gross and histologic evidence of sharp and...

37

Journal of Zoo and Wildlife Medicine 39(1): 37–55, 2008Copyright 2008 by American Association of Zoo Veterinarians

GROSS AND HISTOLOGIC EVIDENCE OF SHARP AND BLUNTTRAUMA IN NORTH ATLANTIC RIGHT WHALES (EUBALAENAGLACIALIS) KILLED BY VESSELS

Regina Campbell-Malone, Ph.D., Susan G. Barco, M.S., Pierre-Yves Daoust, D.V.M., Ph.D., Dipl.A.C.V.P., Amy R. Knowlton, M.M.A., William A. McLellan, B.A., David S. Rotstein, D.V.M.,M.P.V.M., Dipl. A.C.V.P., and Michael J. Moore, Vet. M.B., Ph.D.

Abstract: Vessel-whale collision events represented the ultimate cause of death for 21 (52.5%) of the 40 NorthAtlantic right whales (Eubalaena glacialis) necropsied between 1970 and December 2006. Injuries seen in vessel-struck whales fall into two distinct categories: 1) sharp trauma, often resulting from contact with the propeller, and 2)blunt trauma, presumably resulting from contact with a vessel’s hull. This study analyzes four trauma cases that resultedfrom vessel-whale collisions, which together provide a framework for a more critical understanding of lethal blunt andsharp trauma resulting from vessel collisions with right whales. In case no. 1, contact with a propeller resulted in threedeep lacerations. The animal survived acute trauma only to succumb nearly 14 years later when the lesions reopenedand became infected. In case no. 2, anecdotal reports linked the laceration of large arteries of the peduncle and histologicevidence of perimortem trauma at a bone fracture site to vessel-whale collision trauma. Case no. 3 had a laceration ofthe oral rete and a fracture of the rostrum. Both of the areas displayed histologic evidence of perimortem blunt trauma.Finally, in case no. 4, an antemortem mandibular fracture, two additional skull fractures, and widespread hemorrhagewere consistent with severe blunt trauma. Evidence from each case, including the timing of trauma relative to the timeof death and identifying characteristics of both trauma types, are presented. Before this study, no detailed comparativeanalysis of trauma pathology that resulted from lethal interactions between vessels and right whales had been conducted.This study demonstrates the importance of detailed gross and histologic examination in determining the significanceand timing of traumatic events. This work represents a new paradigm for the differential diagnosis of lethal sharp andblunt trauma in right whales hit by ships and will enhance the present understanding of the impact of anthropogenicmortality on this critically endangered species.

Key words: Eubalaena glacialis, fracture, propeller, right whale, ship-strike, trauma.

INTRODUCTION

The North Atlantic right whale (Eubalaena gla-cialis) population, currently composed of fewerthan 400 known individuals, is inhibited from re-covery by low reproductive success and high an-thropogenic mortality that may contribute to the ex-tinction of the species within 200 years.5,10,18–20 Thetwo primary sources of anthropogenic mortalityidentified in this population include entanglementin fishing gear and vessel-whale collisions.15,18–20,26

Between 1970 and December 2006, 21 right

From Brown University, Providence, Rhode Island02912, USA (Campbell-Malone); the Woods Hole Ocean-ographic Institution, Woods Hole, Massachusetts 02543,USA (Campbell-Malone, Moore); the Virginia Aquariumand Marine Science Center, Virginia Beach, Virginia23451, USA (Barco); the University of Prince Edward Is-land, Charlottetown, Prince Edward Island C1A 4P3, Can-ada (Daoust); the New England Aquarium, Boston, Mas-sachusetts 02110, USA (Knowlton); the University ofNorth Carolina Wilmington, Wilmington, North Carolina28403, USA (McLellan); and the University of Tennessee,Knoxville, Tennessee 37996, USA (Rotstein). Correspon-dence should be directed to Regina Campbell-Malone([email protected]).

whales were involved in fatal vessel-whale colli-sions as determined by necropsies.26,30 Because thisrepresents the cause of death of more than half(52.5%) of the 40 individuals necropsied duringthat time period, the reduction of vessel-whale col-lision mortality has been identified by the UnitedStates and Canadian governmental agencies as animportant goal of their respective right whale man-agement programs.7,20,27,28

Physical trauma seen in right whales struck byvessels falls into two distinct, although not mutu-ally exclusive, categories: sharp trauma and blunttrauma. Sharp trauma is caused when sharp under-water protuberances, including propellers and rud-ders, come into contact with the animal. Propellertrauma occurs when the rotating blades of the ves-sel’s screw incise the soft tissue, and sometimes thebone, of the animal. This type of trauma providesthe most obvious external evidence of injury. Blunttrauma results when the animal is struck by the hullof the vessel. These events typically leave little ex-ternal evidence of the injury, even in the most se-vere cases, because of the thickness of soft tissueand the dark pigment of much of the epidermis,which tends to obscure evidence of swelling andbruising.26

38 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 1. Characteristic propeller trauma in living and dead right whales. a. Propeller wounds to the left fluke ofright whale Eg no. 2425. Note the series of parallel curved cuts that are typical of propeller wounds. Photographer:Monica Zani, New England Aquarium. b. Right whale calf RKB1424 was reportedly struck by a 25-m vessel withtwin screws turning to make 15 knots. Two series of deep propeller cuts were observed. Photograph from Moore etal. 2005. Photographer: Robert Bonde, U.S. Geological Survey.

Although the earliest confirmed case of lethalsharp trauma in right whales is from 1976, propellerinjury in large whales of known and unspecifiedspecies (which, therefore, may have included rightwhales) can be found in the literature dating as farback as 1877.22 Sharp trauma results in peracutetissue damage, with variable levels of severity,ranging from mild nonfatal ‘‘knicks’’ to severe im-mediately lethal wounds, or more chronic sequelae

(see Case study I). Damage from a turning propel-ler leaves a characteristic series of more or less par-allel, evenly spaced, curved (s-shaped or z-shaped)cuts that deepen at the center and become shallowtoward the margin, as seen in Figure 1 (Wood, pers.com.).23 Propeller laceration margins may extend tovariable levels of the epidermis, hypodermis, blub-ber, or skeletal muscle.

Analysis of epidermal scarring suggests that 7%

39CAMPBELL-MALONE ET AL.—TRAUMA IN RIGHT WHALES KILLED BY VESSELS

of the population has healed wounds that are con-sistent with sublethal sharp trauma.14,19 In minorcases, sharp trauma can lead to blood loss, infectionvia open wounds, scarring, and behavioral responseto contact, including avoidance of a stimulus.18,22,26

In severe cases, sharp trauma can lead to deep dis-ruption of underlying soft tissue, extensive bloodloss, and dismemberment. Lethal cases may involvesevere damage to the vertebral column or the axialmuscle, resulting in reduced locomotor function, or,in extreme cases, the complete separation of theanimal into two parts.

