Biodiversity and Conservation 9: 393–402, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands. Biodiversity and distribution of fungi associated with decomposing Nypa fruticans KEVIN D. HYDE1 and SITI A. ALIAS2 1 Centre for Research in Fungal Diversity, Department of Ecology and Biodiversity, The University of Hong Kong, Pokfulam Road, Hong Kong; 2 Institute of Biological Sciences, University of Malaya, Kuala Lumpur, 50603, Malaysia Received 30 April 1999; accepted in revised form 20 July 1999 Abstract. Fungi associated with the decomposition of Nypa fruticans in Malaysia are under investigation. Forty-one fungi have been identified including 35 ascomycetes, four mitosporic fungi and two basidiomycetes. The distribution of intertidal fungi on palm structures including leaves, leaf veins, rachides, petiole bases, and inflorescences, and fungi on terrestrial parts have also been examined. No fungi were found on the leaf material, although several fungi were found on the leaf midribs, and possible reasons for this are given. Very few taxa developed on the inflorescences, but those that were present were abundant. The greatest density of fruiting structures occurred on the rachides, and the greatest diversity of fungal species occurred on the petiole bases. The terrestrial fungi differed from the intertidal fungi, although Linocarpon nipae occurred in both habitats. Reasons for the differences in fungal numbers and diversity on the various palm parts are discussed. The diversity of fungi at Morib mangrove was low when compared to previous studies on fungi on Nypa palm at Kampong Api Api in Brunei and in this study at Kuala Selangor mangrove in Malaysia. Key words: host specificity, marine fungi, palms, saprobes Introduction There have been relatively few studies on the fungi associated with Nypa palm (Nypa fruticans), which is a common mangrove species in South East Asia where it can form extensive stands (Tomlinson 1986). Tirisporella beccariana (as Sphaeria beccariana) was the first fungus reported from Nypa fruticans (Cesati 1880) and, although not reported as so, was almost certainly intertidal in origin. The second taxon reported from Nypa palm was Astrosphaeriella nipicola (as Melanopsamma nipaecola), and this is a terrestrial non-marine species (Hyde and Fröhlich 1998). Subsequently, as few as four other taxa have been reported from aerial parts of this host (Hyde and Alias 1999). The first report of fungi from intertidal fronds of Nypa palm was that of Hyde (1988) who reported Linocarpon appendiculatum, L. livistonae and L. nipae. Two further intertidal species of Linocarpon were described in a monograph on the genus by Hyde (1992c). Hyde and Nakagiri (1989) also reported Oxydothis nypae from 394 ageing or cut fronds of Nypa palm in the intertidal region. Oxydothis has since been monographed (Hyde 1994b), and O. nypae remains the only intertidal species of the 41 species accepted in the genus. Subsequent papers by Hyde and co-workers have described or listed several new species from intertidal Nypa palm (Hyde 1988, 1991a,b, 1992a,b,c, 1993; Hyde and Sutton 1992; Jones et al. 1996) and these are listed in Table 1, with their distribution and appropriate references. A relatively large number of fungi (59) are now known from Nypa palm, and many of the species may be specific to this host. In this study we have investigated the fungi associated with the decomposition of Nypa fruticans in Kuala Selangor and Morib mangroves, in peninsular Malaysia. Both aerial and intertidal parts of the palm have been examined and a quantitative analysis of the fungi occurring on various parts of the mangrove palm has been made. Percentage occurrence is calculated as in Hyde (1992a). Materials and methods Visits were made to Morib mangrove and Kuala Selangor mangroves on 8 July 1997 and 12 July 1997 respectively. A suitable well-developed stand of Nypa fruticans was selected and decomposing