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SPONDYLITIC CHANGES IN LONG-FINNED PILOTWHALES (GLOBICEPHALA MELAS) STRANDED ONCAPE COD, MASSACHUSETTS, USA, BETWEEN 1982AND 2000

Authors: Sweeny, Melinda M., Price, Janet M., Jones, Gwilym S.,French, Thomas W., Early, Greg A., et al.

Source: Journal of Wildlife Diseases, 41(4) : 717-727

Published By: Wildlife Disease Association

URL: https://doi.org/10.7589/0090-3558-41.4.717

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717

Journal of Wildlife Diseases, 41(4), 2005, pp. 717–727q Wildlife Disease Association 2005

SPONDYLITIC CHANGES IN LONG-FINNED PILOT WHALES(GLOBICEPHALA MELAS) STRANDED ON CAPE COD,MASSACHUSETTS, USA, BETWEEN 1982 AND 2000

Melinda M. Sweeny,1 Janet M. Price,2 Gwilym S. Jones,3 Thomas W. French,4 Greg A. Early,1

and Michael J. Moore1,5

1 Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA2 Sepracor, Inc., 84 Waterford Dr., Marlborough, Massachusetts 01752, USA3 Northeastern University, Biology Department, 650 Huntington Ave., Boston, Massachusetts 02115, USA4 Division of Fisheries and Wildlife, 1 Rabbit Hill Rd., Westborough, Massachusetts 01581, USA5 Corresponding author (email: mmoorewhoi.edu)

ABSTRACT: The primary bone pathology diagnoses recognized in cetacea are osteomyelitis andspondylosis deformans. In this study, we determined the prevalence, type, and severity of ver-tebral pathology in 52 pilot whales, a mass stranding species that stranded on Cape Cod, Mas-sachusetts, between 1982 and 2000. Eleven whales (21%) had hyperostosis and ossification oftendon insertion points on and between vertebrae, chevron bones, and costovertebral joints, withmultiple fused blocks of vertebrae. These lesions are typical of a group of interrelated diseasesdescribed in humans as spondyloarthropathies, specifically ankylosing spondylitis, which has notbeen fully described in cetacea. In severe cases, ankylosing spondylitis in humans can inhibitmobility. If the lesions described here negatively affect the overall health of the whale, theselesions may be a contributing factor in stranding of this highly sociable species.

Key words: Ankylosing spondylitis, diffuse idiopathic skeletal hyperostosis, Globicephala me-las, long-finned pilot whale, stranded, vertebral pathology.

INTRODUCTION

Pilot whales, Globicephala melas, arehighly social, traveling in pods of relatedmembers (Amos et al., 1993), and theystrand both singly and en masse (Robson,1984). A single whale may strand as a re-sult of disease, starvation, or abandonment(Geraci and Aubin, 1977). Mass strandingsof pilot whales have been attributed to anumber of causes, including navigationalerror, such as disturbance to the echolo-cation system or coastal geomagnetic char-acteristics (Bernard and Reilly, 1999), orunfamiliarity with an area while feeding ormigrating in or near shore (Dawson et al.,1985). Mass strandings have also beenthought to be initiated by a sick (Duignanet al., 1995) or injured individual of a pe-lagic and tightly social species such as thepilot whale (Robson, 1984). Such a sick in-dividual could subsequently induce othergroup members, healthy or sick, to comeashore (McLeod, 1986). Mass strandingsof pilot whales occur on Cape Cod, Mas-sachusetts (McFee, 1990; Wiley et al.,2001), among other places. Between 1982

and 2000 there were 14 mass strandingevents and 56 single strandings in the NewEngland region. All 14 mass strandings oc-curred on Cape Cod, with 50% (7/14) onWellfleet beaches, 36% (5/14) on Easthambeaches, and 14% (2/14) in Barnstable. Ofthe single strandings 16% (9/56) occurredin Wellfleet, 9% (5/56) in Eastham, 11%(6/56) in Truro, 5% (3/56) in Province-town, 28% (10/56) in various other loca-tions in Massachusetts, and 41% (23/56) inother locations, including Maine andRhode Island (Rubenstein, pers. comm.).Most single strandings resulted fromwhales that had previously died at sea andwashed ashore dead.

