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Ravines as refuges for Orchidaceae in
south-eastern Mexico
ANNE DAMON*, CARLOS ALMEIDA-CERINO, JAVIER VALLE-MORA,
VINCENZO BERTOLINI and JOSÉ-HIGINIO LÓPEZ-URBINA
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Unidad
Tapachula. Carr. Antiguo Aeropuerto km 2.5, Tapachula, Chiapas 30700, Mexico
Received 9 October 2014; revised 27 January 2015; accepted for publication 15 March 2015
Floristic studies of south-eastern Mexico have not considered the ravine component of the landscape and, in this
study, we demonstrate the potential of ravines as refuges for orchids. At elevations of 1442–2358 m in the buffer
zone of the Tacaná Volcano Biosphere Reserve, in the region of Soconusco, south-eastern Mexico, where 7.68% of
the landscape has slopes >45°, we registered 86 species of orchid from 35 genera, 14 (16.25%) of which were
exclusive to ravines, 47 (54.6%) were exclusive to accessible surrounding areas and 25 (29%) colonized both types
of habitat. The tropical mountain cloud forest (TMCF) ecosystem was distributed in the accessible areas
surrounding the ravines and in some sites extended into the ravines themselves. Evergreen mountain scrub forest
(EMSF), only found in the ravines, contributed eight species of orchid exclusive to this ecosystem. The elevation,
orientation and slope of the ravines influenced species richness. The instability of the ‘soils’ on steep slopes and
occasional landslides were negative environmental characteristics of the ravines, which, however, were mostly
dependent on the management of surrounding areas, and epiphytes inhabiting ravines and the surrounding areas
shared similar risks of whole-tree and branch fall, wind and torrential rain. © 2015 The Linnean Society of
London, Botanical Journal of the Linnean Society, 2015, 00, 000–000.
ADDITIONAL KEYWORDS: evergreen mountain scrub forest – Laplace method – Renyi entropy – Soconusco
– Tacaná Volcano Biosphere Reserve – tropical mountain cloud forest.
INTRODUCTION
The Sierra Madre mountain range in Chiapas, which
forms part of the Mesoamerican Biological Corridor, is
an ecologically important transition zone between the
Neoarctic and Neotropical biogeographical regions
(The Nature Conservancy, 2000; Rodríguez & Asquith,
2004), forming a centre of high biodiversity and end-
emism in which many species survived periods of
climate change and extinctions (Castro, 2007). Fur-
thermore, it is an elevationally diverse volcanic zone
isolated from other volcanic regions in Mexico, with
particularly high levels of precipitation (Arriaga et al.,
2000). The region is characterized by a diversity of
forest ecosystems, of which tropical mountain cloud
forests (TMCFs) (equivalent to ‘bosque mesófilo de
montaña’ in Mexico) predominate (Espejo et al., 2005),
with the greatest extension of this type of forest in
northern Mesoamerica (Rodríguez & Asquith, 2004).
TMCFs are generally distributed between 1500 and
2500 m, although they extend up to 3000 m on the
Tacaná Volcano (Challenger et al., 2010).
TMCFs are unique plant communities which, in the
Neotropics, are characterized by persistent cloud cover
in contact with the vegetation (horizontal rain), high
levels of precipitation, steep slopes and high atmos-
pheric humidity (Challenger, 1998; Brown & Kappelle,
2001; Hamilton, 2001). Despite the fact that TMCFs
occupy <1% of Mexican territory, it is the ecosystem
with the greatest diversity of flora and fauna in
relation to area [Ortega & Castillo, 1996; Challenger,
1998; Comisión Nacional para el Conocimiento y uso de
la Biodiversidad (CONABIO), 2010], and the abun-
dance and biomass of epiphytes and lianas are notori-
ous (Rzedowski, 1996). TMCFs provide important
*Corresponding author. E-mail: adamon@ecosur.mx
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Botanical Journal of the Linnean Society, 2015, ••, ••–••. With 5 figures
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–•• 1
ecological services, contributing to hydrological and
nutrient cycles, soil development and the control of
erosion and sedimentation of rivers (Challenger, 1998;
CONABIO, 2010). However, TMCFs are one of the
most threatened ecosystems in the world, because of
logging, non-sustainable extraction of species, fires,
introduction of exotic species and a naturally height-
ened sensitivity to atmospheric contamination (Brown
& Kappelle, 2001; Hamilton, 2001). In Mexico, the
distribution of TMCFs is highly fragmented because of
the continuing extension of the agricultural frontier,
changes in land use for annual crops, coffee planta-
tions, extensive cattle ranching and, to a lesser extent,
landslides and road construction. Navarrete et al.
(2010) found that, in a period of only 26 years (1974–
2000), the Sierra Madre mountain range in Chiapas
had suffered an increase in deforestation from 1.1 to
12.9%.
Ravines are steep mountain slopes which create
abrupt borders in the landscape and can provide a
diversity of unique microhabitats for plants and other
organisms. Because ravines are almost inaccessible,
they are perhaps one of the most conserved habitats
in the forest landscape and can serve as important
refuges for a variety of organisms from the original
ecosystems. Hylander & Hedderson (2007) suggested
that precipitation, summer temperature and the per-
manence and extension of cloud cover are the factors
that determine the diversity and abundance of bryo-
phyte communities in ravines. The analysis of moun-
tain vegetation communities suggests that ravines
have heterogeneous environments and novel micro-
habitats not present in the surrounding areas (Ogata,
Rico-Gray & Nestel, 1996; Shaolin et al., 2008), with
elevational differences as an important component
(Halffter & Pineda, 2005). Furthermore, the relatively
low temperatures and cloud cover typical of TMCF
habitats are considered to limit photosynthesis and
thereby the growth, final height and biomass of trees
(Ash, 1987; Cordero, 1999; Onoda & Anten, 2011); in
ravines, tree growth may be further affected by the
thin soils, slopes, winds and the abundant rainfall
that may propitiate landslides (Luna, Velázquez &
Velázquez, 2001).
