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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(3): 1079-1097, July-September 2021 (Published Sep. 27, 2021)

Floristic composition, structure and environmental characterization of

Cyathea costaricensis population in a remnant cloud forest in Mexico

Miguel Olvera-Vargas

; https://orcid.org/0000-0002-7290-1639

Blanca L. Figueroa-Rangel

; https://orcid.org/0000-0002-5869-5277

Christiam Solís Robles

; https://orcid.org/0000-0002-1341-1605

1. Departamento de Ecología y Recursos Naturales, Centro Universitario de la Costa Sur, Universidad de Guadalajara,

Av. Independencia Nacional # 151. Autlán de Navarro, Jalisco, México; molvera@cucsur.udg.mx (*Correspondence),

bfrangel@cucsur.udg.mx

2. Centro Universitario de la Costa Sur, Universidad de Guadalajara, Av. Independencia Nacional # 151, Autlán de

Navarro, Jalisco, México; sorch94@gmail.com

Received 10-VI-2021. Corrected 26-VIII-2021. Accepted 17-IX-2021.

ABSTRACT

Introduction: Tree ferns are significant components of temperate, tropical and subtropical forests, contributing

to shape complex forest stand structures.

Objectives: 1) to describe the population structure of Cyathea costaricensis in a remnant cloud forest of West-

central Mexico; 2) to characterize and relate the floristic composition and the structure of the most important tree

species associated to the C. costaricensis population and; 3) to describe the environment where C. costaricensis

occurs.

Methods: We estimated the Importance Value Index (IVI) to select the most important canopy-dominant species

associated to C. costaricensis; we constructed height and Diameter at Breast Height (DBH) frequency distribu-

tions for those selected species according to IVI as well as for C. costaricensis population; we computed the

asymmetry of the frequency distributions through the coefficient of skewness and the probability density func-

tion via the Kernel density estimation. We tested for differences between canopy-dominant tree species and C.

costaricensis population structure by the non-parametric Wilcoxon rank sum test.

Results: C. costaricensis individuals presented the smallest heights and intermediate DBH sizes as compared

with the canopy-dominant species, with statistically significant differences for height but not for DBH according

to the Wilcoxon test. Most of the tree fern individuals were located in uneven terrains and over the base slope

of the terrain; canopy openness and Total Radiation Under the Canopy values were similar to those reported for

Cyathea species elsewhere.

Conclusions: We confirm the hypothesis of comparable structure between the canopy-dominant species and the

C. costaricensis population only for DBH; on the contrary, for trunk height, there were statistically significant

differences; the small heights of C. costaricensis suggest their coexistence in the understory through sheltering

from the taller canopy-dominants. Mostly all individuals of C. costaricensis were confined to local environmen-

tal conditions, particularly to physiography.

Key words: tree ferns; population structure; canopy species composition; reversed J-shaped; height categories;

local environment.

Olvera-Vargas, M., Figueroa-Rangel, B. L., & Solís Robles, C.

(2021). Floristic composition, structure and environmental

characterization of Cyathea costaricensis population in

a remnant cloud forest in Mexico. Revista de Biología

Tropical, 69(3), 1079-1097. https://doi.org/10.15517/rbt.

v69i3.47359

https://doi.org/10.15517/rbt.v69i3.47359

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Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(3): 1079-1097, July-September 2021 (Published Sep. 27, 2021)

Tree ferns in some forest communities

are important elements in the development of

complex forest structure over time (Fedrigo

et al., 2019). They inhabit a variety of forest

ecosystems as prominent components of tem-

perate and tropical understories, contributing

significantly to the total basal area and stem

density (Bystriakova et al., 2011; Shepherd

et al., 2019). Several tree ferns: Alsophila

tricolor (Colenso) R. Tryon, A. engelii R.M.

Tryon, Cyathea caracasana (Klotzsch) Domin

are known to be negatively stand density

dependent; such negative density dependence

and strong environmental filtering, may affect

the establishment of tree fern seedlings and

saplings, particularly when they occur near

conspecific adult tree ferns (Brock et al., 2020;

Chacón-Labella et al., 2014).

In preserved areas, combined with under-

story shade, some tree fern species (Cyathea

caracasana) can enter a “persistence mode”

until a canopy gap opens above them; subse-

quently, they begin a rapid growth, producing

spores and seedling recruitment (Arens, 2001).

The recruitment of tree ferns may be controlled

by environmental filters, including forest can-

opy disturbances that create gaps and edges,

which in turns modify local niche conditions

(Bernabe et al., 1999; Brock et al., 2018a).

Sun-light, temperature, humidity, small-scale

physiographic variations, are among the most

important environmental determinants for their

occurrence (Mendoza-Ruiz & Ceja-Romero,

2014). Many tree fern species thrive well

along stream banks, soils rich in organic mat-

ter and over more exposed sites with direct

sunlight; others like Cyathea sinuata Hook.

& Grev. (synonymous of Alsophila sinuata)

succeed well even on rocky stream side banks

(Ranil et al., 2017).

Tree ferns facilitate regeneration of cer-

tain species (Gaxiola et al., 2008); hence they

have an important influence on the regenera-

tion niche of potentially dominant tree species

through macro-litter fall and shading with

effects on nutrient cycling. A number of tree

ferns species are recognized as keystone spe-

cies for their role in casting deep shade on forest

floor environment, acting as a differential eco-

logical filter on regeneration processes (Forbes

et al., 2016). The ecological relevance of tree

ferns has been documented in several regions

of the world, particularly in the understory as

crucial factors determining forest structure,

through the release of shade-intolerant conifers

from angiosperm competition (Brock et al.,

2020). But also, tree ferns can affect succes-

sional processes around their neighborhood

by inhibiting the growth of understory species

through the release of allelochemicals (Negrão

et al., 2017), in some cases, inhibiting and

slowing forest succession (Brock et al., 2018b).

