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Patterns in species richness and distributionof vascular epiphytes in Chiapas, Mexico Jan H. D. Wolf* and Alejandro Flamenco-S El Colegio de la Frontera Sur (ECOSUR),Chiapas, Mexico

AbstractAim We aim to assess regional patterns in the distribution and species richness of vascular epiphytes with an emphasis on forests that differ in altitude and the amount of rainfall.

Location Tropical America, in particularly the 75,000 km 2 large state of Chiapas insouthern Mexico at 14.518.0 N. Chiapas is diverse in habitats with forests from sea-level to the tree-line at c. 3800 m altitude and with annual amounts of rainfall rangingfrom 800 to over 5000 mm. It is also one of the botanical best-explored regions in thetropics.

Methods First we give an overview of epiphyte inventories to date. Such epiphytesurveys were mostly carried out on the basis of surface area or individual trees and wediscuss their problematic comparison. Applying a different methodological approach, wethen used 12,276 unique vascular epiphyte plant collections from Chiapas that aredeposited in various botanical collections. The locality data were georeferenced andcompiled in a relational data base that was analysed using a geographical informationsystem. To compare the number of species between inventories that differed in thenumbers of records, we estimated the total richness, SChao , at each.

Results We recorded 1173 vascular epiphyte species in thirty-nine families (twenty-three angiosperms), comprising c. 14% of all conrmed plant species in the state. Abouthalf of all species were orchids (568). Ferns and bromeliads were the next species-richgroups with 244 and 101 species, respectively. Most species were found in the MontaneRain Forest and in the Central Plateau. Trees of different forest formations, rainfallregimes, altitudes and physiographical regions supported a characteristic epiphyte ora.Main conclusions We were able to conrm the presumed presence of a belt of highdiversity at mid-elevations (5002000 m) in neotropical mountains. In contrast to pre-dictions, however, we observed a decrease in diversity when the annual amount of rainfall exceeded 2500 mm. The decrease is attributed to wind-dispersed orchids, bro-meliads and Pteridophyta that may nd establishment problematical under frequentdownpours. In the wet but seasonal forests in Chiapas, this decrease is not compensatedby plants in the animal-dispersed Araceae that are abundant elsewhere. We presume thatin addition to the annual amount of rainfall, its distribution in time determines thecomposition of the epiphyte community.

Keywords

Botanical collections, canopy biology, elevation gradient, epiphyte quotient, geograph-ical information system, rainfall gradient, SChao estimate of diversity, tropical forests.

*Correspondence and present address: Jan H. D. Wolf, Universiteit van Amsterdam, Institute for Biodiversity and Ecosystem Dynamics (IBED), P.O. Box 94062,1090 GB Amsterdam, The Netherlands. E-mail: [email protected]

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INTRODUCTION

Biotic inventories have shown that the number of speciesnear the equator is substantially larger than at latitudesbeyond the tropics for many groups of organisms (Pianka,1966), even when exceptions (bryophytes) also do exist(Wolf, 1993a). Diversity patterns within the tropics, how-

ever, are less well-documented. In particular, the distributionof organisms in the high forest canopy remains ambiguous,probably because of its difcult accessibility (Moffett, 1993;Mitchell et al. , 2002). On the contrary, it is justied to payspecial attention to the high canopy because the upperstratum in the forest harbours a wealth of species in differentkinds of groups such as mammals, birds, arthropods andepiphytic plants (Stork, 1988; Malcolm, 1991; Nadkarni,1994; Greeney, 2001; Winkler & Preleuthner, 2001). Of allknown vascular plant species, c. 10% occur as epiphytes,depending for support, but not for nutrients or water, onother plants, usually trees (Kress, 1986). In small 0.1-haforest plots epiphytes may comprise up to 35% of all vas-cular plant species (Gentry & Dodson, 1987a). This numberwould even have increased substantially if non-vascularepiphytes were included (Wolf, 1993b).

The great species richness, the variety of growth forms andthe high abundance of the epiphytic component of tropicalforests have attracted botanists since the nineteenth century(Schimper, 1888). Classical epiphyte studies relied heavilyon distance observations and plants were usually collectedfrom the forest oor (Went, 1940; Johansson, 1974). Theusefulness of distance observations for epiphyte inventorieshas always been questioned, and justiably so (Flores-Pala-cios & Garcia-Franco, 2001). As a consequence, epiphytesare well-represented in herbaria world-wide, but were rarelyincluded in systematic forest inventories.

With the advance of new techniques to obtain access tothe canopy such as rope-climbing (Perry, 1978) and the useof construction cranes, oristic inventories that includecanopy epiphytes, however, are available at an increasingrate (Lowman, 2001). In agreement with early epiphytestudies, in situ observations conrm that epiphytes exhibit aclear vertical zonation within the host tree with few speciesshared between the tree crown and the trunk base (Jarman& Kantvilas, 1995).

The larger number of inventories raises expectations thatinsight may also be obtained in the more elusive horizontalpatterns of diversity and distribution of the epiphytes in theforest. Over small distances, earlier observations in treeplantations that epiphytes grow aggregated within the forest

(Madison, 1979) have recently been conrmed for naturalforests (Bader et al. , 2000). Locally, the distribution maythus be better explained from a dispersal-assembly perspec-tive than from a niche-assembly perspective (Hubbell, 2001).On a larger scale, between regions, Gentry & Dodson(1987a) postulated that epiphytes decreased more drasticallythan any other habit group in dryer areas and that epiphyterichness is greatest on mountains at mid-elevations. Thesehypotheses, however, have been difcult to corroborate andhave been questioned (Ibisch et al. , 1996).

The aim of this study is to provide insight into the patternsof distribution and richness of epiphytes on a regional scale.Therefore an overview of epiphyte inventories in the tropicsso far is presented and their problematical comparison dis-cussed. In a different methodological approach, we will nextuse botanical herbarium collections from an environmentallyheterogeneous region and integrate those in a geographical

information system (GIS). In this way, we combine thewealth of information from early botanical explorationswith that of recent epiphyte inventories. For practical rea-sons (mapping), we use a political unit as study area: thestate of Chiapas in southern Mexico. Chiapas has over 1000species of vascular epiphytes and is, with tens of thousandsherbarium specimens, one of the better-explored botanicalregions in the tropics (Breedlove, 1986).

M AT E R I A L S A N D M E T H O D S

Study site

The state of Chiapas in southern Mexico is situatedbetween 14.518.0 N and 90.394.5 W and comprisesc. 75,000 km 2 (Fig. 1). The climate is diverse, ranging fromsemi-desert to areas where annual rainfall exceeds 3500 mmand from lowland tropical to mountain temperate. Much of the area is characterized by an alternate wet and dry seasonwith the dry period lasting between 2 and 6 months. For adescription of the physiographical regions and vegetationtypes we rely on Breedlove (1978).

