An insight into the epidemiology of dolphin morbillivirus worldwide

Serum samples from 288 cetaceans representing 25 species and originating from 11 different countries were collected between 1995 and 1999 and examined for the presence of dolphin morbillivirus (DMV)-specific antibodies by an indirect ELISA (iELISA) (N = 267) or a plaque reduction assay (N = 21). A total of 35 odontocetes were seropositive: three harbour porpoises (Phocoena phocoena) and a common dolphin (Delphinus delphis) from the Northeastern (NE) Atlantic, a bottlenose dolphin (Tursiops truncatus) from Kent (England), three striped dolphins (Stenella coeruleoalba), two Risso's dolphins (Grampus griseus) and a bottlenose dolphin from the Mediterranean Sea, one common dolphin from the Southwest (SW) Indian Ocean, three Fraser's dolphins (Lagenodelphis hosei) from the SW Atlantic, 18 long-finned pilot whales (Globicephala melas) and a bottlenose dolphin from the SW Pacific as well as a captive bottlenose dolphin (Tursiops aduncus) originally from Taiwan. The presence of morbillivirus antibodies in 17 of these animals was further examined in other iELISAs and virus neutralization tests. Our results indicate that DMV infects cetaceans worldwide. This is the first report of DMV-seropositive animals from the SW Indian, SW Atlantic and West Pacific Oceans. Prevalence of DMV-seropositives was 85.7% in 21 pilot whales from the SW Pacific and both sexually mature and immature individuals were infected. This indicates that DMV is endemic in these animals. The same situation may occur among Fraser's dolphins from the SW Atlantic. The prevalence of DMV-seropositives was 5.26% and 5.36% in 19 common dolphins and 56 harbour porpoise from the NE Atlantic, respectively, and 18.75% in 16 striped dolphins from the Mediterranean. Prevalence varied significantly with sexual maturity in harbour porpoises and striped dolphins; all DMV-seropositives being mature animals. The prevalence of seropositive harbour porpoise and striped dolphins appeared to have decreased since previous studies. These data suggest that DMV is not endemic within these populations, that they are losing their humoral immunity against the virus and that they may be vulnerable to new epidemics.     

Histopathological and immunohistochemical studies on cetaceans found stranded on the coast of Italy between 1990 and 1997

Detailed histopathological and immunohistochemical studies were carried out on 24 cetaceans, 17 of which were striped dolphins (Stenella coeruleoalba), four bottlenose dolphins (Tursiops truncatus) and three Risso's dolphins (Grampus griseus), all found stranded on the Italian coast between 1990 and 1997. The most frequently detected lesions were chronic pneumonia (73.7% of the examined lungs), focal chronic pancreatitis (71.4%), non-purulent encephalitis (50%), chronic hepatitis (42.1%), and chronic focal interstitial nephritis (31.2%). The skin and the subcutaneous panniculus were often (33.3%) affected by parasitic diseases (Phyllobothrium delphini and Pennella sp.). An appreciable percentage of animals showed lymphoid depletion in their lymphatic organs (47.2%), as well as a high rate of parasitic infestations in their alimentary tracts (25%).     

