Service has awarded recovery funds to support other efforts related to sea otter research and recovery.
14 FY2010-$5K:Partialsupportforseaottertaggingtechnologyworkshop(MontereyBay Aquarium)
fY2011-$40K:Laborandhardwarerequiredforresearchldevelopmentof5flippertags forseaotterswithelectronicscapableofcollecting solarenergyanddatatodeterminean animal’sposition(DesertStarSystems).ThiscontractwascompletedinFebruary2013. fY2015-$50K:SupportforBeSeaOtterSavvy,aneducationandoutreach programto reduceseaotterdisturbancefromwildlifeviewing activitiesandotherformsofmarine recreation
Five-FactorAnalysis
Thefollowing five-factoranalysis describesandevaluatesthethreats attributabletooneormore ofthefivelisting factorsoutlinedinsection 4(a)(1)oftheAct.For thepurposesofthisanalysis, weconsiderthe current rangeandareasthespeciesmayexpandintooverthe nextseveral years.
FACTORA:Present orThreatenedDestruction,Modification,orCurtailmentofHabitat orRange
Inthelistingrule,weidentifiedthecurtailmentofrangeasanimportant factorinthedesignation ofsouthernseaottersasthreatened,citing the factthatthethen-currentrange encompassedonly about10percentofthesouthernseaotter’shistoricrange(42FR 2965;January14,1977).We alsonotedthatthe“remaining habitatandpopulation[were]potentiallyjeopardizedbyoilspills, andpossiblybypollutionandcompetition”withhumanbeings(42FR2965).Inorderto maintainconsistencywiththelistingrule,inwhichweaddressedoilspillsunder FactorE,we discussnon-oil-spill pollutionandthecurtailmentofrangehereandoilspills andcompetition withhumanbeingsunderFactorE.
Non-Oil-SpillPollution
Non-oil-spill pollutioninthiscontextreferstochemicalandbiologicalcontaminants.The recoveryplanincludesanumberofsub-tasksthatrecommendevaluationoftheeffectsof pollutionunder Task4.3,“Determine concentrationsandpossibleeffectsofdisease,stress,toxic traceelements,andorganochlorinesonseaotters”(Service2003).Significantprogresshasbeen madeonmostofthesesub-tasks.Numerousstudies haveelucidatedthe effectsofasuiteof stressorsonsouthernseaotterhealthanddemographictrends.
Duetoitsproximitytocoastlinesdenselyoccupiedbyhumans,seaotterhabitatispotentially subjecttodegradationresulting fromanthropogenicactivitiesandinputs,includingcontaminants andterrestrialdisease-causingpathogensforwhichtheseaotterisnotanatural host(seeFactor Cforadiscussionofpathogens).Studiesofcontaminantshavedocumentedaccumulationsof dichlorodiphenyltrichloro-ethane(DDT),dichlorodiphenyl-dichloroethylene(DDE)(Bacon 1994,Baconetal.1999),andpolychiorinatedbiphenyls(PCBs)instrandedseaotters(Nakataet al.199$),aswellasthepresenceofbutyltinresidues,whichareknowntobean immunosuppressant(Kannanetat.199$).Kannaneta!.(2006,2007)foundasignificant 15 association between infectious diseases and elevated concentrations of perfluorinated contaminants and polychiorinated biphenyls (PCBs) in the livers of dead stranded sea otters.
While these studies suggest that chemical contaminants may influence susceptibility to disease, confounding factors (such as the mobilization of fat stores shortly before death) prevent any clear conclusions regarding causality. Jessup et al. (2010) found similar levels of persistent organic pollutants in serum from healthy free-ranging sea otters.
Harmful algal or cyanobacterial blooms, which are exacerbated in some cases by anthropogenic inputs of nitrogen or phosphorus into coastal watersheds and the nearshore marine environment (Mos 2001, Kudela et a!. 2008, Vezie et al. 2002), can cause acute, subacute, or chronic effects in exposed sea otters (Kreuder et al. 2003, Miller et al. 20 lOb). Biotoxins released during harmful blooms include domoic acid, which is produced by marine diatoms of the genus Pseudo nitzschia, and microcystin, which is produced by freshwater cyanobacteria of the genus Microcystis. Domoic acid intoxication of sea otters was first reported in 2003 (Kreuder et al. 2003) and has subsequently been associated with cardiac disease (Kreuder et al. 2005).
Microcystin has been implicated as either a primary or contributing cause in the deaths of more than 40 sea otters through 2013 (with the earliest known case occurring in 1999 and the greatest number of cases occurring in 2007) (Miller et al. 2010a, Miller et al. 2013).
Anthropogenic inputs can have profound effects on sea otter health and survival, particularly when combined with other stressors. For instance, exposure to domoic acid may have increased the susceptibility of sea otters to the protozoal parasite Sarcocystis neurona (discussed further under Factor C) and worsened the resulting neurological symptoms during a mortality spike in Morro Bay in 2004 (Miller et al. 20 lOb). The body condition of sea otters in high-density areas of the range (i.e., areas with low per-capita prey availability) appears to strongly influence their susceptibility to additional stressors (Tinker et al. 201 3b).
Because density-dependent resource limitation is the primary factor influencing demographic trends of sea otters in much of the central portion of the mainland range, reducing anthropogenic inputs could reduce cumulative health effects on sea otters, but it would not likely significantly increase survival rates in these high-density areas (Tinker et al. 2013b). For significant population growth to occur, range expansion into areas with higher per-capita prey availability is necessary.
Curtailment of Range
Restrictions on the natural range expansion of sea otters into their historic habitat in southern California waters were put in place in 1987. Ten years after listing the southern sea otter, the Service undertook a translocation program to establish a second population at San Nicolas Island in order to safeguard the species against catastrophic events, such as large oil spiils. Legislation was enacted that specifically authorized the Service to establish a translocation program (Public Law 99-625, November 7, 1986). The legislation required, as a component of the program, the designation of a translocation zone and a management zone. It also specified the regulations to be associated with these zones. The program as implemented included a translocation zone around San Nicolas Island and a management zone, which was to be kept otter-free, that included all other southern California waters (52 FR 29754; August 11, 1987). However, the 16 programwasunsuccessfulasaprimaryrecoveryaction,andmovingseaottersfromthe managementzoneprovedtobemoredifficultthanexpected.3Seaotterswereremovedfromthe managementzoneuntil1993,whenmaintenancewas suspended.By1998,manyfactorsrelated tothestatusofthesouthernseaotterpopulationhadchangedsinceinitiationoftheprogram,and theprogramdidnotappeartobemeetingtherecoveryobjectivesoutlinedforit.We subsequentlyreinitiatedSection7consultationundertheAct.Theresultingbiologicalopinion (Service2000)determinedthatcontainmentofsouthernseaotterswasnotconsistentwiththe requirementoftheActtoavoidjeopardytothe species.In2001,theServiceissuedapolicy statement advisingthe publicthatwewould not captureandremovesouthernseaottersfromthe managementzonependingcompletionofourreevaluationofthetranslocationprogramagainst theestablishedregulatoryfailurecriteriaandundertheNationalEnvironmentalPolicyAct(66 FR6649).
Therecoverypianrecommendsunder Task5thatwe“Evaluatethetranslocationprogramin lightofchangedcircumstancesanddeterminewhetheroneor morefailurecriteriahavebeen met”(Service2003).Wecompletedthisevaluationin2012.Thetranslocationprogram, includingitscomponent translocationandmanagementzones,wasterminatedbyarulemaking publishedintheFederalRegisteronDecember19,2012(77FR75266).Thisdecision retained seaottersatSanNicolasIslandandeliminatedthepossibilitythatthesouthernseaotterrange couldbecurtailedbyresumed enforcementofa“no-otter”managementzone.However,the decisionisthesubjectofpendinglitigation.Anyfutureestablishment(through activemeans ratherthanbynaturalrangeexpansion)ofanew populationofsouthernseaottersoutsideoftheir existingrange,ifundertakenundertheauthorityofPublicLaw99-625,would requirethe establishmentofanewtranslocationzone andotter-freemanagementzone.Thecurrentsouthern seaotterrange—fromapproximatelyPigeonPoint,SanMateo County,inthenorth,toGaviota StateBeach,SantaBarbaraCounty, inthesouth—spansroughly500km(310ml)oflinear coastline(figure4).Asdetailedabove,anadditionaltranslocated populationoccursatSan NicolasIsland.Therangehasincreasedbyapproximately210km(130ml)sincethetimeof listingin1977.Therangeatthattimewasestimatedtobe293km(182ml)(LubinaandLevin 1988).If,asrecentgeneticstudiessuggest,thehistoricnorthernrangelimitisbetweenNewport, Oregon,andNeahBay,Washington(nearthe StraitsofJuandeFuca)(Larsoneta!.2002b, Valentineetal.2008),southernsea ottersoccupyapproximately13percentoftheirhistoric range(assumingseaottersonceoccupiedalloffshoreislandsandSanFranciscoBay,areasthat maynothavebeenincludedinthehistoricrangeestimateat thetimeoflisting).Thecurrent populationindex forsouthernseaotters(2,944)constitutesapproximately19percentofthe carryingcapacityofCaliforniaasdeterminedbyLaidreetal.(2001).Thepopulationindex representsanevensmallerproportionofcarryingcapacityifhistoricsouthernseaotter rangeis viewedinitsentirety,butthisproportionisunknownbecausecarryingcapacityhasnotbeen determinedfor thehistoricsouthernseaotterrange outsideofCalifornia.
ThehistoryoftheprogramisdescribedindetailinAppendixCtotheFinalSupplementalEnvironmentalImpact StatementontheTranslocationofSouthernSeaOffers(Service2012).Itshouldalsobenotedthat,subsequenttothe 1982recoveryplan,therecoverystrategyfundamentally changed,inpartbecauseoftheresultsofthetranslocation program.The2003recoveryplanrecommendsallowingpopulationsizetoincreasebymeansofnaturalrange expansionandrecommendsagainstrelocatingsea otters.
