Whale lice (Isocyamus deltobranchium & Isocyamus delphinii; Cyamidae) prevalence in odontocetes off the German and Dutch coasts – morphological and molecular characterization and health implications

Lehnert, Kristina; IJsseldijk, Lonneke L.; Uy, May Li; Boyi, Joy Ometere; van Schalkwijk, Linde; Tollenaar, Eveline A.P.; Gröne, Andrea; Wohlsein, Peter; Siebert, Ursula

doi:https://doi.org/10.1016/j.ijppaw.2021.02.015

Whale lice (Isocyamus deltobranchium & Isocyamus delphinii; Cyamidae) prevalence in odontocetes off the German and Dutch coasts – morphological and molecular characterization and health implications

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Whale lice (Isocyamus deltobranchium & Isocyamus delphinii; Cyamidae) prevalence in odontocetes off the German and Dutch coasts – morphological and molecular characterization and health implications

Lehnert, Kristina; IJsseldijk, Lonneke L.; Uy, May Li; Boyi, Joy Ometere; van Schalkwijk, Linde; Tollenaar, Eveline A.P.; Gröne, Andrea; Wohlsein, Peter; Siebert, Ursula

(2021) International Journal for Parasitology: Parasites and Wildlife, volume 15, pp. 22 - 30

(Article)

Abstract

Whale lice (Cyamidae; Amphipoda) are ectoparasitic crustaceans adapted to the marine environment with cetaceans as their host. There are few reports of cyamids occurring in odontocetes from the North Sea, and long-term studies are lacking. Marine mammal health was monitored along the German and Dutch coasts in the past decades, ... read more with extensive post mortem investigations conducted. The aim of this study was to analyse archived ectoparasite samples from stranded cetaceans from the North Sea (2010–2019), to determine species, prevalence and impact of ectoparasite infection. Ectoparasites were found on two cetacean species – harbour porpoises (Phocoena phocoena), as the most abundant cetacean species in the North Sea, and on a pilot whale (Globicephala melas), as a rare species here. Prevalence of ectoparasitic crustaceans in cetaceans was low: 7.6% in porpoises stranded in the Netherlands (n = 608) and 1.6% in porpoises stranded in Germany (n = 122). All whale lice infections were found on hosts with skin lesions characterised by ulcerations. Morphological investigations revealed characteristic differences between the cyamid species Isocyamus (I.) delphinii and I. deltobranchium identified. Isocyamus deltobranchium was determined in all infected harbour porpoises. I. delphinii was identified on only the pilot whale. Molecular analyses showed 88% similarity of mDNA COI sequences of I. delphinii with I. deltobranchium supporting them as separate species. Phylogenetic analyses of additional gene loci are required to fully assess the diversity and exchange of whale lice species between geographical regions as well as host specificity. Differing whale lice prevalences in porpoises stranded in the Netherlands and Germany could indicate a difference in severity of skin lesions between these areas. It should be further investigated if more inter- or intraspecific contact, e.g., due to a higher density of porpoises or contact with other cetaceans, or a poorer health status of porpoises in the southern North Sea could explain these differences.

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Keywords: Amphipoda, Ecology, Ectoparasitic crustacean, Host specificity, Odontocetes, Pathology, Parasitology, Animal Science and Zoology, Infectious Diseases