samples were collected randomly from intertidal and aerial parts of the palm. Care was taken to select decomposing parts in each habitat. Intertidal inflorescences, leaves, leaf veins, rachides, and leaf base material were collected from or close to the mangrove floor, while aerial rachides were collected well above the high tide mark. All samples were returned to the laboratory in snap lock plastic bags. Palm parts were incubated separately in sterile plastic boxes on moist sterile tissue paper and incubated for up to 7 days during which time they were examined for higher fungi. The fungi were identified and voucher slides of the specimens are held at the Institute of Biological Sciences, at the Universiti of Malaya, with some replicates at HKU(M). Results Forty-one fungi were identified in this study associated with decomposing parts of the mangrove palm Nypa fruticans. Thirty-eight species were intertidal species, while a further 3 species are probably confined to aerial parts. The intertidal fungi included 32 ascomycetes, 4 mitosporic fungi and 2 basidiomycetes (Tables 2 and 3). There were low numbers of aerial fungi (as it was very dry at the time of collecting) and the 3 species encountered were ascomycetes. The inflorescences were woody and were the only samples that were colonised by marine borers. The greatest diversity of fungi, which comprised mostly ascomycetes, occurred on the intertidal leaf bases, followed by the intertidal rachides (and the upper petiole) Table 1. Fungi associated with Nypa fruticans. Taxa Aerial or intertidal Palm part Known distribution on Nypa References Aniptodera chesapeakensis Shearer & M.A. Mill. Aniptodera intermedia K.D. Hyde & Alias Aniptodera nypae K.D. Hyde Anthostomella nypae K.D. Hyde, B.S. Lu & Alias Anthostomella nypensis K.D. Hyde, B.S. Lu & Alias Anthostomella nypicola K.D. Hyde, B.S. Lu & Alias Apioclypea nypicola K.D. Hyde Arecophila nypae K.D. Hyde Astrosphaeriella nipicola (Cooke & Massee) K.D. Hyde & J. Fröhl. Astrosphaeriella nypae K.D. Hyde Astrosphaeriella striatispora (K.D. Hyde) K.D. Hyde Carinispora nypae K.D. Hyde Cucullosporella mangrovei (K.D. Hyde & E.B.G. Jones) K.D. Hyde & E.B.G. Jones Fasciatispora nypae K.D. Hyde Fasciatispora petrakii (Mhaskar & V.G. Rao) K.D. Hyde Frondicola tunitricuspis K.D. Hyde Halosarpheia abonnis Kohlm. Halosarpheia marina (Cribb & J.W. Cribb) Kohlm. Halosarpheia ratnagiriensis S.D. Patil & Borse Halosarpheia retorquens Shearer & J.L. Crane Halosarpheia viscosa (I. Schmidt) Shearer & J.L. Crane Helicascus nypae K.D. Hyde Herpotrichia nypicola K.D. Hyde & Alias Leptosphaeria australiensis (Cribb & J.W. Cribb) G.C. Hughes I I I I I I I I R B B, In, R B, R B B M M Brunei, Indonesia Malaysia Malaysia Brunei, Malaysia Malaysia Malaysia Malaysia Malaysia Hyde (1989, 1992a) Hyde et al. (1999) Hyde (1994a); this paper Hyde et al. (1999) Hyde et al. (1999) Hyde et al. (1999) Hyde et al. (1998) Hyde (1996) A I I I R R, B L, R, M, B R,B Brunei, Indonesia, Malaysia Brunei, Malaysia Brunei, Indonesia, Malaysia Brunei, Malaysia Hyde & Fröhlich (1998) Hyde (1992a); this paper Hyde (1989) 1992a, 1993; this paper Hyde (1992a, 1993); this paper I I A I I I I I I I I R R R R M B, In, R R R R B,R B Brunei Brunei, Malaysia Malaysia Brunei Malaysia Brunei, Malaysia Brunei Brunei Brunei Brunei; Malaysia Malaysia Hyde (1992a) Hyde (1991a, 1992a, 1993) Hyde and Alias (1999) Hyde (1992a) This paper Hyde (1992a); this paper Hyde (1992a) Hyde (1992a) Hyde (1992a) Hyde (1991b, 1992a); this paper Hyde et al. 1999 I R Brunei Hyde (1992a); Hyde and Jones (1988) 395 396 Table 1. Continued. Taxa Aerial or intertidal Palm part Known distribution on Nypa References Leptosphaeria nypicola K.D. Hyde & Alias Lignincola laevis Höhnk Lignincola longirostris (Cribb & J. Cribb) Kohlm. Lignincola nypae K.D. Hyde & Alias Linocarpon appendiculatum K.D. Hyde I I I I I B, L, M B, R, M B B B, R Hyde et al. (1999) Hyde (1989, 1992a); this