Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
Lichen community structure and richness
in three mid-elevation secondary forests in Costa Rica
Roberto A. Cordero S.
*; https://orcid.org/0000-0001-7270-104X
Ana Garrido
; https://orcid.org/0000-0001-5343-5639
Junior Pastor Pérez-Molina
; https://orcid.org/0000-0002-3396-0599
Óscar Ramírez-Alán
†, 3
José Luis Chávez
; https://orcid.org/0000-0002-3441-6202
1. Laboratorio de Ecología Funcional y Ecosistemas Tropicales, Escuela de Ciencias Biológicas, Universidad Nacional
de Costa Rica, Heredia, Costa Rica; ticolamb@gmail.com, junior.perez.molina@una.ac.cr (Correspondence*)
2. Escuela de Ciencias Ambientales, Universidad Alcalá de Henares, Madrid, España; anagarridoquesada@hotmail.com
3. Escuela de Ciencias Biológicas, Universidad Nacional de Costa Rica, Heredia, Costa Rica.
4. Trabajador independiente. Tilarán, Costa Rica; jlchaves25@gmail.com
Received 10-III-2021. Corrected 19-V-2021. Accepted 02-VI-2021.
Introduction: Lichen diversity, community structure, composition and species abundance have been used as
indicators of the integrity and ecological continuity of tropical forest ecosystems. Objectives: To assess cortico-
lous lichen species composition, diversity, and ecological importance of three forested stands differing in time of
abandonment as indicators of how passive restoration influences the lichen community assemblage. Methods:
We surveyed individual lichens on tree stems of a reference old secondary forest and a young secondary forest
(50 and 14-year-old natural regeneration after pasture abandonment, respectively), and in a 35-year-old exotic
cypress tree plantation, in the oriental Central Valley, in Orosí, Costa Rica. Standard diversity, similarity indexes,
and the importance value index were calculated. An NMDS analysis was performed on the community structure
parameters and in a presence-absence matrix. Results: We found 64 lichen species in 25 families with 42, 21,
and 23 species, and 20, 10, and 15 families, in the young and old secondary forests, and the cypress plantation,
respectively. Cryptothecia sp. possessed the highest importance across sites. More than 87 % of the species are
rare. The combined IVI of the top three families were: 36, 48.5, and 74.8 % in the young and old forests and
the Cypress plantation sites, respectively. Overall, Arthoniaceae is in the top three families. The young forest
had the highest species richness, but the old forest presented the best evenness. Similarity and diversity indexes
suggest a particularly low resemblance in the lichen communities but a smooth gradient differentiation between
the three forests, which was confirmed by the NMDS test. The homogeneity test identified great differences in
ecological importance and composition. Conclusions: This region contains a distinctive assemblage of species
resulting in a strong community differentiation by site, reflecting the influence of ecophysiological and microcli-
matic factors that define lichen establishment and survival and suggesting a great regional beta diversity, within
a fragmented landscape. Greater connectivity and passive restoration strategies resulted in greater diversity and
a more heterogeneous community structure on both forests than the corticolous community of the abandoned
plantation. Protection of forest fragments will maximize the integrity of future forests.
Key words: cloud forest; community composition; corticolous lichens; Costa Rica; hemeroby; lichen diversity.
Cordero S., R.A., Garrido, A., Pérez-Molina, J.P., Ramírez-Alán,
O., & Chávez, J.L. (2021). Lichen community structure
and richness in three mid-elevation secondary forests in
Costa Rica. Revista de Biología Tropical, 69(2), 688-699.
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
Lichens have an important role at both
the ecological and economical levels. Among
their functions, they contribute to forest total
biomass and provide food and shelter to other
organisms (Galloway, 1992; Lehmkuhl, 2004).
Many lichens can fix atmospheric nitrogen
(Honegger, 1991), and they are common pri-
mary colonizers in almost every known eco-
system. Taken together, all these lichen traits
can guide us to think of a relationship between
increases in lichen diversity and biomass with
the increasing structural complexity of forests
(Crites & Dale, 1998; Berryman & McCune,
2006). More and more studies have focused
on the lichen ecology in tropical ecosystems
as model organisms for the study of diversity
patterns (Lücking, 1999a). Recently, Rivas-
Plata et al. (2008) have demonstrated how
lichens can be used as ecological indicators of
hemeroby across a series of life zones ranging
from lowland rain forests to montane forests
and from open to shaded microenvironments.
