Dispersión de semillas por el mono araña (Ateles geoffroyi) en fragmentos y en áreas de un bosque continuo de la selva Lacandona: implicaciones para la conservación

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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO
POSGRADO EN CIENCIAS BIOLÓGICAS
CENTRO DE INVESTIGACIONES EN ECOSISTEMAS
DISPERSIÓN DE SEMILLAS POR EL MONO ARAÑA (ATELES
GEOFFROYI) EN FRAGMENTOS Y EN ÁREAS DE UN BOSQUE
CONTINUO DE LA SELVA LACANDONA: IMPLICACIONES PARA
LA CONSERVACIÓN
TESIS
QUE PARA OBTENER EL GRADO ACADÉMICO DE
DOCTOR EN CIENCIAS BIOLÓGICAS
PRESENTA
OSCAR MAURICIO CHAVES BADILLA
COMITÉ TUTOR
DRA. KATHRYN ELIZABETH STONER (TUTORA PRINCIPAL)
DRA. JULIETA BENÍTEZ MALVIDO
DR. ALEJANDRO ESTRADA MEDINA
MÉXICO, D.F. Junio, 2010

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Agradecimientos
Este proyecto se realizó gracias al apoyo del Posgrado en Ciencias Biológicas de la
Universidad Nacional Autónoma de México (UNAM). El proyecto contó con el apoyo
financiero del Consejo Nacional de Ciencia y Tecnología, México (CONACyT CB2005-
C01-51043 y CB2006-56799). La Secretaría de Relaciones Exteriores de México otorgó
una beca doctoral durante los tres primeros años del proyecto. Quiero agradecer a todo mi
comité tutoral: Kathryn E. Stoner, Julieta Benítez y Alejandro Estrada por sus valiosos
comentarios y recomendaciones para mejorar los diferentes manuscritos que componen esta
tesis. Durante toda esta aventura académica de casi cuatro años, el apoyo incondicional y la
amistad brindada por mi tutora fueron factores clave para que siguiera adelante.
Desde un inicio algunos colegas cuestionaron la factibilidad de este proyecto de tesis
debido a las múltiples complicaciones que conlleva el estudio de los monos araña y a mi
inexperiencia como primatólogo. Pero como a mí las cosas fáciles nunca me han atraído
(porque las puede hacer cualquiera) decidí asumir el reto con trabajo duro y mucha pasión
científica. Fueron muchas las personas que colaboraron con la realización de esta tesis en
uno u otro momento. Pero por cuestiones de brevedad y porque la memoria a veces me
falla, sólo mencionaré algunas. Al Laboratorio de Ecología del Hábitat Alterado, dirigido
por la Dra. Julieta Benítez-Malvido, que junto con su grupo de trabajó generó las bases para
el desarrollo de este proyecto. Celine Hauglustaine, Kathryn Amato, María Concepción
Balderas, Santanita Martínez, Jeannet Herrera, Adolfo Jamangapé, Ana González y Rafael
Lombera brindaron una importante ayuda durante diferentes etapas del trabajo de campo. A
Víctor Arroyo por todas sus recomendaciones y la colaboración que brindó durante el
diseño y revisión crítica de los manuscritos. A Mauricio Quesada por el apoyo logístico
brindado en 2006 para mi ingreso al sistema de posgrado, por su amistad y por las
sugerencias que realizó para el mejoramiento del capítulo II y IV de esta tesis. A Juan
Manuel Lobato, Gumersindo Sánchez y Heberto Ferreira por la asistencia técnica. A mi
amigo Marlon Delgado por apoyarme desde Costa Rica con diversas gestiones. A los
habitantes de los ejidos Zamora Pico de Oro, Reforma Agraria, Loma Bonita, y Boca de
Chajul por toda su colaboración y en especial a don Carlos Piceno y a toda su familia por el
apoyo logístico brindado durante el trabajo de campo, por su amabilidad, y por su
entrañable amistad.

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Dedicatoria
Esta tesis está dedicada al maestro de maestros, Charles Darwin (1809-1882), ese hombre
que demostró que cuando se combinan con pasión el intelecto, el raciocinio, y el método
científico es posible “transformar” el mundo (o al menos una parte de él), es posible
reemplazar las supersticiones milenarias por nuevas realidades fundadas no en los
“dogmas” o en la ignorancia, sino en un arduo proceso de discernimiento y en las
evidencias científicas. Gracias al magnánimo trabajo de Darwin, hoy es posible decir que
quien tenga un conocimiento apropiado del evolucionismo, cuenta con una poderosa
herramienta cognoscitiva para explicar y entender mejor lo que nos rodea, incluyéndonos a
nosotros mismos. A través de sus enseñanzas aprendí a amar con pasión todas las
maravillas del mundo orgánico, aprendí a aceptar mi propia finitud y a comprender que el
ser humano es parte integral de ese fenómeno asombroso e infinitamente complejo que es la
naturaleza. Que descanse en paz el gran maestro pues pese a que el mundo aún no ha
comprendido los alcances de su legado y a la existencia de poderosos grupos religiosos que
han saboteado (y siguen saboteando) la difusión de este conocimiento, Darwin se ha
convertido en la inspiración de muchas generaciones de biólogos alrededor del mundo.
Cierto es que la revolución sin parangón desatada a partir de la publicación del más
importante tratado de biología y evolución jamás escrito, Origin of Species by Means of
Natural Selection (1859), aún está lejos de terminar, pero muchos biólogos alrededor del
mundo seguiremos difundiendo con pasión y valentía los conocimientos sobre la selección
natural y demás mecanismos que gobiernan los procesos evolutivos ¿Y por qué tomarse
semejante molestia? Porque al contrario de las “falacias sagradas” difundidas por los
fundamentalistas religiosos y otros mercaderes de ilusiones, el evolucionismo cuenta con
una sólida base científica que nos permite aproximarnos a la “verdad” sobre el mundo
orgánico y sobre nosotros mismos. Por tanto, es nuestra responsabilidad ética luchar para
que estos conocimientos científicos lleguen a todos los rincones de nuestras sociedades, es
nuestra responsabilidad contribuir a demoler las supersticiones que limitan el desarrollo
cognoscitivo del ser humano y por ende, que mutilan su capacidad de raciocinio.

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Índice
Resumen general ……………………………………………………………....................... 6
Abstract ................................................................................................................................. 8
Introducción general ............................................................................................................ 10
Objetivo general ...................................................................................................... 19
Objetivos específicos ............................................................................................... 19
Predicciones ............................................................................................................. 21
Área de estudio .................................................................................................................... 23
Sitios de estudio .................................................................................................................. 24
Especies de primates en el área de estudio .......................................................................... 28
Referencias .......................................................................................................................... 29
Capítulo I
Differences in Diet Between Spider Monkeys Groups Living in Forest Fragments and
Continuous Forest in Lacandona, Mexico ...................................................................... 38
(Aceptado con cambios menores en Biotropica en fecha: 10/3/2010)
Capítulo II
Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in
Continuous and Fragmented Rainforests in Southern Mexico ..................................... 74
(Aceptado en International Journal of Primatology en fecha: 24/05/2010)

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Capítulo III
Seasonal Differences and Shifts in Activity Patterns of Spider Monkeys Living in
Forest Fragments in Southern Mexico .......................................................................... 119
(Aceptado con cambios mayores en International Journal of Primatology en fecha:
15/3/2010)
Capítulo IV
Absence of spider monkeys in small forest fragments affects the composition of
seedlings in Southern Mexico.......................................................................................... 152
(Manuscrito en preparación, será sometido en Biological Conservation)
Discusión general .............................................................................................................. 193
Conclusiones generales ..................................................................................................... 202
Referencias generales (para discusión y conclusiones generales) .................................... 205
Anexo ................................................................................................................................ 210

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Resumen general
La dispersión de semillas por vertebrados es un proceso fundamental en la determinación
de la estructura y dinámica de las poblaciones de plantas, y por tanto en la regeneración del
bosque. En el caso de las zonas tropicales, los primates representan alrededor del 50% de la
biomasa de frugívoros y diversos estudios sugieren que son dispersores altamente
eficientes. Sin embargo, la mayoría de estos estudios han sido llevados a cabo únicamente
en bosques continuos y se han enfocado en el estudio de aspectos descriptivos de la dieta y
la dispersión de semillas (e.g., cantidad de semillas dispersadas, patrón de defecación) por
primates folívoro-frugívoros de poca movilidad. Hasta la fecha son sumamente escasos los
estudios que evalúen simultáneamente en bosque continuo y en fragmentos boscosos el
comportamiento alimenticio de los primates frugívoros, así como su eficiencia en la
dispersión de semillas, sus patrones de actividad y los efectos potenciales que tendría su
desaparición sobre la regeneración del bosque. En el presente trabajo estudié durante 15
meses todos estos aspectos realizando observaciones de individuos focales en tres grupos
de monos araña (Ateles geoffroyi) en la Reserva de la Biósfera Montes Azules, y otros tres
grupos de monos en fragmentos boscosos del municipio de Marqués de Comillas, Chiapas.
En el primer capítulo de la tesis: “Differences in Diet Between Spider Monkeys Groups
Living in Forest Fragments and Continuous Forest in Lacandona, Mexico”, evalué si las
diferencias en la dieta del mono araña en ambos tipos de hábitat estaban relacionadas con
diferencias en la estructura de la vegetación y la disponibilidad de alimento. En general, los
fragmentos presentaron una menor disponibilidad de especies de frutos para los monos en
comparación con el bosque. Como resultado, en fragmentos los monos incrementaron el
tiempo dedicado al consumo de hojas y frutos inmaduros, e incrementaron el tiempo
dedicado al consumo de partes vegetales de hemiepífitas y palmas. En el segundo capítulo:
“Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in
Continuous and Fragmented Rainforests in Southern Mexico”, comparé la manipulación de
frutos y semillas, los patrones de defecación, la composición de las semillas defecadas, y la
proporción de semillas defecadas en condición intacta en bosque continuo y en fragmentos,
así como el efecto general del tracto digestivo sobre la germinación de las semillas. La
eficiencia de los monos como dispersores fue mayor en el bosque continuo que en los
fragmentos, ya que en los fragmentos: (1) se redujo la proporción de semillas tragadas y se

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incrementó la de semillas arrojadas bajo el parental, y (2) se redujo la proporción de
excretas que contenían semillas. No obstante, la proporción de semillas defecadas en
condición intacta fue igualmente alta en ambos tipos de hábitat (> 86%) y en las cinco
especies analizadas, el paso por el tracto digestivo favoreció la germinación. En el tercer
capítulo: “Seasonal Differences and Shifts in Activity Patterns of Spider Monkeys Living
in Forest Fragments in Southern Mexico”, evalué la influencia de la reducción de recursos
alimenticios en fragmentos y durante la estación seca sobre la cantidad de tiempo dedicado
a la alimentación, al descanso y a la locomoción. En fragmentos el mono invirtió más
tiempo en alimentación y menos en locomoción que en boque continuo. Por otro lado,
como respuestas a las condiciones imperantes en la estación seca, el mono redujo el tiempo
de alimentación e incrementó el tiempo de descanso. Estos resultados sugieren que el mono
araña es capaz de lidiar con la limitación espacial y estacional de recursos a través de
ajustes conductuales que minimizan los gastos energéticos. Sin embargo, desconocemos si
esta flexibilidad conductual es suficiente como para permitir la sobrevivencia del mono
araña a largo plazo, particularmente en los fragmentos. Finalmente, en el cuarto capítulo:
“Absence of spider monkeys in small forest fragments affects the composition of seedlings
in Southern Mexico”, evalué la hipótesis de que la ausencia de los monos araña en
fragmentos priva a las especies con semilla grande de sus dispersores eficientes, lo cual se
traduce en un menor reclutamiento de este tipo de plántulas en comparación con bosques
que presentan monos araña. Para esto, durante 16 meses realicé muestreos del
reclutamiento de plántulas en tres áreas de bosque continuo, tres fragmentos con monos y
tres fragmentos sin monos. Clasifiqué las plántulas en tres categorías de dispersión:
dispersadas por primates, dispersadas por vertebrados pequeños, y dispersadas por medios
abióticos (viento y gravedad). Los resultados indicaron que la ausencia del mono araña
alteró la composición de plántulas, reduciendo la abundancia y riqueza de especies de
semilla grande y favoreciendo tanto la riqueza de especies dispersadas por vertebrados
pequeños como la abundancia de especies dispersadas por medios abióticos. Sin embargo,
para tener un panorama más claro sobre la contribución del mono araña a la regeneración
del bosque y sobre su capacidad para sobrevivir a la limitación espacial y estacional de
recursos es crucial realizar más estudios que evalúen estos aspectos en otros bosques
continuos y fragmentados de Mesoamerica.

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Abstract
Animal seed dispersal may affect the distribution and structure of vegetation, and has
crucial implications for forest regeneration. In tropical areas, primates represent ca. 50% of
the frugivore biomass and several studies suggest that they have a diverse diet, are efficient
seed dispersers, and can make important behavioral adjustments in response to
environmental stresses. However, most of these studies have focused on isolated
descriptive aspects of their diet and feeding behavior, and activity patterns. Furthermore,
most have focused only on a small group of more folivorous primates. Studies evaluating
feeding behavior, seed dispersal efficiency, and activity budgets of highly frugivorous
primates in continuous and fragmented forests are extremely scarce, and the potential
effects of their disappearance on seedling recruitment dynamics has not been evaluated. In
this work, I evaluated these aspects in the largest Mesoamerican frugivorous primate –
spider monkeys (Ateles geoffroyi) –using focal observations from six monkey groups living
in continuous and fragmented forests of the Selva Lacandona rainforest, Chiapas, southern
Mexico. In the first chapter of this thesis: “Differences in Diet Between Spider Monkeys
Groups Living in Forest Fragments and Continuous Forest in Lacandona, Mexico”, I
evaluated the feeding behavior in three sites of continuous forest and three forest fragments,
and relate differences in diet to differences in composition and structure of vegetation
between habitats. Overall, I found that in response to food scarcity in fragments, spider
monkeys diversified their overall diet and increased the consumption of fallback foods
(e.g., leaves) in comparison with the continuous forest. In the second chapter:
“Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in
Continuous and Fragmented Rainforests in Southern Mexico”, I determined the efficiency
of spider monkeys as primary seed dispersers in quantitative and qualitative terms and if
this interaction is altered in forest fragments. My results indicate that efficiency of spider
monkeys as seed dispersers may be limited in fragments as a consequence of changes in
seed handling and a reduction of the percentage of feces with seeds. However, the number
of defecated seed species was similar between habitats and in both cases most seeds (>
86%) were undamaged. Similarly, defecated seeds showed greater germination percentages
than control seeds in all of the five plant species evaluated. In the third chapter: “Seasonal
Differences and Shifts in Activity Patterns of Spider Monkeys Living in Forest Fragments

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in Southern Mexico”, I evaluated the influence of food resource scarcity in fragments and
during the dry season on activity patterns of spider monkeys. Overall, in fragments the
monkeys increased the time devoted to feeding and reduced the time devoted to traveling in
comparison with continuous forest. Furthermore, in response to high temperature and food
scarcity in the dry season monkeys reduced their time devoted to feeding and increased
their time devoted to resting. Although these findings confirm that spider monkeys are able
to make behavioral shifts in order to deal with fruit scarcity in Lacandona, further studies
are necessary to assess if these behavioral changes are adequate to assure their health,
fitness, and most importantly, their long-term persistence in fragmented and seasonal
habitats. Finally, in chapter IV: “Absence of spider monkeys in small forest fragments
affects the composition of seedlings in Southern Mexico”, I address the hypothesis that in
forest fragments the lack of spider monkeys (Ateles geoffroyi) deprive large-seeded plants
of efficient dispersers and hence limit community-wide recruitment of primate-dispersed
species in comparison with forests containing monkeys. For this, during a 16-moths period
I carried out samplings of seedling recruitment in three areas of continuous forest, three
fragments with monkeys and three fragments without monkeys. I classified the seedling
species into four categories according to their dispersal mode: primate-dispersed species
(seeds >1.5 cm), small and medium vertebrate-dispersed species, wind-dispersed species,
and gravity-dispersed species. Overall, my results suggest that the disappearance of spider
monkeys could ultimately affect tree composition, reducing both the abundance and
richness of large-seed species, and favoring small and medium seed-size vertebrate-
dispersed species and abiotic-dispersed species. Nevertheless, to improve our
understanding about the relative contribution of spider monkeys to forest regeneration and
their behavioral responses to environmental stresses imposed by fragmentation and
seasonality, more studies evaluating these and other important factors in populations of
monkeys living in continuous and fragmented forests of Mesoamerica are crucial.

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INTRODUCCIÓN GENERAL
Importancia de los dispersores de semillas
La relación mutualística entre las plantas y sus dispersores animales representa una
de las interacciones más ampliamente distribuidas en el mundo. Por ejemplo, a nivel
global, la dispersión por animales se presenta en el 64% de las familias de gimnospermas y
en un 46% del total de especies de este mismo grupo; mientras que otro 39% de especies
son dispersadas tanto por medios bióticos como abióticos (Herrera 1989). En el caso
particular de la dispersión de semillas por vertebrados, se estima que oscila entre 70 y 94%
en las plantas leñosas de los bosques neotropicales, entre 82 y 88% en los bosques lluviosos
de Australia, entre 50 y 70% en algunos bosques tropicales secos y, entre 30 y 40% en los
bosques de coníferas de las zonas templadas (Jordano 2000).
Entre los principales factores ecológicos que favorecen la dispersión por vertebrados
sobresalen cinco. Primero, el escape de la alta mortalidad de semillas y plántulas cerca de
parentales y conespecíficos debido a la acción densodependiente de los enemigos naturales
(Jazen 1970, Connell 1971). Segundo, la colonización de sitios distantes (Howe & Miriti
2004), lo cual puede repercutir directamente en la distribución geográfica de las plantas.
Tercero, el escape de la competencia intraespecífica (e.g., autosombreo, competencia por
agua y nutrientes del suelo) entre individuos emparentados (Willson & Traveset 2000).
Cuarto, la dispersión directa de las semillas por animales que las defecan en sitios
específicos que favorecen su germinación y establecimiento (e.g., aves: Wenny & Levey
1998, Wenny 2001). Finalmente, los efectos de desinhibición, escarificación y fertilización
que tiene el paso de las semillas por el tracto digestivo y la defecación comúnmente
favorecen la germinación (Robertson et al. 2006). Cualquiera de estos factores que esté

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actuando, podría aumentar la probabilidad de que las semillas y las plántulas sobrevivan
hasta la etapa adulta, en comparación con las semillas que no han sido dispersadas (Howe
& Miriti 2004). Por tanto, no es casualidad que la mayoría de los árboles tropicales
produzcan frutos adaptados para el consumo y la dispersión por vertebrados (Tiffney 2004,
Eriksson 2008). No obstante, debido a que las relaciones coevolutivas entre plantas y
dispersores no son estrechas, sino más bien “difusas” (i.e., es una coevolución entre grupos
de organismos y no entre pares: Herrera 1985), la desaparición de un dispersor rara vez
traerá como consecuencia la extinción de las especies de plantas que produce sus frutos
preferidos (o viceversa). Pese a esto, existe evidencia que indica que la desaparición de los
dispersores eficientes puede reducir considerablemente el flujo génico y alterar la
composición del banco de plántulas, especialmente en el caso de especies con semilla
grande, como se explicará más adelante para el caso de algunos primates frugívoros como
el mono araña (Ateles spp.).
Eficiencia en la dispersión de semillas
Desde la perspectiva de la planta, lo importante no es tanto la cantidad de
dispersores, sino, la eficiencia con que éstos dispersen sus semillas, lo cual afecta
directamente los patrones de reclutamiento y regeneración de los bosques tropicales
(Cordeiro et al. 2009). En términos generales la eficiencia de un dispersor depende dos
componentes principales: (1) la cantidad de semillas dispersadas, que es una función del
número de visitas realizadas y el número de semillas defecadas en cada visita, y (2) la
calidad de la dispersión (i.e., la probabilidad de que las semillas sean defecadas en
condición intacta en sitios apropiados para su germinación y establecimiento) (Schupp
1993, Jordano & Schupp 2000). Ambos componentes son afectados por el tipo de

