recolonization of vascular epiphytes in a shaded coffee agroecosystem

Recolonization of vascular epiphytes in a shaded coffeeagroecosystem

Tarin Toledo-Aceves, Jose G. Garcıa-Franco, Adriana Hernandez-Rojas & Keith MacMillan

Keywords

Biodiversity; Bromeliads; Canopy; Coffee

management; Disturbance; Ferns; Orchids;

Succession

Received 11 January 2011

Accepted 9 May 2011

Co-ordinating Editor: Martin Hermy

Toledo-Aceves, T. (corresponding author,

[email protected]), Garcıa-Franco, J.G.

([email protected]),

Hernandez-Rojas, A.

([email protected]) & MacMillan, K.

([email protected]): Instituto de

Ecologıa, A.C., Red de Ecologıa Funcional,

Antigua Carretera a Coatepec No. 315, El Haya,

Xalapa 91070, Veracruz, Mexico

Abstract

Aim: Shaded coffee plantations constitute an important refuge for biodiversity.

Despite the fact that epiphytic plants form a significant component of these

agroecosystems, their removal from the shade trees is commonplace in Latin

America. To what extent does the epiphyte community recover from this severe

disturbance?

Location: Shaded coffee agroecosystem in Veracruz, Mexico (1912800300 N,

9615505800W; 1200 m asl).

Methods: We assessed the diversity, biomass and recolonization patterns of

vascular epiphytes in shade trees, 8-9 yr after complete epiphyte removal (E�),

and in control ‘non-removal’ sites (E1). In order to evaluate the effects of prior

epiphyte removal, all vascular epiphytes were completely removed from 10

trees per treatment (E� and E1); all epiphyte species collected were identified

and dry biomass measured.

Results: Eight to nine years after removal, epiphyte biomass in the E� shade

trees was 35% of that found in the control sites. A total of 55 epiphyte species,

belonging to 12 families, were registered; 40 in E�, and 48 in E1. Six species

belonging to Bromeliaceae, Orchidaceae, Cactaceae and Araceae accounted for

75% of the biomass in E1 while six species of bromeliads accounted for 76% of

the biomass in E�. Some bromeliads proliferated following disturbance; how-

ever, ferns showed lower recovery.

Conclusions: Epiphyte community recovery, in terms of biomass and diversity,

is considerably higher in the coffee plantation than has been previously

reported for other tropical ecosystems. Epiphyte recolonization patterns re-

flected both the abundance of species in the surrounding matrix and certain

species-specific traits. For such agroecosytems to function as effective reservoirs

of epiphyte diversity, epiphyte stripping should be avoided.

Introduction

Increasing destruction and fragmentation of natural forests

has revealed the crucial importance of shaded coffee agro-

ecosystems as reservoirs of biodiversity (Hylander &

Nemomissa 2008; Philpott et al. 2008), not least because

such systems are frequently established in areas of tropical

montane cloud forest, an ecosystem recognized not only for

its high levels of endemic biodiversity and hydrological

services, but also for its high rates of deforestation (Hamil-

ton et al. 1995; Toledo-Aceves et al. 2011). Epiphytic plants

constitute a key component of the diversity of both cloud

forests and shaded coffee plantations (Hietz 2005; Moor-

head et al. 2010). Epiphytes contribute to the structural

complexity of the agroecosystem, providing a wider avail-

ability of habitats for associated animals (Cruz-Angon &

Greenberg 2005; Hietz 2005; Cruz-Angon et al. 2009).

Within shaded coffee systems in Latin America, the

deliberate removal of epiphytes from the shade trees is a

common management practice (Cruz-Angon & Greenberg

2005). This activity is conducted in order to increase the

availability of light for the coffee plants and because produ-

cers generally consider the epiphytes to be parasites; they

are therefore removed as a maintenance procedure of the

shade trees. Such removal of the epiphytes causes a

Applied Vegetation Science 15 (2012) 99–107

Applied Vegetation ScienceDoi: 10.1111/j.1654-109X.2011.01140.x© 2011 International Association for Vegetation Science 99

simplification of the agroecosystem, with consequent nega-

tive impacts on other components such as the birds and

arthropods (Cruz-Angon & Greenberg 2005; Cruz-Angon

et al. 2009). However, the effects of this practice on the

vascular epiphytic community itself have not been analysed.

Species turnover and succession patterns in epiphytes

can be affected by several factors, including host tree species

and the age, type and successional stage of the ecosystem,

as well as type, frequency and intensity of disturbance,

among others (Wolf 2005). Epiphytes, in general, are

considered to be highly susceptible to forest fragmentation

and disturbance (Holbrook 1991; Wolf 2005). In terms of

recolonization rates, their recovery from disturbance has

been reported to be very slow; seedlings of vascular epi-

phytes only re-established 10 yr after experimental strip-

ping in a cloud forest in Costa Rica (Nadkarni 2000).

