Fungal diversity and the pattern of fungal colonization of Anacardium occidentale leaf litter

Mycology An International Journal on Fungal Biology ISSN: 2150-1203 (Print) 2150-1211 (Online) Journal homepage: https://www.tandfonline.com/loi/tmyc20 Fungal diversity and the pattern of fungal colonization of Anacardium occidentale leaf litter S. Shanthi & B.P.R. Vittal To cite this article: S. Shanthi & B.P.R. Vittal (2012) Fungal diversity and the pattern of fungal colonization of Anacardiumoccidentale leaf litter, Mycology, 3:2, 132-146 To link to this article: https://doi.org/10.1080/21501203.2011.654350 Copyright 2012 Mycological Society of China Published online: 23 Jan 2012. Submit your article to this journal Article views: 809 Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalinformation?journalcode=tmyc20

Mycology Vol. 3, No. 2, June 2012, 132 146 Fungal diversity and the pattern of fungal colonization of Anacardium occidentale leaf litter S. Shanthi* and B.P.R. Vittal Centre for Advanced Studies in Botany, University of Madras, Guindy Campus, Chennai 600025, India (Received 3 August 2011; final version received 19 December 2011) The diversity and succession of microfungi associated with decomposing leaf litter of Anacardium occidentale L. are described from samples collected from a scrub jungle at Adyar, Chennai, at bimonthly intervals between February 2001 and April 2003. To follow fungal colonization patterns, leaf litter samples were collected from three strata representing progressive decomposition stages. The occurrence, distribution, relative frequency and abundance of fungi colonizing the leaf litter of the respective layers were monitored using the moist chamber incubation technique. The study yielded 142 taxa/ 102 genera and the successional stages among the fungal assemblages were observed during the decomposition. Although several fungal species were common components of the mycoflora of all three layers, each layer had its own characteristic species assemblage and periodicity of sporulation. Beltrania rhombica, Subramaniomyces fusisaprophyticus, Beltraniella portoricensis were the dominant and regular inhabitants throughout the study. Keywords: Anacardium occidentale; fungal diversity; leaf litter; microfungi; moist chamber incubation technique; succession; pattern of colonization Introduction Leaf litter is an important component of all the ecosystems and a major source of soil organic matter (Reed et al. 2007). Litter protects and buffers the upper soil horizons against microhabitat fluctuations, soil erosion and compaction, and creates a microclimate that favors fungal fruiting-body production (Eaton et al. 2004). Litter decomposition enables nutrient cycling, humus formation, soil respiration, sustained plant growth and soil organic matter formation (Cooke and Rayner 1984; Eijsackers and Zehnder 1990; Parsons and Congdon 2008). In situ litter decomposition processes are controlled by a combination of abiotic and biotic factors, such as climate, plant litter quality, soil composition and the decomposer community (Heal et al. 1997; Lavelle et al. 1993). Fungi play a vital role in leaf litter decomposition because they are primary decomposers of lignin, which is the major structural component of the litter and often limits the decomposition process (Osono 2007), while other organisms rarely decompose (Cooke and Rayner 1984). Leaf litters from different host plants vary in their chemical content and may influence the fungi growing on it (Duong et al. 2008). During the litter decomposition process, the colonization of various fungal assemblages are sequentially replaced over time (Paulus et al. 2006; Kannangara et al. 2007). Hudson (1968) emphasised the importance of fungal successional patterns and found that Nigrospora and Curvularia spp. were more commonly encountered as primary saprobes in the tropics than in temperate regions. Since Hudson s work, several other studies have investigated the species diversity, colonization, and the richness of litter-inhabiting micro- and macrofungi in tropical and subtropical forests (Bills and Polishook 1994; Lodge and Cantrell 1995; Lodge 1996, 1997; Sharma et al. 1995; Paulus et al. 2003, 2006; Rambelli et al. 2004; Santana et al. 2005) and the succession of fungal assemblages during leaf litter decomposition (Promputtha et al. 2002; Tokumasu and Aoki 2002; Fryar et al. 2004, Tang et al. 2005; Paulus et al. 2006, Seephueak et al. 2010). Leaf litter decomposes faster in tropical soils and there is less soil organic carbon accumulation than in temperate soils (Takeda 1998). Recently, Osono et al. (2009) studied fungal succession and decomposition of Shorea obtusa leaves in a tropical seasonal forest in northern Thailand and recorded Trichoderma asperellum