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manipulación de los frutos y semillas, lo cual depende tanto de las características
morfológicas del fruto y las semillas, como de las características conductuales y
morfológicas del dispersor (Jordano 2000, Izhaki 2002). Debido a esto, se presenta un
continum en la eficiencia de dispersión (Jordano 2000), de modo que un mismo dispersor
puede comportarse algunas veces como depredador de semillas y otras como verdadero
dispersor, con múltiples grados de eficiencia.
El componente cuantitativo es relativamente fácil de comparar y ha sido objeto de
numerosos estudios alrededor del mundo (e.g., Howe & Smallwood 1982, Garber 1986,
Levey et al. 1994, Lobova et al. 2009). En cuanto a la calidad de dispersión la mayoría de
estudios realizados hasta la fecha se han centrado en describir y/o cuantificar la selección y
manipulación de los frutos y semillas (Jordano 2000, Stevenson 2004), el efecto del paso de
las semillas por el tracto digestivo (Stevenson 2000, Robertson et al. 2006), los patrones de
deposición (Wehncke et al. 2004, McConkey & Chivers 2007) y la distancia de dispersión
(Link & Di Fiore 2006, Levey et al. 2008). No obstante, son muy escasos los estudios que
han considerado simultáneamente ambos componentes de la eficiencia y aún menos los que
han evaluado cómo ésta se puede ver afectada por diferentes presiones antropogénicas (e.g.,
fragmentación).
Fragmentación y el papel de los primates en la regeneración de los bosques tropicales
En las zonas tropicales, millones de hectáreas de bosque son convertidas en campos
agrícolas y pastizales cada año. Por ejemplo, sólo durante la década de 1981 a 1990, en los
Neotrópicos se perdieron 74 millones de hectáreas de bosque a una tasa de deforestación
anual del 0.75% (Whitmore 1997). En América Latina (excluyendo México y la selva
Atlántica de Brasil), durante el período de 1990-1997 esta tasa fue del 0.38%, siendo

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superada únicamente por la de las zonas tropicales de África y del Sudeste de Asia (Achard
et al. 2002). En los paisajes fragmentados resultantes, la reducción en la diversidad de
hábitats a nivel local y del área total de hábitat disponible, propicia la extinción de muchas
especies de flora y fauna (Burkey & Reed 2006, Watlin & Donnelly 2006). Esta situación
es especialmente grave en el caso de México, ya que después de Indonesia, Nueva Guinea y
Brasil es el cuarto país con mayor deforestación a nivel mundial, y sólo durante el período
2000-2005 se perdieron 1.3 millones de hectáreas de bosque (FAO 2007). Para revertir esta
situación y establecer estrategias de conservación apropiadas, es prioritario realizar estudios
más profundos sobre la contribución relativa de las diferentes especies de dispersores en la
regeneración de los hábitats fragmentados.
En este sentido, los primates representan uno de los grupos de dispersores primarios
más importantes en los bosques tropicales (Stevenson 2000, Peres & van Roosmalen 2002,
Chapman & Russo 2006, Stevenson & Aldana 2008), y se ha comprobado que en conjunto
pueden movilizar el doble del total de semillas dispersadas por las aves (Clark et al. 2001).
De acuerdo con Sussman (1991), la gran diversificación evolutiva de las angiospermas en
los trópicos está estrechamente asociada con la evolución de los primates frugívoros, hace
unos 65 millones de años (Milton 1993). Sin embargo, no todos los primates son
igualmente eficientes como dispersores de semillas y, por tanto, su contribución relativa a
la regeneración del bosque puede variar considerablemente. Por ejemplo, algunos primates
actúan principalmente como depredadores, y son capaces de masticar y digerir las semillas
(e.g., Propithecus diadema; Overdorff & Strait 1998). Otros primates pueden actuar ya sea
como depredadores de semillas o como dispersores para una misma especie de planta (e.g.,
Papio anubis; Kunz & Linsenmair 2007). Finalmente, muchos primates en el Paleotrópico
(e.g., Gorilla gorilla: Voysey et al. 1999; Pan troglodytes, Cercopithecus ascanius:

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Lambert 1998; Hylobates muelleri: McConkey & Chivers 2007) y en el Neotrópico (e.g.,
Ateles spp: Chapman 1989, Dew 2008; Lagothrix lagotricha: Stevenson 2000, 2007; Cebus
capucinus: Wehncke et al. 2003) funcionan como dispersores especializados, y son capaces
de tragar, defecar en condición intacta, y dispersar a una distancia considerable (> 100 m)
las semillas de muchas especies de plantas. Esto pese al costo energético que representa
para el animal acarrear en su estómago grandes volúmenes de semillas que limitan la
cantidad total de alimento que puede ingerir a lo largo del día.
En el Neotrópico la mayoría de estos estudios, se han enfocado en un pequeño
grupo de primates que habitan en bosques continuos y se han evaluado solamente algunos
aspectos aislados de la ecología alimenticia (diversidad dietética: Nunes 1998, Pinto & Setz
2004, Cristóbal-Azkarate & Arroyo-Rodríguez 2007; variación estacional en la dieta:
Hemingway & Bynum 2005); y de la eficiencia de dispersión (e.g., selección de frutos:
Stevenson 2004, Martins 2008, Stevenson & Link 2010; cantidad de semillas dispersadas:
Link & Di Fiore 2006). Además, la contribución relativa de los primates frugívoros a la
regeneración de la comunidad vegetal en fragmentos y en bosques continuos es un tema
que permanece prácticamente inexplorado (pero ver Stevenson & Aldana 2008).
Pese a lo anterior, la evidencia disponible sugiere que la eficiencia de los primates
neotropicales como dispersores es muy variable en términos del porcentaje de frutos en la
dieta, el número de semillas en las excretas, el patrón de defecación y el efecto del tracto
digestivo sobre la germinación. Por ejemplo, el porcentaje de frugivoría puede variar entre
un 2% (Alouatta seniculus: Orihuela-López et al. 2005) y un 87% (Ateles belzebuth: Dew
2008). La diversidad de semillas en las excretas varía de 9 especies (A. palliata: Wehncke
et al. 2004) hasta133 especies (Ateles belzebuth: Link & Di Fiore 2006). De igual forma, el
patrón de defecación en algunos casos puede ser agregado (e.g., Alouatta seniculus:

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Andresen 2002) y en otros es espaciado (e.g., Cebus capucinus: Wehncke et al. 2004,
Ateles belzebuth: Di Fiore et al. 2008). Finalmente, se han encontrado efectos variables del
tracto digestivo sobre la germinación de las semillas, pero en términos generales prevalecen
los efectos positivos (e.g., en el 75% de especies defecadas por Alouatta guariba: Martins
2006; y en el 56% de las defecadas por Cebus capucinus: Wehncke & Dalling 2005).
Los servicios ecológicos brindados por los primates frugívoros (e.g., Ateles spp.)
pueden tener considerables repercusiones a nivel de conservación. Por ejemplo, éstos
podrían ser importantes aliados para lograr la regeneración y el mantenimiento de
ecosistemas severamente fragmentados, como es el caso de la gran mayoría de bosques
tropicales (FAO 2007). Diversos estudios con poblaciones de primates frugívoros en
fragmentos y bosques continuos de África, indican que estos animales contribuyen
activamente a la regeneración de los parches boscosos puesto que facilitan el flujo de
semillas entre parches (Onderdonk & Chapman 2000, Chapman et al. 2007). En
Sudamérica se ha encontrado que el reclutamiento de las especies con semilla grande (>1
cm de diámetro) en bosques con o sin presiones de cacería, depende principalmente de un
pequeño grupo de dispersores como Ateles, Alouatta y Lagothrix (Julliot 1997, Peres &
van Roosmalen 2002, Nuñez-Iturri & Howe 2007, Nuñez-Iturri et al. 2008). Así, se ha
demostrado que la desaparición de especies de primates frugívoros como Ateles belzebuth y
L. lagotricha afecta negativamente el reclutamiento y la abundancia de especies de semilla
grande en el bosque tropical húmedo de La Macarena, Colombia (Stevenson & Aldana
2008). Un patrón similar también se ha observado para fragmentos boscosos de la Selva
Lacandona, México, en los que ha desaparecido Alouatta prigra (A. González-Di Pierro et
al. datos no publicados). Todo esto sugiere que la eventual desaparición o reducción de las
poblaciones de los primates, acarrearía profundos cambios en las tasas de reclutamiento de

16
plántulas y por ende, en la estructura y la composición de las futuras comunidades de
plantas.
Escasez de recursos y cambios conductuales en los primates
La escasez espacial y temporal de recursos alimenticios puede alterar
considerablemente el comportamiento de muchas especies de primates (Jones 2005). Por
ejemplo, la diversidad y abundancia de especies de árboles que producen frutos carnosos
importantes en la dieta de los primates frecuentemente es menor en fragmentos (Onderdonk
& Chapman 2000, Arroyo-Rodríguez et al. 2007) y durante la estación seca (Chapman
1987, Hemingway & Bynum 2005). Entre los principales ajustes adaptativos que pueden
realizar los primates en respuesta a la escasez de alimento y/o condiciones climáticas
adversas se encuentran: (1) diversicar la dieta incluyendo un mayor consumo de partes
vegetales de bejucos, arbutos y palmas (e.g., Onderdonk & Chapman 2000, Cristóbal-
Azkarate & Arroyo-Rodríguez 2007), (2) compensar la menor disponibilidad de frutos con
un mayor consumo de material foliar (Onderdonk & Chapman 2000, Hemingway &
Bynum 2005, González-Zamora et al. 2009), y (3) reducir el tiempo invertido en
actividades energéticamente costosas como la locomoción mientras que incrementan el
tiempo dedicado al descanso (Campos & Fedigan 2009, Korstjens et al. 2010). En este
último caso, los primates se ven forzados a descansar más tiempo debido a que es una
demanda fisiólogica de una dieta más folívora (Milton 1981, Lambert 1998).
En el caso particular de los primates frugívoros, los ajustes conductuales anteriores
se podrían traducir en un menor nivel de frugivoría (e.g., C. capucinus, Ateles geoffroyi:
Chapman 1987, A. chamek: Wallace 2008), lo cual afectaría directamente la cantidad y
diversidad de semillas defecadas, y por ende, la composición del banco del plántulas, tal y

17
como se mencionó anteriormente en el caso de A. belzebuth y L. lagotricha. Además, se ha
reportado que la menor calidad y abundancia de recursos alimenticios en fragmentos y el
aumento de la temperatura durante la estación seca, puede obligar a ciertos primates
frugívoros a incrementar el tiempo dedicado a la alimentación para obtener suficientes
nutrientes del material foliar, lo cual también puede alterar el tiempo dedicado a la
locomoción y al descanso (e.g., Papio spp.: Dunbar 1992; A. geoffroyi Korstjens et al.
2010).
Importancia de Ateles geoffroyi como dispersor de semillas
El mono araña (Ateles geoffroyi) es uno de los más importantes dispersores de
semillas del Neotrópico debido a su alto nivel de frugivoría y a la diversidad de frutos que
consumen (Russo et al. 2005, González-Zamora et al. 2009). La evidencia disponible
indica que los monos araña son dispersores importantes para la regeneración de las
comunidades de plantas. Por ejemplo, Ateles spp. es capaz de ingerir semillas hasta de 5 cm
(Peres 1994), y de dispersar miles de semillas de cientos de especies (van Roosmalen 1985,
Link & Di Fiore 2006, Dew 2008), por distancias > 100 m (Suarez 2006, Di Fiore &
Campbell 2007). En la Isla Barro Colorado, Panamá y en diferentes países de Sudamérica,
Ateles spp. dispersa semillas de más de 100 especies de plantas distribuidas en unos 59
géneros (Campbell 2000, Russo et al. 2005, Dew 2008). A través de Mesoamérica, A.
geoffroyi se alimenta de 364 especies de plantas de 76 familias (González-Zamora et al.
2009) y es un importante dispersor de diferentes especies de Brosimum, Bursera, Ficus,
Poulsenia, Pouteria, Spondias y Virola entre otras (Estrada et al. 2004a, Russo et al. 2005,
González-Zamora et al. 2009).

18
Sin embargo, a lo largo de la distribución geográfica de A. geoffroyi, las investigaciones
realizadas se han enfocado en aspectos como la filogenia (Collins & Dubach 2000, Collins
2008), la demografía (Cant 1978, Estrada et al. 2002, 2004a), la conducta y la estructura
social (Riba-Hernández et al. 2005, Ramos-Fernández et al. 2006, 2009), la fisiología
(Milton 1981, Laska et al. 2006, Rangel-Negrín et al. 2009), y la dieta en bosques
continuos (Di Fiore et al. 2008, González-Zamora et al. 2009). Pero los estudios sobre su
dieta en hábitats contrastantes (e.g., bosques continuo y fragmentos boscosos), su función
en la dispersión de semillas, su capacidad para realizar ajustes en los patrones de actividad
en respuesta a la escasez de alimento, y sobre el efecto que pueda tener en la composición
del banco del plántulas en hábitats alterados (e.g., fragmentos boscosos de diferentes
tamaños) están prácticamente ausentes. La ausencia de estos estudios es evidente en el caso
de México, ya que A. geoffroyi ha sido considerablemente menos estudiado que las dos
especies de Alouatta (A. palliata y A. pigra), y el 90% del total de investigaciones sobre
esta especie (44% de las cuales se han realizado en cautiverio) se han enfocado en aspectos
ecológicos y demográficos (Estrada & Mandujano 2003, Estrada et al. 2004a,b), en la dieta
(ver González-Zamora et al. 2009), en la estructura social (Ramos-Fernández et al. 2009) y
más recientemente, en el efecto de su ausencia sobre el reclutamiento de algunas especies
de semilla grande (e.g., Manilkara zapota: Gutiérrez-Granados & Dirzo 2010).
Esta información es de gran importancia para: (1) entender mejor las interacciones
entre los monos araña y las plantas de las que se alimenta, (2) mejorar nuestro
conocimiento sobre la contribución de esta especie (y otros primates frugívoros) a la
regeneración de la selva, y (3) dilucidar cuáles son los mecanismos que le permiten a esta
especie lidiar con el estrés ambiental en fragmentos y durante la estación seca. En el
contexto de ecosistemas altamente degradados, como en el caso de ciertas regiones de la

19
Selva Lacandona (ver Mendoza & Dirzo 1999), la información que se presenta en los
cuatro capítulos de esta tesis contribuirá a mejorar nuestro conocimiento sobre la ecología
de A. geofroyi en bosque continuo y en fragmentos y, en particular, al entendimiento de los
factores bióticos y abióticos que afectan la regeneración del bosque y la sobrevivencia de
frugívoros críticamente amenazados, como es el caso de los monos araña.
Objetivo general
Determinar la contribución relativa de A. geoffroyi vellerosus a la regeneración de
las comunidades de plantas presentes en un bosque continuo y en fragmentos de bosque en
la Selva Lacandona, y su capacidad para realizar cambios conductuales que le permitan
lidiar con la menor disponibilidad de frutos en fragmentos y durante la estación seca.
Objetivos específicos
Capítulo I.
1) Someter a prueba la hipótesis de que los cambios en la disponibilidad de alimento
entre fragmentos y bosque continuo resultan en cambios en la dieta de las
comunidades de monos araña en ambos tipos de hábitat.
2) Determinar la diversidad de la dieta en bosque continuo y en fragmentos.
3) Determinar cuáles son las especies de plantas, módulos vegetales, y formas de
crecimiento más importantes en la dieta del mono araña en ambos hábitats.
4) Evaluar la relación de la variación en la dieta con cambios en la disponibilidad de
alimento en ambos hábitat.

20
Capítulo II
1) Someter a prueba la hipótesis de que A. geoffroyi es un dispersor eficiente tanto en
bosque continuo como en fragmentos.
2) Evaluar cómo varía la eficiencia como dispersor del mono araña en bosque continuo
y en fragmentos.
3) Determinar el tipo de manipulación de las semillas de las especies más importantes
en la dieta en bosque continuo y fragmentos.
4) Determinar el patrón de defecación y la diversidad y condición de las semillas
defecadas en ambos hábitats.
5) Determinar el efecto del tracto digestivo sobre el porcentaje de germinación de las
semillas.
Capítulo III
1) Someter a prueba la hipótesis de que para lidiar con la limitación de alimento en
fragmentos y durante la estación seca, los monos araña son capaces de de ajustar el
tiempo que invierten en sus actividades vitales (i.e., alimentación, descaso y
locomoción) para minimizar los costos energéticos de las mismas.
2) Determinar el efecto del hábitat (continuo y fragmentado), la estación (seca y
lluviosa) y la interacción entre ambos factores sobre los patrones de actividad del
mono araña.
3) Discutir los resultados en relación con las variaciones en la dieta de estos mismos
grupos de monos descrita en el capítulo I, así como las implicaciones que podría
tener la flexibilidad conductual de esta especie para la conservación.

21
Capítulo IV
1) Someter a prueba la hipótesis de que la desaparición de monos araña en fragmentos
altera la composición de plántulas, limitando el reclutamiento de las especies con
semilla grande (>1.5 cm de diámetro).
2) Comparar la abundancia, riqueza, y diversidad de plántulas de acuerdo con su
mecanismo de dispersión (i.e., si son dispersadas por primates, por mamíferos
pequeños, o por medios abióticos) en bosque continuo, fragmentos con monos y
fragmentos sin monos.
3) Determinar el efecto relativo de la abundancia de monos araña, la riqueza de
frugívoros grandes, la composición de árboles adultos y las características de los
fragmentos sobre los patrones observados.
Predicciones
Capítulo I
1) Debido a que en los fragmentos existe una menor disponibilidad de árboles grandes
que producen frutos importantes en la dieta de A. geoffroyi en comparación con el
bosque continuo, los monos se verán obligados a diversificar su dieta y a consumir
más material foliar.
2) En ambos hábitats, la mayor parte del tiempo de alimentación estará enfocado en un
pequeño grupo de especies pertenecientes a las familias Anacardiacae, Fabaceae y
Moraceae, entre otras, tal y como se ha reportado para otras comunidades de monos
araña en Mesoamérica (González-Zamora et al. 2009).

22
Capítulo II
1) Debido a los hábitos frugívoros del mono araña, a su capacidad para tragar semillas
grandes, a su alta movilidad, y a su patrón de defecación espaciado (Peres 1994,
Russo et al. 2005, Di Fiore et al. 2008), se espera que sean dispersores eficientes en
términos cuantitativos y cualitativos en boque continuo y en fragmentos.
2) Debido a que en fragmentos la disponibilidad de frutos para los monos
frecuentemente es menor que en bosque continuo (Arroyo-Rodríguez et al. 2007),
se espera que en fragmentos los monos traguen menos semillas, y que sea menor el
número de especies de semillas defecadas y el número de excretas sin semillas.
Capítulo III
1) Para compensar la menor abundancia y calidad de alimento en los fragmentos y
durante la estación seca en comparación en el bosque continuo y en la estación
lluviosa, los monos dedicarán más tiempo a la alimentación.
2) Debido a que en fragmentos y durante la estación seca muchos primates optan por
aumentar el consumo de material foliar (Onderdonk & Chapman 2000, Hemingway
& Bynum 2005), los monos araña invertirán más tiempo en descanso para poder
digerir este material.
3) Los monos araña invertirán menos tiempo en actividades energéticamente costosas
como la alimentación y la locomoción (Suarez 2006, Campos & Fedigan 2009) en
la época seca que en la época lluviosa.