Bartonella species detection in captive, stranded and free-ranging cetaceans

We present prevalence of Bartonella spp. for multiple cohorts of wild and captive cetaceans. One hundred and six cetaceans including 86 bottlenose dolphins (71 free-ranging, 14 captive in a facility with a dolphin experiencing debility of unknown origin, 1 stranded), 11 striped dolphins, 4 harbor porpoises, 3 Risso's dolphins, 1 dwarf sperm whale and 1 pygmy sperm whale (all stranded) were sampled. Whole blood (n = 95 live animals) and tissues (n = 15 freshly dead animals) were screened by PCR (n = 106 animals), PCR of enrichment cultures (n = 50 animals), and subcultures (n = 50 animals). Bartonella spp. were detected from 17 cetaceans, including 12 by direct extraction PCR of blood or tissues, 6 by PCR of enrichment cultures, and 4 by subculture isolation. Bartonella spp. were more commonly detected from the captive (6/14, 43%) than from free-ranging (2/71, 2.8%) bottlenose dolphins, and were commonly detected from the stranded animals (9/21, 43%; 3/11 striped dolphins, 3/4 harbor porpoises, 2/3 Risso's dolphins, 1/1 pygmy sperm whale, 0/1 dwarf sperm whale, 0/1 bottlenose dolphin). Sequencing identified a Bartonella spp. most similar to B. henselae San Antonio 2 in eight cases (4 bottlenose dolphins, 2 striped dolphins, 2 harbor porpoises), B. henselae Houston 1 in three cases (2 Risso's dolphins, 1 harbor porpoise), and untyped in six cases (4 bottlenose dolphins, 1 striped dolphin, 1 pygmy sperm whale). Although disease causation has not been established, Bartonella species were detected more commonly from cetaceans that were overtly debilitated or were cohabiting in captivity with a debilitated animal than from free-ranging animals. The detection of Bartonella spp. from cetaceans may be of pathophysiological concern.     

Malignant seminoma with metastasis, Sertoli cell tumor, and pheochromocytoma in a spotted dolphin (Stenella frontalis) and malignant seminoma with metastasis in a bottlenose dolphin (Tursiops truncatus)

Seminoma with metastasis was diagnosed in a spotted dolphin (Stenella frontalis) and an Atlantic bottlenose dolphin (Tursiops truncatus). Sertoli cell tumor and pheochromocytoma were also diagnosed in the spotted dolphin. The spotted and bottlenose dolphins were adult males that stranded and died on the coasts of northwest Florida and southeast North Carolina, respectively. Neoplasia is infrequently reported in cetaceans. This is the first report of seminoma, Sertoli cell tumor, and pheochromocytoma in a dolphin, the first report of three distinct neoplasms in a dolphin, and one of the few reports of malignant neoplasia in dolphins.     

A pioneering survey of deep-diving and off-shore cetaceans in the northern South China Sea

A pioneering boat-based survey was conducted in 2019, to gather baseline information regarding the presence, composition, relative abundance, and spatial distribution of deep-diving and off-shore cetaceans in the northern South China Sea (SCS). A total of 27 sightings comprising at least 8 cetacean species were recorded during the 13-day survey, including 5 deep-diving species (i.e. Risso's dolphin [Grampus griseus], short-finned pilot whale [Globicephala macrorhynchus], sperm whale [Physeter macrocephalus], Cuvier's beaked whale [Ziphius cavirostris], and an unidentified beaked whale [either the ginkgo-toothed beaked whale, Mesoplodon ginkgodens, or Deraniyagala's beaked whale, Mesoplodon hotaula]), as well as 3 off-shore dolphins (i.e. pantropical spotted dolphin [Stenella attenuate], striped dolphin [Stenella coeruleoalba], and Fraser's dolphin [Lagenodelphis hosei]). With the exception of pantropical spotted dolphins, all other species were sighted and recorded at sea in the northern SCS for the first time. The pantropical spotted dolphin was the most frequently sighted species, comprising 30% of the total sightings. Deep-diving cetaceans were mainly sighted in the northern Xisha Archipelago, whereas off-shore dolphins were distributed across the survey area. The pantropical spotted dolphin was observed in aggregations of more than 100 individuals and nearly all encountered species included calves; these findings suggested that the survey area functions as an important feeding and calving ground for various cetacean species. This pioneering survey provides fundamental information regarding cetacean fauna in the northern SCS and highlights the need to strengthen research and conservation efforts concerning these species.     

