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Prevalence of Nosema Species in a Feral Honey Bee Population: a 20-Year Survey Juliana Rangel, Kristen Baum, William L

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Prevalence of Nosema Species in a Feral Honey Bee Population: a 20-Year Survey Juliana Rangel, Kristen Baum, William L Prevalence of Nosema species in a feral honey bee population: a 20-year survey Juliana Rangel, Kristen Baum, William L. Rubink, Robert N. Coulson, J. Spencer Johnston, Brenna E. Traver To cite this version: Juliana Rangel, Kristen Baum, William L. Rubink, Robert N. Coulson, J. Spencer Johnston, et al.. Prevalence of Nosema species in a feral honey bee population: a 20-year survey. Apidologie, Springer Verlag, 2016, 47 (4), pp.561-571. 10.1007/s13592-015-0401-y. hal-01532328 HAL Id: hal-01532328 https://hal.archives-ouvertes.fr/hal-01532328 Submitted on 2 Jun 2017 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 (2016) 47:561–571 Original article * INRA, DIB and Springer-Verlag France, 2015 DOI: 10.1007/s13592-015-0401-y Prevalence of Nosema species in a feral honey bee population: a 20-year survey 1 2 3 4 Juliana RANGEL , Kristen BAUM , William L. RUBINK , Robert N. COULSON , 1 5 J. Spencer JOHNSTON , Brenna E. TRAVER 1Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX 77843-2475, USA 2Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078, USA 3P.O. Box 2686, Edinburg, TX 78540, USA 4Knowledge Engineering Laboratory, Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA 5Department of Biology, Penn State Schuylkill, 200 University Drive, Schuylkill Haven, PA 17972, USA Received 26 January 2015 – Revised 14 July 2015 – Accepted 20 October 2015 Abstract – Nosema spp. are microsporidian pathogens of honey bees that cause nosemosis, a disease implicated in colony losses worldwide. Few studies have measured Nosema spp. levels in feral honey bees. We evaluated the presence and infection intensity of Nosema apis and Nosema ceranae in a feral Africanized honey bee population in south Texas from 1991 to 2001 and in 2013. Overall, less than 6 % of samples had Nosema spp. spores. N. apis was only found in samples from 1991 to 1995. Conversely, N. ceranae was found every year examined, ranging from 16.7 % infection in 1991 to 85.7 % in 2013. There were no effects of temperature or rainfall on infection with either species over time. This suggests that feral honey bees are relatively free of Nosema spp. compared to managed colonies. More studies on the incidence of Nosema spp. in feral honey bee populations are needed. Apis mellifera / Africanized feral honey bees / Nosema apis / Nosema ceranae /qPCR 1. INTRODUCTION Vegetative stages reproduce within the cells to form spores that are released upon lysis of the Nosemosis, a disease of honey bees that infects cell, which then are freed to infect other midgut epithelial cells of the midgut (Bailey 1981; epithelial cells (Bailey and Ball 1991). Two spe- Matheson 1993), can be caused by the presence cies of Nosema can infect the honey bee Apis of microsporidia species in the genus Nosema mellifera : Nosema apis and Nosema ceranae . (Nosematidae). Nosemosis is transmitted horizon- N. apis affects the western European honey tally between adults through the oral–fecal route, bee (Apis mellifera L.) and is found worldwide where uninfected adults become infected by con- (Matheson 1996). N. ceranae was first discovered tact with food or feces contaminated with Nosema in the Asian honey bee Apis cerana in 1996 (Fries spp. spores (Fries 1993, 1996). Following inges- 1996), was later identified in managed Apis tion, spores germinate within the midgut by mellifera colonies in Spain and Taiwan (Higes ejecting a polar filament that injects the Nosema et al. 2006; Huang et al. 2007), and is now wide- spp. sporoplasm into epithelial cells of the midgut. spread in Europe (Higes et al. 2006, 2009a; Chauzat 2007; Huang et al. 2007, 2008; Klee et al. 2007; Paxton et al. 2007; Topolska and S. Corresponding author: J. Rangel, Kasprzak 2007), North America (Chen et al. [email protected] 2008;Williamsetal.2008;TraverandFell Manuscript editor: Yves Le Conte 2011a, b), Central America (Calderón 2008; 562 J. Rangel et al. Rangel et al. 2013), South America (Invernizzi honey bees (Fries 2003). Feral and managed hon- et al. 2009; Medici et al. 2012; Mendoza et al. ey bee colonies in Central and South America, as 2014), Africa (Fries 2003; Higes et al. 2009b), and well as some regions in the southern United States Australia (Giersch et al. 2009). While honey bee are considered “Africanized,” or hybrids formed colonies infected with N. apis exhibit fecal streak- from a mixture of genes derived from European ing on the hives and comb due to severe dysentery and African ancestors (Taylor 1988;Taylorand (Hassanein 1951;Fries1993), those infected with Spivak 1984;Rubinketal.1996;Pinto2004). N. ceranae