Diverse host-parasite interactions mediate seasonal ecosystem linkages

Nematomorph parasites manipulate terrestrial arthropods, such as crickets and ground beetles, to enter streams where the parasites reproduce. These manipulated arthropods become a substantial prey subsidy for stream salmonids, causing cross-ecosystem energy flow. Diverse nematomorph-arthropod interactions are known to underlie the energy flow. However, whether and how they can mediate the magnitude and temporal attributes of energy flow remains largely unknown. Here, we investigated whether distinct species or phylogenetic groups of nematomorphs respectively manipulate different arthropod hosts, and how the diverse nematomorph-arthropod interactions, if any, mediate seasonal prey subsidy for stream salmonids. We found that distinct phylogenetic groups of Gordionus and Gordius nematomorphs infected ground beetle and orthopteran hosts, respectively. The Gordionus nematomorphs led their ground beetle hosts to enter streams in spring, subsidizing salmonid individuals during that season. By contrast, the Gordius nematomorphs manipulated orthopterans in autumn, causing the prey subsidy for salmonid individuals during that time. Maintaining the two distinct nematomorph-arthropod interactions, thus, resulted in the parasite-mediated prey subsidy in both spring and autumn in the study streams. Manipulative parasites are common, and they often associate with a range of host lineages, suggesting that similar effects of diverse host-parasite interactions on energy flow might be widespread in nature.

Methods
Fish sampling was conducted in Koitoi stream, Uenai stream and Yuuburi stream, which are located in the mid-southern region of Hokkaido, Japan. Stomach contents were classified as nematomorphs, presumed hosts of nematomorphs (ground beetles and orthopterans) and non-host invertebrates (including both aquatic and terrestrial invertebrates) and vertebrates (i.e., fish). Each category was weighted in nearest 1 mg in wet mass.