17 columbia WASHINGTON Sou em Sea Otter
_,.,_—_-— Current and Historic Range
Current (2014 Spring Census)
OREGON Historic sea otter range,
subspecies unknown
CALIFORNIA
I
________
San Francisco Bay
Santa Cruz ““N
Pigeon Point Monterey
Monterey Bay
Blxby Creek Gavicta Stite Beach
•Santa Barbara
Point Conception
Se
San Nlcolas,”7
Island MEXICO
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0 ia c
Ml.. us. Fish and Wildlife Service
— — — obeeilrs WMum Fish and Wildlife Office
o 50 100 200 300 400 October2014
Figure 4. Current and historic range of the southern sea otter.
Summary
The southern sea oiler range, though less restricted than at the time of listing, remains curtailed:
only approximately 13 percent of historic range is occupied. The current level of range curtailment reflects the legacy of the fur trade, the slow pace of sea oiler range expansion along a linear coastline, the factors discussed in this section, and other natural and anthropogenic factors discussed under Factors C and E. Because sea oilers in the central portion of the mainland range have reached equilibrium densities (increasing their susceptibility to natural and anthropogenic stressors and limiting the potential for additional population growth in that area), significant growth of the population as a whole will require range expansion into currently unoccupied habitat.
Area of
Detail Map
1$
FACTORB:OverutilizationforCommercial,Recreational,Scientific,orEducational Purposes
OverutilizationforCommercial Purposes
Overutilizationforcommercialpurposes(intentionaldirectlethaltake)wasthecauseofthenear- extinctionofseaottersthroughouttheNorthPacificrim,butstate,federal, andinternationallaws hadprotectedsouthernseaottersfromcommercialexploitationbythetimeoflisting.Therefore, overutilizationforcommercialpurposeswasnotconsideredtobeafactorinthe1977listingrule (42FR2965),norwoulditbecomeafactorifseaottersweredelistedundertheAct,because MMPAandstateprotectionswouldremaininplace.
OverutilizationforRecreational Purposes
Overutilizationforrecreationalpurposes(in theformofrecreational hunting)isnotcurrentlyan issue,norwoulditbecomeanissueifseaottersweredelistedundertheAct,becauseMMPAand stateprotections thatpreventtherecreationalhuntingofsea otterswouldremaininplace.
However,thedisturbanceofseaottersbykayakers,ecotour operators,andphotographers (includingvideographersandfilmmakers)inthe formofcloseapproachesthatdisruptnatural seaotterbehaviorsisoccurringdailythroughoutportionsoftheseaotter’srange, despite existingMMPAprotectionsagainstharassment.Thedisturbanceofrestingseaottersdepletes theirenergy reservesbyincreasingtheirneedformetabolicheatproductionandmaybe especiallyharmfultonutritionallycompromisedsea otters,suchasend-lactation-stagefemales (Yeatesetal.2007,Thometzeta!.2014).Educationandoutreach,when combinedwiththe presenceofon-the-waterstaff,haveproveneffectiveinreducinginstancesofharassment (Gunvalson2011).Todateaneducationlenforcementpresencehasnotbeenavailableinmost cases,butin2015aprogram calledBeSeaOtterSavvywasinitiatedtoimproveeducationand outreach.Itisnotknownwhetherthelevelsofdisturbancethatarecurrently occurringare havingdemographicallysignificanteffects.
OverutilizationforScientificorEducationalPurposes
Overutilizationforscientificoreducationalpurposesisnotcurrentlyanissue,norwouldit becomeanissueifseaottersweredelistedunder theAct,becauseMMPAandStateprotections wouldremaininplace.MMPApermittingrequirementsarediscussedunder FactorDbelow.
Summary
Overutilizationforcommercial,recreational,scientific,oreducationalpurposesisnotcurrently anissue,norwoulditbecomean issueifseaottersweredelistedundertheAct,becauseMMPA andstateprotectionsandpermittingrequirementswould remaininplace.However,repeated disturbanceofseaottersisoccurringdespiteMMPAprotectionsagainstharassment,reflectinga lackofenforcementcapabilityandalackofeducationand outreach.Itisnotknownwhetherthe levelsofharassmentcurrentlyoccurringarehavingdemographicallysignificanteffects. 19 FACTOR C: Disease or Predation
We did not identify disease or predation as serious threats in the listing rule (42 FR 2965).
Since that time, however, disease and white shark attacks have been identified as important mortality factors for southern sea otters. Gerber et al. (2004) found, based on analysis of beach- cast carcasses, that the two causes of death most important for limiting southern sea otter population growth were infectious disease and white shark attacks. We address these issues in turn.
Disease
Detailed necropsies of sea otters conducted from 1992-95 revealed an unexpectedly high occurrence of infectious diseases, including protozoal encephalitis, acanthocephalan peritonitis, coccidioidomycosis, and various bacterial infections (Thomas and Cole 1996). Sub-tasks 4.3.4 and 4.3.5 in the recovery plan recommend additional research into the prevalence and sources of disease agents and stressors to which southern sea otters are exposed (Service 2003). A significant number of studies have since further elucidated the agents, routes of exposure, frequency of occurrence, and effects of these diseases.
Important disease-causing pathogens in sea otters include the protozoal parasites Toxoplasma gondli, which is shed in the feces of both wild and domestic cats (Dubey et al. 1970, Miller et al. 2002, Miller et al. 2004, Miller et al. 200$) and Sarcocystis neurona, which is shed in the feces of opossums (Didelphis virginiana and D. albiventris) (Kreuder et al. 2003, Miller et a!. 20 lOb).
Both of these pathogens can cause severe encephalitis in sea otters. Protozoal encephalitis was identified as the primary cause of death in approximately 23 percent of beach-cast sea otter carcasses examined between 199$ and 2001 (Kreuder et a!. 2003). Encephalitis caused by T gondii in particular has been associated with shark attack and cardiac disease (Kreuder et al. 2003). A seroprevalence analysis updated through 2004 revealed that 52 percent of 305 freshly dead, beach-cast sea otters and 38 percent of 257 live sea otters sampled along the California coast were infected with T. gondii (Conrad et a!. 2005). Infection by acanthocephalan parasites (Proflhicolfls spp.) was reported as the direct or indirect cause of mortality in 13 percent of 162 beach-cast carcasses sampled from 1997-200 1 (Mayer et al. 2003) and the primary cause of death in 16.2 percent of 105 beach-cast carcasses sampled from 1998-200 1 (Kreuder et al. 2003).
As with contaminants and biotoxins, the susceptibility of sea otters to pathogens and parasites appears to be related synergistically to other factors. As noted under Factor A, susceptibility to $arcocystis neurona may be increased by concurrent domoic acid exposure (Miller et al. 2010b).
Nutritional stress is a particularly important factor in this regard. Lower per-capita food availability leads to poorer body condition and greater reliance on sub-optimal prey, which increases exposure and susceptibility to novel disease-causing pathogens (Johnson et a!. 2009, Tinker et al. 2013b).
White Shark Attacks
Shark attacks have long been an important mortality factor for southern sea otters, particularly at the northern end of the mainland range, but a recent dramatic increase in mortality resulting from 20 non-consumptiveshark-bites,especiallyinthesouthern portionofthemainlandrange (from Estero BaytoPoint Conception),appearstobeinhibitingsouthernseaotterrecoveryandmay preventrecoveryfortheforeseeablefutureifitcontinues unabated(Tinkeretal.2015).
Accordingto amodelinganalysis(Tinkereta!.2013a),ifthe rateofshark bitemortality hadnot increasedafter2000,thecurrent populationsizewouldnowbeapproximately3,400,wellabove thedelistingcriterion identifiedintherecoveryplan(Service2003).Ifsharkbitemortality continuesatcurrentlevels(andifotherparameters remainthesame),theprobabilityofreaching thedelistingcriterion basedonpopulationgrowthinthemainlandrangealone,even25years fromnow,isclosetozero (duringthissameperiod,itmayapproach,butisnotexpectedtodip below,theuplistingcriterionof1,850)(Tinkeretal.2013a).
Thereasonsfortheincreaseinshark bitemortalityarenotwellunderstood. Adult whitesharks, whosedietiscomposedprimarilyofmarinemammals,areassociated with pinnipedrookeries, primarilythoseatAftoNuevoandthe SouthFarallonIslands(reviewedinDewareta!.2004).It maybethat increasingpopulationsofelephantseals andCaliforniasealionsareplayingarolein shiftingthedistributionandabundanceofwhitesharks.TheSouthernCaliforniaBightserves primarilyasasummer puppingareaforpregnantfemalesandanurseryground foryoungsharks (reviewedinDewaretal.2004).Because young whitesharksdonoteatmammalsbutrather invertebratesandfish (reviewedinDewaretal.2004),itispossiblethatastheseaotter range expands furtherintosouthernCaliforniawaters,sea otterstherewillhavealowerriskof mortalityfromwhitesharkbitesthanthoseinmostofthecurrentlyestablishedrange.Despite thehighlevelsofshark-relatedmortalityanddecliningseaotternumbersintheportionofthe rangefromCayucostoPointConception,thesmallportionofthemainlandrangesoutheastof Point Conceptionhasexperienceda positivetrendinsea otternumbers overthepastfiveyears (USGS-WERC2014,LaffertyandTinker2014).Sharkbitemortalityisnotcurrentlyknownto beafactorat SanNicolasIsland.
Summary
Infectiousdiseaseisanimportantcauseofdeath forsouthernsea otters.Increasedsusceptibility topathogensandparasitesappearstobetheconsequenceofpoorbodyconditionresulting from lowper-capitapreyavailabilityinportionsofthe rangethatareator nearlocalcarryingcapacity.
