title: An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds.
abstract: Overlapping distributions of hosts and parasites are critical for successful completion of multi-host parasite life cycles and even small environmental changes can impact on the parasite's presence in a host or habitat. The generalist Cardiocephaloides longicollis was used as a model for multi-host trematode life cycles in marine habitats. This parasite was studied to quantify parasite dispersion and transmission dynamics, effects of biological changes and anthropogenic impacts on life cycle completion. We compiled the largest host dataset to date, by analysing 3351 molluscs (24 species), 2108 fish (25 species) and 154 birds (17 species) and analysed the resultant data based on a number of statistical models. We uncovered extremely low host specificity at the second intermediate host level and a preference of the free-swimming larvae for predominantly demersal but also benthic fish. The accumulation of encysted larvae in the brain with increasing fish size demonstrates that parasite numbers level off in fish larger than 140mm, consistent with parasite-induced mortality at these levels. The highest infection rates were detected in host species and sizes representing the largest fraction of Mediterranean fishery discards (up to 67% of the total catch), which are frequently consumed by seabirds. Significantly higher parasite densities were found in areas with extensive fishing activity than in those with medium and low activity, and in fish from shallow lagoons than in fish from other coastal areas. For the first time, C. longicollis was also detected in farmed fish in netpens. Fishing generally drives declines in parasite abundance, however, our study suggests an enhanced transmission of generalist parasites such as C. longicollis, an effect that is further amplified by the parasite's efficient host-finding mechanisms and its alteration of fish host behaviour by larvae encysted in the brain. The anthropogenic impact on the distribution of trophically-transmitted, highly prevalent parasites likely results in a strong effect on food web structure, thus making C. longicollis an ideal bioindicator to compare food webs in natural communities versus those impacted by fisheries and aquaculture.
authors: Cavanilles Institute for Biodiversity and Evolutionary Biology, Science Park, University of Valencia, P.O. Box 22 085, 46071 Valencia, Spain. Electronic address: A.Isabel.Born@uv.es.
authors: Ana
authors: A
authors: Born-Torrijos
authors: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand.
authors: Robert
authors: R
authors: Poulin
authors: Cavanilles Institute for Biodiversity and Evolutionary Biology, Science Park, University of Valencia, P.O. Box 22 085, 46071 Valencia, Spain.
authors: Ana
authors: A
authors: Pérez-Del-Olmo
authors: Department of Life and Environmental Sciences, University of Cagliari, Via T. Fiorelli, 1, 09126 Cagliari, Italy.
authors: Jacopo
authors: J
authors: Culurgioni
authors: Cavanilles Institute for Biodiversity and Evolutionary Biology, Science Park, University of Valencia, P.O. Box 22 085, 46071 Valencia, Spain.
authors: Juan Antonio
authors: JA
authors: Raga
authors: Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic.
authors: Astrid Sibylle
authors: AS
authors: Holzer
mesh_terms: D000818:Animals; D001715:Bird Diseases / Q000469:parasitology* / Q000635:transmission; D001717:Birds; D059038:Black Sea; D049628:Body Size; D004275:DNA, Ribosomal / Q000737:chemistry; D017753:Ecosystem; D005393:Fish Diseases / Q000469:parasitology* / Q000635:transmission; D005398:Fisheries; D005399:Fishes / Q000033:anatomy & histology / Q000145:classification; D020387:Food Chain; D058507:Host Specificity; D006802:Human Activities; D008018:Life Cycle Stages; D008522:Mediterranean Sea; D008974:Mollusca / Q000145:classification / Q000469:parasitology; D012339:RNA, Ribosomal, 28S / Q000235:genetics; D017422:Sequence Analysis, DNA / Q000662:veterinary; D012908:Snails / Q000469:parasitology; D014200:Trematoda / Q000145:classification / Q000235:genetics / Q000254:growth & development*; D014201:Trematode Infections / Q000469:parasitology / Q000635:transmission / Q000662:veterinary*
chemical_list: D004275:DNA, Ribosomal; D012339:RNA, Ribosomal, 28S
keywords: Cardiocephaloides longicollis; Fishery discards; Host specificity; Human-induced impact; Mediterranean; Trematodes