Article. A new species of Lindsaea (Lindsaeaceae, Polypodiopsida) from Mt. Hamiguitan, Mindanao, Philippines
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1 Phytotaxa 56: (2012) Copyright 2012 Magnolia Press Article ISSN (print edition) PHYTOTAXA ISSN (online edition) A new species of Lindsaea (Lindsaeaceae, Polypodiopsida) from Mt. Hamiguitan, Mindanao, Philippines DIRK NIKOLAUS KARGER 1 *, SAMULI LEHTONEN 2, VICTOR B. AMOROSO 3 & MICHAEL KESSLER 1 1 Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland 2 Department of Biology, University of Turku, FI Turku, Finland 3 Department of Biology, Central Mindanao University, Musuan, Bukidnon, Philippines *Corresponding author: dirk.karger@systbot.uzh.ch Abstract A new species of Lindsaea from the Philippines, Lindsaea hamiguitanensis is described. The phylogenetic relationships of L. hamiguitanensis were analysed by sequencing trnl-trnf and trnh-psba intergenic spacer regions and performing a cladistic analysis of the Lindsaea section Schizoloma. Lindsaea hamiguitanensis groups together with L. bouillodii and L. cf. cambodgensis, from which it differs morphologically by the length of its petioles and the entire pinnules, as well as genetically by three apomorphic substitutions in the trnl-trnf intergenic spacer, and by two apomorphic substitutions in trnh-psba spacer region. Introduction The pantropical fern genus Lindsaea Dryander (1797: 39) comprises ca. 200 species, with about two thirds of the species occurring in the Old World tropics. A few species occur in subtropical Japan and Tasmania. The genus usually occurs in moist forests below 3000 m (Kramer 1971). Most species are terrestrial with some species at higher elevations also growing as epiphytes (Kramer 1971). Some lowland species can also grow on decaying wood (Tuomisto 1998). Mount Hamiguitan Range Wildlife Sanctuary in Davao Oriental, Mindanao, Philippines is a protected area covering ha located between 6 40'N to 6 47'N and 'E to 'E. The mountain range is known for its unique characteristics and the largest pygmy bonsai forest in the Philippines. Ultramafic rocks form the predominant substrate and weather into soil with an unusually high concentration of iron and magnesium (Amoroso et al. 2009). An inventory of pteridophytes revealed 141 species of ferns and 14 lycophytes on the mountain, with 9 being endemic to the range (Amoroso et al. 2011). During botanical fieldwork in 2009, we collected a distinctive species of Lindsaea which we could not identify using standard references (Kramer 1971). Molecular analyses of this species revealed it as distinct, and therefore it is here described as a new species. Methods We investigated the phylogenetic relationships of Lindsaea hamiguitanensis by sequencing trnl-trnf and trnh-psba intergenic spacer regions and performing a cladistic analysis of Lindsaea sect. Schizoloma, with L. linearis Swartz (1801: 78) as outgroup. Laboratory protocols for DNA extraction, amplification, and sequencing followed Lehtonen et al. (2010). Data for other taxa included here were taken from Lehtonen et al. Accepted by Marcus Lehnert: 29 May 2012; published online in PDF: 30 May
2 (2010). Sequences were aligned using default options in Muscle (Edgar 2004). Short inverted sequence fragments are present in the studied spacer regions of some Lindsaea species, and they were replaced with their complementary sequences before the analysis, and a separate binary character was coded to recognise the original orientation (Lehtonen et al. 2010). Sequences were concatenated and analysed with unweighted parsimony analysis using TNT (Goloboff et al. 2008). The search consisted of 50 ratchet replicates holding five trees per replicate. Jackknife support indices (Farris et al. 1996) were calculated by repeating the search 1000 times with a removal probability of 37%. GenBank accession numbers for the studied specimens are given in Table 1. Morphological examinations have been conducted on two collections of L. hamiguitanensis, Karger 444 (Z) and Karger 426 (Z). TABLE 1. DNA vouchers and GenBank accession numbers analysed here. New sequences produced in this study are marked in bold. Taxon Voucher