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See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/278021015 Diversity and Vertical Distribution Characteristics of Vascular epiphytes in Bulong Nature Reserve, Mengsong Section, Xishuangbanna ARTICLE · JANUARY 2015 DOWNLOADS 10 VIEWS 9 7 AUTHORS, INCLUDING: Rhett Daniel Harrison Consultative Group on International Agricu… 89 PUBLICATIONS 1,131 CITATIONS SEE PROFILE Jianchu Xu World Agroforestry Center 74 PUBLICATIONS 1,792 CITATIONS SEE PROFILE EN Paudel Chinese Academy of Sciences 9 PUBLICATIONS 0 CITATIONS SEE PROFILE Available from: Rhett Daniel Harrison Retrieved on: 15 June 2015
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Page 1: Diversity and Vertical Distribution Characteristics of ...

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DiversityandVerticalDistributionCharacteristicsofVascularepiphytesinBulongNatureReserveMengsongSectionXishuangbanna

ARTICLEmiddotJANUARY2015

DOWNLOADS

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VIEWS

9

7AUTHORSINCLUDING

RhettDanielHarrison

ConsultativeGrouponInternationalAgricuhellip

89PUBLICATIONS1131CITATIONS

SEEPROFILE

JianchuXu

WorldAgroforestryCenter

74PUBLICATIONS1792CITATIONS

SEEPROFILE

ENPaudel

ChineseAcademyofSciences

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SEEPROFILE

AvailablefromRhettDanielHarrison

Retrievedon15June2015

西双版纳布龙自然保护区勐宋片区附生维管植物多样性与分布特征lowast

赵明旭1ꎬ2ꎬ3ꎬ Geekiyanage Nalaka4ꎬ5ꎬ Harrison Rhett Daniel1ꎬ3lowastlowastꎬ 许建初1ꎬ3ꎬKhin Myo Myo6ꎬ Ridwan Nurdiana Dian7ꎬ Paudel Ekananda1ꎬ2

(1 中国科学院东亚植物多样性与生物地理学重点实验室ꎬ 昆明  650201ꎻ 2 中国科学院大学ꎬ 北京  100049ꎻ3 世界农用林业中心东亚和中亚区域办公室ꎬ 昆明  650201ꎻ 4 Biomaterial Scienceꎬ Graduate School of AgricultureꎬKyoto Universityꎬ Kitashirakawa Oiwakeꎬ Kyoto Prefectureꎬ Japanꎻ 5 Department of Plant Sciencesꎬ Faculty of AgricultureꎬRajarata University of Sri Lankaꎬ Anuradhapuraꎬ Sri Lankaꎻ 6 Wildlife Conservation Societyꎬ Yangonꎬ Myanmarꎻ

7 Cibodas Botanic Gardenꎬ Indonesian Institute of Sciencesꎬ Cianjurꎬ West Javaꎬ Indonesia)

摘要 利用地面观测和单绳上树法初次对布龙自然保护区勐宋片区开展的附生维管植物调查表明 1) 在

6 个样地 77 株宿主上 (共调查 96 株乔木ꎬ 占地约 01049008 2 ha)ꎬ 共有 1 756 株 丛个体ꎬ 隶属 14 科 47 属 103种ꎻ 相比世界其他区域ꎬ 物种丰富度处于旧世界热带水平区间ꎬ 高于温带ꎬ 但明显低于新世界热带水平ꎻ2) 兰科植物为最丰富的类群 (60)ꎬ 其次为蕨类植物 (24)ꎬ 其他类群占 16ꎻ 3) 垂直分布特征研究

表明ꎬ 距地面 10~15 m 的中等高度带为物种最丰富的区间ꎬ 约有 51的物种ꎻ 0 ~ 5 m 高度带为个体数量

最多的区间ꎬ 共有约 24个体ꎬ 揭示了除中等高度带以外的另一个重要附生生境ꎻ 4) 常见的绞杀型榕属

植物未见ꎬ 而半附生植物密脉鹅掌柴 (Schefflera elliptica) 和多蕊木 (Tupidanthus calyptratus) 数量较多ꎮ关键词 附生维管植物ꎻ 垂直分布ꎻ 生物多样性ꎻ 布龙自然保护区ꎻ 西双版纳ꎻ 中国

中图分类号 Q 948              文献标志码 A              文章编号 2095-0845(2015)03-327-12

Diversity and Vertical Distribution Characteristics ofVascular Epiphytes in Bulong Nature Reserve

Mengsong Sectionꎬ Xishuangbanna

ZHAO Ming ̄xu1ꎬ2ꎬ3ꎬ Geekiyanage Nalaka4ꎬ5ꎬ Harrison Rhett Daniel1ꎬ3lowastlowastꎬ XU Jian ̄chu1ꎬ3ꎬKhin Myo Myo6ꎬ Ridwan Nurdiana Dian7ꎬ Paudel Ekananda1ꎬ2ꎬ3

(1 Key Laboratory for Plant Diversity and Biogeography of East Asiaꎬ Kunming Institute of Botanyꎬ Chinese Academy of SciencesꎬKunmingꎬ Yunnan 650201ꎬ Chinaꎻ 2 University of Chinese Academy of Sciencesꎬ Beijing 100049ꎬ Chinaꎻ 3 World Agroforestry CentreꎬEast and Central Asiaꎬ Kunmingꎬ Yunnan 650201ꎬ Chinaꎻ 4 Biomaterial Scienceꎬ Graduate School of Agricultureꎬ Kyoto Universityꎬ

Kitashirakawa Oiwakeꎬ Kyoto Prefectureꎬ Japanꎻ 5 Department of Plant Sciencesꎬ Faculty of Agricultureꎬ RajarataUniversity of Sri Lankaꎬ Anuradhapuraꎬ Sri Lankaꎻ 6 Wildlife Conservation Societyꎬ Yangonꎬ Myanmarꎻ

7 Cibodas Botanic Gardenꎬ Indonesian Institute of Sciencesꎬ Cianjurꎬ West Javaꎬ Indonesia)

Abstract The first survey of vascular epiphytes was conducted using ground based inventory assisted by single ropetechnique in the recently ̄established Bulong Nature Reserveꎬ Xishuangbannaꎬ China Results indicated that vascularepiphytes were abundant and diverse there On a total of 77 phorophytes in six plots (96 trees were examined in to ̄

植 物 分 类 与 资 源 学 报  2015ꎬ 37 (3) 327~338Plant Diversity and Resources                                    DOI 107677 ynzwyj201514110

lowast

lowastlowast

Funding National Key Basic Research Program of China (2014CB954100)ꎻ The Applied Fundamental Research Foundation of YunnanProvince (2014GA003)

Author for correspondenceꎻ E ̄mail r1049008 harrisoncgiar1049008 orgReceived date 2014-08-13ꎬ Accepted date 2014-10-28作者简介 赵明旭 (1984-) 男ꎬ 博士ꎬ 从事植物分类学和附生植物群落生态学研究ꎮ E ̄mail zhaomingxu1049008 sfa1049008 kmygmail1049008 com

talꎬ covered ca 01049008 2 ha area)ꎬ 1 756 individuals were recorded and were identified to 103 species (47 generaꎬ 14families) Compared with other regionsꎬ the epiphytes were as diverse as Paleotropicsꎬ and more diverse than tem ̄perate zoneꎬ but significantly less than the Neotropics Orchids and ferns comprised 60ꎬ 24 of the total floraꎬ re ̄spectivelyꎬ while others only took up 16 The highest species richness and richest life ̄form diversity was found inthe middle canopy zone from 10 to 15 m (51 of total species)ꎬ where also supported high individual abundance(19 of total individuals) Besides the middle canopyꎬ the most abundant zone of epiphyte individuals was detectedat the base of the trunk (zone 0-5 mꎬ 24 of total individuals and 37 of total species)ꎬ indicating another impor ̄tant niche for epiphytes in this forest environment Primary hemiepiphytic figs were rare in the area and were notfound on the surveyed host treesꎬ while hemiepiphytic Araliaceae species (Schefflera elliptica and Tupidanthus ca ̄lyptratus) were popularKey words Vascular epiphyteꎻ Vertical distributionꎻ Biodiversityꎻ Bulong Nature Reserveꎻ Xishuangbannaꎻ China

  A high diversity of epiphytes is one of the gen ̄erally ̄recognized and distinct characteristics of tropi ̄cal rain forests Epiphytes make up 25 or more ofthe vascular plant diversity in certain Central Amazo ̄nian forests (Kuumlper et alꎬ 2004)ꎬ and a study inVenezuela found that over 50 of all vascular plantspecies were epiphytes (Kelly et alꎬ 1994) Howev ̄erꎬ when extra ̄tropical regions are includedꎬ a largenumber of studies confirmed thatꎬ globallyꎬ about8-10 of vascular plants are epiphytes (Gentryand Dodsonꎬ 1987ꎻ Benzingꎬ 1990ꎻ Lowman andRinkerꎬ 2004ꎻ Zotzꎬ 2013)

Most studies on epiphyte have been conductedin the Neotropics and tropical Africa ( Hsu andWolfꎬ 2009ꎻ Table 3) Relatively few surveys of ep ̄iphyte diversity have been made in tropical Asiaꎬ es ̄pecially in Chinaꎬ although some exist for subtropi ̄cal China (Wang et alꎬ 1996ꎻ Xu and Liuꎬ 2005ꎻYangꎬ 2008) The diversity of epiphyte communityin Hainan Island was recently investigatedꎬ andfound to be much lower than in the Neotropicsꎬ butother aspects of epiphyte ecologyꎬ such as their ver ̄tical stratificationꎬ appeared similar ( Liuꎬ 2010ꎻLiu et alꎬ 2010)

Xishuangbanna comprises the largest area oftropical forest in China (Zhuꎬ 2006) and forms partof the Indo ̄Burma biodiversity hotspot (Myers et alꎬ2000) More than 4 000 species of seed plant occur inthe area (19 690 km2ꎬ Zhu and Yanꎬ 2012) Al ̄though Wang and Zhu suggested that vascular epi ̄phytes were a prominent characteristic of tropical

montane rainforest in Xishuangbanna (Wang et alꎬ2001ꎻ Zhuꎬ 2006)ꎬ quantitative surveys of epiphytediversity and vertical distribution characteristics havenot been conducted

