evaluación experimental sobre la importancia de las epífitas para la

EVALUACIÓN EXPERIMENTAL SOBRE LA IMPORTANCIA
DE LAS EPÍFITAS PARA LA CONSERVACIÓN DE LA
BIODIVERSIDAD EN PLANTACIONES DE CAFÉ
TESIS QUE PRESENTA ANDREA CRUZ ANGÓN
PARA OBTENER EL GRADO DE DOCTOR EN CIENCIAS EN
ECOLOGÍA Y MANEJO DE RECURSOS NATURALES
Xalapa, Veracruz, México, 2007
INSTITUTO DE
ECOlOGIA, A.C.
Aprobación de documento final de tesis de grado:
en plantacionesde café
Director de tesis
Nombre
Dr. Russell Greenberg
Comité Tutorial
Dr. Victor Rico-Gray
Dra. María del Coro
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Dr. José G. García Franco
Jurado
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Dr. Gonzalo Halffter
Dr. Thorsten Kromer
Dra. Guadalupe WilliamsLinera
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RECONOCIMIENTOS
Este trabajo fue posible gracias a los siguientes apoyos institucionales otorgados a Andrea Cruz Angón:
beca de doctorado Conacyt (128767), el Smithsonian Institution Visiting Award (2002 – 2003), el Instituto
de Ecología, A.C. y becas otorgadas al Dr. Russell Greenberg a través de la National Geographic Society y
el Scholarly Studies Fund del Smithsonian Institution.
Al Dr. Russell Greenberg, mi director de tesis y gran amigo, con quien tuve el placer de trabajar todos estos
años, gracias por su apoyo, paciencia y confianza a lo largo de todo este tiempo.
Al Dr. José G. García Franco, mi supervisor, gracias por haberme “adoptado” con tan buen talante, por su
estupendo apoyo (académico, logístico y humorístico), por su interminablemente buena disposición para
ayudarme, sus buenas carcajadas, sus latigazos y su excelente amistad: ¡Pepe eres un tipazo!.
Al Dr. Victor Rico, por sus siempre atinados, eficaces y eficientes apoyos, sugerencias y comentarios a mi
trabajo doctoral.
A la Dr. Maria del Coro Arizmendi por sus excelentes comentarios siempre rápidos a los escritos y por
disposición para atenderme desde cualquier parte del mundo!
A los miembros de mi jurado: Dr. Gonzalo Halffter, Dra. Guadalupe Williams-Linera y Dr. Thorsten Krömer,
gracias por sus excelentes y rápidos comentarios, que permitieron enriquecer la versión final de esta tesis.
El trabajo de campo fue asistido por Alberto Martínez Fernández, pieza fundamental en este trabajo,
gracias por las levantadas temprano, los días de redeo y reavistamiento, por su buen ánimo, su gusto para
aprender y salir adelante.
Martha Lucía Baena, Clementina González Zaragoza, Peter Bichier Garrido y Benjamin Lorr me asistieron
en distintas fases del proyecto, también gracias por los arduos meses de identificación de insectos, días de
redeo, etc. Felipe Becerril realizó las ilustraciones presentadas en este documento.
Al Dr. Francisco Ornelas Rodríguez, quien me abrió las puertas de su laboratorio y me dio las primeras
facilidades para desarrollar este trabajo de tesis.
Al Dr. Alejandro Flores Palacios, gracias su amistad, los buenos momentos de campo, las buenas
platicadas.
Al Dr. Andrew P. Vovides, quien me revisó algunos manuscritos y me proporcionó, además de su amistad,
excelentes buenas vibras, cartas de recomendación y un medio de subsistencia para parte del año 2004.
Al Dr. Vinicio Sosa, quien me ayudó con algunos análisis estadísticos, y revisó algunos de los manuscritos,
excelente maestro y buen amigo.
Las familias que me acogieron durante mis estancias en Washington DC, Paul-Boucher (mi familia
americo-sudafri-australiana: Ellen, Tim y Toodles, gracias por las noches de L&O, pizza y cerveza!) y
Gradwohl-Greenberg (Judy, Russ, Natalie y Jeremy: gracias por todo su apoyo y compañía).
El Staff del Smithsonian Migratory Bird Center (Scott Sillett, Megan Myers, Mary Deinlain, Bob Rice y Greg
Dough) que siempre me apoyaron en lo que necesite.
Stacy Philpott comentó y revisó los documentos que le mandé, siempre de manera rápida y con opiniones
y sugerencias sumamente acertadas.
Las Familias Brio-Xala-Coate-Ranchoviejeñas: González-Zaragoza, Ordano-Burgos, Doña Mica y Don
José, Vovides-Tejeda, gracias por abrirme las puertas de sus casas, por su confianza, solidaridad y buenas
vibras. A la comuna, mis vecinitos (Ivan, Astrid, Camilo, Dario, Marisa, Octavio, Valeria, Rosario y Rita,) y a
Rosa María, que me proporcionó un maravilloso lugar dónde vivir.
3
DEDICATORIA
Por alguna extraña razón he tenido la fortuna de formar parte de una familia (cada vez más grande) chida,
amorosa y solidaria, de la que he aprendido el valor y la responsabilidad del trabajo honesto, el gusto por la
vida y los libros, la compasión y el amor incondicional: Pilar y Gerardo, Ren y Pau, mis referentes de vida,
mis refugios; Leny, Ger, Franco, Mariana y Edu los ojos nuevos a través de los cuales redescubro la vida;
Susen, Anita, Chavo, Elena, Rosalí, Ago, Andrea R., todos ejemplos de fortaleza, bondad, solidaridad,
locuacidad, integridad y tenacidad; Ren, Tarin, Clemen, Ellen, Vicky, Chela y Ufe, mis hermanas, mis
amigas, las viejas, las nuevas, las reencontradas y las reinventadas; Pau, Jaime, Mariano y Pedro mis
referentes XY, mis cuates de siempre... el buen Bantú que me regaló un pez lunafílico; Diego y Macario
siempre presentes y entrañables; Yola y compañía, la oscuridad como principio universal y la luz de la
tranquilidad... Jaime, las constelaciones, los silencios, su paciencia; El cafetal y sus gnomos, con epífitas y
sin ellas, a San Chárbel y San Google, que de más de una me habrán salvado... ¡A los pollitos en fuga que
consiguieron librarse de su karma, bien por ellos! 4
DECLARACiÓN
Excepto cuando es explícitamente
indicado en el texto, el trabajo de investigación
en esta tesis fue efectuado por la Bióloga Andrea Curz Angón como estudiante de
la carrera de Doctorado en Ciencias (Ecología y Manejo de Recursos Naturales)
entre enero de 1998 y enero de 2003, bajo la dirección del Dr. Russell Greenberg.
Las investigaciones
reportadas en esta tesis no han sido utilzadas anteriormente
para obtener otros grados académicos,
ni serán utilizadas para tales fines en el
futu ro.
Candidato
Andrea Cruz Angón
Director de tesis
,¿- ¿-
..;2--
Russell Greenberg
5
ÍNDICE
LISTA DE CUADROS .......................................................................................................................................8
LISTA DE FIGURAS .........................................................................................................................................9
RESUMEN .......................................................................................................................................................10
CAPÍTULO I. INTRODUCCIÓN GENERAL ...................................................................................................13
LA CRISIS GLOBAL DE LA PÉRDIDA DE BIODIVERSIDAD .......................................................................................................................13
CAFÉ EN MÉXICO ..........................................................................................................................................................................14
CAFÉ Y BIODIVERSIDAD ..................................................................................................................................................................16
EPÍFITAS, AVES E INSECTOS ..........................................................................................................................................................17
GRADO DE EPIFITISMO ...................................................................................................................................................................18
CAFÉ, EPÍFITAS, AVES E INSECTOS ................................................................................................................................................19
EFECTOS DE LA REMOCIÓN DE EPÍFITAS EN CAFETALES....................................................................................................................20
HIPÓTESIS ....................................................................................................................................................................................21
OBJETIVOS ...................................................................................................................................................................................21
General ..................................................................................................................................................................................21
Específicos ............................................................................................................................................................................21
SITIO DE ESTUDIO ..........................................................................................................................................................................21
PARCELAS DE ESTUDIO ..................................................................................................................................................................22
CONTENIDO ..................................................................................................................................................................................22
LITERATURA CITADA ......................................................................................................................................................................23
CAPÍTULO II. AN EXPERIMENTAL ASSESSMENT ON THE IMPORTANCE OF EPIPHYTES FOR BIRDS
IN COFFEE PLANTATIONS OF CENTRAL VERACRUZ, MEXICO.............................................................31
SUMMARY .....................................................................................................................................................................................31
INTRODUCTION ..............................................................................................................................................................................32
MATHERIALS AND METHODS ...........................................................................................................................................................33
RESULTS ......................................................................................................................................................................................37
DISCUSSION ..................................................................................................................................................................................39
CONCLUSION ................................................................................................................................................................................42
ACKNOWLEDGEMENTS ...................................................................................................................................................................42
REFERENCES ................................................................................................................................................................................43
APPENDIX .....................................................................................................................................................................................54
CAPÍTULO III. AN EXPERIMENTAL APPROACH TO EVALUATING THE ROLE OF EPIPHYTES IN
HABITAT SELECTION OF BIRDS IN COFFEE PLANTATIONS..................................................................61
ABSTRACT ....................................................................................................................................................................................61
INTRODUCTION ..............................................................................................................................................................................62
METHODS .....................................................................................................................................................................................64
RESULTS ......................................................................................................................................................................................66
DISCUSSION ..................................................................................................................................................................................67
AKNOWLEDGMENTS .......................................................................................................................................................................69
LITERATURE CITED ........................................................................................................................................................................69
CAPÍTULO IV. AN EXPERIMENTAL ASSESSMENT ON THE CONTRIBUTION OF EPIPHYTES TO THE
OVERALL ABUNDANCE AND SPECIES DIVERSITY OF CANOPY INSECTS IN COFFEE
PLANTATIONS IN CENTRAL VERACRUZ, MEXICO...................................................................................78
ABSTRACT ....................................................................................................................................................................................78
INTRODUCTION ..............................................................................................................................................................................79
6
MATHERIALS AND METHODS ...........................................................................................................................................................80
RESULTS ......................................................................................................................................................................................83
DISCUSSION ..................................................................................................................................................................................84
ACKNOWLEDGEMENTS ...................................................................................................................................................................87
LITERATURE CITED ........................................................................................................................................................................87
CAPITULO V. CONCLUSIONES..................................................................................................................100
PRINCIPALES RESULTADOS DE LA INVESTIGACIÓN ..........................................................................................................................100
CONTRIBUCIONES DEL TRABAJO ...................................................................................................................................................102
RECOMENDACIONES DE MANEJO ..................................................................................................................................................103
DIRECTRICES FUTURAS ................................................................................................................................................................103
LITERATURA CITADA ....................................................................................................................................................................104
7
LISTA DE CUADROS
CAPÍTULO I
Cuadro 1. Uso de epífitas por aves por grupo de planta y tipo de recursos que utilizan ............................. 29
CAPÍTULO II
Table 1. Descriptive statistics of vegetation surveys done in four experimental plots (treatments) in a coffee
plantation in Coatepec, México .................…...…............…................….................…...............… 48
Table 2. Bird species richness observed and expected for two pairs of experimental plots in a coffee
plantation in Coatepec, Mexico. .................…….............…................….................…...............…. 49
CAPÍTULO III
Table 1. Estimates of monthly survival probabilities (S ± 1 SE) for Common Bush-Tanagers and Goldencrowned Warblers on a coffee plantation in Coatepec, Veracruz, Mexico, 30 May 2000 – 23 April
2002 ……..............…….............…................…..............….................………….....…...........…....… 73
Table 2. Models of monthly survival (S), recapture (p), and movement (ψ) probabilities for Common BushTanagers (N = 112) and Golden-crowned Warbler (N = 80) on a coffee plantation in Coatepec,
Veracruz, Mexico, 30 May 2000 – 23 April 2002 .............……..............………….....…...............…. 74
CAPÍTULO IV
Table 1. Number of insect morphospecies by order and number of families (in parenthesis) captured during
the canopy fogging of 12 Inga jinicuil trees in an experimental setting in a shade coffee plantation
where six trees (three per plot) were epiphyte removed while other six trees remain with epiphytes,
in Coatepec, Veracruz, Mexico .............……..............………….....…...............…………………….. 93
Table 2. Results from two way crossed ANOSIM test, based on Bray–Curtis dissimilarities in fourth-root
transformed insect abundances from four experimental plots in a coffee plantation, Central
Veracruz, Mexico ...........………………………............………….....…...............…………………….. 94
8
LISTA DE FIGURAS
CAPÍTULO II
Figure 1. Rarefaction curves for the number of bird species observed in experimental plots in a coffee
plantation in Coatepec, Mexico ..………………...........………….....…...............…………………….. 50
Figure 2. Mean abundance of birds observed in four experimental plots in a coffee plantation in Coatepec,
Mexico ……………………………..……………............………….....…...............……………………... 51
Figure 3. Ordination of two matched pairs of experimental plots, based on a multidimensional scaling
analysis used to compare the similarities of the studied plots during the breeding and non-breeding
season (2001-2002) in a coffee plantation in central Veracruz, Mexico ...........…………………….. 52
Figure 4. Correlation between the percentage use of epiphytes as a foraging substrate and the proportion of
individuals (in percentage) observed in the experimental plots with-epiphytes (E +) in a coffee
plantation in Central Veracruz, Mexico ..……..……………..……………..………………………….... 53
CAPÍTULO III
Figure 1. Based on the best-fit model (Table 1), estimated monthly transition probabilities (ψ ± 1 se) for
adult common bush-tanagers differed between experimental shade coffee plots with epiphytes (left)
and without epiphytes (right) ………………...……………..……………..……………..………………. 75
Figure 2. Based on the best-fit model (Table 2), estimated monthly transition probabilities (ψ ± 1 SE) for
Golden-crowned Warblers did not differ between experimental shade coffee plots with epiphytes
(left) and without epiphytes (right) …………...……………..……………..……………..……………… 76
CAPÍTULO IV
Figure 1. Trap setting for a knockdown insecticide fogging of an Inga jinicuil tree with epiphytes in a coffee
plantation, Coatepec, Veracruz, Mexico …..……...……………..……………..……………..………... 95
Figure 2. Mean species accumulation curves for insect species collected by knockdown fogging of three
trees per plot (two samples per tree) in an experimental setting in a coffee plantation in Central
Veracruz, Mexico …………………………...……………..……………..……………..………………… 96
Figure 3. Mean expected number of insect species by experimental plot in a coffee plantation in Central
Veracruz Mexico .…………………………...……………..……………..……………..………………… 97
Figure 4. Ordination of two matched pairs of experimental plots, based on a multidimensional scaling
analysis used to compare the similarities of the studied plots .…………………………...………….. 98
CAPÍTULO V
Figura1. Resumen gráfico de los principales resultados encontrados en esta tesis ..………......………… 106
9
RESUMEN
Las epífitas son un elemento común de bosques tropicales húmedos primarios y secundarios, y
agroecosistemas forestales, tales como plantaciones de café. Se ha aceptado que las epífitas incrementan
la diversidad estructural del dosel, y que proporcionan una gran variedad de recursos adicionales para la
fauna asociada al dosel de los bosques. En plantaciones de café del centro de Veracruz y otras regiones
de Latinoamérica, las epífitas son removidas de los árboles de sombra. Este tipo de manejo presenta una
oportunidad excelente para conocer cuál es el papel ecológico de las epífitas como promotoras de
diversidad, y cuál es el efecto de la presencia/ausencia de las epífitas en la fauna del dosel. En una
plantación de café de Coatepec, Veracruz, se caracterizó la flora epífita y se establecieron dos sitios con
dos parcelas experimentales cada uno. En una de las dos parcelas de cada sitio las epífitas fueron
removidas de todos los árboles del dosel. Se comparó la abundancia y diversidad de aves e insectos entre
parcelas con y sin epífitas. Además, utilizando modelos de captura-recaptura, investigamos cómo la
remoción experimental de epífitas afectó las probabilidades de sobrevivencia mensual y de movimiento de
dos especies de aves residentes Chlorospingus ophthalmicus y Basileuterus culicivorus. Se registraron 48
especies de epífitas verdaderas, 5 hemiepífitas, 3 accidentales, 1 parásito, 1 epífita facultativa. Las
especies de epífitas se distribuyeron en 14 familias, las mejor representadas fueron Bromeliaceae (20
especies), Orchidaceae (12 especies) y Polypodiaceae (8 especies). Cómo resultado de la remoción de
epífitas se encontró que la riqueza de aves no fue significativamente distinta en parcelas con y sin epífitas,
pero la abundancia individuos fue significativamente mayor en parcelas con epífitas, así mismo, la
estructura de la comunidad de aves difirió entre los dos tratamientos. Dieciocho especies de aves fueron
significativamente más abundantes en parcelas con epífitas y sólo tres especies lo fueron en parcelas sin
epífitas. Las especies más afectadas fueron aquellas que utilizan a las epífitas como sustrato de anidación.
En cuanto a la selección de hábitat por las aves, no se encontraron diferencias relacionadas con el tipo de
hábitat (con y sin epífitas) en la sobrevivencia mensual de Chlorospingus ophthalmicus y Basileuterus
culicivorus, no obstante, la probabilidad de movimiento de individuos de Chlorospingus ophthalmicus de
parcelas sin epífitas a parcelas con epífitas fue al menos cinco veces mayor que en el sentido inverso
(parcelas con epífitas a parcelas sin epífitas). Los patrones de dispersión encontrados sugieren que en
nuestro sitio de estudio C. ophthalmicus se encuentra seleccionando activamente sitios basándose en la
presencia de las epífitas. En cuanto a los insectos, se encontró que las parcelas con epífitas presentaron
un número significativamente mayor de especies e individuos; además, insectos mayores a 5mm de
longitud fueron significativamente más abundantes en las parcelas con epífitas. Con base en lo anterior,
10
propongo que las epífitas podrían proveer refugio a insectos en contra de grandes depredadores (eg.
aves), por lo que al no ser detectados por las aves estos pueden adquirir tallas mayores. El presente
estudio es la primera evaluación experimental sobre la importancia de las epífitas para las aves, además
confirma que las epífitas son un elemento importante para el mantenimiento de la diversidad y abundancia
de los insectos del dosel. Como práctica agronómica, la remoción de epífitas del dosel de los cafetales,
además de costosa, puede tener efectos adversos sobre la fauna asociada.
11
CAPÍTULO I
INTRODUCCIÓN GENERAL
12
CAPÍTULO I. INTRODUCCIÓN GENERAL
LA CRISIS GLOBAL DE LA PÉRDIDA DE BIODIVERSIDAD
Una de las mayores amenazas a la pérdida de biodiversidad es la deforestación y la pérdida de
hábitat debida en buena medida, a la expansión de la frontera agrícola, especialmente intensa en las
regiones tropicales (Dobson et al. 1997, Brooks et al. 2002, Donald 2004, Millennium Ecosystem
Assessment 2005). Las consecuencias de la pérdida de biodiversidad están asociadas directamente a la
disminución del bienestar y desarrollo de los humanos (Millennium Ecosystem Assessment 2005). Aunque
las predicciones sobre tasas de pérdida de biodiversidad debidas a la deforestación (Brooks y Balmford
1996, Brooks et al. 1999a, b y c, 2002) han sido hasta cierto punto controvertidas (Pimentel et al. 1992,
Budiansky 1994, Poudevigne y Baudry 2003) la crisis de pérdida de biodiversidad y sus consecuencias
sobre las sociedades es innegable (Millennium Ecosystem Assessment 2005).
Parte de la discusión con respecto a las estimaciones de las tendencias de pérdida de
biodiversidad está en que los estudios realizados no reconocen la habilidad que muchas especies
tropicales podrían tener para sobrevivir en agroecosistemas (Pimentel et al. 1992, Budiansky 1994,
Poudevigne y Baudry 2003). Durante el siglo pasado, buena parte de los esfuerzos de conservación de la
biodiversidad se concentraron en la creación de áreas protegidas, generalmente aisladas e intocables
(Schelhas y Greenberg 1996). Sin embargo, estas políticas no resultaron del todo exitosas debido a que la
gente habitante de las áreas protegidas no era incorporada a los procesos de conservación y tampoco se
planteaban alternativas viables de crecimiento y desarrollo que aseguraran la reducción efectiva de la
presión sobre los ecosistemas o áreas se intentaba proteger.
