PATTERNS OF MORTALITY IN SOUTHERN SEA OTTERS … · cephalitis, acanthocephalan-related disease, shark attack, and cardiac disease were identiﬁed as common causes of death in sea

495

Journal of Wildlife Diseases, 39(3), 2003, pp. 495–509q Wildlife Disease Association 2003

PATTERNS OF MORTALITY IN SOUTHERN SEA OTTERS(ENHYDRA LUTRIS NEREIS) FROM 1998–2001

C. Kreuder,1,3 M. A. Miller,1,2 D. A. Jessup,1,2 L. J. Lowenstine,1 M. D. Harris,2 J. A. Ames,2T. E. Carpenter,1 P. A. Conrad,1 and J. A. K. Mazet1

1 Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, California 95616, USA2 Marine Wildlife Veterinary Care and Research Center, California Department of Fish and Game, Santa Cruz,California 95060, USA3 Corresponding author (email: [email protected])

ABSTRACT: Detailed postmortem examination of southern sea otters (Enhydra lutris nereis)found along the California (USA) coast has provided an exceptional opportunity to understandfactors influencing survival in this threatened marine mammal species. In order to evaluate recenttrends in causes of mortality, the demographic and geographic distribution of causes of death infreshly deceased beachcast sea otters necropsied from 1998–2001 were evaluated. Protozoal en-cephalitis, acanthocephalan-related disease, shark attack, and cardiac disease were identified ascommon causes of death in sea otters examined. While infection with acanthocephalan parasiteswas more likely to cause death in juvenile otters, Toxoplasma gondii encephalitis, shark attack,and cardiac disease were more common in prime-aged adult otters. Cardiac disease is a newlyrecognized cause of mortality in sea otters and T. gondii encephalitis was significantly associatedwith this condition. Otters with fatal shark bites were over three times more likely to have pre-existing T. gondii encephalitis suggesting that shark attack, which is a long-recognized source ofmortality in otters, may be coupled with a recently recognized disease in otters. Spatial clustersof cause-specific mortality were detected for T. gondii encephalitis (in Estero Bay), acanthoceph-alan peritonitis (in southern Monterey Bay), and shark attack (from Santa Cruz to Point AnoNuevo). Diseases caused by parasites, bacteria, or fungi and diseases without a specified etiologywere the primary cause of death in 63.8% of otters examined. Parasitic disease alone causeddeath in 38.1% of otters examined. This pattern of mortality, observed predominantly in juvenileand prime-aged adult southern sea otters, has negative implications for the overall health andrecovery of this population.

Key words: Acanthocephalan, cardiac disease, Enhydra lutris nereis, Sarcocystis neurona,shark predation, southern sea otter, Toxoplasma gondii.

INTRODUCTION

Evidence linking anthropogenic stress-ors to unusual patterns of disease and mor-tality in marine mammals has accumulatedover the past decade (Ross et al., 1996;Harvell et al., 1999; Fair and Becker, 2000;Daszak et al., 2001). Habitat degradation,pollutants, municipal runoff, global cli-mate change, and overharvest of marineresources are likely to have complex ef-fects that both directly and indirectly af-fect marine mammal health. Southern seaotters (Enhyrda lutris nereis) are a usefulindicator of near-shore marine ecosystemhealth because they are heavily exposed tohuman activity in coastal California (USA)and they commonly remain in one geo-graphically localized area for most of theirlives. Despite legal protection since 1911and unlike sympatric California sea lions

(Zalophus californianus), northern ele-phant seals (Mirounga angustirostris), andharbor seals (Phoca vitulina) in California(Carretta et al., 2001), southern sea ottershave made a slower than expected recov-ery after hunting drastically reduced theirnumbers prior to the 20th century (Estes,1990). Annual counts of sea otters overtheir entire range in California have de-clined since 1995 with the current countat slightly over 2,000 animals (U.S. Geo-logical Survey, unpubl. data). Birth rates inCalifornia sea otters appear similar tothose observed in other, rapidly growingotter populations (Riedman et al., 1994;Monson et al., 2000), suggesting that in-creased mortality may be causing the slowrecovery rate in the California population.

A high percent of mortality due to in-fectious disease was detected in detailednecropsies of southern sea otters from

496 JOURNAL OF WILDLIFE DISEASES, VOL. 39, NO. 3, JULY 2003

1992–95, which raised concern over thegeneral susceptibility of this species to in-fection and subsequent mortality (Thomasand Cole, 1996). Furthermore, some dis-eases were newly recognized as importantcauses of mortality in sea otters, and sev-eral pathogens were implicated that werenot expected to cause considerable mor-tality in a free-ranging marine wildlife spe-cies, such as protozoal encephalitis, acan-thocephalan peritonitis, and coccidioido-mycosis (Thomas and Cole, 1996). Contin-ued monitoring of these newly recognizeddiseases in sea otters is essential, not onlyin light of the recent population decline,but also because techniques used to diag-nose causes of death in sea otters have im-proved with time. Furthermore, detailedevaluation of specific patterns of mortalityin sea otters may have broad implicationsfor overall ecosystem health and may im-prove our understanding of the processesthat promote disease in a marine mammalpopulation. In order to evaluate the recentpattern of mortality in sea otters, the de-mographic and geographic distribution ofcauses of death for freshly deceased seaotters found along the California coast be-tween 1998 and 2001 were evaluated.