Chiapas can be divided into seven physiographical regions.A volcanic mountain range, the Sierra Madre, with theTacana volcano (4110 m) as its highest peak, separates thenarrowPacic Coastal Plain from theCentral Depression andthe eastern part of the state. The Central Depression, a dry

terraced valley from 500 to 1200 m, was originally coveredwith a deciduous forest but extensive cultivation has led tolarge sections of thorn woodland and savanna. The strata aremostly marine limestone and slates. The highlands may bedivided into the Central Plateau, The Eastern Highlands andtheNorthernHighlands. The Central Plateau hasan elevationbetween 2100 and 2500 m with a few peaks up to 2900 m. Itis composed of marine limestone with extrusions of volcanicrock on the higher peaks. Tropical deciduous forest and pine-oak forest cover the dryer western part, making place forpineoak Liquidamber and montane rain forest in the easternpart. The Eastern Highlands have similar strata, but at lowerelevations ranging from 400 to 1500 m. Lower montane rainforest is the most common vegetation type. The Northern

Highlands are more diverse in altitude, geology and associ-ated vegetation types. Besides pineoak Liquidamber andmontane rainforest, a transitional forestbetween tropical andlower montane rain forest and thorn woodland also occurs:the evergreen and semi-evergreen seasonal forest. This for-mation is also common on the slopes of the Sierra Madre.North of the highlands the Gulf Coastal Plain reaches intoChiapas. The vegetation is mostly tropical secondary growth.

The diversity in soils, climate and associated forest for-mations helps to explain why the state of Chiapas is among

2003 Blackwell Publishing Ltd, Journal of Biogeography , 30 , 16891707

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the richest in species of Mexico, despite its small territory of slightly < 4%. For example, the number of vascular plantspecies recorded for Chiapas is 8248 species of an estimatedtotal of 22,800 for the whole country (Breedlove, 1981;Breedlove, 1986; Rzedowski, 1992).

Methods

We compiled label data of epiphytes in several herbaria that

are known to have relatively large collections from the stateof Chiapas (Table 1). Hemi-epiphytes were included, butfacultative epiphytes were not if their presence on trees wasregarded as highly unusual (e.g. Agave sp.). The ecologicallydifferent heterotrophic Loranthaceae were also excluded.

We considered only specimens identied to the level of species or below. Varieties and subspecies were treated asindividual species in the diversity estimates. All informationconcerning the collector, collectors number, collection date,taxonomy, locality and habitat were copied from the her-

barium labels and entered in a relational data base (Micro-soft Access). Specic information may be provided onrequest from the rst author. Most labels contained noinformation about the latitude and longitude of the collec-tion site. With the help of topographical maps (InstitutoNacional de Estad stica, Geograf a e Informatica, INEGI,1 : 50.000) such data was estimated to a precision of seconds. In case the identication of duplicate collectionsdiffered, the name given by the experienced taxonomist or

group specialist was adopted. When no clear differentiationbetween taxonomists could be made, both names weremaintained (197 cases).

The spatial distribution of species was analysed in a GIS(ArcInfo, Redlands, California, USA) where the position of species was superimposed on digitized topographical,physiographical, rainfall and vegetation maps that have beenprepared at Ecosur. The topographical overlay was derivedfrom maps (1 : 250.000) published in print by INEGIbetween 1985 and 1989 (locality references E15-07, E15-11,

Figure 1 Distribution of epiphyte collectionsites. Physiographical regions in Chiapasafter Breedlove (Breedlove, 1978).

Table 1 The plant collections that were examined for vascular epiphytes from Chiapas

Institute Acronym Location No. of specimen

California Academy of Sciences CAS San Francisco, CA, USA 5416Instituto de Biolog a, UNAM MEXU Mexico City, Mexico 4437Asociacion Mexicano de Orquideolog a, A. C. AMO Mexico City, Mexico 1440 Jard n de Orqu deas San Cristo bal San Cristo bal de Las Casas, Chiapas, Mexico 508El Colegio de la Frontera Sur ECO-SC-H San Cristo bal de Las Casas, Chiapas, Mexico 210Instituto de Historia Natural CHIP Tuxtla Gutie rrez, Chiapas, Mexico 154Literature records 111

Total 12,276


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E15-12, E15-05, E15-02, E15-10 and D15-01) and frommaps by the Secretar a de Programacio n y Presupuesto (SPP),published in 1983 (locality references E15-08 and E15-09).The vegetation overlay was derived from maps (1 : 250.000)by INEGI (19851988; locality references E15-10, D15-01,E15-02, E15-07, E15-08, and E15-12) and by SPP (1984;locality references E15-09, E15-11 and E15-05). The veget-

ation maps are based on aerial photographs taken between1972 and 1981. We used the physiographical overlay elab-orated by D. Navarrete (Ecosur) on the basis of Mu llerrieds(1957) geological map. As to rainfall, four climatic maps(1 : 500.000) were used, published in 1970 by the Comisio npara el estudio del territorio nacional (Cetenal), UniversidadNacional Auto noma de Me xico (UNAM); locality references15-PI, 15-PII, 15-QVII and 15-QVIII.

We use Chaos nonparametric diversity estimator to esti-mate the overall diversity of the samples which typically willhave continuously rising speciesaccumulation curves (Chao,1984). Her estimator ( SChao ) provides an estimate of thecompleteness of the sampling, enables a comparison betweenunequal-sized samples, has a relatively low sensitivity tovarying sample intensity and species richness, and performsespecially well in data with a preponderance of relatively rarespecies (Colwell & Coddington, 1994; Walther & Morand,1998). SChao is, moreover, easy to compute: SChao Sobs: F 21=2F 2 , where Sobs. is the number of observed species; F 1, thenumber of species with one record, the singletons and F 2, thenumber of doubletons. The estimator variance may also becomputed: var( SChao ) F 2(G 4 /4 G 3 G2 /2), whereG F 1 / F 2. Computations were made using Excel and thestatistical program EstimateS (Colwell, 1997).

Species nomenclature follows regional checklists andoras (Smith, 1981; Breedlove, 1986; Soto Arenas, 1988;Utley, 1994).

