DISEASES

A comprehensive review of diseases of Australian ceta­ceans is provided in Blyde and Vogelnest (2008).

4.1 Infectious diseases

4.1.1 Viral diseases

a. Cetacean morbillivirus

Cetacean morbillivirus (CeMV) has a worldwide distribu­tion and is endemic in several cetacean species, including

Fig.

pilot whales (Globicephala spp.) (Van Bressem et al. 2014). One out of five of a pod of 25 stranded common bottle­nosed dolphins chased ashore by common killer whales (Orcinus orca) in Tas. was serologically positive for CeMV antibodies (Van Bressem et al. 2001). A seroprevalence of 85.7% was demonstrated in 21 long-finned pilot whales (Globicephala melas) sampled from NZ waters, with anti­bodies detected in both mature and immature animals and without outbreaks of severe disease, suggesting ende- micity in this population. As pilot whales are gregarious and associate with other cetaceans, they may act as reser­voirs of infection for other species, including Indo-Pacific bottle-nosed dolphins in the south-western Pacific. Mor- billiviruses are generally transmitted horizontally by the respiratory route, with aerosol transmission of infection among odontocetes likely facilitated by their social cohe­siveness, synchronous breathing and explosive respiration (Duignan 2001).

In March 2010, a juvenile, male common bottle-nosed dolphin was found stranded on Fraser Is., Qld. The animal was in fair body condition, unresponsive to exter­nal stimuli and unable to swim or float unassisted. Sev­eral attempts to refloat the animal were unsuccessful. The animal died and CeMV infection was confirmed via electron microscopy, immunohistochemistry and reverse transcription PCR.

CeMV infection appears to be endemic within the melon-headed whale (Peponocephala electra) population and frequent within the Indo-Pacific bottle-nosed dolphin population in Australian waters and both species may serve as reservoirs of CeMV infection in this region. Of 13 (15.4%) managed cetaceans sampled between November 2005 and January 2011 two were positive for CeMV anti­bodies. Both animals were common bottle-nosed dolphins wild-caught in 1985. It is highly unlikely that CeMV infection occurred while in managed care; therefore CeMV infection appears to have been present within Aus­tralian free-ranging cetaceans since at least 1985.

Subsequent to the death of the animal on Fraser Is., outbreaks of this disease were documented in WA and SA (Stephens et al. 2014; Kemper et al. 2016). In 2009, six Indo-Pacific bottle-nosed dolphins in the Swan River, WA, died and CeMV infection was confirmed (Stephens et al. 2014). These animals had an unusual form of CeMV characterised by severe lymphoid depletion and over­whelming opportunistic infections. In 2013 an unusual mortality event in both bottle-nosed dolphins (T. aduncus and T. truncatus) and short-beaked common dolphins (Delphinus delphis) around Spencer Gulf and Gulf St Vin­cent, SA, was confirmed as CeMV infection (Kemper et al. 2016). This event coincided with a major climatic anomaly in south-eastern Australia, including SA, that resulted in water temperatures substantially higher (3-5°C) than normal. A die-off of fish in the area at the same time may have affected food availability for ceta­ceans in this region, predisposing them to disease. Sub- clinical CeMV infection may result in immune suppression, making animals more susceptible to other diseases such as toxoplasmosis, nocardiosis and brucello­sis (Bossart et al.

Most cetaceans with CeMV disease wash ashore dead or strand moribund and die shortly after, with some dis­playing neurological or behavioural changes. CeMV infection should be included in the differential diagnosis of stranded cetaceans in Australia, particularly if they display neurological signs. However, these clinical signs are not pathognomonic and can be seen with other dis­eases affecting the brain and meninges. Serology can be suggestive of past or current infection. Serum neutralisa­tion titres >1:32 can be indicative of active CeMV infec­tion. PCR on swabs from the blowhole of live animals can be used to diagnose active infection.

Submission of fresh and fixed tissues (particularly lung and brain) from dead animals for histopathology, immunohistochemistry, electron microscopy and PCR is recommended to confirm CeMV infection. On histopa­thology, the presence of large multinucleated ‘Warthin- Finkeldey’ type syncytia and/or acidophilic viral inclusions are highly suggestive of morbillivirus infection and further confirmation should be pursued.

b. Herpesviruses

Lesions caused by cetacean herpesviruses include non­suppurative meningoencephalitis with occasional eosino­philic intranuclear inclusion bodies and sometimes necrotising lesions in multiple organ systems. Gamma­herpesviruses have been associated with vesicular oral or genital lesions without death in common bottle-nosed dolphins in the USA (Rehtanz et al. 2012). Similar oral and genital lesions have been observed in free-ranging and oceanarium-housed bottle-nosed dolphins in Aus­tralia but have not been confirmed as being caused by a herpesvirus.