MATERIALS AND METHODS

Carcass collection and evaluation

Sea otter carcasses were recovered througha large-scale stranding network conducted bythe California Department of Fish and Game(CDFG), the United States Geological Survey(USGS), the Monterey Bay Aquarium (MBA),and The Marine Mammal Center (TMMC).Collaborating veterinary pathologists atCDFG’s Marine Wildlife Veterinary Care andResearch Center (MWVCRC, Santa Cruz, Cal-ifornia) and the University of California (UC)School of Veterinary Medicine (Davis, Califor-nia) examined three of four freshly dead otters;every fourth carcass was sent to the NationalWildlife Health Center (Madison, Wisconsin,USA). Necropsy findings from otters examinedat MWVCRC/UC from February 1998 throughJune 2001 were included in these analyses.

Stranding location for all otters was deter-mined at the time of carcass recovery. Otterswere assigned the corresponding latitude andlongitude value of their stranding location to

the nearest 0.5 km increment along a smoothedCalifornia coastline. Stranding locations werealso categorized as north or south based ontheir relation to Cape San Martin (358899N,1218469W), which is at the center of the south-ern sea otter range. Age class was determinedat necropsy and was estimated as follows: ju-veniles—milk teeth present (younger than 1yr), subadults—unworn adult dentition (ap-proximately 1–3 yr old), prime-aged adults—adult dentition with evidence of some toothwear (approximately 4–9 yr old), and agedadults—marked tooth wear (approximately 10yr and older). When evaluating age as a riskfactor for specific causes of death, age classeswere collapsed into a juvenile category (juve-niles and subadults) and an adult category(prime-aged adults and aged adults). Pregnancyand lactation status were recorded for femalesat necropsy.

Only otters that were in good postmortemcondition (dead for ,4 days) were included inthis study. Otters heavily scavenged prior tonecropsy and those with incomplete histopa-thology were excluded. For otters that strandedalive but were subsequently euthanized or diedwhile undergoing rehabilitation, the pathologicconditions that were the likely cause of strand-ing were reported. Otters that remained in re-habilitation for longer than 4 wk were exclud-ed. All otters received a complete gross nec-ropsy, as well as microscopic examination ofmajor tissues including heart, lung, liver, kid-ney, spleen, stomach, small intestine, colon,omentum, multiple lymph nodes, skeletal mus-cle, spinal cord, and brain. Tissue sections wereplaced in 10% neutral buffered formalin, par-affin-embedded, sectioned at 5 mm, and stainedwith hematoxylin and eosin for examination bylight microscopy. Acanthocephalan parasitesknown to infect sea otters (Hennessy and Mo-rejohn, 1977) were identified to genus by over-all size and proboscis morphology at gross nec-ropsy (Amin, 1992). Laboratory evaluation ofbacterial, fungal, and parasite samples and tox-icologic screening for domoic acid were per-formed when indicated. Swabs for bacterialculture were collected from heart, blood, in-testinal tract, and lung, plated on tryptic soyagar with 5% sheep blood, MacConkey agar,and XLT-4 agar (Hardy Diagnostics, Santa Ma-ria, California). Plates were incubated at 37 C.Bacterial isolates were identified by the Micro-biology Laboratory at the UC Veterinary Med-ical Teaching Hospital (Davis, California) usingstandard biochemical and molecular tech-niques. Tissues swabs collected from necrop-sied otters with suspected fungal infectionswere also submitted to the Microbiology Lab-oratory. Samples were placed on wet mounts

KREUDER ET AL.—PATTERNS OF MORTALITY IN SOUTHERN SEA OTTERS 497

FIGURE 1. A. Low magnification of a hematoxylin and eosin (HE) stained section of cerebrum from asouthern sea otter with encephalitis due to Toxoplasma gondii. Note moderate perivascular to diffuse mono-nuclear inflammatory infiltrate with marked expansion of Virchow-Robbins spaces by exocytosing inflammatorycells. Near the center of the affected neuropil is a small focus of necrosis (N.). A T. gondii tissue cyst (T.C.)is present in the upper right hand corner of the photo. B. High magnification view of HE-stained sea ottercerebrum showing a T. gondii tissue cyst filled with hundreds of elongated bradyzoites.

for the direct observation of spherules. Sampleswere also cultured on inhibitory mold agar withchloramphenicol (Hardy Diagnostics) and in-cubated at 30 C in air for 3 wk. If fungal growthoccurred, gross colonial morphology was eval-uated and a lactophenol cotton blue prepara-tion (Hardy Diagnostics) was made for micro-scopic examination of arthroconidia for theidentification of Coccidioides immitis (St Ger-main and Summerbell, 1996). Suspect C. im-mitis positive cultures were submitted to a spe-cialty laboratory for confirmation (D. Pappa-gianis, Microbiology and Immunology, UC Da-vis School of Medicine, Davis, California). Onhistopathology, C. immitis was identified by thepresence of round (5–50 mm in diameter),thick-walled spherules containing endospores.

Death was attributed to domoic acid intoxi-cation when substantially elevated levels of do-moic acid were detected in urine (Scholin etal., 2000) and gross or histologic lesions sug-gestive of another cause of mortality were ab-sent. Domoic acid was initially detected by re-ceptor-binding assay (Dr. Vera Trainer, Nation-al Oceanic and Atmospheric Administration,Northwest Fisheries Science Center, Environ-mental Conservation Division, Marine BiotoxinProgram, Seattle, Washington, USA) and, whenpossible, results were confirmed by liquid chro-matography-tandem mass spectroscopy (Dr.Francis Van Dolah, National Oceanic Atmo-spheric Administration, Center for Coastal En-vironmental Health and Biomolecular Re-search, Marine Biotoxin Program, Charleston,South Carolina, USA).