and Aspergillus sp. frequently during the decomposition process. Shirouzu et al. (2009) found that Subramaniomyces fusisaprophyticus and Rhinocladiella intermedia are early colonisers, and Trichoderma koningii and T. harzianum are later colonisers in the succession on the decomposing leaves of Quercus myrsinefolia. Anacardium occidentale (cashew, Anacardiaceae), a native to South America, was introduced to India four centuries ago. Cashew is an important cash crop and India ranks second to Brazil in production, with 300,000 ha under cultivation. When the plant is grown in coastal sand *Corresponding author. Email: shanthisomasundaram@gmail.com ISSN 2150-1203 print/issn 2150-1211 online 2012 Mycological Society of China http://dx.doi.org/10.1080/21501203.2011.654350 http://www.tandfonline.com Published online 23 Jan 2012

Mycology 133 dunes, it is a slow-spreading, evergreen, perennial, bushy, low-branched tree, about 2.8 4.2 m tall, and its lower branches often bend to touch the heavy litter accumulation on the ground. Coastal sandy soils have poor structural stability, a sparse microbial community and poor nutrient retention capacity (Parrotta 1999; Sall et al. 2003). Organic matter decomposition is the main source of ecosystem energy in these soils and plays a major role in the soil plant relationship (Lavelle and Spain 2001; Diallo at al. 2005). Cashew plantations have vast potential for making organic biomass available for recycling and the leaf litter is extensively used for composting (Panda et al. 2010). The quantity of litter available under different age groups of cashew plantations ranged from 1.38 to 5.2 tonnes/ha/year for 10 15 and 25 40-year-old plantations, respectively (Kumar and Hegde 1999). Despite its high litter production and its utility in composting, except for studies on ex situ biodegradation of leaf litterof A. occidentale in the humid tropics of Kerala (Isaac and Nair 2005) and a decomposition dynamics study in coastal habitats of Orissa (Panda et al. 2010), no systematic attempts have been made to investigate the fungal diversity associated with the leaves and litter of this plant during the decomposition process in coastal sand dunes. Patterns of microfungal assemblage colonization associated with decomposing leaf litter of A. occidentale, a non-native tree growing in coastal areas of a man-made ecosystem, is reported in this paper. The principal aims of this study were (1) to evaluate the fungal diversity of A. occidentale leaf litter in terms of the composition of fungal communities during the decomposition process, and (2) to describe the successional patterns of fungi over a 27-month period of leaf litter decomposition and to estimate species richness at different stages of litter decomposition. Materials and methods Study site The study site was a 20-year-old cashew plantation of the Theosophical Society, located at Adyar, southeast of Chennai, India, (13.08 N, 80.19 E), along the coast of Bay of Bengal. The cashew trees were evergreen, 2.8 4.2 m tall and 16 21 cm in diameter at chest height, with a natural, heavy undisturbed accumulation of surface leaf litter. The study site encompassed an area of 266 acres, formerly occupied by three distinct vegetation types: mangroves, psammophytes and tropical dry evergreen elements, and classified as tropical dry evergreen vegetation with sandy loam soil of high porosity. The vegetation was mostly dominated by A. occidentale, occupying 120 acres. About 60% of the litter floor was comprised of cashew leaf litter. The climate of the sampling site was hot and humid for 8 months of the year and received rainfall between October to mid-december due to the onset of north-east monsoon. The summer lasted from March to June. Mean annual precipitation is 913.1 mm; average maximum and minimum temperatures are 39.43 and 20.68 C, respectively, and the mean annual temperature is 28.6 C (84 F) (Figure 1). Sampling procedure To measure fungal diversity and colonization pattern, litter samples of A. occidentale were collected every second month from 2 nd February 2001 through to 4 th April 2003 from three strata of litter decomposition: L (litter), F1 (fermentation 1) and F2 (fermentation 2), based on the progressive stages of decomposition (Figure 2). The layer classification was similar to previous definitions (Watson et al. 1974, Visser and Parkinson 1975). The L layer mostly consisted of the uppermost, recently fallen dry senescent leaves lying loosely on the surface and without any visible fungal growth. F1, which occurs immediately below the L layer, had a high moisture content and consisted of dark brown to grey leaves, usually compacted, and showed visible fungal growth, suggesting that they were under active decomposition. F2 was the lowermost