Given their epiphytic position, lichens are
indicators of habitat loss and ecosystem deg-
radation because they rely on the permanence
of their arboreal available substrates (Estrabou
et al., 2005). A recent paleotropical study
showed how lichen functional traits and tax-
onomy were useful to detect forest condition
(Thüs et al., 2021).
For the same token, given their extreme
ability to tolerate some extreme environmen-
tal conditions and their sensitivity to subtle
changes in their microenvironmental situa-
tions, lichens have been traditionally used for
biomonitoring atmospheric pollution around
the world based solely on growth or domi-
nance reduction (Monge-Nájera et al., 2002;
Bustamante et al., 2011). More detailed studies
use them coupled to bioindication techniques
based on lichen species reduction and its direct
relationship with some atmospheric pollutants
(Giordani, 2007; Cristofolini et al., 2008).
In addition, lichen studies have been related
to ecosystem changes due to recent climate
change and temperature increases. For exam-
ple, a reduction of lichen dominance has been
associated with increasingly milder conditions
in some artic habitats due to increasing repre-
sentation of vascular plant biomass (Cornelis-
sen et al., 2001), and are considered excellent
ecosystem indicators in several ways (Petrokas
& Baliuckas, 2017). Traditionally, lichen stud-
ies in more pristine areas have been mostly
related to site-specific environmental gradients,
such as the temperature, moisture, and latitu-
dinal gradients (McCune, 2000), and, more
recently, to include other microsites besides
tree trunks (Gasparyan et al., 2018). Large
scale studies in a paleotropical forest found
that some tree species, bark traits, and tree size
are key factors determining lichen community
structure (Thüs et al., 2021).
In this study, we use lichens to compare
how passive restoration after the abandonment
of two pasture areas and a cypress plantation
influenced the development of the lichen com-
munity and diversity. Recent evidence points
out that the epiphytic lichen richness requires
a mean of 180 years to reach old-growth forest
richness (Spake et al., 2015). A simple way to
compare communities based on species pres-
ence data and its dominance can be executed
through the calculation of several well-known
parameters and indexes, which are extensively
used and discussed in the ecological literature
such as Heltshe and Forrester (1983), Krebs
(1999), Hubbell (2001), Condit et al. (2005),
and López and Duque (2010).
This study aims to evaluate the corticolous
lichen’s diversity in terms of species rich-
ness and diversity as indicators of ecosystem
condition in three forest covers differing in
previous land use and time of abandonment.
It emphasizes the significant role played in
the time after abandonment and passive res-
toration in the diversity and distribution of
lichens within a mid-elevation cloud forest in a
tropical landscape.
Study sites: This study comprises three
different forested areas differing in the modes
and degrees of restoration located around the
Orosí Valley, on the oriental side of the Costa
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
Rican Central Valley. The first two sites are
located near the Río Macho Biological Station
at El Llano (9°46’ N & 83°51’ W), and a third
one is close to Orosí town (Table 1). The first
site is considered as the reference old secondary
forest (OF) located in the lower montane rainy
forest located at 1 700 m.a.s.l. (Ortiz-Mala-
vassi, 2014), with more than 50 yo of regen-
eration from abandoned pastures. We have
observed more than 50 species of trees which
include: Myrsine coriacea, Billia hippocasta-
num, Marila laxiflora, Miconia dodecandra,
Cornus disciflora, Vismia baccifera, Clusia sp.,
Symphonia globulifera, Quercus sp., Saurauia
montana, Saurauia yasicae, and several Ocotea
species. In the same life ecological zone, the
second site is a young secondary forest (YF),
and it is located less than 1 km away from the
forested site (at 1 680 m.a.s.l.). This YF con-
tains a natural regeneration forest of approxi-
mately 13 yo from pastures and an abandoned
Syzygium jambos (Myrtaceae) plantation, and
it is surrounded by other farms, old pastures in
different states of abandonment, and the West-
ern section limits with the natural forest. At
least 16 tree species had been recorded, includ-
ing M. coriacea, M. dodecandra, V. baccifera,
Clusia sp., S. montana, S. yasicae, Topobea
maurofernandeziana, Rubus roseifolius and S.
