688

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.

ABSTRACT

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.

https://doi.org/10.15517/rbt.v69i2.46162

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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.

MATERIALS AND METHODS

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

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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.

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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 (β = 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.

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RESULTS

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.

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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

max

. 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

OF YF CP

N 20 30 25

H´ 4.02 4.80 3.30

max

4.39 5.46 4.52

J´ 0.92 0.88 0.73

α 9.43 15.44 6.34

100

23 31 18

200

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

max

), α: Fisher alpha, S

100

y S

200

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

Sørensen similarity coefficient

OF YF CP

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.

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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).

DISCUSSION

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

IVI

≥ 66.7

percentile 66.7

– 33.3

percentile ≤ 33.3

percentile

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.

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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

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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

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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.

ACKNOWLEDGMENTS

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.

RESUMEN

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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