c. Poxvirus

Cetacean pox (‘tattoo’) is caused by cetacean poxviruses, most closely related to the Orthopoxvirus genus in the Family Chordopoxvirinae (Blacklaws et al. 2013). Lesions have been reported in multiple species of both managed and free-ranging odontocetes globally (Van Bressem et al. 2009). Skin lesions are circular to irregular, grey with black stippling and occur anywhere on the body (Geraci et al.

d. Papillomaviruses

Type 1 and type 2 cetacean papillomavirus cause small cutaneous wart-like lesions that are generally self-limiting. These proliferative lesions are generally found on the skin, frenulum of the tongue, tongue, penis and vagina. Hyper­plastic epidermis with rete pegs and intranuclear, eosino­philic inclusion bodies within the stratum spinosum and stratum corneum is seen histologically. Infection results in long-lasting protective immunity (Dold 2015).

e. Circovirus

A novel circovirus, beaked whale circovirus (BWCV) has been described in stranded cetaceans throughout the Pacific Basin. It was first isolated in a Longman’s beaked whale (Indopacetus pacificus) stranded in Hawaii. BWCV has since been isolated from archived tissues of 11 species of stranded cetaceans (Clifton et al. 2023). Circoviruses have been associated with necrosis in the brain, lung, liver, spleen, intestine and lymphoid tissues in other species. This was not observed in cetacean in which BWCV was isolated. Lymphoid depletion, a common finding associ­ated with circoviral infections can cause immunosuppres­sion leading opportunistic co-infection by other pathogens.

4.1.2 Bacterial diseases

a. Nocardia

Nocardia are aerobic actinomycete bacteria present in soil, water and marine sediments that can infect humans and other animals, causing localised and systemic dis­ease. Infection can occur through inhalation, inocula­tion through skin lesions and ulcers in the GIT (Leger et al. 2009). Very strong wind and heavy rain may increase the risk of exposure to the organism. Immunocompro­mised animals are at higher risk of severe and dissemi­nated infections. If nocardiosis is suspected or diagnosed, investigation of predisposing immunosuppressive fac­tors is recommended.

Nocardiosis caused by N. asteroides, N. farcinica, N. brasiliensis, N. cyriacigeorgica and N. levis has been described in free-ranging and managed cetaceans over­seas (Leger et al. 2009). The systemic form is typical, with involvement of lungs and thoracic lymph nodes and occa­sionally brain. In Australia, Nocardia sp. infection was described in an oceanarium-housed false killer whale (Pseudorca crassidens) with liver and lung abscesses (Needham 1978). Nocardiosis was diagnosed in a stranded adult female pantropical spotted dolphin (Stenella attenuata) in northern NSW. Necropsy revealed pyometra and multifocal small abscesses on the surface of the brain (Plate 46.1). Suppurative meningoencephali­tis, chronic non-suppurative pneumonia, suppurative endometritis and mild multifocal interstitial nephritis, consistent with nocardiosis, was seen histologically. Nocardia brasiliensis was cultured from cerebrospinal fluid, uterine contents, meninges, cerebellum, brain and liver.

Nocardia has been successfully treated in cetaceans using trimethoprim-sulfonamides supplemented with folic acid (Schmitt et al. 2013).

b. Streptococcus

Streptococcus agalactiae is a significant bacterial pathogen (Batalis et al. 2007) and has been reported to cause necro- tising fasciitis and abscesses in oceanarium-housed common bottle-nosed dolphins (Zappulli et al. 2005). It was cultured from muscle and kidney from a dead free- ranging common bottle-nosed dolphin. The isolate was biochemically similar to S. agalactiae cultured from mullet in the same area during a fish die-off, implicating food fish as the potential source of infection (Evans et al. 2006).

