Journal of Biogeography, 30, 1689–1707
Patterns in species richness and distribution
of vascular epiphytes in Chiapas, Mexico
Jan H. D. Wolf* and Alejandro Flamenco-S El Colegio de la Frontera Sur (ECOSUR),
Chiapas, Mexico
Abstract
Aim 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 km2 large state of Chiapas in
southern Mexico at 14.5–18.0N. Chiapas is diverse in habitats with forests from sealevel to the tree-line at c. 3800 m altitude and with annual amounts of rainfall ranging
from 800 to over 5000 mm. It is also one of the botanical best-explored regions in the
tropics.
Methods First we give an overview of epiphyte inventories to date. Such epiphyte
surveys were mostly carried out on the basis of surface area or individual trees and we
discuss their problematic comparison. Applying a different methodological approach, we
then used 12,276 unique vascular epiphyte plant collections from Chiapas that are
deposited in various botanical collections. The locality data were georeferenced and
compiled in a relational data base that was analysed using a geographical information
system. To compare the number of species between inventories that differed in the
numbers of records, we estimated the total richness, SChao, at each.
Results We recorded 1173 vascular epiphyte species in thirty-nine families (twentythree angiosperms), comprising c. 14% of all confirmed plant species in the state. About
half of all species were orchids (568). Ferns and bromeliads were the next species-rich
groups with 244 and 101 species, respectively. Most species were found in the Montane
Rain Forest and in the Central Plateau. Trees of different forest formations, rainfall
regimes, altitudes and physiographical regions supported a characteristic epiphyte flora.
Main conclusions We were able to confirm the presumed presence of a belt of high
diversity at mid-elevations (500–2000 m) in neotropical mountains. In contrast to predictions, however, we observed a decrease in diversity when the annual amount of
rainfall exceeded 2500 mm. The decrease is attributed to wind-dispersed orchids, bromeliads and Pteridophyta that may find establishment problematical under frequent
downpours. In the wet but seasonal forests in Chiapas, this decrease is not compensated
by plants in the animal-dispersed Araceae that are abundant elsewhere. We presume that
in addition to the annual amount of rainfall, its distribution in time determines the
composition of the epiphyte community.
Keywords
Botanical collections, canopy biology, elevation gradient, epiphyte quotient, geographical 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]
2003 Blackwell Publishing Ltd
1690 J. H. D. Wolf and A. Flamenco-S
INTRODUCTION
Biotic inventories have shown that the number of species
near the equator is substantially larger than at latitudes
beyond the tropics for many groups of organisms (Pianka,
1966), even when exceptions (bryophytes) also do exist
(Wolf, 1993a). Diversity patterns within the tropics, however, are less well-documented. In particular, the distribution
of organisms in the high forest canopy remains ambiguous,
probably because of its difficult accessibility (Moffett, 1993;
Mitchell et al., 2002). On the contrary, it is justified to pay
special attention to the high canopy because the upper
stratum in the forest harbours a wealth of species in different
kinds of groups such as mammals, birds, arthropods and
epiphytic plants (Stork, 1988; Malcolm, 1991; Nadkarni,
1994; Greeney, 2001; Winkler & Preleuthner, 2001). Of all
known vascular plant species, c. 10% occur as epiphytes,
depending for support, but not for nutrients or water, on
other plants, usually trees (Kress, 1986). In small 0.1-ha
forest plots epiphytes may comprise up to 35% of all vascular plant species (Gentry & Dodson, 1987a). This number
would even have increased substantially if non-vascular
epiphytes were included (Wolf, 1993b).
The great species richness, the variety of growth forms and
the high abundance of the epiphytic component of tropical
forests have attracted botanists since the nineteenth century
(Schimper, 1888). Classical epiphyte studies relied heavily
on distance observations and plants were usually collected
from the forest floor (Went, 1940; Johansson, 1974). The
usefulness of distance observations for epiphyte inventories
has always been questioned, and justifiably so (Flores-Palacios & Garcia-Franco, 2001). As a consequence, epiphytes
are well-represented in herbaria world-wide, but were rarely
included in systematic forest inventories.
With the advance of new techniques to obtain access to
the canopy such as rope-climbing (Perry, 1978) and the use
of construction cranes, floristic inventories that include
canopy epiphytes, however, are available at an increasing
rate (Lowman, 2001). In agreement with early epiphyte
studies, in situ observations confirm that epiphytes exhibit a
clear vertical zonation within the host tree with few species
shared between the tree crown and the trunk base (Jarman
& Kantvilas, 1995).
The larger number of inventories raises expectations that
insight may also be obtained in the more elusive horizontal
patterns of diversity and distribution of the epiphytes in the
forest. Over small distances, earlier observations in tree
plantations that epiphytes grow aggregated within the forest
(Madison, 1979) have recently been confirmed for natural
forests (Bader et al., 2000). Locally, the distribution may
thus be better explained from a dispersal-assembly perspective than from a niche-assembly perspective (Hubbell, 2001).
On a larger scale, between regions, Gentry & Dodson
(1987a) postulated that epiphytes decreased more drastically
than any other habit group in dryer areas and that epiphyte
richness is greatest on mountains at mid-elevations. These
hypotheses, however, have been difficult to corroborate and
have been questioned (Ibisch et al., 1996).
The aim of this study is to provide insight into the patterns
of distribution and richness of epiphytes on a regional scale.
Therefore an overview of epiphyte inventories in the tropics
so far is presented and their problematical comparison discussed. In a different methodological approach, we will next
use botanical herbarium collections from an environmentally
heterogeneous region and integrate those in a geographical
information system (GIS). In this way, we combine the
wealth of information from early botanical explorations
with that of recent epiphyte inventories. For practical reasons (mapping), we use a political unit as study area: the
state of Chiapas in southern Mexico. Chiapas has over 1000
species of vascular epiphytes and is, with tens of thousands
herbarium specimens, one of the better-explored botanical
regions in the tropics (Breedlove, 1986).
MATERIALS AND METHODS
Study site
The state of Chiapas in southern Mexico is situated
between 14.5–18.0N and 90.3–94.5W and comprises
c. 75,000 km2 (Fig. 1). The climate is diverse, ranging from
semi-desert to areas where annual rainfall exceeds 3500 mm
and from lowland tropical to mountain temperate. Much of
the area is characterized by an alternate wet and dry season
with the dry period lasting between 2 and 6 months. For a
description of the physiographical regions and vegetation
types we rely on Breedlove (1978).
Chiapas can be divided into seven physiographical regions.
A volcanic mountain range, the Sierra Madre, with the
Tacaná volcano (4110 m) as its highest peak, separates the
narrow Pacific Coastal Plain from the Central Depression and
the eastern part of the state. The Central Depression, a dry
terraced valley from 500 to 1200 m, was originally covered
with a deciduous forest but extensive cultivation has led to
large sections of thorn woodland and savanna. The strata are
mostly marine limestone and slates. The highlands may be
divided into the Central Plateau, The Eastern Highlands and
the Northern Highlands. The Central Plateau has an elevation
between 2100 and 2500 m with a few peaks up to 2900 m. It
is composed of marine limestone with extrusions of volcanic
rock on the higher peaks. Tropical deciduous forest and pineoak forest cover the dryer western part, making place for
pine–oak Liquidamber and montane rain forest in the eastern
part. The Eastern Highlands have similar strata, but at lower
elevations ranging from 400 to 1500 m. Lower montane rain
forest is the most common vegetation type. The Northern
Highlands are more diverse in altitude, geology and associated vegetation types. Besides pine–oak Liquidamber and
montane rain forest, a transitional forest between tropical and
lower montane rain forest and thorn woodland also occurs:
the evergreen and semi-evergreen seasonal forest. This formation is also common on the slopes of the Sierra Madre.
North of the highlands the Gulf Coastal Plain reaches into
Chiapas. The vegetation is mostly tropical secondary growth.
The diversity in soils, climate and associated forest formations helps to explain why the state of Chiapas is among
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1691
Figure 1 Distribution of epiphyte collection
sites. Physiographical regions in Chiapas
after Breedlove (Breedlove, 1978).
Table 1 The plant collections that were examined for vascular epiphytes from Chiapas
Institute
Acronym
Location
California Academy of Sciences
Instituto de Biologı́a, UNAM
Asociación Mexicano de Orquideologı́a, A. C.