jambos. The third site is a small, private, and
unmanaged cypress plantation (CP) (Cupressus
lusitanica) at least 35 yo originally planted on a
previous coffee plantation, presently surround-
ed by sunny and shade-grown coffee and small
riparian relicts of original forest (Table 1). This
site is in the humid premontane forest life zone
(Ortiz-Malavassi, 2014) at approximately 1
300 m.a.s.l. and 1 km North of Orosí town. In
addition to the complete canopy dominance by
the cypress tree crowns, at least 36 other tree
species are starting to reach the lower canopy
level. The most common tree species are sev-
eral: Miconia spp., Viburnum spp., Zanthoxy-
lum spp., Coffea arabica, Conostegia spp., and
S. jambos.
Sampling methods: Despite the great
diversity of available phorophytes for lichen
establishment, we consider only corticolous
(epixylic) lichens, those who establish only on
standing tree barks. We consider the following
aspects that may determine lichen establish-
ment on tree trunks to sample, and measure:
twenty subplots of 10 × 10 m were randomly
selected from 50 in each forest plot of 0.5 ha
(Table 1). Within each subplot, the first two
trees found with a diameter at breast height >
10 cm were chosen to sample lichens. Bended
trees (> 10° inclination) and extremely smooth
or rough bark textures were avoided to homog-
enize possible species preferences for bark sur-
faces. Phorophyte species were not registered
but, for the cypress plantation, all chosen trees
were C. lusitanica (Cupressaceae).
Lichen sampling: A transparent plastic
template 20 × 10 cm was located against the
tree bark at 1.5 m from the tree base to make
TABLE 1. Characteristics of the three study plots
Locality Reserva Forestal Río Macho Reserva Forestal Río Macho Finca La Laja Orosí
Plot name OF plot at El Llano YF plot CP plot
Origin/age Old secondary 50 yo
Abandoned farm
and plantation 13 yo
Coffee Plantation 35 yo
Elevation (m.a.s.l.) 1 720 1 700 1 300
Annual rainfall (mm) 2 400 2 400 2 300
Mean annual temperature (ºC) 17 18 22
Holdridge life zone Lower montane wet forest Lower Montane wet forest Premontane wet forest
Plot size (subplots) 0.5 ha (50) 0.5 ha (50) 0.5 ha (50)
Forest connectivity* High Medium Low
OF: Old Secondary Forest, YF: Young Secondary Forest, CP: Cypress Plantation. *Forest connectivity refers to the degree
of connection to continuous and non-disturbed cloud forest around the plot areas.
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
silhouette drawings for every lichen. Similar
templates have been utilized in lichen biomoni-
toring, and has been successfully tested for
pollution studies in Costa Rica (Monge-Nájera
et al., 2002; Neurohr et al., 2011). The cardi-
nal orientation points were changed system-
atically for every chosen tree, to confound any
microsite differences introduced by trunk face
orientation due to light, wind, moisture, slope
aspect, and stem flow. Tree sample size varied
between plots because some chosen trees ended
with no lichens. The final sampled trees with
lichens were 20, 30, and 25 for the OF, YF, and
CP plots.
In the field, a photograph of every tree
bark and template was also taken, and a lichen
sample was collected for identification. A total
of 75 templates were sampled for a total of 13
800 cm
. Taxonomic keys to assign lichen’s
genera (Sipman, 2020) and other published
keys were used for species identification (i.e.
Sipman et al., 2012). Species not completely
identified were considered as morphotypes
and treated as species for the analyses. The
taxonomic resolution was 100 % at the family
and genera level, and 50 % at the species level.
Voucher samples were deposited in the herbar-
ium at the Instituto Nacional de Biodiversidad,
Heredia, Costa Rica.
Data Analysis: Every template was ana-
lyzed with the Image Tools program, (UTHSC-
SA, Texas, USA) for recording individual lichen
surface area. The sampling method allowed to
calculate the relative frequency, density, and
area-based dominance of lichens. The Impor-
tance Value Index (IVI) per species by forest
was calculated as the sum of the relative fre-
quency (number of times in different templates/
number of templates of all species), plus the
relative abundance (number of individual/total
number of individual) plus the relative domi-
nance (surface area of every lichen species/
total surface area of all lichens of all species)
of every species, based on a modified method
applied for lichens by Pinokiyo et al. (2008).