Blunt trauma that results from a vessel-whalecollision is marked by hemorrhage, edema, and, of-ten, a concomitant premortem fracture or displace-ment of skeletal elements. Hemorrhage and edemamay be observed in the affected blubber, subdermalsheath, and skeletal muscle. Generally, the epider-mis is not disrupted, and there is little external ev-idence to indicate the presence or the extent of sub-dermal injury, although swelling and bruising areat times evident externally. For this reason, com-plete forensic necropsy, including systematic flens-ing and examination of soft tissue and skeletal el-ements, is the only true diagnostic tool availablefor the differential diagnosis of trauma from a ves-sel-whale collision as the primary cause of deathwhen a collision was not documented.25,26 Internalviscera are often autolyzed in these rapidly decom-posing carcasses, although evidence of traumaticperforations of the gastrointestinal tract or activeforaging may provide insight into the perimortemdisposition of the whale.13

Previously, the standard classification of injuryfrom vessel collisions with right whales includedfour somewhat overlapping and often coincidentcategories, namely, 1) acute propeller trauma, 2)severed fluke, 3) bone fracture, and 4) hemorrhageand hematoma.18 At this time, there is no detailedanalysis of the nature or timing of trauma pathologythat resulted from lethal interactions with sharp andblunt vessel structures. This study analyses fourtrauma cases and provides a framework for a morecritical definition of lethal blunt trama and sharptrauma in right whales. The characterization of in-juries seen in right whales struck by vessels willaid prosectors in assessing future necropsy findingsof tissue trauma and linking them to their under-lying causes and timing of trauma relative to thetime of death. Future determinations based on thistrauma classification scheme will provide more ac-curate vessel-whale collision mortality statistics andwill help inform managers of the impact of vessel-whale collision mitigation efforts.

MATERIALS AND METHODS

The examination of the four animals discussedhere was conducted according to the currently ac-cepted right whale necropsy protocol to the extentpractical.25 Lesions, including affected and unaf-fected margins, were sampled for histology. Thecondition of the carcass was evaluated according tostandard condition codes for marine mammals.13

The condition of the remains is not directly pro-portional to the time since death but, instead, cat-egorizes the appearance of the carcass. Code twois fresh. Code three is moderately decomposed.Code four is significantly decomposed. Code fiveis mummified. Necropsy reports for these animalsinclude the known history of the animal, based onprior reports and field observation, carcass discov-ery and retrieval, and gross necropsy. Each reportculminates with the findings of postnecropsy labo-ratory analyses and diagnosis. These reports can beobtained via a request for data access to the RightWhale Consortium.30

RESULTS

The forensic necropsy observations and test re-sults of four individual North Atlantic right whalesthat suffered trauma from vessel strikes and thatwere examined between October 2003 and January2005 are presented below, beginning with the mostrecent case. Available life history data for each caseare summarized in Table 1.

Case study I—Eg no. 2143

Eg no. 2143 was first sighted in 1991 as a calfwith its mother in the right whale calving groundsoff the southeastern U.S. coast. At that time, it hadthree deep, open wounds on its left flank that hadthe characteristic parallel pattern and curvature ofpropeller wounds. Despite the severity of thesewounds and a poor prognosis for survival, Eg no.2143 was resighted in the Bay of Fundy 6 monthslater and was observed each consecutive yearthrough 2003. It was last seen alive on 5 January2005 off the Florida coast. At the time of its death,the animal was pregnant with its first known fetus.The code three carcass of Eg no. 2143 was found30 km east of Cumberland Island, Georgia, on 12January 2005.

Three large, healed propeller wounds were visi-ble on the left abdominal wall and were perpendic-ular to the long axis of the animal (Fig. 2). Thecranial-most lesion consisted of inactive scar tissueand was limited to the dorsum. When in the supineposition, the lesion was not visible. The centralwound was also composed of inactive uncompro-


Table 1. Life history and necropsy findings from four right whales killed by vessels.

Eg no. Necropsy location and date Sex Age, ya Pregnant?Condition

code Comments

2143 Cumberland Island, GeorgiaJan 2005

F 13 Yes 3 Sharp trauma. Succumbed to sequelae ofpropeller trauma nearly 14 years afterinjury.

1909 Ocean Sands, North CarolinaNov 2004

F 14 Yes 3 Blunt trauma. Left fluke blade complete-ly severed. Proximal caudal margin ofright fluke lacerated. Vessel collisionreported—mechanism unspecified.

1004 Nags Head, North CarolinaFeb 2004

F 29� Yes 3 Blunt trauma. Extensive hemorrhageseen in subdermal sheath. Fracturedrostrum, premaxilla, and vomer. Lac-eration of oral rete.

2150 Culloden Cove, Nova Scotia,Canada Oct 2003

F 12� No 4 Blunt trauma. 1.5-m-long fracture ofcaudal aspect of cranium. Completefracture of right jawbone. Fracture ofleft rear vomer.

a Numbers followed by a ‘‘�’’ represent the ‘‘minimum age’’ for individuals first identified as juveniles or adults.

Figure 2. Close up of caudal (left) and central (right) propeller scars on left flank of right whale Eg no. 2143. Thewhale is oriented with the caudal end to the left of the image, cranial end to the right, lying on its dorsum with itsventral surface facing up. The caudal scar was opened from the epidermis through the subdermal sheath perpendicularto the longitudinal axis of the body. Copious ectoparasitic cyamids were associated with the wounds and are visiblehere as small beige dots. The caudal (left) and central wounds are visible here, the cranial-most scar is out of theframe. Photographer: Alicia Windham-Reid, Florida Fish and Wildlife Conservation Commission.


mised scar tissue and measured approximately 209-cm curved length. The cranial margin of the le-sion’s ventral origin was 585-cm from the center ofthe eye. The caudal lesion measured approximately210-cm curved length. The caudal margin of thelesion’s ventral origin was 687-cm from the centerof the eye. This lesion had an open region thatmade the axial muscle visible. Other than the pro-peller wounds, there were no significant findings ofhuman interaction, blunt trauma, or fractures.

The cervix and caudal margin of the uterus ap-peared normal, and a full-term female fetus wasfound in the thoracic cavity and was necropsiedseparately. It was suspected that the fetus wasforced cranially through a rupture in the diaphragm,perhaps as a result of the purging of gases associ-ated with putrefaction. The uterine horns, ovaries,cranial margin of the uterus, gastrointestinal tract(from the esophagus to the intestine), larynx, lungs,and trachea were not found.

The most remarkable finding was the caudal pro-peller lesion. The caudal scar extended between thedorsal and lateral lines at the level of the genitalslit. It included an active, open wound that exudedlarge amounts of green pus and was 53-cm longand 16-cm wide. The active region of the caudalscar was open from the epidermis through the sub-dermal sheath, which left deep axial muscle clearlyvisible. The dorsal margin of the active site was27-cm from the dorsal tip of the caudal lesion. Al-though the axial muscle examined in other parts ofthe body appeared normal, the muscle deep to thiswound was liquefied in a cranially oriented coneshape, and, when opened, it explosively releasedapproximately 5 L of tan mucopurulent debris. Torntendons and muscle fibers were associated withboth the cranial and caudal margins of the wound.The lesions and exudate were surrounded by hardconnective and scar tissue approximately 0.5-mthick.

Microscopic examination of cranial and caudalscar tissue revealed irregular and undulating super-ficial epithelium and neutrophilic infiltration of thepapillary and superficial reticular dermis (Fig. 3).There was extensive fibrosis, with little associatedinflammation in the middle and deep dermis andadipose tissue (Fig. 4).

Findings indicate that severe, sublethal propellertrauma had delayed but ultimately fatal complica-tions. Secondary intention wound healing may haveresulted in decreased strength and compromised in-tegrity of tissues injured by the propeller. Potentialcomplications, including sepsis secondary to bac-teremia via the open caudal propeller scar, likelyarose as a result of girth expansion during pregnan-

cy, which led to loss of scar tissue integrity, woundreopening, and severe infection.

