Species of Laboulbeniales fungi parasitic on some common Indian insects: Isolation, visualization and characterization by Scanning Electron Micrographs (SEM)
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Abstract
The Laboulbeniales are a group of lesser-known fungi. They occur as ectoparasites on the exoskeleton of various arthropod species, mainly beetles, cockroaches, ants, dipterans and a few millipede genera appearing as hairs/bristles coming out of their cuticle. They are small, non-mycelial fungi forming compact multicellular thalli, starting from a two-celled sheathed ascospore which continues to envelop the mature thallus. The fungi, being obligate, spend their entire life cycle on their insect hosts. The present study attempted to locate the Laboulbeniales fungi in the common insects of India, isolate them and identify them based on morphology. Different species of insects; Carabid beetles - Stenolophus sp., Bembidion sp., Black ants - Camponotus sp., and Earwigs - Labidura riparia; were collected from different habitats of damp garden soil, river banks, light sources and entomological collection museum situated as different sites New Delhi. The insects were scrutinized for the presence of fungi through light and scanning electron microscopy. The morphological features of each fungus were recorded, and the species were characterized. The studies showed the presence of Laboulbenia anaplogenii and L. stenolophi on the legs of Stenolophus sp.; L. egens on Bembidion sp. legs; L. camponoti on the wings of black ants and Dimeromyces anisolabis on the legs of earwigs. The identification was made primarily based on the size, shape and structure of basal foot, receptacles, antheridia and foot of the thallus or it’s remnant scar found on the insect cuticle. This is the first Indian report of conducting scanning imaging of the Laboulbeniales fungi.
Article Details
Article Details
Keywords
Fungi, Laboulbeniales, Scanning study, Thallus
References
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Boucias, D.G. & Pendland, J.C. (1991). Attachment of mycopathogens to cuticle: the initial event of mycoses in arthropod hosts. In: Garry, T.C. & Hoch, H.C. (Eds.): The fungal spore and disease initiation in plants and animals, Plenum Press, New York, NY, and London, UK, pp. 101-127.
Csősz S, Rádai, Z., Tartally, A., Ballai, L.E. & Báthori, F. (2021). Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants. Scientific. Reports, 11, 14355. https://doi.org/10.1038/s41598-021-93583-0.
De Kesel, A. (1993). Relations between host population density and spore transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales) from Pogonus chalceus (Coleoptera, Carabidae). Belgian Journal of Botany, 126, 155–163.
De Kesel, A. (1995). Relative importance of direct and indirect infection in the transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales). Belgian Journal of Botany, 128, 124–130.
De Kesel, A. (1996). Host specificity and habitat preference of Laboulbenia slackensis. Mycologia, 88, 565–573.
Enghoff, H. (2017). A new East African genus of spirostreptid millipedes (Diplopoda, Spirostreptida, Spirostreptidae), with notes on their fungal ectoparasite Rickia gigas. Zootaxa, 4273(4), 501–530. https://doi.org/10.11646/zootaxa.4273.4.3.
Haelewaters, D. (2012). The first record of Laboulbeniales (Fungi, Ascomycota) on Ants (Hymenoptera, Formicidae) in the Netherlands. Ascomycete.Org, 4, 65-69.
Haelewaters, D., Kesel, A.D., Gorczak, M., Bao, K., Gort, G., Zhao, S.Y. & Pfister, D.H. (2019). Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and Other Localities): species parasitizing carabidae, and the Laboulbenia flagellata species complex. Research at the Boston Harbor Islands NRA, Northeastern Naturalist, 25(Special Issue 9): 110–149.
Haelewaters, D., Hiller, T., Kemp, E.A., van Wielink, P.S., Shapiro-Ilan, D.I., Aime, C.M., Nadvěd, O., Pfister, D.H. & Cottrell, T.E. (2020a). Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. Peer J, 8, e10110. https://doi.org/10.7717%2Fpeerj.10110
Haelewaters, D., Dima, B., Abdel-Hafiz, B.I.I., et al., (2020b). Fungal systematics and evolution: FUSE 6. Sydowia 72, 231–356.
Haelewaters, D., Gorczak, M., Kaishian, P., De Kesel, A. & Blackwell, M. (2021) Laboulbeniomycetes, enigmatic fungi with a turbulent taxonomic history. Encylopedia of Mycology, 1, 263-283. https://doi.org/10.1016/B978-0-12-819990-9.00049-4
Kaishian, P.J. (2021). Insects and their Laboulbeniales (Ascomycota, Fungi) of Lake Eustis and Emeralda Marsh Conservation Area: A case study on urbanization and diversity. Ecology and Evolution, 11(23), 16618-16633. https://doi.org/10.1002/ece3.8246
Kaishian, P. & Weir, A. (2018). New species of Prolixandromyces (Laboulbeniales) from South America. Mycologia, 110(1), 222-229. https://doi.org/10.1080/00275514.2 017.1419779.
