Bc

TAI

a

ARR2A

KBCCDFH

1

(2t

(

0h

Agriculture, Ecosystems and Environment 181 (2013) 149– 156

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

jo ur nal ho me page: www.elsev ier .com/ locate /agee

enefits and costs of epiphyte management in shadeoffee plantations

arin Toledo-Aceves ∗, Klaus Mehltreter, José G. García-Franco,driana Hernández-Rojas, Vinicio J. Sosa

nstituto de Ecología, A.C., Red de Ecología Funcional, Carretera Antigua a Coatepec No. 351, El Haya, Xalapa 91070, Veracruz, Mexico

r t i c l e i n f o

rticle history:eceived 25 June 2013eceived in revised form6 September 2013ccepted 27 September 2013

eywords:romeliadsanopyoffee managementiversified productionernsarvesting

a b s t r a c t

While epiphytes contribute to the biodiversity and structural complexity of shade coffee, their removalfrom the shade trees is a common management practice in Latin America. We studied the impact of epi-phyte removal on coffee productivity and the potential for epiphyte harvesting in a large coffee plantation(200 ha), and measured the supply of naturally fallen epiphytes in two small coffee plantations (<10 ha)unsuitable for epiphyte harvesting due to low epiphyte recovery rates following removal. Ten trees werestripped of all epiphytes (E−) and a further ten trees were used as control (E+) in the large coffee plan-tation. Four coffee plants under each tree canopy were selected and the production of flowers and fruitswas registered over two consecutive years. Photosynthetic Active Radiation (PAR), relative humidity andtemperature were also measured under the canopy of all 20 trees. To estimate the potential harvestof epiphytic bromeliads in the large coffee plantation, all the plants stripped from the ten trees wererecorded. The supply of naturally fallen epiphytes was recorded in ten plots (5 × 5 m) in the two smallcoffee plantations. From January to June, all fallen plants inside these plots were collected monthly, iden-tified, measured and their condition recorded. Finally, we conducted a cost-benefit analysis of epiphytemanagement in coffee plantations. Epiphyte removal had a significant positive effect on coffee produc-tivity; coffee plants produced 225% and 366% more flowers and fruits, respectively. Epiphyte removalsignificantly increased mean PAR, but had no effect on temperature and relative humidity. At the largecoffee plantation 48 species of vascular epiphytes were registered, 20 of which were bromeliads. On aver-age 727 ± 227 bromeliad rosettes were recorded per individual tree (considering all bromeliad species).In the small coffee plantations, 33 and 37 vascular epiphyte species were recorded, 21 of which werebromeliads. Approximately 21% of fallen epiphytes at the small coffee plantations were in a conditionsuitable for commercialization. Considering all the species and only plants in suitable condition, approx-imately 2252 ± 397 and 1421 ± 166 plants ha−1 per month could be collected for commercialization fromthe small coffee plantations. The potential profits from the sale of bromeliads can be considerable; $

−1 −1 −1 −1

8923 USD ha y from direct harvesting, and $6857 to $11070 USD ha y from collection from theground. A controlled rotation system of epiphyte harvesting should be implemented in large coffee plan-tations in order to allow the recuperation of the epiphytic community. Collection of fallen epiphytes isrecommended in the small coffee plantations that represent the majority in Central Veracruz. Appropri-ate management of epiphytes in shade coffee plantations could contribute to an income diversificationfor coffee farmers with potential for replication in other countries.

. Introduction

Shade coffee plantations are an important refuge for biodiversity

Perfecto et al., 1996; Moguel and Toledo, 1999; Beenhouwer et al.,013). Epiphytes are a key component of this agrosystem; they con-ribute to the biodiversity and structural complexity and provide

∗ Corresponding author. Tel.: +52 (228) 8421800x4217.E-mail addresses: tarintoledo@gmail.com, tarin.toledo@inecol.mx

T. Toledo-Aceves).

167-8809/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.agee.2013.09.026

© 2013 Elsevier B.V. All rights reserved.

a wider range of habitats for associated animals (Cruz-Angón andGreenberg, 2005; Hietz, 2005; García-Estrada et al., 2006; Cruz-Angón et al., 2009). The deliberate removal of epiphytes from shadetrees has been a common management practice within coffee sys-tems in Latin America (Cruz-Angón and Greenberg, 2005). Thisactivity forms part of the maintenance of the shade trees, sinceproducers commonly consider epiphytes to be tree parasites and a

damage risk to the coffee plants when they fall. Epiphyte removalsimplifies the agroecosystem, with negative impacts on the asso-ciated fauna (Greenberg et al., 1997; Cruz-Angón and Greenberg,2005; Cruz-Angón et al., 2009) and on the epiphytic community

1 stems

itrmpner

aiaTipVcm(owteihhptascctc

2

2

tstsimc(afisgTmtVppdl

tcfS

50 T. Toledo-Aceves et al. / Agriculture, Ecosy

tself (Toledo Aceves et al., 2012). Epiphyte removal may also affecthe coffee plants through increased irradiance and temperature andeduced humidity, with increased fluctuations of these environ-ental factors. However, to date the effects of this practice on the

erformance of coffee plants have not been evaluated. Determi-ation of the impact of epiphyte removal on the coffee yield maynable the economic and environmental costs of this practice to beeduced.

Although epiphytes are removed from coffee plantations, theyre currently not commercialized even though there is an increas-ng demand for these plants in Southern Mexico (Flores-Palaciosnd Valencia-Díaz, 2007; Haeckel, 2008; Hornung-Leoni, 2011;oledo-Aceves and Wolf, 2008; Wolf and Konings, 2001). Thellegal trade of large amounts of epiphytes for ornamental pur-oses is widespread in Mexico and Guatemala (Flores-Palacios andalencia-Díaz, 2007; Hietz et al., 2002). Epiphyte harvesting inoffee plantations has been recommended as part of a manage-ent plan, under favorable conditions for epiphyte recolonization

Toledo Aceves et al., 2012). However, commercial harvestingf epiphytes would be unsustainable in small coffee plantationshere rotation systems cannot be implemented in order to main-

ain the populations. The main cause of natural mortality inpiphytes is detachment from the trees (Winkler et al., 2007) and,n montane forests, detachment occurs in thousands of plants perectare (Mondragón-Chaparro and Ticktin, 2011); however, thereave been no reports of the collection of fallen plants from coffeelantations. To provide recommendations for optimized produc-ion and biodiversity conservation in the coffee agroecosystem, weddressed the following questions: Does epiphyte removal fromhade trees increase coffee yield? How many epiphytic bromeliadsan be harvested from shade trees? How many detached epiphytesan be collected from the ground? What is the potential produc-ivity of epiphytes with which to diversify the production of shadeoffee plantations?