R E S U LT S A N D D I S C U S S I ON

Epiphyte inventories and their assessment

The number of epiphyte inventories has recently increasedconsiderably (Appendix 1). Epiphyte diversity patterns onenvironmental gradients, however, remain elusive becauseseveral restrictions hinder a comparison between inventories.First, it is not always clear whether next to true epiphytes,the parasitic, accidental, facultative, and hemi-epiphytes thatspend part of their life cycle rooted in the soil, were alsoincluded. Secondly, there is no agreement on the samplingunit of inventories. Epiphytes are either sampled per tree or

parts thereof, per ground surface area or included in localorulas or regional oras. Epiphyte diversity and abundanceon trees cannot be compared with epiphytes in surface areaplots in the absence of additional data about the structure of the forest. An ecologically meaningful comparison betweenoras requires information about the diversity in habitatswithin the area, the beta diversity. Thirdly, the sample effortmay vary considerably between inventories, ranging fromone to more than 100 trees or from 0.01 to 1.5 ha. The sizeof orulas often determined by the size of nature reserves

and the size of regional oras is mostly politically based. As ageneral rule, epiphyte inventories where the sample effortwas different can only be compared if the sampling wasadequate, i.e. containing a large portion of all species. Thefact that local orulas invariably contain many more speciesthan plot or tree-based inventories suggests otherwise. Toestimate the total species richness of an inventory through

extrapolation, small samples also do not perform well(Colwell & Coddington, 1994). The aggregated distributionof epiphytes in the forest, moreover, calls for relatively largesamples.

Sample size also inuences the quantication of epiphytesuccess, if the relative contribution of epiphyte diversity tothe entire ora is used: the Epiphyte Quotient (EQ; Hos-okawa, 1950). Epiphytes contribute more in smaller plots,because their accumulation curves per ground surface areaare steeper than those of forest trees, as pointed out byNieder et al. (1999, 2001). Single trees may support up toseventy-seven epiphyte species (Freiberg, 1999). Small plotsof < 1 ha often have EQs of over 40%. In local orulas, thenext larger spatial scale, epiphytes contribute less but reg-ularly still over 20%, as for example at Rio Palenque (22%),La Selva (23%) and at Maquipucuna (27%). In large regionssuch as Peru or the Guianas c. 10% of all vascular plantspecies are epiphytes, a proportion comparable with theepiphyte contribution world-wide (Madison, 1977). Inaddition to scale, the EQ is prejudiced by an edge effect if theepiphytes in the crown fraction outside the plot boundaryare included. Transect studies in particular would be subjectto this source of error, possibly explaining the high EQ(35%) in Rio Palenque (Gentry & Dodson, 1987a).

The spatial scale dependence of diversity patterns persurface area applies also to the three-dimensional space thatepiphytes inhabit. Johansson (1974) already pointed out that

comparisons of epiphytes of various regions must be per-formed on host trees of the same size (and species) because of the strong correlation between host tree and epiphyte. Forexample, the signicance of the higher diversity in the SierraNevada de Santa Marta plot at 2450 m in comparison withthe 3100-m plot is hard to appreciate because of the smallerheight of the forest (Sugden & Robins, 1979).

In conclusion, much care is needed with the comparison of the currently available epiphyte inventories. Increased com-munication among canopy researchers is essential in thedevelopment and implementation of standardized protocolsfor comparative studies (Barker & Pinard, 2001). One wayto compare epiphytes between inventories is to plot epi-phytes against trees of different sizes (Hietz & Hietz-Seifert,

1995b; Hietz-Seifert et al. , 1996; Wolf & Konings, 2001).The drawing of species accumulation curves, preferablyagainst some 3D-sampling unit, facilitates a comparisonbetween inventories. Such curves visualize the samplingeffort and may be used to estimate local species richness(Colwell & Coddington, 1994). In this study we avoid thedifcult comparison of dened samples by compiling theplotless data from botanical collections in a data base. Thatapproach also has its drawbacks that are discussed in thesection on data quality.




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The Chiapas epiphyte data base

The nal data base comprised 12,276 records in 1173 spe-cies. Most records correspond to plants in the six visitedherbaria but c. 100 were taken from regional oras(Table 1). The label information did not make it possible todetermine the altitude with condence of 269 records

(2.2%) and the longitude and latitude to minutes of 507records (4.1%). Of the remaining 11,769 records, 782(6.7%) could not be estimated to seconds.

The oldest epiphyte collection in Chiapas dates from 1890by J. N. Rovirosa. Germa n Mu nch (19001905), E. Matuda(19361979) and F. Miranda (19381959) made importantbotanical explorations in the early days of exploration with31, 677 and 121 collections, respectively. More recently,others, either as rst collector or in combination with othershave contributed a great number of collections: M. A. SotoA. (659), A. Shilom Ton (358), A. Reyes Garc a (302), E.Hagsater (213), M. Heath and A. Long (189), R. M.Laughlin (131), T. G. Cabrera C. (106), and T. B. Croat(102). However, D. E. Breedlove and E. Mart nez S. havemade by far the largest contributions with 3161 and 2079collections, respectively.

Data quality

The quality of the taxonomy of the data is as good as onecan expect because group specialists classied most speci-mens. To use only herbarium collections has the advantagethat the difcult identication of sterile individuals in theeld is avoided (Gradstein et al. , 1996). All identicationsmay, moreover, be veried. Many collections were identiedby A. R. Smith (ferns, 1871), E. Ha gsater (orchids, 1002),De Ada Mally (orchids, 995), T. B. Croat (aroids, 563),

Gerardo A. Salazar (orchids, 518), K-Burt Utley and J. Utley(bromeliads, 453), D. E. Breedlove (mostly ferns, 431), J. T.Mickel (ferns, 287), E. Matuda (mostly ferns and orchids,218), R. Solano G. (orchids, 187), R. Riba (ferns, 180) andT. G. Cabrera C. (orchids, 134).

The quality of the sampling is more difcult to appreciate.Botanical collections are not randomly distributed in spaceand probably biased for particular species. The geographicalbias in our data is evident from a map of collection sites(Fig. 1). In certain areas, the site map closely resembles astate road/river map. Collecting was also centred in or nearnatural reserves such as Lagos de Montebello (828) andReserva El Triunfo (353) and near archaeological sitessuch as Bonampak (eighty-nine), Palenque (153) and Tenam

Puente (thirty-nine). Other areas such as the Pacic andGulf Coastal Plains, the northern part of the Sierra Madre,the south-eastern Central Depression, and much of theEastern Highlands are under-represented. In addition, col-lectors seem to have a bias for certain species. For example,one of the most common epiphytes in the Central Plateauis Tillandsia vicentina Standley, reaching densities of 20,000 rosettes ha ) 1 (Wolf & Konings, 2001). Nevertheless,only fteen specimens are encountered in the herbaria.Tillandsia eizii L. B. Smith, a species with a showy hanging

inorescence that is heavily collected for ceremonial purpo-ses, is present with only seven records. For comparison, thealso weedy Tillandsia schiedeana Steudel is known fromeighty records. The most collected species are all orchidswith a widespread distribution in Central America: Encycliacochleata (L.) Leeme (115), Maxillaria variabilis Bateman exLindley (101) and Epidendrum radicans Pavon (82). Per-

ceived beauty and/or distinctiveness, owering period,handling ease and a special interest of the botanist may makea species more attractive for collection. As to the latter, thepublication of a volume on Pteridophyta in the ora of Chiapas probably contributed to the high number of fernrecords (3184) in the data base (Smith, 1981).