There has been no systematic review ofthe vertebral pathology of specimens ofmass-stranded individuals in Massachu-setts. It is unclear if specific pathology mayunderlie some of these mass strandingevents. Full necropsy with histopathologyis often impractical because of the logisticconstraints associated with mass strand-ings. The goal of this study was to deter-mine if vertebral pathology was presentand, if present, whether it severe enough


718 JOURNAL OF WILDLIFE DISEASES, VOL. 41, NO. 4, OCTOBER 2005

FIGURE 1. Map of pilot whale stranding loca-tions, Cape Cod, Massachusetts, USA, and numberof stranded animals. (A) Campground Beach, Eas-tham; (B) Boatmeadow Creek, Eastham; (C) SquawIsland, Hyannisport; (D) Lieutenant Island, Wellfleet;(E) Eastham.

to compromise health and possibly inducea stranding event. In this study, cleanedpilot whale spinal columns were examinedto assess the nature and degree of verte-bral lesions.

MATERIALS AND METHODS

Vertebrae

Four hundred seventy pilot whales strandedon Cape Cod from 1982 to 2000 (Rubenstein,pers. comm.). Bones from 52 animals (fourmass stranding events, one single whale washedashore dead) were collected on beaches andmarshes of the eastern shore of Cape Cod Bay,Massachusetts, USA, from 1982 to 2000 (Fig.1). The time interval between stranding andcollection ranged from the time of stranding toas many as 6 yr. Bones were assigned to specificindividuals on the basis of contiguity at the timeof collection (Table 1). All bones were archivedeither at Northeastern University in Boston,Massachusetts (n551), or at the University ofArkansas (n51) and were identified by museumnumbers (and field numbers, when available).When collected, most bones had already beencleaned by natural decomposition. Bones (col-lected before 1990) with dried tissue remainswere boiled. After 1990, horse manure (fol-lowed by washing and drying) was used to re-move the remaining tissue.

Examination

Mature animals were recognized by the pres-ence of fused epiphyseal plates, while those

with incomplete fusion or unfused plates wereconsidered immature (Kompanje, 1995a). Thevertebral formula for G. melas has been re-ported as cervical (7), thoracic (11), lumbar(12–24), and caudal (28–29) (Tomilin, 1967).For this examination, the vertebral regionswere determined as follows: cervical vertebraewere highly compressed and naturally fused ei-ther C1-5, C1-6, or C1-7; thoracic vertebraehave articular facets for the ribs; lumbar ver-tebrae do not have articular facets for ribs orchevron bones; and the first 17 caudal verte-brae have articular facets for chevron bones,while the remainder are significantly reducedin size. Sex was determined either at the timeof stranding or by morphometrics of the ver-tebrae (Van Beusichem, 2000).

The gross examination of each vertebra in-cluded an assessment of smoothness and reg-ularity of surfaces, bilateral symmetry, anoma-lies, bone growths, fusion, fractures, or abnor-mal fistulae (Fig. 2). Any lesions found wereranked as follows: minor (those involving lessthan 10% of total vertebral surface area), mod-erate (involving 11% to 50% of vertebral sur-face area), and severe (covering greater than50% of the vertebral surface area with or with-out fusion of two or more vertebrae).

For each animal, the following informationwas recorded: museum identification number,spinal region, presence/absence of pathology,measurement of pathology, sex (when avail-able), epiphyseal fusion (maturity), and dateand location of stranding. Digital photographswere taken (dorsal, ventral, right lateral, andleft lateral views) of each bone with pathologyand of a subsample of normal bones. A subsam-ple of normal and diseased bones were radio-graphed as well as scanned with computed to-mography (Siemens Somatom Emotion, Mal-vern, Pennsylvania, USA). The contrast andpixel grayscale levels of scanned images wereadjusted to maximize the different structuralfeatures.

RESULTS

The number of vertebrae examined peranimal varied from 1 to 68; the maximumnumber expected was 71 (Tomilin, 1967).Gross examination revealed osseouschanges in 11 of 52 (21%) individuals ex-amined (estimated prevalence is 2165.6%)(Table 1). Osseous changes ranged fromdevelopment of minor osteophytes to se-vere ankylosis of vertebral bodies; threehad severe pathology (Table 1). In the 11animals with lesions, two of three atlas/axis


SWEENY ET AL.—SPONDYLITIC CHANGES IN PILOT WHALES 719

TABLE 1. Samples examined from pilot whales stranded on Cape Cod, Massachusetts, USA.