layer between the F1 layer and the soil surface, with leaves in advanced stages of decomposition, that were usually fragmentary, very thin and tightly compressed and also moldy. Altogether 14 time intervals were sampled during the study. The litter leaves in the three different layers did not differ significantly in size (12 18 cm) and, therefore, it was considered valid to directly compare their species richness. Twenty leaves from each of the three different strata were randomly selected and incubated in sterile moist chambers for a period of 48 96 h and examined under a stereomicroscope from the 48 th hour onwards. A total of 840 leaves were studied. All fungi in the sporulating state after moist chamber incubation were examined and identified down to species level. Identification was based on morphological examinations under stereo and compound microscopes (Manoch et al. 2008), using various keys and references (Booth 1971; Ellis 1971, 1976; Matsushima 1971, 1975, 1980, 1981, 1983, 1985, 1987, 1989, 1993, 1995; Pirozynski 1962; Pirozynski and Hodges 1973; Sutton 1980). If necessary, species were cultured on 2% malt extract agar medium. All fungal cultures were deposited in Madras University Fungal Germplasm Collection. Statistical analysis Species richness, diversity and pattern of colonization, periodicity of occurrence (POC) and frequency of occurrence (FOC) for each fungal species were calculated. The POC was the number of samplings in which a taxa was recorded relative to the total samplings (14). The FOC was calculated as on the basis of the number of leaves on which a particular taxon was recorded relative to the total leaves

134 S. Shanthi and B.P.R. Vittal Figure 1. Monthly average temperatures and relative humidity in the study area. Figure 2. Leaf litter samples of Anacardium occidentale collected from the sampling site at three different decomposition layers: (a)llayer,(b)f1layerand(c)f2layer. (20) examined per each category (Yanna et al. 2002; Wang et al. 2008). The data were expressed as periodicity of occurrence percentage (%POC) and percentage frequency of occurrence (%FOC). Species diversity was measured using species diversity indices (species richness and species evenness). Species richness was the number of fungal species in each stratum. Species evenness refers to the contribution (relative abundance or equability) of individuals. A Shannon diversity index was used to estimate species diversity and evenness. Similarities among fungal communities from different stages of litter decay over the sampling period were estimated using Sørensen s similarity index (S). To evaluate the effect of sampling date of layers on the number of species, diversity index, evenness and the frequencies of occurrence of individual fungal species, generalised linear

Mycology 135 modeling through linear regression was utilised. The correlation between climatic factors temperature, humidity and rainfall and species diversity was also tested using Pearson s correlation. Because the data were percentages, a χ2 test was applied to examine the difference in the frequency of occurrence of individual fungal taxa between different layers of decomposing litter. The relative similarities among the fungal assemblages during the different stages of decomposition were grouped using average linkage cluster analysis from SAS version 9.2. Calculations were based on average percentage frequency of occurrence and group average as the cluster distance measure and linkage method, respectively. Results Fungal taxonomic composition A total of 840 decaying leaves of A. occidentale at three stages of decomposition were examined and 142 taxa belonging to 102 genera were identified during the experimental period (Table 1). Among the total number of species recorded, fungal taxa from the L layer (86 species) was considerably less than those from the F1 (97 species) or F2 (104 species) layers. Seasonal changes in each litter layer were clearly evident (Figure 3). The number of taxa recorded per sampling was high in F2 (ranging 12 42 species) compared with the L (15 37 species) or F1 (14 36 species) layers (Figure 3). Among the three layers, the maximum and minimum taxa per sampling was recorded during October 2002 (42 taxa) and February 2001 (12 taxa), respectively, from the F2 layer. The total number of fungi and their composition recorded during each sampling (L, F1 and F2) are presented in Table 2. Mitosporic fungi were the dominant category (94.3%) followed by zygomycetes (5.3%) and basidiomycetes (0.4%). Species richness The total number of fungal assemblages recorded per sampling from the L, F1 and F2 layers ranged between 32 and 58 species (Table 2). The species richness, in the case of the L layer, gradually increased from 15 20 