Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

Diversity patterns of vascular and non-vascular epiphytes

along tropical dry forest

Edier Soto Medina1*; https://orcid.org/0000-0002-1518-4805

Catalina Montoya2; https://orcid.org/0000-0002-1038-5595

Alejandro Castaño3; https://orcid.org/0000-0002-4164-748X

Jonathan Granobles3; https://orcid.org/0000-0001-8572-446X

1. Grupo de Ecología Vegetal, Universidad del Valle, Cali, Colombia; ediersot@gmail.com (*Correspondence)

2. Universidad de Antioquia, Medellín, Colombia; catalina.montoyam@udea.edu.co

3. Grupo de Biodiversidad Neotropical, Instituto para la Investigación y la Preservación del Patrimonio Cultural y

Natural del Valle del Cauca-INCIVA, Cali, Colombia; alecastulua@gmail.com, jnathanoblesc@gmail.com

Received 17-I-2023. Corrected 08-VI-2023. Accepted 12-X-2023.

ABSTRACT

Introduction: Epiphytes (vascular and non-vascular) are one of the most diverse groups in the Neotropics, but

despite their importance in the functioning of many ecosystems, much of their taxonomy and ecology is still

unknown in the dry forest of Colombia.

Objective: To compare the diversity patterns and species composition of vascular and non-vascular epiphytes

along tropical dry forest remnants of Cauca Valley, Colombia.

Methods: Ten permanent plots (50 x 20 m2) were established in tropical dry forest remnants. The epiphytes were

sampled in 40-50 trees per plot. Alpha and gamma diversity were calculated using the richness (q0) and Shannon

index (q1) (alpha was estimated as the average for phorophytes). Beta diversity was measured using the Whitaker

index. To evaluate the relationship between diversities and environmental variables, GLM analysis was used.

Results: We found 50 morphospecies of vascular epiphytes, 77 of bryophytes and 290 of lichens. The 𝛼 and 𝛾

diversity of bryophytes from each remnant was significantly explained by temperature. The abundance of lichens

per tree was significantly related with the DBH and tree height of each remnant. The 𝛼 diversity of vascular epi-

phytes shown can be explained by temperature and precipitation. The 𝛾 diversity was strongly influenced by the

beta diversity in bryophytes and lichens. This pattern is because the sites with high disturbance present a lower

diversity, as a consequence of a homogenizing effect, that is, a low turnover of species between sampling units.

Conclusions: Precipitation and temperature affected the diversity of bryophytes and vascular epiphytes, while

it did not show a relationship with the lichen’s diversity, for which there is not a high congruence between the

diversity and composition of these epiphytes.

Key words: lichens, corticolous, ecology, mosses, liverworts, TDF.

RESUMEN

Patrones de diversidad de epífitas vasculares y no vasculares a lo largo del bosque seco tropical

Introducción: Los epífitos (vasculares y no vasculares) son uno de los más diversos grupos de plantas en el

Neotrópico, pero a pesar de su importancia para el funcionamiento de varios ecosistemas, existen grandes vacíos

en su conocimiento taxonómico y ecológico en el bosque seco de Colombia.

Objetivo: Comparar los patrones de diversidad y composición de especies de epífitas vasculares y no vasculares

a lo largo de remanentes de bosque seco tropical del Valle del Cauca, Colombia.

https://doi.org/10.15517/rev.biol.trop..v71i1.53522

BOTANY & MYCOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

INTRODUCTION

Dry forests are ecosystems with a marked

seasonality, with dry periods interrupted by

rainy months. Formally, a tropical dry forest

(TDF) is defined as one with a closed canopy,

where the average annual precipitation is less

than 1 800 mm, with periods of three to six

months with precipitation of less than 100

mm per month, during which the vegetation

is deciduous (Gentry, 1995; Murphy & Lugo,

1986; Sánchez-Azofeifa et al., 2005). The topical

dry forest also encompasses taxonomic, compo-

sitional, and structural variations that depend

on climate, topography, and hydrogeography

(Ramos & Silverstone, 2018). As these ecosys-

tems normally occur in agriculturally fertile

areas, often large human populations have set-

tled there, exacerbating the pressures on these

forests, and drastically reducing their extension

to only 10 % of the original. In Colombia, dry

forest is the most threatened ecosystem, with

only 5 % of their original extension left (Ramos

& Silverstone, 2018).

The Colombian dry forest is restricted to

the inter-Andean valleys, the Caribbean region,

part of the plains and rivers. The floristic com-

position and physiognomy of TDF in Colombia

differs markedly between regions, with several

endemic species (Ramos & Silverstone, 2018).