The IVI calculations were also performed
grouping species by lichen families, to obtain
the Family Importance Value Index (FIVI). A
species-rank ordination based on IVI by forest
was also performed; the species accumulation
curve was calculated with both the number
of individuals using the Fisher alpha index
to estimate the number of species up to 1 000
individuals and with the number of plots per
site, using the Clench model (Fagan & Kareiva,
1997), respectively.
The following diversity and community
index were calculated: Shannon-Wiener Index
(log base two), evenness (J), Fisher alpha (α),
species richness per 100 and 200 individuals
from α (S100 y S200, respectively), Simp-
son reciprocal Index (1/D), average species
richness per plot (φ), beta diversity = g/φ)
which is used here as the number of spe-
cies change across sites (Neitlich & McCune,
1997), gamma diversity (g = total species rich-
ness), and g ´(first-order jackknife estimator
of total species richness), as in Palmer (1990).
The mean lichen species per plot (template)
(φ) was analyzed with a Kruskal-Wallis test.
We calculated the qualitative species similarity
index of Sørensen (Polo, 2008) and the quanti-
tative Bray-Curtis (BC) calculated as 1 minus
BC value (Krebs 1999), among the three sites.
All diversity analyses were performed with
the “Vegan” package” (Oksanen et al., 2014)
in the R language program (R Core Team,
2020). Finally, non-metric multidimensional
scaling (NMDS) for abundance, frequency,
dominance, and presence/absence of the lichen
species for three forest covers were done with
the “Vegan” package” in R; abundance, fre-
quency, and dominance data were standardized
by dividing the values by the total margin and
then obtaining the square root (see details in
Legendre & Gallagher, 2001). We also tested
the hypothesis that the ecological importance
of the species differs between sites from a
random distribution by comparing the number
of species assigned to three categories of per-
centile distribution of the IVI values (0-33.3,
33.3-66.6, and 66.6-100). A homogeneity test
adjusted by a Fisher correction based on a spe-
cies categorization was applied.
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
Importance Values and species-area
curve: A total of 64 species of lichens were
found on the three studied sites, belonging to 25
families. Sixteen percent of the entire sampled
area was covered by lichens. The YF showed
the highest species richness (42 species), fol-
lowed by the CP (23 species) and the OF (21
species) (Digital Appendix 1, Digital Appendix
2, Digital Appendix 3). Cryptothecia sp. had
the highest IVI in the three sites, increasing
in the following order: OF (10.4 %), YF (15.6
%), and CP (24 %). These lichen communities
are characterized by a large proportion of spe-
cies with a low IVI (Digital Appendix1, Digital
Appendix 2, Digital Appendix 3). More than
87 % of the lichen species present in the three
sites had an IVI lower than 10 %. In the OF site
(Digital Appendix 1), 57 % of lichen species
have an IVI less than 5 %, increasing to the 77
and 90 % in the CP and YF sites, respectively
(Digital Appendix 1). The top three species
have an IVI of 29, 31, and 54 % in the OF, YF,
and CP sites, respectively.
The three forests contain a contrasting
number of families, with 15, 20 and 10 fami-
lies in the OF, YF, and CP sites, respectively.
The family Arthoniaceae occupied the highest
IVI in the CP site, followed by the YF and the
smaller IVI in the OF site (Digital Appendix
4, Digital Appendix 5, Digital Appendix 6). In
the CP site, the family Arthoniaceae reached 51
% importance value given the high abundance
and dominance of a Cryptothecia species and
five different Herpothallon species. However,
the IVI for this family went down to 22.8 in
the YF and 12 % in the OF (Digital Appendix
4). The top three families in the OF, YF, and
CP sites had a FIVI of 36.2, 48.5, and 74.8 %,
respectively. The other two families in the top
three were completely different between sites:
Lobariaceae and Hygrophoraceae in the OF,
Pyrenulaceae and Parmeliaceae in the YF, and
Stereocaulaceae and Coenogoniaceae in the
OF, adding about 23, 20, and 13 % of the FIVI
in the three sites, respectively.
IVI-based species-rank curves showed
striking differences among sites (Fig. 1A).