Biased sampling inuences the quality of the data, butquality is also affected by the amount of effort invested in thesampling. Sampling effort will be constrained by factors suchas the amount of time and resources available. The highnumber of records in the data base (12,276) suggests that notmany more species will be found with continued explora-tion, but the sustained rise of the speciesaccumulation curveimplies otherwise (Fig. 2). Subsets, for example, per altitu-dinal interval, are even further removed from species sat-uration. The large number of species ( n 253) that are onlyknown from single collections particularly highlights theincompleteness of the sampling. More than half of all species(600) is known from ve or fewer collections.

Because of the non-random approach of the botanist toplant collecting, the distribution and diversity patterns are tobe interpreted with care. However, the bias in sampling isnot probably very different between regions and individualcollectors. Also because of the high number of records, wepresume that a meaningful assessment of the observedpatterns is possible.

Species diversity and composition

As Mexico is situated at the northern limits of the Americantropics it predictably harbours fewer species of vascular epi-phytes than countries near the equator (Gentry & Dodson,1987a). In apparent agreement, a preliminary inventory of Mexican vascular epiphytes listed 1207 species (Aguirre-Leon, 1992), compared with 2110 species in Peru (Ibischet al. , 1996). Surprisingly however, our data base yields 1173conrmed species for the state of Chiapas alone and theestimated total number of species present in Chiapas ( SChao ) is1377 species. This high diversity is unexpected when, forexample, compared with the c. 950 species in the Guianas(Boggon et al. , 1997, cited in Ek, 1997). As to epiphytic

bryophytes and lichens, Chiapas is also considered unusuallyrich and potentially the richest in Mexico (Delgadillo &Ca rdenas-S, 1989; Sipman & Wolf, 1998). That these evo-lutionary unrelated groups are all diverse suggests that theirhigh richness is related to the high beta diversity in the state.

In accordance with other epiphyte inventories, Orchida-ceae make up the bulk of the number of species followed byBromeliaceae, Araceae, Piperaceae and Pteridophyta, i.e.ferns and fern-allies (Table 2). Orchid dominance in Chiapas(48%) is less pronounced than in Peru, where nearly




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two-thirds (63%) of all epiphytes are orchids (Ibisch et al. ,1996). The most species-rich orchid genera are Epidendrum(seventy-nine), Pleurothallis (fty-two), Encyclia (thirty-seven), Maxillaria (thirty-three), Oncidium (thirty-one),Spiranthes (twenty-one), Lepanthes (twenty-one), and Stelis(twenty-one). In the Bromeliaceae, most species are tilland-sias (sixty-four); of the remaining genera, Catopsis (fourteen)and Vriesea (eight) are the most species rich. In contrast toSouth American orulas, Guzmania (two) has only fewspecies. Peperomia (Piperaceae) contributes similar (forty-nine species, 4.2%) to the total ora as in Peru (seventy-seven species, 3.6%). Cactaceae, however, do contributemore in Chiapas than in Peru with 2.3 and 0.6%, respect-

ively. The contribution of species in the Pteridophyta is with21% also larger than in Peru (16.6%). Possibly this reectsbiased sampling. Ferns in Chiapas have been the subject of aregional ora (Smith, 1981) and their relatively low col-lecting efciency indicates a high collecting effort. Remark-able in the Pteridophyta ora of Chiapas is the high numberof Asplenium species (forty-nine). From altitudinal transectson Mt Kinabalu, Borneo and Carrasco, Bolivia, respectively,only thirty-seven and twenty-six Asplenium species havebeen reported, including terrestrial species (Kessler et al. ,2001). The number of Polypodiaceae (sixty-six) in Chiapas,the largest fern family, was similar to that in those twomountain regions (sixty and fty-ve), while the number of Elaphoglossum species (thirty-eight) is higher than in Borneo

(eight), but lower than in Bolivia (eighty-seven).

Epiphyte distribution patterns

AltitudeWe recorded epiphytes up to an altitude of 4100 m onisolated trees above the timberline. Highest species richnessin Chiapas is found at mid-elevations between 500 and2000 m (Fig. 3) corroborating Gentry and Dodsons hypo-thesis (Gentry & Dodson, 1987a). The pattern is largely

because of orchids, but other epiphyte-rich groups such asPteridophyta and bromeliads show a similar distribution. InCosta Rica, epiphytic bromeliads are also most common inmountain areas (Rossi et al. , 1997). Above 2000 m, thenumber of epiphytic aroids and orchids decreases rapidly.The Pteridophyta decline in richness in a lower rate; butsimilar to the rate reported for Bolivia and Borneo (Kessler,2001; Kessler et al. , 2001). Hence, the relative contributionof ferns to total epiphyte diversity is higher in the temperatemountain climates (Fig. 4). The common ferns Campylo-neuron amphostenon (Kunze ex Klotzsch) Fe e and Poly- podium ssidens Maxon are characteristic for highelevations.

Moreover, our compilation of epiphyte inventories world-wide points towards an unimodal richness pattern on trop-ical mountains (Appendix 1). In Central America, BarroColorado Island ( < 100 m, 204 species) and La Selva(< 150 m, 380 species) have fewer epiphytes than mountainforests at Monteverde (7001800 m, 878 species). In SouthAmerica the peak in richness appears to lie somewhat higher.In plots of < 1 ha, mid-elevation forests such as Sehuencas(21002300 m, 204 species), La Carbonera (22002700 m,191 species), Merida (2600 m, 128 species) and Cajanuma(2900 m, 138 species), are richer in species than lowlandforests at R o Palenque, (< 220 m, 127 species) and Sur-omoni (100 m, fty-three species), and forests near the uppertree limit at La Can a (3300 m, thirty-nine species) and Santa

Marta (30003200 m, thirty species). The number of epi-phytes in the orulas of Otonga (2000 m, 193 species), R oGuajalito (2000 m, 230 species), Maquipucuna (11002800 m, 441 species) and San Francisco (18003150 m, 627species) is also higher than in the vast, 10,000 ha, MaburaHill area in Guyana ( < 100 m, 191 species).