Encephalitis was determined to be a primary

cause of death when moderate to severe in-flammation of the cerebral and/or cerebellarneuropil was present on histopathology (Fig.1a). This criterion was chosen because moder-ate encephalitis was identified histologically inotters undergoing rehabilitation with recurrentseizures and severe neurologic dysfunction.Protozoal infection with either Toxoplasmagondii or Sarcocystis neurona was determinedto be the cause of encephalitis when protozoalstages were directly visualized within inflam-matory foci in the neuropil on histopathology(Fig. 1) and/or when laboratory tests confirmedinfection through isolation of protozoa frombrain tissue (Miller et al., 2001b). Antibody ti-ters to T. gondii and S. neurona were not usedto diagnose these parasites as the cause of en-cephalitis because positive titers do not distin-guish between past exposure and active infec-tion. Otters with encephalitis but without histo-pathologic or laboratory confirmation of proto-zoal infection were diagnosed with encephalitisof unconfirmed cause.

Trauma noted at necropsy was attributed toshark attack when shark tooth fragments wererecovered from wounds or when multiple stab-like lacerations in soft tissue or scratches, char-acteristic of contact with serrated shark teeth,were detected on underlying bone or cartilage(Ames and Morejohn, 1980) (Fig. 2). Similarly,trauma was attributed to boat strike in caseswith soft tissue lacerations and fractures or cutsin underlying bone in a pattern consistent witha propeller injury (Ames and Morejohn, 1980).Severe blunt trauma suggestive of a high speedcollision with a boat hull was also attributed to


FIGURE 2. A. Southern sea otter with a shoulder laceration caused by shark attack. Note the typical stabwound-like pattern and minimal soft tissue removal associated with penetration by shark teeth. B. Highermagnification view of the scapula from the same sea otter shown in Figure A showing a transverse cut of thescapular spine. This cut has distinct comb-like edges, typical of wounds inflicted by great white sharks, whichhave serrated teeth.

boat strike. Cases were diagnosed with traumaor lacerations of unknown cause when clear ev-idence for shark attack or boat strike was notdetected.

Causes of death were rigorously standardizedso that the primary cause identified for eachotter was the most substantial injury or illnessinitiating the sequence of events leading di-rectly to death. Otters were assigned two equal-ly weighted primary causes of death if two un-related and independent conditions were eachsevere enough to have caused death. Contrib-uting causes of death were noted only if path-ologic conditions were identified that added tothe probability of death, but were not part ofthe primary disease complex. To ensure inde-pendence of primary and contributing causesof death, diagnoses of conditions were basedsolely on the severity of the individual lesionsregardless of other conditions present.

Statistical analyses

Proportionate mortality, noted as a percent,was used to identify the major causes of deathin sea otters from 1998 to 2001. Cause-specificproportionate mortality was calculated as theproportion of otters with a specific condition asthe primary cause of death among all ottersthat met the inclusion criteria during the studyperiod. Distribution of the four most commoncauses of death among sex and age classes wasevaluated by the standard two-sided chi squaretest of independence using statistical software(Epi Info Version 6, Centers for Disease Con-trol and Prevention, Atlanta, Georgia, USA).One-sided chi-square test of independence wasused to test associations between each of thefour most common primary causes of death and

the common contributing causes of death withat least nine cases each. If age or sex were sig-nificantly associated with a primary cause ofdeath, associations among primary and contrib-uting causes of death were stratified by the sig-nificant variable (age or sex), and the associa-tion was evaluated for each stratum. For di-chotomous distributions with an expected fre-quency less than five, the Fisher exact test(Fisher, 1935) was calculated using statisticalsoftware (SPSS Base 10.0, SPSS Inc., Chicago,Illinois, USA). When appropriate, strength ofthe association was estimated by the odds ratio.

Geographic and temporal clustering of over-all carcass retrieval and temporal clustering ofeach primary cause of death were evaluated bythe scan test (Carpenter, 2001). This test eval-uates whether carcass retrieval was uniform us-ing the binomial distribution to estimate theprobability of the maximum observed numberof cases within sequential distances of 5 km, 10km, 15 km, and 20 km for geographic cluster-ing and within 1, 2, 3 and 4 mo for temporalclustering. These spatial and temporal periodswere specified because increased carcass re-trieval within these time periods was consid-ered biologically significant based on sea otterbehavior and habitat use. Geographic cluster-ing of specific primary causes of death was eval-uated only for the four most common primarycauses of death with 10 cases or more. Specif-ically, the spatial scan statistic (Kulldorf andNagarwalla, 1995) was used to test whether aprimary cause of death was randomly distrib-uted along the coastline where sea otters car-casses were recovered. The Bernoulli modelwas selected for this procedure, which used thecase and control approach to adjust for differ-


ential retrieval of carcasses along the coastline.In this manner, stranding locations for eachspecific cause of death were compared to lo-cations for otters with all other causes of death.A Monte Carlo iterative technique was used todetermine distribution of the likelihood ratiotest statistic (Kulldorf and Nagarwalla, 1995).