taxa and reached maximum during April 2002 (37 taxa), plateaued at 26 27 taxa and then declined later. A more or less similar observation was made for the F1 litter whereas the species richness for the F2 layer was greater during the October 2002 sampling. The Shannon diversity index increased from the beginning of the study and reached a maximum of 4.8 and 4.9 during April 2002 for the L and F1 layers, respectively, and thereafter decreased gradually. The highest diversity index value was observed during October 2002 (4.89) for the F2 litter. The occurrence of fungal communities recorded from the L and F1 layers peaked (420 540 days) before the F2 layer (600 660 days) (Table 3). Species evenness was relatively constant throughout the decomposition process, an indication that species were evenly distributed. Species richness was significantly correlated (p < 0.05) with mean annual temperature (r = 0.594, n = 14, p = 0.000538) but showed no correlation (p > 0.05) with relative humidity (r = 0.23, n = 14, p = 0.902) or mean annual rainfall (r = 0.053, n = 14, p = 0.998). The Sørensen s similarity index was greatest during August 2002 (0.7878). The similarity indices of the L and F2 layers (0.944) were higher than other combinations: L and F1 layer (0.732) or F1 and F2 layer (0.697) (Table 3). Temporal changes in fungal diversity and occurrence When species composition of the three strata was compared, some species were common to all the three strata (55 of 142 species). A few species appeared in two strata, while some were restricted to a single stratum. About 37% of taxa were observed in one of the three litter strata. Although many fungi were found in all three strata, their POC values varied (Table 1). When compared, the occurrence distribution of the fungal taxa over the sampling period for the three strata of litter, the majority recorded lower POC values (Figure 4). Taking the average percentage frequency of occurrence as an index of colonizing efficiency of a species, the most active colonisers in the LlayerwereBeltraniella portoricensis, Subramaniomyces fusisaprophyticus, Beltrania rhombica, Circinotrichum maculiforme, Gyrothrix circinata, Parasympodiella laxa, Aspergillus japonicus and Thozetella tocklaiensis, in that order. In the F1 layer, the most efficient colonisers were B. portoricensis, S. fusisaprophyticus, B. rhombica, G. circinata, T. tocklaiensis, C. maculiforme, Acremonium strictum and Trichoderma harzianum, in that order. B. portoricensis, S. fusisaprophyticus, B. rhombica, G. circinata, T. tocklaiensis, Circinotrichum falcatisporum, A. strictum and Alternaria alternata were the active colonisers in the F2 layer. When the FOC of the dominant taxa were compared, B. rhombica (41.43%) and S. fusisaprophyticus (50.95%) had the highest value and were regular inhabitants in all samples from the three litter strata (Figure 5). Colonization patterns on different layers of litter Based on POC values, the dominant species were B. rhombica (100%), B. portoricensis (100%), S. fusisaprophyticus (100%), A. japonicus (85.7%), C. maculiforme (85.7%), Parasympodiella laxa (85.7%) and Dactylaria biseptata (64.29%) on the L litter; B. rhombica (100%), B. portoricensis (100%), S. fusisaprophyticus (100%), G. circinata (85.71) and Penicillium citrinum (71.43%) on F1 litter; B. rhombica (100%), S. fusisaprophyticus (100%), B. portoricensis (85.71%), G. circinata (85.71%), C. falcatisporum (78.57%), C. maculiforme (71.43%),

136 S. Shanthi and B.P.R. Vittal Table 1. Periodicity (%) and average frequency of occurrence (%) of fungal taxa recorded from three layers of leaf litter (L, F1 and F2) with their linear regression showing the effect of sampling dates and the layers on FOC. Periodicity of occurrence (POC) Frequency of occurrence (FOC) Fungal taxa L F1 F2 L F1 F2 Significance of FOC of three layers ZYGOMYCOTA Lichtheimia corymbifera (Cohn) Vuill. 28.57 14.29 14.29 2.86 1.79 2.5 Mucor racemosus Bull. 28.57 7.14 35.71 2.14 0.36 2.86 M. mucedo de Bary & Woron 21.43 35.71 1.79 4.29 ns Rhizopus stolonifer (Ehrenb.) Vuill. 14.29 21.43 1.43 2.14 ns Syncephalastrum racemosum Cohn ex 7.14 7.14 0.36 0.36 ns J. Schröt. ASCOMYCOTA Ascotricha chartarum Berk. 7.14 7.14 0.36 0.36 ns Chaetomium globosum Kunze 14.29 7.14 1.07 0.71 ns C. spirale Zopf 7.14 7.14 0.36 0.36 ns Emericella nidulans (Eidam) Vuill. 14.29 14.29 14.29 0.71 1.79 1.43 ns Meliola sp. 21.43 14.29 2.5 1.79 ns BASIDIOMYCOTA Tetrapyrgos nigripes (Schwein.) E. Horak 7.14 7.14 0.36 0.36 ns T. subcinerea (Berk. & Broome) E. Horak 7.14 0.36 ns MITOSPORIC FUNGI HYPHOMYCETES Acremonium strictum W. Gams 50 57.14 64.28 9.29 11.779 12.14 Acrostalagmus luteoalbus (Link) Zare, 7.14 7.14 35.71 0.36 0.36 2.5 ns W. Gams & Schroers Alternaria alternata (Fr.) Keissl. 