paper Hyde (1992a, 1993); this paper Hyde and Alias (1999) Hyde (1988, 1989, 1992a,c, 1993); this paper Linocarpon angustatum Alias & K.D. Hyde Linocarpon bipolaris K.D. Hyde Linocarpon livistonae (Henn.) K.D. Hyde Linocarpon longisporum K.D. Hyde Linocarpon nipae (Henn.) K.D. Hyde Lulworthia grandispora Meyers Lulworthia sp. (300–400 lm) Neolinocarpon globosicarpa K.D. Hyde Neolinocarpon nypicola K.D. Hyde & Alias Nipicola carbonispora K.D. Hyde Nipicola selangorensis K.D. Hyde Oxydothis nypae K.D. Hyde & Nakagiri I I A, I I A, I I I I A I I I B R B R R In, R R B, R R R R B, R Malaysia Brunei, Indonesia, Malaysia Brunei, Malaysia Malaysia Brunei, Malaysia, Indonesia, Papua New Guinea Malaysia Brunei Malaysia Brunei Brunei, Malaysia, Philippines, Thailand Brunei, Indonesia, Malaysia Brunei, Malaysia Brunei, Malaysia Malaysia Brunei Malaysia Brunei, Malaysia, Thailand Oxydothis nypicola K.D. Hyde Phomatospora nypae K.D. Hyde Phomatospora nypicola K.D. Hyde & Alias Rhipidocarpon javanicum (Pat.) Theiss. & Syd. Rosellinia sp. Savoryella lignicola R.A. Eaton & E.B.G. Jones Swampomyces sp. Tirisporella beccariana (Ces.) E.B.G. Jones, K.D. Hyde & Alias Verruculina enalia (Kohlm.) Kohlm. & Volkm.-Kohlm. A I I A I I I R B, M B L B, In, R In, R B Brunei, Malaysia Malaysia Malaysia Indonesia, Philippines Brunei, Malaysia Malaysia Malaysia Hyde and Alias (1999) Hyde (1992a,c) This paper Hyde (1992a,c) Hyde (1988, 1992a,c, 1993); this paper Hyde (1989, 1992a); this paper Hyde (1992a) Hyde (1992a, 1993); this paper Hyde and Alias (1999) Hyde (1992a,b) Hyde (1994a) Hyde (1992a, 1994b); Hyde and Nakagiri (1989); this paper Hyde (1994b); this paper Hyde (1993); this paper Hyde and Alias (1999) Patouillard (1897) Hyde (1992a); this paper This paper This paper I I B R Malaysia, Philippines Brunei Jones et al. (1996); this paper Hyde (1992a) Vibrissea nypicola K.D. Hyde & Alias I B, R Brunei, Malaysia Hyde (1992a); Hyde and Alias (1999); this paper Basidiomycota Halocyphina villosa Kohlm. & E. Kohlm. I In, R Brunei, Indonesia, Malaysia Hyde (1989, 1992a); Hyde and Jones (1988); this paper I I I I I I I I I In R R R B R M M R Malaysia Brunei Brunei Brunei Malaysia Brunei Brunei, Malaysia Brunei, Malaysia Brunei This paper Hyde (1992a) Hyde (1992a) Hyde (1992a) Hyde et al. (1999) Hyde (1992a) Hyde and Sutton (1992); this paper Hyde and Sutton (1992); this paper Hyde and Sutton (1992) I I R B, R Brunei Brunei, Malaysia Hyde (1992a) Goh and Hyde (1999); Hyde (1992a); Hyde et al. (1999) Mitosporic fungi Agerita sp. Cirrenalia pygmea Kohlm. Cirrenalia tropicalis Kohlm. Dictyosporium pelagicum (Linder) G.C. Hughes. Helicorhoidion nypicola K.D. Hyde & Goh Monodictys pelagica (T.W. Johnson) E.B.G. Jones Nypaella frondicola K.D. Hyde & B. Sutton Plectophomella nypae K.D. Hyde & B. Sutton Pleurophomopsis nypae K.D. Hyde & B. Sutton Trichocladium alopallonellum (Meyers & R.T. Moore) Kohlm. & Volkm.-Kohlm. Trichocladium nypae K.D. Hyde & Goh A – aerial, I – intertidal, B – Base of petiole, In – Inflorescence, R – rachid, M – midrib of leaf, L – leaf. 397 Taxa Inflorescence (15) Leaf (20) Leaf midrib (20) Rachis (20) Petiole base (20) Aerial parts (11) Aegerita sp. Aniptodera intermedia Arecophila nypae Astrosphaeriella striatispora Carinispora nypae Halosarpheia abonnis Helicascus nypae Helicorhoidion nypicola Herpotrichia nypicola Leptosphaeria nypicola Lignincola longirostris Lignincola nypae Linocarpon appendiculatum Linocarpon angustatum Linocarpon nipae Lulworthia grandispora Neolinocarpon nypicolum Nypaella frondicola Oxydothis nypae Oxydothis nypicola Phomatospora nypae Phomatospora nypicola Plectophomella nypae Rosellinia sp. Savoryella lignicola Swampomyces sp. Trichocladium nypae Vibrissea nypicola Total no. species 3 – – – – – – – – – – – – – – 1 – – – – – – – 12 1 – – – 4 – – – – – – – – – – – – – – – – – – – – – – – – – – – – 0 – – 1 16 – 1 – – – 2 – – – – – – – 3 – – – – 5 – – – – – 6 – – – 