Abstract

In marine mammals, nematode-inflicted pathological lesions combined with other pathogens and factors (i.e., pollution, climate change, domoic acid poisoning events, and seasonal El Nino starvation events) negatively impact pinnipeds’ health and may cause mortality. Five California sea lions (Zalophus californianus)—a female pup, three male yearlings, and an adult female—suffered mortalities during rehabilitation at the Marine Mammal Care Center Los Angeles (San Pedro, CA). According to the necropsy reports, animals developed multisystemic parasitism as a leading cause of death, combined with malnutrition and hypoglycemia. In order to reveal host–parasite dynamics that may play a role in pinniped health and recovery, we examined the type and level of histopathological stomach lesions in California sea lions caused by anisakid nematodes. All isolated anisakids were morphologically and molecularly identified, and their phylogenetic relationships were reconstructed using the sequence of the mitochondrial COII gene. Co-parasitation of different Anisakidae spp. within the same host or lesions presented the opportunity to evaluate the existence of recombinant haplotypes and their eventual pathological pressure exerted onto host. The lesions were presented as chronic granulomatous gastritis, with moderate edema and hyperemia of the tunica submucosa and lamina propria, followed by mild, focal fibrosis of the gastric wall. Ulcerative changes with mixed leukocytic infiltrate showed to be localized, shallow, and non-perforative and with no apparent bacterial coinfection, mostly accompanied by healing granulation tissue. Isolated anisakids are grouped into three distinctively separated monophyletic clades corresponding to generaAnisakis,Contracaecum, andPseudoterranova. Most abundant were representatives ofContracaecum ogmorhini sensu lato(55.36%), followed byAnisakis pegreffii(23.21%),Pseudoterranova azarasi(17.86%),Pseudoterranova decipiens sensu lato(1.79%), andAnisakis simplex(1.79%). Phylogenetic trees revealed no differentiation at intra-species level. Our analysis of divergence revealedContracaecumseparated from other lineages in the Jurassic period at the 176.2 Mya andAnisakisdiverging fromPseudoterranovain Cenozoic period at 85.9 Mya.

Highlights

  • Existing data on marine mammal diversity, spatial and temporal distribution, abundance, and population structure within the marine ecosystem worldwide indicate mammals’ extreme vulnerability to exposure to significant anthropogenic impacts, such as disturbance, bycatch, and hunting (van der Elst and Everett, 2015)

  • Whether a similar pattern is followed by other nematode species, anisakids, should be evaluated in a broader population study of the California sea lions

  • In contrast to maternally transmitted U. lucasi, anisakids are trophically transmitted to sea lions, occurring well after the pup’s weaning period, which might warrant a better level of innate and acquired immunity in those animals and better prognosis for their survival, if not affected by other comorbid factors

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Summary

Introduction

Existing data on marine mammal diversity, spatial and temporal distribution, abundance, and population structure within the marine ecosystem worldwide indicate mammals’ extreme vulnerability to exposure to significant anthropogenic impacts, such as disturbance, bycatch, and hunting (van der Elst and Everett, 2015). These animals are gravely affected by various infectious diseases (Aznar et al, 2001), among which parasitic diseases represent a tipping over factor responsible for the regulation of marine mammal populations, on both the ecological and evolutionary scales (Raga et al, 1998). The US population (US or Pacific Temperate) and the western Baja California population, show population sizes above maximum net productivity level (MNPL) and within its optimum sustainable population (OSP) range but are still vulnerable to increasing sea surface temperature associated with El Nino events or similar regional ocean temperature anomalies (Laake et al, 2018).

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