The vertical gradient is a defining feature of for ̄estsꎬ because habitat structure and microclimate fac ̄tors (lightꎬ waterꎬ and mineral nutrition) (Benzingꎬ1990ꎬ 2012) are vertically organized (Dhanmanon ̄daꎬ 1996ꎻ Steege and Cornelissenꎬ 1989ꎻ Benzingꎬ1990ꎻ McCune et alꎬ 1997ꎻ Lowman and Rinkerꎬ2004) With increasing heightꎬ the humidityꎬ lightavailabilityꎬ and substrate conditions (including pH)all vary ̄which defines different microhabitats for epi ̄phyte communities (Pittendrighꎬ 1948ꎻ Johanssonꎬ1974ꎻ Kellyꎬ 1985ꎻ Cornelissen and Steegeꎬ 1989ꎻParkerꎬ 1995ꎻ Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997ꎻKroumlmer et alꎬ 2007) For exampleꎬ Dhanmanonda(1996) found that light availability increased expo ̄nentially with increasing height above the forestfloorꎬ and epiphytes vertical distribution characteris ̄tics had been shown to be influenced by the photonflux density (Pittendrighꎬ 1948ꎻ Steege and Cornel ̄issenꎬ 1989) Humidity is also believed to be one ofthe most important factors in determining epiphytecommunity assembly (Steege and Cornelissenꎬ 1989ꎻPittendrighꎬ 1948ꎻ Freibergꎬ 1997ꎻ Nieder et alꎬ1999) The adaptation of epiphytesꎬ in terms oftheir anatomy and physiologyꎬ to vertical microhabi ̄tat heterogeneityꎬ has been comprehensively reviewedby Benzing (1990)

Our aims in this research are to describe the di ̄

823                                  植 物 分 类 与 资 源 学 报                            第 37 卷

versity and vertical distribution characteristics of epi ̄phyte community in the tropical montane forest of Xi ̄shuangbannaꎬ addressing this knowledge gap in tropi ̄cal China Thusꎬ our study is an observational studyaimed at documenting diversityꎬ andꎬ henceꎬ can on ̄ly be suggestive of the community assembly processes(Johanssonꎬ 1974ꎻ Kellyꎬ 1985ꎻ Zotzꎬ 2007)

1  Methods11049008 1  Study site

Our study was conducted in the recently ̄estab ̄lished Bulong Nature Reserveꎬ Mengsong Section(MS ̄BNRꎬ 2009)ꎬ in Xishuangbannaꎬ China (Fig1049008 1)The vegetation type has been categorized as tropicalmontane rainforest and monsoon evergreen broadleafforestꎬ the former located in relatively humid regions(montane valleyꎬ riparian)ꎬ while the latter usuallyis found on the dry slopes The elevation ranges from1 110 m to 2 039 m (the peak of Sanduogeque)ꎬ and

mean monthly temperatures fluctuates between 15 -21 (at 1 600 m asl) The study site has a typicalmonsoon climate ( greatly influenced by the IndiaOcean monsoons) and the annual precipitation ran ̄ges between 1 800-2 379 mmꎬ 80 of which occursbetween the months of May and October The atmos ̄phere has an annual relative humidity of 83 (Zhuet alꎬ 2004)11049008 2  Field observations

Field work was conducted during the dry seasonNovember to Decemberꎬ 2012ꎬ when the crown lay ̄ers were clear and epiphytes were easy to observeSix previously ̄establishedꎬ one hectare ( 100 m times100 m)ꎬ permanent sampling plots in the old growtharea of the forest ( ca 35 m of canopy height) inMS ̄BNR were selected for this present studyꎬ threeof which were located in a tropical montane rainforestand three in an evergreen broadleaf forest ( Fig1049008 1ꎬTable 1) Plots were separated by a minimum straight

Fig1049008 1  Location of sampling plots and the MS ̄BNRꎬ Xishuangbanna The map showing the old growth forest area of MS ̄BNRꎬthe remaining blank areas are mainly covered by secondary forest or open land

9233 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

Table 1  Basic information of sampling plots in MS ̄BNRꎬ Xishuangbanna

Plot Elevation m Forest type Dominate tree Host occupancy

Basal area

Plot area(m2 ha)Epiphyte No of Ind

No of species

107 1450 MEBF CASMEKꎬ STYTON 561049008 3 241049008 4 217 24189 1700 MEBF CASMEKꎬ LITMAR 871049008 5 221049008 2 264 31192 1785 MEBF CASMEKꎬ ANNFRA 1001049008 0 251049008 6 389 30214 1670 TMRF SYZBRAꎬ LITBAC 811049008 3 451049008 6 399 48217 1700 TMRF ALAKURꎬ CRYBRA 931049008 8 221049008 2 310 36240 1750 TMRF CALPOLꎬ CASCAL 621049008 5 341049008 1 177 21

Note MEBF=Monsoon Evergreen Broadleaf Forestꎬ TMRF=Tropical Montane Rain Forest Dominate trees were selected by the first two importancevalue in a plot (nine sub plots tree data was appliedꎬ respectively) CASMEK=Castanopsis mekongensisꎬ STYTON=Styrax tonkinensisꎬ LITMAR=

Litsea martabanicaꎬ ANNFRA=Anneslea fragransꎬ SYZBRA=Syzygium brachythyrsumꎬ LITBAC=Lithocarpus bacgiangensisꎬ ALAKUR=Alangiumkurziiꎬ CRYBRA=Cryptocarya brachythyrsaꎬ CALPOL=Calophyllum polyanthumꎬ CASCAL=Castanopsis calathiformis Host occupancy was calcu ̄lated by 100 times epiphyte occupied trees total trees (16) in a plot

line distance of 700 m and a maximum of 3 600 mNine 10 m ̄radius circle subplots were set inside abig plotꎬ and trees (dbhge10 cmꎬ dbh = diameter atbreast height ) were measured and identified Ateach big plotꎬ a random point was marked near thecentral subplot of nineꎬ and the 16 nearest trees(dbhge10 cmꎬ covering an area of approximately 10 mradius subplot) were examined for epiphytesꎬ and96 trees were checked in total

Binoculars and a spotting ̄scope were first usedto check host tree roughlyꎬ only if epiphyte was de ̄tected on the groundꎬ we would access the crown u ̄sing single rope technique at least to the main forksite to assist specimen collecting and the latter epi ̄phytes countingꎬ attaching height measurement work(Perryꎬ 1978) A telescopic pruning shears withmaximum 5 m was also implemented to assist the col ̄lecting process Digital photographs were also takento document observations and assist in the identifica ̄tion process Due to identification barriersꎬ all smallseedlings were omitted and orchids that were hard toidentified without flower were all kept alive in green ̄houses until identifiedꎬ then herbarium specimenwere made

Epiphyte attaching height above ground wasmeasured using a 5 m poleꎬ orꎬ for those speciesdistributed in the outer of crownꎬ where could not beaccessedꎬ by estimating the height using the 5 mpole as a reference When estimating heightsꎬ the

observer stood at least 20 m away from the tree Epi ̄phytes that covered a substantial portion of the hostcrown (creeping or clustered speciesꎬ like Pyrrosialingua and Cylindrolobus marginatus)ꎬ the heightwas taken from the lowest to the highest points

Two schemes of forest canopy zonation were ap ̄plied in the former studiesꎬ six vertical tree zones(Steege and Cornelissenꎬ 1989) and equal height in ̄terval vertical tree zones (Zotz and Schultzꎬ 2008)ꎬboth were proved to be efficient approachesꎬ we fol ̄lowed the latter and forest canopy was divided intoseven height zones using a 5 m interval (the highestcrown layer was about 35 m) as several other studiesdid ( Zotz and Schultzꎬ 2008ꎻ Liu et alꎬ 2010)ꎬhence our results could be compared both in the tropi ̄cal forest domestically and abroadꎬ and the micro en ̄vironmental factors were more consistent in the paral ̄lel upper zones than the former arc ̄shaped scheme

To define epiphyte individualsꎬ we referred tothe individual definition of lsquostandrsquo (Sanfordꎬ 1968)A stand was defined as a cluster of pseudobulbs (orthe same epiphyte species leaves) was spatially sep ̄arated from anothermdasheither by an area devoid of ep ̄iphytes or occupied by other species When the samearea was occupied by an intermingling of more thanone speciesꎬ one stand was counted for each speciespresent If a stand of epiphyte covered two or morevertical zonesꎬ especially those with long rhizomes orlarge ̄area clustered pseudobulbsꎬ both individual

033                                  植 物 分 类 与 资 源 学 报                            第 37 卷

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

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Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

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munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 2: Diversity and Vertical Distribution Characteristics of ...

西双版纳布龙自然保护区勐宋片区附生维管植物多样性与分布特征lowast

赵明旭1ꎬ2ꎬ3ꎬ Geekiyanage Nalaka4ꎬ5ꎬ Harrison Rhett Daniel1ꎬ3lowastlowastꎬ 许建初1ꎬ3ꎬKhin Myo Myo6ꎬ Ridwan Nurdiana Dian7ꎬ Paudel Ekananda1ꎬ2

(1 中国科学院东亚植物多样性与生物地理学重点实验室ꎬ 昆明  650201ꎻ 2 中国科学院大学ꎬ 北京  100049ꎻ3 世界农用林业中心东亚和中亚区域办公室ꎬ 昆明  650201ꎻ 4 Biomaterial Scienceꎬ Graduate School of AgricultureꎬKyoto Universityꎬ Kitashirakawa Oiwakeꎬ Kyoto Prefectureꎬ Japanꎻ 5 Department of Plant Sciencesꎬ Faculty of AgricultureꎬRajarata University of Sri Lankaꎬ Anuradhapuraꎬ Sri Lankaꎻ 6 Wildlife Conservation Societyꎬ Yangonꎬ Myanmarꎻ

7 Cibodas Botanic Gardenꎬ Indonesian Institute of Sciencesꎬ Cianjurꎬ West Javaꎬ Indonesia)

摘要 利用地面观测和单绳上树法初次对布龙自然保护区勐宋片区开展的附生维管植物调查表明 1) 在

6 个样地 77 株宿主上 (共调查 96 株乔木ꎬ 占地约 01049008 2 ha)ꎬ 共有 1 756 株 丛个体ꎬ 隶属 14 科 47 属 103种ꎻ 相比世界其他区域ꎬ 物种丰富度处于旧世界热带水平区间ꎬ 高于温带ꎬ 但明显低于新世界热带水平ꎻ2) 兰科植物为最丰富的类群 (60)ꎬ 其次为蕨类植物 (24)ꎬ 其他类群占 16ꎻ 3) 垂直分布特征研究

表明ꎬ 距地面 10~15 m 的中等高度带为物种最丰富的区间ꎬ 约有 51的物种ꎻ 0 ~ 5 m 高度带为个体数量

最多的区间ꎬ 共有约 24个体ꎬ 揭示了除中等高度带以外的另一个重要附生生境ꎻ 4) 常见的绞杀型榕属

植物未见ꎬ 而半附生植物密脉鹅掌柴 (Schefflera elliptica) 和多蕊木 (Tupidanthus calyptratus) 数量较多ꎮ关键词 附生维管植物ꎻ 垂直分布ꎻ 生物多样性ꎻ 布龙自然保护区ꎻ 西双版纳ꎻ 中国

中图分类号 Q 948              文献标志码 A              文章编号 2095-0845(2015)03-327-12

Diversity and Vertical Distribution Characteristics ofVascular Epiphytes in Bulong Nature Reserve

Mengsong Sectionꎬ Xishuangbanna

ZHAO Ming ̄xu1ꎬ2ꎬ3ꎬ Geekiyanage Nalaka4ꎬ5ꎬ Harrison Rhett Daniel1ꎬ3lowastlowastꎬ XU Jian ̄chu1ꎬ3ꎬKhin Myo Myo6ꎬ Ridwan Nurdiana Dian7ꎬ Paudel Ekananda1ꎬ2ꎬ3