Whitesharkattacksarecurrentlythe singlemost importantcauseofmortalityforsouthernsea otters.Shark bitemortalityhaslongbeenanimportantfactoratthenorthernendofthemainland range,butithasincreaseddramaticallyoverthepast10yearsinthe southernportionofthe mainlandrangebetweenCayucosandPoint Conception.
FACTORB:InadequacyofExistingRegulatoryMechanisms
Inthe listingrule,wedeterminedthat existing federalandstatelawswereadequatetoprotect southernseaottersfromdirect takingbutstatedthattheselawsdid not affordsufficienthabitat protection,asituationthatwouldbeimprovedthroughapplicationofsection7ofthe Act(42FR 2965,January14,1977).
The legalprotections thatapplytosouthernseaottersthroughoutmostoftheircurrent rangeare similartothoseineffectatthetimeoflisting.Theregulatory mechanismsthatcurrentlyafford 21 protection to southern sea otters include the Act, the MMPA (under which southern sea otters are considered a “depleted” species), and the fish and Wildlife Code of the State of California, (under which southern sea otters are listed as a “fully protected” mammal (section 4700) and protected marine mammal (section 4500)). New state laws and regulations have been enacted since listing that provide additional protection to sea otters from fisheries-related impacts. The protections afforded to sea otters by federal and state legislation were reduced in the waters south of Point Conception as a result of translocation program criteria specified in Public Law 99-625, which was passed subsequent to the listing, but upon termination of the program in 2012, these provisions ceased to apply (see discussion below).
Endangered Species Act
Since the species’ listing, the Service has analyzed the potential effects of federal projects under section 7(a)(2) of the Act, which requires federal agencies to consult with the Service prior to authorizing, funding, or carrying out activities that may affect listed species. A jeopardy determination is made for a project that is reasonably expected, either directly or indirectly, to appreciably reduce the likelihood of the survival and recovery of a listed species in the wild by reducing its reproduction, numbers, or distribution (50 C.f.R. § 402.02). A non-jeopardy opinion may include reasonable and prudent measures that minimize the impact of incidental take of listed animal species associated with a project. Incidental take refers to taking of listed animal species that results from, but is not the purpose of, carrying out an otherwise lawful activity by a federal agency or applicant (50 C.f.R. § 402.02). In cases where some incidental take is unavoidable, the Service works with the agency to include additional conservation measures to minimize negative impacts. For projects without a federal nexus that may result in incidental take of listed animal species, the Service may issue incidental take permits pursuant to section 10(a)(1)(B). To qualify for an incidental take permit, applicants must develop, fund, and implement a Service-approved habitat conservation plan (HCP) that details measures to minimize and mitigate the impacts of the take of listed species resulting from the project.
Regional HCPs are often coordinated with Natural Community Conservation Plans approved under the State of California’sNatural Community Conservation Planning Act. In order to authorize incidental take of a marine mammal under section 7(a)(2), the Service must first authorize such take under the more protective MMPA (discussed below). As a result, the Service has only rarely authorized incidental take of southern sea otters under section 7(a)(2). To date, the Service has not issued any permits for the incidental take of sea otters under section 10(a)(1)(B). Take for research purposes is permitted under section l0(a)(1)(A) of the Act but also requires authorization under the MMPA. Since the subspecies’ listing, the Service has routinely issued threatened marine mammal research permits.
Marine Mammal Protection Act
The MMPA was enacted on October 21, 1972, and protects all marine mammals. The MMPA prohibits, with certain exceptions, the “take” of marine mammals in U.S. waters and by U.S. citizens on the high seas, and the importation of marine mammals and marine mammal products into the U.S. Congress passed the MMPA of 1972 based on the following findings and policies:
some marine mammal species or stocks may be in danger of extinction or depletion as a result of human activities; these species or stocks must not be permitted to fall below their optimum 22 sustainablepopulationlevel(“depleted”); measuresshouldbetakentoreplenishthesespeciesor stocks;thereisinadequateknowledgeoftheecologyandpopulationdynamics;andmarine mammalshaveproventoberesourcesofgreatinternationalsignificance.TheMMPAwas amended substantiallyin1994toprovidefor:certainexceptionstothetakeprohibitions,suchas forAlaska Nativesubsistenceandpermitsandauthorizationsforscientific research;aprogram toauthorizeandcontrolthetakingofmarinemammalsincidentaltocommercialfishing operations(however,theapplicablesectionoftheMMPA, section118,doesnotgovernthe incidentaltakingofCaliforniasea otters,andthusthetakeofsouthernseaottersincommercial fisheries cannotbeauthorized);thepreparationofstockassessmentsforallmarinemammal stocksinwatersunderU.S.jurisdiction;and studiesofpinniped-fisheryinteractions.Sections 101(a)(5)(A)and(D)oftheMMPA,asamended(16U.S.C.1371(a)(5)(A)and(D)),authorize theSecretaryoftheInteriortoallow,uponrequest,theincidental, butnotintentional, takingof smallnumbersofmarinemammalsbyU.S.citizenswho engagein aspecified activity(other thancommercialfishing)withinaspecified geographicalregion,provided thatwemakecertain findingsandeitherissueregulationsor,ifthetakingislimitedtoharassment,provideanoticeof aproposedauthorizationtothepublicforreviewand comment.Todate,the Servicehasissued two IncidentalHarassmentAuthorizationsundertheMMPAfortheincidentalharassmentof southernseaotters.
CaliforniaFishandWildlifeCode
CDFWclassifiesthesouthernseaotterasahillyprotectedspecies(section4700).Ahilly protectedspeciesmay notbetakenorpossessedatanytime, andnolicensesorpermitsmaybe issuedfortheirtakeexceptforcollectingfornecessaryscientific research.Hence,incidentaltake andpurposefultakearenotauthorizedforafullyprotectedspeciesexceptforcollectingfor necessaryscientificresearch(andrelocationofthebirdspeciesfortheprotectionoflivestock, butthisprovisionisnotapplicabletosouthernseaotters).CaliforniaFish and WildlifeCode (section4500)statesthatitisunlawfultotake anymarine mammal exceptinaccordancewith provisionsoftheMMPAorprovisionsofTitle50oftheCodeofFederalRegulations,oruntil such timeasfederallawsorregulationspermitthestatetoassumejurisdictionovermarine mammals,atwhichpointtheFishand GameCommissionmayadoptregulationsgoverning marinemammalsandthetakingthereof.
PublicLaw99-625
PublicLaw99-625wasenactedonNovember7,1986.ItauthorizedtheSecretaryoftheInterior todevelopandimplementasouthernseaottertranslocation programandmandatedaregulatory regimethatwouldaccompany theprogramifitwereimplemented.In1987,theServiceinitiated theprogram,designatingthearea surroundingSanNicolasIslandasatranslocationzoneandall other waterssouthofPointConceptionasamanagementzone(52FR29754;August11,1987).
UnderPublic Law99-625,seaottersinthetranslocationzoneweretobetreatedasathreatened species,exceptwithrespecttodefense-relatedagencyactions,inwhichcasethey weretobe treatedasaspeciesthatwasproposedto be listed.4Additionally,anyseaottersfoundinthe “forspecies thatareproposedtobelisted,federalagenciesarenotrequiredtoconsultunderSection7oftheAct butonlytoconferencewiththeService (ortheNationalMarine FisheriesService,asappropriate)ifaproposed actionislikelytojeopardizethecontinuedexistenceofthe species. 23 management zone were required to be non-lethally removed and, while in the management zone, were also to be treated as a proposed species. Any incidental taking that occurred during the course of an otherwise lawful activity within the management zone was not to be considered a violation of either the Act or the MMPA. Regulatory mechanisms otherwise available to avoid or minimize the impacts of incidental take of sea otters in southern California waters would thus have remained absent had the translocation program continued. Although Public Law 99-625 has not been repealed, the translocation program to which it applied (including the translocation and management zones and their associated regulatory regimes) was terminated by regulation on December 19, 2012 (77 FR 75266).
State Laws and Regulations
Several state laws and regulations have been enacted to protect sea otters from injury or mortality in fisheries since the time of listing. A 1991 closure restricted gill and trammel nets to waters deeper than 30 fathoms throughout most of the southern sea otter’s range (California Senate Bill No. 2563). Fishing with set gill nets has since been further restricted throughout the range of the southern sea otter. An order prohibiting the use of gill and trammel nets year-round in ocean waters of 110 m (60 fathoms) or less from Point Reyes in Mann County to Point Arguello in Santa Barbara County was made permanent in September 2002. In the waters south of Point Arguello, the Marine Resources Protection Act of 1990 (California Constitution Article 1 OB) defined a Marine Resources Protection zone in which the use of gill and trammel nets is banned. This zone includes waters less than 128 m (70 fathoms) or within 1.6 km (1 mile), whichever is less, around the Channel Islands, and waters generally within three nautical miles offshore of the mainland coast from Point Arguello to the Mexican border. This closure generally encompasses the depths (less than 40 m or 131 fi) to which sea otters most commonly dive (Tinker et al. 2006a).
Summary
The regulatory mechanisms currently in effect are generally adequate to protect the southern sea otter. Even if the southern sea otter were delisted under the Act, MMPA and state protections would remain in place.
FACTOR E: Other Natural or Manmade Factors Affecting its Continued Existence In the listing rule, we identified oil spili risk as the most serious potential threat to the species (42 FR 2965). We discussed that the loss of genetic diversity and competition with humans are possible but unproven threats (42 FR 2965).