However, dry forests in Colombia are being

destroyed at accelerated rates due to intensive

agriculture such as the cultivation of sugar-

cane, rice and soybeans and transformation

into pastures for cattle (Ramos & Silverstone,

2018). This destruction is very noticeable in

the region of the geographic valley of the Cauca

River, where the sugarcane cultivation and

cattle ranching reduced the dry forest to small

patches, with an estimated total extension of

less than 500 ha. These remnants are largely iso-

lated due to the persistence of the agricultural

lands (Ramos & Silverstone, 2018).

One of the most threatened floristic com-

ponents in the tropics are the epiphytes, plants

that use other plants as substrate without para-

sitizing the host and can be classified into

vascular and non-vascular epiphytes (algae,

bacteria, bryophytes, and lichens) (Mendieta-

Leiva, Porada et al., 2020). Despite the taxo-

nomic heterogeneity of the group, epiphytes

show ecological and functional similarities.

Epiphytes have important functions in ecosys-

tems ranging from the cycling of nutrients and

water to serving as food source for other organ-

isms (Benzing, 1992). The greatest diversity

of these plants occurs in the neotropics, with

cloud forests being one of the most diverse

habitats (Gentry, 1995; Soto et al., 2019). These

organisms depend on tree structure, climatic

factors, and other epiphytes for their establish-

ment (e.g., non-vascular epiphytes form litter

Métodos: Se establecieron diez parcelas permanentes (50 x 20 m2) en remanentes de bosque seco tropical. Las

epífitas se muestrearon en 40-50 árboles por parcela. La diversidad alfa y gamma se calculó utilizando la riqueza

(q0) y el índice de Shannon (q1) (alfa se estimó como el promedio para los forófitos). La diversidad beta se midió

utilizando el índice de Whitaker. Para evaluar la relación entre diversidades y variables ambientales se utilizó el

análisis GLM.

Resultados: Se encontraron 50 morfoespecies de epífitas vasculares, 77 de briófitas y 290 de líquenes. La diversi-

dad de 𝛼 y 𝛾 de briófitas de cada remanente fue explicada significativamente por la temperatura. La abundancia

de líquenes por árbol se relacionó significativamente con el DAP y la altura del árbol de cada remanente. La diver-

sidad 𝛼 de epífitas vasculares que se muestra puede explicarse por la temperatura y la precipitación. La diversidad

𝛾 estuvo fuertemente influenciada por la diversidad beta en briófitas y líquenes. Este patrón se debe a que los

sitios con alta perturbación presentan una menor diversidad, como consecuencia de un efecto homogeneizador,

es decir, un bajo recambio de especies entre unidades de muestreo.

Conclusiones: La precipitación y la temperatura afectaron la diversidad de briófitas y epífitas vasculares, mientras

que no mostró relación con la diversidad de líquenes, por lo que no existe una alta congruencia entre la diversidad

y composición de estas epífitas.

Palabras clave: líquenes, cortícolas, ecología, musgos, hepáticas, BST.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

that allows vascular establishment) (Gentry,

1995). Epiphytes also interact with each other

(vascular and non-vascular), with variations

according to the type of ecosystem, as in cloud

forests, where vascular and bryophytes are

dominant compared to lichens (Soto et al.,

2019; Wolf, 1993). However, there is no con-

sensus regarding the relationship between the

diversity of vascular and non-vascular epi-

phytes, showing patterns of positive, nega-

tive, or absent relationship (Affeld et al., 2008;

Bacaro et al., 2019). Currently, progress has

been made in the study of epiphytes, which has

allowed a better understanding of their ecol-

ogy, conservation, distribution, and large-scale

patterns, as well as standardizing sampling pro-

tocols (Wolf, 1993; Wolf et al., 2009). However,

due to both taxonomic and sampling complex-

ity of these groups, there are few studies that

include vascular and non-vascular epiphytes

(Affeld et al., 2008; Bacaro et al., 2019, Ramos &

Silverstone, 2018; Soto et al., 2015). Therefore,

there are still several gaps of knowledge about

the interaction and ecological dynamics of the

relationship between vascular and non-vascular

epiphytes (e.g., relationship between the diver-

sity of vascular vs. non-vascular epiphytes and

their responses to environmental gradients).

Currently, vascular epiphytes in the Neo-

tropics are of high interest due to their high

diversity, but not well known in ecology, bio-

geography and macroecology (Mendieta-Leiva,

Porada et al., 2020). However, it is known that

epiphytes are less diverse in dry ecosystems,

but little is known about their ecology (Gen-

try, 1995; Mendieta-Leiva, Ramos et al., 2020;

Werner & Gradstein, 2009). On the other hand,

non-vascular epiphytes show growing inter-

est, but are perhaps less well known in the

neotropics both taxonomically and ecologi-

cally (Benitez et al., 2019; Cornelissen & Steege,

1989). There are also very few ecological stud-

ies that integrate vascular and non-vascular

epiphytes, despite their obvious interaction

(Ramos & Silverstone, 2018; Soto et al., 2015).