Varios estudios han demostrado que un número relativamente alto de individuos y especies
(animales y plantas) de bosque pueden encontrarse y sobrevivir en agroecosistemas (Daily et al. 2001,
Hughes et al. 2002, Petit y Petit 2003), por lo que actualmente se reconoce que las políticas de
conservación de la biodiversidad deben incluir el manejo sustentable de fragmentos de bosque; la
promoción de prácticas agrícolas ecológicamente menos dañinas (Schelhas y Greenberg 1996, Waltert et
al. 2005), así como la conexión entre remanentes de bosque y agroecosistemas arbolados a través de
corredores biológicos.
El valor de conservación que pueden tener algunos agroecosistemas ha sido evaluado a través de
la comparación de gradientes de intensificación en el manejo de los mismos, utilizando como indicadores la
diversidad de especies o el número de especies especialistas de bosque que habitan estas áreas de
13
manejo de los agroecosistemas (Philpott y Dietsch 2003). Un ejemplo de lo anterior son los distintos
estudios en el agroecosistema cafetalero que han demostrado que los cafetales florística y
estructuralmente más diversos conservan una mayor proporción de especies de bosque (Perfecto et al.
1996, Greenberg et al. 1997a y b, Gordon et al. 2007) y que las diferencias en el manejo de la sombra
afectan grandemente la riqueza de especies (Perfecto y Snelling 1995, Calvo y Blake 1998, Perfecto y
Vandermeer 2002).
CONSERVACIÓN DE LA BIODIVERSIDAD EN MÉXICO
En México, uno de los doce países con mayor biodiversidad del mundo, la deforestación y
fragmentación de los ecosistemas naturales ha sido particularmente alarmante. Se calcula que entre 1970
y 1990, la tasa anual de pérdida de bosques fue de 800 mil ha/año. Las cifras oficiales entre 2000 y 2005
indican que esta tasa fue de poco más de 300 mil ha/año (SEMARNAT 2005). Los costos de la pérdida de
biodiversidad en el país no han sido evaluados de manera formal, aunque podrían ser considerablemente
altos y con impactos negativos irreversibles (CONABIO 2006).
Como en otros países del mundo, la estrategia gubernamental de conservación de la biodiversidad
en México ha sido el establecimiento de áreas naturales protegidas (ANP), que en conjunto abarcan el
9.24% de la superficie del territorio terrestre nacional. Sin embargo, la mayor parte de la biodiversidad de
México se encuentra fuera de las ANP y sujeta al manejo humano (CONABIO 2006). Por lo anterior, queda
claro que para el país es necesario consolidar otras estrategias de conservación y uso sustentable de los
recursos naturales fuera de las áreas naturales protegidas.
CAFÉ EN MÉXICO
El café es una de los bienes (commodities) de comercio e intercambio más importantes del mundo,
siendo superado únicamente por el petróleo. Producido en más de 60 países, mundialmente da sustento a
más 20 millones de familias (Rice y Ward 1999) y ha generado ganancias anuales hasta por 70 mil
millones de dólares (Internacional Coffee Organization 2007).
Desde su introducción en México, a finales del siglo XVIII, el cultivo de café ha sido de gran
importancia para la economía del país. Hasta hace algunos años era el principal producto agrícola de
exportación y el valor de las exportaciones del grano eran únicamente superadas por las del petróleo
(Santoyo-Cortes et al. 1996). Actualmente, otros productos como el tomate, el pimiento, el pepino y el
aguacate se encuentran entre los principales productos de exportación (SAGARPA 2007). El café se cultiva
14
en más de 700 mil has en 12 entidades del país. Sin embargo, el 90.43% del área de cultivo se encuentra
en Chiapas, Oaxaca, Veracruz, Puebla y Guerrero (SAGARPA 2007). El 66% de los más de 400 mil
productores hablan al menos una lengua indígena (SAGARPA 2006). A nivel internacional, México se
encuentra entre los primeros diez países con mayor producción de café (Moguel y Toledo 1999, SAGARPA
2006).
Históricamente el café comenzó a cultivarse bajo la sombra del dosel de selvas y bosques
tropicales. Las plantas nativas del sotobosque eran sustituidas por los arbustos de café; el dosel del
bosque era sometido a un aclareo selectivo y moderado y los efectos de este tipo de manejo (sistema
rústico o rusticano) sobre el paisaje eran mínimos (Moguel y Toledo 1996, 1999).
A partir de la década de los 60 y 70 iniciativas gubernamentales de los países productores de café,
apoyadas por agencias internacionales como la USAID (United States Agency for Internacional
Development) promovieron paquetes tecnológicos que permitieran a los cafetaleros en primer lugar
prevenir la expansión de la roya del café (Hemilea vastarix), que había tenido impactos devastadores sobre
la producción cafetalera de países como India y Sri Lanka en el siglo XIX. Adicionalmente, se pretendía
aumentar la producción de café mediante el incremento de la densidad de arbustos por unidad de área, el
uso de nuevas variedades de café y, especialmente la reducción o remoción completa de los árboles de
sombra (Rice y Ward 1997, Moguel y Toledo 1999). En México, el Instituto Mexicano del Café
(INMECAFÉ), fundado en 1957 y liquidado en 1989 fungió un papel importante en este sentido (Potvin et
al. 2005). Desde su creación, esta institución se planteó como objetivos tanto el incremento del consumo
nacional de café mexicano, como el de los rendimientos, así como la reconversión productiva de los
predios ubicados en zonas desfavorables para el cultivo (SAGARPA 2006).
El INMECAFÉ tenía, además, la facultad de expedir permisos de exportación de café y realizaba el
control de precios internos, desempeñando un papel tanto de representante y mediador de los productores
en los mercados internacionales, cómo de asesor técnico-financiero de los mismos y comprador de la
producción.
Desde el punto de vista productivo, el aumento en la producción del café es deseable, si el precio
en el mercado del producto es lo suficientemente bueno como para contrarrestar los costos de los mayores
insumos y trabajos que implican la intensificación del cultivo. Sin embargo, los precios internacionales del
café han estado sujetos a las variaciones propias del mercado, con épocas de crisis, cuya más grave y
profunda se sitúa entre 1999 y 2004 (SAGARPA 2006). Esta crisis, originada en buena medida por una
sobreproducción mundial del café, ha tenido graves consecuencias sobre los productores que viendo
15
reducidos sus ingresos, han sido obligados abandonar sus fincas, dedicarse a otros cultivos,
ambientalmente menos amigables (como el cultivo de caña de azúcar), emigrar hacia Estados Unidos o
incorporarse a las filas del desempleo (Osorio 2002).
Afortunadamente, la remoción de la sombra de los cafetales en México no fue un proceso muy
extendido, debido en parte a la reticencia de los mismos productores a eliminar por completo la sombra de
sus plantaciones. Hoy en día el 99% de la superficie cultivada en el país se realiza bajo sombra
diversificada (SAGARPA 2006). Lo anterior es una de las principales fortalezas de la cafeticultura
mexicana, que a través de algunas organizaciones consolidadas ha podido posicionar al café mexicano en
el mercado de café de especialidad (orgánico, de comercio justo, de sombra), que esta sujeto a mejores
precios de mercado. Sin embargo, el acceso a este tipo de mercados no es una práctica generalizada entre
los productores de café, debido al alto grado de organización y control de los procesos que se requieren.
CAFÉ Y BIODIVERSIDAD
El valor que las plantaciones de café y otros sistemas agroforestales, como el cacao, tienen para la
conservación de la biodiversidad en áreas tropicales ha sido reconocido en varios estudios (Greenberg et
al. 2000, Perfecto et al. 1996 y referencias incluidas). No obstante, el papel que los cafetales juegan en el
mantenimiento y la conservación de la biodiversidad depende del manejo al que son sometidos (Greenberg
1997a).
La importancia de la diversidad estructural de la sombra de los cafetales en el mantenimiento de la
biodiversidad ha sido reconocida ampliamente, especialmente en estudios con aves (Aguilar-Ortiz 1982,
Wunderle y Waide 1993, Wunderle y Latta 1996, Greenberg et al. 1997a, Jones et al. 2000) y artrópodos
(Perfecto y Vandermeer 1994, Perfecto et al. 1996, Ricketts et al. 2001, Arellano y Halffter 2003, Mas y
Dietsch 2003). Otros grupos como mamíferos (Gallina et al. 1996, Gallina et al. en prensa; Sosa et al. en
prensa) y anfibios (Pineda y Halffter 2004) también han sido estudiados en este tipo de agroecosistemas.
Por otro lado, los estudios multitaxonómicos han sido relativamente escasos (Pineda et al. 2005, Gordon et
al. 2007).
Actualmente el cultivo del café de sombra implica tanto el manejo del sotobosque, como el del
dosel. El sotobosque de las plantaciones es limpiado periódicamente; las herbáceas y plantas invasoras
son eliminadas y los arbustos de café son podados y/o replantados. Por otro lado, el manejo del dosel se
enfoca a controlar la cobertura y sombreado bajo el cual crecen los arbustos de café. Dependiendo de la
intensidad de manejo, las podas suelen ser anuales o bianuales. En algunos cafetales, las epífitas y
16
muérdagos son removidos del dosel. En el centro de Veracruz, este proceso es conocido coloquialmente
como “destenche”, debido a que los campesinos y lugareños conocen a las epífitas con el nombre de
“tenchos”.
Aunque la remoción de epífitas es una práctica relativamente común en la zona cafetalera del
centro de Veracruz y otros sitios de Latino América, los efectos de este proceso sobre la fauna asociada no
han sido evaluados. La simplificación de la estructura del cafetal y particularmente la pérdida de la flora
epífita, podría afectar marcadamente la estructura y dinámica de las poblaciones de aves e insectos
asociados (Greenberg et al. 1997a).
EPÍFITAS, AVES E INSECTOS
Las epífitas son un componente importante de la biodiversidad en los trópicos (Flores-Palacios y
García Franco 2001, Krömer 2005). Han sido postuladas como un recurso potencialmente importante y
poco estudiado para las aves e insectos en los trópicos, debido a que incrementan la complejidad
estructural del dosel y proveen recursos adicionales a aquellos provistos por los árboles hospederos (aves:
Remsen 1985, Nadkarni y Matelson 1989, Sillett 1996, Sillett et al. 1997; insectos: Stork 1987, Kitching et
al. 1997, Ødegard 2000). Estas plantas pueden llegar a constituir hasta un 50% de la flora vascular en
algunos bosques tropicales húmedos (Gentry y Dodson 1987) y su biomasa puede igualar hasta el 50% de
la biomasa de hojas de árboles en algunos bosques montanos (Edwards y Grubb 1977, Nadkarni 1984).
Pocos estudios han reconocido la importancia de la flora epífita para las comunidades de aves en
los trópicos (Remsen 1985, Nadkarni y Matelson 1989, Sillett 1996). Nadkarni y Matelson (1989) realizaron
un estudio en 14 sitios de bosque tropical, mesófilo de montaña y pastizales en Costa Rica. En este trabajo
los autores estudiaron el uso de epífitas por las aves. Particularmente, observaron el tipo de epífitas que
las aves utilizaban, la frecuencia de uso, el comportamiento de forrajeo asociado al uso de estas plantas y
el grado de especialización en la utilización de grupos particulares de epífitas por algunas especies de
aves. Además, realizaron una revisión de 55 trabajos reuniendo información acerca del uso de epífitas por
aves. Los tipos de recursos que las aves obtienen de las epífitas, pueden ser néctar de las flores, frutos,
agua, insectos que habitan en las epífitas, material para nidos (semillas de bromelias) y sitios de anidación
(Cuadro 1). Sin embargo, el estudio fue realizado en un periodo corto de tiempo, por lo que se desconoce
la extensión y la variación estacional en el uso de epífitas dentro de una temporada o a lo largo del año
(Sillett 1996). Por otro lado, aunque se conoce la fenología de algunos árboles tropicales, se sabe poco
acerca de la fenología de las epífitas, las cuales podrían estar proveyendo recursos críticos a las aves,
17
cuando los árboles no presentan ni flores, ni frutos, ni otros recursos como sitios y materiales de anidación
(Dean et al. 1990, Sillett 1996). La utilización de recursos epifíticos por aves migratorias no ha sido
cuantificada (Nadkarni y Matelson 1989).
Por otro lado, aunque se ha reconocido que las epífitas podrían ser un factor importante para la
diversificación de insectos del dosel en bosques tropicales, pocos trabajos han abordado explícitamente el
tema (Stuntz 2001). La mayor parte de los estudios realizados se han enfocado a evaluar la riqueza de
insectos dentro de las epífitas mismas (Paoletti et al. 1991, Cotgreave et al. 1993, Richardson 1999,
Richardson et al. 2000, Stuntz 2001, Wittman 2000), pero muy pocos estudios han establecido la
contribución relativa de las epífitas a la diversidad de insectos del dosel con respecto a la copa de los
árboles. Por ejemplo, Stork (1987) encontró que la cantidad de lianas y epífitas presentes en los árboles
estudiados en Brunei, Borneo era más importante para explicar la similitud faunística en algunos taxa
particulares de insectos (e.g. Homoptera, Grilllidae, Anthicidae y Chrysomeliadae) en los árboles que la
relación taxonómica entre los árboles estudiados.
Stuntz (2001) estudió la contribución de las epífitas a la diversidad de insectos del dosel de un
árbol tropical Annona glabra L. (Annonaceae). En el estudio, la autora colectó los artrópodos de árboles de
A. glabra con distintas especies de epífitas y sin epífitas. Stuntz no encontró diferencias significativas, en la
abundancia y composición de la comunidad de artrópodos entre los tratamientos analizados. Sin embargo,
es posible que los resultados de este estudio no puedan ser extrapolados a otras áreas debido a que los
autores trabajaron con un árbol relativamente pequeño (< 6 m) y en un área inundada, donde la
abundancia de epífitas en los árboles de Annona no parecería significativa.
La mayor parte de los estudios han omitido señalar la presencia de epífitas en el dosel y por lo
tanto no es posible saber si la presencia de epífitas ha sido cuantificada o controlada, de manera que es
posible que al menos en algunos estudios la diversidad de insectos del dosel reportada para una especie
particular de árbol este parcialmente confundida con la presencia de epífitas en el árbol hospedero. No
existen estudios que a la fecha hayan evaluado la importancia de las epífitas para los insectos del dosel en
cafetales.
GRADO DE EPIFITISMO
Aunque generalmente se consideran epífitas únicamente a las plantas vasculares de vida libre
(epífitas verdaderas como las orquídeas y bromelias) (Benzig 1987), en este estudio se incluyeron también
a las plantas hemiepífitas, accidentales, facultativas y parásitas, por lo que se considera en un sentido
18
amplio el concepto de epífita (Kress 1986). Las hemiepífitas son aquellas que germinan en el dosel y
después establecen contacto con el suelo (hemiepífitas primarias como el Ficus matapalos) o que
germinan en el suelo y posteriormente trepan al dosel (hemiepífitas secundarias como especies de la
familia Araceae, que eventualmente pueden perder contacto con el suelo); las epífitas accidentales son
aquellas especies de plantas que no tienen modificaciones para vivir en el dosel, usualmente terrestres,
que germinan y se establecen como plántulas como epífitas, pero que no pueden llegar a desarrollarse en
el dosel (Coffea); Las epífitas facultativas son aquellas que pueden vivir y alcanzar la madurez ya sea
como terrestres o epífitas (Cactacea); Por último, las parásitas (muérdagos) que germinan sobre el árbol
que desarrollan un haustorio y dependen del hospedero para vivir (pueden retener la capacidad de
fotosintetizar, pero obtienen agua del hospedero). Así mismo, se define al grado de epifitismo como el
porcentaje de infestación de epífitas y muérdagos que presentan los árboles hospederos en sus ramas y
troncos.
CAFÉ, EPÍFITAS, AVES E INSECTOS
Un estudio realizado en plantaciones de café y remanentes de bosque en Venezuela (Jones et al.
2000) demostró que el nivel de epifitismo encontrado en las plantaciones se correlacionaba positivamente
con la diversidad de especies de aves de distintos gremios, especialmente insectívoros y nectarívoros. Sin
embargo, un factor importante en la diversidad y abundancia en las plantaciones es el grado de
conectividad con remanentes de bosques, lo cual oscurece la relación encontrada con el grado de
epifitismo.
La mayoría de los estudios realizados sobre aves en plantaciones de café se han enfocado
principalmente a la diversidad y abundancia de aves migratorias neotropicales, dejando a un lado las
especies residentes o estudiándolas durante la época de invernación, cuando se traslapan con las
migratorias (Richter 1998). En plantaciones de café con distinto grado de epifitismo, Richter (1998) realizó
un estudio sobre el éxito reproductivo de Chlorospingus ophthalmicus. La autora encontró que la mayoría
de los nidos exitosos ocurrieron en la plantación de café que presentaba el mayor grado de epifitismo y que
además las parejas de C. ophthalmicus parecían estar seleccionando sitios de anidación con árboles más
grandes y con un grado de epifitismo mayor al encontrado en sitios seleccionados al azar. Por otro lado, se
ha observado que la mayoría de las especies que construyen nidos abiertos en el dosel de plantaciones de
café de la región de Coatepec, Veracruz, anidan en el interior de grupos de epífitas (Cruz-Angón et al.
datos no publicados). Algunas aves utilizan semillas de bromelias, que presentan apéndices plumosos
19
especializados para la dispersión por viento, para forrar el interior de sus nidos. Este tipo de dispersión de
semillas ha sido documentada por algunos autores (Trejo 1975, Dean et al. 1990).
EFECTOS DE LA REMOCIÓN DE EPÍFITAS EN CAFETALES
La remoción de epífitas y muérdagos del dosel provoca una simplificación mayor en la estructura
vertical y diversidad de los cafetales, que, comparados con un bosque primario, son ya de por sí es un
ecosistema simplificado. La eliminación de la flora epífita de los cafetales, podría considerarse como un
tipo de fragmentación (vertical y horizontal) del ambiente en el continuo cafetal, y los efectos que este tipo
de perturbación del hábitat pueda tener sobre las aves e insectos no han sido estudiados.
Partiendo de la hipótesis de que la descendencia de las plantas podría ser afectada directamente
por cambios microclimáticos inducidos por la fragmentación y que esta, a su vez, podría afectar las
densidades en las poblaciones de animales y modificar las relaciones ecológicas planta-animal (v.gr.,
polinización, dispersión), Aizen y Feisinger (1994) encontraron que la fragmentación de los bosques secos
en la región del Chaco en Argentina, tenía efectos negativos en los niveles de polinización y producción de
semillas de algunas plantas de este tipo de hábitat. La perturbación "vertical y horizontal" de los cafetales
podría estar provocando efectos similares sobre las relaciones ecológicas entre animales y plantas, las
cuales, hasta el momento no han sido estudiadas.
La remoción de las epífitas supone una mayor apertura del dosel que podría incrementar los
niveles de depredación. Aunado a esto, la reducción de los sustratos de forrajeo, alimento, sitios y
materiales de anidación, como resultado de la remoción de epífitas, podría elevar la competencia intra e
interespecífica y, por lo tanto aumentar en número y/o intensidad las interacciones agonísticas entre los
individuos. Varios autores han demostrado que la adecuación de los individuos puede ser afectada por
factores ambientales, tales como la temperatura, la escasez de alimento o la depredación (Calder 1984,
Peters 1986, Nager y Zandt 1994). El cambio en biomasa (i.e. disminución de peso) de los individuos,
como resultado de un incremento del estrés ambiental, podría traducirse en una evaluación indirecta de la
adecuación de los individuos.
Por otro lado, algunos esquemas de certificación de café de sobra (Bird Friendly, Smithsonian
Migratory Bird Center) contemplan la no remoción de las epífitas de los árboles de sombra como un criterio
importante para el mantenimiento de las comunidades de aves de los cafetales. Como explico en el
siguiente capítulo, este criterio fue establecido con base en estudios observacionales, sin embargo, hasta
20
el presente trabajo no existían evaluaciones experimentales que permitieran corroborar lo anterior y dar un
mejor sustento a la exigencia de este criterio de certificación.
En función de los temas tratados anteriormente, el sistema estudiado en este trabajo abarca las
relaciones entre las epífitas como proveedoras de recursos adicionales a faunas del dosel (aves e insectos)
y su influencia en la organización de las comunidades y ensamblajes de aves e insectos en el cafetal.
HIPÓTESIS
Si las epífitas ofrecen recursos (flores y frutos, al igual que una variedad de nichos) que podrían
ser consumidos o utilizados por aves e insectos, se esperaría que la diversidad y abundancia de estos dos
grupos este correlacionada con la presencia de epífitas en el dosel del cafetal.