Museum ID No. Total vertebrae Pathology (yes/no [y/n] Sexa Epiphyseal fusion (y/n)

Mass stranded animalsLieutenant Island, Wellfleet—16 November 1982 (n566); 418539N, 708019W

NUVC 21512157217421732178

113211

nynnn

ffufu

yynyn

21762175217221712179

11531

nnnnn

uufff

nnyyy

21882189218621872190

11111

nnnnn

uuuuu

nnnnn

21602152215321162115

1 (At/Ax)a36363130

nynyy

ufff

m

uyyyy

21332131212421232128

3430

111

nnnnn

uuuuu

nnnnn

21272126212521292136

11111

nnnnn

fuuuu

ynnnu

21432130211717711772

156

1186

nnynn

fffuu

yyynu

18972344

121

ny

uf

ny

Mass Stranded AnimalsEastham-6 October, 1984 (n594) 418 499 N, 708 009 W

NUVC 2132 25 n f y211921212118219721982120

131611393119

nnnynn

umfff

m

nnyyyy

Mass stranded animalsBoatmeadow Creek, Eastham—3 December 1986 (n588); 418489N, 708009W

NUVC 22042345214821492150

Uarkb

5847474354

61 1 At/Ax

nynnyy

fmffff

nyyyyy

Mass stranded animalsSquaw Island, Hyannisport—12 December 1990 (n556); 418379N, 708199W

NUVC 2340 61 n u nSingle stranded animalsCampground Beach, Eastham—16 March 2000 (n51); 418519N, 708009W

NUVC 4247 44 1 At/Ax y f y

a f 5 female; m 5 male; u 5 unknown; At/Ax 5 atlas/axis.b Uark 5 University of Arkansas.



FIGURE 2. Gross morphology of pilot whale vertebrae. (a) Anterior view of normal pilot whale caudal vertebra(Ca6) (same sample as 3a and 4a) (NUVC 2157). (b) Posterior view of pilot whale lumbar vertebra (L11). Notesubchondral cysts of vertebral body and periarticular syndesmophytes (same sample as 3c) (NUVC 4247). (c) Ventralview of pilot whale thoracic vertebra (T9). Note bony growth and erosion of distal transverse processes; morepronounced on the left. (NUVC 2345). (d) Right lateral view of four fused pilot whale caudal vertebrae (Ca9-12).Note syndesmophyte production and ankylosis (same sample as 4b, 4c, and 4d) (NUVC 4247).



bones, nine of the 45 (20%) cervical ver-tebrae complexes, 22 of the 77 (29%) tho-racic vertebrae, 21 of the 103 (20%) lum-bar vertebrae, 33 of the 120 (28%) caudalvertebrae, and one of one chevron boneshad lesions. Pathology was present in boththe naturally fused and unfused cervicalvertebrae. Both NUVC 4247 (singlestranding) and UArk (mass stranding),which had lesions in all regions, had cer-vical vertebrae that were fused normallybut also exhibited abnormal bony growthand erosion.

The presence of skeletal abnormalitieswas not associated with any particularstranding location or date (Table 1). Threeof the four mass stranding events (all ofwhich occurred between October and De-cember) had at least one whale with le-sions. The only mass stranding withoutbone pathology was at Squaw Island,Hyannisport, Massachusetts, where onlyone of 56 stranded whales was examined,and this animal was a calf. Animals withlesions were from Lieutenant Island, Well-fleet (six of 38 whales examined, 16%);Eastham 1984 (one of six examined, 17%);Boat Meadow Creek, Eastham (three ofsix examined, 50%); and CampgroundBeach, Eastham (one single strandedwhale). Three of six spatially related indi-viduals from the 3 December 1986 strand-ing at Boat Meadow Creek had bone le-sions.

Of the 427 animals that mass strandedon Cape Cod between 1982 and 2000, 234(55%) were females, 95 (22%) were males,and 98 (23%) were of undetermined sex(Rubenstein, pers. comm.). The 52 whalessampled included 23 females (44%), fourmales (8%) and 25 animals of unknown sex(48%); 24 (46%) were immature, 25 (48%)were mature, and three (6%) were of un-determined age. Of the 11 animals withlesions, nine were females (82%), twowere males (18%), and all were mature.

