A new meliolaceos foliicolous fungus from the Plio-Pleistocene of Arunachal Pradesh, eastern Himalaya

Review of Palaeobotany and Palynology 268 (2019) 55–64

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A new meliolaceos foliicolous fungus from the Plio-Pleistocene of Arunachal Pradesh, eastern Himalaya Mahasin Ali Khan a, Meghma Bera b, Subir Bera b,⁎ a b

Department of Botany, Sidho-Kanho-Birsha University, Ranchi Road, Purulia 723104, India Centre of Advanced Study, Department of Botany, University of Calcutta, 35, B.C. Road, Kolkata 700019, India

a r t i c l e

i n f o

Article history: Received 29 October 2018 Received in revised form 13 May 2019 Accepted 16 June 2019 Available online 19 June 2019 Keywords: Meliolinites Siwalik Plio-Pleistocene Host–ectoparasite interaction Paleoecology Arunachal sub-Himalaya

a b s t r a c t We report in this article, the in situ occurrence of a new species of Meliolinites (fossil Meliolaceae), Meliolinites neogenicus sp. nov. on the abaxial cuticular surface of fossilized leaf cuticle fragments of the angiosperm Litsea cf. salicifolia Khan et al. (Lauraceae) recovered from the upper part of the Siwalik succession of Neogene sediments (Kimin Formation: late Pliocene to early Pleistocene) of Arunachal Pradesh, eastern Himalaya, India. This Plio-Pleistocene melioloid foliicolous fungal morph features a well-preserved unique mycelium consisting of superficial, dark brown, thick-walled and branching hyphae with bicellular appresoria and unicellular phialides. The fungal colonies also include globose, dark brown perithecia, as well as one ellipsoidal, 5-celled, 4-septate, dark brown ascospore. The fossil leaf of Litsea, together with the foliicolous fungal remains indicates the prevalence of a warm, humid, climate in the Arunachal sub-Himalaya during the Plio-Pleistocene. The in situ evidence of Meliolinites on host leaf cuticle indicates the possible existence of a host–ectoparasite relationship in the ancient warm and humid tropical evergreen forest of this area during the Plio-Pleistocene. Based on present and earlier records it is suggested that Lauraceae has been a common host for meliolaceous fungi since the early Cenozoic. Meliolinites neogenicus sp. nov. might have thrived under a warm and humid climate with a mean annual temperature (MAT) from 21 to 26 °C and a mean annual precipitation (MAP) from 1000 to 2000 mm in the Plio-Pleistocene of Arunachal sub-Himalaya which is in conformity with our earlier published qualitative and quantitative climatic data. © 2019 Elsevier B.V. All rights reserved.

1. Introduction The family Meliolaceae Martin ex Hansf. usually consists of epiphyllous obligate ectoparasitic fungi inhabiting higher plants that are widely distributed in the tropical and subtropical regions (Mibey and Hawksworth, 1997; Song et al., 1996; Hosagoudar et al., 1998a, 1998b, 1998c; Kirk et al., 2008; Hongsanan et al., 2015). These fungi can infect plant species belonging to numerous families and usually cause benign diseases commonly known as “black mildews” or “dark mildews” (Alexopoulos and Mims, 1979). The black mildews are parasites, penetrating their host's epidermal cells through the cuticle by means of haustoria that arise from the characteristic superficial hyphopodiate mycelium. Meliolaceous fungi are predominantly foliicolous and rarely infect the soft stems and tender shoots. Members of Meliolalaceae are generally shade and moisture loving and prefer temperatures between 21 and 26 °C temperature, 1000–2000 mm precipitation, 50–65% relative humidity and 40–200 mm rainfall (Schmiedeknecht, 1995; Thomas et al., 2013; Ma et al., 2015). Indian meliolaceous mycobiota (533 taxa) form 22% of the world meliolaceous ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (S. Bera).

https://doi.org/10.1016/j.revpalbo.2019.06.005 0034-6667/© 2019 Elsevier B.V. All rights reserved.

