NovaHedwigia 67 1—2 125—138 Stuttgart, August 1998

Succession of epiphytic bryophytes in a Quercus pyrenaica forest

from the Spanish Central Range (Iberian Península)

by

Francisco Lara and Vicente Mazimpaka

Departamento de Biología (Botánica). Facultad de Ciencias.

Universidad Autónoma de Madrid. Cantoblanco. 28049 Madrid (Spain)

With 5 figures and 1 table

Lara, F. & V. Mazimpaka (1998): Succession of epiphytic bryophytes in a Quercus pyrenaica forest

from the Spanish Central Range (Iberian Peninsula). - Nova Hedwigia 67: 125-138.

Abstract: Succession among epiphytic bryophytes is studied in a deciduous forest of Quercus pyrenaica

Willd. from the Spanish Central Range, with the objective of assessing fluctuations of species and life-

forms throughout the life-span of trees. For this purpose, an indirect method is used, which consists of

studying epiphytes occurring on different-aged trees. Additionally, a new index, called the "índex of

Ecological Significance (ÍES)" and derived from a combination of relative frequency and mean cover,

is used to evalúate the ecological importance of taxa in epiphytic habitats.

Results show qualitative and quantitative changes in epiphytic community composition during the tree

life-span. Young trees are colonized by pioneer species. Some of them become more extensive on

older trees, while others disappear, and a group of additional species occur exclusively on oíd trees.

Similarly, species richness and bryophytic cover increase with tree age, while community composition

and structure change, due to species and life-form replacement. These changes take place in a similar

way on bases and trunks, although the former are always bryofloristically richer. As for successional

patterns, both bases and trunks feature a main lineal and allogenic series, which is completed by a

secondary cyclic and autogenic series that is restricted to oíd trees.

Resumen: Se ha estudiado la sucesión de los briófitos epífitos en un bosque de Quercus pyrenaica

Willd. en el Sistema Central español, con la finalidad de conocer las fluctuaciones de especies y de

formas de vida que tienen lugar durante el crecimiento del árbol. Para ello, se ha utilizado un método

de estudio indirecto, consistente en el análisis de la cubierta briofítica de árboles de diferentes edades.

Para expresar la importancia de cada briófito en las comunidades epifíticas, se ha utilizado un nuevo

índice, al que se ha denominado "índice de significación ecológica", el cual resulta de la combinaciónde la frecuencia relativa y la cobertura media de cada especie.

Los resultados muestran cambios cualitativos y cuantitativos en la composición de las comunidades

briofiticas epífitas durante el crecimiento de los árboles. Los más jóvenes son colonizados por especies

pioneras, algunas de las cuales se mantienen en los árboles de más edad, mientras que otras desaparecen

y un grupo de especies adicionales aparecen restringidas a los árboles más viejos. Del mismo modo, la

riqueza y el recubrimiento briofíticos aumentan con la edad de los árboles, a la vez que se producen

cambios en la composición y estructura de las comunidades epifíticas. Estos cambios se producen de

modo similar en las bases y en troncos, aunque aquellas son brioflorísticamente más ricas. En cuanto

a los patrones sucesionales, tanto las bases como los troncos presentan una serie principal de carácter

alogénico, la cual se complementa con una serie cíclica secundaria autogénica, restringida a los árboles

más viejos.

0029-5035/98/0067-0125 $ 3.50©1998 J. Cramer in der Gebrüder Borntraeger

Verlagsbuchhandlung, D-14129 Berlín • D-70176 Stuttgart

125

Introduction

The evolution of epiphytic vegetation over the life-span of trees has been studied in

températe humid áreas (Olsen 1917, Quaterman 1949, Phillips 1951, Barkman 1958,

Slack 1976, Smith 1982, Studlar 1982b, Stone 1989, McCune 1990,1993). Observed

changes affect species type and dominance, inducing succession of communities.

These changes are climate and phorophyte-type dependent, but are in general more

closely related to modifications of bark characteristics and microclimate of epiphytic

habitáis. As the tree matures, bark undergoes changes affecting rugosity, peeling,

hardness, water retention, dust deposition and chemical properties. Additionally,

changes in tree architecture modify the microclimate of epiphytic habitáis. Thus,

variation in crown morphology and leaf density are very important due to their

influence on light and water supply to the different tree strata. Finally, interspecifíc

relationships among corticolous bryophytes (e.g., interactions due to competition or

facilitation) and microenvironmental changes induced by epiphytes modify the

composition and physiognomy of corticolous communities (Barkman 1958).

