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      Crassicaudiasis in three geographically and chronologically distant Cuvier's beaked whales ( Ziphius cavirostris) stranded off Brazil

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          Abstract

          The Cuvier's beaked whale (CBW; Ziphius cavirostris) is a cosmopolitan marine mammal found in deep tropical and temperate waters of all oceans. CBW strandings have been recorded sporadically in Brazil; however, there is lack of information available regarding their causes of stranding and/or death. Herein, we report the epidemiologic, pathologic, morphologic parasitologic features and molecular identification of arterial and renal crassicaudiasis by Crassicauda sp. in three geographically and chronologically distant CBW stranded off Brazil. CBW-1 was an adult male stranded dead in Rio Grande do Sul State. CBW-2 was an adult female that stranded alive in Sergipe State and died shortly after. CBW-3 was and adult male that stranded dead in Santa Catarina State. The most relevant pathologic findings in these three CBW were severe, chronic proliferative mesenteric and caudal aortic endarteritis and chronic granulomatous and fibrosing interstitial nephritis with renicular atrophy and loss, and numerous intralesional Crassicauda sp. nematodes. Furthermore, CBW-1 had concomitant gram-negative bacterial pneumonia and pulmonary and hepatic thromboembolism. Morphologic analysis of renal adult nematodes identified Crassicauda sp. in the three CBW. Molecular analyses targeting the 18S and ITS-2 ribosomal loci of renal nematodes in CBW-2 and CBW-3 identified C. anthonyi. It is believed that severe arterial and renal crassicaudiasis likely resulted or contributed significantly to morbidity and death of these animals. These results expand the known geographical range of occurrence of crassicaudiasis in CBW. Specifically, the present study provides the first accounts of arterial and renal crassicaudiasis in CBW off the southern hemisphere, specifically in CBW off Brazil, and to the authors' knowledge, it is the first record of C. anthonyi in the southern Atlantic Ocean.

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          Highlights

          • First record of Crassicauda anthonyi in cetaceans off the southern Atlantic Ocean.

          • Arterial and renal crassicaudiasis may be fatal in Ziphius cavirostris.

          • ITS-2 gene sequence analysis enables Crassicauda species identification.

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          Most cited references33

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          MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.

          The Molecular Evolutionary Genetics Analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.
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            "Gas and fat embolic syndrome" involving a mass stranding of beaked whales (family Ziphiidae) exposed to anthropogenic sonar signals.

            A study of the lesions of beaked whales (BWs) in a recent mass stranding in the Canary Islands following naval exercises provides a possible explanation of the relationship between anthropogenic, acoustic (sonar) activities and the stranding and death of marine mammals. Fourteen BWs were stranded in the Canary Islands close to the site of an international naval exercise (Neo-Tapon 2002) held on 24 September 2002. Strandings began about 4 hours after the onset of midfrequency sonar activity. Eight Cuvier's BWs (Ziphius cavirostris), one Blainville's BW (Mesoplodon densirostris), and one Gervais' BW (Mesoplodon europaeus) were examined postmortem and studied histopathologically. No inflammatory or neoplastic processes were noted, and no pathogens were identified. Macroscopically, whales had severe, diffuse congestion and hemorrhage, especially around the acoustic jaw fat, ears, brain, and kidneys. Gas bubble-associated lesions and fat embolism were observed in the vessels and parenchyma of vital organs. In vivo bubble formation associated with sonar exposure that may have been exacerbated by modified diving behavior caused nitrogen supersaturation above a threshold value normally tolerated by the tissues (as occurs in decompression sickness). Alternatively, the effect that sonar has on tissues that have been supersaturated with nitrogen gas could be such that it lowers the threshold for the expansion of in vivo bubble precursors (gas nuclei). Exclusively or in combination, these mechanisms may enhance and maintain bubble growth or initiate embolism. Severely injured whales died or became stranded and died due to cardiovascular collapse during beaching. The present study demonstrates a new pathologic entity in cetaceans. The syndrome is apparently induced by exposure to mid-frequency sonar signals and particularly affects deep, long-duration, repetitive-diving species like BWs.
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              Pathology and causes of death of stranded cetaceans in the Canary Islands (1999-2005).