mycobiota (2400 taxa). Meliolaceous genera like Amazonia Theiss (27 taxa), Appendiculella von Hoehnel (8 taxa), Armatella (12 taxa), Asteridiella Mcalpine (60 taxa), Irenopsis F. Stevens (27 taxa), Meliola Fr. (397 taxa) and Prataprajella Hosagoudar (2 taxa) have been reported from India (Hosagoudar, 2006). Of all these genera, the genus Meliola is the most species rich genus of the family Meliolaceae, and is versatile, having a wide host range and occuring in all altitudes and ecological conditions. The members of the meliolaceous fungi are generally characterized by superficial, dark brown, thick-walled, appresoriate mycelium, with phialides and setae, and globose perithecia with 1–4 septate ascospores (Hosagoudar, 2006; Hongsanan et al., 2015; Wang et al., 2017). The fossil records of Meliolaceae however, are limited (Köch, 1939; Dilcher, 1963, 1965; Selkirk, 1975; Daghlian, 1978; van Geel and Aptroot, 2006; van Geel et al., 2006; Yeloff et al., 2007; Kar et al., 2010; Mandal et al., 2011; Saxena and Tripathi, 2011). To date, eight authentic foliicolous fossil species of Meliolaceae have been reported (Table 1). Three have been recovered from the Eocene sediments of Tennessee, America (Dilcher, 1965; Daghlian, 1978; Kalgutkar and Jansonius, 2000), one from the Oligocene of China (Ma et al., 2015); two from the Miocene of China (Wang et al., 2017), one from the Miocene sediments of Australia (Selkirk, 1975); and one from the Holocene

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Table 1 Fossil record of the fossil-genus Meliolinites. Age

Fossil Meliolaceae

Host

Locality

Citation

Eocene

Meliolinites spinksii M. anfractus

Chrysobalanus L. (Chrysobalanacea)

Tennessee, North-America

Sapindus L. (Sapindaceae)

Tennessee, North-America

M. dilcheri M. buxi M. nivalis M. siwalika M. fotanensis M. zhangpuensis M. neogenicus

Lauraceae Buxus L. (Buxaceae) ? Lauraceae Lauraceae Lauraceae Litsea salicifolia (Roxb. ex Nees) Hook.f. Calluna vulgaris (L.) Hull. (Ericaceae)

Tennessee, North-America Guangxi, China Australia Darjeeling, India Fujin, China Fujin, China Arunachal Pradesh, India

Dilcher (1965), Kalgutkar and Jansonius (2000) Dilcher (1965), Kalgutkar and Jansonius (2000) Daghlian (1978) Ma et al. (2015) Selkirk (1975) Mandal et al. (2011) Wang et al. (2017) Wang et al. (2017) Present study

Eocene Eocene Oligocene Miocene Miocene Miocene Miocene Late Pliocene-early Pleistocene Holocene

Meliola ellisii

of England (van Geel et al., 2006). However, only one foliicolous fossilspecies of Meliolinites has been reported from the Miocene of India (Mandal et al., 2011). The present investigation adds another new fossil-species of Meliolinites, i.e., Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. to the diversity of fossil Meliolaceae from the Neogene sediments of India. Epiphyllous fungi provide valuable information about paleoenvironmental reconstructions (Dilcher, 1963, 1965; Alvin and Muir, 1970; Daghlian, 1978; Lange, 1978, 1980; Zheng and Zhang, 1986; Phadtare, 1989; Currah et al., 1998; Taylor, 1990; Wells and Hill, 1993; Taylor and Osborn, 1996; Phipps and Rember, 2004; Shi et al., 2010; Ding et al., 2011; Hübers et al., 2011; Du et al., 2012). Microfungal remains from India including Meliolaceae are frequently found in different Cenozoic sedimentary deposits as dispersed spores, fruiting bodies, and fragments of vegetative hyphae (Ramanujam and Rao, 1978; Jain and Kar, 1979; Phadtare and Kulkarni, 1984; Varma and Patil, 1985; Yeloff et al., 2007; Kar et al., 2010; Saxena and Tripathi, 2011). However, in situ records of epiphyllous fungal remains on host leaf cuticles are meager (Das et al., 2007; Mandal et al., 2009, 2011; Mitra and Banerjee, 2000; Mitra et al., 2002; Bonde et al., 2004; Khan et al., 2018a; Vishnu (nee Mandal et al., 2017; Vishnu (nee Mandal et al., 2018). During the last decade, diverse types of leaf megafossils have been reported from the Neogene sediments of Arunachal subHimalaya allowing for its paleoecological and paleoclimatic characterization (Joshi et al., 2003; Joshi and Mehrotra, 2007; Khan and Bera, 2007, 2014, 2016; Khan et al., 2011, 2014, 2015, 2016, 2017a, 2017b, 2018b, 2018c). So far, only four records of fossil foliicolous fungi are known from this area (Das et al., 2007; Vishnu (nee Mandal et al., 2017; Vishnu (nee Mandal et al., 2018; Khan et al., 2018a). In the present article, we (1) describe and illustrate a new well-preserved foliicolous fungal species Meliolinites neogenicus sp. nov. on the abaxial cuticular surface of fossilized leaf fragments of Litsea cf. salicifolia Khan et al., 2011 (comparable to modern Litsea salicifolia of the family Lauraceae) from the Plio-Pleistocene Kimin Formation of Arunachal sub-Himalaya; (2) compare morphologically the present fungal species with the published fossil-taxa; and (3) provide evidence of the past biodiversity of this genus. Furthermore, based on the life habits of extant Meliolaceae, reconstruction of paleoecology of Arunachal subHimalaya during Plio-Pleistocene time is also attempted with special emphasis on the ecto–parasitic interaction and evolutionary process between Meliolinites neogenicus and its host. 2. Material and methods The leaf remains of Lauraceae with the associated epiphyllous fungi were collected from the upper Siwalik strata (Kimin Formation, late Pliocene to early Pleistocene; Kumar, 1997) exposed along the ItanagarBanderdewa road in Papumpare district, Arunachal Pradesh (N 27° 07′