A less diverse vascular epiphyte community could be

expected in disturbed sites, as a result of the slow recoloni-

zation rates reported for this group. However, if shaded

coffee agroecosystems predominantly maintain epiphytic

species with high rates of growth and fecundity and greater

drought-resilience (Hietz 2005), the rate of recolonization is

hypothesized to be higher in comparison with forest eco-

systems. We assessed the recolonization of vascular epi-

phytes in a shaded coffee plantation in central Veracruz,

Mexico, 8-9 yr after experimental removal, providing an

approximation to the temporal patterns of the recoloniza-

tion dynamic process. Considering the high rates of cloud

forest deforestation and the particular vulnerability of

epiphytes to ecosystem degradation, evaluation of post-

disturbance recolonization patterns is important for the

development of sustainable coffee management strategies

to enhance the capacity of the agroecosystem to provide

reservoirs of biodiversity within fragmented landscapes.

Methods

Study area

The shaded coffee plantation used in this study is 40 yr

old, 200 ha in area, and located in Central Veracruz,

Mexico (1912800300 N, 9615505800W; 1200 m asl). Before

coffee plantation, the original vegetation in the area was

tropical montane cloud forest (Williams-Linera 2002).

The original trees were removed and 17 species of shade

trees planted, including 13 native and four non-native

species (Lopez-Gomez et al. 2008). Inga jinicuil Schltdl. &

Cham. Ex. G. Don. is the predominant shade tree

(143 trees ha�14 5 cm diameter at breast height (DBH);

Lopez-Gomez et al. 2008), and is a nitrogen-fixing fast-

growing legume frequently planted in order to improve

soil fertility. Shade trees were pruned every 2 yr to main-

tain shade cover at around 60%. For a detailed description

of the site see Cruz-Angon & Greenberg (2005).

Experimental design

Two experimental sites, located approximately 1 km apart,

were established in 1999 and 2000 by Cruz-Angon &

Greenberg (2005). At each site, two 3 ha plots were delim-

ited and all epiphytes removed from the trees in one plot

(E�) while the other plot was left undisturbed as a control

(E1), with no further manipulation of the canopy carried

out (Cruz-Angon & Greenberg 2005). Non-vascular epi-

phytes may favour the colonization of vascular epiphytes

(Zotz & Vollrath 2003), however, in this study, we focused

only on vascular species because the initial experimental

removal of plants concentrated only on this group. To assess

the recolonization of vascular epiphytes following experi-

mental removal, five I. jinicuil trees were selected at random

in each of the four plots in 2007 and 2008 (5 trees � 2

treatments (E� and E1)� 2 sites = 20 trees). Vascular epi-

phytes were completely removed from the selected trees in

the traditional manner, which entailed climbing the tree

and manually scraping the epiphytes from the trunk and

canopy with the sickle-like bladed tool used locally for this

purpose (‘destenchador’). This procedure left only bare

bark in the places where the epiphytes had been attached;

however, some lichens and mosses remained in those

places where there had been no epiphytes and therefore

where the scraping tool had not been applied. As far as

possible, the ground below each tree was cleared of litter

before stripping the epiphytes in order to be able to identify

and collect all (and only) the epiphytes removed from the

tree and fallen to the ground.

For each tree, the following measurements were taken:

DBH, number of branches Z10 cm in diameter at the

insertion point, projected canopy tree area and canopy

cover. The percentage of canopy cover was measured with

a spherical densiometer at the four cardinal points, and

four intercalated points, with the tree in the centre; the

eight measurement points per tree were located at points

below the canopy and above the coffee plants, at a height

of 2 m from the ground.

Species identification was conducted at the Herbarium

XAL of INECOL A.C., Mexico, using taxonomic keys,

comparison with herbarium collections and specialist

consultation. Specimens that could not be identified to

species, owing to a lack of sufficient diagnostic character-

istics, were identified to genus. Smaller plants could not

be identified with confidence, therefore species was de-

termined for plants of longest leaf length 45 cm, except

in the case of Pleurothallidinae orchids.

The fresh weight of all plants collected was measured,

but dry biomass was estimated based on regression equa-

tions for the most abundant species only. To calculate this

equation for each species, the fresh and dry biomass of 30

plants covering the whole range of sizes was quantified.

Applied Vegetation Science100 Doi: 10.1111/j.1654-109X.2011.01140.x© 2011 International Association for Vegetation Science

Recolonization of epiphytes Toledo-Aceves, T. et al.

Soil particles, dead plant material and non-vascular epi-

phytes associated with sampled plants were removed by

hand before processing. Plants were oven-dried for 48–72

hours at 80 1C, until reaching constant weight, and the

regression equations calculated for each abundant spe-

cies. Dead epiphyte organic matter present in the canopy

was not quantified because during the epiphyte removal

and collection process it was impossible to differentiate it

from throughfall and litter already present on the ground.

Data analyses

Following a split-plot design, an ANOVA was used to analyse

the effects of epiphyte treatment (fixed), site (random)

and their interaction, on canopy cover and tree epiphyte

biomass. Tree size was also included as a covariate (Quinn

& Keough 2002). As neither covariate nor site were found

to be significant (P4 0.05), these were omitted from the

model. The percentage of canopy cover was arcsine

square-root transformed before analysis.

Regression analyses were used to evaluate the depen-

dence of epiphytic species number and dry biomass on host

tree size (DBH, number of branches and canopy area).

Slopes of the regression equations between treatments were

compared using the t statistic (Zar 1996). To identify possible

relationships between epiphyte assemblage complexity and

the tendency of a species to increase or decrease, regression

analyses were applied, in which the relationship between

the proportion of biomass of each species and the number of

species present per tree in each treatment were used. The

proportion of biomass was also arcsine square-root trans-

formed. Statistical analyses were performed with MINITAB

Statistical Software (version 14.12, Coventry, UK).