50 14.29 64.28 5.71 1.43 10.71 Annellophora phoenicis M.B. Ellis 7.14 7.14 0.36 0.71 ns Aspergillus brasiliensis Varga, Frisvad & 35.71 28.57 35.71 3.21 1.79 1.79 Samson A. flavipes (Bainier & R. Sartory) Thom & 21.43 14.29 7.14 1.43 1.79 1.43 Church A. flavus Link 28.57 7.14 2.5 1.07 ns A. fumigatus Fresen. 7.14 7.14 7.14 0.71 0.71 1.07 ns A. japonicus Saito 85.7 50 71.43 13.93 9.29 9.64 A. nidulans (Eidam) G. Winter 21.43 14.29 21.43 1.43 1.79 1.43 ns A. ochraceus G. Wilh. 7.14 21.43 21.43 0.36 1.43 2.86 A. terreus Thom 21.43 35.71 35.71 1.43 2.5 3.93 Beltrania malaiensis Wakef. 28.57 7.14 1.43 0.71 ns B. rhombica Penz. 100 100 100 46.79 41.43 36.07 Beltraniella portoricensis (F. Stevens) Piroz. 100 100 85.71 65.71 55 49.64 & S.D. Patil Beltraniopsis esenbeckiae Bat. & 14.29 7.14 1.43 0.36 ns J.L. Bezerra Camposporium antennatum Harkn. 14.29 21.43 7.14 2.5 1.79 0.71 ns Chalara aurea (Corda) S. Hughes 7.14 7.14 1.07 1.07 ns Circinotrichum falcatisporum Piroz. 42.86 42.86 78.57 3.93 5.36 15.71 C. maculiforme Nees 85.7 71.43 71.43 23.93 13.21 8.93 C. olivaceum (Speg.) Piroz. 7.14 7.14 0.71 0.36 ns Cladosporium cladosporioides (Fresen.) G.A. 57.14 57.14 50 6.43 6.43 7.5 de Vries C. oxysporum Berk. & M.A. Curtis 28.57 14.29 7.14 2.14 0.71 0.36 ns C. spongiosum Berk. & M.A. Curtis 7.14 7.14 0.36 0.36 ns Cochliobolus australiensis (Tsuda & 7.14 7.14 7.14 0.36 0.36 0.36 ns Ueyama) Alcorn C. hawaiiensis Alcorn 7.14 7.14 0.71 0.71 ns C. lunatus R.R. Nelson & F.A. Haasis 7.14 7.14 50 0.71 0.71 7.5 C. tuberculatus Sivan. 7.14 7.14 0.36 0.71 ns Corynespora citricola M.B. Ellis 7.14 7.14 0.36 0.71 ns (Continued)

Mycology 137 Table 1. (Continued). Periodicity of occurrence (POC) Frequency of occurrence (FOC) Fungal taxa L F1 F2 L F1 F2 Significance of FOC of three layers Curvularia brachyspora Boedijn 7.14 14.29 1.07 0.71 ns Dactylaria biseptata Matsush. 64.29 42.86 35.71 5.36 7.86 3.93 Dicyma vesiculifera Piroz. 28.57 14.29 7.14 2.5 0..71 0.36 Fusarium dimerum Penz. 21.43 14.29 1.43 1.43 ns F. oxysporum E.F. Sm. & Swingle 21.43 35.71 1.79 3.21 ns Gibberella bacata (Wallr.) Sacc. 35.71 14.29 3.21 0.71 ns Gyrothrix circinata (Berk.&M.A.Curtis) 71.4 85.71 85.71 21.43 25.71 17.86 S. Hughes G. podosperma (Corda) Rabenh. 14.29 28.57 35.71 0.71 2.14 4.29 Hansfordia pulvinata (Berk. & 21.43 21.43 14.29 1.07 2.5 1.79 ns M.A. Curtis) S. Hughes Henicospora coronata B. Sutton & 7.14 7.14 0.36 0.71 ns P.M. Kirk Idriella lunata P.E. Nelson & S. Wilh. 14.29 14.29 21.43 0.71 0.71 1.79 Khuskia oryzae H.J. Huds. 14.29 7.14 0.71 0.36 ns Leptosphaerulina chartarum Cec. Roux 7.14 7.14 0.36 0.36 ns Memnoniella echinata (Rivolta) Galloway 14.29 28.57 21.43 0.71 3.57 2.14 Metulocladosporiella musae (E.W. Mason) 28.57 7.14 7.14 2.14 1.07 0.36 Crous, Schroers, J.Z. Groenew., U. Braun & K. Schub. Paecilomyces carneus (Duché & R. Heim) 7.14 7.14 0.36 0.71 ns A.H.S. Br. & G. Sm. Parasympodiella laxa (Subram. & Vittal) 85.7 35.71 35.71 17.5 7.5 8.21 Ponnappa Penicillium citrinum Thom 50 71.43 57.14 7.86 9.64 9.64 P. funiculosum Thom 7.14 21.43 14.29 0.71 3.93 1.07 P. oxalicum Currie & Thom 14.29 14.29 21.43 1.43 1.79 1.43 P. verruculosum Peyronel 21.43 7.14 7.14 2.14 0.36 1.07 ns Phaeotrichoconis crotalariae (M.A. Salam 35.71 50 50 3.57 3.93 7.14 & P.N. Rao) Subram. Pithomyces maydicus (Sacc.) M.B. Ellis 7.14 21.43 7.14 0.36 2.14 1.07 Polyscytalum fecundissimum Riess 7.14 7.14 7.14 0.36 0.36 0.36 ns Pseudobeltrania penzigii Piroz. 21.43 14.29 7.14 1.07 0.71 0.36 ns Pseudocochliobolus eragrostidis Tsuda & 7.14 7.14 1.79 1.43 ns Ueyama Scolecobasidium tshawytschae (Doty & 28.57 21.43 7.14 1.79 3.21 1.07 ns D.W. Slater) McGinnis & Ajello Selenodriella fertilis (Piroz. & Hodges) 7.14 7.14 14.29 0.36 0.36 2.5 ns R.F. Castañeda & W.B. Kendr. Selenosporella curvispora G. Arnaud 7.14 14.29 7.14 0.71 1.07 1.43 Setosphaeria rostrata K.J. Leonard 7.14 14.29 21.43 0.71 1.43 2.14 Stachybotrys chartarum (Ehrenb.) 14.29 7.14 7.14 1.43 0.71 0.71 ns S. Hughes Staphylotrichum coccosporum J.A. Mey. & 7.14 7.14 0.36 0.71 ns Nicot Subramaniomyces fusisaprophyticus 100 100 100 56.42 48.57 47.86 (Matsush.) P.M. Kirk Thozetella tocklaiensis (Agnihothr.) 42.86 57.14 57.14 13.93 19.29 17.5 Piroz. & Hodges Torula herbarum (Pers.) Link 7.14 14.29 0.36 0.71 ns Trichoderma harzianum Rifai 28.57 50 64.28 1.79 10.36 8.21 T. viride Pers. 28.57 50 14.29 3.21 5.36 3.6 Trichothecium roseum (Pers.) Link 7.14 7.14 2.14 2.14 0.71 ns Volutella ciliata (Alb. & Schwein.) Fr. 7.14 7.14 21.43 0.36 1.07 1.79 ns Wiesneriomyces laurinus (Tassi) P.M. Kirk 7.14 14.29 0.71 1.43 ns (Continued)

