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Apicystis Gen Nov and Apicystis Bombi Neogregarinida), a Cosmopolitan

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Apicystis Gen Nov and Apicystis Bombi Neogregarinida), a Cosmopolitan Original article Apicystis gen nov and Apicystis bombi (Liu, Macfarlane & Pengelly) comb nov (Protozoa: Neogregarinida), a cosmopolitan parasite of Bombus and Apis (Hymenoptera: Apidae) JJ Lipa O Triggiani 1 Institute of Plant Protection, Miczurina 20, 60-318 Poznan, Poland; 2 Istituto di Entomologia Agraria, Universita degli Studi, via Amendola 165/A, 70125 Bari, Italy (Received 20 May 1995; accepted 22 December 1995) Summary — A new genus Apicystis and a new combination Apicystis bombi (Liu, Macfarlane & Pen- gelly) is proposed for a neogregarine parasitic on Bombus spp and Apis mellifera. The genus Apicys- tis is characterized by having navicular oocysts containing only four sporozoites and basically differs from the genus Mattesia which has spindle oocysts with eight sporozoites. This parasite was recorded in ten species of Bombus in Europe and North America, but has been observed only once in Apis mel- lifera in Finland. Apicystis / Apis / Bombus / new genus / protozoan / parasite INTRODUCTION the paper by Liu et al (1974) in which these authors described Mattesia bombi Liu, Mac- farlane & Pengelly from Bombus spp in Based on research undertaken in Italy, Canada. Further studies et al 1988 and in Finland, 1990 we published a (Macfarlane short note (Lipa and Triggiani, 1992) in 1995, 1996) strongly support our original that the involved does which we reported finding a neogregarine opinion neogregarine not to the but parasite on Bombus hortorum, B terrestris belong genus Mattesia, rep- resents a new which we describe in and Apis mellifera. After describing the mor- genus this phological characteristics of the neogre- paper. garine, at the end of our note we stated ’All these features indicate that this neogre- MATERIAL AND METHODS garine constitutes both a new species and a new genus. It also represents the first record of neogregarine infection in the Api- As previously reported (Lipa and Triggiani, 1992) dae’. At that time we were not familiar with infected queens and workers of Bombus spp were collected in Italy in open-air in 1988, and various bumble bee species (Bombus spp), one infected worker of Apis mellifera was col- Schmid-Hempel (unpublished data) esti- lected in hive in Finland in 1990. In of 1995 July mated the neogregarine infection at a level additional infected males and of B ter- queens of 4-7% in Switzerland. restris were collected at the University Campus in Bari, Italy, and from fields at Valenzano, 15 Neogregarine oocysts were observed in km from Bari. Collected insects were dissected queens and workers of B hortorum and B and their fat body tissue and gut were examined terrestris collected by sweep net in Southern under a light microscope. Morphology and life Italy (Apuglia) (Lipa and Triggiani, 1992). cycle of the pathogen were studied on smeared The of identical was fat body tissue preparations fixed for 2 min in presence oocysts methanol and stained in 0.25% Giemsa for noticed in one A mellifera worker out of 34 8-12 h. collected in July 1990 from one hive of the of the In spite of our efforts we were not able to experimental apiary Agricultural locate and access any oocyst material, stained Research Center, Jokioinen, Finland. Micro- microscope slides or photos concerning Matte- scopic examination of additional individu- sia bombi occurring in Bombus spp in Canada als of Bombus spp in Italy (Triggiani, 1991), on which the original description was based. New Zealand and Japan (Macfarlane et al, to information obtained from RP Mac- According Denmark and Finland farlane (Christchurch, New Zealand) and P Kevan 1995), (Lipa, unpub- lished failed to reveal (Guelph, Canada), all documentation material data) neogregarine concerning M bombi, deposited at the University infection. of Guelph, was discarded when the authors left or In July 1995 the neogregarine infection retired. After to several bum- making enquiries was detected in B terrestris collected ble bee researchers for information and infected again in Bari out of three one insect material, P Schmid-Hempel (Institute of Italy: (5th): males, Microbiology, ETH Zurich, Switzerland) informed was one infected with neogregarine and one us about observations of neogregarine infection was infected with both neogregarine and in Bombus spp in Switzerland and provided pho- Nosema bombi; Bari (10th): out of two tographs of its oocysts. males, one was infected with neogregarine and Crithidia bombi; Bari (14th) one male and one queen were infected with neogre- RESULTS AND DISCUSSION garine; Valenzano (18th), out of three work- ers, two queens and ten males examined one queen and one male were infected with Geographic distribution, neogregarine. hosts and infection level The above data indicate that neogre- garine infection is common, but its level is The neogregarine concerned was first low in Bombus