The OF and YF curves show an almost perfect
reverted sigmoid curve, but a steady decline in
the OF site. The species accumulation curves
based on the Fisher α showed similarities
between all three sites, they are concave down-
wards, and showing that the OF had intermedi-
ate species richness. None of the curves seems
to reach an asymptote (Fig. 1B). However, spe-
cies accumulation curve based on the sampled
plots on the trees (Fig. 1C) suggested that sam-
pling effort was sufficient to get an estimation
of species richness of the corticolous lichens in
the three communities.
Richness and diversity indexes: The YF
site had the highest species richness and diver-
sity as a whole, followed by the OF and the
Fig. 1. Species-rank curves based on the A. Importance Value Index (IVI), B. Species accumulation curve per number of
individuals through Fisher α index, and C. Species accumulation curve per number of plots for three forests cover in Orosí
Valley, Costa Rica. In C, solid lines represent a Clench model for three forests covers. OF: Old Secondary Forest, YF: Young
Secondary Forest, CP: Cypress Plantation.
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
CP sites (Table 2). Also, the YF had the high-
est species number according to the S100 and
S200 predictions, the Beta, the gamma, the
gamma´ jackknife estimator, and the highest
. However, the CP site had the lowest
species number, but the Fisher α, S100, and
S200, Simpson reciprocal, but Beta diver-
sity were greater than the values of the OF. In
addition, the OF site shows the best evenness
as expressed by the J´ index (Table 2). How-
ever, there was no difference between the mean
number of species per tree template between
the three sites, with the OF having less than two
species per sampled tree.
Community similarity: Both the simi-
larity coefficient and the Bray-Curtis Index
showed remarkable low values between com-
pared sites, confirming a particularly low
resemblance in lichen communities over the
three sites. Both indexes differ at identifying
the two most dissimilar sites: YF/CP pair (by
Sørensen Coefficient), and the OF/CP pair (by
the Bray-Curtis index) (Table 3). In addition,
the homogeneity test showed that the number
of species based on the IVI values (by sites)
do not follow a random distribution (Table 4).
Non-metric multidimensional scal-
ing (NMDS): Community data of lichens for
TABLE 2. Richness and diversity indexes estimated for each forest type
N 20 30 25
4.02 4.80 3.30
4.39 5.46 4.52
0.92 0.88 0.73
α 9.43 15.44 6.34
23 31 18
29 41 22
1/D 14.17 21.62 5.85
φ (± SE) * 1.70 (0.21) 2.78 (0.40) 2.16 (0.19)
β 12.35 15.11 10.19
g 21 42 22
g´** 35 67 38
N: numbers of plots per site, H´: Shannon-Wiener´s index, J´: evenness (H´/H
), α: Fisher alpha, S
y S
are species
richness per each 100 and 200 individuals from α, respectively, 1/D: Simpsons´s index, φ: average species richness per plot
(± standard error), β: beta (g/φ), g: gamma diversity (total species richness), and g´: first-order jackknife estimator of total
species richness.
* Kruskall-Wallis´s test between sites = 3.274, d.f. = 2, 75, P > 0.05.
** The estimate for g´ is based on the number of single-occurrence species in the plots (Palmer, 1990). OF: Old Secondary
Forest, YF: Young Secondary Forest, CP: Cypress Plantation.
TABLE 3. Community similarity based on Sørensen similarity coefficient
and the Bray-Curtis Index between forest covers
rensen similarity coefficient
Bray-Curtis OF 0.34(11) 0.33(7)
YF 0.19 0.28(9)
CP 0.15 0.26
Upper right: Sorensen similarity coefficient, in brackets the number of species shared, and down left: Bray-Curtis. OF: Old
Secondary Forest, YF: Young Secondary Forest, CP: Cypress Plantation.
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
subplot sample did not show a clustering for
abundance, frequency, dominance, and pres-
ence/absence for three forest covers (Fig. 2A,
Fig. 2B, Fig. 2C and Fig. 2D, respectively;
NMDS with stress index less than 0.049).
The species diversity and community
composition of the corticolous lichens in the
mountains of the Orosí Valley seem to be rela-
tively high considering the sampling effort, the
taxonomic resolution, the restricted tree stem
sampling, and the ecological life zones studied.
