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A new parasitic fungus on the cleptoparasite of bees Braula coeca (Insecta, Diptera): Dimeromyces braulae (Ascomycota, Laboulbeniales)

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A new species of Dimeromyces (Ascomycota, Laboulbeniales) parasitic on the bee louse Braula coeca Nitzsch (Diptera, Braulidae) is described. The most obvious differences between the new species and the others are the more inflated and more numerous antheridia (up to ten), the longer appendages, and the distinctly truncate perithecial apex. The fungus appears to be relatively common in the Czech Republic, with an infection rate of 12.6% (n = 372).
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© 2015 J. Cramer in Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, www.borntraeger-cramer.de
Germany. DOI: 10.1127/nova_hedwigia/2015/0309 0029-5035/2015/0309 $ 1.00
Nova Hedwigia Vol. 102 (2016) Issue 1–2, 271–274
published online October 6, 2015; published in print February 2016 Article
C
A new parasitic fungus on the cleptoparasite of bees
Braula coeca (Insecta, Diptera): Dimeromyces braulae
(Ascomycota, Laboulbeniales)
Walter Rossi1*, Jan Máca2 and Jiři Preisler3
1 University of L’Aquila, Dept. MeSVA, Sect. Environmental Sciences,
67100 Coppito (AQ), Italy
2 Na Potoce 276, CZ-391 81 Veselí nad Lužnicí, Czech Republic
3 Vlnařská 692, CZ-460 01 Liberec 6, Czech Republic
With 1 gure
Abstract: A new species of Dimeromyces (Ascomycota, Laboulbeniales) parasitic on the bee louse
Braula coeca Nitzsch (Diptera, Braulidae) is described. The most obvious differences between the
new species and the others are the more inflated and more numerous antheridia (up to ten), the longer
appendages, and the distinctly truncate perithecial apex. The fungus appears to be relatively common
in the Czech Republic, with an infection rate of 12.6% (n = 372).
Key words: apiculture, bee louse, biodiversity, hyperparasite.
Introduction
The Laboulbeniales, with more than 2,000 described species, are one of the most
biodiverse groups among the non-lichenized Ascomycota (Weir & Hammond 1997).
They are obligate ectoparasites of arthropods: a few are found on mites and millipedes,
but the vast majority has been found on insects. About 10% of the known species are
parasitic on the Diptera, of which 144 belong to the genus Stigmatomyces (Rossi &
Leonardi 2013) and 24 to Laboulbenia (Rossi & Kirk-Spriggs 2011). Among the other
genera occurring on flies is also the dioecious genus Dimeromyces with 7 species
(Thaxter 1924; Rossi et al. 2015).
In the present paper we describe a new species of Dimeromyces that seems to be
rather common on the bee louse Braula coeca Nitzsch (Diptera, Braulidae) in the
*Corresponding author: valter.rossi@univaq.it
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Czech Republic. This species brings the number of the Laboulbeniales reported from
the Czech Republic to 58 (Rossi & Máca 2006; Rossi et al. 2010), and the number of
species in the genus Dimeromyces is raised to 113 (Rossi et al. 2015).
Materials and methods
Dead host insects were collected from the debris in the beehives at the end of winter. In the Czech
Republic surveys of hives are now compulsory in order to predict localities infested by Varroa
mites for the coming year. Insects were stored in 75% ethyl alcohol for transport to the laboratory,
where they were examined with a dissecting microscope. The parasitic fungi were removed from
the hosts by means of an entomological pin (# 3) and temporarily transferred to a small drop of
Hoyer’s medium (Arabic gum 30 g; chloral hydrate 200 g; glycerol 16 ml; distilled water 50 ml)
on a clean slide. Permanent slides were then prepared broadly following the method described by
Benjamin (1971) with a few modifications (Rossi & Santamaria 2015). These slides are deposited
in the Botanical Museum in Florence (FI).
Photomicrographs were made with a Jenoptik ProgRes 10 Plus digital camera on a Leica DMR
microscope equipped with differential interference contrast optics (DIC).
Taxonomy
Dimeromyces braulae W.Rossi, sp. nov. Fig. 1
MycoBank: MB814218
Description: Female thallus faintly tinged with brownish yellow, except for the darker
perithecial tip and lowermost cell of both appendages. Receptacle composed of four
cells, the large basal cell consisting of a rounded basal portion from which arises the
subconical upper portion; the suprabasal cell very small and flattened, bearing the
single secondary appendage; the third cell also small, subtriangular or subtrapezoidal,
bearing the (usually) single perithecium; the fourth cell longer than broad, bearing
distally the primary appendage. The latter is long and slender, whip-like, consisting of
elongate cells, the shortest being the lower, darker cell which is twice as long as broad;
the secondary appendage is similar, but distinctly longer than the primary. Perithecium
subsessile, with stalk and basal cells very small; perithecial body oblong, slightly
inflated, regularly and symmetrically tapering to the broad tip and subtruncate apex.
Length from foot to perithecial apex 190–210 µm. Perithecia 105–145 × 28–37 µm.
Longest appendage 265 µm.
Male thallus concolorous with the female. Receptacle elongate and falcate, consisting
of a series of (5)8–11 cells, the basal much larger, subcylindrical or subtrapezoidal,
arising from a globose base, the others small, gradually longer and more slender
from below upwards, each laterally bearing a single ampoule-like antheridium with
an inflated venter and a narrow curved efferent neck; the uppermost cell of the series
bears apically a long appendage similar to the primary appendage of the female thallus.
Length from foot to the apex of the uppermost antheridium 120–140 µm. Length from
foot to the apex of the appendage 185 µm. Length of a single antheridium about 27 µm.