138 S. Shanthi and B.P.R. Vittal Table 1. (Continued). Periodicity of occurrence (POC) Frequency of occurrence (FOC) Fungal taxa L F1 F2 L F1 F2 Significance of FOC of three layers Zygosporium gibbum (Sacc., M. Rousseau & 28.57 35.71 21.43 1.43 3.57 2.14 E. Bommer) S. Hughes Z. masonii S. Hughes 14.29 42.86 64.28 1.43 4.64 5.71 Z. oscheoides Mont. 14.29 21.43 21.43 0.71 1.79 1.79 COELOMYCETES Lasiodiplodia theobromae (Pat.) Griffon & 35.71 14.29 14.29 3.57 1.79 2.86 Maubl. Pestalotiopsis theae Sawada 35.71 28.57 35.71 3.57 3.21 3.57 Gloeosporium musarum Cooke & Massee 14.29 7.14 7.13 1.07 0.36 1.07 Bartalinia robillardoides Tassi 7.14 7.14 14.29 0.36 0.36 1.79 Colletotrichum dematium (Pers.) Grove 7.14 7.14 7.14 0.36 0.36 1.43 Ciliochorella mangiferae Syd. 21.43 14.29 1.43 0.71 ns Glomerella tucumanensis (Speg.) Arx & E. Müll. 14.29 21.43 14.29 1.07 1.07 1.07 ns p < 0.01, p < 0.05, ns; not significant (p > 0.05). The following are the fungal taxa which appeared in a single litter layer and are not significant. Blakeslea trispora, Thamnostylum piriforme, Annellophora dendrographii, Ellisembia leptospora, Corynespora cassiicola, Graphiopsis chlorocephala, Solosympodiella clavata, Trichoderma koningii, Aschersonia aleyroidis, Pseudolachnea hispidula from L layer. Mycotypha microspora, Cunninghamella echinulata, Alternaria longipes, Gongronella butleri, Leptosphaeria eustoma, Calonectria quinqueseptata, Microdochium griseum, Papulaspora irregularis, Phaeostalagmus tenuissimus, Scolecobasidium humicola, Robillarda sessilis from F1 layer. Chaetomium seminudam, Euantennaria sp., Farrowia seminuda, Aspergillus sydowii, A. tamari, Aureobasidium pullulans, Bipolaris papendorfii, Chlamydomyces palmarum, Cladosporiella cercosporicola, Clonostachys rosea f. rosea, Cylindrocladiella parva, Fusarium arthrosporioides,geomyces pannorum, Helicoma muelleri, Helicosporium griseum, Mammaria echinobotryoides, Monodictys castaneae, M. putredinis, Monographella nivalis, Myrothecium advena, M. roridum, M. verrucaria, Periconia minutissima, P. sacchari, Septonema secedens, Tetraplosphaeria tetraploa, Xepiculopsis graminea, Zalerion maritima, Zygosporium mycophilum, Phoma herbarum from F2 layer. A. japonicus (71.43%), A. strictum (64.28%) and A. alternata (64.28%) on F2 litter. The linear regression to test the effect of sampling date and layers on FOC for individual fungal taxa resulted in A. strictum showing a high significant correlation at p < 0.01 (p = 0.0068) and B. rhombica, B. portoricensis, C. falcatisporum, D. biseptata, Gyrothrix podosperma, T. tocklaiensis, Trichoderma harzianum and T. viride showing a significant correlation at p < 0.05. The effect of sampling date of the litter layers was not significantly correlated with species richness, diversity index or evenness (p > 0.05) (Table 4). The significance of FOC of individual fungal taxa among the layers was tested by a χ 2 test (Table 1). Analysis of the similarity of fungi during the decomposition process using cluster analysis generated a dendrogram which showed three distinct successional fungal communities (Figure 6). Discussion Incubating leaf litter samples in moist chambers and observing fungal development (Webster 1956, 1957; Hering 1965; Hogg and Hudson 1966; Promputtha et al. 2002; Kodsueb et al. 2008; Shanthi and Vittal, 2010a,b; Seephueak et al. 2010) enables one to observe many typical litter fungi in their sporulating state, which may not be evident under cultural methods. The direct method, in which the substratum is examined in the field or laboratory for fruiting bodies, was regarded as a simple and direct approach for taxonomic purposes (Paulus et al. 2003). Therefore, the direct observation method after moist chamber incubation was selected for identifying fungal communities on leaf litter. However, the method is intrinsically biased by the investigator s identification skills and patience. For instance, different isolation media or sample processing techniques, such as particle filtration, could have produced different or even more culturable species (Collado et al. 2007). To understand the pattern of colonization of microfungi on litter, mycologists periodically sample litter and analyse the colonizing mycota. Promputtha et al. (2002) studied the fungal succession on senescent leaves of Mangletia garretti for 56 days and recorded 22 fungal taxa with the fungal community composition differing at each stage of succession. Greater fungal communities were recorded from the mature stages of decomposition (F2 litter). A similar trend was observed by Kodsueb et al. (2008) who studied the succession of the woody litter of Magnolia liliifera for 35 months at bimonthly samplings, where the number of fungal species was higher during the mature stages of the decomposition. On the other hand, species diversity tends to be richest and the number of fungi usually highest during the early and middle stages of colonization; thereafter the number of species begins to decline (Seephueak et al.

