Abstract

Parasite life histories are considered the result of adaptation of the parasite to its hosts and their environment. In this adaptive process most parasites reach an equilibrium with their host to cause mild or moderate levels of harm, or virulence.¹ Hookworms are widespread parasites of terrestrial mammals; however, they have successfully colonized marine environments by infecting most otariid species.^2,3,4 This process could have led to adaptations in the otariid hookworms responsible for the high levels of virulence observed in the marine hookworms. To test this hypothesis, in the Austral summers of 2014–2016, we collected epidemiological and physiological data, and experimentally manipulated hookworm infection in a rookery of South American fur seals (SAFS) in order to i) describe the life cycle of Uncinaria sp. in SAFS, ii) determine if parasite and host life history traits are correlated, iii) determine if parasite fitness is maximized at high levels of host exploitation (virulence). Fur seal pups acquired hookworms through their mother's milk and became patent at day 14–18 post-infection; however, all pups that survived hookworm infection eliminated hookworms by 10-weeks-old. The embryonated eggs larvated in the soil rookery between 48 and 72 hours and became infective stage 3 larvae (L3) in other 48 to 72 hours. The infective L3 penetrated the skin of females and became hypobiotic in the subcutaneous tissue until the next reproductive cycle. Environmental survival of infective L3s was poor, with most larvae dying a few weeks after being in the rookery soil. Hookworms were very efficient at transforming host resources (blood) in infective stages (embryonated eggs), and female parasites did not experience a decline in egg production despite reaching high densities within a pup (>1000 nematodes). Therefore, the level of parasite fitness, measured as their basic reproductive number R₀, increased with higher levels of pup anemia and pup mortality (virulence) (Third-order polynomial regression, r² =0.65, p<0.0001). The parasites with the highest R₀ (higher fitness)were those that produced large numbers of infective stages early in the fur seal breeding season, when the density of the next susceptible host in the transmission cycle, female fur seals, is also higher (GLM.NB, p-value <0.0001, df=109). Otariids hookworms cause acute infections, which differ from terrestrial hookworms that usually establish chronic infections. The early host mortality or parasite clearance observed in hookworms of otariids, suppose a problem for the parasite as fitness is drastically decreased (parasite die young). However, otariid hookworms have overcome this problem by producing large numbers of infective stages in a short period of time (parasite live fast). This translates in high levels of resource extraction despite the adverse health consequences for the host.^3,4 We present empirical evidence that in some parasite-host systems, maintenance of the parasite in the population is favored by high levels of virulence. The development of this increased virulence in otariid hookworms could be related to specific adaptations to the marine lifestyle of their hosts.

Acknowledgements

Work partially funded by Morris Animal Foundation (grant D16ZO-413), Society for marine mammalogy small grants-in-aid and Rufford small grant foundation. We appreciate the field collaboration of Dr Lorraine Barbosa, Dr Ignacio Silva and Eugene DeRango. We thank the logistical support of the Chilean Navy and Guafo Island lighthouse crews.

Literature Cited

1.  Schmid-Hempel P. 2011. Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. New York, NY, USA: Oxford University press; 350 pp.

2.  Lyons ET, Spraker TR, De Long RL, Ionita M, Melin SR, Nadler SA, Tolliver SC. 2011. Review of research on hookworms (Uncinaria lucasi Stiles, 1901) in northern fur seals (Callorhinus ursinus Linnaeus, 1758). Parasitol Res. 109:257–65.

3.  Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Submitted for publication.

4.  Seguel M, Muñoz F, Navarrete MJ, Howerth E, Paredes E, Gottdenker N. Hookworm infection in South American fur seal (Arctocephalus australis) pups: pathology and factors associated with host tissue damage and mortality. Vet Pathol. In press.

5.  Seguel M, Paves H, Paredes E, Schlatter R. 2013. Causes of mortality in South American fur seal pups (Arctophoca australis gracilis) at Guafo Island, southern Chile (2004–2008). Mar Mammal Sci. 29:36–47.