Compared to lower-elevation tropical forests,
diversity is much lower than the 217 foliaceous
lichen species sampled in the lowland rain
forest of Costa Rica (Lücking, 1999a), or the
150 corticolous crustose lichen species in the
Brazilian Atlantic rain forest (Cáceres et al.,
2007), but very similar to the 61 species found
in degraded dry forest remnants in Colombia
(Lücking et al., 2019). The most important
component of the corticolous lichen diversity
appears to belong to lichens occurring in rela-
tively open and early successional fields.
Lichen traits, richness and diversity:
Temperate and boreal data suggest that there
is a corresponding relationship between forest
complexity and lichen biomass, and its diver-
sity (Crites & Dale, 1998). However, the pres-
ent analyses indicate that young successional
forest (13 yo) contains a greater number of
TABLE 4. Number of species classified by the importance value index (IVI) percentile categories for the three forests
≥ 66.7
percentile 66.7
– 33.3
percentile ≤ 33.3
OF 9 3 9
YF 4 8 30
CP 5 1 16
Fisher adjusted χ
, P= 0.019. OF: Old Secondary Forest, YF: Young Secondary Forest, CP: Cypress Plantation.
Fig. 2. Non-metric Multi-dimensional Scaling (NMDS) for A. Abundance, B. Frequency, C. Dominance, and D. Presence/
absence of lichens for community data for the three forests in the Orosí Valley, Costa Rica. OF: Old Secondary Forest, YF:
Young Secondary Forest, CP: Cypress Plantation.
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
lichens and significantly high species richness
and diversity. Traditionally, lichens have been
categorized as open area dwellers, a trait biased
by the ability of lichens to cope with extreme
habitats around the world, where they seem to
reach higher biodiversity values (Galloway,
1992). In this sense, the present study entirely
agrees with this general trend. This typical
situation is favored because the YF contains
a high concentration of small-diameter trees
along with the abandoned and relatively older
trees of S. jambos (Myrtaceae), which were
practically covered by mosses and lichens,
creating ideal microclimatic conditions based
on a minutely grained gradient of moisture and
light. Contrarily, the foliaceous lichen com-
munity from tropical lowland forest (Lücking,
1999b) presented a reduced species account for
open, human-modified vegetation by lacking
typical forest understory species.
Lichen species composition also varies
greatly along gradients of temperature and
moisture (Neitlich & McCune, 1997; Crites &
Dale, 1998). Given the climatic and topograph-
ic traits of this region, along with abandoned
farms, early and intermediate successional
areas, all may play a significant role in the
maintenance and dynamics for lichen species
richness, providing habitats and a great avail-
ability of tree trunk phorophytes that interact
with the microenvironmental gradients. As
previously stated, the boundary layer scale of
micro topographic microsites may generate a
significant gradient of smaller-scale strategies
for poikilohydric organisms (Proctor, 2014).
However, tree trunk microenvironments below
canopies of natural forests, like in the old
secondary forest, can be considered highly
homogeneous, providing a dim environment,
and much more constant humidity conditions,
which could be restricting the growth and
development of many lichen species.
A large amount of information demon-
strated that tree species, bark texture, bark
pH, lenticels traits, milk sap (Cáceres et al.,
2007), circumference and inclination of the
trunk were relevant factors influencing the
abundance and distribution of lichen species
worldwide, explaining about 50 % of the total
variation (Cristofolini et al., 2008). In this
sense, we found the lower evenness, and lower
Fisher α and β diversities in the CP site (Table
2), where all sampled trees were C. lusitanica.
This situation indicates obvious differences in
the availability and bark trait parameters of
potential phorophytes between the three tree
communities studied.