Interest in the conservation of these plants

has increased, with greater representation in

management plans and conservation priorities.

Because of this, it is necessary to contribute to

the knowledge of these groups of organisms,

especially in poorly studied ecosystems, such as

the dry forest.

Bryophytes and lichens are organisms that

are an important part of the primary eco-

logical succession, as well as of the water cycle

through horizontal rainfall (Blum, 1973; Kap-

pen, 1973; Proctor, 1982). Furthermore, they

can be used as bioindicator organisms of pol-

lution and disturbance since they are poikilo-

hydrous, that is, their water content depends

on the environment (Conti & Cecchetti, 2001).

Non-vascular epiphytes strongly depend on

deterministic factors such as microclimate and

stochastic factors such as dispersal, already

showing changes in their community composi-

tion with small environmental changes. Simi-

larly, vascular epiphytes also depend on factors

such as climate, plant structure, characteristics

of the phorophyte and dispersal capacity. Due

to these similarities, vascular epiphytes have

been used as surrogates for establishing nature

reserves, identifying conservation priorities,

and for environmental planning (Ryti, 1992). In

the dry forests of Colombia, fauna and flora are

mainly used as priorities for conservation and

to establish guidelines for management plans,

under the principle that these groups are substi-

tutes for other groups of organisms. However,

there are studies that show that the relationship

between the diversity of vascular and non-vas-

cular epiphytes is not consistent, with positive

or negative relationships, for which there is not

a high congruence between these taxa (Bacaro

et al., 2019). Thus, understanding the relation-

ship between the diversity and composition

of vascular epiphytes, bryophytes and lichens

would help improve conservation strategies in

the Colombian dry forest.

The objective of this study was to compare

the diversity patterns and species composition

of vascular and non-vascular epiphytes along

tropical dry forest remnants. The hypothesis is

that vascular and non-vascular epiphytes will

show similar patterns of diversity with respect

to an environmental and disturbance gradient

of dry forest.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

MATERIALS AND METHODS

Study zone: Sampling was carried out in

the dry forest of Cauca Valley, a department

in the Southwestern part of Colombia. This

department ranges from the Pacific coast to

the central and western mountain ranges, with

elevations above 4 000 m. The dry forest of

the geographic Cauca valley is found along the

Cauca River, which is located between the two

aforementioned mountain ranges. Ten dry for-

est remnants (sites) were chosen as sampling

sites, mainly in the North-central part of Cauca

Valley: Chimbilaco (Yotoco), PNR El Vínculo

(Buga), Gitana (Riofrío), Higueroncito (Rolda-

nillo), PNR Mateguadua (Tuluá), El Medio

(Zarzal), Valenzuela (Tuluá), La Venta (Buga-

lagrande), Verdun (Andalucia) and El Volcán

(Yotoco) (Table 1). The ten localities present

dry forests in different states of conservation,

with an elevation range between 993-1 150 m

and precipitation between 1 057 and 1 593 mm.

Sampling: For vegetation sampling (forest

structure) plots of 50 x 20 m2 were established

and all the trees with a diameter at breast height

(DBH) > 2.5 cm were counted. For each tree

DBH, height and number of branches were

noted down. Phorophytes with a DBH > 20

cm were selected from the dominant species

of each locality. The phorophytes were at a dis-

tance > 10 m from the forest edges. The species

and number of vascular epiphyte individuals

were counted in three vertical strata (stratum 1:

from the base up to the first branching; stratum

2: between the first and second branching; stra-

tum 3: after the second branching) (Gradstein

et al., 2003). In total, 50 trees were selected for

each plot. One specimen of each species was

deposited in the TULV Herbarium.

For the sampling of non-vascular epiphytes,

three strata were established: base (between

0.5-1 m), trunk (between 1-2 m) and branches

(branches were collected from the upper parts)

(Gradstein et al., 2003). In each stratum, a 30 x

20 cm2 quadrant (divided into 1 cm2 cells) was

placed and the coverage of each non-vascular

species was estimated (Déleg et al., 2021). One

specimen of each species was deposited in the

TULV Herbarium. For more information on

the species found, consult Soto & Moncaleano

(2021). Additionally, Annual Mean Tempera-

ture (Bio 1), Annual Precipitation (Bio 12) and

Temperature seasonality (Bio 4) were estimated

for each forest remnant using the Worldclim

databases (Fick & Hijmans, 2017). Layers were

used at a resolution of 2.5 minutes and values

of the variables were extracted by site (ten for-

est remnants). Only these variables were used

because they were the ones with the highest

correlation between them (Pearson R > 0.7) and

variation among the remnants (since the study

sites are in the same geographical valley).

Statistical analysis: Initially, the abun-

dance of bryophytes and lichens was measured

Table 1

Location and climate data of the remnants of dry forest that were chosen as study sites.