. Methods

.1. Study area

Three coffee plantations (“fincas”) that can be classified asraditional polycultures (Hernández-Martínez et al., 2009), weretudied because the owners expressed an interest in diversifyingheir plantation production. Traditional polycultures are usuallymall to medium-sized with different combinations of native andntroduced shade trees (typically fruit-bearing species); manage-

ent includes manual weed control and occasional pruning of theoffee plants, but excludes the application of fertilizers or pesticidesHernández-Martínez et al., 2009). The dominant shade tree speciest all sites was Inga jinicuil Schltdl. & Cham. ex. G. Don., a nitrogenxing, fast-growing legume frequently planted in order to improveoil fertility; other species present include Citrus aurantium, Psidiumuajava, Alchornea latifolia, Musa sapientum and Rapanea myricoides.he effect of epiphyte removal on coffee plant performance and theicroenvironment was evaluated in the large (200 ha) coffee plan-

ation “Finca La Orduna”, located in the municipality of Coatepec,eracruz, Mexico (19◦ 28′ 03′′ N, 96◦ 55′ 58′′ W; 1200 m asl). Epi-hyte harvesting has been recommended as part of a managementlan for this coffee plantation, based on the composition and abun-ance of epiphytes, the rates of recovery for some species and the

arge area of the plantation itself (Toledo Aceves et al., 2012).Coffee plantation sizes in the region show a skewed dis-

ribution (range: 0.97–18.73 ha, mode = 1.00 ha, mean = 3.92 ha,alculated from data for n = 60 plantations randomly selectedrom the Padrón Nacional Cafetalero, January 2010 update,IAP–SAGARPA–AMECAFE). Since most coffee plantations in the

and Environment 181 (2013) 149– 156

region are small in area, they are unsuitable for sustainable epi-phyte harvesting, considering post-removal rates of recovery forvascular epiphytes (Toledo Aceves et al., 2012). To evaluate thepotential supply of naturally fallen epiphytes, two small shade cof-fee plantations were studied: “Finca Nebel”, with one ha of plantedshade coffee, in the municipality of Coatepec (19◦ 54′ 19′′N, 96◦ 58′

32′′ W; 1200–1300 m asl) and “Finca San Rafael”, of 6 ha, located inthe municipality of Cosautlán de Carvajal (19◦ 56′ 16.77′′ N, 96◦ 56′

52.93′′ W; 1200–1300 m asl).

2.2. Effect of epiphyte removal on coffee plants andmicroenvironment

To measure the effect of epiphyte removal on coffee plants, werandomly selected 20 Inga jinicuil trees at La Orduna in May 2011.The prevalence of I. jinicuil as a shade tree in local coffee plantations(López-Gómez et al., 2008), with its simple, mono-layered canopy,standardizes the evaluation of the impact of epiphyte removal oncoffee plant performance and facilitates future comparisons withother coffee plantations. All epiphytes were completely removedfrom ten of the trees (treatment E−) by climbing the trees and strip-ping the epiphytes. Ten trees were left undisturbed as a control(treatment E+). All trees were located at least 10 m apart. For eachtree, diameter at 1.3 m height (dbh) and projected canopy area weremeasured. At each of the four cardinal directions of each tree, weselected one coffee plant below the tree canopy, totaling 40 coffeeplants per treatment. For each coffee plant, we measured height,canopy projected area, number of main branches, number of flow-ers and fruits produced and specific leaf area (SLA = leaf area/leafdry weight cm2 g−1), in 2011 and 2012. In each coffee plant, twobranches were randomly selected and the number of flowers andfruits produced were counted (in May and November, respectively),while a rectangle of 3 × 5 cm was cut from two leaves and dried toquantify the SLA. The two values were averaged to calculate themean number of flowers, fruits and SLA per plant.

To evaluate the effect of epiphyte removal on the understorymicroenvironment, a set of data loggers (HOBO Microstation OnsetComputer Corporation), with sensors for light (PAR), temperatureand humidity, were located on top of one coffee plant per sampledtree. Due to the limited number of available data loggers, one groupof three pairs was measured at a time (three in E− and three in E+). Inorder to measure all the trees, the measurements had to be carriedout on different days.

2.3. Potential supply of epiphytes

Since the impact of epiphyte removal on the epiphytic com-munity showed that bromeliads displayed higher rates of recoverythan other groups, such as ferns and orchids (Toledo Aceves et al.,2012), the number of bromeliad rosettes that could be suppliedfrom harvesting at the large coffee plantation “Finca la Orduna”was quantified. For this purpose, all bromeliads removed fromten trees were measured and each rosette assigned to one ofthe following size classes of maximum leaf length: (1) 5–10 cm,(2) 11–20 cm, (3) 21–30 cm, (4) 31–40 cm, (5) 41–50 cm, and (6)>50 cm. Many species of bromeliads produce various rosettes orshoots per genet, and the rosettes can be separated for sale as sin-gle plants. Presence of reproductive organs was registered for eachrosette. Because small plants could not be identified with confi-dence, only plants > 5 cm in height were identified to species level.

In the two small coffee plantations, ten plots (5 × 5 m) wereestablished to estimate the potential supply of fallen epiphytes.

This vertical flux was recorded to determine a reliable number ofplants available for collection from the ground. All fallen plants inthe plots were collected, identified, measured and their conditionevaluated monthly from January to June 2012, thus including the

stems and Environment 181 (2013) 149– 156 151

soigcawcom

dw

2a

cIfphr

tsareaDtfaifStiCmc

2

uaKsrmoSda

3

3

omctp

Table 1Tree and coffee plant attributes (mean ± 1 SE) prior to epiphyte removal (treatmentsE+ and E−) in a shade coffee plantation in central Veracruz, Mexico. No significantdifferences were found between plants assigned to either treatment (P > 0.05).