Holotype: Czech Republic, Cheb, Jindřichov, 2 March 2009, leg. Jiří Preisler, at the tip of the
abdomen of Braula coeca Nitzsch (Diptera, Braulidae), no. 3840 (FI).
eschweizerbart_xxx
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paratypes: Karlovy Vary, Kyselka, Feb. 2009, no. 3955; Semily, Ktová, 5 Feb. 2010, no. 3954;
Semily, Příkrý, 22 Nov. 2011, no. 3841 (all collected by J.Preisler on B. coeca).
Discussion
Dimeromyces braulae is likely allied to the other seven species in the same genus
associated with flies. In all these fungi the cells forming the receptacle are arranged in
an almost vertical series and the perithecia are subsessile (Thaxter 1908, plate XXVIII,
figs 1–8; 1924, plate IX, figs 239–250, 1926, plate I, figs 7–10). The most obvious
differences between the new species and the others are the more inflated and more
numerous antheridia (up to ten), the longer appendages, and the distinctly truncate
perithecial apex.
Another characteristics distinguishing D. braulae from the other seven species on
Diptera is the way it is fixed to the host-insect. Its "foot" is inconspicuous and the
basal cell is modified to form a depression laterally, which works as a sucker. A similar
structure was described by Thaxter (1918) in another species associated with flies:
Laboulbenia lagarocerina Thaxter, parasitic on Lagaroceras sp. (Chloropidae) from
West Africa.
Among the 372 specimens of Braula coeca examined, 47 bore Dimeromyces braulae
(= 12.6%), in other words about one of every eight. This is a very high rate of infection
Fig. 1. One male (on the left) and two female thalli of Dimeromyces braulae from the type slide.
Scale bar = 100 µm.
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for the Laboulbeniales, likely the highest infection rate ever observed on the Diptera.
In comparison, in NE Brazil Bergonzo et al. (2004) found only 180 specimens bearing
Laboulbeniales of the genera Stigmatomyces and Ilytheomyces among 30,000 flies of
various families collected in the field; this is a 0.6% infection rate (one infected fly
out of more than 160).
Acknowledgments
The authors express their gratitude to C.Keil and D.H.Pfister (USA) for helpful suggestions. W.R.
wishes to thank also A.Cicchino (Argentina) for pointing out the presence of a parasitic fungus on
the bee louse. Special thanks are due to S.Santamaria (Spain) for the photograph of the new fungus.
References
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Manuscript submitted July 8, 2015; accepted August 31, 2015.
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Bats serve as hosts to many lineages of arthropods, of which the blood-sucking bat flies (Nycteribiidae and Streblidae) are the most conspicuous. Bat flies can in turn be parasitized by Laboulbeniales fungi, which are biotrophs of arthropods. This is a second level of parasitism, hyperparasitism, a severely understudied phenomenon. Four genera of Laboulbeniales are known to occur on bat flies, Arthrorhynchus on Nycteribiidae in the Eastern Hemisphere, Dimeromyces on Old World Streblidae, Gloeandromyces on New World Streblidae, and Nycteromyces on Streblidae in both hemispheres. In this chapter, we introduce the different partners of the tripartite interaction and discuss their species diversity, ecology, and patterns of specificity. We cover parasite prevalence of Laboulbeniales fungi on bat flies, climatic effects on parasitism of bat flies, and coevolutionary patterns. One of the most important questions in this tripartite system is whether habitat has an influence on parasitism of bat flies by Laboulbeniales fungi. We hypothesize that habitat disturbance causes parasite prevalence to increase, in line with the “dilution effect.” This can only be resolved based on large, non-biased datasets. To obtain these, we stress the importance of multitrophic field expeditions and international collaborations.
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Laboulbeniales (Ascomycota: Laboulbeniomycetes) are obligate ectoparasitic fungi of arthropods with a worldwide distribution. Their effects on host physiology and behaviour as well as their ecology have recently gained wider attention. One aspect that is virtually unknown regarding Laboulbeniales and arthropod-associated fungi in general, is how abiotic factors shape the distribution of these parasites. We used ant- and bat fly-associated Laboulbeniales to study whether climatic elements play a role in the distribution of fungal species. We collected uninfected and Laboulbeniales-infected insects belonging to three species: bat flies Nycteribia schmidlii and Penicillidia conspicua (Diptera: Nycteribiidae) and the ant Myrmica scabrinodis (Hymenoptera: Formicidae). We used climatic variables and performed statistical analyses to explain the distribution of Laboulbeniales infection. Our results show a higher likelihood of Laboulbeniales presence in habitats with low annual mean temperature and humidity, suggesting that climatic elements can considerably shape the distribution of Laboulbeniales species.
... A few more species were appended later: Rickia wasmannii Cavara from Slovakia (Bezděčka & Bezděčková 2011), Hesperomyces virescens Thaxt. from the Czech Republic (Ceryngier & Twardowska 2013) and from Slovakia ( Haelewa- ters et al. 2016), Dimeromyces braulae W. Rossi from the Czech Republic ( Rossi et al. 2016). To date, the total numbers of Laboulbeniales from the Czech Republic and from Slovakia are 58 and 24 respectively. ...
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  • R Thaxter
THAXTER, R. 1908: Contribution toward a monograph of the Laboulbeniaceae. Part II. -Mem. Am. Acad. Arts Sci. 13: 217-469.
  • R Thaxter
THAXTER, R. 1918: Extra-American Dipterophilous Laboulbeniales. -Proc. Am. Acad. Arts Sci. 53: 697-749. http://dx.doi.org/10.2307/20025703
  • R Thaxter
THAXTER, R. 1924: Contribution towards a monograph of the Laboulbeniaceae. Part III. -Mem. Am. Acad. Arts Sci. 14: 309-426.