Northern England, Netherlands and Germany

van Geel et al. (2006)

06.67″/E 93° 47′ 34.79″) (Fig. 1). The upper part of the Siwalik succession of sediments are assigned to the Kimin Formation which is considered late Pliocene to early Pleistocene (Kumar, 1997). Chirouze et al. (2012) proposed that the Siwalik sedimentation of Arunachal Pradesh took place between 13 and 2.5 Ma on the basis of magnetostratigraphic data. The transition between the lower and middle Siwalik is dated at about 10.5 Ma and the middle to upper Siwalik transition is dated at 2.6 Ma. The Kimin Formation is characterized lithologically by loosely packed, pebbly, very coarse to fine grained gray sandstone with high limonitisation at places, and is intercalated with claystone and shale containing plant fossils (Fig. 1). The fossil fungi on the leaf cuticles of Litsea cf. salicifolia were prepared for microscopic analysis by the standard maceration technique of Kerp and Krings (1999) and the process was adjusted for the present material (treatment with 48% hydrofluoric acid followed by oxidation with 50% nitric acid and repeated washing after treating with 2–5% potassium hydroxide). The upper and lower leaf cuticles were separated using dissecting needles. The cuticles were then dehydrated in an alcohol series (30%, 50%, 70%, 90%, 100%) and stored in 70% alcohol. For light microscopic (LM) study the samples were fixed on glass slides using 2% polyvinyl alcohol followed by mounting in Euparal. The epiphyllous fungi associated with leaf epidermis were observed on the fossil cuticles under LM and photographed with a transmitted light compound microscope with photographic attachment (Zeiss Axioskop 2). Handdrawings of the fossil fungal species were done using CorelDraw X6 software. For descriptions of morphological characters of the present fungal morph of Meliolaceae, we followed Hu (1996). The fossil leaf specimen and all prepared cuticular slides are deposited in the Herbarium and Museum (CUH) of the Department of Botany (Paleobotany– Palynology Section), University of Calcutta, India. For the quantitative reconstruction of paleoclimate, CLAMP (Climate Leaf Analysis Multivariate Program) analysis was done on the PlioPleistocene fossil leaf assemblages of Arunachal sub-Himalaya (Khan et al., 2014). 3. Results 3.1. Systematics of foliicolous fungi Order: MELIOLALES Gäum ex Hawksw. & Erikss., 1986 Family: MELIOLACEAE Martin ex Hansford, 1946 Genus: MeliolinitesSelkirk, 1975 Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. (Fig. 2; Plates I, II, III) Host plant: Litsea cf. salicifolia Khan et al., 2011 (Lauraceae, Plate I, 1). Diagnosis: Mycelial colony foliicolous, dark brown; hyphae septate, thick-walled, straight to slightly sinuous, generally with opposite branching at acute angle, bearing both appressoria and phialides;

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Fig. 1. (a) Location of study area in Papumpare district, Arunachal Pradesh and a geological setting of the area around Itanagar-Banderdewa road; triangle indicates the fossil locality.

