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MYCOLOGIA December 2014 NOVEMBER Vol. 106 No. 6 106/6 M Y COL O G I A November / December 2014 November MYCOLOGIA December 2014 ECOLOGY – 1065–1072 Zombie bugs? The fungus Purpureocillium cf. lilacinum may manipulate the behavior of its host bug Edessa rufomarginata • WILLIAM EBERHARD, JESSICA PACHECO-ESQUIVEL, FARAH CARRASCO-RUEDA, YULIANA CHRISTOPHER, CELY GONZALEZ, DANIEL RAMOS, HECTOR URBINA & MEREDITH BLACKWELL 1073–1089 Fodinomyces uranophilus gen. nov. sp. nov. and Coniochaeta fodinicola sp. nov., two uranium mine-inhabiting Ascomycota fungi from northern DECEMBER Australia • XABIER VÁZQUEZ-CAMPOS, ANDREW S. KINSELA, T. DAVID WAITE, RICHARD N. COLLINS & BRETT A. NEILAN EVOLUTION 1090–1105 Novel endophytic lineages of Tolypocladium provide new insights into the ecology and evolution of Cordyceps-like fungi • ROMINA GAZIS, DEMETRA SKALTSAS & PRISCILA CHAVERRI PLANT PATHOGENS 1106–1118 Two clonal lineages of Phytophthora citrophthora from citrus in South Africa represent a single phylogenetic species • CHRISTOFFEL F.J. SPIES, JULIA C. MEITZ-HOPKINS, SHAUN D. LANGENHOVEN, MATHYS C. PRETORIUS & ADÉLE MCLEOD 2014 1119–1126 Phaeoacremonium italicum sp. nov., associated with esca of grapevine in southern Italy • MARIA LUISA RAIMONDO, FRANCESCO LOPS & ANTONIA CARLUCCI SYSTEMATICS 1127–1142 Toward a stable classification of genera within the Entolomataceae: a phylogenetic re-evaluation of the Rhodocybe-Clitopilus clade • KERRI L. KLUTING, TIMOTHY J. BARONI & SARAH E. BERGEMANN 1143–1158 Affinities and architecture of Devonian trunks of Prototaxites loganii • G.J. RETALLACK & ED LANDING 1159–1167 Vibrisseaceous fungi from the southern hemisphere, including Chlorovibrissea chilensis (Helotiales, incertae sedis) sp. nov. • P. SANDOVAL-LEIVA, MYCOLOGIA C.C. CARMARÁN, D. PARK, A.I. ROMERO & P.R. JOHNSTON 1168–1187 Alessioporus and Pulchroboletus (Boletaceae, Boletineae), two novel genera for Xerocomus ichnusanus and X. roseoalbidus from the European Mediterranean basin: molecular and morphological evidence • MATTEO GELARDI, GIAMPAOLO SIMONINI, ENRICO ERCOLE & ALFREDO VIZZINI 1188–1198 Irineochytrium, a new genus in Chytridiales having zoospores and aplanospores • PETER M. LETCHER, JOYCE E. LONGCORE & MARTHA J. POWELL 1199–1211 Combining morphological and phylogenetic analyses to unravel systematics in Geastrum sect. Schmidelia • JUAN CARLOS ZAMORA, FRANCISCO DE DIEGO CALONGE & MARÍA P. MARTÍN 1212–1219 A new species of Alwisia (Myxomycetes) from New South Wales and Tasmania • DMITRY V. LEONTYEV, STEVEN L. STEPHENSON & MARTIN SCHNITTLER 1220–1232 Morphological and molecular characterization of three Agaricus species from tropical Asia (Pakistan, Thailand) reveals a new group in section Xanthodermatei • NARITSADA THONGKLANG, RIZWANA NAWAZ, ABDUL N. KHALID, JIE CHEN, KEVIN D. HYDE, RUILIN ZHAO, LUIS A. PARRA, MUHAMMAD HANIF, MAGALIE MOINARD & PHILIPPE CALLAC WITH GRATITUDE VO 1233 L . 10 6 • P P . 1065 – 1236 ISSN 0027-5514 MYCOAE 106(6):1065–1236 (2014) ISSUED 17 NOVEMBER 2014 OFFICIAL BIMONTHLY PUBLICATION of the MYCOLOGICAL SOCIETY OF AMERICA Mycologia, 106(6), 2014, pp. 1065–1072. DOI: 10.3852/13-264 # 2014 by The Mycological Society of America, Lawrence, KS 66044-8897 Issued 17 November 2014 Zombie bugs? The fungus Purpureocillium cf. lilacinum may manipulate the behavior of its host bug Edessa rufomarginata William Eberhard1 Key words: Costa Rica, insect, parasitic manipula- Smithsonian Tropical Research Institute, Department of tion, pentatomid bug Biological Sciences, Escuela de Biologı´a, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica, and Department of Biological Sciences, Louisiana State INTRODUCTION University, Baton Rouge, Louisiana 70803 Some parasitic organisms, including fungi, alter or Jessica Pacheco-Esquivel manipulate the behavior of their hosts in ways that Laboratorio de Ecologı´a de Plantas, Escuela de Ciencias promote the survival and reproduction of the parasite Biolo´gicas, Pontifica Universidad Cato´lica del Ecuador, (summaries in Libersat et al. 2009, Hughes et al. Apartado 17-01-2184, Quito, Ecuador 2012). Several groups of entomopathogenic fungi Farah Carrasco-Rueda induce their hosts to occupy a position that is thought Center for Conservation Education and Sustainability, to be advantageous for spore dispersal. Some zygo- Smithsonian Conservation Biology Institute, National mycetes in Entomophthorales induce insects to move Zoological Park, P.O. Box 37012, MRC 705, upward on plants. Just before killing the host fly, Washington, DC 20013-7012 Scathophaga stercoraria, Entomophthora muscae induc- Yuliana Christopher es the fly to perch at unusual sites on emergent Cely Gonzalez vegetation in open fields in atypical ways: higher Center for Biodiversity and Drug