trnl-trnf trnh-psba Lindsaea agatii (Brack.) Lehtonen & Tuomisto Braithwaite 4519 (U) GU GU Lindsaea annamensis K.U.Kramer Averyanov VH2540 (AAU) GU GU Lindsaea austrosinica Ching Averyanov VH4816 (AAU) GU GU Lindsaea blotiana K.U.Kramer 1 Rakotondrainibe 6350 (P) GU GU4785 Lindsaea blotiana K.U.Kramer 2 Rakotondrainibe 4327 (MO) GU GU Lindsaea bouillodii Christ Nielsen 592 (AAU) FJ FJ Lindsaea cf. cambodgensis Christ Iwatsuki (AAU) GU GU Lindsaea chienii Ching Kramer 7554 (U) FJ FJ Lindsaea dissectiformis Ching Averyanov VH2557 (AAU) FJ FJ Lindsaea ensifolia Sw. 1 Larsen (AAU) GU GU Lindsaea ensifolia Sw. 2 Kessler (GOET) n.a. GU Lindsaea fraseri Hook. Streimann 8951 (L) FJ FJ Lindsaea gomphophylla Baker Hotta (U) GU GU Lindsaea goudotiana (Kunze) Mett. ex Kuhn Deroin 112 (P) GU n.a. Lindsaea grandiareolata (Bonap.) K.U.Kramer Rakotondrainibe 4090 (MO) GU GU Lindsaea hamiguitanensis D.N.Karger & V.B.Amoroso Karger 444 (Z) JQ JQ Lindsaea heterophylla Dryand. Charoenphol 5081 (AAU) GU n.a. Lindsaea javanensis Blume 1 Hennipman 3937 (U) FJ FJ Lindsaea javanensis Blume 2 Poulsen 1714 (TUR) FJ FJ Lindsaea kawabatae Kurata Saiki 1093 (Z) GU GU Lindsaea linearis Sw. Braggins 589 (AAU) FJ FJ Lindsaea madagascariensis Baker Rakotondrainibe 6349 (P) GU GU Lindsaea media R.Br. 1 Gittinss.n. (AAU) GU GU Lindsaea media R.Br. 2 van der Werff (MO) GU GU Lindsaea millefolia K.U.Kramer 1 Lan en Meeuse 5065 (L) GU GU Lindsaea millefolia K.U.Kramer 2 Guillaumet 4206 (P) GU n.a. Lindsaea orbiculata (Lam.) Mett. ex Kuhn Averyanov VH4814 (AAU) FJ FJ Lindsaea oxyphylla Baker Gautier 2662 (P) GU GU Lindsaea schizophylla (Baker) Christ Sledge 613 (Z) GU GU Lindsaea sp. Laegaard (AAU) FJ FJ Lindsaea subtilis K.U.Kramer Werff (MO) GU GU Lindsaea walkerae Hook. Bostock 638 (Z) GU GU Lindsaea vieillardii Mett. McKee 5304 (U) GU GU Phytotaxa Magnolia Press KARGER ET AL.
3 Results Our cladistic analysis resulted in three most parsimonious trees of 183 steps, with a CI of 0.87 and RI of 0.93 (Fig. 1). Lindsaea hamiguitanensis grouped together with L. bouillodii Christ (1909: 59) and L. cf. cambodgensis Christ (1909: 58), although this clade did not receive >50% jackknife support. Lindsaea hamiguitanensis differed from these two species by three apomorphic substitutions in the trnl-trnf intergenic spacer, and by two apomorphic substitutions in trnh-psba spacer region. The studied L. bouillodii and L. cf. cambodgensis specimens had identical sequences. Lindsaea hamiguitanensis shows various morphological characteristics that separate it from L. bouillodii. Rhizomes of L. hamiguitanensis are short-creeping and thinner than in L. bouillodii. The pinnae are entire in L. hamiguitanensis while they are shallowly incised in L. bouillodii. The petioles of L. hamiguitanensis are about twice as long as in L. bouillodii. DNA sequence data of non-coding chloroplast markers revealed that Lindsaea hamiguitanensis differs from its closest relatives. Although the differences are not great, they are still larger than the variation observed between different species in the L. annamensis Kramer (1972: 18) group, for example. The differences in morphological characters in comparison with the closely related species underline the molecular results. FIGURE 1. Strict consensus tree of three most parsimonious trees found in a combined analysis of trnl-trnf and trnh-psba intergenic spacer regions. Jackknife support (>50%) is indicated below the branches. A NEW SPECIES OF LINDSAEA (LINDSAEACEAE, POLYPODIOPSIDA) Phytotaxa Magnolia Press 17
4 Taxonomy Lindsaea hamiguitanensis D.N.Karger & V.B.Amoroso, sp. nov. (Fig. 2) Type: PHILIPPINES. Mindanao: Davao Oriental, Mount Hamiguitan, 6 44'4.16" N, 126 9'59.88" E, 1100 m, 1 November 2009, Karger 444 (holotype PNH!, isotypes UC!, Z!). Lindsaea rhizomate breve repente, pinnulis alternis, remotis, utrinque circa 2 5, cm longis, cm latis, non incisis, textura herbacea, colore laete virente, petiolibusque rigidis, cm longis, quadrangularibus. FIGURE 2. A C. Lindsaea hamiguitanensis D.N.Karger & V.B.Amoroso. A. Habit. B. Rhizome scale. C. Pinnule, abaxial, showing indusium. All from Karger 444 (Z). 18 Phytotaxa Magnolia Press KARGER ET AL.