Species accumulation curves (Mao Tau) were calcu-

lated, without replacement, using 100 sample randomiza-

tions based on presence–absence data (Colwell 2006).

Species richness estimators were used to evaluate suffi-

ciency of sampling effort (Bootstrap and Jackknife 1). The

ESTIMATES programme was used for these analyses (Colwell

2006). Diversity a (species richness) per treatment was

evaluated with Shannon–Wiener and Simpson indices,

while b diversity (difference between treatments) was

estimated with the bw index (Magurran 2004). The SPECIES

DIVERSITY AND RICHNESS IV programme (Seaby & Henderson

2006) was used for these analyses.

Results

Coffee plantation structure

Between treatments, there were no significant differences

(P40.05) in tree DBH (E�= 53� 4.6 cm; E1 = 54.9� 7),

number of branches (E�= 51� 13.2; E1 = 40� 7.3), cano-

py area (E�= 148.5� 16 m2; E1 = 115.7� 25) or percen-

tage of canopy cover (E�= 71.8� 0.6; E1 = 72.9� 1).

In both treatments, trees of greater DBH hosted more

epiphyte species than smaller trees (Fig. 1); the slopes of the

regressions equations differed significantly between treat-

ments (t test= 2.17; P = 0.05). Number of branches and

canopy area were not related to number of species in any

treatment. There was no significant relationship (P4 0.05)

between epiphyte dry biomass and tree DBH, number of

branches or canopy area in either of the treatments.

Effect of removal on vascular epiphyte diversity

We recorded a total of 55 species (and one morphospecies),

belonging to 12 families (Table 1). In E1, 48 species were

found, of which 16 were exclusive to E1 (Table 1). In E�, 40

species were identified, of which eight (four species and

four morphospecies) were exclusive to E�. Three of the

species found only in E�were not true epiphytes: Ficus sp.

(hemi-epiphyte), Psittacanthus sp. (parasite) and the climber

Cissus sp. The beta diversity index bw was 1.23, signifying

that the epiphyte assemblages in the two treatments were

very similar (Whittaker 1960). Species accumulation curves

showed a tendency to approach an asymptote for adequate

completeness of the inventory, but did not reach stability

(Fig. 2). Species richness estimators produced slightly super-

ior values to the actual recorded number of species in both

treatments (Bootstrap: E�= 41.76 and E1 = 52.21; Jackknife

1: E�= 45.3 and E1 = 57). For the highest estimate (Jack-

knife 1), 84% and 88% were recorded for E� and E1,

respectively. The Shannon–Wiener and Simpson indices

were lower in E� than in E1: HE�= 3.47 and HE1 = 3.63;

DE� = 33.49 and DE1 = 38.27.

Dynamics of epiphyte succession

Mean epiphyte biomass per tree was significantly lower in

E� than in E1 (Table 1; F = 5.46, df = 1, P = 0.03), while site

Tree dbh (cm)20 40 60 80 100 120

No.

of e

piph

yte

spec

ies

10

15

20

25

30

35

40

E R = 0.71 P = 0.002E R = 0.58 P = 0.02

Fig. 1. Relationship between tree DBH (cm) and epiphyte species rich-

ness per tree following epiphyte removal (E�), and in ‘non-removal’

control sites (E1), in a shaded coffee plantation in Veracruz, Mexico.


Toledo-Aceves, T. et al. Recolonization of epiphytes

Table 1. Vascular epiphytes found on Inga jinicuil trees 8–9 yr following complete removal of epiphytes (E�) and in control sites (E1) in a shaded coffee

plantation (n = 10) in Veracruz, Mexico. aConservation status according to Mexican legislation (SEMARNAT, 2002): V = vulnerable.

Family and species Conservation statusa Number of trees Dry mass per tree (g; mean� 1 SE)