Mycology 139 Figure 3. Comparison of the number of species in the L, F1, F2 layers and the total number of species recorded from all three layers at different sampling times. The mean of the number of species with the standard error (n = 20) is as follows: L layer: 21 ± 1.55; F1 layer: 20.93 ± 1.52; F2 layer: 23.29 ± 2.15. Table 2. Date of collection and number of fungi found at each sampling time during the succession study. Sampling date Mitosporic fungi Zygomycetes Ascomycetes Basidiomycetes Total 2/2/2001 34 0 0 0 34 3/4/2001 35 0 0 0 35 5/6/2001 33 2 2 0 37 2/8/2001 42 1 0 0 43 5/10/2001 40 2 2 0 44 4/12/2001 38 3 0 0 41 2/2/2002 47 2 2 0 51 2/4/2002 55 2 1 0 58 4/6/2002 37 1 2 0 40 7/8/2002 27 3 3 0 33 2/10/2002 48 4 1 0 53 6/12/2002 34 4 0 0 38 1/2/2003 24 1 1 2 28 4/4/2003 25 5 2 0 32 Mean ± SE (n = 14) 37.07 ± 2.38 2.14 ± 0.4 1.14 ± 0.26 0.14 ± 0.13 40.5 ± 2.3 2010). Although leaf fall from cashews was observed throughout the year, leaf fall was abundant during June to August. The rate of decomposition was found to be highest for A. occidentale during the rainy season followed by winter and summer months (Manlay et al. 2004, Panda et. al. 2010). The rate of decomposition was greater during the initial 8 months after leaf fall and gradually slowed down thereafter (Shanthi and Vittal, 2010a). Panda et al. (2010) noted that the correlation matrix between loss of leaf litter and measured biotic and abiotic variables during different months was significantly correlated with fungal abundance, rainfall, soil moisture, soil respiration

140 S. Shanthi and B.P.R. Vittal Table 3. Diversity indices of saprobic fungi recovered from A. occidentale leaf litter during the study. Diversity indices Sampling year Richness Shannon s diversity index Shannon s evenness Sampling month L F1 F2 L F1 F2 L F1 F2 Sørensen s similarity index 2001 February 20 16 12 3.646 3.416 2.992 0.844 0.854 0.835 0.412 April 19 21 15 3.513 3.865 3.068 0.827 0.88 0.785 0.6 June 15 15 26 3.255 3.184 3.982 0.833 0.815 0.847 0.514 August 18 23 27 3.468 4.146 4.376 0.832 0.917 0.92 0.615 October 23 24 25 3.908 4.036 4.379 0.864 0.88 0.943 0.568 December 19 19 18 3.748 3.541 3.718 0.882 0.834 0.892 0.366 2002 February 20 27 33 3.586 4.376 4.71 0.83 0.92 0.934 0.588 April 37 36 27 4.846 4.903 4.193 0.93 0.948 0.882 0.724 June 26 19 26 4.434 3.951 4.318 0.943 0.93 0.919 0.6 August 27 17 24 4.137 3.902 4.251 0.87 0.955 0.915 0.788 October 17 23 42 3.373 4.022 4.89 0.825 0.889 0.907 0.245 December 20 19 18 3.638 3.562 3.771 0.842 0.838 0.904 0.5 2003 February 16 14 16 3.247 3.507 3.861 0.812 0.921 0.965 0.643 April 17 20 17 3.318 3.691 3.585 0.812 0.854 0.877 0.688 Mean ± SE (n = 14) 21 ± 1.55 20.93 ± 1.52 23.29 ± 2.15 3.72 ± 0.12 3.86 ± 0.12 4 ± 0.15 0.85 ± 0.01 0.89 ± 0.01 0.89 ± 0.01 0.56 ± 0.04 Shannon diversity index accounts for abundance of species present (H) was calculated via: H = pi.log2 pi (pi: proportion of ith species). Shannon evenness accounts for equability of the species present (E) was calculated via: E = H/lnS (S: total species number). Sørensen s similarity index was calculated via: S = ab+ac+bc abc/a+b+c, where a, b, c are the number of species recorded from L, F1 and F2 leaf litter layers, respectively; ab, ac, bc are the number of species shared by L F1, L F2 and F1 F2 liter stages, respectively; abc the number of species found in all the three layers. Similarity is expressed as values between 0 (no similarity) and 1 (absolute similarity) (Wang et al. 2008).

Mycology 141 Figure 4. Fungal species occurrence distribution at different sampling times. rate, k value and relative humidity. In the present study, temperature was significantly correlated with species diversity, whereas the relative humidity and rainfall were not significantly correlated. The differences in resource quality, such as nitrogen, and the presence of inhibitory tannin concentrations involved in decay are important (Kannangara and Deshapriya, 2005). Other factors that affect the fungal colonisers include leaf thickness, toughness and metabolites (from the plant itself or from endophytes and other fungi), such as glycol, chlorohydrins and bromohydrin (Varma et al. 2004; Paulus et al. 2006) or phenolic compounds in plant cells (Polishook et al. 1996; Sallé et al. 2005; Paulus et al. 2006). The phytochemical content of

142 S. Shanthi and B.P.R. Vittal Figure 5. Comparison of percentage frequency of occurrence of some dominant fungal taxa in the three litter layers. A. occidentale leaves include carbohydrates, tannins, glycosides, saponins, flavonoids, alkaloids, resins and sterols (Abulude et al. 2010). The succession may be strongly affected by nutrient levels of the litter and/or competition between fungi. Species diversity tends to be richest and number of fungi usually highest during the early and middle stages of colonization; thereafter the number of species begins to decline (Tiwari et al. 1994; Seephueak et al. 2010). However, in contradiction, in the present study, diversity was highest in the F2 layer of litter (final stages of colonization) compared with the early and middle stages of colonization (Table 3). Changes in species composition throughout the decomposition process were observed in the present study and communities can be grouped into the three succession stages. In general, many fungi appeared sporadically with low frequency. Only a few species, such as B. rhombica, B. portoricensis, S. fusisaprophyticus, T. tocklaiensis and C. maculiforme, which were constant and frequently isolated from Anacardium litter, are common inhabitants of tropical forest soil (Bills and Polishook 