Abstract
We report the in situ occurrence of a new species of Meliolinites (fossil Meliolaceae, Ascomycota), Meliolinites pliocenicus, on the lower epidermal surface of fossilized angiosperm leaf of Shorea siwalika (Dipterocarpaceae) recovered from the middle Siwalik stratum (Subansiri Formation: Pliocene) of Arunachal sub-Himalaya. This fungal morph is characterized by well-preserved unique mycelia consisting of superficial, dark brown, thick-walled, branching hyphae with appressoria as well as phialides and dispersed ellipsoidal, 3-septate, 4-celled, dark brown ascospores. The in situ evidence of the fungus on the fossil leaf cuticle indicates the prevalence of a warm, humid, tropical climate in Arunachal sub-Himalaya during the deposition and further suggests that a possible host-ectoparasite relationship existed in the ancient forest of this area during the Pliocene time.
Similar content being viewed by others
References
Alexopoulos CJ, Mims C (1979) Introductory mycology, 3rd edn. John Wiley & Sons, NY 632 pp
Alvin K, Muir M (1970) An epiphyllous fungus from the Lower Cretaceous. Biol J Linn Soc 2(1):55–59
Bagchee K (1953) The fungal diseases of Sal (Shorea robusta)-I. Indian For Res NS 1:11–23
Bannister JM, Conran JG, Lee DE (2016) Life on the phylloplane: Eocene epiphyllous fungi from Pikopiko Fossil Forest, Southland, New Zealand. N Z J Bot 54(4):412–432
Chirouze F, Dupont-Nivet G, Huyghe P, van der Beek P, Chakraborti T, Bernet M, Erens V (2012) Magnetostratigraphy of the Neogene Siwalik Group in the far eastern Himalaya: Kameng section, Arunachal Pradesh, India. J Asian Earth Sci 44:117–135
Colani M (1920) Etude sur les flores tertiaires de quelques gisements de lignite de L’Indochine et du Yunnan. 1. Structure microscopique d’un bois fossile. Bull de Service Geol 8: 397–446
Daghlian CP (1978) A new melioloid fungus from the Early Eocene of Texas. Palaeontology 21:71–176
Das P, Khan MA, DE B, Samajpati N, Bera S (2007) Evidence of exoparasitic relationship between Asterina (Asterinaceae) and Chonemorpha (Apocynaceae) from the Upper Siwalik (Kimin Formation) sediments of Arunachal subhimalaya, India. J Mycopathol Res 45(2):225–230
Dilcher DL (1963) Eocene epiphyllous fungi. Science 142:667–669
Dilcher DL (1965) Epiphyllous fungi from Eocene deposits in Western Tennessee. Palaeontogr Abt B 116:1–54
Ding ST, Sun BN, Wu JY, Li XC (2011) Miocene Smilax leaves and associated epiphyllous fungi from Zhejiang, East China and their paleoecological implications. Rev Palaeobot Palynol 165(3):209–223
Du BX, Yan DF, Sun BN, Li XC, Dao KQ, Li XQ (2012) Cunninghamia praelanceolata sp. nov. with associated epiphyllous fungi from the upper Miocene of eastern Zhejiang, S. E China and their palaeoecological implications. Rev Palaeobot Palynol 182(4):32–43
Eriksson OE, Hawksworth DL (1986) Notes on ascomycete systematic – nos 1993. Syst Ascomycetum 5:113–184
Hansford CG (1961) The Meliolineae. A monograph. Sydowia Beih 2:1–806
Hirata K (1966) Host range and geographical distribution of powdery mildews. J Fac Agr Niigata Univ, Niigata
Hongsanan S, Tian Q, Peršoh D, Zeng X-Y, Hyde KD, Chomnunti P, Boonmee S, Bahkali AH, Wen T-C (2015) Meliolales. Fungal Divers. https://doi.org/10.1007/s13225-015-0344-7
Hosagoudar VB (1987a) Meliolaceae of South India. Ibid 11:157–160
Hosagoudar VB (1987b) Meliolaceae of South India-II. Sydowia 40:113–121