Predation on Large Mammals in the Kafue National Park,Zambia

Clymene dolphins, Stenella clymene, are endemic to the tropical and subtropical Atlantic Ocean, where their occurrence is documented from fewer than 200 records. The species is particularly poorly known in the eastern Atlantic off the coast of Africa where only 12 verified records exist, predominantly comprising dead animals. Marine mammal survey work was carried out off central West Africa during 2004 and 2005, producing two new observations of freeranging Clymene dolphins. Both sightings occurred in deep-water (466 and 684 m) over the shelf edge, off northern Angola and Congo respectively. A pod of 250 Clymene dolphins was observed off Congo, while the Angola sighting was of a mixed-species group of 12 Clymene dolphins with common dolphins, Delphinus sp. These records represent the first confirmed presence of Clymene dolphins off Angola and Congo, and extend the known southern limit of the confirmed distribution range of this species in the South-East Atlantic to 06°26‘S.     

Pathological and immunohistochemical study of gastrointestinal lesions in dolphins stranded in the Canary Islands

This paper describes the gross, histopathological and immunohistochemical characteristics of gastrointestinal lesions and regional lymph nodes of six common dolphins (Delphinus delphis), 11 striped dolphins (Stenella coeruleoalba) and six Atlantic spotted dolphins (Stenella frontalis) found stranded along the coasts of the Canary Islands. The most common lesion was chronic granulomatous gastritis of the glandular stomach, associated with the parasite Pholeter gastrophilus, and characterised by the parasites, their eggs, or parasite debris in the mucosa, submucosa or tunica muscularis, surrounded by numerous lysozyme-positive macrophages and neutrophils, and more peripherally by abundant fibrous tissue containing variable numbers of immunoglobulin (Ig) G+ plasma cells, and small numbers of CD3+ T lymphocytes and IgM+ and IgA+ plasma cells. Anisakis simplex nematodes were found in two dolphins that were also parasitised by P gastrophilus and had parasitic granulomatous gastritis and multiple small chronic gastric ulcers. Lymphoplasmacytic enteritis was found in eight cases, three of them parasitised by Diphyllobothrium species; the lesion was characterised by moderate to severe infiltrations of CD3+ T lymphocytes and IgG+ plasma cells, with small numbers of IgM+ and IgA+ plasma cells in the lamina propria and submucosa, mainly of the small intestine. One dolphin had severe fibrinopurulent peritonitis, which may have been secondary to gastric perforation caused by the large mural granulomatous gastritis associated with P gastrophilus parasitism.     

Pathology of morbillivirus infection in striped dolphins (Stenella coeruleoalba) from Valencia and Murcia, Spain.

During the summer and fall of 1990 hundreds of striped dolphins (Stenella coeruleoalba) died in the Spanish Mediterranean as a result of morbillivirus infection. A pathological investigation was carried out on dolphins from Valencia and Murcia which were among the first to die in the epizootic. The dolphins were in poor body condition and pneumonia was the main necropsy finding. Microscopic lung lesions characterized by necrosis of bronchial and bronchiolar epithelium and infiltration of alveoli with macrophages, lymphocytes, neutrophils and multinucleated syncytia were seen in most dolphins. Cytoplasmic and nuclear eosinophilic viral inclusions were present in bronchial and bronchiolar epithelium and in syncytia. Focal granulomatous inflammation associated with nematodes was also present. Brain lesions included diffuse degeneration and necrosis of neurons, microgliosis, perivascular cuffing, formation of syncytia and focal demyelination. Cytoplasmic and nuclear eosinophilic inclusions were present in neurons and glial cells. There was severe lymphoid necrosis and depletion of spleen and lymph nodes and syncytia also occurred in lymph nodes. Biliary and transitional epithelium contained nuclear and cytoplasmic eosinophilic inclusions. Immunoperoxidase staining using monoclonal antibodies to phocine distemper virus confirmed the presence of morbillivirus antigens in lung and brain. The distribution and severity of lesions in striped dolphins are similar to those of distemper in seals, harbor porpoises and terrestrial mammals. The formation of syncytia in the lung and brain may be a useful pathological indicator of morbillivirus infection and may be used in the investigation of pinniped and cetacean strandings in North America.     