Jardı́n de Orquı́deas San Cristóbal
El Colegio de la Frontera Sur
Instituto de Historia Natural
Literature records
CAS
MEXU
AMO
–
ECO-SC-H
CHIP
–
San Francisco, CA, USA
Mexico City, Mexico
Mexico City, Mexico
San Cristóbal de Las Casas, Chiapas, Mexico
San Cristóbal de Las Casas, Chiapas, Mexico
Tuxtla Gutiérrez, Chiapas, Mexico
–
Total
the richest in species of Mexico, despite its small territory of
slightly <4%. For example, the number of vascular plant
species recorded for Chiapas is 8248 species of an estimated
total 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 state
of Chiapas (Table 1). Hemi-epiphytes were included, but
facultative epiphytes were not if their presence on trees was
regarded as highly unusual (e.g. Agave sp.). The ecologically
different heterotrophic Loranthaceae were also excluded.
We considered only specimens identified to the level of
species or below. Varieties and subspecies were treated as
individual species in the diversity estimates. All information
concerning the collector, collector’s number, collection date,
taxonomy, locality and habitat were copied from the her 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
No. of specimen
5416
4437
1440
508
210
154
111
12,276
barium labels and entered in a relational data base (Microsoft Access). Specific information may be provided on
request from the first author. Most labels contained no
information about the latitude and longitude of the collection site. With the help of topographical maps (Instituto
Nacional de Estadı́stica, Geografı́a e Informática, INEGI,
1 : 50.000) such data was estimated to a precision of
seconds. In case the identification of duplicate collections
differed, the name given by the experienced taxonomist or
group specialist was adopted. When no clear differentiation
between taxonomists could be made, both names were
maintained (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 been
prepared at Ecosur. The topographical overlay was derived
from maps (1 : 250.000) published in print by INEGI
between 1985 and 1989 (locality references E15-07, E15-11,
1692 J. H. D. Wolf and A. Flamenco-S
E15-12, E15-05, E15-02, E15-10 and D15-01) and from
maps by the Secretarı́a de Programación 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 (1985–1988; 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 vegetation maps are based on aerial photographs taken between
1972 and 1981. We used the physiographical overlay elaborated by D. Navarrete (Ecosur) on the basis of Müllerried’s
(1957) geological map. As to rainfall, four climatic maps
(1 : 500.000) were used, published in 1970 by the Comisión
para el estudio del territorio nacional (Cetenal), Universidad
Nacional Autónoma de México (UNAM); locality references
15-PI, 15-PII, 15-QVII and 15-QVIII.
We use Chao’s nonparametric diversity estimator to estimate the overall diversity of the samples which typically will
have continuously rising species–accumulation curves (Chao,
1984). Her estimator (SChao) provides an estimate of the
completeness of the sampling, enables a comparison between
unequal-sized samples, has a relatively low sensitivity to
varying sample intensity and species richness, and performs
especially well in data with a preponderance of relatively rare
species (Colwell & Coddington, 1994; Walther & Morand,
1998). SChao is, moreover, easy to compute: SChao ¼ Sobs: þ
F12 =2F2 , where Sobs. is the number of observed species; F1, the
number of species with one record, the singletons and F2, the
number of doubletons. The estimator variance may also be
computed: var(SChao) ¼ F2(G4/4 þ G3 þ G2/2), where
G ¼ F1/F2. Computations were made using Excel and the
statistical program EstimateS (Colwell, 1997).
Species nomenclature follows regional checklists and
floras (Smith, 1981; Breedlove, 1986; Soto Arenas, 1988;
Utley, 1994).
RESULTS AND DISCUSSION
Epiphyte inventories and their assessment
The number of epiphyte inventories has recently increased
considerably (Appendix 1). Epiphyte diversity patterns on
environmental gradients, however, remain elusive because
several restrictions hinder a comparison between inventories.
First, it is not always clear whether next to true epiphytes,
the parasitic, accidental, facultative, and hemi-epiphytes that
spend part of their life cycle rooted in the soil, were also
included. Secondly, there is no agreement on the sampling
unit of inventories. Epiphytes are either sampled per tree or
parts thereof, per ground surface area or included in local
florulas or regional floras. Epiphyte diversity and abundance
on trees cannot be compared with epiphytes in surface area
plots in the absence of additional data about the structure of
the forest. An ecologically meaningful comparison between
floras requires information about the diversity in habitats
within the area, the beta diversity. Thirdly, the sample effort
may vary considerably between inventories, ranging from
one to more than 100 trees or from 0.01 to 1.5 ha. The size
of florulas often determined by the size of nature reserves
and the size of regional floras is mostly politically based. As a
general rule, epiphyte inventories where the sample effort
was different can only be compared if the sampling was
adequate, i.e. containing a large portion of all species. The
fact that local florulas invariably contain many more species
than plot or tree-based inventories suggests otherwise. To
estimate the total species richness of an inventory through
extrapolation, small samples also do not perform well
(Colwell & Coddington, 1994). The aggregated distribution
of epiphytes in the forest, moreover, calls for relatively large
samples.
Sample size also influences the quantification of epiphyte
ÔsuccessÕ, if the relative contribution of epiphyte diversity to
the entire flora is used: the ÔEpiphyte QuotientÕ (EQ; Hosokawa, 1950). Epiphytes contribute more in smaller plots,
because their accumulation curves per ground surface area
are steeper than those of forest trees, as pointed out by
Nieder et al. (1999, 2001). Single trees may support up to
seventy-seven epiphyte species (Freiberg, 1999). Small plots
of <1 ha often have EQs of over 40%. In local florulas, the
next larger spatial scale, epiphytes contribute less but regularly still over 20%, as for example at Rio Palenque (22%),
La Selva (23%) and at Maquipucuna (27%). In large regions
such as Peru or the Guianas c. 10% of all vascular plant
species are epiphytes, a proportion comparable with the
epiphyte contribution world-wide (Madison, 1977). In
addition to scale, the EQ is prejudiced by an edge effect if the
epiphytes in the crown fraction outside the plot boundary
are included. Transect studies in particular would be subject
to this source of error, possibly explaining the high EQ
(35%) in Rio Palenque (Gentry & Dodson, 1987a).
The spatial scale dependence of diversity patterns per
surface area applies also to the three-dimensional space that
epiphytes inhabit. Johansson (1974) already pointed out that
comparisons of epiphytes of various regions must be performed on host trees of the same size (and species) because of
the strong correlation between host tree and epiphyte. For
example, the significance of the higher diversity in the Sierra
Nevada de Santa Marta plot at 2450 m in comparison with
the 3100-m plot is hard to appreciate because of the smaller
height of the forest (Sugden & Robins, 1979).
In conclusion, much care is needed with the comparison of
the currently available epiphyte inventories. Increased communication among canopy researchers is essential in the
development and implementation of standardized protocols
for comparative studies (Barker & Pinard, 2001). One way
to compare epiphytes between inventories is to plot epiphytes against trees of different sizes (Hietz & Hietz-Seifert,
1995b; Hietz-Seifert et al., 1996; Wolf & Konings, 2001).
The drawing of species accumulation curves, preferably
against some 3D-sampling unit, facilitates a comparison
between inventories. Such curves visualize the sampling
effort and may be used to estimate local species richness
(Colwell & Coddington, 1994). In this study we avoid the
difficult comparison of defined samples by compiling the
plotless data from botanical collections in a data base. That
approach also has its drawbacks that are discussed in the
section on data quality.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1693
The Chiapas epiphyte data base
The final data base comprised 12,276 records in 1173 species. Most records correspond to plants in the six visited
herbaria but c. 100 were taken from regional floras
(Table 1). The label information did not make it possible to
determine the altitude with confidence of 269 records
(2.2%) and the longitude and latitude to minutes of 507
records (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 1890
by J. N. Rovirosa. Germán Münch (1900–1905), E. Matuda
(1936–1979) and F. Miranda (1938–1959) made important
botanical explorations in the early days of exploration with
31, 677 and 121 collections, respectively. More recently,
others, either as first collector or in combination with others
have contributed a great number of collections: M. A. Soto
A. (659), A. Shilom Ton (358), A. Reyes Garcı́a (302), E.
Hágsater (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. Martı́nez S. have
made by far the largest contributions with 3161 and 2079
collections, respectively.