Oil spili risk
Sea otters are particularly vulnerable to oil contamination. When sea otters come into contact with oil, it causes their fur to mat, which prevents it from insulating their bodies. Without this natural protection from the frigid water, sea otters can quickly die from hypothermia. The toxicity of oil can also be harmful to sea otters, causing liver and kidney failure and damage to their lungs and eyes (Kooyman and Costa 1979, Siniff et al. 1982, Lipscomb et al. 1993). 24 Oilspiiiriskfromtankersandotherlargevesselsthat transittheCaliforniacoast remainsa primary threattothesouthernseaotter. Thetranslocationprogramwasundertaken,inpart,to establishacolonysufficientlyfarfromtheexistingpopulationtominimizethelikelihoodof simultaneouslossfromcatastrophicevents,suchasoilspills.However,astherecoveryplan notes,theExxonValdezoilspilldemonstratedthatSanNicolas Islandwasnotsufficientlyfar fromthemainlandrangetosafeguard againstanoilspiiiofthatmagnitude(Service2003).The Deepwater Horizonoilspillof2010hassinceillustratedthepotentialforreleasesofoilofa much greatermagnitude.TheDeepwaterHorizonspillreleasedanestimated4.9millionbarrels ofoil(ofwhichabout$00,000barrelswerecapturedbycontainmentefforts), almost19times theamountofoilspilledduringtheExxonVatdezdisaster(about261,905barrels) (http://www.eoearth.org/article/Deepwater_Horizon_oil_spill).TheruptureofaPlainsAll- AmericanpipelineonMay19,2015,releasedanestimated2,500barrels(101,000U.S.gallons) ofcrudeoilinto theenvironmentnear RefugioBeachState Park,ofwhich approximately500 barrels(21,000U.S.gallons)mayhavemigratedtothe water
(http://www.refugioresponse.coml).Althoughthespilloccurredjustoutsidethecurrentsouthern edgeofthemainlandrange, andnoseaottersarebelievedtohavebeendirectly affectedbythe spilledoil,theincidentdemonstratesthecontinuingpotentialforoilspillstooccurinthe southernseaotters’range.
Substantialvolumesofcrudeoilandpetroleum productscontinuetobetransportedoffthe Californiacoast fromAlaska, fromforeigncountries,andbetweenCaliforniaproductionsources.
An increaseintankeringandshipping activitiesisexpectedandmayposeagrowingthreat (McCraryetal.2003). Initsevaluationofoilspillriskfrom vessel traffic,theWest Coast Offshore Vessel TrafficRiskManagement Projectfoundthatcoastwisetrafficdensityishigher alongthesectionofthewestcoastbetweentheStraitofJuandeFuca(attheUS/Canadian border)andLosAngeles/Long Beach thaneithernorthofthe StraitorsouthofLos Angeles/LongBeach,withhighesttraffic densitiesspecifically1)betweentheStraitofJuande FucaandtheColumbiaRiver,and2)betweenSanFranciscoandLosAngeles/LongBeach (http://library.state.or.us/repository/2010/201007070951103/index.pdf).The LosAngeles/Long Beach andSanFranciscoBayharborsinclude someofthehighestvolumeoilimportingports andrefiningfacilitiesintheUnitedStates
(http://resources.ca.gov/oceanl97AgendalChap5VTS.html).Althoughtheseportsareoutsidethe current rangeofthesouthernseaotter,collisionsorshipgroundingsofftheCaliforniacoast,or withincongestedportsorharborareas, havethepotentialtooccuras aresultoftheseoperations andtokilllargenumbersofseaottersifspilledoilenterstherange.Avesseltrafficmanagement system wasputinplacein2000(http://montereybay.noaa.gov/vt/vtexec.html),reducingtherisk ofoilspillsthroughoutthesouthernseaotterrange, butitisclearthatspillsstillhavethe potentialtooccur.ThisfactisexemplifiedbytheCoscoBusanspill,which,althoughitoccurred outsidethecurrentrange,released203,099liters (53,653gallons)ofbunkerfuel intotheocean whenthecontainershipstruck the SanFrancisco-OaklandBayBridgeonNovember7,2007 (UnitedStatesCoastGuard2009).
Platformspills mayalsobecomeafactorastheseaotterrangeexpandsintosouthernCalifornia watersbecausenumerousoffshoreoilplatformsarelocatedinthe SouthernCaliforniaBight.
However,thethreatfromoilproducedattheseplatformsisexpectedtodecreaseoverthenext 25 several decades as offshore oil production declines (McCrary et al. 2003). Even assuming continued production at late20thcentury levels, the volume of a future spill on the Pacific Outer Continental Shelf resulting from offshore oil production would likely be relatively small, probably less than 200 barrels (8,400 U.S. gallons), and almost certainly less than 500 barrels (21,000 U.S. gallons) (McCrary et al. 2003).
Despite significant advances in techniques for washing oiled sea otters made during the last 20 years at the CDFW’s Marine Wildlife Veterinary Care and Research Center, it is clear that a spill of sufficient magnitude to cause population-level effects would overwhelm the capacity of rehabilitators to rescue sea otters and return them to the wild.
Loss of genetic diversity
Since the time of listing, a number of studies have identified low genetic diversity in sea otters generally and particularly low levels of genetic diversity in southern sea otters (Larson et al. 2002a, Larson et al. 2002b, Aguilar et al. 2008). Sea otter populations have a very low level of variation at major histocompatibility complex (MHC) genes (Aguilar et al. 2008). Low genetic variability has the potential to compromise the ability of southern sea otters to withstand environmental change and increase their susceptibility to land-borne (novel) pathogens.
However, inbreeding depression in southern sea otters has not been demonstrated.
Competition
Because certain areas of the mainland sea otter range appear to be food-limited (Tinker et al. 2008a, Tinker et al. 2013b), it would be logical to surmise that reductions in prey abundance due to overfishing by humans could pose a threat to southern sea otters. However, there is currently no empirical evidence of direct effects of competition by human fishing on sea otters (Estes pers. comm. 2007).
Mortality in fishing gear
In the listing rule, we did not explicitly identify mortality in fishing gear as a threat to southern sea otters. However, it is clear that sea otters may become entangled/entrapped and drown in commercial fishing gear that is deployed or abandoned in the nearshore marine environment. A period of decline in the southern sea otter population from 1976 to 1984 was likely due to incidental mortality in set-net fisheries (Estes et al. 2003), although gill and trammel nets have since been restricted throughout most of the range of the southern sea otter. The potential exists for sea otters to drown in traps set for crabs, lobsters, and finfish, but only limited documentation of mortalities is available. Hatfield and Estes (2000) summarize records of 18 sea otter mortalities in trap gear, 14 of which occurred in Alaska. With the exception of one sea otter, which was found in a crab trap, all of the reported Alaska mortalities involved Pacific cod traps and were either recorded by National Marine Fisheries Service (NMFS) observers or reported to NMFS observers by fishers. Four sea otters are known to have died in trap gear in California:
one in a lobster trap near Santa Cruz Island in 1987; a mother and pup in a trap with a 10-inch diameter opening (presumed to be an experimental trap) in Monterey Bay in 1987; and one in a rock crab trap 0.8 km (0.5 mi) off Pt. Santa Crnz, California (Hatfield and Estes 2000). In 1995, 26 USGSbeganopportunisticeffortstoobservethefinfishtrapfisheryinCalifornia.These efforts weresupplementedwithobservationsby CDFWin1997andtwohired observersin1999.No seaotterswerefoundinthe1,624trapsobserved(HatfieldandEstes2000).However,avery highlevelofobserver coveragewouldberequiredtoseeanyindicationoftrapmortality,evenif mortalitylevelswerehighenoughtosubstantiallyreducetherateofpopulationgrowth(Hatfield etal.2011).
Controlledexperimentsconducted bytheUSGSand theMontereyBayAquarium demonstrated thatseaotterscouldenterabaited commercial finfishtrapwithinnertrapfunnel openingsof14 cm(5.5in)indiameter (HatfieldandEstes2000).Hatfieldetal.(2011)confirmedthatsome sea ottersexposedtofinfish, lobster,andmockDungenesscrabtrapsinacaptive setting could succeedinenteringthem. Basedonexperimentswithcarcassesandlivesea otters,they concluded thatfinfishtraps with13cm(5in)diameter circularopeningswould largely exclude divingseaotters;that circularopeningsof14to15.2cmto(5.5to6in)indiameterand rectangularopenings10.2cm(4 in)high(typicalofDungenesscrab pots)couldallowthe passageofseaottersuptoabout2yearsofage;andthatthelargerfykeopeningsofspinylobster potsandfinfishtrapswithopenings larger than13cm(5in)could admit largersea otters.
Reducingthefyke-openingheightofDungenesscrabtrapsby2.5cm(1in)to7.6cm(3in) wouldexcludenearlyalldivingseaotterswhile notsignificantly affectingthenumberor sizeof harvestedcrabs(Hatfieldetal.2011).
SinceJanuary2002,CDfWhasrequired12.7cm(5in)seaotterexclusionringstobeplacedin live-fishtraps used alongthe centralcoastfromPt.MontarainSanMateoCountytoPt.Arguello inSantaBarbaraCounty.Noringsarerequiredforlive-fishtrapsusedinthewaterssouthof PointConception,andnoringsarecurrently requiredforlobsterorcrabtrapsregardlessoftheir locationinCaliforniawaters.
Climatechange
Climatechangeisathreatthathasbeenidentifiedsince listing.OuranalysesundertheAct includeconsiderationofongoingandprojectedchangesinclimate.Theterms “climate”and “climatechange”aredefinedbytheIntergovernmentalPanelonClimateChange (IPCC). The term“climate”referstothe meanandvariabilityofdifferent typesofweatherconditions over time,with30yearsbeingatypicalperiodfor suchmeasurements(IPCC 2013a).Theterm “climatechange”thusreferstoachangeinthemeanorvariabilityofone ormoremeasuresof climate(forexample,temperatureorprecipitation) thatpersists foranextendedperiod,whether thechangeisduetonatural variabilityorhumanactivity(IPCC 2013a).
