Understanding the role of arthropod vectors in the emergence and spread of plant, animal and human diseases. A chronicle of epidemics foretold in South of France Didier Fontenille, Astrid Cruaud, Laurence Vial, Claire Garros To cite this version: Didier Fontenille, Astrid Cruaud, Laurence Vial, Claire Garros. Understanding the role of arthropod vectors in the emergence and spread of plant, animal and human diseases. A chronicle of epidemics foretold in South of France. Comptes Rendus Biologies, Elsevier Masson, 2020, 343 (3), pp.311-344. 10.5802/crbiol.34. hal-03137373 HAL Id: hal-03137373 https://hal.archives-ouvertes.fr/hal-03137373 Submitted on 10 Feb 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Comptes Rendus Biologies Fontenille Didier, Cruaud Astrid, Vial Laurence and Garros Claire Understanding the role of arthropod vectors in the emergence and spread of plant, animal and human diseases. A chronicle of epidemics foretold in South of France Volume 343, issue 3 (2020), p. 311-344. <https://doi.org/10.5802/crbiol.34> © Académie des sciences, Paris and the authors, 2020. Some rights reserved. This article is licensed under the Creative Commons Attribution 4.0 International License. http://creativecommons.org/licenses/by/4.0/ Les Comptes Rendus. Biologies sont membres du Centre Mersenne pour l’édition scientifique ouverte www.centre-mersenne.org Comptes Rendus Biologies 2020, 343, nO 3, p. 311-344 https://doi.org/10.5802/crbiol.34 Articles / Reviews / Articles / Revues Understanding the role of arthropod vectors in the emergence and spread of plant, animal and human diseases. A chronicle of epidemics foretold in South of France Comprendre le rôle des arthropodes vecteurs dans l’émergence et la propagation des maladies infectieuses végétales, animales et humaines. Chronique d’épidémies annoncées dans le sud de la France , a b c, d c, d Fontenille Didier¤ , Cruaud Astrid , Vial Laurence and Garros Claire a MIVEGEC unit, Université de Montpellier, Institut de Recherche pour le Développement (IRD), CNRS, BP 64501, 34394 Montpellier, France b CBGP,INRAE, CIRAD, IRD, Montpellier SupAgro, Université de Montpellier, Montpellier, France c ASTRE unit, Université de Montpellier, CIRAD, INRAE, Montpellier, France d Cirad, UMR ASTRE, 34398 Montpellier, France E-mails: [email protected] (F.Didier), [email protected] (C. Astrid), [email protected] (V. Laurence), [email protected] (G. Claire) Abstract. Southern France, like the rest of the world, is facing the emergence of diseases aVecting plants, animals and humans, of which causative agents (viruses, parasites, bacteria) are transmitted by arthropod vectors. Global changes are accelerating the emergence and spread of these diseases. After presenting some examples related to vectors of yellow fever and dengue viruses (Aedes aegypti and Ae. albopictus), Crimean-Congo hemorrhagic fever (Hyalomma marginatum), Bluetongue (Culicoides sp.), and the phytopathogen Xylella fastidiosa (Hemiptera spp.), we will discuss what are the intrinsic and extrinsic factors that make an arthropod a vector in a given place and at a given time. We also propose some thoughts regarding these emergences, possible scenarios for their evolution and some recommendations for the future. ¤ Corresponding author. ISSN (electronic) : 1768-3238 https://comptes-rendus.academie-sciences.fr/biologies/ 312 Fontenille Didier et al. Résumé. Le sud de la France, comme le reste du monde, est confronté à l’émergence de maladies aVectant les plantes, les animaux et les populations humaines, dont les agents étiologiques (virus, parasites, bactéries) sont transmis par des arthropodes vecteurs. Les changements globaux auxquels nous faisons face accélèrent l’apparition et la diVusion de ces pathologies. Après avoir pris quelques exemples concernant les vecteurs des virus de la fièvre jaune et de la dengue (Aedes aegypti et Ae. albopictus), de la fièvre de Crimée-Congo (Hyalomma marginatum), de la fièvre catarrhale ovine (Culicoides sp.) et de la bactérie phytopathogène Xylella fastidiosa (Hemiptera spp.), nous verrons quels sont les facteurs intrinsèques et extrinsèques qui font qu’un arthropode devient un vecteur en un lieu et à un moment donné. Nous proposons des pistes de réflexion sur ces émergences et le possible devenir des maladies transmises par arthropodes. Nous concluons par quelques recommandations pour mieux anticiper les émergences. Keywords. Vector, Mosquito, Tick, Midges, Xylella, Emergence, Risk. Mots-clés. Vecteur, Moustique, Tique, Moucherons, Xylella, Émergence, Risque. Manuscript