E+ E−

Tree dbh (cm) 39.1 ± 3.0 34.3 ± 1.4Tree canopy area (m2) 99.2 ± 9.8 97.6 ± 9.4Coffee SLA (cm2 g−1) 107.3 ± 1.8 105.1 ± 1.5Coffee height (m) 3.0 ± 0.1 2.8 ± 0.1Coffee diameter (cm) 12.2 ± 0.7 11.7 ± 1.0Coffee number of branches 4.4 ± 0.3 4.4 ± 0.4Coffee canopy area (m2) 5.2 ± 0.3 4.7 ± 0.3

No.

flow

ers

/ cof

fee

plan

t

0

200

400

600

800 E+ E-

2011 20 12

No.

frui

ts /

coffe

e pl

ant

0

50

100

150

200

250

300

a

b

a

b

Fig. 1. Effect of epiphyte removal from shade trees on performance of coffee plants(mean ± 1 SE) after 6 and 18 months (2011 and 2012, respectively) in a shade cof-

T. Toledo-Aceves et al. / Agriculture, Ecosy

eason of northern cold-fronts, as well as the dry and the beginningf the rainy seasons. Species were classified as large or mediumn size, and all plants were assigned to one of the six size cate-ories described. Condition categories were: (1) Good, healthy andomplete, without damage, (2) Fair, healthy but with signs of dam-ge such as partially eaten and/or withered leaves, and (3) Poor,ith signs of disease such as spots on the leaves and/or rotten

enter. Plants with damage or signs of disease could contaminatether plants and would require maintenance, which would increaseanagement costs.Species were identified at the Herbarium (XAL) of the Instituto

e Ecología, A.C. Specimens that could not be identified to speciesere identified to genus level.

.4. Epiphyte management in coffee plantations and cost-benefitnalysis

To estimate the frequency of epiphyte removal in the region, 32offee farmers were interviewed in central Veracruz State, Mexico.nterviews consisted of six questions regarding the practice andrequency of epiphyte removal from shade trees, reasons for thisractice, species recognized, whether epiphytes are consideredarmful for the coffee plantation and interest in participating inegulated management of the epiphytes.

To evaluate the costs and benefits of removing all epiphytes fromhe shade trees, in terms of coffee productivity and profit from theale of epiphytes, we calculated the investment in epiphyte removalnd in collection of fallen epiphytes. All epiphytes were manuallyemoved from 10 trees in the large coffee plantation and fallenpiphytes were collected and processed (separating by conditionnd species when possible) at the two small coffee plantations.espite the importance of coffee production in central Veracruz,

here is no data available concerning the cost-benefit balance of cof-ee production. Most producers have several productive activitiesnd investment and income are assessed globally. Due to the lack ofnformation in the region, we used coffee production costs reportedor traditionally managed (without fertilization) plantations in thetate of Chiapas (production cost $477.4 USD/ha). To estimate theotal income, we used the reported earnings from cherry coffee salen Chiapas ($495.4 USD/ha net income) (López-López and Caamal-avich, 2009) and the price paid for bromeliads sold in the localarket (unpublished data). Based on these data, we estimated the

osts and benefits of epiphyte management in coffee plantations.

.5. Data analysis

The effects of epiphyte removal on measured variables of thenderstory microenvironment and coffee plant performance werenalyzed with ANOVA of a general linear model (GLM; Quinn andeough, 2002). Epiphyte removal treatment (E+ and E−) was con-idered a fixed factor, and the coffee plants nested within the tree asandom factors. To increase homoscedasticity and approach a nor-al distribution, numbers of flowers and fruits and percentages

f relative humidity were Box-Cox transformed (Crawley, 2002).ince environmental measurements were registered on differentays, day was included in the model as a block (random factor). Allnalyses were performed with MINITAB 16 (Minitab Inc. 2010).

. Results

.1. Epiphyte management in coffee plantations

Forty six percent of coffee plantation owners reported carrying out the removal

f epiphytes from shade trees at least once because epiphytes were considered detri-ental to the coffee plantation; the main reasons given were that epiphyte load can

ause tree branches to break, dry out and kill the support tree, causing damage tohe coffee plants below. Forty percent could recognize 1–3 different types of epi-hytes (not species), and 34% could recognize 4–10 different types. None of the

fee plantation. E+ = Control (black), E− = Epiphyte removal (grey). Different lettersdenote significant differences between epiphyte treatments (P < 0.05).

coffee owners interviewed collected epiphytes from the “fincas” and 75% expressedan interest in participating in their sustainable management.

3.2. Effects of epiphyte removal on coffee plants and microclimate

Tree and coffee plant size and SLA were similar between treatments prior toepiphyte removal in La Orduna (Table 1). Eighteen months after epiphyte removal,coffee plants produced significantly more flowers (225%) and fruits (366%) thanthose in the control treatment (Fig. 1; P < 0.05). Coffee plants also displayed sig-nificantly lower SLA at six months after epiphyte removal (SLA E+ = 161.6 ± 3.05,E− = 147.77 ± 3.01; P < 0.05), but this effect disappeared after 18 months (SLAE+ = 120.99 ± 2.33, E− = 118.97 ± 1.87; P > 0.05). Although microenvironmental vari-ables varied strongly among recording days, mean PAR increased significantlysix months after epiphyte removal (E+ = 241.5 ± 45.8, E− = 383.0 ± 44.8 mol m2 s;

+

P < 0.05). This difference, however, disappeared after 18 months (E = 277.7 ± 22.6;E− = 291.9 ± 36.1 mol m2 s; P > 0.05). Epiphyte removal had no significant effect onthe mean, maximum, minimum or variance values of temperature or relative humid-ity (P > 0.05 in each case).

152 T. Toledo-Aceves et al. / Agriculture, Ecosystems

Table 2Income (USD) from (a) harvesting and (b) direct collection of epiphytes from theground, in shade coffee plantations in central Veracruz, Mexico (number of fallenbromeliads in good condition from Appendix B). Production costs do not includeplant cultivation or maintenance in nurseries.