E� E1 E� E1

Araceae

Anthurium scandens (Aubl.) Engl. — 8 10 240� 159 3119� 1449

Syngonium podophyllum Schott — 6 0 85.2� 30.9 —

Aspleniaceae

Asplenium sp. 0 1 — 0.5

Bromeliaceae

Catopsis spp. 10 10 186.5� 37.7 229.9� 65.8

Tillandsia belloensis W. Weber — 7 10 178� 37.9 1007� 234

Tillandsia butzii Mez — 3 5 5.24� 4 4.88� 2.34

Tillandsia brachycaulos Schltdl. — 0 2 — 30.8� 15.4

Tillandsia depeanna Steud. — 0 1 — 191

Tillandsia fasciculata Sw. — 0 6 — 162.4� 35.3

Tillandsia filifolia Schltdl. & Cham. — 5 4 0.85� 0.43 8.9� 6.14

Tillandsia foliosa M. Martens & Galeotti — 2 10 82.6� 23 468� 158

Tillandsia heterophylla E. Morren — 10 10 199.3� 41.6 644� 184

Tillandsia ionantha Planch. — 3 5 4.05� 1.92 5.7� 3.36

Tillandsia juncea (Ruiz & Pav.) Poir. — 10 10 2861� 511 14 002� 4689

Tillandsia kirchhoffiana Wittm. — 0 1 — 192.2

Tillandsia limbata Schltdl. — 10 10 229.3� 57.9 329.8� 94.1

Tillandsia multicaulis Steudel — 0 1 — 13

Tillandsia polystachia (L.) L. — 9 9 327.3� 60.7 211.7� 56.2

Tillandsia punctulata Schltdl. & Cham. — 1 5 14.72� 8.33 70.4� 36.9

Tillandsia recurvata (L.) L. — 3 0 3.47� 1.37 —

Tillandsia schiedeana Steud. — 10 10 1876� 374 3777� 866

Tillandsia tricolor Schltdl. & Cham. V 0 8 — 303.6� 92.1

Tillandsia usneoides (L.) L. — 0 4 — 147� 121

Tillandsia variabilis Schltdl. — 3 4 7.61� 2.88 16.95� 4.75

Tillandsia sp. 1 1 0 70.84 —

Cactaceae

Rhipsalis baccifera (J.S. Muell.) Stearn — 9 10 102.0� 32.9 3511� 1441

Lycopodiaceae

Huperzia sp. 0 2 — 50� 49.9

Loranthaceae

Psittacanthus sp. 1 0 0.03 —

Meliaceae

Trichilia havanensis Jacq. — 0 1 — 21.6

Moraceae

Ficus sp. 1 0 1.7 —

Orchidaceae

Encyclia polybulbon (Sw.) Dressler — 4 8 18.79� 7.56 20.7� 10.7

Encyclia sp 1 — 0 3 — 8.15� 5.15

Epidendrum rigidum Jacq. — 0 1 — 9.6

Dichaea sp. 0 1 — 3

Isochilus unilateralis B. L. Rob — 1 1 218 1.5

Jacquiniella sp 1. 0 2 — 58.4� 31.6

Jacquiniella sp 2. 10 10 32.64� 6.04 420� 109

Lepanthes avis Rchb. F. — 8 2 1.76� 0.64 0.7� 0.5

Maxillaria densa Lindl. — 8 9 21.8� 12.5 3647� 1330

Nidema bothii (Lindl.) Schltr. — 4 1 8.69� 2.62 1.2

Pleurothallis tribuloides (Sw.) Lindley — 0 2 — 1.98� 1.13

Prosthechea ochracea (Lindl.) W.E. Higgins — 8 6 16.37� 4.98 190.2� 77.8

Scaphyglottis livida (Lindl.) Schltr. — 10 10 842� 227 967� 365

Trichosalpinx blaisdellii (S. Watson) Luer — 6 5 3.66� 1.04 24.9� 8.33

Piperaceae

Peperomia dendrophila Schltdl. & Cham. — 9 10 531� 311 253.1� 64



had no significant effect (P4 0.05). Eight to nine years

following complete removal from the support trees, epi-

phyte biomass was 35% of that found in the control sites.

The vascular epiphyte dry biomass load calculated was

E�= 2.6� 0.12 t ha�1 and E1 = 8.4� 0.5 t ha�1 [based on

the number of trees reported for the studied sites by Cruz-

Angon & Greenberg (2005)].

Species abundance, based on dry biomass in E� and E1,

is shown in Fig. 3. With the exception of the two most

dominant species, there was an occurrence of species

turnover in E�, with the same position in the ranking

occupied by different species in the two treatments. In E�,

the six species of bromeliads that contributed to 76% of

the total biomass were: Tillandsia juncea (21%), Tillandsia

schiedeana (14%), Tillandsia polystachia (13%), Tillandsia

limbata (10%), Tillandsia heterophylla (9%) and Catopsis

spp. (8%). In E1, six species accounted for 75% of the

total dry biomass; T. juncea (34%), T. schiedeana (10%),

Rhipsalis baccifera (9%), Maxillaria densa (9%), Anthurium

scandens (8%) and Tillandsia belloensis (5%). The remain-

ing species each contributed o 0.6% to the total biomass

in E1.

In E�, the proportion of biomass of T. schiedeana

decreased significantly with the number of species present

per tree (R2 = 59.2, P = 0.01). This was the only species

to show a significant response in this treatment. In E1,

T. juncea also decreased with number of species (R2 = 41.4,

P = 0.05), while Phlebodium pseudoaureum biomass in-

creased significantly (R2 = 46.5, P = 0.03).

Discussion

Vascular epiphyte recovery after major disturbance in

shaded coffee agroecosystems

Post-disturbance epiphyte recovery depends on the sur-

viving seeds and seedlings, supply of incoming propa-

gules, germination and early establishment of seedlings,

and on species-specific interactions as well as the capacity

of the species to reproduce in order to maintain the

population. In terms of biomass and diversity, the recolo-

nization of the vascular epiphytes in the coffee plantation

studied is considerably higher than has previously been

reported for cloud forest by Nadkarni (2000) in Costa

Rica. However, that study involved the removal of only a

few branch segments from five trees in a montane cloud

forest. In contrast, epiphytes were completely removed

from the trees in the present study (including the trunk),

in 3 ha at each site (although only 10 trees were sampled

in each treatment for the present analysis) – a process that

could be expected to reduce the arrival of propagules from

Table 1. Continued

Family and species Conservation statusa Number of trees Dry mass per tree (g; mean� 1 SE)