(1 Key Laboratory for Plant Diversity and Biogeography of East Asiaꎬ Kunming Institute of Botanyꎬ Chinese Academy of SciencesꎬKunmingꎬ Yunnan 650201ꎬ Chinaꎻ 2 University of Chinese Academy of Sciencesꎬ Beijing 100049ꎬ Chinaꎻ 3 World Agroforestry CentreꎬEast and Central Asiaꎬ Kunmingꎬ Yunnan 650201ꎬ Chinaꎻ 4 Biomaterial Scienceꎬ Graduate School of Agricultureꎬ Kyoto Universityꎬ

Kitashirakawa Oiwakeꎬ Kyoto Prefectureꎬ Japanꎻ 5 Department of Plant Sciencesꎬ Faculty of Agricultureꎬ RajarataUniversity of Sri Lankaꎬ Anuradhapuraꎬ Sri Lankaꎻ 6 Wildlife Conservation Societyꎬ Yangonꎬ Myanmarꎻ

7 Cibodas Botanic Gardenꎬ Indonesian Institute of Sciencesꎬ Cianjurꎬ West Javaꎬ Indonesia)

Abstract The first survey of vascular epiphytes was conducted using ground based inventory assisted by single ropetechnique in the recently ̄established Bulong Nature Reserveꎬ Xishuangbannaꎬ China Results indicated that vascularepiphytes were abundant and diverse there On a total of 77 phorophytes in six plots (96 trees were examined in to ̄

植 物 分 类 与 资 源 学 报  2015ꎬ 37 (3) 327~338Plant Diversity and Resources                                    DOI 107677 ynzwyj201514110

lowast

lowastlowast

Funding National Key Basic Research Program of China (2014CB954100)ꎻ The Applied Fundamental Research Foundation of YunnanProvince (2014GA003)

Author for correspondenceꎻ E ̄mail r1049008 harrisoncgiar1049008 orgReceived date 2014-08-13ꎬ Accepted date 2014-10-28作者简介 赵明旭 (1984-) 男ꎬ 博士ꎬ 从事植物分类学和附生植物群落生态学研究ꎮ E ̄mail zhaomingxu1049008 sfa1049008 kmygmail1049008 com

talꎬ covered ca 01049008 2 ha area)ꎬ 1 756 individuals were recorded and were identified to 103 species (47 generaꎬ 14families) Compared with other regionsꎬ the epiphytes were as diverse as Paleotropicsꎬ and more diverse than tem ̄perate zoneꎬ but significantly less than the Neotropics Orchids and ferns comprised 60ꎬ 24 of the total floraꎬ re ̄spectivelyꎬ while others only took up 16 The highest species richness and richest life ̄form diversity was found inthe middle canopy zone from 10 to 15 m (51 of total species)ꎬ where also supported high individual abundance(19 of total individuals) Besides the middle canopyꎬ the most abundant zone of epiphyte individuals was detectedat the base of the trunk (zone 0-5 mꎬ 24 of total individuals and 37 of total species)ꎬ indicating another impor ̄tant niche for epiphytes in this forest environment Primary hemiepiphytic figs were rare in the area and were notfound on the surveyed host treesꎬ while hemiepiphytic Araliaceae species (Schefflera elliptica and Tupidanthus ca ̄lyptratus) were popularKey words Vascular epiphyteꎻ Vertical distributionꎻ Biodiversityꎻ Bulong Nature Reserveꎻ Xishuangbannaꎻ China

  A high diversity of epiphytes is one of the gen ̄erally ̄recognized and distinct characteristics of tropi ̄cal rain forests Epiphytes make up 25 or more ofthe vascular plant diversity in certain Central Amazo ̄nian forests (Kuumlper et alꎬ 2004)ꎬ and a study inVenezuela found that over 50 of all vascular plantspecies were epiphytes (Kelly et alꎬ 1994) Howev ̄erꎬ when extra ̄tropical regions are includedꎬ a largenumber of studies confirmed thatꎬ globallyꎬ about8-10 of vascular plants are epiphytes (Gentryand Dodsonꎬ 1987ꎻ Benzingꎬ 1990ꎻ Lowman andRinkerꎬ 2004ꎻ Zotzꎬ 2013)

Most studies on epiphyte have been conductedin the Neotropics and tropical Africa ( Hsu andWolfꎬ 2009ꎻ Table 3) Relatively few surveys of ep ̄iphyte diversity have been made in tropical Asiaꎬ es ̄pecially in Chinaꎬ although some exist for subtropi ̄cal China (Wang et alꎬ 1996ꎻ Xu and Liuꎬ 2005ꎻYangꎬ 2008) The diversity of epiphyte communityin Hainan Island was recently investigatedꎬ andfound to be much lower than in the Neotropicsꎬ butother aspects of epiphyte ecologyꎬ such as their ver ̄tical stratificationꎬ appeared similar ( Liuꎬ 2010ꎻLiu et alꎬ 2010)

Xishuangbanna comprises the largest area oftropical forest in China (Zhuꎬ 2006) and forms partof the Indo ̄Burma biodiversity hotspot (Myers et alꎬ2000) More than 4 000 species of seed plant occur inthe area (19 690 km2ꎬ Zhu and Yanꎬ 2012) Al ̄though Wang and Zhu suggested that vascular epi ̄phytes were a prominent characteristic of tropical

montane rainforest in Xishuangbanna (Wang et alꎬ2001ꎻ Zhuꎬ 2006)ꎬ quantitative surveys of epiphytediversity and vertical distribution characteristics havenot been conducted

The vertical gradient is a defining feature of for ̄estsꎬ because habitat structure and microclimate fac ̄tors (lightꎬ waterꎬ and mineral nutrition) (Benzingꎬ1990ꎬ 2012) are vertically organized (Dhanmanon ̄daꎬ 1996ꎻ Steege and Cornelissenꎬ 1989ꎻ Benzingꎬ1990ꎻ McCune et alꎬ 1997ꎻ Lowman and Rinkerꎬ2004) With increasing heightꎬ the humidityꎬ lightavailabilityꎬ and substrate conditions (including pH)all vary ̄which defines different microhabitats for epi ̄phyte communities (Pittendrighꎬ 1948ꎻ Johanssonꎬ1974ꎻ Kellyꎬ 1985ꎻ Cornelissen and Steegeꎬ 1989ꎻParkerꎬ 1995ꎻ Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997ꎻKroumlmer et alꎬ 2007) For exampleꎬ Dhanmanonda(1996) found that light availability increased expo ̄nentially with increasing height above the forestfloorꎬ and epiphytes vertical distribution characteris ̄tics had been shown to be influenced by the photonflux density (Pittendrighꎬ 1948ꎻ Steege and Cornel ̄issenꎬ 1989) Humidity is also believed to be one ofthe most important factors in determining epiphytecommunity assembly (Steege and Cornelissenꎬ 1989ꎻPittendrighꎬ 1948ꎻ Freibergꎬ 1997ꎻ Nieder et alꎬ1999) The adaptation of epiphytesꎬ in terms oftheir anatomy and physiologyꎬ to vertical microhabi ̄tat heterogeneityꎬ has been comprehensively reviewedby Benzing (1990)

Our aims in this research are to describe the di ̄

823                                  植 物 分 类 与 资 源 学 报                            第 37 卷

versity and vertical distribution characteristics of epi ̄phyte community in the tropical montane forest of Xi ̄shuangbannaꎬ addressing this knowledge gap in tropi ̄cal China Thusꎬ our study is an observational studyaimed at documenting diversityꎬ andꎬ henceꎬ can on ̄ly be suggestive of the community assembly processes(Johanssonꎬ 1974ꎻ Kellyꎬ 1985ꎻ Zotzꎬ 2007)

1  Methods11049008 1  Study site

Our study was conducted in the recently ̄estab ̄lished Bulong Nature Reserveꎬ Mengsong Section(MS ̄BNRꎬ 2009)ꎬ in Xishuangbannaꎬ China (Fig1049008 1)The vegetation type has been categorized as tropicalmontane rainforest and monsoon evergreen broadleafforestꎬ the former located in relatively humid regions(montane valleyꎬ riparian)ꎬ while the latter usuallyis found on the dry slopes The elevation ranges from1 110 m to 2 039 m (the peak of Sanduogeque)ꎬ and

mean monthly temperatures fluctuates between 15 -21 (at 1 600 m asl) The study site has a typicalmonsoon climate ( greatly influenced by the IndiaOcean monsoons) and the annual precipitation ran ̄ges between 1 800-2 379 mmꎬ 80 of which occursbetween the months of May and October The atmos ̄phere has an annual relative humidity of 83 (Zhuet alꎬ 2004)11049008 2  Field observations

Field work was conducted during the dry seasonNovember to Decemberꎬ 2012ꎬ when the crown lay ̄ers were clear and epiphytes were easy to observeSix previously ̄establishedꎬ one hectare ( 100 m times100 m)ꎬ permanent sampling plots in the old growtharea of the forest ( ca 35 m of canopy height) inMS ̄BNR were selected for this present studyꎬ threeof which were located in a tropical montane rainforestand three in an evergreen broadleaf forest ( Fig1049008 1ꎬTable 1) Plots were separated by a minimum straight

Fig1049008 1  Location of sampling plots and the MS ̄BNRꎬ Xishuangbanna The map showing the old growth forest area of MS ̄BNRꎬthe remaining blank areas are mainly covered by secondary forest or open land

9233 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

Table 1  Basic information of sampling plots in MS ̄BNRꎬ Xishuangbanna

Plot Elevation m Forest type Dominate tree Host occupancy

Basal area

Plot area(m2 ha)Epiphyte No of Ind

No of species

107 1450 MEBF CASMEKꎬ STYTON 561049008 3 241049008 4 217 24189 1700 MEBF CASMEKꎬ LITMAR 871049008 5 221049008 2 264 31192 1785 MEBF CASMEKꎬ ANNFRA 1001049008 0 251049008 6 389 30214 1670 TMRF SYZBRAꎬ LITBAC 811049008 3 451049008 6 399 48217 1700 TMRF ALAKURꎬ CRYBRA 931049008 8 221049008 2 310 36240 1750 TMRF CALPOLꎬ CASCAL 621049008 5 341049008 1 177 21

Note MEBF=Monsoon Evergreen Broadleaf Forestꎬ TMRF=Tropical Montane Rain Forest Dominate trees were selected by the first two importancevalue in a plot (nine sub plots tree data was appliedꎬ respectively) CASMEK=Castanopsis mekongensisꎬ STYTON=Styrax tonkinensisꎬ LITMAR=

Litsea martabanicaꎬ ANNFRA=Anneslea fragransꎬ SYZBRA=Syzygium brachythyrsumꎬ LITBAC=Lithocarpus bacgiangensisꎬ ALAKUR=Alangiumkurziiꎬ CRYBRA=Cryptocarya brachythyrsaꎬ CALPOL=Calophyllum polyanthumꎬ CASCAL=Castanopsis calathiformis Host occupancy was calcu ̄lated by 100 times epiphyte occupied trees total trees (16) in a plot

line distance of 700 m and a maximum of 3 600 mNine 10 m ̄radius circle subplots were set inside abig plotꎬ and trees (dbhge10 cmꎬ dbh = diameter atbreast height ) were measured and identified Ateach big plotꎬ a random point was marked near thecentral subplot of nineꎬ and the 16 nearest trees(dbhge10 cmꎬ covering an area of approximately 10 mradius subplot) were examined for epiphytesꎬ and96 trees were checked in total