Locality Elevation (m) Latitude Longitude Temperature (°C) Temperature

Seasonality Precipitation (mm)

Chimbilaco 1 092 3.935672 -76.356558 22.5 288 1 176

El Vinculo 1 150 3.836200 -76.296503 23.7 290 1 057

Gitana 1 122 4.166017 -76.333967 22.9 275 1 466

Higueroncito 993 4.497430 -76.109160 23.6 348 1 109

Mateguadua 1 150 4.027992 -76.159331 21.6 248 1 584

Medio 1 000 4.335278 -76.081111 23.9 335 1 239

Valenzuela 1 050 4.010607 -76.171244 21.6 287 1 372

La Venta 1 166 4.198944 -76.065611 23.1 280 1 465

Verdun 1 056 4.215492 -75.996389 22.2 314 1 593

Volcán 1 100 4.021400 -76.362817 22.2 263 1 260

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

as the cover (cm2) per sampled quadrant, while

the abundance of vascular plants was measured

as the number of individuals. Alpha diversity

of epiphytes was evaluated by the number of

species (Hill number q0) and Shannon diver-

sity indices (Hill number q1) per sampling

unit (phorophyte) (Chao et al., 2014). Alpha

diversity per site was calculated as the average

of q0 and q1 of the phorophytes. Gamma diver-

sity was calculated as q0 (richness) and (q1)

(index Shannon’s diversity) for the entire rem-

nant (McCune & Grace, 2002) and beta diver-

sity as the Whitaker index for each remnant,

which considers the average alpha diversity and

gamma diversity of each site (Hammer et al.,

2001). In this way, an alpha (average between

phorophytes), gamma (Hill number) and beta

diversity value was obtained for each remnant.

These indices were calculated with the PAST

2.0 ® software (Hammer et al., 2001).

General Linear Models (GLM) were per-

formed to evaluate the relationship between

abundance, alpha, beta and gamma diversities,

and the environmental variables (temperature,

precipitation, and Temperature seasonality,

abundance, diversity, DBH and tree height).

Previously, Spearman’s correlation analysis

(between the predictor variables) was per-

formed to select variables with high correlation

(R > 0.7) and avoid collinearity. These analyzes

were also made between the alpha, beta, and

gamma diversities. The variables followed a

normal distribution (Shapiro Wilk: P > 0.05).

Statistical analyzes were conducted with the

software STATISTICA® 7.0 (StatSoft, 2004).

To evaluate the relationship between the

remnants based on their epiphyte composition

(similarity), a multidimensional non-metric

scaling (NMDS) was performed. The Bray-

Curtis similarity index was used to make the

NMDS (McCune & Grace, 2002). To evaluate

the relationship between environmental vari-

ables and epiphyte composition, a Spearman

correlation was performed between the NMDS

axes and environmental variables. These analy-

ses were conducted with the PAST 2.0 ® soft-

ware (Hammer et al., 2001).

The 10 remnants were also grouped

according to whether they had a conservation

status assigned (natural reserve or a similar

status) or not (Remnants on farms or without

protection), to establish differences in alpha,

beta, and gamma diversities of the epiphytes.

For this purpose, t-tests were used to compare

the remnants with a conservation status vs. no

conservation in terms of diversity and abun-

dance of epiphytes. Alpha and gamma diversi-

ties were compared between remnants using

t-tests (Hammer et al., 2001).

RESULTS

There were 50 morphospecies of vascular

epiphytes, 77 of bryophytes and 290 of lichens.

The most abundant lichen species were Crypto-

thecia striata (15 743 cm2), Coenogonium mag-

dalenae (11 887 cm2), Porina imitatrix (10 229

cm2) and Zwackhia viridis (Ach.) Poetsch &

Schied (8 451 cm2), while Emmanuellia tenuis,

Bacidia sp.2, Bulbothrix isidiza, Byssoloma

leucoblepharum, Herpothallon confluenticum,

Hyperphyscia minor, Lopezaria sp., Physcia sp.,

Porina sp., Lichen sp. and Usnea sp. had 1 cm2.

The most frequent species in the ten remnants

were Coenogonium linkii (9 remnants), Herpo-

thallon rubrocinctum, Diorygma australasicum

(Elix) Lücking et al., Herpothallon roseocinc-

tum, Zwackhia viridis, Porina imitatrix, Coe-

nogonium magdalenae and Cryptothecia striata

(8 remnants), while 175 species were very rare

(singletons: occurred in only 1 remnant).

For bryophytes, Lejeunea sp., Radula pal-

lens, Helicodontium capillare, Schiffnerolejeunea

polycarpa and Lejeunea subsessilis Spruce were

most abundant (13 074, 4 755, 3 488, 3 313 and

3 230 cm2, respectively), whereas Plagiochila

deflexirama, Bryophyte sp. and Leskeadelphus

angustatus, were the least abundant (5, 3 and

3 cm2, respectively). The most frequent spe-

cies were Sematophyllum subpinnatum (Brid.)