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Fig. 2. (a) Hand-drawing of Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. (from Plate I, 2), showing mycelia colony with vegetative hyphae, appressoria (marked by green arrow) and phialides (marked by blue arrow); (b) Hand-drawing of single dispersed 5-celled, 4-septate ascospore (from Plate I, 7).

appressoria 2-celled, alternate, straight to antrorse; stalk cells cylindrical to cuneate; head cells capitate, thick-walled, long, globose-elliptical or irregularly rounded, occasionally 2-lobed or entire; phialides ampulliform, with pointed and tapering apex, alternate or opposite, rarely mixed with appressoria; perithecia scattered, globose in shape, with concentric appearance, non-ostiolate, edges crenate to crenulate, about 70–100 μm in diameter; ascospore 5-celled, 4-septate; mycelial and perithecial setae absent. Holotype: CUH/PPL/IB7/36/AS1 Type locality: Road cutting section along the Itanagar-Banderdewa road in Papumpare district, Arunachal Pradesh (N 27° 07′ 06.67″/E 93° 47′ 34.79″). Type horizon: Upper part of the Siwalik strata (Kimin Formation: late Pliocene to early Pleistocene). Etymology: The specific epithet “neogenicus” refers to the stratigraphical occurrence (Neogene deposits) of the present fossil-species of Meliolinites. Collectors: Mahasin Ali Khan and Subir Bera. Repository: Herbarium and Museum, Department of Botany, University of Calcutta, India (CUH). Description: Three independent fungal colonies observed on the fossil leaf cuticles (Plate I, 2, 3, 4), fungal colonies thin to sub-dense, dark brown; vegetative hyphae dark brown, septate, thick-walled, straight to slightly undulate, branching unilateral, or opposite at 45°–75° angles, bearing both appressoria and phialides (Fig. 2a; Plates I, 2, 3, 4, 5, 6; II, 1, 2, 3, 4, 5); hyphal cells cylindrical, with uneven, irregular margin, thickwalled, 25–38 μm in length and 6–9 μm in width (Plates I, 2–6; II, 1–5); appressoria straight to antrorse, mostly branching alternately while some appear unilaterally, emerging from a point just behind the septa of vegetative hyphae; each appressorium consisting of two cells, a short stalk cell and a capitate head cell (Plates I, 3, 4, 5; II, 1, 2, 3, 4, 5), rarely unicellular (Plate I, 6); stalk cells dark brown, cylindrical to cuneate, 3.1–4.3 μm in length and 4.2–9.8 μm in width, sometimes short and inconspicuous (Plate II, 5); head cells dark brown, 14.5–20.5 μm in length and 9.3–16.5 μm in width, globose-elliptical or irregularly rounded, sometimes 2-lobed, distinctly thick-walled, long, straight or curved or sometimes bent towards the apex (Fig. 2a; Plate II, 1, 2); phialides dark brown, rarely mixed with appressoria, opposite to