Binoculars and a spotting ̄scope were first usedto check host tree roughlyꎬ only if epiphyte was de ̄tected on the groundꎬ we would access the crown u ̄sing single rope technique at least to the main forksite to assist specimen collecting and the latter epi ̄phytes countingꎬ attaching height measurement work(Perryꎬ 1978) A telescopic pruning shears withmaximum 5 m was also implemented to assist the col ̄lecting process Digital photographs were also takento document observations and assist in the identifica ̄tion process Due to identification barriersꎬ all smallseedlings were omitted and orchids that were hard toidentified without flower were all kept alive in green ̄houses until identifiedꎬ then herbarium specimenwere made

Epiphyte attaching height above ground wasmeasured using a 5 m poleꎬ orꎬ for those speciesdistributed in the outer of crownꎬ where could not beaccessedꎬ by estimating the height using the 5 mpole as a reference When estimating heightsꎬ the

observer stood at least 20 m away from the tree Epi ̄phytes that covered a substantial portion of the hostcrown (creeping or clustered speciesꎬ like Pyrrosialingua and Cylindrolobus marginatus)ꎬ the heightwas taken from the lowest to the highest points

Two schemes of forest canopy zonation were ap ̄plied in the former studiesꎬ six vertical tree zones(Steege and Cornelissenꎬ 1989) and equal height in ̄terval vertical tree zones (Zotz and Schultzꎬ 2008)ꎬboth were proved to be efficient approachesꎬ we fol ̄lowed the latter and forest canopy was divided intoseven height zones using a 5 m interval (the highestcrown layer was about 35 m) as several other studiesdid ( Zotz and Schultzꎬ 2008ꎻ Liu et alꎬ 2010)ꎬhence our results could be compared both in the tropi ̄cal forest domestically and abroadꎬ and the micro en ̄vironmental factors were more consistent in the paral ̄lel upper zones than the former arc ̄shaped scheme

To define epiphyte individualsꎬ we referred tothe individual definition of lsquostandrsquo (Sanfordꎬ 1968)A stand was defined as a cluster of pseudobulbs (orthe same epiphyte species leaves) was spatially sep ̄arated from anothermdasheither by an area devoid of ep ̄iphytes or occupied by other species When the samearea was occupied by an intermingling of more thanone speciesꎬ one stand was counted for each speciespresent If a stand of epiphyte covered two or morevertical zonesꎬ especially those with long rhizomes orlarge ̄area clustered pseudobulbsꎬ both individual

033                                  植 物 分 类 与 资 源 学 报                            第 37 卷

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

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eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

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munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 3: Diversity and Vertical Distribution Characteristics of ...

talꎬ covered ca 01049008 2 ha area)ꎬ 1 756 individuals were recorded and were identified to 103 species (47 generaꎬ 14families) Compared with other regionsꎬ the epiphytes were as diverse as Paleotropicsꎬ and more diverse than tem ̄perate zoneꎬ but significantly less than the Neotropics Orchids and ferns comprised 60ꎬ 24 of the total floraꎬ re ̄spectivelyꎬ while others only took up 16 The highest species richness and richest life ̄form diversity was found inthe middle canopy zone from 10 to 15 m (51 of total species)ꎬ where also supported high individual abundance(19 of total individuals) Besides the middle canopyꎬ the most abundant zone of epiphyte individuals was detectedat the base of the trunk (zone 0-5 mꎬ 24 of total individuals and 37 of total species)ꎬ indicating another impor ̄tant niche for epiphytes in this forest environment Primary hemiepiphytic figs were rare in the area and were notfound on the surveyed host treesꎬ while hemiepiphytic Araliaceae species (Schefflera elliptica and Tupidanthus ca ̄lyptratus) were popularKey words Vascular epiphyteꎻ Vertical distributionꎻ Biodiversityꎻ Bulong Nature Reserveꎻ Xishuangbannaꎻ China

  A high diversity of epiphytes is one of the gen ̄erally ̄recognized and distinct characteristics of tropi ̄cal rain forests Epiphytes make up 25 or more ofthe vascular plant diversity in certain Central Amazo ̄nian forests (Kuumlper et alꎬ 2004)ꎬ and a study inVenezuela found that over 50 of all vascular plantspecies were epiphytes (Kelly et alꎬ 1994) Howev ̄erꎬ when extra ̄tropical regions are includedꎬ a largenumber of studies confirmed thatꎬ globallyꎬ about8-10 of vascular plants are epiphytes (Gentryand Dodsonꎬ 1987ꎻ Benzingꎬ 1990ꎻ Lowman andRinkerꎬ 2004ꎻ Zotzꎬ 2013)

Most studies on epiphyte have been conductedin the Neotropics and tropical Africa ( Hsu andWolfꎬ 2009ꎻ Table 3) Relatively few surveys of ep ̄iphyte diversity have been made in tropical Asiaꎬ es ̄pecially in Chinaꎬ although some exist for subtropi ̄cal China (Wang et alꎬ 1996ꎻ Xu and Liuꎬ 2005ꎻYangꎬ 2008) The diversity of epiphyte communityin Hainan Island was recently investigatedꎬ andfound to be much lower than in the Neotropicsꎬ butother aspects of epiphyte ecologyꎬ such as their ver ̄tical stratificationꎬ appeared similar ( Liuꎬ 2010ꎻLiu et alꎬ 2010)

Xishuangbanna comprises the largest area oftropical forest in China (Zhuꎬ 2006) and forms partof the Indo ̄Burma biodiversity hotspot (Myers et alꎬ2000) More than 4 000 species of seed plant occur inthe area (19 690 km2ꎬ Zhu and Yanꎬ 2012) Al ̄though Wang and Zhu suggested that vascular epi ̄phytes were a prominent characteristic of tropical

montane rainforest in Xishuangbanna (Wang et alꎬ2001ꎻ Zhuꎬ 2006)ꎬ quantitative surveys of epiphytediversity and vertical distribution characteristics havenot been conducted

The vertical gradient is a defining feature of for ̄estsꎬ because habitat structure and microclimate fac ̄tors (lightꎬ waterꎬ and mineral nutrition) (Benzingꎬ1990ꎬ 2012) are vertically organized (Dhanmanon ̄daꎬ 1996ꎻ Steege and Cornelissenꎬ 1989ꎻ Benzingꎬ1990ꎻ McCune et alꎬ 1997ꎻ Lowman and Rinkerꎬ2004) With increasing heightꎬ the humidityꎬ lightavailabilityꎬ and substrate conditions (including pH)all vary ̄which defines different microhabitats for epi ̄phyte communities (Pittendrighꎬ 1948ꎻ Johanssonꎬ1974ꎻ Kellyꎬ 1985ꎻ Cornelissen and Steegeꎬ 1989ꎻParkerꎬ 1995ꎻ Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997ꎻKroumlmer et alꎬ 2007) For exampleꎬ Dhanmanonda(1996) found that light availability increased expo ̄nentially with increasing height above the forestfloorꎬ and epiphytes vertical distribution characteris ̄tics had been shown to be influenced by the photonflux density (Pittendrighꎬ 1948ꎻ Steege and Cornel ̄issenꎬ 1989) Humidity is also believed to be one ofthe most important factors in determining epiphytecommunity assembly (Steege and Cornelissenꎬ 1989ꎻPittendrighꎬ 1948ꎻ Freibergꎬ 1997ꎻ Nieder et alꎬ1999) The adaptation of epiphytesꎬ in terms oftheir anatomy and physiologyꎬ to vertical microhabi ̄tat heterogeneityꎬ has been comprehensively reviewedby Benzing (1990)

Our aims in this research are to describe the di ̄

823                                  植 物 分 类 与 资 源 学 报                            第 37 卷

versity and vertical distribution characteristics of epi ̄phyte community in the tropical montane forest of Xi ̄shuangbannaꎬ addressing this knowledge gap in tropi ̄cal China Thusꎬ our study is an observational studyaimed at documenting diversityꎬ andꎬ henceꎬ can on ̄ly be suggestive of the community assembly processes(Johanssonꎬ 1974ꎻ Kellyꎬ 1985ꎻ Zotzꎬ 2007)

1  Methods11049008 1  Study site

Our study was conducted in the recently ̄estab ̄lished Bulong Nature Reserveꎬ Mengsong Section(MS ̄BNRꎬ 2009)ꎬ in Xishuangbannaꎬ China (Fig1049008 1)The vegetation type has been categorized as tropicalmontane rainforest and monsoon evergreen broadleafforestꎬ the former located in relatively humid regions(montane valleyꎬ riparian)ꎬ while the latter usuallyis found on the dry slopes The elevation ranges from1 110 m to 2 039 m (the peak of Sanduogeque)ꎬ and

mean monthly temperatures fluctuates between 15 -21 (at 1 600 m asl) The study site has a typicalmonsoon climate ( greatly influenced by the IndiaOcean monsoons) and the annual precipitation ran ̄ges between 1 800-2 379 mmꎬ 80 of which occursbetween the months of May and October The atmos ̄phere has an annual relative humidity of 83 (Zhuet alꎬ 2004)11049008 2  Field observations

Field work was conducted during the dry seasonNovember to Decemberꎬ 2012ꎬ when the crown lay ̄ers were clear and epiphytes were easy to observeSix previously ̄establishedꎬ one hectare ( 100 m times100 m)ꎬ permanent sampling plots in the old growtharea of the forest ( ca 35 m of canopy height) inMS ̄BNR were selected for this present studyꎬ threeof which were located in a tropical montane rainforestand three in an evergreen broadleaf forest ( Fig1049008 1ꎬTable 1) Plots were separated by a minimum straight

Fig1049008 1  Location of sampling plots and the MS ̄BNRꎬ Xishuangbanna The map showing the old growth forest area of MS ̄BNRꎬthe remaining blank areas are mainly covered by secondary forest or open land

9233 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

Table 1  Basic information of sampling plots in MS ̄BNRꎬ Xishuangbanna

Plot Elevation m Forest type Dominate tree Host occupancy

Basal area

Plot area(m2 ha)Epiphyte No of Ind

No of species

107 1450 MEBF CASMEKꎬ STYTON 561049008 3 241049008 4 217 24189 1700 MEBF CASMEKꎬ LITMAR 871049008 5 221049008 2 264 31192 1785 MEBF CASMEKꎬ ANNFRA 1001049008 0 251049008 6 389 30214 1670 TMRF SYZBRAꎬ LITBAC 811049008 3 451049008 6 399 48217 1700 TMRF ALAKURꎬ CRYBRA 931049008 8 221049008 2 310 36240 1750 TMRF CALPOLꎬ CASCAL 621049008 5 341049008 1 177 21