Streptococcus agalactiae has been confirmed as the cause of death in a free-ranging grouper (Epinephalus lanceolatus) in northern Qld (Bowater et al. 2012) and in aquarium-housed stingrays in south-east Qld (Bowater et al. 2018). The organism is therefore present in Australian waters, infecting potential food sources for cetaceans and is a potential pathogen for both managed and free-rang­ing cetaceans. Streptococcus iniae was the cause of a fatal bacterial septicaemia in an oceanarium-housed common bottle-nosed dolphin in China. The source of the bacte­rium in this case was thought to be food fish (Song et al. 2017). It has been confirmed as the cause of death in free- ranging marine turtles and fish in north-west WA and similarly to S. agalactiae could be a potential pathogen for free-ranging cetaceans (E Young pers. comm.). Autoge­nous vaccines can be prepared for S. agalactiae and S. iniae and may be useful in the face of outbreaks of the disease.

c. Brucellosis

Brucella ceti is a recognised cause of encephalitis, hydro­cephalus and vestibulocochlear nerve pathology (leading to hearing deficits) and subsequent stranding in North American cetaceans (Colegrove et al. 2016). Brucellosis was diagnosed in a late-term Indo-Pacific bottle-nosed dolphin aborted fetus in Australia. Brucella ceti was cul­tured from the spleen, kidney and liver of the fetus. His­topathology revealed a mild placentitis and encephalitis. Serological surveys have confirmed its presence in free- ranging cetaceans, including Indo-Pacific bottle-nosed dolphins and pantropical spotted dolphins in Australian waters.

Confirming a diagnosis of brucellosis in cetaceans is difficult because the organism is difficult to isolate. Infec­tions are often chronic and very few organisms remain by the time the animal succumbs to the disease. Cerebellum, brainstem or spinal cord are the preferred tissues for cul­ture and PCR. Cerebrospinal fluid collected antemortem or postmortem may also be useful.

4.1.3 Protozoal diseases

Toxoplasmosis is the only significant protozoal pathogen of cetaceans in Australian waters and is covered in Chapter 21.

4.1.4 Fungal diseases

a. Paracoccidiomycosis

Paracoccidiomycosis (formerly known as Lacaziosis) is a chronic fungal disease of the skin and SC tissues that affects only cetaceans and humans. It has a worldwide distribution. Recent re-classification of the fungi associ­ated with this disease suggests the species that affects dolphins (Paracoccidiodes ceti) may be distinct from that which is associated with human disease (Paracoccidiodes brasiliensis). It has been described as affecting three spe­cies of free-ranging cetaceans in Australian waters - one Indo-Pacific bottle-nosed dolphin, two common bottle­nosed dolphins and two Australian snub-finned dolphins (Orcaella heinsohni) in Darwin harbour - between 2004 and 2022. (Australian Registry of Wildlife Health pers. comm.). Lacaziosis-like lesions have been reported in many species of cetaceans in Australian waters. Lacazio- sis in cetaceans is characterised by greyish, whitish to slightly pink, verrucous lesions that may ulcerate (Fig. 46.5). The disease is usually slowly progressive and may be fatal. It is not known to be transmitted horizontally between dolphins and is likely an environmental patho­gen that causes disease in poor environmental conditions (e.g. low salinity, increased turbidity and polluted water­ways) or in immunocompromised animals. Superficial

Fig. 46.5. Lacaziosis-Iike lesions in an Indo-Pacific bottle-nosed dolphin (Tursiops aduncus) calf, Jervis Bay, NSW. Photo: Scott Sheehan and Heidi Russell

skin wounds represent a probable route of colonisation. Treatment of cetaceans has not been attempted. It is a potential but unlikely zoonosis (Reif et al. 2013).

b. Other fungi

Various species of fungi can cause invasive disease in cetaceans. The majority of these are secondary to pri­mary immunosuppressive diseases such as CeMV. Opportunistic fungi isolated from cetaceans include Coccidioides spp., Cryptococcus spp., Blastomyces spp., Histoplasma spp., Aspergillus spp. and Zygomycetes. Only Aspergillus spp. have been identified in cases of mycoses in Australian cetaceans. Serological tests are available for many of these fungi, but their sensitivity and specificity are unknown in cetaceans (Dold 2015). In most cases the affected organs are lungs, lymph nodes, brain and skin.

4.1.5 Parasitic diseases

a. Lung nematodes

Heavy burdens of nematodes are frequently found in the lungs of free-ranging neonatal cetaceans at necropsy. Burdens in adults are lower, with less effect on the animal. Tomo et al. (2010) found nematode parasites in short-beaked common, Indo-Pacific bottle-nosed and common bottle-nosed dolphins in SA. Younger animals were more likely to be infected. Three species of nema­todes were identified: Halocercus lagenorhynci, Stenurus ovatus and Pharurus alatus. The life cycles of these par­asites are unknown but given that neonates have high burdens, transplacental or transmammary transmission seems likely. Adults are likely infected through inges­tion of intermediate host in prey species. They very likely contribute to morbidity and mortality, given the high burdens of infection. Pulmonary nematodiasis should be considered as a differential diagnosis in neonatal and juvenile stranded cetaceans and if rescued and an attempt at treatment and rehabilitation made, presumptive treatment with ivermectin at 200 μg∕kg PO may be of use.