Genotyping of Toxoplasma gondii isolates in meningo-encephalitis affected striped dolphins (Stenella coeruleoalba) from Italy

This study reports the occurrence of Toxoplasma gondii in the brain of three striped dolphins (Stenella ceoruleoalba) found stranded on the Ligurian Sea coast of Italy between 2007 and 2008. These animals showed a severe, subacute to chronic, non-purulent, multifocal meningo-encephalitis, with the cerebral parenchyma of two dolphins harbouring protozoan cysts and zoites immunohistochemically linked to T. gondii. Molecular, phylogenetic and mutation scanning analyses showed the occurrence of Type II and of an atypical Type II T. gondii isolates in one and two dolphins, respectively. In spite of the different molecular patterns characterizing the above T. gondii genotypes, the brain lesions observed in the three animals showed common microscopic features, with no remarkable differences among them. The role of T. gondii in causing the meningo-encephalitis is herein discussed.     

Pathologic and immunocytochemical studies of morbillivirus infection in striped dolphins (Stenella coeruleoalba).

Hundreds of striped dolphins (Stenella coeruleoalba) died along the Spanish Mediterranean coast during the second half of 1990. We necropsied 58 dolphins. Partial collapse of the lungs with patchy atelectasis, subcutaneous edema, icterus, and stomatitis were the most prominent gross morphologic changes. Histologically, a bronchiolo-interstitial pneumonia was the most frequent lesion (72% of the animals). It was characterized by hyperplasia of alveolar epithelial type II cells and formation of multinucleate syncytia in alveolar and bronchiolar lumina. Other prominent lesions were encephalitis (69%), lymphoid depletion, and formation of multinucleate syncytia in the cortex of lymph nodes. The distribution of morbillivirus antigen was investigated in 23 well-preserved dolphins using a monoclonal antibody against the hemagglutinin glycoprotein of phocine distemper virus. Positive immunostaining was found in brain (77%), in lung (70%), and in mesenteric (61%), mediastinal (47%), and prescapular (45%) lymph nodes. Phocine distemper virus antigen was demonstrated less frequently in trachea, stomach, biliary epithelium, intestine, kidney, and mammary gland. Necrotizing-hemorrhagic pneumonia and encephalitis due to Aspergillus fumigatus were seen in three dolphins, whereas two animals had lesions of toxoplasmosis. Changes in our dolphins were similar to those caused by distemper in seals and porpoises. The origin of the dolphin virus and the relationships among dolphin, seal, and porpoise morbilli viruses are unknown.     

Distributive and phagocytic characteristics of hepatic macrophages in five cetaceans belonging to Delphinidae and Ziphiidae

Details of morphology and distribution of hepatic macrophages in cetaceans were investigated using the immunohistochemistry with an antibody (SRA-E5) generated against human macrophage scavenger receptor antigen. Liver samples were obtained from five species of cetaceans (Baird's beaked whales, short-finned pilot whales, Risso's dolphins, bottlenose dolphins, and pantropical spotted dolphins). Except for two species of whales, the number of SRA-E5-positive Kupffer cells was greatest in the perivenous zone (zone 3), followed by the mid-zonal (zone 2) and periportal (zone 1) zones; this distribution pattern was different from that in cattle examined here and previously reported rodents with the highest number in zone 1. The frequency of Kupffer cell in each of zones was significantly different among species, and interestingly, the total mean of the Kupffer cell number in three zones increased as the body-length of species was small. In cetaceans, Kupffer cells in zone 1 appeared larger and more stellate in shape, whereas those in zone 3 were smaller and rounder. All cetaceans but Baird's beaked whales had the black pigment-containing Kupffer cells, with the greatest number in zone 3, and macrophages with the similar pigments were also seen in the hepatic intermediate septa, indicating an active phagocytosis. Most of the black pigments were considered to be lipofuscin and such pigments were not seen in the bovine livers. These results indicate that cetacean hepatic macrophages show differences in the distribution and phagocytosis among hepatic lobular zones, or between cetacean species and terrestrial animals.     