RESULTS

Between February 1998 and June 2001,105 sea otter carcasses met our inclusioncriteria and received a complete necropsyand diagnostic work up in order to deter-mine the cause of death. Of these otters,27 were alive at the time of stranding butdied or were euthanized at rehabilitationcenters. Sea otter carcass retrieval was spa-tially clustered along the coastline duringour study period. Both Monterey Bay andEstero Bay had significant (P,0.01) clus-ters of beachcast carcasses. No carcasseswere retrieved from the remote and rocky140 km long coastal segment in the centerof the sea otter range south of YankeePoint (368489N, 1218949W) to north of SanSimeon Point (358639N, 1218199W). Over-all carcass retrieval was not temporallyclustered during the study period. Car-casses recovered consisted predominantlyof prime-aged adults (46.7%), with fewerjuveniles (29.5%), subadults (11.4%), andaged adults (12.4%). Distribution of pri-mary causes of death among sex and ageclasses is shown in Table 1. While 25 dif-ferent primary causes of death were iden-tified, 53.3% of otters (56/105) died fromone of four major causes: T. gondii en-cephalitis, acanthocephalan parasite infec-tion, shark attack, or cardiac disease. Acan-thocephalan infection, cardiac disease, andT. gondii encephalitis were also recognizedas common contributing causes of death(Table 1).

Encephalitis due to T. gondii was one ofthe two leading causes of mortality iden-tified in sea otters during the time periodstudied. This condition, characterized bymoderate to severe, multifocal, non-sup-purative and necrotizing meningoenceph-alitis (Fig. 1), was a primary cause of deathin 16.2% of the otters examined and was

a contributing factor in another 11.4% ofotters examined. A marginally significantspatial cluster of T. gondii encephalitis cas-es was detected in a 25 km area at thesouthern end of Estero Bay in central Cal-ifornia (P50.06, centered at 358319N,1208889W, Fig. 3). Half of the otters (8/16)recovered in this section of Estero Baywere determined to have T. gondii en-cephalitis as the primary cause of death.Encephalitis caused by S. neurona wascharacterized by severe, necrotizing,mixed non-suppurative and suppurativeencephalitis, which was often most severein the cerebellum and brainstem. Enceph-alitis due to S. neurona was the primarycause of death identified in 6.7% of otters,all of which were detected during springmonths (March through May). Cases weresignificantly clustered temporally in thespring of 2001 (P50.01). Purely suppura-tive encephalitis was detected in only onesea otter, but the primary cause of deathin this case was attributed to facial bitewounds, which caused a ganglioneuritisand ascending infection with Archanobac-terium phocae. Encephalitis of unknownor unconfirmed cause was a primary causeof death for another 4.8% of otters exam-ined. Overall, encephalitis of all typescaused death in 28% of otters examinedand contributed to death in another 18%of otters.

Similar in proportionate mortality to T.gondii encephalitis, infection with acan-thocephalan parasites was a primary causeof death in 16.2% of otters examined, andthis parasite contributed to death in anoth-er 9.5% of otters. Septic peritonitis, causedby migrating Profilicollis spp., was themost common consequence of heavy acan-thocephalan infection (Fig. 4). This type ofperitonitis was the primary cause of deathin 14.3% (15/105) of otters examined andwas 3.5 times more likely to have causeddeath in juveniles and subadults thanadults or aged adults (two-sided chi squaretest, P50.03). Acanthocephalan infectioneither directly caused, or was a contribut-ing factor for, death in 40% (17/43) of the


TABLE 1. Primary and contributing causes of death in 105 southern sea otters from February 1998 to July2001. Sex and age class distributions are provided for primary causes of death.

Cause of deatha Primary Contributing Male Female Juvenile Subadult AdultAgedadult

Acanthocephalan infectionToxoplasma gondii encephalitisCardiac diseaseShark attackLacerations or trauma (unknown cause)

17171414

8

101212

00

911

466

86

1082

94012

24140

67985

02411

Sarcocystis neurona encephalitisEncephalitis - unconfirmed causeOther intestinal diseaseb

Boat strikePerinatal mortality

75554

07000

41353

34201

32214

2020

n/a

1312

n/a

1002

n/aStarvation (early maternal separation)Domoic acid intoxicationBite woundsc

Gastric ulcerationNose wounds due to mating trauma

44322

31079

13210

31112

40000

n/a0000

n/a3222

n/a1100

GunshotBacterial pneumoniaSepsis (unknown cause)Fungal pneumonia (Coccidioides immitis)Gill net drowning

22211

10010

20211

02000

00000

00000

22111

00100

Delayed closure of foramen ovaleOilingEmaciationPeritonitis (unknown cause)Dental disease

11000

00

1633

11———

00———

10———

00———

00———

01———

a A total of 14 otters had two equally weighted primary causes of death. Multiple primary diagnoses were shark attack andT. gondii encephalitis (n 5 5), and one otter each with shark attack and encephalitis of unconfirmed cause, shark attack andsmall bowel volvulus, boat strike and T. gondii encephalitis, domoic acid and T. gondii encephalitis, gill net drowning andT. gondii encephalitis, cardiac disease and encephalitis of unconfirmed cause, cardiac disease and T. gondii encephalitis,domoic acid and trauma of unknown cause, and acanthocephalan infection and encephalitis of unconfirmed cause. One otterhad the three equally weighted primary causes of acanthocephalan infection, S. neurona encephalitis, and small bowelvolvulus. A single contributing cause of death was identified in 63 otters and two contributing causes of death were identifiedin 23 otters.

b Other intestinal diseases included small bowel volvulus (n 5 2), intussusception (n 5 1), intestinal perforation of unknowncause (n 5 1), and bacterial enteritis (n 5 1).

c Bite wounds were not characteristic of shark attack and were most likely caused by aggressive interactions with other ottersor sympatric species.

juvenile and subadult otters examined. Ageographic cluster of acanthocephalanperitonitis was detected at the southernend of Monterey Bay (P50.02, centered at368609N, 1218889W, Fig. 3). In this 1.8 kmarea, five of six carcasses recovered hadacanthocephalan peritonitis as a primarycause of death, while only one case wasexpected if this condition had been dis-tributed evenly across locations where car-casses were recovered along the coast. Thesixth carcass recovered in this area hadacanthocephalan peritonitis as a contrib-uting cause of death.

