Difference between revisions of "Entomopathogenic fungi"

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Revision as of 17:36, 14 June 2019

A synopsis of the abundant widespread neotropical fungi Ophiocordyceps unilateralis (likely a group of species) from Wikipedia [1] provides an introduction to this topic:

Ophiocordyceps unilateralis is an entomopathogen, or insect-pathogenising fungus, discovered by the British naturalist Alfred Russel Wallace in 1859, and currently found predominantly in tropical forest ecosystems. O. unilateralis, also referred to as a zombie fungus, infects ants of the Camponotini tribe, with the full pathogenesis being characterized by alteration of the behavioral patterns of the infected ant. Infected hosts leave their canopy nests and foraging trails for the forest floor, an area with a temperature and humidity suitable for fungal growth; they then use their mandibles to affix themselves to a major vein on the underside of a leaf, where the host remains until its eventual death. The process leading to mortality takes 4–10 days, and includes a reproductive stage where fruiting bodies grow from the ant's head, rupturing to release the fungus's spores. O. unilateralis is in turn also susceptible to fungal infection itself, an occurrence which can limit its impact on ant populations, which has otherwise been known to devastate ant colonies.

The genus of ant infecting fungi were once all in the genus Cordyceps but most have been moved to the genus Ophiocordyceps (Sung et al. 2007).

Photo Gallery

  • Camponotus atriceps infected by Ophiocordyceps camponoti-atricipis, biting onto a leaf edge. (Photo by João P. M. Araújo)
  • Camponotus atriceps infected by Ophiocordyceps camponoti-atricipis biting onto a liana, after a heavy rain at Brazilian Amazon. (Photo by João P. M. Araújo)
  • Camponotus renggeri infected by Ophiocordyceps camponoti-renggeri, biting onto liana. The leg joints and antenna are covered by specialized cells that produce asexual spores that are transmitted by contact. The round structures (ascoma), suspended by the long stalks (stroma) produce sexual spores that will be released onto the forest 􀃓oor. (Photo by João P. M. Araújo)
  • Camponotus nidulans infected by Ophiocordyceps camponoti-nidulantis on its typical display where the antennae are spread in order to optimize the transmission of asexual spores produced along the antenna. Dead on a summit position, aiming to spread the sexual spores. (Photo by João P. M. Araújo)
  • Daceton armigerum infected by Ophiocordyceps dacetini. (Photo by João P. M. Araújo)
  • Paraponera clavata infected by Ophiocordycceps ponerinarum. In this association, the fungus leads the ant to climb up on a tree, to die attached to the trunk. (Photo by João P. M. Araújo)
  • Polyrhachis sp. infected by Ophiocordyceps buquetii, in Ghana. (Photo by João P. M. Araújo)
  • Paltothyreus tarsatus biting onto a green stem. Once infected by an Ophiocordyceps species (still undescribed), it climbs up to a vertical stem to die biting onto it. In this case, the fungus we see is actually a hyerparasite of the Ophiocordyceps fungus, which overcame it and procuced these torrubielloid sexual structures. (Photo by João P. M. Araújo)
  • Very tip of a palm leaf, showing Camponotus hippocrepis infected by Ophiocordyceps camponotihippocrepidis. (Photo by João P. M. Araújo)
  • Campontus bispinosus biting onto a palm spine, as it typically dies from infection of Ophiocordyceps camponotibispinosi. (Photo by João P. M. Araújo)
  • Camponotus floridanus attached to Spanish moss moments after the final manipulated biting behavior induced by Ophiocordyceps camponoti-floridani. Photo by Charissa de Bekker.
  • Likely killed by the fungus Desmidiospora myrmecophila. Photo by Michal Kukla.
  • Likely killed by the fungus Desmidiospora myrmecophila. Photo by Michal Kukla.
  • Likely killed by fungus Desmidiospora myrmecophila. Photo by Michal Kukla.
  • Camponotus ligniperda queen likely killed by the parasitic fungus Desmidiospora myrmecophila. Photo by Michal Kukla.

