Bioinvasion of vector-borne filarioid nematodes in the arctic and boreal ecosystems

Authors: LAAKSONEN, SAULI - Helsinki University; OKSANEN, ANTTI - Finnish Food Safety Authority; KUTZ, SUSAN - University Of Calgary; JOKELAINEN, PIKKA - Estonian University Of Life Sciences; HOLMA-SUUTARI, ANNIINA - Wazama Media; Hoberg, Eric

Submitted to: Game Meat Hygiene in Focus
Publication Type: Book / Chapter
Publication Acceptance Date: 5/9/2016
Publication Date: 7/1/2016
Citation: Laaksonen, S., Oksanen, A., Kutz, S., Jokelainen, P., Holma-Suutari, A., Hoberg, E.P. 2016. Bioinvasion of vector-borne filarioid nematodes in the arctic and boreal ecosystems. Game Meat Hygiene in Focus. p. 101-120.

Interpretive Summary: Ecological impacts of long-term climate warming and short-term extreme events linked to temperature and precipitation/humidity directly influence the distribution of animal pathogens and patterns of disease in significant food animals on a global scale. We explore these relationships based on deep empirical data for the nematodes Setaria tundra, Onchocerca spp. and Rumenfilaria andersoni which have emerged in Fenno-Scandinavian reindeer during the latter half of the 20th century. Filarioid nematode faunas now recognized in Fennoscandia are a mosaic assembled from disparate sources, over extended but recent time frames, through anthropogenic introduction, establishment and processes of environmentally driven geographic expansion. Geographic shifts linked to climate warming and host colonization to reindeer from sources in white-tailed deer, roe deer and red deer have structured this fauna, serving as precursors and drivers of emerging disease. For example,thousands of reindeer died in 1973 during emergence of S. tundra followed by recurrent outbreaks in 1989 among moose and in 2003 -06 and 2014 among reindeer leading to condemnation of carcasses during reindeer slaughter. Concurrently, disease caused by Onchocerca spp., is increasingly common in reindeer and moose as revealed during meat inspection. In 2004-06, previously unrecognized parasites were found in the lymphatic vessels of reindeer, and were identified, for the first time in Europe, as Rumenfilaria andersoni. Genetic comparisons of North American and Finnish isolates of R. andersoni, suggest this filarioid became established in Finland recently, coincidental with introduction of white-tailed deer from North America in 1935. As R. andersoni is now found in all the four cervid species in Finland through host colonization, it can be anticipated to spread more extensively in Eurasia. Although not zoonotic through meat consumption, filarioids can cause significant morbidity, affecting the appearance, texture and quality of meat and organs, as well as impacting body condition, and in some cases, causing mortality. The consequent meat condemnation, and possible population level impacts (declines), have broader impacts on the food security for northern aboriginal people who depend on wild reindeer and caribou for food and income. Our observations are of considerable importance to veterinarians, wildlife conservation biologists, food inspection agencies and disease ecologists throughout the world and in North America where this fauna is poorly known; there is clear empirical evidence for the expanding impact of these parasites on a global stage.

Technical Abstract: The nematodes Setaria tundra, Onchocerca spp. and Rumenfilaria andersoni appear to have emerged in Fenno-Scandinavian reindeer during the latter half of the 20th century, associated with microfilaremia, peritonitis, necrotic granulomas and tarsitis. Filarioid nematode faunas now recognized in Fennoscandia are a mosaic assembled from disparate sources, over extended but recent time frames, through anthropogenic introduction, establishment and processes of environmentally driven geographic expansion. Geographic shifts linked to climate warming and host colonization to reindeer from sources in white-tailed deer, roe deer and red deer have structured this fauna, serving as precursors and drivers of emerging disease. Thousands of reindeer died in 1973 during emergence of S. tundra followed by recurrent outbreaks in 1989 among moose and in 2003 -06 and 2014 among reindeer leading to condemnation of carcasses during reindeer slaughter. Concurrently, chronic tarsitis and necrotic granulomas in liver and muscles, caused by Onchocerca spp., were increasingly common in reindeer and moose as revealed during meat inspection. In 2004-06, previously unrecognized parasites were found in the lymphatic vessels of reindeer, and were identified, for the first time in Europe, as Rumenfilaria andersoni (Splendidofilariinae). In Finnish semi-domesticated reindeer, prevalence of R. andersoni was locally up to 95 %. In moose, the observed prevalence was 10 %, in wild forest reindeer 69 %, white-tailed deer 15 % and roe deer 3 %. The impact of R. andersoni to cervid health and meat quality is unknown but visible changes were seen around lymphatic vessels. Our current data, including genetic comparisons of North American and Finnish isolates of R. andersoni, suggest this filarioid became established in Finland recently, coincidental with introduction of white-tailed deer from North America in 1935. As R. andersoni is found in all the four cervid species in Finland through host colonization, it can be anticipated to spread more extensively in Eurasia. Mosquitoes transmit S. tundra and black flies Onchocerca spp., whereas the vector of R. andersoni is unknown. Incremental and accelerating climate warming and extreme or ephemeral events of elevated temperature appear to interact to directly influence the overall limits on northern distribution and the potential for population amplification leading to disease emergence on local to regional scales for this nematode assemblage. We demonstrated that high mean summer temperatures exceeding 14 °C drive the emergence of disease outbreaks due to S. tundra, where morbidity manifests in the following summer, if conditions remain warm. This hypothesis was further supported in autumn of 2014 following 2 consecutive exceptionally warm summers, leading to the emergence of the most recent outbreaks of S. tundra and Onchocerca in Finnish reindeer. Although not zoonotic through meat consumption, Filarioids can cause significant morbidity, affecting the appearance, texture and quality of meat and organs, as well as impacting body condition, and in some cases, causing mortality. The consequent meat condemnation, and possible population level impacts (declines), have broader impacts on the food security for northern aboriginal people who depend on wild reindeer and caribou for food and income.