Lichen community patterns: These
lichen communities follow the typical pattern
of tropical tree communities; a dominance of
very common and few species in combina-
tion with a great number of very uncommon
or “rare” species (Condit et al., 1996). Mean
species per tree trunk was lowest in the OF
trees, which suggests dimmer light conditions
within the forest and greater competition for
corticolous habitats with bark bryophytes. The
more complex OF site showed the higher even-
ness, and it was situated in intermediate posi-
tions in the ranking of indexes calculated. This
situation is also reflected in the importance
values calculated at family level, where the
second and third most important families were
completely different in the three sites. Even
though species composition in a given area has
a strong effect on the biogeographical affini-
ties between species (Santos et al., 2020) and
higher taxa, it is possible to hypothesize that
specific microclimatic conditions may select
for distantly related species adapted to them. In
other words, species composition may rely on a
gradient of fine-tune microenvironmental pref-
erences from a pool of ecologically equal spe-
cies randomly established. This suggestion has
also been addressed from diversity and species/
area curves from tree species communities in
complex structures in large-scale areas (Condit
et al., 1996; Condit et al., 2005). Second, it is
well known that lichen richness is high at edge
environments such as the forest-grassland eco-
tone, and this trend hold for both hemispheres
(Galloway, 1992) which supports the idea of
the YF possessing the highest diversity. And,
third, local or regional level lichen biodiversity
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
may be the result of disturbance (Galloway,
1992), which produces a much richer and
heterogeneous habitat for lichens than the one
in the understory of an almost fully developed
forest. In this sense, a dynamic perturbation
cycle for a long period of human intervened
landscape along with sequential changes of
available land abandonment may provide the
required potential for the maintenance of a
highly dynamic species turnover, mainly based
on the high species source provided by the rela-
tively close, pristine and gigantic forest conser-
vation area. Finally, it is possible that our final
community composition is also affected by the
stochastic effects of species dispersal, espe-
cially of rare species, as suggested by Cáceres
et al. (2007) for the formation of a lichen
community in a tropical rainforest understory.
Dispersal limitation has also been suggested to
affect similarly the successful establishment of
epiphytic bromeliads in the interiors of tropical
montane forests (Cascante-Marín et al., 2009).
As a result, we detect a strong resemblance
of community structure of the three sites but
great differences in ecological importance and
composition. The species richness gradient
between the three restoration sites seems to be
enhanced by the way the species assemblages
were developed in time, microclimatic condi-
tions in and around the phorophytes, and in
other factors determining lichen abundance and
establishment, such as light environment, pho-
rophyte specificity, temperature and moisture
gradients, and site history. These characteristics
are determinants of the heterogeneity of the
species composition and in turn are associ-
ated with the high abundance of rare species
on a larger scale (Enquist et al., 2019). Such
rarity seems to define the strong dissimilarity
of the studied forest stands, e.g., phorophyte
specificity was explained for the NMDS analy-
sis, because colonization aspects of lichen are
heterogeneous at the level of the host tree in
a forest stand with high tree diversity, leading
to the non-clustering and differentiation of the
lichen community.
Lichens as indicator species: This study
suggests the use of the importance of the lichen
genera Cryptothecia as indicator of ecological
position of forested areas in the mountains sur-
rounding the Oriental Central Valley of Costa
Rica. This species is dominant in the OF but
with a relatively low IVI value. Its ecological
importance increased in the YF and even more
in the CP, reflecting a negative relationship
with forest integrity reflecting some passive
restoration traits such as restoration age, veg-
etation structure, and microclimate variations,
and some possible substrate-specific traits for
lichen formation associated to the diversity of
phorophytes. As a whole, there was not any
relationship between restoration preference,
forest condition, and association of lichen fam-
ilies as found for a variety of dry and lowland
environments of Costa Rica as found by Rivas-
Plata et al. (2008), possibly as a consequence
of the extreme differences in sampling between
studies, or because our study is located in the
highest part of the elevation gradient consid-
ered in that study. This is why developing a
fast indicator procedure for forest condition
and fragmentation status must be established
cautiously and clearly restricted and applied to
the life zone considered and the level of human
interventions. As hemeroby bioindicators, we
support Williams and Ellis (2018) conclusion
about the importance of the spatial associations
between forest fragments to interpret individual
lichen species or family indicators as markers
of threat and conservation value.
Restoration implications: The entire
region has probably the potential for greater
species richness; however, dispersal limitation
associated with a strong habitat fragmentation
after a long history of human utilization of
resources produced the present and reduced
local species diversity. Natural and passive res-
toration efforts are slow but better strategies for
obtaining a more structured and diverse lichen
community. As previously stated by McCune
(2000) for some temperate ecosystems, this
study will contribute and will provide the
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 688-699, April-June 2021 (Published Jun. 21, 2021)
documentation of invasion and extinction of
species, the lichen species distributions along
with larger scales, and it will enhance the
appreciation for lichens given its importance
for ecosystem functioning and diversity.