In Mexico, between 50 and 60% of Orchidaceae
are found in TMCFs [International Union for Con-
servation of Nature/Species Survival Commis-
sion (IUCN/SSC) Orchid Specialist Group, 1996;
Rzedowski, 1996; Espejo et al., 2005; Hágsater et al.,
2005]. The Tacaná–Boquerón biological corridor
(Arriaga et al., 2000), in the state of Chiapas, is the
second richest region for orchid species in Mexico,
with 314 species registered, after El Mormón-Las
Margaritas-Montebello, also in Chiapas, with 333
species (Soto-Arenas, 2001; Soto-Arenas & Salazar,
2004; R. Solano & A. Damon, unpubl. data). Of that
total, 37 species are classified as threatened and are
included in the ‘Norma Oficial Mexicana-059’ [Secre-
taría del Medio Ambiente y Recursos Naturales
(SEMARNAT), 2010].
Various floristic studies have been carried out in
south-eastern Mexico. Some have focused on orchids
(Breedlove, 1986; Soto-Arenas, 1986, 1994, 2001; Long
& Heath, 1991; Bachem & Rojas, 1994; Castillo, 1996;
Damon & Colín-Martínez, 2004; Levy et al., 2006;
Pérez-Farrera et al., 2006; Martínez-Meléndez, Pérez-
Farrera & Farrera-Sarmiento, 2008; Damon, 2010),
but none has studied the floral communities of the
ravine component of the landscape. For that reason,
the objective of this study was to determine the diver-
sity of the orchid communities in ravines and compare
it with inventories for the accessible surrounding
areas, at selected sites in the Tacaná Volcano Bio-
sphere Reserve in Soconusco, Mexico, and thereby
evaluate the importance of ravines as refuges for the
conservation of the orchids of the region.
METHODS
STUDY AREA
The study was carried out in three localities in the
buffer zone of the Volcán Tacaná Biosphere Reserve,
in the region of Soconusco, in the state of Chiapas,
south-eastern Mexico: Chiquihuites (Municipality of
Unión Juárez), Benito Juárez El Plan and Agua Cali-
ente (Municipality of Cacahoatán). This area forms
part of the Tacaná–Boquerón biological corridor,
which, in turn, is integrated into the Mesoamerica–
Mexico biological corridor (Fig. 1).
The TMCFs are restricted to areas with abrupt
topography, with slopes relatively protected from
exposure to winds, and where cloud cover is almost
constant. Forest structure reaches 10–25 m with
abundant climbing plants and epiphytes and ever-
green species of trees (for a detailed habitat descrip-
tion, refer to: Provisional Management Plan for the
Volcán Tacaná Biosphere Reserve, 2008 and Godínez-
Ibarra et al., 2012, unpubl. data).
STUDY SITES
Chiquihuites (CH) is situated at 15°05′13.6″N and
92°05′36.7″W, at an elevation of 2092 m. The climate is
temperate humid with an annual precipitation of
2000–2500 mm in summer and mean annual tempera-
tures of <18 °C [Japan International Cooperation
Agency (JICA), 1999]. Benito Juárez El Plan (BJ) is
localized at coordinates 15°03′18″N and 92°11′28″W, at
an elevation of 1459 m. The climate is warm with an
annual precipitation of 4500–5000 mm in summer and
mean annual temperatures of <24 °C (JICA, 1999).
Agua Caliente (AC) is situated at 15°09′49″N and
2A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
92°09′18″W, at an elevation of 1594 m. The climate is
temperate humid with an annual precipitation of
1500–2000 mm in summer and mean annual tempera-
tures of <18 °C (JICA, 1999).
CHARACTERIZATION OF THE RAVINES
In each of the three localities, two or three ravines
with pronounced 45–90° slopes were selected. A rep-
resentative section of each ravine was sampled, estab-
lishing a total of six transects per locality, giving a
total of 18. Slope was expressed as the percentage
inclination of the terrain, calculated using cartogra-
phy (contour maps) and corroborated in the field
using a GPS (Global Positioning System, Garmin
eTrex Vista). The elevation, orientation and vegeta-
tion of each ravine were noted, together with the
general characteristics of the soil and topography.
SAMPLING TECHNIQUES
We carried out two types of survey. (1) In the ravines
(slopes >45°), each transect consisted of a 40-m line
divided into four sampling sites at intervals of 10 m,
which were accessed using modified alpine climbing
equipment (Perry, 1978). We registered the orchids
present within reach at each sampling site and noted
the dominant components of the vegetation of each
ravine in general and each transect in particular.
(2) For the surrounding areas (accessible and
slopes <30°), a general inventory of the orchid species
present in accessible areas within each locality was
drawn up, covering an area approximately equivalent
to 1–2 ha, as near as possible to each ravine, but highly
variable depending on the terrain. The accessible
surrounding areas, which, in all cases, consisted of
TCMF, disturbed to varying degrees by human activity,
were not characterized in detail, serving only as a
reference for the orchid species present in the vicinity
of each ravine. Binoculars were used to identify orchids
in the tree crowns. For both surveys, data were taken
of the growth habit (epiphyte, lithophyte, terrestrial)
and the substrates colonized by the orchids.