23
Capítulo IV
1) En fragmentos sin monos araña, la composición de plántulas será distinta a la de los
fragmentos con monos y el bosque continuo. Específicamente, en fragmentos sin
monos serán más abundantes las especies dispersadas por medios abióticos y menos
abundantes las especies dispersadas por primates, en comparación con los otros dos
hábitats.
2) Las especies más afectadas por la ausencia del mono araña serán las de semilla
grande (>1.5 cm de largo), ya que como se mencionó arriba, entre más grande es la
semilla, más reducido es el gremio de dispersores potenciales que pueden ingerirlas
(Jordano 2000).
3) La composición de plántulas en cada hábitat estará explicada principalmente por la
presencia de monos araña.
Área de estudio
Esta investigación se llevó a cabo durante un período de 17 meses (enero-junio y agosto-
noviembre del 2007, y febrero-mayo y julio-septiembre de 2008) en la región de la Selva
Lacandona, Chiapas, México (16°05'58" N, 90º52'36" W; elevación 10-50 m snm). Esta
zona contiene el bosque tropical lluvioso más grande de Mesoamérica (ca. 300,000 ha) y
comprende bosques de México, Guatemala y Belice (Dirzo 1994). La región es altamente
estacional, y se pueden diferenciar con claridad una estación lluviosa (junio-diciembre) y
una estación seca (enero-mayo). La precipitación promedio anual es 2881mm, la mayor
parte de la cual se concentra en los meses de junio a septiembre (variando de 423 a 511 mm
mes-1). La temperatura promedio anual es 24 °C, variando de 20 a 25 °C/mes en la estación
lluviosa y de 22 a 28 °C/mes durante en la estación seca (Comisión Federal de Electricidad,

24
México, http://app.cfe.gob.mx/Aplicaciones/QCFE/Meteorologico
/WebForms/Bol_Matutino.aspx). La vegetación original está representada por el bosque
lluvioso y el bosque lluvioso semideciduo, con un gradiente altitudinal que varía entre 60 y
2450 msnm (Mendoza & Dirzo 1999).
Desde su colonización en los años 1960, la cobertura forestal original
(aproximadamente 500,000 ha) de la región de la Selva Lacandona en México se ha
reducido en una tercera parte, y actualmente la mayoría de bosques remantes se encuentra
en la Reserva de la Biósfera Montes Azules (Mendoza & Dirzo 1999). En esta zona el
bosque está dominado por plantas perennifolias de bosque lluvioso como Brosimum
alicastrum, Swietenia macrophylla, y Pouteria campechiana. También existen zonas de
bosque ripario con especies como Spondias radlkoferi, Ficus glabrata, y Lonchocarpus
guatemalensis. Además, esta región es de una importancia clave para la conservación, ya
que alberga la mayor diversidad biológica de México, con alrededor del 25% del total de
especies de plantas y animales reportadas hasta la fecha en un área inferior al 1% de la
superficie del país (Medellín 1996). Por ejemplo, existen al menos 4300 especies de plantas
vasculares (Martínez et al. 1994), 112 especies de mamíferos (Medellín 1994), 340
especies de aves y 800 especies de mariposas diurnas (De la Maza & De la Maza 1991).
Sitios de estudio
El estudio se concentró en tres sitios de bosque continuo de la Reserva de la Biósfera
Montes Azules (REBIMA), en tres fragmentos de bosque con A. geoffroyi y en tres
fragmentos de bosque sin A. geoffroyi ubicados en el municipio de Marqués de Comillas
(Fig. 1). Esta última región ha estado sometida a una considerable deforestación desde que
fue colonizada por el ser humano a inicio de los años sesentas (Marquez-Rosano 2006). En

25
general, el tamaño de los grupos de estudio varió entre 35 y 44 individuos. Todos los
fragmentos con y sin monos fueron aislados hace al menos17 años y sus tamaños varían de
6.4 a 1125 ha (Cuadro 1). Tanto en los fragmentos con monos con los fragmentos sin
monos, la distancia al parche boscoso más cercano varía entre 100 m y 450 m (Cuadro 1), y
en la mayoría de los casos están rodeados por una matriz antropogénica mixta, constituida
principalmente por pastizales, plantaciones de cacao y/o especies forestales (e.g., Cedrella
odorata y Swietenia humilis), y por acahuales o bosques secundarios de diferentes edades.
Además, en contraste con el bosque continuo y los fragmentos con monos, en los
fragmentos sin monos la mayoría de frugívoros grandes están ausentes (ver capítulo IV).

26
Fig. 1. Distribución espacial de los sitios de bosque continuo (C1, C2, C3), los fragmentos
con monos (F1, F2, F3) y los fragmentos sin monos (FS1, FS2, FS3). En el Cuadro 1 se
indican las principales características de cada sitio.
F2
F1
Reserva de la Biósfera
Montes Azules Municipio Marqués de Comillas
3.5 km
F3
C1
C2
C3 FS1 FS2
FS3
Río Lacantún

27
Cuadro 1. Descripción de los sitios de estudio en la Selva Lacandona, Chiapas, México.
Sitio
Tamaño
(ha) Localización DF (m)a DB (m)b AFc
Grupod
TDe
Bosque Continuo 331,000 Montes Azules
CF1 ─ 16°06'58.2"N, 90°56'18.4"W ─ ─ ─ 40 ─
CF2 ─ 16°09'32.0"N, 90°54'06.6"W ─ ─ ─ 36 ─
CF3 ─ 16°09'40.0"N, 90°54'04.5"W ─ ─ ─ 44 ─
Fragmentos con monos Marqués de Comillas
F1 14.4
ejido Zamora Pico de Oro
(16°19'52.0"N, 90°51'06.1"W) 450 200 29
35 ─
F2 31
ejido Zamora Pico de Oro
(16°19'24.5"N, 90°50'43.7"W) 150 1200 24
39 ─
F3 1125
ejido Reforma Agraria
(16°15'12.2"N, 90°49'59.5"W) 100 1100 26
41 ─
Fragmentos sin monos Marqués de Comillas
FS1 6.4
ejido Boca de Chajul
(16°06'39.5"N, 90°56'04.6"W) 200 150 25
0 15
FS2 11.4
ejido Boca de Chajul
(16°06'15.7"N, 90°55'34.9"W) 160 1400 25
0 22
FS3 28
ejido Boca de Chajul
(16°06'02.0"N, 90°56'03.7"W) 125 990 17
0 16
aDistancia al fragmento más cercano
bDistancia al bosque continuo
cAños de haber sido fragmentado
d Número de individuos en cada grupo de monos araña (incluyendo adultos, juveniles e infantes)
eTiempo de desaparición de los monos araña (en años)

28
Especies de primates en el área de estudio
En la Selva Lacandona existen dos especies de primates: el mono araña (Ateles
geoffroyi vellerosus Kuhl 1820) y el mono aullador negro (Alouatta pigra). Ateles geoffroyi
está distribuido en bosques continuos y remanentes boscosos de diversos tamaños, desde el
estado de Veracruz, en México, hasta el extremo norte del Chocó, Colombia (Rylands et al.
2006). En México se presentan las subespecies A.g. vellerosus y A.g. yucatanensis (Estrada
et al. 2004a), la primera de las cuales está distribuida en el sureste del país y la segunda se
encuentra restringida a la península de Yucatán (Watts & Rico-Gray 1987). Por su parte,
Alouatta pigra Lawrence 1933 es una especie endémica del sureste de México, Belice y
Guatemala (Rylands et al. 2006). En Montes Azules la densidad poblacional de A. geoffroyi
se ha estimado en 2.9 ind/km2, y para A. pigra ésta se ha estimado en 14.4 ind/km2,
mientras que una estimación cruda de las poblaciones de estas dos especies en un
fragmento grande de Marqués de Comillas (fragmento F3, ver Cuadro 1), indica que en
estos hábitats la densidad es 9.3 y13.3 ind/km2, respectivamente (Estrada et al. 2004b). En
general, los monos aulladores se caracterizan por tener un ámbito hogareño pequeño (1–62
ha: Ostro et al. 1999), una dieta fundamentalmente folívora, y por ser relativamente
tolerantes a la fragmentación (Di Fiore & Campbell 2007). En contraste, los monos araña
presentan un ámbito hogareño más amplio (37–98 ha: Fedigan et al. 1988) y una dieta
especializada en frutos maduros (39 a 82% del tiempo total de alimentación) que combina
con hojas, flores, y madera podrida (González-Zamora et al. 2009). Además, debido a su
preferencia por el bosque conservado, sus amplios requerimientos espaciales, la cacería, y
la pérdida de su hábitat natural, actualmente se encuentran clasificados en la lista roja de
IUCN como especie críticamente amenazada (Ramos-Fernández & Wallace 2008). Debido
a las anteriores características, las poblaciones de monos araña son más vulnerables a la
pérdida de hábitat y la fragmentación del bosque que los monos aulladores (Boyle 2008,
Ramos-Fernández & Wallace 2008).

29
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CAPÍTULO I

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LRH: Chaves, Stoner, and Arroyo-Rodríguez
RRH: Diet of Spider Monkeys in Lacandona
Differences in Diet between Spider Monkey Groups Living in Forest
Fragments and Continuous Forest in Lacandona, Mexico
(accepted with minor corrections 10 March 2010, Biotropica, IF=2.17)
Óscar M. Chaves1, Kathryn E. Stoner, and Víctor Arroyo-Rodríguez
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de Mexico
(UNAM), Antigua Carretera a Pátzcuaro No. 8701, Ex Hacienda de San José de la Huerta,
58190 Morelia, Michoacán, Mexico
1 Corresponding author; e-mail: ochaba@gmail.com
Received_____; revision accepted_____.

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ABSTRACT
Fragmentation can lead to an important reduction in food availability, especially for
some large-bodied tropical mammals such as spider monkeys. Information on species’
behavioral responses to these changes is critical for species conservation; however, little is
known about this topic. During a 15-mo period, we assessed the diet of the largest
Mesoamerican primate species – the spider monkey– in continuous forest and forest
fragments in the Lacandona region of Chiapas, southern Mexico, and related differences in
diet to differences in composition and vegetation structure between forest types. Compared
with the continuous forest, spider monkeys in fragments: (1) diversified their overall diet,
(2) increased consumption of immature and mature leaves, and (3) reduced time feeding on
trees with a consequent increase in time feeding on hemiepiphytes (particularly Ficus spp.)
and palms, both of which were common in fragments. We attribute these differences in diet
to a probable response to food scarcity in fragments, as both the sum of the importance
value index of top food species and the density of large trees were lower in fragments than
in continuous forest. Overall, our findings suggest that spider monkeys are able to adjust
their diet according to food availability in fragments, and thus persist in many small and
medium-sized fragments. We show that some forest fragments harbor high plant diversity,
providing important food sources for spider monkeys. We suggest that these fragments may
function as stepping stones that increase the landscape’s connectivity facilitating inter-
fragment movements and ultimately enhancing seed dispersal.
Key words: food availability; forest fragmentation; dietary flexibility; Neotropical primates.

41
ACCELERATED DEFORESTATION, FRAGMENTATION AND TRANSFORMATION of tropical
rainforests around the world are considered to be the main reasons for the global decline in
animal populations (e.g., butterflies, fish, and mammals: Brook et al. 2003, birds: Sehgal
2010). These threats are particularly important in tropical primates (Cowlishaw & Dunbar
2000, Marsh 2003a), including spider monkeys (Ateles spp.). Owing to their large body,
their large home range requirements (Fedigan et al. 1988), their low fecundity (Campbell &
Gibson 2008), high hunting pressure (Duarte-Quiroga & Estrada 2003) and the drastic
human alteration of their natural habitats (Ramos-Fernández & Wallace 2008), Ateles
geoffroyi could be one of the first Mesoamerican primates to become locally extinct in the
coming decades (Garber et al. 2006). Indeed, as a probable consequence of habitat
fragmentation and disturbance, from the seven subspecies of A. geoffroyi recognized by
Collins & Dubach (2000), six are currently included in the IUCN red list (Vulnerable: A. g.
frontatus; Endangered: A. g. ornatus, A. g. yucatanensis; Critically Endangered: A. g.
panamensis, A. g. geoffroyi, A. g. vellerosus; Cuarón et al. 2008).
One of the most frequent threats posed by forest fragmentation is the reduction in
the food supply for different animal taxa (e.g., birds: Robinson 1998; primates: Arroyo-
Rodríguez et al. 2007). For instance, primates in fragments may face a loss of important
food resources (see Marsh 2003a, Arroyo-Rodríguez & Dias 2009). In smaller fragments,
home range size is usually smaller, limiting the amount of resources available to each group
(e.g., Bicca-Marques 2003, Chapman et al. 2007, Cristóbal-Azkarate & Arroyo-Rodríguez
2007). Additionally, as fragments become smaller, more irregularly shaped, and more
isolated, their floristic composition, plant species diversity, and vegetation structure are
increasingly modified (Hill & Curran 2003, Arroyo-Rodríguez & Mandujano 2009).
Changes in vegetation structure that can reduce food availability to primates in fragments

42
include the loss of large food trees (Arroyo-Rodríguez & Mandujano 2006, Dunn et al.
2009) and the reduction of plant species richness (Norconk & Grafton 2003, Arroyo-
Rodríguez & Mandujano 2009). Since larger trees produce more fruits than smaller ones
(Chapman et al. 1992), the reduction in richness and abundance of large trees could
negatively affect the survival of many tropical primates (e.g., A. palliata: Arroyo-
Rodríguez et al. 2007; Protocolobus pennantii, Colobus guereza: Onderdonk & Chapman
2000), especially in the case of highly frugivoruous monkeys such as Ateles spp. (Di Fiore
et al. 2008, González-Zamora et al. 2009).
Under this scenario, the persistence of primate populations/species in fragments
largely depends on their ability to adjust their diet to food shortage (e.g., Alouatta pigra:
Rivera & Calmé 2006, A. palliata: Dunn et al. 2009, A. seniculus, Ateles paniscus, Cebus
apella: Boyle 2008). Evidence suggests that the success of primates in coping with habitat
fragmentation is related to their capacity to: (1) diversify their diet by feeding from many
different plant species/items, and adjust their diet to the species available in their habitat
(Silver & Marsh 2003, Cristóbal-Azkarate & Arroyo-Rodríguez 2007, González-Zamora et
al. 2009), (2) consume exotic and secondary successional species frequent in disturbed
habitats (Onderdonk & Chapman 2000, Cristóbal-Azkarate & Arroyo-Rodríguez 2007),
and/or (3) rely on some keystone food resources (e.g., Ficus spp.: Cristóbal-Azkarate &
Arroyo-Rodríguez 2007). Without these important feeding adjustments, primates may face
episodes of generalized famine, which can affect their long-term persistence (Milton 1990,
Hanya et al. 2004).
Studies about diet and feeding behavior of atelids are largely focused on more
folivorous species such as howler monkeys (Alouatta spp.) and biased toward continuous
forests (reviewed by Di Fiore & Campbell 2007). Although recent papers have reviewed

43
the diet of spider monkeys throughout their range (Di Fiore et al. 2008, González-Zamora
et al. 2009), little is known about their ability to adjust their diet to food shortage in
fragments. The little available data show that spider monkeys increase the consumption of
leaves in small unprotected forest fragments compared to large protected forests (González-
Zamora et al. 2009), but the potential relationship between their diet shifts and local
structure of vegetation remain unexplored.
We evaluate differences in diet of A. geoffroyi between continuous forest and forest
fragments in the Lacandona rainforest, southeastern Mexico, and relate these differences to
the composition and structure of vegetation within both forest types. In particular, we
evaluate differences in: (1) dietary diversity; (2) top food plant species (i.e., those
comprising > 80% of total feeding time); (3) relative contribution of different plant items
and plant growth forms to the diet; and (4) overlap of plant species in the diet between
habitats. We hypothesized that the changes in food availability for spider monkeys between
fragments and continuous forest result in dietary differences between monkey groups living
in both forest types. We expect that lower structural and compositional diversity of
vegetation in forest fragments will result in a more diverse diet including less nutritious
food items. Assessing the changes in diet of spider monkeys in continuous and fragmented
forests will be critical for the design and establishment of appropriate management
strategies for the conservation of this and many other frugivorous species (Di Fiore et al.
2008)

44
METHODS
STUDY SPECIES.—The black-handed spider monkey (Ateles geoffroyi Kuhl, 1820) is the
largest Mesoamerican primate species, and is distributed from Mexico, throughout most of
Central America to the border of Panama and Colombia (Rylands et al. 2006). Spider
monkeys are characterized by having a highly frugivoruous diet, large home range
requirements, rapid speed of travel, and a fission-fusion social organization in which the
multi-male/multi-female community regularly divides into subgroups of fluctuating size
and composition for foraging (Di Fiore & Campbell 2007).
STUDY AREA AND STUDY SITES.—Fieldwork was conducted in the Lacandona rainforest,
southern Chiapas, Mexico (16°05'58" N, 90º52'36" W; elevation 10–50 m a.s.l.). The study
was conducted in two areas separated by the Lacantún river: the Marqués de Comillas
region (MCR, eastern side of the river), and the Montes Azules Biosphere Reserve (MABR,
western side). Covering parts of Mexico, Guatemala, and Belize, this region encompasses
the largest portion of tropical rainforest in Mesoamerica and one of the most important in
the Neotropics (Dirzo 1994). The original vegetation in the area is tropical wet forest and
semideciduous rainforest. The climate in the region is hot and humid with 24 °C average
temperature and 2881 mm average annual rainfall. The greatest rainfall concentration is
found in June-September (range: 423–511 mm/month), and the lowest in February-April
(46–61 mm/month) (Comisión Federal de Electricidad, Mexico, unpubl. data).
Human colonization of MCR began in the 1960s and 1970s and cattle ranching
resulted in the rapid disappearance and fragmentation of the forest (Mendoza & Dirzo
1999). Approximately 50% of the land surface of MCR is nowadays used for agricultural

45
purposes, but small (0.5–30 ha) and large (850–1500 ha) fragments still remain in the area.
The protected area of MABR was created in 1978 and consists of approximately 300,000
ha of undisturbed forest.
STUDY SITES AND MONKEY GROUPS.—We studied the diet of six groups of spider monkeys:
three independent groups in three different areas of the MABR separated by at least 4 km,
and three groups in three different fragments located in MCR. All fragments in MCR were
isolated ≥ 24 years ago, and their sizes were 14, 31, and 1125 ha (Table S1). Distances
among fragments were ≥ 100 m, and distances from fragments to MABR ranged from 200
to 1400 m. Spider monkeys’ group size ranged from 35 to 44 individuals (Table S1). For
the three study sites of MABR and for the largest fragment, we restricted our data
collection of spider monkey groups to an area of 30–90 ha (according to the home range
recognized a posteriori for each focal group, see Supporting information), whereas for the
other two smaller fragments the entire area was sampled.
DIET.—Diet of spider monkeys was studied during a 15-mo period (6 mo in the dry season:
February-April 2007 and 2008; and 9 mo in the rainy season: May-October 2007, and
August-October 2008). Diet was documented for each of the six focal groups during three
consecutive days once every three weeks, using 5-min focal animal sampling (Altmann
1974). During the follows, spider monkeys were sighted with the aid of visual and auditory
cues (e.g., vocalizations, rustling tree crowns, and dropping branches or fruits) and high
resolution binoculars (Swarovski SLC 10 x 42). Individuals were identified through unique
marks found in skin pigmentation, hair, and other distinguishing marks (i.e., scars). Focal
animals were randomly changed at 5-min intervals or when animals moved out of sight.