Data quality
The quality of the taxonomy of the data is as good as one
can expect because group specialists classified most specimens. To use only herbarium collections has the advantage
that the difficult identification of sterile individuals in the
field is avoided (Gradstein et al., 1996). All identifications
may, moreover, be verified. Many collections were identified
by A. R. Smith (ferns, 1871), E. Hágsater (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) and
T. G. Cabrera C. (orchids, 134).
The quality of the sampling is more difficult to appreciate.
Botanical collections are not randomly distributed in space
and probably biased for particular species. The geographical
bias in our data is evident from a map of collection sites
(Fig. 1). In certain areas, the site map closely resembles a
state road/river map. Collecting was also centred in or near
natural reserves such as Lagos de Montebello (828) and
Reserva El Triunfo (353) and near archaeological sites
such as Bonampak (eighty-nine), Palenque (153) and Tenam
Puente (thirty-nine). Other areas such as the Pacific and
Gulf Coastal Plains, the northern part of the Sierra Madre,
the south-eastern Central Depression, and much of the
Eastern Highlands are under-represented. In addition, collectors seem to have a bias for certain species. For example,
one of the most common epiphytes in the Central Plateau
is Tillandsia vicentina Standley, reaching densities of
20,000 rosettes ha)1 (Wolf & Konings, 2001). Nevertheless,
only fifteen specimens are encountered in the herbaria.
Tillandsia eizii L. B. Smith, a species with a showy hanging
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
inflorescence that is heavily collected for ceremonial purposes, is present with only seven records. For comparison, the
also weedy Tillandsia schiedeana Steudel is known from
eighty records. The most collected species are all orchids
with a widespread distribution in Central America: Encyclia
cochleata (L.) Leeme (115), Maxillaria variabilis Bateman ex
Lindley (101) and Epidendrum radicans Pavón (82). Perceived beauty and/or distinctiveness, flowering period,
handling ease and a special interest of the botanist may make
a species more attractive for collection. As to the latter, the
publication of a volume on Pteridophyta in the flora of
Chiapas probably contributed to the high number of fern
records (3184) in the data base (Smith, 1981).
Biased sampling influences the quality of the data, but
quality is also affected by the amount of effort invested in the
sampling. Sampling effort will be constrained by factors such
as the amount of time and resources available. The high
number of records in the data base (12,276) suggests that not
many more species will be found with continued exploration, but the sustained rise of the species–accumulation curve
implies otherwise (Fig. 2). Subsets, for example, per altitudinal interval, are even further removed from species saturation. The large number of species (n ¼ 253) that are only
known from single collections particularly highlights the
incompleteness of the sampling. More than half of all species
(600) is known from five or fewer collections.
Because of the non-random approach of the botanist to
plant collecting, the distribution and diversity patterns are to
be interpreted with care. However, the bias in sampling is
not probably very different between regions and individual
collectors. Also because of the high number of records, we
presume that a meaningful assessment of the observed
patterns is possible.
Species diversity and composition
As Mexico is situated at the northern limits of the American
tropics it predictably harbours fewer species of vascular epiphytes than countries near the equator (Gentry & Dodson,
1987a). In apparent agreement, a preliminary inventory of
Mexican vascular epiphytes listed 1207 species (AguirreLeon, 1992), compared with 2110 species in Peru (Ibisch
et al., 1996). Surprisingly however, our data base yields 1173
confirmed species for the state of Chiapas alone and the
estimated total number of species present in Chiapas (SChao) is
1377 species. This high diversity is unexpected when, for
example, 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 unusually
rich and potentially the richest in Mexico (Delgadillo &
Cárdenas-S, 1989; Sipman & Wolf, 1998). That these evolutionary unrelated groups are all diverse suggests that their
high richness is related to the high beta diversity in the state.
In accordance with other epiphyte inventories, Orchidaceae make up the bulk of the number of species followed by
Bromeliaceae, 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
1694 J. H. D. Wolf and A. Flamenco-S
Figure 2 Species collection curves for vascular epiphytes in Chiapas. The curves were
obtained by randomly sequencing the collections ten times.
two-thirds (63%) of all epiphytes are orchids (Ibisch et al.,
1996). The most species-rich orchid genera are Epidendrum
(seventy-nine), Pleurothallis (fifty-two), Encyclia (thirtyseven), Maxillaria (thirty-three), Oncidium (thirty-one),
Spiranthes (twenty-one), Lepanthes (twenty-one), and Stelis
(twenty-one). In the Bromeliaceae, most species are tillandsias (sixty-four); of the remaining genera, Catopsis (fourteen)
and Vriesea (eight) are the most species rich. In contrast to
South American florulas, Guzmania (two) has only few
species. Peperomia (Piperaceae) contributes similar (fortynine species, 4.2%) to the total flora as in Peru (seventyseven species, 3.6%). Cactaceae, however, do contribute
more in Chiapas than in Peru with 2.3 and 0.6%, respectively. The contribution of species in the Pteridophyta is with
21% also larger than in Peru (16.6%). Possibly this reflects
biased sampling. Ferns in Chiapas have been the subject of a
regional flora (Smith, 1981) and their relatively low collecting efficiency indicates a high collecting effort. Remarkable in the Pteridophyta flora of Chiapas is the high number
of Asplenium species (forty-nine). From altitudinal transects
on Mt Kinabalu, Borneo and Carrasco, Bolivia, respectively,
only thirty-seven and twenty-six Asplenium species have
been 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 two
mountain regions (sixty and fifty-five), while the number of
Elaphoglossum species (thirty-eight) is higher than in Borneo
(eight), but lower than in Bolivia (eighty-seven).
Epiphyte distribution patterns
Altitude
We recorded epiphytes up to an altitude of 4100 m on
isolated trees above the timberline. Highest species richness
in Chiapas is found at mid-elevations between 500 and
2000 m (Fig. 3) corroborating Gentry and Dodson’s hypothesis (Gentry & Dodson, 1987a). The pattern is largely
because of orchids, but other epiphyte-rich groups such as
Pteridophyta and bromeliads show a similar distribution. In
Costa Rica, epiphytic bromeliads are also most common in
mountain areas (Rossi et al., 1997). Above 2000 m, the
number of epiphytic aroids and orchids decreases rapidly.
The Pteridophyta decline in richness in a lower rate; but
similar to the rate reported for Bolivia and Borneo (Kessler,
2001; Kessler et al., 2001). Hence, the relative contribution
of ferns to total epiphyte diversity is higher in the temperate
mountain climates (Fig. 4). The common ferns Campyloneuron amphostenon (Kunze ex Klotzsch) Fée and Polypodium fissidens Maxon are characteristic for high
elevations.
Moreover, our compilation of epiphyte inventories worldwide points towards an unimodal richness pattern on tropical mountains (Appendix 1). In Central America, Barro
Colorado Island (<100 m, 204 species) and La Selva
(<150 m, 380 species) have fewer epiphytes than mountain
forests at Monteverde (700–1800 m, 878 species). In South
America the peak in richness appears to lie somewhat higher.
In plots of <1 ha, mid-elevation forests such as Sehuencas
(2100–2300 m, 204 species), La Carbonera (2200–2700 m,
191 species), Merida (2600 m, 128 species) and Cajanuma
(2900 m, 138 species), are richer in species than lowland
forests at Rı́o Palenque, (<220 m, 127 species) and Suromoni (100 m, fifty-three species), and forests near the upper
tree limit at La Caña (3300 m, thirty-nine species) and Santa
Marta (3000–3200 m, thirty species). The number of epiphytes in the florulas of Otonga (2000 m, 193 species), Rı́o
Guajalito (2000 m, 230 species), Maquipucuna (1100–
2800 m, 441 species) and San Francisco (1800–3150 m, 627
species) is also higher than in the vast, 10,000 ha, Mabura
Hill area in Guyana (<100 m, 191 species).