In Mediterranean áreas, studies of structure and composition of bryophytic commu

nities growing on two tree-stands of different ages (Hébrard 1987,1989) have demon-

strated the existence of qualitative changes, but little is known about successional

trends among epiphytic bryophytes. The work presented here focuses on epiphytic

bryophytes growing on bases and trunks of 3 different-aged groups of Quercus

pyrenaica trees from the same forest. Its aim was to study the evolution of species

richness and dominant life-forms on these trees, and thus describe successional trends

and infer the ecological factors governing these changes.

Methods

Epiphytic succession can be studied using direct or indirect methods. The former consists of establishing

permanent quadrats on young trees and surveying their evolution over tree lifetimes. This method is

impractical, since it takes too much time. Another direct method consists of studying bryophyte

establishment and succession on branches of different ages (Stone 1989), but results are partial for they

only involve the peripheral área of trees, which, in Mediterranean áreas, is very poor in bryophytes

(Mazimpaka & Lara 1995). Most studies on epiphytic succession have used an indirect method that

consists of studying epiphytic vegetation of trunks of different ages. This is the method used in this

study, since we think that it is the most reliable and suitable to the Mediterranean área.

Study área

As phorophyte characteristics and epiphyte interactions are both climate-dependent,

studied trees must belong to a climatically homogeneous área. In accordance with

this criterion, a 0.5 ha área was defined in a Quercus pyrenaica forest from the Sierra

de Guadarrama, in the Spanish Central Range. The forest is located on a NE mountain

slope near Lozoya del Valle (Madrid, 40°58'00"N, 3°49'40"W, 1600 m). It is a well

conserved deciduous formation growing in a mountainous zone where Mediterrane

an conditions are somewhat mollified by the altitudinal effect. Estimates based on

data from neighbouring meteorological stations suggest an annual precipitation

126

average of 900 mm, with equinoctial máxima, and a strong water déficit in summer

(records of July and August rainfall do not reach a 50 mm monthly average). Mean

annual temperature is approximately 8-9°C and mean monthly temperature is around

18°C in summer months. According to Rivas-Martínez (1987), it could be classifíed

within the supramediterranean subhumid belt.

Sampling procedures

Quercus pyrenaica trees were assigned to three classes, on the basis of trunk diameter,

measured at 1 m from the ground: young (< 15 cm), middle-aged (25-35 cm) and

oíd trees (70-85 cm). Ten trees from each class were sampled. On each tree, bryophytes

were collected from 4 dm2 quadrats from two zones: Lower base (10-30 cm above

ground), and trunk (150-170 cm). A total of 60 samples were collected. Before

removal of samples, total bryophyte cover of each quadrat was estimated for subse-

quent calculation of cover of each species in the laboratory.

Data processing

Different parameters have been employed as measures of the importance of taxa in

epiphytic communities and habitats (for review, see Bates 1982). Frequency and

cover are the most commonly used, while a few authors have used the biomass

(Rhoades 1981, Nadkarni 1984, McCune 1990). Finally, some authors have devised

Índices combining frequency or cover with another parameter. For example, Stringer

& Stringer (1974) developed the Prominency índex (PI), that combines mean cover

of a species in a tree face and the height reached by the species in that face. Studlar

(1982a) proposed the índex of Dominancy (ID), intended to indicate the importance

of the 3 most abundant epiphytes. The index is of limited use in ecology, and the

author herself suggested that a combination of frequency and cover was the most

appropriate. Schmitt & Slack (1990) used the Prominency Valué (PV) to quantify

the importance of an epiphyte at a given site. This valué is product of absolute

frequency and relative cover of a species (Slack et al. 1980). This index yields

valuable results concerning the importance of taxa, but the use of absolute frequency

limits the possibilities of comparing results from different studies, since it requires

an identical number of samples. In this paper, a new index, the índex of Ecological

Significance (ÍES) is used. It is based on the combination of the relative frequency

and the mean cover of a species at a given site or habitat in the following way:

ÍES = F + FC or, in other way, ÍES = F (1 + C).

F (relative frequency) = lOOx/n and C (mean cover) = Zc./x, where x represents the

number of samples containing the species, n the total number of samples, c. the

cover class attributed to the species in each sample. In fact, percentage valúes of

cover were grouped into 6 classes according to the following scale: 0.5 (<1%); 1 (1-

5%); 2 (6-25%); 3 (26-50%); 4(51-75%); 5 (>75%). Development of the previous

formula gives: ÍES = (100 x/n) + [(100 x/n) (¿c./x)] or ÍES = (100 x/n) + (100 £ c./n), that simplifies to

127

ÍES = 100/n (x + I c.).

The index yields valúes between O and 600, but in practice, valúes over 400 are very

rare, since they represent a consistent and almost absolute dominance of the taxon.