Tree ferns are important components of cloud

forests in Mexico (Hernández-Álvarez et al.,

2019; Ruiz Coyoahua, 2020), however, eco-

logical information on these vascular plants has

been largely restricted to taxonomic descrip-

tions (Mendoza-Ruiz & Ceja-Romero, 2014)

and to assess species richness (Ramírez-Bara-

hona et al., 2011). Cloud forest is a community

included in the humid forest ecosystems of

Mexico, mostly located between 1 000 to 3 000

m.a.s.l. (Villaseñor, 2010) where high humid-

ity, due to cloud condensation, is common. In

Mexico, one of the most important tree fern

genera is Cyathea; it contains approximately

10 species under different conservation catego-

ries, mostly growing in sub-tropical, tropical

and cloud forests (Ruiz Coyoahua, 2020). One

of these tree fern species is Cyathea costari-

censis (Mett. ex Kuhn) Domin, a Mesoameri-

can endemic species distributed from Western

Mexico to Western Panama (Mickel & Smith,

2004); although it is tagged as an Endangered

species according to the Mexican Red List

NOM-059-SEMARNAT-2010 (Secretaría del

Medio Ambiente y Recursos Naturales, 2010),

there is no documented studies on its ecology.

Accordingly, this study seeks to answer: how

tree ferns coexist with the canopy-dominant

shade-tolerant species of a remnant cloud forest

in West-Central Mexico? Therefore, the objec-

tives in the present study were: 1) to describe

the population structure of C. costaricensis in a

remnant cloud forest of West-Central Mexico;

we hypothesized that C. costaricensis is an

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important element beneath the canopy of domi-

nant trees with a typical behavior of a shade-

tolerant species, thus its diameter and height

frequency distribution will be characterized by

a reversed J-shape showing a gradual lessen-

ing of individuals as its diameter and height

category increase; 2) to characterize and relate

the canopy floristic composition including the

structure of the most important tree species,

to C. costaricensis population structure; we

hypothesized that the canopy-dominant species

and the C. costaricensis population, will show

a similar structural pattern due to their shade-

tolerance behavior; 3) to describe the environ-

ment where C. costaricensis occurs, we expect

that sun-light related variables should explain

the presence of this species in our study area.

MATERIALS AND METHODS

Study site: We carried out this research

in a remnant cloud forest which contains a

unique ancient flora of Pleistocene origin,

mainly dominated by Acer binzayedii Y.L.

Vargas-Rodr., Podocarpus reichei J. Buch-

holz & N.E. Gray and Abies religiosa (Kunth)

Schltdl. & Cham. (Del Castillo-Batista et al.,

2018; Vargas-Rodríguez et al., 2012). The

study area is located over the East-Southeast

zone in Talpa de Allende Jalisco, Mexico

(between the coordinates (20º13’46.28” N &

104º44’2.69” W), at 1 798 m.a.s.l.), within

the tributary Talpa watershed. Annual aver-

age precipitation extends from 1 600 to 1 800

mm and temperature from 16 to 22 ºC. This

floristic zone is characterized by a complex

biogeographical history that combines Holarc-

tic, Tropical, Pantropical and Asian-American

elements as a result of the convergence of the

Nearctic and the Neotropic biogeographical

zones (Vázquez-García et al., 2000).

Data collection method: First, we con-

ducted a field exploration on the whole area

covered by the relict cloud forest in the study

area where we observed Cyathea costaricensis

individuals (around 3 ha); in a second stage, we

census all individuals of Cyathea costaricensis

present in the study area.

Vegetation characterization: Field-work

explorations revealed that Cyathea costaricen-

sis population in the study area has a fragment-

ed and rather small population size. Therefore,

we established seven circular plots (500 m

each). In each plot, all C. costaricensis indi-

viduals were counted, identified and their total

height and diameter at breast height (DBH;

measured at 1.30 m height above the forest

floor) were measured. Tree species ≥ 5 cm

DBH, co-occurring with C. costaricensis, were

also recorded by species, DBH and height.

When necessary, we removed any obstacle (e.g.

lichens, dead material, creeper plants, etc.) that

might impede an accurate DBH measurement.

All individuals were identified during the field-

work to species level according with the speci-

mens deposited in the ZEA Herbarium of the

Department of Ecology and Natural Resources

of the Centro Universitario de la Costa Sur,

University of Guadalajara; the scientific spe-

cies names were cross-checked according to

Tropicos.org database (Tropicos.org, 2021).

Environment characterization: In each

plot, we recorded the following variables: ele-

vation (m.a.s.l.); slope inclination (as a indica-

tive of soil moisture and depth due to surface

runoff) measured in the steepest down-slope

of the terrain; aspect expressed as azimuth in

degrees from 0 to 360° and then transformed

into a continuous variable according to Beers

et al. (1966); topography, visually evaluated in

two categories, even and uneven terrains (Table

1); stones and rocks (a visual evaluation of the

amount of this material covering the surface of

the plot; both assessed into five categories) and

canopy strata (a visual assessment of the num-

ber of vertical strata formed by crown of the

trees, evaluated in four categories) (Table 1).

The environmental characterization was carried

out following the criteria proposed by Olvera-

Vargas et al. (1996). We also assessed the light

environment using hemispherical photographs

following the protocol proposed by Zhang et al.

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(2005). For this purpose, we took three hemi-

spherical photographs within each 500 m

plot,

one at the upper slope, one at the middle and

one at the lower. We used a Nikon Coolpix 990

digital camera and a Nikon Fish-eye Converter

FC-E8 0.21×lens attached to a self-leveling tri-

pod mount. For hemispherical image analysis,

we used WinSCANOPY (Regent Instruments

Inc., 2005) considering the following variables:

canopy openness (CO), canopy gap fraction

(CGF), leaf area index (LAI), photosynthetic

photon flux density (PPFDu), total radiation

over the canopy (TROC), total radiation under

the canopy (TRUC), direct radiation (DiR) and

diffuse radiation (DfR) (Table 1). We recorded

the date and the time of the day in which each

photo was taken. We used this information as

input during image analysis in WinSCANOPY.