Shark-inflicted mortality was detected in13.3% of otters examined. All cases hadbite wounds that were consistent with at-tack by white sharks (Carcharodon car-charias, Fig. 2). A significant spatial clusterof otters attacked by sharks was noted inthe 80 km stretch of coastline from PointAno Nuevo to Santa Cruz (P50.02, cen-tered at 378119N, 1228339W, Fig. 3). In thisarea, six of 10 otters recovered were killedby sharks, while only 1.3 cases of shark at-tack were expected had this conditionbeen distributed evenly in areas wherecarcasses were recovered. Histopathologic


FIGURE 3. Central California showing significantclusters of major causes of mortality in sea ottersfrom 1998 through July 2001. Each arrow points tothe highlighted section of coastline where beachcastotters had a significantly higher likelihood of havingthe specified cause of death.

FIGURE 4. A. Mucosal surface of the small intestine in a sea otter with intestinal acanthocephalidiasis.Both Profilicollis spp. (arrowhead) and Corynosoma enhydri (arrow) are adhered to the mucosa. The smallerProfilicollis spp. are in various stages of mural penetration. B. Omentum from a southern sea otter withacanthocephalan peritonitis. Profilicollis spp. have migrated through the intestinal wall and are attached tothe omentum (arrowheads), which is grossly thickened and opaque.

examination of brain tissue from shark-at-tacked otters revealed that eight of 14 ot-ters (57%) attacked by sharks had pre-ex-isting encephalitis. Otters with moderateto severe T. gondii encephalitis were 3.7times more likely to be attacked by sharksthan otters without this condition (one-sid-ed Fisher exact test, P50.05). Shark-in-flicted mortality was not significantly as-sociated with acanthocephalan infection,cardiac disease, or emaciation.

Cardiac lesions in otters were newly rec-ognized during this study period and car-diac disease was diagnosed as a primarycause of death in 13.3% of otters exam-ined. Cardiac lesions consisting of mild tosevere non-suppurative (lymphocytic)myocarditis (Fig. 5) were a common find-ing in otters examined (n541). These le-sions were considered a cause of deathonly when myocarditis was accompaniedby a grossly enlarged, rounded, dilated,and thin walled heart (Fig. 5) and/orstrong evidence for congestive heart fail-ure (pulmonary edema, pleural and peri-toneal effusion, and hepatic congestion).Nearly all cardiac disease cases were ob-served in prime-aged adults or aged adults,and this condition was 3.5 times more like-ly to be a primary cause of death in fe-males than males (two-sided chi squaretest, P50.04). Severe nose wounds were


FIGURE 5. A. Southern sea otter with congestive heart failure secondary to cardiac disease. Note grossabdominal distension caused by hepatomegaly and peritoneal effusion. B. Gross photographs of the chest andabdomen from the otter in Fig. A, showing the enlarged and rounded heart. Also visible are the markedlyenlarged liver, characterized by prominent rounding of the hepatic lobes, and diffuse pulmonary edema. C.HE-stained ventricular myocardium from a sea otter showing multifocal to coalescing areas of fibrosis andinflammation with accompanying myofiber loss. D. Higher magnification photomicrograph of the same sitein Fig. 5C showing the predominantly lymphocytic inflammatory infiltrate.

found in half of the otters (7/14) with car-diac disease as a primary cause of death.Nose wounds are commonly acquired byfemales during mating (Staedler and Ried-man, 1993) but also result from intraspe-cific aggression in males. Both male otterswith severe nose wounds had cardiac dis-ease as a primary cause of death (one-sid-ed Fisher exact test, stratified on sex,P,0.01) and five of nine female otters withsevere nose wounds had cardiac disease asa primary cause of death (one-sided Fisherexact test, stratified on sex, P50.01). In allcases, severe nose wounds were acute orsubacute and seemed to have occurred af-ter development of cardiac disease. Whilesignificant localized geographic clusters ofcardiac disease cases were not detected,otters with this condition were 5.6 times

more likely to be recovered from thesouthern half of the California sea otterrange (two-sided chi square test, P,0.01),which is also where the cluster of T. gondiiencephalitis was detected. Otters diag-nosed with cardiac disease were 2.9 timesmore likely to have concurrent T. gondiiencephalitis than otters without cardiacdisease (one-sided chi square test,P50.01). Cardiac disease was not associ-ated with any other common contributingcause of death.

While emaciation was not determinedto be a primary cause of death in any ot-ters examined, emaciation was identifiedas a contributing cause of death in 15% ofotters. Emaciation was most significantlyassociated with cardiac disease (one-sidedFisher exact test, P50.01) and was 3.2


times more likely to be a contributingcause of death in females than males (two-sided chi square test, P50.03). Of 27 adultand aged adult females that were necrop-sied, nine were confirmed to be lactatingat the time of death. Most lactating fe-males (7/9) were emaciated at death andfour of nine lactating females had cardiacdisease as a primary cause of death.