Case study II—Eg no. 1909

Eg no. 1909 was first sighted as a calf in 1989.It was seen each consecutive year from 1989 to2003. It was last seen on 21 April 2003 in the GreatSouth Channel. At the time of its death, the cowwas pregnant with its first known fetus. The codethree carcass was found on shore 24 November2004 at Ocean Sands, North Carolina.

The left fluke blade was completely severed, andlarge dorsal and ventral arteries (2- to 3-cm in di-ameter) that originated in the tail stock were lac-erated and exposed along the midline (Fig. 5). Adeep, linear laceration was observed in the soft tis-sue superficial to the left caudal third of the ros-trum. The lesion extended through the epidermis,deep into the premaxilla. A small amount of tissuebridging was evident, and the exposed margins ofthe wound were brown-green in color, similar to thethick pasty fluid that coated the underlying bone.When viewed in dorsoventral cross section, mild,abruptly demarcated hemorrhage was observed,which extended 1 cm around the margin of the le-sion.

Examination of the blubber layer and postcranialskeletal elements revealed no additional evidenceof trauma. A linear soft tissue wound (approxi-mately 11.6-cm deep) was seen through the rostrumand the premaxilla. The linear laceration, perpen-dicular to the longitudinal axis of the body, extend-ed from the left lateral lip to the dorsal midline intothe premaxilla. This wound measured approximate-ly 1-cm wide by 15-cm long. This lesion was as-sociated with two lesions in the underlying boneand hemorrhage that extended 5-cm around thewound in the overlying soft tissue. The first bonelesion was a linear laceration into the premaxillathat measured approximately 1.5-cm across and8.5-cm long. A second lesion was a ‘‘v-shaped’’laceration into the left premaxilla.

A near-term female fetus, between 3- to 4-mlong, was found in the thoracic cavity and was nec-ropsied separately. As was discussed previously, inthe case of Eg no. 2143, postmortem decompositionand gas buildup presumably led to increased ab-dominal pressure and a rupture of the diaphragm,followed by extrusion of organs through the phar-ynx.

An analysis of soft tissue from the wound over-lying the premaxilla revealed marked necrotizingand hemorrhagic panniculitis. Also evident weremild multifocal hemorrhage in adipocyte lobulesand mild multifocal to coalescing intermysial ede-


Figure 3. Hematoxylin and eosin stained section of epithelium from propeller scar. Neutrophils (N) are present insmall aggregates and can be seen transmigrating through the epithelium (NT). Epithelial cells (EC) with intracytoplas-mic melanin are also visible. 400�. Photographer: David Rotstein, University of Tennessee.

ma, with separation of fine collagen bundles con-sistent with traumatic ‘‘stretching.’’ A bone samplefrom the damaged premaxilla had a comminutedfracture. Microscopic examination of decalcifiedbone revealed bone fractures that involved individ-ual or multiple trabeculae. The fracture marginswere irregular, and the margin surface was coveredwith extravasated erythrocytes and small amountsof an eosinophilic substance consistent with fibrin.

Laceration of the large vessels of the peduncleand tissue trauma to the rostrum and the premaxillasuggest extensive trauma to both the fluke and thehead, accompanied by significant blood loss, whichled to traumatic, hypovolemic shock. Extravasatederythrocytes, fibrin deposition, and trabecular frac-ture of the premaxilla support the acute, perimor-tem nature of these injuries as opposed to post-mortem or chronic lesions.

These findings are consistent with two reports ofa bleeding whale seen on 17 November 2004 andlater received by the Virginia Aquarium and Marine

Science Center Stranding Program. A general pub-lic report described a whale, with a fresh wound toits tail, that was moving slowly just off the coastof North Carolina. The whale was reportedly bleed-ing and was missing a large portion of its flukewhen seen at 12:00 PM. A second report receivedfrom the U.S. Navy 5 days later detailed a vessel-whale collision event that involved a Navy Am-phibious Assault Ship on 17 November 2004 at 10:46 AM. Global Positioning System coordinates fromthe public report placed the whale 4 nautical milessouthwest of the naval whale strike coordinates.The close proximity (in both time and space) makeit likely that the same whale was seen by both ves-sels and was in all probability Eg no. 1909 thatwashed ashore 7 days later.

Case study III—Eg no. 1004

Eg no. 1004 was first seen as an adult in 1975.Eg no. 1004 was last seen alive in the Great SouthChannel on 29 May 2003 and was pregnant with


Figure 4. Dermis from propeller scar. Within the superficial dermis, there is deposition of abundant mature collagen(C) with few entrapped adipocytes (A). 200�. Photographer: David Rotstein, University of Tennessee.

its sixth known offspring at the time of its death.The early code three carcass of Eg no. 1004 wasnecropsied in February 2004 in Nags Head, NorthCarolina.

There was no evidence of fresh or recent humaninteraction on the epidermis, although white, healedscarring from old fishing gear entanglements wasfound on the ventral peduncle and on the left sideat the angle of the mouth and trailed cranially tothe mid arch of the lingual surface of the left lip.The posterior insertion of both flippers also exhib-ited white, healed entanglement scars. There was aslight discoloration and bulging near the caudal in-sertion of the left mandible that was consistent withof subdermal edema. A deep incision through theepidermis, blubber, and muscle was made just cau-dal to the skull down to the atlanto-occipital joint,with the animal lying on its dorsum. This incisionrevealed substantial hemorrhage and edema in thesubdermal sheath that extended from the nuchalcrest through the right lateral midline to the ventralsubdermal sheath (Fig. 6).

There were areas of hemorrhage deep to theblubber on both the ventral and dorsal aspects ofthe animal at the level of the subdermal sheath andmuscle. Edema, corresponding to the externalswelling, was found in the subdermal sheath andmuscle overlying the left mandible (Fig. 7). Dorsaledema extended along the dorsal midline from theblowhole, caudally to the anus, and was 5-cm deep.Dorsal edema extended laterally to the midline onthe left side at the level of the posterior insertionof the axilla and crossed the dorsal midline to theright lateral midline. Ventral edema extended fromthe posterior insertion of the left flipper caudally tothe insertion of the peduncle. Ventral edema ex-tended laterally to the midline just caudal to theanus.

Examination of the oral cavity revealed a lacer-ation in the oral rete overlying a fracture of therostrum (Fig. 8). The area of baleen that surroundedthe oral rete laceration was coated in a thick yel-low-brown fluid in a spray-like pattern that ema-nated from the laceration. Upon removal of soft


Figure 5. Extensive soft tissue damage to fluke and peduncle of right whale Eg no. 1909. Note that the entire leftfluke and soft tissue of the left lateral and ventral peduncle are missing. Three or four of the caudal vertebrae are notpresent. The proximal quarter of the ventral right fluke is not present. The remaining proximal caudal margin of theright fluke was lacerated. Photographer: Virginia Aquarium Stranding Program.

tissue, a complete transverse fracture of the ros-trum, maxilla, premaxilla, and vomer was evidentat the site of the laceration. Displacement was ob-served; however, it is unknown how much displace-ment resulted from carcass handling versus the ini-tial trauma. The fracture plane of each bone wassampled for histology. Postcranial skeletal elementsshowed no signs of fracture or damage. The fetuswas necropsied separately, although no significantfindings were recorded.