Orchid plants without flowers that could not be
identified were collected and maintained in the living
Figure 1. Location of the Tacaná Volcano Biosphere Reserve and the study areas.
RAVINES AS REFUGES FOR ORCHIDS IN MEXICO 3
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
collection managed by the project (Jardín Botánico
Regional ‘El Soconusco’, Tuzantán, Chiapas, Mexico) to
be identified at a later date. Meanwhile, unidentified
plants were grouped according to morphological char-
acteristics into morphospecies (Kremen et al., 1993;
Derraik et al., 2002) and included in the analysis.
DATA ANALYSIS
To compare orchid species richness between the
ravines, we used an analysis of Renyi entropy (Hill,
1973), which employs the following expressions.
q=0, 0Dis equivalent to the number of species
observed in the community (species richness).
q=1,1Dis the exponential function of the Shannon–
Wiener index H′, so that 1D=f(x)=eH′, in which
species is weighted according to its proportional
abundance.
q=2, 2Dis the reciprocal of the Simpson index (D)
such that 2
2
1
11
DDP
i
i
S
==
=
∑gives the effective
number of species obtained when the weighted
arithmetic mean is used to quantify the average
proportional abundance.
We used the method recently described by
Shtilerman et al. (2014) to compare the estimated
numbers of orchid species in the ravines, surrounding
areas and in combination. The technique involves the
use of the Laplace method to approximate the asymp-
totic integrals and, according to the evidence pre-
sented by the authors, performs better than most
options currently available.
Sn S A
n
B
n
()
=−+
⎛
⎝
⎜
⎜
⎞
⎠
⎟
⎟
⎛
⎝
⎜⎞
⎠
⎟⎛
⎝
⎜⎞
⎠
⎟
*1 12
αα
where S(n) represents the species accumulation
curve derived from the samples carried out in this
study. A,Band S* are the estimated parameters of
the model, in which S* is the asymptote of the model
and represents the number of species. The parameter
αis taken to be ‘2’, which gives good results in the
majority of the applications of this model. The model
was adjusted using a non-linear model in R (Ritz &
Streibig, 2008; Grothendieck, 2013).
Using the platform ArcGis Desktop 9x, the propor-
tion of the study area present in the form of ravines
with different slopes was calculated, using the follow-
ing methods.
1. Using contour lines at 5-m intervals, a model was
generated of the interpolation of the curves
derived from the triangular irregular network
(TIN).
2. A map of the inclination of the slopes was devel-
oped, according to the software SIG, and further
modified according to the requirements of this
study. We chose to work with the following ranges:
0–45°, 45–50°, 50–60°, 60–70° and <70°.
3. Finally, the data were converted to modelo digital
de elevación in the form of a raster to produce a
vectorial-type layer. At this stage, the surface area
covered by each of the selected slope ranges was
calculated, using the field ‘Hectare’.
RESULTS
CHARACTERIZATION OF THE RAVINES
The ravines were situated in an elevational range of
1442 to 2358 m, with slopes of 45° to 90° (transect 4
included a small section with a slope of 38°), and
depths of 90–300 m, distributed as shown in Table 1.
All the ravines had rocky outcrops and abundant
organic material. On extreme slopes, where runoff
displaces the organic material, the rocks were instead
covered by abundant bryophytes. Terracing was
observed in various sites, promoting the accumulation
of organic matter, and, on the vertical walls, there
were various species of bromeliads, Adiantaceae,
Begoniaceae and Selaginellaceae. Twelve of the
transects were oriented towards the east, exposed to
sunlight during the early hours of the morning, and
six were oriented towards the west, exposed to sun-
light in the late afternoon (Table 1).
In the ravines, there were two basic types of forest
vegetation: tropical mountain cloud forest (TMCF)
and evergreen mountain scrub forest (EMSF) (equiva-
lent to ‘matorral perennifolio de neblina’ in Mexico),
the latter of which was only found in the ravines and
which did not overlap with TMCF. EMSF consisted of
dwarf trees and shrubs of Araliaceae, Betulaceae,
Caprifoliaceae, Ericaceae, Fagaceae, Lauraceae,
Rosaceae and Theaceae, measuring 4–15 m in height,
with twisted trunks and branches, and several
species of epiphytic ferns, orchids and bromeliads.
The herbaceous stratum consisted of species of Aster-
aceae, Melastomataceae, Rubiaceae, Scrophulari-
aceae and Urticaceae.
Within the ravines of two localities (CH and BJ), six
transects consisted of EMSF, although the surround-
ing areas always consisted of TMCF. By contrast, all
the transects in the locality AC, four in BJ and two in
CH consisted of TMCF (Table 1), with heights of
15–25 m, associated with tree ferns of Cyatheaceae,
and the communities were dominated by tree species
of Betulaceae, Fagaceae, Lauraceae, Pinaceae, Rubi-
aceae and Theaceae. The shrub layer reached heights
of between 1 and 12 m, and consisted of plants from
the families Arecaceae, Clusiaceae, Ericaceae, Melas-
4A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
tomataceae, Myrtaceae and Rubiaceae. Both trees
and shrubs were host to a variety of epiphytic species
of ferns, orchids and bromeliads. The herbaceous
layer contained plants from the families Acanthaceae,
Arecaceae Asteraceae and Urticaceae.
ORCHID INVENTORY AND DIVERSITY
Eighty-six species and 35 genera of orchid were reg-
istered in the ravines and surrounding areas
(Table 2), equivalent to 26.2% of the species regis-
tered in the region of Soconusco and 11.2% of the
orchids found in the state of Chiapas. Of these, 12
species could only be identified to genus and there
were 15 clearly distinct species without flowers that
could not be identified and were assigned to morphos-
pecies so as to be included in the analysis.
