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Ascomycota: Laboulbeniales): Ectoparasitic Fungi on Ants (Hymenoptera: Formicidae)

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Ascomycota: Laboulbeniales): Ectoparasitic Fungi on Ants (Hymenoptera: Formicidae) Myrmecological News 23 81-89 Vienna, September 2016 Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae) Simon TRAGUST , András TARTALLY , Xavier ESPADALER & Johan BILLEN Abstract Among the many associations between fungi and ants, the associations involving the ectoparasitic fungi Laboulbeniales (Ascomycota: Laboulbeniales) have remained largely enigmatic even today. However, for two of the six ant-parasitizing Laboulbeniales, it has been found that parasitism is correlated with diminished survival of their hosts, especially under resource limitation. In the present study, we investigate whether these fitness impacts are linked to an intrusion into the body cavity by the ectoparasites. Light, scanning and transmission electron microscopy were used to study the mode of attachment and the presence of penetrating structures in four of the six currently recognized ant-parasitizing Laboul- beniales. No indication of penetration was found, suggesting that the reported fitness impacts are not linked to an intru- sion into the body cavity. A better understanding of host-parasite interactions involving Laboulbeniales on ant hosts is necessary, considering that Laboulbeniales parasitizing ants impact their hosts' fitness and that monitoring studies have revealed that an infection with Laboulbeniales is much more common in European ants than previously thought. Key words: Host-parasite interaction, symbiosis, haustoria, nutrition, invasive species, ant-fungus association. Myrmecol. News 23: 81-89 (online 31 May 2016) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 15 February 2016; revision received 18 March 2016; accepted 21 March 2016 Subject Editor: Chris R. Smith Simon Tragust (contact author) , Animal Ecology I , University of Bayreuth , Universitätsstr. 30 , D-95447 Bayreuth , Germany. E-mail: [email protected] András Tartally , Department of Evolutionary Zoology and Human Biology , University of Debrecen , Egyetem tér 1 , Debrecen , 4032 , Hungary. Xavier Espadaler , Ecology Unit and CREAF , Universitat Autònoma de Barcelona , Cerdanyola del Vallès , E-08193 , Spain. Johan Billen , Zoological Institute , University of Leuven , Naamsestraat 59 , box 2466 , B-3000 Leuven , Belgium. Introduction Ants (Hymenoptera: Formicidae) are well-known to enter- benia formicarum THAXTER , 1902 but also that parasitized tain a variety of associations with diverse organisms (H ÖLL - colonies seemed less prosperous than non-parasitized col- DOBLER & W ILSON 1990). Among these organisms, fungi onies (for similar observations, see also RICK 1903, S MITH cover the whole spectrum of relationships from mutualism 1917). Recently, possible fitness effects of Laboulbeniales to parasitism (V EGA & B LACKWELL 2005). While some parasitizing ant hosts have been addressed more explicitly. ant-fungus associations are comparably well studied, e.g., Two species, L. formicarum and Rickia wasmannii CA- in the tribe Attini (Hymenoptera: Formicidae: Myrmicinae: VARA , 1899 parasitizing Formicinae and Myrmicinae ant Attini) (M EHDIABADI & S CHULTZ 2010), other associa- species, respectively, have been found to reduce the sur- tions, e.g., involving the fungi of the order Laboulbeniales vival of their European ant hosts (C SATA & al. 2014, (Ascomycota: Laboulbeniales) have received less attention. KONRAD & al. 2015). Furthermore, although the potenti- Laboulbeniales are obligate biotrophic fungi living as ecto- ally interacting factors of individual ant age and infection parasites mostly on insects (W EIR & B LACKWELL 2005) level were not disentangled, mortality was found to be with currently six different species from three genera de- more pronounced under resource limitation, i.e., food and scribed on ant hosts (S ANTAMARIA & E SPADALER 2014). / or water restriction (B ÁTHORI & al. 2015a, K ONRAD & A common view is that Laboulbeniales have little or al. 2015). no effect on parasitized hosts (B ENJAMIN 1971, T AVARES Generally, Laboulbeniales are believed to draw resour- 1985, K AUR & M UKERJI 2006). This is likely in part due ces from their hosts for growth and development, either to the existence of only few controlled studies investigating through absorption or via contact with living tissues (S CHE - fitness effects of Laboulbeniales (W HISLER 1968, S TRAND - LOSKE 1969, B ENJAMIN 1971, T AVARES 1985). Although BERG & T UCKER 1974). Early notes on Laboulbeniales some Laboulbeniales appear to only attach to the integu- parasitizing ants also report contradictory results. For ex- ment of their hosts, others produce penetration structures ample, WHEELER (1910) noted the behaviour of Lasius (reviewed