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A new species of Laboulbenia (Ascomycota) parasitic on an African fly (Diptera: Curtonotidae), with a brief review of Diptera-associated species of the genus.

INTRODUCTION

Laboulbeniales is a large group of ascomycete fungi which complete their entire lifecycle on living arthropods. Most are found on insects, but a few are known to parasitise mites and millipedes. These fungi are chiefly ectoparasitic, but a small number of the nearly 2,000 described species penetrate the insect's cuticle by means of more-or-less developed rhizoids.

With almost 600 described species, the genus Laboulbenia is by far the largest among the Laboulbeniales (Rossi 2011). The number of species of Laboulbenia parasitic on the Diptera is, however, relatively small, only 23 having been described to date. These are reported from the dipterous families Celyphidae, Curtonotidae (as Drosophilidae), Chloropidae, Diopsidae, Lauxaniidae, Psilidae, Richardiidae, Tephritidae and various unidentified flies (Balazuc 1980; Lee & Majewski 1986; Rossi & Kotrba 2004; Rossi & Ponziani 2008; Rossi 1986, 1987; Thaxter 1901, 1902, 1917, 1918). A review of all previous records of Laboulbenia spp. associated with the Diptera is presented in tabulated form below (Table 1). Included names are updated, although some familial names were not specified in the original publications and some may represent misidentifications. It should be borne in mind that about half of the listed associations represent records from the African continent. It is also noteworthy that only a single fungal species, Laboulbenia diopsidis Thaxt., has subsequently been recorded after its original description. This does not represent evidence of rarity, but rather bears witness to the scarcity of research done in this field.

During the course of an ongoing revision of Madagascan Curtonotum Macquart, 1844 by A. Kirk-Spriggs, numerous specimens of the Malagasy endemic species Curtonotum balachowskyi Tsacas, 1974, were discovered parasitised by a fungus (e.g., Figs 1, 2). Further examination revealed that this parasite represents a new species of the genus Laboulbenia, which is described herein.

MATERIAL AND METHODS

Insects bearing Laboulbeniales were found in samples preserved in 95 % ethanol, resulting from Mike Irwin's Arthropod Survey of Madagascar's Protected Areas, on loan from the California Academy of Sciences, USA (CASC). Thalli were carefully removed from the hosts with a size 3 insect pin. Permanent microscope slides of fungi were prepared following

the method described by Benjamin (1971), using Amann's solution, which is a mixture of glycerol, phenol and lactic acid, as mounting medium; cover slips were ringed with transparent nail varnish.

Slides of the type series are preserved in the Botanical Museum of Florence, Italy (FI) except for the isotype, which is deposited at the National Museum, Bloemfontein, South Africa (BMSA).

TAXONOMY

Order Laboulbeniales Lindau, 1898

Genus Laboulbenia Mont. & C.P. Robin, 1853

Laboulbenia curtonoti sp. n.

Figs 1-5

Etymology: The specific epithet curtonoti is derived from the name of the host insect (Curtonotum).

Description:

Cellula Ifere sphaerica, tota aut ex maiore parte inserta in corporem hospitis; thallus infra integumentum in magnam hypham productus. Cellula IIfere hyalina, elongatum ac uniformem stipitem efficiens, sursum paulo dilatatum. Cellula appendicem sufferens grisea, sesqui longior quam latior, tertia superiore parte soluta, superficie superioris ac exterioris partis striata. Psallium clare brevius quam latitudo cellulae subiacentis. Exterior appendix grisea, constans e magna basali cellula extra prominenti et 3-4 superpositis cellulis gradatim minoribus, ex quibus confertus caespes elongatorum ac fusciorum antheridiorum gignit. Interior appendix ex una parva cellula constans ex qua oriuntur duo breves deducti ramuli singulum caespitem antheridiorum in summoferentes; in maturis speciminibus interior appendix in tenues, hyalinos ac curvatos ramulos producitur. Cellula VI grisea, striata, tam longa quam maxima latitudo. Perithecii venter solutus, fuscus, ovoideus, verticalibus septis in laxam spiram tortis. Perithecii collum abrupte angustatum, griseum, breve, incurvatum, tres protuberationes ferens. Dilute griseus apex tres protuberationes fert, in duo magna, hyalina ac paulo deducta labia, aures asini efficientia, desinens. Tota longitudo 410-520 pm, ascosporae 55 pm. Parasitus Curtonoti balachowskyi in Africa meridionali, in insula Madagascar nominata.

