A review of lobomycosis and lobomycosis-like skin disease in cetaceans worldwide, with new data from the Gulf of Guayaquil, Ecuador.

Lobomycosis, also called paracoccidioidomycosis ceti, is a chronic mycotic cutaneous disease affecting odontocetes. Lobomycosis-like disease (LLD) has a clinical presentation consistent with lobomycosis but lacks a histological and molecular diagnosis. We review the literature on lobomycosis aetiology, clinical signs and pathogenesis, species affected and geographic distribution and examine the factors influencing the presence, transmission and prevalence of the disease, to better understand its ecology. In addition, we provide unpublished information on LLD in two common bottlenose dolphin (Tursiops truncatus) communities inhabiting the Gulf of Guayaquil, Ecuador. Lobomycosis and LLD occur in Delphinidae from the Atlantic, Pacific, and Indian Oceans between 33°N and 35°S. Primary risk factors include habitat, sex, age, sociality, and pollution. In dolphins from the Americas and Japan, lobomycosis is caused by Paracoccidioides ceti, family Ajellomycetaceae. The disease is characterized by cutaneous granulomatous lesions that may occur anywhere on the body, grow to large size, and may ulcerate. Histologically, the lesions consist of acanthosis and histiocytic granulomas between the skin and subcutaneous tissues, with inflammatory changes that extend deep into the dermis. Multiple yeast cells with a double refringent layer stained positive using Gomori-Grocott methenamine silver in the dermis of a T. truncatus from Ecuador diagnosed with LLD since 2011, a first record for the Southeast Pacific. Injuries may enable the entry of P. ceti into the dermis while skin contact likely favours transmission, putting males at higher risk than females. Lobomycosis and LLD may have a negative impact on small communities already threatened by anthropogenic factors.

We review lobomycosis and lobomycosis-like disease in cetaceans and give new information for bottlenose dolphins (Tursiops truncatus) from the Gulf of Guayaquil, Ecuador. Caused by Paracoccidioides ceti, the disease affects several dolphin species worldwide, including in Ecuador, for which we present a first record.

Role of social behaviour in the epidemiology of lobomycosis-like disease (LLD) in estuarine common bottlenose dolphins from Ecuador.

Lobomycosis-like disease (LLD) is a chronic granulomatous skin disorder that affects Delphinidae worldwide. LLD has been observed in common bottlenose dolphins Tursiops truncatus from the Gulf of Guayaquil, Ecuador, since 1990. Although exogenous factors such as salinity and pollution may play a role in the pathogenesis of this disease in estuarine and coastal dolphin communities, we hypothesized that demography and social behaviour may also influence its epidemiology. To address this issue, the role of social behaviour in the distribution and prevalence of LLD was assessed through hierarchical cluster analysis and spatial distribution analysis in 7 dolphin communities inhabiting the inner estuary. Individuals with LLD lesions were observed in 5 of the 7 dolphin communities, with 13 of the 163 (8%) animals being positive, all adults. Among 8 dolphins of known sex, LLD affected mostly males (86%), who usually were found in pairs. Prevalence was low to moderate (5.1-13%) in dolphin communities where low-rank males had LLD. Conversely, it was high (44.4%, n = 9) in a small community where a high-rank male was infected. LLD affected both dolphins in 2 of the 4 male pairs for which large time series data were available, suggesting horizontal transmission due to contact. Thus, association with LLD-positive males seems to be an important risk factor for infections. Additionally, low-rank males had larger home ranges than high-rank males, indicating that low-status LLD-affected dolphins are likely responsible for the geographic dissemination of the disease in this population.

Modular organizations of novel cetacean papillomaviruses.

The phylogenetic position of cetacean papillomaviruses (PVs: Omikron-PVs and Upsilon-PVs) varies depending on the region of the genome analysed. They cluster together with Alpha-PVs when analysing early genes and with Xi-PVs and Phi-PVs when analysing late genes. We cloned and sequenced the complete genomes of five novel PVs, sampled from genital and oesophageal lesions of free-ranging cetaceans: Delphinus delphis (DdPV1), Lagenorhynchus acutus (TtPV3 variant), and Phocoena phocoena (PphPV1, PphPV2, and PphPV3). Using Maximum Likelihood and Bayesian approaches, all cetacean PVs constituted a monophyletic group with Alpha-, Omega-, and Dyodelta-PVs as inferred from E1-E2 early genes analyses, thus matching the shared phenotype of mucosal tropism. However, cetacean PVs, with the exception of PphPV3, were the closest relatives of Xi-PVs and Phi-PVs in L2-L1 late genes analyses, isolated from cow and goat, thus reflecting the close relationship between Cetacea and Artiodactyla. Our results are compatible with a recombination between ancestral PVs infecting the Cetartiodactyla lineage. Our study supports a complex evolutionary scenario with multiple driving forces for PV diversification, possibly including recombination and also interspecies transmission.

Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors.

We reviewed prominent emerging infectious diseases of cetaceans, examined their potential to impact populations, re-assessed zoonotic risk and evaluated the role of environmental stressors. Cetacean morbilliviruses and papillomaviruses as well as Brucella spp. and Toxoplasma gondii are thought to interfere with population abundance by inducing high mortalities, lowering reproductive success or by synergistically increasing the virulence of other diseases. Severe cases of lobomycosis and lobomycosis-like disease (LLD) may contribute to the death of some dolphins. The zoonotic hazard of marine mammal brucellosis and toxoplasmosis may have been underestimated, attributable to frequent misdiagnoses and underreporting, particularly in developing countries and remote areas where carcass handling without protective gear and human consumption of fresh cetacean products are commonplace. Environmental factors seem to play a role in the emergence and pathogenicity of morbillivirus epidemics, lobomycosis/LLD, toxoplasmosis, poxvirus-associated tattoo skin disease and, in harbour porpoises, infectious diseases of multifactorial aetiology. Inshore and estuarine cetaceans incur higher risks than pelagic cetaceans due to habitats often severely altered by anthropogenic factors such as chemical and biological contamination, direct and indirect fisheries interactions, traumatic injuries from vessel collisions and climate change.

Genital warts in Burmeister's porpoises: characterization of Phocoena spinipinnis papillomavirus type 1 (PsPV-1) and evidence for a second, distantly related PsPV.

We identified sequences from two distantly related papillomaviruses in genital warts from two Burmeister's porpoises, including a PV antigen-positive specimen, and characterized Phocoena spinipinnis papillomavirus type 1 (PsPV-1). The PsPV-1 genome comprises 7879 nt and presents unusual features. It lacks an E7, an E8 and a bona fide E5 open reading frame (ORF) and has a large E6 ORF. PsPV-1 L1 ORF showed the highest percentage of nucleotide identity (54-55 %) with human papillomavirus type 5, bovine papillomavirus type 3 (BPV-3) and Tursiops truncatus papillomavirus type 2 (TtPV-2). This warrants the classification of PsPV-1 as the prototype of the genus Omikronpapillomavirus. PsPV-1 clustered with TtPV-2 in the E6 and E1E2 phylogenetic trees and with TtPV-2 and BPV-3 in the L2L1 tree. This supports the hypothesis that PV evolution may not be monophyletic across all genes.

Diseases, lesions and malformations in the long-beaked common dolphin Delphinus capensis from the Southeast Pacific.

Miscellaneous lesions of the head, skull, teeth, trunk, appendages, skin and genital tract were observed in 120 of 930 long-beaked common dolphins Delphinus capensis taken in fisheries off Peru between 1985 and 2000. Seven subsamples were defined according to the varying field sampling protocols. Forty-two dolphins showed at least 2 types of injuries or diseases affecting 1 or more organs. The majority (5 of 7) of traumas encountered were diagnosed as caused by violent, fisheries-related interactions, and the skin in 20.4 % of specimens (n = 54) showed healed scars from such interactions. Prevalences of malformations and traumas of crania (n = 103) were 2.9 and 1.9%, respectively. Lytic cranial lesions were present in 31.1% of dolphins (n = 103) and accounted for 84.2% of all bone injuries. Skull damage diagnostic for Crassicauda sp. infestation was encountered in 26.5% of dolphins (n = 98) and did not differ among sex and age classes. Crassicauda sp. and tooth infections were responsible for, respectively, 78.8 and 6.1% of the lytic lesions. Adult dolphins showed a high prevalence of worn and broken teeth (35%, n = 20) as well as damaged alveoli (20%, n = 70). Prevalence of 'paired teeth', a congenital condition, was 9.4% (n = 32). Lesions of the head, body and appendages were present in 10 dolphins and included traumas, deformations (e.g. scoliokyphosis and brachygnathia) and chronic mastitis. Ovarian cysts suggestive of follicular cysts were observed in 1 of 24 females. Chronic orchitis affected 1 of 78 males. Of 12 dolphins 2 had vesicular lesions of the penis. Prevalence of cutaneous lesions, abnormalities and scars ranged between 1.8% (n = 56) and 48.2% (n = 27).

Uterine adenocarcinoma with generalised metastasis in a bottlenose dolphin Tursiops truncatus from northern Patagonia, Argentina.

An endometrial adenocarcinoma with areas of squamous differentiation and generalised metastasis was observed in a bottlenose dolphin Tursiops truncatus stranded in northern Patagonia in July 1997. This is the second report of a uterine adenocarcinoma in a free-living cetacean and the first in a Delphinidae. This neoplasm likely compromised reproduction for several years. In addition, the dolphin presented tattoo-like skin lesions and its digestive tract was infested by Anisakis simplex, Pseudoterranova sp., Braunina cordiformis and Corynosoma australe.