In the discussion of the observed altitudinal pattern, it is
useful to make a comparison with the non-vascular component of the epiphyte community as bryophytes and lichens
provide much information on the altitudinal patterns of
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1695
Table 2 Representation of vascular epiphyte families in the data
base and their collection efficiency, i.e. the number of species
encountered per 100 collections (– ¼ few data)
No. of
No. of Contribution Collection
collections species (%)
efficiency
Angiosperms
Araceae
Araliaceae
Asteraceae
Begoniaceae
Bignoniaceae
Bromeliaceae
Burmanniaceae
Cactaceae
Crassulaceae
Cyclanthaceae
Dioscoreaceae
Ericaceae
Gesneriaceae
Guttiferae
Lentibulariaceae
Liliaceae
Marcgraviaceae
Moraceae
Onagraceae
Orchidaceae
Piperaceae
Rubiaceae
Solanaceae
Subtotal
67
14
3
23
2
101
2
27
12
4
1
14
10
14
1
1
6
4
1
568
52
1
1
929
5.7
1.2
0.2
2.0
0.2
8.6
0.2
2.3
1.0
0.3
0.1
1.2
0.8
1.2
0.1
0.1
0.5
0.3
0.1
48.4
4.4
0.1
0.1
79.2
8.0
5.1
7.7
11.0
–
9.3
–
30.0
30.8
–
–
9.5
15.9
8.6
–
–
11.8
12.9
2.6
10.6
8.3
–
5.9
10.2
Pteridophyta, i.e. ferns and allies
Adiantaceae
56
6
Aspleniaceae
697
49
Blechnaceae
146
12
Dennstaedtiaceae
8
2
Dryopteridaceae
6
2
Grammitidaceae
70
10
Hymenophyllaceae
319
32
Lomariopsidaceae
370
38
Lycopodiaceae
42
8
Nephrolepidaceae
71
7
Polypodiaceae
1310
66
Psilotaceae
1
1
Schizaeaceae
4
2
Tectariaceae
19
2
Vittariaceae
69
6
Woodsiaceae
1
1
Subtotal
3189
244
0.5
4.2
1.0
0.2
0.2
0.9
2.7
3.2
0.7
0.6
5.6
0.1
0.2
0.2
0.5
0.1
20.8
10.7
7.0
8.2
–
–
14.3
10.0
10.3
19.1
9.9
5.0
–
–
10.5
8.7
–
7.7
100.0
9.6
Total
838
273
39
210
3
1087
3
90
39
8
3
147
63
162
2
1
51
31
38
5350
629
3
17
9087
12,276
1173
epiphytes on tropical mountains to date (Reenen &
Gradstein, 1983; Kürschner, 1990; Frahm & Gradstein,
1991; Wolf, 1993a; Kessler, 2000). The study of non-vascular epiphytes is often easier than that of their vascular
co-inhabitants because the classification of sterile specimen
is mostly possible, aided by an increasing number of taxonomic reference books, and because of relatively small
minimal areas (Gradstein et al., 1996). Wolf (1993a),
working in the northern Andes of Colombia, paid full
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
attention to the vegetation in the canopy and we use that
study to summarize the three main altitudinal patterns that
have been observed. First, there was a continuous increase
with elevation in the richness of fruticose lichens. Also in
terms of abundance these dependent outer canopy specialists
thrive on the combination of high light intensities and
re-occurring (fog) precipitation. This pattern exhibited by
the specialist fruticose lichens, however, was exceptional.
Secondly, there was a continuous decline in species numbers with elevation for epiphytic mosses and for crustose
and foliose lichens. This decline was most significant in the
cool and humid forests at higher elevations where branches
were enveloped in a heavy cloak of bryophytes, mainly
liverworts, suggesting increased competition for space. In
addition, mass effect, i.e. the influx of propagules from an
adjacent core area to an area where the species cannot be
self-maintaining (Shmida & Wilson, 1985), has been postulated to produce a decline of richness with elevation,
in combination with Rapoport’s rule (Stevens, 1992).
According to Rapoport’s rule, the elevational (and latitudinal) range of species increases with increasing elevation.
According to Stevens’s Rapoport rescue hypothesis, lowlands may thus be richer in species because they are
potentially sink habitats for a larger number of species. We
tested Rapoport’s rule for our data and indeed found a
good correlation (Pearson) between the mid-elevation of
the distribution of the species and their altitudinal range
(only species with more than ten occurrences; n ¼ 378,
r ¼ 0.36, P < 0.001). According to Stevens’s hypothesis we
expect a monotonically decrease of richness with elevation,
but observed a unimodal pattern. This pattern, the third,
was in Wolf’s study shown by the liverworts, the group
with 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 it
coincided with a zone of overlap between a low- and a
high-elevation flora (Wolf, 1993a). The presence of a zone
where the altitudinal distributions of many species overlap
may also have induced the high species richness at midelevations in Chiapas. Most species-rich families have their
highest diversity in this belt, which suggests a common
factor (Fig. 3). In addition, forests at both low and high
elevations have a distinct epiphyte flora (Table 3). In this
view, between 500 and 2000 m, typical tropical lowland
species coincide with the temperate species from the highlands. The temperate origin of the mountain vegetation of
Chiapas is evidenced by the presence of holarctic tree
genera such as Abies, Acer, Alnus, Juniperus, Pinus,
Prunus, Quercus, Sambucus, Ulmus and Viburnum.
A separate factor that may contribute to the mid-elevational hump results from the geometric constraint on species
ranges (e.g. Colwell & Lees, 2000). When species are distributed stochastically within a bounded domain (from sea
level to mountaintop), null models predict that there is a
mid-domain peak in richness. Unfortunately, the high
number of rare species in the data base render a detailed
analysis of the altitudinal ranges of species impossible and
the presence of zones of overlap or a mid-domain effect
1696 J. H. D. Wolf and A. Flamenco-S
Figure 3 The number of observed species
(Sobs.) and the estimated number of species
(SChao) in main plant groups per altitudinal
interval in the state of Chiapas. For the total
number of epiphytes, SChao diversity at adjacent altitudinal intervals is significantly different in all cases (unpaired t-test,
P < 0.001). *Note that the total number of
collections (12,276) is larger than that of the
summed intervals (12,007), because in this
column 269 collections for which no altitudinal data were available are also included.
Figure 4 Relative contribution of main plant
groups to epiphyte species richness per altitudinal interval.
could thus not be confirmed. The occurrence of overlap, a
mid-domain effect and Stevens’s Rapoport rescue hypothesis
are not mutually exclusive. In general, we agree with Lawton
(1996) and Rahbek (1997) that the quest for single explanations of patterns is unhelpful.
Perhaps the high diversity between 500 and 2000 m
results from a higher diversity of habitats, because next to
the wet mountain forests, the dry Central Depression also
falls in this altitudinal range (Fig. 1). A separate analysis of
the diversity pattern exclusively in the wet Sierra Madre
mountain range, however, also showed a unimodal distribution (Table 4). In addition to habitat diversity, Gentry and
Dodson offer two more hypotheses as to why species
diversity is especially high on mid-elevations at wet mountains: finer niche partitioning and evolutionary explosion.
The latter is associated with the dynamic character of the
young Andean mountains. Our data show that the species
richness patterns are comparable also on more stable
mountains in Chiapas.
Finally, in Bolivia a mid-elevational belt of high epiphyte
pteridophyte diversity is correlated with high amounts of
precipitation in that zone (Kessler, 2001). In Chiapas,
however, there is no such relationship. The collection sites in
the lowlands (<500 m) receive more rainfall annually than
the sites between 500 and 2000 m, respectively, 2580 and
1750 mm.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1697
Table 3 Relative contribution of species in the data base per altitudinal interval (number of records/total number of records in a particular
interval, times 10,000). Only species with a preference for a certain interval are shown, arbitrarily defined as being collected there at least ten
times more often than in any of the other intervals. Rare species having a relative contribution <0.50% in those intervals are not considered
Anthurium pentaphyllum (Schott) Madison
Asplenium auritum Sw.
Asplenium serratum L.
Bolbitis portoricensis (Spreng.) Hennipman
Dryadella linearifolia (Ames) Luer
Encyclia bractescens (Lindley) Hoehne
Epidendrum nocturnum Jacq.
Maxillaria aciantha Rchb. f.
Maxillaria uncata Lindley
Microgramma percussa (Cav.) de la Sota
Nephrolepis pendula (Raddi) J. Smith
Platystele stenostachya (Rchb. f.) Garay
Pleurothallis grobyi Bateman ex Lindley
Polystachya foliosa (Hook.) Rchb. f.
Sobralia decora Bateman
Sobralia fragrans Lindley
Stelis oxypetala Schltr.
Tillandsia bulbosa Hook.
Tillandsia valenzuelana A. Rich.
Trigonidium egertonianum Bateman ex Lindley
Stelis microchila Schltr.
Campyloneurum amphostenon (Kunze ex Klotzsch) Fée
Encyclia varicosa (Lindley) Schltr.
Encyclia vitellina (Lindley) Dressler
Epidendrum eximium L. O. Williams
Fuchsia splendens Zucc.