E.Britton, Neckeropsis undulata, Frullania eri-

coides (Mart.) Mont., Radula tectiloba and Fru-

lania sp.2., occurring between in 5-6 remnants,

while 10 were rare (doubletons: occurred in 2

remnants) and 55 species (71 %) were very rare.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

The most abundant species among the

vascular epiphytes were Tillandsia recurvata

(2 221 individuals), Pleopeltis astrolepis (160),

Tillandsia usneoides (159) and Tillandsia juncea

(115). The most frequent species were Monstera

adansoni (8 remnants), Tillandsia recurvata

(7 remnants), Tillandsia juncea (6 remnants),

Philodendron barrosoanum and Tillandsia elon-

gata (5 remnants), while 34 species were only

present in one remnant.

Diversity 𝛼, β and 𝛾 in dry forest rem-

nants: The remnants with the highest bryo-

phyte gamma diversity (q0) were Mateguadua

(24 species) and Verdun (23 species), while El

Vínculo was the place with the lowest diversity

(six species). In terms of q1, Verdun was the site

with the highest diversity, while the Medio had

the lowest bryophyte diversity. Alpha diversity

was highest in Mateguadua and lowest in Vín-

culo (Table 2). Verdun was the remnant with

the highest beta diversity, while Vínculo had

the least beta diversity. The abundance of bryo-

phytes was highest in the Gitana and lowest in

the Volcan.

Regarding lichens, it was found that

Higueroncito was the place with the greatest

diversity 𝛾, while Chimbilaco was the one with

Table 2

Diversity 𝛼, β and 𝛾 for epiphytes (bryophytes, lichens and vascular) in ten dry forest remnants.

Epiphyte Locality β𝛼 𝛾

Abundance/tree Richness q1 Total abundance Richness q1

Bryophytes Chimbilaco 4.47 427.36 2.83 2.34 10 043 10 4.31

El Vinculo 4 360.51 2.20 2.08 6 309 6 3.82

Gitana 4.35 484.00 2.87 2.41 11 132 10 3.22

Higueroncito 8.93 205.83 2.51 2.20 4 837 15 5.10

Mateguadua 7.64 397.00 3.78 2.69 7 146 24 8.08

Medio 6.15 407.46 2.54 2.18 5 297 11 2.53

Valenzuela 8.21 395.88 3.06 2.51 6 334 19 7.54

Venta 5.25 364.36 3.08 2.48 9 109 13 5.10

Verdun 9.36 477.71 3.22 2.46 9 793 23 11.25

Volcán 5.6 169.91 2.82 2.39 1 869 12 6.82

Lichens Chimbilaco 6.6 231.12 3.54 2.27 11 831 28 11.59

El Vinculo 5.91 474.70 4.34 2.48 24 000 31 16.28

Gitana 8.36 254.98 5.02 2.64 11 474 47 12.55

Higueroncito 10.39 312.21 6.94 3.29 14 986 80 28.50

Mateguadua 8.33 327.29 7.07 3.60 13 746 66 16.95

Medio 9.48 313.92 4.49 2.03 11 615 47 13.33

Valenzuela 9.27 571.06 6.43 3.42 26 840 66 23.34

Venta 9.43 349.96 6.52 3.19 17 498 68 21.33

Verdun 11.01 400.63 6.16 2.86 19 631 74 21.33

Volcán 8.06 590.74 6.40 3.22 20 676 58 16.95

Vascular Chimbilaco 3.75 18.21 2.47 3.13 173 7 2.20

El Vinculo 1.77 123.50 2.08 1.08 741 3 2.01

Gitana 3.67 3.50 2.42 3.67 21 6 2.27

Higueroncito 1.76 49.29 2.45 1.43 764 4 2.23

Mateguadua 4.5 14.53 3.00 7.24 109 11 2.56

Medio 6.12 21.00 2.55 2.56 231 11 2.23

Valenzuela 79.60 2.25 4.39 96 11 2.16

Venta 6.6 31.53 2.58 2.66 599 13 2.25

Verdun 6.58 24.61 3.64 5.16 443 20 2.77

Volcán 2.08 7.60 2.30 2.34 38 4 2.10

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

the least diversity. Regarding the diversity 𝛼,

Mateguadua was the remnant that showed the

highest values, while the Medio presented the

lowest q1 and Chimbilaco the lowest q0. Diver-

sity β was highest in Verdun, while Vínculo

showed the lowest values. The abundance of

lichens was highest in Valenzuela (total abun-

dance) and El Volcan (average abundance).