46
Data were collected from 0700 h to 1730 h, totaling 1010 h of focal observations (496 h in
continuous forest and 514 h in fragments), from which 448 h (44%) were feeding
observations (205 h in continuous forest and 243 h in fragments).
During feeding we recorded the plant species used (hereafter “food plant species”)
and food item consumed: fruits (mature and immature), leaves (mature and immature),
flowers, young branch piths, decayed wood and other plant items (e.g., terminal stipules,
roots, bulb, and secretions). Plant growth forms were classified as: trees, shrubs, palms,
climbers (vines and lianas), epiphytes, and hemiepiphytes. We report the consumption of
plant species, food items and plant growth forms in terms of percentage of total feeding
time (TFT), that is, time spent consuming each plant species/item/growth form in relation
to the total time spent consuming all plant species/items/growth forms.
DIET OVERLAP.—The annual overlap of fruit and leaves in diet between continuous forest
and fragments was calculated using the Morisita-Horn index: C = 2∑xiyi/(∑ xi2 + yi2), where
xi is the proportion of the fruit/leaves i in the diet of spider monkeys in continuous forest,
and yi is the proportion of the same fruit/leaves in the diet of spider monkeys in fragments.
This index ranges from 0 (no diet overlap) to 1 (complete diet overlap) (Krebs 1999).
VEGETATION ATTRIBUTES AND INDICATORS OF FOOD AVAILABILITY.—A posteriori, we
sampled vegetation within the home range of each group (see Supporting Information)
following the Gentry (1982) protocol. Throughout these areas, we randomly located ten 50
x 2 m transects and identified and measured the diameter at breast height (dbh) of all trees,
shrubs, and palm species (and woody hemiepiphytes whenever possible) with dbh ≥ 10 cm.
We chose this method because it is logistically simple, it is economical (in both time and

47
money), and it is appropriate for the analysis of species diversity in tropical forests (Gentry
1982). Furthermore, since this method has been used to characterize vegetation in several
Neotropical forests, and also to characterize the habitat of other Neotropical primates (e.g.,
Alouatta palliata: Arroyo-Rodríguez & Mandujano 2006, Arroyo-Rodríguez et al. 2007,
Dunn et al. 2009), it is possible to compare our data with other Mexican sites. Plant species
not identified in the field were collected for later identification using the Lacandona seed
reference collection located at the Centro de Investigaciones en Ecosistemas (CIEco,
UNAM, Morelia, Mexico). Plant nomenclature followed the Missouri Botanical Garden
nomenclatural update database (http://mobot.org/W3T/search/vast.html).
We pooled the transect data for each of the 6 sites and treated each one as a unit for
all subsequent analyses. For each site, we quantified species richness, density and basal
area for all plant species. Using data from a recent review of spider monkey diet in
Mesoamerica (González-Zamora et al. 2009), we identified all plant species that constituted
> 80 percent of total feeding time in this review paper and that were present in our study
plots. We considered these species as potential top food species (Table S2) contributing to
resource abundance. Using this information we calculated three indicators of food
availability in continuous and fragmented forests: the total number of food plant species
(excluding lianas and climbers, which were not sampled in the plots), the density of large
trees (> 60 cm in dbh) from top food species, and the sum of the importance value index
(IVI) of top food species. In both continuous and fragmented forests, the IVI was calculated
for each of the top food plant species based on the sum of density (trees/3000 m2),
frequency (number of transects in which each species appeared/30 transects), and
dominance (total basal area for each species in the 3000 m2) (see Arroyo-Rodríguez et al.
2007).

48
STATISTICAL ANALYSIS.— We used generalized linear models (GLM; Crawley 1993) to test
the effect of forest type (continuous or fragmented) on proportion of time consuming each
plant item and each growth form. We constructed the following models: PROPORTION OF
TIME = PLANT ITEM (or PLANT GROWTH FORM) nested in FOREST TYPE + FOREST TYPE.
Proportion data were first arcsine transformed, and we selected a normal distribution with
an identity link-function to the response variable (Crawley 1993). To identify which
treatments were statistically different between each other we used post-hoc analyses with
contrasts (Crawley 1993). To compare the number of food plant species between forest
types (continuous and fragmented) we also used GLM. As suggested for count dependent
variables, we fixed a Poisson distribution and a log-link function to the response variable
(Crawley 1993). We considered each of the three sites per forest type as replicates. The
same procedure also was used to compare the number of food plant species and the density
of large trees (> 60 cm in dbh) from top food species present in each forest type. In the
former case, we previously standardized the sampling effort in each study site to control for
differences in species density using the rarefaction approach. All tests were performed with
JMP software (version 7.0, SAS Institute Inc., Cary, N.C.).
RESULTS
DIET DIVERSITY.—Overall, spider monkeys fed from a total of 121 plant species (and 53
morphospecies) belonging to 96 genera and 39 families. Diet diversity was higher in
fragments (65.7 ± 3.1 species) than in continuous forests (50.3 ± 3.2 species; χ2 = 6.1, df =
1, P = 0.01). This pattern also was observed when comparing the number of top food
species: spider monkeys fed from almost twice as many top food species in fragments (11.7

49
± 2.1 species) than in continuous forest (6.7 ± 0.6 species; χ2 = 4.1, df = 1, P = 0.04) (Table
1).
In both forest types, most top food species were large tree species with fleshy fruits
(Table 1). The families that were most used as food sources in both forest types were
Moraceae, Anacardiaceae, Fabaceae, and Chrysobalanaceae, together representing ca. 77%
of total feeding time (Table 1). Interestingly, monkeys in fragments used more Moraceae
species (7 species) and devoted more time foraging on species from this family (39.1% of
TFT) than in continuous forest (3 species, 11.5% of TFT). In fragments, spider monkeys
exploited more top food species of Ficus (4 species, 25.8% of TFT) than in continuous
forest (2 species, 7.1% of TFT; Table 1). Dialum guianense also was consumed more in
fragments (18.3% of TFT) than in continuous forest (3.8% of TFT). However, Spondias
spp. and Licania platypus were consumed notably more in continuous forest (28.7% and
31.2% of TFT, respectively) than in fragments (12.7% and 4.9%, respectively).
CONSUMPTION OF PLANT ITEMS.—Overall, fruit was the most eaten item (55.6% of TFT, 88
species), followed by leaves (18.5%, 66 species), decayed wood (15.7%, 3 species),
branches (7.3%, 20 species), flowers (1.2%, 18 species), and other plant items (1.7%, 32
species). However, the proportion of different plant items in the diet of spider monkeys
differed significantly between forest types (χ2 = 69.5, df = 14, P < 0.0001), with the
consumption of mature and immature leaves being higher in fragments than in continuous
forest (contrast tests, P < 0.05 in both cases, Fig. 1A).
In general, we found a high overlap between forest types in the plant species used as
fruit sources (Morisita-Horn’s index = 0.84). In continuous forest the consumption of
mature fruits was focused on Spondias radlkoferi (29.6% of the time spent eating mature

50
fruits), S. mombin (11.2%), and Ficus tecolutensis (10.9%), whereas in fragments it was
focused on three Ficus species (35.3%), S. radlkoferi (13.3%), and Calatola laevigata
(5.9%). Similarly, the consumption of immature fruits in continuous forest was focused on
S. radlkoferi (69.3% of the time spent eating immature fruits), whereas in fragments it was
focused on S. radlkoferi (32.1%), and Brosimum alicastrum (27.0%).
We also found a high overlap between forest types in the plant species used as leaf
sources (Morisita-Horn’s index = 0.82). For example, the consumption of immature leaves
was focused on D. guianense and B. alicastrum in both continuous forests (39.5% and
25.2% of the time spent eating immature leaves, respectively) and fragments (62.5% and
10.2%, respectively). However, in continuous forest consumption of mature leaves was
focused on Machaerium sp. (43.7% of the time spent eating mature leaves) and Bravaisia
integerrima (14.1%), while in fragments it was focused on Ficus sp. (63.9%).
CONSUMPTION OF GROWTH FORMS.—Overall, in terms of total feeding time, trees were the
most consumed plant growth form in terms of total feeding time (73% of TFT, 70 species),
followed by hemiepiphytes (17.0%, 11 species), climbers (4.7%, 18 species), epiphytes
(2.3%, 11 species), palms (2.1%, 4 species), and shrubs (0.7%, 7 species). The proportion
of different growth forms in the diet of spider monkeys differed between forest types (χ2 =
127.3, df = 14, P < 0.0001), with the consumption of trees being higher in continuous forest
than in fragments (contrast test, P < 0.0001; Fig. 1B), whereas the opposite pattern was
found when analyzing hemiepiphytes and palms (contrast tests, P < 0.05 in both cases, Fig.
1B). Spider monkeys exploited more hemiepiphytes in fragments (11 Ficus species: 29.5%
of TFT, and 2 Philodendron species: 0.8% of TFT) than in continuous forest (7 Ficus
species: 9.6% of TFT, and 3 Philodendron species: 1.5% of TFT). Similarly, in fragments

51
spider monkeys exploited more palm species (Attalea butyracea, Bactris balanoidea, B.
mexicana and Sabal mexicana: 3.7% of TFT) than in continuous forest (Attalea butyracea
and B. balanoidea: 0.6% of TFT).
COMPOSITION AND STRUCTURE OF VEGETATION.—We recorded a total of 1774 plants, from
96 species (and 36 morphospecies) belonging to 78 genera and 34 families within the
foraging areas. In general, the families with the highest number of individuals were
Meliaceae (18%), Malvaceae (17%), Fabaceae (12%), and Moraceae (10%). Both
continuous forest and fragments presented top food species for spider monkeys (recognized
based on review of spider monkey diet; see methods), and 5 of them (B. alicastrum, D.
guianense, Guarea glabra, L. platypus, and S. radlkoferi) were among the ten species with
the highest IVI in both forest types (Table 2). However, the sum of the IVI of top food
species was notably greater in continuous forest (IVI = 217) than in fragments (IVI = 149;
Table S2). The number of food plant species was similar in both forest types (mean ± SD;
67.5 ± 7.2 species in continuous forest; 64.1 ± 2.1 species in fragments; χ2 = 0.4, df = 1, P =
0.5). However, the density of large trees (> 60 cm in dbh) from top food species was higher
in continuous forest (4 ± 1 stems/1000 m2) than in fragments (1.3 ± 1.1 stems/1000 m2; χ2 =
4.2, df = 1, P = 0.04).
DISCUSSION
As in most vertebrates, in primates the ability to make shifts in diet in response to
environmental pressures influences the costs and benefits of different foraging strategies,
affecting nutrient acquisition, survival and reproduction (Felton et al. 2009a, MacArthur &
Pianka 1966, Harrison 1984, Garber 1987). Our results suggest that, as a probable response

52
to fruit shortage in fragments (e.g., lower IVI of top food species and lower density of large
top food trees), spider monkeys in the Lacandona rainforest are able to carry out notable
adjustments in their diet. Spider monkeys in fragments: (1) diversified their overall diet; (2)
increased consumption of immature and mature leaves; and (3) increased time feeding on
non-tree growth forms (e.g., hemiepiphytes and palms).
Based on optimal foraging theory (MacArthur & Pianka 1966), we would expect
that the diet becomes less selective when profitable items are less common. Therefore,
when and where fruit and top food species are less available (i.e., in fragments), primates
should diversify their diets. Other studies also have found that the diet of primates is more
diverse in forest fragments than in large forest reserves (e.g., Alouatta pigra: Rivera &
Calmé 2006, A. palliata: Cristóbal-Azkarate & Arroyo-Rodríguez 2007). Also, fruit
shortage in fragments could ‘force’ primates to use foods of lower energetic content and
with higher concentration of secondary compounds, such as leaves (Milton 1980, Peres
1994, Cristóbal-Azkarate & Arroyo-Rodríguez 2007, Felton et al. 2009a, present study).
Therefore, to avoid potential negative health problems (Freeland & Janzen 1974, Glander
1982) and obtain the macronutrients, vitamins and minerals that a primate requires to meet
its nutritional needs (Lambert 2007, Felton et al. 2009a, 2009b) primates tend to increase
the number of plant species when consuming more leaves.
Although we found that spider monkeys are able to switch to a more folivorous diet
when necessary (see also Wallace 2005, González-Zamora et al. 2009), we do not know if
this dietary adjustment may favor their persistence in altered landscapes. This behavior
could in fact have negative consequences not only for spider monkeys (Karesh et al. 1998,
Wallace 2005), but also for the plant assemblage (e.g., reduced seed dispersal efficiency;
Chaves et al. in press). As the digestive system of spider monkeys appears to be designed

53
essentially for a diet mainly composed of easily digestible food items like fleshly fruits
(e.g., they have fast gut passage rates and relatively small hind-gut: Milton 1981, Lambert
1998), this species is apparently constrained in how much folivorous material they are able
to digest (Rosenberger & Strier 1989). Karesh et al. (1998) and Wallace (2005) found that
body condition of spider monkeys dropped dramatically during periods in which their diet
was more folivorous. Similarly, Rangel-Negrín et al. (2009) argued that food scarcity in
fragments could explain the increment of physiological stress of spider monkey in these
areas. Primate socio-ecological models indicate that an increase in folivory results in an
increase in the enforced resting time (i.e., resting needed for digestive and/or
thermoregulatory purposes), which may limit noticeably the time available for other vital
activities, and hence affect the survival of the primates (Kortjents et al. 2010). Future
studies are necessary to quantify changes in foraging strategies in fragmented habitats and
their potential effects on health of individuals and population sizes.
Since top food species are not as common in fragments, spider monkeys are likely
‘forced’ to use non-tree growth forms more common in fragments such as palms and
hemiepiphytes (Fig. 1B). The higher consumption of hemiepiphytes in fragments is
explained by the exploitation of hemiepiphytic Ficus spp., which are commonly found in
fragmented habitats. Although we only could determine the IVI of two Ficus species in the
region (Table S2), it is probable that some characteristics of this light demanding genus
(e.g., fast growing, high ability to proliferate in disturbed and open habitats, large number
of potential dispersers: Shanahan et al. 2001, Serrato et al. 2004) result in a greater
abundance of these species in fragments than in continuous forest. The palms used as food
sources also were very common in fragments (e.g., Sabal mexicana; see Table S2).

54
Despite the capacity to feed from many different species, spider monkeys in
Lacandona spent most of their time feeding on Ficus spp., Spondias spp., Brosimum spp.,
Dialium guianense, and Licania platypus. These top food species also have been reported
as top food species throughout the distribution range of A. geoffroyi in Mesoamerica
(González-Zamora et al. 2009), and the three former ones are top food species for Ateles
spp. in different forests in Central and South America (see Di Fiore et al. 2008). The fact
that spider monkeys concentrate their feeding time on these plant taxa in both forest types
(continuous and fragmented) is likely related to several characteristics of these species
including: (1) their high abundance in the study sites (Table 2), (2) their large size and
consequent large fruit and leaf production, and (3) in the particular case of Ficus spp., their
asynchronous fruit phenology with more than one fruit crop per year (Milton 1991,
Shanahan et al. 2001). The marked and continued use of Ficus suggests that figs represent a
staple food resource for spider monkeys (Weghorst 2007, Felton et al. 2008). As it has been
widely demonstrated that presence and abundance of primates in their habitats are strongly
associated with the abundance of important food resources (e.g., Pan troglodytes: Balcomb
et al. 2000, Neotropical primates: Stevenson 2001, Cercopithecus mitis: Worman &
Chapman 2006, Alouatta palliata: Arroyo-Rodríguez et al. 2007), it is crucial to consider
these top food species as a priority for conservation to develop effective management and
restoration plans for Ateles spp.
Since spider monkeys have large home range requirements (37–98 ha: Fedigan et al.
1988), it is unlikely that the small size of two of the three study fragments (14 and 31 ha,
Table S1) can maintain viable populations of spider monkeys in the long-term. Small forest
fragments by themselves cannot provide sufficient habitat for viable populations of many
animal species (Zuidema et al. 1996, Arroyo-Rodríguez et al. 2007, Chapman et al. 2007),

55
especially in the case of large-bodied mammal species such as spider monkeys. Despite the
fact that our study contained extremely variable sized fragments, our data support the idea
that even small fragments (< 30 ha) are undoubtedly valuable for primate conservation as
they may function as stepping stones that increase the landscape’s connectivity facilitating
inter-fragment movements (Marsh 2003b, Arroyo-Rodríguez et al. 2007). Thus, although
the urgent need to conserve the most extensive areas of well-protected rainforest cannot be
forgotten, in highly deforested and fragmented regions, such as the Marqués de Comillas
region, primate persistence requires the preservation and restoration of small- and
intermediate-sized forest remnants. By increasing the size and connectivity of small
fragments, it is reasonable to expect the reduction of some important environmental
pressures (e.g., selective logging, hunting, vulnerability to predation, edge effects)
constraining the survival of primates and many other mammals in these habitats
(Michalski & Peres 2007, Stoner et al. 2007, Asensio et al. 2009). Finally, we suggest that
future long-term studies evaluating the temporal and spatial variability of diet as well as the
nutritional ecology of spider monkeys (and other atelids) in contrasting habitats (e.g.,
fragmented and continuous forests, logged and unlogged forests) could be crucial to a better
understanding of the ability of these primates to cope with stressful environmental
conditions.
ACKNOWLEDGEMENTS
This research was supported by grants from the Consejo Nacional de Ciencia y Tecnología,
Mexico (CONACyT Grant CB-2005-51043 and CB-2006-56799). The Instituto para la
Conservación y el Desarrollo Sostenible, Costa Rica (INCODESO) provided logistical

56
support. OMC obtained a scholarship from the Dirección General de Estudios de Posgrado,
UNAM, and from the Secretaría de Relaciones Exteriores (SRE) of Mexico. A postdoctoral
fellowship was given to VAR by the Consejo Técnico de la Investigación Científica
(UNAM). A. Estrada and J. Benítez-Malvido provided useful comments and suggestions in
the development of this research. This study would not have been possible without the
collaboration of the local people in Loma Bonita, Chajul, Reforma Agraria and Zamora
Pico de Oro ejidos. We thank C. Balderas, C. Hauglustaine, J. Herrera, R. Lombera and S.
Martínez, for field assistance and J. M. Lobato and G. Sánchez for technical support. We
finally thank J.C. Dunn and one anonymous reviewer for valuable criticisms and
suggestions that improved the manuscript.

57
SUPPORTING INFORMATION
TABLE S1. Characteristics of the sites and groups of spider monkeys studied in
Lacandona, Chiapas, Mexico.
TABLE S2. Importance value index (IVI) of the top food species for spider monkeys in 6
study sites: Three sites within the continuous forest of the Montes Azules Biosphere
Reserve, and 3 forest fragments within the Marqués de Comillas region, Lacandona,
Chiapas, Mexico.
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TABLE 1. Species contributing to 80% of feeding time of A. geoffroyi in continuous and
fragmented forests in Lacandona, Chiapas, Mexico. Species are ordered based on the
percentage of feeding time. Plant growth form (GF), relative percentage of frugivory
(%FR), percentage of total feeding time (%TFT), and percentage of tree abundance (%TA).
(HE) Hemiepiphyte. (─) Undetermined data.
Species Family GF PIa %FR %TFT %TA
Top
foodb
Continuous forest
Licania platypus Chrysobalanaceae Tree 1,4,5,6 0.9 (0–1) 31.2 (0.4–45) 1.73 Yes
Spondias radlkoferi Anacardiaceae Tree 1,2,4 96.7 (91–100) 22.5 (7.4–46) 1.09 Yes
Spondias mombin Anacardiaceae Tree 1,2 100 (0–100) 6.2 (0–10) 0.01 Yes
Ficus tecolutensis Moraceae HE 1,2,4 99.8 (99–100) 4.6 (4–6) 0.27 Yes
Brosimum alicastrum Moraceae Tree 1,2,4 50.7 (33–63) 4.4 (3–6) 3.9 Yes
Dialium guianense Fabaceae Tree 1,2,4 16.2 (7–25) 3.8 (3–6) 5.2 Yes
Ampelocera hottlei Ulmaceae Tree 1,5 98.2 (68–100) 3.6 (0.3–7) 6 Yes
Ficus obtusifolia Moraceae HE 1 100 2.5 (0–9) ─ Yes
Strychnos tabascana Loganiaceae Vine 1,5 33.8 (19–82) 1.9 (0–4) ─
Forest fragments
Dialium guianense Fabaceae Tree 1,2,4 21.9 (17–27) 18.3 (12–27) 4.05 Yes
Ficus tecolutensis Moraceae HE 1,2,4 98.8 (99–100) 12.2 (7–23) 0.18 Yes
Spondias radlkoferi Anacardiaceae Tree 1,2,4 99.5 (99–100) 10.7 (8–19) 1.06 Yes
Brosimum alicastrum Moraceae Tree 1,2,4 70.6 (0–83) 10 (4–16) 4.05 Yes
Ficus sp1 Moraceae HE 1,4,6 58.7 (42–97) 8.2 (1–15) ─ Yes
Licania platypus Chrysobalanaceae Tree 1,4,5,6 8.3 (0–9) 4.9 (2–9) 0.7 Yes

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Ficus insipida Moraceae Tree 1,6 9.7 (0–12) 3.2 (0.7–6) 0.01 Yes
Sabal mexicana Arecaceae Palm 1,2 100 (0–100) 2.2 (0–8) 1.06 Yes
Calatola laevigata Icacinaceae Tree 1,2 100 (0–100) 2.2 (0–3.2) 0.7
Ficus sp2 Moraceae HE 1,4,7 98.7 (0–100) 2.2 (0.2–7) ─ Yes
Spondias mombin Anacardiaceae Tree 1,2 100 2.0 (1–3) 0.18 Yes
Maclura tinctoria Moraceae Tree 1,2,4 88.1 (0–88) 1.7 (0–3) 0
Poulsenia armata Moraceae Tree 1,2,7 5.9 (0–6) 1.6 (0–3) 1.76 Yes
Guarea glabra Meliaceae Tree 1,2,4 77.3 (43–100) 1.3 (0.8–2) 13.6 Yes
aPlant items: 1, mature fruits; 2, immature fruits; 3, mature leaves; 4, immature leaves; 5,
young branch piths; 6, decayed wood; 7, others.
bPlant species representing > 80% of feeding time of spider monkeys throughout
Mesoamerica (González-Zamora et al. 2009).