(a) Epiphyte harvesting (ha−1 y−1) Coffee Plantation

La Orduna215 trees (1 ha)

Cost of removing all epiphytes 4945Number of bromeliads in good condition 32680Cost of plant collection and processing 2472Potential income from plant sale 16340Income 8923

(b) Collection of fallen epiphytes (ha−1 y−1) Nebel San Rafael Average

Cost of plant collection and processing 1260 781 1020Number of bromeliads in good condition 24660 15276 19968

3

pbAipNd

osgai

Gaai

FTbwdboi

vf7iema$d(ab1im

4

4

dev

Potential income from plant sale 12330 7638 9984Income 11070 6857 8964

.3. Potential supply of epiphytes and cost-benefit analysis

Forty eight species of vascular epiphytes were registered in the large coffeelantation La Orduna; these are reported in Toledo Aceves et al. (2012). Nineteenromeliad species of the genera Tillandsia and Catopsis were registered (Appendix); the most abundant were Catopsis spp. (46.1% of the total number of rosettes reg-

stered), Tillandsia foliosa (23.6%) and T. belloensis (7.6%). In most species, only a smallroportion of plants had inflorescences (Fig. 2). On average, 727 ± 227 (mean ± S.E.;

= 10 trees) bromeliad rosettes were recorded per tree in this coffee plantation; foretails of the non-bromeliad species see Toledo Aceves et al. (2012).

In the small coffee plantations, Nebel and San Rafael, 33 and 37 morphospeciesf vascular epiphytes were recorded, respectively; 24 species were shared betweenites (Appendix B). Bromeliads and ferns (Polypodiaceae) were the most diverseroups at both sites, followed by orchids. Bromeliad abundance accounted for 67.6%nd 89.7% (of the total number of plants registered), and ferns for 11.1% and 7.82%,n Nebel and San Rafael, respectively.

The average percentage of fallen epiphytes per condition category wasood = 21.5% and 20.8%; Fair = 48.3% and 40.1% and Poor = 30.2% and 39.1%, in Nebelnd San Rafael, respectively. Considering only the fallen plants in good condition,pproximately 2252 ± 397 and 1421 ± 166 plants ha−1 mo−1 (mean ± 1 S.E.; includ-ng all species) could be collected at Nebel and San Rafael, respectively.

The condition of fallen plants was highly variable among species (Appendix B).ew abundant species (>20 plants ha−1 mo−1 e.g. Catopsis spp., Rhipsalis, T. limbata,. heterophylla, T. juncea) presented a high proportion of plants in good condition inoth coffee plantations. Although a small proportion of fallen T. schiedeana plantsere in good condition, this species was very abundant. The majority of speciesisplayed contrasting values between the two studied sites: Encyclia ochracea, T.otterie and T. tricolor for example, were fairly abundant and had a high proportionf plants in good condition at Nebel, but were substantially less abundant and mainlyn poor condition at San Rafael.

Regarding the costs and benefits, we summarize the balance for epiphyte har-esting and collection from the ground in Table 2. The complete removal of epiphytesrom a single tree (dbh = 39.1 ± 3.0 cm) had a labor cost of $ 23 USD. On average,27 rosettes of bromeliads could be obtained, of which approximately 152 were

n suitable condition for commercialization (other plant families were not consid-red due to the lower post-removal recovery capacity). In contrast, the number ofonthly fallen bromeliads in good condition ranges from 2055 to 1273 ha−1 at Nebel

nd San Rafael, respectively (Appendix B), with a collection cost of around $53 to33 USD (one person can collect and process approximately 225 plants in 1 workay, local daily pay is $US 11.5). Considering a mean price of $ 0.5 USD per rosettewholesale prices vary from $0.2 to 8 USD, depending on the aesthetic appearancend size of the plant, Toledo-Aceves unpubl. data), the estimated potential profit ofromeliad sales is approximately $ 8923 USD ha−1 y−1 from direct harvesting, and $1069–6857 USD ha−1 y−1 from the collection of fallen plants (Table 2). The estimate

s based on freshly collected plants and does not include the cost of cultivation oraintenance in a nursery.

. Discussion

.1. Impact of epiphyte removal on coffee productivity

Epiphyte removal produced a threefold increase in coffee pro-uction, which supports the rationale of this management practice,specially in shade coffee plantations with high canopy cover. Pre-ious studies evaluating the effect of canopy cover on coffee yield

and Environment 181 (2013) 149– 156

have found contradictory results (Perfecto et al., 2005; Soto-Pintoet al., 2000). Some studies show a significant increase in yield of10–30% after shade trees removal or pruning (Beer et al., 1998;Ostendorf, 1962; Pérez, 1977; Perfecto et al., 2005), but othersfound yield improvement or better grain quality with more shade(Beer et al., 1998; Muschler, 2001), while others find no differ-ence between shade and non-shade coffee (Hernández et al., 1997;Romero-Alvarado et al., 2002; Steiman et al., 2011), and other stud-ies found a “hump-shaped” relationship, with the highest yieldsproduced at intermediate light levels (Soto-Pinto et al., 2000; Staveret al., 2001). Such inconsistent results are probably due to widelyvarying site conditions and management. As stated by Beer et al.(1998), quantitative data about the level of shading in plantationsare often lacking or are difficult to compare since they have beenmeasured using different light sensors and methodologies. Analyz-ing the effect of shade on multiple, yield-reducing factors such asweeds, diseases and pests, Staver et al. (2001) concluded that coffeeyield is optimum between 35 and 65% of shade. Based on our find-ings, we associate increased flowering and fruit production withthe increase in irradiance produced by epiphyte removal. At thestudied coffee plantation La Orduna, Cruz-Angón and Greenberg(2005) reported a reduction in canopy cover from approximately52% to 25.45% as a result of the complete removal of epiphytes fromall shade trees in a total of 3 ha.

While changes in canopy cover strongly correlate with light con-ditions, air temperature is less affected by such changes (Brown,1993). The lack of a significant effect of epiphyte removal on airtemperature and humidity could be explained by the fact that thesefactors are not restricted to the area under the tree canopy; airtemperature and humidity in the coffee plantation are predomi-nantly influenced by air movement, which can equalize conditionsat a larger scale. The localized removal of epiphytes of some shadetrees was therefore insufficient to cause larger changes in thosevariables. In order to determine the impact of epiphyte removalon these and other factors, the complete removal of epiphytesfrom trees over a wider area is required, such as that carried outin the study by Cruz-Angón and Greenberg (2005). Regardlessof the lack of effects of epiphyte removal on the microenviron-ment, our results show that the coffee plants were significantlyaffected by epiphyte removal. Supporting these results, an experi-ment carried out in 2006 also showed that epiphyte removal causeda significant increase in the production of fruits per coffee plant(no. fruits/branch: E+ = 18.40 ± 2.30 and E− = 33.46 ± 3.77; Toledo-Aceves unpublished data).

