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Ophiocordyceps Unilateralis: a Keystone Species for Unraveling Ecosystem Functioning and Biodiversity of Fungi in Tropical Forests?

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Ophiocordyceps Unilateralis: a Keystone Species for Unraveling Ecosystem Functioning and Biodiversity of Fungi in Tropical Forests? Communicative & Integrative Biology ISSN: (Print) 1942-0889 (Online) Journal homepage: https://www.tandfonline.com/loi/kcib20 Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? Harry C. Evans, Simon L. Elliot & David P. Hughes To cite this article: Harry C. Evans, Simon L. Elliot & David P. Hughes (2011) Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?, Communicative & Integrative Biology, 4:5, 598-602, DOI: 10.4161/cib.16721 To link to this article: https://doi.org/10.4161/cib.16721 Copyright © 2011 Landes Bioscience Published online: 01 Sep 2011. Submit your article to this journal Article views: 1907 View related articles Citing articles: 23 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=kcib20 Communicative & Integrative Biology 4:5, 598-602; September/October 2011; ©2011 Landes Bioscience Ophiocordyceps unilateralis A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? Harry C. Evans,1,* Simon L. Elliot1 and David P. Hughes2 1Department of Entomology; Universidade Federal de Viçosa (UFV); Viçosa; Minas Gerais, Brazil; 2Department of Entomology and Department of Biology; Penn State University; University Park; PA USA phiocordyceps unilateralis (Ascomy- thus far4—this group of organisms still O cota: Hypocreales) is a specialized receives relatively little press in terms of parasite that infects, manipulates and its biodiversity and the pivotal role it plays kills formicine ants, predominantly in ecosystem functioning. Recently, how- in tropical forest ecosystems. We have ever, the subject has been revisited within reported previously, based on a prelimi- the context of microbes associated with nary study in remnant Atlantic Forest beetles.5 Of the near one million species ©2011 Landesin Minas Gerais (Brazil), thatBioscience. O. uni- of insects that have been described, beetles lateralis represents a species complex. are by far the most numerous. However, in On each of the four species of infected terms of overall biodiversity, “beetles may carpenter ant (Camponotus) collected, represent just the tip of the iceberg,”5 since the fungus—characterized macroscopi- “A single beetle species itself can house Do notcally by a singledistribute. stalk arising from the an entire community of associated [pre- dorsal neck region on which the sexual dominantly fungal] species.”5 The prem- structures (stromatal plates) are borne ise put forward is that microbial diversity laterally—can readily be distinguished and ecology have been neglected in favor both microscopically and functionally. of other disciplines, especially in the area Here, we describe and discuss the biol- of biological mutualisms and antagonisms ogy, life cycle and infection strategies of between macro- and micro-organisms.1,5 O. unilateralis s.l. and hypothesize that An illustration of Ophiocordyceps unilate- there may be hundreds of species within ralis on its ant host was chosen by the the complex parasitizing formicine ants latter authors to emphasize their point, worldwide. We then address the diversity that—for most of the insect-microbial within related hypocrealean fungi, with interactions—the ecology and, more Key words: zombie ants, particular reference to symbionts (mutu- pragmatically, the pharmacological prop- Ophiocordyceps, Hypocreales, tropical alists through to parasites), and argue erties of the microbes involved remain forests, fungal diversity, symbionts that the widely-quoted total of extant unknown. Submitted: 05/30/11 fungi (1.5 million species) may be grossly We have now shown6 that the inter- underestimated. actions between and its Accepted: 05/31/11 O. unilateralis Camponotus hosts are much more com- DOI: 10.4161/cib.4.5.16721 “How many species?” has been the ral- plex than has previously been supposed.7-10 *Correspondence to: Harry C. Evans; lying cry for systematists and ecologists, It had been posited that the morphologi- Email: [email protected] championing the interests of their partic- cal variation noted in global collections ular organismic group, since the question of this fungus from formicine ants “is Addendum to: Evans HC, Elliot SL, Hughes DP. was posed over 30 years ago.1,2 Although it undoubtedly a consequence of its wide geo- Hidden diversity behind the zombie-ant fungus 8 Ophiocordyceps unilateralis: four new species was answered soon after for the Kingdom graphic range,” and that this would best described from carpenter ants in Minas Gerais, Fungi3—with an estimated total in the be resolved at