Fungal Species

Aegeritella superficialis

These fungi were first noted by Wisniewski in 1967 although their fungal nature was not proven then. The fungi grow over the cuticle like dark protuberances (= bulbils). On first sight, they look like dirt, and its form is usually a dome, rounded in perimeter, and up to 400 μm diameter. The number of bulbils may be from a single one to several hundred. The distribution of bulbils on the body of ants is heterogeneous, being more abundant at the rear part. The total number of bulbils is inversely related to ant size, with bigger ants having less bulbils than smaller ants. Bulbils have been detected in workers and queens.

The ant-fungus relationship has not been properly ascertained although a reduced life duration or activity level has been suggested. In a similar vein, Bałazy et al. note some workers with hundreds of bulbils, having immobilized bucal palps, all covered by hyphae. Nothing is known of the dynamics of infestation or transmission mechanisms of those enigmatic fungi, not even its phylogenetic position within the realm of Fungi.

See Espadaler & Santamaria (2012) for further details.

Aegeritella maroccana

These fungi were first noted by Wisniewski in 1967 although their fungal nature was not proven then. The fungi grow over the cuticle like dark protuberances (= bulbils). On first sight, they look like dirt, and its form is usually a dome, rounded in perimeter, and up to 400 μm diameter. The number of bulbils may be from a single one to several hundred. The distribution of bulbils on the body of ants is heterogeneous, being more abundant at the rear part. The total number of bulbils is inversely related to ant size, with bigger ants having less bulbils than smaller ants. Bulbils have been detected in workers and queens.

The ant-fungus relationship has not been properly ascertained although a reduced life duration or activity level has been suggested. In a similar vein, Bałazy et al. note some workers with hundreds of bulbils, having immobilized bucal palps, all covered by hyphae. Nothing is known of the dynamics of infestation or transmission mechanisms of those enigmatic fungi, not even its phylogenetic position within the realm of Fungi.

See Espadaler & Santamaria (2012) for further details.

Aegeritella roussillonensis

These fungi were first noted by Wisniewski in 1967 although their fungal nature was not proven then. The fungi grow over the cuticle like dark protuberances (= bulbils). On first sight, they look like dirt, and its form is usually a dome, rounded in perimeter, and up to 400 μm diameter. The number of bulbils may be from a single one to several hundred. The distribution of bulbils on the body of ants is heterogeneous, being more abundant at the rear part. The total number of bulbils is inversely related to ant size, with bigger ants having less bulbils than smaller ants. Bulbils have been detected in workers and queens.

The ant-fungus relationship has not been properly ascertained although a reduced life duration or activity level has been suggested. In a similar vein, Bałazy et al. note some workers with hundreds of bulbils, having immobilized bucal palps, all covered by hyphae. Nothing is known of the dynamics of infestation or transmission mechanisms of those enigmatic fungi, not even its phylogenetic position within the realm of Fungi.

See Espadaler & Santamaria (2012) for further details.

Aegeritella superficialis

Aegeritella tuberculata

These fungi were first noted by Wisniewski in 1967 although their fungal nature was not proven then. The fungi grow over the cuticle like dark protuberances (= bulbils). On first sight, they look like dirt, and its form is usually a dome, rounded in perimeter, and up to 400 μm diameter. The number of bulbils may be from a single one to several hundred. The distribution of bulbils on the body of ants is heterogeneous, being more abundant at the rear part. The total number of bulbils is inversely related to ant size, with bigger ants having less bulbils than smaller ants. Bulbils have been detected in workers and queens.

The ant-fungus relationship has not been properly ascertained although a reduced life duration or activity level has been suggested. In a similar vein, Bałazy et al. note some workers with hundreds of bulbils, having immobilized bucal palps, all covered by hyphae. Nothing is known of the dynamics of infestation or transmission mechanisms of those enigmatic fungi, not even its phylogenetic position within the realm of Fungi.