Some radiographs revealed a ’moth-eat-en’ appearance in the vertebral body, sug-gestive of osteoporosis (Fig. 3b, c), as wellas peridiscal vacuolization (i.e., pitting;

Fig. 3b–d). The computed tomographyscans illustrated significant loss of inter-vertebral disk space and ossification (whiteareas) of the intervertebral disk in thefused caudal vertebrae of NUVC 4247(Fig. 4c, d). Decreased central ossificationin the vertebral body, also suggestive of os-teoporosis (darker areas), was apparent insome specimens, along with peridiscal vac-uolization (Fig. 4b, d). Bony excrescencesappear to merge from the dorsal and ven-tral vertebral margins, while leaving radio-lucent areas at the level of the interverte-bral disk spaces.

DISCUSSION

Understanding the pathobiology ofbeached and beaching marine mammals iscritical to their management. In the caseof mass stranded odontocetes, understand-ing clinical observations is important fortriage on the beach, possible treatment re-gimes, and in prognosis for recovery. Inthis study, vertebral lesions were found inat least 21% of pilot whales examined. Thisobservation raises the following issues: 1)quality of the data, 2) differential diagnosisand pathogenesis of the lesion, 3) whetherthe lesions impair mobility, and 4) if thelesions initiate stranding behavior.

Data quality

At the time of collection, available ver-tebrae per carcass ranged in number fromone to an entire set. These results aretherefore a conservative estimate of bothseverity and prevalence of bone pathology,as we do not know the condition of themissing vertebrae and/or other animals inthe stranding. Although collection of skel-etal parts was undertaken systematically,some vertebrae may be from one individ-ual, despite being represented by severaldifferent identification numbers, sincebones are sometimes scattered by tidal ac-tion or scavengers. Such an overestimationin total number of individuals would alsorender the results conservative. If the totalnumber of animals was overestimated, theactual prevalence of pathology would be



FIGURE 3. X-radiographs of pilot whale vertebrae. (a) Posterior view of normal pilot whale caudal vertebra(Ca6) (same sample as 2a and 4a) (NUVC 2157). (b) Anterior view of pilot whale lumbar vertebra (L12).Note ’moth-eaten’ osteoporotic body (NUVC 4247). (c) Posterior view of pilot whale lumbar vertebra (L11)Note vacuolization, dark area in upper mid-body and osteoporotic body (same sample as 2b). (NUVC 4247).(d) Anterior view of pilot whale caudal vertebra (Ca15). Note ’shaggy’ vertebral rim and narrowing of theneural canal. (NUVC 2344).



FIGURE 4. Computed tomographs of pilot whale vertebrae. (a) Anterior view of normal pilot whale caudalvertebra (Ca 6) (same sample as 2a and 3a) (NUVC 2157). (b) Anterior view of mid-body of one of four fusedpilot whale caudal vertebra (Ca 9-12). Note hyperostosis of the spinal process, subchondral cysts, and oste-oporosis (same sample as 2d, 4c, and 4d) (NUVC 4247). (c) Anterior view of intervertebral disk of one offour fused pilot whale caudal vertebra (Ca 9-12). Note syndesmophyte production and ossification of inter-vertebral disk (same sample as 2d, 4b, and 4d) (NUVC 4247). (d) Lateral view of four fused pilot whalecaudal vertebrae (Ca 9-12). Note syndesmophyte bridging between vertebrae, ossified intervertebral discs,and subchondral cysts in the body (same sample as 2d, 4b, and 4c) (NUVC 4247).



higher. It is also possible that the totalnumber of animals was underestimated,where multiple vertebrae were thought torepresent different individuals but wereactually from one animal. Spatial separa-tion at the time of collection makes thisunlikely.

Conservative or not, the data reveal thata large number of pilot whales stranded onCape Cod had bone pathology. Pathologyhas also been reported in bones from pilotwhales driven onto Newfoundland shores,the difference being that only one case ofsevere bone pathology (a block of fourfused vertebrae) was found among hun-dreds of carcasses and bones in a ‘‘grave-yard of flensed bones’’ (Cowan, 1966).Those pilot whale carcasses were left froma whale drive fishery, rather than from’naturally’ stranded pilot whales. Anothersource of nonstranded pilot whale carcass-es is from the Faroe Islands, where a tra-ditional drive fishery of pilot whales hasbeen maintained since the archipelago wasinhabited 1,000 yr ago (Bloch, 1998); nobone pathology has been reported fromthose pilot whales driven ashore (Bloch,pers. comm.). The stock structure of theNorth Atlantic long-finned pilot whalepopulation is uncertain (Fullard et al.,2000), but Fullard et al. (2000) have pro-posed a stock structure that is correlatedto sea surface temperature, including acold-water population west of the Labra-dor/North Atlantic current and a warm-water population extending across the At-lantic in the Gulf Stream. Therefore, pilotwhales from the Faroe Islands, Newfound-land, and those that stranded on Cape Codmay belong to the same population. Con-sidering the number of lesions found inthe present study, it is noteworthy that pa-thology has not been reported from non-stranding sources of potentially the samepopulation.