Cell I subspherical, partially to entirely inserted within host's integument; thallus penetrating beneath integument with large haustorium (rhizomycelium). Cell II subhyaline, forming elongated stalk of uniform diameter throughout, only slightly enlarged apically. Stalk-cell of appendage (cells III+IV+V) greyish, about 1.5* longer than broad, its upper third free, although often in contact with base of perithecium; surface of upper, outer portion finely striate. Insertion cell dark, but not opaque, distinctly narrower than stalkcell of appendage. Outer appendage greyish, with large basal cell bulging externally, followed by series of 3 or 4 gradually narrowing, superimposed cells, bearing dense tuft of elongate, brownish antheridia on inner side. Inner appendage consisting of small basal cell giving rise on either side to very short branchlets, bearing apically crown of antheridia; in older specimens antheridia replaced by slender, hyaline, curved, sterile appendages, which barely reach half the height of perithecium. Stalk-cell of perithecium (cell VI) greyish, about as long as maximum width, its surface inconspicuously striate, separated from cell below by distinctly oblique septum. Perithecial venter free, blackish brown, ovoid, wall cells slightly twisted. Neck abruptly constricted, greyish, relatively short, distinctly curved, bearing two symmetrical, rounded prominences on inner (dorsal) side and smaller and paler bulge on outer side. Tip pale grey, also bearing three prominences positioned above those of neck; two inner ones hemispherical, surmounted by two small, erect, parallel, finger-like lips; outer one larger and less protruding, giving rise to two large, hyaline, slightly diverging, pointed, horn-like lips. Total length (from insect cuticle) 410-520 um, ascospores 55 [micro]m.

[FIGURES 1-5 OMITTED]

Holotype: MADAGASCAR:MajungaProv. : Maintirano District, Asondrodava dry forest 15 km N of Maintirano, 17[degrees]57.92'S:44[degrees]2.13'E, 200 ft [61 m], Malaise trap, 31.xii.2007-7.i.2008, M. Irwin & R. Harin'Hala, on the underside of the abdomen of Curtonotum balachowskyi Tsacas (Diptera: Curtonotidae), No. 3510a (FI).

Isotype: same data as the holotype, No. 3510b (BMSA).

Paratypes: MADAGASCAR: Majunga Prov. : Same data as the type, No. 3486; Besalampy District, Marofotofra palm forest 17 km W of Besalampy, 16[degrees]43.30'S:44[degrees]25.42'E, 35 ft [11 m], Malaise trap, 19-26.xi.2007, M. Irwin & R. Harin'Hala, Nos. 3540 & 3546 (FI).

DISCUSSION

The small group of species of Laboulbenia parasitic on Diptera is paraphyletic. From the morphological standpoint it can be divided in three groups: one in which cells III, IV and V are distinct; one with these cells undivided; and one with a distinct cell V and cells III+IV fused together.

The very peculiar distal portion of the perithecium of Laboulbenia curtonoti sp. n., with the two large lips resembling the ears of a donkey, makes it possible to immediately distinguish it from all other species of the genus. The only species to which it can eventually be compared is L. dahlii (Thaxt.) Thaxt. (= Ceraiomyces dahlii Thaxt.), described from an unidentified "flower fly" from New Britain (Thaxter 1901). This latter parasite also penetrates the host with a long haustorium and shares the undivided stalk cell of the appendage, but differs from L. curtonoti in almost every other respect.

Preservation for extended periods in 95 % ethanol, as these specimens had been, results in host insects becoming stiff and brittle, and as a result, it was not possible to extract the penetrating haustorium intact. It was possible, however, to observe that the basal portion of the haustorium is still quite large (diameter ca 30 [micro]m) and undivided after 420 um. From this it can be inferred that it is long and ramified in the distal portion as in L. dahlii (Thaxter 1908, pl. XLIII, fig. 4).