Discovery, Institute for above the ground than usual, at the tips of leaves or Scientific Research and High Technology Science, City of flowers on the downwind side of the plant, facing Knowledge, P.O. Box 0843-01103, Panama inward toward the plant, grasping the leaf or flower Daniel Ramos with its legs, and lowering its wings and elevating its Universidad Laica Eloy Alfaro de Manabı´-Manta, abdomen from which the spores will emerge (Mait- Ecuador Calle 12, Vı´a San Mateo, Manta, Ecuador land 1994). Another entomophthoralean fungus may Hector Urbina induce a related host fly, Musca domestica, to raise its Meredith Blackwell abdomen, raise its wings and extend its mouthparts to the substrate, allowing a strong attachment to form Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 (Brobyn and Wilding 1983, Krasnoff et al. 1995). Such modifications probably increase the release and dispersal of the spores when they are shed from the Abstract: Just before dying, Edessa rufomarginata fly. (Hemiptera, Pentotomidae) individuals that are Similar behavior by ‘‘zombie’’ ants is caused by infected with the fungus Purpureocillium cf. lilacinum certain ascomycetes (Evans et al. 2011). Some (Ascomycota: Ophiocordycipitaceae) move from the members of Ophiocordyceps (5 Cordyceps) spp. (Hy- leaves onto the stems of their Solanum sp. host and pocreales, Ophiocordycipitaceae) (Sung et al. 2007) firmly grasp the stems in ways seldom employed by induce infected worker ants to seize a twig, a leaf or uninfected bugs. These alterations in host behavior another object firmly with their legs and mandibles probably improve the chances that the subsequently (Pontoppidan et al. 2009, Evans et al. 2010, Evans produced fungal spores will be dispersed aerially. 2012). Infected workers of the ant Campanotus Purpureocillium cf. lilacinum is a member of the leonardi, the principal host of Ophiocordyceps unilater- Ophiocordycipitaceae, a group in which other species alis, grasp the undersides of leaves just before dying also modify the behavior of their hosts. As in the case (Pontoppidan et al. 2009). Ascospores escape from of newly distinguished relatives of Ophiocordyceps perithecia embedded in an elongated stroma on the unilateralis associated with ‘‘zombie ants’’ the discov- dorsum of the ant, and they are thought to be ery of P. cf. lilacinum infecting bugs reveals that P. dispersed more successfully than if the ant had stayed lilacinum may be more diverse than previously within its nest and been dumped onto the refuse pile appreciated. within its nest or had simply fallen to the ground after death (Hughes 2012). The biting behavior of the ants Submitted 18 Aug 2013; accepted for publication 17 Jul 2014. and their tendency to be in plants above the forest 1 Corresponding author. E-mail: [email protected] floor are aberrant behaviors induced by the infection; 1065 1066 MYCOLOGIA uninfected ants do not normally hold leaves with their the legs contacted the plant on the tips of the trichomes mandibles. Biting the substrate maintains the ant in and spines that covered the stem or on the surface of the situ after it dies, giving the fungus time to produce an stem itself; and whether the bug’s mouthparts were inserted adhesive pad that more permanently binds the ant’s into the plant (with the protective labrum folded posteri- orly). Sample sizes are not equal for all legs; in some cases it body to the plant (Pontoppidan et al. 2009). was either not possible to check all legs without disturbing This report presents observations suggesting that the bug or some legs were missing. the fungus Purpureocillium cf. lilacinum modifies the The presence of fungus was confirmed in two dead bugs behavior of the pentatomid bug Edessa rufomarginata. found on the host plant that did not show visible fungal Other strains of P. lilacinum have been isolated from growth externally, by dissecting one (which proved to be soil, air and animals, including immunocompromised tightly packed with fungal hyphae) and by keeping the humans (Saghroun et al. 2013), nematodes and other in a humid environment for 2 d, after which fungal various insects, such as curculionid beetles, homop- hyphae emerged from its membranes. We use the term terans and lepidopteran larvae (Spatafora et al. 2007), ‘‘infected’’ in the descriptions below to indicate dead bugs and from a related bug, Edessa meditabunda (Humber with fungus. We noted no differences between male and female bugs and combine them in the descriptions. We kept 2007); one species of Ophiocordyceps, O. pentatomae several infected bugs in closed humid chambers for up to (Koval) (MycoBank MB504321) was isolated from a 2 wk after collection and noted changes in the morphology pentatomid bug in Russia (Sung et al. 2007b). of the
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