Differential diagnosis

Although there are no other studies in-volving stranded, by-caught, or captive pi-lot whale bone pathology, there are studies

on other stranded cetaceans with bony le-sions, the diagnoses for which includespondylitis (Paterson, 1984), spondylosisdeformans (Kompanje, 1995a), osteomye-litis (Kompanje, 1995b), and discospon-dylitis (Alexander et al., 1989). The differ-ential diagnosis for the lesions describedhere includes osteomyelitis, spondylosisdeformans, diffuse idiopathic skeletal hy-perostosis (DISH), and ankylosing spon-dylitis (AS).

Vertebral osteomyelitis can have effu-sive bony growth and pitting, as seen inthese cases; however, osteomyelitis doesnot usually span more than two vertebraebecause of the resistive properties of in-tervertebral discs (Jubb et al., 1992). Inthis case, there are multiple animals withblocks of three and four fused vertebrae.In the case of spondylosis deformans, thecostovertebral or apophyseal joints are notinvolved, and the intervertebral discs donot typically calcify (Resnick and Niwaya-ma, 1988c). In this study, intervertebraldisk calcification and costovertebral jointlesions are present. Therefore, both oste-omyelitis and spondylosis deformans canbe ruled out.

Diffuse idiopathic skeletal hyperostosisis characterized by flowing or undulatingcalcification and ossification along the ven-trolateral aspect of at least four contiguousvertebral bodies, with relative preservationof intervertebral disk height in the in-volved vertebral segments. Additionally,there is an absence of apophyseal jointbony ankylosis (Resnick, 2002b). Lucentareas between the ossified ventral longi-tudinal ligament and ventral vertebral sur-faces are also characteristic (Resnick,2002b). Lesions in this study are presentin apophyseal joints as well as interverte-bral discs; therefore, DISH can also beruled out.

The lesions found in this study havecharacteristics of AS. This disease belongsto a group of diseases in humans known asspondyloarthropathies; this group of dis-eases involves inflammation and eventualankylosis of the sacroiliac joints (absent in



cetacean), costovertebral joint changes,calcification of intervertebral discs, and os-teoporosis (Resnick and Niwayama,2002a). Ankylosing spondylitis is describedas a chronic, nonpurulent inflammatorydisease of the axial joints and both sacro-iliac joints in quadrupeds (Wollheim,1993).

In humans, AS characteristically showsossification within the annulus fibrosus inthe form of syndesmophytes. This beginswith cellular infiltration of plasma cells andlymphocytes, followed by fibrin accumu-lation and swelling in the outer layer of theannulus fibrosus; chondrocytes then format the junction of the intervertebral diskand vertebral edge and, in the later stagesof disease, these chondrocytes undergocalcification, with eventual bridging toneighboring vertebral joints (Resnick andNiwayama, 2002a). Joints affected by ASinclude the discovertebral junctions, cos-tovertebral joints, and apophyseal joints,with potential fusion throughout the ver-tebral column (Resnick and Niwayama,2002a) caused by inflammation not only inthe joints but also in the entheses (i.e., lig-ament and tendon insertion points; Wol-lheim, 1993). As entheses become in-flamed (enthesitis), they can eventually os-sify, producing syndesmophytes, potential-ly forming a ‘‘bony’’ bridge betweenvertebrae (Resnick and Niwayama, 1988a);periostitis at the entheses is also observed.Radiographically, lesions can result in ir-regular or ‘‘shaggy’’ periarticular surfaces(Fig. 3d; Resnick and Niwayama, 1988a)with thin, flowing syndesmophytes extend-ing from one vertebral body to the next,with surrounding eburnation (i.e., thick-ening) and excessive discal calcification(Fig. 4c). While the bone surface has pro-duced extra bone, internally there is a lossof trabecular density (i.e., osteoporosity;Figs. 3b, 4b) within the vertebral body(Khan, 1993b).