The locality with the greatest species richness was
BJ with 56 species (65.8%) in 29 genera, followed by AC
with 40 species (47%) in 17 genera, and CH with 26
species (30.5%) in 13 genera. In general, orchid species
richness in TMCF in the ravines was lower than in
the same ecosystem in the surrounding areas, and
also lower than the species richness in EMSF in the
ravines. There were eight orchid species exclusive to
EMSF in this study (a species of Coelia Lindl., Epiden-
drum parkinsonianum Hook., Macroclinium bicolor
(Lindl.) Dodson, Rhynchostele uroskinneri (Lindl.) Soto
Arenas & Salazar, Trichopilia tortilis Lindl. and three
morphospecies).
As explained previously, a direct statistical compari-
son of the orchid species diversity in the ravines and
the surrounding areas was not possible; instead, they
were compared numerically and by means of accumu-
lation curves. Including species, species identified to
genus and morphospecies, orchid species richness was
greater in the surrounding areas than in the ravines,
with 72 (75.5%) and 39 (48.8%) species, respectively.
However, of these, 33.5% (13) of the total number of
species found in ravines and 34.7% (25) of the total in
surrounding areas were observed only once. Consider-
ing the total number of species (including those iden-
tified to genus and morphospecies) registered in this
study, 14 species (16.2%) were exclusive to the ravines,
13 (92.9%) of which were single records. There were
47 species (54.6%) exclusive to the surrounding areas,
25 (53.2%) of which were single records. Finally, 25
species (29%) were found in both habitats. Of these,
Table 1. Characteristics of the transects sampled in the ravines in three localities in the Tacaná Volcano Biosphere
Reserve, south-eastern Mexico
Transect Orientation
Number
of species
Elevation
(m)
Depth
(m)
Slope
(deg) Vegetation
CH
t1 E–SE 3 2368 120 64–75 EMSF
t2 E–NE 3 2365 120 55–90 EMSF
t3 NE 5 2360 150 46–90 EMSF
t4 S–SE 2 2404 120 61–90 EMSF
t5 SW 1 2408 120 54–71 TMCF
t6 E–SE 0 2358 130 58–90 TMCF
BJ
t1 W–SW 2 1687 200 45–90 TMCF
t2 W–SW 0 1690 200 57–67 TMCF
t3 W–SW 1 1542 180 50–90 TMCF
t4 E–NE 6 1595 300 38–90 TMCF
t5 E–NE 11 1562 300 54–85 EMSF
t6 E–NE 13 1569 300 65–72 EMSF
AC
t1 E–NE 3 2095 100 64–75 TMCF
t2 W–SW 3 2121 90 70–90 TMCF
t3 E–NE 2 2173 150 48–59 TMCF
t4 W–SW 9 2156 150 40–90 TMCF
t5 E–SE 0 2119 120 60–70 TMCF
t6 E–SE 2 2105 150 60–90 TMCF
Shaded rows indicate transects facing west.
AC, Agua Caliente; BJ, Benito Juárez El Plan; CH, Chiquihuites; EMSF, Evergreen Mountain Scrub Forest; TMCF,
Tropical Mountain Cloud Forest.
RAVINES AS REFUGES FOR ORCHIDS IN MEXICO 5
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
Table 2. Inventory of orchid species registered in ravines and surrounding areas in three locations in the Tacaná Volcano
Biosphere Reserve, south-eastern Mexico
Orchid species
Habitat
Both
habitats
Type of vegetation
Rav Surr TMCF EMSF
Arpophyllum medium Rchb.f. + + +
Brassia verrucosa Lindl. + + +
Camaridium hagsaterianum (Soto Arenas) M.A.Blanco +++
Campylocentrum microphyllum Ames & Correll +++
Coelia sp. ++
Cuitlauzina candida (Lindl.) Dressler & N.H.Williams ++
Cyrtochiloides ochmatochila (Rchb.f.) N.H.Williams & M.W.Chase ++
Dichaea glauca (Sw.) Lindl. ++
Dichaea muricatoides Hamer & Garay +++
Dichaea suaveolens Kraenzl. +++
Dichaea sp. ++
Elleanthus cynarocephalus (Rchb.f.) Rchb. f. +++
Epidendrum alticola Ames & Correll ++
Epidendrum cnemidophorum Lindl. ++
Epidendrum eximium L.O.Williams ++
Epidendrum parkinsonianum Hook. ++
Epidendrum polychromum Hágsater ++
Epidendrum polyanthum Lindl. ++
Epidendrum ramosum Jacq. ++
Epidendrum verrucosum Sw. +++
Epidendrum clowesii Bateman ex Lindl. ++
Epidendrum trianthum Schltr. ++
Gongora cassidea Rchb.f. ++
Isochilus alatus Schltr. +++
Isochilus aurantiacus Hamer & Garay ++
Isochilus chiriquensis Schltr. ++
Jacquiniella cobanensis (Ames & Schltr.) Dressler +++
Lepanthes oreocharis Schltr. ++
Lockhartia verrucosa Lindl. ex Rchb.f. ++
Macroclinium bicolor (Lindl.) Dodson ++
Masdevallia tuerckheimii Ames ++
Maxillaria ringens Rchb.f. ++
Maxillaria sp. ++
Maxillaria sp.1 ++
Maxillaria sp.2 ++
Maxillariella houtteana (Rchb.f.) M.A.Blanco & Carnevali ++
Maxillariella variabilis (Bateman ex Lindl.) M.A.Blanco & Carnevali ++
Nemaconia striata (Lindl.) Van den Berg, Salazar & Soto Arenas ++
Oncidium aff. laeve (Lindl.) Beer ++
Oncidium suttonii Bateman ex Lindl. ++
Oncidium sp. ++
Platystele ovatilabia (Ames & C.Schweinf.) Garay ++
Platystele stenostachya (Rchb.f.) Garay ++
Pleurothallis leucantha Schltr. ++
Pleurothallis matudana C.Schweinf. ++
Pleurothallis nelsonii Ames ++
Pleurothallis sp. ++
Pleurothallis sp.1 ++
Prosthechea varicosa (Bateman ex Lindl.) W.E.Higgins +++
Restrepia trichoglossa F.Lehm. ex Sander ++
Rhynchostele bictoniensis (Bateman) Soto Arenas & Salazar +++
6A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
comparing the three localities CH, BJ and AC, of
the 26, 56 and 40 orchid species registered, six, 13
and four species were exclusive to the ravines, respec-
tively (Table 3). As shown in Figure 2, in this study,
there was a slight tendency towards greater orchid
species richness in the transects at lower elevation
(R2= 0.1611).