Infectious diseases (caused by parasites,bacteria, and fungi) and diseases without aspecified etiology (cardiac disease, intesti-nal disease, and encephalitis of uncon-firmed cause) were implicated as a primarycause of death in 63.8% of otters exam-ined. Disease was most commonly a pri-mary cause of death in prime-aged adults(n530) compared to juveniles (n519),subadults (n510), and aged adults (n58).Parasitic diseases alone, caused by T. gon-dii, S. neurona, and Profilicollis spp, weredetermined to be a primary cause of deathin 38.1% of the otters examined.

DISCUSSION

Encephalitis, caused by T. gondii and S.neurona, was first recognized as a sourceof mortality in sea otters only after detailednecropsies were begun in 1992 (Cole etal., 2000; Lindsay et al., 2000; Miller et al.,2001a). Because encephalitis can only bediagnosed by microscopic examination ofbrain tissue, this cause of death was likelymissed in the past when carcasses werenot examined in such detail. However, thereported percent of mortality attributed toprotozoal encephalitis appears to have in-creased substantially over the short periodduring which detailed examinations havebeen undertaken. Of otters examined from1992–95, 8.5% had protozoal encephalitiswhile 22.9% of otters we examined hadprotozoal encephalitis as a primary causeof death. This apparent increase in prev-alence may be a consequence of improveddiagnostics, a difference in criteria for es-tablishing this diagnosis among laborato-ries and pathologists, or temporal variationin the occurrence of this disease. Othercauses of encephalitis should also be con-

sidered, particularly for cases with an asyet unconfirmed cause. However, the mag-nitude of this most recent temporal trendcertainly warrants attention, particularly asthe increased prevalence of this conditioncoincides with a period of population de-cline.

Protozoal infections in sea otters may beexamples of spillover of land-based path-ogens into the marine ecosystem becausethe only identified definitive hosts for T.gondii and S. neurona are felids and opos-sums (Didelphis virginiana), respectively.The spatial cluster of mortality due to T.gondii encephalitis in Estero Bay may bea consequence of local factors, such as in-creased sea otter exposure to T. gondii, en-hanced parasite virulence, or increased seaotter susceptibility in this particular area.In a separate study, sea otter carcassesfound in Estero Bay had higher prevalenceof antibodies to T. gondii than otters sam-pled elsewhere (Miller et al., 2002), sug-gesting that mortality may be due to highlevels of parasite exposure. Seasonal peaksof T. gondii encephalitis mortality in otterswere not detected even though coastalfreshwater runoff has been associated withincreased odds of exposure to T. gondii insea otters (Miller et al., 2002). Runoff ishighest during the winter rainy season andspring in California. However, many un-recognized environmental and host factorscould affect the timing of death from thisdisease. Otters with S. neurona encepha-litis, which may be a more acutely severeand rapidly progressive disease, strandedonly in spring months (March throughMay), which follows maximal seasonal run-off and coincides with the season whenopossums were more likely to shed spo-rocysts (Rickard et al., 2001).

While infection with T. gondii is com-mon in terrestrial mammals, it is usuallysubclinical in immune competent hosts(Frenkel, 1988). Disseminated systemicdisease with severe brain infection is moretypical of immune suppressed humans,such as HIV infected AIDS patients (Ar-nold et al., 1997). Fatal T. gondii infections


have been reported in neotropical marsu-pials and nonhuman primates, whichevolved in ecologic isolation from domes-tic cats (Frenkel, 1988). Expansion of do-mestic cat and opossum populations anddecreased natural filtration of watershedrunoff through coastal estuaries may haveincreased sea otter exposure to a pathogenfor which they are immunologically ill-pre-pared. These protozoal pathogens are notlikely to have been abundant in the marineenvironment centuries ago. The substan-tial proportionate mortality caused by pro-tozoal encephalitis in juvenile and primeaged adult otters is of concern, particularlybecause T. gondii encephalitis was shownhere to be associated with two other im-portant causes of death, shark attack andcardiac disease. If T. gondii infection in-creases the risk of death from shark attackor cardiac disease, this parasite may havea complex but critical role in a high levelof mortality in sea otters.

Toxoplasma gondii infection may haveother deleterious effects that are difficultto document by the methods used here.Fetal infection with T. gondii is associatedwith serious birth defects and a high fre-quency of abortion in terrestrial animalsand humans. These effects would be dif-ficult to detect in free-living sea otters be-cause aborted fetuses and pups that dieshortly after birth are less likely to befound in fresh condition. Underlying caus-es for the perinatal mortality noted in re-covered pup carcasses could not be deter-mined but all were near full term pupsthat died shortly after birth and none hadpathologic findings consistent with proto-zoal infection.

The high prevalence of pre-existing T.gondii encephalitis in shark attacked otterssuggests that otters with encephalitis mayexhibit aberrant behavior that rendersthem more vulnerable to attack by sharks.Otters with protozoal encephalitis fre-quently exhibit fine muscle tremors, re-current seizures, dull mentation, and de-creased or abnormal motor function (M.Murray, pers. comm.). Neurologic dys-

function might cause otters to be less ableto evade attacks, to move offshore out ofthe protected areas, or to attract shark at-tention through abnormal movements andseizures. Wounds inflicted upon otters bysharks were typically large gashes withminimal soft tissue removal, consistentwith open-mouth slashing or raking bysharks (Fig. 2). This bite pattern is similarto that seen when sharks attack humans(Byard et al., 2000) and is not consistentwith a bite pattern used for intended prey.Sharks feeding on pinniped prey often re-move large pieces of soft tissue (Lucas andStobo, 2000). The wound pattern observedin otters suggests that they may not be in-tended prey and the high percent of shark-attacked otters with pre-existing encepha-litis is consistent with the hypothesis thatsharks are more likely to attack otters ifthey are acting abnormally.