Isochilus aurantiacus Hamer & Garay
Peperomia campylotropa A. W. Hill
Polypodium fissidens Maxon
Rhynchostele stellata Soto Arenas & Salazar
Stelis ovatilabia Schltr.
<1000
(n ¼ 4714)
1000–2000
(n ¼ 4962)
>2000
(n ¼ 2331)
Total number
of records
59.4
59.4
63.6
50.9
50.9
87.0
78.5
59.4
87.0
57.3
50.9
87.0
76.4
82.7
67.9
78.5
53.0
59.4
70.0
65.8
4.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
4.2
0.0
2.0
0.0
2.0
2.0
0.0
8.1
0.0
2.0
6.0
4.0
2.0
4.0
4.0
2.0
6.0
0.0
0.0
2.0
4.0
4.0
52.4
8.1
16.1
6.0
0.0
4.0
4.0
2.0
0.0
4.0
2.0
0.0
4.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
94.4
205.9
60.1
60.1
154.4
77.2
60.1
77.2
115.8
60.1
31
29
31
26
24
46
37
29
44
29
25
43
40
40
35
37
25
29
35
34
29
26
58
17
15
38
20
15
18
31
16
Table 4 Number of epiphyte species in the Sierra Madre region per
altitudinal interval. Given are the number of records (n), the number
of observed species (Sobs.), and the estimated number of species
(SChao) with the 95% confidence interval
Altitudinal interval
n
Sobs.
SChao
SChao 95% CI
0–500 m
500–1000 m
1000–1500 m
1500–2000 m
2000–2500 m
2500–3000 m
>3000 m
0–4100
279
172
210
454
437
159
37
1748
108
106
154
228
193
93
28
605
166.78
211.09
394.67
408.88
306.64
156.03
83.13
1302.69
(162.6,
(204.3,
(384.1,
(403.2,
(302.3,
(151.4,
(69.2,
(1294.2,
170.9)
217.9)
405.2)
414.6)
311.0)
160.7)
97.0)
1311.1)
Possibly, a mid-elevational zone of higher species richness
is not encountered everywhere. Ibisch et al. (1996) report a
decrease of epiphyte richness with elevation for the whole of
Peru and the lowland florula at Rı́o Palenque (<220 m, 227
species) in the Ecuadorian part of the Chocó biogeographical
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
region is not poorer than many mountain forests. In the
Colombian part of that same region, 0.4 and 0.1 ha plots
contain 140 species on average which is also remarkably rich
(Galeano et al., 1998). On the other side of the Andean
mountains, the Amazonian Rı́o Caquetá region is with 212
species in a 0.75 ha inventory also rich in epiphytes. Presumably, the high diversity in the Chocó and Caquetá
regions is related to the high amounts of annual rainfall
(Gentry & Dodson, 1987a) of c. 3000, 7000 and 3000 mm,
respectively. Next, the rainfall–diversity relationship is
analysed.
Rainfall
Recent epiphyte inventories in neotropical lowland forests
corroborate Gentry & Dodson’s (1987a) hypothesis that
species richness increases with the amount of rainfall
(Fig. 5). For the entire state of Chiapas that in contrast also
includes mountain forests, a different pattern emerges
(Fig. 6). After an initial rise in species richness, the number
of epiphytes decreases again when rainfall exceeds 2500 mm
annually. All species-rich groups exhibit this pattern, except
1698 J. H. D. Wolf and A. Flamenco-S
400
La Selva, Costa Rica
350
Number of species
300
250
BCI, Panama
Mabura Hill, Guyana
200
150
R o Palenque, Ecuador
R o CaquetÆ, Colombia
Coqu , Colombia
R o Manu, Brazil
Tiputini, Ecuador
R o Palenque, Ecuador
100
Nuqu , Colombia
El Amargal, Colombia
El Ducke,
Horquetas, Costa Rica
Suromoni, Venezuela
Brazil
Jauneche, Ecuador
Los Tuxtlas, Mexico
El Verde, Puerto Rico
Capeira, Xalapa, Mexico
Xalapa, Mexico
Los Tuxtlas, Mexico
Ecuador
Santa
Jauneche, Ecuador
Rosa, CR
50
0
0
1000
2000
3000
4000
5000
Annual rainfall (mm)
6000
7000
Figure 5 Vascular epiphyte species richness
in plots (open circles, r Pearson ¼ 0.71) and
local florulas (closed circles, r Pearson ¼
0.95) in areas with different amounts of
annual rainfall. All areas below 1000-m
elevation; data from Appendix 1.
Figure 6 The number of observed species
(Sobs.) and the estimated number of species
(SChao) per annual rainfall (mm) cohort. The
SChao diversity of the Ôepiphytes totalsÕ is significantly different between all cohorts
(unpaired t-test, P < 0.001). For family
totals, see Table 6.
the aroids that remain comparatively stable. The positive
relationship between rainfall and epiphyte diversity thus
breaks down when mountain sites at high elevations are
included. The cool mountains are effectively more humid
than their amounts of rainfall suggest because of the high
average relative humidity of the air and low evapotranspiration (Wolf, 1993a). Cloud precipitation, not measured in
rainfall gauges, may further enhance the moisture availability 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 in
Chiapas could not be found. Again in important plant
groups such as ferns, the bromeliads and orchids, the number 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 in
forests that are relatively dry (Gentry & Dodson, 1987a;
Gentry, 1991). In contrast, the extremely wet forests in the
Chocó have an unusual high number of animal-dispersed
species (Gentry, 1986). As Gentry & Dodson (1987a) postulate, in wet forests wind-dispersed propagules are hampered in their establishment, i.e. dispersal and attachment, in
the face of abundant rainfall. As to bromeliads, rainfall may
fuse the coma hairs of seeds to an inert mass (pers. observ.).
Moreover many orchids, bromeliads and ferns are well
adapted to survive periods of drought (Benzing, 1990).
In agreement with the establishment hypothesis, we
observe that with increased rainfall the characteristic species
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1699
Table 5 Relative contribution of species in
the data base per rainfall cohort (number of
records/total number of records in a particular cohort, times 10,000). All records from
£1000-m altitude are included. All species
with a preference for a certain cohort are
shown, arbitrarily defined as being collected
there at least five or ten times (in bold) more
often than in the other cohort. Rare species
with fewer than ten records are omitted
<2500 mm ‡2500 mm
(n ¼ 3584) (n ¼ 1359)
Araceae
Anthurium lucens Standley ex Yuncker
Orchidaceae Laelia rubescens Lindley
Maxillaria meleagris Lindley
Stelis gracilis Ames
Stelis guatemalensis Schltr.
Trichosalpinx ciliaris (Lindley) Luer
30.7
27.9
30.7
30.7
47.4
50.2
0.0
0.0
0.0
0.0
7.4
7.4
Piperaceae
Peperomia asarifolia S. & C.
Pteridophyta Antrophyum ensiforme Hook.
Asplenium abscissum Willd.
Asplenium auriculatum Sw.
Cochlidium serrulatum (Sw.) L. E. Bishop
Elaphoglossum guatemalense (Klotzsch) Moore
Hymenophyllum polyanthos (Swartz) Swartz
Pecluma divaricata (Fourn.) Mickel & Beitel
Polypodium echinolepis Fée
Polypodium polypodioides (L.) Watt
44.6
30.7
36.3
33.5
36.3
47.4
53.0
61.4
30.7
50.2
7.4
0.0
0.0
0.0
0.0
7.4
7.4
0.0
0.0
7.4
Anthurium flexile Schott ssp. muelleri Croat & Baker 2.8
Monstera acuminata C. Koch
25.1
Philodendron hederaceum (Jacq.) Schott
14.0
Philodendron inaequilaterum Liebm.
11.2
Syngonium angustatum Schott
8.4
Syngonium salvadorense Schott
11.2
66.2
206.0
88.3
80.9
58.9
110.4
Araceae
Gesneriaceae Drymonia serrulata (Jacq.) Martius ex DC.
16.7
100
95.7
Other epiphytes
Piperaceae
90
Bromeliaceae
Ferns and allies
80
Orchidaceae
Araceae
70
Figure 7 Familial composition of epiphyte
floras in neotropical lowland rain forests with
high amounts of rainfall. La Selva, Costa
Rica (Hartshorn & Hammel, 1994). Rı́o
Palenque, Ecuador (Gentry & Dodson,
1987a). Barro Colorado Island, Panama
(Croat, 1978). Rı́o Caquetá, Colombia
(Benavides, 2002). Horquetas, Costa Rica;
the ÔothersÕ category includes Piperaceae
(Whitmore & R. Peralta, 1985). Suromoni,
Venezuela (Engwald, 1999).