In the discussion of the observed altitudinal pattern, it isuseful to make a comparison with the non-vascular com-ponent of the epiphyte community as bryophytes and lichensprovide much information on the altitudinal patterns of

Figure 2 Species collection curves for vas-cular epiphytes in Chiapas. The curves wereobtained by randomly sequencing the collec-tions ten times.




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epiphytes on tropical mountains to date (Reenen &Gradstein, 1983; Ku rschner, 1990; Frahm & Gradstein,1991; Wolf, 1993a; Kessler, 2000). The study of non-vas-cular epiphytes is often easier than that of their vascularco-inhabitants because the classication of sterile specimenis mostly possible, aided by an increasing number of taxo-nomic reference books, and because of relatively smallminimal areas (Gradstein et al. , 1996). Wolf (1993a),working in the northern Andes of Colombia, paid full

attention to the vegetation in the canopy and we use thatstudy to summarize the three main altitudinal patterns thathave been observed. First, there was a continuous increasewith elevation in the richness of fruticose lichens. Also interms of abundance these dependent outer canopy specialiststhrive on the combination of high light intensities andre-occurring (fog) precipitation. This pattern exhibited by

the specialist fruticose lichens, however, was exceptional.Secondly, there was a continuous decline in species num-bers with elevation for epiphytic mosses and for crustoseand foliose lichens. This decline was most signicant in thecool and humid forests at higher elevations where brancheswere enveloped in a heavy cloak of bryophytes, mainlyliverworts, suggesting increased competition for space. Inaddition, mass effect, i.e. the inux of propagules from anadjacent core area to an area where the species cannot beself-maintaining (Shmida & Wilson, 1985), has been pos-tulated to produce a decline of richness with elevation,in combination with Rapoports rule (Stevens, 1992).According to Rapoports rule, the elevational (and latitu-dinal) range of species increases with increasing elevation.According to Stevenss Rapoport rescue hypothesis, low-lands may thus be richer in species because they arepotentially sink habitats for a larger number of species. Wetested Rapoports rule for our data and indeed found agood correlation (Pearson) between the mid-elevation of the distribution of the species and their altitudinal range(only species with more than ten occurrences; n 378,r 0.36, P < 0.001). According to Stevenss hypothesis weexpect a monotonically decrease of richness with elevation,but observed a unimodal pattern. This pattern, the third,was in Wolfs study shown by the liverworts, the groupwith by far the largest number of species in his transect.Interestingly, the mass effect was also associated with the

presence of a mid-elevation zone of high richness as itcoincided with a zone of overlap between a low- and ahigh-elevation ora (Wolf, 1993a). The presence of a zonewhere the altitudinal distributions of many species overlapmay also have induced the high species richness at mid-elevations in Chiapas. Most species-rich families have theirhighest diversity in this belt, which suggests a commonfactor (Fig. 3). In addition, forests at both low and highelevations have a distinct epiphyte ora (Table 3). In thisview, between 500 and 2000 m, typical tropical lowlandspecies coincide with the temperate species from the high-lands. The temperate origin of the mountain vegetation of Chiapas is evidenced by the presence of holarctic treegenera such as Abies, Acer, Alnus, Juniperus , Pinus ,

Prunus , Quercus , Sambucus , Ulmus and Viburnum .A separate factor that may contribute to the mid-eleva-

tional hump results from the geometric constraint on speciesranges (e.g. Colwell & Lees, 2000). When species are dis-tributed stochastically within a bounded domain (from sealevel to mountaintop), null models predict that there is amid-domain peak in richness. Unfortunately, the highnumber of rare species in the data base render a detailedanalysis of the altitudinal ranges of species impossible andthe presence of zones of overlap or a mid-domain effect

Table 2 Representation of vascular epiphyte families in the database and their collection efciency, i.e. the number of speciesencountered per 100 collections ( few data)

No. of collections

No. of species

Contribution(%)

Collectionefciency

Angiosperms

Araceae 838 67 5.7 8.0Araliaceae 273 14 1.2 5.1Asteraceae 39 3 0.2 7.7Begoniaceae 210 23 2.0 11.0Bignoniaceae 3 2 0.2 Bromeliaceae 1087 101 8.6 9.3Burmanniaceae 3 2 0.2 Cactaceae 90 27 2.3 30.0Crassulaceae 39 12 1.0 30.8Cyclanthaceae 8 4 0.3 Dioscoreaceae 3 1 0.1 Ericaceae 147 14 1.2 9.5Gesneriaceae 63 10 0.8 15.9Guttiferae 162 14 1.2 8.6Lentibulariaceae 2 1 0.1

Liliaceae 1 1 0.1 Marcgraviaceae 51 6 0.5 11.8Moraceae 31 4 0.3 12.9Onagraceae 38 1 0.1 2.6Orchidaceae 5350 568 48.4 10.6Piperaceae 629 52 4.4 8.3Rubiaceae 3 1 0.1 Solanaceae 17 1 0.1 5.9Subtotal 9087 929 79.2 10.2

Pteridophyta, i.e. ferns and alliesAdiantaceae 56 6 0.5 10.7Aspleniaceae 697 49 4.2 7.0Blechnaceae 146 12 1.0 8.2Dennstaedtiaceae 8 2 0.2 Dryopteridaceae 6 2 0.2 Grammitidaceae 70 10 0.9 14.3Hymenophyllaceae 319 32 2.7 10.0Lomariopsidaceae 370 38 3.2 10.3Lycopodiaceae 42 8 0.7 19.1Nephrolepidaceae 71 7 0.6 9.9Polypodiaceae 1310 66 5.6 5.0Psilotaceae 1 1 0.1 Schizaeaceae 4 2 0.2 Tectariaceae 19 2 0.2 10.5Vittariaceae 69 6 0.5 8.7Woodsiaceae 1 1 0.1 Subtotal 3189 244 20.8 7.7

Total 12,276 1173 100.0 9.6




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could thus not be conrmed. The occurrence of overlap, amid-domain effect and Stevenss Rapoport rescue hypothesisare not mutually exclusive. In general, we agree with Lawton

(1996) and Rahbek (1997) that the quest for single expla-nations of patterns is unhelpful.

Perhaps the high diversity between 500 and 2000 mresults from a higher diversity of habitats, because next tothe wet mountain forests, the dry Central Depression alsofalls in this altitudinal range (Fig. 1). A separate analysis of the diversity pattern exclusively in the wet Sierra Madremountain range, however, also showed a unimodal distri-bution (Table 4). In addition to habitat diversity, Gentry andDodson offer two more hypotheses as to why species

diversity is especially high on mid-elevations at wet moun-tains: ner niche partitioning and evolutionary explosion.The latter is associated with the dynamic character of the

young Andean mountains. Our data show that the speciesrichness patterns are comparable also on more stablemountains in Chiapas.