Hemorrhagic tissue, irregular margins of fractureplane, and adherent fibrillar material localized atthe vomer and maxillary fracture sites were sug-gestive of perimortem fractures of the vomer, pre-maxilla, maxilla, and rostrum. Microscopic obser-vation of pallor in tissues from the colon, uterus,and cervix were consistent with exsanguination orblood loss because of shock.

A combination of severe subdermal bruisingfound in dorsal and ventral tissues, complete frac-ture of the rostrum that involved the maxilla, pre-maxilla, and vomer; and severe laceration of oralrete that resulted in rapid loss of blood directly con-tributed to the death of Eg no. 1004. This evidence

suggests death resulted from traumas associatedwith catastrophic impact with a vessel.

Case study IV—Eg no. 2150

Eg no. 2150 was first sighted as an animal ofunknown age in Massachusetts Bay in 1991. It waslast seen alive off the coast of Georgia in February2002. The code four carcass of Eg no. 2150 wasnecropsied in Culloden Cove, Nova Scotia, Canada,in October 2003.

Photographs taken during the initial encounter on2 October 2003 were viewed after the necropsy.The images revealed a large area of epidermal dis-coloration and swelling overlying the right mandi-ble, although most of the epidermis was absentwhen the animal was necropsied 2 days later. De-spite extreme autolysis, the main findings upon in-ternal examination included deep subdermal hem-orrhage in the blubber, subdermal sheath, and mus-cle overlying the right mandible; abnormal fluidsand substances noted in the abdominal and thoraciccavities; and three distinct fractures in the skull.

There was a closed (simple), linear, longitudinalfracture along the caudal aspect of the cranium


Figure 6. View of right side of postcranial cross section of Eg no. 1004 after decapitation reveals the first signsof extensive blunt trauma. The animal is lying ventral-side up. The black epidermis (right), overlying the creamy whiteblubber layer, is superficial to a gelatinous layer of hemorrhagic tissue and brown (autolysed) muscle (all tissue to theleft of the blue scale bar in hand). The 5-cm-thick hemorrhagic tissue is consistent with perimortem blunt trauma.Photographer: Regina Campbell-Malone, Woods Hole Oceanographic Institution.

(Fig. 9). The fracture plane extended from the mid-sagittal plane at the dorsal margin of the fracturethrough the occipital bone approximately 20-cm tothe left of the foramen magnum. The ventral marginof the fracture extended through the base of theoccipital, such that it was completely dissociatedwith the lateral aspects separated by a 15- to 30-cm gap. The fracture measured approximately 1.5-m in length and communicated with the brain case.Soft tissue overlying this cranial vault fracture wastoo autolyzed to permit the detection of discolor-ation, edema, or hemorrhage associated with a peri-mortem fracture. Severe bruising was noted in theconnective tissue and muscle overlying a fracturedright lower jaw (Fig. 10a, b), although the blubber

layer was unremarkable. All postcranial skeletal el-ements were intact. Disarticulated right ribs wereassociated with hemorrhage near the axilla of theright flipper. There were three distinct fractures inthe cranial skeleton. The right mandible was com-pletely fractured approximately 1.5-m from themandibular symphysis. A fracture of the left rearof the vomer was also found (not pictured).

Histologic analyses of bone fragments revealedthat the mandibular fracture plane contained re-gions of necrotic bone (demonstrated by the pres-ence of fibrous tissue and islands of cartilage), col-lagen (as confirmed by Masson trichrome), and wo-ven bone (not shown). These were considered ab-normal and indicative of bone healing and,


Figure 7. Schematic representation of subdermal hemorrhage and edema in right whale Eg no. 1004. Both thedorsal and ventral surfaces were extensively bruised. Except for bruising overlying the left mandible, bruising seen onright side (not shown) mirrored that seen on the left side. Image from Eg no. 1004 necropsy report adapted fromstandard right whale necropsy protocol.25,30

Figure 8. Evidence of significant blood loss in oral cavity of right whale Eg no. 1004. Inspection of the roof ofthe mouth revealed a laceration to the oral rete (between two arrows) and apparent ‘‘blood-spatter’’ staining (traced bygray curve) on the lingual surface of baleen plates. The tongue and black lip can be seen at the bottom of thephotograph. Removal of soft tissue revealed a complete fracture of the rostrum, vomer, and premaxilla. Staining patternindicates that vessel contents were under pressure when the laceration occurred, thereby providing evidence of peri-mortem trauma. Photographer: Regina Campbell-Malone, Woods Hole Oceanographic Institution.


Figure 9. Caudal view of skull of right whale Eg no. 2150. The dorsal aspect of the cranium is resting on softtissue seen at the bottom of the photograph. The foramen magnum is noted by a vertical arrow. The 1.5-m longitudinalfracture (horizontal arrow) penetrated the brain case and divided the skull into two distinct sections. Photographer:Andrea Bogomolni, Woods Hole Oceanographic Institution.

potentially, an antemortem disease process. Histo-logic analysis of the bone fragments from the frac-tured vomer and cranium revealed no evidence ofinflammatory or repair response. Gross evidence ofhemorrhage in the soft tissue overlying these frac-tures would allow them to be conservatively clas-sified as perimortem trauma.

The ultimate cause of death was traumatic injurythat resulted from skull fractures subsequent to avessel-whale collision. The applied stress was suf-ficient to result in a longitudinal fracture along thecaudal aspect of the skull, which compromised the

brain case, with complete dissociation along theventral aspect of the occipital bone. Histologic ev-idence indicates that this lethal strike may havebeen preceded either by an earlier, nonfatal strikethat fractured the right mandible or a perimortemmandibular fracture of a section of the jawboneweakened by preexisting disease.

DISCUSSION

These four cases present evidence of traumaticand ultimately lethal encounters between vesselsand whales. The types of tissue damage identified


Figure 10. Internal signs of hemorrhage and a complete fracture of the right mandible of right whale Eg no. 2150.a. Hemorrhage discovered upon reflection of skin and blubber layer. A knife penetrates the plane of the completetransverse fracture of the right mandible (seen in b). b. Fractured right mandible. Photographer: Andrea Bogomolni,Woods Hole Oceanographic Institution.

during necropsy can be evaluated and categorizedby using the diagnostic characteristics of sharp andblunt trauma, thus creating an effective field stan-dard to which future forensic necropsy cases can

be compared. Findings that are important to the dis-cussion include the overall health and nutritionalstatus of the individual, the relative timing of skel-etal fractures compared with the time of death of


the animal, and the categorization of sharp traumawounds seen in whales. Accepted criteria used fordiagnosing sharp and blunt trauma will now be ap-plied to evaluate the postmortem findings in thesecases.8,23,32

Overall health and nutritional status

The nutritional status of the four individuals ex-amined here was qualitatively evaluated postmor-tem based on the thickness and overall appearanceof the blubber layer. Typically, the blubber of a ma-ture, adult female is creamy white in color, opaque,and firm, and, on average, measures 13.93 cm(�2.49 cm SD, N � 32) when measured by usingultrasound on live free-ranging animals.1,25 Thesame study found no significant difference betweenmeasurements of excised blubber specimen thick-ness taken by using an ultrasound probe and thosetaken with a ruler.1

In the four case study animals, the blubber layerwas described as ‘‘thick’’ and ‘‘robust’’ (Eg no.2150, Eg no. 1004), ‘‘measuring 20- to 30-cmalong the dorsal midline’’ (Eg no. 1909), or theanimal was categorized as ‘‘not emaciated’’ in theabsence of blubber measurements (Eg no. 2143).The blubber appearance was noted as ‘‘normal (i.e.,creamy white) in color,’’ and ‘‘creamy white’’ (Egno. 2150, Eg no. 1004) or was retrospectively de-termined to be creamy white in color from photo-graphs in the absence of specific commentary (Egno. 1909). In each case, the animal was found tohave sufficient blubber thickness (evaluated at mul-tiple stations according to standard protocol) andappearance, such that the animal was equal to orabove the average blubber thickness measured inlive free-ranging adult females.1 Similarly, all car-casses had moderate-to-marked postmortem autol-ysis microscopically characterized by the loss ofcellular detail and the presence of large bacterialrods. The bacteria were considered postmortemovergrowth or cadaver bacilli and were not thoughtto have played a role in the death of the animal. Assuch, in all four cases, compromised nutritional sta-tus was not considered a significant factor that con-tributed to the death of the animal.