It must be considered, however, that epiphyte removal causesa simplification of the agroecosystem, with negative effects onthe epiphytic community, wild fauna (Cruz-Angón and Greenberg,2005; Greenberg et al., 1997) and probably on other processesat the agroecosystem level, such as nutrient cycling. In naturalforests, epiphytes play an important role in nutrient and watercycling (Hofstede et al., 1993; Nadkarni, 1986) and these resourcescould be altered and their availability reduced as a result of epi-phyte removal. For example, epiphyte removal was reported tocause a reduction in soil moisture and an increase in stemflow andrain through-fall (Lorr, 2001 in Cruz-Angón and Greenberg, 2005).Such changes could cause a reduction in water availability for cof-fee plants. Evaluation over a longer time period would provide amore comprehensive evaluation of the impact of epiphyte removalon the coffee agroecosystem, in terms of the synergistic effects ofincreased canopy openness.

4.2. Potential for epiphyte management in shade coffee

plantations

Based on our assessment, and the findings of a previous studyin the region (Toledo Aceves et al., 2012), a selective epiphyte

T. Toledo-Aceves et al. / Agriculture, Ecosystems and Environment 181 (2013) 149– 156 153

5 -10 11-21 21-30 31-40 41-50 > 5 0 0

20

40

60

80

100

120

140

160

Tilland sia po lystach ia

N = 27 4

5 -10 11-21 21-30 31-40 41-50 > 50

No.

rose

ttes

0

20

40

60

80

100

120

140

160

Tilland sia he teroph ylla

N = 422

5 -10 11-21 21-30 31-40 41-50 > 5 0 0

20

40

60

80

100

120

140

160

Tillandsi a li mba ta

N = 341

5 -10 11 -21 21 -30 31 -40 41 -50 > 50

No.

rose

ttes

0

20

40

60

80

100

120

140

160

Tilland sia belloen sis

N = 56 4

5 -10 11-21 21-30 31-40 41-50 > 50 0

200

400

600

800Tilland sia f oli osa

N = 171 7

Tilland sia punct ulata

Length (cm)5 -10 11 -21 21 -30 31 -40 41 -50 > 50

0

20

40

60

80

100

120

140

160

Tilland sia t rico lor

Length (cm)

5 -10 11-21 21-30 31-40 41-50 > 50

No.

rose

ttes

0

20

40

60

80

100

120

140

160

N = 34 1 N = 75

No.

rose

ttes

Catopsis spp.

5 -10 11-21 21-30 0

500

1000

1500

2000

N = 335 0

F m leafi hite: p

httoBtSicctdt

ig. 2. Number of epiphytic bromeliad rosettes according to size category (maximun Central Veracruz, Mexico. Only the eight most abundant species are shown. In w

arvesting rotation system could be implemented in coffee planta-ions with a canopy cover >50%. Toledo Aceves et al. (2012) reporthat, following complete epiphyte removal, plants recovered 35.5%f their biomass (regardless of species) over a period of 8–9 years.ased on this figure, it is estimated that full biomass recovery couldake approximately 22–29 years (considering the mean value ± 1E). Due to the lack of more detailed information, this calculations based on various suppositions that may not be all satisfied:onstant recolonization rate, recovery of the entire epiphytic

ommunity in terms of structure and composition equivalent tohe recovery of biomass, and similar patterns of recovery acrossifferent coffee plantations. Under this scenario, a coffee planta-ion could be divided into 22–29 subareas in order to harvest one

length) registered on 10 shade trees in the large shade coffee plantation La Ordunalants without inflorescence; in grey, plants with inflorescence.

subarea per year. If the minimum harvesting area is 1 ha, the coffeeplantation would have to be 22–29 ha in extension. However,smaller harvesting areas could also be managed applying the samerotation system. In the large coffee plantation La Orduna, there areon average 215 Inga trees ha−1 (Cruz-Angón and Greenberg, 2005).Epiphyte removal in 1 ha y−1 could therefore supply thousands ofplants in suitable condition for commercial purposes, providing awindow of 29 years for the epiphytic community to reestablish,while simultaneously increasing the coffee yield.

We recommend that areas are not harvested contiguously butdispersed widely in order to ensure that harvested areas are sur-rounded by areas with epiphytes to favor seed dispersal. Also, thecontrolled removal of epiphytes from only the trunk and lower

154 T. Toledo-Aceves et al. / Agriculture, Ecosystems and Environment 181 (2013) 149– 156

Number of fallen epiphytes (number of plants ha−1 mo−1; mean ± 1 S.E.) and number of plants suitable for commercialization in the small shade coffee plantations FincaNebel (1 ha) and Finca San Rafael (6 ha), in central Veracruz, Mexico. The number of plants for collection represents plants in good condition only.

Family and Species No. of fallen plants/ha/month Plants in good condition (%) No. of plants suitable forcommercialization/ha/month

Nebel San Rafael Nebel San Rafael Nebel San Rafael

AraceaeAnthurium scandens (Aubl.) Engl. 63.6 ± 55.8 20.0 ± 11 11.5 60.0 18.9 12.0Syngonium sp. 6.3 0.0 100 0.0 6.3 0.0