the varietal level, as with the Brazil. PLoS One 2011; 6:17024, PMID: 21399679; region of 1.5 million species, of which, less Ophiocordyceps species complexes associ- DOI: 0.1371/journal.pone than 100,000 (~7%) have been described, ated with myrmicine and ponerine ants.11,12 598 Communicative & Integrative Biology Volume 4 Issue 5 ARTICLE ADDENDUM ©2011 Landes Bioscience. Do not distribute. Figure 1. Most common carpenter ant species infected with Ophiocordyceps s.l. in Atlantic rain forest in Minas Gerais, Brazil. (A) Sample area, Mata do Paraíso, near Viçosa, a small (300 ha) reserve of remnant forest; (B) Camponotus rufipes showing early stage in development of Ophiocordyceps camponoti-rufipedis with a single asexual synnema arising from the dorsal pronotum, the ant had died biting into a plastic label identifying a disease- outbreak site, (bar = 1.5 mm); (C) Camponotus balzani with mature Ophiocordyceps camponoti-balzani, showing the elaborate, branching, antler-like synnema/clava bearing scattered ascostromata with prominent semi-erumpent ascomata (compare E, bar = 1.0 mm); (D) Camponotus rufipes in more typical death position biting into leaf margin, with unbranched synnema/clava producing groups of stromata (arrow, bar = 4 mm); (E) inset, shows the ascomatal necks with the ascomata buried within the stroma (bar = 0.4 mm). However, working in remnant fragments of arthropod population dynamics and, holis- fungal pathogen must attach securely Atlantic Forest (Mata Atlántica) in Minas tically, in ecosystem functioning. to the arthropod exoskeleton and pen- Gerais, Brazil,6 we discovered a far more etrate it—avoiding or suppressing host complex scenario: one that will necessitate The Host-Pathogen System: defences—then, control the behavior of a re-evaluation of the diversity of species A Diversity of Interactions the host before killing it; and finally, it within Ophiocordyceps unilateralis s.l., as must protect the cadaver from microbial well as in the genus Ophiocordyceps and As has been emphasized previously in and scavenger attack. What is not gener- related genera of Hypocreales—and, eventu- reference 2 and 5, insect-microbial asso- ally realized—certainly not by drug com- ally, within the kingdom fungi—with par- ciations have been a source of useful panies—is that such coevolved fungi are ticular reference to tropical forests. These drugs: although, “The pharmacologi- pleiomorphic, with well-defined parasitic, ecosystems harbor a hyperdiversity of cal properties of the ant-infesting fun- necrotrophic and saprophytic phases: fungi, especially when we consider they are gus [O. unilateralis s.l.] have yet to be each one morphologically, genetically found as symbionts (ranging from mutual- investigated.”5 What can we expect from and physiologically distinct. Only now, ists to parasites) of the extremely diverse such specialized fungi, and from related are we beginning to try to understand the flora and entomofauna, and even of other entomopathogenic Hypocreales, in gen- mechanisms and the biochemical path- fungi. Based on such studies, it may also eral? Throughout the life cycle, there are ways that drive these systems. be possible to better interpret their role in unique challenges that must be met by Our initial studies are focused on equally unique metabolic activities. The investigating the form and function of www.landesbioscience.com Communicative & Integrative Biology 599 ©2011 Landes Bioscience. Do not distribute. Figure 2. Variations on a theme. (A) Ascospore of Ophiocordyceps camponoti-rufipedis germinating to produce secondary spores (capilliconidia) on needle-like capilliconidiophores (bar = 30 μ); (B) Ascospore of O. camponoti-melanotici producing true Hirsutella phialide with swollen base tapering to a needle-like neck (bar = 15 μm); (C) Ascospore of O. camponoti-balzani becoming swollen with bead-like cells and the formation centrally of an appressorial-like structure (bar = 30 μm); (D) Ascospore of an un-named Ophiocordyceps sp. from Camponotus atriceps producing numerous swollen side branches of unknown function (bar = 30 μm); (E and F) Two undescribed, specialized mycoparasites on Ophiocordyceps illustrating the biodiver- sity and complexity associated with the system (E, bar = 2 mm; F, bar = 2 mm). the weaponry deployed by the pathogen ant activity is at its peak and the potential as the ecological significance of the world- (O. unilateralis s.l.) to breach the ant host’s targets are in range and, therefore, that wide collections of the zombie-ant fun- formidable defenses. We suppose that the microclimatic factors (light, temperature, gus, especially of the somewhat bizarre, heavy armament “of choice” is the stroma- humidity) will play a crucial role. What we multiple asexual stages (synanamorphs) tal
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