Vascular epiphytes presented a higher

diversity 𝛾 in Verdun, while it was lower in

Vínculo. Diversity 𝛼 was highest in Verdun

(average richness) and Mateguadua (average

q1), while it was lowest in Vínculo. Regarding

β diversity, the Valenzuela remnant was the one

that showed the greatest diversity, while the

Vinculo had the lowest values (Table 2). The

abundance of vascular epiphytes was highest in

Higueroncito (total abundance) and El Vínculo

(average abundance per tree), in contrast, La

Gitana was the site with the lowest total and

average abundance.

Diversities 𝛼, β, and 𝛾 and environmental

variables: The gamma diversity of epiphytic

bryophytes from each remnant was signifi-

cantly explained by alpha and beta diversities

(Table 3). The diversities 𝛼 and 𝛾 were related

with temperature and precipitation, indicat-

ing that the sites with the highest precipitation

and lowest temperature tended to present the

highest diversity of corticolous bryophytes. The

average DBH was significant to the 𝛼 diversity,

suggesting that the sites with the largest trees

tended to present the highest diversity of bryo-

phytes per tree.

The diversity 𝛾 of corticolous lichens was

explained by 𝛼 and β diversities. The abun-

dance of lichens per tree was significantly

related with the DBH and tree height of each

remnant (Table 4). Alpha diversity was affected

by temperature.

The alpha diversity of vascular epiphytes

was explained by temperature with precipita-

tion (Table 5). Gamma diversity was related to

precipitation. Gamma diversity was explained

only by alpha diversity. The total abundance of

vascular epiphytes per tree showed a negative

relationship with the DBH.

When comparing the diversity among the

remnants with some figure of conservation vs.

without conservation, it was observed that the

richness and diversity of trees was greater for

these last (Table 6). Regarding the epiphytes,

no significant differences were found for the

diversities 𝛼, β and 𝛾.

Composition of epiphytes: The NMDS

for vascular epiphytes, lichens, and bryophytes,

Table 3

GLM between diversity and environmental variables for epiphytic bryophytes. Significant Chi- Square are in bold.

Gamma Temperature Precipitation q1 trees DBH Height (m)

Abundance/tree 0.21 3.39 0.00 0.38 2.38

Abundance 0.08 3.19 3.27 1.95 2.39

Gamma 8.93 0.19 0.04 1.99 0.00

Alfa 6.14 12.62 10.96 3.09 1.31 1.01

Beta 4.59 1.33 0.34 0.08 0.06 1.18

Table 4

GLM between diversity and environmental variables for epiphytic lichens. Significant Chi- Square are in bold.

Gamma Temperature Precipitation q1 trees DBH Height (m)

Abundance/tree 3.82 1.34 1.68 20.74 4.82

Abundance 0.60 1.50 4.67 1.15 0.12

Gamma 0.11 0.00 0.06 0.07 0.76

Alfa 0.026 4.21 0.06 0.00 0.13 0.01

Beta 0.018 0.04 3.49 0.03 1.79 0.30

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

showed different clustering patterns related to

the different environmental variables evaluated

(Fig. 1). The bryophytes were grouped accord-

ing to precipitation and temperature, with a

group formed by Chimbilaco, El Medio and El

Vínculo, and another by Volcán, Venta, Mateg-

uadua and Valenzuela. Regarding lichens, the

grouping patterns were related to the coordi-

nates (latitude and longitude), and the param-

eters related to the vegetation. The NMDS of

Table 5

GLM between diversity and environmental variables for vascular epiphytes. Significant Chi- Square are in bold.

Gamma Temperature Precipitation q1 trees DBH Height (m)

Abundance/tree 3.82 1.34 1.68 20.74 4.82

Abundance 4.71 0.01 0.02 4.65 2.22

Gamma 1.80 7.74 0.61 1.42 0.30

Alfa 0.14 9.76 10.17 0.20 1.93 2.13

Beta 0.015 1.03 4.36 0.64 3.10 7.59

Table 6

Comparison of diversity 𝛼, β and 𝛾 between remnants of dry forest with Conservation vs. without Conservation.