Scientificmeasurementsspanning several decadesdemonstratethatchangesinclimateare occurring,andthattherateofchangehasincreasedsincethe195Os.Examplesincludewarming oftheglobalclimate system,andsubstantial increasesinprecipitationinsomeregionsofthe worldanddecreasesinotherregions(fortheseandother examples,seeSolomonetal.2007, IPCC2O13b,IPCC2014).Resultsofscientific analysespresentedbytheIPCCshowthat most ofthe observedincrease inglobalaveragetemperaturesincethemid-2Othcenturycannotbe explainedbynaturalvariabilityinclimateandis“verylikely”(definedbytheIPCCas90 percentorhigherprobability)duetotheobservedincreaseingreenhousegas(GHG) 27 concentrations in the atmosphere as a result of human activities, particularly carbon dioxide emissions from use of fossil fuels (Solomon et al. 2007, IPCC 2013b). Further confirmation of the role of GHGs comes from analyses by Huber and Knutti (2012), who concluded it is extremely likely that approximately 75 percent of global warming since 1950 has been caused by human activities.
Scientists use a variety of climate models, which include consideration of natural processes and variability, as well as various scenarios of potential levels and timing of GHG emissions, to evaluate the causes of changes already observed and to project future changes in temperature and other climate conditions (Meehl et al. 2007, Ganguly et al. 2009, Prinn et al. 2011). All combinations of models and emissions scenarios yield very similar projections of increases in the most common measure of climate change, average global surface temperature (commonly known as global warming), until about 2030. Although projections of the magnitude and rate of warming differ after about 2030, the overall trajectory of all the projections is one of increasing global warming through the end of this century, even for the projections based on scenarios that assume that GHG emissions will stabilize or decline. Thus, there is strong scientific support for projections that warming will continue through the 21st century, and that the magnitude and rate of change will be influenced substantially by the extent of GHG emissions (Meehl et al. 2007, Ganguly et al. 2009, Prinn et al. 2011, IPCC 2013b). See IPCC 2013b, for a summary of other global projections of climate-related changes, such as frequency of heat waves and changes in precipitation.
Various changes in climate may have direct or indirect effects on species. These effects may be positive, neutral, or negative, and they may change over time, depending on the species and other relevant considerations, such as threats in combination and interactions of climate with other variables (for example, habitat fragmentation) (IPCC 2014). Identifying likely effects often involves aspects of climate change vulnerability analysis. Vulnerability refers to the degree to which a species (or system) is susceptible to, and unable to cope with, adverse effects of climate change, including climate variability and extremes, Vulnerability is a function of the type, magnitude, and rate of climate change and variation to which a species is exposed, its sensitivity, and its adaptive capacity (Glick et al. 2011, IPCC 2014). There is no single method for conducting such analyses that applies to all situations (Glick et al. 2011). We use our expert judgment and appropriate analytical approaches to weigh relevant information, including uncertainty, in our consideration of the best scientific information available regarding various aspects of climate change.
Global climate projections are informative, and, in some cases, the only or the best scientific information available for us to use. However, projected changes in climate and related impacts can vary across and within different regions of the world (IPCC 2013b). Therefore, we use “downscaled” projections when they are available and have been developed through appropriate scientific procedures, because such projections provide higher resolution information that is more relevant to spatial scales used for analyses of a given species (see Glick et al. 2011 for a discussion of downscaling).
Coastal zones are particularly vulnerable to climate variability and change. In addition to sea level rise, climate change is also expected to affect rainfall-runoff patterns, with expected trends 28 towardsincreasedannualriverrunoffinthewintertime(SouthernCaliforniaCoastalWater ResearchProject2009).Climatechangemaythusaffectsouthernseaottersbymodifying hydrological processesthat influencethetransportofpathogensandcontaminantsfromlandto thenearshore marine environment(Waitheretal.2002).Italsohasthepotentialtoalter(in unknownways)thefrequencyofalgalbloomsinbothfreshwaterandthemarineenvironment.
Increasingoceantemperaturesmay increasetheincidenceandspreadofdisease amongmarine organisms(Burgeetal.2014),with potentially negativeorpositiveeffects onseaotters dependingon theparticularecologicalrelationshipsaffected.Inadditiontoincreasing ocean temperatures,changesinthecarbonatechemistryoftheoceansduetoincreasingatmospheric CO2levels(ocean acidification) mayposeaseriousthreattomarineorganisms,particularly calcifying organisms(Kroekeretal.2010,Kuriharaetal.2004,Kuriharaetal.200$,Stumppet a!.2011,Gazeauetal.2013),manyofwhichareimportantpreyforseaotters.Becauseofthe apparent synergisticrelationshipbetweenfoodlimitationanddisease,potentialclimate-driven declinesinfoodavailability mayinturnresultinincreasedsusceptibilitytodisease.
Summary
NumerousnaturalandanthropogenicfactorsnotcapturedunderFactors A-Dcontinuetoaffect thesouthernseaotter.Ofthese,themostsignificantthreats appeartobethepotentialforalarge oilspillwithinthesouthernseaotter’s rangeandtheimpacts that mayresultfromclimate change.
III.RECOVERYCRITERIA
RecoveryplansprovideguidancetotheService,States,andotherpartnersandinterestedparties onwaystominimizethreatstolistedspecies,andoncriteriathatmaybeusedtodeterminewhen recoverygoalsareachieved. Therearemanypathstoaccomplishingtherecoveryofaspecies, andrecoverymaybeachievedwithoutfullymeetingallrecoveryplancriteria.Forexample,one ormorecriteriamayhavebeenexceededwhileother criteriamaynothavebeenaccomplished.
Inthatinstance,wemaydeterminethat,overall,the threatshavebeenminimizedsufficiently, andthespeciesisrobust enoughtodownlistordelist.Inothercases,newrecovery approaches and/oropportunitiesunknownatthetime therecoveryplanwasfinalizedmaybemore appropriate waystoachieve recovery. Likewise,new informationmay changetheextent that criterianeedtobemetforrecognizing recoveryofthespecies. Overall,recoveryisadynamic processrequiringadaptive management,andassessingaspecies’degreeofrecoveryislikewise anadaptiveprocessthatmay,ormaynot,fullyfollowtheguidanceprovidedinarecoveryplan.
Wefocusourevaluationofspeciesstatusinthis5-yearreviewonprogressthathasbeenmade towardsrecoverysincethe specieswaslistedbyeliminatingorreducingthethreatsdiscussedin thefive-factoranalysis.Inthatcontext,progresstowardsfulfillingrecoverycriteriaservesto indicate theextenttowhichthreatfactorshavebeenreducedoreliminated.
TheFinalRevised RecoveryPlanwasapprovedin2003(Service 2003).Itestablishesone recoverycriterion:“Theaveragepopulationlevelovera3-yearperiodexceeds3,090animals.
Thiscriterionaccountsforthenumberofsouthernseaottersthat wouldbeneededtoensure with reasonablecertainty thatanexcessof1,$50animalswouldsurvivefollowingamajoroilspillof the sizeoftheExxonValdezoilspill(over10milliongallons)andtoensurethatadeclining 29 trend of 5 percent per year would be detected before the population reached the threshold level for endangered status. The threshold level for endangered status (1,850 animals) is based on the minimum number of animals needed to ensure a genetically effective population size of 500 if the ratio between effective population size and actual population size is 27 percent” (Service 2003).
The recovery criterion has not been met. The 3-year running average population level for 2014 is 2,944. Reaching the criterion may ensure that the subspecies remains above the criterion for endangered status in the event of an oil spiil of the magnitude of the Exxon Valdez and afford the opportunity to detect a declining trend, but it does not specifically address the threats that are currently limiting population growth. Before delisting, a full five-factor analysis would be undertaken to determine whether threats to the subspecies have been ameliorated sufficiently to allow for the long-term conservation of the species.
IV. SYNTHESIS
The southern sea otter population has expanded considerably in range and number since its near- extinction by the end of the 19th century and since the time of listing in 1977. The 2014 population index of 2,944 animals is now within approximately 150 animals of the delisting threshold identified in the 2003 recovery plan. However, the subspecies remains restricted to a small fraction of its historic range. Despite progress in vessel management to avoid oil spills and advances in washing oiled sea otters, it remains possible that a large spill could occur, and it is likely that in the case of a large spill most oiled sea otters would die despite rescue efforts.
Factors affecting the southern sea otter that have emerged or been recognized more fully since listing include shark-bite mortality, food limitation, disease/biotoxin intoxication, mortality in fishing gear, recreation-related harassment, and climate change. Some of these factors are known to operate synergistically. The limited genetic diversity in southern sea otters may conceivably impede the ability of the population to confront novel pathogens and to adapt to changes resulting from climate change, although there is currently no evidence to suggest that low genetic diversity is negatively affecting the population. Of the abovementioned factors, the most significant drivers of demographic trends along the mainland range (where the vast majority of southern sea otters occur) appear to be food limitation and shark bite mortality. Sea otter range expansion into areas that are not subject to food-limitation or high shark-bite mortality would allow for increased population growth and increase security from the effects of catastrophic or widespread events. However, natural range expansion has halted along the mainland in recent years, presumably due to the effects of shark-bite mortality on the once-growing population segment near the southern end of the range. Because the southern sea otter remains below the delisting criterion, and because of the ongoing effects of these other factors, we believe that the southern sea otter still meets the definition of threatened and recommend no status change at this time.