Relative timing of trauma

It is important, albeit challenging, to distinguishbetween premortem and postmortem trauma. Thecharacteristics of antemortem, perimortem, andpostmortem trauma were considered when analyz-ing a carcass and interpreting histopathologic find-ings.3,8,12,16 For this analysis, an antemortem lesionwas defined as one that occurs more than 6 hoursbefore death, thus allowing sufficient time for the

initiation of tissue response. For example, in hu-mans, acute hematoma and coagulation at a fracturesite occurs within 6 to 8 hours of the injury and isfollowed by inflammatory cell localization and dif-ferentiation.2 These changes are detectable upongross or histologic examination of fresh samples;however, they may become less evident as tissuequality declines. Evidence of bone healing is rela-tively resistant to decomposition and is a definitiveindicator that an injury occurred 7 to 14 days beforedeath.2

Perimortem lesions are those that occur within 6hours of death, be it just before or immediately af-ter death.2 Postmortem lesions occur after the deathof the animal and generally lack evidence of tissuereaction, particularly with increased time betweendeath and injury. Distinguishing between antemor-tem and postmortem processes is not always a sim-ple task.8,12,32 Cases that lack definitive evidence ofantemortem or postmortem injury are conservative-ly classified as perimortem. Characteristics and ex-amples of relevant antemortem, perimortem, andpostmortem bone pathology are shown in Table2.12,24 Carcasses that display evidence of perimor-tem bone fracture co-occurring with extensive sub-dermal edema and hemorrhage are believed to re-sult from blunt trauma attributed to vessel-whalecollisions.

It is particularly difficult to distinguish betweenperimortem and postmortem fractures without fo-rensic necropsy records that detail the direct ex-amination of accompanying soft tissue.32 Histologicexamination that reveals inflammatory response issufficient to determine that the wounds occurredbefore death.16 Histologic examination may also beused to determine if fractures may have occurredin bone weakened by preexisting pathologic pro-cesses.12 Indirect evidence may also be used to es-tablish timing of trauma. Right whale carcasses atsea are typically found floating with either the ven-tral or the lateral midline facing upward, at orabove the sea surface.35 As such, injuries to the dor-sum are taken as indirect evidence of premortem orperimortem trauma. This indirect evidence is par-ticularly useful in support of (or in the absence of )direct evidence of the relative timing of trauma.

Sharp trauma

The three categories of sharp trauma are stabwounds, incised wounds, and chop wounds.8 Stabwounds, once common in the whaling era, are nowrarely found, given the ban on harvesting rightwhales. The depth of a stab wound is characteris-tically much greater than its length and thereby pro-vides important clues regarding the size and shape


Table 2. Definition and appearance of antemortem, perimortem, and postmortem bone pathology of a traumaticorigin.

Timing of pathology Antemortem Perimortem Postmortem

Examples Healed or healing fracturesOsteoarthritisPittingAccretion

Unhealed fractures noticedduring necropsy.

Unhealed fractures frompostmortem vessel strike,surf trauma, machineryduring necropsy, damagein storage.

Characteristics Abnormal density or morpholo-gy, possible asymmetry whencomparing paired bones. Orga-nizing and organized hemato-ma.

Obvious lack of completehealing. Often accompa-nied by soft tissue edemaand hemorrhage. Unorga-nized coagulation.

Specific detail in necropsyreport that no fractureswere evident in bones ex-amined.

Fracture margins Potential osteoblast repair(smoothing or rounding atmargin) with some postfrac-ture survival.

Irregular margins. Jagged, linear, or squarededges, and splintering,particularly seen whendry bone is broken.

Signs of healing Variable depending on postfrac-ture survival (nonunion, mal-union, or angulation may beapparent). Increased density ofremodeled bone is visible ra-diographically in adult hu-mans.

Absent Absent

Presence of callus Callus apparent if fracture is re-cent. Variable presence of fi-brous or bony callus depend-ing on postfracture survivaltime.

Absent Absent

Soft tissue appear-ance

Potential edema or hemorrhagewith recent actively healingfracture.

Associated edema or hemor-rhage. Histologic evi-dence of inflammatory re-sponse.

No hemorrhage, thoughpostmortem processes re-sembling ‘‘bruising’’ areknown.

of the penetrating object. A recent source of stabwounds is the implantable tag, a subdermal trans-mitter used by researchers to track whales. None ofthe four animals examined had been tagged.30

Incised wounds occur when a body comes intocontact with a sharp-edged object. These woundshave characteristically smooth, straight edges, andthe length of the wound is generally much greaterthan its depth.8 There are no abrasions or contu-sions associated with incised wounds, and the tissueis cut clean through to the base of the wound.21,31

The length and depth of an incised wound providefew clues as to what type of object created it.8

Chop wounds are seen when a relatively heavyobject, with a cutting edge, contacts soft tissue and,often, underlying bone.31 These wounds are typi-cally incised but often have some characteristics ofa laceration (a blunt trauma injury defined below).As with incised wounds, the depth of the wound

may vary and present as relatively superficial at themargins, deepening toward the center of the wound.Unlike incisions, tissue bridging (remnants of softtissue connecting opposing margins of the wound)and hemorrhage may be observed, and the mor-phology of a chop wound may provide significantclues as to the object that created it.8

When boat propellers contact soft tissue, theycreate a chop wound in the form of a series of moreor less parallel, curved, evenly spaced s-shaped orz-shaped gashes that are often deeper in the centerthan at the margins.8,23 The angle to the line of trav-el and the shape, spacing, depth, and length of cutsprovide evidence of the rotation and approximatediameter and pitch of the screw, although the num-ber of blades has to be assumed. Propeller traumais usually acute and ranges in severity from mild,superficial epidermal wounds to more severe dam-age to the underlying blubber, muscle, viscera, and


bone, and complete dismemberment.18,19,26 Histolog-ic analysis may provide evidence of hemorrhage orrepair, a definitive feature of antemortem trauma.

Wounds or scars from propeller trauma weredocumented in both dead and living rightwhales.14,17,18,26,30 Fifteen of the 71 right whale mor-talities (21.1%) since 1970 displayed wounds con-sistent with propeller trauma.26,30 Because forensicnecropsy is presently the only method that permitsother causes of mortality to be ruled out, a moreconservative estimate would eliminate mortalitycases that were not necropsied, despite the presenceof ‘‘propeller gashes.’’ Thus, of the 40 necropsiedcarcasses, 11 (27.5%) were fatalities that resultedfrom sharp trauma.17,26,30 Studies of live animalsshed further light on the prevalence of nonfatal pro-peller trauma in the species.