Kaur, S., Pathak, A. & Mukerji, K.G. (1993). Studies on Indian Laboulbeniomycetes I. Three unrecorded species of the genus Laboulbenia Mont et Robin. Cryptogamic Botany, 3, 357-360.
Kaur, S. & Mukerji, K.G (1995). Studies on Indian Laboulbeniales IV. Three species of laboulbenia. Mycoscience, 36(3), 311-314.
Kaur, S. & Mukerji K.G. (1996a). Studies on Indian Laboulbeniales II, Three unrecorded species. Nova Hedwigia, 61, 111-116.
Kaur, S. & Mukerji K.G. (1996b). Studies on Indian Laboulbeniales III Three unrecorded dioecious genera. Mycoscience, 37, 61-64.
Kaur, S. & Mukerji, K.G. (2006). The Laboulbeniales (Ascomycetes): distribution and host parasite relationships. Current concepts in botany. Mukerji, K.G. & Manoharachary, C. (Ed.), I. K. International Publishing House Pvt. Ltd., New Delhi, pp. 19-35.
Meola, S. & Devaney, J. (1976). Parasitism of mallophaga by Trenomyces histophtorus. Journal of Invertebrate Pathology, 28. 195–201. https://doi.org/10.1016/0022-2011(76)90122-1
Narang, A., Shukla, A. & Kaur, S. (2023). Developmental studies of Indian Laboulbeniales - Dimeromyces anisolabis (Ascomycota, Laboulbeniomycetes). Kavaka, 59(2), 85-91. https://doi.org/10.36460/Kavaka/59/2/2023/85-91
Pathak, A. & Mukherji, K.G. (1997). Studies on Indian Laboulbeniales VIII. Two neew species. Phytomorphology, 47(3), 333-337.
Reboleira, A.S.P.S., Enghoff, H. & Santamaria, S. (2018) Novelty upon novelty visualized by rotational scanning electron micrographs (rSEM): Laboulbeniales on the millipede order Chordeumatida. PLoS One, 13(11), e0206900. https://doi.org/10.1371/journal.pone.0206900
Reboleira, A.S.P.S., Moritz, L., Santamaria, S. & Enghoff, H. (2021). Penetrative and non-penetrative interaction between Laboulbeniales fungi and their arthropod hosts. Scientific Reports, 11, 22170. https://doi.org/10.1038/s41598-021-01729-x
Santamaria, S. (2006). New or interesting Laboulbeniales (Fungi, Ascomycota) from Spain, V. Nova Hedwigia, 82(3–4), 349–363. https://doi.org/10.1127/0029-5035/2006/0082-0349.
Santamaria, S., Enghoff, H. & Reboleira, A.S.P.S. (2014). Laboulbeniales on millipedes: the genera Diplopodomyces and Troglomyces. Mycologia, 106(5), 1027–1038.https://doi.org/10.3852/13-381.
Santamaria, S., Enghoff, H., Gruber, J. & Reboleira, A.S.P.S. (2017). First Laboulbeniales from harvestmen: the new genus Opilionomyces. Phytotaxa, 305(4), 285–29 https://doi.org/10.11646/phytotaxa.305.4.4.
Santamaria, S., Enghoff, H. & Reboleira, A.S.P.S. (2018). New species of Troglomyces and Diplopo domyces (Laboulbeniales, Ascomycota) from millipedes (Diplopoda). European Journal of Taxonomy, 429, 1–20. https://doi.org/10.5852/ejt.2018.429.
Thaxter, R. (1895) Notes on Laboulbeniaceae with description of new species. Proceedings of the American Academy of Arts and Science, 30, 467-481.
Thaxter, R. (1896) New species of Laboulbeniaceae from various localities. Proceedings of the American Academy of Arts and Science, 12,187-429.
Thaxter, R. (1899) Preliminary diagnoses of new species of Laboulbeniaceae I. Proceedings of the American Academy of Arts and Science, 35, 407-450.
Thaxter, R. (1908) Contribution towards a monograph of the Laboulbeniaceae, Part II. Memoirs of the American Academy of Arts and Science, 13, 217-469.
Thaxter, R. (1931) Contribution towards a monograph of the Laboulbeniaceae, Part V. Memoirs of the American Academy of Arts and Science, 16, 1-435.
Thomas, C.D. (2000). Dispersal and extinction in fragmented landscapes. Proceedings of the Royal Society of London B, 267, 139–145.
Tragust, S, Tartally. A, Espadaler. X & Billen. J (2016) Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae). Myrmecology News, 23, 81-89.