Note MEBF=Monsoon Evergreen Broadleaf Forestꎬ TMRF=Tropical Montane Rain Forest Dominate trees were selected by the first two importancevalue in a plot (nine sub plots tree data was appliedꎬ respectively) CASMEK=Castanopsis mekongensisꎬ STYTON=Styrax tonkinensisꎬ LITMAR=

Litsea martabanicaꎬ ANNFRA=Anneslea fragransꎬ SYZBRA=Syzygium brachythyrsumꎬ LITBAC=Lithocarpus bacgiangensisꎬ ALAKUR=Alangiumkurziiꎬ CRYBRA=Cryptocarya brachythyrsaꎬ CALPOL=Calophyllum polyanthumꎬ CASCAL=Castanopsis calathiformis Host occupancy was calcu ̄lated by 100 times epiphyte occupied trees total trees (16) in a plot

line distance of 700 m and a maximum of 3 600 mNine 10 m ̄radius circle subplots were set inside abig plotꎬ and trees (dbhge10 cmꎬ dbh = diameter atbreast height ) were measured and identified Ateach big plotꎬ a random point was marked near thecentral subplot of nineꎬ and the 16 nearest trees(dbhge10 cmꎬ covering an area of approximately 10 mradius subplot) were examined for epiphytesꎬ and96 trees were checked in total

Binoculars and a spotting ̄scope were first usedto check host tree roughlyꎬ only if epiphyte was de ̄tected on the groundꎬ we would access the crown u ̄sing single rope technique at least to the main forksite to assist specimen collecting and the latter epi ̄phytes countingꎬ attaching height measurement work(Perryꎬ 1978) A telescopic pruning shears withmaximum 5 m was also implemented to assist the col ̄lecting process Digital photographs were also takento document observations and assist in the identifica ̄tion process Due to identification barriersꎬ all smallseedlings were omitted and orchids that were hard toidentified without flower were all kept alive in green ̄houses until identifiedꎬ then herbarium specimenwere made

Epiphyte attaching height above ground wasmeasured using a 5 m poleꎬ orꎬ for those speciesdistributed in the outer of crownꎬ where could not beaccessedꎬ by estimating the height using the 5 mpole as a reference When estimating heightsꎬ the

observer stood at least 20 m away from the tree Epi ̄phytes that covered a substantial portion of the hostcrown (creeping or clustered speciesꎬ like Pyrrosialingua and Cylindrolobus marginatus)ꎬ the heightwas taken from the lowest to the highest points

Two schemes of forest canopy zonation were ap ̄plied in the former studiesꎬ six vertical tree zones(Steege and Cornelissenꎬ 1989) and equal height in ̄terval vertical tree zones (Zotz and Schultzꎬ 2008)ꎬboth were proved to be efficient approachesꎬ we fol ̄lowed the latter and forest canopy was divided intoseven height zones using a 5 m interval (the highestcrown layer was about 35 m) as several other studiesdid ( Zotz and Schultzꎬ 2008ꎻ Liu et alꎬ 2010)ꎬhence our results could be compared both in the tropi ̄cal forest domestically and abroadꎬ and the micro en ̄vironmental factors were more consistent in the paral ̄lel upper zones than the former arc ̄shaped scheme

To define epiphyte individualsꎬ we referred tothe individual definition of lsquostandrsquo (Sanfordꎬ 1968)A stand was defined as a cluster of pseudobulbs (orthe same epiphyte species leaves) was spatially sep ̄arated from anothermdasheither by an area devoid of ep ̄iphytes or occupied by other species When the samearea was occupied by an intermingling of more thanone speciesꎬ one stand was counted for each speciespresent If a stand of epiphyte covered two or morevertical zonesꎬ especially those with long rhizomes orlarge ̄area clustered pseudobulbsꎬ both individual

033                                  植 物 分 类 与 资 源 学 报                            第 37 卷

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

5333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 4: Diversity and Vertical Distribution Characteristics of ...

versity and vertical distribution characteristics of epi ̄phyte community in the tropical montane forest of Xi ̄shuangbannaꎬ addressing this knowledge gap in tropi ̄cal China Thusꎬ our study is an observational studyaimed at documenting diversityꎬ andꎬ henceꎬ can on ̄ly be suggestive of the community assembly processes(Johanssonꎬ 1974ꎻ Kellyꎬ 1985ꎻ Zotzꎬ 2007)

1  Methods11049008 1  Study site

Our study was conducted in the recently ̄estab ̄lished Bulong Nature Reserveꎬ Mengsong Section(MS ̄BNRꎬ 2009)ꎬ in Xishuangbannaꎬ China (Fig1049008 1)The vegetation type has been categorized as tropicalmontane rainforest and monsoon evergreen broadleafforestꎬ the former located in relatively humid regions(montane valleyꎬ riparian)ꎬ while the latter usuallyis found on the dry slopes The elevation ranges from1 110 m to 2 039 m (the peak of Sanduogeque)ꎬ and

mean monthly temperatures fluctuates between 15 -21 (at 1 600 m asl) The study site has a typicalmonsoon climate ( greatly influenced by the IndiaOcean monsoons) and the annual precipitation ran ̄ges between 1 800-2 379 mmꎬ 80 of which occursbetween the months of May and October The atmos ̄phere has an annual relative humidity of 83 (Zhuet alꎬ 2004)11049008 2  Field observations

Field work was conducted during the dry seasonNovember to Decemberꎬ 2012ꎬ when the crown lay ̄ers were clear and epiphytes were easy to observeSix previously ̄establishedꎬ one hectare ( 100 m times100 m)ꎬ permanent sampling plots in the old growtharea of the forest ( ca 35 m of canopy height) inMS ̄BNR were selected for this present studyꎬ threeof which were located in a tropical montane rainforestand three in an evergreen broadleaf forest ( Fig1049008 1ꎬTable 1) Plots were separated by a minimum straight

Fig1049008 1  Location of sampling plots and the MS ̄BNRꎬ Xishuangbanna The map showing the old growth forest area of MS ̄BNRꎬthe remaining blank areas are mainly covered by secondary forest or open land

9233 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

Table 1  Basic information of sampling plots in MS ̄BNRꎬ Xishuangbanna

Plot Elevation m Forest type Dominate tree Host occupancy

Basal area

Plot area(m2 ha)Epiphyte No of Ind

No of species

107 1450 MEBF CASMEKꎬ STYTON 561049008 3 241049008 4 217 24189 1700 MEBF CASMEKꎬ LITMAR 871049008 5 221049008 2 264 31192 1785 MEBF CASMEKꎬ ANNFRA 1001049008 0 251049008 6 389 30214 1670 TMRF SYZBRAꎬ LITBAC 811049008 3 451049008 6 399 48217 1700 TMRF ALAKURꎬ CRYBRA 931049008 8 221049008 2 310 36240 1750 TMRF CALPOLꎬ CASCAL 621049008 5 341049008 1 177 21

Note MEBF=Monsoon Evergreen Broadleaf Forestꎬ TMRF=Tropical Montane Rain Forest Dominate trees were selected by the first two importancevalue in a plot (nine sub plots tree data was appliedꎬ respectively) CASMEK=Castanopsis mekongensisꎬ STYTON=Styrax tonkinensisꎬ LITMAR=

Litsea martabanicaꎬ ANNFRA=Anneslea fragransꎬ SYZBRA=Syzygium brachythyrsumꎬ LITBAC=Lithocarpus bacgiangensisꎬ ALAKUR=Alangiumkurziiꎬ CRYBRA=Cryptocarya brachythyrsaꎬ CALPOL=Calophyllum polyanthumꎬ CASCAL=Castanopsis calathiformis Host occupancy was calcu ̄lated by 100 times epiphyte occupied trees total trees (16) in a plot

line distance of 700 m and a maximum of 3 600 mNine 10 m ̄radius circle subplots were set inside abig plotꎬ and trees (dbhge10 cmꎬ dbh = diameter atbreast height ) were measured and identified Ateach big plotꎬ a random point was marked near thecentral subplot of nineꎬ and the 16 nearest trees(dbhge10 cmꎬ covering an area of approximately 10 mradius subplot) were examined for epiphytesꎬ and96 trees were checked in total

Binoculars and a spotting ̄scope were first usedto check host tree roughlyꎬ only if epiphyte was de ̄tected on the groundꎬ we would access the crown u ̄sing single rope technique at least to the main forksite to assist specimen collecting and the latter epi ̄phytes countingꎬ attaching height measurement work(Perryꎬ 1978) A telescopic pruning shears withmaximum 5 m was also implemented to assist the col ̄lecting process Digital photographs were also takento document observations and assist in the identifica ̄tion process Due to identification barriersꎬ all smallseedlings were omitted and orchids that were hard toidentified without flower were all kept alive in green ̄houses until identifiedꎬ then herbarium specimenwere made

Epiphyte attaching height above ground wasmeasured using a 5 m poleꎬ orꎬ for those speciesdistributed in the outer of crownꎬ where could not beaccessedꎬ by estimating the height using the 5 mpole as a reference When estimating heightsꎬ the

observer stood at least 20 m away from the tree Epi ̄phytes that covered a substantial portion of the hostcrown (creeping or clustered speciesꎬ like Pyrrosialingua and Cylindrolobus marginatus)ꎬ the heightwas taken from the lowest to the highest points

Two schemes of forest canopy zonation were ap ̄plied in the former studiesꎬ six vertical tree zones(Steege and Cornelissenꎬ 1989) and equal height in ̄terval vertical tree zones (Zotz and Schultzꎬ 2008)ꎬboth were proved to be efficient approachesꎬ we fol ̄lowed the latter and forest canopy was divided intoseven height zones using a 5 m interval (the highestcrown layer was about 35 m) as several other studiesdid ( Zotz and Schultzꎬ 2008ꎻ Liu et alꎬ 2010)ꎬhence our results could be compared both in the tropi ̄cal forest domestically and abroadꎬ and the micro en ̄vironmental factors were more consistent in the paral ̄lel upper zones than the former arc ̄shaped scheme

To define epiphyte individualsꎬ we referred tothe individual definition of lsquostandrsquo (Sanfordꎬ 1968)A stand was defined as a cluster of pseudobulbs (orthe same epiphyte species leaves) was spatially sep ̄arated from anothermdasheither by an area devoid of ep ̄iphytes or occupied by other species When the samearea was occupied by an intermingling of more thanone speciesꎬ one stand was counted for each speciespresent If a stand of epiphyte covered two or morevertical zonesꎬ especially those with long rhizomes orlarge ̄area clustered pseudobulbsꎬ both individual

033                                  植 物 分 类 与 资 源 学 报                            第 37 卷

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

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Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

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Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

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Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

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Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

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Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 5: Diversity and Vertical Distribution Characteristics of ...