30 V.RESULTS
RecommendedListingAction:
____
DownlisttoThreatened
____
UplisttoEndangered
____
Delist(indicatereasonfordelistingaccordingto50CfR424.11):
____
Extinction
_____
Recovery
____
OriginaldataforclassWcationinerror
XNoChange
NewRecoveryPriorityNumberandBriefRationale:No change.Therecoverypriority numberremains9Cbecausethetaxonisasubspeciesthatfacesamoderatelevelofthreatand hashigh potentialfor recovery.Althoughfoodlimitation/diseaseandsharkbitemortalityare importantfactorsinfluencingrecovery,seaottersexpandingtheirrangeintosouthernCalifornia watersareexpectedtoencounterhigherper-capitapreyavailabilityandlowersharkbiterisk thanseaottersalong thecentralCaliforniacoastandthustocontributetopopulationgrowthin thefuture.The “C”indicatesthepotentialforcontinuingconflictwitheconomicactivity.
VI.RECOMMENDATIONSFORACTIONSOVERTHENEXT5YEARS
Therecoveryplanoutlinessevenmaintasks.Anumberoftasks/subtaskshavebeencompleted, asdescribedinthe“ReviewAnalysis”portionofthisreport.forongoingtasks,emphasisshould beplacedoncontinuedimplementationofthefollowingactivities,incoordinationbetweenthe Serviceandourpartners:
•Monitorexistingandtranslocatedpopulations(Task1;thisactionincludesthe developmentofnewtaggingtechnologies);
•Implementplanstoreducetheprobabilityofanoilspillintheseaotterrangeand minimizeeffectsofaspillontheotter population,intheeventthatoneoccurs(Task2); •Monitortheincidentaltakeofseaottersincommercialfisheries(Sub-task3.1.1)and minimizeintentionaltakeofsouthernseaotters(Sub-task3.2); •Developandimplementapubliceducationandoutreachprogram(Task7;thisaction shouldincludesignificantnew efforts1)tominimizerecreation-relatedandother harassment(i.e.,theBeSeaOtterSavvyprogram)and2)toincreasepublicunderstanding ofthebroadrangeofseaottercommunityeffectsandecosystemservices).
ThefollowingactionsarenotaddressedintheRecoveryPlanbutshouldbeinitiated,in coordinationbetweentheServiceandourpartners,duringthenext5years:
•CompletespatiallyexplicitIntegratedPopulationModel(incorporating resultsfromSub task4.3)toprioritizerecoveryactionswith rigorousdemographicsensitivityanalyses; •Determinethecause(s)ofthegeographicshift/increaseinshark-bitemortality; •Developandimplementaplantoenhancenaturalrangeexpansionthroughreleasesof smallnumbersofrehabilitatedlive-strandedseaotters.
31 VII. REFERENCES CITED
Aguilar, A., D.A. Jessup, J. Estes, and J.C. Garza. 200$. The distribution of nuclear genetic variation and historical demography of sea otters. Animal Conservation 11:35-45.
Bacon, C.E. 1994. An ecotoxicological comparison of organic contaminants in sea otters among populations in California and Alaska. Master’s Thesis, University of California, Santa Cruz.
Bacon, C.E., W.M. Jarman, J.A. Estes, M. Simon, and R.J. Norstrom. 1999. Comparison of organochiorine contaminants among sea otter (Enhydra lutris) populations in California and Alaska. Environmental Toxicology and Chemistry 1$:452-45$.
Bryant, H.C. 1915. Sea otters near Point Sur. California Department of Fish and Game Bulletin 1:134-135.
Burge, C.A., C.M. Eakin, C.S. Friedman, et al. 2014. Climate change influences on marine infectious diseases: implications for management and society. Annual Review of Marine Science 6:249-277.
California Department of Fish and Game. 1976. A proposal for sea otter protection and research, and request for the return of management to the state of California. Sacramento, California. 270 pp.
California Department of Fish and Game. 1999. Letter to Michael Spear, U.S. Fish and Wildlife Service, regarding the draft evaluation of the southern sea otter translocation program and the draft biological opinion on the containment program for the southern sea otter. Dated May 11. Sacramento, California.
Conrad P.A., M.A. Miller, C. Kreuder, E.R. James, I. Mazet, H. Dabritz, D.A. Jessup, F.
Gulland, M.E. Grigg. 2005. Transmission of toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondil flow into the marine environment. International Journal for Parasitology 35:1155—1 16$.
Costa, D.P. and G.L. Kooyman. 19$2. Oxygen consumption, thermoregulation, and the effect of fur oiling and washing on the sea otter, Enhydra lutris. Canadian Journal of Zoology 60:2761-2767.
Cronin, M.A., J. Bodkin, B. Ballachey, J. Estes, J.C. Patton. 1996. Mitochondrial-DNA variation among subspecies and populations of sea otters (Enhydra lutris). Journal of Mammalogy 77:546-557.
Dewar, H., M. Domeier, and N. Nasby-Lucas. 2004. Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight. Environmental Biology of Fishes 70:133—143.
32 Dubey, J.P.,N.L. Miller, andD.K.Frenkel.1970.Toxoplasmagondillifecycleincats.Journal oftheAmerican VeterinaryMedicalAssociation157:1767—1770.
Duggins,D.O.1980.Kelp beds andseaotters:anexperimentalapproach.Ecology61:447-53.
Estes,J.A.1990.Growthandequilibriuminseaotterpopulations.JournalofAnimalEcology 59:385-401.
Estes,J.A.andR.J.Jameson.1988.Adouble-surveyestimateforsightingprobabilityofsea ottersinCalifornia.JournalofWildlifeManagement52:70-76.
Estes,l.A.andJ.F.Palmisano.1974.Seaotters:theirroleinstructuringnearshoremarine communities.Science185:1058-60.
Estes,l.A.,N.S.Smith,andJ.F.Palminsano.1978.Seaotter predationandcommunity organizationinthewestern Aleutianislands,Alaska.Ecology59:822-833.
Estes,J.A.andC.Harrold.1988.Seaotters,seaurchins,andkelpbeds:somequestionsofscale.
Pp.116-150,inG.R.VanBlaricomandl.A.Estes,eds.,TheCommunityEcologyofSea Otters.Berlin:Springer-Verlag.
Estes,l.A.,K.E.Underwood,andM.J.Karmann.1986.Activity-timebudgetsofseaottersin California. JournalofWildlifeManagement50:626-636.
Estes,J.A.,B.B.Hatfield,K.Rails,andJ.Ames.2003.CausesofmortalityinCaliforniasea otters duringperiodsofpopulationgrowthanddecline.MarineMammalScience19:198- 216.
Ganguly,A.R.,K.Steinhaeuser,D.J.EricksonIII,M.Branstetter,E.S.Parish,N.Singh,J.B.
Drake,andL.Buja.2009.Highertrendsbutlargeruncertaintyandgeographicvariability in21stcentury temperatureandheatwaves.ProceedingsoftheNationalAcademyof Sciences106:15555-15559.
GazeauF.,L.M.Parker,S.Comeau,etal.2013.Impactsofoceanacidificationonmarineshelled molluscs.MarineBiology160:2207-45.
Gerber,LR.,M.T.Tinker,D.F.Doak,J.A.Estes,andD.A.Jessup.2004.Mortalitysensitivityin life-stage simulationanalysis:acase studyofsouthernseaotters.EcologicalApplications 14:1554-1565.
Glick,P.,B.A.Stein,andN.A.Edelson,eds.2011.Scanningtheconservationhorizon:aguideto climatechangevulnerabilityassessment.NationalWildlifeFederation,Washington,D.C.
Gunvalson,M.M.2011.Reducingdisturbancestomarine mammalsbykayakersintheMonterey Bay.Master’sThesis.SanJoseStateUniversity,SanJose,California. 33 Hatfield, B.B. and J.A. Estes. 2000. Preliminary results of an evaluation of the potential threat to sea otters posed by the nearshore finfish trap fishery. Unpublished. 6 pp. + appendices.
Hatfield, B.B., J.A. Ames, J.A. Estes, M.T. Tinker, A.B. Johnson, M.M. Staedler, and M.D.
Harris. 2011. Sea oiler mortality in fish and shellfish traps: estimating potential impacts and exploring possible solutions. Endangered Species Research 13:219—229.
Hines, A.H. and J.S. Pearse. 1982. Abalones, shells, and sea otters: dynamics of prey populations in central California. Ecology 63:1547-1560.
Huber, M., and R. Knutti. 2012. Anthropogenic and natural warming inferred from changes in Earth’s energy balance. Nature Geoscience 5:31—36.
Hughes, B.B., R. Eby, E. Van Dyke, M.T. Tinker, C.I. Marks, K.S. Johnson, and K. Wasson. 2013. Recovery of a top predator mediates negative eutrophic effects on seagrass.
Proceedings of the National Academy of Sciences 110:15313-15318.
Intergovernmental Panel on Climate Change. 2013a. Annex III: Glossary. P. 1450 in T.F.
Stocker, D. Qin, G.-K. Plailner, et al., eds., Climate Change 2013: The Physical Science Basis. Contribution of Working Group Ito the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge and New York: Cambridge University Press.
__________
2013b. Summary for policymakers. Pp. 3-29 in T.F. Stocker, D. Qin, G.-K.
Plattner, et al., eds., Climate Change 2013: The Physical Science Basis. Contribution of Working Group Ito the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge and New York: Cambridge University Press. __________
2014. Summary for policymakers. Pp. 1-32 in Field, C.B., V.R. Barros, D.J.
Dokken, et al., eds., Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge and New York: Cambridge University Press..
Jameson, R.J. 1998. Sexual segregation in sea oilers and its role in range expansion. The Oiler Raft 60:6-8.
Jameson, R.J. 1989. Movements, home range, and territories of male sea oilers off central California. Marine Mammal Science 5:159-172.
Jameson, R.J. and S. Jeffñes. 1999. Results of the 1999 survey of the Washington sea oiler population. Unpublished. 5 pp.
Jameson, R.J. and S. Jeffries. 2005. Results of the 2005 survey of the reintroduced Washington sea oiler population. Unpublished. 6 pp.