Hosagoudar VB (1987c) Meliola rantacharii sp. nov. from Tamil Nadu, India. Kavaka 15:5–6
Hosagoudar VB (1987d) Meliolaceae of S. India, 1. Eeon Tax Bot 11(1):157–160
Hosagoudar VB (1988a) Meliolaceae of South India-IV. Indian Bot Reptr 1:58–60
Hosagoudar VB (1988b) Meliolaceae of South India-V. Nova Hedwigia 47:535–542
Hosagoudar VB (1989) A new variety of Meijola carissae Doidge from India. Curr Sci 58(3):145–146
Hosagoudar VB (1991a) Meliolaceae of South India – VIII. Crypt Bot 2/3:183–187
Hosagoudar VB (1991b) Meliolaceae of South India - IX. Nova Hedwigia 52:497–503
Hosagoudar VB (1996) Meliolales of India. Botanical Survey of India. Culcutta 363 pp
Hosagoudar VB (2006) Biogeographical distribution of Meliolaceae members in India. Zoos’ Print J 21(12):2495–2505
Hosagoudar VB, Goos RD (1994) Geographical distribution of the Meliolaceae with special reference to India. Paper presented in IMC 5
Hosagoudar VB, Abraham TK, Pushpangadan P (1997) The Meliolineae a supplement. The Director TBG and RI, Pal ode, Thiruvananthapuram, 20
Hosagoudar VB, Abraham T, Goos R (1998a) Meliolaceae of Kerala, India-III. Mycotaxon 66:109–113
Hosagoudar VB, Abraham T, Goos R (1998b) Meliolaceae of Kerala, India-IV. Mycotaxon 66:115–119
Hosagoudar VB, Abraham T, Goos R (1998c) Meliolaceae of Kerala. India II Mycotaxon 66:103–108
Hu Y (1996) Flora Fungorum Sinicorum, vol 4. Meliolales (I). Science Press, Beijing, China 270p
Hübers M, Bomfleur B, Krings M, Kerp H (2011) An Early Carboniferous leaf-colonizing fungus. Neues Jahrb Geol Paläontol-Abh 261(1):77–82
Kalgutkar RM, Jansonius J (2000) Synopsis of fossil fungal spores, mycelia and fructifications. Published by American Association of Stratigraphic Palynologists Foundation, Dallas, Texas, U.S.A
Kerp H, Krings M (1999) Light microscopy of cuticle in fossil plants and spores. In: Jones TP, Rowe NP (eds) Modern techniques, pp 52–56
Khan MA, Bera S (2007) Dysoxylum miocostulatum sp. nov.-a fossil leaflet of Meliaceae from the Lower Siwalik sediments of West Kameng district, Arunachal Pradesh, Eastern India. Indian J Geol 79(3–4):63–68
Khan MA, Bera S (2014) New lauraceous species from the Siwalik forest of Arunachal Pradesh, eastern Himalaya, and their palaeoclimatic and palaeogeographic implications. Turk J Bot 38:453–464
Khan MA, Bera S (2016) First fossil evidence of Connaraceae R. Br. from Indian Cenozoic and its phytogeographical significance. J Earth Syst Sci 125(5):1079–1087
Khan MA, Ghosh R, Bera S, Spicer RA, Spicer TEV (2011) Floral diversity during Plio-Pleistocene Siwalik sedimentation (Kimin Formation) in Arunachal Pradesh, India, and its palaeoclimatic significance. Palaeobio Palaeoenv 91:237–255
Khan MA, Spicer RA, Bera S, Ghosh R, Yang J, Spicer TEV, Guo S, Su T, Jacques F, Grote PJ (2014) Miocene to Pleistocene floras and climate of the eastern Himalayan Siwaliks, and new palaeoelevation estimates for the Namling-Oiyug Basin, Tibet. Glob Planet Change 113:1–10
Khan MA, Bera S, Ghosh R, Spicer RA, Spicer TEV (2015) Leaf cuticular morphology of some angiosperm taxa from the Siwalik sediments (middle Miocene to lower Pleistocene) of Arunachal Pradesh, eastern Himalaya: systematic and palaeoclimatic implications. Rev Palaeobot Palynol 214:9–26
