Introduction
The classification of the large and heterogeneous group of
microorganisms called protozoans has been recently updated
as increased knowledge of the biology and phylogenetics is acquired.
The Committee on Systematics and Evolution of the Society of
Protozoologists established seven phyla in the elevated subkingdom
Protozoa under the Kingdom Protista more than two decades ago
(Levin, et al., 1980). Later, it was suggested that the protists should be
reorganized into the broader category protoctists that would also
include fungi and algae besides the small eukaryotes consisting of a
single or a few cells (Margulis et al., 1990). However, with the rapidly
increasing phylogenetic data accumulating, this higher order
taxonomy is no longer accurate. Based on molecular phylogenies,
microsporidia are actually included into the cluster Fungi, rank
Opisthokonta which comprises the animals, the fungi and others
eukaryotes (Sina et al., 2005). Microsporidia are, thus, to be regarded
as highly specialized parasitic fungi.
Only two microsporidian parasites are described so far from honey
bees (Nosema apis Zander 1909 and Nosema ceranae Fries et al. 1996).
Nosema apis was detected in the European honey bee (Apis mellifera L
1758) and is one of the first microsporidia to be described (Zander,
1909). Although the parasite and its life cycle have been described by
many authors (see Gray et al., 1969), vegetative stages are difficult to
recognize and identify by light microscopy.These early descriptions have
later been complemented with ultrastructural features of the parasite
(Liu, 1984; Fries, 1989) and also with a molecular characterization
(Gatehouse & Malone, 1998). Nosema ceranae, isolated from the Asian
honey bee (Apis cerana Fabricius 1793) in China is a more recent
description (Fries et al., 1996). There are good reasons to assume that
other microsporidia species are also present in honey bees and await
full descriptions (i.e. Buys, 1977; Clark 1980).
Prior to the description of N. ceranae, observations of microsporidian
infections in A. cerana had already been made (Sing, 1975). Yakobson
(1992) observed microsporidia infections in both A. cerana and A.
mellifera in apiaries with both honey bee species mixed and suggested
that cross infection experiments using N. apis spores could perhaps
elucidate the question of host specificity in N. apis. Many species of
microsporidia cannot be distinguished using light microscopy and only
with difficulty using electron microscopy (Larsson, 1986; Rice, 2001) and
it cannot be excluded that some earlier observations of microsporidia
infections in A. cerana, and possibly also in A. mellifera, may in fact have
been observations of N. ceranae. Reports in the past of damage to A.
cerana colonies attributed to N. apis infections (Lian, 1980) may actually
be reports of N. ceranae, since differences between N. ceranae and N.
apis may have gone unnoticed when investigated under the light
microscope (Fries et al., 1996).
Cross infections between the two host species have
demonstrated that N. apis is in fact infective for A. cerana, but
also that this parasite develops less well in the Asian host
compared to the European host (Fries & Feng, 1995). It has also
been stated that N. ceranae is infective for A. mellifera and
multiplies more readily in A. mellifera than N. apis does in A.
cerana (Fries, 1997), although detailed data were never published.
At the annual meeting of Society for Invertebrate Pathology
in Anchorage, Alaska, 2005 it was reported that N. ceranae had
been found in natural infections in A. mellifera in Taiwan (Huang
et al ., 2005). The apiary where the infection was detected had
harboured both A. mellifera and A. cerana. Thus, it was apparent
that N. ceranae could cross the host species barrier, although no
data on bee pathological repercussions due to N. ceranae in Apis
mellifera were mentioned by the authors.
Almost at the same time and following progressively increased
incidences of problems with nosema disease in Spain (Martin et
al ., 2005), the laboratory of Centro Apícola Regional, involved in
Journal of Apicultural Research 45(3): 230–233 (2006) © IBRA 2006
REVIEW ARTICLE
Natural infections of Nosema ceranae
in European honey bees
I Fries
1*
, R Martín
2
, A Meana
3
, P García-Palencia
3
, M Higes
2
1
Swedish University of Agricultural Sciences, Department of Entomology, 75007 Uppsala, Sweden
2
Centro Apícola Regional. Servicio de Investigación Agraria de la Dirección General de la Producción Agropecuaria. Consejería de Agricultura
de la Junta de Comunidades de Castilla-La Mancha. San Martín s/n. 19180 Marchamalo. Guadalajara. Spain
3
Facultad de Veterinaria. Universidad Complutense de Madrid. Avda Puerta de Hierro s/n 28040 Madrid. Spain
Received 10 May 2006, accepted subject to revision 12 June 2006, accepted for publication 16 August 2006.
* Corresponding author. Email: ingemarf@mail1.slu.se
Keywords: Protozoa, parasites, Nosema apis, Apis mellifera, Apis cerana, Nosema ceranae, Nosema bombi, fumagillin, microsporidia
infections, Taiwan, Spain.