The area from Santa Cruz to Point AnoNuevo with high shark-related mortality insea otters is known for white shark pre-dation on pinnipeds (Long et al., 1996).Shark-inflicted mortality has been long-recognized as an important cause of mor-tality in sea otters since carcasses were firstevaluated in 1968 and the number ofshark-bitten beachcast carcasses has variedconsiderably by year (Ames et al., 1996).However, the annual proportion of shark-attacked sea otter carcasses relative to theannual population count has increasedthrough time particularly during periods ofpopulation decline (Estes et al., 2003). Be-cause interactions with sharks may bemodified by encephalitis in otters, preva-lence of shark attack may be linked toprevalence of encephalitis. Both shark at-tack and encephalitis may be under-rep-resented as a cause of death if carcasseswith penetrating wounds from shark bitesare more likely to sink than wash ashore(Lucas and Stobo, 2000) or if otters areconsumed by sharks, although the latterhas never been observed.

Cardiac disease has not previously beenreported in sea otters and the substantialpercent of deaths attributed to cardiac dis-


ease was unexpected. Stress-related car-diac disease has been documented instranded cetaceans (Turnbull and Cowan,1998), but the contraction band-necrosisof myocardium detected in dolphins andwhales differed from the pattern of non-suppurative myocarditis and gross cardiacdilation observed in sea otters. The inflam-matory nature of the cardiac lesions notedhere suggests an infectious etiology al-though infectious agents were not detect-ed during microscopic examination of seaotter myocardium. Our observation thatotters with cardiac disease are more likelyto have concurrent T. gondii encephalitisimplies that these two conditions are caus-ally linked or are somehow coupled by anunknown mechanism. Rare accounts ofmyocarditis in animals infected with T.gondii have been reported in dolphins(Inskeep et al., 1990), a northern fur seal(Callorhinus ursinus; Holshuh et al.,1985), and a California sea lion (Zalophuscalifornianus; Migaki et al., 1977), al-though disseminated toxoplasmosis withprotozoal cysts in cardiac myofibers wereobserved in all cases. In humans, T. gondii-related cardiomyopathy has been docu-mented in AIDS patients (Matturri et al.,1990) and immune-suppressed hearttransplant patients (Arnold et al., 1997).Efforts are currently being directed at un-derstanding the immunopathology of toxo-plasmosis in sea otters, improving detec-tion methods for protozoal stages, andevaluating other possible etiologies andrisk factors for cardiac disease.

Cardiac disease was a common cause ofdeath in female otters and was often as-sociated with severe nose wounds andemaciation. Emaciation and severe nosewounds may be a secondary consequenceof the debilitating effects of heart failure,which could prevent afflicted otters fromforaging effectively and defending them-selves against aggressive males. Adult fe-males appear to be highly susceptible toboth mating trauma and emaciation, par-ticularly at the end of lactation, possiblybecause they are at a nutritional disadvan-

tage after caring for a pup and enteringestrus, which attracts male attention. Thetransition from pup care and lactation toestrus and breeding appears to be a par-ticularly vulnerable period for adult femalesea otters in California.

Acanthocephalan peritonitis continuesto be a substantial cause of mortality in seaotters, and the recent prevalence (16.2%)is similar to the 14% reported from 1992–95 (Thomas and Cole, 1996). Sand crabs(Emerita analoga) and possibly spiny molecrabs (Blepharipoda occidentalis) serve asintermediate hosts for these acanthoceph-alan parasites (Hennessy and Morejohn,1977), and these crabs are found in pre-dominantly sandy habitat. It is thereforelikely that otters foraging in sandy bays willhave a high level of exposure to Profilicol-lis spp. As expected, mortality due to acan-thocephalan peritonitis during this studyperiod was detected exclusively in carcass-es retrieved from Monterey Bay and Es-tero Bay, both of which are largely sandyhabitat. While sand crabs may not be pre-ferred sea otter prey, they are abundantand easy to capture. Juvenile otters mayingest large numbers of these prey specieswhen they are first searching for suitablehome-range habitat and learning to forageon their own, which may explain the highlevel of exposure and subsequent mortalityin this age class.

Even though acanthocephalan peritoni-tis is readily apparent at necropsy throughgross evidence of peritonitis associatedwith parasites in the abdominal cavity, thiscondition was reported only once in nec-ropsies performed on otters from 1968–76(Hennessy and Morejohn, 1977), suggest-ing that fatal acanthocephalan infectionsmay have increased in prevalence. The ap-parent increased prevalence of acantho-cephalan peritonitis may reflect increasedhost susceptibility to infection or increasedexposure through a shift in preferred preyavailability, intermediate host abundance,foraging behavior, or habitat use. South-erly otter range expansion into the pre-dominantly sandy habitat south of Point


Estero is unlikely to have contributed sub-stantially to the higher prevalence of thiscondition in recent years because 80% ofthe otters with fatal acanthocephalan in-fections from 1998–2001 were retrievedfrom Monterey Bay, which has been oc-cupied by sea otters since the 1970s (Ried-man and Estes, 1990).

Domoic acid intoxication has not beenpreviously reported in sea otters and nec-ropsy findings and preliminary laboratorytests suggest that domoic acid intoxicationwas a primary cause of death in four ottersexamined here. Domoic acid is a marinebiotoxin produced by Pseudonitzchia spp.and is known to cause severe neurologicdysfunction and death in California sea li-ons (Scholin et al., 2000) and seabirds(Work, 1993). Domoic acid exposurecaused characteristic brain and cardiac le-sions in sea lions (Scholin et al., 2000), andhistologic lesions associated with domoicacid exposure in sea otters are currentlybeing evaluated. Domoic acid intoxicationmay be established as a more commoncause of mortality in sea otters once di-agnostic capabilities are refined andscreening is performed more routinely.