At the onset of AS, clinical signs in af-flicted humans include anorexia, weightloss, and a low-grade fever. As the diseaseprogresses, 25–30% of humans develop

anterior uveitis, inflammation of the as-cending aorta and aortic valve, fibrosis andcavitation in the upper lobes and pleuritisof the lungs, and amyloid involvement ofthe kidneys (Resnick and Niwayama,2002a). In humans, AS is caused by a ge-netically determined immune response toenvironmental factors (Resnick and Ni-wayama, 2002a). It has been suggestedthat some gram-negative bacteria, such asKlebsiella sp., may play a role in triggeringankylosing spondylitis, but the supportingevidence is controversial (Khan, 1993a).Examination of extraskeletal tissues wasnot possible in this study.

In this study of pilot whales, lesions arepresent in both costovertebral and discov-ertebral joints; in addition, there is calci-fication of intervertebral joints, osseouserosions, osteoporosis, and bony lesionsthat cross more than one intervertebralspace, all features that are consistent withAS.

Effects on mobility

In humans, AS can cause pain and stiff-ness as well as debilitation (Resnick andNiwayama, 2002a). Assuming spinal flexi-bility has importance to other mammals,including pilot whales, the effects on mo-bility could be more significant. The prin-cipal locomotory organ of whales is thebody axis (i.e., the vertebral column, spinalmuscles of the back, and tail flukes) (Sli-jper, 1961). Cetaceans produce thrust byvertical movements of the tail and flukes(as opposed to the lateral strokes of fish)(Arkowitz and Rommel, 1985). An anky-losed spine not only causes a decrease inspinal mobility, but it also creates vulner-ability as a result of a rigid vertebral col-umn that cannot bend or rotate on impactto absorb traumatic stress (Resnick,2002a). In the case of AS, the rigidity ofthe spine in fused sections also causesmore vulnerability to fracture and osteo-porosis (both present in this study) in oth-er sections of the vertebral column (Palm-er, 1990). The complication of likely spinalpain and fusion is serious for any organism



that must swim without an opportunity torest to allow bone pathology to heal, incontrast to terrestrial mammals. Such painis likely, even though pilot whales are es-sentially weightless in water, as the rib andchevron bones are force-bearing analoguesacting as compression members on thevertebrae while the animal flexes and ex-tends the vertebral column to swim.

Consequences of mass stranding

Bone pathologies have been document-ed in single stranded cetaceans (Kompan-je, 1995a). Thus, a pilot whale with a se-verely compromised vertebral column maybe likely to strand. However, would suchan animal’s beaching lead the healthy, re-lated members inshore? Mass strandingsof pilot whales have involved morbillivirusinfection (Duignan et al., 1995), parasiticnerve damage (Morimitsu et al., 1987),and physical, clinical, and histologic evi-dence of illness (Walsh et al., 1991). Nostudies to date have investigated chronic,noninfectious diseases in mass strandings.This study reveals that over the past 18years, 88 vertebrae from 11 animals andfive separate pilot whale stranding eventsshowed bone disease suggestive of AS thatmay have affected the whales’ mobility.

There is a need for further investigationof the skeletal and extraskeletal features ofankylosing spondylitis and other osteologicpathology in pilot whales and other speciesof whales and dolphins. Histopathologicexamination of periarticular and extraske-letal tissue for inflammatory changes, im-munopathologic histochemistry, and moreextensive epidemiologic studies are allneeded to better understand the role ofthe observed changes in the mass strand-ing events commonly observed in this spe-cies.

ACKNOWLEDGMENTS

Thanks are due to Michael Scherer and Ma-rine Research, Inc., to William Henry and Buz-zards Bay Animal Hospital, and to DarleneKetten, Scott Kramer, and Julie Aruda. We alsothank Nancy McCartney at the University ofArkansas (Accession number 88-52-1). This

study was funded in part by NOAA FisheriesGrant NA03NMF4390046. Conclusions andrecommendations are those of the authors anddo not necessarily reflect the views of theNOAA. Samples were collected under NationalMarine Fisheries Service authorization to theNew England Aquarium. This paper representsWoods Hole Oceanographic Institution contri-bution number 11299.

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Received for publication 2 July 2004.


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