5 Plants terrestrial. Rhizomes short-creeping, mm diameter, scales ferruginous, very narrowly triangular, to 1.5 mm long. Petioles cm long, to 4 times longer than the laminae, sharply quadrangular, dark reddish brown (proximally) to pale, with more or less well defined paler margins. Laminae triangular, 6 13 cm long, bipinnate to (basally) tripinnate-pinnatifid, rachises reddish brown, with pale margins, sharply quadrangular. Major primary pinnae 4 6 to a side, spreading to moderately ascending, triangular, the largest (at the bases) to 6 cm long, to 4 cm wide, the proximal ones up to their width apart, the distal ones closer to each other. Distal pinnae gradually reduced, with a conform terminal pinna, costae dark green, slightly winged, adaxially sulcate. Proximal primary pinnae basally with some pinnules 1 3 cm long. Pinnules 2 5 on each side, herbaceous, light green when dry, slightly ascending, not contiguous, dimidiate-ovate to subtrapeziform (basally), the larger ones cm long, cm wide, times longer than wide, margins continuous, rarely incised. Pinnules at lower primary pinnae shallowly incised. Distal pinnules gradually reduced, distal ones confluent with the acuminate terminal segment. Veins free, ca. 1.5 mm apart, 1- or 2-forked. Sori continuous, rarely incised on the basiscopic pinnules of the proximal primary pinnae, convex, extending 1/2 to 2/3 of the length of the pinnules along the sides of the pinnules, to 15 mm long, multinerval. Indusia coloured as the pinnules, indusial margins entire, rarely slightly erose, mm wide, not reaching the margin by times of their width. Spores trilete. Distribution and habitat: Known only from Mount Hamiguitan, Mindanao, Philippines, where it grows in lower montane rainforest at m. Etymology: The species is named for the type locality. Additional specimen examined (paratype): PHILIPPINES. Mindanao: Davao Oriental, Mount Hamiguitan, 6 44'4.16" N, 126 9'59.88" E, 1100 m, 1 November 2009, Karger 426 (Central Mindanao University Herbarium!, UC!, Z!). Acknowledgements We thank the officials of the Protected Areas and Wildlife Bureau (PAWB)-Department of Environment and Natural Resources (DENR), DENR Region XI, Protected Areas Management Board (PAMB) of Mount Hamiguitan Wildlife Sanctuary for the gratuitous permit, Alan R. Smith for initiating and revising this manuscript, and Fulgent Coritico and Elisea Bebet Gozun for logistic support. This study was funded by the Swiss National Science Foundation (SNF) and the Claratz Schenkung. References Amoroso, V.B. & Aspiras, R.A. (2011) Hamiguitan Range: A sanctuary for native flora. Saudi Journal of Biological Sciences 18: Amoroso, V.B., Obsioma, L., Arlalejo, J., Aspiras, R., Capili, D., Polizon, J. & Sumile, E.B. (2009) Inventory and conservation of endangered, endemic and economically important flora of Hamiguitan Range, southern Philippines. Blumea 54: Christ, H. (1909) Filices novœ cambodgenses. Notulae Systematicae 1: Dryander, J. (1797) Lindsaea, a new genus of ferns. Transactions of the Linnean Society of London 3: Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: Farris, J.S., Albert, V.A., Källersjö, M., Lipscomb, D. & Kluge, A.G. (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics 12: Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2008) TNT, a free program for phylogenetic analysis. Cladistics 24: Kramer, K.U. (1971) Pteridophyta-Lindsaea-group. In: Flora Malesiana, series II, 1(3). Wolters-Noordhoff Publishing, Groningen, pp Kramer, K.U. (1972) The lindsaeoid ferns of the Old World VI. Continental Asia, Japan and Taiwan. The Gardens Bulletin Singapore 24: Lehtonen, S., Tuomisto, H., Rouhan, G. & Christenhusz, M.J.M. (2010) Phylogenetics and classification of the A NEW SPECIES OF LINDSAEA (LINDSAEACEAE, POLYPODIOPSIDA) Phytotaxa Magnolia Press 19
6 pantropical fern family Lindsaeaceae. Botanical Journal of the Linnean Society 163: Swartz, O. (1801) Genera et species filicum. Schraders Journal für die Botanik 2: Tuomisto, H. (1998) What satellite imagery and large-scale field studies can tell about biodiversity patterns in Amazonian forests. Annals of the Missouri Botanical Garden 85: Phytotaxa Magnolia Press KARGER ET AL.
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