Data analysis: Confidence intervals at 95

% were computed by plot for all quantitative

environmental variables while the mode was

computed for qualitative variables. Confidence

intervals were also estimated for DBH, height

and basal area for Cyathea costaricensis and all

canopy-dominant species. In order to establish

the relative ecological importance of each spe-

cies to the overall forest community dominance,

we first calculated the Importance Value Index

(IVI) (Etherington et al., 1987). This index

represents the sum of relative density (number

of individuals per species/total number of indi-

viduals all species), relative frequency (number

of plots in which species appear/total number

of plots) and relative basal area (total basal

area per species/total basal area all species).

To further describe the tree canopy-dominant

species composition, we selected those species

whose IVI were higher than 70 %. We first

computed quartiles for height and DBH for

the most important species and display them

using box and whisker plots. We analyzed size

frequency distributions for C. costaricensis and

for the canopy-dominant species with the high-

est IVI. For DBH, we used histograms with 5

cm intervals. For height categories, we used the

approach by Pérez-Paredes et al. (2014); these

authors used the following categories in their

study with Cyathea fulva (M. Martens & Gale-

otti) Fée: Juveniles: individuals < 3 m height;

Intermediate: individuals 3-7 m height; Mature:

individuals > 7 m height; we decided to apply

the same height categories since C. costaricen-

sis and C. fulva have relatively similar growth

in terms of maximum height of their stems. To

further compare height class frequency dis-

tribution of C. costaricensis with height class

frequency distribution of the species with the

highest IVI, at plot level, we constructed histo-

grams using the following height intervals (in

meters): < 3, 3-7, 7-11, 11-15, 15-19, 19-24,

24-27, > 27. We also estimated total basal area

by height class for C. costaricensis in order to

discern the contribution in basal area by each

height sizes. The coefficient of skewness (g

)

was computed for both height and DBH fre-

quency distributions to assess symmetry. A g

= 0 indicates a symmetric distribution. A g

< 0

indicates a negative asymmetry skewed to the

left, while a g

> 0 indicates a positive asym-

metry skewed to the right. We estimated the

coefficient of skewness following the Wright

et al. (2003) metric approach:

Where: n, xi, x, and s represent the number of

individuals, the logarithm of DBH or height

for individual i, the mean of the xi, and the

standard deviation (Std) of the xi, respectively.

In order to compare height and DBH

sizes of C. costaricensis with the tree canopy-

dominant species with the highest IVI, a kernel

probability density function was computed and

plotted, one for C. costaricensis and one for

the canopy-dominant species with the high-

est IVI. The shape of the kernel probability

density function does not rely on the number

of class intervals subjectively chosen and it

is built on the individuals’ location of all data

(Węglarczyk, 2018); those characteristics were

suitable as we want to compare dissimilar

sizes for height and DBH of C. costaricensis

and its canopy-dominant species. Shapiro-Wilk

normality test was applied to test the normality

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TABLE 1

Environmental variables recorded in the study plots with Cyathea costaricensis following Olvera-Vargas et al. (1996)

Variable name Acronym

Acronym for

categorical

variables

Measurement units

or names for

categorical variables

Variable Description

1. Elevation Elev Metres above sea

level

Distance above sea level measured with

a Suunto altimeter.

2. Slope inclination Slope Percentage Percentage of slope terrain inclination

measured in the steepest down-slope.

3. Aspect Aspect Degrees Azimuth of dominant direction of

downward-facing slope-inclination.

Log-transformed into a continuous

variable.

4. Topography Top A measure of the terrain evenness.

Top1 Even terrain Continuous and homogeneous terrain

inclination.

Top2 Uneven terrain Discontinuous and heterogeneous

terrain inclination.

5. Rocks Rck Rck0 Absence Visual evaluation of the amount of rocks

covering the surface of the plot.

Rck1 Hardly visible

Rck2 Scarce

Rck3 Moderate

Rck4 Abundant

6. Stones Sto Sto0 Absence Visual evaluation of the amount of

stones covering the surface of the plot.

Sto1 Hardly visible

Sto2 Scarce

Sto3 Moderate

Sto4 Abundant

7. Canopy strata CStr CStr1 One vertical stratum Visual assessment of the number

of vertical strata formed by the tree

crowns. Shrubs were not considered for

this assessment.

CStr2 Two vertical strata

CStr3 Three vertical strata

CStr4 No discernible

vertical stratums

8. Canopy openness CO Percentage

9. Canopy gap fraction CGF Percentage

10. Leaf area index LAI (m

-2

)

11. Photosynthetic photon

flux density under the

canopy

PPFDu (μmol/s-m

)

12. Total radiation over the

canopy

TROC (MJ/m

day)

13. Total radiation under the

canopy

TRUC (MJ/m

day)

14. Direct radiation DiR Percentage

15. Diffuse radiation DfR Percentage

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of height and DBH class frequency distribu-

tion for C. costaricensis and for the canopy-

dominant species with the highest IVI. To test

for differences between the canopy-dominant

species and the C. costaricensis population

structure, using DBH and height as indicators

of structural behavior, the non-parametric Wil-

coxon rank sum test was estimated for DBH

and height; the Wilcoxon test compares two

independent groups when data are not nor-

mally distributed (MacFarland & Yates, 2016).

Descriptive statistics and hypothesis tests (Sha-

piro-Wilks and Wilcoxon) were estimated in R

software-v.3.6 (R Core Team, 2018); for the

coefficient of skewness, we used the e1071

library and for graphs, the ggplot2 library.

RESULTS

Floristic composition and structural

characterization: We recorded a total of 333

individuals ≥ 5 cm of DBH distributed in 27

species, 24 genera and 24 families. Cyathea

costaricensis was represented by 62 individu-

als, representing 18.61 % of the total number

of individuals, followed by Carpinus tropicalis

(Donn. Sm.) Lundell (50 individuals), Podo-

carpus reichei (with 38), Clusia salvinii Donn.