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TABLE 2. The ten plant species with the highest importance value indices (IVI) for trees ≥
10 dbh within continuous and fragmented rainforests in Lacandona, Chiapas, Mexico.
Species Family
Density
(stems/3000 m2)
Basal area
(m2) IVI Top fooda
Continuous forest
Guarea glabra Meliaceae 27 28.9 74.6 Yes
Dialium guianense Fabaceae 13 10.9 33.9 Yes
Ampelocera hottlei Ulmaceae 15 8.0 32.3 Yes
Quararibea funebris Malvaceae 18 8.4 29.5 Yes
Spondias radlkoferi Anacardiaceae 5 4.6 14.2 Yes
Pouteria campechiana Sapotaceae 7 1.8 12.8 Yes
Brosimum alicastrum Moraceae 5 1.6 17.0 Yes
Bravaisia integerrima Acanthaceae 8 1.5 2.8
Nectandra reticulata Lauraceae 4 0.4 6.1 Yes
Licania platypus Chrysobalanaceae 2 1.8 5.6 Yes
Forest fragments
Guarea glabra Meliaceae 27 16.5 54.1 Yes
Theobroma cacao Malvaceae 23 10.1 11.2
Dialium guianense Fabaceae 12 8.4 28.4 Yes
Bravaisia integerrima Acanthaceae 11 9.0 8.8
Brosimum alicastrum Moraceae 7 5.5 10.2 Yes
Brosimum lactescens Moraceae 9 1.5 12.3 Yes
Spondias radlkoferi Anacardiaceae 5 2.9 10.8 Yes
Licania platypus Chrysobalanaceae 6 2.2 7.6 Yes
Cojoba arborea Fabaceae 4 1.2 2.5 Yes
Poulsenia armata Moraceae 5 0.6 2.4 Yes
a See Table 1 legend.

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Figure legend
FIGURE 1. Diet composition in continuous and fragmented forests according to percentage
of total feeding time (mean ± SD) consuming different plant items (A) and different growth
forms (B). Different letters above bars indicate significant differences between continuous
forest and fragments (P < 0.05). Plant items: mature fruits (MF), immature fruits (IF),
immature leaves (IL), mature leaves (ML), young branches (BR), flowers (FL), decayed
wood (DW), and other plant items (OT). Growth forms: trees (T), hemiepiphytes (H),
climbers (C), palms (P), epiphytes (E), and shrubs (S).

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FIGURE 1. O. M. Chaves, K.E. Stoner and V. Arroyo-Rodríguez.
SUPPORTING INFORMATION
B
a
aaaaa
b
b
abaa
0
10
20
30
40
50
60
70
80
90
100
THCPES
Growth forms
Percentage of total feeding time
A
a
a
a
a
a
a
aa
a
a
b
b
aa
a
a
0
10
20
30
40
50
60
MF IF ML IL BR FL DW OT
Plant item
Continuous forest
Fragments

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SUPPORTING INFORMATION
HOME RANGE OF THE MONKEY GROUPS.— From February-Jun and August-October 2008,
we daily recorded with GPS the location of each focal group foraging in continuous forest
and in the fragment F3 during the morning and the afternoon. Following Spehar et al.
(2010), for each focal group a map of the home range was created in Arc View GIS 3.3
(Environmental System Research Institute Inc., USA) using all GPS coordinates. A set of
100 m x100 m (1 ha) grid squares was then superimposed over these maps, and a
representation of the monkey group’s home range was created by calculating the number of
100 m x 100 m grid squares into which monkey group ranged as well as the minimum
convex polygon (MCP) encompassing all of the location points. We preferred MCP method
rather than adaptive kernel (AK) or fixed kernel (FK) because it allow a more accurate
estimation of home range when sample size is small (see Boyle et al. 2009).
LITERATURE CITED
BOYLE, S. A., W. C. LOURENÇO, L. R. DA SILVA, AND A. T. SMITH. 2009. Home range
estimates vary with sample size and methods. Folia Primatol. 80: 33–42.
SPEHAR, S. N., A. LINK, AND A. DI FIORE. 2010. Male and female range use in a group of
white-bellied spider monkeys (Ateles belzebuth) in Yasuní National Park, Ecuador.
Am. J. Primatol. 72: 129–141.

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TABLE S1. Characteristics of the sites and groups of spider monkeys studied in
Lacandona, Chiapas, México. DNF, distance to nearest forest fragments; DCF, distance to
the continuous forest; YFF, year since fragmentation.
Sites Size
(ha) Location DNF
(m)
DCF
(m) YFF Group
size
Home range
(ha)b
Continuous forest 300,000 Montes Azules Biosphera Reserve
C1 ─ 16°06'58.2"N, 90°56'18.4"W ─ ─ ─ 40 29.7
C2 ─ 16°09'32.0"N, 90°54'06.6"W ─ ─ ─ 36 47.3
C3 ─ 16°09'40.0"N, 90°54'04.5"W ─ ─ ─ 44 89.6
Forest fragments
F1 31 Zamora Pico de Oro
(16°19'24.5"N, 90°50'43.7"W) 150 1200 24 39 31
F2 14.4 Zamora Pico de Oro
(16°19'52.0"N, 90°51'06.1"W) 450 200 29 35 14.4
F3 1125a Reforma Agraria
(16°15'12.2"N, 90°49'59.5"W) 100 1100 26 41
63.1
aTotal size of this fragment is 1450 ha, but due to the presence of many wide trails along
and within of the fragment, the presence of cocoa (Teobroma cacao) and pita (Aechmea
magdalenae) plantations, and the different reserve restructuring, the potential successful
habitat for spider monkeys is restricted to ca. 1125 ha of disturbed tropical rainforest.

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TABLE S2. Importance value index (IVI) of the top food species for spider monkeys in 6
study sites: Three sites within the continuous forest of the Montes Azules Biosphere
Reserve, and 3 forest fragments within the Marques de Comillas region, Lacandona,
Chiapas, Mexico. Asterisks indicate the cases in which IVI was greater in continuous forest
than in fragments.
IVI
Species Family Continuous forest Fragments
Ampelocera hottlei Ulmaceae 32.3 7.2*
Brosimum alicastrum Moraceae 17.0 10.2*
Bursera simaruba Burseraceae 2.1 1.6*
Castilla elastica Moraceae 4.1 6
Cupania spp. (2) Meliaceae 3.8 0.5*
Dialium guianense Fabaceae 33.9 28.4*
Ficus insipida Moraceae 0 0.7
Ficus tecolutensis Moraceae 0.6 0.5*
Guarea glabra Meliaceae 74.6 54.1*
Licania platypus Chrysobalanaceae 5.6 7.6
Poulsenia armata Moraceae 0 7.2
Pouteria campechiana Sapotaceae 12.8 3*
P. sapota Sapotaceae 1.9 1.5*
Protium copal Burseraceae 3.3 1.5*
Mortoniodendron Malvaceae 1.8 0*
Nectandra reticulata Lauraceae 6.1 1.5*
Sabal mexicana Arecaceae 0 4.9
Spondias radlkoferi Anacardiaceae 14.2 10.8*
S. mombin Anacardiaceae 0 1.5
Virola guatemalensis Myristicaceae 2.9 0*
Total 217 148.7
*Indicates the cases in which IVI was greater in continuous forest than in fragments.

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CAPÍTULO II

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Running title: Spider Monkey Seed Dispersal Effectiveness
Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed
Dispersers in Continuous and Fragmented Rainforests in Southern
Mexico
(accepted 24 May 2010, International Journal of Primatology, IF=1.78)
Óscar M. Chaves; Kathryn E. Stoner; Víctor Arroyo-Rodríguez; Julieta Benítez-
Malvido; Alejandro Estrada
O. M. Chaves (corresponding author); K. E. Stoner; V. Arroyo-Rodríguez; J. Benítez-
Malvido, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de
México (UNAM), Antigua Carretera a Pátzcuaro No. 8701, Ex Hacienda de San José de la
Huerta, 58190 Morelia, Michoacán, Mexico
email: ochaba@gmail.com
A. Estrada
Laboratorio de Primates, Instituto de Biología, Universidad Nacional Autónoma de
México. Apartado Postal 176, San Andrés Tuxtla, Veracruz, Mexico
Received:__ /Revised:__/Accepted:__

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Abstract Seed dispersal is considered a key process determining spatial structure and
dynamics of plant populations, and has crucial implications for forest regeneration. We
evaluated the effectiveness of spider monkeys (Ateles geoffroyi) as seed dispersers in
continuous and fragmented habitats to test if this interaction is altered in forest fragments.
We documented fruit and seed handling, defecation patterns, diversity and composition of
seeds in feces, and seed germination of defecated and control seeds in the Lacandona
rainforest, Mexico. For most species contributing to 80% of total fruit feeding time,
monkeys swallowed and spat seeds, but swallowing was the most frequent seed handling
category in continuous and fragmented forests. However, the proportion of feeding records
of swallowed seeds was higher in continuous forest (0.59) than in fragments (0.46), whilst
the opposite was true for proportion of dropped seeds (0.16 versus 0.31). This pattern was
reflected in the number of fecal samples containing seeds, which was greater in continuous
(95.5%) than fragmented forests (82.5%). Seeds in fecal samples included a total of 71
species from 23 plant families. The number of defecated seed species was similar between
forest conditions and in both cases most seeds (> 86%) were undamaged. Defecated seeds
showed greater germination percentages than control seeds in all of the five species
evaluated. Although we identified some differences in seed handling and the percentage of
feces with seeds between continuous forest and fragments, our results indicate that, in
general terms, spider monkeys are efficient seed dispersers in both forest conditions.
Keywords forest regeneration; fragmentation; frugivorous primates; seed dispersal

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Introduction
Plant recruitment, distribution and regeneration of tropical forest species largely depend on
the effectiveness of animals as seed dispersers (Cordeiro et al. 2009). Disperser
effectiveness is defined in terms of the contribution a disperser makes to the future
reproduction of a plant or to plant fitness, and may be considered from the perspective of
both the dispersal agents and the dispersed plants at a variety of scales from individuals to
communities (Jordano and Schupp 2000; Schupp 1993).
From the plant perspective, seed dispersal effectiveness depends on two main
components (1) the quantity of dispersed seeds, and (2) the quality of seed dispersal (i.e.,
the probability that seeds are deposited intact in sites with high prospects for establishment)
(Muller-Landau and Hardesty 2005; Schupp 1993). According to Schupp (1993), the first
component is a function of the number of visits made to the plant by a disperser and the
number of seeds dispersed per visit, which depends on the abundance of the disperser, its
feeding behavior, the fruit/seed handling strategies, and the reliability of visitation. The
second component is a function of the quality of treatment given a seed in the mouth and in
the gut (i.e., percentage of handled seeds destroyed, and percentage of germination of
defecated seeds) and the quality of seed deposition (i.e., defecation pattern, predator
pressures, and probability of establishment). In sum, both the quantity and quality of seed
dispersal determine the final fate of a seed and in turn, the relative impact dispersers have
on plant community structure and composition (Jordano and Schupp 2000; Schupp 1993).
Seed dispersal effectiveness may be particularly critical in forest fragments, in
which some fruit-eating animal species disappear (e.g., birds: Martensen et al. 2008; bats:
Cosson et al. 1999; large birds and mammals: Melo et al. 2010; primates: Arroyo-

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Rodríguez et al. 2008), affecting plant species diversity and vegetation structure (Moran et
al. 2009). This threat is higher for large-seeded tree species because their dispersal agents
are often large-bodied and hence, at greater risk of local extinction in fragments (i.e. with
greater hunting pressures, lower reproductive rates, smaller population sizes, and in many
cases, with larger home range requirements: Stoner et al. 2007). This is the case for
primates, which constitute 25–40% of the frugivore biomass in tropical forests (Chapman
1995), and are important seed dispersers for many tree species (Link and Di Fiore 2006).
Overall, ecological services provided by primates through seed dispersal are critical for the
recruitment of many medium- and large-seeded plant species in both continuous and
fragmented forests (Stevenson and Aldana 2008).
In Neotropical primates seed dispersal effectiveness has been evaluated only in a
few species, and mainly in continuous forests (e.g., Lagothrix lagotricha: Stevenson 2000;
Alouatta seniculus: Julliot 1996; Cebus capucinus: Valenta and Fedigan 2009). These
studies have assessed only isolated aspects of dispersal effectiveness (e.g., dispersal
distance and germination rates: Stevenson 2000; fruit choice: Stevenson 2004; dispersal
quantity: Link and Di Fiore 2006; Stevenson 2007) and did not consider the potential effect
of the site-specific vegetation structure (e.g. abundance and diversity of food species for
primates) on the aspects evaluated. Thus, for a given primate species, observed patterns of
seed dispersal may be more related to differences in inter-site plant species composition
and abundance (which result in differential fruit availability at each site), than only to
differences in the behavior of the disperser among habitats (e.g., Ateles spp.: Russo et al.
2005). Despite these facts, evidence suggests that effectiveness of primates as seed
dispersers is highly variable in terms of proportion of fruit in the diet, number of seed
species in feces, size of swallowed seeds, percentage of fecal samples without seeds, and

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effect of gut passage on seed germination (Table S1). For example, fruit in the diet for
some sympatric primates may range from 2% (Alouatta seniculus: Orihuela-López et al.
2005) to 87% (Ateles belzebuth: Dew 2008). The number of seed species in feces may
range from 9 (A. palliata: Wehncke et al. 2004) to 133 species (Ateles belzebuth: Link and
Di Fiore 2006). Contrasting defecation patterns have been reported for different primates
(e.g., scattered in Cebus capucinus: Wehncke et al. 2004; clumped in Alouatta seniculus:
Andresen 2002), which may differentially affect the probability of seed and seedling
survival (see Howe 1989). Similarly, positive, neutral and negative net effects of primate
gut passage on seed germination have been reported; nevertheless, positive effects are more
frequent (Table S1).
Finally, post-dispersal seed fate including the effect of secondary seed dispersers
and predators (e.g., dung beetles and scatter hoarding rodents) represent additional elements
influencing the effect of primary seed dispersers on plant fitness (Schupp and Fuentes
1995). Although most secondary dispersers move seeds short distances and frequently bury
them close to the original deposition microsite (e.g., < 1 m in dung beetles: Andresen
2002), the cached seeds often have a higher survival than the uncached seeds (Andresen
and Levey 2004; Forget and Cuijpers 2008). However, secondary dispersal is less likely to
occur when highly frugivorous and mobile primates, such as spider monkeys, are the
primary seed dispersers than when they are not (Forget and Cuijpers 2008).
In continuous forests evidence suggests that spider monkeys are legitimate seed
dispersers for a large number of plant species because they swallow large quantities of
seeds and defecate them intact (Di Fiore et al. 2008), and they transport seeds far away
from parent trees (> 100 m) to sites with higher probability of seedling establishment (Link
and Di Fiore 2006). Nevertheless, no study to date has examined simultaneously different

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quantitative and qualitative aspects of Ateles’ seed dispersal effectiveness and how these
attributes are modified in forest fragments. In spite of this fact, evidence suggests that
primate-plant interactions may be negatively affected in forest fragments because these
habitats often present less availability of fruit resources for primates in comparison with
continuous forests (Arroyo-Rodríguez and Mandujano 2006; Dunn et al. 2009), forcing
frugivorous primates to adjust their feeding behavior (e.g., exploiting alternative plant
items: González-Zamora et al. 2009; Onderdonk and Chapman 2000).
We aimed to determine the effectiveness of spider monkeys (Ateles geoffroyi
vellerosus) as primary seed dispersers in quantitative and qualitative terms and to assess if
this interaction is altered in forest fragments. Seed dispersal effectiveness was estimated in
areas of continuous and fragmented forest in Lacandona, Chiapas, Mexico, by analyzing (1)
seed handling of the top fruit plant species and its relationship with seed size; (2) defecation
patterns; (3) diversity and composition of defecated seed species, and percentage of
undamaged seeds; and (4) germination of defecated versus control seeds. Since spider
monkeys are highly frugivorous and commonly defecated in a scattered pattern (Di Fiore et
al. 2008; Howe 1989; Russo 2005) we predict that they will be efficient seed dispersers in
terms of number of defecated seeds, defecation pattern, and the effect of gut passage on the
germination in continuous forest and fragments. However, since fragmentation often
reduces fruit availability and promotes shifts in feeding behavior (see above), we also
predict that fragments will experience a decrease in the proportion of seeds ingested, the
number of seed species defecated, and the proportion of feces with seeds. This is the first
study that documents the importance of a Neotropical monkey on seed dispersal
effectiveness in forest fragments (but see González-Di Pierro et al. in press).

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Methods
Study Sites and Spider Monkey Communities
We studied the fruit-eating behavior of six communities of spider monkeys: three
independent communities in three different areas of the Montes Azules Biosphere Reserve
(MABR, > 3000 km2) separated by at least 4 km (i.e., the closest distance among home
range perimeters), and three communities in three different fragments located in the
Marqués de Comillas Region (MCR), Chiapas, Mexico (for further details see Electronic
supplementary material). All fragments in MCR were isolated ≥ 24 years ago, and their
sizes were 14, 31, and 1125 ha (Table S2). For the three study sites of MABR and for the
largest fragment, we restricted spider monkey follows to an area of 30–100 ha (depending
on the movements of focal communities), whereas for the other two fragments the entire
area was sampled. Finally, although there are differences in size and distance among sites,
both forest conditions (continuous forest and fragments) had a similar adult tree
composition (see Electronic supplementary material).
Primate Species in the Study Area
Two primate species are present in the study area: the black-handed spider monkey (Ateles
geoffroyi vellerosus) and the black howler monkey (Alouatta pigra). In MABR population
density of A. geoffroyi has been estimated as 2.9 ind/km2, while that for A. pigra is 14.4
ind/km2, whilst a gross estimate of these population densities in a large fragment at MCR
are 9.3 and 13.3 ind/km2, respectively (Estrada et al. 2004). Overall, howler monkeys are

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characterized by having a folivorous diet (Di Fiore and Campbell 2007). By contrast, Ateles
spp. has been described as a fruit specialist (Di Fiore et al. 2008) that accounts for more
than 70% (ranging from 39 to 82%) of their feeding time (González-Zamora et al. 2009).
Feeding Behavior and Seed Handling
Diet of spider monkeys was studied during a 15-mo period (6 months in the dry season:
February-April 2007 and 2008; and 9 months in rainy season: May-October 2007, and
August-October 2008). Feeding behavior was documented for each of the 6 focal
communities during 3 consecutive days once every 3 weeks, using 5-min focal animal
sampling (Altmann 1974). Follows were conducted from 7:00 h to 17:30 h, totaling 223
observation days and 1000 h of focal observations. Further details of feeding sampling are
provided in Electronic supplementary material.
We recorded the feeding behavior to determine how much of the diet was devoted to
consumption of different plant items (Chaves et al. in press) but here we focus on the fruit
diet. When monkeys were feeding on fruits we identified whether they were consuming
ripe or unripe pulp/aril and we recorded growth-form (trees, shrubs, epiphytes and
climbers), species and seed handling behavior (see below). When fruit development could
not be determined because of poor illumination, we simply recorded the food item as fruit.
The relative importance of different fruit species in the diet was calculated as percent time
spent consuming a particular fruit species in relation to total time feeding on fruits. We
ranked the fruit species based on the percent of time spent consuming each fruit species in
relation to the total time spent consuming all fruit species until the sum was 80% and hence
recorded the seed handling only for these species (hereafter named top fruit species).We