E� E1 E� E1

Peperomia tetraphylla (G. Forst) Hook. & Arn. — 5 10 13.65� 5.55 104� 41.6

Polypodiaceae

Campyloneurum sp. 0 2 — 2.1� 0.8

Phlebodium pseudoaureum (Cav.) Lellinger — 8 10 92.4� 57.9 1685� 795

Pleopeltis angusta var. angusta Humb. & Bonpl. ex Willd. — 5 5 6.98� 5.12 11.22� 2.14

Pleopeltis crassinervata (Fee) T. Moore — 10 10 324.2� 85.3 1115� 424

Polypodium furfuraceum Schldl. & Cham. — 10 9 82.8� 22.2 262� 124

Polypodium polypodioides (L.) Watt. — 1 0 10.5 —

Polypodium pyrrholepis (Fee) Maxon — 4 1 6.31� 5.19 16.2

Polypodium rhodopleuron Kunze — 1 0 42.5 —

Polypodium triseriale Swartz V 1 3 2.58 437� 391

Vitaceae

Cissus sp. — 1 0 44.8 —

Total (kg) 13.26� 1.78 37.31� 1.01

Tree0 2 4 6 8 10

Spe

cies

acc

umul

ated

15

20

25

30

35

40

45

50

55

EE

Fig. 2. Species accumulation curves of vascular epiphytes 8-9 yr after

removal (E�) and in ‘non-removal’ control sites (E1), in a shaded coffee

plantation in Veracruz, Mexico. Sample-based rarefaction method (Mao-

Tau), mean and bars indicate 95% confidence intervals calculated based

on 100 randomizations.



neighbouring trees. The considerable increase in recruit-

ment rate we found could result from the higher levels of

solar radiation in the coffee plantation than is common in

tropical montane cloud forest fragments (� 80-90% ca-

nopy cover; Williams-Linera 2003). Survival rates of

juveniles of Tillandsia spp., and the probability of reaching

reproductive maturity in T. juncea and T. punctulata,

increase with higher light availability (Winkler et al.

2005, 2007). While the removal of epiphytes was carried

out exhaustively, seeds were not specifically targeted and

it is possible that seedlings and segments of rhizomes may

have been missed and therefore the ‘new’ available space

could have been occupied by species that happened to

already be in place. This would have given an advantage

for early establishment, accelerating the recolonization

process, in contrast to Nadkarnis’ findings (2000). None-

theless, this study provides strong evidence that, follow-

ing a severe disturbance, vascular epiphyte recovery can

be very high in this type of agroecosystem.

Patterns of recolonization of vascular epiphytes

The epiphyte biomass recorded in both treatments was

intermediate to that reported for vascular epiphytes in

other tropical ecosystems (Hofstede et al. 1993; Dıaz et al.

2010). Species accumulation curves and richness estima-

tors indicated that a greater number of species in the

studied agroecosystem than was actually recorded by the

present study. Nonetheless, the richness we found was

superior to that found in previous studies at the same site

(Cruz-Angon & Greenberg 2005; Hietz 2005).

When an epiphyte community is severely disturbed,

some species spread while others diminish or even disap-

pear, resulting in a less evenly distributed community. In

E�, the epiphyte community has become less rich and less

even as a result of the dominance of certain groups, such as

the bromeliads, while dominance in E1 is more evenly

distributed among different taxa. The higher slope of the

relationship between tree DBH and number of species in E�

represents a supply of vacant substrate, permitting a more

or less continuous arrival of new species. As proposed by

Benzing (1981), disturbance in forest canopies might main-

tain diversity in epiphyte communities by preventing com-

petitive exclusion in the community. According to this

proposal, the greater availability of space produced by

epiphyte removal could reduce competitive exclusion and

lead to a moderately diverse community. However, it

remains to be demonstrated whether competition or other

processes are responsible for the patterns observed in the

epiphyte community.

The immediate source area from which new colonists

may arrive is the surrounding trees in the coffee planta-

tion where reproductively mature epiphytes are already

established. Thus, we could expect the pattern of recolo-

nization to reflect the growth rates, abundance of species

and the quantity of propagules produced by each species

in the surrounding matrix (Yeaton & Gladstone 1982;

Cascante-Marın et al. 2006). Several life-history traits

20

Peperomia dendrophila

T. polystachia

Catopsis spp.

T. limbata

Scaphyglottis livida

Pleopeltis crassinervata

T. heterophylla

Phlebodium pseudoaureum

T. belloensis

Anthurium scandens

Maxillaria densa

Rhipsalis baccifera

T. schiedeana

T. juncea

Biomass (kg)

Sp

ecie

s

E+

E–

0 5 10 15

Fig. 3. Abundance (mean� 1 SE; n = 10) diagram of vascular epiphytes 8-9 yr after removal (E�) and in ‘non-removal’ control (E1) treatments. Species are

ordered according to absolute abundance in dry biomass. The figure is sorted according to the rank in E1. All species shown account for 93% and 97% of

the total biomass in E1 and E�, respectively.



contribute to reproductive success: While T. juncea, the

most dominant species in both treatments, is reported to

become fertile only after about 18 yr and to have a

relatively low growth rate of the leading shoot, it assigns

a high proportion of biomass to the production of off-

shoots, which results in high population growth rates

(Winkler et al. 2007). This strategy favours the rapid

colonization of available space and, being also tolerant to

drought, this species can quickly and successfully colonize

the trees in the coffee plantation. Tillandsia schiedeana, the

second most dominant species, is also drought tolerant

(Martin & Adams 1987) and displays a similar strategy in

terms of production of offshoots.