See Espadaler & Santamaria (2012) for further details.

Hormiscium myrmecophilum

The species was described from an Amazonian Pseudomyrmex and remained elusive since its original description until it was found in Europe eighty years later. The filamentous, somewhat dichotomic thallus is undifferentiated and grows directly out of different parts of the ant body, without any apparent attaching structure. Mycelia have a maximum length of 163 μm and constant width of 10 μm. Spores are unknown.

See Espadaler & Santamaria (2012) for further details.

Laboulbeniales

Laboulbeniales - fungi found growing on adult ants; also associated with other arthropods

Laboulbenia camponoti

Under the binocular, the thallus of this species looks like a distorted ant hair and is found all over the body, albeit more abundant in dorsal surfaces and external surface of legs. Density is much lower than in other ant-specific Laboulbeniales. In the Holarctic, it has been detected exclusively in Camponotus species, all six from the subgenus Tanaemyrmex

See Espadaler & Santamaria (2012) for further details.

Laboulbenia formicarum

This is one of the smallest Laboulbeniales species (up to 0.3mm total length). Thalli can be extremely abundant on infested workers, which go foraging seemingly unaffected amid noninfested workers.

See Espadaler & Santamaria (2012) for further details.

Myrmicinosporidium

This fungi were first noted by Holldobler although it was formally described later, in 1933. Its phylogenetic position is still unknown, and its true fungal nature has been only proved recently. Infested ants are usually well detected because the darker spores are visible through the integument; spores number may be very low, but usually they reach more than one hundred in a single ant. The caveat here is that the fungus may be much difficult to detect in ants having fuscous or black colouration. As a consequence, host range is probably biased. The usual aspect of concave spores, with a bow-like depression, is an artefact of fixation in alcohol.

Although the infested workers are almost certainly killed by the fungus when spores begin producing hyphae, life span seems not to be curtailed. Infested workers seem scarcely affected in its normal behaviour, and infested queens may participate in swarming flights and show normal fertility. Males have been found infected too. Life cycle and mode on infestation are unknown although reports of Myrmicinosporidium from callow workers in Pogonomyrmex badius indicate that the infection is carried over from immature stages. It is perhaps significant that the majority of diseased ants were collected in late summer and fall. After hibernation, those infected workers die. Its geographical distribution is ample as is also the range of hosts.

See Espadaler & Santamaria (2012) for further details.

Rickia wasmannii

This species is extremely characteristic in its microscopic morphological aspect and is limited to several species of Myrmica. Infested ants may harbour from a few thalli to several hundred thalli all over the body. Heavy infestations are visible to the naked eye and give a greyish shade, a pulverulent image to living individuals. Worker and queens may be infested.

See Espadaler & Santamaria (2012) for further details.

Ant Hosts

See also the list of known hosts.