Acute and chronic gas bubble lesions in cetaceans stranded in the United Kingdom

The first evidence suggestive of in vivo gas bubble formation in cetacea, including eight animals stranded in the UK, has recently been reported. This article presents the pathologic findings from these eight UK-stranded cetaceans and two additional UK-stranded cetacean cases in detail. Hepatic gas-filled cavitary lesions (0.2-6.0 cm diameter) involving approximately 5-90% of the liver volume were found in four (two juvenile, two adult) Risso's dolphins (Grampus griseus), three (two adult, one juvenile) common dolphins (Delphinus delphis), an adult Blainville's beaked whale (Mesoplodon densirostris), and an adult harbour porpoise (Phocoena phocoena). Histopathologic examination of the seven dolphin cases with gross liver cavities revealed variable degrees of pericavitary fibrosis, microscopic, intrahepatic, spherical, nonstaining cavities (typically 50-750 microm in diameter) consistent with gas emboli within distended portal vessels and sinusoids and associated with hepatic tissue compression, hemorrhages, fibrin/organizing thrombi, and foci of acute hepato-cellular necrosis. Two common dolphins also had multiple and bilateral gross renal cavities (2.0-9.0 mm diameter) that, microscopically, were consistent with acute (n = 2) and chronic (n = 1) arterial gas emboli-induced renal infarcts. Microscopic, bubblelike cavities were also found in mesenteric lymph node (n = 4), adrenal (n = 2), spleen (n = 2), pulmonary associated lymph node (n = 1), posterior cervical lymph node (n = 1), and thyroid (n = 1). No bacterial organisms were isolated from five of six cavitated livers and one of one cavitated kidneys. The etiology and pathogenesis of these lesions are not known, although a decompression-related mechanism involving embolism of intestinal gas or de novo gas bubble (emboli) development derived from tissues supersaturated with nitrogen is suspected.     

Dolphins and their diseases

Thirty-eight species of small cetaceans termed "dolphins" and "porpoises" are listed. This review is a contribution to the growing community and veterinary interest in the welfare and diseases of these animals.     

An assessment of the effects of ruminal selenium pellets given to young sheep grazing selenium-deficient pastures

Thirty-eight species of small cetaceans termed “dolphins” and “porpoises” are listed. This review is a contribution to the growing community and veterinary interest in the welfare and diseases of these animals.     

Complex polysaccharide inclusions in the skeletal muscle of stranded cetaceans

Skeletal muscle samples were examined post-mortem in 148 cetaceans over a 12-year period. Histological analysis included haematoxylin and eosin (HE) and periodic acid-Schiff (PAS) staining with and without diastase digestion. In addition, histological muscle sections were immunostained for ubiquitin and fast and slow heavy-chain myosin isoforms. PAS-positive, diastase-resistant inclusions were detected in 26 animals from 11 different species. Older cetaceans were preferentially affected. These intrafibre inclusions varied from large aggregates to multiple coarse granules and were typically associated with type II fibres. All diastase-resistant inclusions were positive for ubiquitin. These features resembled those inclusions described as complex polysaccharide in horses. Based on these histological findings and the ubiquitin staining pattern, a morphological diagnosis of complex polysaccharide storage myopathy is proposed.     