alternate, ampulliform, with pointed and tapering apex, sometimes bent, 18.5–25.6 μm in length and 4.3–6.5 μm in width (Fig. 2a; Plates I, 2; II, 4, 5); perithecia brown to dark brown, scattered, globose in shape, with concentric appearance and more or less crenulate edges; compact, mature fruitbody about 70–100 μm in diameter (Plates I, 2, 6; III, 1, 2, 3, 4, 5, 6), non-ostiolate, young hyphae radiating from the perithecia (Plate III, 2, 5, 6), developing young perithecia with small globose bodies, about 35–40 μm diameter (Plates I, 3; II, 3); ascospore dispersed, dark brown to black, ellipsoidal, thick-walled, 5-celled, 4septate, septation distinct, constricted at the septa, 76 × 25 μm in size (Fig. 2b; Plate I, 7); no mycelial or perithecial setae observed. 4. Discussion 4.1. Comparisons The characteristic two-celled appressoria, one-celled phialides and four-septate, five-celled ascospore make the fungal species closely comparable to the extant members of Meliolaceae. As no setae were observed, the above described fossil-species cannot be assigned to one of the extant genera of the Meliolaceae. So, here we assign the fungus to a fossil-species of the fossil-genus Meliolinites Selkirk, which was erected for fossil epiphyllous fungi that lack setae but otherwise shows the characters similar to extant members of the family Meliolaceae (Selkirk, 1975; Daghlian, 1978). On comparison the presently described fossil fungus appears to be distinctly different from the previously published fossil-species of Meliolaceae (Table 2). Meliolinites anfractus differs from the current specimen by having characteristic mycelial setae and four-celled ascospores. It is also different from the M. neogenicus in terms of spacing, arrangement, and angle of hyphae and appressoria. M. spinksii differs from our Siwalik species in the arrangement and shape of appressoria. It lacks lobe in the head cell of appressoria differentiating it from the M. neogenicus. Meliolinites dilcheri can be distinguished from our fossil-species by the absence of phialides. Meliolinites nivalis differs in the shape of appressoria and hyphal features. The head cells of appressoria are non-splitting and have a different shape and size compared to that of M. neogenicus. Meliolinites siwalika differs in the shape of the perithecia, size of hyphal

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Plate I. Light micrographs of Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. (CUH/PPL/IB7/36/AS1) recovered from the cuticle of Litsea cf. salicifolia leaf (Meliaceae) from the Kimin Formation (late Pliocene to early Pleistocene), Arunachal Pradesh, eastern Himalaya. (1) Fossil leaf of Litsea cf. salicifolia (Meliaceae) (specimen number CUH/PPL/IB7/36) (scale bar = 1 cm); (2) Mycelial colony of M. neogenicus on the leaf epidermal surface showing septate hyphae with cylindrical hyphal cells, two-celled appressoria (marked by blue arrow), phialides (marked by green arrow) and globose perithecium (marked by red arrow); (3) Hypha of M. neogenicus showing two-celled appressoria (marked by blue arrow) and young developing fruitbody (marked by red arrow); (4) Septate (marked by black arrow) hyphal cells with two-celled appressoria (marked by blue arrow); (5) A hypha of M. neogenicus showing ruptured perithecium (marked by dark green arrow) and one scattered young perithecium (marked by red arrow); (6) A hypha of M. neogenicus showing two-celled appressoria (marked by blue arrow); (7) Single dark brown, 4-septate (marked by numbering), 5-celled ascospore.

cells and thickness of appressoria. The non-lobed head cells of appressoria of M. Siwalika also distinguish it from M. neogenicus. Both Meliola ellisii and Meliolinities zhangpuensis differ from our Siwalik fungus in having fourcelled ascospores. Meliola ellisii also differs in having distinct setae. Meliolinities zhangpuensis can be distinguished from the fungus studied here by the absence of phialides. The head cell shapes of appressoria of M. zhangpuensis are mucronate and are different compared to the globose-elliptical or irregularly rounded shape of the current fossilspecies. Meliola buxi differs from M. neogenicus in having a wider angle between hyphae and hyphopodia, and globose to pyriform head cells. Absence of ascospore in M. buxi also distinguishes it from the newly

described fungus. Meliolinites fotanensis differs from the present fossilspecies in size, shape of the fruiting bodies, appressoria and size of hypal cells. Meliolinites fotanensis shows alternate arrangement of phialides whereas alternate to opposite arrangement is found in M. neogenicus. 4.2. Paleoecological implications Epiphyllous fossil fungi can provide information about the paleoecology and past habitats (Dilcher, 1965; Phadtare, 1989; Taylor and Taylor, 1993; Tripathi, 2001; Phipps and Rember, 2004; Shi et al., 2010; Du et al., 2012; Bannister et al., 2016). Species of extant

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Plate II. Light micrographs of Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. (CUH/PPL/IB7/36/AS1) recovered from the cuticle of Litsea cf. salicifolia leaf (Meliaceae) from the Kimin Formation (late Pliocene to early Pleistocene), Arunachal Pradesh, eastern Himalaya. (1) A part of hypha of M. neogenicus showing capitate appressoria with head cells (marked by blue arrow) and stalk cells (marked by green arrow); an indistinct haustorial pore (marked by white mark) in the globose head cell; (2) Close-up of of Fig. 1 showing septate (marked by light blue mark) cylindrical hyphal cells and haustorial pore (marked by white mark) in the globose head cell (marked by blue mark) of appressorium; (3) A hypha of M. neogenicus showing capitate appressoria and young developing fruitbody; (4) A part of mycelial colony of M. neogenicus showing appressoria and phialides (marked by blue arrow); (5) Close-up of figure 4 showing showing appressorium and phialides (marked by blue arrow).