In general, valúes over 50 reveal a significant ecological importance. Ecologically,

this index is similar to the Prominency Valué of Slack et al. (1980), but use of

relative frequency allows comparability of valúes. Overvaluation of the frequency is

intended to avoid the distortion resulting from the fact that occasional taxa (with a

small record number) with extensive cover (e.g., some facultative pleurocarpous

mosses) could show much higher ÍES valúes than those of taxa more frequent, but

with less extensive cover (e.g., most Orthotrichum species).

Results

Species richness and succession

Twenty bryophytes (18 mosses and 2 liverworts) were found at the studied site

(Table 1). The acrocarpous group is represented by 11 mosses belonging to Ortho-

trichaceae, Pottiaceae and Bryaceae, whereas 7 mosses from the Brachytheciaceae,

Hypnaceae, Leucodontaceae and Leskeaceae represent the pleurocarpous group. This

taxonomic make-up (the families represented, the dominance of mosses over hepatics

and the predominance of the acrocarpous group) and especially, the dominance of

Orthotrichaceae are features of most Mediterranean epiphytic bryophyte communities.

Table I. Epiphytic bryophytes found in the studied site. Life-form types follow Mágdefrau (1982). B:

base. T: trunk. Y: young trees. MA: middle-aged trees. O: oíd trees. (*): all possibilities within each

column.

TAXA

Radula complanata (L.) Dum.

Porella platyphylla (L.) Pfeiff.

Tortula laevipila (Brid.) Schwaegr.

Tortula princeps De Not.

Tortula virescens (De Not.) De Not.

Bryum súbelegans Kindb.

Orthotrichum affine Brid.

Orthotrichum lyellii Hook. & Tayl.

Orthotrichum rupestre Schwaegr.

Orthotrichum speciosum Nees

Orthotrichum striatum Hedw.

Orthotrichum stramineum Brid.

Zygodon rupestris Lor.

Antitrichia californica Sull.

Antitrichia curtipendula (Hedw.) Brid.

Leucodon sciuroides (Hedw.) Schwaegr.

Pterigynandrum filiforme Hedw.

Brachythecium velutinum (Hedw.) B. & S.

Homalothecium sericeum (Hedw.) B. & S.

Hypnum cupressiforme Hedw.

LIFE-FORM

TYPES

mat

mat

short turf

short turf

short turf

shortturf

cushion

cushion

cushion

cushion

cushion

cushion

cushion

tail

mat

tail

tail

mat

mat

mat

COLONIZED

STRATA

B

B

T*

*

*

*

B*

*

B

*

B

*

*

B

B

B

AGEOF

TREES

MA

MA-O

O

O

O

O*

*

*

Y-MA*

MA-O

O

O

Y

*

*

Y-MA

MA-O*

128

Nineteen species (all but Tortula laevipila which was exclusively found on oíd trunks)

were found on tree bases, where communities were consistently dominated by the

pleurocarpous Pterigynandrum filiforme and Leucodon sciuroides. In contrast, only

13 species were found on trunks. Most of them were Orthotrichum species that may

become dominant on this stratum, except on oíd trunks where they are replaced by

the two pleurocarpous species that are dominant on bases. Tree bases have a higher

bryophytic cover than trunks, although both show a relatively large surface devoid

of bryophytes. However, bryophyte cover increases with tree age, so that the bryo-

phyte-free área declines notably on oíd trees. Except for the mat-type which was

restricted to bases, all life-form types were present on both strata. The changes in

species composition and life-form dominance are described below.

Pterigynand. filiforme

Leucodon sciuroides

Orthotrichum lyellii

Orthotrichum rupestre

Brachythec.velutinum

Orthotrichum affine

Orthotrichum striatum

Hypnum cupressiforme

Orthotrichum speciosum

Antitric. curtipendula

Porella platyphylla

Radula complanata - *

Homalothecium sericeum

Bryum subelegans

Tortula princeps

Orthotrich. stramineum

Tortula virescens

Zygodon rupestris -^¡

Antitrich. californica

ÍES 100 200 300 400

Tres diameter

E3(O-15cm) ■(25-35cm) ■ (70-85cm)

Fig. 1. Comparative representation of ÍES valúes of bryophytic species from bases of different-

trees.

Tree base

Ten bryophytes were collected from young trees (Fig. 1). Pterigynandrum filiforme

was the most frequent and abundant, followed by Orthotrichum lyellii, Hypnum

cupressiforme, Orthotrichum rupestre, O. affine, O. striatum and Leucodon sciuroides.

Antitrichia curtipendula and Brachythecium velutinum were less frequent (high I.E.S.