MOST FREQUENT SPECIES,THREATENED AND
ENDEMIC SPECIES,AND NEW RECORDS
Fifteen orchid species (17.4%) were recorded five
times, whereas the majority (71; 82.5%) were regis-
Table 2. Continued
Orchid species
Habitat
Both
habitats
Type of vegetation
Rav Surr TMCF EMSF
Rhynchostele cordata (Lindl.) Soto Arenas & Salazar ++
Rhynchostele stellata (Lindl.) Soto Arenas & Salazar ++
Rhynchostele uroskinneri (Lindl.) Soto Arenas & Salazar + +
Rossioglossum grande (Lindl.) Garay & G.C.Kenn. + +
Scelochilus tuerckheimii Schltr. + +
Sobralia macrantha Lindl. + + +
Specklinia segregatifolia (Ames & C.Schweinf.) Solano & Soto Arenas + +
Specklinia tribuloides (Sw.) Pridgeon & M.W.Chase + +
Specklinia sp. + +
Stanhopea graveolens Lindl. + + +
Stanhopea sp. ++
Stelis hymenantha Schltr. + + +
Stelis lamprophylla (Schltr.) Karremans + +
Stelis megachlamys (Schltr.) Pupulin + + +
Stelis ovatilabia Schltr. + +
Stelis tacanensis R.Solano & Soto Arenas +++
Stelis sp. ++
Trichocentrum bicallosum (Lindl.) M.W.Chase & N.H.Williams ++
Trichocentrum sp. ++
Trichopilia tortilis Lindl. ++
Morphospecies 1 ++
Morphospecies 2 ++
Morphospecies 3 ++
Morphospecies 4 +++
Morphospecies 5 ++
Morphospecies 6 ++
Morphospecies 7 ++
Morphospecies 8 ++
Morphospecies 9 ++
Morphospecies 10 +++
Morphospecies 11 ++
Morphospecies 12 ++
Morphospecies 13 +++
Morphospecies 14 ++
Morphospecies 15 ++
EMSF, Evergreen Mountain Scrub Forest; Rav, ravines; Surr, surrounding area; TMCF, Tropical Mountain Cloud Forest.
Table 3. Distribution of orchid species in ravines, sur-
rounding areas and both habitats in the Tacaná Volcano
Biosphere Reserve in south-eastern Mexico
Number of orchid
species present CH BJ AC
Ravines 6 13 4
Both habitats 6 12 11
Surrounding areas 14 31 25
Total 26 56 40
AC, Agua Caliente; BJ, Benito Juárez El Plan; CH, Chiqui-
huites.
RAVINES AS REFUGES FOR ORCHIDS IN MEXICO 7
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
tered only one to four times. Sobralia macrantha
Lindl., Dichaea suaveolens Kraenzl. and Stelis hyme-
nantha Schltr. were the most frequent orchid species
in the three localities in this study. However, previous
studies in the region as a whole have indicated that
even these species are relatively restricted in their
range. The frequent and flexible Stelis lamprophylla
(Schltr.) Karremans [previously Anathallis dolicho-
pus. (Schltr.) Pridgeon & M.W.Chase; Karremans,
2014] was the only species found in the surrounding
areas of all three localities studied, but this species
was absent from the ravines.
Of the 86 orchid species recorded, nine are consid-
ered to be threatened species [Cuitlauzina candida
(Lindl.) Dressler & N.H.Williams, Cyrtochiloides
ochmatochila (Rchb.f.) N.H.Williams & M.W.Chase,
Epidendrum alticola Ames & Correll, Epidendrum
cnemidophorum Lindl., Oncidium suttonii Bateman
ex Lindl., Pleurothallis nelsonii Ames, Restrepia tri-
choglossa F.Lehm. ex Sander, Rhynchostele cordata
(Lindl.) Soto Arenas & Salazar and Scelochilus tuerck-
heimii Schltr.] and two, Rhynchostele uroskinneri and
Rossioglossum grande (Lindl.) Garay & G.C.Kenn., are
in danger of extinction (SEMARNAT, 2010). Of these,
four were only observed once (C. ochmatochila,S. tuer-
ckheimii, R. uroskinneri and R. grande). Two of the
threatened species were found in the ravines; there
was one record of Oncidium suttonii in a ravine and
four in the surrounding areas, and the only register of
Rhynchostele uroskinneri was in the ravine habitat.