Meliolaceae are mainly distributed in tropical to subtropical regions (Schmiedeknecht, 1995; Song et al., 1996; Mibey and Hawksworth, 1997; Hosagoudar et al., 1998a, 1998b, 1998c; Kirk et al., 2008). So, the recovery of epiphyllous fossil-species Meliolinites neogenicus sp. nov. is generally indicative of a warm and humid tropical climate favored by high rate of precipitation during the Plio-Pleistocene in the ancient forests of Arunachal sub-Himalaya. This hypothesis is supported by our published qualitative climatic data (Khan and Bera, 2007, 2014, 2016; Khan et al., 2011, 2015, 2016, 2017a, 2017b, 2018a, 2018b, 2018c). The distribution of the modern Meliolaceae

suggests that they survive under a warm and humid climate with a MAT from 21 to 26 °C and a MAP from 1000 to 2000 mm (Schmiedeknecht, 1995; Ma et al., 2015). So, Meliolinites neogenicus sp. nov. might also have lived under similar climatic conditions for its growth and development in the area during deposition. This interpretation is consistent with our published quantitative climatic parameters (Khan et al., 2014). CLAMP analysis suggests a MAT (mean annual temperature) of 25.3 ± 2.8 °C; a CMMT (cold month mean temperature) of 20.8 ± 4 °C, a WMMT (warm month mean temperature) of 28 ± 3.3 °C and a weak monsoonal climate with

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Plate III. Light micrographs of Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov. (CUH/PPL/IB7/36/AS1) recovered from the cuticle of Litsea cf. salicifolia leaf (Meliaceae) from the Kimin Formation (late Pliocene to early Pleistocene), Arunachal Pradesh, eastern Himalaya. (1, 2) Scattered compact and ruptured young fruitbodies perithecia on the lower epidermis of the recovered fossil leaf; (3) A compact, non-ostiolate perithecium; (4) A ruptured perithecium; (5) A globose perithecium with radiating hyphae (marked by green arrow) and concentric appearance (marked by white arrow); (6) Another globose perithecium having distinct concentric appearance (marked by white arrow).

GSP (growing season precipitation) of 1898 ± 920 mm during the Pliocene–early Pleistocene (Khan et al., 2014). So, the newly described fungus together with other published paleobotanical data shed further light on the paleoecology and importance of meliloid fungi in the ancient ecosystems. 4.3. Host–fungi interactions Members of the extant Meliolaceae which are known to be obligate parasites on leaves and stems, demonstrate a limited range of biological interactions (Thomas et al., 2013; Hongsanan et al., 2015; Ma et al., 2015). Here, a parasitic interaction between Litsea and Meliolinites neogenicus is documented. The fungi penetrate the cuticle and epidermis of the host with the help of appressoria (Hansford, 1961; Emmett

and Parbery, 1975; Tucker and Talbot, 2001). The main function of appressoria is to penetrate the surface of host cells (Emmett and Parbery, 1975). The well-preserved, bicellular appressoria represent a direct host response. The head cells of the appressoria have pores that are in direct association with pores in the epidermis of the host leaf (Plate II, 1, 2). Modern Meliolaceae are ectoparasites growing on the leaf surfaces of different members of tropical angiosperm families (Hosagoudar, 1987a, 1987b, 1987c, 1988a, 1988b, 1989, 1991a, 1991b; Hosagoudar et al., 1998a, 1998b, 1998c). At present, meliolaceous fungi are still found to be associated with the host genus Litsea Lam. and other genera of the same host family Lauraceae from India (Table 3). It is interesting to note that among earlier reported species of Meliolinites, 45% of the fossil species were associated with lauraceous leaves recovered from