Percentage
60
50
40
30
20
10
0
Horquetas,
Costa Rica
(4000 mm)
in the vegetation shift from wind-dispersed orchids and ferns
to Araceae (Table 5). The decrease in anemochoric species is,
however, not fully compensated by zoochoric species. This
appears contrary to other neotropical wet lowland forests,
where aroids contribute more to total diversity (Fig. 7). In a
0.9-ha inventory in the extremely wet forests along the Pacific
Coast in Colombia (annual rainfall of 5100–7150 mm),
aroids were with 100 species even the largest plant family,
comprising over 10% of the total vascular flora (Galeano
et al., 1998). Alongside less than fifteen bromeliads and only
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
La Selva,
Costa Rica
(4000 mm)
Río Caquetá,
Colombia
(3060 mm)
Río Palenque,
Ecuador
(2980 mm)
BCI,
Panama
(2750 mm)
Suromoni,
Venezuela
(2700 mm)
This study,
Mexico
(>2500 mm)
fifty-three orchid species were found. Most aroids had a treedependent growth form, Anthurium and Philodendron being
the largest genera, with forty-eight epiphyte species in total.
Our data base of Chiapas (75,000 km2) contains only sixtyseven epiphytic Araceae. Rı́o Palenque, as well in the Chocó
biogeographic region, is also rich in Araceae (Gentry &
Dodson, 1987a) and this pattern repeats itself on trees of wet
forest in the Amazon where aroids have fifty-two species
compared with thirty-seven orchids and thirty-seven ferns
(Benavides, 2002). Aroid preponderance in wet climates is
1377.5
1173
89.7
25
725.0
545
864.1
650
748.4
492
548.3
417
–
–
385.0
58.6
191.8
49.6
5.5
5.0
345.2
35.1
196.6
53.1
7
–
374.1
31.2
186.0
49.0
790.1
588
–
–
–
–
338.5
35.3
210.3
41.3
–
–
–
–
–
216.1
23.6
150.0
32.4
–
–
51
Total
115.8
87.2
114.9
55.2
30.0
14.3
14.5
648.0
82.3
126.5
275.5
67
101
27
12
14
10
568
52
90
244
–
–
–
–
–
–
–
–
–
–
4
3
0
0
0
1
9
2
4
2
44.3
62.5
36
40
4
0
2
4
277
23
128
31
38.3
82.3
74.5
18.0
28
62
14
10
9
1
293
39
155
39
46.1
68.4
32
50
7
1
5
5
183
27
143
39
37.1
70.1
19.1
30
46
13
1
4
2
158
23
114
26
58.1
66.4
48
50
10
1
7
5
263
28
137
39
–
–
–
–
–
–
–
–
–
–
10
7
1
0
1
2
12
6
8
4
Araceae
Bromeliaceae
Cactaceae
Crassulaceae
Ericaceae
Gesneriaceae
Orchidaceae
Piperaceae
Pteridophyta
Others
SChao
Sobs.
SChao
Sobs.
SChao
Sobs.
SChao
Sobs.
SChao
Sobs.
SChao
The whole
of Chiapas
(n ¼ 12,276*)
Gulf Coastal
Plain (n ¼ 26)
Eastern
Highlands
(n ¼ 2879)
Central Plateau
(n ¼ 3529)
Northern
Highlands
(n ¼ 1482)
Central
Depression
(n ¼ 1338)
Sobs.
SChao
Sobs.
Schao
Sobs.
Vegetation type
In total, 8485 collections could be ascribed to one of the
forest formations of Chiapas, following Breedlove’s classification (Breedlove, 1978). Both the evergreen cloud forest
and the pine-oak Liquidamber forest were lumped with the
montane rain forest, because on the aerial photographs it
was not possible to discern these formations. Collections in
riparian forests and savannas were too few to merit analysis.
Nearly one-third of the collections (2699) were taken from
forests that are now degenerated. This could be recognized
on the aerial photographs, but as we do not know the condition of the forest when the plant was sampled we cannot
assess the influence of forest disturbance on the epiphyte
vegetation. For the 745 species that were collected (3213
Sierra Madre
(n ¼ 2398)
Physiographical region
For the analysis of the distribution of species over the seven
physiographical regions in the state (Fig. 1), 11,724 records
were used that could be attributed to a particular region,
comprising 1153 species. Of all regions, the Central Plateau
is the richest in epiphytes, and richer than the Eastern and
Northern Highlands that have lower elevations and higher
amounts of rainfall (Table 6). In the mountain regions, the
estimated number of species varies between 725 and 864
species. The similarity in diversity suggests that these regions
share many species, but in reality the floristic similarity
between the regions is always <60% (Table 7). With continued exploration the similarities will increase, but clearly
each region has a characteristic combination of species
(Table 8). Of the more common species, the Eastern Highlands in particular have many characteristic species, mostly
orchids. Next to differences in the historical biogeography of
that region, this may be because of the favourable combination of high temperatures at lower elevations and high
amounts of rainfall. It is the region with the largest extension
of lower montane rain forest (Breedlove, 1978).
Pacific Coastal
Plain (n ¼ 72)
not restricted to South America. The flora at La Selva in
Costa Rica also contains many Araceae (ninety-nine species)
and from wet Barro Colorado Island (BCI) in Panama
twenty-four epiphytic aroids are reported compared with
relatively few (eighty-two) tree-dwelling orchids (Croat,
1978; Hartshorn & Hammel, 1994). Also on trees in the
Mexican 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 a
separate hypothesis, we propose that the relatively high
contribution of anemochorous epiphytes is related to the dry
season that gives these plants a good opportunity to disperse.
In contrast to the aforementioned wet lowland forests, the
forests in southern Mexico are subject to a distinct dry
period that lasts several months. As the rainfall regime is an
important element on which the internal division of Chiapas
in physiographical regions and associated vegetation types is
based, we expect that regions and forest formations have
distinctive epiphytes (Breedlove, 1978).
Table 6 The number of observed epiphyte species, Sobs. and the number of estimated species, SChao, per physiographical region in epiphyte rich families. The SChao diversity of the
(column) totals is significantly different between all regions, except for the two coastal plains (unpaired t-test, P < 0.001). Ô–Õ no sufficient data (n < 20) to calculate SChao. *Note that the
total number of collections (12,276) is larger than that of the summed regions (11,724), because in this column 552 difficult to assign borderline cases are also included
1700 J. H. D. Wolf and A. Flamenco-S
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1701
Table 7 Floristic similarity (%) between the physiographical regions, using the qualitative Sørensen index
Region
Pacific
Central Plain
Sierra
Madre
Central
Depression
Northern
Highlands
Central
Plateau
Eastern
Highlands
Gulf Central
Plain
Pacific Coastal Plain
Sierra Madre
Central Depression
Northern Highlands
Central Plateau
Eastern Highlands
Gulf Coastal Plain
x
13.5
13.2
10.3
7.7
11.7
18.9
x
53.9
55.9
59.0
46.2
6.3
x
56.1
51.5
50.7
6.8
x
56.6
55.2
6.2
x
47.5
3.0
x
7.0
x
Table 8 Relative contribution of species in the data base per region (number of records/total number of records in a particular region,
times 10,000). Only species with a preference for a certain region are shown, arbitrarily defined as being collected there at least ten times
more often than in any of the other regions. Rare species having a relative contribution <0.50% in those regions are not considered as are
the coastal plains because there the sampling effort was low (<100 records)
Anthurium chiapasense Standley
Oncidium laeve (Lindley) Beer
Stelis ovatilabia Schltr.
Dryadella linearifolia (Ames) Luer
Epidendrum nocturnum Jacq.
Lycaste cochleata Lindley
Maxillaria pulchra (Schltr.) L. O. Williams
Nephrolepis pendula (Raddi) J. Smith
Platystele stenostachya (Rchb. f.) Garay
Polystachya foliosa (Hook.) Rchb. f.
Psygmorchis pusilla (L.) Dodson & Dressler
Stelis oxypetala Schltr.