Without Conservation Conservation Tgl p

Bio4 294.67 290.00 0.22 8.00 0.83

Temperature 227.50 227.00 0.09 8.00 0.93

Precipitation 1 344.83 1 313.00 0.24 8.00 0.81

Richness trees 21.00 34.50 -2.91 8.00 0.02

Abundance trees 324.00 564.75 -0.83 8.00 0.43

D tres 0.37 0.11 1.77 8.00 0.12

H trees 1.72 2.74 -2.37 8.00 0.05

DBH 21.39 20.94 0.10 8.00 0.92

Height 7.91 7.60 0.17 8.00 0.87

Vascular β 4.07 4.85 -0.55 8.00 0.60

Abundance/tree 22.46 42.16 -0.85 8.00 0.42

𝛼 q0 2.64 2.47 0.58 8.00 0.58

𝛼 q1 1.04 1.12 -0.20 8.00 0.85

Abundance total 339.67 294.25 0.23 8.00 0.82

𝛾 q0 8.83 8.75 0.02 8.00 0.98

𝛾 q1 0.83 0.80 0.48 8.00 0.64

Bryophytes β 6.33 6.50 -0.13 8.00 0.90

Abundance/tree 354.86 390.21 -0.50 8.00 0.63

𝛼 q0 2.89 2.89 -0.02 8.00 0.98

𝛼 q1 0.87 0.85 0.22 8.00 0.83

Abundance total 7797.17 6271.50 0.81 8.00 0.44

𝛾 q0 13.83 15.00 -0.29 8.00 0.78

𝛾 q1 1.70 1.59 0.36 8.00 0.73

Lichens β 8.97 8.25 0.69 8.00 0.51

Abundance/tree 22.46 42.16 -0.85 8.00 0.42

𝛼 q0 5.76 5.58 0.22 8.00 0.83

𝛼 q1 1.06 1.03 0.22 8.00 0.83

Abundance total 16 016.00 19 050.25 -0.85 8.00 0.42

𝛾 q0 59.17 52.50 0.56 8.00 0.59

𝛾 q1 2.88 2.84 0.21 8.00 0.84

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

Fig. 1. NMDS epiphytes from TDF Valle del Cauca. A. vascular, B. bryophytes and C. lichens.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

vascular epiphytes showed that temperature,

temperature seasonality and precipitation were

the variables associated with the grouping pat-

terns of the remnants, with Chimbilaco, Venta,

Higueroncito, El Vínculo forming a group and

Valenzuela, Volcán, Gitana and Mateguadua

the other.

DISCUSSION

This study is the first to explore the epi-

phyte diversity in the dry forest of the geo-

graphic valley of the Cauca River. The diversity

of vascular epiphytes was low compared to other

tropical ecosystems (Mendieta-Leiva, Porada et

al., 2020), which may be since the conditions

of high temperature and low rainfall nega-

tively impacted the abundance and richness

of these organisms (Gentry, 1992). Regarding

bryophytes, a low diversity was found com-

pared to the Andean life zones, but like other

dry forests in Colombia (García-Martínez &

Mercado-Gómez, 2017; Lombo-Sánchez &

Suarez-Contento, 2018; Ramírez-Morán et al.,

2016). Regarding lichenized fungi, high diver-

sity was observed compared to other dry forests

in Colombia (Lücking et al., 2019, Soto et al.,

2021). However, this diversity is still low com-

pared to the Andean zone and humid forests at

low elevations, which may be because the for-

ests have low precipitation and high tempera-

tures (Sipman, 1996; Soto et al., 2019).

The most frequent and abundant vascular

epiphyte species found in this study are com-

mon in the dry forest of the geographic valley

of the Cauca River, both in artificial and natural

ecosystems (Benzing et al., 1992). These species

were dominant in remnants with a plant struc-

ture with greater dominance than few species,

which suggests that these epiphytes are favored

by the disturbance.

The most abundant lichen species were

Cryptothecia striata, C. magdalenae, Porina imi-

tatrix and Zwackhia viridis. The most frequent

species in the ten remnants were Coenogonium

linkii, Herpothallon rubrocinctum, Diorygma

australasicum, H. roseocinctum, Z. viridis, Porina

imitatrix, Coenogonium magdalenae y C. striata,

while 175 species were very rare. Thus, the

most important species of lichens belong to

the Arthoniaceae, Coenogoniaceae, Porinaceae

and Lecanographaceae families, typical families

in open and disturbed ecosystems. It should be

noted that species of the Graphidaceae, Rama-

linaceae and Trypetheliaceae families were not

dominant, families that are considered the most

diverse in the Neotropics (Menezes et al., 2018).

On the other hand, there is a high presence of

rare to very rare species, which is a common

pattern in communities of lichenized fungi in

the Neotropics, since many species of lichens

have microclimate and microsite specialists

(Cáceres et al., 2007).

The abundance of bryophytes was highest

in the Gitana and lowest in the Volcan. The

greater abundance of bryophytes in La Gitana

may be since this site is a dry forest-premontane

transition, for which climatic conditions favor a

greater abundance and richness of bryophytes,

which are photophobic organisms (Glime,

2007; Proctor, 1999; Proctor & Tuba, 2002). In

contrast, Verdun was the site with the highest

diversity, although it was not the one with the

highest abundance and richness, which indi-

cates that it is the site with the greatest diversity

of bryophytes since the Shannon index corrects

the effects of abundances. In this way, it is pos-

sible that Verdun is a forest with a higher degree

of conservation even though it is immersed in

a cattle farm, since bryophytes are indicators of

habitat quality (Czerepko et al., 2021).