129

valúes were due to their extensive cover). Twelve bryophytes were collected from

middle-aged trees. Pterigynandrum filiforme was still the most dominant, followed

by Hypnum cupressiforme, Orthotrichum lyellii, O. striatum, O. affine and O. rupestre.

Some liverworts - Porella platyphylla and Radula complanata - occurred sporadically.

Finally, fourteen taxa were found on oíd trees. Pterigynandrumfiliforme and Leucodon

sciuroides were the dominant species, while Homalothecium sericeum, Bryum sub-

elegans, Tortula princeps and Orthotrichum striatum were also highly represented.

These data suggest that tree base communities are floristically rich but physiognomically

dominated by a small number of bryophytes. In the course of phorophyte growth,

this richness increases progressively. However, this is not a simple progression of

species number and abundance, but several overlapping evolutionary trends, which

may be summarized as follows:

1. Several bryophytes - Orthotrichum lyellii, O. affine, O. striatum, Hypnum cu

pressiforme - found on young trees (primary colonists or pioneer) increase their

frequency and cover on middle-aged trees, but their importance declines on oíd

trees, where some of them (e.g., Orhotrichum rupestre and Brachythecium velutinum)

disappear.

2. Two mosses, Orthotrichum speciosum and Antitrichia curtipendula, present on

young trees, decline on middle-aged trees and are absent on oíd ones.

3. Only two primary colonists become significantly more important as the diameter

of trees increases: Pterigynandrumfiliforme and Leucodon sciuroides. These become

codominant on oíd trees.

4. Some taxa occur for the first time on middle-aged trees (secondary colonists) and

show a varying evolution on further tree stages: Homalothecium sericeum becomes

more abundant on oíd trees, whereas Porella platyphylla declines and Radula com

planata disappears.

5. Some bryophytes have been found exclusively on oíd trees (tertiary or final col

onists): Bryum subelegans, Tortula princeps, Orthotrichum stramineum, Antitrichia

californica, Tortula virescens and Zygodon rupestre.

Analysis of life-form types and their replacement during the tree lifetime allows the

profile of bryophytic succession to be completed (Studlar 1982b), and gives an

accurate idea of the structure of epiphytic communities (Iwatsuki 1960). One striking

result of our study is the large bryophyte-free área on young and middle-aged trees

(Fig. 2). This área, which is generally dominated by lichens, decreases in the later

stages of tree life-span, comprísing only 12% of the total área of oíd trees. Conversely,

áreas of tail mosses increase from 19% on young trees to 66% on oíd ones. The

cover of mat-type mosses rises from 7% on young trees to 14% on middle-aged

ones, and to 12% in final communities of oíd trees. Cushion-type mosses are relatively

abundant on young trees (5%), but are reduced to vestigial forms in communities of

middle-aged and oíd trees. Finally, short-turf forms occur only on oíd trees where

they are relatively abundant (7%).

130

Cover (%)

100 f

60

40

20

bryophyte-free áreatails

-short turfs

YOUNG TREES MIDDLE-AGED TREES OLD TREES

Fig. 2. Evolution of life-form cover on bases.

Trunks

Only three mosses (Orthotrichum lyellii, O. striatum and O. ajfine) occur on young

trees, which are characterised by a low bryophytic cover (Fig. 3). In addition to

these mosses which maintain their importance on middle-aged trees, five mosses

also occur but with low ÍES valúes: Leucodon sciuroides, Pterigynandrumfiliforme,

Orthotrichum stramineum, O. rupestre and O. speciosum. Finally, twelve bryophytes

were collected from oíd oaks, of which Leucodon sciuroides and Pterigynandrum

filiforme were dominant.

As the phorophyte ages, bryophyte diversity increases due to the progressive

establishment of new taxa, combined with very little loss of species that were already

present. The processes observed may be summarized as follows:

1. Young trees are colonized by a few mosses (primary colonists: Orthotrichum

lyellii, O. striatum and O. affine) that become more extensively represented on middle-

aged trees, but less so on oíd ones.

2. Middle-aged trees are also colonized by a group of secondary colonists whose

evolution on oíd trees differs: Orthotrichum stramineum undergoes a small increase,

while Leucodon sciuroides and Pterigynandrumfiliforme become the most dominant

in mature communities. However, other secondary colonists decrease on oíd trees:

Orthotrichum rupestre becomes rare and O. speciosum disappears.

3. Oíd trees are additionally colonised by several bryophytes not found on young or

middle-aged trees. Some of these final colonists (Antitrichia californica, Bryum

subelegans and Tortula virescens are frequent and abundant, while others (Tortula

princeps and T. laevipila) are infrequent and scarce.