34 Jameson,R.J.andA.M.Johnson.1993.Reproductivecharacteristicsoffemaleseaotters.
MarineMammalScience9:156—167.
JessupD.A.,M.A.Miller,M.Harris,B.B.Hatfield,andJ.A.Estes.2004.The2003southernsea otter(Enhydralutrisnereis)unusualmortalityevent:apreliminaryreporttoNOAAand USFWS. Unpublished.38pp.
JessupD.A.,C.K.Johnson,J.Estes,D.Carison-Bremer,W.M.Jarman,S.Reese,E.Dodd,M.T.
Tinker,M.H.Ziccardi.2010.Persistentorganicpollutantsinthebloodoffree-ranging seaotters(Enhydralutrisssp.)inAlaskaandCalifornia.JournalofWildlifeDiseases46:
1214—1233.
Johnson,C.K.,M.T.Tinker,l.A.Estes,P.A.Conrad,M.Staedler,M.A.Miller,D.A.Jessup,and J.A.K.Mazet.2009.Preychoiceandhabitatusedriveseaotterpathogenexposureina resource-limitedcoastalecosystem. ProceedingsoftheNational AcademyofSciences 106:2242-2247.
Kannan,K.,E.Perrotta, andN.J.Thomas.2006.Associationbetweenperftuorinatedcompounds andpathologicalconditionsinsouthernseaotters.EnvironmentalScience&Technology 40:4943-4948.
Kannan,K.,E.Perrotta,N.J. Thomas,andK.M.Aldous.2007.Acomparativeanalysisof polybrominateddiphenylethersandpolychlorinatedbiphenylsinsouthernseaottersthat diedofinfectiousdiseasesandnoninfectiouscauses.ArchivesofEnvironmental ContaminationandToxicology53:293-302.
KannanK.,K.S.Guruge,N.J. Thomas,S.Tanabe,J.P.Giesy.199$.Butyltinresiduesinsouthern seaotters(Enhydralutrisnereis)founddead alongCaliforniacoastalwaters.
EnvironmentalScienceandTechnology32:1169-1175.
Kenyon,K.W.1969.TheseaotterEnhydratutrisintheeastern PacificOcean.NorthAmerican fauna68:1-352.
Kooyman,G.L.andD.P.Costa.1979.Effectsofoilingontemperatureregulationinseaotters.
Yearlyprogressreport, OuterContinentalShelfEnergyAssessmentProgram.
Kreuder,C.,M.A.Miller,D.A.Jessup,L.J.Lowenstein,M.D.Harris,l.A.Ames,T.E.Carpenter, P.A.Conrad,andJ.A.K.Mazet.2003.Patternsofmortalityinsouthernseaotters (Enhydralutrisnereis)from1998-2001.JournalofWildlifeDiseases39:495-509.
Kreuder,C.,M.A.Miller,L.J.Lowenstine,P.A.Conrad,I.E.Carpenter,D.A.Jessup,andJ.A.K.
Mazet.2005.Evaluationofcardiac lesionsandriskfactorsassociatedwithmyocarditis anddilatedcardiomyopathyinsouthernsea otters(Enhydratutrisnereis).American JournalofVeterinaryResearch66:289-299.
35 Kroeker, K. J., R.L. Kordas, R. N. Crim, and G.G. Singh. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13:1419- 1434.
Kudela, R.M., J.Q. Lane, W.P. Cochian. 200$. The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA. Harmful Algae 8:103-1 10.
Kurihara, H., and Y. Shirayama. 2004. Effects of increased atmospheric C02 on sea urchin early development. Marine Ecology Progress Series 274:161-169.
Kurihara, H., M. Matsui, H. Furukawa, M. Hayashi, and A. Ishimatsu. 200$. Long-term effects of predicted future seawater C02 conditions on the survival and growth of the marine shrimp Palaemon pacficus. Journal of Experimental Marine Biology and Ecology 367:41-46.
Lafferty, K.D. and M.T. Tinker. 2014. Sea otters are recolonizing southern California in fits and starts. Ecosphere 5.5:1-11.
Laidre, K.L., R.J. Jameson, and D.P. DeMaster. 2001. An estimation of carrying capacity for sea otters along the California coast. Marine Mammal Science 17:294-309.
Larson, S., R. Jameson, J. Bodkin, M. Staedler, and P. Bentzen. 2002a. Microsatellite DNA and mitochondrial DNA variation in remnant and translocated sea otter (Enhydra lutris) populations. Journal of Mammalogy 83:893-906.
Larson, S., R. Jameson, M. Etnier, M. Fleming, and P. Bentzen. 2002b. Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries.
Molecular Ecology 11:1899-1903.
Larson, S., R. Jameson, M. Etnier, T. Jones, and R. Hall. 2012. Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741—1911.
PLoS ONE 7(3): e32205. doi:10.1371/journal.pone.0032205.
Lipscomb, T.P., R.K. Harris, R.B. Moeller, J.M. Pletcher, R.J. Haebler, and B.E. Ballachey. 1993. Histopathologic lesions in sea otters exposed to crude oil. Veterinary Pathology 30:1-11.
Lowry, L.F. and J.S. Pearse. 1973. Abalones and sea urchins in an area inhabited by sea otters.
Marine Biology 23 :213-219.
Lubina, J. and S. Levin, 198$. The spread of a reinvading species: range expansion in the California sea otter. American Naturalist 131:526-543.
Mayer, K.A., M.D. Dailey, and M.A. Miller. 2003. Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance, distribution, and pathology.
Diseases of Aquatic Organisms 53:77-88.
36 McCrary,M.D.,D.E.Panzer,andM.O.Pierson.2003. Oilandgasoperationsoffshore California:status,risks,andsafety.MarineOrnithology31:43-49.
Meehl,G.A.,T.F.Stocker,W.D.Collins,etal.2007.Globalclimateprojections.InS.Solomon, D.Qin,M.Manning,etal.,eds.,ClimateChange2007:ThePhysicalScienceBasis.
ContributionofWorkingGroupItotheFourthAssessmentReportofthe IntergovernmentalPanelonClimateChange.CambridgeandNewYork:Cambridge UniversityPress.
Miller,M.A.,E.Dodd,E.Berberich,F.Batac,L.Henkel,J.Kunz, andT.Tinker.2013.
PreliminaryfindingsfromnecropsyoftaggedseaottersfromtheMonterey-BigSur study.Pp.206-234,inM.T.Tinker,ed.,SeaofferpopulationbiologyatBigSurand MontereyCalifornia:Investigatingtheconsequencesofresourceabundanceand anthropogenicstressorsforseaotterrecovery.DraftfinalReporttoCaliforniaCoastal ConservancyandU.S.FishandWildlifeService.UniversityofCalifornia,SantaCmz,
24.2pp.
Miller,M.A.,M.E.Grigg,C.Kreuder,F.R.James,A.C.Melli,P.R.Crosbie,D.A.Jessup,J.
C.Boothroyd,D.Brownstein,andP.A.Conrad.2004.Anunusual genotypeof ToxoplasmagondliiscommoninCaliforniaseaotters(Enhydralutrisnereis)andisa causeofmortality.InternationalJournalforParasitology34:275-284.
Miller,M.A.,l.A.Gardner,C.Kreuder,D.M.Paradies,K.R.Worcester,D.A.Jessup,E.Dodd, M.D.Harris,J.A.Ames,A.E.Packham,andP.A.Conrad.2002.Coastalfreshwater runoffisariskfactorforToxoplasmagondiiinfectionofsouthernseaotters(Enhydra lutrisnereis).InternationalJournalforParasitology32:997-1006.
Miller,M.A.,R.M.Kudela,A.Mekebri,D.Crane,S.C.Oates,M.T.Tinker,M.Staedler,W.A.
Miller,S.Toy-Choutka,C.Domink,D.Hardin,G.Langlois,M.Murray,K.Wardand D.A.Jessup.2010a.Evidenceforanovelmarineharmfulalgalbloom:cyanotoxin (Microcystin)transferfromlandtoseaotters.PLoSONE5:el2576.
Miller,M.A.,P.A.Conrad,M.Harris,B.Hatfield,G.Langlois,D.A.Jessup,S.L.Magargal, A.E.Packham,S.Toy-Choutka,A.C.Melli,M.A.Murray,F.M.GullandandM.E.Grigg. 20lOb.Aprotozoal-associatedepizooticimpactingmarinewildlife:mass-mortalityof southernseaoffers(Enhydralutrisnereis)dueto$arcocystisneuronainfection.
VeterinaryParasitology172:183—194.
Miller,M.A.,W.A.Miller,P.A.Conrad,E.R.James,A.C.Mdli,C.M.Leutenegger,H.A.
Dabritz,A.E.Packham,D.Paradies,M.Harris,I.Ames,D.A.Jessup,K.Worcester, M.E.Grigg.2008.TypeXToxoplasmagondiiinawildmusselandterrestrialcarnivores fromcoastalCalifornia:new linkagesbetweenterrestrialmammals,runoffand toxoplasmosisofseaoffers.InternationalJournalofParasitology38(11):1319-28. 37 Monson, D., J.A. Estes, D.B. Siniff, and J.L. Bodkin. 2000. Life history plasticity and population regulation in sea otters. Oikos 90:457-468.
Morrison, P., M. Rosenmann, and J.A. Estes. 1974. Metabolism and thermoregulation in the sea otter. Physiological Zoology 47:218-229.
Mos, L. 2001. Domoic acid: a fascinating marine toxin. Environmental Toxicology and Pharmacology 9:79-85.
Nakata, H., K. Kannan, L. Jing, N. Thomas, S. Tanabe, and J.P. Giesy. 1998. Accumulation pattern of organochlorine pesticides and polychiorinated biphenyls in southern sea otters (Enhydra lutris nereis) found stranded along coastal California, USA. Environmental Pollution 103:45-53.