Si a nivel de la comunidad existen especies de aves e insectos relacionadas íntimamente con las
epífitas, la remoción de epífitas podría influir en la dinámica poblacional de las especies y en la estructura
de las comunidades de aves e insectos del cafetal. A nivel específico las especies de aves e insectos más
estrechamente relacionadas con las epífitas podrían ver reducida su adecuación al disminuir la calidad del
hábitat del cafetal.
OBJETIVOS
General
Evaluar la importancia de la flora epífita para la conservación de la biodiversidad de aves e
insectos en una plantación de café de la región de Coatepec, Veracruz, México.
Específicos
1. Determinar el grado de epifitismo y caracterizar la comunidad epífita del cafetal.
2. Determinar la manera en que las aves utilizan los recursos ofrecidos por epífitas (i.e. néctar floral, frutos
e insectos asociados) a lo largo del año.
4. Evaluar el efecto de la remoción de epífitas del dosel del cafetal, sobre las aves asociadas.
5. Evaluar el efecto de la remoción de epífitas del dosel del cafetal, sobre los insectos del dosel.
SITIO DE ESTUDIO
El trabajo se desarrolló en un cafetal de 200 ha, situado en un terreno plano (19° 29' N, 90° 42' W;
1200 msnm) de la congregación "La Orduña", municipio de Coatepec, Veracruz. El clima de la zona es
21
templado, con temperatura media anual entre 16 y 18° C; precipitación total anual entre 2000 y 2500 mm, y
más de 150 días al año con precipitación apreciable (Gómez y Soto 1990).
El cafetal es un policultivo comercial (sensu Moguel y Toledo 1999), tipo de manejo predominante
del centro de Veracruz, en el cual el bosque original ha sido removido en su totalidad, y en su lugar se han
introducido árboles de sombra como leguminosas fijadoras de nitrógeno (Inga spp.) y algunas otras
especies con valor comercial como cítricos (Citrus spp.) y plátanos (Musa spp.) (Moguel y Toledo 1996). En
el cafetal bajo estudio el género de árbol dominante es Inga. El manejo del cafetal incluye la aplicación de
herbicidas, alternado con el chapeo periódico de malezas y la aplicación anual de urea como fertilizante.
Hasta 1998, la sombra del dosel era regulada por podas bianuales y las epífitas sólo eran removidas de los
arbustos de café. A partir de abril de 1999 y hasta diciembre del 2000, en algunas porciones del cafetal, se
inició la remoción de epífitas de los árboles de sombra.
PARCELAS DE ESTUDIO
En 1999 se establecieron dos sitios experimentales: Norte y Sur, separados ca. 1 km. En cada
orientación se ubicaron dos parcelas contiguas de tres ha, aproximadamente, cada una. En cada sitio una
de las parcelas fue destenchada y la otra permaneció intacta. El proceso de remoción de las epífitas fue
realizado por el personal del cafetal, por lo que los criterios de poda y destenche son representativos del
manejo aplicado en la zona. Como consecuencia del destenche, la cobertura del dosel disminuye,
permitiendo una mayor entrada de luz hacia al sotobosque. Las epífitas removidas de los árboles, son
apiladas en el suelo en pequeños montones esparcidos en toda la parcela. Las epífitas tiradas aportan
materia orgánica al suelo del cafetal. En cada parcela se estableció una cuadrícula con cuadrantes de 25 x
25 m identificados con coordenadas alfanuméricas. Todos los experimentos y observaciones fueron
realizados en las parcelas antes mencionadas, de 1998 al 2003, con excepción de algunas de las
observaciones de forrajeo presentadas en el capítulo II, que fueron realizadas en el mismo cafetal de 1995
al 1998.
CONTENIDO
En el presente documento de tesis evalúo la influencia de la presencia de las epífitas sobre la
diversidad y abundancia de aves e insectos en un cafetal de sombra de la región de Coatepec, Veracruz.
En este capítulo he presentado una revisión sobre los estudios que se han hecho con referencia al valor de
conservación de los cafetales de sombra, las tendencias de tecnificación y simplificación, entre ellos la
remoción de epífitas del dosel y establezco las hipótesis sobre las que desarrollé este trabajo de tesis. En
22
el segundo capítulo evalúo los efectos de la remoción de las epífitas sobre la comunidad de aves en un
cafetal, asociando los resultados que encontré con la utilización que las aves hacen de las epífitas y los
“servicios” que las epífitas dan a este grupo. En el tercer capítulo exploro el papel que las epífitas pueden
tener como estructuras claves para la evaluación de la calidad del hábitat en dos especies de aves
Chlorospingus ophthalmicus y Basileuterus culicivorus, evaluando la sobrevivencia y la probabilidad de
emigración de individuos marcados de estas dos especies en función de la presencia o ausencia de
epífitas, como una manera de inferir patrones de selección de hábitat por parte de las aves. En el cuarto
capítulo valoro el papel que las epífitas pueden tener en los patrones de diversidad y abundancia de los
ensamblajes de insectos del dosel del cafetal. Finalmente, en el último capítulo (Discusión General) integro
los resultados de la tesis en el contexto del manejo de cafetales de sombra y en la importancia ecológica
de las epífitas como promotoras de diversidad. Los capítulos II al IV se presentan en ingles y en el formato
de las revistas en el que fueron aceptados o al que han sido enviados para su publicación como artículos
científicos. Los capítulos I y V se presentan en español. Por ser los capítulos introductorio y conclusivo
respectivamente, proporcionan al lector un marco de referencia básico sobre este trabajo de tesis y
abordan los principales resultados y conclusiones de la investigación. Con la lectura de los dos capítulos
antes mencionados, los lectores no familiarizados con el idioma Inglés podrán tener una idea básica de
este estudio, así como de sus principales conclusiones.
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28
Cuadro 1. Uso de epífitas por aves por grupo de planta y tipo de recursos que utilizan. Tipo
de recurso de epífita: In = Invertebrados; Fl = Flor; Fr = Fruto o semillas; Mn = Material para
nido, sitios de anidación; A= Agua. (Tomado de Nadkarni y Matelson 1989).
Número de especies de aves
Grupo de Planta
utilizando el recurso epífita
Tipo de recurso utilizado
58
Bromeliaceae*
In Fl Fr Mn A
53
Bryophyta*
In Mn A
50
Loranthaceae
Fl Fr
39
Marcgraviaceae
In Fl Fr
18
Ericaceae
Fl Fr Mn
12
Gesneriaceae
Fl Fr
9
Guttiferae
Fl Fr
8
Solanaceae
Fr
6
Aracea*
Fr Mn
6
Araliaceae*
Fr
5
Líquenes*
In Mn
5
Orchidaceae*
Fr Mn
5
Cactaceae*
Fr
3
Pteridophyta
Mn
1
Begoniaceae
Mn
1
Piperaceae*
Mn
1
Rubiaceae*
Fr
Se señalan con asterisco (*) los grupos de epífitas registradas en el área de estudio del
presente trabajo.
29
CAPÍTULO II
AN EXPERIMENTAL ASSESSMENT ON THE
IMPORTANCE OF EPIPHYTES FOR BIRDS IN COFFEE
PLANTATIONS OF CENTRAL VERACRUZ, MEXICO
ANDREA CRUZ-ANGÓN Y RUSSELL GREENBERG
(Cruz-Angón, A. and R. S. Greenberg. 2005. Are epiphytes important for birds in coffee
plantations? An experimental assessment. Journal of Applied Ecology 42:150-159)
30
CAPÍTULO II. AN EXPERIMENTAL ASSESSMENT ON THE IMPORTANCE OF EPIPHYTES FOR BIRDS IN COFFEE
PLANTATIONS OF CENTRAL VERACRUZ, MEXICO
SUMMARY
Shade coffee plantations with high levels of structural diversity are good refuges for forest-dependent birds.
In Latin America, some coffee managers remove epiphytes from shade trees. We examined the effects of
this practice on birds in a coffee plantation in Coatepec, Veracruz, Mexico.
After workers removed all epiphytes from shade trees in one of two plots in two pairs of matched plots in a
coffee plantation, we conducted daily bird censuses and foraging observations. We compared bird diversity
and abundance during the breeding season of 2001 (August – September) and the non-breeding season
(October 2001 – March 2002). We used information previously gathered on epiphyte use by birds as
foraging and nesting substrates to explain the presence of bird species in the plots with-epiphytes.
Non-epiphyte plots tended to be less diverse than with-epiphyte plots, but Rarefaction and ANOVA
analyses showed no significant differences in bird diversity between treatments in any of the seasons. Mean
bird abundance was significantly higher in plots with-epiphytes during both seasons, and a multidimensional
scaling analysis showed that bird community structure differed among plots with opposite treatment.
Several forest-dependent bird species (18) were significantly more abundant in the with-epiphyte plots. Few
species (3) were more common in the non-epiphyte plots and these species are associated with non-forest
habitats. The resident species that use epiphytes as a nesting substrate were significantly more abundant in
the with-epiphyte plots.
No significant correlation was found between the percentage use of epiphytes as a foraging substrate and
the proportion of individuals observed in the with-epiphyte versus non-epiphyte plots, due to the high degree
of variability of the species in the use of epiphytes.
When epiphytes are removed, canopy cover, foraging substrates, nest sites and nest materials are
eliminated and microclimatic conditions change. These effects could result in an increase in predation on
adult birds and nests, intra- and interspecific competition, and a decrease in individual survivorship.
Synthesis and Applications. This is the first experimental assessment on the importance of epiphytes for
birds. Shade coffee plantations with epiphytes enhance bird abundance and diversity. This study supports
the use of epiphyte management in shade coffee certification criteria, where the goal is to maintain avian
diversity.
Key words: birds, biodiversity, community structure, shade coffee management, vascular epiphytes.
31
INTRODUCTION
Shaded coffee plantations provide refuge for forest birds in otherwise deforested landscapes
(Aguilar-Ortiz 1982, Wunderle & Waide 1993, Warkentin, Greenberg & Salgado-Ortiz 1995, Wunderle &
Latta 1996, Perfecto et al. 1996, Greenberg et al. 1997). High levels of structural diversity in coffee
plantations canopy are critical for maintaining high bird diversity and abundance (Greenberg et al. 1997,
Greenberg, Bichier & Sterling 1997, Johnson 2000). However, emphasis has been placed on the presence
or absence of trees that form an arboreal canopy (Perfecto et al. 1996 and references therein).
Epiphytes frequently occur in some shaded agroecosystems, such as coffee (Williams-Linera, Sosa
& Platas 1995, Sosa & Platas 1997), and might play a critical role in supporting avian biodiversity
(Greenberg et al. 1997, Johnson 2000, Mas 1999, Mas & Dietsch 2003). Epiphytes increase the structural
complexity of forests by creating a variety of supplementary microhabitats and adding considerable biomass
and surface area to the tree crowns (Remsen 1985, Gentry & Dodson 1987, Sillett 1996, Nadkarni, Merwin
& Nieder 2001). Furthermore, epiphytes can provide birds with nest sites, nest materials, and food in the
form of flower nectar, fruits, water, small vertebrates and invertebrates that inhabit the epiphytes (Dean et
al. 1990, Richter 1998, A. Cruz-Angón, personal observations).
The few studies that have assessed the importance of epiphyte flora for bird communities in the
tropics have focused on the use of epiphytes for foraging birds during a portion of the annual cycle (Remsen
1985, Nadkarni & Matelson 1989, Sillett 1996, Sillett, James & Sillett 1997). This approach cannot detect all
the influences that the presence of epiphytes might have on bird distribution, particularly indirect effects
such as changes in microclimate. Only experimental removal can fully assess bird dependence on
epiphytes, and such experimental studies have not been conducted.
In this study, we take advantage of a common management practice in shaded plantations
throughout Latin America (Jones et al. 2000, Cruz-Angón, personal observation), in which epiphytes are
removed. There is no clear reason why coffee plantation managers remove epiphytes from shade trees in
their plantations. Some managers believe that all epiphytes are parasites that will harm or even kill trees.
Perhaps the most important reason is that farmers assume that an increase canopy openness and ambient
light levels will increase coffee yields. In fact, no increase in coffee yields has ever been demonstrated as a
direct result of epiphyte removal. In contrast, epiphyte elimination results in the structural simplification of
coffee plantations canopies, which could affect the structure and dynamics of avian communities in these
habitats (Greenberg et al. 1997).
In recent years, shade coffee certification programs have emerged to verify that coffee marketed as
32
“shade grown” is grown on farms with high structural diversity and adequate resources to support a diverse
associated fauna (Mas & Dietsch 2003). Correlative evidence supports the hypothesis that epiphytes might
be important for canopy faunas (Greenberg et al. 1997, Mas 1999, Johnson 2000, Stuntz 2001) and all the
shade coffee certification programs consider the management of epiphytes as an important factor for
evaluation (Mas 1999, Mas & Dietsch 2003). The need to conduct experimental studies that supports and
reinforces this criterion is clear. In this paper, we present the first experimental evaluation of the influence
that the presence of epiphytes has on bird communities.
MATHERIALS AND METHODS
Study site
We worked in one 35 yr old - 200 ha shaded coffee plantation (19° 28’ 03” N, 96° 55’ 58” W; 1224
m elevation) located in Coatepec, Veracruz, Mexico. We chose to work in a single large coffee plantation
rather than in several small coffee farms in order to control for inter-regional variation (e.g. weather,
altitude). Furthermore, this plantation has relatively little relief, so controlling for slope and topography was
not an issue.
The study farm is a commercial polyculture, the prevalent management type of coffee plantation in
central Veracruz (Moguel & Toledo 1999). Under this management technique, forest trees are completely
removed, and shade trees planted over coffee. In cental Veracruz, the original forest cover is tropical
montane cloud forest, which since the beginning of the century has been replaced by coffee plantations,
cattle pastures, sugarcane, cornfields, secondary vegetation and human settlements (Williams-Linera 2002,
Williams-Linera, Manson & Isunza. 2002). In our study site, although up to 35 species of trees can be found
in the canopy, shade is dominated by nitrogen-fixing, fast-growing legumes such as Inga spp. Farm
management also includes the use of herbicides (once a year) and mechanical elimination of weeds (by
machete). Shade trees are pruned every two years. Before 1999, epiphytes, which are abundant, were
removed only from coffee shrubs every two years, but during the dry seasons of 1999 and 2000, coffee
managers began to remove epiphytes from shade trees. We convinced the plantation managers to remove
the epiphytes in accordance with our experimental design.
Experimental design
In 1999 and 2000 we established two experimental sites located in opposite sides of the coffee
plantation (hereafter SITE: N = North and S = South), and separated by a distance of approximately 1 km.
Each site was divided into two 3 ha plots surrounded by a matrix of shaded coffee with epiphytes. Plantation
workers removed all the epiphytes from shade trees of one of the two plots at each site (hereafter
33
TREATMENT: E+ = With-epiphytes, E- = Without-epiphytes). Epiphyte removal involves climbing on
branches, which can be done safely only during the dry season (February to May), when epiphyte mats are
dried and are not holding great amounts of water. Workers tossed the removed epiphytes to the ground and
stacked them into small piles, where they decomposed. We established a grid of 25 x 25 m per quadrat in
the four plots, with alphanumeric coordinates for subsequent experiments and observations.
Vegetation surveys. - Canopy management is not uniform throughout the plantation, and variation among
plots was expected. To measure the variation in vegetation variables among plots we randomly choose five
quadrats per plot and measured shade cover with a spherical densiometer (Lemmon 1957). We counted the
number of tree species and tree individuals (> 10 cm DBH), and calculated tree height per species. We
measured the density of coffee shrubs as a percentage of ground cover in the quadrat and the mean coffee
shrub height.
The dominant tree species in the plantation is Inga jinicuil Schltdl. & Cham. Ex G. Don (Table 1)
and typifies the vascular epiphyte community in the plantation (A. Cruz-Angón, unpublished data). We
randomly selected and measured 15 I. jinicuil individuals (DBH > 10cm) in each plot and identified all
vascular epiphytes present in each tree. Observations were conducted from the ground and with binoculars
(Shaw y Bergstron 1997). With the exception of the southern plot without-epiphytes (SE-), which had no
epiphytes before we started the observations, we were able to establish the epiphyte richness on the other
three plots.
Vegetation measurements by sites and treatments are summarized in Table 1. Shade cover was
the only significantly different variable between plots (F (1, 16) = 24.98, P ≤ 0.001). As a result of the epiphyte
removal the plots without-epiphytes (NE- and SE-) had significantly less shade cover than their respective
control plots (NE+ and SE+; Tukey HSD, P < 0.001). We found 40 species of vascular epiphytes of the 57
total canopy dwelling species found on the farm. Bird pollinated bromeliads are the most dominant epiphyte
group (A. Cruz-Angón unpublished data). Mean epiphyte richness per tree among plots did not differ (F (2, 42)
= 0.88, P = 0.42).
Bird diversity and abundance. – Two observers conducted daily bird surveys in each plot, from 5 May
2001 to 23 March 2002. To ensure that observers had comparable abilities to detect birds, we considered
the first three months of the survey to be a training period and removed the resulting data from further
analyses. The results presented in this paper cover the observations taken from 1 August 2001 to 23 March
2002. This time span covers the last part of the breeding season (seven observation days per plot) and
most of the non-breeding season (16 observation days per plot). We alternated survey days between sites
34
and plots, covering one plot each day. Each day one observer zigzagged forward through the entire plot at
a constant rate for 3.5 hrs (07:00 – 10:30). All birds seen or heard at a distance within 25 m at each side of
the observer were recorded. In order to minimize double-counting individuals we did not record birds that
were behind the observer or beyond 25 m from the observer. Species were classified according to their
migratory status in the following categories: 1) migrants: species that nest in the Neartic region and winter in
the Neotropics, 2) resident breeders: species that breed in the coffee plantation (A. Cruz-Angón,
unpublished data), 3) resident non-breeders: Veracruz resident species that are only seen in coffee
plantations during the non-breeding season, and 4) residents: species seen all year in the area, but not
observed breeding in coffee plantations. Common and Latin names of the bird species observed follows
AOU (1993), and are presented in the Appendix.
Epiphyte use by birds. - Based on our study, we classified birds by their use of epiphytes as 1) foraging
substrate and 2) nesting sites, and materials. To describe the foraging behavior of birds, we used 2629
foraging observations gathered in the same plantation prior to the experiment, from 1995 to 1998 (R.
Greenberg, unpublished data). Additionally, we conducted 130 days of foraging observations (N = 2403) on
the experimental plots from 5 May 2001 to 3 March 2002. We took only one foraging observation per
individual to maximize the independence of the samples. We collected data on bird species, age and sex
(when possible), height of the bird in the tree when foraging, maneuver type, foraging substrate, tree
species and type of food obtained (nectar, arthropods, fruit) (methods based on Remsen & Robinson 1990,
modified by Greenberg et al. 1999). When an individual bird obtained a food item from an epiphyte, we
identified the family and species whenever possible.
To determine breeding status of resident birds and to assess the use of epiphyte by birds as nests
or for nesting materials, we observed nesting behaviors during the summers of 1995 through 1999 in this
coffee plantation (A. Cruz-Angón, unpublished data). We present the percentage use of epiphytes as a
nesting substrate, and the total number of nests found for species we were able to find and describe nests.
Data Analysis
We conducted separate analyses for each season studied, because bird diversity and abundance is
much higher during the non-breeding season when neotropical migrants are present.
Bird diversity and abundance.- To assess the reliability of our surveys recording bird diversity we carried out
a Rarefaction analysis (Hurlbert 1971, James & Ratburn 1981) using EcoSim v. 7 (Gottelli & Entsminger
2001). We set a maximum number of individuals for the breeding season to 200 and for the wintering
season to 900. To examine the effect of epiphyte removal on bird abundance and species richness, we
35
conducted ANOVA tests for a split-plot design where observation day was considered a random block that
contained the site split into smaller experimental plots (TREATMENT). This allowed us to maximize power
of test for the factor (TREATMENT) in which we were more interested (Sahai & Ageel 2000). We tested the
data for normality and homoscedasticity and transformed data using square root transformations (Zar 1999,
Quinn & Keogh 2002).
To quantify the similarity of community composition among plots we used the Bray-Curtis
coefficient. This index is calculated as CN =
2 Nj
, where Na = total number of individuals in site A, Nb
Na + Nb
= total number of individual in site B, and Nj = the sum of the lower of the two abundances recorded for
species found in both sites. The index ranges from 1, when communities are identical, to 0, when they are
entirely dissimilar (Magurran 1988). We then used a multidimensional scaling algorithm (NMDS, Gauch,
Whittaker & Singer 1981, Gauch 1982, StatSoft, Inc. 2000) to examine for clustering by community
composition. We plotted the values obtained through this procedure in a scatter plot where the proximity of
the sites is proportional to the degree of similarity. This allowed us to detect meaningful underlying
dimensions and explain the observed similarities among the investigated plots. The degree of
correspondence between the distances among points implied by NMDS plot and the matrix input by the
user is measured (inversely) by a stress function. Finally, we carried out a Mantel’s test (Mantel, 1967) to
calculate the probability of acquiring a given level of clustering by chance (Quinn & Keogh 2002).