Coccidioidomycosis, caused by the soilfungus C. immitis was diagnosed as a pri-mary cause of death in only one otter (1%)during our study period. In otters exam-ined from 1992–95, eight cases had severedisseminated coccidioidomycosis (Thomasand Cole, 1996), so there may be somevariation in mortality due to this pathogen.

Our approach of identifying more thanone primary cause of death in sea otterswith two equally severe, yet independent,causes of death has resulted in slightlyhigher proportionate mortality for someconditions than if diagnoses had been lim-ited to one primary cause of death per ot-ter. This strategy allowed for an unbiasedaccount of important causes of death, butthe proportionate mortality reported heremay not be comparable to mortality stud-ies using more traditional methods. Also,many of these causes of mortality may besubject to substantial inter-annual varia-

tion and other causes of mortality are like-ly to be identified retrospectively as newdiagnostic techniques are developed andimplemented as screening tools.

In this study, carcasses were recoveredprimarily along accessible sandy shores.Sea otter carcasses are not likely to washashore along rocky precipitous coastlinesand those that do are not likely to be re-covered while in fresh condition becausemost of these areas are not readily acces-sible. Therefore, very little is known ofcauses of mortality in sea otters livingalong the rocky and remote coastline inthe center of the sea otter range in Cali-fornia. A directed search effort would benecessary to collect fresh carcasses fromthese unpopulated and inaccessible areas.An estimated one-half of all recently de-ceased sea otters were recovered as beach-cast carcasses, and one-fourth of thesewere retrieved in adequately fresh condi-tion to allow detailed necropsy for specificcause of death determination (Estes et al.,2003). Based on these estimates and thespecific inclusion criteria for this study, ap-proximately one of ten deceased southernsea otters was evaluated. Because the agedistribution of carcasses reported hereclosely matches the age distribution of allcarcasses recovered recently (Estes et al.,2003), the carcasses included in this studyare likely to be representative of all recov-ered carcasses. Consequently, the majorcauses of death reported here are probablysimilar to what would be observed if de-tailed cause of death information could beobtained from decomposed or heavilyscavenged carcasses. While a relativelyhigh proportion of the population wasavailable for cause of death determination,certain causes of death, such as drowningdue to accidental entanglement in fishtraps or nets, may be under-represented inbeachcast carcasses. These carcasses maybe less likely to float and wash ashore priorto decomposing, and drowning is very dif-ficult to document even with detailed nec-ropsy. Therefore, the cause-specific pro-portionate mortality reported here may


not be directly referable to the southernsea otter population.

Identification of pathogens responsiblefor substantial morbidity and mortality insea otters and the geographic distributionof these pathogens is an important firststep toward understanding the role of pop-ulation health in the recovery of thisthreatened species. However to fully un-derstand the underlying mechanisms cre-ating the observed pattern of mortality,factors that may be affecting nutrition, im-mune system competency, and sources ofincreased pathogen exposure must be eval-uated. Studies have detected elevated tis-sue levels of potentially immunotoxic con-taminants in southern sea otters with in-fectious disease (Kannan et al., 1998; Nak-ata et al., 1998), but immune systemfunction in wild animals is difficult to mea-sure because species-specific tests must bedeveloped and validated for different ageclasses.

The high percent of prime-aged adultsamong beachcast sea otter carcasses inCalifornia, and the very high prevalence ofdisease noted in this age class are not con-sistent with a healthy population destinedfor recovery. Sea otter populations expe-riencing a decline from increased levels ofmortality typically have a high percent ofprime-aged adults among beachcast car-casses (Estes et al., 2003). Certainly, theprevalence of acanthocephalan-related dis-ease in juveniles and the prevalence of T.gondii encephalitis, cardiac disease, andshark attack in prime aged adults have thepotential to exert a population-level effectand may be limiting sea otter populationgrowth in California. The underlying pro-cesses promoting increased levels of par-asitic disease in sea otters should be a fo-cus of future investigation. Special atten-tion should be given to non-native terres-trial species that are endemically infectedwith protozoal pathogens and have the ca-pacity to serve as a reservoir for persistentexposure and infection in sea otters. Re-covery of the southern sea otter populationmay face a significant challenge as this iso-

lated population struggles to expand in anear-shore system that may have been sub-stantially altered in terms of prey abun-dance, water quality, and pathogens in thetime since the near-extirpation and earlyrecovery of sea otters.

ACKNOWLEDGMENTS

This work was made possible by the timelyretrieval of beachcast sea otters by staff andvolunteers at the California Department ofFish and Game, the United States GeologicalSurvey, the Monterey Bay Aquarium, and TheMarine Mammal Center. We also thank N.Kock who examined additional fresh sea ottercarcasses; E. Dodd and N. Ottum for technicalassistance; and J. Estes for his discussion andcritical review of this manuscript. Funds wereprovided by the University of California MarineCouncil Coastal Environmental Quality Initia-tive Program, the Morris Animal Foundation,and the PKD Trust.

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Received for publication 20 August 2002.

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PATTERNS OF MORTALITY IN SOUTHERN SEA OTTERS … · cephalitis, acanthocephalan-related disease, shark attack, and cardiac disease were identiﬁed as common causes of death in sea