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Table 2 Comparison of the known fossil-species of the Meliolinites. Fossil species of Meliolaceae

Diagnostic characters Hyphae

Appressoria

Branching arrangement

Angle

Meliolinites neogenicus Khan, Bera, M et Bera S, sp. nov. M. fotanensisWang et al., 2017

Opposite to unilateral Opposite

45°-75° straight to slightly undulate 45° Straight

M. zhangpuensisWang et al., 2017

Alternate to unilateral Opposite to alternately Alternate

60–80°

40–80°

M. nivalisSelkirk, 1975

Alternate to unilateral Alternate to unilateral Alternate

M. siwalikaMandal et al., 2011

Alternate

45°

Meliola ellisiiVan Geel et al., 2006

Opposite

45–60°

M. spinksii (Dilcher, 1965) Kalgutkar and Jansonius, 2000 M. anfractus (Dilcher, 1965) Kalgutkar and Jansonius, 2000 M. dilcheriDaghlian, 1978 M. buxiMa et al., 2015

Fossil species of Meliolaceae

Agreement

Cell size (Length × Width μm)

Thickess

Arrangement Angle

25–38 × 6–9

Thin to Sub-dense Dense

Alternate

40–50° Sub-dense

2

Alternate

45°

Dense

2

Loose

Alternate

90°

Loose

2

Thin to sub-dense Sub-dense to dense Thin to sub-dense Dense

Opposite

30–60° Loose

2

Alternate

90°

2

Alternate Alternate

45–60° Dense to sub-dense 45–70° Sub-dense

2

Dense

Alternate

80–90° Dense

2

Dense

Alternate

80–90° Sub-dense

2

Dense

Alternate

80–90° Sub-dense

2

90°

Straight to slight sinuous Straight

13.9–18.2 × 4.9–9.9 23.9–34.4 × 3.6–5.5 14–50 × 5–9

60–80°

Straight

14–37 × 4–9

45–60°

Straight to slight sinuous Straight to slight sinuous Straight

24.6 × 6.6

45°

Straight to slight sinuous Straight to slight sinuous

14.0–20.5 × 4.9–8.0 19.0–34.0 × 1.6–2.7 22–46 × 9–10 19.3–26.6 × 4.8–6.3

Thickness

No of cells

Dense

2

Diagnostic characters Appressoria Stalk cell shape

Meliolinites neogenicus Khan, Bera, M Cylindrical to cuneate, et Bera S, sp. nov. narrow (base) M. fotanensisWang et al., 2017 Cylindrical, narrow (base) M. zhangpuensisWang et al., 2017 Cylindrical, narrow (base) M. spinksii (Dilcher, 1965) Kalgutkar Cylindrical, narrow and Jansonius, 2000 (apex) M. anfractus (Dilcher 1965) Cylindrical, narrow Kalgutkar and Jansonius, 2000 (base) M. dilcheriDaghlian, 1978 Cylindrical, narrow (apex) M. buxiMa et al., 2015 Cylindrical, narrow (base) M. nivalisSelkirk, 1975 Cylindrical, uniform M. siwalikaMandal et al., 2011 Cylindrical, uniform Meliola ellisiiVan Geel et al., 2006 Cylindrical, narrow (base) Fossil species of Meliolaceae

Phialides Stalk cell L: W (Length:Width)

Head cell shape

Head Cell L: W (Length:Width)

Head cell size

Head cell lobed number

Present or Absent

1.3–2.2

globose-elliptical 1.87

2

Present

2–3

Present

3–5

Absent

1.45

14.5–20.5 μm × 9.3 16.5 μm 16.3–22.3 × 12.8–12.4 9.7–10.3 × 6.1–7.6 8–13 × 5–10

1.05

Oblong

1.98

2.44

Mucronate

1.57

0.6

Oblong to ovoid

0

Present

1.1

Angular

0.95

10–17 × 10–15

5–6

Absent

0.76

Ovoid

1.3

15.4 × 15.4–17.6

2–4

Absent

0.9–1.8

Globose

1.12

2–4

Present

1.2 0.7 0.8

Globose Oblong to ovoid Globose

1.6 1.2 1.35

13.5–16.5 × 13.5–20.5 7.13 × 4.43 14.3 × 12 11.23 × 11.63

0 0 0–2

Present Present Absent

Diagnostic characters Reproductive bodies Perithecia

Meliolinites neogenicus Khan, Bera, M et Bera S, sp. nov. M. fotanensisWang et al., 2017 M. zhangpuensisWang et al., 2017 M. spinksii (Dilcher, 1965) Kalgutkar and Jansonius, 2000 M. anfractus (Dilcher, 1965) Kalgutkar and Jansonius, 2000 M. dilcheriDaghlian, 1978 M. buxiMa et al., 2015 M. nivalisSelkirk, 1975 M. siwalikaMandal et al., 2011 Meliola ellisiiVan Geel et al., 2006