Epidendrum alticola and Stelis tacanensis R.Solano &
Soto Arenas are endemic to the region and were found
to be distributed in both ravines and surrounding
areas. The rest of the inventory consisted of many
species which, although not considered as threatened,
are naturally rare, infrequent or localized across their
entire geographical distribution, as is the case for
many Orchidaceae. We report the first records in the
region for Epidendrum clowesii Bateman ex Lindl.,
found in areas surrounding the ravines, and Epiden-
drum trianthum Schltr., found in ravines and the
surrounding areas.
The distribution of these threatened species between
the three localities did not follow the tendency shown
by the analysis of species richness in general, with two
threatened species in CH (Pleurothallis nelsonii and
Rhynchostele uroskinneri), three in BJ (Pleurothallis
nelsonii,Restrepia trichoglossa and Scelochilus tuer-
ckheimii) and five in AC (Cuitlauzina candida,Epi-
dendrum alticola,Rhynchostele cordata,Oncidium
suttonii and Rossioglossum grande). Of these species,
Pleurothallis nelsonii, although restricted in geo-
graphical range, is relatively abundant in the region
and shows resistance to habitat deterioration.
COMPARISON OF RENYI ENTROPY VALUES OF ORCHID
SPECIES IN RAVINES AND RAVINE TRANSECTS
Observed species richness (q= 0) was highest in ravine
2 at locality BJ, with transect 6 of this ravine, with the
EMSF ecosystem and facing east–north-east, having
the highest number of species (13). However, for the
parameter q= 1, weighted according to the propor-
tional abundance of each species, the highest value
(8.99) was for transect 5 of BJ ravine 2 (EMSF,
east–north-east) and transect 4 of AC ravine 2 (TMCF,
west–south-west). The highest values for q= 2 were
similar, although transect 4 of AC ravine 2 was placed
below transect 5 of BJ ravine 2 (Table 4a, b). The
lowest values for the observed species richness (q=0)
were found in CH transect 5 (TMCF; south-west) and
BJ transect 3 (TMCF; west–south-west) and were
supported by the q= 1 and q= 2 values (Table 4a, b).
In the ravines at localities CH and BJ, the most
species-rich transects were those facing east, but, at
locality AC, this situation was reversed. At the first
two localities, there was a tendency towards higher
orchid species richness in transects with the EMSF
ecosystem (in AC, there were no transects with
EMSF) (Table 4a, b). The slope of the ravines clearly
affected the distribution of the orchids, with the three
sample sites with the greatest species richness occur-
ring between 70° and 80°; there was, however, no
significant trend overall (R2= 0.0002).
ACCUMULATION CURVES
Analysis of the accumulation curves gave an estimate
of a total of 67–77, 129–145 and 131–144 orchid
species for ravines, surrounding areas and the com-
bination of both, respectively (Fig. 3A–C; Table 5);
this can be compared with the 86 species registered in
this study, 14 of which were exclusive to ravines, 47
y = -0.0046x + 12.9 85
R² = 0.1611
0
2
4
6
8
10
12
14
1400 1600 1800 2000 2200 2400 2600
Number of species
Elevation (m.a.s.l.)
Figure 2. Relationship between orchid species richness
and altitude, combining data taken from the ravines and
surrounding areas, in three localities in the Tacaná
Volcano Biosphere Reserve, south-eastern Mexico.
8A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
were exclusive to the surrounding area and 25 colo-
nized both areas. The estimation for the combination
of both habitats is similar to that of the surrounding
areas alone because of the large number of orchid
species that are shared and the much smaller number
of species found in the ravines (Table 2). However, in
the case of the combination of both habitats, the
estimation of the number of species includes less
variability (the interval is smaller), leading us to
conclude that the growth of the rarefaction curve is
maintained at an almost constant level.
Table 4. Renyi entropy analysis for orchids in ravines in
three locations in the Tacaná Volcano Biosphere Reserve,
south-eastern Mexico: a, ravines; b, transects of ravines
a. Ravines
Renyi entropy
q=0 q=1 q=2
CH 1 9 7.5836908 6.43
CH 2 3 3.0011634 3
BJ 1 3 2.829217 2.67
BJ 2 23 18.522755 14.29
AC 1 5 4.3710358 3.77
AC 2 10 7.322853 5
AC 3 2 1.8908 1.8
b. Transects
CH
1 EMSF 3 2.829217 2.67
2 EMSF 3 2.829217 2.67
3 EMSF 5 4.7114702 4.46
4 EMSF 2 1.9997057 2
5111
BJ
1 2 1.9997057 2
3111
4 6 5.743105 5.44
5 EMSF 11 8.997979 7.05
6 EMSF 13 12.3419 11.64
AC
1 3 2.829217 2.67
2 3 3.0011634 3
3 2 1.5698813 1.38
4 9 8.997979 9
6 2 1.8908 1.8
Shaded lines indicates transects facing west.
EMSF, Evergreen Mountain Scrub Forest [all others are
Tropical Mountain Cloud Forest (TMCF)]. Locality: AC,
Agua Caliente; BJ, Benito Juárez El Plan; CH, Chiquihu-
ites. There were no orchids recorded in transects CH 5, BJ
2 and AC 5.
q= 0, species richness; q= 1, exponential of the Shannon
index; q= 2, inverse of the Simpson index.
Figure 3. A–C, Accumulation curves for orchid species
registered in ravines (A), ravines and surrounding areas
(B) and surrounding areas (C), considering three localities
in the Tacaná Volcano Biosphere Reserve, south-eastern
México.