Table 1  Basic information of sampling plots in MS ̄BNRꎬ Xishuangbanna

Plot Elevation m Forest type Dominate tree Host occupancy

Basal area

Plot area(m2 ha)Epiphyte No of Ind

No of species

107 1450 MEBF CASMEKꎬ STYTON 561049008 3 241049008 4 217 24189 1700 MEBF CASMEKꎬ LITMAR 871049008 5 221049008 2 264 31192 1785 MEBF CASMEKꎬ ANNFRA 1001049008 0 251049008 6 389 30214 1670 TMRF SYZBRAꎬ LITBAC 811049008 3 451049008 6 399 48217 1700 TMRF ALAKURꎬ CRYBRA 931049008 8 221049008 2 310 36240 1750 TMRF CALPOLꎬ CASCAL 621049008 5 341049008 1 177 21

Note MEBF=Monsoon Evergreen Broadleaf Forestꎬ TMRF=Tropical Montane Rain Forest Dominate trees were selected by the first two importancevalue in a plot (nine sub plots tree data was appliedꎬ respectively) CASMEK=Castanopsis mekongensisꎬ STYTON=Styrax tonkinensisꎬ LITMAR=

Litsea martabanicaꎬ ANNFRA=Anneslea fragransꎬ SYZBRA=Syzygium brachythyrsumꎬ LITBAC=Lithocarpus bacgiangensisꎬ ALAKUR=Alangiumkurziiꎬ CRYBRA=Cryptocarya brachythyrsaꎬ CALPOL=Calophyllum polyanthumꎬ CASCAL=Castanopsis calathiformis Host occupancy was calcu ̄lated by 100 times epiphyte occupied trees total trees (16) in a plot

line distance of 700 m and a maximum of 3 600 mNine 10 m ̄radius circle subplots were set inside abig plotꎬ and trees (dbhge10 cmꎬ dbh = diameter atbreast height ) were measured and identified Ateach big plotꎬ a random point was marked near thecentral subplot of nineꎬ and the 16 nearest trees(dbhge10 cmꎬ covering an area of approximately 10 mradius subplot) were examined for epiphytesꎬ and96 trees were checked in total

Binoculars and a spotting ̄scope were first usedto check host tree roughlyꎬ only if epiphyte was de ̄tected on the groundꎬ we would access the crown u ̄sing single rope technique at least to the main forksite to assist specimen collecting and the latter epi ̄phytes countingꎬ attaching height measurement work(Perryꎬ 1978) A telescopic pruning shears withmaximum 5 m was also implemented to assist the col ̄lecting process Digital photographs were also takento document observations and assist in the identifica ̄tion process Due to identification barriersꎬ all smallseedlings were omitted and orchids that were hard toidentified without flower were all kept alive in green ̄houses until identifiedꎬ then herbarium specimenwere made

Epiphyte attaching height above ground wasmeasured using a 5 m poleꎬ orꎬ for those speciesdistributed in the outer of crownꎬ where could not beaccessedꎬ by estimating the height using the 5 mpole as a reference When estimating heightsꎬ the

observer stood at least 20 m away from the tree Epi ̄phytes that covered a substantial portion of the hostcrown (creeping or clustered speciesꎬ like Pyrrosialingua and Cylindrolobus marginatus)ꎬ the heightwas taken from the lowest to the highest points

Two schemes of forest canopy zonation were ap ̄plied in the former studiesꎬ six vertical tree zones(Steege and Cornelissenꎬ 1989) and equal height in ̄terval vertical tree zones (Zotz and Schultzꎬ 2008)ꎬboth were proved to be efficient approachesꎬ we fol ̄lowed the latter and forest canopy was divided intoseven height zones using a 5 m interval (the highestcrown layer was about 35 m) as several other studiesdid ( Zotz and Schultzꎬ 2008ꎻ Liu et alꎬ 2010)ꎬhence our results could be compared both in the tropi ̄cal forest domestically and abroadꎬ and the micro en ̄vironmental factors were more consistent in the paral ̄lel upper zones than the former arc ̄shaped scheme

To define epiphyte individualsꎬ we referred tothe individual definition of lsquostandrsquo (Sanfordꎬ 1968)A stand was defined as a cluster of pseudobulbs (orthe same epiphyte species leaves) was spatially sep ̄arated from anothermdasheither by an area devoid of ep ̄iphytes or occupied by other species When the samearea was occupied by an intermingling of more thanone speciesꎬ one stand was counted for each speciespresent If a stand of epiphyte covered two or morevertical zonesꎬ especially those with long rhizomes orlarge ̄area clustered pseudobulbsꎬ both individual

033                                  植 物 分 类 与 资 源 学 报                            第 37 卷

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

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Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

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munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 6: Diversity and Vertical Distribution Characteristics of ...

number and its name were repetitively recorded ineach zone Epiphyte species were registered either byscientific or morphological names in the field tableꎬand the individual number of each species was alsorecorded Specimens were identified by comparing tospecies at the herbarium at the Xishuangbanna Tropi ̄cal Botanical Garden Vouchers were lodged at theKunming Institute of Botany The plant names andfamilies followed Flora of China (eFlorasꎬ 2008)

The epiphyte life forms were defined followingBenzing ( 1990 ) scheme Iꎬ and categories werebased on relationships to the host (A Autotrophs)true epiphyteꎬ hemiepiphyteꎬ facultative and acci ̄dental epiphyte Howeverꎬ when we applied theserules in fieldꎬ distinguishing of epiphytic life formswas difficult in some cases for the lack of formerquantitative information Hereꎬ besides the definitionin the schemeꎬ some additional rules were set wegrouped the species can live on treesꎬ rocks or anysurfaces where the substrate layers was thin or absent(for exampleꎬ the moss mat or the thin layer of ca ̄nopy soil) into true epiphyteꎬ like most of the epi ̄phytic orchids and ferns Hemiepiphyte referred tothose species both had epiphytic and terrestrial pha ̄ses in their whole life processesꎬ and according tofirst living on tree or groundꎬ they could be dividedinto primary and secondary hemiepiphyte sub ̄catego ̄ries To avoid any confusion of lianas and secondaryepiphyte (Zotzꎬ 2013)ꎬ we excluded the secondaryepiphyte from hemiepiphyte categoryꎬ such as Ar ̄oidsꎬ Piperoids and climber Ficus sppꎬ only specieslike epiphytic Schefflera spp would root in ground fi ̄nallyꎬ were retained as primary hemiepiphyte Facul ̄tative epiphyte refers to species could inhabit forestcanopies and the ground interchangeablyꎬ such asPeperomia sppꎬ Medinilla spp and Hedychium sppThose species only few individuals anchored in thecanopy occasionallyꎬ but most of their individuals ofrooting in the groundꎬ were assigned to accidentalepiphyte category The species records from Flora ofChina and Flora of Yunnan (Wuꎬ 2006) were con ̄sulted during the life from determination

2  Results21049008 1  Floristics

Across the six plotsꎬ 96 trees were surveyedNineteen trees were without any epiphytesꎬ and theremaining 77 trees (80) were colonized by 1 756epiphyte individualsꎬ which were identified to 103species in 46 generaꎬ 14 families The epiphyte com ̄munity in MS ̄BNR was dominated by Orchidaceae(60) and ferns ( 24)ꎬ while other epiphyticspecies only took up 16 of the total flora recorded(Fig1049008 2ꎬ Appendix I)

Fig1049008 2  Epiphyte community floristic composition of

MS ̄BNRꎬ Xishuangbanna

21049008 2  Life form compositionNinety ̄Six species of true epiphytes were recor ̄

ded All 62 orchid species and all 25 ferns belongedto this group The most common species were Mycar ̄anthes pannea (215 individuals) and Davallia trich ̄omanoides (171 individuals) Other true epiphytesincluded five Asclepiadaceaeꎬ three Gesneriaceaeꎬand one Ericaceae species Surprisinglyꎬ we did notobserve any strangler figs in this tropical areaꎬ whichare normally a prominent characteristic of tropicalrain forests ( Harrison et alꎬ 2003) Tupidanthuscalyptratus and Schefflera elliptica were the hemiepi ̄phytes we recorded Five epiphytes were facultativein characterꎬ occurring as both terrestrial and epi ̄phytic plants and no accidental epiphyte were found

1333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

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Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

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munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 7: Diversity and Vertical Distribution Characteristics of ...

21049008 3  Species and life forms vertical distributionA summary of the vertical profile of epiphytes

observed in MS ̄BNR is given in Table 2 and Fig1049008 3The highest species richness was found in 10-15 mzoneꎬ which was in the mid ̄canopy of the forestꎬand the lowest zone was gt30 m tree height zoneꎬ onthe topmost canopy layer Howeverꎬ in terms of theabundance of individualsꎬ the base of host trees wasthe most important nicheꎬ where about 24 of epi ̄phyte individuals were found The highest attachedspeciesꎬ Hoya chinghungensisꎬ was observed at aheight of 32 m

Fig1049008 3  Vertical distribution profile of epiphyte communityof MS ̄BNRꎬ Xishuangbanna

As to the vertical profile of life ̄formsꎬ true epi ̄phytes dominated in terms of abundance in eachheight zoneꎬ and above 20 m of tree heightꎬ the pro ̄portion approached 100 In the 15-20 m zone andthe 25-30 m zoneꎬ Hedychium villosum and Micholit ̄zia obcordata were the only facultative epiphytes sha ̄ring the upper canopy with true epiphytes True epi ̄phytes showed a humped shape of distribution of

species richness along the vertical zonesꎬ while fa ̄cultative epiphytes declined in species richness withincreasing height The hemiepiphytes were abundantin the mid ̄zonesꎬ but only limited around the mainfork area21049008 4  Vertical zone details of the epiphyte community

0-5 m zone Usuallyꎬ this is a moist area withthick mossesꎬ very similar to the habitat of moss cov ̄ered rocks or hard soil surfacesꎬ and is a transitionalzone for terrestrial to epiphytic lives It is typified bysufficient water and mineral nutrients supplyꎬ butlight availability is usually low Overallꎬ we observed421 epiphyte individuals from 38 species in 11 fami ̄lies in this zone About 601049008 5 of these epiphyteswere ferns (23 spp)ꎬ mainly Polypodiaceae species(15 spp)ꎬ and the most abundant species were Pyr ̄rosia lingua and Lepisorus scolopendrium Other prom ̄inent epiphytes in this zone were Orchidaceae species(eight spp) Most of the orchids growing here werespecies that were generalist ( widely distributedthroughout the vertical zones)ꎬ like Pholidota articu ̄lataꎬ Dendrobium falconeri and Dendrobium chryso ̄toxum Howeverꎬ Liparis cespitosa and Dendrobiumcompactum were specialists (limited distribution spe ̄cies) in this zone The remaining epiphytes found inthis zone included species of Aspleniaceaeꎬ Davalli ̄aceaeꎬ Hymenophyllaceae and so on Excluding trueepiphytes ( 33 spp)ꎬ facultative epiphyte was themost abundant life ̄form Most of these facultative ep ̄iphytes had succulent functional organs to survive indry seasonꎬ such as leavesꎬ stemsꎬ and roots ( forinstanceꎬ the stem and leaves of Peperomia blandaꎬPellionia heteroloba and Medinilla himalayanaꎬ and

Table 2  Occurrence of vascular epiphytes in the vertical profile of the MS ̄BNR forest

Height m Indi No Spp No Indi( total)

Spp( total) Typical species (gt10 of total height zone)

  0-5 421 38 24 37 Haplopteris flexuosaꎬ Davallia trichomanoides51049008 1-10 330 40 19 39 Davallia trichomanoides

101049008 1-15 325 53 19 51 Mycaranthes pannea151049008 1-20 349 39 20 38 Mycaranthes panneaꎬ Coelogyne viscosaꎬ Coelogyne fuscescens201049008 1-25 117 28 7 27 Bulbophyllum levineiꎬ Mycaranthes pannea251049008 1-30 200 25 11 24 Mycaranthes panneaꎬ Cylindrolobus marginatus

gt301049008 1    14 7 1 7 Mycaranthes panneaꎬ Bulbophyllum pectinatum

233                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

5333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 8: Diversity and Vertical Distribution Characteristics of ...