Two separate photographic studies of right whaleepidermal scarring indicate that at least 7% of thewhales examined have scars from vessel propel-lers.14,19 Animals that survived massive sharp trau-ma have been documented. The most recent docu-mented case of sharp trauma involved an adult rightwhale (Eg no. 2425) hit, in March 2005, by thepropeller of a 43-foot yacht that was traveling at20 knots.35 The propeller struck the submergedwhale; this resulted in a series of propeller incisionsand avulsion of the distal half of the left fluke (Fig.1a). It is important to note that the margins of thedeepest wound are irregular and would be classifiedas a laceration, much like the distal margin of thewound seen in Eg no. 1909. Eg no. 2425 was sight-ed alive but in very poor condition in September2005. Although the fate of this animal remains un-clear, other propeller strike cases, such as RKB1424(Fig. 1b), proved immediately fatal.

The first case study animal (Eg no. 2143) initiallysurvived particularly severe and invasive propellerwounds, only to succumb nearly 14 years later tocomplications that stemmed from those injuriesduring the stress of pregnancy. The presence ofneutrophils within the supporting stroma confirmedthat these injuries were antemortem in nature (Fig.3). This leads to the consideration of sepsis sec-ondary to bacteremia associated with the open cau-dal propeller scar (concomitant with increased ab-dominal pressure resulting from pregnancy) as thecause of death of the animal.

The second case, Eg no. 1909, represents a morecommon outcome of severe propeller trauma. Theanimal had extensive tissue damage, and the lac-eration of major vessels that led to impaired loco-motor function and rapid exsanguination. These in-juries, combined with the postnecropsy naval reportof a whale strike and a second report of a whale

seen in the vicinity of the strike, bleeding from itstail, and missing a fluke lobe, leave little doubt thatthe trauma resulted from contact with a vessel.

The amputation of the entire left fluke blade anda portion of the proximal right fluke blade mayhave resulted in the loss of direct evidence of pro-peller trauma. This case documents vessel-whalecollision as an etiology for fluke amputation vialaceration. As such, future cases that display a sim-ilar wound pattern without anecdotal evidence maybe interpreted in light of the precedent set by thiscase and conservatively classified as a ‘‘possibleship strike.’’

A few notable individuals survived the acute vas-cular and tissue trauma caused by fluke damage(Fig. 1a). Damage to small peripheral vessels anddistal fluke tissue may not be as lethal as trauma tothe proximal flukes and the peduncle.33 Involve-ment of large-bore vessels may lead to rapid lossof blood volume from an open wound (as indicatedin two independent reports of Eg no. 1909 bleedingafter collision with a vessel) or disruption of caudalcirculation if the vessel is constricted (as seen insevere entanglement).26 Thus, it seems that the se-verity of the trauma (depth, length, and surface areainvolved) as well as the anatomical location of thewound are important in determining the immediatelethality of sharp trauma injury, whereas chronicsequelae from infection, improper healing, or re-duced function may prove lethal in a far less pre-dictable manner.

Blunt trauma

Mechanical stress applied to a body causes bluntforce trauma. To cause a blunt force injury, stressapplied to the tissue must be great enough to de-form the elastic or viscoelastic tissue beyond itsability to recover or maintain integrity.9,11 This canoccur in situations where 1) the magnitude of theapplied stress is greater than the ultimate strengthof the tissue; 2) the stress is imparted in an unnat-ural direction, loading the tissue in a direction withweaker material properties; or 3) the stress is ap-plied to mechanically inferior pathologic tissue.

From a biomechanics perspective, the severity ofthe injury is dependent upon many factors, includ-ing the magnitude of the force, the area acrosswhich it is applied, the angle of contact, tissue elas-ticity and plasticity, and the contact time, whichtogether influence the amount of energy transferredto the animal.8,9,11 A first-order estimate of the ul-timate strength (�ult) can be found by using theequation

� � F/Ault i


where F is the load at failure and Ai is the initialcross-sectional area of the tissue. Thus, even a rel-atively small force applied over a very small areacan result in severe injury.

In general, blunt force injuries are classified intofour categories: 1) abrasions, 2) lacerations, 3) con-tusions, and 4) skeletal fractures.8,9 Anecdotal andforensic evidence of all four categories of blunttrauma were established in dead or living rightwhales.17,18,22,30 Abrasions are produced as a resultof friction that leads to scraping or scuffing of theepidermis. Abrasions are often seen on the epider-mis of right whale carcasses; however, they aregenerally superficial and of unknown origin. A se-ries of equally spaced, parallel, superficial abra-sions may be taken as evidence of tooth-mark scarsfrom predators or scavengers. Lacerations are tearsor fissures in the tissue caused by shear stresses andstretching forces across a tissue plane (see Casestudy II, Fig. 5). Lacerations are more likely to oc-cur in tissue superficial to bone than in tissue over-lying additional soft-tissue layers. Typically, lacer-ations have irregular margins and tissue bridgingwhen select intact remnants of more resilient tissue(e.g., vessels and nerves) traverse the wound.8,21,31

The margins of a laceration are typically associatedwith hemorrhage.21

Contusions are bruises or areas of soft tissuehemorrhage. They result when an applied stresscauses blood vessels to rupture, releasing blood intosurrounding tissues. Hematoma can follow tissuehemorrhage (see case studies III and IV, and Figs.6, 7, and 10). Skeletal fractures occur when bonesbreak in response to mechanical stress. In rightwhales hit by vessels, it is common to find fracturesin the mandibles, cranium, rostrum, or vomer; dis-articulated vertebrae; and tympanic bullae (see casestudies III and IV, and Fig. 9).6,30

The number of fatal versus nonfatal vessel-whalecollisions that occur each year is unknown. Unlikevessel collisions that involve sharp trauma frompropeller damage, nonfatal interactions between awhale and the hull of a vessel leave little immediateor lasting external evidence. Because forensic nec-ropsy is presently the only reliable method that bothexposes externally obscure evidence of blunt trau-ma and permits other causes of mortality to be in-vestigated, a conservative estimate would consideronly those animals that were thoroughly necrop-sied. Thus of the 40 necropsied carcasses, 9(22.5%) were fatalities that resulted from blunttrauma.17,26,30

The necropsy findings from Eg no. 1004 revealedextensive hemorrhage and edema, which suggestswidespread contact with an object before death

(Fig. 7). The laceration to the oral rete occurredbefore death, as evidenced by the blood-spray pat-tern on the lingual surface of baleen and the roofof the mouth. This would not have been apparentif it was indeed a postmortem injury. Histologicanalysis of the broken rostrum revealed irregularbone margins and no signs of healing in the formof woven bone. Both of these findings are consis-tent with a perimortem fracture induced by blunttrauma.

In the case of Eg no. 2150, the substantial blacktarry substance found in the thoracic cavity provid-ed evidence of trauma and blood loss into this re-gion. Similarly, the hemorrhage found overlyingthe fractured left vomer, around disarticulated ribs,and in soft tissue surrounding the fractured man-dible also implicated a perimortem vessel-whalecollision event. However, histologic analysis of thefracture plane of the right mandible revealed thepresence of necrotic and woven bone, as well ascartilaginous tissue, indicative of a healing processthat occurred at least several days before death.Gross examination and computed tomography re-vealed an area of pitted bone that flanked both sidesof the fracture plane and extended a total length ofapproximately 45 mm, consistent with histologicfindings of necrosis.