In contrast, it was found that Higueroncito

was the place with the greatest diversity 𝛾 of

corticolous lichens, while Chimbilaco was the

one with the least diversity. The β diversity was

highest in Verdun, while the Vinculo showed

the lowest values. The abundance of lichens

was highest in Valenzuela (total abundance)

and Volcán (average abundance). These results

differ from those of bryophytes because the

diversity of lichens is modulated by other fac-

tors. Higueroncito was one of the sites with

the highest temperature of the ten remnants,

in addition to a possible effect of a fog current,

which favors a high abundance and diver-

sity of lichens (Stanton, 2015). The sites with

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

the lowest rainfall tended to have the lowest

lichen diversity.

Vascular epiphytes presented greater diver-

sity 𝛼 and 𝛾 in Verdun, while it was lower in

Vínculo. Regarding β diversity, the Valenzuela

remnant was the one that showed the great-

est diversity, while the Vinculo had the lowest

values. The abundance of vascular epiphytes

was higher in Higueroncito (total abundance)

and Vínculo (average abundance per tree), in

contrast, La Gitana was the site with the lowest

total and average abundance. The greater diver-

sity of vascular epiphytes in Verdun may be due

to the fact that it is a site with premontane forest

characteristics, which are characterized by high

epiphytism (Gentry, 1992). On the other hand,

the Vínculo was a site with a low diversity and

high abundance of epiphytes, which suggests

that this site presents a high disturbance.

Regarding the diversity of epiphytic

bryophytes, 𝛾 diversity of each remnant was

significantly related with precipitation and

temperature. The diversity 𝛼 was explained

by temperature, indicating that the sites with

the highest precipitation and lowest tempera-

ture tended to present the highest diversity

of corticolous bryophytes. The foregoing is

in line with what was previously said that the

remnants with higher precipitation and lower

temperature tended to present the greatest

diversity and abundance of bryophytes (Grass

et al., 2015). Bryophytes are poikilohydrous

organisms since they do not have mechanisms

for regulating their water content. This condi-

tion makes them organisms with high water /

humidity requirements to maintain adequate

hydration and maintain biological processes

(Glime, 2007; Proctor, 1999; Proctor & Tuba,

2002). The average DBH was positively related

to the diversity 𝛼 and 𝛾, suggesting that the

sites with the largest trees tended to present the

greatest diversity of bryophytes. This may indi-

cate that the diversity of bryophytes is higher

in potentially more conserved sites (with larger

trees), since they are forests with favorable

climatic conditions for these organisms (Alva-

renga & Pôrto, 2007; Bates et al., 2005; Bisang

& Hedenäs, 2005; Czerepko et al., 2021). This

response is because bryophytes show particular

physiological and ecological aspects related to

tolerance to light (photophobic), habitat spe-

cialization and reproductive strategies, there-

fore an alteration of their habitat negatively

affects their diversity.

With respect to lichenized fungi, diver-

sity 𝛾 was only explained by 𝛼 and β diversi-

ties. The abundance of lichens per tree was

positively correlated with the abundance of

trees in each remnant. In lichens it has been

observed that the total diversity of a place is

strongly influenced by the exchange of species

among phorophytes (Cáceres et al., 2007; Lück-

ing, 1999). This pattern is since lichens have a

strong microclimate and microsite specializa-

tion, which is why a high presence of rare and

restricted species is observed.

In general terms, in bryophytes and lichens

𝛾 diversity was explained by 𝛼 and β diversi-

ties, but in vascular epiphytes it was only alpha

diversity. This pattern is because the sites that

have a high disturbance, present a lower diver-

sity, is usually due to a homogenizing effect, that

is, a low turnover of species between sampling

units (Ardila-Ríos et al., 2015). In this way,

even though a high diversity 𝛼 is conserved,

the diversity β falls and this is expressed in a

low diversity 𝛾; However, in vascular epiphytes,

alpha diversity was more important for the total

diversity of each site, which can be explained

by the fact that microenvironmental factors

are less important in modulating the diversity

of these epiphytes at a site (Soto-Medina et al.,

2015). On the other hand, precipitation and

temperature affected the diversity of bryophytes

and vascular epiphytes, while it did not show a

relationship with the lichen’s diversity. In this

way, the results show that there are contrasting

patterns between the two groups of epiphytes,

which is very important when making con-

servation decisions: e.g., using only vascu-

lar epiphytes to take conservation measures

could negatively affect epiphytic lichens. In this

sense, these results are an important basis for

establishing conservation strategies in tropical

dry forests.

Ethical statement: the authors declare

that they all agree with this publication and

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53522, enero-diciembre 2023 (Publicado Oct. 30, 2023)

made significant contributions; that there is

no conflict of interest of any kind; and that we

followed all pertinent ethical and legal proce-

dures and requirements. All financial sources

are fully and clearly stated in the acknowled-

gments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

To the Institute for Research and Preser-

vation of the Cultural and Natural Heritage of

Valle del Cauca” (INCIVA) (Colombia), with

the project “Dry Forest”.

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