While various bromeliad species recovered in terms of

biomass, and some even proliferated following disturbance

(e.g. T. polystachia), other bromeliad species (e.g. Tillandsia

foliosa, Tillandsia tricolor and Tillandsia fasciculata), and ferns

and orchids in general, were more susceptible to distur-

bance, regardless of their high dispersal capability. We found

a reduced richness of ferns in the coffee plantation in

comparison with that reported for cloud forest in the region

(Hietz & Hietz-Seifert 1995a, b). Our results support pre-

vious findings: disturbed habitats harbour fewer fern and

orchid species, but more bromeliad species, than is typically

the case in primary forest habitats (Barthlott et al. 2001;

Larrea & Werner 2010). While Haro-Carrion et al. (2009)

report that Pteridophyta were less species-rich in cocoa

plantations than in forests, there were no differences found

in Orchidaceae and Bromeliaceae. Various bromeliads have

been found to increase in abundance and to contribute

greatly to the diversity of disturbed montane forests

(Kromer & Gradstein 2003; Flores-Palacios & Garcıa-Franco

2004; Hietz et al. 2006). An increase in canopy openness

and exposure to solar radiation in those trees stripped of

epiphytes could explain the higher abundance of some

bromeliads. Tillandsia seedlings in epiphyte-free trees could

benefit from the increased availability of photosynthetically

active radiation (Hietz 1997; Winkler et al. 2005) compared

with the plants in E1. Even though epiphyte seedlings are

intolerant to desiccation, many Tillandsia species have

strategies that allow them to establish in xeric environments

(Martin 1994; Zotz & Andrade 1998). Such attributes would

favour the establishment and proliferation of some epiphy-

tic bromeliads while simultaneously limiting other groups

such as orchids and ferns. The dominant species are those

more common in drier forests of the region (Hietz & Hietz-

Seifert 1995a). Because of the dry microclimate typical of

shaded coffee agroecosystems, a predominance of more

drought-tolerant species over those that are more shade

tolerant and drought sensitive tends to occur in comparison

with natural tropical forests (Hietz 2005).

Turnover of vascular epiphyte species occurs during

succession in montane forests, with drought-tolerant

species being replaced by those better adapted to more

humid micro-environmental conditions (Barthlott et al.

2001; Wolf 2005). We found a similar pattern in the coffee

plantation: T. schiedeana and T. juncea biomass displayed a

significant reduction in species-rich assemblages. Early

colonizers can be considered inferior competitors, and are

expected to be replaced in more complex assemblages.

The opposite pattern was found in Phlebodium pseudoaur-

eum, a common species in humid cloud forests and one

that is intolerant to desiccation (although it has xeric

adaptations such as succulent rhizomes) (Hietz & Briones

1998; Hietz 2001), which indicates its preference for

species-rich assemblages. This characteristic could make

it a good indicator of the presence of more advanced

successional communities; however, complete life his-

tories would be needed to confirm roles as pioneers and

successors (Benzing 1990). The decline in T. polystachia,

T. limbata, T. heterophylla and Catopsis spp. in E1 could be

the result of their replacement by species such as Rhipsalis

baccifera, Maxillaria densa and Anthurium scandens. Crassu-

lacean acid metabolism allows the cacti to occur in the

driest of sites (Andrade & Nobel 1997), while Anthurium

tends to occupy more mesic microsites in the canopy,

rarely occupying the drier conditions typical of the outer

canopy (Lorenzo et al. 2009).

Epiphyte management in shaded coffee plantations

For agroecosytems such as shaded coffee plantations to

function as effective reservoirs of epiphyte diversity, we

propose the following recommendations: (1) Cessation of

epiphyte stripping solely to reduce shade because of the

negative effects on the epiphyte community and asso-

ciated fauna. In order to control levels of canopy shade,

pruning of tree branches could be carried out instead. This

still implies epiphyte loss but to a much lesser extent than

their complete removal. The potential detrimental or

beneficial effects of epiphyte removal on agroecosystem

productivity have not yet been established; in natural

forests, epiphytes play an important role in water and

nutrient cycling (Nadkarni 1986; Hofstede et al. 1993)

and, while we could expect a similarly significant con-

tribution to those processes in shaded coffee plantations,

this remains to be investigated. Epiphytes can cause some

physical damage to their support trees (Benzing 1990),

therefore the possible negative effects of epiphyte load on

the shade trees should be adequately evaluated; (2) Old

native trees from the original ecosystem should be

maintained, as these favour a high diversity of epiphytes

and associated organisms; (3) Initiatives promoting

coffee cultivation under a diverse canopy need to be

expanded and favoured by producers and consumers;

and (4) Commercial epiphyte harvesting, as part of a



management plan, should be encouraged to diversify

production in cases where the agroecosystem is suitable

for this purpose. In order to design precise sustainable

canopy harvesting plans, a more detailed evaluation of

target species population dynamics and harvesting yield,

accompanied by monitoring, would be required.