From a practical point of view, practi-
tioners may use this simple methodology by
monitoring lichen diversity for easy compari-
sons of forest integrity and restoration trajec-
tories. However, an analysis of the ecological
complexity of tropical forests from lichen com-
munities has to be considered carefully by
defining a complete sampling of the different
microenvironments they live, and the ecologi-
cal and phorophyte preferences, and life forms.
Practitioners may also apply this method for a
description of vertical gradients in lichen com-
munity composition as a way to relate them
to corresponding changes in canopy structure.
They need to be careful because they may also
indicate differences in successional gradients,
through vertical displacement as the forest
became older (Neitlich & McCune, 1997; Will-
Wolf et al., 2006).
Ethical statement: authors declare that
they all agree with this publication and made
significant contributions; that there is no con-
flict of interest of any kind; and that we fol-
lowed all pertinent ethical and legal procedures
and requirements. All financial sources are
fully and clearly stated in the acknowledge-
ments section. A signed document has been
filed in the journal archives.
We greatly appreciate the suggestions to
previous versions of this manuscript to R.
Lücking, and to Deanna Sekulich, Kotochi B.
Anita, and Stefany Solano for revising the Eng-
lish. We give our thanks to ICE and Estación
de Acuicultura and Biología Tropical de Río
Macho for facilities provided. To SINAC for
facilitation of research permits. This study
was funded by a Fondo Especial de Educación
Superior (FEES) from the Consejo Nacional
de Rectores (CONARE) of Costa Rica to RCS.
Estructura y riqueza de la comunidad liquénica de tres
bosques secundarios de elevación media en Costa Rica
Introducción: La diversidad de líquenes, la estructu-
ra y composición de la comunidad y la abundancia de algu-
nas especies y familias se ha usado como indicadores de la
salud y continuidad ecológica de los ecosistemas boscosos
tropicales. Objetivos: Evaluar la composición, diversidad
e importancia ecológica de las especies de líquenes en tres
ecosistemas boscosos que difieren en el tiempo regenera-
ción natural, como indicadores de la influencia de la restau-
ración pasiva en el ensamble de la comunidad de líquenes
cortícolas. Métodos: Se midieron los líquenes individuales
sobre los troncos de árboles en un bosque secundario
avanzado (OF), en un bosque secundario joven (YF, con
50 y 14 años de regeneración natural tras abandono del
potrero, respectivamente), y en una plantación abandonada
de ciprés exótico con 35 años de edad (CP), en la región
oriental del Valle Central de Costa Rica. Se calcularon
los índices estándares de diversidad, similitud y valor de
importancia (IVI), además de un análisis de NMDS sobre
los parámetros de la estructura de la comunidad en una
matriz de presencia-ausencia. Resultados: Encontramos
64 especies en 25 familias, con 42, 23 y 21 especies y 20,
10 y 15 familias en los sitios YF, CP y OF, respectivamente.
Una especie de Cryptothecia sp. presentó el IVI más alto en
los tres bosques. Más del 87 % de las especies son raras. El
IVI combinado de las tres familias más importantes fue: 36,
48.5 y 74.8 % en los sitios: YF, OF y CP, respectivamente.
Arthoniaceae está entre las tres familias más importantes
en los tres sitios. El YF es el sitio con más especies, pero el
sitio OF presentó la mayor igualdad. Los índices de simi-
litud y diversidad sugieren una semejanza particularmente
baja entre las comunidades liquénicas, pero separadas
por una gradiente de diferenciación difusa entre los tres
sitios, lo cual es confirmado por el análisis NMDS. La
prueba de homogeneidad confirmó grandes diferencias en
la importancia ecológica y la composición. Conclusiones:
La región contiene un ensamblaje propio de especies que
resulta en una fuerte diferenciación comunitaria entre bos-
ques, reflejo de la influencia de factores ecofisiológicos y
microclimáticos en el establecimiento y supervivencia de
líquenes; lo que sugiere una gran diversidad beta regional,
en un paisaje fragmentado. Una mayor conectividad y
estrategias de restauración pasiva dieron como resultado
una mayor diversidad y una estructura comunitaria más
heterogénea en ambos bosques que la comunidad cortí-
cola de la plantación exótica abandonada. La protección
de fragmentos forestales maximizará la integridad de los
bosques futuros.
Key words: bosque nuboso; composición de la comuni-
dad; Costa Rica; líquenes cortícolas; hemerobia; diversidad
de líquenes.
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