Finally, in Bolivia a mid-elevational belt of high epiphytepteridophyte diversity is correlated with high amounts of precipitation in that zone (Kessler, 2001). In Chiapas,however, there is no such relationship. The collection sites inthe lowlands ( < 500 m) receive more rainfall annually thanthe sites between 500 and 2000 m, respectively, 2580 and1750 mm.

Figure 3 The number of observed species(Sobs. ) and the estimated number of species(SChao ) in main plant groups per altitudinalinterval in the state of Chiapas. For the totalnumber of epiphytes, SChao diversity at adja-cent altitudinal intervals is signicantly dif-ferent in all cases (unpaired t -test,P < 0.001). *Note that the total number of collections (12,276) is larger than that of thesummed intervals (12,007), because in thiscolumn 269 collections for which no altitu-dinal data were available are also included.

Figure 4 Relative contribution of main plantgroups to epiphyte species richness per alti-tudinal interval.




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Possibly, a mid-elevational zone of higher species richnessis not encountered everywhere. Ibisch et al. (1996) report adecrease of epiphyte richness with elevation for the whole of Peru and the lowland orula at R o Palenque ( < 220 m, 227species) in the Ecuadorian part of the Choco biogeographical

region is not poorer than many mountain forests. In theColombian part of that same region, 0.4 and 0.1 ha plotscontain 140 species on average which is also remarkably rich(Galeano et al. , 1998). On the other side of the Andeanmountains, the Amazonian R o Caqueta region is with 212species in a 0.75 ha inventory also rich in epiphytes. Pre-sumably, the high diversity in the Choco and Caqueta regions is related to the high amounts of annual rainfall(Gentry & Dodson, 1987a) of c. 3000, 7000 and 3000 mm,respectively. Next, the rainfalldiversity relationship isanalysed.

Rainfall Recent epiphyte inventories in neotropical lowland forestscorroborate Gentry & Dodsons (1987a) hypothesis thatspecies richness increases with the amount of rainfall(Fig. 5). For the entire state of Chiapas that in contrast alsoincludes mountain forests, a different pattern emerges(Fig. 6). After an initial rise in species richness, the numberof epiphytes decreases again when rainfall exceeds 2500 mmannually. All species-rich groups exhibit this pattern, except

Table 3 Relative contribution of species in the data base per altitudinal interval (number of records/total number of records in a particularinterval, times 10,000). Only species with a preference for a certain interval are shown, arbitrarily dened as being collected there at least tentimes more often than in any of the other intervals. Rare species having a relative contribution < 0.50% in those intervals are not considered

< 1000(n 4714)

10002000(n 4962)

> 2000(n 2331)

Total numberof records

Anthurium pentaphyllum (Schott) Madison 59.4 2.0 0.0 31

Asplenium auritum Sw. 59.4 0.0 4.3 29Asplenium serratum L. 63.6 2.0 0.0 31Bolbitis portoricensis (Spreng.) Hennipman 50.9 2.0 0.0 26Dryadella linearifolia (Ames) Luer 50.9 0.0 0.0 24Encyclia bractescens (Lindley) Hoehne 87.0 8.1 0.0 46Epidendrum nocturnum Jacq. 78.5 0.0 0.0 37Maxillaria aciantha Rchb. f. 59.4 2.0 0.0 29Maxillaria uncata Lindley 87.0 6.0 0.0 44Microgramma percussa (Cav.) de la Sota 57.3 4.0 0.0 29Nephrolepis pendula (Raddi) J. Smith 50.9 2.0 0.0 25Platystele stenostachya (Rchb. f.) Garay 87.0 4.0 0.0 43Pleurothallis grobyi Bateman ex Lindley 76.4 4.0 0.0 40Polystachya foliosa (Hook.) Rchb. f. 82.7 2.0 0.0 40Sobralia decora Bateman 67.9 6.0 0.0 35Sobralia fragrans Lindley 78.5 0.0 0.0 37

Stelis oxypetala Schltr. 53.0 0.0 0.0 25Tillandsia bulbosa Hook. 59.4 2.0 0.0 29Tillandsia valenzuelana A. Rich. 70.0 4.0 0.0 35Trigonidium egertonianum Bateman ex Lindley 65.8 4.0 0.0 34Stelis microchila Schltr. 4.2 52.4 0.0 29Campyloneurum amphostenon (Kunze ex Klotzsch) Fe e 0.0 8.1 94.4 26Encyclia varicosa (Lindley) Schltr. 0.0 16.1 205.9 58Encyclia vitellina (Lindley) Dressler 0.0 6.0 60.1 17Epidendrum eximium L. O. Williams 0.0 0.0 60.1 15Fuchsia splendens Zucc. 0.0 4.0 154.4 38Isochilus aurantiacus Hamer & Garay 0.0 4.0 77.2 20Peperomia campylotropa A. W. Hill 0.0 2.0 60.1 15Polypodium ssidens Maxon 0.0 0.0 77.2 18Rhynchostele stellata Soto Arenas & Salazar 4.2 4.0 115.8 31Stelis ovatilabia Schltr. 0.0 2.0 60.1 16

Table 4 Number of epiphyte species in the Sierra Madre region peraltitudinal interval. Given are the number of records ( n), the numberof observed species ( Sobs. ), and the estimated number of species(SChao ) with the 95% condence interval

Altitudinal interval n Sobs. SChao SChao 95% CI

0500 m 279 108 166.78 (162.6, 170.9)5001000 m 172 106 211.09 (204.3, 217.9)10001500 m 210 154 394.67 (384.1, 405.2)15002000 m 454 228 408.88 (403.2, 414.6)20002500 m 437 193 306.64 (302.3, 311.0)

25003000 m 159 93 156.03 (151.4, 160.7)> 3000 m 37 28 83.13 (69.2, 97.0)04100 1748 605 1302.69 (1294.2, 1311.1)




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the aroids that remain comparatively stable. The positiverelationship between rainfall and epiphyte diversity thusbreaks down when mountain sites at high elevations areincluded. The cool mountains are effectively more humid

than their amounts of rainfall suggest because of the highaverage relative humidity of the air and low evapotranspi-ration (Wolf, 1993a). Cloud precipitation, not measured inrainfall gauges, may further enhance the moisture availab-ility of the epiphyte habitat (e.g. Clark et al. , 1998).