131

Orthotrichum lyellii

Orthotrichum striatum

Orthotrichum affine

Leucodon sciuroidos

Pterigynand. filiforme

Orthotrich. stramineum

Orthotrichum rupestre

Orthotrichum speciosum

Antitrich. californica -

Bryum subelegans -

Tortula virescens -

Tortula princeps -

Tortula laevlpila

ÍES o 100 200 300 400

Tree diameter

Ü¡(0-15cm) ■(25-35cm) ■(70-85cm)

Fig. 3. Comparative representation of ÍES valúes of bryophytic species from trunks of different-aged

trees.

Cover (%)

100

60

20

YOUNG TREES MIDDLE-AGED TREES

Fig. 4. Evolution of life-form cover on trunks.

short turfs

OLD TREES

132

Fig. 4 displays the evolution of life form cover on trunk. On young trees, most of

the surface is free of bryophytes and only a small portion (2%) is covered by cushion-

type mosses. However, on middle-aged trees, bryophyte cover increases, leading to

communities dominated by cushions of Orthotrichum species. Eventually, grooves

are colonized by tail mosses such as Pterigynandrumfiliforme or Leucodon sciuroides.

Nevertheless, more than 75% of the surface remains free of bryophytes. Instead,

folióse lichens of Parmelia spp. and some fruticose lichens of the genera Ramalina

and Usnea are abundant. On oíd trees, tail mosses predomínate, whereas the cushion-

type is reduced to sparse tufts. Short turfs also occur in the openings of pleurocarpous

lawns. The bryophyte-free área is still large (30%) and is always occupied by invading

crustose or folióse lichens.

Successional patterns

Both trunk and base display a main linear succession whose evolution is closely

associated with tree age (Fig. 5). The lower base features numerous early colonizers

with different life-form types, but dominated by tails. As the diameter increases, the

number of pleurocarpous moss species increases at the same time as some acrocarpous

species disappear. The series culminates in the expansión of tail mosses that cover

almost the entire surface of the stratum, relegating cushion mosses to a vestigial

presence. Thus, in the final community, only tail and mat-shaped mosses predomínate.

Colonization of trunks begins with a few cushion species that become established

sparsely on young trees. These pioneers become more extensive, at the same time as

new cushion and tail-shaped mosses appear. Further events culminate in a final com

munity dominated by tail-shaped mosses, and in which cushion forms are very scarce.

On oíd trees, however, both strata show an additional series, which is cyclic and

basically autogenic: mature communities dominated by tail-shaped mosses are

incidentally and partially destroyed, due to invasión by hyper-epiphytic lichens (e.g.,

Anaptychia ssp.) and to mechanical factors (wind or animáis).

This produces openings that are not colonized by species of earlier stages of the

main series, but by a group of colonists characteristic of the final stage: short turf

mosses, whose establishment in these openings is facilitated by bark alterations.

Some time after their establishment, they disappear under cover of invading tail

mosses.

Discussion

Epiphytic community structure and composition are influenced by a complex hierarchy

of interacting biotic and abiotic (microclimatic, chemical and physical) factors of

substrate and habitat (Barkman 1958, Studlar 1982b). In Mediterranean áreas, these

parameters remain to be measured. However, field observations and studies of species

distribution in epiphytic habitats have shown that environmental dryness is one of

the most influential factors (Hebrard 1989, Burgaz et al. 1994, Mazimpaka & Lara

1995). Such dryness is directly related to sunlight intensity and atmospheric moisture

and indirectly related to habitat characteristics such as tree height, canopy size and

tree density. In winter, epiphytic bryophytes of deciduous trees receive high insolation.

133

Main successional series

Phorophyte growing

-allogenic (microenviron-

mental) changes.

-pioneers expansión

-facilitatíon processes and

autogenic changes.

Phorophyte growing

-allogenic changes

-competition processes

and autogenic changes

Young trees

few cushions

Middle-aged trees

abundant cushions

sparse tails

\

Oíd trees \

abundant tails (+ mats on bases) j

vestigial cushions \

I

invasión of the openings

by tails and disappearance

of turfs and cushions

induced openings

in mature communities

\Secondary cyclic succession

Oíd trees

establishment of short turfs

or small cushions in the openings

Fig. 5. Summary of successional patterns at trunk level.

