Abstract

The biliary trematode Pseudamphistomum truncatum parasitizes a wide range of fish-eating mammals, including humans. Here we report the emergence of this parasite in grey seals (Halichoerus grypus) in the Baltic Sea. One hundred eighty-three of 1 554 grey seals (11.9%) examined from 2002–2013 had detectable hepatobiliary trematode infection. Parasite identification was confirmed as P. truncatum by sequencing the ITS2 region of a pool of five to 10 trematodes from each of ten seals collected off the coast of seven different Swedish counties. The proportion of seals parasitized by P. truncatum increased significantly over time and with increasing age of seals. Males were 3.1 times more likely to be parasitized than females and animals killed in fishery interactions were less likely to be parasitized than animals found dead or hunted. There was no significant difference in parasitism of seals examined from the Gulf of Bothnia versus those examined from the Baltic Proper. Although the majority of infections were mild, P. truncatum can cause severe hepatobiliary disease and resulted in liver failure in at least one seal. Because cyprinid fish are the second intermediate host for opisthorchiid trematodes, diets of grey seals from the Baltic Sea were analysed regarding presence of cyprinids. The proportion of gastrointestinal tracts containing cyprinid remains was ten times higher in seals examined from 2008 to 2013 (12.2%) than those examined from 2002 to 2007 (1.2%) and coincided with a general increase of trematode parasitism in the host population. The emergence and relatively common occurrence of P. truncatum in grey seals signals the presence of this parasite in the Baltic Sea ecosystem and demonstrates how aquatic mammals can serve as excellent sentinels of marine ecosystem change. Investigation of drivers behind P. truncatum emergence and infection risk for other mammals, including humans, is highly warranted.

Highlights

  • The grey seal (Halichoerus grypus) population in the Baltic Sea has suffered numerous insults including excessive hunting in the beginning of the 20th century followed by reproductive failure from polychlorinated biphenyls (PCBs) and other environmental contaminants in the latter half of the century [1]

  • Pseudamphistomum truncatum was first recorded in Baltic grey seals in 1986, whereas only scattered cases were observed prior to 2002 [15]

  • Based on a highly significant increase in annual parasite prevalence from 2002 to 2013 it can be stated that P. truncatum is recently emerging in grey seals from Swedish waters of the Baltic Sea

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Summary

Introduction

The grey seal (Halichoerus grypus) population in the Baltic Sea has suffered numerous insults including excessive hunting in the beginning of the 20th century followed by reproductive failure from polychlorinated biphenyls (PCBs) and other environmental contaminants in the latter half of the century [1]. As part of an on-going monitoring program to investigate health and environmental contaminants in grey seals from the Swedish Baltic coast, approximately 100– 150 animals that have been hunted, incidentally caught in fishing gear, or found stranded are examined by the Swedish Museum of Natural History each year. The biliary trematode, Pseudamphistomum truncatum, has an indirect life cycle, which includes a broad range of fish-eating mammals as the definitive host. The life cycle in the Baltic environment is poorly understood, opisthorchiid trematodes typically have two intermediate hosts: freshwater gastropods and cyprinid fish [2]. Described in marine mammal species (Caspian seals, Pusa caspisca) [6,7] and various terrestrial and semi-aquatic mammals such as wild mustelids and canids [8,9,10,11], cats (Felis domesticus) [12] and even humans [13] in Asia and Europe, this trematode recently has emerged in otters (Lutra lutra) and American mink (Mustela vison) in Great Britain and Ireland [14,5]

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