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recognized three categories of seed handling: (1) swallowed—ingestion of the entire fruit
swallowing pulp and seeds; (2) spat out—when monkeys ate the fruit pulp or aril and spat
out the seeds under the parent tree while eating; and (3) dropped—when monkeys ingested
only fruit pulp and dropped seeds under the parent tree. Finally, because the top fruit
species were not the same in continuous forest and fragments, we restrict the statistical
analysis to the five top fruit species present in both forest conditions (Brosimum alicastrum,
Ficus tecolutensis, Ficus sp1., Spondias mombin and S. radlkoferi) in order to control for
seed handling effects at the species level.
Defecation Pattern, Defecated Species, and Germination Trials
Following Wehncke et al. (2004), we classified deposition or defecation pattern as scattered
(i.e., when monkeys defecated individually in space and time creating a scatter of small
defecations) or clumped (i.e., when a monkey community or subgroup defecated
simultaneously in a particular place producing large areas of clumped defecations). In
contrast to Russo and Augspurger (2004), we did not discriminate between sleeping sites
and in-transit sites because in Lacandona the location of sleeping sites (both diurnal resting
trees and nocturnal sleeping trees) varied constantly over time. Furthermore, we did not
sample at dawn or dusk when the entire community was found together, but rather sampled
from subgroups while foraging and moving throughout the day.
Fecal samples were collected from individual monkeys immediately after
defecation, and placed individually in labeled plastic bags and later processed in the field
laboratory. Each sample was thoroughly rinsed with water in a sieve using successively
decreasing mesh size (3 mm and 1 mm mesh, respectively). The number, composition, and

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damage level of seed species in each sample was recorded using a stereoscope (10–40X
magnification). Seeds were classified as: (1) undamaged—intact seeds or with ≤ 5% of the
testa damaged; (2) moderate damage—seeds with > 5% to ≤ 25% of the testa damaged; and
(3) heavy damage—> 25% of the testa damaged. In both forest conditions, we ranked the
defecated seed species based on the percent of fecal records containing each seed species in
relation to the total fecal records for all seed species until the sum was 80% (hereafter
named top defecated seed species). To identify seed species we used the Lacandona seed
reference collection located at the Centro de Investigaciones en Ecosistemas (UNAM,
Morelia, Mexico). Plant nomenclature followed the Missouri Botanical Garden
nomenclatural update database (http://mobot.org/W3T/search/vast.html).
To examine the effect of seed passage through spider monkeys´
digestive tract, we performed a series of germination trials in four tree species (S.
radlkoferi, Ampelocera hottlei, Brosimum lactescens, and Faramea occidentalis), and one
vine (Cissus verticilata) with large seeds (1.4–4.5 cm in length) . These species were
selected because they represent important fruit sources for spider monkeys in the study area
(comprising 6–40% of their fruit feeding time for the first three species and ca. 2% for the
latter two species: Chaves et al. in press), and because their size limits potential dispersers
to primates and a few large-bodied birds (Jordano 1995). Seeds for germination trials were
collected from fresh feces just after defecation and from mature fruits (control seeds).
Mature fruits were collected under the crowns of 5–14 parent trees where the monkeys fed.
Pulp or aril was manually removed and all seeds were observed with a stereoscope (10–
40X magnification) in order to select only intact seeds (i.e., seeds without holes,
malformations or other damage to the testa). For each species, we used 14–40 seeds from
12–36 mature fruits (control seeds) and 15–30 seeds from 10–20 fecal samples. Defecated

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and control seeds were similar in size and weight and were collected from continuous
forest. Seeds were placed in 10 x 20 cm plastic boxes containing river sand and placed in a
greenhouse (ca. 40% full sun) located in a 1-ha fragment at 150 m from MABR. Seeds
were watered daily for 12 weeks and germination (i.e., radicle emergence) was recorded
daily.
Data Analysis
To evaluate if seed handling differed between continuous forest and fragments we used
generalized linear models (GLM: Crawley 1993). We estimated the proportion of records
devoted to each category of seed handling per study site considering each of the three sites
as replicates within each forest condition. As different seed handling occurs within each
forest condition (Fig. 1), we nested seed handling within forest condition, with the whole
model being: PROPORTION OF RECORDS = SEED HANDLING nested within
FOREST CONDITION + SEED HANDLING*SPECIES nested within FOREST
CONDITION + FOREST CONDITION. Proportion data were first arcsine transformed,
and tested for a normal distribution with a Shapiro Wilk test (passed, p>0.1). We then
selected Normal distribution with an identity link-function to the response variable. To
identify which seed handling categories were statistically different among each other we
used post-hoc analyses with contrasts (Crawley 1993). We also explored the relationship
between percentage of swallowed seeds and seed size in each forest condition with a linear
regression of arcsine transformed proportions. To compare the defecation pattern in
continuous and fragmented forest we used a GLM, fixing a Poisson distribution and log-
link function to the response variable (i.e., number of defecation records) (Crawley 1993).

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Previously, we standardized the number of defecation records in each forest condition to
control for differences in sample size. Additionally, to test for consistency between fruit
diet data obtained from foraging observations and defecated seeds, we estimated the species
overlap between these two techniques with the Morisita-Horn index.
To test for differences in the number of defecated seed species per site and in the
number of seed species per fecal sample between continuous and fragmented forests, we
used analyses of deviance with GLM. As suggested for count response variables, we fixed a
Poisson distribution to a log-link function (Crawley 1993). First, we standardized the
number of fecal samples to control for differences in species density using the rarefaction
approach (EcoSim: Gotelli and Entsminger 2001). The number of fecal samples that
contained no seeds was compared with GLM, fixing a Poisson distribution and log-link
function to the response variable. Finally, to compare the number of seeds that germinated
from defecated versus control seeds we constructed a 2 x 2 contingency table for each
species and tested differences with G-tests. All statistical analyses were performed using
JMP software (version 7.0, SAS Institute, Cary, N.C.).
Results
Feeding Behavior and Seed Handling
Overall, fruit made up 55.6 ± 18.9% (mean ± SD) of the spider monkeys’ diet (57.0 ±
27.1% in continuous forest and 54.1 ± 12.5% in fragments). The monkeys consumed fruits
from 73 species in continuous forest and 61 species in fragments. In general, for most top
fruit species (ca. 90%) spider monkeys showed more than one category of seed handling,

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with swallowed being the most frequent category in both continuous (55.6% of species) and
fragmented forests (60% of species; Table I). The number of feeding records did not differ
between forest conditions (χ2 = 0.28, df = 1, p = 0.9). However, it was significantly
different among categories of seed handling nested within forest condition (χ2 = 68, df = 4,
p < 0.0001), with the proportion of swallowed seeds being greater than spat out and
dropped seeds in both forest conditions (contrast tests, p < 0.05 in all cases; Fig. 1). The
proportion of swallowed seeds was higher in continuous forest than in fragments (0.59
versus 0.46, contrast test: p = 0.01), while the opposite was true for the proportion of
dropped seeds (0.16 versus 0.31, contrast test: p = 0.03; Fig. 1). Furthermore, we found
significant differences among categories of seed handling by species nested within forest
condition (χ2 = 155, df = 16, p < 0.0001), with seeds of Spondias mombin swallowed more
in continuous forest than in fragments (mean ± SD, 24 ± 27% and 5 ± 4.5% respectively;
contrast test: p = 0.001), while the opposite pattern occurred with the proportion of dropped
seeds (28 ± 25% and 73 ± 6% respectively; contrast test: p < 0.004). No other significant
differences were detected in the remaining four species (contrast tests: p > 0.05 in all
cases). Finally, the percentage of seeds swallowed was inversely related to seed size in both
continuous (r = -0.84, p = 0.005) and fragmented forests (r = -0.71, p = 0.02; Table I).
Defecation Pattern, Defecated Species, and Germination Trials
Scattered defecations were significantly more common than clumped defecations in
continuous forest (94%, n = 523) and fragments (89.4%, n = 496, χ2 = 912, df = 2, p <
0.0001). However, the number of scattered and clumped defecations did not differ between
forest conditions (contrast tests: p = 0.1 in both cases).

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We collected a total of 957 fecal samples (519 in continuous forest and 438 in
fragments) and found seeds from 71 species (of which 52 were identified to species and 19
to morphospecies), 39 genera, and 23 families. The number of defecated seed species was
similar between continuous forest (37 species and 9 morphospecies, range = 18–27 species)
and fragments (38 species and 13 morphospecies, range = 18–24 species, χ2 = 0.03, df = 1,
p = 0.86). Although species composition was similar between forest conditions (Electronic
supplementary material), only 21 out of 52 defecated seed species were shared between
continuous forests and fragments, resulting in a moderate species overlap between forest
conditions (Morisita-Horn’s index = 0.62).
The mean (± SD) number of seed species per fecal sample was 1.3 ± 0.8 species,
ranging from 0 to 6 species, and no significant differences were detected between
continuous forest and fragments (1.3 ± 0.8 and 1.3 ± 1.0 species, respectively; χ2 = 0.64, df
= 1, p = 0.42). More than 90% of the fecal samples contained seeds, but the average
percentage of feces without seeds was greater in fragments (17.5 ± 10%) than in continuous
forest (4.5 ± 3.7%, χ2 = 26.5, df = 1, p < 0.0001). Finally, the overlap in the composition of
fruit species in the diet based on direct observations from foraging data and seed species in
feces was relatively high (Morisita-Horn’s index = 0.75), indicating that seeds collected
from fecal samples reflect approximately 75% of what monkeys are feeding on.
In general, seed size in feces ranged from < 0.1 cm in length and width (e.g., Ficus
spp.) to 3.7–4.5 cm in length and 2.1–2.7 cm in width (e.g., Spondias radlkoferi and Attalea
butyracea). However, spider monkeys also ate the fruit pulp and dropped the seeds of
Licania platypus (ca. 10 x 7 cm) in both forest conditions. Considering the top defecated
seed species for all samples, spider monkeys defecated seeds of 12 species belonging to 9
genera, and 7 families, with Ficus spp. (Moraceae) and Spondias radlkoferi

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(Anacardiaceae) being the most frequent in fecal samples (18.3% and 17.5% of fecal
records, respectively). However, the number of species constituting the top defecated seed
species was higher in fragments than in continuous forest (20 and 10 species, respectively;
Table II). Seven out of 16 top defecated seed species were the same in both forest
conditions (Celtis iguanaea, Dialium guianense, Ficus tecolutensis, Ficus sp1., Guarea
glabra, S. radlkoferi, and S. mombin, Table II). Of these species, S. radlkoferi and F.
tecolutensis were the most frequent seed species in continuous forest, and F. tecolutensis
and Sabal mexicana the most frequent in fragments (Table II). Overall, the percentage of
undamaged seeds was greater than 86% for most seed species in both forest conditions
(Table II).
Finally, in the five studied species, the number of seeds that successfully germinated
was significantly higher for defecated than for control seeds, indicating a positive effect in
all cases (Table III).
Discussion
As predicted, spider monkeys were efficient seed dispersers in quantitative and qualitative
terms. In both continuous forest and fragments they fed on a large number of fruit species
and swallowed seeds of most of them, most feces contained seeds, a scattered deposition
pattern was the most common, and the majority of defecated seeds were undamaged.
Furthermore, defecated seeds showed greater germination percentages than control seeds in
all of the five plant species evaluated. Our results concur with previous studies on spider
monkeys, which have shown that they are efficient in terms of fruit diet diversity, seed
handling, richness of seeds dispersed and defecation pattern (e.g., Ateles spp.: Russo et al.

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2005; A. belzebuth: Link and Di Fiore 2006; Dew 2008). Although we identified some
differences in the seed handling and the percentage of feces with seeds between continuous
forest and fragments, our study concurs with some recent studies showing that animal seed
dispersal effectiveness is not notably affected by fragmentation (e.g., understory birds:
Figueroa-Esquivel et al. 2009).
Seed Handling
Seed handling differed between forest conditions. Compared to communities in continuous
forests, spider monkeys in fragments swallowed proportionally less seeds and dropped
more seeds, which support our second prediction. Although we did not measure if seed
handling is related to fruit shortage in fragments, there is some evidence that supports this
possibility (e.g., Arroyo-Rodríguez and Mandujano 2006). Although overall adult tree
composition was similar in continuous and fragmented forests (Electronic supplementary
material), we found a greater abundance of larger trees (> 60 cm in DBH) of top fruit
species in continuous forest compared to fragments (see Fig. S2). Since the abundance of
large trees is a good indicator of fruit availability (Chapman et al. 1992), it is likely that
less fruit was available for spider monkeys in the studied fragments. Lower fruit availability
often results in primates eating alternative plant items and/or more species (e.g., Ateles
geoffroyi, Alouatta palliata and Cebus capucinus: Chapman 1987; Alouatta palliata:
Cristóbal-Azkarate and Arroyo-Rodríguez 2007). Indeed, this same pattern has been
observed in our same studied monkey communities. Chaves et al. (in press) found that
spider monkeys in fragments invest proportionally more time consuming leaves and
immature fruits than in continuous forest.

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Since immature fruits are less palatable and contain more secondary metabolites than
mature fruits (Waterman 1984), primates that eat immature fruits frequently drop or spit out
more seeds (Norconk et al. 1998). We observed that spider monkeys feeding on immature
fruits usually ate a small portion of the fruit pulp or aril and dropped and/or spat out the
seeds directly under the parent tree. This is particularly the case for S. radlkoferi and S.
mombin, in which spider monkeys dropped a higher proportion of seeds in fragments than
in continuous forest. Exploiting more immature fruits in fragments may influence the seed
dispersal effectiveness in two ways. First, seeds from immature fruits may have lower
germination success due to the presence of immature embryos and second, even if the seeds
are viable and germinate, seeds dropped under parent trees commonly experience higher
density-dependant mortality (Janzen 1970; Nathan and Casagrandi 2004). Finally, we found
that the percentage of swallowed seeds decreased with seed size, which also has been
reported in other primate studies (e.g., Ateles geoffroyi, A. palliata, and C. capucinus:
Chapman 1989; L. lagotricha: Stevenson et al. 2005). Although from the animal’s
perspective spitting out (or dropping) medium ( 0.5–1.5 cm in length) to large (> 1.5 cm in
length) seeds may be the most successful seed handling strategy, the ability of these
primates to swallow large seeds certainly favors seed dispersal of large-seeded species in
continuous and fragmented forests (e.g., Attalea butyracea and Spondias spp.). However,
this does not necessarily imply that spider monkeys are more effective dispersers for small
than for large-seeded species, but rather the amount of swallowed seeds for each fruit
species is negatively affect by their seed size due to mechanical limitations related to fruit
and seed handling (Jordano 1995). Further information about seed dispersal distance and
seed fate is needed to clarify whether spider monkey seed dispersal effectiveness differs
between seeds with contrasting sizes.

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Defecation Pattern and Defecated Seed Assemblages
The effectiveness of primates as seed dispersers largely depends on the defecation pattern,
and diversity of seeds in feces. The higher the number of scattered depositions, seeds
dispersed, and seed species in feces, the higher the probability of successful seed dispersal
and seedling recruitment due to a decrease in both the density and/or distance dependent
mortality near parents (Howe 1989; Muller-Landau and Hardesty 2005) and sibling
competition for resources (Cheplick 1992; Queenborough et al. 2007 ). Although, most
defecations were scattered in both forest conditions, the proportion of feces without seeds
was significantly higher in fragments than in continuous forest suggesting that some aspects
of seed dispersal effectiveness may be negatively affected by fragmentation. Additionally,
the greater proportion of feces without seeds, as well as the higher number of species
contributing to the top defecated seed species is likely due to changes in foraging patterns
in fragments (described above).
Fecal samples contained seeds from 71 plant species (46 in continuous and 51 in
fragments), indicating that spider monkeys provide seed dispersal services for many fleshy
fruit species in both forest conditions. The number of defecated seed species was notably
higher than that reported for spider monkeys in tropical dry forests (Chapman 1989) and for
most Alouatta species in many tropical forests (Table S1), however, we found fewer plant
species than those reported for some South American primates (e.g., Alouatta seniculus:
Julliot 1996, Ateles belzebuth: Link and Di Fiore 2006; Table S1). This result can be
explained by the higher plant species diversity in South America in comparison with
Mesoamerica (Gentry 1982). Overall, dietary diversity in Ateles spp. is directly related with
both proximity to the equator and mean annual rainfall (Di Fiore et al. 2008).

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Despite the large number of seed species in feces, only a small number of species
were abundant. This pattern is consistent with the selective foraging behavior characteristic
of spider monkeys throughout their geographic range (Di Fiore et al. 2008; González-
Zamora et al. 2009). In general, spider monkeys prefer to feed on species with large tree
sizes, fleshy fruits, long fruiting periods and clumped distributions (Di Fiore et al. 2008).
Our results concur with two recent reviews (Di Fiore et al. 2008; González-Zamora et al.
2009), showing that plant families such as Moraceae, Fabaceae and Anacardiaceae, and
genera such as Ficus, Brosimum, Spondias, Dialium and Inga are keystone species for
spider monkeys.
Effects of Gut Passage
In the five plant species evaluated, seed germination was significantly higher in defecated
than in control seeds. This finding illustrates the positive effect that spider monkeys have
on seed germination, a finding similar to that observed in other Neotropical primates (e.g.,
Alouatta, Cebus and Lagothrix; Table S1). Additionally, while some primates can
negatively affect the germination of some plant species (see Table S1), in our study A.
geoffroyi did not affect negatively the germination for any of the species studied,
suggesting that it may be a more efficient seed disperser than some other highly
frugivoruous species. For example, negative gut passage effect on seed germination ranges
from 5% in Lagothrix lagotricha (Stevenson et al. 2002) to 28.6% in Ateles belzebuth (Link
and Di Fiore 2006).
Although our study has some limitations that make it difficult to infer the effects of
seed dispersal by these monkey communities on plant populations (e.g. we did not

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determine fruit availability in each study site, we did not provide a quantification of seed
dispersal at the monkey population level, we restricted the germination tests to a small
number of species, and we did not evaluate the final fate of defecated seeds), our findings
clearly demonstrate that, at least for the aspects of effectiveness evaluated, spider monkeys
are efficient seed dispersers in both continuous forest and fragments. Dispersal services
provided by spider monkeys in Lacandona may be especially important for large-seeded
species such as Ampelocera hottlei and Spondias spp. (Chaves et al., unpublished data),
due to the limited number of animals that can swallow seeds of these large-seeded species
(e.g. Stevenson and Aldana 2008). Although evidence suggests relationships among
angiosperms and their animal dispersers are generally best described as diffuse networks
rather than close coevolutionary relationships (see Herrera 1985), services provided by
legitimate dispersers, such as spider monkeys, undoubtedly may favor gene flow, and
recruitment of their top food plant species (Schupp and Fuentes 1995; Stevenson et al.
2002). We suggest that more long-term studies quantifying seed dispersal by spider
monkeys at the population level, as well as the final fate of defecated seeds are critical to
improve our understanding about the contribution of spider monkeys (and other
Neotropical primates) to plant regeneration.
Acknowledgements This research was supported by grants from the Consejo Nacional de
Ciencia y Tecnología, México (CONACyT Grant CB-2005-51043 and CB-2006-56799).
This paper constitutes a partial fulfillment of the Graduate Program in Biological Sciences
of the National Autonomous University of México (UNAM). The organization Idea Wild
provided equipment. This study would not have been possible without the collaboration of
the local people in Loma Bonita, Chajul, Reforma Agraria and Zamora Pico de Oro ejidos.

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V. Sork, D. Scofield, P. Thompson, and M. Quesada provided useful comments and
suggestions in advanced drafts of this paper. We thank to C. Hauglustaine, C. Balderas, S.
Martínez, J. Herrera, A. González-Di Pierro and R. Lombera for field assistance. J.
Rodríguez collaborated in the identification of seeds, and J. M. Lobato, G. Sánchez, H.
Ferreira, and A. Valencia provided technical support. We also thank J.M. Setchell, E.W.
Shcupp and one anonymous reviewer for valuable criticisms and suggestions that improved
the manuscript.
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Electronic supplementary material The online version of this article (doi:__) contains
supplementary material which is available to authorized users.