Pseudostems of Hedychium villosum)5-10 m zone This height zone forms the tran ̄

sition from the trunk to the main fork Compared tothe lower part of the tree trunkꎬ because most of thestem flowꎬ this region is drier than ̄but still not asdry as ̄the upper layers of crown 40 species in 10families of 330 individuals were recorded in thiszone The flora composition of the epiphyte commu ̄nity in zone 5-10 m was similar to that in zone 0-5mꎬ but orchids (17 spp) became more abundantꎬand the most common species were Coelogyne viscosaand Dendrobium falconeri Ferns were also a promi ̄nent part of the epiphyte community in this zone (18spp)ꎬ still mainly Polypodiaceae species (11 spp)The most abundant ferns were Davallia trichoman ̄oides and Polypodiastrum argutum Hemiepiphyte(Schefflera elliptica) made an appearance hereꎬ andthe remaining nine species belonged to AspleniaceaeꎬDavalliaceae Hymenophyllaceaeꎬ Vittariaceaeꎬ Gesn ̄eriaceaeꎬ Araliaceaeꎬ Piperaceae and Urticaceae

10-15 m zone The micro habitat environmentalfactors here are all at a moderate levelꎬ together withsufficient surfaces for adheringꎬ the epiphyte commu ̄nity diversity was expected high in this zone To thatendꎬ just as we anticipatedꎬ epiphyte species diversi ̄ty was highest in this zoneꎬ with 53 species in ninefamilies and 325 individuals represented The domi ̄nant species were Mycaranthes pannea and Davalliatrichomanoides Orchids (36 spp) took up the mostproportion of the community Ferns were also a sub ̄stantial component (11 spp)ꎬ and again were mainlyPolypodiaceae species (7 spp)ꎬ like Pyrrosia lin ̄guaꎬ Lepisorus henryiꎬ and Lepisorus sinensis Otherferns included Asplenium antrophyoidesꎬ Humata grif ̄fithianaꎬ and Haplopteris flexuosa Another character ̄istic of this zone was the prevalence of hemiepiphytesSchefflera elliptica and Tupidanthus calyptratusꎬ thetwo hemiepiphytes were both found in this zone Theremaining epiphytes of this zone included Asclepia ̄daceaeꎬ Piperaceaeꎬ Gesneriaceae and Davalliaceaespeciesꎬ such as Dischidia tonkinensisꎬ Peperomiablandaꎬ and Aeschynanthus austroyunnanensis

15 - 20 m zone The microhabitat in this zonebecomes drierꎬ and branches have smoother barkand relatively ̄smaller adherence surfacesꎬ but lightconditions improve A total of 349 individuals among39 species in seven families were recorded Domi ̄nant species here were Mycaranthes pannea andCoelogyne viscosa Orchids still comprised the majori ̄ty of species (23 spp)ꎬ followed by ferns (10 spp)Species like Coelogyne fuscescensꎬ Polypodiastrum ar ̄gutumꎬ and Pholidota yunnanensis were all prevalentin this zone The six remaining species were from As ̄clepiadaceaeꎬ Gesneriaceae and Zingiberaceae Epi ̄phyte life forms diversity decreased in this zoneꎬ be ̄sides the true epiphytesꎬ only one facultative species(Hedychium villosum) were recorded

20-25 m zone We recorded 117 individuals a ̄mong 28 species in five families in this zone Com ̄pared to the typical densely clustered appearances ofepiphyte community observed in lower zonesꎬ epi ̄phytes here were scattered throughout on smallerbranches and forks The dominant epiphytes were or ̄chidsꎬ Bulbophyllum levinei and Mycaranthes panneaꎬand the proportion of orchids in the community washigh ( 20 spp or 71)ꎬ while there were fewerferns (6 spp or 21)ꎬ including Pyrrosia linguaꎬAraiostegia perdurans and Lepisorus scolopendriumAgapetes mannii here was the only Ericaceae epi ̄phytic species in the study area

25-30 m zone Most epiphytes in this zone weredistributed on the relatively ̄larger branchesꎬ onlyvery few species occurred on the smaller forks ortwigs inside the canopy 25 speciesꎬ 200 individualsin four families were observed hereꎬ and the commu ̄nity was dominated by Mycaranthes pannea and Cy ̄lindrolobus marginatus Most species were orchids(19 spp)ꎬ and four Polypodiaceaeꎬ one Asclepia ̄daceaꎬ and one Ericaceae species constituting theremaining community members

30-35 m zone This zone covers the uppermostlayer of canopyꎬ and was the most instable of habitatamong all zonesꎬ and could be described as theharshest environment for most epiphytes Only 14 in ̄

3333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

5333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 9: Diversity and Vertical Distribution Characteristics of ...

dividuals of seven species in four families occurredhere Most of these species were generalists occur ̄ring throughout the vertical profileꎬ including or ̄chids (four spp) like Mycaranthes pannea and Bul ̄bophyllum pectinatumꎬ and ferns (two spp)ꎬ Dava ̄llia trichomanoides and Pyrrosia lingua Hoya ching ̄hungensis (Asclepiadaceae) six individuals were on ̄ly found in upper zones (16-32 m of canopy) andseemed to be a specialist to high canopy layers Den ̄drolirium tomentosum was also only found in thiszoneꎻ howeverꎬ as only one individual was observedꎬwe cannot deduce anything about the vertical nicheof this species

3  Discussion31049008 1  Floristics

This is the first study to document the vascularepiphyte community in MS ̄BNRꎬ and the first suchstudy performed in Xishuangbannaꎬ which is other ̄wise well ̄known for its high plant diversity (Zhu andYanꎬ 2012) Although it was still an incomplete in ̄ventory of the areaꎬ we recorded 103 species in 47genera and 14 families on 77 host trees ( total plotarea ca 01049008 2 ha)ꎬ confirming the assertion that epi ̄phytes are abundant and diverse in the tropical area(Kuumlper et alꎬ 2004)

The survey of epiphytes in Huanglian mountaincloud forest found 151 species (including lianas likePiperoidsꎬ Aroids and Vitis) on 233 trees (Yangꎬ2008) Liu (2010) found 120 species in BawangRidge in Hainan Island among six forest types over a31049008 6 ha area Other studies from China reported fromsubtropical or warm temperate areas all recordedlower levels of species richness than we found at MS ̄BNR For exampleꎬ Xu and Liu (2005) only found32 species on 80 host trees in a montane moist ever ̄green broad ̄leaved forest on Ailao Mountain (about200 km north of MS ̄BNR)ꎬ and in a semi ̄humidevergreen broad ̄leaved forest only nine species ofepiphyte were found in 01049008 1 ha area ( Xu et alꎬ2006) Similarlyꎬ Liu et al (2010) found 27 spe ̄cies in a 01049008 6 ha natural tropical coniferous forestꎬ

while Wang et al (1996) found 41 species of ob ̄ligate vascular epiphytes in a subtropical evergreenbroadleaf forest Hsu (2009) recorded a high levelof epiphyte species richness for the whole of Taiwan(336 speciesꎬ including lianas like Figsꎬ Piperoidsand Aroids)ꎬ not only that was based on the totalflora for a large island in many ecological zonesꎬ butalso included the confusing secondary hemiepiphytes(Hsu and Wolfꎬ 2009)

Epiphyte research in tropical Africa suggestsepiphyte species richness is similar to the levels wefound in MS ̄BNR and for tropical China in generalꎬmuch higher than the Temperate zone ( Hsu andWolfꎬ 2009ꎬ Table 2)ꎬ but much lower than theNeotropics This may be explained by the lack someimportant epiphyte families like Bromeliaceae ( ca1 770 epiphytic spp)ꎬ Cactaceae (ca 125 epiphyticspp) and some Orchid genera like Pleurothallis (1500spp) in the Paleotropics (Zotzꎬ 2013)31049008 2  Vertical structure

Different micro ̄environmental factors are thoughtto structure the vertical distribution of epiphytesꎬ asdescribed in several studies (Johanssonꎬ 1974ꎻ Stee ̄ge and Cornelissenꎬ 1989ꎻ Benzingꎬ 1990ꎻ Lowmanand Rinkerꎬ 2004ꎻ Zotzꎬ 2007ꎻ Kroumlmer et alꎬ 2007)Moreoverꎬ investigations into microclimatic variationhave confirmed the expected patterns of vertical het ̄erogeneity (Dhanmanondaꎬ 1996ꎻ Freibergꎬ 1997)We found that the middle canopy had the highestspecies richnessꎬ which is consistent with earlierstudies ( Steege and Cornelissenꎬ 1989ꎻ Freibergꎬ1996ꎻ Zotz and Schultzꎬ 2008ꎻ Pos and Sleegersꎬ2010) The humped shape distribution profile throug ̄hout the forest canopy may be explained by the mod ̄erate water and light conditions in the middle cano ̄pyꎬ combined with the relative larger effective sur ̄face area and more suitable substrate ( Nadkarniꎬ1984ꎻ Freiberg and Freibergꎬ 2000) Kroumlmer et al(2007) found thatꎬ besides the diverse and abun ̄dant epiphyte flora of the middle canopyꎬ there wasa conspicuous epiphyte flora in the understory (40aroidsꎬ 35-40 piperoids and 25-30 ferns)

433                                  植 物 分 类 与 资 源 学 报                            第 37 卷

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

5333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 10: Diversity and Vertical Distribution Characteristics of ...

