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Preliminary Findings on Identification of Mycorrhizal Fungi from Diverse Orchids in the Central Highlands of Madagascar

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Preliminary Findings on Identification of Mycorrhizal Fungi from Diverse Orchids in the Central Highlands of Madagascar Mycorrhiza DOI 10.1007/s00572-015-0635-6 ORIGINAL PAPER Preliminary findings on identification of mycorrhizal fungi from diverse orchids in the Central Highlands of Madagascar Kazutomo Yokoya & Lawrence W. Zettler & Jonathan P. Kendon & Martin I. Bidartondo & Andrew L. Stice & Shannon Skarha & Laura L. Corey & Audrey C. Knight & Viswambharan Sarasan Received: 8 August 2014 /Accepted: 26 February 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract The Orchid flora of Madagascar is one of the most damage and species loss. The diversity of culturable fungal diverse with nearly 1000 orchid taxa, of which about 90 % are associates, their density, and distribution within the Itremo endemic to this biodiversity hotspot. The Itremo Massif in the orchid hotspot areas will be discussed. Central Highlands of Madagascar with a Highland Subtropi- cal climate range encompasses montane grassland, igneous Keywords Orchidaceae . Fungal symbiont . Rhizoctonia . and metamorphic rock outcrops, and gallery and tapia forests. Tulasnella . Ceratobasidium . Sebacina . In vitro Our study focused on identifying culturable mycorrhizae from epiphytic, lithophytic, and terrestrial orchid taxa to understand their diversity and density in a spatial matrix that is within the protected areas. We have collected both juvenile and mature roots from 41 orchid taxa for isolating their orchid mycorrhi- Introduction zal fungi (OMF), and to culture, identify, and store in liquid nitrogen for future studies. Twelve operational taxonomic About 44 % of all vascular plant species are confined to 34 units (OTUs), of three known orchid mycorrhizal genera, global biodiversity hotspots (Mittermeier et al. 2005). were recognized by analysis of internal transcribed spacer Investing resources to the entire global hotspot could lead to (ITS) sequences of 85 isolates, and, by comparing with spreading of the resources too thinly on the ground, making GenBank database entries, each OTU was shown to have conservation of an entire hotspot area untenable, and there- closely related fungi that were also found as orchid associates. fore, conservation approaches must focus on selected areas of Orchid and fungal diversity were greater in gallery forests and maximum diversity and/or endemism (Murray-Smith et al. open grasslands, which is very significant for future studies 2009). Fenu et al. (2010) proposed the terms Bmicro-hotspots^ and orchid conservation. As far as we know, this is the first (i.e., endemism-rich areas analogous to biogeographic units) ever report of detailed identification of mycorrhizal fungi from and Bnano-hotspots^ (i.e., areas <3 km2 with an exceptional Madagascar. This study will help start to develop a pro- concentration of endemic taxa). By most estimates, Madagas- gramme for identifying fungal symbionts from this unique car is home to 4 % of the world’s plant and animal species all biodiversity hotspot, which is undergoing rapid ecosystem confined to just 0.4 % of the Earth’slandsurface,earningits reputation as one of the top five biodiversity Bhotspots^ (Tyson 2000). About 90 % of Madagascar’s natural vegetation : : : K. Yokoya J. P. Kendon M. I. Bidartondo V. Sarasan (*) has been cleared or permanently altered, and the remaining Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK 10 % is by no means secure. Roos et al. (2004) studied the e-mail: [email protected] vascular plants in the Malesian Islands and observed that spe- – L. W. Zettler : A. L. Stice : S. Skarha : L. L. Corey : A. C. Knight cies area relationships of families are dependent on species Department of Biology, Illinois College, 1101 West College Avenue, number; they found that island surface area is a predictor for Jacksonville, IL 62650, USA island percent endemism in the study area. Madagascar, the world’s second largest island, has 10,000–12,000 vascular M. I. Bidartondo Department of Life Sciences, Imperial College London, South plant species, of which roughly 1 in 10 (about 1000) are or- Kensington Campus, London SW7 2AZ, UK chids and about 90 % of which are endemic (Tyson 2000; Mycorrhiza Moat and Smith 2007). The Itremo Massif within the Central flora and fauna. The area covered by the study represented Highlands is a Bmicro-hotspot,^ home to more than 50 orchid around 13 km2 both within and adjacent to the protected area taxa of which the majority are endemic and some species are (Fig. 1). locally endemic (e.g., Angraecum protensum, Angraecum In light of the ongoing demise of tropical ecosystems in magdalenae). Madagascar and worldwide, there is an urgent need to docu- Itremo Massif consists of a plateau of mixed igneous and ment and safeguard the full gamut of life forms in the land- metamorphic rock at an elevation of 1400–1923 m above sea scape, and to understand how these biotic agents interact with level. The average temperature is in the range of 18–21 °C, one another in this age of extinction. Among angiosperms, annual rainfall of 1416 mm with a 