In summer, the leaf cover protects against insolation, but the atmospheric moisture

is so low that epiphytes are subject to very dry conditions. However, the impact of

this dryness on epiphytic communities depends on substrate conditions and dessication

tolerance of the different species. The smooth, thin bark of twigs and young trees is

drier than the thick and fissured bark of oíd ones and, under similar climatic conditions,

both will support different bryophytic communities. In fact, the few available data

on vertical distribution show that upper tree zones are poorer in bryophytes and only

colonized by cushion-type and drought-tolerant bryophytes (Orthotrichum spp.),

while bases are richer and frequently colonized by mesophytic bryophytes (Hébrard

134

1987, 1989, Lara & Mazimpaka 1994, Mazimpaka & Lara 1995). According to

McCune's (1993) hypothesis regarding the similarity of epiphytic bryophyte response

to vertical, moisture and temporal gradients, a similar situation should be expected

on different-aged trees. Data obtained in this study support this hypothesis and point

out that the change to mesic conditions is more marked on trunks than on tree bases.

In the basal zone, soil proximity and suitable moisture conditions allow an early

establishment of mat, tail and cushion-type mosses. However, most of the surface

remains free of bryophytes. As the tree ages, most of these pioneers undergo a hori

zontal and vertical expansión, and cover a larger surface. In contrast, other pioneers

scarcely represented on young trees (Othotrichum speciosum, Antitrichia curtipendula)

decline or disappear, probably due to their low competitive potential. Occurrence of

new species (secondary colonists), all relatively mesophytic and mat-typed, suggests

that moisture conditions of tree bases improve during the tree growth. Only a few

primary and secondary colonists increase and become dominant on oíd oaks. All

have a high competitive potential, due to a suitable combination of creeping growth-

form (tail, and to a lesser extent, mat), dense branching, and fast growing rate

(Gimingham & Birse 1957, Barkman 1958). Expansión of these bryophytes could

be the main reason for the disappearance of many pioneer species from oíd oaks.

Nevertheless, influence of microenvironmental changes induced by the phorophyte

cannot be ruled out. In fact, occurrence of final colonists is related to microclimatic

and bark physico-chemical changes taking place on this stratum. Some mosses like

Antitrichia californica and Orthotrichum stramineum are moisture indicators in this

área. Others such as Bryum subelegans, Tortula princeps, T. virescens and Zygodon

rupestris tend to be neutrophilous (preferring substraía with a neutral pH). This

means that, in addition to mesic conditions, oíd bark provides chemical conditions

(pH, nutrients) favourable to some bryophytes. Moreover, life forms of some final

colonists (short turfs and small cushions) reveal that these are not highly competitive

bryophytes, but oportunistic ones (due to a high multiplication rate) that establish

themselves in the openings of mature communities of oíd trees, making use of the

smooth, humus and nutrient-rich substraía brought about by epiphyte activity and

ritidome decomposition (Barkman 1958, Studlar 1982b). After a relatively short

time interval, they are replaced by pleurocarpous mosses proceeding from surrounding

communities.

Evolution of community composition and structure on trunks is essentially similar

to that described on tree bases. The large surface devoid of bryophytes and the

dominance of drought-tolerant cushion-type mosses confirm that trunk bark of young

oaks is less favourable to bryophyte establishment. Thinness and scarce rugosity

combined with high sunlight intensity form an ecologically selective habitat, colonized

only by a small number of adapted cushion-type mosses of the genus Orthotrichum.

Middle-aged oaks provide better conditions, since the larger crown and the thicker

and more fissured bark reduce the moisture stress. Under these conditions, cushion-

type pioneers of young trees expand and form the dominant group. Likewise, other

cushion-type Orthotrichum species {O. stramineum, O. rupestre and O. speciosum)

and eventually, some tail mosses {Antitrichia californica) occur. As the tree ages,

pleurocarpous mosses increase, reducing the surface occupied by cushion mosses

135

and lichens. On oíd oaks, biogenic changes of bark surface and canopy enlargement

facilítate the establishment of new mosses characteristic of the final community, or

colonists of the openings produced by mechanical factors or by the action of hyper-

epiphytic lichens (e.g., Anaptychia spp.). However, environmental limitations are

still important, since tail mosses (more mesophytic and abundant on tree bases) are

very scarce.

Succession of epiphytic vegetation is a complex case of community replacement,

due to numerous factors that are difficult to study separately. Barkman (1958) stated

that two categories of factor were involved: intrinsic or autogenic factors due to

epiphyte activity, and extrinsic or allogenic factors due to other agents than epiphytes

themselves. Although they ascribe different importance to these categories, other

authors (Yarranton 1972, Studlar 1982b, Stone 1989) are agreed about the mixed

nature of successional processes. The foregoing results allow some general comments

about the origin and evolution of succession under Mediterranean conditions. Both

tree base and trunk show an increase in bryophytic richness correlated with tree

growth. Studlar (1982b) suggested a challenge of determining if such increases were

due to changes in the tree bark or to the fact that oíd trees had a longer exposure.