in SCHELOSKE 1969, B ENJAMIN 1971, T AVARES neoniger EMERY , 1893 ants to be unaffected by Laboul- 1985, see also Tab. 1). Invasion into the body cavity in the Tab. 1: Overview of current literature indicating the presence of penetration structures in species of ectoparasitic Laboul- beniales (Ascomycota) together with arthropod host species that were examined, the type of evidence given (photographs, histological sections, drawings, reports or indirect evidence through staining) and reported fitness impact (yes, no, un- known, together with type of evidence given and related literature reference). Superscript small letters indicate: a de- b c scribed as Paracoreomyces thaxteri , described as Herpomyces tricuspidatus see BENJAMIN (1971: p. 33), according to d e TAVARES (1979) the structure could also simply be cracks in the cuticle, described as Sunius prolixus , Orifice is the passage for the penetration structure on the base of the foot of the thallus, f described as Menopon pallidum , g described as Goniocotes abdominalis , h Herpomyces spp. on Parcoblatta lata , i Trenomyces spp. on unspecified hosts, j Scheloske (1969) reported this species in the genus Harpalus . Laboulbeniales Host species Reference Evidence Fitness imp act species (Order) Arthrorhynchus Penicillidia conspicua BLACKWELL (1980) Fig. 2: photograph of unknown nycteribiae (Diptera) penetration structure Arthrorhynchus Cyclopodia macrura THAXTER (1896) Plate XLVIII Fig. 2: drawing unknown cyclopodiae (Diptera) of penetration struc ture Coreomyces Stenocorixa protrusa POISSON (1929) reports penetration structure unknown thaxteri a (Hemiptera) Coreomyces Corixa affinis POISSON (1929) reports penetration structure unknown corisae (Hemiptera) Dimeromyces unknown species THAXTER (1908) Plate XXVIII Figs. 6, 7: draw- yes: report of injury to abdo- rhizophorus (Diptera) ing of penetration structure minal tissues ( THAXTER 1908) Gloeandromyces Pterellipsi aranea THAXTER (1931) Plate XX Fig. 16: drawing of unknown nycteribiidarum (Diptera) penetration structure Herpomyces Blattella germanica TAVARES (1985) Plate 10 b, c: histological sec- yes: higher mortality (GEMENO ectobiae (Blattodea) tions of penetration structure & al. 2004) h Herpomyces Blattella germanica RICHARDS & S MITH reported as similar to H. yes and no: report of unaffected ectobiae (Blattodea) (1956) stylopygae on B. orientalis motility, reproduction and lon- gevity, but damage of the epi- dermis (RICHARDS & S MITH 1956) Herpomyces Blatta orientalis RICHARDS & S MITH Figs. 16 - 23: histological sec- see above (RICHARDS & S MITH stylopygae (Blattodea) (1956) tions of penetration structure 1956) (3 types: Ø 0.1 - 0.3, Ø 1.5 - 2 and Ø 2 - 5 µm) Herpomyces Blaberus cranifer RICHARDS & S MITH reported as similar to H. see above (RICHARDS & S MITH paranensis b (Blattodea) (1956) stylopygae on B. orientalis 1956) Herpomyces Blaberus cranifer TAVARES (1979) Fig. 9.3: histological sections see above (RICHARDS & S MITH paranensis (Blattodea) of penetration structure 1956) Hesperomyces Chilocorus bipustulatus KAMBUROV & al. Plate 2, Plate 4b: photographs yes: reduced survival (KAM - virescens (Coleoptera) (1967) of penetration structures (Ø BUROV & al. 1967, R IDDICK 2.5 - 3 µm) 2010) no: unaffected metabolism (APPLEBAUM & al. 1971) Hesperomyces Cycloneda sanguinea TAVARES (1979) Fig. 9.4: histological sections unknown virescens (Coleoptera) of penetration structures Hesperomyces Cycloneda sanguinea TAVARES (1985) Plate 16 a - c: histological sec- unknown virescens (Coleoptera) tions of penetratio n structure Hesperomyces Adalia bipunctata WEIR & B EAKES Figs. 17, 18: photograph of pe- unknown virescens (Coleoptera) (1996) netration pore on cuticle (Ø 3 µm with Ø 1 µm penetration pore) Hesperomyces Olla v-nigrum WEIR & BEAKES unknown virescens (Coleoptera) (1996) Hydrophilomyces Phaenonotum TAVARES (1985) Plate 31e: photograph of pene- unknown reflexus extriatum (Coleoptera) tration structure Laboulbenia Aulonogyrus THONGHINI (1913) Fig. 10: drawing of penetra- unknown gyrinidarum concinnus (Coleoptera) tion structure c 82 Laboulbenia Demetrias monostigma CÉPÉDE (1914) Plate VI, Figs. 4, 5, 7, 8, 10, unknown blanchardii (Coleoptera) 11: drawing of penetration structure (Ø 0.5 - 6 µm) Laboulbenia Leistus fulvibarbis POISSON (1929) reports penetration structure unknown fasciculata (Coleoptera) Laboulbenia unknown species COLLA (1926) Fig. 2c: drawing of penetra- unknown vulgaris (Coleoptera) tion structure Laboulbenia Harpalus affinis SCHELOSKE (1969) reports penetration structure unknown macrotheca (Coleoptera) j Laboulbenia Pseudoophonus rufipes SCHELOSKE (1969) infers penetration structure unknown coneglanensis (Coleoptera) from successful staining j Laboulbenia Ophonus puncticollis SCHELOSKE (1969) infers penetration structure unknown ophoni (Coleoptera) from successful
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