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Abstract
Hookworms are highly pathogenic hematophagous nematodes that parasitize more than 100 species of wild animals. Hookworms of fur seals and sea lions are particularly virulent, causing high levels of mortality, however little is known about the drivers of these effects. During 10 reproductive seasons, the dynamics of hookworm diseases was studied in the South American fur seals (SAFS, Arctocephalus australis, Otariidae) rookery at Guafo Island, Chilean Patagonia. Fur seal hookworms (Uncinaria sp.) reached 100% prevalence among pups, and in animals with high burdens (>300 nematodes) there was marked hemorrhagic enteritis, sometimes with peritoneal penetration. The life cycle of Uncinaria sp. in SAFS involved brief lactogenic transmission of infective larvae. This hookworm species has a live fast die young life history strategy that translates into aggressive feeding behavior and high rates of extraction of host resources. Therefore, pups with high burdens, a third of pups born each year, suffered significant levels of anemia and up to 60% hookworm-related mortality. These pups contributed disproportionally to parasite fitness, and increases in host mortality (virulence) always paid off in terms of parasite fitness, selecting for higher virulence within the parasite population. Pups that survived hookworm infection developed an efficient immune-mediated parasite clearance where T-lymphocytes, basophils, mast cells and parasite specific IgG were key players. Pups that received higher levels of maternal attendance had better energy balance and a more reactive immune system. These pups cleared hookworm infection earlier, increasing their chances of survival. Maternal attendance decreased in years with high sea surface temperature (SST), probably reflecting less availability of prey in the environment. Therefore, in years with high SST, fur seal pups exhibited a weaker immune response and higher levels of hookworm mortality. Hookworm disease is the most significant cause of death in many otariid populations, and the present study demonstrates that the parasite is selected for higher virulence, especially when a high hookworm burden is favored. The key role of parasite immune clearance in hookworm infection dynamics and the link between environmental conditions and pups immune system present a scenario where global climate change may lead to increased hookworm virulence and mortality of fur seal pups.