              Between 1999 and 2005, 233 stranded cetaceans (comprising 19 species) were reported in the waters of the Canary Islands. Of these, 138/233 (59.2%) were subjected to a complete or partial standardized necropsy, including 4 Balaenopteridae, 9 Physeteridae, 8 Kogiidae, 27 Ziphiidae and 90 Delphinidae. Of these, 46/138 (33.3%) cetaceans were diagnosed with anthropogenic pathological categories (i.e. the cause of death was anthropogenic). These included fishing interaction (bycatch) (19 individuals), 'atypical' mass stranding events linked to naval exercises (13), ship collisions (8) and other anthropogenic-related pathology (6). 'Natural' (i.e. non-anthropogenic) causes of death accounted for another 82/138 (59.4%) cases, including infectious and non-infectious diseases (63), neonatal pathology (8), intra- and interspecific interactions (6) and mass strandings (5). The cause(s) of death could not be determined in 10/138 (7.3%) necropsied animals. The most common causes of death were ship collisions in 6/9 (66.6%) Physeteridae, 'atypical' mass stranding linked to naval exercises in 13/27 (48.1%) Ziphiidae, and 'natural' infectious and non-infectious diseases in 55/90 (61.1%) Delphinidae. Interaction with fishing activities was established as cause of death in 15/90 (16.7%) Delphinidae. These data show that a range of anthropogenic and natural single and mass mortality events occur in multiple cetacean species stranded in the Canary Islands.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                06 November 2021
                December 2021
                06 November 2021
                : 16
                : 262-269
                Affiliations
                [a ]Laboratório de Ecologia e Conservação - Centro de Estudos do Mar/UFPR, Universidade Federal do Paraná, Avenida Beira Mar, s/n, Pontal do Sul, 83255-000, Pontal do Paraná, Paraná, Brazil
                [b ]Setor de Patologia Veterinária, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, UFRGS. Av. Bento Gonçalves - Agronomia, Porto Alegre, RS, 90650-002, Brazil
                [c ]Animal Service, Rua Vinte e Cinco, 49007, 134reia Branca, Aracaju, SE, Brazil
                [d ]Centro de Estudos Costeiros, Limnológicos e Marinhos (CECLIMAR), Av. Tramandaí, Campus Litoral Norte, UFRGS, 95625-000, Imbé, RS, Brazil
                [e ]Centro Universitário São Judas – Campus Unimonte, Rua Comendador Martins, 52, Vila Mathias, 11015-530, Santos, SP, Brazil
                [f ]Fundação Mamíferos Aquáticos, Estrada de Matapuã, 411, Anexo Chácara Anjo Gabriel, Mosqueiro, 49100-00, São Cristovão, SE, Brazil
                [g ]Instituto Brasileiro para a Medicina da Conservação – Tríade, Rua Silveira Lôbo, 52061-030, Recife, PE, Brazil
                [h ]Instituto BW para conservação e medicina da fauna marinha, Rua Professora Sueli Brasil Flores n.88, bairro da Praia seca, 28972-765, Araruama, RJ, Brazil
                [i ]Laboratório de Helmintologia Veterinária, Faculdade de Veterinária, UFRGS, Rua Vinte e Cinco, 91540-000, Porto Alegre, RS, Brazil
                [j ]Associação R3 Animal, Parque Estadual do Rio Vermelho, 88061-500, Florianópolis, SC, Brazil
                [k ]Instituto Australis, Av. Atlântica sn CP. 201 - Itapirubá Norte, 88780-000, Imbituba, SC, Brazil
                [l ]Department of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, 77843, College Station, TX, USA
                [m ]Texas A&M Veterinary Medical Diagnostic Laboratory, 483 Agronomy Rd., 77843, College Station, TX, USA
                Author notes
                []Corresponding author. josue.diazdelgado@ 123456tvmdl.tamu.edu
                Article
                S2213-2244(21)00112-7
                10.1016/j.ijppaw.2021.10.010
                8605309
                0d2f9151-0d02-4cdb-b488-05b92a289930
                © 2021 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 8 July 2021
                : 24 October 2021
                : 25 October 2021
                Categories
                Article

                crassicauda,cetacean,bronchopneumonia,marine mammal,nematode,parasitism

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