BromeliaceaeCatopsis spp. 1485.0 ± 199 2906.0 ± 576 22.0 18.0 327.2 521.8Catopsis morreniana Mez 0.0 20.1 ± 12.7 0.0 40.0 0.0 8.0Tillandsia belloensis W. Weber 321.0 ± 80.0 337.2 ± 60.3 25.5 8.3 81.8 28.1Tillandsia botterie Baker 251.8 ± 63.1 220.8 ± 73.2 52.5 7.3 132.2 16.1Tillandsia butzii Mez 208.0 ± 108 32.1 3.0 100 6.30 32.1Tillandsia chlorophylla L. B. Smtih 37.8 ± 23.1 0.0 50.0 0.0 18.90 0.0Tillandsia filifolia Schltdl. & Cham. 0.0 76.3 ± 20.5 0.0 10.5 0.0 8.03Tillandsia heterophylla E. Morren 378.0 ± 110 116.4 ± 17.3 60.0 29.0 226.8 44.2Tillandsia ionantha Planch. 0.0 4.01 0.0 0.0 0.0 0.0Tillandsia juncea (Ruiz & Pav.) Poir. 2253 ± 298 807 ± 285 31.0 51.2 698.6 413.5Tillandsia limbata Schltdl. 327.3 ± 25.6 36.1 ± 22.4 25.9 55.6 84.9 20.1Tillandsia polystachia (L.) L. 182.5 ± 61.7 12 20.69 0.0 37.8 0.0Tillandsia punctulata Schltdl. & Cham. 264.4 ± 47.3 28.1 ± 15 16.7 0.0 44.1 0.0Tillandsia schiedeana Steud. 1290 ± 228 1365 ± 116 15.1 12.1 195.1 164.6Tillandsia tricolor Schltdl. & Cham. 346 ± 293 68.2 ± 53.7 54.5 5.9 188.7 4.0Tillandsia usneoides (L.) L. 0.0 60.2 ± 11 0.0 0.0 0.0 0.0Tillandsia variabilis Schltdl. 0.0 16.1 ± 11.7 0.0 50.0 0.0 8.1Tillandsia viridiflora (Beer) Baker 6.3 0.0 0.0 0.0 0.0 0.0Tillandsia sp 1. 0.0 4.0 0.0 100 0.0 4.0Tillandsia sp 2. 18.9 ± 7.7 12 66.7 0.0 12.6 0.0Tillandsia sp 3. 0.0 4.01 0.0 0.0 0.0 0.0CactaceaeRhipsalis baccifera Stearn 925 ± 295 24.1 ± 4.0 31.3 33.3 289.5 8.0LycopodicaceaeHuperzia linifolia (L.) Trevis. 151 ± 113 0.0 29.2 0.0 44.0 0.0

OrchidaceaeEncyclia ochracea (Lindl.) Dressler 25.2 ± 18.4 20.0 ± 12.7 75.0 0.0 18.9 0.0Jacquiniella sp. 88.1 ± 39.1 4.01 35.7 0.0 31.5 0.0Lepanthes avis Rchb. f. 56.6 ± 49.2 0.0 44.4 0.0 25.2 0.0Masdevallia sp.1 0.0 4.01 0.0 100 0.0 4.0Maxilaria densa Lindley 69.2 ± 25.2 12.0 ± 8.0 45.5 0.0 31.4 0.0Scaphyglottis livida (Lindl.) Schltr. 100.7 ± 37.8 8.0 ± 4.9 12.5 0.0 12.6 0.0

PiperaceaePeperomia dendrophila Schltdl. & Cham. 352 ± 101 0.0 17.9 0.0 62.9 0.0Peperomia tetraphylla Hook. & Arn. 579 ± 266 44.2 ± 11.1 17.4 36.4 100.7 16.1Peperomia quadrifolia (L.) Kunth 207.7 ± 83.6 8.0 ± 8.0 45.4 0 94.4 0Peperomia sp. 0.0 32.1 0.0 37.5 0.0 12.0PolypodiaceaeNiphidium crassifolium (L.) Lellinger 6.29 0.0 100 0.0 6.3 0.0Phlebodium pseudoaureum (Cav.) Lellinger 428 ± 61.8 128.5 ± 32.7 0.0 9.38 0.0 12.0Pleopeltis crassinervata (Fée) T. Moore 258.1 ± 75.4 148.5 ± 53.3 12.2 37.8 31.5 56.2Pleopeltis furfuracea A.R. Sm. 151.1 ± 37.8 172.4 ± 46.5 20.8 7.0 31.5 12.0Polypodium lepidotrichum (Fée) Maxon 0.0 16.1 ± 7.5 0.0 25.0 0.0 4.0Polypodium polypodioides (L.) Watt 0.0 4.0 0.0 0.0 0.0 0.0Polypodium sp. 1 0.0 4.0 0.0 100 0.0 4.0Polypodium sp. 2 0.0 4.0 0.0 100 0.0 4.0

15

cuKdbr

rrroAte

Serpocaulon triseriale (Sw.) A.R. Sm 12.6 48.2 ±Total 10950 6828

anopy has been recommended, in order to allow plants from thepper canopy to act as seed sources for recolonization (Wolf andonings, 2001). Removal of plants from the upper canopy is moreifficult in any case. Finally, such a harvesting system should ideallye selective, and take into account factors such as aesthetic appeal,elative abundance and response to disturbance.

In small coffee plantations, such as the studied sites and those ofeduced canopy cover (<50%), collection of fallen epiphytes couldepresent a good opportunity to diversify products. Althoughecording of fallen epiphytes was conducted over five months

nly, we did not find high variation among the sampled months.ccordingly, Mondragón-Chaparro and Ticktin (2011) reported

hat the number of fallen epiphytes in a montane forest in South-rn Mexico did not differ significantly among sampling seasons.

0.0 8.3 0.0 4.0– – 2854 1421

Direct collection of plants from the ground is recommended inorder to reduce the detrimental effects of epiphyte removal atthe agroecosystem level, such as the negative impact on theassociated fauna and the epiphyte community. However it shouldbe considered that plants on the ground might be more prone todecomposition and disease associated with the higher humidity atsoil level, in comparison to the canopy. Mondragón-Chaparro andTicktin (2011) reported that approximately 80% of fallen epiphyticbromelias died after three months on the forest floor. Even thoughplants in poor condition could be collected for cultivation as

mother plants, maintenance of such plants in nurseries is not rec-ommended, as this would increase production costs. Due to the lowproportion of bromeliads with inflorescence, commercializationshould target non-reproductive plants, which command a lower

T. Toledo-Aceves et al. / Agriculture, Ecosystems

Abundance of epiphytic bromeliads on shade trees in the large shade coffee planta-tion La Orduna in central Veracruz, Mexico (mean ± 1 S.E.; N = 10).

