Nosema Ceranae in Europe: an Emergent Type C Nosemosis Mariano Hges, Raquel Martín-Hernández, Aranzazu Meana
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Nosema ceranae in Europe: an emergent type C nosemosis Mariano Hges, Raquel Martín-Hernández, Aranzazu Meana To cite this version: Mariano Hges, Raquel Martín-Hernández, Aranzazu Meana. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, Springer Verlag, 2010, 41 (3), 10.1051/apido/2010019. hal-00892102 HAL Id: hal-00892102 https://hal.archives-ouvertes.fr/hal-00892102 Submitted on 1 Jan 2010 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. Apidologie 41 (2010) 375–392 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2010 www.apidologie.org DOI: 10.1051/apido/2010019 Review article Nosema ceranae in Europe: an emergent type C nosemosis* Mariano Higes1, Raquel Mart´in-Hernandez´ 1, Aranzazu Meana2 1 Laboratorio de Patología Apícola, Centro Apícola Regional, JCCM, 19180 Marchamalo, Spain 2 Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain Received 11 December 2009 – Revised 2 February 2010 – Accepted 12 February 2010 Abstract – In this review, relevant data is presented on an emerging disease of the 21th century in European countries, caused by Nosema ceranae. Within a few years after it was detected in Spain in 2005, the rest of European countries that had technical capacity to differentiate Nosema apis from N. ceranae reported its presence. In a similar way as the initial detection of Varroa in Europe, active scientific work is raising many questions due to the absence of clinical symptoms in infected colonies and a long incubation period of the pathogen. N. ceranae presents a different epidemiological pattern and pathology compared to N. apis. The disease caused by N. ceranae is now named nosemosis type C (COLOSS workshop, 2009) and is characterized by the ability to detect the disease-causing agent throughout the year. The continuous death of highly infected bees, mostly foragers, has a clear effect on colony population and productivity. Although there has been a huge effort in the last years to increase knowledge about this disease, significant research is still needed on epidemiology, pathology, prophyllaxis and treatment. Nosema ceranae / Nosema apis / Apis mellifera / nosemosis / Europe 1. INTRODUCTION the etiological agent was discovered. The bright oval corpuscles found in the digestive The detection of Nosema ceranae (Mi- tract indicated the fungal origin of the dis- crosporidia: Nosematidae) in Apis mellifera ease (Donhov, 1857; Higgins, 1858; data from Linnaeus was reported in 2005 in both Eu- Neveu-Lemaire, 1938). In Germany, the cor- rope and Asia (Higes et al., 2005, 2006; puscles were finally attributed as the cause Huang et al., 2007). Originally described in of the disease, and were classified as N. apis Apis cerana (Fries et al., 1996), the spread by Zander in 1909. There have been several of N. cerana from A. cerana to A. mellif- studies concerning the biology and epidemi- era probably occurred within the last decade ology of nosemosis (see particularly Fantham (Klee et al., 2007), although this must still and Porter, 1912; Maassen, 1912, 1914; and be confirmed (Fries, 2009). To date, two mi- Trappmann, 1920: data from Neveu-Lemaire, crosporidian species infect honey bees world- 1938), and there is a huge body of work related wide: Nosema apis Zander and N. ceranae. to nosemosis due to N. apis, although it was N. apis was shown to infect A. mellifera more detected molecularly only recently (Webster than one hundred years ago and was one of et al., 2004). the first microsporidia to be described. In- In contrast, studies on N. ceranae were deed, the disease caused by this microsporidia limited to the discovery of the parasite in in honey bees was even recognized before A. cerana (Fries et al., 1996). Until 2005, it was assumed that when microsporidian spores Corresponding author: Mariano Higes, were present in honey bees they were always [email protected] N. apis. However, in 2005, a sequence was ob- * Manuscript editor: Yves Le Conte tained from a microsporidian isolate in a study Article published by EDP Sciences 376 M. Higes et al. of diseased A. mellifera workers thought to be aim is to summarize the findings of all the infected by N. apis (Huang et al., 2007). In the studies on N. ceranae, highlighting the pathol- same year but in a different continent, N. cer- ogy caused in honey bees and the epidemio- anae was isolated in European worker honey logical factors related to this emergent disease bees while trying to standardize the molecu- in Europe. lar detection of N. apis from samples collected from colonies