4–6-month dry season. orchids are particularly vulnerable given their dependency Savanna is the dominant habitat, with humid gallery forest, on other organisms—namely mycorrhizal fungi and insect remnant tapia (Uapaca bojeri) forest and rocky and montane pollinators—to complete their life cycles in nature (Swarts moorland habitats also present. The raising of cattle is com- and Dixon 2009). Thus, studying these connections becomes monplace in the region, and burning grassland is practiced crucial for orchid conservation. While orchids have received annually. While some advocate carefully controlled burning considerable study with respect to classification and phyloge- as a management strategy for tapia forest in Itremo and else- netic relationships, other important aspects (e.g., pollination, where in the Central Highlands (Alvarado et al. 2014), other propagation) have received less attention, and this is especial- habitats can be badly affected (Whitman et al. 2011). We ob- ly true of Orchidaceae in Madagascar (Cribb and Hermans served evidence of fire damage on two separate rocky ridges 2009), with a few exceptions (e.g., Nilsson et al. 1992a, b; and speculate that adjacent man-made grass fires were the Whitman et al. 2011). To date, virtually nothing is known cause. In addition to this, illegal mining for precious stones about the identity, distribution, and ecology of orchid mycor- is causing habitat degradation in some areas (Vorontsova et al. rhizal fungi (OMF) in Madagascar, or the physiological roles 2013). Following a proposal in 2008, a 273-km2 area was played by these fungi with native orchids. Madagascar’sre- given Protected Area status in 2012, thanks to Itremo’s unique mote location, coupled with its rugged terrain, continue to Fig. 1 Map depicting the study sites near Itremo in the Central Highlands of Madagascar. Circles Gallery forest dominated by epiphytic orchids, also terrestrial orchids on river banks; squares rocky montane grassland with lithophytic and terrestrial orchids; triangles montane moorland with terrestrial orchids; T terrestrial, L lithophyte, E epiphyte, L/T lithophyte/terrestrial, Cer Ceratobasidium, Seb Sebacina, Tul Tulasnella. Numbers 2, 3, 4, 5,and7 denote sites; solid line depicts core protected area. Site 1 is off the area of this map to the east. No Rhizoctonia-like fungi were isolated from collections at site 6. Image © 2014 Google Earth Mycorrhiza pose challenges to specialists seeking to gain access to orchid- labs in Europe (Kew) and North America (Illinois) will also rich habitats in search of such knowledge. This is especially be discussed. To our knowledge, this is the first report that true for mycologists faced with the burden of expediting fresh documents fungal associates from orchids of different life tissue samples harboring viable fungal material (e.g., forms and diverse ecosystems from Madagascar. pelotons) to the lab for further study. The main objective of this study was to understand symbi- otic relationships of orchids of the Itremo Massif in Madagas- Materials and methods car. This study was conducted to achieve the ultimate goal of producing symbiotic propagules for reintroduction by under- This joint study was conducted between Royal Botanic Gar- standing the role of mycorrhizal fungi in seed germination, dens Kew (Kew) and Illionis College with logistic and taxo- seedling development, and establishment of plants in the wild. nomic support from Kew Madagascar Conservation Centre While orchids throughout Madagascar require study, we chose (KMCC) and Parc Botanique et Zoologique de Tsimbazaza to focus on species inhabiting the Central Highlands—are- (PBZT). More than 40 taxa within 24 genera were selected for gion encompassing nearly 40 % of the island (Cribb and study. Root samples were shared between two partners, and to Hermans 2009)—and spontaneous seedlings in particular. facilitate the legal collection and international transport of The Itremo Massif has the largest area of exposed quartzitic orchid material from Madagascar to the UK and USA, a Con- substrate in Madagascar (du Puy and Moat 1996) with a mix- vention on International Trade in Endangered Species of Wild ture of ecosystems found nestled within a complex of hills and Fauna and Flora (CITES) permit was obtained, which allowed valleys separated by species-poor grasslands (Cribb and three tubes each containing seedling and mature roots per Hermans 2009). Several well-known, showy taxa are found species to be collected. Due to the limited availability of plants in the region, many of which persist as lithophytes on sun- in the wild, further restrictions were put in place locally to exposed rocks (e.g., Angraecum longicalcar). Others exist as collect from three each of juvenile and mature plants. This terrestrials of grasslands (e.g., Benthamia cinnabarina), moist was followed by a phytosanitary certificate, which was se- forests (e.g., Cynorkis purpurea), or well-drained soils (e.g., cured prior to departure from the country. For the import of Habenaria ambositrana), and a modest number cling to root samples (with soil) and seeds to the USA, two permits gnarled branches of host trees in open areas as epiphytes were needed from the US Department of Agriculture (USDA).
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