Warren, M., Hill, J., Thomas, J., Asher, J., Fox, R., Huntley, B., Roy, D.B., Telfer, M.G., Jeffcoate, S., Harding, P., Jeffcoate, G., Willis, S.G., Greatorex‐Davies, J.N., Moss, D., & Thomas, C.D. (2001). Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature, 414, 65–69.
Weir, A. & Hammond, P.M. (1997). Laboulbeniales on beetles: Host utilization patterns and species richness of the parasites. Biodiversity and Conservation, 6, 701–719.
Benjamin, R.K. (1971). Introduction and supplement to Roland Thaxter's contribution towards a monograph of the Laboulbeniaceae. Bibliography of Mycology, 30, 1-155.
Billen, J. (2009). Diversity and morphology of exocrine glands in ants. Annals XIX Symposium of Myrmecology. Lectures Part 2. – Universidade Federal de Ouro Preto, Ouro Preto, Brazil, 6 pp.
Blackwell, M., Haelewaters, D. & Pfister, D.H. (2020). Laboulbeniomycetes: evolution, natural history, and Thaxter’s final word. Mycologia, 112(6), 1192–1202. https://doi.org/10.1080/00275514.2020.1718442.
Boucias, D.G. & Pendland, J.C. (1991). Attachment of mycopathogens to cuticle: the initial event of mycoses in arthropod hosts. In: Garry, T.C. & Hoch, H.C. (Eds.): The fungal spore and disease initiation in plants and animals, Plenum Press, New York, NY, and London, UK, pp. 101-127.
Csősz S, Rádai, Z., Tartally, A., Ballai, L.E. & Báthori, F. (2021). Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants. Scientific. Reports, 11, 14355. https://doi.org/10.1038/s41598-021-93583-0.
De Kesel, A. (1993). Relations between host population density and spore transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales) from Pogonus chalceus (Coleoptera, Carabidae). Belgian Journal of Botany, 126, 155–163.
De Kesel, A. (1995). Relative importance of direct and indirect infection in the transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales). Belgian Journal of Botany, 128, 124–130.
De Kesel, A. (1996). Host specificity and habitat preference of Laboulbenia slackensis. Mycologia, 88, 565–573.
Enghoff, H. (2017). A new East African genus of spirostreptid millipedes (Diplopoda, Spirostreptida, Spirostreptidae), with notes on their fungal ectoparasite Rickia gigas. Zootaxa, 4273(4), 501–530. https://doi.org/10.11646/zootaxa.4273.4.3.
Haelewaters, D. (2012). The first record of Laboulbeniales (Fungi, Ascomycota) on Ants (Hymenoptera, Formicidae) in the Netherlands. Ascomycete.Org, 4, 65-69.
Haelewaters, D., Kesel, A.D., Gorczak, M., Bao, K., Gort, G., Zhao, S.Y. & Pfister, D.H. (2019). Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and Other Localities): species parasitizing carabidae, and the Laboulbenia flagellata species complex. Research at the Boston Harbor Islands NRA, Northeastern Naturalist, 25(Special Issue 9): 110–149.
Haelewaters, D., Hiller, T., Kemp, E.A., van Wielink, P.S., Shapiro-Ilan, D.I., Aime, C.M., Nadvěd, O., Pfister, D.H. & Cottrell, T.E. (2020a). Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. Peer J, 8, e10110. https://doi.org/10.7717%2Fpeerj.10110
Haelewaters, D., Dima, B., Abdel-Hafiz, B.I.I., et al., (2020b). Fungal systematics and evolution: FUSE 6. Sydowia 72, 231–356.
Haelewaters, D., Gorczak, M., Kaishian, P., De Kesel, A. & Blackwell, M. (2021) Laboulbeniomycetes, enigmatic fungi with a turbulent taxonomic history. Encylopedia of Mycology, 1, 263-283. https://doi.org/10.1016/B978-0-12-819990-9.00049-4
Kaishian, P.J. (2021). Insects and their Laboulbeniales (Ascomycota, Fungi) of Lake Eustis and Emeralda Marsh Conservation Area: A case study on urbanization and diversity. Ecology and Evolution, 11(23), 16618-16633. https://doi.org/10.1002/ece3.8246
Kaishian, P. & Weir, A. (2018). New species of Prolixandromyces (Laboulbeniales) from South America. Mycologia, 110(1), 222-229. https://doi.org/10.1080/00275514.2 017.1419779.
Kaur, S., Pathak, A. & Mukerji, K.G. (1993). Studies on Indian Laboulbeniomycetes I. Three unrecorded species of the genus Laboulbenia Mont et Robin. Cryptogamic Botany, 3, 357-360.
Kaur, S. & Mukerji, K.G (1995). Studies on Indian Laboulbeniales IV. Three species of laboulbenia. Mycoscience, 36(3), 311-314.
Kaur, S. & Mukerji K.G. (1996a). Studies on Indian Laboulbeniales II, Three unrecorded species. Nova Hedwigia, 61, 111-116.