We conducted a comparison of proportions using a Chi-square tests to determine if the number of
individuals of a given species were significantly more abundant in any of the treatments (with or without
epiphytes). The null hypothesis was that individuals were evenly distributed in both treatments. We
performed tests for only those species whose frequencies fulfilled test assumptions (Zar 1999). We then
assigned species to one of three categories based on whether they were significantly more abundant in
either of the treatments: 1) species more abundant on E- plots, 2) species evenly distributed among
treatments (E- and E+), and 3) species significantly more abundant on E+. Significance levels of the Chisquare tests were corrected with the Bonferroni method to counteract for the number of simultaneous tests.
Epiphyte use by birds.- For those bird species where we had at least 20 foraging observations (N = 33),
we calculated the percentage of foraging incidents that occurred on epiphytes. We correlated this
percentage with the percentage of individuals of each of those species found in the E+ plots. With nesting
observation data, we used a Kruskall-Wallis test (Zar 1999) to determine the species that use epiphytes as
nest sites where significantly more abundant in the E+ plots, than those that do not use epiphytes for
36
nesting.
RESULTS
Bird diversity and abundance
We recorded 91 species; 46 of these are neotropical migrants and 45 are residents. Among the
residents, 29 are confirmed breeders in the study site and 11 are year-round residents for which we had no
information on breeding status. The remaining five species do not spend the breeding season in the area
(Appendix).
Total species richness was similar among plots and ranged from 57 to 65. No one plot contained all
the 91 species. During the breeding season, the NE+ plot had the lowest diversity (26 species) and the SE+
the highest (40 species). During the non-breeding season, the with-epiphyte plots (NE+ and SE+) had more
species than the non-epiphyte plots (NE- and SE-). Estimated species richness, as determined by
rarefaction analysis, confirmed this pattern for both seasons (Table 2). We present the rarefaction curves at
three moments of the sampling: 50, 100 and 200 individuals for the breeding season and 300, 600 and 900
individuals for the non-breeding season (Fig. 1). The confidence intervals at 95% overlapped widely among
plots in both seasons, with the exception of the NE+ plot, that remained with the lowest species diversity
during the breeding season.
The ANOVA showed no significant differences in the mean number of species observed within
treatment in any of the seasons (breeding season: F (1, 6) = 2.13, P = 0.19, non-breeding season: F (1, 15) =
3.64, P = 0.07). The site was not a significant factor during the breeding season (F (1, 6) = 2.00, P = 0.20) but
there were significantly more bird species in the plots on the northern site of the plantation in the nonbreeding season (F (1, 15) = 6.67, P = 0.02). Nonetheless, E- plots tended to have fewer species than their E+
counterparts. There was no significant site by treatment effects for either season (all P > 0.05). The mean
number of individuals observed was significantly higher in E+ plots than in the E- plots in both seasons
(breeding season: F (1, 6) = 43.61, P < 0.001; non-breeding season: F (1, 15) = 8.52, P < 0.05). Neither plot
site nor site by treatment effects were significant factors for either season (P >0.05) (Fig. 2).
Even though rarefaction analysis and ANOVA test for species richness showed somewhat
inconsistent results between treatments, the multidimensional scaling (NMDS) procedure showed a more
coherent pattern. Two dimensions were obtained (stress = 0.006); Dimension 1 grouped plots according to
the season (breeding vs. non-breeding). This pattern is explained by the presence of neotropical migrants
that modify the structure of tropical communities during the non-breeding season; Dimension 2 grouped
37
plots according to the treatment (with or without-epiphytes). This pattern was more evident in the breeding
season, whereas during the non-breeding season community structure was very similar among plots;
however, equal treatments remained closer to each other (Fig. 3). Mantel’s test showed a significant
correlation (r = 0.39, P < 0.01) between the similarity matrix and the one produced by NMDS procedure.
These results indicate that the grouping observed in the Shepard diagram was not acquired by chance.
Several individual bird species were significantly more common in the E+ plots, while only a few
species were more common in the E- plots. Seven migrant species (Olive- sided Flycatcher, Solitary Vireo,
Chestnut-sided and Tennessee Warblers, Summer Tanager, Baltimore Oriole and Orchard Oriole) were
significantly more abundant in the E+ plots (χ2, df = 1, P < 0.05). Among the residents, 11 species were
significantly more abundant in the E+ plots (χ2, df = 1, P < 0.05) — two hummingbirds (White-bellied
Emerald and Wedge-tailed Hummingbird), the four breeding tanagers (Common Bush-tanager, Redthroated Ant-tanager, White-winged Tanager, Yellow-throated Euphonia), and three under story breeding
birds (Spot-breasted Wren, Golden-crowned Warbler and Rusty Sparrow). Two resident non-breeding
flycatchers, the Greater Pewee and Tufted Flycatcher were also more abundant in the E+ plots. Only two
migrants (both granivores) — Painted and Indigo Bunting — and one breeding resident, the Golden-fronted
Woodpecker, were more abundant in the E- plots (χ 2, df = 1, P < 0.05). When the Bonferroni correction was
conducted 11 of the 18 species that were more abundant in the E+ remained significant (P < 0.005), and
only two of the three species that where more abundant in the E- remained significant (Appendix).
Epiphyte use by birds
Foraging.- We recorded 33 species (15 migrants and 18 residents) using epiphytes as a foraging
substrate (observed foraging incidents; n ≥ 20). The percentage use ranged from 3% to 74% among
species. For example, the Yellow-throated Euphonia and the Band-backed Wren foraged on epiphytes 74%
of the observed incidents. The Wedge-tailed Sabrewing, the Gray Catbird and the Black–and-white Warbler
were observed using epiphytes in about 50% of foraging incidents. The Common Bush-Tanager, the most
common resident in the plantation and the most common species in the epiphyte plots, foraged in epiphytes
around 30% of the time. Foraging guilds using epiphytes included omnivores, insectivores and nectarivores.
We did not observe any granivore species foraging in epiphytes. The correlation between the proportion of
individuals found in the with-epiphyte plots and the percentage use of epiphytes as forgaging substrate was
not significant (Fig. 4, r = 0.19, P = 0.07).
Nesting.- Overall, species that use epiphytes as a nesting site or for material were significantly
more abundant in the E+, than those species that do not nest in epiphytes (H 1, 26 = 3.42, P = 0.03). The
38
type of use varied considerably between species. Among the 29 confirmed breeders in the coffee
plantation, seven species use epiphytes as nesting sites —Band-backed Wren, Blue Bunting, Common
Bush-tanager, Squirrel Cuckoo, Tropical Parula, White-winged Tanager and Yellow-throated Euphonia.
Usually birds build their nest inside epiphyte clumps, most commonly bromeliads. The percentage use
varied from 38 to 100 %. Three of the four breeding tanagers were particularly dependent upon epiphyte
clumps as nesting sites using them for 84 to 100% of their nests (see Appendix). Other species such as the
Wedge-tailed Hummingbird and, the Azure-crowned Hummingbird use epiphytic lichens and mosses to
“decorate” their nest. The Band-backed Wren used Tillandsia spp. with plumose seeds as a lining material
for their nests.
DISCUSSION
Our data suggest that the presence of epiphytes may have both direct and indirect effects, not only
on the canopy avifauna, but on the understory birds as well. The four experimental plots differed only in the
treatment applied as shown by the vegetation surveys, where canopy cover, determined by epiphyte
density, was the only variable were plots differed significantly. Therefore, we assume that the differences
between treatment and control plots are attributable to the presence or absence of epiphytes. We did not
find significant differences between treatments in the total species richness recorded and the mean number
of species observed. The use of complementary biodiversity measurements, such as similarity coefficients
that take in to account both, species richness and abundance may reflect the ecological patterns in a more
integral manner. Thus, we were able to detect differences on bird abundance in a number of forestdependent taxa, which in turn had a strong influence on overall community structure.
Focusing only on patterns of species presence and absence may be too limited. Changes in
individual numbers, as a result of human intervention or a natural disturbance, may be the first indication of
the species local extinction (Ferraz et al. 2003). Furthermore, the mere presence of a species does not
imply that a viable population is supported (Martin 1992, Donovan et al. 1995, Robinson et al. 1995, Mas &
Dietsch 2003). Even abundance measures do not address this concern and further research is required to
explore the demographic consequences of epiphyte removal.
As we would expect, species more strongly associated with epiphytes were less abundant in the
non-epiphyte plots, which in turn, may influence the structure of the entire avian assemblage. For example,
the Common-Bush Tanager was significantly more abundant in the with-epiphyte plots, a pattern evident in
all the tanager species recorded in our study site. This species uses epiphytes as forage (30% of the time)
39
and as a nesting substrate (80 % of the time). The use of epiphyte resources by the Common Bush-tanager
has been previously described (Powell 1979, Isler & Isler 1987, Nadkarni & Matelson 1989, Sillett 1996,
Richter 1998); however, this study confirms the direct dependence and the importance of epiphyte
resources for tanager species such as the Common Bush-Tanager. What makes the dependence of BushTanagers on epiphytes particularly interesting is that they are highly intraspecifically gregarious and play an
important role in mixed species flock structure and function (Valburg 1992; A. Cruz-Angón, personal
observation.) and their decline due to the absence of epiphytes might affect the behavior of many other
species.
Epiphytes may play a key role in reducing phenological gaps in resources. In floristically
impoverished plantations such as commercial polycultures in the central region of Veracruz, tree species of
the genus Inga can comprise up to 70% of the shade trees. In this type of plantations, epiphytes may
become a critically important food resource when other tree hosts are not flowering or fruiting (WilliamsLinera 1997). In the plantation, epiphytes like Anthurium scandens and Rhipsalis baccifera produce large
quantities of fruits that are regularly consumed by resident tanagers and Euphonias (i.e, Common Bushtanager, White-winged Tanager and Yellow-throated Euphonia, Snow 1981, A. Cruz-Angón, personal
observation). Fruit production of these epiphytes coincides with the birds breeding season (April –
September). Breeding is a highly energy demanding activity, and adult birds search for high-protein food
items such as arthropods only to feed their offspring. In this sense, fruit consumption is an easy, fast and
secure way to obtain energy and water during this particular and highly vulnerable period of the year
(Greenberg 1981, Denslow, Moermond & Levey 1986). In addition, the sequential flowering of several birdpollinated Tillandsia occurring in the with-epiphyte plots of our study site, guaranteed year-round nectar
supply for nectarivores, such as Wedge-tailed Hummingbird (García-Franco, Martínez-Burgoa & Pérez
2001, A. Cruz-Angón, personal observation).
Interestingly, we did not find a significant correlation between the percentage use of epiphytes as a
foraging substrate and the proportion of individuals per species in the with-epiphyte plots. This result
suggests that the use of epiphytes as forage substrate may not be the most important factor that could
explain the presence of birds in the with-epiphyte plots. Nonetheless, the removal of epiphytes modifies the
canopy’s vertical structure, by decreasing foliage surface and biomass (Hoefestede, Wolf & Benzig 1993).
These changes in foliage structure may affect birds by influencing encounter rates with prey, prey
accessibility, and energetic costs of attacking and capturing prey (Gradwhol & Greenberg 1980, Robinson &
Holmes 1982, Schmidt 1998, Whelan 2001). Furthermore, the loss of epiphytes might disrupt the life cycle
40
of arthropods that are encountered by bird species outside of epiphytes at particular stages of their
development (Kitching et al. 1997).
The significant relationship found between the species that use epiphytes as a nesting site and their
greater abundance in the with-epiphyte plots confirms the close dependence of resident species upon
epiphyte resources. The use of epiphytes as a nesting site may give additional concealment against
potential predators.
On the other hand, some species that were more abundant in the E+ plots, did not display any type
of direct use of epiphytes. This is particularly true for certain migrant species such as the Olive-sided
Flycatcher, the Solitary Vireo, the Summer Tanager or the Tennessee Warbler which did not focus their
foraging efforts on epiphytes, but were more abundant in the E+ plots. Some species may have preferred
E+ plots because they use epiphytes as a simple cue to assess appropriate (forest) habitat (Lack, 1933).
In addition, some understory resident breeders, which neither forage nor nest in epiphytes, such as
the Golden-crowned Warbler, Spot-breasted Wren and Rusty Sparrow, were more abundant in the E+ plots.
Epiphytes may play an indirect role in maintaining the abundance of many species. Such indirect effects
would be undetectable from observational studies on the use of epiphytes by birds. Influence on
microclimate is one such effect. Lorr (2001) working on our experimental plots, found that as a
consequence of epiphyte removal, canopy cover and soil moisture are reduced, while stem-flow and
through-fall increase. Thus, more water is getting to the ground in less time, but it evaporates faster.
During the breeding season, this sudden increase of water running through the ground could flood nests
and affect ground nesters like the Golden-crowned Warbler and the Rusty Sparrow. Moreover, the
unexpected changes in the microclimate could influence the abundance and diversity of arthropods, not
only in the canopy but in the understory arthropod fauna, as well, and important prey species may become
less abundant and less accessible (Stuntz 2001, Cruz-Angón et al. unpublished data). In addition, greater
canopy openness due to epiphyte removal may increase birds’ detection by potential predators. Several
authors have demonstrated that individual fitness can be affected by environmental factors such as extreme
temperature, food shortage and predation (Calder 1984, Peters 1986, Carrascal et al. 1998, Nager & Zandt
1994).
As a consequence of canopy openness and a greater light incidence in the without-epiphyte plots,
weeds might overgrow. This could explain the significantly higher abundance in the non-epiphyte plots of
the weed-dependent granivores like Indigo Bunting and Painted Bunting. However, weeds are an
ephemeral resource in coffee plantation, since they are regularly removed from the understory. The only
41
resident species that was significantly more abundant in the non-epiphyte plot was the Golden-fronted
Woodpecker, which paradoxically used epiphytes as a foraging substrate about 50% of the time. The
higher abundance of this species could be explain because ones the epiphytes have been removed the
Woodpecker can drill on tree bark more easily and also, for a primary cavity nester might be advantageous
to have a epiphyte-free tree that allows a better tree selection.
CONCLUSION
This study has provided the first experimental evidence on the importance of epiphytes for
supporting bird abundance and diversity in coffee plantations, specially, to forest dependent species.
Although focused on coffee plantations, these findings might enlighten the ecological importance of
epiphytes for birds in other ecosystems, such as tropical montane cloud forests. This study also validates
the use of the epiphyte management as an important criterion to certify shade-grown coffee. Epiphytes are
an important resource for birds, not only because they may provide critical resources such as food or nest
materials but also because epiphytes mediate in microclimate regulation, offer refuge and cover to the
inhabitant fauna. Subsequent follow up on long- term effects of epiphyte removal are needed. Although,
coffee plantations where epiphyte removal is practiced give a unique research opportunity that may include
direct and indirect effects of this process, it should not be promoted and given the various ways this
technique affects birds it should rather be discouraged.
ACKNOWLEDGEMENTS
We thank A. Martínez-Fernández, P. Bichier-Garrido and B. Lorr for assistance with fieldwork. The
Martínez family and plantation manager R. Monge provided generous access to their coffee plantation. V.J.
Sosa-Fernández, T.S. Sillett and A. Flores-Palacios provided advice with statistical analysis, and comments
on the manuscript. J.G. García-Franco, V. Rico-Gray, E.I. Paul, S. Philpot, A. Vovides, J.A. GonzálezAstorga, P. Bichier-Garrido and M. Coro-Arizmendi improved the manuscript with their comments and
corrections. Funding to ACA was provided by CONACYT (scholarship 128767), the Smithsonian Institution
Visiting Award 2002-2003 and the Departamento de Ecología Vegetal of the Instituto de Ecología and
grants from the National Geographic Society and Scholarly Studies Fund of the Smithsonian Institution to
RSG. This study constitutes partial fulfillment of A. Cruz-Angón Ph.D. in Ecology and Natural Resources
Management at the Instituto de Ecología, A.C.
42
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Table 1. Descriptive statistics of vegetation surveys done in four experimental plots (treatments) in a coffee plantation in Coatepec, México. Data are
Mean values with Standard Error in parenthesis, based on estimates made at five 625 m2 quadrats per plot. Epiphyte richness surveys were based
on 15 Inga jinicuil trees per plot, before workers removed all epiphytes from shade trees in one of two plots at each site. Treatment: With-epiphytes
(E+), Without-epiphytes (E-). Significant differences are shown with superscript letter (P < 0.0001). Not available information (NA).
Site
Tree
Canopy cover (%)
Coffee
Inga jinicuil
Epiphyte
richness
Tree/ha
Treatment
species
height (m)
height (m)
density (%)
dominance (%)
North
E-
21.9 (2.6)a
230.4 (62.7)
3.8 (0.2)
7.7 (0.7)
2.1 (0.2)
76.0 (4.0)
56.1 (12.0)
15.9 (0.6)
E+
38.7 (5.7)b
262.4 (36.7)
4.2 (0.8)
8.1 (0.8)
1.9 (0.2)
64.0 (4.0)
48.3 (13.9)
15.9 (0.7)
E-
29.0 (2.3)a,c
172.8 (15.5)
3.2 (0.6)
8.7 (1.0)
2.8 (0.3)
60.0 (5.5)
77.7 (6.9)
E+
65.3 (1.2)d
195.2 (13.8)
1.8 (0.2)
9.0 (1.0)
2.5 (0.1)
79.0 (4.6)
58.7 (1.7)
South
48
NA
14.8 (0.8)
Table 2. Bird species richness observed and expected for two pairs of experimental plots in a coffee plantation in Coatepec, Mexico. Expected
species richness is based on Rarefaction analysis of 200 individuals for the breeding season and 900 individuals for the non-breeding season. Total
numbers of individuals observed are shown in parenthesis after the observed species richness per season. Treatment: With-epiphytes (E+), Withoutepiphytes (E-).
Species richness per season
Site
Total
Breeding
Treatment
Non-breeding
richness
Observed
Estimated (SD)
Observed
Estimated (SD)
E+
26 (280)
24.5 (1.0)
54 (1227)
51.7 (1.3)
60
E-
35 (249)
33.0 (1.2)
50 (1042)
48.6 (1.1)
62
E+
40 (378)
33.9 (1.9)
54 (1238)
51.9 (1.3)
65
E-
33 (201)
32.9 (0.04)
48 (977)
47.3 (0.8)
57
North
South
49
Figure 1. Rarefaction curves for the number of bird species observed in experimental plots in a coffee
plantation in Coatepec, México. Species richness is shown at three moments of the individual re-sampling:
a) 50, 100 and 200 individuals for the breeding season; and b) 300, 600 and 900 individuals for the nonbreeding season. Data points are mean expected diversity, bars are 95% Confidence Intervals.
Experimental Plots: North with-epiphytes (♦), North without-epiphytes (■), South with-epiphytes (▲), South
without-epiphytes (X).
40
a) Breeding season
35
30
25
20
Number of species
15
10
50
100
200
55
b) Non-breeding season
50
45
40
35
30
300
600
Number of individuals
50
900
Figure 2. Mean abundance of birds observed in four experimental plots in a coffee plantation in Coatepec,
Mexico, during a) Breeding season, and b) Non-breeding season. Sites: North and South; Treatments: With
Epiphytes (E+), Without epiphytes (E-). Data points represent mean abundance, and whiskers are 95%
Confidence Intervals.
a) Breeding season
70
60
50
Number of individuals
40
30
20
E+
E-
E+
ESOUTH
NORTH
b) Non-breeding season
90
80
70
60
50
E+
E-
E+
NORTH
ESOUTH
51
Figure 3. Ordination of two matched pairs of experimental plots, based on a multidimensional scaling analysis used to compare the similarities of the
studied plots during the breeding and non-breeding season (2001-2002) in a coffee plantation in central Veracruz, Mexico. Plots: North withepiphytes (NE+), North without-epiphytes (NE-), South with-epiphytes (SE+), South without-epiphytes (SE-). Stress = 0.006.
1.0
Non-breeding season
Breeding season
SE-
0.6
Dimension 2
NENE-
0.2
SENE+
SE+
-0.2
NE+
-0.6
-1.0
-1.2
SE+
-0.8
-0.4
0.0
Dimension 1
52
0.4
0.8
1.2
Figure 4. Correlation between the percentage use of epiphytes as a foraging substrate and the proportion of individuals (in percentage) observed in
the experimental plots with-epiphytes (E+) in a coffee plantation in Central Veracruz, México. Resident breeders (■), residents with unknown
breeding status (◊), Residents non-breeders (●), and neotropical migrants (▲). r = 0.19, P = 0.07.