Even when only records from low elevations ( < 1000 m)are considered, a positive relationship with rainfall inChiapas could not be found. Again in important plantgroups such as ferns, the bromeliads and orchids, the num-ber of epiphytes decreases when annual rainfall exceeds

2500 mm, while aroids remain stable (Fig. 6). In general,wind-dispersed epiphytes and lianas are better represented inforests that are relatively dry (Gentry & Dodson, 1987a;Gentry, 1991). In contrast, the extremely wet forests in the

Choco have an unusual high number of animal-dispersedspecies (Gentry, 1986). As Gentry & Dodson (1987a) pos-tulate, in wet forests wind-dispersed propagules are ham-pered in their establishment, i.e. dispersal and attachment, inthe face of abundant rainfall. As to bromeliads, rainfall mayfuse the coma hairs of seeds to an inert mass (pers. observ.).Moreover many orchids, bromeliads and ferns are welladapted to survive periods of drought (Benzing, 1990).

In agreement with the establishment hypothesis, weobserve that with increased rainfall the characteristic species

0

50

100

150

200

250

300

350

400

0 1000 2000 3000 4000 5000 6000 7000

Annual rainfall (mm)

Coqu, Colombia

Los Tuxtlas, MexicoLos Tuxtlas, Mexico

Horquetas, Costa RicaSuromoni, Venezuela

R o Palenque, Ecuador

Jauneche, Ecuador

Nuqu , ColombiaEl Amargal, Colombia

El Verde, Puerto RicoXalapa, Mexico

Xalapa, Mexico

BCI, Panama

La Selva, Costa Rica

SantaRosa, CR

Mabura Hill, Guyana

El Ducke,Brazil

R o Palenque, Ecuador

Jauneche, Ecuador

Capeira,Ecuador

R o Manu, Brazil

R o Caquet, Colombia

N u m

b e r o f s p e c

i e s

Tiputini, Ecuador

Figure 5 Vascular epiphyte species richnessin plots (open circles, r Pearson 0.71) andlocal orulas (closed circles, r Pearson 0.95) in areas with different amounts of annual rainfall. All areas below 1000-melevation; data from Appendix 1.

Figure 6 The number of observed species(Sobs. ) and the estimated number of species(SChao ) per annual rainfall (mm) cohort. TheSChao diversity of the

epiphytes totals is sig-nicantly different between all cohorts(unpaired t -test, P < 0.001). For familytotals, see Table 6.




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in the vegetation shift from wind-dispersed orchids and fernsto Araceae (Table 5). The decrease in anemochoric species is,however, not fully compensated by zoochoric species. Thisappears contrary to other neotropical wet lowland forests,where aroids contribute more to total diversity (Fig. 7). In a0.9-ha inventory in theextremely wet forests along the PacicCoast in Colombia (annual rainfall of 51007150 mm),aroids were with 100 species even the largest plant family,comprising over 10% of the total vascular ora (Galeanoet al. , 1998). Alongside less than fteen bromeliads and only

fty-three orchid species were found. Most aroids had a tree-dependent growth form, Anthurium and Philodendron beingthe largest genera, with forty-eight epiphyte species in total.Our data base of Chiapas (75,000 km 2) contains only sixty-seven epiphytic Araceae. R o Palenque, as well in the Choco biogeographic region, is also rich in Araceae (Gentry &Dodson, 1987a) and this pattern repeats itself on trees of wetforest in the Amazon where aroids have fty-two speciescompared with thirty-seven orchids and thirty-seven ferns(Benavides, 2002). Aroid preponderance in wet climates is

Table 5 Relative contribution of species inthe data base per rainfall cohort (number of records/total number of records in a partic-ular cohort, times 10,000). All records from 1000-m altitude are included. All specieswith a preference for a certain cohort areshown, arbitrarily dened as being collectedthere at least ve or ten times (in bold) more

often than in the other cohort. Rare specieswith fewer than ten records are omitted

< 2500 mm(n 3584)

2500 mm(n 1359)

Araceae Anthurium lucens Standley ex Yuncker 30.7 0.0Orchidaceae Laelia rubescens Lindley 27.9 0.0

Maxillaria meleagris Lindley 30.7 0.0Stelis gracilis Ames 30.7 0.0Stelis guatemalensis Schltr. 47.4 7.4Trichosalpinx ciliaris (Lindley) Luer 50.2 7.4

Piperaceae Peperomia asarifolia S. & C. 44.6 7.4Pteridophyta Antrophyum ensiforme Hook. 30.7 0.0

Asplenium abscissum Willd. 36.3 0.0Asplenium auriculatum Sw. 33.5 0.0Cochlidium serrulatum (Sw.) L. E. Bishop 36.3 0.0Elaphoglossum guatemalense (Klotzsch) Moore 47.4 7.4Hymenophyllum polyanthos (Swartz) Swartz 53.0 7.4Pecluma divaricata (Fourn.) Mickel & Beitel 61.4 0.0Polypodium echinolepis Fe e 30.7 0.0Polypodium polypodioides (L.) Watt 50.2 7.4

Araceae Anthurium exile Schott ssp. muelleri Croat & Baker 2.8 66.2Monstera acuminata C. Koch 25.1 206.0Philodendron hederaceum (Jacq.) Schott 14.0 88.3Philodendron inaequilaterum Liebm. 11.2 80.9Syngonium angustatum Schott 8.4 58.9Syngonium salvadorense Schott 11.2 110.4

Gesneriaceae Drymonia serrulata (Jacq.) Martius ex DC. 16.7 95.7

0

10

20

P e r c e n t a g e

30

40

50

60

70

80

90

100

Horquetas,Costa Rica(4000 mm)

La Selva,Costa Rica(4000 mm)

Ro Caquet,Colombia

(3060 mm)

Ro Palenque,Ecuador

(2980 mm)

BCI,Panama

(2750 mm)

Suromoni,Venezuela(2700 mm)

This study,Mexico

(>2500 mm)

Other epiphytes

Piperaceae

Bromeliaceae

Ferns and allies

Orchidaceae

Araceae

Figure 7 Familial composition of epiphyteoras in neotropical lowland rain forests withhigh amounts of rainfall. La Selva, CostaRica (Hartshorn & Hammel, 1994). R oPalenque, Ecuador (Gentry & Dodson,1987a). Barro Colorado Island, Panama(Croat, 1978). R o Caqueta , Colombia(Benavides, 2002). Horquetas, Costa Rica;the others category includes Piperaceae(Whitmore & R. Peralta, 1985). Suromoni,Venezuela (Engwald, 1999).