1994; Parungao et al. 2002; Promputtha et al. 2002; Tokumasu and Aoki 2002; Tang et al. 2005; Paulus et al. 2006; Duong et al. 2008, Osono, 2011). Decomposition is often impeded during the dry seasons compared with rainy seasons in tropical seasonal forests (Swift and Anderson 1989), but the retarding effect of seasonal drought was not obvious in the present study. We observed that the sampling date had no significant effect on climate, litter quality or fungal variables of the three layers of litter. No similarity was found either in species diversity and richness or the pattern of colonization of the fungal assemblages between the sampling years 2001 and 2002 (Table 3). The pattern of colonization observed on the leaves and litter of A. occidentale is in general agreement with that outlined by Hudson (1968) for plant remains above the soil, except that mucoraceous fungi were recorded in the early stages of decay rather than at the end of succession. The dominance of mucoraceous fungi, such as Circinella simplex, Rhizopus nigricans and Syncephalastrum racemosum, in the early stages of decay of leaves of Cassia

Mycology 143 Average distance between clusters 40 30 20 10 0 III II I Acremonium strictum L Aspergillus japonicus F1 Penicillium citrinum F1 Aspergillus japonicus F2 Penicillium citrinum F2 Cladosporium cladosporioides L Cladosporium cladosporioides F1 Dactylaria biseptata F1 Parasympodiella laxa F1 Cladosporium cladosporioides F2 Dactylaria biseptata L Circinotrichum facatisporum F1 Penicillium citrinum L Circinotrichum maculiforme F2 Parasympodiella laxa F2 Trichoderma harzianum F2 Circinotrichum maculiforme L Dacty;aria bisepta F2 Trichoderma harzianum L Acremonium strictum F1 Trichoderma harzianum F1 Acremonium strictum F2 Circinotrichum maculiforme F1 Circinotrichum falcatisporum F2 Thozetella tocklaiensis F1 Gyrothrix circinata F2 Thozetella tocklaiensis F2 Gyrothrix circinata F1 Beltrania rhombica F1 Beltrania rhombica F2 Subramaniomyces fusisaprophyticus F1 Beltraniella portoricensis F2 Subramaniomyces fusisaprophyticus F2 Beltraniella portoricensis F1 Aspergillus japonicus L Thozetella tocklaiensis L Parasympodiella laxa L Circinotrichum maculiforme L Gyrothrix circinata L Beltrania rhombica L Beltraniella portoricensis L Subramaniomyces fusisaprophyticus L Figure 6. Dendrogram of fungal assemblages on A. occidentale litter via the average percentage FOC and group average method of cluster analysis. glauca and Euphorbia geniculata has been observed previously (Manoharachary et al. 1976) and was consistent with the scheme of fungal succession proposed by Garrett (1963). According to that scheme, the primary saprophytes to invade are non-cellulytic members of Zygomycota or sugar fungi, which rely upon readily available hexose and pentose sugars and other carbon sources, such as pectin and starch. Hudson (1986) has suggested that the Mucorales, which appear in the final stages of decomposition, are mostly soil inhabiting and are not using simple carbohydrates initially present in the leaves, as these would have been utilised already. A clear successional pattern with the primary colonisers were the foliicolous fungi which were succeeded by true litter inhabiting fungi. On this basis, species belonging to genera, such as Annellophora, Beltrania, Beltraniella, Beltraniopsis, Camposporium, Circinotrichum, Dicyma, Gyrotrhix, Hansfordia, Helicoma, Helicosporium, Idriella, Monodictys, Polyscytalum, Pseudobeltrania, Selenosporella, Solosympodiella, Subramaniomyces, Tetraploa, Torula, Thozetella, Wiesneriomyces and Zygosporium, are considered true litter inhabiting fungi. B. rhombica was reported to be a dominant fungus on leaf litter of tropical plants (Kiffer et al. 1981; Rambelli et al.

144 S. Shanthi and B.P.R. Vittal Table 4. Correlation coefficients for linear relationship between date of sampling and climatic, litter quality and fungal variables for the three layers of leaf litter. Explanatory variable r n Mean annual temperature 0.12 ns 14 Annual precipitation 0.051 ns 14 Mean relative humidity 0.117 ns 14 Species richness 0.211 ns 14 Shannon s diversity index 0.331 ns 14 Shannon s evenness 0.563 ns 14 Sørensen s similarity index 0.205 ns 14 ns, not significant (p > 0.05). 1983; Heredia 1993). B. rhombica and B. portoricensis cause selective loss of holocellulose, are regarded as cellulolytic, occur frequently from Castanopsis and Shorea leaf litter and are common inhabitants of tropical forest soils (Bills and Polishook 1994; Parungao et al. 2002; Promputtha et al. 2002; Tokumasu and Aoki 2002; Tang et al. 2005; Paulus et al. 2006; Duong et al. 2008; Osono et al. 2008, Osono 2011). Osono (2006) emphasised that the phyllosphere fungi are primarily saprobic and are specifically adapted to colonise dead host tissue and decompose litter components. While addressing the succession of fungal assemblages in the decomposition of leaves of Quercus myrsinaefolia, Shirouzu et al. 2009 recorded S. fusisaprophyticus along with Rhinocladiella intermedia as the early colonisers of fallen leaves. The pattern of colonization of fungi was classified into three successive decomposition stages, viz. pioneer, mature and impoverished stages (Osono 2005; Kodsueb et al. 2008). The pioneer communities are typically composed of a larger number of different species occurring at low frequency with no dominant species. Mature fungal communities consist of fewer species with one or two obviously dominant species common to all samples at a similar stage in the development of the fungal community (Dix and Webster 1985). 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