There are two possible interpretations of thesefindings. The woven bone may be taken as a signthat the animal survived for a period of days toweeks after an initial vessel-whale collision thatcaused the mandibular fracture. This would lead tothe conclusion that a second collision resulted inthe massive skull fracture that involved the braincase. Alternately, healing, indicated by the presenceof woven bone, may have preceded the fracture,where bone disease in the right mandible may havepredisposed the area to fracture when the animalwas hit by a single vessel, resulting in all of theperimortem fractures and bruising found upon nec-ropsy. Although neither interpretation is exception-ally parsimonious, both implicate a vessel-whalecollision event as the underlying cause of mortality.Further analysis of the pathologic region of bonesurrounding the fracture plane may improve diag-nostic conclusions.

CONCLUSIONS

The documentation of the number of deaths andthe sources of mortality in the highly endangeredright whale population is a main goal of right whalebiologists and managers. The characterization ofdeaths that result from human interactions, includ-ing vessel-whale collision events and entanglementin fishing gear, provides valuable statistics to those


agencies responsible for right whale protection. Thedirect classification of wounds and the identifica-tion of indicators of disease process or human in-teraction are essential for future necropsies, accu-rate diagnoses, and precise mortality statistics.

Here, four carcasses were examined and classi-fied by comparing the type of tissue damage iden-tified during forensic necropsy to the diagnosticcharacteristics of sharp and blunt trauma. Thesecases present evidence of traumatic and ultimatelylethal encounters between vessels and whales. Thisstudy does not include all of the right whales thatdied or were necropsied during this time; however,in their thoroughness and rigor, these cases are rep-resentative of forensic necropsy results reportedover the past decade.26

A critical assessment of these cases proves thatforensic necropsy remains the key to determiningthe cause of death. This is particularly important incases of whales that sustain blunt force injuries, be-cause external evidence of internal trauma is gen-erally minimal. The importance of documenting in-juries seen during necropsy of animals anecdotallytied to a ship strike is clear upon review of casestudy II. The observed trauma (i.e., avulsion of theleft fluke via laceration) had not been previouslyassociated with a vessel-whale collision. This casesets a precedent for future cases where similar in-juries are seen in the absence of anecdotal evidenceof a collision. The classification of these cases pro-vides an effective field standard to which future fo-rensic necropsy cases can be compared for the ap-propriate characterization of traumatic injury suitestypically encountered during right whale necropsy.

Because more than half (52.5%) of the 40 rightwhales necropsied to date displayed evidence ofvessel-whale collision trauma, and additional rightwhales that were not necropsied showed signs ofserious injury and scarring from encounters withvessels, reducing the occurrence or lethality of ves-sel-whale collisions was identified as a key com-ponent in the management plan by the NationalOceanic and Atmospheric Administration Fisher-ies.14,18,28 Efforts to mitigate vessel-whale collisionsby implementing coastal speed restrictions androuting changes in right whale critical habitat andmigratory corridors in the United States are beingconsidered.29,36 Past efforts, including the reroutingof shipping channels to avoid right whale feedinggrounds between New Brunswick and Nova Scotia,and two Mandatory Ship Reporting Systems arepresently being evaluated for efficacy.

Furthermore, studies that rely on samples ob-tained during necropsy are vital to ongoing researchregarding vessel-whale interactions. For example,

the extraction of the tympanic bullae and subse-quent computed tomography imaging has providedinsight into the auditory range and ability of rightwhales to detect vessel noise.34 In addition, necrop-sy records indicate that the right whale mandiblehas been fractured in a third of the cases that dis-played evidence of blunt trauma because of vesselcollisions, yet healed mandibular fractures havenever before been seen in right whale skeletal re-mains.35 As such, a mandibular fracture representsan appropriate fatal end point for vessel-whale col-lision modeling. Material property analyses of man-dibular bone and soft tissue overlying the rightwhale mandible will be used to model the stressescapable of fracturing right whale bone.4 When com-bined with potential stresses presented by vesselstraveling at a given speed, speed restrictions maybe evaluated as a means of reducing vessel-whalecollision fatalities. The aforementioned studies,along with data obtained from future necropsiesand the appropriate characterization of trauma find-ings will continue to inform ongoing efforts to re-duce vessel-whale collision mortalities.

Acknowledgments: The authors would especiallylike to thank Blair Mase Guthrie and Dana Hartley(both of National Oceanic and Atmospheric Admin-istration); Andrea Bogomolni and Nadine Lysiak(both of Woods Hole Oceanographic Institution);Denise Boyd (Florida Fish and Wildlife Conserva-tion Commission); Tod Leighfield, Gretchen Lov-ewell, and Jamison Smith (National Oceanic andAtmospheric Administration); D. Ann Pabst (theUniversity of North Carolina Wilmington); MarkSwingle (Virginia Aquarium and Marine ScienceCenter); David Taylor, New England AquariumSoutheastern United States survey team; the VirginiaAquarium and Marine Science Center Stranding Re-sponse Team, Katie Moore (United States CoastGuard), Fisheries and Oceans Canada; the many vol-unteers that necropsy efforts somehow manage toattract; and to the many institutions and individualsthat contribute sighting records to the North AtlanticRight Whale Consortium. Special thanks to DarleneKetten (Woods Hole Oceanographic Institution),Ken Schopf, and the reviewers, whose thoughtfulcomments helped to improve the final manuscript.

This report was prepared by the authors indicatedunder award numbers NA04NMF4720402 (Camp-bell-Malone/Moore) and NA04NMF4720392(Moore/McLellan) from the National Oceanic andAtmospheric Administration (NOAA), U.S. De-partment of Commerce (U.S. DOC) and a NationalScience Foundation (NSF) Graduate Research Fel-lowship (Campbell-Malone). The statements, find-


ings, conclusions and recommendations are thoseof the authors and do not necessarily reflect theviews of the NOAA, U.S. DOC, or the NSF.

LITERATURE CITED

1. Angell, C. M. 2006. Body Fat Condition of Free-Ranging Right Whales, Eubalaena glacialis and Eubalae-na australis. Ph.D., Boston Univ., Boston, Massachusetts.

2. Aufderheide, A. C., and C. Rodriguez-Martin. 1998.The Cambridge Encyclopedia of Human Paleopathology.Cambridge Univ. Press, Cambridge, Massachusetts.

3. Burke, M. P., A. K. Olumbe, and K. Opeskin. 1998.Postmortem extravasation of blood potentially simulatingantemortem bruising. Am. J. Forensic Med. Pathol. 19:46–49.

4. Campbell-Malone, R. 2007. Biomechanics of NorthAtlantic Right Whale Bone: Mandibular Fracture as a Fa-tal Endpoint for Blunt Vessel-Whale Collision Modeling.Doctoral, Massachusetts Institute of Technology/WoodsHole Oceanographic Institution, Cambridge, Massachu-setts.

5. Caswell, H., M. Fujiwara, and S. Brault. 1999. De-clining survival probability threatens the North Atlanticright whale. Proc. Nat. Acad. Sci. USA 96: 3308–3313.

6. De Guise, S., and D. St. Aubin. 1999. A non-unionchronic fracture in a north Atlantic right whale: the im-portance of histopathology. (Abstr.). In: 13th BiennialConference of the Biology of Marine Mammals, Maui,Hawaii.