Khan MA, Spicer RA, Spicer TEV, Bera S (2016) Occurrence of Shorea Roxburgh ex C. F. Gaertner (Dipterocarpaceae) in the Neogene Siwalik forests of eastern Himalaya and its biogeography during the Cenozoic of Southeast Asia. Rev Palaeobot Palynol 233:236–254
Khan MA, Spicer RA, Spicer TEV, Bera S (2017a) Evidence for diversification of Calophyllum L. (Calophyllaceae) in the Neogene Siwalik forests of eastern Himalaya. Plant Syst Evol 303:371–386
Khan MA, Bera M, Spicer RA, Spicer TEV, Bera S (2017b) First occurrence of mastixioid (Cornaceae) fossil in India and its biogeographic implications. Rev Palaeobot Palynol 247:83–96
Khan MA, Bera M, Bera S (2018a) Vizellopsidites siwalika, a new fossil epiphyllous fungus from the Plio-Pleistocene of Arunachal Pradesh, eastern Himalaya. Nova Hedwigia 107(3–4):543–555
Khan MA, Bera M, Spicer RA, Spicer TEV, Bera S (2018b) Floral diversity and environment during the middle Siwalik sedimentation (Pliocene) in the Arunachal sub-Himalaya. Palaeobio Palaeoenv. https://doi.org/10.1007/s12549-018-0351-2
Khan MA, Bera M, Spicer RA, Spicer TEV, Bera S (2018c) Evidence of simultaneous occurrence of tylosis formation and fungal interaction in a late Cenozoic angiosperm from the eastern Himalaya. Rev Palaeobot Palynol 259:171–184
Kirk PM, Cannon PF, Stalpers JA (2008) Dictionary of the Fungi, 10th edn. CAB International, Walingford, p 784p
Kock C (1939) Fossile Kryptogamen aus der eozanen Braunkohle des Geiseltales. Nova Acta Leopoldina 6:333–359
Kumar G (1997) Geology of Arunachal Pradesh. Geological Society of India, Bangalore
Lange RT (1978) Southern Australian tertiary epiphyllous fungi, modern equivalents in the Australasian region, and habitat indicator value. Can J Bot 56(5):532–541
Lange RT (1980) Evidence of lid-cells and host-specific micro-fungi in the search for tertiary Eucalyptus. Rev Palaeobot Palynol 29:29–33
Ma FJ, Sun BN, Wang QJ, Dong JL, Yang GL, Yang Y (2015a) A new species of Meliolinites associated with Buxus leaves from the Oligocene of Guangxi, southern China. Mycologia 107(3):505–511
Ma FJ, Wang QJ, Dong JL, Yang Y, Wang WJ, Yan DF, Sun BN (2015b) Buxus leaves from the Oligocene of Guangxi, China and their biogeographical significance. Acta Geol Sin 89(5):1453–1469
Mandal A, Samajpati N, Bera S (2009) In situ occurrence of epiphyllous fungus Phomites Fritel from the Lower Siwalik sediments of Darjeeling Foothills. J Bot Soc Bengal 63(1):37–40
Mandal A, Samajpati N, Bera S (2011) A new species of Meliolinites (fossil Meliolales) from the Neogene sediments of sub-Himalayan West Bengal, India. Nova Hedwigia 92(3):435–440
Mibey RK, Hawksworth DL (1997) Meliolaceae and Asterinaceae of the Shimba Hills, Kenya. Mycol. Papers 174:103–108
Parbery IH, Brown JF (1986) Sooty moulds and black mildews in extra-tropical rainforests. In: Fokkema NJ, van der Heuvel J (eds) Microbiology of the phyllosphere. Cambridge University Press, New York, NY, pp 101–120
Parbery DG, Emmett RW (1977) Hypotheses regarding appressoria, spores, survival and phylogeny in parasitic fungi. Revue de Mycologie 41:429–447
Phipps CJ, Rember WC (2004) Epiphyllous fungi from the Miocene of Clarkia, Idaho: reproductive structures. Rev Palaeobot Palynol 129(1):67–79
Schmiedeknecht M (1995) Environmental tolerance range of Meliolales as mirrored in their horizontal and vertical distribution patterns. Microbiol Res 150:271–280
Selkirk DR (1975) Tertiary fossil fungi from Kiandra, New South Wales. Proc Linn Soc NSW 100:70–94