2 1 – – – – – – – 14 – 8 – – – 13 – – – – – 1 – 3 1 8 – 1 – 1 – – 1 2 6 1 6 1 1 2 – – – – – – 1 1 – 3 – 1 – 1 15 – – – – – – – – – – – – – – – – 20 – – 4 – – – – – – – – 2 398 Table 2. Frequency of occurrence of fungi associated with decomposing Nypa fruticans at Kuala Selangor mangrove. Number of samples examined in brackets. Table 3. Frequency of occurrence of fungi associated with decomposing Nypa fruticans at Morib mangrove. Number of samples examined in brackets. Taxa Inflorescence (15) Leaf (20) Leaf midrib (20) Rachis (20) Petiole base (20) Aerial parts (11) Aniptodera nypae Anthostomella nypae Anthostomella nypensis Anthostomella nypicola Astrosphaeriella nypae Astrosphaeriella striatispora Carinispora nypae Fasciatispora petrakii Halocyphina villosa Halosarpheia marina Lignincola longirostris Lignincola laevis Linocarpon appendiculatum Linocarpon angustatum Linocarpon livistonae Linocarpon nipae Lulworthia sp. Oxydothis nypae Neolinocarpon globosicarpa Neolinocarpon nypicola Tirisporella baccariana Total no. species 2 – – – – – – – 1 1 – – – – – – – – – – – 3 – – – – – 1 – – – – – – – – – – – – – – – 1 – – – – – 10 – – – – – 9 – – – – – – – – – 2 5 – – – 1 2 – – – – – – 1 – – 2 1 – – – – 6 9 1 1 1 1 – 1 – – 1 1 3 – 2 1 – – 1 1 – 3 14 – – – – – – – 3 – – – – – – – 3 – – – 5 – 3 399 400 (Tables 2 and 3). Very few fungi occurred on the leaf material and those that did were mainly confined to the midrib. Although the diversity of fungi on the inflorescences was relatively low, the fungi that were present were abundant. Discussion This study compares the fungi occurring on the intertidal and terrestrial (non-marine) fronds of Nypa palm, but does not investigate vertical distribution patterns within the tidal range. The only other study that has looked at the mycota of intertidal Nypa palm is that of Hyde (1992a), who reported 43 intertidal fungi from decaying fronds in Brunei. In this study 41 intertidal fungi are reported. The most common intertidal species reported by Hyde (1992a), were Linocarpon appendiculatum, Oxydothis nypae, Lignincola laevis, Linocarpon nipae and Astrosphaeriella nypae. In this study the intertidal species Aniptodera nypae, Astrosphaeriella striatispora and Lignincola laevis were common at Morib mangrove and Astrosphaeriella striatispora, Linocarpon appendiculatum, Oxydothis nypae and Rosellinia sp. were common at Kuala Selangor mangrove. It is not clear why the common species should vary from one mangrove site to another, but Astrosphaeriella striatispora, Lignincola laevis, Linocarpon appendiculatum and Oxydothis nypae were common at two of the three sites investigated. Hyde (1992a) did not look at the fungi on aerial fronds, nor did he differentiate between palm parts. In this study only 3 fungi were identified from aerial (nonmarine) parts, and this is markedly low. Studies on terrestrial palms have shown them to have an extremely rich and diverse mycota (Fröhlich and Hyde 1999). The period before collecting, however, had been extremely dry and this is probably the reason for the low numbers of fungi collected. Neolinocarpon nypicolum was notably common on dead and senescent terrestrial petioles. We believe this is an endophyte that changes to a saprobic lifestyle once the fronds die. In this way not only is it the first fungus to colonise dead fronds, but it can utilise the moisture in the senescent petioles before they dry out. Different parts of the fronds (i.e. leaves, leaf midribs, petioles, petiole bases) were found to support different fungi. This indicates that some fungi may preferentially develop on certain tissue types. In fungal biodiversity studies it is therefore important to examine different plant structures. Similar results have been found with terrestrial palms (Yanna 1997). The fungi occurring on aerial non-marine, as compared to intertidal parts of Nypa palm differed, with only Linocarpon nipae occurring in both habitats. This