120
+
Individuals in E plots (%)
100
80
60
40
20
0
-20
-20
0
20
40
60
80
Epiphyte use as foraging subtrate (%)
53
100
120
APPENDIX
Bird abundance and epiphyte use by bird species recorded in the experimental plots in a coffee plantation in Coatepec, Mexico. Birds are classified
by migratory status: Migrant (M), Resident breeder (RB), Resident non-breeder (RNB), Year round resident with no information on breeding status
(R); for resident breeders the percentage use of epiphytes as nesting substrate is presented, with the total number of nests found in parenthesis.
Guild: Omnivore (O), Insectivore (I), Nectarivore (N), Granivore (G); Epiphyte Use.-Numbers show the percentage of total foraging observations
where birds used epiphytes as a foraging substrate, total number of foraging observations in parenthesis. Bird abundance is shown as the total
number of individuals in plots with epiphytes (E+) or in plots from which epiphytes were experimentally removed (E-). For Bird Abundance Category,
1 = species more abundant on E- plots, 2 = evenly distributed among treatments, and 3 = species significantly more abundant on E+, NT = Not
tested. (χ 2, test, 1 df, *P ≤ 0.05, ** P ≤ 0.005, *** P < 0.0005).
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
Number of Individuals
use (n)
E+
E-
Bird abundance
Category
COLUMBIDAE
Leptotila verreauxi White-tipped Dove
RB
G
0 (1)
1
1
NT
M
I
0 (8)
6
4
2
RB, 50 (4)
O
9 (11)
1
3
RB
O
0
4
4
NT
RB
N
52 (89)
61
12
3***
R
N
17 (6)
10
0
3**
Amazilia cyanocephala Azure-crowned Hummingbird
RB
N
18 (50)
3
0
NT
Amazilia yucatanensis Buff-bellied Hummingbird
RB
N
13 (70)
23
37
NT
M
N
8 (25)
4
9
2
CUCULIDAE
Coccyzus americanus Yellow-billed Cuckoo
Piaya cayana Squirrel Cuckoo
STRIGIDAE
Glaucidium brasilianum Ferruginous Pygmy-Owl
TROCHILIDAE
Campylopterus curvipennis Wedge-tailed Sabrewing
Amazilia candida White-bellied Emerald
Archilochus colubris
Ruby-throated Hummingbird
54
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
Number of Individuals
use (n)
E+
E-
Bird abundance
Category
TROGONIDAE
Trogon violaceus Violaceous Trogon
R
O
26 (35)
6
2
NT
RB
O
0 (4)
7
10
2
RB, 0 (6)
O
44 (75)
43
69
1*
Picoides scalaris Ladder-backed Woodpecker
R
I
0 (1)
4
2
NT
Piculus rubiginosus Golden-olive Woodpecker
RB
O
0 (6)
7
3
2
R
I
0 (1)
3
2
NT
Myiopagis viridicata Greenish Elaenia
RB 0 (1)
I
0 (3)
2
0
NT
Tolmomyias sulphurescens Yellow-olive Flycatcher
RB, 0 (3)
I
0 (13)
13
13
2
RNB
I
0 (11)
14
4
3*
M
I
0 (4)
12
1
3**
RNB
I
4 (27)
15
6
3*
Contopus virens Eastern Wood-Pewee
M
I
0 (1)
1
1
NT
Empidonax flaviventris Yellow-bellied Flycatcher
M
I
0 (5)
7
5
2
Empidonax hammondii Hammond´s Flycatcher
M
I
6 (116)
41
36
2
Empidonax occidentalis Cordilleran Flycatcher
RB
I
5 (21)
10
7
2
RB, 0 (6)
I
0
33
38
2
Myiarchus crinitus Great Crested Flycatcher
M
I
0 (15)
10
5
2
Myiarchus tyrannulus Brown-crested Flycatcher
M
I
0
2
2
NT
RB, 0 (3)
I
67 (3)
2
0
NT
MOMOTIDAE
Momotus momota Blue-crowned Motmot
PICIDAE
Melanerpes aurifrons Golden-fronted Woodpecker
Dryocopus lineatus Lineated Woodpecker
TYRANNIDAE
Mitrephanes phaeocercus Tufted Flycatcher
Contopus cooperi Olive-sided Flycatcher
Contopus pertinax Greater Pewee
Myiarchus tuberculifer Dusky-capped Flycatcher
Myiozetetes similis Social Flycatcher
55
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
Number of Individuals
use (n)
E+
E-
Bird abundance
Category
Pachyramphus aglaiae Rose-throated Becard
R
O
50 (2)
3
0
NT
Pachyramphus major Gray-collared Becard
R
O
0 (10)
1
0
NT
RB, 0 (1)
I
0 (1)
11
12
2
Sayornis saya Say´s Phoebe
M
I
0
0
1
NT
Tyarnnus couchii Couch´s Kingbird
R
I
0
0
1
NT
Vireo griseus White-eyed Vireo
M
O
21 (53)
18
24
2
Vireo solitarius Solitary Vireo
M
O
18 (120)
90
60
3*
Vireo gilvus Warbling Vireo
M
O
20 (5)
0
1
NT
Vireo leucophrys Brown-capped Vireo
R
O
26 (35)
6
2
NT
Vireo philadelphicus Philadelphia Vireo
M
O
40 (40)
2
1
NT
Vireo flavoviridis Yellow-green Vireo
M
O
25 (8)
18
13
2
Campylorhynchus zonatus Band-backed Wren
RB, 0 (4)
O
74 (31)
6
6
2
Thryothorus maculipectus Spot-breasted Wren
RB, 0 (2)
I
9 (23)
92
55
3**
M
I
0
0
1
NT
M
I
0 (3)
101
120
M
I
0 (5)
0
1
NT
RB
O
11 (9)
22
44
2
RNB
O
0 (1)
0
2
NT
Tityra semifasciata Masked Tityra
VIREONIDAE
TROGLODYTIDAE
REGULIDAE
Regulus calendula Ruby-crowned Kinglet
SYLVIIDAE
Polioptila caerulea Blue-Gray Gnatcatcher
2
TURDIDAE
Hylocichla mustelina Wood Thrush
Turdus grayi Clay-colored Robin
Turdus assimilis White-throated Robin
56
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
Number of Individuals
use (n)
E+
E-
Bird abundance
Category
MIMIDAE
Dumetella carolinensis Gray Catbird
M
O
56 (18)
18
35
2
Vermivora pinus Blue-winged Warbler
M
I
11 (37)
6
0
NT
Vermivora peregrina Tennessee Warbler
M
O
6 (17)
11
0
3*
Vermivora celata Orange-crowned Warbler
M
O
17 (46)
27
28
2
Vermivora ruficapilla Nashville Warbler
M
O
5 (209)
112
103
2
Parula americna Northern Parula
M
I
8 (8)
0
3
NT
RB, 100 (4)
I
5 (65)
9
5
2
Dendroica magnolia Magnolia Warbler
M
I
3 (74)
49
50
2
Dendroica virens Black-throated Green Warbler
M
I
9 (419)
353
327
2
Dendroica caerulea Cerulean warbler
M
i
0
0
1
NT
Dendroica pensylvanica Chestnut-sided Warbler
M
I
0 (8)
9
1
3*
Dendroica fusca Blackburnian Warbler
M
I
0 (6)
1
0
NT
Mniotilta varia Black-and-white Warbler
M
I
55 (128)
108
108
Setophaga ruticilla American Redstart
M
I
13 (8)
6
0
NT
Protonotaria citrea Prothonotary Warbler
M
I
0
1
0
NT
Helmitheros vermivorus Worm-eating Warbler
M
I
0 (2)
1
0
NT
Seiurus aurocapilla Ovenbird
M
I
0 (18)
39
41
NT
Seiurus noveboracensis Northern Waterthrush
M
I
0
0
1
NT
Seiurus motacilla Louisiana Waterthrush
M
I
0
2
0
NT
Oporornis tolmiei MacGillivray´s Warbler
M
I
0 (5)
13
8
2
Geothlypis nelsoni Hooded Yellowthroat
R
I
0 (1)
0
1
2
PARULIDAE
Parula pitiayumi Tropical Parula
57
2
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
Number of Individuals
use (n)
E+
E-
Bird abundance
Category
Wilsonia citrina Hooded Warbler
M
I
0
0
3
NT
Wilsonia pusilla Wilson´s Warbler
M
I
5 (402)
18
24
2
Wilsonia canadensis Canada Warbler
M
I
13 (8)
19
23
2
RNB
I
0 (1)
0
1
NT
RB, 0 (10)
I
1 (235)
199
159
3*
RB
I
8 (37)
28
30
2
RNB
I
0 (2)
1
0
NT
M
O
0 (13)
79
65
2
Habia fuscicauda Red-throated Ant-tanager
R
O
0 (11)
49
3
3***
Piranga rubra Summer Tanager
M
O
5 (19)
11
0
3***
RB, 100(6)
O
7 (41)
32
13
3**
RB, 84(168)
O
38 (589)
563
257
3***
R
G
0 (2)
0
3
NT
Buarremon brunneinucha Chestnut-capped Brush-Finch
RB, 0(2)
I
0 (8)
35
26
2
Arremonops virenticeps Olive Sparrow
RB, 0(2)
I
0 (2)
4
6
2
RB
I
0 (2)
10
2
3*
RB, 100(3)
I
0 (29)
46
46
2
Passerina caerulea Blue Grosbeak
M
O
0 (3)
0
1
NT
Passerina cyanea Indigo Bunting
M
G
0 (42)
0
11
1**
Passerina ciris Painted Bunting
M
G
0 (2)
0
16
1***
Myioborus miniatus Slate-throated Redstart
Basileuterus culicivorus Golden-crowned Warbler
Basileuterus rufifrons Rufous-capped Warbler
Basileuterus belli Golden-browed Warbler
Icteria virens Yellow-breasted Chat
THRAUPIDAE
Piranga leucoptera White-winged Tanager
Chlorospingus ophthalmicus Common Bush-Tanager
EMBERIZIDAE
Tiaris olivacea Yellow-faced Grassquit
Aimophila rufescens Rusty Sparrow
CARDINALIDAE
Cyanocompsa parellina Blue Bunting
58
Migratory
FAMILY/Latin name Common name
Guild
Status
Epiphyte
use (n)
Number of Individuals
E+
E-
Bird abundance
Category
ICTERIDAE
Icterus galbula Baltimore Oriole
M
O
11 (44)
22
7
3**
Icterus spurius Orchard Oriole
M
O
0 (4)
28
4
3***
RB, 94 (32)
F
74 (102)
91
13
3***
R
O
100 (5)
5
0
NT
FRINGILLIDAE
Euphonia hirundinacea Yellow-throated Euphonia
Euphonia elegantissima Elegant Euphonia
59
CAPITULO III
AN EXPERIMENTAL APPROACH TO EVALUATING THE
ROLE OF EPIPHYTES IN HABITAT SELECTION OF
BIRDS IN COFFEE PLANTATIONS
Andrea Cruz-Angón, T. Scott Sillett y Russell Greenberg
En prensa: Ecology, 2008
60
CAPÍTULO III. AN EXPERIMENTAL APPROACH TO EVALUATING THE ROLE OF EPIPHYTES IN HABITAT SELECTION OF
BIRDS IN COFFEE PLANTATIONS
ABSTRACT
Unique components of tropical habitats, such as abundant vascular epiphytes, influence the distribution of
species and can contribute to the high diversity of many animal groups in the tropics. However, the role of
such features in habitat selection and demography of individual species has not been established.
Understanding the mechanisms of habitat selection requires both experimental manipulation of habitat
structure and detailed estimation of the behavioral and demographic response of animals, e.g., changes in
movement patterns and survival probabilities. Such studies have not been conducted in natural tropical
forest, perhaps because of high habitat heterogeneity, high species diversity, and low abundances of
potential target species. Agroforestry systems support a less diverse flora, with greater spatial homogeneity,
which, in turn, harbors lower overall species diversity with greater numerical dominance of common
species, than natural forests. Furthermore, agroforestry systems are already extensively managed and lend
themselves easily to larger scale habitat manipulations than protected natural forest. Thus, agroforestry
systems provide a good model environment for beginning to understand processes underlying habitat
selection in tropical forest animals. Here, we use multistate, capture – recapture models to investigate how
the experimental removal of epiphytes affected monthly movement and survival probabilities of two resident
bird species (Common Bush-Tanager Chlorospingus ophthalmicus and Golden-crowned Warbler
Basileuterus culicivorus) in a Mexican shade coffee plantation. We established two paired plots of epiphyte
removal and control. We found that bush-tanagers were at least 5 times more likely to emigrate from plots
where epiphytes were removed compared to control plots. Habitat-specific movement patterns were not
detected in the warbler. However, unlike the warbler, bush-tanagers depend upon epiphytes for nest sites
and (seasonally) for foraging. These dispersal patterns imply that active habitat selection based on the
presence or absence of epiphytes occurs in C. ophthalmicus on our study area. Survival rates did not vary
with habitat in either species. Interestingly, in both species, survival was higher in the non-breeding season,
when birds were in mixed-species flocks. Movement by bush-tanagers into areas with epiphytes occurred
mostly during the breeding season, when mortality-driven opportunity was greatest.
Key words: coffee plantations, epiphytes, Common Bush-Tanager, Chlorospingus ophthalmicus, Goldencrowned Warbler, Basileuterus culicivorus, habitat manipulation, multistate capture-recapture models,
tropical ecosystems
61
INTRODUCTION
A strong gradient of increasing richness of bird species can be found between temperate and tropical
forests (Terborgh 1980). What ultimate and proximate factors contribute to the development of latitudinal
gradients in diversity remains a classic question of ecology – a question that has no single answer. A
number of authors have argued that bird species are “added” to Neotropical over equivalent temperate
systems because of the presence of stable habitat features or resources, such as bamboo (Parker 1982,
Kratter 1997), aerial leaf litter (Gradwohl and Greenberg 1982, Remsen and Parker 1984, Rosenberg
1997), and abundant epiphytic growth (Remsen 1985, Nadkarni and Matelson 1989, Sillett 1994, Sillett et
al. 1997), not present in more depauperate, temperate zone habitats.
Patterns in community attributes, such as species richness, are based in the distribution of species
across habitats that result, in part, from decisions of individual animals (Morris 2003). Habitat selection
therefore integrates the behavior of individuals with ecological and evolutionary processes. Decisions about
where to settle determine the distribution of a population across space (Jones 2001), and thus set the
selective environment shaping adaptations. The term “habitat selection” is often used interchangeably with
“habitat use”, a static description of a species’ distribution. However, the power of the concept of habitat
selection lies in an understanding of the mechanisms by which individuals chose habitat and the
consequences of that decision. Over the past 20 years, the traditional approach of correlating the
abundance of individuals of a given species with specific habitat features or overall habitat gestalt has given
way to studies that investigate the dynamic response of individuals (Martin 1985, Morse 1985, Wiens 1986,
Jones 2001).
Experimental manipulations are the best approach for revealing the mechanisms of habitat selection.
Laboratory experiments (Partridge 1974, Greenberg 1992) are most powerful for determining intrinsic
preferences. Field experiments, although logistically difficult, are superior for examining habitat selection as
it actually occurs under natural conditions, using more realistic spatial scales, and incorporating social
interactions. The response of individuals to manipulations can be estimated by examining the patterns of
immigration and emigration to and from the effected habitat patch. Furthermore, demographic parameters,
such as fecundity and survival probability provide information about the consequences of habitat selection
(Loery et al. 1997). Although experimental manipulations in the field are now frequently used to assess the
influence of one particular habitat feature, like snags, understory cover, and leaf litter, on temperate bird
assemblages (e. g., Scott 1979, Wiens 1986, Lohr et al. 2002), such studies have not been attempted in
natural tropical forest. The paucity of field manipulations in tropical forest systems can be attributed to four
62
factors: 1) local heterogeneity of forest composition (Condit et al. 2002) and structure, making the
establishment of replicate plots difficult; 2) high tree species diversity; 3) low abundance of individual
species (e.g., Loiselle 1988); and 4) overall structural complexity of the habitat.
Tropical agroforestry systems, such as those involved with the cultivation of coffee (Coffea arabica),
can provide a simplified, model forest environment that allows habitat manipulations while circumventing the
aforementioned complications. Even relatively diverse shaded coffee plantations have a far more
depauperate tree flora, usually dominated by a few species, and possess a relatively simple and spatially
homogeneous vegetative structure, with only two major layers of vegetation, compared to intact forest.
Replicate control and experimental plots similar in initial habitat structure can therefore be readily
established. Coffee agroecosystems can also exhibit ecological attributes that are qualitatively similar to
those of natural forests. For example, coffee plantations in the highlands of eastern Mexico provide
microclimates and pollinator assemblages, and enable reproductive success for vascular epiphytes that are
comparable to those in intact forest (Solis-Montero et al. 2005).
In 1999, we initiated an experimental manipulation of avian habitat structure via epiphyte removal on a
Mexican coffee plantation (see Methods). The effect of epiphytes on birds can be direct or indirect. Direct
effects include the use of epiphytes for nesting and foraging sites. Indirect effects include the influence on
overall insect abundance and microclimate. As part of the epiphyte removal study, Cruz-Angón and
Greenberg (unpubl.) determined through canopy-fogging that arthropods are both more diverse and
numerous in trees with epiphytes compared to similar trees with epiphytes removed. Moreover, areas with
epiphytes experienced greater canopy cover and hence a more buffered microclimate due to the shade
provided by epiphytes. Cruz-Angón and Greenberg (2005) found that 18 forest bird species were
significantly more abundant in sites with epiphytes, whereas only three open-habitat species were
significantly more abundant in the sites where epiphytes were experimentally removed from shade trees.
Here, we test if the above patterns in avian diversity were a result of active habitat selection in
individual birds. We focus our analysis on the two most abundant resident species, the Common BushTanager (Chlorospingus ophthalmicus) and the Golden-crowned Warbler (Basileuterus culicivorus).
Together these species comprised 35% of the resident birds surveyed on the plot (unpubl. data) and are the
only two species with sufficient sample size to undertake the modeling approach described in this paper.
Both species were more numerous in plots with epiphytes (Cruz-Angón and Greenberg 2005). However,
bush-tanagers were 118% more abundant on plots with epiphytes relative to removal plots (mean per
survey = 12.2 ± 0.5 vs. 5.6 ± 0.5), whereas only 20% more warblers were found on epiphyte-containing
63
plots (4.2 ± 0.4 vs. 3.5 ± 0.4). Bush-tanagers commonly used epiphytes for nesting and foraging. In
contrast, the warbler nested on the ground and rarely foraged in epiphytes (Cruz-Angón and Greenberg
2005), so that any benefits of epiphytes to this species were probably indirect (such as humidity of the
ground layer). We use systematic recapture and resighting of color-banded individuals and multistate, markrecapture models (Hestbeck 1991, Brownie et al. 1993, Nichols and Kendall 1995) to assess the role of
habitat selection (movement) and its consequences (mortality) in these two species. We predicted that
epiphyte removal would result in higher movement and lower survival probabilities in the bush-tanager
compared to the warbler.
METHODS
Experimental Design
The study site was a 35 yr old, 200 ha shaded coffee plantation located in “La Orduña” (19° 28’ 03” N,
96° 55' 58” W; 1220 m elevation), in Coatepec, near Xalapa, Veracruz, Mexico. Epiphyte removal from
shade trees is part of normal management practices of coffee plantations in the Xalapa region. By
convincing farm managers to remove epiphytes from two plots, we were able to document the ecological
effects of this procedure (see Cruz-Angón and Greenberg 2005). In 1999, we established two experimental
sites located in the north and south sides of the coffee plantation, respectively, and separated by a distance
of 1 km. Each site was divided into two adjacent 3 ha plots surrounded by a matrix of shaded coffee with
epiphytes. Plantation workers removed the epiphytes from all shade trees between 1999 – early 2000 in
one of the two plots at each site (hereafter TREATMENT: E+ = control, with epiphytes, E- = epiphytes
experimentally removed); otherwise epiphytes were not manipulated in the rest of the farm. The four plots
were delineated with flagging tape into a 25 x 25 m grid to facilitate mapping and resighting banded birds.