Shi G, Zhou Z, Xie Z (2010) A new Cephalotaxus and associated epiphyllous fungi from the Oligocene of Guangxi, South China. Rev Palaeobot Palynol 161(3):179–195
Skirgiełło OA (1961) Flora kopalna Turowa kolo Bogatynia II. [Fossil flora of Turow near Bogatyni II]. (Ascomycetes–Roselliniaceae, Amphisphaeriaceae,?Meliolaceae), Basidiomycetes (Polyporaceae) Prace Muzeum Ziemi 4: 5–12 [in Polish and English]
Song B, Ouyang Y, Hu Y (1996) New species and new records of meliolaceae (fungi) in China. J Trop Subtrop Bot 5(2):33–40
Taylor TN, Osborn JM (1996) The importance of fungi in shaping the paleoecosystem. Rev Palaeobot Palynol 90(3–4):249–262
Taylor TN, Taylor EL (1993) The biology and evolution of fossil plants. Prentice Hall, New Jersey, USA
Van Geel B, Aptroot A, Mauquoy D (2006) Sub-fossil evidence for fungal hyperparasitism (Isthmospora spinosa on Meliola ellisii, on Calluna vulgaris) in a Holocene intermediate ombrotrophic bog in northern-England. Rev Palaeobot Palynol 141(1):121–126
Vishnu (n M)A, Khan MA, Bera M, Dilcher DL, Bera S (2017) Fossil Asterinaceae in the phyllosphere of the eastern Himalayan Neogene Siwalik forest and their palaeoecological significance. Bot J Linn Soc 185(2):147–167
Vishnu (n M)A, Khan MA, Bera M, Acharya K, Dilcher DL, Bera S (2019) Occurrence of Phoma Sacc. in the phyllosphere of Neogene Siwalik forest of Arunachal sub-Himalaya and its palaeoecological implications. Fungal Biol 123:18–28
Wang ZX, Sun BN, Sun FK, Wang JD, Dong JL, Sun MX, Du BX (2017a) Identification of two new species of Meliolinites associated with Lauraceae leaves from the middle Miocene of Fujian. China Mycologia 109(4):676–689
Wang ZX, Sun FK, Wang JD, JD DF, Dong JL, Sun MX, Sun BN. (2017b) New fossil leaves and fruits of Lauraceae from the Middle Miocene of Fujian, southeastern China differentiated using a cluster analysis. Hist Biol 1‒19
Wells AK, Hill RS (1993) Epiphyllous microorganisms as palaeoclimate estimators: the developmental sequence of fungal ‘germlings’ on their living host. Aust Syst Bot 6(5):377–386
Yeloff D, Charman D, van Geel B, Mauquoy D (2007) Reconstruction of hydrology, vegetation and past climate change in bogs using fungal microfossils. Rev Palaeobot Palynol 146:102–145
Zheng S, Zhang W (1986) The cuticles of two fossil cycads and epiphytic fungi. Acta Bot Sin 28:427–436
Acknowledgments
We acknowledge the UGC-CAS VII, Department of Botany, University of Calcutta, for the necessary facilities. We thank Sri Bimalendu De, Ex Dy. D.G., and Sri Sambhu Chakrabarty, Sr. Geologist, Geological Survey of India, Operation Arunachal, Itanagar, for their help during the field work. MB acknowledges the help and inspiration from Prof. Krishnendu Acharya, Head of the Department of Botany, University of Calcutta.
Funding
The authors MAK and SB thank Department of Science and Technology (DST), Government of India, New Delhi [grant number: SR/S4/ES-67/2003 to S.B.], for the financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Editorial Responsibility: Roland Kirschner
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bera, M., Khan, M.A. & Bera, S. A new foliicolous melioloid fungus from the Pliocene of eastern Himalaya. Mycol Progress 18, 921–931 (2019). https://doi.org/10.1007/s11557-019-01502-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-019-01502-5