From preserved museum specimens it is also impossible to ascertain the degree of damage caused by the parasite to its host. Experimental studies undertaken with Stigmatomyces ceratophorus Whisler indicated that the life span of its host, the fly Fannia canicularis (L.), was not influenced by the presence of Laboulbeniales (Whisler 1968). This example provides only limited evidence, however, as S. ceratophorus is a "pure" ectoparasite and flies reared under experimental condition are not subject to predator pressure or food shortages. It can be assumed in the present case that the presence of large haustoria of L. curtonoti sp. n. may be detrimental to the host, especially when these occur in critical numbers on a single host fly (Fig. 3).

Three additional species of Laboulbenia have been reported on flies of the family Curtonotidae. These fungi, which were all found on unidentified species of Cyrtona Seguy sensu lato (as Cyrtoma [sic!]), are L. cyrtomatis Balazuc (Senegal), L. matilei Balazuc (Central African Republic), and L. tsacasii Balazuc (KwaZulu-Natal Province, South Africa) (Balazuc 1980). Besides having a very different perithecial neck and tip, the last-named three species also differ from L. curtonoti in having different appendages and a "normal" basal cell (cell I), bearing the "usual" black foot at the base, not penetrating the host.

ACKNOWLEDGMENTS

Specimens used in this study were kindly loaned by N. Penny (CASC). These specimens were sorted in Sacramento, USA, by D. Woods and S.D. Gaimari.

REFERENCES

BALAZUC, J. 1980. Laboulbeniales nouvelles (Ascomycetes) parasites de Coleopteres et de Dipteres. Bulletin du Museum National d'histoire naturelle, 4e ser., 2, section B 2: 209-219.

BENJAMIN, R.K. 1971. Introduction and supplement to Roland Thaxter's monograph of the Laboulbeniaceae. Bibliotheca Mycologica 30: 1-155.

LEE, Y.-B. & MAJEWSKI, T. 1986. Three new species of Laboulbeniales

from Malaysia. Mycologia 78: 401-406.

MACQUART, J. 1844 [1843]. Dipteres exotiques nouveaux ou peu connus. Tome 2e. 3e partie. Paris: N.E. Roret.

ROSSI, W. 1986. Su alcune specie di Laboulbenia nuove o interessanti della Sierra Leone. AccademiaNazionale dei Lincei, Quaderno 260: 77-96.

--1987. New Laboulbeniales (Ascomycetes) parasitic on Diptera. NovaHedwigia 44: 461-464.

--2011. New species of Laboulbenia from Ecuador, with evidence for "host switch" events in the Laboulbeniales. Mycologia 103 (1): 184-194.

ROSSI, W. & KOTRBA, M. 2004. A new, polymorphic species of Laboulbenia parasitic on a South American fly. Mycological Research 108: 1315-1319.

ROSSI, W. & PONZIANI, P.R. 2008. New Laboulbeniales (Ascomycotina) from French Guyana. Cryptogamie, Mycologie 29: 3-9.

THAXTER, R. 1901. Preliminary diagnoses of new species of Laboulbeniaceae. III. Proceedings of the American Academy of Arts and Sciences 36: 397-414.

--1902. Preliminary diagnoses of new species of Laboulbeniaceae. V. Proceedings of the American Academy of Arts and Sciences 38: 7-57.

--1908. Contribution toward a monograph of the Laboulbeniaceae. Part II. Memoirs of the American Academy of Arts and Sciences 13: 217-469.

--1917. New Laboulbeniales, chiefly dipterophilous American species. Proceedings of the American Academy of Arts and Sciences 52: 649-721.

--1918. Extra-American dipterophilous Laboulbeniales. Proceedings of the American Academy of Arts and Sciences 53: 697-749.

TSACAS, L. 1974. Etude preliminaire des Curtonotidae de Madagascar [Diptera]. Annales de la Societe en tomologique de France (N.S.) 10: 703-719.

WHISLER, H.C. 1968. Experimental studies with a new species ofStigmatomyces (Laboulbeniales). Mycologia 60 (1): 65-75.

Walter Rossi (1) and Ashley H. Kirk-Spriggs (2)

(1) Department of Environmental Sciences, University of L'Aquila, 67100 Coppito (AQ), Italy; valter.rossi@univaq.it

(2) Department of Entomology, National Museum, P.O. Box 266, Bloemfontein 9300 and Research Associate, Department of Zoology & Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa; ashley.kirk-spriggs@nasmus.co.za
TABLE 1

Species of Laboulbenia parasitic on Diptera.