Selected ant-fungus relationships
Ant Fungus Location citation
Atta cephalotes Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Bothroponera pachyderma Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Camponotus aberrans Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus americanus Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus atriceps Ophiocordyceps camponoti-atricipis South America Shrestha et al. 2017
Camponotus atriceps Ophiocordyceps lloydii South America Shrestha et al. 2017
Camponotus atriceps Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus balzani Ophiocordyceps camponoti-balzani South America Shrestha et al. 2017
Camponotus bispinosus Ophiocordyceps camponoti-bispinosi South America Shrestha et al. 2017
Camponotus brutus Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus buchneri Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus cruentatus Ophiocordyceps halabalaensis Asia Shrestha et al. 2017
Camponotus cruentatus Ophiocordyceps ridleyi Asia Shrestha et al. 2017
Camponotus simillimus indianus Ophiocordyceps camponoti-indiani South America Shrestha et al. 2017
Camponotus japonicus Ophiocordyceps formicarum Asia Shrestha et al. 2017
Camponotus sanctaefidei leonhardi Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus ligniperda Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus melanoticus Ophiocordyceps camponoti-melanotici South America Shrestha et al. 2017
Camponotus novogranadensis Ophiocordyceps camponoti-novogranadensis South America Shrestha et al. 2017
Camponotus obscuripes Ophiocordyceps formicarum Asia Shrestha et al. 2017
Camponotus obscuripes Ophiocordyceps pulvinata Asia Shrestha et al. 2017
Camponotus obscuripes Ophiocordyceps sessilis Asia Shrestha et al. 2017
Camponotus paradoxus Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus pennsylvanicus Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus piceus Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Camponotus rufipes Ophiocordyceps camponoti-rufipedis South America Shrestha et al. 2017
Camponotus saundersi(?) Ophiocordyceps camponoti-saundersi Asia Shrestha et al. 2017
Camponotus saundersi(?) Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus sericeiventris Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Camponotus sp. Ophiocordyceps irangiensis Africa and Asia Shrestha et al. 2017
Camponotus sp. Ophiocordyceps japonensis Asia Shrestha et al. 2017
Camponotus sp. Ophiocordyceps lloydii var. binata South America Shrestha et al. 2017
Camponotus sp. Ophiocordyceps rami Asia Shrestha et al. 2017
Camponotus sp. Ophiocordyceps septa Asia Shrestha et al. 2017
Camponotus vividus Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Cephalotes atratus Ophiocordyceps cucumispora South America Shrestha et al. 2017
Cephalotes atratus Ophiocordyceps kniphofioides South America Shrestha et al. 2017
Cephalotes atratus Ophiocordyceps evansii South America Sanjuan et al. 2015
Dinoponera gigantea Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Dolichoderus attelaboides Ophiocordyceps cucumispora var. dolichoderi South America Shrestha et al. 2017
Dolichoderus attelaboides Ophiocordyceps kniphofioides var. dolichoderi South America Shrestha et al. 2017
Dolichoderus bispinosus Ophiocordyceps kniphofioides var. monacidis South America Shrestha et al. 2017
Echinopla melanarctos Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Formica fusca Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Formica polyctena Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Formica pratensis Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Formica rufa Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Formica sanguinea Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Formica sp. Ophiocordyceps subunilateralis South America Shrestha et al. 2017
Megaponera analis Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Megaponera analis Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Myrmica rubra Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Odontomachus sp. Cordyceps morakotii Asia Shrestha et al. 2017
Pachycondyla crassinoda Ophiocordyceps australis South America Sanjuan et al. 2015
Pachycondyla harpax Ophiocordyceps evansii South America Sanjuan et al. 2015
Pachycondyla impressa Ophiocordyceps evansii South America Shrestha et al. 2017
Pachycondyla striata Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Paltothyreus tarsatus Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Paltothyreus tarsatus Cordyceps carnata Africa Shrestha et al. 2017
Paltothyreus tarsatus Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Paraponera clavata Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Paraponera clavata Cordyceps doiana South America Shrestha et al. 2017
Paraponera clavata Ophiocordyceps ponerinarum South America Sanjuan et al. 2015
Phrynoponera sp. Ophiocordyceps australis Africa and South America Shrestha et al. 2017
Polyrhachis armata Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis decemdentata Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis fissa Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis furcata Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis hippomanes Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis laboriosa Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis lamellidens Ophiocordyceps unilateralis var. clavata Asia Shrestha et al. 2017
Polyrhachis latharis Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis latispina Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis militaris Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis monista Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis proxima Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis revoili Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis rufofemorata Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
Polyrhachis sp. Ophiocordyceps irangiensis Africa and Asia Shrestha et al. 2017
Polyrhachis sp. Ophiocordyceps myrmecophila Asia, Europe, North and South America Shrestha et al. 2017
Polyrhachis sulcata Ophiocordyceps unilaterialis Asia, North and South America Shrestha et al. 2017
xxx Cordyceps myrmecogena Asia Shrestha et al. 2017
xxx Cordyceps pilifera South America Shrestha et al. 2017