Sm (with 32), Conostegia volcanalis Standl. &

Steyerm. (with 23) and Acer binzayedii (with

23). In contrast, 18 species were present with

fewer than ten individuals. Quercus (3 spe-

cies) was the most diverse genus, followed by

Eugenia (2 species). Considering those spe-

cies with ≥ 3 individuals, Acer binzayedii Y.L.

Vargas-Rodr. was the species with the biggest

DBH and Eugenia crenularis Lundell with the

smallest DBH; the tallest species corresponded

to Quercus uxoris McVaugh and the smallest

height to Cyathea costaricensis (Table 2).

IVI results revealed that 10 species, out

of the 27 recorded in the study plots, contrib-

uted with > 70 % to the total dominance in the

community; Cyathea costaricensis showed the

second higher IVI value (127 %) only after

Carpinus tropicalis (135 %); A. binzayedii

and P. reichei attained similar IVI’s (around

118 %); these dominant species were followed

by Quercus nixoniana S. Valencia & Lozada-

Pérez (100 %), Clusia salvinii (99 %), Conoste-

gia volcanalis (95 %), Clethra fragrans L.M.

González & R. Delgad. (93 %), Quercus uxoris

(83 %) and Ilex brandegeeana (75 %). The

remaining of the species reported IVI’s with

less than 50 % (Fig. 1).

Cyathea costaricensis, Carpinus tropicalis

and Podocarpus reichei were the most frequent

species, recorded in the seven plots, while 11

species with frequencies around 14 % were

present in only one plot. The same three species

with the highest relative frequency, were also

the most abundant. Acer binzayedii (around

26 %) and Carpinus tropicalis (21 %) were

the most dominant species according to their

relative basal area, while 21 species contrib-

uted with less than 5 % (Fig. 1). Trunk height

was variable among the ten species with the

highest IVI. Cyathea costaricensis showed the

smallest mean height, even smaller than those

shade-tolerant species commonly found in the

understory in our study area such as Clusia

salvinii and Conostegia volcanalis; the largest

mean heights were reported for Quercus uxo-

ris and Acer binzayedii; this last species also

showed the tallest individuals, with tree heights

up to 40 m. In terms of stem height, Carpinus

tropicalis and Quercus nixoniana showed the

greatest variation (Fig. 2A, Table 2). In terms

of DBH, C. costaricensis displayed an interme-

diate mean size when compared with the rest

of the species; highest values for DBH corre-

sponded to A. binzayedii, Q. uxoris, C. tropica-

lis and Q. nixoniana in that order of magnitude;

the highest DBH variation corresponded to A.

binzayedii and the lowest variation to C. cos-

taricensis (Fig. 2B, Table 2).

Structural variation by plot: The num-

ber of individuals for C. costaricensis varied

among plots, with plot 2 showing the highest

number of individuals (N= 18), followed by

plot 5 (N= 12), whilst the lowest number (N=

4) was present in plots 1 and 4; the smallest

mean for DBH, height and basal area cor-

responded to plot 2 and the highest to plot 6

(Table 3).

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TABLE 2

List of species present in the remnant cloud forest in west-central Mexico

Species Family Acronym N DBH Ht BA

Cyathea costaricensis (Met. ex

Kuhn) Domin

Cyatheaceae Cycos 62 11.32 ± 0.96 6.01 ± 0.48 0.03 ± 0.004

Carpinus tropicalis (Donn. Sm)

Lundell

Betulaceae Catro 50 17.76 ± 3.14 13.81 ± 2.28 0.09 ± 0.03

Podocarpus reichei J. Buchholz

& N.E. Gray

Podocarpaceae Porei 38 11.20 ± 2.74 9.09 ± 1.90 0.04 ± 0.02

Clusia salvinii Donn. Sm.

Clusiaceae Clsal 32 10.45 ± 1.95 7.21 ± 0.90 0.03 ± 0.01

Acer binzayedii Y.L.Vargas-

Rodr.

Sapindaceae Acbin 23 25.03 ± 10.27 15.28 ± 4.30 0.26 ± 0.20

Conostegia volcanalis Sandl. &

Steyerm.

Melastomataceae Covol 23 9.05 ± 1.69 7.28 ± 1.39 0.021 ± 0.008

Quercus nixoniana S. Valencia

& Lozada-Pérez

Fagaceae Qunix 19 17.11 ± 6.70 15.00 ± 4.55 0.10 ± 0.07

Clethra fragrans L.M. González

& R. Delgad.

Clethraceae Clfra 16 10.87 ± 2.40 9.88 ± 2.60 0.03 ± 0.01

Quercus uxoris McVaugh

Fagaceae Quuxo 13 20.68 ± 8.87 15.69 ± 5.43 0.14 ± 0.11

Zinowiewia concinna Lundell

Celastraceae Zicon 9 9.04 ± 2.23 9.33 ± 3.28 0.02 ± 0.009

Ilex brandegeeana Loes.

Aquifoliaceae Ilbra 7 10.62 ± 7.40 9.21 ± 5.16 0.03 ± 0.04

Eugenia crenularis Lundell

Myrtaceae Eucre 6 8.26 ± 3.41 9.00 ± 4.19 0.017 ± 0.013

Juglans major (Torr.) A.Heller

Juglandaceae Jumaj 6 15.05 ± 6.91 13.00 ± 9.29 0.05 ± 0.05

Inga laurina (Sw.) Willd.

Fabaceae Inlau 5 12.08 ± 6.58 11.3 ± 5.61 0.037 ± 0.04

Magnolia pacifica A. Vázquez

Magnoliaceae Mapac 3 13.5 ± 6.57 13.33 ± 15.17 0.04 ± 0.04

Prunus cortapico Kerber ex

Koehne

Rosaceae Prcor 3 13.76 ± 11.28 12.33 ± 6.23 0.05 ± 0.17

Quercus laurina Bonpl.

Fagaceae Qulau 3 9.36 ± 1.0 7.33 ± 3.79 0.019 ± 0.004

Dendropanax arboreus (L)

Decne. & Planch.