suffering unexpected population loss and/or lower honey production (Martín- 2. COLONIZATION AND SPREAD Hernández et al., 2005; Higes et al., 2006). OF NOSEMA CERANAE IN Traditionally, the term “nosemosis” is con- EUROPE sidered to be the infection of ventricular cells of adult honey bees by N. apis, the etiological In the last few years, infection of honey agent (OIE, 2004). This disease was charac- bees (A. mellifera)byN. ceranae has been re- terized, in acute forms, by trembling of honey ported in a number of European countries, in- bee workers, bees with a dilated abdomens, cluding Spain, France, Germany, Switzerland, brown faecal marks on combs and the front of Denmark, Finland, Greece, Hungary, Holland, the hives, sick or dead bees in the vicinity of United Kingdom, Italy, Serbia, Poland, Slove- the hives, and a decrease in brood production nia, Bosnia I Herzegovina and Sweden (Higes and in the size of bee colony particularly in et al., 2006; Fries et al., 2006; Martín- spring (Bailey, 1955; Cornejo and Rosi, 1975; Hernández et al., 2007; Klee et al., 2007; Faucon, 2005; OIE, 2008). Chauzat et al., 2007; Topolska and Kasprzak, However the emergent disease caused by 2007; Paxton et al., 2007; Tapaszti et al., 2009; N. ceranae, now known to be present in all Kryeger, 2009; Santrac, 2009), as well as in five continents (Martín-Hernández et al., 2007; other continents (Huang et al., 2007; Cox- Klee et al., 2007; Giersch et al., 2009;Higes Foster et al., 2007; Giersch et al., 2009;Higes et al., 2009a), presents a different epidemio- et al., 2009a). The exact date of the arrival of logical pattern, symptomology and pathology. N. ceranae into Europe has not been deter- Indeed, it is now considered a major health mined. The concurrent detection of the para- problem in both individual honey bees (Paxton site in Europe and Asia may not have been re- et al., 2007; Martín-Hernández et al., 2009a; lated to its jump to A. mellifera but rather to Antúnez et al., 2009) and in whole colonies the development of new highly sensitive and (Higes et al., 2008a, 2009b). Prior to the iden- specific molecular tools. N. apis and N. cer- tification of N. ceranae in honey bees, a “dry anae spores are not easily distinguished from nosemosis” was observed with different symp- each other so molecular tools to identify each toms from the acute form described for N. apis species have played a decisive role in studies (Faucon, 2005). The different symptoms pre- on them (Weiss and Vossbrinck, 1999,inKlee sented by these Nosema species in honey bees et al., 2007). highlights the need to consider two differ- The colonization of A. mellifera by N. cer- ent clinical patterns: nosemosis type A caused anae first implied that the parasite reached by N. apis and nosemosis type C caused by new geographical areas. Retrospective analy- N. ceranae as agreed in a recent International sis of data and samples suggest that N. cer- Meeting (COLOSS, 2009). anae has been in Europe for the past decade Most studies on N. ceranae in Europe (Higes et al., 2006; Martín-Hernández et al., have been reported at meetings of a European 2007; Klee et al., 2007;Paxtonetal.,2007). working group, EU COST Action (FA0803) This is not surprising since the dynamics of that initially met in Wageningen in March population growth in a new habitat usually fol- 2007. This group, now known as COLOSS low a characteristically sigmoid curve (Bush (Prevention of Honey Bee Colony Losses; et al., 2001). Currently, the near-exponential www.coloss.org, organized by Dr. Neumann) increase in population size of N. ceranae is as- currently has more than 150 members from sociated with a high prevalence due to the sta- 40 countries, including non-EU countries Our ble population growth in almost all countries Nosema ceranae in Europe 377 where A. mellifera is reared. A similar situa- ies concerning honey bee-Nosema interac- tion was described for the mite Varroa destruc- tions, the identification of new epidemiologi- tor (formerly Varroa jacobsoni: Anderson and cal markers and new targets for therapeutics. Trueman, 2000), that spread around the world According to the epidemiological charac- after its first detection in Asian honey bees in teristics of N. ceranae, infection by this mi- 1904. Although the historical samples are still crosporidian presents a different pattern to limited, the data obtained clearly indicate that that described for N. apis in temperate areas N. ceranae is an exotic pathogen of A. mellif- of Europe. Specifically, colonies affected by era in Europe. N. apis generally display low levels of infec- Understanding the origins and spread of tion during summer, a small peak in autumn N.