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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
1
Department 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
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
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 plate (the sexual stage or teleomorph) do know, from our preliminary study in described on Polyrhachis ants infected
produced laterally on a stalk or clava reference 6, is that there is a species com- with O. unilateralis s.l. from West Africa.8
emerging from behind the head of the plex of macroscopically-similar pathogens From studies of other entomopatho-
ant—the emblematic feature of the zom- (O. unilateralis s.l.) producing not only genic fungi,13 we know that there are also
bie-ant fungus—buried within the stroma sexual stages (teleomorphs), but also asex- critical host-recognition factors to trigger
are the flask-shaped, thick-walled asco- ual stages (anamorphs), that differ widely the formation of the limpet-like appres-
mata producing sac-like structures called in form and function, each equipped with sorium: the “beach-head” from which the
asci. Each of these is fitted with a special- in-built insurance mechanisms to increase infective hypha drills through the com-
ized firing cap containing the missiles: the chances of success if the primary mis- plex multi-layered exoskeleton using a
large (from 80 > 200 μm long) multisep- siles fail to hit their targets. combination of mechanical pressure and
tate, sexual spores (ascospores). These are Currently, we are working on docu- enzymes (chitinase, lipase and protease).
released under pressure from the launch menting the diverse strategies employed We now have circumstantial evidence
pad—the ant cadaver—typically, affixed by this newly-delimited complex of from our work with freshly-released asco-
to the underside of a leaf on an under- Ophiocordyceps species to reach new spores of Ophiocordyceps from different
storey forest shrub. We also assume that hosts. Thus, we will be in a better posi- Camponotus hosts, which suggests that
the system is designed to operate when tion to re-interpret the taxonomic, as well there are also sophisticated signals between