received and accepted 8th December 2020. Are the tiger mosquito (Aedes albopictus), the gi- 17% of infectious diseases and are responsible for ant tick (Hyalomma marginatum), the biting midge more than 700,000 deaths per year worldwide. Eco- Culicoides imicola and the meadow spittlebug (Phi- nomic costs of human VBDs (surveillance, medical laenus spumarius), all still unknown in Southern and non-medical costs, vector control, productivity France a few years or decades ago, our new plagues losses) account for billions of euros annually. of Egypt? Moreover, the economic consequences of some These four species of arthropods are related of these vector-borne diseases on agriculture and to vector-borne diseases (VBDs). The superlatives livestock production are colossal. They have key sometimes associated with these new scourges con- direct macro-economic impacts: morbidity of live- cerning the health of humans, animals and plants, stock, economic losses such as reduced produc- reflect the concerns they generate in the general tion and farm income, ban on livestock and se- population, among livestock breeders, farmers and men trade, imposed quarantine, costs of biological among decision-makers. tests, surveillance and control measures. For exam- Enemies needing surveillance or a fight, against ple, in Germany and in the Netherlands [1,2], the which we seem to be quite helpless, these vectors impact of Bluetongue on cattle was estimated up- used as examples give us the opportunity to ask the wards of hundreds of million Euros. In the field of following questions: how did we get there? What has plant health, Citrus greening (Huanglongbing dis- led these arthropods and pathogens to become a ease, HLB) caused by Candidatus Liberibacter spp. threat? transmitted by psyllids, is the most destructive citrus Beyond the stereotypes on very real phenomena pathosystem worldwide with an estimated cost for with serious consequences such as climate change, Florida of $8.92 billion in revenue and $4.62 billion in environmental modifications, changes in agricul- gross domestic product between the 2006/2007 and tural practices, urbanization, intensification of world 2010/2011 crop productions [3]. Sharka, caused by trade, it is often the conjunction of a set of events, Plum pox virus transmitted by Aphididae, is the most most of the time with a low probability of occurrence, devastating disease of stone fruit trees. It generates which leads to the emergence of the transmission of annual losses accounting for hundreds of millions of a pathogen by a vector: insect, mite, mollusc, nema- euros [4]. tode (see definition below). In other words, the worst In addition, there are also indirect socio-economic is never sure, but it is the worst that holds our atten- impacts that concern any VBDs aVecting plants ani- tion as humans, when we are directly concerned. mals or humans: inability of breeders, farmers, work- For humans only, the World Health Organization ers to achieve daily demands, disruption of mar- (WHO) estimates that vector-borne diseases (such as ket chains, and concerns of consumers and citi- malaria, dengue, Chagas disease, leishmaniosis, hu- zens regarding health threats and environmental is- man African trypanosomiasis) account for more than sues (concerns of contracting disease, change in C. R. Biologies, 2020, 343, nO 3, 311-344 Fontenille Didier et al. 313 consumption habits, public authorities questioned tive of many French Regions, of the European Union on use of insecticides, vaccines, massive culling, with the Green deal, and of the United Nations in a environmental and sanitary side eVects), costs of “One Health” strategy integrating sustainable devel- surveillance and tests for the (early) detection of the opment goals. disease to avoid large outbreaks etc. However, years of research and development ef- Risk assessment, prevention and control of these forts have not been able to entirely solve the prob- emerging diseases or their invasive vectors are major lems and there is a perpetual arms race between health, ecological, social and economic challenges. humans, vectors and pathogens. New tools are being The most problematic recent examples in metro- developed (not all of them are consensual), or are politan France concern dengue fever, Zika disease, yet to be invented: diagnostics, treatments, green chikungunya, West Nile fever, arboviruses transmit- chemistry,