Araliaceae Dearb 2 * * *

Myrsine coriacea (Sw.) R. Br.

ex Roem. & Schult.

Myrtaceae Mycor 2 * * *

Perrottetia longistylis Rose

Dipentodontaceae Pelon 2 * * *

Saurauia serrata DC.

Actinidiace Saser 2 * * *

Symplocos citrea Lex. Ex La

Llave & Lex

Symplocaceae Sycit 2 * * *

Cordia prunifolia I.M. Johnst.

Boranginaceae Copru 1 * * *

Eugenia culminicola McVaugh

Myrtaceae Eucul 1 * * *

Persea hintonii C.K. Allen

Lauraceae Pehin 1 * * *

Pinus herrerae Martínez

Pinaceae Piher 1 * * *

Styrax radians P.W. Fritsch

Styracaceae Strad 1 * * *

N = Total number of individuals; DBH = Mean diameter at breast height (cm); Ht = Mean tree height (m.); BA = Mean

Basal Area (m

/ha). Confidence intervals (95 %) for DBH, Ht and BA. *Parameter estimation confidence intervals were not

computed as only two individuals were present.

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Height class frequency distribution pre-

sented an unbalanced pattern at plot level. The

coefficient of skewness, g1 was > 0 in all plots,

revealing a positive asymmetry; their values

were near to 1.0 in five (1, 2, 3, 6 and 7) of the

seven plots exhibiting very irregular patterns in

their distributions; on the contrary, plots 4 and

5 with higher g1values; the 2 words have to be

separated (2.75 and 2.35 respectively), showed

a reversed J-shaped with individuals mainly

concentrated over the smallest height classes

(between 7 to 11 m height) (Fig. 3). The high-

est number of C. costaricensis individuals were

in the intermediate height category in all plots,

while only plots 2 and 3 showed individuals in

the three height categories (mature, intermedi-

ate and juveniles). The tallest individuals corre-

sponded to A. binzayedii, Carpinus tropicalis,

Quercus uxoris and Q. nixoniana in all plots,

while Clusia salvinii and Conostegia volca-

nalis were also recurrent with small values in

height (Fig. 3).

DBH class frequency distribution was

moderately characterized by the classic

J-shaped in plots 2, 4 and 5; this represents a

large number of small- to middle diameter size

classes of intermediate to shade tolerant spe-

cies. The coefficient of skewness (g1) revealed

that all the studied plots showed positive asym-

metry, reinforcing that individual over smaller

DBH classes dominated the plots (Fig. 4).

Most of the species contained individuals

in 10, 15 and 20 cm DBH classes; C. cos-

taricensis individuals were also concentrated in

these DBH classes in the seven plots. Only few

old-growth trees (corresponding to A. binzaye-

dii, C. tropicalis, Q. uxoris and Q. nixoniana)

were recorded with diameters higher than 40

Fig. 1. Importance Index Value (IVI) of the species present in the remnant cloud forest in West-central Mexico. Percentage

values are displayed in descending order for IVI, Relative Basal Area (BA), Relative Density and Relative Frequency.

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cm. In certain plots, some of the species with

the highest IVI, were represented in all DBH

categories; for instance, A. binzayedii and

Carpinus tropicalis in plot 1, Q. uxoris and

Clethra fragrans in plot 3, Clusia salvinii in

plot 5 (Fig. 4).

Structural comparison of Cyathea cos-

taricensis with canopy dominant species:

Heights for C. costaricensis ranged from 2.0 to

10.5 m with marked differences in number of

individuals by height class. The intermediate

class reported the highest number of individu-

als (N= 43), followed by the mature class (N=

15) and the juvenile class (N= 4). The highest

contribution in basal area (1.060 m

) was esti-

mated for the intermediate class (Fig. 5A). The

coefficient of asymmetry (g1) was very close to

zero (g1= 0.06) representing a symmetric distri-

bution; however, results from the Shapiro-Wilk

Fig. 2. Box and whisker plots representing quartiles for A. Height and B. DBH of the species with Importance Index

Values > 70 %.

TABLE 3

Structural variables for Cyathea costaricensis by plot in the remnant cloud forest, West-central Mexico

Plot Number of individuals Mean DBH (cm) Mean Height (m) Mean Basal Area (m

/plot)

1 4 12.4 6.5 0.013

2 18 8.7 4.7 0.006

3 8 10.0 5.6 0.009

4 4 12.1 6.1 0.012

5 12 13.5 6.9 0.014

6 9 13.6 7.1 0.015

7 7 11.6 6.3 0.011

CI 8.8 ± 3.64 11.32 ± 0.96 6.01 ± 0.48 0.011 ± 0.001

CI = confidence intervals at 95 %.

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normality test revealed that height was not

normally distributed (P < 0.0001).

Regarding frequency distribution for the

canopy-dominant species, the Shapiro-Wilk

normality test revealed that height was not nor-

mally distributed (P < 0.0001) as well.

A key difference emerged between the

kernel probability density function of C. cos-

taricensis population (around 0.25) and the

canopy-dominant species with the highest IVI

(< 0.10); in both cases, the highest probability

was detected for heights < 10 m (Fig. 5B).

The results of the Wilcoxon rank sum test

showed statistically significant differences in

height between C. costaricensis population

and the canopy-dominant species (W= 10018,

P < 0.0001).

Concerning DBH, C. costaricensis ranged

from 5 to 19.5 cm, consequently it was only

distributed in the first 4 classes (5, 10, 15 and

20 cm) of the eight reported for the rest of the

canopy-dominant species; even that coefficient

of skewness was negative (g1= -0.176) suggest-

ing a negative asymmetry with most individu-

als in the 15 cm class, its value proximate to

zero also indicates symmetry in the distribution

which is representative of a normal distribu-

tion (Fig. 5C); results which were corroborated

with the Shapiro-Wilk normality test for DBH

(P= 0.1335). For the canopy-dominant species,

the Shapiro-Wilk normality test revealed that

Fig. 3. Height class frequency distribution by plot considering the ten species with Importance Index Values > 70 %. g1 =

coefficient of skewness.