Ascospores

Diameter (μm)

Shape and margin

Shape

Size (μm)

Spore cell number

Spore L: W

70–100 μm 88 66–154.9 ? ? 44–155 150–230 ?

Globose, non-entire Globose, non-entire Globose, non-entire ? ? Globose, non-entire Globose, non-entire ?

Ellipsoidal Ellipsoidal Ellipsoidal Ellipsoidal Ellipsoidal Ellipsoidal ? ?

150–300

Globose, non-entire

Ellipsoidal

76 × 25 51.1–60.2 × 21–27.3 21-24 × 8.5–10.7 37–43 × 12–15 50 × 12–20 44 × 15.4 ? 57.59 × 15.62 46 × 22 41–55 × 14–18

5 5 4 5 4 5 ? 4 5 4

3.1 1.96 2.3 3.42 2.69 2.86 ? 3.69 2.1 2.9

M.A. Khan et al. / Review of Palaeobotany and Palynology 268 (2019) 55–64 Table 3 Record of modern meliolaceous fungi on different genera of Lauraceae from India. Fossil Meliolaceae member from Arunachal Pradesh

Recovered fossil host

Record of modern meliolaceous fungi with similar host (lauraceae) association

Meliolinites neogenicus Khan, Bera M et Bera S, sp. nov.

Litsea cf. salicifolia Khan et al., 2011 (Lauraceae)

Armatella cinnamomicola Hansf. on Cinnamomum malabatrum Armatella cryptocaryae Hosagoudar on Cryptocarya bourdillonii Armatella indica Hosagoudar on Cinnamomum malabatrum Armatella katumotoi Hosagoudar on Persea macrantha Armatella litsea (P. Henn.) Theiss. & Sydow on Neolitsea zeylanica Armatella phoebecola Hosagoudar on Phoebe lanceolata Diporotheca litseae Patil on Litsea sp. Amazonia actinodaphnis Hosagoudar on Actinodaphne hookeri Amazonia cinnamomi Hosagoudar on Cinnamomum riparium Armatella balakrishnanii Hosagoudar on Cinnamomum malabatrum Armatella cinnamomi Hansf. & Thirum. on Cinnamomum verum Meliola beilschmiediae Yamam. var. cinnamomicola Hosagoudar on Cinnamomum malabatrum Meliola drepanochaeta Sydow var. insignis Hosagoudar on Litsea insignis Meliola floridensis Hansf. on Persea macrantha Meliola floridensis Hansf. var. pudukadensis Hosagoudar on Persea macrantha Meliola linderae Yamam. on Actinodaphne hookeri Meliola litseae Sydow & Sydow var. florubundae Hosagoudar on Litsea floribunda Meliola litseae Sydow & Sydow var. insignis Hosagoudar on Litsea insignis Meliola litseae Sydow & Sydow var. keralense Hosagoudar on Litsea stocksii var. glabrescens Meliola litseae Sydow & Sydow var. microspora Hosagoudar on Litsea floribunda Meliola litseae Sydow & Sydow var. rotundipoda Hansf. on Litsea coriacea Meliola machili Yamam. on Persea macrantha Meliola neolitseae Yamam. on Neolitsea scrobiculata Meliola pudukadensis Hosagoudar on Litsea sp. Meliola ramacharii Hosagoudar on Persea macrantha Meliola irypiocariicoia on Cryptocarya bourdilloni Mieliola sempeiensis on Litsea sp.

the Eocene and Miocene sediments (Table 1). So, based on present and earlier records, it is observed that this fossil fungal genus has not changed its host preference at the family level and still continues to be associated with the same host family since Eocene.

63

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