Fungus species         Host family            Host (of type)

admirabilis Y.B. Lee   Celyphidae             Spaniocephylus sp.
& T. Majewski

anguifera Thaxt.       Chloropidae            Hippelates sp.

apotropinae W. Rossi   Chloropidae            Apotropina
& Ponziani                                    panamensis Malloch

clavulifera Thaxt.     ? Lauxaniidae          ?Physogenia sp.

crispata Thaxt.        Chloropidae            Hippelates sp.

curtonoti sp. n.       Curtonotidae           Curtonotum
                                              balachowskyi

cyrtomatis Balazuc     Curtonotidae           Cyrtona sensu lato
                                              sp.

dahlii (Thaxt.)        ? family               flower fly [sic!]
Thaxt.

diopsidis Thaxt.       Diopsidae              Diopsis longicornis
                                              Macquart

gratiellae W. Rossi    Diopsidae              Cyrtodiopsis
                                              dalmanni (Wiedemann)

lagarocerina Thaxt.    Chloropidae            Lagaroceras sp.

lomaensis W. Rossi     Tephritidae            gen. sp.

matilei Balazuc        Curtonotidae           Cyrtona sensu lato
                                              sp.

muiriana Thaxt.        Chloropidae            gen. sp.

muscariae Thaxt.       Lauxaniidae            Xenochaetina
                                              flavipennis
                                              (Fabricius)

pachylophi Thaxt.      Chloropidae            Pachylophus
                                              frontalis Loew

pectinulifera Thaxt.   ? Lauxaniidae          ?Physogenia sp.

porrigens Thaxt.       ? family               gen. sp.

psilina Thaxt.         Psilidae               ?Psila sp.

richardiana W. Rossi   Richardiidae           Richardia teevani
& Kotrba                                      Curran

sapromyzae Thaxt.      Lauxaniidae            Sapromyza triseriata
                                              Coquillet

sphyracephalae W.      Diopsidae              Sphyracephala
Rossi                                         detrahens Walker

steleoceri Thaxt.      Chloropidae            Mepachymerus baculus
                                              Speiser

tsacasii Balazuc       Curtonotidae           Cyrtona sensu lato
                                              sp.

                       Country
Fungus species         (of type)              Reference

admirabilis Y.B. Lee   Malaysia               Lee & Majewski
& T. Majewski                                 (1986)

anguifera Thaxt.       Grenada                Thaxter (1917)

apotropinae W. Rossi   French Guyana          Rossi & Ponziani
& Ponziani                                    (2008)

clavulifera Thaxt.     Cameroon               Thaxter (1918)

crispata Thaxt.        Panama                 Thaxter (1917)

curtonoti sp. n.       Madagascar             this paper

cyrtomatis Balazuc     Senegal                Balazuc (1980)

dahlii (Thaxt.)        New Guinea             Thaxter (1901)
Thaxt.

diopsidis Thaxt.       Liberia                Thaxter (1902)

gratiellae W. Rossi    Malaysia               Rossi (1987)

lagarocerina Thaxt.    Gambia                 Thaxter (1918)

lomaensis W. Rossi     Sierra Leone           Rossi (1986)

matilei Balazuc        Central African Rep.   Balazuc (1980)

muiriana Thaxt.        Papua New Guinea       Thaxter (1918)

muscariae Thaxt.       Guatemala              Thaxter (1917)

pachylophi Thaxt.      Tanzania               Thaxter (1918)

pectinulifera Thaxt.   Cameroon               Thaxter (1918)

porrigens Thaxt.       Cameroon               Thaxter (1901)

psilina Thaxt.         Cameroon               Thaxter (1901)

richardiana W. Rossi   French Guyana          Rossi & Kotrba
& Kotrba                                      (2004)

sapromyzae Thaxt.      Guatemala              Thaxter (1917)

sphyracephalae W.      Philippines            Rossi (1987)
Rossi

steleoceri Thaxt.      Gambia                 Thaxter (1918)

tsacasii Balazuc       South Africa           Balazuc (1980)
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Author:Rossi, Walter; Kirk-Spriggs, Ashley H.
Publication:African Invertebrates
Article Type:Report
Geographic Code:6MADA
Date:Jun 1, 2011
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