RAVINES AS REFUGES FOR ORCHIDS IN MEXICO 9
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
ANALYSIS OF THE PROPORTION OF THE STUDY AREA
PRESENT IN THE FORM OF RAVINES
A total of 1825.21 ha, equivalent to 7.68% of the area
analysed (Fig. 4), was found to consist of ravines with
slopes with a gradient of greater than 45°.
GROWTH HABIT AND SUBSTRATES
Most of the orchid species registered were epiphytes
(69; 80.2%), a few were lithophytes (six; 6.9%) and
only two species (2.3%) were terrestrial. There were
nine species (10.4%) with an indistinct life form. Most
of the orchid species were epiphytes found on trunks
and branches of trees and shrubs, or were generalists
and capable of colonizing a variety of substrates
or microhabitats. We observed fewer trunks and
branches available for colonization in the ravines, and
the analysis showed that there were two microhabi-
tats unique to the ravines: rocks covered in vegetation
and bare rocks (Fig. 5). Four orchid species, with
generalist behaviour, were found growing in these two
unique microhabitats: Dichaea suaveolens and Pros-
thechea varicosa (Bateman ex Lindl.) W.E.Higgins on
rocks with vegetation, and Epidendrum clowesii and
Sobralia macrantha on bare rocks, but, of these, only
E. clowesii could be considered rare in the region.
DISCUSSION
In the selected sites in the Tacaná Volcano Biosphere
Reserve, we found 11.4% of the approximately 750
species of orchid that inhabit the TMCF ecosystem in
Mexico (Espejo et al., 2005; Hágsater et al., 2005).
The ravines were situated at varying elevations
offering different microclimates (Halffter & Pineda,
2005) and, in general, ravine vegetation offered fewer
branches and trunks for colonization than the sur-
rounding areas, as the slope and more extreme envi-
ronmental conditions may be less conducive to the
establishment of trees and, in ravines, tree growth
may be further affected by the thin soils, slopes and
winds (Luna et al., 2001). Two substrates or micro-
habitats were only present in ravines, which,
however, were mainly colonized by common generalist
orchid species. It should be stressed that small and
scattered populations are characteristic of many
orchid species (Koopowitz, 2001) and should not nec-
essarily be interpreted as a conservation problem,
although this poses difficulties for objective analysis
of orchid frequency and diversity. For this reason, the
39 orchid species only observed once in this study
were not removed from the database. Furthermore,
heterogeneity was notable between the different
localities and between transects of the same ravines,
which also causes problems for objective and statis-
tical analysis, and highlights the need for extensive
surveys and conservation efforts to guarantee repre-
sentativeness.
We found 86 species, 14 of which were exclusive to
ravines, 47 to the surrounding area and 25 colonized
both areas. According to the Laplace method applied
Table 5. Approximate accumulation curves of the Laplace model for the estimation of orchid species present in ravines,
surrounding areas and a combination of ravines and surrounding areas in three locations in the Tacaná Volcano
Biosphere Reserve, south-eastern Mexico. S, estimated number of species; Aand B, estimated parameters of the model
Parameters Estimate
Standard
error tvalue Pr[T>t]
Combined: ravines and surrounding areas
S137.23567 3.28586 41.89 2.0e-16*
A2.31987 0.05729 40.50 2.0e-16*
B1.40613 0.06939 –20.27 1.01e-15*
95% confidence interval for number of species: 130.8291, 144.458
Ravines
S72.19296 2.43472 29.65 1.35e-12*
A2.21051 0.06179 35.77 1.45e-13*
B1.28457 0.07076 −18.16 4.30e-10*
95% confidence interval for number of species: 66.888, 77.497
Surrounding areas
S137.2356 3.40707 40.28 1.51e-09*
A1.83448 0.0432 42.47 1.51e-09*
B0.94395 0.0453 –20.83 1.48e-07*
95% confidence interval for number of species: (129.1792, 145.2921)
*Parameters highly significant (0).
The tvalues are Wald statistics to test the significance of the estimated parameters of the adjusted model.
10 A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
in this study, by extending the survey, we could expect
to find a further 53–63 species that exclusively colo-
nized ravines, 82–98 more species that exclusively
colonized the surrounding areas and 106–119 more
species that colonized both conditions. This analysis
highlights the limitations of our study, but also the
potential of the ravines as a refuge for orchids.
Despite the limitations and implicit difficulty in the
study of ravine vegetation, our 18 ravine transects
and general surveys of surrounding areas could be
considered as a limited, but representative, sample of
the TMCF ecosystem in the region.
Rhynchostele uroskinneri is almost extinct in
Mexico, as a result of deforestation, unsustainable
exploitation and restricted habitat preference, and, in
this study, one individual was found in a ravine. The
colonization of difficult to access areas could be impor-
tant for the protection of R. uroskinneri, as the other
few sites recorded for this species are all relatively
easily accessed and the species has been collected to
near extinction. Other threatened species, Epiden-
drum alticola and Oncidium suttonii, were also found
in the ravines, as well as in the surrounding areas;
however, in total, more threatened species were found
Figure 4. Distribution and percentage surface area of slopes in the Tacaná Volcano Biosphere Reserve, south-eastern
Mexico.
RAVINES AS REFUGES FOR ORCHIDS IN MEXICO 11
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
in the surrounding areas (Cyrtochiloides ochma-
tochila,Epidendrum cnemidophorum,Pleurothallis
nelsonii,Rhynchostele cordata,Rossioglossum grande
and Scelochilus tuerckheimii) than in the ravines.
There were nine common and widely distributed
orchid species, seven of which have been reported in
other types of vegetation in the Sierra Madre of
Chiapas (Long & Heath, 1991; Martínez-Meléndez
et al., 2008; Provisional Management Plan for the
Volcán Tacaná Biosphere Reserve, 2008, unpubl.
data), but were, however, only found in the ravines in
this study. All but one of these were only found in
EMSF, indicating the importance of this ecosystem,
which, in the study zone, is only found in the ravines.
