Abstract

Changing environmental conditions and human encroachment on natural habitats bring human populations closer to novel sources of parasites, which might then develop into new emerging diseases. Diseases transmitted by host generalist vectors are of special interest due to their capacity to move pathogens into novel hosts. We hypothesize that humans using forests for recreation are exposed to a broad range of parasites from wild animals and their vectors. A corollary of this is that new vector-host, parasite-host, and vector-parasite associations could eventually develop. Thus, we expect to observe atypical vector-host associations. Using molecular bloodmeal analysis via amplification of the mtDNA COI gene we identified the vertebrate hosts of Culicoides (Diptera: Ceratopogonidae) species in a sub-urban forest of Southwestern Germany. Bloodmeals were also checked for haemosporidian infections by amplifying a fragment of the mtDNA cyt b gene. We identified a total of 20 Culicoides species, thirteen of which fed on humans. From 105 screened bloodmeals we obtained high quality sequences for 77 samples, 73 (94.8%) originated from humans, two from livestock (Bos taurus and Equus caballus), and two from wild birds (Sylvia atricapilla and Turdus merula). We found that four Culicoides species previously assumed to feed exclusively on either birds (C. kibunensis) or domestic mammals (C. chiopterus, C. deltus, C. scoticus) fed also on humans. A total of six Culicoides abdomens were infected with avian haemosporidian parasites (Plasmodium or Haemoproteus), four of those abdomens contained blood derived from humans. Our results suggest that parasites of wild animals may be transferred to humans through infectious bites of Culicoides vectors. Further, we show that Culicoides vectors believed to be a specialist on specific vertebrate groups can have plastic feeding preferences, and that Culicoides are susceptible to infection by Plasmodium parasites, though vector viability must still be experimentally demonstrated.

Highlights

  • Haemosporidian parasites are responsible for millions of infections and thousands of deaths in humans, as well as domestic and wild animals each year [1,2]; this is a pattern that is becoming more relevant on the face of environmental changes because warming climate is helping the geographic expansion of both parasites and vectors into regions where they were previously absent [3]

  • Culicoides vectors have broad host feeding preferences, even for those species that have been assumed to feed exclusively on birds or mammals, which opens the possibility for transferring parasites across distantly related vertebrate hosts, including humans

  • It has been suggested that some vectors from different Diptera families have restricted host feeding preferences, but we suggest that specificity is less than previously assumed and may partly reflect a biased research agenda towards a limited set of vectors and hosts (e.g., [1,2]), and that many vectors around the world probably will have to adapt to new hosts in the light of rapid environmental changes because depending on their ecology they will experience a geographical range expansion or contraction

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Summary

Introduction

Haemosporidian parasites are responsible for millions of infections and thousands of deaths in humans, as well as domestic and wild animals each year [1,2]; this is a pattern that is becoming more relevant on the face of environmental changes because warming climate is helping the geographic expansion of both parasites and vectors into regions where they were previously absent [3]. Despite its relevance for human and animal health, knowledge on the insect vectors feeding on different vertebrate species and transmitting haemosporidians is poor [1]. If vectors sucking blood from humans feed on other vertebrates (e.g., [4,5,6]), humans will be exposed to a wide range of parasites existing in the animal community surrounding them (e.g., [7]). It is important to know what blood parasites make it into the blood stream of humans, even if initially they do not develop into an infection, because this is the first step towards new emerging diseases (e.g., West Nile Virus [12],). Our current knowledge on what vectors are feeding on humans is insufficient, and we cannot assess which parasites and their associated diseases represent a possible threat to human health

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