This time factor, also suggested by Slack (1976), could be important for some

epiphytes, e.g., those with a low reproductive rate or uncommon in the study área.

In the studied área, however, several bryophytes colonize bases of young trees, but

do not occur on trunks until trees are mature. Most of these bryophytes (Leucodon

sciuroides, Pterigynandrumfiliforme, Tortula princeps, Bryum subelegans, Zygodon

rupestris) do not come from neighbouring soils (a fact that could explain their

preferential occurrence on tree bases). They come from rupicolous and corticolous

environments. Moreover, most of these late trunk colonists show an intensive vege-

tative multiplication {Bryum subelegans, Leucodon sciuroides, Zygodon rupestis) or

"fructify" abundantly on trees {Leucodon sciuroides, Pterigynandrum filiforme,

Orthotrichum stramineum, Antitrichia californica). Finally, it has been observed

that not all the phorophytes show an increase of the epiphyte species number with

age. A reduction of epiphyte number has been observed on Acer saccharum Marsh.

(Slack 1976), while Fagus sylvatica L. and F. grandifolia Ehrh. did not vary

(Rasmussen 1975, Studlar 1982a) and Quercuspubescens Willd. and Quercus ilexL.

reduced the number of epiphytes (Hébrard 1989). Therefore, it may be assumed that

time is not a determinant factor for most of these bryophytes. So, what factors do

account for their establishment and succession on trunks? Some of them are relatively

mesophytic in that they colonize bark fissures, from which they expand to other

zones. Others have a xeromorphic life-form, although in some cases, their geographical

distribution implies a low resistance to long dry periods; in other cases, phorophyte

preference indicates an affinity for neutral substrata. These features suggest that two

types of environmental change take place during the maturation of Quercus pyrenaica

trees:

- An improvement of physical conditions, allowing the establishment of mesophytic

or scarcely drought-tolerant species: bark undergoes major fissuring that creates a

substratum better suited for propagule germination and gametophyte development.

Additionally, bark thickening and porosity increase the water retention capacity,

136

while enlargement of the tree canopy reduces light intensity, improving moisture

conditions and favouring the establishment of bryophytes with lower compensation

points of temperature and light (Hosokawa & Odani 1957, Hosokawa et al. 1964

Studlar 1982b).

- An increase of bark pH, due to the buffer effect of epiphytes or to changes in

ritidome composition. Barkman (1958) reported an increase of bark acidity with

tree age, suggesting that this could be due to dust accumulation or acidic humus

produced by epiphytes. However, this contrasts with the same author's statements

about the lesser acidity of the tree base, which is obviously older than trunk.

Mediterranean climatic conditions interfere with the processes determining the

successional events on each phorophyte. In the case of Quercus pyrenaica, although

species type may vary with sites, there is a consistent pattern of life-form substitution,

which is composed of two complementary series: a main allogenic series that begins

with xerophytic cushion-type mosses which are progressively replaced by mesophytic

tail and mat-type mosses. Destruction of mature communities gives rise to an autogenic

secondary succession that is restricted to oíd trees. According to Barkman (1958),

cyclic autogenic series are very rare and confined to trees showing an intensive

desquamation, which is not the case of Quercus pyrenaica oaks.

Acknowledgements

Our thanks are due to Phil Masón for correction of the English versión of the manuscript.

References

BATES, J.W. (1982): Quantitative approaches in bryophyte ecology. In: SMITH, A.J.E. (Ed.) Bryophyte

Ecology. - Chapman & Hall, London. Pp: 1-44.

BARKMAN, JJ. (1958): Phytosociology and ecology of cryptogamic epiphytes. - Van Gorcum &

comp. N.V. Assen.

BURGAZ, A.R., E. FUERTES & A. ESCUDERO (1994): Ecology of cryptogamic epiphytes in deciduous

forests in Mediterranean Spain. - Vegetatio 112: 73-86.

GIMINGHAM, C.H. & E.M. BIRSE (1957): Ecological studies on growth-form in bryophytes. 1.

Correlations between growth-form and habitat. - J. Ecol. 45: 533-545.

HÉBRARD, J.P. (1987): Étude comparée de la végétation bryophytique des parties basses et moyennesdes troncs de chéne vert et de chéne pubescent (peuplements jeunes) dans la forét domaniale de la

Gardiole de Rians (Var, France). - Bull. Soc. Bot. Centre-Ouest, n.s. 18: 125-144.