Tillandsia bulbosa Hook
Trichosalpinx ciliaris (Lindley) Luer
Sierra Madre
(n ¼ 2398)
Central
Depression
(n ¼ 1338)
Northern
Highlands
(n ¼ 1482)
Central
Plateau
(n ¼ 3529)
75.1
79.2
62.6
–
4.2
–
–
4.2
–
4.2
4.2
–
–
–
–
–
–
–
–
–
7.5
7.5
7.5
–
–
–
–
–
–
–
–
–
–
–
–
–
6.7
–
–
–
6.7
–
5.7
–
–
–
–
–
–
–
–
2.8
–
–
2.8
0.0
collections) from sites that currently are devoid of any forest
cover, however, it must be feared that their local populations
have become extinct. The large number of rare species in the
data base raises concerns that recently many species may
have gone extinct in Chiapas, possibly before they were ever
sampled. The current situation is likely even gloomier
because the assessment of forest cover is based on aerial
photographs taken over 20 years ago. In the Central Plateau
of Chiapas, annual deforestation rates for 1974–1984 and
1984–1990 were 1.58 and 2.13%, respectively (OchoaGaona & González-Espinosa, 2000).
Most epiphytes are found in the montane rain forest
(Table 9). Both in the tropical and lower montane rain
forest and in the two other forest types from lower elevations that are all subject to a more prolonged dry season,
the important Orchidaceae and Pteridophyta are less
diverse. However, some of these formations are not well
collected, and additional species are likely to be found.
Remarkably, the bromeliads are most diverse in the pine–
oak forest of the highlands. Of the two main tree genera,
bromeliads are mostly found on oaks and are apparently
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Eastern
Highlands
(n ¼ 2879)
3.5
–
–
83.4
125.0
72.9
52.1
79.9
142.4
132.0
52.1
83.4
93.8
66.0
No. of
records
21
19
15
24
37
21
16
25
43
40
17
24
29
19
well adapted to the semi-deciduous habit of these trees. A
thick water-absorbing bark may facilitate bromeliad survival, in particular that of the seedlings (Castro-Hernandez
et al., 1999). High diversity is not associated with a unique
flora, Tillandsia carlsoniae L.B. Smith being the only
exclusive species.
CONCLUSIONS
For a region at 15N, the flora of Chiapas with 1173 species
is remarkable rich in vascular epiphytes. Presumably this
relates to the high diversity in habitats of the state. Each
physiographical region and forest formation supports characteristic epiphytes, indicating a low expansion rate and/or
habitat specialization.
We were able to corroborate Gentry & Dodson’s (1987a)
hypothesis that on neotropical mountains most species are
present in a mid-elevational belt, in Chiapas between 500
and 2000 m altitude. A predicted increase of epiphyte
diversity when rainfall increases, however, was not
observed. After an initial rise, the number of species
1702 J. H. D. Wolf and A. Flamenco-S
Table 9 The number of observed epiphyte species, Sobs., and the number of estimated species, SChao, per vegetation type in epiphyte rich
families. Forest formations from Breedlove (1978). The SChao diversity of the column totals is significantly different between all formations
(unpaired t-test, P < 0.001). The montane rain forest includes the evergreen cloud forest and the pine–oak Liquidamber Forest. Ô–Õ, no sufficient
data (n < 20) to calculate SChao. For family totals for the entire state of Chiapas, see Table 6
Forest
formation
Tropical
deciduous forest
(n ¼ 313)
Evergreen and
semi-evergreen
seasonal forest
(n ¼ 236)
Tropical and
lower montane
rain forest
(n ¼ 2637)
Montane rain
forest
(n ¼ 3030)
Pine–oak
forest
(n ¼ 2269)
Altitude
Dry season
0–1200 m
3–5 months
SChao
Sobs.
0–1200 m
1–3 months
Sobs.
SChao
0–800 m
<1 months
Sobs.
SChao
800–3300 m
1 week–3 months
Sobs.
SChao
1200–4000 m
3–6 months
Sobs.
SChao
40
44
6
0
2
5
258
27
126
31
342.0
76.0
208.3
36.0
40
46
7
0
11
6
322
30
183
47
430.9
50.2
235.2
63.2
40
61
12
5
7
3
263
35
141
41
751.1
692
909.3
608
Araceae
Bromeliaceae
Cactaceae
Crassulaceae
Ericaceae
Gesneriaceae
Orchidaceae
Piperaceae
Pteridophyta
others
Total
18
33
5
1
2
0
66
14
26
14
179
42.0
56.1
144.9
24.7
45.6
17.1
7
10
2
0
2
1
52
10
56
12
351.6
152
–
–
–
–
–
–
–
–
–
–
196.6
–
78.8
–
302.0
decreases when the annual amount of rainfall exceeds
2500 mm. In southern Mexico, even the wettest forests are
subject to a dry period. Wind-dispersed orchids, bromeliads
and Pteridophyta are the most species-rich groups. They
appear well-adapted to the dry season when they disperse
their seeds and decline in the wetter forest. In the wettest
forests, animal-dispersed plants in the Araceae gain in
importance, but these are less diverse as in rain forests
elsewhere. As a consequence, in Chiapas the rainfall–diversity relationship is unusual. We conclude that next to the
annual amount of rainfall, its distribution in time determines
the composition of the epiphyte community.
As we were able to interpret the diversity patterns, we also
conclude that herbarium collections may be used to obtain a
good impression of those patterns when large numbers of
collections are available and despite the non-systematic
sampling of the botanist.
ACKNOWLEDGMENTS
We thank Juan Castillo, José L. Godónez-A., Teresa Santiago-V. and in particular Guadalupe Olalde who between
them compiled most of the information in the data base. We
are grateful for the hospitality and co-operation encountered
in all the institutions where we examined the botanical
collection. The information of orchid enthusiast Cisco Dietz
yielded many new records for the state. Miguel Angel
Castillo and Dario Navarrete at the Ecosur GIS laboratory
are acknowledged for providing digitized information on the
distribution of rainfall, forest formations and physiographical regions. Gerard Oostermeijer and two anonymous
reviewers provided valuable suggestions to improve the
manuscript. Financial support was provided by Comisión
539
47.6
71.0
–
–
–
–
42.6
66.3
–
–
11.3
–
60.3
81.0
–
–
8.0
–
397.5
45.3
179.3
49.3
869.9
Nacional para el uso y Conocimiento de la Biodiversidad,
CONABIO, grants B060 and L050.
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BIOSKETCHES
Jan Wolf is a former senior scientist at Ecosur. Currently
he is professor holding the Dr Jakoba Ruinen Chair,
Phyllosphere Sciences at the Institute for Biodiversity and
Ecosystem Dynamics, Universiteit van Amsterdam. His
general interest in canopy biology centres on the conservation and ecology of epiphytes and epiphyte communities, particularly in tropical America.
Alejandro Flamenco-S, left his academic position at
Ecosur to enrol in the PhD programme at the Instituto de
Ecologı́a, Universidad Nacional Autónoma de México
(UNAM). He is interested in the application of geographic information systems for biodiversity conservation issues.
1706 J. H. D. Wolf and A. Flamenco-S
Appendix 1 Inventories of epiphytic vascular plants, arranged by sampling unit. EQ is Epiphyte Quotient (Hosokawa, 1950).
Location
Latitude
Altitude
(m a.s.l.)