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DBH frequency distribution was not normally

distributed (P < 0.0001).

Results of the comparison using the kernel

probability density function, exposed that both

density-plots coincided in DBH < 25 cm. C.

costaricensis probability was nearly 0.1 and for

the rest of the species < 0.075. For DBH > 25

cm, the rest of the most important species (IVI

> 70 %) presented irregular probabilities with

values under 0.025 (Fig. 5D). The results of the

Wilcoxon rank sum test showed no statistically

significant differences in DBH between C. cos-

taricensis population and the canopy-dominant

species (W= 6954, P < 0.8511).

Environmental characterization: The

environment surrounding the cloud forest

where C. costaricensis population occurs,

showed important differences among plots,

mainly in physiographic and light variables

(Table 4). Elevation ranged from 1 663 to 1

745; slope percentages ranged from 0 to 39 %,

with high variation according to confidence

intervals (16.75 ± 12). We did not observe dif-

ferences in topography; hence all the plots were

established over uneven terrains located on the

base of slope terrains (Table 4). For rocks and

stones, the mode was 0, representing absence of

these materials on the forest floor; for canopy

strata, three vertical strata characterized most

of the plots according to the mode value; none-

theless four canopy strata were observed in two

plots (Table 4). In the case of light variables,

our results showed slight dissimilarities among

Fig. 4. Diameter at Breast Height (DBH) class frequency distribution by plot considering the ten species with Importance

Index Values > 70 %. g1 = coefficient of skewness.

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plots (Table 4). Canopy openness ranged from

3.97 to 7.83 %, extending only 1.13 % from

the mean (5.28 %), leaf area index ranged from

2.72 to 3.99 (m

-2

), Photosynthetic Photon

Flux Density and Total Radiation Over Canopy

values ranged from 2.18 to 7.81(μmol/s-m

)

and from 35.95 to 60.09 (MJ/m

day) respec-

tively (Table 4).

DISCUSSION

Floristic composition characterization:

The canopy species composition associated to

C. costaricensis in our study area was repre-

sented by the typical cloud forests reported for

Mexico; this vegetation type is characterized

by a high number of species and high structural

complexity (Carvajal-Hernández et al., 2018;

Rosas Rangel et al., 2019). Our results showed

a combination of very abundant (Carpinus

tropicalis) with sparse species (Magnolia paci-

fica A. Vázquez, Quercus laurina Bonpl.) in all

the plots. We also found a number of species

with low number of individuals (Eugenia cul-

minicola McVaugh, Saurauia serrata DC, Myr-

sine coriacea (Sw.) R. Br. ex Roem. & Schult.),

which is a common feature of highly diverse

cloud forests in Western Mexico (Morales-

Arias et al., 2018). The remnant forest in our

study area is particularly diverse, characterized

by species typical of cloud forests of such as:

Carpinus tropicalis Magnolia pacifica, Matu-

daea trinervia Lundell, Podocarpus reichei,

Ostrya virginiana (Mill.) K. Koch, Abies gua-

temalensis subsp. jaliscana (Martínez) Silba

and Zinowiewia concinna Lundell (Vargas-

Rodríguez et al., 2012). This vegetation type

has been present in our study area with a rela-

tively similar species composition assembly

since 1230 AD, dominated in the canopy by

Acer-Podocarpus-Abies with Cyathea popula-

tion in the understory; cyclical environmental

changes had maintained this relict community

over the last millennium (Del Castillo-Batista

et al., 2016).

Community and population structur-

al characterization: Our structural analysis

TABLE 4

Summary of environmental variables per plot

Plot Sto Rck CStr

Light variables

TRUC

(MJ/m

day)

DiR

(%)

DfR

(%)

Elevation

(m asl)

Slope

(%)

Aspect

(degrees)

Top

(%)

CGF

(%)

LAI

-2

)

PPFDu

(μmol/s-m

)

TROC

(MJ/m

day)

1 0 1 4 1704 39 0.20 2 4.24 3.93 3.98 7.81 35.95 3.47 89.43 10.56

2 3 0 3 1745 0 1.70 2 5.39 5.09 3.39 4.8 59.39 5.28 87.38 12.61

3 0 0 4 1663 20 1.68 2 3.97 3.7 3.76 6.08 56.76 5.546 90.32 9.67

4 0 0 3 1745 19 1.12 2 7.83 7.38 2.72 2.18 58.72 7.17 86.88 13.11

5 0 0 4 1740 19 1.79 2 6.34 6 2.77 6.84 57.39 3.97 81.47 18.52

6 1 2 3 1723 21 1.70 2 5.35 5.71 2.94 4.84 60.09 8.33 90.88 9.11

7 0 1 3 1717 0 1.70 2 3.90 4.2 3.99 5.79 59.27 6.13 90.21 9.78

CI/mode 0 0 3 1719.5 ± 27 16.75 ± 12 1.41 ± 0.5 2 5.28 ± 1.13 5.14 ± 1.22 3.36 ± 0.52 5.47 ± 1.66 55.36 ± 7.99 5.69 ± 1.54 88.08 ± 3.04 11.90 ± 3.04

Top = Topography (1: Even terrain, 2: Uneven terrain); Sto = Stones (0: Absence, 1: Hardly visible, 3: Moderate); Rck = Rocks (0: Absence, 1: Hardly visible, 2: Scarce); CStr =

Canopy strata (3: Three vertical strata, 4: Four vertical strata); CO = Canopy Openness; CGF = Canopy Gap Fraction; LAI = Leaf Area Index; PPFDu = Photosynthetic Photon Flux

Density Under the Canopy; TROC Total Radiation Over Canopy; TRUC = Total Radiation Under Canopy; DiR = Direct Radiation; DfR = Diffuse Radiation. CI/mode = confidence

intervals at 95 % for continuous variables/mode for categorical variables.