Conclusions

This study demonstrates that the biomass and diversity of

vascular epiphytes, such as certain bromeliads, can re-

cover from a severe disturbance in shaded coffee planta-

tions much more quickly than has been reported

previously in other tropical ecosystems. However, groups

such as the ferns exhibit lower recovery. Epiphyte recolo-

nization patterns reflect both the abundance of species in

the immediate surrounding matrix and the individual

traits of the species in question. For these agroecosystems

to function as effective reservoirs of epiphyte diversity,

epiphyte stripping, when the objective is solely to main-

tain the shade trees while reducing the shade level,

should be avoided as this practice has negative effects on

the epiphyte community.

Acknowledgements

We thank A. Cruz-Angon for permission to use the experi-

mental plots and R. H. Manson for supporting the project.

We thank the owners and manager of ‘La Orduna’ coffee

plantation for permission to carry out the study. We thank

C. Gallardo for help with the identification of specimens,

and A. Vela and A. Lepe for their assistance with field

data collection. This project was funded by SEMARNAT-

CONACYT (‘BIOCAFE’ C01-94) and INECOL A.C. (20030-

10144), and supported by the personnel and facilities of

INECOL A.C. We are grateful to A. Flores-Palacios for

helpful comments to a previous version of the manuscript.

References

Andrade, J.L. & Nobel, P.S. 1997. Microhabitats and water

relations of epiphytic cacti and ferns in a lowland

neotropical forest. Biotropica 29: 261–270.

Barthlott, W., Schmit-Neuerburg, V., Nieder, V. & Engwald, S.

2001. Diversity and abundance of vascular epiphytes: a com-

parison of secondary vegetation and primary montane rain

forest in the Venezuelan Andes. Plant Ecology 152: 145–156.

Benzing, H.D. 1981. Bark surfaces and the origin and main-

tenance of diversity among angiosperm epiphytes: a

hypothesis. Selbyana 5: 248–255.

Benzing, H.D. 1990. Vascular epiphytes. Cambridge University

Press, Cambridge, US.

Cascante-Marın, A., de Jong, M., Borg, E., Oostermeijer,

J.G.B., Wolf, J.H.D. & den Nijs, J.C.M. 2006. Reproductive

strategies and colonizing ability of two sympatric epiphytic

bromeliads in a tropical premontane area. International

Journal of Plant Science 167: 1187–1195.

Colwell, R.K. 2006. EstimateS: Statistical estimation of species

richness and shared species from samples. Version 8 (User’s

guide and application).

Cruz-Angon, A. & Greenberg, R. 2005. Are epiphytes

important for birds in coffee plantations? An experimental

assessment. Journal of Applied Ecology 42: 150–159.

Cruz-Angon, A., Baena, M.L. & Greenberg, R. 2009. The

contribution of epiphytes to the abundance and species

richness of canopy insects in a Mexican coffee plantation.

Journal of Tropical Ecology 25: 453–463.

Dıaz, I.A., Sieving, K.E., Pena-Foxon, M.E., Larraın, J. &

Armesto, J.J. 2010. Epiphyte diversity and biomass loads

of canopy emergent trees in Chilean temperate rain forests:

a neglected functional component. Forest Ecology and

Management 259: 1490–1501.

Flores-Palacios, A. & Garcıa-Franco, J.G. 2004. Effect of

isolation on the structure and nutrient content of oak

epiphyte communities. Plant Ecology 173: 259–269.

Hamilton, L.S., Juvik, J.O. & Scatena, F.N. 1995. Tropical

montane cloud forests. Springer Verlag, New York, NY, US.

Haro-Carrion, X., Lozada, T., Navarrete, H. & de Koning, G.H.J.

2009. Conservation of vascular epiphyte diversity in shade

cacao plantations in the Choco region of Ecuador. Biotropica

41: 520–529.

Hietz, P. 1997. Population dynamics of epiphytes in a Mexican

humid montane forest. Journal of Ecology 85: 767–775.

Hietz, P. 2001. Photosynthesis, chlorophyll fluorescence and

within-canopy distribution of epiphytic ferns in a Mexican

cloud forest. Plant Biology 3: 279–287.

Hietz, P. 2005. Conservation of vascular epiphyte diversity in

Mexican coffee plantations. Conservation Biology 19: 391–399.

Hietz, P. & Briones, O. 1998. Correlation between water

relations and within-canopy distribution of epiphytic ferns

in a Mexican cloud forest. Oecologia 114: 305–316.

Hietz, P. & Hietz-Seifert, U. 1995a. Composition and ecology of

vascular epiphyte communities along an altitudinal gradient

in Central Veracruz, Mexico. Journal of Vegetation Science 6:

487–498.

Hietz, P. & Hietz-Seifert, U. 1995b. Structure and ecology of

epiphyte communities of a cloud forest in central Veracruz,

Mexico. Journal of Vegetation Science 6: 719–728.

Hietz, P., Buchberger, G. & Winkler, M. 2006. Effect of forest

disturbance on abundance and distribution of epiphytic

bromeliads and orchids. Ecotropica 12: 103–112.

Hofstede, R.G.M., Wolf, J.H.D. & Benzing, D.H. 1993.

Epiphytic biomass and nutrient status of a Colombian

upper montane rain forest. Selbyana 14: 37–45.