Kaur, S. & Mukerji K.G. (1996b). Studies on Indian Laboulbeniales III Three unrecorded dioecious genera. Mycoscience, 37, 61-64.
Kaur, S. & Mukerji, K.G. (2006). The Laboulbeniales (Ascomycetes): distribution and host parasite relationships. Current concepts in botany. Mukerji, K.G. & Manoharachary, C. (Ed.), I. K. International Publishing House Pvt. Ltd., New Delhi, pp. 19-35.
Meola, S. & Devaney, J. (1976). Parasitism of mallophaga by Trenomyces histophtorus. Journal of Invertebrate Pathology, 28. 195–201. https://doi.org/10.1016/0022-2011(76)90122-1
Narang, A., Shukla, A. & Kaur, S. (2023). Developmental studies of Indian Laboulbeniales - Dimeromyces anisolabis (Ascomycota, Laboulbeniomycetes). Kavaka, 59(2), 85-91. https://doi.org/10.36460/Kavaka/59/2/2023/85-91
Pathak, A. & Mukherji, K.G. (1997). Studies on Indian Laboulbeniales VIII. Two neew species. Phytomorphology, 47(3), 333-337.
Reboleira, A.S.P.S., Enghoff, H. & Santamaria, S. (2018) Novelty upon novelty visualized by rotational scanning electron micrographs (rSEM): Laboulbeniales on the millipede order Chordeumatida. PLoS One, 13(11), e0206900. https://doi.org/10.1371/journal.pone.0206900
Reboleira, A.S.P.S., Moritz, L., Santamaria, S. & Enghoff, H. (2021). Penetrative and non-penetrative interaction between Laboulbeniales fungi and their arthropod hosts. Scientific Reports, 11, 22170. https://doi.org/10.1038/s41598-021-01729-x
Santamaria, S. (2006). New or interesting Laboulbeniales (Fungi, Ascomycota) from Spain, V. Nova Hedwigia, 82(3–4), 349–363. https://doi.org/10.1127/0029-5035/2006/0082-0349.
Santamaria, S., Enghoff, H. & Reboleira, A.S.P.S. (2014). Laboulbeniales on millipedes: the genera Diplopodomyces and Troglomyces. Mycologia, 106(5), 1027–1038.https://doi.org/10.3852/13-381.
Santamaria, S., Enghoff, H., Gruber, J. & Reboleira, A.S.P.S. (2017). First Laboulbeniales from harvestmen: the new genus Opilionomyces. Phytotaxa, 305(4), 285–29 https://doi.org/10.11646/phytotaxa.305.4.4.
Santamaria, S., Enghoff, H. & Reboleira, A.S.P.S. (2018). New species of Troglomyces and Diplopo domyces (Laboulbeniales, Ascomycota) from millipedes (Diplopoda). European Journal of Taxonomy, 429, 1–20. https://doi.org/10.5852/ejt.2018.429.
Thaxter, R. (1895) Notes on Laboulbeniaceae with description of new species. Proceedings of the American Academy of Arts and Science, 30, 467-481.
Thaxter, R. (1896) New species of Laboulbeniaceae from various localities. Proceedings of the American Academy of Arts and Science, 12,187-429.
Thaxter, R. (1899) Preliminary diagnoses of new species of Laboulbeniaceae I. Proceedings of the American Academy of Arts and Science, 35, 407-450.
Thaxter, R. (1908) Contribution towards a monograph of the Laboulbeniaceae, Part II. Memoirs of the American Academy of Arts and Science, 13, 217-469.
Thaxter, R. (1931) Contribution towards a monograph of the Laboulbeniaceae, Part V. Memoirs of the American Academy of Arts and Science, 16, 1-435.
Thomas, C.D. (2000). Dispersal and extinction in fragmented landscapes. Proceedings of the Royal Society of London B, 267, 139–145.
Tragust, S, Tartally. A, Espadaler. X & Billen. J (2016) Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae). Myrmecology News, 23, 81-89.
Warren, M., Hill, J., Thomas, J., Asher, J., Fox, R., Huntley, B., Roy, D.B., Telfer, M.G., Jeffcoate, S., Harding, P., Jeffcoate, G., Willis, S.G., Greatorex‐Davies, J.N., Moss, D., & Thomas, C.D. (2001). Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature, 414, 65–69.
Weir, A. & Hammond, P.M. (1997). Laboulbeniales on beetles: Host utilization patterns and species richness of the parasites. Biodiversity and Conservation, 6, 701–719.
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Species of Laboulbeniales fungi parasitic on some common Indian insects: Isolation, visualization and characterization by Scanning Electron Micrographs (SEM). (2024). Journal of Applied and Natural Science, 16(1), 110-117. https://doi.org/10.31018/jans.v16i1.5347