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results suggested that most of the plots dis-

played a DBH distribution resembling a reverse

J-shaped curve (de Liocourt, 1898; Meyer,

1952), declining monotonically as DBH

increased. Ecologically, this curve is explained

by equal mortality rates among diameter

classes across the entire range of diameters

(Westphal et al., 2006), but this curve is also

a common DBH pattern showed by tropical

and cloud old-growth forests of shade-tolerant

species (Rzedowski, 1978; Whitmore, 1998).

In contrast, DBH distribution including only

C. costaricensis population, showed a bell-

shape resembling a normal distribution, a result

which was tested by the Shapiro-Wilks test; in

contrast, trunk height was not normal accord-

ing to the test, even when the symmetry of the

curve was positive showing an approximation

to the bell-shape distribution. Therefore, we

could not confirm the hypothesis posed in this

Fig. 5. A. Height class frequency distribution for Cyathea costaricensis population, B. Kernel probability density plot for

height for Cyathea costaricensis (blue line) and the canopy-dominant species with IVI > 70 % (red line), C. DBH class

frequency distribution for Cyathea costaricensis population, D. Kernel probability density plot for DBH for Cyathea

costaricensis (blue line) and the canopy-dominant species with IVI > 70 % (red line).

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research where we assumed that C. costaricen-

sis will follow a reversed J-shape in terms of

DBH and height sizes.

Dynamic populations, which can be char-

acterized by a bell-shape, have been reported

for several tree ferns: Dicksonia sellowiana

(Schmitt et al., 2009), Alsophila firma (Mehl-

treter & García-Franco, 2008) Cyathea fulva

(Pérez-Paredes et al., 2014) and C. henryi

(Baker) Copel. (Balkrishna et al., 2020). A

dynamic population behavior is generally attrib-

uted to a continuous regeneration pattern with

good recruitment along time (Schmitt & Win-

disch, 2007), together with cycles of recruit-

ment during successive episodes of canopy gap

formation (Arens, 2001). However, an opposite

trunk height pattern is also common in several

tree ferns: for Alsophila spinulosa (Wall. ex

Hook.) R.M. Tryon, located on the Eastern

coast of Japan, Nagano and Suzuki (2007)

reported a J-shaped trunk height frequency

distribution, with the number of individuals

gradually decreasing as the height increased. A

similar pattern was reported for Cyathea brun-

oniana (Wall. ex Hook.) C.B. Clarke & Baker

and C. henryi in Northeast India, but consider-

ing the diameter size (Balkrishna et al., 2020).

This pattern of distribution is indicative of a

stable population structure with a successful

natural seedlings-saplings-adults replacement

(Balkrishna et al., 2020). Habitat quality and

anthropogenic impacts are significant factors

determining the population size of tree ferns

(Praptosuwiryo, 2011). Mehltreter and García-

Franco (2008) reported a low frequency of

individuals in the smallest height size classes in

Alsophila firma, in Veracruz Mexico, linked to

a constraint of micro-sites and to anthropogenic

disturbances hindering a successful regenera-

tion establishment or the lack thereof, as some

light-demanding tree fern species (e.g. Cyathea

medullaris (G. Forst.) Sw.) prefer disturbances

to regenerate and for their establishment (Bys-

triakova et al., 2011).

In the present study, the low number of

individuals of C. costaricensis in the < 3 m

height class could be explained by: 1) the poten-

tial failure of tree fern natural regeneration due

to the paucity of available micro-sites; tree

ferns recruitment success may be determined

by habitat suitability to a larger degree, rather

than their subsequent survival (Jones et al.,

2007); 2) the impact of frequent forest fires,

uncontrolled grazing and frequent tourist visi-

tation (personal observations), could have neg-

ative impacts, not only in the C. costaricensis

population structure, but also in the structure

of the co-occurring canopy-dominant species,

as it was previously discussed. Cyathea cos-

taricensis in our study area is not involved in

silvicultural activities; nevertheless, they are

collected for ornamental uses, mainly through

the direct cutting of their saplings. In the

Philippines, tree ferns are extracted for com-

mercial and medicinal purposes and even for

household utility (Dadang et al., 2020). As a

result of the constant tree fern “harvesting”,

their populations are gradually declining; these

practices are contributing to a restricted popu-

lations distribution, mainly due to habitat loss

and overexploitation (Kholia & Joshi, 2010).

This overexploitation is plausible to be tak-

ing place in our study area, no in an intensive

manner but commonly individual by individual

by tourist visitations, this could explain why

population size of C. costaricensis in our study

area is small and even fragmented. A number

of tree ferns, mainly of the Cyatheaceae fam-

ily (e.g. Cyathea srilankensis Ranil, C. sledgei

Ranil, Pushpak. & Fraser-Jenk, C. sinuata

Hook. & Grev., and C. hookeri Thwaites) are

area-specific and they are usually confined to a

few localities; as a consequence of such area-

specific requirements, their population sizes

are frequently small (Ranil et al., 2017).

The typical reversed J-shaped was not

observed for DBH or trunk height when plot-

ting C. costaricensis population alone; how-

ever, the comparison of the kernel probability

density function of C. costaricensis with the

most important canopy-dominant species,

exposed the shade tolerant behavior of this tree

fern; the evidence is suggested as most of the

canopy-dominant species of the remnant cloud

forest in West-central Mexico were taller than

C. costaricensis and by the fact they occupy

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the highest canopy strata; a high probability

of occurrence was associated with tree ferns

smaller than 11 m tall which consistently

inhabit the lower strata in the study area. This

structure is probably enabling the understory

colonization by C. costaricensis individuals

due to the recognized shade-tolerant behavior

reported for some Cyathea species (Bystriako-

va et al., 2011). This result was also corroborat-

ed by the Wilcoxon non-parametric test which

showed statistically significant differences for

height between C. costaricensis individuals

and the canopy-dominant species, confirming

the hypotheses established in this study.