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Table I Seed handling and seed size of top fruit species in the diet of A. geoffroyi
communities inhabiting continuous forest and forest fragments in Lacandona, Chiapas.
% Seed handling
Forest
condition/species Family Mean Seed
size (cm. %TFTa n Swallowed Spat out Dropped
Continuous forest
Spondias radlkoferi Anacardiaceae 3.87 33.1 661 10.4 37.4 47.0
Ficus sp1 Moraceae <0.1 10.3 27 100 0 0
Spondias mombin Anacardiaceae 1.97 9.5 151 31.8 25.8 33.8
Ficus tecolutensis Moraceae <0.1 7.0 155 100 0 0
Calatola laevigata Icacinaceae 1.20 5.6 35 100 0 0
Ampelocera hottlei Ulmaceae 1.38 5.4 126 36.9 59.1 3.6
Ficus obtusifolia Moraceae <0.1 3.9 68 100 0 0
Brosimum alicastrum Moraceae 1.58 3.4 85 14.2 61.2 24.6
Inga punctata Fabaceae 1.32 2.1 27 75.9 24.1 0
Forest fragments
Spondias radlkoferi Anacardiaceae 3.87 20.5 358 7.1 32.5 59.6
Brosimum alicastrum Moraceae 1.58 13.4 182 12.5 65 22.5
Ficus tecolutensis Moraceae <0.1 10.2 188 100 0 0
Ficus sp1 Moraceae <0.1 9.3 194 99.0 1.0 0
Dialium guianense Fabaceae 1.01 7.7 40 13.8 86.3 0
Sabal mexicana Arecaceae 0.60 4.3 87 78.7 21.3 0
Ficus sp2 Moraceae <0.1 4.2 77 100 0 0
Calatola laevigata Icacinaceae 1.20 4.0 40 100 0 0
Spondias mombin Anacardiaceae 1.97 3.8 64 6.3 17.2 76.6
Inga punctata Fabaceae 1.32 2.5 40 100 0 0
The number of seed handling records for each plant species is indicated (n). All species are
trees with the exception of the palm Sabal mexicana
aSpecies were ranked based on the percent of time spent consuming each fruit species in
relation to the total time spent consuming all fruit species until the sum was 80%

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Table II Top defecated seed species in A. geoffroyi communities inhabiting continuous
forest and forest fragments in Lacandona, Chiapas
Forest condition/species Family GF FR %TFRan %US
Continuous forest
Spondias radlkoferi Anacardiaceae Tree 187 26.8 579 100
Ficus tecolutensis Moraceae Tree 85 12.2 >23300 ─
Cissus verticillata Vitaceae Vine 57 8.2 250 100
Spondias mombin Anacardiaceae Tree 47 6.7 136 100
Guarea glabra Meliaceae Tree 40 5.7 142 100
Ampelocera hottlei Ulmaceae Tree 39 5.6 174 95.0
Dialium guianense Fabaceae Tree 39 5.6 202 97.5
Celtis iguanaea Ulmaceae Vine 29 4.2 216 100
Paullinia costata Sapindaceae Vine 18 2.6 59 100
Ficus sp1 Moraceae Tree 18 2.5 >2800 ─
Fragmented forest
Ficus tecolutensis Moraceae Tree 140 22.3 >58800 ─
Sabal mexicana Arecaceae Palm 50 8.0 293 100
Dialium guianense Fabaceae Tree 46 7.3 161 93.7
Guarea glabra Meliaceae Tree 46 7.3 120 100
Ficus sp1 Moraceae Tree 32 5.1 >4450 ─
Spondias radlkoferi Anacardiaceae Tree 28 4.5 154 96.4
Guarea grandifolia Meliaceae Tree 26 4.2 93 100
Inga sp1 Fabaceae Tree 22 3.5 233 86.4

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Castilla elastica Moraceae Tree 21 3.4 90 100
Spondias mombin Anacardiaceae Tree 19 3.0 77 100
Acacia farnesiana Fabaceae Shrub 14 2.2 64 92.3
Ficus sp2 Moraceae Tree 14 2.2 >2000 ─
Attalea butyracea Arecaceae Palm 10 1.6 15 100
Bactris balanoidea Arecaceae Palm 8 1.3 16 100
Inga sp2 Fabaceae Tree 7 1.1 68 100
Sapium sp. Euphorbiaceae Tree 6 1.0 91 100
Celtis iguanaea Ulmaceae Vine 4 0.6 39 100
Faramea occidentalis Rubiaceae Shrub 4 0.6 27 100
Ficus sp3 Moraceae Tree 4 0.6 >300 ─
Nectandra sp. Lauraceae Tree 4 0.6 23 100
Column headings: GF = growth form; FR = number of fecal records; %TFR = percent of
total fecal records; n = total number of seeds in feces; %US = percent undamaged seeds for
each plant species; ─ = undetermined data. Species are ordered based on %TFR
aSpecies were ranked based on the percent of fecal records in which each seed were found
in relation to the total fecal records for all seed species until the sum was 80%

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Table III Germination success of defecated versus control seeds
% Germination
Plant species Defecated n Control n G-test p Effect
Ampelocera hottlei 33 15 6.6 15 7.93 0.005 +
Brosimum lactescens 100 15 29 14 23.9 0.0008 +
Cissus verticilata 55 20 6.2 16 10.8 0.001 +
Faramea occidentalis 90 10 50 16 4.9 0.03 +
S. radlkoferi 38 24 2.5 40 14.6 0.001 +
Germination trials were 90 days except for B. lactescens which was 20 days.

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Figure legend
Fig. 1 Seed handling in continuous and fragmented forest in Lacandona, Chiapas. Different
capital letters indicate significant differences among forest conditions, while different lower
case letters indicate differences among seed handling categories within each habitat
(contrast tests, p < 0.05).

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Fig. 1
B b
A b
A a
A a
A a
B a
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
Continuous Fragmented
Forest condition
Proportion of feeding records
Swallowed Spat out Dropped

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Electronic Supplementary Material
Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed
Dispersers in Continuous and Fragmented Rainforests in Southern
Mexico
Journal: International Journal of Primatology
Authors: O. M. Chaves1; K. E. Stoner1; V. Arroyo-Rodríguez1; J. Benítez-Malvido1 & A.
Estrada2
1Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México
(UNAM), Antigua Carretera a Pátzcuaro No. 8701, Ex Hacienda de San José de la Huerta,
58190 Morelia, Michoacán, Mexico
email: ochaba@gmail.com
2Laboratorio de Primates, Instituto de Biología, Universidad Nacional Autónoma de
México. Apartado Postal 176, San Andrés Tuxtla, Veracruz, Mexico

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Study Area
Fieldwork was conducted during a 15-mo period in 2007 and 2008 in the Lacandona
rainforest, southern Chiapas, Mexico (16°05'58" N, 90º52'36" W; elevation 10–50 m a.s.l.).
Covering parts of Mexico, Guatemala, and Belize, this region encompasses the largest
portion of tropical rainforest in Mesoamerica and one of the most important in the
Neotropics (Dirzo 1994). The original vegetation in the area is lowland tropical rainforest
and semideciduous rainforest. The climate in the region is hot and humid with 24 °C
average temperature and 2881 mm average annual rainfall. Greatest rainfall concentration
is found in June–September (range: 423–511 mm/month), and lowest in February-April
(46–61 mm/month) (Comisión Federal de Electricidad, Mexico, unpublished data).
The study was conducted in two adjacent areas separated by the Lacantún river: the
Marqués de Comillas region (MCR, eastern side of the river), and the Montes Azules
Biosphere Reserve (MABR, western side) (Table S2). Human colonization of MCR began
in the 1960’s (Mendoza and Dirzo 1999), and cattle ranching resulted in the rapid
disappearance and fragmentation of the forest. Approximately 50% of the land surface of
MCR is currently used for agricultural purposes, but small (0.5–30 ha) and large (850–1465
ha) fragments still remain in the area. The protected area of MABR was created in 1978
and consists of approximately 300 000 ha of continuous forest.
Methodological Details of Feeding Behavior
Focal animals were randomly changed at 5-min intervals or when animals moved out of
sight. Since spider monkeys split into foraging subgroups, data were collected from more

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than one subgroup throughout the day whenever possible. We collected 116 observation
days in continuous forest and 107 observation days in fragments. These observation days
corresponded to 18923 5-min records in 1000 h of focal observations (496 h in continuous
forest and 504 h in fragments), from which 442 h (44.2%) were feeding observations (204 h
in continuous forest and 238 h in fragments).
Tree Composition, Statistical Analysis and Results
To determine the vegetation structure in continuous and fragmented forests, we fixed 10 50
× 2 m linear transects randomly (Gentry 1982) within each of the 6 sites, for a total of 60
transects. We recorded all trees and shrubs with diameter at breast height (DBH) ≥10 cm.
To compare adult tree community structure among the six study sites, we used a Principal
Component Analysis (PCA) and a nonparametric t-test (Mann-Whitney U test) to compare
the PCA component scores between continuous and fragmented forests (for the first axis,
which explained 59.4% of total variance, Table S3, Fig. S1). To compare the abundance of
fruit trees exploited in four different DBH categories (10–30 cm, 30–50 cm, 50–70 cm and
>70 cm) in each forest condition, we used generalized linear models (GLM) fixing a
Poisson distribution and log-link function to the response variable (Crawley 1993). To
identify which DBH categories were statistically different among each other we used post-
hoc analyses with contrasts (Crawley 1993). All statistical analyses were performed using
JMP software (version 7.0, SAS Institute, Cary, N.C.).
Tree composition between continuous and fragmented forests was not significantly
different (Mann-Whitney U = 6, df. = 1, p = 0.51, Fig. S1). We found significant
differences in the number of individuals among DBH categories (χ2 = 106, df = 6, p <

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0.0001), being the number of individuals in the latter DBH category (>70 cm) greater in
continuous than in disturbed forests (contrast test, p = 0.04). However, no other significant
differences were detected in the other DBH categories (p > 0.05, Fig. S2).

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Table S1 Seed dispersal by twelve Neotropical primates
Gut passage net effect
Primate species
% FRU DSS
(no. feces)
Seed length
(cm)
% FWS
(no. feces) n %Positive %Negative %Neutral
Site Ref
Alouatta guariba ─ 14 (─) ─ 45 (66) 4 75 25 0 FBR 1
A. palliata 28 12 (53) ─ 15.1 (─) ─ ─ ─ ─ SRNP 2
A. palliata ─ 15 (250) <0.1–3.5 ─ 6 83.3 0 16.7 TUX 3
A. palliata ─ 9 (─) <0.1–2.4 46 (31) ─ ─ ─ ─ PVNP 4
A. seniculus ─ 80 (─) ─ ─ 7 57.1 14.3 28.6 TNP 5
A. seniculus 44 14 (27) ─ 21 (─) ─ ─ ─ ─ MNP 6
A. seniculus ─ 86 (236) <0.1–4 ─ 17 23.5 35.3 41.2 NS 7
Brachyteles arachnoides ─ 18 (─) ─ 21 (25) 6 50 16.7 33.3 FBR 1
Cebus capucinus ─ ─ ─ ─ 9 55.5 22.2 22.3 BCI 8
C. capucinus 81 14 (28) ─ 0 (─) ─ ─ ─ ─ SRNP 2
C. capucinus ─ 30 (─) <0.1–>1.5 2 (3) ─ ─ ─ ─ PVNP 4
C. capucinus 53 67 (─) 0.1–3 7.5 (13) ─ ─ ─ ─ BCI 9
Lagothrix lagotricha ─ 76 (─) ─ ─ 16 50 6.2 43.7 TNP 5

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Saguinus mystax 70 67 (1094) 0.06–2.3 5.2 (57) ─ ─ ─ ─ EBQB 10
S. fuscicollis 60 81 (1376) 0.06–2.3 3.8 ( 52) ─ ─ ─ ─ EBQB 10
S. midas 87.5 12 (─) 0.5–2.4 ─ ─ ─ ─ ─ FVI 11
Ateles belzebuth ─ 75 (─) ─ ─ 14 42.8 28.6 28.5 TNP 5
A. belzebuth 79 133 (916) <0.1–4 ─ ─ ─ ─ ─ YNP 12
A. belzebuth 87 27 (144) <0.2–2.7 1 (176) ─ ─ ─ ─ YNP 13
A. paniscus 80 71 (47) ─ 0 (─) ─ ─ ─ ─ MNP 6
A. geoffroyi 78 17 (39) ─ 0 (─) ─ ─ ─ ─ SRNP 2
A. geoffroyi 54 71 (957)a <0.1–4.5 9.9 (95) 6 83.3 0 0 LAC 14
Abbreviations: DSS, number of defecated seed species; %FRU, percent of fruit in the diet; %FWS, percent fecal samples without seeds; SDD,
seed dispersal distance (m); (─) data unavailable.
Site abbreviations: BCI, Barro Colorado Island, Panama; EBQB, Estación Biológica Quebrada Blanco, Perú; FBR, Fazenda Barreiro Rico,
Brazil; FVI, Fazenda Vitória, Brazil; LAC, Lacandona, Chiapas, Mexico; MNP, Manú National Park, Peru; NS, Nouragues Station, French
Guiana; PVNP, Palo Verde National Park, Costa Rica; SRNP, Santa Rosa National Park, Costa Rica; TNP, Tinigua National Park, Colombia;
TUX, Los Tuxtlas Biological Station, Mexico; YNP, Yasuní National Park, Ecuador.
References: 1. Martins (2006); 2. Chapman (1989); 3. Estrada and Coates-Estrada (1984); 4. Wehncke et al. (2004); 5. Stevenson et al. (2002); 6.
Andresen (1999); 7. Julliot (1996); 8. Wehncke and Dalling (2005); 9. Stevenson (2000); 10. Knogge and Heymann (2003); 11. Oliveira and
Ferrari (2000); 12. Link and Di Fiore (2006); 13. Dew (2008); 14. present study.

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Table S2 Study sites and groups of Ateles geoffroyi studied in the Montes Azules
Biosphere Reserve (MABR) and the Marqués de Comillas region (MCR), Chiapas,
Mexico
Study site Size (ha) Location
DNF
(m)
DCF
(m) YSF
Group
size
Continuous forest 331000 Montes Azules Biosphera Reserve
C1 ─ 16°06'58.2"N, 90°56'18.4"W ─ ─ ─ 40
C2 ─ 16°09'32.0"N, 90°54'06.6"W ─ ─ ─ 36
C3 ─ 16°09'40.0"N, 90°54'04.5"W ─ ─ ─ 44
Forest fragments
F1 31 16°19'24.5"N, 90°50'43.7"W 150 1200 24 39
F2 14.4 16°19'52.0"N, 90°51'06.1"W 450 200 29 35
F3 1125 (16°15'12.2"N, 90°49'59.5"W) 100 1100 26 41
DNF, distance to the nearest forest fragment; DCF, distance to the continuous forest;
YSF, years since fragmentation
Table S3 Principal component scores for the three main axes by study site
Study site PC 1 PC 2 PC 3
C1 1.2 0.14 -0.61
C2 1.12 -0.23 0.02
C3 1.17 0.8 0.82
F1 1.35 0.07 -0.23
F2 0.94 -1.1 0.44
F3 0.77 0.13 -0.47
Percent of total variance explained 59.40% 15.30% 12.1%

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Figure S1. Principal component analysis of tree composition by study site. The percent
of total variance explained by each axis is indicated in parenthesis.
Figure S2. Total abundance of fruit trees in the diet of spider monkeys by forest
condition and DBH category. Different letters on the bars indicate significant
differences (p < 0.05).
-
2-10 1 2
-2
-1
0
1
2
PC1 (59.4%)
PC2 (15.3%)
C3
C1
F3
F1
C2
F2
a
a
a
a
b
a
a
a
0
10
20
30
40
50
60
10–30 cm 30–50 cm 50–70 cm >70 cm
DBH category
No. individual
s
Continuous forest
Fragmented forests

117
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CAPÍTULO III

120
Short title: Activity Patterns of Spider Monkeys in Mexico
Seasonal Differences and Shifts in Activity Patterns of Spider Monkeys
Living in Forest Fragments in Southern Mexico
(accepted with major changes 15 March 2010, International Journal of Primalogy, IF=1.78)
Óscar M. Chaves*, Kathryn E. Stoner, Víctor Arroyo-Rodríguez
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México.
Morelia, Michocán, Mexico.
2
Óscar M. Chaves (corresponding author), Kathryn E. Stoner, Víctor Arroyo-Rodríguez
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de Mexico,
Antigua Carretera a Pátzcuaro No. 8701, Ex Hacienda de San José de la Huerta, 58190
Morelia, Michoacán
email: ochaba@oikos.unam.com

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Abstract. Understanding how primates adjust their behavior to resource limitations
imposed by habitat fragmentation is a fundamental challenge for primatologists and
conservation biologists. During a 15-month period, we studied the activity patterns of six
communities of Ateles geoffroyi living in continuous forest and fragments in the Lacandona
rainforest, Mexico. We tested, for the first time, the effects of forest type (continuous and
fragmented), season (dry and rainy) and the interaction between these variables on activity
patterns of this primate. Overall, monkeys spent more time feeding in fragments than in
continuous forest, while traveling showed the opposite pattern. These results can be
explained by both a more folivorous diet and the spatial limitations in fragments. Regarding
seasonality, time spent feeding was higher in the rainy than in the dry season, whereas time
spent resting followed the opposite pattern. We suggest these results are likely related to the
lower fruit availability during the dry season (and concomitant increase in percent leaves
consumed) and higher temperature, both contributing to ‘force’ monkeys to spend more
time resting. Forest type and seasonality did not interact with activity patterns, indicating
that the effect of seasonality on activities was similar across all sites. Although our findings
confirm that spider monkeys are able to make behavioral shifts in forest fragments and
during the dry season, further studies are necessary to assess if these shifts are adequate to
assure their health, fitness, and most importantly, their long-term persistence in fragmented
habitats.
Keywords Ateles geoffroyi; behavioral flexibility; environmental stresses; habitat
fragmentation; Lacandona

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Introduction
Habitat fragmentation imposes critical resource limitations for survival and reproduction of
tropical vertebrates (e.g., fish, mammals: Brook 2003; birds: Sehgal 2010; primates:
Chapman et al. 2007). This is particularly important for arboreal primates, as they rely on
the presence and abundance of large canopy food trees (Arroyo-Rodríguez et al. 2007;
Arroyo-Rodríguez and Dias 2009; Stevenson 2001), and changes in vegetation derived
from fragmentation can result in reduced food availability (e.g., reduced tree basal area:
Arroyo-Rodríguez and Mandujano 2006; Laurance et al. 1997; reduced plant species
richness: López et al. 2005). This process may be particularly critical during periods of
food scarcity in seasonal forests (e.g., Hemingway and Bynum 2005; Stoner and Timm
2004). Food availability is often lower during the dry season than during the rainy season
(Hemingway and Bynum 2005; Zimmerman et al. 2007), and hence, this could have
negative effects on food availability for primates. Although some primates can make
behavioral adjustments to cope with resource limitations in fragmented and/or seasonal
habitats (Hemingway and Bynum 2005; Jones 2005), our current knowledge about this
topic is scarce, even when considering the most studied primates (e.g., howler monkeys:
Arroyo-Rodríguez and Dias 2009).
A few studies have demonstrated that primates can adjust their behavior in response
to habitat and seasonal-related differences in resource availability. Overall, these studies
indicate that in response to fragmentation and seasonal fruit scarcity and adverse climatic
conditions, primates often switch to lower-quality diets (e.g., a more folivorous diet:
Hemingway and Bynum 2005; Onderdonk and Chapman 2000), which may increase the
time spent feeding and hence can affect time devoted to other core activities such as

123
traveling and/or resting (Dunbar 1992; Korstjens et al. 2010). For instance, activity patterns
of some primates change in response to resource limitations in fragments (e.g., guenons
spend a low time feeding in fragments: Tutin 1999; howler monkeys spend more time
feeding after the partial deforestation of their habitats; Clarke et al. 2002). In Colombia,
populations of Alouatta seniculus inhabiting in a continuous forest spend 59% of their total
activity budget resting (Stevenson et al. 2000), while in forest fragments this percentage
increases to 78% (Gaulin and Gaulin 1982).
Seasonal variation in food availability also can ‘force’ primates to shift activity
patterns. For example, African primates respond to seasonal food scarcity by spending less
time resting and in social activities (e.g., baboons: Dunbar 1992) or spending more time
feeding on leaves and reducing day range and party size during the dry season than during
rainy season (e.g., chimpanzees: Doran 1997). Similarly, during periods of high-frugivory
(i.e., during the rainy season) gorillas spend less time feeding and more time traveling than
during the dry season (Masi et al. 2009).
This evidence shows that activity patterns of some species of primates are
influenced by forest type and seasonality (Dunbar et al. 2009), nevertheless, few studies
have evaluated the effects of forest type (i.e., continuous and fragmented) and seasonality
simultaneously. In the Neotropics, Ateline primates may be particularly amenable subjects
for this type of research since they typically live in seasonal environments where food
abundance and distribution can vary greatly over the course of a year (Di Fiore and
Campbell 2007). However, studies evaluating the potential effects of fragmentation and/or
seasonality on activity patterns of this taxon are scarce, and mainly focused on more
folivorous species such as howler monkeys (e.g., Bicca-Marques 2003; Cristóbal-Azkarate
and Arroyo-Rodríguez 2007; Stoner 1996). Although a number of studies have briefly

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described the activity patterns of frugivorous Ateline primates such as Lagothrix spp. (e.g.,
Defler 1995; Stevenson et al. 1994) and spider monkeys (Ateles spp.) in continuous forests
(reviewed by Di Fiore and Campbell 2007; Wallace 2001; Table 1), no studies to date have
attempted to determine how resource limitation imposed by fragmentation and seasonality
modify their activity patterns.
Here we assess variations in activity patterns of spider monkeys (Ateles geoffroyi
vellerosus) in two contrasting forest types (continuous and fragmented) and during two
seasons (dry and rainy) in the Lacandona rainforest, southern Mexico. We discuss our
results in relation to documented variations in primate diet and food availability across the
study sites in the same monkey communities (Chaves et al. in press). We hypothesize that
spider monkeys can adjust their activity patterns in order to deal with food scarcity in forest
fragments and during the dry season. We expect that feeding time will be greater in
fragments than in continuous forest in order to compensate for the lower abundance and
quality of foods for primates frequently found in fragments (e.g., Onderdonk and Chapman
2000). Furthermore, since both fragmentation and fruit scarcity in the dry season often
force primates to increase their consumption of low-energy content items such as leaves,
we expect that in fragments and during the dry season time spent resting will be higher
because resting is an energy-saving strategy particularly important during digestion of
fibrous material (Korstjens et al. 2010; Milton 1981a). Finally, since during the dry season
animals are exposed to more stressful conditions than during the rainy season (e.g.,
temporal food scarcity, drought, high ambient temperature: Murphy and Lugo 1995; Stoner
and Timm 2004), we also expect that spider monkeys will spend less time in high energy-
cost activities, such as feeding and traveling (Asensio et al. 2009) in the former than in the
latter season.