HÉBRARD, J.P. (1989): Étude comparée de la végétation bryophytique des troncs de chéne vert et dechéne pubescent (peuplements ágés) dans la forét domaniale de la Gardiole de Rians (Var, France). -

Cryptogamie, Bryol. Lichénol. 10: 253-266.

HOSOKAWA, T. & N. ODANI (1957): The daily compensation period and vertical ranges of epiphytes

in a beech forest. - J. Ecol. 45: 901-916.

HOSOKAWA, T., N. ODANI & H. TAGAWA (1964): Casuality of the distribution of corticolous

species in forests with special reference to the physio-ecological approach. - Bryologist 67: 396-411.

IWATSUKI, Z. (1960): The epiphytic bryophyte communities in Japan. - J. Hattori Bot. Lab. 22: 159-

350.

LARA, F. & V. MAZIMPAKA (1994): Briófitos corticícolas de los robledales de la Sierra de Gredos

(Ávila, España). - Cryptogamie, Bryol. Lichénol. 15: 161-169.

137

MÁGDEFRAU, K. (1982): Life-forms of bryophytes. In: SMITH, AJ.E. (Ed.) Bryophyte ecology. -

Chapman & Hall, London. Pp: 45-58.

MAZIMPAKA, V. & F. LARA (1995): Corticolous bryophytes of Quercus pyrenaica forests from

Gredos Mountains (Spain): vertical distribution and ecological affinity for epiphytic habitats. - Nova

Hedwigia 61: 446.

McCUNE, B. (1990): Rapid estimation of abundance of epiphytes on branches. - Bryologist 93: 39-

43.

McCUNE, B. (1993): Gradients in epiphyte biomass in three Pseudotsuga-Tsuga forests of different

ages in Westem Oregon and Washington. - Bryologist 96: 405-411.

NADKARNI, N.M. (1984): Biomass and mineral capital of epiphytes in an Acer macrophyllum

community of a températe moist coniferous forest, Olympic Peninsula, Washington State. - Can. J. Bot.

62: 2223-2228.

OLSEN, C. (1917): Studies on the succession and ecology of epiphytic bryophytes on the bark of

common trees in Denmark. - Bot. Tidsskr. 34: 313-342.

PHILLIPS, E.A. (1951): The associations of bark-inhabiting bryophytes in Michigan. - Ecol. Monogr.

21: 301-316.

QUARTERMAN, E. (1949): Ecology of the cedar glades. III. Corticolous bryophytes. - Bryologist 52:

153-165.

RASMUSSEN, L. (1975): The bryophytic epiphyte vegetation in the forest Slotved Skov, Northern

Jutland. - Lindbergia 3: 15-38.

RHOADES, F.M. (1981): Biomass of epiphytic lichens and bryophytes on Abies lasiocarpa on a Mt.

Baker lava flow, Washington. - Bryologist 84: 39-47.

RIVAS-MARTÍNEZ, S. (1987): Memoria del mapa de series de vegetación de España. - ICONA-

MAPA, Madrid.

SCHMITT, C.K. & N.G. SLACK (1990): Host specifity of epiphytic lichens and bryophytes: A

comparison of the Adirondack Mountains (New York) and the Southern Blue Ridge Mountains (North

Carolina). - Bryologist 93: 257-274.

SLACK, N.G. (1976): Host specifícity of bryophytic epiphytes in Eastem North América. - J. Hattori

Bot. Lab. 41: 107-132.

SLACK, N.G., D.H. VITT & D.G. HORTON (1980): Vegetation gradients of minerotrophically rich

fens in western Alberta. - Can. J. Bot. 58: 330-350.

SMITH, AJ.E. (1982): Epiphytes and epiliths. In: SMITH, AJ.E. (Ed.) Bryophyte ecology. - Chapman

& Hall, London. Pp: 191-227.

STONE, D.F. (1989). Epiphyte succession on Quercus garryana branches in the Willamete Valley of

Western Oregon. - Bryologist 92: 81-94.

STRINGER, P.W. & M.H.L. STRINGER (1974): A quantitative study of corticolous bryophytes in the

vicinity of Winnipeng, Manitoba. - Bryologist 77: 551-560.

STUDLAR, S.M. (1982a): Host specifícity of epiphytic bryophytes near Mountain Lake, Virginia. -

Bryologist 85: 37-50.

STUDLAR,S.M.( 1982b): Succession of epiphytic bryophytes near Mountain Lake,Virginia. - Bryologist

85: 51-63.

YARRANTON, G.A. (1972). Distribution and succession of epiphytic lichens on black spruce near

Cochrane, Ontario. - Bryologist 75: 462-480.

Received 15 March 1997, accepted in revised form 10 October 1997.

138