Species Abundance (no. rosettes/tree)

Catopsis spp. 335 ± 112Tillandsia belloensis 55.4 ± 19.6T. brachycaulos 2.20 ± 2.09T. butzii 2.70 ± 1.51T. depeanna 0.10T. fasciculata 2.20 ± 0.97T. filifolia 1.70T. aff. foliosa 171.7 ± 71.9T. heterophylla 42.2 ± 13T. ionantha 4.60 ± 3.02T. juncea* 0.90 ± 0.10T. kirchhoffiana 1.50T. limbata 35.1 ± 18.30T. multicaulis 0.20T. polystachya 27.4 ± 10.3T. punctulata 7.50 ± 4.34T. schiedeana* 1.00 ± 0.01T. tricolor 34.4 ± 14.5

*

sces

esbcaMh12prcthfsba

fcirrctaiapoce

5

fc

T. usneoides 0.40 ± 0.16T. variabilis 1.20 ± 0.57

* For these species, groups of several plants were registered.

ale price. Because coffee plantations also differ widely in speciesomposition (Hietz, 2005), the potential income from the sale ofpiphytes may vary considerably depending on which epiphytepecies are in higher demand and achieve higher sale prices.

Coffee plantations not only provide secure sites for epiphytestablishment, but also the conditions necessary to support self-ustained epiphyte populations (Solís-Montero et al., 2005). Theeneficial conditions of the coffee plantations for the spread ofertain epiphyte species represent an opportunity for the sustain-ble management of these plants (Toledo Aceves et al., 2012).oreover, diverse agroecosystems can provide alternative liveli-

oods for families, reducing economic risks (Moguel and Toledo,996) and the pressure on natural forests (Blackman and Albers,003; Gordon et al., 2007). The results of the estimate of epi-hyte management costs and benefits suggest that both epiphyteemoval and direct collection from the ground could supplementoffee production. Appropriate epiphyte management could con-ribute to diversification of the agroecosystem productivity whileelping to reduce the pressure from illegal canopy harvesting

rom natural forests. In order to support the development ofuch strategies, coffee owners, managers and consumers need toe informed of the important role that epiphytes play in thisgroecosystem.

Epiphytes are an important component of biodiversity in cof-ee agroecosystems; Philpott et al. (2008) report the significantontribution of epiphytes in the Neotropics, particularly in lessntensively managed coffee farms. In one of the few studiesegarding this group in Africa, Hylander and Nemomissa (2008)eport important epiphyte diversity in home gardens growingoffee in Ethiopia. Méndez et al. (2010) also found a significant con-ribution of epiphytes to biodiversity in coffee farms in Nicaraguand El Salvador. According to these authors epiphytes have anmportant value for Nicaraguan farmers as ornamental plants, andre sold illegally. Considering the important contribution of epi-hytes to biodiversity in coffee farms reported in various countries,ur findings and recommendations could be adjusted to particularoffee farm conditions in different countries in order to improveconomic sustainability in the management of biodiversity.

. Conclusions

High potential for epiphyte management exists in the shade cof-ee plantations of Central Veracruz; thousands of epiphytes in goodondition could be harvested per year from shade trees in large

and Environment 181 (2013) 149– 156 155

coffee plantations, or collected directly from the ground (fallenplants) in small coffee plantations, for commercial purposes. Ourassessment indicates that epiphyte removal produces a signifi-cant increase in coffee yield. Appropriate epiphyte managementcan reinforce the capacity of shade coffee plantations to functionas reservoirs of biodiversity while simultaneously enhancing theireconomic productivity.

Acknowledgments

We thank Laura Cabanas, Efrén Melchor and Raúl Monge fortheir support with the studies in the coffee plantations and LeticiaMonge for field data collection. We are grateful to Keith MacMillanfor field data collection and revision of the manuscript. We thankGabriel Díaz and Rafael Guajardo for providing data about coffeeplantations extension. We thank R.H. Manson for coordinating thisproject, which was funded by FORDECYT (No. 139378 “Consoli-dación de una red agroecológica intersectorial de innovación paralograr una cafeticultura sustentable en el centro del estado de Vera-cruz”) and supported by the personnel and facilities of the Institutode Ecología, A.C.

Appendix A.

Appendix B.

References

Beenhouwer, M.D., Aerts, R., Honnaya, O., 2013. A global meta-analysis of the bio-diversity and ecosystem service benefits of coffee and cacao agroforestry. Agric.Ecosyst. Environ. 175, 1–7.

Beer, J., Muschler, R., Kass, D., Somarriba, E., 1998. Shade management in coffee andcacao plantations. Agroforestry Syst. 38, 139–164.

Blackman, A., Albers, H., Ávalos-Sartorio, B., Crooks, B., 2003. Land cover in a managedforest ecosystem: Mexican shade coffee. Discussion paper 03–60. Resources forthe Future, Washington, D.C.

Brown, N.D., 1993. The implications of climate and gap microclimate for seedlingsin a Bornean lowland rain forest. J. Trop. Ecol. 9, 153–168.

Crawley, M., 2002. Statistical Computing. An Introduction to Data Analysis usingS-Plus. John Wiley & Sons Ltd., Chichester, UK.

Cruz-Angón, A., Baena, M.L., Greenberg, R., 2009. The contribution of epiphytes to theabundance and species richness of canopy insects in a Mexican coffee plantation.J. Trop. Ecol. 25, 453–463.

Cruz-Angón, A., Greenberg, R., 2005. Are epiphytes important for birdsin coffee plantations? An experimental assessment. J. Appl. Ecol. 42,150–159.

Flores-Palacios, A., Valencia-Díaz, S., 2007. Local illegal trade reveals unknown diver-sity and involves a high species richness of wild vascular epiphytes. Biol. Conserv.136, 372–387.

García-Estrada, C., Damon, A., Sánchez-Hernández, C., Soto-Pinto, L., Ibarra-Núnez,G., 2006. Bat diversity in montane rainforest and shaded coffee under differ-ent management practices in southeastern Chiapas, Mexico. Biol. Conserv. 132,351–361.

Gordon, C., Manson, R., Sundberg, J., Cruz-Angón, A., 2007. Biodiversity, profitabil-ity, and vegetation structure in a Mexican coffee agroecosystem. Agric. Ecosyst.Environ. 118, 256–266.

Greenberg, R., Bichier, P., Sterling, J., 1997. Bird populations in rustic and plantedshade coffee plantations of eastern Chiapas. Biotropica 29, 501–514.

Haeckel, I.B., 2008. The Arco Floral: Ethnobotany of Tillandsia and Dasylirion spp. ina mexican religious adornment. Econ. Bot. 62, 90–95.