do not show obvious external symp- Interestingly, infection of workers by Nosema in toms. Despite the key symptomatic differences Latin America is observed mostly in Africanized caused by different Nosema species, infection honey bees. However, that observation may reflect with one or both species causes significant de- incomplete sampling, as most studies of nosemosis clines in a colony’s overall worker population in Africanized honey bees in that region have been (Wang and Mofller 1970; Higes et al. 2008)and done in managed colonies (Calderón 2008; honey production (Hassanein 1951; Fries et al. Invernizzi et al. 2009;Rangeletal.2013; 1984; Rinderer and Sylvester 1978; Anderson Mendoza et al. 2014). and Giacon 1992;Maloneetal.1995). There have only been three studies reporting The decrease in the worker population (colony Nosema levels in unmanaged honey bees living as size) is mainly caused by worker mortality associated feral colonies in diverse habitats, and those three with digestive disorders and shortened lifespan studies only reported N. apis infection. Manning (Hassanein 1951). Antúnez et al. (2009)showed et al. (2007) reported high levels of N. apis infection evidence that N. ceranae infections result in immu- in feral honey bee colonies around southwestern nosuppression in workers, hypothesizing that Australia from 2002 to 2003. While all the colonies N. ceranae infection can make a colony more sus- surveyed were infected with N. apis , the presence ceptible to other pathogens, particularly viruses and severity of infection were significantly affected (Bailey et al. 1983;Dainatetal.2012). Several studies by the location of the colony and the weather during have also reported detrimental synergistic interactions sample collection. In the USA, only two studies between N. ceranae and other stressors such as have reported the prevalence of Nosema spp. in pesticides, on honey bee health (Alaux et al. 2010; feral Africanized honey bees. Gilliam and Taber Vidau et al. 2011;Wuetal.2012; Higes et al. 2013). (1991) first reported the presence of N. apis in feral Colonies may be infected by one or both strains honey bees from Arizona, where they found a very of Nosema . A recent study found direct evidence low level of infection, with 9 of 21 individuals suggesting that N. ceranae and N. apis undergo sampled being infected with only one to five severe interspecific competition inside the gut of N. apis spores per infected bee. More recently, honey bees and that when co-infecting bees with Szalanski (2014) explored the prevalence of both microsporidia, N. ceranae infection exhibit- Nosema spp. in feral Africanized honey bees in ed stronger inhibition of N. apis than vice versa Arkansas, New Mexico, Mississippi, New (Natsopoulou et al. 2014). Because the spores of Mexico, Oklahoma, Texas, and Utah. Using PCR- both species look very similar using traditional restriction fragment length polymorphism (PCR- miscroscopy, the cause of nosemosis, whether by RFLP), the authors found that only 8.3 % of the N. apis or N. ceranae , or both, is most reliably samples analyzed tested positive for N. apis , with distinguished using polymerase chain reaction infections being more common in Texas than in any (PCR) (Martin-Hernandez et al. 2007; Roudel other state surveyed. et al. 2013) and quantitative polymerase chain All of the aforementioned surveys were reaction (qPCR) techniques (Higes et al. 2006; done only for N. apis and were conducted on Klee et al. 2007; Paxton et al. 2007; Traver and samples collected in a single year. Therefore, Fell 2011a, b;Rangeletal.2013). data are lacking on the presence of N. apis and N. apis will infect the African honey bee, Apis N. ceranae in feral honey bee populations in mellifera scutellata , causing diagnostic symptoms the USA over time. In this study, we surveyed that are similar to those found in infected European the same population of feral honey bees in Prevalence of Nosema in feral honey bees 563 south Texas from 1991 to 2001 and again in 2.2. Genomic DNA extraction 2013 and used molecular techniques to deter- and quantitative real-time PCR mine the presence and levels of infection in these colonies by N. apis , N. ceranae , or both, Genomic DNA was extracted from individual abdo- over the last two decades. mens of ten workers from each cavity sampled per year as described previously (Traver et al. 2009; Traver and Fell 2011a). Briefly, a Bender buffer lysis followed by a 2. METHODS proteinase K digestion and phenol/chloroform extrac- tion was performed. After the first separation step, the 2.1. Study site and sample collection organic layer was saved for spore analysis. DNA was precipitated with isopropanol and resuspended over- The feral honey bees sampled for this study were night in DEPC-treated water kept at room temperature.
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