The greater species richness of orchids in the sur-
rounding areas could simply be a result of the greater
sampling intensity as compared with the ravines, but
the greater availability of trunks and branches to
colonize could also be a factor. The scarcity of terres-
trial orchids in our data could be explained by the
instability of the ‘soils’ in the ravines, human impact
in the surrounding areas and the ephemeral nature of
above-ground structures.
In the case of EMSF, only present in the ravines,
the structural characteristics of this ecosystem offer a
distinct advantage because of the greater protection
from the sun, retention of humidity and retention of
organic matter as a result of the low, dense, contorted
and tangled branches. Gómez (2010) made a similar
observation relating to studies in Cerro El Triunfo
and Tres Picos, also situated in the Sierra Madre of
Chiapas, and also noted the relatively lower tempera-
tures in the EMSF cloud forest ecosystem.
In this study, elevation had a limited effect on the
orchid species richness observed in the ravines and
surrounding areas. A more pronounced effect has been
reported in other studies in Mexico; for example,
Ceja-Romero et al. (2010) found the greatest concen-
tration of species at elevations between 1250 and
2250 m, and Wolf & Flamenco (2003) recorded most
species between 500 and 2000 m. It has been reported
that the temperature descends 0.56 °C per 100 m
increase in elevation and, above a certain elevation,
which varies with latitude, no trees are found. Simi-
larly, precipitation declines above 2000 m (JICA,
1999), producing not only a cooler but also a drier
climate, which is less conducive to orchid develop-
ment. Therefore, ravines at lower elevations may
have greater impact and relevance as refuges for the
conservation of orchids.
In temperate zones, such as mountains, orientation
is an important factor determining the structure of
plant communities (Killeen, Louman & Grimwood,
1990), particularly the development and persistence of
the TMCF ecosystem (Luna et al., 2001). In this study,
ravines oriented towards the east, which received
sunlight in the morning, tended to have greater species
richness. Ravines oriented towards the west received
sunlight in the afternoon, which was frequently inter-
rupted by the thick clouds present at that time.
The slopes of the sampling sites of each transect
were varied and could not be compared statistically,
but observation suggested that slope could be an
important factor. The slope of a ravine affects the
retention of material precipitated from above, derived
from both within and in the surrounding area of the
ravine and, in the case of the EMSF ecosystem, the
compact, dense, tangled structure permits the reten-
tion of a greater proportion of this material than the
more open structure of the TMCF. In the study sites,
ravines with slopes >50° had terraces on which abun-
dant organic material collected, potentially forming an
ideal habitat for terrestrial and lithophytic orchids.
Nonetheless, these ‘soils’ are prone to collapse caused
by rain, wind or run-off, which may explain the unex-
pectedly few terrestrial orchid species.
Despite the difficulties implicit in working in the
ravines, and the fact that only one or a few individuals
were found of most of the species, and also the hetero-
geneity at all levels, especially between the three
localities and within the TMCF, we can say that, in the
study zone, we found a representative sample of
orchids, amounting to 25.9% of the species recorded for
Soconusco (Damon, 2013). It is important to mention
that an inventory is never completed (Jiménez-
Valverde & Hortal, 2003), and the total number of
species depends on the scale of the survey in space
5
1
7
11
8
5
11
5
002
16
37
2
10
0
5
10
15
20
25
30
35
40
Terr Rb Rv Rw Tr Br Tw Gn
Number of Species
Guilds
Rav
Surr
Figure 5. Number of orchid species per guild, defined as
substrate type, comparing ravines with the surrounding
areas, in three localities in the Tacaná Volcano Biosphere
Reserve, south-eastern Mexico. Rav, ravines; Surr, sur-
rounding areas. Guilds: Terr, terrestrial; Rb, bare rocks
(rocks without vegetation); Rv, rocks with vegetation; Rw,
rocks with water; Tr, trunks of trees or bushes; Br,
branches of trees or bushes; Tw, twigs; Gn, generalists.
12 A. DAMON ET AL.
© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, ••, ••–••
and time. The analysis of accumulation curves was,
however, a useful tool for comparing sampling effort,
predicting the number of species present in the study
areas and comparing the ravine habitat as a potential
refuge for orchids (Halffter, Moreno & Pineda, 2001).
The analysis of the proportion of the study area
present in the form of ravines indicates that there is a
substantial opportunity for a variety of orchids to grow
and develop in these areas, inaccessible to the vast
majority of the human population.
We propose that ravines in cloud forest ecosystems
should be included in conservation strategies for
orchids, as sites inaccessible to the vast majority of the
human population and which offer a variety of sub-
strates and microhabitats. Ravines at intermediate
elevations, facing east and with EMSF may be particu-
larly valuable as refuges for a variety of orchid species
in the Soconusco region of south-eastern Mexico.
ACKNOWLEDGEMENTS
We thank the specialists Víctor Velasco López and
Luis Reyes Zarate for training us in rappel tech-
niques and for accompanying and guiding us through-
out this study. We are grateful to Nelson Pérez Miguel
and the inhabitants of the localities selected for study
for the long hours dedicated to helping us with the
fieldwork. Anne Damon was granted permission by
the officials of the Tacaná Volcano Biosphere Reserve
to carry out the study within the reserve, and Carlos
Almeida-Cerino received a grant for MSc studies from
the Mexican ‘Consejo Nacional de Ciencia y Tec-
nología’ (CONACYT).
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