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not restricted to South America. The ora at La Selva inCosta Rica also contains many Araceae (ninety-nine species)and from wet Barro Colorado Island (BCI) in Panamatwenty-four epiphytic aroids are reported compared withrelatively few (eighty-two) tree-dwelling orchids (Croat,1978; Hartshorn & Hammel, 1994). Also on trees in theMexican forest at Los Tuxtlas, the northernmost tropical

lowland rain forest, aroids are more species rich than orchids,bromeliads and Pteridophyta (Hietz-Seifert et al. , 1996).The low manifestation of Araceae in Chiapas may be

related to the historical biogeography of the family. As aseparate hypothesis, we propose that the relatively highcontribution of anemochorous epiphytes is related to the dryseason that gives these plants a good opportunity to disperse.In contrast to the aforementioned wet lowland forests, theforests in southern Mexico are subject to a distinct dryperiod that lasts several months. As the rainfall regime is animportant element on which the internal division of Chiapasin physiographical regions and associated vegetation types isbased, we expect that regions and forest formations havedistinctive epiphytes (Breedlove, 1978).

Physiographical regionFor the analysis of the distribution of species over the sevenphysiographical regions in the state (Fig. 1), 11,724 recordswere used that could be attributed to a particular region,comprising 1153 species. Of all regions, the Central Plateauis the richest in epiphytes, and richer than the Eastern andNorthern Highlands that have lower elevations and higheramounts of rainfall (Table 6). In the mountain regions, theestimated number of species varies between 725 and 864species. The similarity in diversity suggests that these regionsshare many species, but in reality the oristic similaritybetween the regions is always < 60% (Table 7). With con-

tinued exploration the similarities will increase, but clearlyeach region has a characteristic combination of species(Table 8). Of the more common species, the Eastern High-lands in particular have many characteristic species, mostlyorchids. Next to differences in the historical biogeography of that region, this may be because of the favourable combi-nation of high temperatures at lower elevations and highamounts of rainfall. It is the region with the largest extensionof lower montane rain forest (Breedlove, 1978).

Vegetation typeIn total, 8485 collections could be ascribed to one of theforest formations of Chiapas, following Breedloves classi-cation (Breedlove, 1978). Both the evergreen cloud forest

and the pine-oak Liquidamber forest were lumped with themontane rain forest, because on the aerial photographs itwas not possible to discern these formations. Collections inriparian forests and savannas were too few to merit analysis.Nearly one-third of the collections (2699) were taken fromforests that are now degenerated. This could be recognizedon the aerial photographs, but as we do not know the con-dition of the forest when the plant was sampled we cannotassess the inuence of forest disturbance on the epiphytevegetation. For the 745 species that were collected (3213 T

a b l e 6

T h e n u m b e r o f o b s e r v e d e p i p h y t e s p e c i e s ,

S o

b s .

a n d t h e n u m b e r o f e s t i m a t e d s p e c i e s ,

S C h a o

, p e r p h y s i o g r a p h i c a l r e g i o n i n e p i p h y t e r i c h f a m i l i e s . T

h e S

C h a o

d i v e r s i t y o f t h e

( c o l u m n ) t o t a l s i s s i g n i c a n t l y d i f f e r e n t b e t w e e n a l l r e g i o n s , e

x c e p t f o r t h e t w o c o a s t a l p l a i n s ( u n p a i r e d t - t e s t , P

3000 < 35 22,000 ha 441 26.89Ecuador, Res. Biol. San Francisco 7 358 S 18003150 2500 > 5000 < 35 1000 ha 627

REGIONAL FLORA

Mexico1

1532 N 1,958,000 km2

2900 coll. 1207 Mexico, this study 1518 N 04100 8005000 75,000 km 2 12276 coll. 1173 13.90Mexico, Yucata n Peninsula 37 1822 N < 200 5001500 625 (30) 10,000 km 2 107 Guianas 5 cited in 10 19 N 02750 20004000 470,000 km 2 c. 950 10.33Peru 27 018 S 1,285,000 km 2 2110 10.30

OLD WORLDZa re4 150 S 800900 18002500 32 Tree < 20 106 c. 2.5Rwanda 4 230 S 18002200 16002000 22 Tree < 20 62 c. 2.5Liberia, Nimba mountains 31 68 N 5001300 15003100 1045 Tree 463 153 Liberia, Nimba mountains 31 7N 500600 1500 4045 plot (0.075 ha) 3 (96 trees) 65 j India, Varagalaiar 2 10 25 N 630 1600 plot (1 ha) 30 26 New Zealand, Moeraki river 25 45 43 S 010 3455 2237 Tree 3 61WORLD 35 28,200 c. 10WORLD 34 23,456 c. 10WORLD 18 29,505 c. 10

a only Annona glabra L. trees; b only lower part of the tree trunk; c only oak trees; d average per tree; e with 8 months of dry season; f onlyVellozia piresiana L. B. Smith treelets; g with 6 months of dry season; h excluding grasses; i based on 4946 herbarium specimens, mainlyterrestrials; j the number of species per plot was thirty-seven, thirty-seven and forty-four with highest richness at lower elevation because of orchids.1 Aguirre-Leon (1992); 2 Annaselvam & Parthasarathy (2001); 3 Benavides (2002); 4 Biedinger & Fischer (1996); 5 Boggon et al. (1997); 6Bgh (1992); 7 Bussmann (2001); 8 Catling & Lefkovitch (1989); 9 Croat (1978).; 10 Ek (1997); 11 Engwald (1999); 12 Foster (1990); 13Freiberg (1996); 14 Freiberg (1999); 15 Freiberg & Freiberg (2000); 16 Galeano et al . (1998); 17 Gentry & Dodson (1987b); 18 Gentry &Dodson (1987a); 19 Haber (2001); 20 Hartshorn & Hammel, (1994); 21 Hietz (1997); 22 Hietz & Hietz-Seifert (1995a); 23 Hietz & Hietz-Seifert (1995b); 24 Hietz-Seifert et al. (1996); 25 Hofstede et al. (2001); 26 Ibisch (1996); 27 Ibisch et al. (1996); 28 Ingram & Nadkarni(1993); 29 Janzen & Liesner (1980); 30 Jaramillo (2001); 31 Johansson (1974); 32 Kelly et al. (1994); 33 Ko ster et al. (2003); 34 Kress (1986);35 Madison (1977); 36 Nowicki (2001); 37 Olmsted & Go mez-Juarez (1996); 38 Prance (1994); 39 Rauer & Rudolph (2001); 40 Ribeiro et al .(1994); 41 Schneider (2001); 42 Smith (1970); 43 Sugden & Robins (1979); 44 Ter Steege & Cornelissen (1989); 45 Webster & Rhode (2001);46 Werneck & Esp rito-Santo (2002); 47 Whitmore & Peralta (1985); 48 Wolf & Konings (2001); 49 Zotz (1999).



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