Hernández-Martínez, G., Manson, R.H., Contreras Hernández, A., 2009. Quantitativeclassification of coffee agroecosystems spanning a range of production intensi-ties in central Veracruz, Mexico. Agric. Ecosyst. Environ. 134, 89–98.

Hernández, O., Beer, J., Von Platen, H., 1997. Rendimiento de café (Coffea arabicacv Caturra), producción de madera (Cordia alliodora) y análisis financiero deplantaciones con diferentes densidades de sombra en Costa Rica. Agroforester.Américas 4, 8–13.

Hietz, P., 2005. Conservation of vascular epiphyte diversity in Mexican coffee plan-tations. Conserv. Biol. 19, 391–399.

Hietz, P., Ausserer, J., Schindler, G., 2002. Growth, maturation and survival ofepiphytic bromeliads in a Mexican humid montane forest. J. Trop. Ecol. 18,

177–191.

Hofstede, R.G.M., Wolf, J.H.D., Benzing, D.H., 1993. Epiphytic biomass and nutrientstatus of a Colombian upper montane rain forest. Selbyana 14, 37–45.

Hornung-Leoni, C.T., 2011. Avances sobre usos etnobotánicos de las Bromeliaceaeen Latinoamérica. Bol. Latinoam. Caribe Plant. Med. Aromát. 10, 297–314.

1 stems

H

L

L

M

M

M

M

M

N

O

P

P

P

P

56 T. Toledo-Aceves et al. / Agriculture, Ecosy

ylander, K., Nemomissa, S., 2008. Home garden coffee as a repository of epiphytebiodiversity in Ethiopia. Front. Ecol. Environ. 6, 524–528.

ópez-Gómez, A.M., Williams-Linera, G., Manson, R.H., 2008. Tree species diver-sity and vegetation structure in shade coffee farms in Veracruz, Mexico. Agric.Ecosyst. Environ. 124, 160–172.

ópez-López, E.C., Caamal-Cavich, I., 2009. Los costos de producción del café orgánicodel estado de Chiapas y el precio justo en el mercado internacional. Rev. Mex.Econom. Agríc. Recurs. Natur. 2, 175–198.

éndez, V.E., Bacon, Ch.M., Olson, M., Morris, K.S., Shattuck, A., 2010. Agrobiodi-versity and shade coffee smallholder livelihoods: a review and synthesis of tenyears of research in Central America. Profess. Geogr. 62, 357–376.

oguel, P., Toledo, V.M., 1996. El café en México, ecología, cultura indígena y sus-tentabilidad. Ciencias 43, 40–51.

oguel, P., Toledo, V., 1999. Biodiversity conservation in traditional coffee systemsin Mexico. Conserv. Biol. 13, 1–12.

ondragón-Chaparro, D., Ticktin, T., 2011. Demographic effects of harvesting epi-phytic bromeliads and an alternative approach to collection. Conserv. Biol. 25,797–807.

uschler, R.G., 2001. Shade improves coffee quality in a sub-optimal coffee-zone ofCosta Rica. Agroforestry Syst. 51, 131–139.

adkarni, N.M., 1986. The nutritional effects of epiphytes on host trees with specialreference to alteration of precipitation chemistry. Selbyana 9, 44–51.

stendorf, F.W., 1962. The Coffee shade problem. A review article. Tropical Abstract17, 577–581.

erfecto, I., Rice, R.A., Greenberg, R., van der Voort, M.E., 1996. Shade coffee: a dis-appearing refuge for biodiversity. BioScience 46, 598–608.

érez, V., 1977. Veinticinco anos de investigación sistematica del cultivo del café en

Costa Rica: 1950-1975. Agronomía Costarricense 1, 169–185.

erfecto, I., Vandermeer, J., Mas, A., Soto-Pinto, L., 2005. Biodiversity, yield, and shadecoffee certification. Ecol. Econ. 54, 435–446.

hilpott, 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.,

and Environment 181 (2013) 149– 156

Williams-Linera, G., Valenzuela, J., Zolotoff, J.M., 2008. Biodiversity loss in LatinAmerican coffee landscapes: review of the evidence on ants, birds, and trees.Conserv. Biol. 22, 1093–1105.

Romero-Alvarado, Y., Soto-Pinto, L., García-Barrios, L., Barrera-Gaytán, J.F., 2002. Cof-fee yields and soil nutrients under the shades of Inga sp. vs. multiple species inChiapas, Mexico. Agroforestry Systems 54, 215–224.

Quinn, G., Keough, M.J., 2002. Experimental Design and Data Analysis for Biologists.Cambridge University Press, Cambridge, UK.

Solís-Montero, L., Flores-Palacios, A., Cruz-Angón, A., 2005. Shade-coffee plantationsas refuges for tropical wild orchids in central Veracruz, Mexico. Conserv. Biol.19, 908–916.

Soto-Pinto, L., Perfecto, I., Castillo-Hernández, J., Caballero-Nieto, J., 2000. Shadeeffect on coffee production at the northern Tzeltal zone of the state of Chiapas,Mexico. Agric. Ecosyst. Environ. 80, 61–69.

Staver, C., Guharay, F., Monterroso, D., Muschler, R.G., 2001. Designing pest-suppressive multistrata perennial crop systems: shade-grown coffee in CentralAmerica. Agroforestry Syst. 53, 151–170.

Steiman, S., Idol, T., Bittenbender, H.C., Gautz, L., 2011. Shade coffee inHawai’i—exploring some aspects of quality, growth, yield, and nutrition. Sci.Horticult. 128, 152–158.

Toledo-Aceves, T., Wolf, J.H., 2008. Germination and establishment of Tillandsia eizii(Bromeliaceae) in the canopy of an oak forest in Chiapas. México Biotrop. 40,246–250.

Toledo Aceves, T., García-Franco, J.G., Hernández-Rojas, A., MacMillan, K., 2012.Recolonization of vascular epiphytes in a shaded coffee agroecosystem. Appl.Vegetat. Sci. 15, 99–107.

Winkler, M., Hülber, K., Hietz, P., 2007. Population dynamics of epiphytic bro-

meliads: life strategies and the role of host branches. Basic Appl. Ecol. 8,183–196.

Wolf, J.H.D., Konings, C.J.F., 2001. Toward the sustainable harvesting of epiphyticbromeliads: a pilot study from the highlands of Chiapas, Mexico. Biol. Conserv.101, 23–31.