Parasites of cetaceans stranded on the Pacific coast of Costa Rica

Information regarding parasitic fauna of cetaceans from Costa Rica is provided for the first time. A total of 25 stranded dolphins and whales were examined between 2001 and 2009, including striped dolphin (Stenella coeruleoalba) (n=19), pantropical spotted dolphin (S. attenuata) (n=2), spinner dolphin (S. longirostris) (n=1), bottlenose dolphin (Tursiops truncatus) (n=1), dwarf sperm whale (Kogia sima) (n=1) and Cuvier's beaked whale (Ziphius cavirostris) (n=1). Pathological findings associated with the parasites are also presented. In the most representative dolphin species, S. coeruleoalba, the prevalence of parasites was 89.5%; moreover, all examined specimens of S. attenuata, S. longirostris, T. truncatus and Z. cavirostris presented parasites. No parasites were recovered from K. sima. Fourteen helminth taxa were identified, including six species of cestodes (Strobilocephalus triangularis, Tetrabothrius forsteri, Trigonocotyle sp., Phyllobothrium delphini, Monorygma grimaldi, Tetraphyllidea gen. sp. plerocercoid), four digeneans (Nasitrema globicephalae, Brachycladium palliatum, B. pacificum and Oschmarinella albamarina) and four nematodes (Anisakis spp., Halocercus lagenorhynchi, Halocercus sp. and Crassicauda anthonyi). A commensal crustacean, Xenobalanus globicipitis, was also identified. All identified parasites representing new geographic records for the Pacific coast of Central America and new host records are presented. Parasitological information is valuable for conservation of cetaceans in Pacific coast of Costa Rica.     

Determination of the immunotoxic potential of heavy metals on the functional activity of bottlenose dolphin leukocytes in vitro

Heavy metals may affect the immune system of cetaceans. But no information exists on their effects on the bottlenose dolphin (Tursiops truncatus) immune system, although this species is a coastal top predator which can bioaccumulate high concentrations of them. This work studies the effects of Hg (1, 5 and 10mg/L), Al (2,5, 25 and 50mg/L), Cd (1, 10, 20 and 40mg/L), Pb (1, 10, 20 and 50mg/L) and Cr (1 and 10mg/L), on the function of phagocytes and lymphocytes isolated from the peripheral blood of bottlenose dolphins under in vitro conditions. Cell viability, apoptosis, lymphocyte proliferation and phagocytosis were evaluated. Viability and lymphoproliferation were measured with Alamar Blue assay, and apoptosis and phagocytosis were evaluated with flow cytometry. Apoptosis was detected as mechanism of cell death after cadmium and mercury exposure. A significant reduction in the lymphoproliferative response was registered by exposure to 1mg/L of mercury, 10mg/L of cadmium and 50mg/L of lead. Decreased phagocytosis was also observed at 5mg/L of mercury, 50mg/L of aluminium and 10mg/L of cadmium. Chromium did not present any effects on any immune assay at the concentrations tested. The concentrations of heavy metals that were found to affect the functional activity of bottlenose dolphin leukocytes are within the environmental ranges reported in the tissues of bottlenose dolphins. These results support the hypothesis that exposure to these contaminants, particularly mercury and cadmium could lead to a reduction in host resistance to disease in these animals.     

Novel gastric helicobacters and oral campylobacters are present in captive and wild cetaceans

The mammalian gastric and oral mucosa may be colonized by mixed Helicobacter and Campylobacter species, respectively, in individual animals. To better characterize the presence and distribution of Helicobacter and Campylobacter among marine mammals, we used PCR and 16S rDNA sequence analysis to examine gastric and oral samples from ten dolphins (Tursiops gephyreus), one killer whale (Orcinus orca), one false killer whale (Pseudorca crassidens), and three wild La Plata river dolphins (Pontoporia blainvillei). Helicobacter spp. DNA was widely distributed in gastric and oral samples from both captive and wild cetaceans. Phylogenetic analysis demonstrated two Helicobacter sequence clusters, one closely related to H. cetorum, a species isolated from dolphins and whales in North America. The second related cluster was to sequences obtained from dolphins in Australia and to gastric non-H. pylori helicobacters, and may represent a novel taxonomic group. Dental plaque sequences from four dolphins formed a third cluster within the Campylobacter genus that likely represents a novel species isolated from marine mammals. Identification of identical Helicobacter spp. DNA sequences from dental plaque, saliva and gastric fluids from the same hosts, suggests that the oral cavity may be involved in transmission. These results demonstrate that Helicobacter and Campylobacter species are commonly distributed in marine mammals, and identify taxonomic clusters that may represent novel species.