The environment surrounding Cyathea

costaricensis: Interesting results emerged on

the assessment of the environment where C.

costaricensis grows: concerning the physio-

graphical variables, we found individuals of

this species growing in dissimilar percent-

ages of slope terrain inclination and aspect

orientation, but this mostly occurred on uneven

terrains located at the base of the slope inclina-

tion. Studies undertaken on tree fern ecology

have revealed that habitat specialization is cru-

cial for their occurrence; particularly the results

reported by Jones et al. (2007) on four species

of tree ferns of the Cyatheaceae family; these

authors unveiled the importance of soil chemi-

cal variables for tree fern growth, followed by

their position on the slope terrain inclination

and stand structural characteristics; they report-

ed tree fern individuals growing at lower topo-

graphical positions such as riparian areas and

stream valleys, similar to the location where

C. costaricensis was observed to grow in our

study. With respect to light variables, C. cos-

taricensis was present in relatively similar light

values across the seven plots. But we did not

observe a pattern in which high values percent-

ages of Canopy openness were associated to a

high or a low number of tree fern individuals or

were associated to big or small DBH and height

size; however, mean canopy openness values

in our study plots resemble those reported

(1.07-4.05 %) for other Cyatheaceae (Cyathea

medullaris; a synonymous of Sphaeropteris

medullaris (G. Forst.) Bennh. and C. dealbata

(G. Forst.) Sw.) species in New Zealand (Brock

et al. 2019). Total Radiation Under Canopy val-

ues in this study (5.69 ± 1.54 MJ/m

day) was

also similar to the values (5.8 to 6.5 MJ/m

day)

reported in that study.

Conclusions: The structure of canopy-

dominant species and the C. costaricensis

population differed in height and DBH class

distribution. We verify the hypothesis of simi-

lar structure between the canopy-dominant

species and the C. costaricensis population

only for DBH; in the horizontal stratum, C.

costaricensis is coexisting with shade-tolerant

species of the remnant cloud forest showing

similar sizes in DBH < 25 cm. On the contrary,

there were statistical significant differences

for trunk heights, the small statures of C. cos-

taricensis allow their coexistence in the under-

story through the sheltering from the taller

canopy-dominants.

Furthermore, the disjunct distribution in

this relict forest, along the rather small popula-

tion requires an appeal for its strict protection.

Most, if not all individuals of C. costaricensis

are confined to local environmental condi-

tions, particularly to physiography. During

our fieldwork we did not find any individuals

of this species over fully open forest canopy

gaps. Thus, habitat specialization, as it has

been reported for a number of tree ferns else-

where, could be the reason to explain why

the C. costaricensis population size in our

study area is small. The results of this paper

are valuable for the conservation of this relict

forest, in particular for Cyathea costaricensis

tree fern population. Hence, conservation (e.g.

protection against illegal harvesting, control of

human visitation, protection against frequent

uncontrolled forest fires, etc.) and management

(e.g. build a forest management program for

the area) strategies should be implemented in

view of the limited area occupied by C. costari-

censis and the constantly increasing levels of

human-induced disturbances such as frequent

forest fires, uncontrolled recreation visitation

and the impact of climate change.

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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 thank to José Guadalupe Arias Morales

and Maxy Adrian Hernández Araiza for their

valuable help during the fieldwork; José Gua-

dalupe also helped us to identify the most of

species. We also thank the Editors and three

anonymous reviewers for their valuable com-

ments and suggestions which substantially

improved the first version of this paper.

RESUMEN

Composición florística, estructura y caracterización

ambiental de una población de Cyathea costaricensis en

un relicto de bosque mesófilo de montaña en México

Introducción: Los helechos arborescentes son compo-

nentes importantes de los bosques templados, tropicales

y subtropicales, que contribuyen a dar forma a rodales de

estructuras complejas.

Objetivos: 1) Describir la estructura poblacional de

Cyathea costaricensis en un remanente de bosque nuboso

del centro-oeste de México; 2) Caracterizar y relacionar

la composición florística y la estructura de las especies

arbóreas más importantes asociadas a la población de C.

costaricensis y; 3) Describir el ambiente donde se encuen-

tra C. costaricensis.

Métodos: Estimamos el Índice de Valor de Importancia

(IVI) para seleccionar las especies dominantes más impor-

tantes del dosel asociadas a C. costaricensis; para las espe-

cies seleccionadas según IVI, construimos distribuciones

de frecuencia de alturas y diámetros a la altura del pecho

(DAP), así como para la población de C. costaricensis.

Calculamos la asimetría de las distribuciones de frecuencia

a través del coeficiente de asimetría y la función de den-

sidad de probabilidad mediante la estimación de densidad

de Kernel. Probamos las diferencias entre las especies de

árboles dominantes en el dosel y la estructura de la pobla-

ción de C. costaricensis mediante la prueba no paramétrica

de suma de rangos de Wilcoxon.

Resultados: los individuos de C. costaricensis presentaron

las menores alturas y tamaños intermedios de DAP en com-

paración con las especies dominantes del dosel, con dife-

rencias estadísticamente significativas para la altura, pero

no para el DAP según la prueba de Wilcoxon. La mayoría

de los individuos de helechos arborescentes se ubicaron en

terrenos irregulares y sobre la pendiente baja del terreno.

Los valores de apertura del dosel y Radiación total bajo el

dosel fueron similares a los reportados para las especies de

Cyathea en otros lugares.

Conclusiones: Confirmamos la hipótesis de que hay una

estructura similar entre las especies dominantes del dosel

y la población de C. costaricensis solo para el DAP; por el

contrario, para la altura del fuste, hubo diferencias estadís-

ticamente significativas; las pequeñas alturas de C. costa-

ricensis sugieren su coexistencia en el sotobosque a través

de la cobertura árboles dominantes del dosel. La mayoría

de los individuos de C. costaricensis fueron encontrados

confinados a condiciones ambientales locales, en particular

a la fisiografía.

Palabras clave: helechos arborescentes; estructura pobla-

cional; composición de especies del dosel; forma de J

invertida; categorías de altura; ambiente local.

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