Palmisano, J.f. and J.A. Estes. 1977. Ecological interactions involving the sea oiler. P. 527, in M.S. Merritt and R.G. fuller, eds., The Environment of Amchitka Island, Alaska. U.S.
Energy Research and Development Administration, Springfield, Virginia.
Palmisano, J.f. 1983. Sea otter predation: its role in structuring rocky intertidal communities in the Aleutian Islands, Alaska USA. Acta Zoologica Fennica 174: 209-11.
Prinn, R., S. Paltsev, A. Sokolov, M. Sarofim, I. Reilly, H. Jacoby. 2011. Scenarios with MIT integrated global systems model: significant global warming regardless of different approaches. Climatic Change 104:515-537.
Ralls, K. and D.B. Siniff. 1990. Time budgets and activity patterns in California sea oilers.
Journal of Wildlife Management 54:251-259.
Ralls, K., T.C. Eagle, and D.B. Siniff. 1996. Movement and spatial use patterns of California sea oilers. Canadian Journal of Zoology 74:1841-1849.
Riedman, M.L. and J.A. Estes. 1990. The sea oiler (Enhydra lutris): behavior, ecology, and natural history. U.S. Fish and Wildlife Service, Biological Report. 126 pp.
Sanchez, M.S. 1992. Differentiation and variability of mitochondrial DNA in three sea oiler, Enhydra lutris, populations. Master’s Thesis, University of California, Santa Crnz.
Schramm, Y., G. Heckel, A. Sáenz-Arroyo, E. López-Reyes, A. Baez-Flores, G. Gómez Hernández, A. Lazo-de-la-Vega-Trinker, D. Lubinsky-Jinich, and M. de los Angeles Milanés-Salinas. 2014. New evidence for the existence of southern sea oilers (Enhydra lutris nereis) in Baja California, Mexico. Marine Mammal Science 30:1264-1271.
Staedler, M.M. 2011. Maternal care and provisioning in the southern sea otter (Enhydra tutris nereis): reproductive consequences of diet specialization in an apex predator. Master’s Thesis, University of California, Santa Cruz.
38 Stumpp,M.,J.Wren,FrankMelzner,M.C.Thorndyke,andS.T.Dupont.2011.CO2induced seawateracidificationimpactsseaurchinlarvaldevelopmentI:elevated metabolicrates decreasescope forgrowthandinducedevelopmentaldelay.ComparativeBiochemistry andPhysiology,PartA:Molecular&IntegrativePhysiology160:331-340.
SouthernCaliforniaCoastalWaterResearchProject.2009.
<http://www.sccwrp.org!view.php?id=251>.
Siniff,D.B.,T.D.Williams,A.M.Johnson, andD.L.Garshelis.1982.Experimentsonthe responseofseaotters,Enhydralutris,tooilcontamination.BiologicalConservation2:
261-272.
Solomon,S.,D.Qin,M.Manning,etal.2007.Technicalsummary.InSolomon,S., D.Qin,M.
Manning,et al.,eds.,ClimateChange2007:ThePhysicalScienceBasis.Contributionof WorkingGroupItotheFourthAssessmentReportoftheIntergovernmentalPanelon ClimateChange.CambridgeandNewYork:CambridgeUniversityPress.
Thomas,NJ.,andR.A.Cole.1996.Theriskofdiseaseandthreatstothewildpopulation.
EndangeredSpeciesUpdate13:23-27.
Thometz,N.M.,M.T.Tinker,M.M.Staedler,K.A.Mayer,andT.M.Williams.2014.Energetic demandsofimmatureseaotters frombirthtoweaning:implicationsformaternalcosts, reproductivebehaviorandpopulation-leveltrends.JournalofExperimentalBiology 217:2053-2061.
Tinker,M.T.,G.Bentall,andJ.A.Estes.2008a.Foodlimitationleadstobehavioral diversificationanddietaryspecializationinseaotters.ProceedingsoftheNational AcademyofSciencesoftheUnitedStatesofAmerica105:560-565.
Tinker,M.T.,D.F.Doak,andl.A.Estes.200$b.Usingdemographyandmovementbehaviorto predictrangeexpansionofthesouthernseaotter.EcologicalApplications18:1781—1794.
TinkerM.T.,D.P.Costa,l.A.Estes,N.Wieringa.2007.Individualdietaryspecializationand divebehaviorintheCaliforniaseaotter:Using archivaltime-depthdatatodetect alternativeforagingstrategies.DeepSeaResearchII54:330—342.
Tinker, M.T.,B.B.Hatfield,M.D.Harris,andl.A.Ames.2013a.Whenthesharkbites:
implicationsofincreasingwhitesharkattacksforsouthernseaotters.Paperpresentedat theSeattleAquariumSeaOtterConservationWorkshopVIII,March22-24,2013.
Tinker,M.T.,B.B.Hatfield,M.D.Harris,andl.A.Ames.2015.Dramatic increaseinseaotter mortalityfromwhite sharksinCalifornia.MarineMammalScience. doi:I0.1111/mms.12261.
Tinker, M.T.,J.A.Estes,K.Ralls,T.M.Williams,D.Jessup,andD.P.Costa.2006a.Population dynamicsandbiologyoftheCaliforniaseaotter(Enhydralutrisnereis)atthesouthern 39 end of its range. MMS OCS Study 2006-007. Coastal Research Center, Marine Science Institute, University of California, Santa Barbara. MMS Cooperative Agreement Number 14-35-0001-31063.
Tinker, M.T., D.F. Doak, J.A. Estes, B.B. Hatfield, M.M. Staedler, and J. Bodkin. 2006b.
Incorporating diverse data and realistic complexity into demographic estimation procedures for sea otters. Ecological Applications 16:2293-23 12.
Tinker, M.T., et al., eds. 2013b. Sea otter population biology at Big Sur and Monterey California: investigating the consequences of resource abundance and anthropogenic stressors for sea otter recovery. Draft Final Report to California Coastal Conservancy and U.S. Fish and Wildlife Service. University of California, Santa Cmz, 243 pp.
U.S. Coast Guard. 2009. Report of investigation into the collision of the Cosco Busan with the Delta tower of the San Francisco-Oakland Bay Bridge in San Francisco Bay, November 7, 2007. MISLE Activity Number: 3095030. Washington, DC. 34 pp. + appendix. <http://www.uscg.mi1/foiaJcoscobuscanJcoscobusanfina1030609.pdf5’ U.S. Fish and Wildlife Service. 1984. Assessment of significant points of concern relative to the southern sea otter (S SO) 5-year review, the Friends of the Sea Otter petition to reclassify the SSO as endangered, and the Save Our Shellfish, Greater Los Angeles Council of Divers, and Pacific Legal Foundation Joint Petition to delist the SSO. 38 pp.
U.S. Fish and Wildlife Service. 2000. Reinitiation of formal consultation on the containment program for the southern sea otter (1-8-99-FW-81). California/Nevada Operations Office. 19 July.
U.S. Fish and Wildlife Service. 2003. Final Revised Recovery Plan for the Southern Sea Otter (Enhydra lutris nereis). Portland, Oregon. xi + 165 pp.
U.S. Fish and Wildlife Service. 2012. Final Supplemental Environmental Impact Statement on the Translocation of Southern Sea Otters. Ventura Fish and Wildlife Office, Ventura, California. 348 pp. + front matter and appendices.
U.S. Geological Survey-Western Ecological Research Center. 2014. California sea otter surveys and research. U.S. Geological Survey, Sacramento, CA. Available at <http:!/www.werc.usgs.gov/seaottercount>.
Valentine, K., D.A. Duffield, L.E. Patrick, D.R. Hatch, V.L. Butler, R.L. Hall, and N. Lehman. 2008. Ancient DNA reveals genotypic relationships among Oregon populations of the sea otter (Enhydra lutris). Conservation Genetics 9:933-932.
Vezie, C., J. Rapala, J. Vaitomaa, J. Seitsonen, and K. Sivonen. 2002. Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microbial Ecology 43:443-454. 40 Waither,G.-R,F.Post,P.Convey,A.Menzel,C.Parmesank,T.J.C.Beebee,J.-M.fromentin,
0.Hoegh-Guldberg,andF.Bairlein.2002.Ecologicalresponsestorecentclimate change.Nature416:389-395.
Wilson,D.E.,M.A.Bogan,R.L.Brownell,Jr.,A.M.Burdin,andM.K.Maminov.1991.
Geographicvariationinseaotters,Enhydralutris.JournalofMammalogy72:22-36.
Yeates,L.C.,T.M.Williams,andT.L.Fink.2007.Divingandforagingenergeticsofthesmallest marinemammal,theseaotter(Enhydralutris).JournalofExperimentalBiology 210:1960-1970.
PERSONALCOMMUNICATIONS
Carretta,Jim.2008.Southwest Fisheries ScienceCenter,NOAA,U.S.NationalMarineFisheries Service,LaJolla,CA.
Tinker,M.Tim.U.S.GeologicalSurvey-WesternEcologicalResearchCenterandDepratmentof EcologyandEvolutionaryBiology,UniversityofCalifornia,SantaCruz.
Estes,JamesA.2007.DepartmentofEcologyandEvolutionaryBiology,Universityof California,SantaCruz.
41 U.S. FISH AND WILDLIFE SERVICE
5-YEAR REVIEW
Southern sea otter (Enhydra tutris nereis)
Current Classification: Threatened
Recommendation Resulting from the 5-Year Review:
____
Downhist to Threatened
____
Uplist to Endangered
_____
Delist
X No change needed
Review Conducted By: Lilian Carswell
FIELD OFFICE APPROVAL:
Approve Date
Field $u’ervisor, Ventura Fi and id1ife Office
42