Rainfall
(mm year)1)
Tree
height (m)
NEW WORLD
Mexico, Xalapa21
Costa Rica, Monteverde28
Mexico, Los Tuxtlas24
Panama, BCI49
Guatemala, Las Minas8
Mexico, Chiapas48
Guyana, Mabura Hill, DEF10
Guyana, Mabura Hill, MOR10
Guyana, Mabura Hill, MGH10
Guyana, Mabura Hill44
French Guiana, Nouragues14
French Guiana, Saül10
French Guiana, Saül13
Ecuador, Yasumi15
Ecuador, Tiputini15
Brazil, Serra do Cipó46
Ecuador, Los Cedros15
Ecuador, Otonga15
Ecuador, Otonga36
Ecuador, Rı́o Guajalito39
1931¢ N
1018¢ N
1825¢ N
909¢ N
1407¢ N
1642¢ N
520¢ N
520¢ N
520¢ N
520¢ N
359¢ N
532¢ N
338¢ N
040¢ S
045¢ S
19–20S
019¢ N
025¢ S
025¢ S
014¢ S
1300
1500
100–400
0–100
2225
2300–2450
<100
<100
<100
<100
45
200
200
250–300
250–300
1400
1400
1800
2000
1800–2200
1500
2250
4700
2750
–
1040
2700
2700
2700
2700
3750
2413
2000
2750
2750
1500e
3050
2750
2600
2700
24
20–30
30–35
7
–
25
30
40–50
35
30–35
52
30–35
45–55
19–44
30–38
2
30–39
25–28
25
25
Mexico, Los Tuxtlas24
Mexico, Los Tuxtlas24
Costa Rica, Horquetas47
Puerto Rico, El Verde42
Mexico, Xalapa22
Mexico, Xalapa22
Mexico, Xalapa22
Mexico, Xalapa22
Mexico, Xalapa23
Mexico, Xalapa22
Venezuela, Suromoni11
Ecuador, Rio Palenque18
Ecuador, Jauneche18
Ecuador, Capeira18
Ecuador, Tiputini33
Colombia, Nuquı́, Chocó16
Colombia, Coquı́, Chocó16
Colombia, El Amargal, Chocó16
Colombia, Rı́o Caquetá, Caquetá3
Colombia, Serrania de Macuira43
Colombia, Santa Marta43
Colombia, Santa Marta43
Colombia, Santa Marta43
Bolivia, Sehuencas26
Venezuela, Merida32
Ecuador, Cajanuma6
Venezuela, La Carbonera11
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
Venezuela, La Caña41
1825¢ N
1825¢ N
1022¢ N
1815¢ N
1941¢ N
1941¢ N
1941¢ N
1941¢ N
1941¢ N
1941¢ N
310¢ N
c. 2S
c. 2S
c. 2S
038¢ S
529¢ N
529 N
529¢ N
100¢ S
1210¢ N
1054¢ N
1054¢ N
1054¢ N
1730¢ S
835¢ N
405¢ S
837¢ N
843¢ N
843¢ N
843¢ N
843¢ N
843¢ N
843¢ N
843¢ N
843¢ N
100–400
100–400
100
480
720
1000
1370
1430
1980
2370
100
<220
<220
<220
230
<300
<300
<300
<300
600–800
1400–2000
2300–2600
3000–3200
2100–2300
2600
2900
2200–2700
2300
2550
2650
2750
2950
3000
3080
3300
4700
4700
4000
2920
1552
1678
1780
1790
1787
1686
2700
2980
1855
804
3200
5100–7150
5100–7150
5100–7150
3060
–
–
–
–
3500
2500
3000
1500
1200–1600
1200–1600
1200–1600
1200–1600
1200–1600
1200–1600
1200–1600
1200–1600
30–35
30–35
17
–
13.2
15.9
22
20.3
18.5
27.3
20–30
–
–
–
–
–
–
–
10–>30
2–7.5
15–20
12–15
4–9
–
10–22
10–12
35 ()47)
25–30
18–22
18–22
16–20
18–22
16–20
14–17
7–9
Sampling
unit
TREE/BRANCH
Branch section
Branch section
Tree
Treea
Treeb
Treec
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Treef
Tree
Tree
Tree
Tree
PLOT
0.17 ha
0.16 ha
0.01 ha
0.04 ha
0.15 ha
0.068 ha
0.09 ha
0.063 ha
0.063 ha
0.09 ha
1.5 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
0.4 ha
0.4 ha
0.1 ha
0.025 ha
0.01 ha
0.01 ha
0.01 ha
0.01 ha
0.08 ha
1.5 ha
0.0172 ha
0.08 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
0.1 ha
Sampling
effort
No. of
species
EQ (%)
170
231
38
1210
327
105
11
15
105
25
1
30
3
5
5
98
5
4
10
17
44
65
58
68
68
30
64
84
93
96
74
174
77
21d
30d
6
31d
42d
159
81
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
1 (58 trees)
1 (69 trees)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
30
14
4
4
10
1
1
1
1
1
1
1
1
1
1
1
1
29
42
61
42
42
40
22
53
39
23
53
127
13
3
146
122
183
114
212
28
26
41
30
230
128
138
191
53
64
60
62
61
53
52
39
–
–
26.18
–
–
–
–
–
–
–
–
34.79
7.69
1.73
–
25.00
37.42
25.79
–
–
–
–
–
38.00
58.45
–
45.00
46.00
42.00
48.00
41.00
51.00
50.00
49.00
32.00
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707
Epiphyte distributions in Chiapas, Mexico 1707
Appendix 1 continued
Location
Latitude
Altitude
(m a.s.l.)
Rainfall
(mm year)1)
Tree
height (m)
Sampling
unit
Sampling
effort
No. of
species
EQ (%)
Venezuela, La Caña41
843¢ N
2300–3300
1200–1600
<30
0.1 ha
8
152
41.00
Panama, BCI9
Costa Rica, La Selva20
Costa Rica, Santa Rosa29
Costa Rica, Monteverde19
Guyana, Mabura Hill10
Brazil, Reserva Florestal Ducke38;40
Ecuador, Rio Palenque17
Ecuador, Jauneche17
Ecuador, Capeira17
Brazil, Rio Manu floodplain12
Ecuador, Otonga36
Ecuador, Rı́o Guajalito30
Ecuador, Maquipucuna45
Ecuador, Res. Biol. San Francisco7
909¢ N
1026¢ N
1050¢ N
1012¢ N
520¢ N
305¢ S
c. 1S
c. 2S
c. 2S
1154¢ S
025¢ S
014¢ S
00¢ N
358¢ S
0–100
35–137
<400
700–1800
<100
100
<220
<220
<220
300–400
1680–2251
1800–2200
1100–2800
1800–3150
2750
4000
1600g
2500
2700
2100
2980
1855
804
2028
2600
2700
>3000
2500–>5000
22–30
40
–
–
30–50
–
–
–
–
–
25
25
<35
<35
FLORULA
1560 ha
1536 ha
37,000 ha
–
10,000 ha
10,000 hai
170 ha
321 acres
–
<2000 ha
600 ha
400 ha
22,000 ha
1000 ha
–
–
–
–
–
–
–
–
–
–
–
–
–
–
204
380
19
878
191
51
227
58
8
150
193
230
441
627
14.90
22.65
3.15h
29.41
13.33
4.56
21.97
10.96
1.73
12.35
–
31.64
26.89
–
Mexico1
Mexico, this study
Mexico, Yucatán Peninsula37
Guianas5 cited in10
Peru27
15–32N
15–18N
18–22N
1–9N
0–18S
–
0–4100
<200
0–2750
–
–
800–5000
500–1500
2000–4000
–
–
–
6–25 (30)
–
–
REGIONAL FLORA
1,958,000 km2 2900 coll.
75,000 km2
12276 coll.
10,000 km2
–
470,000 km2
–
1,285,000 km2 –
1207
1173
107
c. 950
2110
–
13.90
–
10.33
10.30
OLD WORLD
Zaı̈re4
Rwanda4
Liberia, Nimba mountains31
Liberia, Nimba mountains31
India, Varagalaiar2
New Zealand, Moeraki river25
WORLD35
WORLD34
WORLD18
150¢ S
230¢ S
6–8N
7N
1025¢ N
4543¢ S
–
–
–
800–900
1800–2200
500–1300
500–600
630
0–10
–
–
–
1800–2500
1600–2000
1500–3100
1500
1600
3455
–
–
–
32
22
10–45
40–45
–
22–37
–
–
–
Tree
Tree
Tree
plot (0.075 ha)
plot (1 ha)
Tree
–
–
–
106
62
153
65j
26
61
28,200
23,456
29,505
c. 2.5
c. 2.5
–
–
–
a
<20
<20
463
3 (96 trees)
30
3
–
–
–
c. 10
c. 10
c. 10
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 only
Vellozia piresiana L. B. Smith treelets; g with 6 months of dry season; h excluding grasses; i based on 4946 herbarium specimens, mainly
terrestrials; 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-León (1992); 2 Annaselvam & Parthasarathy (2001); 3 Benavides (2002); 4 Biedinger & Fischer (1996); 5 Boggon et al. (1997); 6
Bøgh (1992); 7 Bussmann (2001); 8 Catling & Lefkovitch (1989); 9 Croat (1978).; 10 Ek (1997); 11 Engwald (1999); 12 Foster (1990); 13
Freiberg (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 & HietzSeifert (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 Köster et al. (2003); 34 Kress (1986);
35 Madison (1977); 36 Nowicki (2001); 37 Olmsted & Gómez-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 & Espı́rito-Santo (2002); 47 Whitmore & Peralta (1985); 48 Wolf & Konings (2001); 49 Zotz (1999).
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1689–1707