Based on vegetation surveys (Cruz-Angón and Greenberg 2005), canopy cover was the only habitat
structure variable, in addition to the presence or absence of epiphytes themselves, that significantly differed
between experimental and control plots; the floristic composition of trees did not differ, with Inga jinicuil
comprising 48-77% of total trees. Canopy cover was significantly higher in control plots, mostly due to the
shading of the epiphytes themselves. Because bird abundance did not differ between sites (Cruz-Angón
and Greenberg 2005), we pooled data for the north and south sites before modeling the effect of epiphytes
on bird movement and survival.
Focal Species
Common Bush-Tanagers are 15 – 20g passerines that occur from central Mexico to northern Argentina
64
and Bolivia in mid-elevation (1000-2500m) primary and secondary forests (Isler and Isler 1987, Howell and
Webb 1995). In coffee plantations of central Veracruz, bush-tanagers are most common in older and less
managed coffee farms (pers. obs.). This species is considered a generalist, but several authors associate
them with abundant epiphytes (Isler and Isler 1987, Howell and Webb 1995, Richter 1998). In our study site,
30% of their foraging efforts are on epiphytic substrates and 80% of their nests are built inside clumps of
vascular epiphytes (Cruz-Angón and Greenberg 2005). During the September – February non-breeding
(dry) season, bush-tanagers move in conspecific and mixed-species flocks, but during the March – August
breeding (wet) season, pairs separate from flocks to defend territories of about 0.5 – 1 ha.
Golden-crowned Warblers are 9 – 12g passerines that occur from the lowlands to 2100 m and are
common in dense understory habitats in submontane humid forests, forest edges, second growth, and
plantations from northeastern Mexico to northern Argentina (Curson et al. 1994). We did not observe any
nesting association with epiphytes for this ground and understory-foraging species in central Veracruz
(Cruz-Angón and Greenberg 2005). Golden-crowned Warblers occur in small conspecific groups and join
mixed species flocks during the September – February nonbreeding season. Pairs defend 0.5 – 1 ha
territories in the March – August breeding season.
Data Collection
Birds were captured with mist nets and each individual was marked with a unique combination of
colored plastic leg bands. We set up 14, 12 m permanent mist net locations per plot and conducted nine
mist-netting sessions per plot from 30 May 2000 – 15 March 2002, totaling 3276 mist net hours. Mist nets
were open from 0700 – 1330 hr. Birds captured were aged by plumage characters, eye color, and skull
ossification following Pyle et al. (1987) and Howell and Webb (1995). Reproductive state was determined by
the condition of a brood patch or cloacal protuberance. However, both species are monomorphic, making
sex determination at capture only possible for breeding adults.
We used resighting surveys and mist-net recaptures to generate data on individual survival and
movement. Resighting surveys entailed intensive searching for color-banded individuals from 0700 – 1030
hr, and were conducted from 31 May 2000 – 23 April 2002, totaling 560 observation hours (140 hours per
plot). We alternated survey days between plots, covering one plot day per survey period. Plots were
surveyed in May, October, and December 2000, and at least once per month from May 2001 – April 2002.
When a marked individual was resighted, we noted its color band combination and its location based on the
nearest plot grid intersection. All mist-netting and resighting surveys were restricted to the four study plots;
no individuals caught and banded in one side of the coffee plantation were seen or caught in the opposite
65
side of the study area. In order to obtain robust parameter estimation, observations were pooled into 15
monthly encounter occasions: May, October, and December 2000, and May 2001 – April 2002. A bird
detected in more than one habitat in a given month was assigned to the habitat that had the most
encounters within that month. If a tie existed, we assigned the bird to the habitat that minimized information
loss on movements (Béchet et al. 2003).
Data Analysis
We estimated monthly survival, movement, and recapture probabilities with open-population, multistate
capture-recapture models implemented in program MARK (version 4.1; White and Burnham 1999). Our
candidate model set contained four models (see Tables 1, 2) that were chosen prior to data analysis based
on our understanding of Common Bush-Tanager and Golden-crowned Warbler biology and on the sample
size limitations of our dataset. In all models, survival (S) and movement (ψ) were parameterized as
functions of age class (adult, juvenile) and season (breeding, non-breeding). Both S and ψ for individuals
captured as juveniles were modeled as adults in March following their hatch year (i.e. at the start of their
first breeding season). We investigated if epiphyte removal affected survival or movement by modeling S
and ψ as functions of habitat (E+, E-). To account for heterogeneity of capture and to provide unbiased
estimates of resident survival, all models also included a transient parameterization of S for adults in the
non-breeding season and for juveniles prior to their first breeding season (Pradel et al. 1997, Hines et al.
2003). Recapture probability (p) was always parameterized as fully time-dependent, but independent of age
class or habitat. We tested the same candidate model set for both species. Models were fit using a sine link
function and ranked by second-order Akaike’s information criterion (AICc) scores; relative likelihood of each
model was estimated with AICc Weights (wi; Burnham and Anderson 2002). Results are given as a
parameter estimate ± 1 SE.
RESULTS
Patterns of monthly survival and recapture probabilities were similar between species. In both the
bush-tanager and warbler, S differed by age and season (Table 1), but was not strongly affected by the
presence or absence of epiphytes (Tables 2). Adults had higher monthly survival probabilities than
juveniles, and mortality of both age classes was concentrated during the breeding season (Table 2).
Monthly recapture probabilities for the bush-tanager ranged from 0.09 ± 0.06 to 0.81 ± 0.08, and from 0.09
± 0.04 to 0.48 ± 0.09 for the warbler.
Based on wi, habitat-specific movement (Table 2: models 1, 3) in the Common Bush-Tanager was 9
66
times more likely, given our data, than habitat-independent movement (Table 2, models 2, 4). During the
breeding season, adults were at least three times more likely to move from E- habitat to E+ habitat than in
the opposite direction (Fig. 1). Adult movement probabilities during the non-breeding season were lower
than during the breeding season, but the probability of moving from E- habitat to E+ habitat was still higher
than the probability of moving in the opposite direction (Fig. 1). High variability made interpretation of
juvenile movement inconclusive. Juvenile movement probabilities were not appreciably different between
habitats, but tended to be higher during the March – August breeding season (ψE- to E+ = 0.20 ± 0.14; ψE+ to
E-
= 0.35 ± 0.20) than during the non-breeding season (ψE- to E+ = 0.11 ± 0.07; ψE+ to E- = 0.07 ± 0.06).
Monthly movement probabilities of the Golden-crowned Warbler did not differ between habitats: based
on wi, habitat-independent movement (Table 2: models 1, 3) was 24 times more likely than habitat-specific
movement (Table 2, models 2, 4). Like the bush-tanager, adult warblers tended to move between habitats
more during the breeding season than during the non-breeding season (Fig. 2). Juvenile warblers were
never observed moving between habitats during the breeding season (ψMarch – August = 0) and seldom moved
during the non-breeding season (ψSeptember – February = 0.03 ± 0.02).
DISCUSSION
Epiphytes as a Cue for Habitat Selection
Multistate, mark-recapture models in conjunction with a field manipulation allowed us to infer, for the
first time, habitat selection in a tropical bird species based on a single habitat feature. Our results provide
strong evidence that Common Bush-Tanagers actively select habitat on the basis of the presence or
absence of epiphytes. As predicted, bush-tanagers selectively moved from coffee plots where epiphytes
were removed from shade trees to plots with intact epiphyte cover. In contrast, Golden-crowned Warblers
showed no difference in the probability of movement towards or away from plots with epiphytes. In
Coatepec, Common Bush-Tanagers nest and forage in epiphytes, whereas Golden-crowned Warblers do
not regularly use epiphytic substrates. Our habitat selection results are therefore consistent with the
importance of epiphytes in the foraging and breeding requirements of the two species. Higher bird
occupation and use of the epiphyte plots may be based on an additional effect of epiphyte presence:
Canopy fogging experiments (Cruz-Angón and Greenberg, unpubl.) showed that arthropods were twice as
abundant in tree canopies with epiphytes than in those with epiphytes removed.
Fitness Consequences of Habitat Selection
Contrary to our prediction, monthly survival probabilities of both species, at least in the short-term,
67
were unrelated to the presence or absence of epiphytes, despite the fact that bush-tanagers selected
habitat with intact epiphyte cover. One explanation for this pattern would be an ideal free distribution
(Fretwell and Lucas 1970) for Common Bush-Tanagers. Epiphytes could be a cue for preferred habitat, but
under the conditions of our experiment, density-dependent factors might limit the benefits of occupying such
habitat. Alternatively, annual fecundity of bush-tanagers, not quantified in this study, rather than survival,
could be the key vital rate associated with epiphytes. A complete understanding of the consequences of
habitat selection by Common Bush-Tanagers requires further study and additional years of mark-recapture
data.
Seasonal Patterns of Movement, Survivorship, and Habitat Selection
Movement and survival probabilities of both species differed between the breeding and non-breeding
seasons. Movements between E+ and E- habitats by Common Bush-Tanagers occurred primarily in the
breeding season, when individuals were territorial. Adult and hatch-year mortality for both species was also
concentrated during the breeding season. To our knowledge, these are the first estimates of seasonal
survival probabilities for a tropical resident bird species. Higher breeding season mortality might be the
result of higher levels of starvation and predation during that season (Martin 1987). Adult Common BushTanagers and Golden-crowned Warblers do not join mixed-species flocks while breeding, which can be an
important anti-predation strategy of tropical birds (Powell 1985). The benefits of flocking might be enhanced
in coffee plantations, where a simplified habitat structure may favor predator success. Indeed, we observed
an unusual number of attacks by predators, such as accipiter hawks, in the coffee plots, and most of these
occurred during the breeding season (pers. obs.). Finally, juvenile passerines appear to be most vulnerable
to predation and starvation immediately after fledging (e.g., Anders et al. 1997, Cohen and Lindell 2004),
which could contribute to lower survival probabilities of juveniles that we documented between March and
August.
Common Bush-Tanagers and Golden-crowned Warblers are territorial toward conspecifics when
breeding in our study system. Thus, successful immigration into preferred breeding habitat probably
depends, in part, upon mortality-driven turnover of territory holders. Both species show a peak in local
habitat occupancy during the breeding season and this is, therefore, the time of the year where active
habitat selection should primarily occur. In fact, our models and data demonstrate that in Common BushTanagers, movement into epiphyte-containing habitat occurs during the breeding season. We conclude that
habitat selection in the bush-tanager comes at the nexus of behavior and demographic opportunity.
68
Studying Avian Habitat Selection in Agroforestry Systems
Our results demonstrate the usefulness of studies in agroforestry systems and the power of multistate
mark-recapture models to understanding habitat selection. Mechanistically determining the role of individual
factors in habitat selection is largely impossible, especially in complex, heterogeneous tropical habitats
where many ecological processes covary. Taking advantage of a common practice of epiphyte removal in
coffee plantations, we were able to single out this important habitat character as a determinant of the habitat
selection of one bird species, and not important for habitat selection of another. Moreover, our data
revealed the seasonal context in which habitat selection occurs. Similar studies of individually marked
animals in agroecosystems could elucidate the operation and timing of habitat selection mechanisms for a
broad range of tropical and temperate species.
AKNOWLEDGMENTS
We thank A. Martínez-Fernández, J. González-Astorga, P. Bichier-Garrido, C. González-Zaragoza,
and B. Lorr and for assistance with fieldwork. The Martínez family and plantation manager R. Monge gave
generous access to their coffee plantation. F. Becerril made illustrations used in Figs. 1 and 2. This
manuscript was improved by the comments of suggestions of S. Philpott, J. García-Franco, V. Rico-Gray,
and M. Coro-Arizmendi. Funding was provided by CONACYT (scholarship 128767 to ACA), a Smithsonian
Institution fellowship to ACA in 2002-2003, the Departamento de Ecología Funcional and Laboratorio de
Bioacústica of the Instituto de Ecología, and grants from the National Geographic Society and the Scholarly
Studies Fund of the Smithsonian Institution to RSG.
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72
Table 1. Estimates of monthly survival probabilities (S ± 1 SE) for Common Bush-Tanagers and Goldencrowned Warblers on a coffee plantation in Coatepec, Veracruz, Mexico, 30 May 2000 – 23 April 2002.
Species
S ± 1 SE
breedinga
non-breedinga
(March – August)
(September – February)
adult
0.88 ± 0.02
0.99 ± 0.01
0.98 ± 0.03
juvenile
0.81 ± 0.10
0.99 ± 0.01
0.70 ± 0.07
adult
0.89 ± 0.03
0.99 ± 0.01
0.93 ± 0.14
juvenile
0.95 ± 0.29
0.94 ± 0.04
0.96 ± 0.04
Common Bush-Tanager
transientb
Golden-crowned Warbler
aresident
bSi to i+1
individuals
for adults in the non-breeding season and for juveniles prior to their first breeding season, where i = initial
capture occasion
73
Table 2. Models of monthly survival (S), recapture (p), and movement (ψ) probabilities for Common BushTanagers (N = 112) and Golden-crowned Warbler (N = 80) on a coffee plantation in Coatepec, Veracruz,
Mexico, 30 May 2000 – 23 April 2002. Columns provide model rank, model name, number of estimable
parameters (K), second-order Akaike's information criterion values (AICc), AICc differences (∆i), and AICc
Weights (wi). Subscripts indicate parameterizations for S, p, and ψ (see Methods).
Common Bush-Tanager
Rank
Model
K
AICc
∆i
wi
1
Sage*season, pt, ψage*season*habitat
28
986.29
0
0.89
2
Sage*season, pt, ψage*season
24
990.66
4.37
0.10
3
Sage*season*habitat, pt, ψage*season*habitat
34
996.39
10.10
0.01
4
Sage*season*habitat, pt, ψage*season
30
1000.49
14.20
0.00
Golden-crowned Warbler
Rank
Model
K
AICc
∆i
wi
1
Sage*season, pt, ψ age*season
24
710.80
0
0.96
2
Sage*season, pt, ψ age*season*habitat
28
717.35
6.56
0.04
3
Sage*season*habitat, pt, ψ age*season
30
725.88
15.08
0.00
4
Sage*season*habitat, pt, ψ age*season*habitat
34
733.37
22.58
0.00
74
Figure 1. Based on the best-fit model (Table 1), estimated monthly transition probabilities (ψ ± 1 SE) for
adult Common Bush-Tanagers differed between experimental shade coffee plots with epiphytes (left) and
without epiphytes (right). Values in black indicate transition probabilities during the breeding season; nonbreeding season values are in gray italics.
ψ = 0.03 ± 0.02
ψ = 0.02 ± 0.02
epiphytes
no epiphytes
ψ = 0.09 ± 0.04
ψ = 0.19 ± 0.07
75
Figure 2. Based on the best-fit model (Table 1), estimated monthly transition probabilities (ψ ± 1 SE) for
Golden-crowned Warblers did not differ between experimental shade coffee plots with epiphytes (left) and
without epiphytes (right). Values in black indicate transition probabilities during the breeding season; nonbreeding season values are in gray italics.
ψ = 0.10 ± 0.04
ψ = 0.02 ± 0.02
epiphytes
no epiphytes
76
CAPITULO IV
AN EXPERIMENTAL ASSESSMENT ON THE
CONTRIBUTION OF EPIPHYTES TO THE OVERALL
ABUNDANCE AND SPECIES DIVERSITY OF CANOPY
INSECTS IN COFFEE PLANTATIONS IN CENTRAL
VERACRUZ, MEXICO
Andrea Cruz-Angón y Russell Greenberg
Enviado: Journal of Tropical Ecology
77
CAPÍTULO IV. AN EXPERIMENTAL ASSESSMENT ON THE CONTRIBUTION OF EPIPHYTES TO THE OVERALL ABUNDANCE
AND SPECIES DIVERSITY OF CANOPY INSECTS IN COFFEE PLANTATIONS IN CENTRAL VERACRUZ, MEXICO
ABSTRACT
The abundance of epiphytes has been considered potentially important in explaining the high diversity of
tropical canopy arthropods. In this study we assessed the possible role that the presence of epiphytes may
have on the diversity and abundance of canopy insects in an experimental study conducted in a coffee
plantation in Coatepec, Veracruz, Mexico. Epiphytes were removed from trees in one of two plots in two
sites of the coffee plantation. In each plot we collected insects from three Inga jinicuil trees by knockdown
insecticide fogging. Insects were sorted to morphospecies, counted and measured. Plots with epiphytes had
significantly higher number of species and individuals and insects larger than 5 mm were also more diverse
and abundant in plots with epiphytes. Although we expected that epiphytes would contribute to to arthropod
abundance and diversity the magnitude of the enhancement was surprisingly large with the epiphyte plot
samples having, on average 90% more individual and 22% more species than plots without epiphytes. This
suggests that the local resources that epiphytes provide to arthropods have a large, general effect on
canopy arthropods.
Key words: canopy arthropods, biodiversity, community structure, shade coffee, vascular epiphytes,
78
INTRODUCTION
The canopy of tropical forest supports a very high diversity of arthropods (Erwin 1982, Stork 1987,
Basset et al., 1996, Novotny & Basset 2000, Lucky et al. 2002, Basset, et al. 2003). This phenomenon has
also been documented for agroforestry systems, such as coffee and cacao (Perfecto et al. 1997, Bos et al.
2007). So substantial is canopy arthropod species richness that Erwin´s publications (Erwin 1982, 1983) on
beetle diversity of the tree Luehua seemannii in Panama spawned new estimates on the number of total
species thought to inhabit the earth’s ecosystems. Although the debate on the overall estimates of species
numbers still continues, the investigations of proximate and ultimate mechanisms responsible for the high
diversity of tropical canopy fauna have only just begun (Ellwood et al. 2002, Stuntz et al. 2002b, Basset et
al., 2003).
In general, complex vegetation structure and floristic diversity is thought to support high insect
diversity. Epiphytes, including bryophytes, orchids, bromeliads, aroids, ferns, among others are key
components of tropical species richness (Gentry & Dodson 1987, Krömer 2005), maintain water balance
and nutrient cycling (Nadkarni 1994, Coxson & Nadkarni 1995) and provide food resources and habitat for
other organisms (Nadkarni & Matelson 1989, and references therein; Benzig 1990). It is therefore important
to consider the role of epiphytes in supporting diversity in the forest canopy (Stork 1987, Kitching et al.
1997, Ødegard 2000, Ellwood et al. 2002). Although, epiphytes have been shown to be important
resources for canopy vertebrate (Nadkarni & Matelson 1989, Sillett 1996, Chan 2003, Raboy et al. 2004),
Cruz-Angón & Greenberg 2005, Cruz-Angón et al., in press), little work has assessed the contribution of
epiphytes to the diversity of arthropods (Gerson 1982, Nadkarni & Longino 1990, Paoletti et al. 1991,
Ellwood et al. 2002, Yanoviak et al. 2006), the groups that contributes, by far the greatest number of
species to overall canopy diversity.
There are several mechanisms by which epiphytes may be important for canopy arthropods.
Epiphytes, particularly long-lived Bromeliads (Benzig 1994), provide important microhabitats, protected from
the often harsh conditions of a tropical forest canopy (Ellwood et al. 2002, Stuntz et al. 2002b). They may
enhance arthropod diversity by the production of soil and litter environment and have foliage that is
consumed by herbivorous insects. Epiphytes also attract predators and parasites of herbivorous insects
groups as well as pollinators of epiphytic angiosperms (Wittman 2000). These arthropods may only spend a
portion of their life in the Bromeliads and thus contribute to the overall abundance of arthropods throughout
the canopy (Stork 1987, Richardson et al. 2000, Wittman 2000).
Several authors have specifically assessed insect/arthropod diversity within the epiphyte
79
microcosm (Paoletti et al. 1991, Cotgreave et al. 1993, Stuntz 2001, Richardson 1999, Richardson et al.
2000, Wittman 2000, Yanoviak et al. 2006), but very few studies have established the relative contribution
of epiphytes to entire tree crown’s insect diversity (Ellwood et al. 2002, Stuntz 2003).
The development of new techniques to access the canopy of tropical trees resulted in a great
number of studies conducted within the last two decades (Floren & Linsenmair 1997). Among these,
knockdown insecticide fogging has been one of the most commonly used methodologies to collect from the
ground big samples of canopy arthropods (Erwin 1982, 1983, Stork 1987, Basset & Kitching 1991, Stork &
Blackburn 1993, Perfecto et al. 1997). In most studies of canopy arthropods authors have failed to report
the presence or absence of epiphytic components in the trees they have sampled, and only in very few
studies where the presence of epiphytes actually controlled or quantified or their influence on canopy
insects assessed (Stork 1987, Stuntz 2001, Ellwood et al. 2002). Furthermore, epiphytes are an important
resource in human-managed ecosystems such as agroforests, but none have examined the contribution of
epiphytic plants to arthropod diversity in these important tropical habitats.