b. Nasitrematinae

Nasitrema spp. are trematodes that inhabit the cranial sinuses and upper airways of odontocete cetaceans. They are likely a normal inhabitant, but may adversely affect immunocompromised individuals, and have been impli­cated in deaths of free-ranging cetaceans (Phillips and Suepaul 2017). Eggs of parasites can be seen in smears of discharge from the blowhole. In certain circumstances it can travel from the sinuses to the brain and cranial nerves. Treatment can be difficult and efficacy is debata­ble. The most appropriate treatment is 20 mg∕kg praziqu­antel PO or IM.

4.2 Non-infectious diseases

4.2.1 Gastrointestinal volvulus

Gastrointestinal volvulus has been reported in managed cetaceans (Begeman et al. 2012). Clinical signs include sudden onset of lethargy, dull mentation and anorexia (perhaps indicative of pain), particularly if the animal has had a history of chronic GI problems. Predisposing fac­tors can include foreign bodies in the first stomach, large feeds, bacterial and viral gastroenteritis and GI parasit­ism. Elevated bilirubin (>10 μmol∕L) and inversion of calcium:phosphorus ratios may corroborate the diagno­sis. Ultrasonography and radiography may be useful. Treatment is palliative and euthanasia is indicated if the animal continues to deteriorate.

4.2.2 Dilated cardiomyopathy

Dilated cardiomyopathy has been diagnosed in stranded dwarf sperm whales (Kogia sima) and pygmy sperm whales (K. breviceps) (Bossart et al. 2007). High levels of mercury were found in several of these individuals and may play a role in the disease, either as a primary aetio- logical agent or as a result of interacting with other trace minerals such as selenium (Bryan et al. 2012). Gross nec­ropsy findings are limited to congested lungs and an abnormally dilated heart. Histopathology includes patchy ventricular myocardial oedema, disorganisation of cardiomyocytes with vacuolation or fragmentation of scattered myocytes, intense periacinar congestion of the liver with extensive loss of hepatocytes and congestion of the lungs.

4.2.3 Keratopathy

Keratopathy, manifesting primarily as corneal oedema, is the most common ocular lesion in managed cetaceans (Colitz et al. 2016). Exposure to ultraviolet radiation appears to be the most important predisposing factor. Several features of enclosure design, water treatment and quality and husbandry are important for prevention of ocular damage (see Chapter 45). Treatment includes the use of tacrolimus or ketorolac eye drops and husbandry and environmental changes.

4.2.4 Miscellaneous skin diseases

A range of skin diseases of unknown aetiology have been reported in free-ranging cetaceans in Australian waters, including hump-backed whales, bottle-nosed dolphins and Indo-Pacific hump-backed dolphins (Sousa chinen- sis). Lesions may be mild to severe. Obtaining diagnostic samples from free-ranging cetaceans is difficult.

A syndrome seen sporadically in hump-backed whales is characterised by ulceration and necrosis (Fig. 46.6). Various aetiologies have been suggested, including lacazi- osis and photohypersensitisation caused by toxins, but no diagnostic investigations have been undertaken to date.

4.2.5 Neoplasia

Neoplasia in managed and free-ranging cetaceans is rare.

a. Lymphoma

A multicentric lymphoma was diagnosed in an oceanarium- housed common bottle-nosed dolphin at necropsy (Blyde and Sandy 2016). Sheets of lymphocytes partially affected

Fig. 46.6. Stranded hump-backed whale (Megaptera novaeangliae) with severe necrotising dermatitis of unknown aetiology.

the splenic parenchyma and were extensively distributed throughout the hepatic parenchyma. Increased numbers of circulating lymphocytes were seen within the lung vas­culature and occasionally throughout vessels of the heart. The spleen had ruptured, resulting in haemoperitoneum. There were no premonitory signs. Interestingly, this ani­mal’s mother also had lymphoma at necropsy. Both were typed as B-cell lymphomas. Electron microscopy did not reveal the presence of a retrovirus in either case.

b. Squamous cell carcinoma

Squamous cell carcinoma (SCC) was diagnosed in a 38-yr-old oceanarium-housed male Indo-Pacific bottle­nosed dolphin. It presented with papillomatous lesions on the intermandibular frenulum and an infiltrative lesion of the soft palate. Treatment with piroxicam and doxycy­cline resulted in a marked reduction of the tumour’s size and a reversible hepatopathy. Complete resolution was not achieved but the lesion remains stable (March et al. 2016). Brachytherapy has been described as a treatment for this condition in a common bottle-nosed dolphin (McKinnie et al. 2005).