spp and sporadic in A mel- reported as Mattesia bombi (Liu et al, 1974; lifera. This is not surprising as infections Macfarlane et al, 1995, 1996) in the Ontario of Bombus spp and A mellifera by eugre- province of Canada in the queens and some garines and flagellates reach very low lev- males of various Bombus spp. Of the 3 045 els and have been reported from very few overwintered queens examined, 5.3% were localities (Lipa and Triggiani, 1988; Mac- parasitized: Bombus vagans being the most farlane et al, 1995). However, since the heavily infected, with 8.2% of its queens parasitic neogregarine was found in parasitized (Liu et al, 1974; Macfarlane et Canada, Finland, France, Italy and Switzer- al, 1995). Recently Macfarlane et al (1996) land it must be assumed that it is a cos- reported this neogregarine in France where mopolitan parasite so it is only a matter of it infected various Bombus spp. Based on time before it is reported from other coun- the dissection of several hundred workers of tries. Life Cycle lifera from Finland were identical and this allows us to conclude that in all cases of infection the same is Electron microscopy studies undertaken by neogregarine species involved. The oocysts were navicular in Liu et al combined with our previous (1974), and the of them had distinct observations (Lipa and 1992) and shape majority Triggiani, Fresh measured in water the results of the present study, provide caps. oocysts were 16.2-21.6 μm long and 5.6 μm wide sufficient data to allow an understanding of after and were the complete life cycle of this neogregarine (fig 1); oocysts fixing staining 11.1-14.4 and 3.6-5.4 wide. in host insects and recognition of the main μm long μm Inside the stained young oocysts, four uni- stages necessary for its identification and nucleate were visible the description of the new genus. sporozoites readily (fig 2). However, they became less visible in The that in the intes- sporozoites emerge the mature oocysts. tine from ingested oocysts penetrate through the midgut wall into the body cavity and infect the fat body cells in which they grow, Taxonomic position develop and multiply. Heavily infected fat tissue is strikingly white and much reduced but microscopic examination for presence Liu et al (1974) described this neogre- of oocysts is required to diagnose infection garine as Mattesia bombi and placed it and identify the pathogen. into the family Ophryocystidae (the authors misspelled it as Ophrocystidae). However, On smeared gut and fat body prepara- the life cycle and of meronts tions of the infected Bombus spp and A mel- morphology and indicate that the lifera oocysts various developmental stages oocysts (spores) Bombus and were observed. Micronuclear meronts have neogregarine infecting spp A mellifera to the diameters up to 45 μm and contain up to 40 belongs family in the order small nuclei, each measuring 1.3 μm. Later Lipotrophidae Neogregarinida micronuclear merozoites are produced that (= Schizogregarinida) (Levine, 1988). to Levine the are oval or elongated and measure According (1988) family contains five 5-9 x 2.5-3.5 μm. Macronuclear meronts Lipotrophidae genera: Mat- measure 20 x 15 μm and give rise to ovoidal Farinocystis, Lipocystis, Lipotropha, tesia, and Menzbieria which have or pyriform macronuclear merozoits oocysts that contain (gamonts) 5-8 μm in diameter. Through the always eight sporozoites. Levine M bombi, process of gametogony, oocysts containing (1988) incorrectly placed which has navicular with four four sporozoites are produced (fig 2). The oocysts 1 and into the presence of empty oocysts in the tissue sporozoites (figs 2) genus Mattesia which has different smears suggests that autoinfection may take quite spindle with 3 place. Liu et al (1974) reported the presence oocysts eight sporozoites (figs of oocysts in the spermatheca of mated and 4). queens and this indicates a possible con- For the reasons explained above, we genital means of transmission of the neogre- remove the neogregarine Mattesia bombi garine. infecting Bombus and Apis from the Matte- sia genus and classify it as Apicystis bombi (Liu et al, 1974) comb nov in a newly estab- Oocyst morphology lished genus Apicystis gen nov. This generic name is proposed to emphasize that the The oocysts observed in Bombus spp from neogregarine is associated with insects Canada, Italy and Switzerland and in A mel- belonging to the family Apoidea. Host specificity tivity of A bombi to bumble bees or honey bees have been conducted. Since infec- All host records refer to insects infected in tion has been recorded in ten species of nature, and thus far no tests on the infec- Bombus, on two continents and in four countries, it may be concluded that bum- bimaculatus, B fervidus, B griseocollis, B ble bees are the principal hosts for A bombi. hortorum, B impatiens, B perplexus, B ter- Observations in Finland indicate that A restris, B terricola, and B vagans in bombi can also infect honey bees (A mel- Canada, France, Italy and Switzerland, and lifera).
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