In this paper we report upon the impact on canopy arthropod diversity and abundance of a
controlled experimental removal of epiphytes from two plots in a shade coffee plantation.
MATHERIALS AND METHODS
Study site
Our study site was a 35 yr old, 200 ha shaded coffee plantation located in Coatepec, Veracruz,
Mexico (19°28’ 03” N, 96° 55’ 58” W; 1224 m elevation). The coffee management system can be described
as a commercial polyculture shade type (Moguel and Toledo 1999); We recorded 35 species of trees in
the canopy, but the tree assemblage was dominated by Inga jinicuil Schltdl. & Cham. Ex G. Don, a nitrogenfixing, fast-growing legume (Roskoski 1981, 1982). Epiphytes were abundant in the plantation where we
have recorded up to 40 species of vascular epiphytes in the experimental plots out of 57 total canopy
dwelling species found on the farm (Cruz-Angón unpl. data). The most common species include bromeliads
such as Tillandsia schiedeana Steud., T. heterophylla E. Morren, and T. juncea (Ruiz & Pav.) Poir. as. The
cactus Rhipsalis baccifera (Mill.) Stearn and the aroid Anthurium scandens (Aubl.) Engl. are also common.
Experimental design. We established two experimental sites located in opposite sides (hereafter SITE: N
= North, S = South) of the coffee plantation, and separated by a distance of approximately one km. Each
site was divided into two 3 ha plots surrounded by a matrix of shaded coffee with epiphytes. During the dry
seasons of 1999 and 2000 plantation workers removed all the epiphytes from the shade trees of one of the
80
two plots in the SOUTH site, and NORTH site respectively (hereafter PLOTS: NE+ = North with epiphytes,
NE– = North without epiphytes; SE+ = South with epiphytes, SE– = North with epiphytes). In each plot we
established a grid of 625 m2 (25 x 25 m) quadrants identified by alphanumeric coordinates. NORTH plots
had a significantly more open canopy than SOUTH plots, however vegetation surveys among plots showed
that as a result of the treatment applied, plots without epiphytes (NE– and SE–) had significantly more open
canopy than their respective counterparts (NE+ and SE+), and this was the only significantly different
variable between plots with opposite treatments; an extended description of the study site and experimental
plots can be seen at Cruz-Angón & Greenberg (2005). Mean epiphyte richness per tree among plots did not
differ (F (2, 42) = 0.88, P = 0.42) (Cruz-Angón & Greenberg 2005).
Tree selection - We restricted our samplings to I. jinicuil, the dominant shade tree of the plantation, which
represented 48-88% of the todal trees.. In our study site I. jinicuil trees supported a typical vascular epiphyte
community and it is usually covered with epiphytes. Trees had on average 15.55 ± SE 0.4 epiphyte species
per tree.
In each plot we randomly selected three grid points and located the nearest I. jinicuil tree. Trees
were selected trying to control for foliage (shade diameter ≈ 8 m), height (8 > 11 m), dbh (30 ≥ 60 cm), and
epiphyte loads (50-60% branch covered with vascular epiphytes, primarily Bromeliads). One advantage of
working in a coffee plantation with commercial polyculture shade management is that most shade trees are
planted , thus they belong to the same cohort and epiphyte colonization may have occurred at the same
time. Also, in commercial polycultures trees are usually pruned within the same year, and tree crowns do
not overlap facilitating fogging an collecting insects from a single tree crown.
Trap setting.- A day before we conducted the fogging, we set up two 4 x 4 m plastic sheets at each tree
side, just above of the coffee shrubs (>2 m height), in order to cover most of the tree canopy (Fig. 1) (Majer
& Delabie 1993). Plastic sheets were kept folded until the fogging day when they were unfolded and
extended. To collect insects dropping from canopy, we placed a 1.89 lt plastic container with alcohol (70%)
at the center of each plastic sheet, simulating a funnel. A total surface of 384 m2 was sampled.
Canopy fogging and insect collection.- Arthropods were sampled by knock-down insecticide fogging,
where a warm fog containing a pyrethrine-based insecticide (non-residual insecticide) is generated by a
thermal pulse-jet engine, which rises into a tree canopy (Stork 1991). Arthropods coming into contact with
the chemical are either killed or rendered unconscious, and fall to the plastic sheets. Fogging was
conducted from December 14 to 16, 2000 from 6:30 - 8:30 am, when wind speeds are low, which allowed
the fog to go up slowly covering the entire tree before dispersing. The fogging process took about 15 min
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per tree; we allowed a 2 hr drop-out period, then plastic sheets were screened very carefully and all insects
in them were collected and placed in the containers. Insect containers were sealed and transported to the
Entomology Lab of the Instituto de Ecología, for further examination. Although we collected all invertebrates
from fogged trees, we restricted our analysis to adult stages, because most of nymphs and larvae were not
possible to accurately been assign to a given morphospecies. With the exception of Lepidoptera (which we
were unable to sort), all adult individuals were counted, measured (length and wide) and sorted to
morphospecies (hereafter species) based on external morphology. Immatures were sorted only to family,
measured and counted. All animals were cross-referenced with a voucher collection to ensure singularity of
assigned species. The order Lepidoptera was excluded from all analyses regarding species richness and
diversity, but was included for the abundance analyses.
Data Analysis
Insect diversity and abundance. To assess the completeness of our sampling, we constructed smoothed
species accumulation curves (Gotelli & Colwell 2001) by randomizing samples by plot 100 times. We then
compared the observed values with the mean expected number of species using Chao1 index (Colwell &
Coddington 1997). We used EstimateS 7.5.0 (Colwell 2005) to randomize samples and to obtain the
expected number of species. To search for individuals abundance and species richness differences
between treatments (E+ vs. E–) for all insects collected and for insects larger than 5 mm, we conducted
GLMs for a for a split-plot design where the whole plot were the sites (SITE: NORTH and SOUTH) that
contained the partial – experimental plots (TREATMENTS: E+ and E–), trees were nested into the smaller
plots. This allowed us to maximize the power of test for the factor (TREATMENT) in which we were most
interested (Sahai & Ageel 2000). Following tests for normality and homoscedasticity we used a square root
transformation on the data (Zar 1999).
Composition and similarities of assemblages. To quantify the similarity in the compostion of
assemblages among plots, we generated a similarity matrix that was used for all multivariate analysis
described below. The similarity matrix consisted of pair-wise comparisons between samples, based on the
Bray-Curtis similarity index from observed species abundances transformed to the fourth root. This
transformation reduces the influence of the most common taxa and focus attention on patterns within the
whole assemblage (Clarke 1993, Clarke & Warwick 1998, Schnell et al. 2003). Subsequently, we performed
a two way crossed ANOSIM (analysis of similarity) using PRIMER 5 program (Clarke 1993; Clarke &
Warwick 1994; Clarke & Gorley 2001) to test for significant differences in community composition between
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site groups (North and South) and between treatment groups (E+ and E–). Finally, we conducted a
Multidimensional scaling (MDS) using the MDS program in PRIMER, to graphically ordinate differences in
species assemblages between treatment plots onto two dimensional charts.
RESULTS
Insect diversity and abundance
We collected 23, 199 arthropods. Non-insect arthropods accounted for only 30% of the collected
items with Collembolla accounting for 70% of the non-insects collected. Insect adults , 61% of the collected
individuals, comprised 12 orders, 168 families and 602 species. Of collected insect adults, 90% were <5mm
long. Hymenoptera and Diptera were the most abundant insect orders, representing 39.8% and 31.2% of
the collected adult individuals, respectively. The most species-rich orders were Coleoptera with 248 species
in 48 families and Diptera with 144 species in 67 families (Table 1).
In general, 75.4% (454 species) of the species were represented by less than 10 individuals,
contributing to less than 10% (1169 individuals) of the total catch. Only 6 % of the species (37) were
represented by at least 50 individuals and of these and only 19 species (3%) were collected in numbers
higher than a 100 individuals. The latter species represented 61% of the collected individuals. 34% were
represented by a single individual (singletons).
Response to Epiphyte Removal
The orders that showed a consistent pattern of higher diversity in E+ plots than in E- plots were
Coleoptera, Diptera, Hymenoptera and Orthoptera (Table 1). Ants (Formicidae) were three times more
abundant in E+ than in E- plots (F(1,12) = 19.01, P > 0.001; Mean ± SE: E+ = 244.83 ± 76.79; E– = 69.58 ±
25.91).
Randomized species accumulation curves show that plots in the South site had significantly more
species than plots in the North site. None of the plots showed an asymptotic curve. Plots with epiphytes
(NE+ and SE+) had significantly more species than their E– counterparts. Confidence intervals at 95%
show no overlap between plots with and without epiphytes (Fig. 2). Expected number of species showed a
consistent pattern of the species accumulation by treatment and sites (Fig. 3). Richness estimates for E–
plots indicate that inventory levels were above 70%, whereas for E+ plots inventory completeness were
below 70% (Table 1). This indicates that in order to accomplish a greater percentage of completeness E+
plots would require a greater sampling effort than E– plots.
The ANOVA analysis showed that sites differed significantly in both mean number of species and
individuals (species: F (1,12) = 36.8, P < 0.001; individuals: F (1,12) = 79.7, P < 0.001). Mean species richness
83
and abundance by tree were significantly greater in South plots (species: 103.3 ± 10.9SE; individuals:
660.9 ± 126.2 SE) than in the North plots (species: 58.6 ± 7.3 SE; individuals: 338.3 ± 96.9 SE). The
TREATMENT factor was significant for both mean number of species and individuals (species: F (1,12) = 8.9,
P = 0.01; individuals: F (1,12) = 23.1, P < 0.001). Mean number of species and individuals was significantly
greater in plots with epiphytes (species: 89.2 ± 13.4 SE; individuals: 655.2 ± 143.4 SE) than in plots
without epiphytes (species 72.7 ± 8.6 SE; individuals: 344.1 ± 71.3 SE ). There was no significant SITE by
TREATMENT effects for either number of species or individuals (species: F (1,12) = 1.3, P < 0.27; individuals:
F (1,1) = 0.02, P < 0.90). Treatment effects for abundance and diversity of insects larger than 5 mm where
consistent with the pattern found for all insects (species: F (1,12) = 9.6, P = 0.009; individuals: F (1,12) = 9.9, P
= 0.008). Mean number of species and individuals for this group size was significantly greater in plots with
epiphytes (species: 23.83 ± 6.09 SE; individuals: 135.83 ± 56.14 SE) than in plots without epiphytes
(species 11.16 ± 1.22 SE; individuals: 47.67 ± 9.62 SE).
Community structure and similarities.
Community structure varied greatly among sites and treatments. Mean dissimilarity within plots was
almost as great as dissimilarity among plots (Table 2). ANOSIM showed that all plots significantly differed in
community composition. Averaged dissimilarity among plots was about 80%. Despite the high species
turnover and community structure differences, the nMDS generated two well defined dimension plot (Stress
= 0.17) dimension 1 separated samples by site, whereas dimension 2 separated samples by treatment (Fig.
4).
DISCUSSION
Insect diversity, abundance, and size distribution
Our results show that in the focal shade coffee farm epiphytes contribute to a high abundance and
diversity of insects. In our study the main difference between plots within a site (North and South) was the
presence or absence of epiphytes. Trees with epiphytes had an average of 22% more arthropod
morphospecies and 90% more individuals than their treatment counterparts. Differences among sites may
be explained by the difference in canopy cover, which was greater in the South sites. Sites in the South had
significantly more species and individuals than plots in the North. This indicates that the amount of tree
foliage (canopy cover) may also an important factor for canopy insect faunas (Wilkens et al. 2005).
The relatively small number of insects larger than 5 mm was expected since it has been reported
that insecticide fogging may not be a good method to collect large canopy insects (Basset et al. 1997,
Ellwood 2002). However, it is worth noticing that greater numbers of large insects (> 5 mm), which are the
84
most important food items for insectivorous vertebrates, were collected in trees with epiphytes than in trees
without them. Experimental studies conducted in coffee plantations have shown that when plants are
excluded from birds, insects within the exclosures tend to be larger and more abundant than insects outside
the exclosure (Greenberg et al. 2000). Epiphytes may function as natural insect exclosures and insects may
find a way to hide within the epiphyte microcosm from potential big predators that prefer large preys such as
lizards or birds (Dial & Roughgarden 1995, Greenberg et al. 2000) and therefore be able to be more
abundant and gain larger sizes. This may explain the significantly greater abundance of large insects in the
E+ plots.
In terms of the effects of epiphytes on specific groups, only Hymenoptera (predominantly ants)
showed significantly greater abundance in plots with epiphytes; ants have previously been reported to be
the dominant insect species in epiphytes (Longino & Nadkarni 1990, Wittman 2000, Ellwood et al. 2002,
Stuntz et al. 2002a). In addition to Hymenoptera three other orders (Coleoptera, Diptera, and Orthoptera)
showed a higher species richness in plots with epiphytes.
In our study a large number of species (454) were represented by less than ten individuals, and this
seems to be a generalized pattern for tropical canopy (Morse et al. 1988, Floren & Linsenmair, 1998,
Basset and Kitching 1991, Novotny & Basset 2000, Lucky et al. 2002). Given the large number of species
found with less than ten individuals it is possible that part of these species may be “tourist species”. Tourist
species are those that have no long-lasting relationship with the plant, but which may be attracted to trees
for short-term use, such as for shelter and sustenance (honey-dew and other substances), or as a site for
sunbasking and sexual display (Gaston et al. 1993). So our “true canopy” insect species richness may have
been overestimated by the presence of tourist species, which we were not able to identify. However, the
presence of tourist species should not contribute to a systematic bias towards higher diversity estimates for
the epiphyte versus non-epiphyte plots. Furthermore, the influence of tourist upon our estimate of faunal
similarities should be low, since the index used is less sensitive to rare species.
Although very few studies have been based on an experimental removal of epiphytes (Ellwood et
al. 2002), the overall contribution of epiphytes to canopy insect abundance and composition has been
reported to be low at an ordinal level (Stuntz et al. 2003). Stuntz and collaborators (2003) studied the
contribution of epiphytes to the overall arthropod diversity of the small tropical tree Annona glabra L.
(Annonaceae). In this study the authors collected the arthropods from A. glabra trees that had different
species of epiphyte loads and no epiphytes at all. The authors found no significant differences in the
abundance or community composition of arthropods between trees with and without epiphytes. However,
85
their results may not be applicable to all tropical forest types, because they worked with a rather small tree
(6m) in an inundated area, and epiphytes did not seem to be quite abundant in this tree.
On the other hand, Ellwood and collaborators (2002) found that a single large Bird’s Nest Fern
(Asplenium nidus complex) an epiphytic fern that occurs through out the forest of Southeast Asia, might
contain from 7 to 93 percent of the total number of invertebrates in the tree crown. These observations are
more consistent with our results.
Even though, insecticide knockdown fogging has proven not to be a good method for collecting the
fauna of non-vascular epiphyte fauna (Yanoviak et al. 2003), the method has been reported to work well for
vascular epiphytes (Stork & Hammond 1997). Furthermore, any underestimation of the abundance of
arthropods in epiphytes due to the collection method would bias the results away from supporting the
hypothesis of greater arthropod abundance on the epiphyte control plots. Still, we consider canopy fogging
the first approach and it should be followed up with more fine-tuned sampling and observational techniques
to further assess guild composition, proportion of rare species versus tourist.
Community structure and similarities
Our results showed great species dissimilarities between treatment and control plots, as well as
trees within a plot. Such high turnover between trees has been a consistent result of all tropical canopy
arthropod studies. (Erwin and Scott 1980, Davies et al. 1997, Floren & Linsenmair 1998, Lucky et al. 2002).
Furthermore, high insect species turnover between epiphyte species has also been documented
(Richardson 1997, Stuntz 2002a). For example, Stuntz and collaborators (2002a) found very little overlap in
insect species composition for three species of epiphytes studied in an inundated forest in Panama. Despite
the high levels of between tree turn-over in our study, we were able to document a pattern of faunal
similarity within treatment groups based on Multi-dimensional Scaling, which indicates that regardless of the
great species turnover, trees with epiphytes had similar insect community structure when compared to trees
without them. Our results are consistent with Stork (1987) who found that the amount of vines and
epiphytes was more important for faunal similarity in particular insect groups (i.e. Homoptera, Grilllidae,
Anthicidae, Chrysomeliadae and scavengers) than taxonomic relatedness of the trees, in a study conducted
in Borneo.
Conservation implications of epiphyte removal
Over the last few decades several coffee producing countries have simplified the shade of coffee
plantations by reducing the diversity and abundance of shade trees (Romero-Alvarado et al. 2002). In
Mexico, it has been estimated that over 49% of the producing area has been transformed from highly
86
diverse shade systems to legume-dominated systems (Santoyo et al. 1994). In the latter systems, epiphyte
removal from shade trees is a relatively common management practice (Cruz-Angón & Greenberg 2005).
The elimination of epiphytes and mistletoes from the canopy results in simplification of the vertical structure
and diversity of the coffee plantations that in fact are already simplified compared to pristine forests.
Experimental evidence indicates that epiphyte removal may have negative effects in bird communities of
coffee plantations (Cruz-Angón & Greenberg 2005), even in species that do not have a direct relationship
with epiphytes (do not use epiphytes as nesting sites or feeding substrate). In particular, insectivorous
species that do not feed or nest in epiphytes were significantly less abundant in site without epiphytes than
in sites with epiphytes, the reduction of non-epiphyte related bird species may be explained by the overall
reduction in the number of insects observed in plots without epiphytes. Our results confirm that epiphytes
might represent a ‘‘keystone resource’’ in coffee plantation, just as they are in other tropical forests because
of their important role in controlling major functional characteristics of these ecosystems (Nadkarni 1994).
Tropical forest canopies are complex, making the detection of ecological relationships difficult.
Some ecological patterns might be studied in simpler systems, with fewer confounding variables, rather
than in undisturbed and more elaborated ecosystems (Stuntz 2001). Coffee plantations can be good model
systems to deal with this question. Our results study may give a glance of the complexity and important
interactions held in more complex ecosystems, such as the remnant montane forests of the region.
ACKNOWLEDGEMENTS
We thank A. Martínez-Fernández, M.L. Baena for assistance with fieldwork. M.L. Baena identified
all insects to morphospecies. The Martínez family and plantation manager R. Monge provided access to
their coffee plantation and permission to tree fogging. F. Becerril drew the Inga jinicuil with epiphytes and
trap setting for figure 1. M. Ordano, R. Munguía and C. Tejeda, gave statistical advice; J.G. García-Franco,
V. Rico-Gray, M. Coro-Arizmendi improved the manuscript with their comments and corrections. Funding to
ACA was provided by CONACYT (scholarship 128767), Smithsonian Institution Fellowship 2002-2003,
Departamento de Ecología Funcional and Laboratorio de Bioacústica of the Instituto de Ecología and grants
from the National Geographic Society and Scholarly Studies Fund of the Smithsonian Institution to RSG.
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not effectively sampled by canopy fogging. Biodiversity and Conservation 12: 731–741.
YANOVIAK S. P., NADKARNI N. M. & SOLANO J. R. 2006. Arthropod assemblages in epiphyte mats of Costa
Rican cloud forests. Biotropica 36: 202–210.
ZAR, J. H. 1999. Biostatistical analysis. Prentice Hall, Inc. Upper Saddle River, NJ, USA.
92
Table 1. Number of insect morphospecies by order and number of families (in parenthesis) captured during
the canopy fogging of 12 Inga jinicuil trees in an experimental setting in a shade coffee plantation where six
trees (three per plot) were epiphyte removed while other six trees remain with epiphytes, in Coatepec,
Veracruz, México. Sites: NORTH, SOUTH, Treatments: E+ = With Epiphytes, E– = Without Epiphytes.
Total columns show total number of families and species per site. Expected number of species was
obtained using Chao 1 estimate. Completeness represents the percentage of observed versus estimated
species richness. Within Dissimilarity represents the mean percentage dissimilarity between samples within
plots. In bold are the groups that showed a consistent pattern of higher diversity in E+ plots.
