title: Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host.
abstract: Parasitic infection has a direct physiological cost to hosts but may also alter how hosts interact with other individuals in their environment. Such indirect effects may alter both host fitness and the fitness of other individuals in the host's social network, yet the relative impact of direct and indirect effects of infection are rarely quantified. During reproduction, a host's social environment includes family members who may be in conflict over resource allocation. In such situations, infection may alter how resources are allocated, thereby redistributing the costs of parasitism between individuals. Here, we experimentally reduce parasite burdens of parent and/or nestling European shags (Phalacrocorax aristotelis) infected with Contracaecum nematodes in a factorial design, then simultaneously measure the impact of an individual's infection on all family members. We found no direct effect of infection on parent or offspring traits but indirect effects were detected in all group members, with both immediate effects (mass change and survival) and longer-term effects (timing of parents' subsequent breeding). Our results show that parasite infection can have a major impact on individuals other than the host, suggesting that the effect of parasites on population processes may be greater than previously thought.
authors.affiliation: Wellcome Centre for Infection, Immunity and Evolution, Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Building, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK hanna@granroth-wilding.co.uk.
authors.forename: Hanna M V
authors.initials: HM
authors.lastname: Granroth-Wilding
authors.affiliation: NERC Centre for Ecology and Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK.
authors.forename: Sarah J
authors.initials: SJ
authors.lastname: Burthe
authors.affiliation: Wellcome Centre for Infection, Immunity and Evolution, Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Building, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK.
authors.forename: Sue
authors.initials: S
authors.lastname: Lewis
authors.affiliation: Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Jarrett Building, Bearsden Road, Glasgow G61 1QH, UK.
authors.forename: Katherine A
authors.initials: KA
authors.lastname: Herborn
authors.affiliation: Wellcome Centre for Infection, Immunity and Evolution, Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Building, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK.
authors.forename: Emi A
authors.initials: EA
authors.lastname: Takahashi
authors.affiliation: NERC Centre for Ecology and Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK.
authors.forename: Francis
authors.initials: F
authors.lastname: Daunt
authors.affiliation: Wellcome Centre for Infection, Immunity and Evolution, Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Building, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK.
authors.forename: Emma J A
authors.initials: EJ
authors.lastname: Cunningham
mesh_terms: D000818:Animals; D000969:Antinematodal Agents / Q000008:administration & dosage / Q000494:pharmacology; D017191:Ascaridida Infections / Q000469:parasitology / Q000662:veterinary*; D001199:Ascaridoidea / Q000502:physiology*; D001715:Bird Diseases / Q000469:parasitology*; D001717:Birds; D006790:Host-Parasite Interactions; D007559:Ivermectin / Q000008:administration & dosage / Q000494:pharmacology; D011897:Random Allocation; D012606:Scotland
chemical_list: D000969:Antinematodal Agents; D007559:Ivermectin
keywords: anisakid; endoparasite; life-history decision; parent–offspring conflict; seabird; trade-off