References

  • Andersen, S.B., Ferrari, M., Evans, H.C., Elliot, S.L., Boomsma, J.J., Hughes, D.P. 2012. Disease dynamics in a specialized parasite of ant societies. PLoS ONE 7(5): e36352 (DOI 10.1371/journal.pone.0036352).
  • Andersen, S., Hughes, D. 2012. Host specificity of parasite manipulation - Zombie ant death location in Thailand vs. Brazil. Communicative & Integrative Biology 5: 163–165 (DOI 10.4161/cib.18712).
  • Araújo, J.P.M., Evans, H.C., Kepler, R., Hughes, D.P. 2018. Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. Studies in Mycology 90: 119–160 (DOI 10.1016/j.simyco.2017.12.002).
  • Espadaler, X., Santamaria, S. 2012. Ecto- and Endoparasitic Fungi on Ants from the Holarctic Region. Psyche Article ID 168478, 10 pages (doi:10.1155/2012/168478).
  • Evans, H.C., Elliot, S.L., Hughes, D.P. 2011. Ophiocordyceps unilateralis. A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? Communicative & Integrative Biology 4: 598-602 (DOI 10.4161/cib.4.5.16721).
  • Evans, H.C., Elliot, S.L., Hughes, D.P. 2011. Hidden diversity behind the zombie-ant fungus Ophiocordyceps unilateralis: Four new species described from carpenter ants in Minas Gerais, Brazil. PLoS ONE 6(3): e17024 (DOI 10.1371/journal.pone.0017024).
  • Gomez, K., X. Espadaler, and S. Santamaria. 2017. First Record of an Epizoic Laboulbenia (Fungi: Laboulbeniales) on Ants (Hymenoptera: Formicidae) in Africa. Sociobiology. 64:155-158. doi:10.13102/sociobiology.v64i2.1532
  • Loreto, R. G., Araújo, J. P. M., Kepler, R. M., Fleming, K. R., Moreau, C. S., & Hughes, D. P. (2018) Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions. Evolution. (DOI: 10.1111/evo.13489).
  • Loreto, R.G., Elliot, S.L., Freitas, M.L.R., Pereira, T.M., Hughes, D.P. 2014. Long-term disease dynamics for a specialized parasite of ant societies: A field study. PLoS ONE 9(8): e103516 (DOI 10.1371/journal.pone.0103516).
  • Sanjuan, T. I., A. E. Franco-Molano, R. M. Kepler, J. W. Spatafora, J. Tabima, A. M. Vasco-Palacios, and S. Restrepo. 2015. Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps. Fungal Biology. 119:901-916. doi:10.1016/j.funbio.2015.06.010
  • Shrestha, B., E. Tanaka, M. W. Hyun, J. G. Han, C. S. Kim, J. W. Jo, S. K. Han, J. Oh, J. M. Sung, and G. H. Sung. 2017. Mycosphere Essay 19. Cordyceps species parasitizing hymenopteran and hemipteran insects. Mycosphere. 8:1424-1442. doi:10.5943/mycosphere/8/9/8
  • Sung, G.-H., N. L. Hywel-Jones, J.-M. Sung, J. J. Luangsa-ard, B. Shrestha, and J. W. Spatafora. 2007. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology. 57:5-59. doi:10.3114/sim.2007.57.01
  • Sobczak, J. F., L. F. A. Costa, J. Carvalho, G. Salgado-Neto, J. Moura-Sobczak, and Y. F. Messas. 2017. The zombie ants parasitized by the fungi Ophiocordyceps camponotiatricipis (Hypocreales: Ophiocordycipitaceae): new occurrence and natural history. Mycosphere. 8:1261-1266. doi:10.5943/mycosphere/8/9/1