NORTH
E+
E–
SOUTH
total
E+
E–
total
TOTAL
Coleoptera
63 (22)
57 (20)
104 (31)
151 (35)
123 (29)
205 (41)
248 (48)
Dermaptera
2 (1)
2 (1)
3 (1)
7 (1)
6 (1)
9 (1)
9 (1)
60 (34)
47 (24
76 (39)
99 (45)
65 (37)
123 (58)
144 (67)
0 (0)
0 (0)
0 (0)
1 (1)
0 (0)
1 (1)
1 (1)
Hemiptera
23 (10)
26 (8)
39 (11)
34 (11)
24 (9)
46 (13)
63 (14)
Homoptera
15 (6)
13 (5)
20 (7)
8 (5)
13 (6)
14 (7)
23 (9)
Hymenoptera
35 ( 6
24 (7)
43 (8)
58 (14)
31 (8)
69 (15)
82 (16)
0 (0)
0 (0)
0 (0)
1 (1)
0 (0)
1 (1)
1 (1)
Orthoptera
10 (4)
5 (3)
12 (5)
9 (4)
2 (2)
10 (4)
15 (5)
Psocoptera
0 (0)
0 (0)
0 (0)
13 (4)
1 (1)
13 (4)
13 (4)
Thysanoptera
1 (1)
0 (0)
1 (1)
1 (1)
1 (1)
1 (1)
1 (1)
Diptera
Embioptera
Isoptera
TOTAL
209 (94)
174 (68) 298 (102)
383 (120) 267 (93)
Expected richness
390.5
245.56
553.41
361
Completeness (%)
53.5
70.9
69.2
73.9
77.81
71.05
67.86
Within Dissimilarity (%) 77.61
93
494 (148) 602 (168)
Table 2. Results from two way crossed ANOSIM test, based on Bray–Curtis dissimilarities in fourth-root
transformed insect abundances from four experimental plots in a coffee plantation, Central Veracruz,
México. Pairwise ANOSIM tests for differences between plots. Experimental plots: NE+ = North with
epiphytes, NE– = North without epiphytes, SE+ = South with epiphytes, SE– = South without epiphytes.
Plot comparison
R
Mean dissimilarity
P
(%)
NE+, NE–
0.233
0.01
82.99
NE+, SE+
0.565
0.002
83.29
NE+, SE–
0.583
0.002
85.43
NE–, SE+
0.47
0.002
88.04
NE–, SE–
0.339
0.004
82.52
SE+, SE–
0.483
0.002
77.60
94
Figure 1. Trap setting for a knockdown insecticide fogging of an Inga jinicuil tree with epiphytes in a coffee
plantation, Coatepec, Veracruz, México. Inga jinicuil trees experimentally depleted of epiphytes were also
fogged and insects collected.
95
Figure 2. Mean species accumulation curves for insect species collected by knockdown fogging of three
trees per plot (two samples per tree) in an experimental setting in a coffee plantation in Central Veracruz
México. Experimental Plots: North with epiphytes (♦), North without epiphytes (□), South with epiphytes
(▲), and South without epiphytes (○). Error bars represent 95% Confidence Intervals.
450
Number of species
400
350
300
250
200
150
100
50
0
0
1
2
3
4
Number of samples
96
5
6
Figure 3. Mean expected number of insect species by experimental plot in a coffee plantation in Central
Veracruz México. Mean expected number of species were based on Chao 1 index form the 100 iteration.
Experimental plots: NE+ = North with epiphytes, NE– = North without epiphytes, SE+ = South with
epiphytes, SE– = South without epiphytes. Error bars represent 95% Confidence Intervals.
Expected number of species (95% CI)
700
600
500
400
300
200
100
0
NE+
NE-
SE+
97
SE-
Figure 4. Ordination of two matched pairs of experimental plots, based on a multidimensional scaling
analysis used to compare the similarities of the studied plots. Experiment consisted on removing epiphytes
from all trees in one of two plots in two sites. Two samples per trees, three trees per site were fogged and
insects were collected. Experimental Plots: North with epiphytes (♦), North without epiphytes (□), South with
epiphytes (▲), and South without epiphytes (○). Stress = 0.16
Dimension 2
1
0.8
0.6
0.4
0.2
0
-0.2
-0.4
-0.6
-0.8
-1
-2
-1
0
1
Dimension 1
98
2
3
CAPITULO IV
CONCLUSIONES
99
CAPITULO V. CONCLUSIONES
En el presente trabajo de tesis planteé como hipótesis que la remoción de epífitas podría tener un
efecto negativo sobre la diversidad y abundancia de aves e insectos del cafetal, partiendo de la afirmación
hecha a través de estudios observacionales realizados por varios autores en bosques tropicales (Remsen
1985, Nadkarni y Matelson 1989, Dean et al. 1990, Sillett 1996, Stuntz 2001) de que las epífitas suponen
una mayor disponibilidad y variedad de recursos para las faunas asociadas del dosel (aves e insectos) y
por lo tanto promueven una mayor diversidad y abundancia de los mismos. Los efectos que podrían
observarse dependerían del grado de relación que la fauna tenga con las epífitas. Es decir, especies con
un grado de dependencia mayor, ya sea en cuanto a recursos alimenticios, refugio o sitios de anidación, se
verían más fuertemente afectadas por la ausencia de este recurso.
Los objetivos particulares que consideré pertinentes para evaluar esta hipótesis fueron caracterizar la flora
epífita de un cafetal, determinar el grado de utilización de los recursos ofrecidos por la epífitas para las
aves, así como evaluar los efectos de la remoción de las epífitas sobre las comunidades de aves e insectos
del cafetal, a través de muestreos apropiados para cada uno de los grupos antes mencionados.
Este trabajo podría ubicarse en dos esferas de aplicación. Primero, el papel de las epífitas como
promotoras de diversidad es una pregunta que desde el ámbito de la ecología de los ecosistemas
tropicales ha importado a varios investigadores. Por otro lado, el efecto de la remoción de epífitas sobre las
faunas asociadas a un agroecosistema como los son los cafetales, tiene implicaciones sobre la
aplicabilidad de este tipo de manejo y sobre la robustez de criterios de certificación de café de sombra.
PRINCIPALES RESULTADOS DE LA INVESTIGACIÓN
Los principales resultados de este trabajo son resumidos de manera esquemática en la figura 1. La
evaluación experimental de la presencia de las epífitas en el agroecosistema cafetalero estudiado, mostró
claramente que estas tienen un papel importante en la estructura y composición de la comunidad de aves.
A pesar de que el número de especies no fue significativamente distinto entre las parcelas con y sin
epífitas, se observó una tendencia de riqueza mayor de especies (especialmente durante la época de
invernación) en los sitios con epífitas. Sin embargo, la estructura de la comunidad de aves sí fue distinta.
Dieciocho especies de aves mostraron una abundancia significativamente mayor en los sitios donde las
epífitas estaban presentes, que en donde no hubo epífitas. Este cambio ocurrió tanto en la época de
invernación (noviembre – febrero), como en la de anidación (mayo – agosto). Los recursos a través de los
cuales las epífitas pueden afectar la distribución de las especies de aves, incluyen disponibilidad de
100
materiales para construcción de nidos, sitios de anidación y/o refugio, frutos y néctar, así como insectos
(Nadkarni y Matelson 1989). Es importante que la riqueza de especies como único patrón de evaluación
puede enmascarar algunos otros procesos y fenómenos que no alcanzan a reflejarse en este indicador,
como la estructura de la comunidad que toma en cuenta tanto la riqueza, como la abundancia de las
especies y que en este caso permitieron elucidar las diferencias tan contrastantes en ambos tipos de
hábitat.
Entre los mecanismos que pueden ser afectados por el cambio en la disponibilidad de los recursos
antes mencionado están: la competencia intra e interespecífica y la vulnerabilidad a la depredación, que
inciden sobre la sobrevivencia de los individuos (Calder 1984, Peters 1986, Nager y Zandt 1994). En este
sentido, es importante considerar la dependencia y capacidades de respuesta diferenciales de las especies
al cambio en las condiciones ambientales. La evaluación del mecanismo de selección de hábitat en dos
especies, permitió evidenciar este aspecto. Chlorospingus ophthalmicus, mostró una preferencia activa por
sitios con epífitas, mientras que Basileuterus culicivorus no evidenció esta preferencia de hábitat. Esta
selección por parte de C. ophthalmicus se manifestó claramente en las dos temporadas evaluadas, siendo
especialmente importante en adultos durante la temporada de anidación, cuando la presión de la
competencia por sitios y materiales de anidación es mayor.
Aunque la supervivencia de ambas especies fue mayor durante la época de invernación, no estuvo
relacionada con la presencia de epífitas. La supervivencia equitativa en los dos sitios podría ser explicada
en términos de la relación existente entre la disponibilidad de recursos y la tasa de utilización de los
mismos, es decir, el nivel de competencia. La intensidad competitiva está determinada por la cantidad neta
de recursos disponibles. Esta a su vez es el resultado de la diferencia entre la cantidad bruta de recursos,
menos la cantidad de recursos utilizados (Keddy 1989). Así, en los sitios con epífitas aún cuando hay una
mayor cantidad bruta de recursos, también hay una mayor utilización de los mismos, por efecto de la mayor
densidad de aves. En cambio, en el otro sitio donde hay una menor cantidad de recursos, hay una menor
presión sobre ellos, debido a una menor densidad de aves y por lo tanto las oportunidades de
sobrevivencia individual en uno y otro sitio pueden ser equivalentes (Fretwell y Lucas 1970). Lo anterior
resalta la importancia de llevar a cabo evaluaciones a nivel específico, dado que los procesos de los
ecosistemas están determinados en gran medida por la identidad de las especies involucradas. Tal fue el
caso de los resultados contrastantes en la selección de hábitat en C. ophthalmicus y B. culicivorus.
El estudio sobre la comunidad de insectos permitió demostrar que la remoción de epífitas tiene
efecto directo sobre otros grupos de organismos. La abundancia y diversidad de especies de este grupo
101
fue afectada negativamente con la remoción de epífitas. En comparación con las aves donde la riqueza no
fue afectada, el número de especies e individuos de insectos fueron significativamente menores en los
sitios sin epífitas. Además, el tamaño corporal de los mismos fue menor, lo cual puede representar una
reducción en la disponibilidad y calidad de alimento para otros grupos como las aves. Así, la remoción de
epífitas puede tener efectos directos e indirectos en cadena sobre las interacciones entre diferentes
grupos. Siendo los insectos una fuente de alimento importante para las aves, su reducción en los sitios sin
epífitas podría ser uno de los factores que explican la menor abundancia registrada de algunas especies de
aves, especialmente insectívoras. Es probable que otros grupos de vertebrados, como mamíferos
pequeños, anfibios y reptiles asociados al dosel de las plantaciones de café, también sean afectados. Por
otro lado, procesos como la polinización y la dispersión de frutos podrían ser alterados como resultado de
la remoción de epífitas, aspecto que requiere estudios particulares.
CONTRIBUCIONES DEL TRABAJO
El cafetal estudiado como sistema modelo, permitió la evaluación de algunos patrones ecológicos
que están presentes en sistemas más complejos como los bosques tropicales, pero donde fue posible
tener un mejor control de algunas variables. Así, se pudo controlar en gran medida el efecto de la
diversidad de árboles del dosel, plantas del sotobosque y la estructura vertical asociada a esta diversidad,
que pueden incidir en los patrones y procesos evaluados en este estudio.
Aunque algunos trabajos ya habían reportado observaciones sobre la posible importancia de las
epífitas para las aves, no había cuantificaciones experimentales directas al respecto. Los resultados de
este trabajo demuestran que puede existir una selección activa de hábitat de algunas especies de aves por
la presencia de epífitas, así como respuestas diferenciales dependientes de las especies involucradas.
Frecuentemente, los trabajos sobre la diversidad de insectos en el dosel, no distinguen entre la
diversidad de insectos asociada a los árboles de la asociada a las epífitas presentes en los mismos. De tal
manera que en los reportes de la diversidad de insectos del dosel frecuentemente ha estado confundida
con la diversidad de insectos presentes en epífitas. Además, si bien existen estudios donde se ha evaluado
la diversidad de insectos presente en algunas especies de epífitas en particular, la contribución de las
epífitas sobre la diversidad de insectos en un tipo de hábitat determinado no había sido cuantificada.
En resumen, esta investigación resalta el papel relevante que los cafetales de sombra tienen,
donde las epífitas no son removidas, para el mantenimiento de la diversidad de aves e insectos y las
posibles interacciones entre ellos.
102
RECOMENDACIONES DE MANEJO
Los resultados encontrados apuntan claramente hacia la importancia de la conservación de la flora
epífita en cafetales de sombra. Hasta el momento, los efectos de la remoción de las epífitas sobre el
aumento en el rendimiento de los arbustos de café no habían sido determinados (pero ver García-Franco y
Toledo, en prensa). Sin embargo, si lo que se busca con la remoción de epífitas es el incremento en la
radiación de luz incidente sobre los arbustos de café (Soto-Pinto et al. 2000), la poda de los árboles podría
ser una estrategia ecológicamente más apropiada.
Se ha registrado que la diversidad de epífitas en cafetales es mayor en árboles remanentes del
bosque original que en árboles plantados (Hietz 2005), por lo que el mantenimiento de árboles
pertenecientes al primer grupo debería ser favorecido. Si la remoción de epífitas es inevitable, sería
recomendable que al menos algunos árboles se dejarán intactos, ya que el mantener árboles con estas
características podría asegurar una fuente diversa de propágulos. De preferencia se recomienda que se
mantengan intactos aquellos árboles de mayores dimensiones (más viejos), ya que estos frecuentemente
albergan una mayor riqueza de epífitas (Hietz 2005, Solís-Montero et al. 2005). Con base en los resultados
encontrados en este estudio, el manejo de la flora epífita en cafetales de sombra, es un criterio que debe
ser considerado en los estándares para certificación de sombra (amigable con las aves, con la fauna, de
conservación de la biodiversidad) de este tipo de agroecosistema. Aunque los precios que ha alcanzado el
café en la última década sean tan bajos que desincentivan prácticas tales como la remoción de epífitas,
debido a sus altos costos de implementación, es importante que las instituciones académicas, de
conservación y reguladoras de la calidad de café (consejos reguladores y otros) difundan a cefeticultores la
importancia ecológica del mantenimiento de un dosel con los atributos antes mencionados.
DIRECTRICES FUTURAS
Como se mencionó anteriormente se requiere de una evaluación precisa de los efectos de la
remoción de epífitas en la productividad de los cafetales de sombra. Una evaluación de este tipo debería
tomar en consideración no solo la cantidad de frutos producidos sino también su calidad. Si existe un
beneficio de la remoción de epífitas en el incremento de la producción de café, como resultado de una
mayor incidencia de luz, sería importante evaluar el posible aumento en la competencia a nivel del
sotobosque, al favorecerse el establecimiento de especies pioneras (o secundarias). Al respecto, sería
103
necesario tomar en cuenta la relación costo beneficio de esta práctica, no sólo en términos económicos
sino también en términos ecológicos. Por ejemplo, el efecto sobre el ciclaje de nutrientes, la captación y
reserva de agua, y las variaciones microclimáticas. En caso de tener un dosel con especies caducifolias la
presencia de epífitas puede tener un efecto benéfico al proveer de sombra durante la temporada en el que
follaje arbóreo no está presente, además de que las epífitas aportan nutrientes, contribuyen a reducir el
golpe del agua de lluvia y liberan de manera paulatina de la misma contenida en sus agregados.
También sería interesante analizar el posible impacto de las fluctuaciones medioambientales,
como resultado de esta práctica, sobre el desempeño de los organismos y las interacciones ecológicas.
Tomando en consideración las ventajas del sistema de estudio, se podría estudiar el posible cambio en la
composición de grupos funcionales de insectos y sus efectos sobre las interacciones tróficas.
Si bien la importancia ecológica de las epífitas para las aves e insectos fue evaluada en
plantaciones de café, los resultados encontrados evidencian la posible importancia de este grupo en otros
ecosistemas de la región, como el bosque mesófilo de montaña. En sistemas más diversos la importancia
relativa de las epífitas podría ser menor debido a una mayor variedad y disponibilidad de otros recursos,
que una diversidad mayor de árboles implica. Evaluaciones experimentales al respecto y un seguimiento
por un periodo de tiempo mayor para determinar los efectos a largo plazo de la ausencia epífitas y el
desempeño de los organismos en el sistema, serían necesarias, ya que no existen evaluaciones sobre la
capacidad de respuesta de las especies a cambios de esta naturaleza.
Hasta donde se tiene conocimiento el presente trabajo es la primera evaluación experimental sobre
la importancia de las epífitas para las aves y en términos de la selección de hábitat, es la primera
evaluación experimental de selección de hábitat en un sistema y especies tropicales.
LITERATURA CITADA
Calder, W. A. III. 1984. Size, function and life history. Harvard University Press. Cambridge, Massachusetts.
Dean, W. R. J., S. J. Milton y W. R. Siegfried. 1990. Dispersal of seeds as nest material by birds in semiarid
Karoo shrubland. Ecology 71: 1299–1306.
Fretwell, D. S. y H. L. Lucas. 1970. On territorial behavior and other factors influencing habitat distribution in
birds. Acta Biotheoretica 19:19-32.
García-Franco, J.G. y Toledo-Aceves M.T. (en revisión). Diversidad de epífitas vasculares en sistemas
cafetaleros. En: R. Manson, S. Gallina, K. Mehltreter y V. Hernández (eds.). INE-INECOL
Hietz, P. 2005. Conservation of vascular epiphyte diversity in Mexican coffee plantations. Conservation
104
Biology 19: 391-399.
Keddy, P. A. 1989. Competition. Chapmann & Hall, Great Britain.
Nadkarni, N. M. y T. J. Matelson. 1989. Bird use of epiphyte resources in neotropical trees. The Condor
91:891-907.
Nager, R. G. y H. S. Zandt. 1994. Variation in egg size in Great tits. Ardea 82: 315–328.
Peters, R. H. 1986. The ecological implications of body size. Cambridge University Press. Cambridge,
Massachusetts.
Remsen, J. V. Jr. 1985. Community organization and ecology of birds of high elevation humid forests of the
Bolivian Andes. Pp. 733-756. En : M. L. Morrison, M.S. Foster, E. S. Morton, R. S. Ridgely y F. G.
Buckley [eds.], Neotropical Ornithology. Ornithological Monographs. 36.
Solís-Montero, L., A. Flores-Palacios y A. Cruz-Angón. 2005. Shade-coffee plantations as refuges for
tropical wild orchids in central Veracruz, Mexico. Conservation Biology 19: 908-916.
Sillett, T. S. 1996. Foraging ecology of epiphyte-searching insectivorous birds in Costa Rica. The Condor
96: 866-877.
Soto-Pinto, L., I. Perfecto, J. Castillo-Hernández y J. Caballero-Nieto. 2000. Shade Effect on coffee
production at the northern Tzeltal zone of the state of Chiapas, Mexico. Agriculture Ecosystems &
Environment 80: 977-987.
Stuntz, S. 2001. The influence of epiphytes on arthropods in the tropical forest canopy. PhD. Tesis.
Würzburg. 111 pp.
105
Figura 1. Resumen gráfico de los principales resultados encontrados en esta tesis. En un cafetal se establecieron
cuatro parcelas experimentales. En dos de ellas se removieron las epífitas de todos los árboles del dosel (árbol de la
derecha), en las otras dos las epífitas permanecieron intactas. A través de muestreos de aves e insectos se encontró
que la abundancia de aves, la diversidad y abundancia de insectos fue mayor en las parcelas con epífitas que en las
parcelas sin epífitas. Además con respecto a las aves, se demostró que un ave residente del cafetal Chlorospingus
ophthalmicus selecciona activamente los sitios con epífitas. La remoción de epífitas implica cambios importantes en
la composición de las comunidades de aves e insectos.
Aves
≈
Diversidad
La riqueza (numero) de especies de aves fue similar en ambos tipos de parcelas
Abundancia
Especies
abundantes
Seleccionado por
aves
Comunidad
+
Se observó un mayor
número de individuos
18
Colibríes, tangaras y
algunos
insectívoros
fueron más abundantes
Chlorospingus
ophthalmicus
selecciona los sitios
con epífitas
Abundancia
Insectos < 5 mm
Comunidad
El número de aves fue
menor.
3
Únicamente
especies
características de sitios
abiertos fueron más
abundantes.
Chlorospingus
ophthalmicus emigra de
estos sitios hacia sitios
con epífitas
∆
Este símbolo indica cambio. La comunidad de aves de los sitios con epífitas fue muy distinta a la de los sitios
sin epífitas
Insectos
Diversidad
-
+
+
+
Los sitios con epífitas
tuvieron una mayor
diversidad de insectos
-
Los sitios con epífitas
tuvieron un mayor
número de insectos
Los insectos de mayor
tamaño fueron más
abundantes
Los sitios sin epífitas
tuvieron
una
menor
diversidad de insectos
Los sitios con epífitas
tuvieron un menor número
de insectos
Los insectos de mayor
tamaño
fueron
más
abundantes
∆
Este símbolo indica cambio. La comunidad de insectos de los sitios con epífitas fue muy distinta a la de los
sitios sin epífitas
106