is in agreement with previous studies where intertidal fungi in the mangrove were found to differ from fungi on aerial parts of the same mangrove host (e.g. Sabada et al. 1995; Poon and Hyde 1998). The fungi developing on decaying terrestrial palm fronds have been found to differ considerably from those (marine fungi) growing on intertidal 401 fronds (Yanna 1997). This is not surprising, as fungi growing on intertidal parts must have the ability to grow and reproduce in saline conditions. Marine fungi generally grow more slowly than terrestrial fungi, but have the ability to grow and reproduce when totally or periodically submerged in seawater or estuarine water (Kohlmeyer and Kohlmeyer 1979). The large number of fungi known to occur on Nypa palm is remarkable considering that Hawksworth (1991) has calculated world numbers of fungal species to be in the region of 1.5 million, based on, amongst other things, a ratio of one plant host to six fungal species. The numbers are not incongruous when compared to the large numbers of fungi known from other palm species (e.g. Livistona chinensis (Yanna 1997); Licuala spp. (Fröhlich and Hyde 1999). However, considering that most of the fungi found on Nypa palm are intertidal and do not appear to occur on non-palm hosts, the evidence indicates that there are probably more than 40 species that are unique to Nypa fruticans. There are only two other species of mangrove palm which may support these intertidal palm fungi (i.e. Calamus erinaceus, Oncosperma tigillarium; Tomlinson 1986), and although there are no published reports, limited examination of decaying parts of these intertidal hosts by KDH have not revealed many similar fungi. The large number of probable host specific fungi occurring on Nypa fruticans is significant in relation to global fungal diversity estimates (Hawksworth 1991). This emphasises the pressing need for a detailed study of the fungi on other intertidal palm hosts. Acknowledgements We would like to thank Helen Leung and A.Y.P. Lee for technical assistance. Siti Aisyah Alias would like to thank the Institute of Biological Sciences, Universiti Malaya for the award of a grant to study on Nypa fruticans. References Cesati V (1880) Mycetum in itinere Borneensi lectorum a cl. od. Baccari. Atti Accad. Sci. Fis. Mat. Napoli 8: 1–28 Fröhlich J and Hyde KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodiversity and Conservation 8: 977–1004 Goh TK and Hyde KD (1999) A synopsis of Trichocladium species, based on the literature. Fung. Divers. 2: 101–118 Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol. Res. 95: 641–655 Hyde KD (1988) The genus Linocarpon from the mangrove palm Nypa fruticans. Trans. Mycol. Soc. Japan 29: 339–350 Hyde KD (1989) Intertidal fungi from north Sumatra. Canadian Journal of Botany 67: 3078–3082 Hyde KD (1991a) A new amphisphaeriaceous fungus from intertidal fronds of Nypa fruticans. Trans. Mycol. Soc. Japan 32: 265–271 402 Hyde KD (1991b) Helicascus kanaloanus, Helicascus nypae sp. nov. and Salsuginea ramicola gen. et sp. nov. from intertidal mangrove wood. Bot. Mar. 34: 311–318 Hyde KD (1992a) Fungi from decaying intertidal fronds of Nypa fruticans, including three new genera and four new species. Bot. J. Linn. Soc. 110: 95–110 Hyde KD (1992b) Fungi from Nypa fruticans: Nipicola carbospora gen. et sp. nov. (Ascomycotina). Crypt. Bot. 2: 330–332 Hyde KD (1992c) Fungi from palms. I. The genus Linocarpon, a revision. Sydowia 44: 32–54 Hyde KD (1993) Fungi from palms. V. Phomatospora nypae sp. nov. and notes on marine fungi from Nypa fruticans in Malaysia. Sydowia 45: 199–203 Hyde KD (1994a) Fungi from palms. XII. Three new intertidal ascomycetes from submerged palm fronds. Sydowia 46: 257–264 Hyde KD (1994b) Fungi from palms. XIII. The genus Oxydothis, a revision. Sydowia 46: 265–314 Hyde KD (1996) Fungi from palms. XXIX. Arecophila gen. nov. 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