Holbrook, N.M. 1991. Small plants in high places: the

conservation and biology of epiphytes. Trends in Ecology and

Evolution 6: 314–315.

Hylander, K. & Nemomissa, S. 2008. Home garden coffee as a

repository of epiphyte biodiversity in Ethiopia. Frontiers in

Ecology and the Environment 6: 524–528.



Kromer, T. & Gradstein, S.R. 2003. Species richness of vascular

epiphytes of two primary forest and fallows in the Bolivian

Andes. Selbyana 24: 190–195.

Larrea, M.L. & Werner, F.A. 2010. Response of vascular

epiphyte diversity to different land-use intensities in a

neotropical montane wet forest. Forest Ecology and

Management 260: 1950–1955.

Lopez-Gomez, A.M., Williams-Linera, G. & Manson, R.H.

2008. Tree species diversity and vegetation structure in

shade coffee farms in Veracruz, Mexico. Agriculture,

Ecosystems and Environment 124: 160–172.

Lorenzo, N., Gilson-Mantuano, D. & Mantovani, A. 2009.

Comparative leaf ecophysiology and anatomy of seedlings,

young and adult individuals of the epiphytic aroid Anthurium

scandens (Aubl.) Engl. Environmental and Experimental Botany

68: 314–322.

Magurran, A.E. 2004. Measuring biological diversity. Blackwell

Publishing, Oxford, UK.

Martin, C.E. 1994. Physiological ecology of the Bromeliaceae.

Botanical Review 60: 1–82.

Martin, C.E. & Adams, W.W.I. 1987. Crassulacean acid

metabolism, CO2-recycling, and tissue desiccation in the

Mexican epiphyte Tillandsia schiedeana Steud (Bromeliaceae).

Photosynthesis Research 11: 237–244.

Moorhead, L.C., Philpott, S.M. & Bichier, P. 2010. Epiphyte

biodiversity in the coffee agricultural matrix: canopy stratifi-

cation and distance from forest fragments. Conservation Biology

24: 737–746.

Nadkarni, N.M. 1986. The nutritional effects of epiphytes on

host trees with special reference to alteration of

precipitation chemistry. Selbyana 9: 44–51.

Nadkarni, N.M. 2000. Colonization of stripped branch surfaces

by epiphytes in a lower montane cloud forest, Monteverde,

Costa Rica. Biotropica 32: 358–363.

Philpott, S.M., Arendt, W.J., Armbrecht, I., Bichier, P., Diestch, T.,

Gordon, C., Greenberg, R., Perfecto, I., Reynoso-Santos, R.,

Soto-Pinto, L., Tejeda-Cruz, C., Williams-Linera, G.,

Valenzuela, J. & Zolotoff, J.M. 2008. Biodiversity loss in

Latin American coffee landscapes: review of the evidence on

ants, birds, and trees. Conservation Biology 22: 1093–1105.

Quinn, G. & Keough, M.J. 2002. Experimental design and data

analysis for biologists. Cambridge University Press,

Cambridge, UK.

Seaby, R.M.H. & Henderson, P.A. 2006. Species diversity and

richness IV. Pisces Conservation LTD, Hampshire, UK.

Toledo-Aceves, T., Meave, J.A., Gonzalez-Espinoza, M. &

Ramırez-Marcial, N. 2011. Tropical montane cloud forests:

current threats and opportunities for their conservation

and sustainable management in Mexico. Journal of

Environmental Management 92: 974–981.

Whittaker, R.H. 1960. Vegetation of the Siskiyou Mountains,

Oregon and California. Ecological Monographs 30: 279–338.

Williams-Linera, G. 2002. Tree species richness complementary,

disturbance and fragmentation in a Mexican tropical montane

cloud forest. Biodiversity and Conservation 11: 1825–1843.

Williams-Linera, G. 2003. Temporal and spatial phenological

variation of understory shrubs in a tropical montane cloud

forest. Biotropica 35: 28–36.

Winkler, M., Karl, H. & Hietz, P. 2005. Effect of canopy position

on germination and seedling survival of epiphytic

bromeliads in a Mexican humid montane forest. Annals of

Botany 95: 1039–1047.

Winkler, M., Hulber, K. & Hietz, P. 2007. Population dynamics

of epiphytic bromeliads: life strategies and the role of host

branches. Basic and Applied Ecology 8: 183–196.

Wolf, J.H.D. 2005. The response of epiphytes to anthropogenic

disturbance of pine-oak forests in the highlands of Chiapas,

Mexico. Forest Ecology and Management 212: 376–393.

Yeaton, R.I. & Gladstone, D.E. 1982. The pattern of colonization

of epiphytes on calabash trees (Crescentia alata HBK.) in

Guanacaste Province, Costa Rica. Biotropica 14: 137–140.

Zar, J.H. 1996. Biostatistical analysis. Prentice Hall, Prentice, NJ, US.

Zotz, G. & Andrade, J.L. 1998. Water relations of two co-

occurring epiphytic bromeliads. Journal of Plant Physiology

152: 545–554.

Zotz, G. & Vollrath, B. 2003. The epiphyte vegetation of the

palm Socratea exorrhiza correlations with tree size, tree age

and bryophyte cover. Journal of Tropical Ecology 19: 81–90.



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