We did not check the epiphyte flora on smaller trees(dbhlt10 cm)ꎬ but obtained a similar resultꎬ thatthe highest abundance of epiphyte individuals wasobserved in 0-5 m zone

True epiphytes are the overwhelming majority inevery zoneꎬ and they mix with little proportion withother epiphytic life ̄forms in and under middle zonesFacultative and hemiepiphytes could be hardly foundabove 15 m of canopy The tree base areaꎬ corre ̄sponding to 0 - 5 m zoneꎬ is a transition area fromterrestrial to epiphytic lives Much of the host treebase area is covered by a thick moss mat in humidenvironments (Freibergꎬ 1997)ꎬ which could be agood explanation of abundant facultative epiphyteshere In 5-10 m and 10-15 m zonesꎬ the appear ̄ance and prevailing of hemiepiphytes was the mostapparent characteristic The upper zones of canopy(15-35 m)ꎬ where almost only true epiphytes werefoundꎬ had more than half of the true epiphytes com ̄prised of orchids Epiphytic orchids are generally re ̄garded as drought ̄enduring plantsꎬ and have succu ̄lent structures ( pseudobulbꎬ terete leafꎬ or fleshyroot) (Benzingꎬ 1990)ꎬ thus can be used as a goodexplanation for this phenomenon

4  ConclusionOur survey recorded a high diversity of epiphytesꎬ

as is generally reported in studies of tropical forestsꎬand confirmed a similar humped vertical structuringof the epiphyte community around mid canopy TheMS ̄BNR could potentially provide a protected habi ̄tat for a large diversity of epiphytes We suggest fu ̄ture studies focus on species of conservation con ̄cernꎬ as many other forests in China ̄and even inXishuangbanna ̄have been over ̄harvested for epi ̄phytes ( in particularꎬ orchidsꎬ such as medicinaland ornamental Dendrobium sppꎬ Vanda spp andCymbidium spp)

Acknowledgement We thank Xishuangbanna Tropical Bo ̄tanical Garden and the Program for Field Studies in TropicalAsia for supporting the ldquoAdvanced Field Course in Ecology

and Conservationrdquo in Xishuangbanna (AFEC ̄X) during whichthe field research for this study took place We wish to thankthe resource staff and colleagues on the AFEC ̄X 2012 forcritical comments and suggestions Funding for ZM and KMMwas provided by the Centre for Mountain Ecosystem StudiesOther authors were funded by AFEC ̄X

ReferencesBenzing DHꎬ 1990 Vascular Epiphytes General Biology and Related

biota [M] UK Cambridge University PressBenzingꎬ DHꎬ 2012 Air Plants Epiphytes and Aerial Gardens [M]

Ithaca Cornell University PressCornelissen Jtꎬ Steege HTꎬ 1989 Distribution and ecology of epiphyt ̄

ic bryophytes and lichens in dry evergreen forest of Guyana [J] Journal of Tropical Ecologyꎬ 5 (2) 131mdash150

eFlorasꎬ 2008 Published on the Internet [OL] http www1049008efloras1049008org [accessed 2012 ̄2014] Missouri Botanical Gardenꎬ St LouisꎬMO Harvard University Herbariaꎬ Cambridgeꎬ MA

Dhanmanonda Pꎬ 1996 Three ̄dimensional distribution of light inten ̄sity in the dry dipterocarp forest at Sakaeratꎬ Northeastern Thai ̄land [J] Thai Journal of Forestryꎬ 15 (2) 81mdash88

Freiberg Mꎬ 1996 Spatial distribution of vascular epiphytes on threeemergent canopy trees in French Guiana [ J] Biotropicaꎬ 28(3) 345mdash355

Freiberg Mꎬ 1997 Spatial and temporal pattern of temperature andhumidity of a tropical premontane rain forest tree in Costa Rica[J] Selbyanaꎬ 18 (1) 77mdash84

Freiberg Mꎬ Freiberg Eꎬ 2000 Epiphyte diversity and biomass in thecanopy of lowland and montane forests in Ecuador [J] Journal ofTropical Ecologyꎬ 16 (05) 673mdash688

Gentry AHꎬ Dodson Cꎬ 1987 Diversity and biogeography of neotropi ̄cal vascular epiphytes [J] Annals of the Missouri Botanical Gar ̄denꎬ 74 (2) 205mdash233

Harrison RDꎬ Hamid AAꎬ Kenta T et alꎬ 2003 The diversity of he ̄mi ̄epiphytic figs ( Ficusꎻ Moraceae) in a Bornean lowland rainforest [J] Biological Journal of the Linnean Societyꎬ 78 (4)439mdash455

Hsu Rꎬ Wolf JHꎬ 2009 Diversity and phytogeography of vascular epi ̄phytes in a tropical ̄subtropical transition islandꎬ Taiwan [ J] Floraꎬ 204 (8) 612mdash627

Johansson Dꎬ 1974 Ecology of vascular epiphytes in West Africanrain forest [J] Acta Phytogeographica Suecicaꎬ 59 1mdash136

Kelly Dꎬ Tanner Eꎬ Lughadha et alꎬ 1994 Floristics and biogeogra ̄phy of a rain forest in the Venezuelan Andes [J] Journal of Bio ̄geographyꎬ 21 (4) 421mdash440

Kelly DLꎬ 1985 Epiphytes and climbers of a Jamaican rain forestvertical distributionꎬ life forms and life histories [ J] Journal ofBiogeographyꎬ 12 (3) 223mdash241

Kelly DLꎬ OprimeDonovan Gꎬ Feehan J et alꎬ 2004 The epiphyte com ̄

5333 期        ZHAO Ming ̄xu et al Diversity and Vertical Distribution Characteristics of Vascular Epiphytes in 1049018       

munities of a montane rain forest in the Andes of Venezuela pat ̄terns in the distribution of the flora [J] Journal of Tropical Ecol ̄ogyꎬ 20 (6) 643mdash666

Kroumlmer Tꎬ Kessler Mꎬ Gradstein SRꎬ 2007 Vertical stratification ofvascular epiphytes in submontane and montane forest of the Bo ̄livian Andes the importance of the understory [J] Plant Ecol ̄ogyꎬ 189 (2) 261mdash278

Kuumlper Wꎬ Kreft Hꎬ Nieder J et alꎬ 2004 Large ̄scale diversity pat ̄terns of vascular epiphytes in Neotropical montane rain forests[J] Journal of Biogeographyꎬ 31 (9) 1477mdash1487

Liu Gꎬ 2010 Diversity and distribution of vascular epiphytes of tropi ̄cal forests in Hainan Islandꎬ China [D] Dissertationꎬ Chineseacademy of forestryꎬ Beijing

Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

Lowman MDꎬ Rinker HBꎬ 2004 Forest Canopies [M] SandiegoꎬCaliforniaꎬ USA Academic Pressꎬ 2004

McCune Bꎬ Amsberry Kꎬ Camacho F et alꎬ 1997 Vertical profile ofepiphytes in a Pacific Northwest old ̄growth forest [ J] North ̄west Scienceꎬ 71 (2) 145mdash152

Myers Nꎬ Mittermeier RAꎬ Mittermeier CG et alꎬ 2000 Biodiversityhotspots for conservation priorities [ J] Natureꎬ 403 (6772)853mdash858

Nadkarni NMꎬ 1984 Epiphyte biomass and nutrient capital of a neo ̄tropical elfin forest [J] Biotropicaꎬ 16 (4) 249mdash256

Nieder Jꎬ Engwald Sꎬ Barthlott Wꎬ 1999 Patterns of neotropical epi ̄phyte diversity [J] Selbyanaꎬ 20 (1) 66mdash75

Parker GGꎬ 1995 Structure and microclimate of forest canopies [A] Lowman MDꎬ Nadkarni NM edꎬ Forest Canopies [M]ꎬ 1stedn San Diegoꎬ USA Academic Pressꎬ 73mdash106

Perry DRꎬ 1978 A method of access into the crowns of emergent andcanopy trees [J] Biotropicaꎬ 10 155mdash157

Pittendrigh CSꎬ 1948 The bromeliad ̄Anopheles ̄malaria complex inTrinidad I ̄The bromeliad flora [J] Evolutionꎬ 2 (1) 58mdash89

Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

Goeldi Ciecircncias Naturaisꎬ 5 (3) 335mdash344Sanford WWꎬ 1968 Distribution of epiphytic orchids in semi ̄decidu ̄

ous tropical forest in southern Nigeria [J] The Journal of Ecolo ̄gyꎬ 56 (3) 697mdash705

Steege Htꎬ Cornelissen Jꎬ 1989 Distribution and ecology of vascularepiphytes in lowland rain forest of Guyana [ J] Biotropicaꎬ 21(4) 331mdash339

Wang Jꎬ Wei Pꎬ Huang Zꎬ 1996 The epiphyte of Dinghu Mountain[J] Journal of Jilin Agricultural Universityꎬ 18 (3) 40mdash44

Wang Hꎬ Zhu Hꎬ Li Bꎬ 2001 A study on the tropical montane rainforest in Mengsongꎬ Xishuangbannaꎬ S Yunnan [J] Guihaiaꎬ21 (4) 303mdash314

Wu ZYꎬ 2006 Flora of Yunnan [M] Beijing Science PressXu Hꎬ Liu Wꎬ 2005 Species diversity and distribution of epiphytes in

the montane moist evergreen broad ̄leaved forest in Ailao Moun ̄tainꎬ Yunnan [J] Biodiversity Scienceꎬ 13 (2) 137mdash147

Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

Yang Jꎬ 2008 Biodiversity and spatial distribution of vascular epi ̄phytes in cloud forest on Huanglian Mountainꎬ Yunnan Province[D]ꎬ MSc Thesisꎬ Kunming Institute of Botanyꎬ Chinese Acad ̄emy of Sciencesꎬ Beijing

Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

Zhu Hꎬ 2006 Forest vegetation of Xishuangbannaꎬ south China [J] Forestry Studies in Chinaꎬ 8 (2) 1mdash58

Zhu Hꎬ Yan Lꎬ 2012 Native Seed Plants in Xishuangbanna of Yun ̄nan [M] Beijing Science Press

Zotz Gꎬ 2007 Johansson revisited the spatial structure of epiphyteassemblages [J] Journal of Vegetation Scienceꎬ 18 (1) 123mdash130

Zotz Gꎬ Schultz Sꎬ 2008 The vascular epiphytes of a lowland forest inPanamamdashspecies composition and spatial structure [ J] PlantEcologyꎬ 195 (1) 131mdash141

Zotz Gꎬ 2013 The systematic distribution of vascular epiphytesmdashacritical update [ J] Botanical Journal of the Linnean Societyꎬ171 (3) 453mdash481

633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

书书书

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()+

-01-2

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833                                  植 物 分 类 与 资 源 学 报                            第 37 卷

Page 11: Diversity and Vertical Distribution Characteristics of ...

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Liu Gꎬ Ding Yꎬ Zang R et alꎬ 2010 Diversity and distribution ofvascular epiphytes in the tropical natural coniferous forest of Hain ̄an Islandꎬ China [J] Chinese Journal Plant Ecologyꎬ 34 (11)1283mdash1293

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Pos ETꎬ Sleegers ADMꎬ 2010 Vertical distribution and ecology ofvascular epiphytes in a lowland tropical rain forest of Brazil [J] Boletim do Museu Paraense Emiacutelio Goeldi Bol Mus Para Emilio

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Xu Hꎬ Liu Wꎬ Shen Y et alꎬ 2006 A preliminary study of epiphytes insemi ̄humid evergreen broad ̄leaved forest in Stone ̄forest KarstRegionꎬ Yunnan Province [J] Guihaiaꎬ 26 (1) 43mdash48

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Zhu Hꎬ Wang Hꎬ Li Bꎬ 2004 Plant diversity and physiognomy of atropical montane rain forest in Mengsongꎬ South Yunnanꎬ China[J] Acta Phytoecologica Sinicaꎬ 28 (3) 351mdash360

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633                                  植 物 分 类 与 资 源 学 报                            第 37 卷

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