7. Department of Fisheries and Oceans. 2000. A Ca-nadian Recovery Plan for the North Atlantic Right Whale.Prepared by the World Wildlife Fund for the Departmentof Fisheries and Oceans, Dartmouth, Nova Scotia, Cana-da.

8. DiMaio, V. J. M., and D. J. DiMaio. 2001. ForensicPathology. CRC Press, New York, New York.

9. Fierro, M. F., and J. P. Ongley. 1990. Blunt forceinjuries. In: Froede, R. C. (ed.). Handbook of ForensicPathology. College of American Pathologists, Northfield,Illinois. Pp. 171–180.

10. Fujiwara, M., and H. Caswell. 2001. Demographyof the endangered North Atlantic right whale. Nature 414:537–541.

11. Galloway, A. 1999. The biomechanics of fractureproduction. In: Galloway, A. (ed.). Broken Bones: An-thropological Analysis of Blunt Force Trauma. Charles CThomas, Springfield, Illinois. Pp. 35–62.

12. Galloway, A., S. A. Symes, W. D. Haglund, and D.L. France. 1999. The role of forensic anthropology in trau-ma analysis. In: Galloway, A. (ed.). Broken Bones: An-thropological Analysis of Blunt Force Trauma. Charles CThomas, Springfield, Illinois. Pp. 5–31.

13. Geraci, J. R., and V. J. Lounsbury. 1993. MarineMammals Ashore: A Field Guide for Strandings. SeaGrant College Program Texas A&M Univ., Galveston,Texas.

14. Hamilton, P. K., M. K. Marx, and S. D. Kraus.1998. Scarification Analysis of North Atlantic RightWhales (Eubalaena glacialis) as a Method of AssessingHuman Impacts. A report submitted to The Island Foun-

dation, Marion MA. New England Aquarium, Boston,Massachusetts.

15. International Maritime Organization. 2002. Routingof Ships, Ship Reporting and Related Matters; Amend-ment of the Traffic Separation Scheme in the Bay of Fun-dy and Approaches. NAV 48/3/5, Submitted to the Inter-national Maritime Organization by Canada.

16. Kibayashi, K., K. Hamada, K. Honjyo, and S. Tsu-nenari. 1993. Differentiation between bruises and putre-factive discolorations of the skin by immunological anal-ysis of glycophorin A. Forensic Sci. Int. 61: 111–117.

17. Knowlton, A. R. 1997. The Regulation of Shippingto Protect North Atlantic Right Whales: Need and Feasi-bility. Univ. of Rhode Island, Kingston, Rhode Island.

18. Knowlton, A. R., and S. D. Kraus. 2001. Mortalityand serious injury of northern right whales (Eubalaenaglacialis) in the western North Atlantic Ocean. J. CetaceanRes. Manag. Spec. Issue 2: 193–208.

19. Kraus, S. D. 1990. Rates and potential causes ofmortality in North Atlantic right whales (Eubalaena gla-cialis). Mar. Mamm. Sci. 6: 278–291.

20. Kraus, S. D., M. W. Brown, H. Caswell, C. W.Clark, M. Fujiwara, P. K. Hamilton, R. D. Kenney, A. R.Knowlton, S. Landry, C. A. Mayo, W. A. McLellan, M.J. Moore, D. P. Nowacek, D. A. Pabst, A. J. Read, and R.M. Rolland. 2005. North Atlantic right whales in crisis.Science 309: 561–562.

21. Kumar, V., A. K. Abbas, and N. Fausto (eds). 2005.Robbins and Cotran Pathologic Basis of Disease. ElsevierSaunders, Philadelphia, Pennsylvania.

22. Laist, D. W., A. R. Knowlton, J. G. Mead, A. S.Collet, and M. Podesta. 2001. Collisions between shipsand whales. Mar. Mamm. Sci. 17: 35–75.

23. Lightsey, J. D., S. A. Rommel, A. M. Costidis, andT. D. Pitchford. 2006. Methods used during gross necrop-sy to determine watercraft-related mortality in the Floridamanatee (Trichechus manatus latirostris). J. Zoo Wildl.Med. 37: 262–275.

24. Lowell, N. C. 1997. Trauma analysis in paleopa-thology. Yearb. Phys. Anthropol. 40: 139–170.

25. McLellan, W. A., S. Rommel, M. J. Moore, and D.A. Pabst. 2004. Right Whale Necropsy Protocol. U.S. De-partment of Commerce, National Oceanic and Atmospher-ic Administration, National Marine Fisheries Service, Of-fice of Protected Resources, Silver Spring, Maryland.

26. Moore, M. J., A. R. Knowlton, S. D. Kraus, W. A.McLellan, and R. K. Bonde. 2004. Morphometry, grossmorphology and available histopathology in north Atlanticright whale (Eubalaena glacialis) mortalities (1970 to2002). J. Cetacean Res. Manag. 6: 199–214.

27. National Marine Fisheries Service. 1991. RecoveryPlan for the Northern Right Whale (Eubalaena glacialis).Prepared by the Right Whale Recovery Team for the Na-tional Marine Fisheries Service, Silver Spring, Maryland.

28. National Marine Fisheries Service. 2004. NOAAFisheries Releases Recovery Plan for Endangered NorthAtlantic Right Whales. National Marine FisheriesService. http://www.nero.noaa.gov/shipstrike/whatsnew/04-080�north�atlantic�right�whale�recovery�plan.pdf.

29. National Marine Fisheries Service. 2006. Proposed


Rule to Implement Speed Restrictions to Reduce theThreat of Ship Collisions with North Atlantic RightWhales. National Oceanic and Atmospheric Administra-tion. Department of Commerce. Federal Register 71(122):36299–36313.

30. New England Aquarium. 1986–2005. Photo-iden-tification, Sightings, Tagging history, Genetics, ContaminantAnalyses and Necropsy reports. www.rightwhaleweb.org.

31. Ongley, J. P., and R. K. Wright. 1990. Cutting andstabbing. In: Froede, R. C. (ed.). Handbook of ForensicPathology. College of American Pathologists, Northfield,Illinois. Pp. 234–238.

32. Ortner, D. J. 2003. Identification of PathologicalConditions in Human Skeletal Remains. Academic Press,Boston, Massachusetts.

33. Pabst, D. A., S. A. Rommel, and W. A. McLellan.1999. The functional morphology of marine mammals. In:Reynolds, J. E. III and S. A. Rommel (eds.). Biology of

Marine Mammals. Smithsonian Institution Press, Wash-ington D.C. Pp. 15–72.

34. Parks, S. E. 2003. Acoustic Communication in theNorth Atlantic Right Whale (Eubalaena glacialis). Ph.D.Dissertation, Massachusetts Institute of Technology, Cam-bridge, Massachusetts.

35. Right Whale Consortium. 2007. North AtlanticRight Whale Consortium Photo-ID, Sightings, Genetics,Contaminants and Necropsy Database. New EnglandAquarium, Boston, Massachusetts.

36. Russell, B. 2005. Report on Nine Industry Stake-holder Meetings 30 September 2004 through 27 October2004 in Support of Advanced Notice of Proposed Rule-making (ANPR) on NOAA Fisheries’ Strategy to ‘‘Re-duce Mortalities to North Atlantic Right Whales (NARW)as a Result of Vessel Collisions.’’ Contract Order NumberEA 133F-04-SE-1176, JS&A.

Received for publication 19 December 2006

gross and histologic evidence of sharp and...

Documents