DOI: https://doi.org/10.1016/j.ijppaw.2021.02.015

ISSN: 2213-2244

Publisher: Elsevier BV

Note: Funding Information: Whale lice (Cyamidae; Amphipoda) are ectoparasitic crustaceans adapted to the marine environment with cetaceans as their host. There are few reports of cyamids occurring in odontocetes from the North Sea, and long-term studies are lacking. Marine mammal health was monitored along the German and Dutch coasts in the past decades, with extensive post mortem investigations conducted. The aim of this study was to analyse archived ectoparasite samples from stranded cetaceans from the North Sea (2010?2019), to determine species, prevalence and impact of ectoparasite infection. Ectoparasites were found on two cetacean species ? harbour porpoises (Phocoena phocoena), as the most abundant cetacean species in the North Sea, and on a pilot whale (Globicephala melas), as a rare species here. Prevalence of ectoparasitic crustaceans in cetaceans was low: 7.6% in porpoises stranded in the Netherlands (n = 608) and 1.6% in porpoises stranded in Germany (n = 122). All whale lice infections were found on hosts with skin lesions characterised by ulcerations. Morphological investigations revealed characteristic differences between the cyamid species Isocyamus (I.) delphinii and I. deltobranchium identified. Isocyamus deltobranchium was determined in all infected harbour porpoises. I. delphinii was identified on only the pilot whale. Molecular analyses showed 88% similarity of mDNA COI sequences of I. delphinii with I. deltobranchium supporting them as separate species. Phylogenetic analyses of additional gene loci are required to fully assess the diversity and exchange of whale lice species between geographical regions as well as host specificity. Differing whale lice prevalences in porpoises stranded in the Netherlands and Germany could indicate a difference in severity of skin lesions between these areas. It should be further investigated if more inter- or intraspecific contact, e.g., due to a higher density of porpoises or contact with other cetaceans, or a poorer health status of porpoises in the southern North Sea could explain these differences.Molecular analyses of the mDNA sequences supported that I. delphinii and I. deltobranchium are separate species but morphological and genetic differences are relatively small. All sequences of I. deltobranchium regardless of the origin of the porpoise host (Dutch or German waters) were 100% identical supporting that they are conspecific. It could also reflect a less rapid evolution of COI in I. deltobranchium or effective dispersion between hosts in the North Sea (Trobajo et al., 2010; Kaliszewska et al., 2005), however, I. deltobranchium sequences from other parts of the North Atlantic are required to support this. The intra-specific differences observed in sequences of I. delphinii specimens from the pilot whale could be a support for a faster evolution rate in the parasite than the host (Kaliszewska et al., 2005; Iwasa-Arai et al., 2017b). Phylogenetic comparison with other cyamid species COI sequences available in GenBank revealed two distinct clades, the Isocyamus and Cyamus clades. The two Isocyamus species obtained from this study were most closely related with an Isocyamus sp. sequence (Accession FJ751181.1) from GenBank, which was sampled from a short-finned pilot whale stranded in Humboldt County, California and putatively identified as I. globicipitis (Christopher Callahan, pers. comm.). According to the phylogenetic analysis, Isocyamus delphinii from this study is interpreted as sister species of the Isocyamus sp. sequence by Callahan (2008) from the US West coast, however, the genetic differences in the COI with about 12% are substantial, and similar to the molecular difference between I. delphinii and I. deltobranchium, indicating reproductive isolation for some time.Ethical standards: Ethical review and approval was not required for the animal study because all animals in our study were found dead, died naturally or were euthanized based on welfare grounds and none of the animals were killed for the purpose of this study. This publication was supported by Deutsche Forschungsgemeinschaft and University of Veterinary Medicine Hannover, Foundation within the funding programme Open Access Publishing.The authors wish to thank all individuals who report and collect marine mammals in Germany and the Netherlands, in particular the S?H national park rangers and seal hunters in Germany and all volunteers and organisation associated with the Dutch stranding network, as well as all ITAW and UU colleagues and assistants for their support during necropsies. The authors wish to thank Nadine Dup?rr? at CeNak, Hamburg for access to photo equipment. Furthermore, we would like to thank Juan Antonio Balbuena for providing reference specimens of I. delphini from Faroese pilot whales. The post-mortem investigations in Germany were partly funded by the Ministry of Energy, Agriculture, the Environment, Nature and Digitalisation in Schleswig-Holstein, Germany, and the Schleswig?Holstein National Park Service. The post-mortem investigations in the Netherlands are commissioned by the Dutch Ministry of Agriculture, Nature and Food Quality (2008?2015 under project reference number 140000353; 2016?2019 under project reference number WOT04-009-045), but no specific funding was acquired for this study. This publication was supported by Deutsche Forschungsgemeinschaft and the University of Veterinary Medicine Hannover, Foundation within the funding programme Open Access Publishing. Funding Information: The post-mortem investigations in Germany were partly funded by the Ministry of Energy, Agriculture, the Environment , Nature and Digitalisation in Schleswig-Holstein, Germany , and the Schleswig–Holstein National Park Service . The post-mortem investigations in the Netherlands are commissioned by the Dutch Ministry of Agriculture, Nature and Food Quality (2008–2015 under project reference number 140000353 ; 2016–2019 under project reference number WOT04-009-045 ), but no specific funding was acquired for this study. This publication was supported by Deutsche Forschungsgemeinschaft and the University of Veterinary Medicine Hannover, Foundation within the funding programme Open Access Publishing. Publisher Copyright: © 2021 The Author(s)

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