4.2.6 Biotoxins

Between August 2014 and June 2015, 23 Risso’s dolphins stranded on the east coast of Australia from south-east Qld to Tas. (the historic annual average is 1). All were single stranded animals, other than a mother and calf. Most appeared to be young adults, both males and females. The majority were in poor body condition and there were no external signs of trauma or entanglement. Many were found dead or died soon after or were euthanased. One animal was returned to the sea but re-stranded the next day and was euthanased. One animal was taken into care for reha­bilitation, but despite encouraging early signs the animal’s condition deteriorated and it was euthanased. One animal was returned to the sea and was not sighted again.

At necropsy, gross pathology was unremarkable in most cases. Blubber layers were reduced and the stom­achs of many of the animals were empty or contained unidentified tunicates or salps. A definitive diagnosis of disseminated toxoplasmosis was made in only one case, the first reported stranding. Histopathology revealed focal ischaemic neuronal necrosis of areas of the brain, including the hippocampus in a few of the cases. There were no other significant histological or microbiological findings. All were negative for morbillivirus, leptospiro­sis and brucellosis.

Toxicological investigations, including biotoxins, were inconclusive. Genetic testing was undertaken to examine the relatedness of all the stranded animals (results pending at time of writing). Based on the histo­logical changes in the brain, a marine biotoxin was pos­tulated as the cause of this unusual mortality event (D Blyde unpublished).

Domoic acid toxicity has been implicated as a possible cause of seasonal cetacean mass stranding events in Tas. (Nash et al. 2017).

4.2.7 Organic pollutants

Cagnazzi et al. (2013) found evidence of accumulation of organochlorine compounds, including dichlorodiphenyl­trichloroethane (DDTs), polychlorinated biphenyls (PCBs), hexachlorobenzene (HCB) and polycyclic aro­matic hydrocarbons (PAHs) in blubber biopsies from Indo-Pacific hump-backed dolphins and Australian snub-finned dolphins from the central and southern Great Barrier Reef. PAH levels were comparable to those reported from highly industrialised countries. DDTs and HCB were found at low levels, but in some individuals, PCBs were above the thresholds over which immunosup­pression and reproductive anomalies occur. Weijs et al. (2016) examined several carcasses of Indo-Pacific hump­backed dolphins and found levels of PCBs and dichlo­rodiphenyls (DDXs) in blubber at near or above toxicological thresholds associated with immune and reproductive toxicity.

Hump-backed whales were found to have levels of HCBs in their blubber at concentrations that could cause immunosuppression and negatively affect thyroid hor­mone homeostasis (Nash et al. 2013). They also found that this compound was concentrated further during fasting on their annual migration.

Stranded cetaceans including common bottle-nosed dolphins, Indo-Pacific bottle-nosed dolphins and short- beaked common dolphins along the southern coast of Australia were found to have high levels of per- and poly­fluoroalkyl substances (PFAS) in liver samples obtained at necropsy (Foord et al. 2024). Perfluorooctane sul­fonate (PFOS) - a PFAS compound - was also measured and was the major contributor to total PFAS levels. Although no direct link to the strandings could be attributed to the high levels of PFAS, these levels have the potential to impact the health of free-ranging cetacean populations.

4.2.8 Heavy metals

Although heavy metals have been found at reasonably high concentrations in free-ranging cetaceans in Austral­ian waters, there is no evidence to suggest that there is an association with stranding or deaths. Heavy metals could, however, have subclinical effects at a population level in areas where sediments are high in heavy metals, such as the Gladstone and Mackay harbours. Weijs et al. (2016) measured a suite of heavy metals and found the levels were similar to other studies in different countries and not at toxic levels. Lavery et al. (2008) showed that stranded common and bottle-nosed dolphins from Spen­cer Gulf had higher levels of hepatic lead levels, while those from Gulf St Vincent had higher hepatic mercury and selenium levels as well as higher bone lead levels..

An oceanarium-housed dolphin was diagnosed with lead poisoning after ingesting a diver’s lead weight. The animal was lethargic and had a reduced appetite. Radio­graphs and elevated blood lead levels (1.97 μmol∕L) were diagnostic. The removal of the object from the stomach and a 6-wk course of dimercaptosuccinic acid (600 mg bid PO) resolved the condition.

5.