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This is a timely study for the conservation of this critically endangered primate, as
the Lacandona rainforest has been highly fragmented during the last 40 years, but several
small communities of spider monkeys still remain isolated in some forest fragments
(Chaves et al. in press). Understanding how primates cope with environmental stresses
(e.g., food scarcity) in fragmented and seasonal forests, such as the one we studied, is
therefore critical for the design and establishment of appropriate management strategies for
the conservation of this and many other animal species.
Methods
Study Area
Fieldwork was conducted in the Lacandona rainforest, southern Chiapas, Mexico
(16°05'58" N, 90º52'36" W; elevation 10–50 m a.s.l.). This region encompasses the largest
portion of tropical rainforest in Mesoamerica, covering parts of Mexico, Guatemala, and
Belize (ca. 800,000 ha, De la Maza and De la Maza 1991). The original vegetation in the
area is lowland tropical rainforest and semideciduous rainforest. The region is highly
seasonal presenting two clearly defined seasons: a rainy season (June-December) and a dry
season (January-May). Average annual rainfall is 2881 mm, and the greatest rainfall
concentration is found in June-September (ranging from 423 to 511 mm/month), while the
lowest is found in February-April (ranging from 46 to 60.6 mm/month). Average annual
temperature is 24 °C, being greater in the dry season (average per month: 26.3 °C; range
22–28 °C) than in the rainy season (average per month: 23.5 °C; range: 20–25 °C). Average
maximum daily temperature occurs in the dry season from March to May (ca. 38 °C in each
month; Comisión Federal de Electricidad, Mexico, unpublished data). Average monthly

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temperature in fragments is ca. 2 °C greater than in continuous forest (González-Di Pierro
et al. in press). Although there are no long-term published records of phenological data for
the region, an 8-year study of tree community dynamics indicates that fleshy fruit (the main
food item for A. geoffroyi; González-Zamora et al. 2009) production at Lacandona is
concentrated within the rainy season, while fruit is scarce during the dry season (M.
Martínez-Ramos, unpublished data). This pattern is consistent with that observed in other
Neotropical rainforests (see Zimmerman et al. 2007).
The study was conducted in 2 adjacent areas separated by the Lacantún River: the
Marqués de Comillas region (MCR, eastern side of the river) encompassing ca. 176,200 ha
of disturbed forests and human settlements (Marquez-Rosano 2006) and the Montes Azules
Biosphere Reserve (MABR, western side) comprising ca. 331,000 ha of old-growth
undisturbed forest (Gómez-Pompa and Dirzo 1995). Human colonization and deforestation
of MCR began in the decade of the sixties and cattle ranching resulted in the rapid
disappearance and fragmentation of the forest (Marquez-Rosano 2006). Approximately
50% of the land surface of MCR is nowadays used for agricultural purpose, but several
forest fragments (0.5–1500 ha) still remain in the area.
Study Sites and Spider Monkey Communities
We studied activity patterns of 6 independent spider monkey communities: 3 communities
located in 3 different areas within the MABR continuous forest separated by at least 4 km,
and 3 communities located in 3 different forest fragments within the MCR (Table 2). We
chose these sites because they were occupied by well-habituated monkey communities (i.e.,
the monkeys were habituated to tourists, researchers, and local people that visit these sites).

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In addition, all the study fragments were easily accessible, and have been protected by the
land owners since 1985 (avoiding potential confounding effects of hunting and selective
logging). These communities ranged from 35 to 44 individuals, and their home ranges
varied from 14 to 90 ha (Table 2). All fragments in MCR were isolated ≥ 24 years ago, and
their sizes were 14, 31, and 1125 ha (Table 2). Despite the variation in size, we consider all
three sites as fragments because all: (1) are surrounded by an anthropogenic matrix (i.e.,
crops, pastures, and human settlements) and are isolated from the continuous forest by 200–
1200 m, and (2) the vegetation has noticeable signs of disturbance (e.g., plantations such as
Teobroma cacao and Aechmea magdalenae, and lower density of emergent trees in the
canopy, see below). Fragments F1 and F2 each contained 1 monkey community. Although
fragment F3 contained 3 monkey communities, they could be distinguished by their home
ranges, group composition and individuals with unique marks (see below), and we only
studied 1 of the 3 communities. In addition to the forest fragment, the monkey community
inhabiting fragment F1 also exploited adjacent areas in the matrix consisting of cocoa
plantations (2.5 ha), a 9-year old secondary forest (5 ha), and live fences and pastures (ca.
10 ha) with isolated adult trees of several top food species for A. geoffroyi including Ficus
insipida, Brosimum alicastrum, Inga spp., and Spondias spp (see González-Zamora et al.
2009). Similarly, the monkey community inhabiting fragment F2 exploited an additional
area comprised of cocoa plantations (2 ha) and a 12-year old secondary forest (3.7 ha).
During our study, monkey communities did not present inter-site movements between
fragments, or between fragments and the continuous forest.
A detailed description of the diet and food availability within the home range of
each monkey community has been reported elsewhere (Chaves et al. in press); only a brief
overview is given here to facilitate the interpretation of our results about activity patterns.

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The diet of the A. geoffroyi communities within the study sites is comprised of 121 plant
species belonging to 39 families. Overall, fruits are the most eaten item (56% of total
feeding time, 21 species), followed by leaves (18.5%, 66 species), and other plant items.
The consumption of both mature and immature leaves is higher in fragments than in
continuous forest. In our 6 study sites food availability is lower in forest fragments than
continuous forest (Chaves et al. in press). Although the average number of food plant
species is similar in continuous forest and fragments (71 versus 66 species), the average
density of large trees (DBH > 60 cm) of fleshly-fruit species is higher in continuous than
fragmented habitats (4 versus 1.3 stems/1000 m2). Additionally, the sum of the Importance
Value Index (IVI) of top food species is also greater in continuous forest (IVI = 249) than
in fragments (IVI = 166). Furthermore, some top food species for spider monkeys such as
Ampelocera hottlei, Brosimum alicastrum, Pouteria campechiana, and Virola
guatemalensis are much less abundant (if not absent) in fragments than in continuous forest
(Chaves et al. in press). Since we did not report seasonal variation in the diet composition
of spider monkeys in our previous study on diet, we used the same data base and
methodology described by Chaves et al. (in press) to calculate this and report it here.
Activity Pattern Data Collection
Activity patterns of spider monkey communities were studied during a 15-mo period: 6
months in the dry season (February-April 2007 and 2008), and 9 months in rainy season
(May-October 2007, and August-October 2008). We used high resolution binoculars to
record the activity patterns of each of 6 communities during 3 consecutive days once every
3 weeks, using focal animal sampling (Altmann 1974). We alternated observations among

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communities every 3 days. Individuals were identified utilizing unique marks found in skin
pigmentation, hair, genitals (shape, size, and pigmentation of clitoris and penis), face
(distinctive facial shapes), body size, and other distinguishing marks such as scars. Focal
animals were randomly changed after each 5-min interval or when animals moved out of
sight. Whenever possible, data were collected from >1 subgroup throughout the day. Data
were collected from 0700 h to 1730 h, totaling 1010 h of focal observations (496 h in
continuous forest and 514 h in fragments). To minimize the potential effect of age class
(i.e., adults, subadults, juveniles, and infants) on monkey behavior, all focal individuals
included in our analyses were adults or subadults.
During the focal observations we recorded 4 mutually exclusive activities: 1)
feeding (masticating or consuming food items), 2) resting (period of inactivity), 3) traveling
(movement between tree crowns or within the crown of a tree that was not directly food
related), and 4) other activities (e.g., social activities).
Data Analysis
We used an analysis of deviance (ANODE) with a generalized linear model (Crawley
2002) to compare activity patterns among forest types and seasons. Since in each study site
we observed an independent monkey community, we considered each of the three sites per
forest type as replicas. Proportion time data were first arcsine-transformed, and we used a
Normal distribution with an identity link-function with the response variable (Crawley
2002). The whole model was: TIME = ACTIVITY + FOREST + ACTIVITY*FOREST +
SEASON + SEASON*ACTIVITY + SEASON*FOREST +
ACTIVITY*FOREST*SEASON (asterisks indicate interactions among factors). To

130
identify the levels of each factor that were statistically different between each other we used
post-hoc analyses with contrasts (Crawley 2002). A similar statistical procedure was used
to compare the proportion of time devoted to each plant item (i.e., fruits, leaves, branch
piths, flowers, and others) between seasons. Statistical analyses were performed using JMP
software (version 7.0, SAS Institute, Cary, N.C.).
Results
Overall, spider monkeys spent different amounts of time per activity (ACTIVITY; χ2 =
94.9, df = 3, p < 0.0001), with time feeding (average percentage ± SD, 44 ± 9% of total
time) and resting (34 ± 7%) higher than time spent traveling (12 ± 4%) and other activities
(10 ± 3%) (contrast tests, p < 0.01 in all cases; Fig. 1). However, notable variations in
percentages of time spent in each activity were observed across sites and seasons (Table 3).
Activity patterns differed between forest types (ACTIVITY*FOREST; χ2 = 9.9, df =
3, p = 0.02, Fig. 1A) with the percentage of time spent feeding significantly higher in forest
fragments (average percentage ± SD, 48 ± 9%) than in continuous forest (41 ± 8%),
whereas traveling was higher in continuous forest (15 ± 4%) than in fragments (9 ± 2%)
(contrast test, p < 0.03; Fig. 1A). Time spent resting and in other activities did not differ
between forest types (contrast tests, p > 0.1 in both cases; Fig. 1A).
Activity patterns also differed between seasons (ACTIVITY*SEASON; χ2 = 17.2,
df = 3, p = 0.0006; Fig. 1B). The percentage of time spent feeding was higher in the rainy
(51 ± 10%) than in the dry season (37 ± 11%; contrast test, p < 0.001; Fig. 1B), whereas
resting was higher in the dry (38 ± 8%) than in the rainy season (29 ± 9%; contrast test, p =
0.02; Fig. 1B). Both of these patterns were observed across most study sites (with exception

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of C2; Table 3). Time dedicated to traveling and to other activities did not differ between
seasons (contrast test, p > 0.05 in all cases; Fig. 1B). Finally, we found that forest type and
season did not interact with activity patterns (ACTIVITY*FOREST*SEASON; χ2 = 1.3, df
= 3, p = 0.7), indicating that the effect of season on activity patterns was similar across all
study sites.
We found significant differences in consumption of leaves (young and mature)
between seasons (χ2 = 11.5, df = 2, p < 0.01), being higher in the dry than in the rainy
season (contrast tests, p < 0.02 in all cases; Fig. 2). However, the time spent on fruits
(immature and mature) was similar between seasons (χ2 = 0.60, df = 2, p = 0.6; Fig. 2).
Discussion
In general, our results were consistent with our hypothesis and most of our predictions:
spider monkeys in Lacandona adjust their activity patterns in order to deal with forest type
and seasonal changes in food availability. As a consequence of lower food availability in
fragments, leaf consumption is higher in this forest type than in continuous forest (Chaves
et al. in press; see Methods). Also, we found here that independent of study site, monkeys
spent more time feeding on leaves during the dry season (i.e., the period of fruit scarcity;
see Methods) than during the rainy season. Our findings are therefore consistent with the
idea that variations in food availability can affect the diet of primates, ultimately affecting
the time that primates devote to core activities (e.g., feeding, resting, and traveling:
Bronikowski and Altmann 1996; Dunbar 1992; Korstjens et al. 2010). However, as we
discuss below the implications that variations in food availability and diet have on activity

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patterns of spider monkeys can be different when analyzing: 1) differences between
continuous forest and forest fragments, and 2) differences between seasons.
Habitat-Related Shifts in Activity Patterns
Compared to monkeys inhabiting continuous forest, spider monkeys in fragments spent
more time feeding, less time traveling and similar time resting. Fruit scarcity in fragments
would promote spider monkeys to compensate energy expenditure by increasing their time
feeding on items that are less nutritious, and low in energy (i.e., poorer in nonstructural
carbohydrates) such as leaves. As the digestive system of A. geoffroyi is designed
essentially for a diet mainly composed of easily digestible food items like fleshly fruits
(Lambert 1998; Milton 1981 a, b), monkeys must invest more time feeding when eating
leaves (i.e., for procuring more leaves) to obtain sufficient amounts of energy and nutrients.
This would be particularly true for those nutrients that are poor in leaves but abundant in
fleshy fruits, such as lipids and carbohydrates (Milton 2008). This idea is supported by
different primate studies in Paleotropical continuous forests (e.g., baboons: Dunbar 1992;
lemurs: Overdorff 1996; gorillas: Masi et al. 2009), which indicate that time spent feeding
is directly related to the proportion of leaves in the diet. Our results for fragments are
consistent with this prediction. Iwamoto and Dunbar (1983) also found that time spent
feeding by gelada baboon populations in three different habitats was inversely related to
variation in food quality among habitats; a pattern similar to that reported by Watts (1988)
for mountain gorillas.
The observation that monkeys spent less time traveling in fragments compared to
continuous forest may partially be explained by the limited foraging area available in the

133
fragments. In fragments as small as 14 ha, food is scarce and space is limited, and hence
there is not much traveling that they can do. Furthermore, since traveling is an energy-cost
activity (Chapman and Chapman 2000), the reduction of time traveling in fragments could
also be an energy-saving strategy to cope with resource limitations in fragments. Finally,
spider monkeys in fragments might spend less time traveling because they spend more time
feeding on leaves (Chaves et al. in press), which are generally more readily available (in
contrast to the patchiness of fruits; Milton 1981b). Overall, in conjunction these factors
would explain why monkeys in fragments spent less time traveling than in continuous
forest.
The lack of significant differences between continuous and fragmented forests in time
spent resting could indicate that this activity is more constrained by changes in temperature
between seasons (as suggested by Korstjens et al. 2010), than changes in food sources
between forest types since in Lacandona differences in average daily temperature are higher
between seasons than between forest types (see Methods). Nevertheless, further studies
assessing the potential effect of temperature on activity patterns of spider monkeys are
needed to evaluate this hypothesis.
Seasonal-Related Differences in Activity Patterns
Overall, independent of the forest type, time spent feeding was higher during the rainy than
during the dry season. This pattern may be explained by two nonexclusive explanations.
First, in this region fruit availability is higher during the rainy season (see Methods), and
monkeys spent less time feeding on leaves during this season (Fig. 2). Although we found
that time spent on fruits did not differ between seasons, other studies have demonstrated

134
that when fruits are temporally available, spider monkeys include more fruit in their diet
(Chapman 1987; Felton et al. 2008). It is reasonable to expect that time spent feeding
should be lower when eating on highly energetic, nutritionally balanced and easily
digestible plant items such as fruits. Nevertheless, Felton et al. (2009) interpret greater
feeding in the rainy season as a strategy for spider monkeys to take advantage of peak
seasonal foods allowing them to ingest surplus energy and store it as fat in preparation for
the impending period of food scarcity. This and other Ateline species (e.g., Ateles paniscus:
Milton 1998; A. chamek: Wallace 2005) accumulate fat during peaks of fruit abundance,
which is a logical strategy for animals experiencing fluctuating food supply (Felton et al.
2009). Second, evidence suggests that seasonal increase in ambient temperature, such as
that occurring during the dry season (ca. 3 °C; see Methods), may propitiate that primates
reduce heat-generating activities like feeding in order to avoid thermal overload and its
associated energetic costs (Dunbar et al. 2009; Korstjens et al. 2010), which is consistent
with several studies on spider monkeys (Chapman 1988; Korstjens et al. 2006; Table 1).
However, further information on energetic strategies of spider monkeys is needed to
determine the relative influence of each of these factors.
Primate socio-ecological models indicate that in spider monkeys and other tropical
primates, time spent resting is a function of seasonality, the percentage of leaves in their
diet, and the mean annual temperature (e.g., Korstjens et al. 2006; 2010). Thus, as the
percentage of leaves in the diet and the mean temperature increase, the enforced resting
time (i.e., resting needed for digestive and/or thermoregulatory purposes: Korstjens et al.
2010) also increases (Dunbar et al. 2009; Korstjens et al. 2010). In concurrence with this
hypothesis, we found that time resting was higher during the dry season (when
consumption of leaves was greater; Fig. 2) than during the rainy season. This may facilitate

135
more efficient digestion of foliar material (Milton 1981a) and at the same time minimize
thermoregulatory costs during the hottest period of year (Korstjens et al. 2006; 2010).
Similar findings also have been reported in other studies in Mesoamerica and South
America. For instance, in the tropical dry forest of Santa Rosa, Costa Rica, the time that A.
geoffroyi devote to resting is directly related to the proportion of time devoted to eating
leaves (Chapman 1991). Other Atelids also spend more time resting during the dry season
when fruit is scarce (e.g., Ateles paniscus: van Roosmalen 1980; Lagothrix lugens:
Stevenson et al. 1994). Finally, a recent meta-analysis of the activity patterns of A.
geoffroyi through Mesoamerica shows that time spent resting is mainly related (positively)
to the average annual temperature in seasonal forests (González-Zamora et al., unpublished
data).
Our study has some limitations (e.g., we did not measure directly spatial and
temporal food availability in each site), but it is unique in that we studied multiple spider
monkey communities´ activity budgets in the context of both fragmentation and seasonality
and the interaction between them. We suggest, however, that further long-term behavioral
studies of spider monkeys are needed to improve our understanding of the behavioral
responses of primates to environmental stresses imposed by habitat disturbance,
fragmentation, and seasonality, as our knowledge about this topic is still very scarce.
Although, in general, our findings indicate that spider monkeys in Lacandona can adjust
their activity patterns and diet in order to cope with food scarcity in forest fragments and
during the dry season, it is not clear if this behavioral flexibility is large enough to assure
their health and persistence in the long-term, especially if we consider the high rates of
deforestation and forest fragmentation affecting Neotropical forests. Studies analyzing the
consequences of these behavioral adjustments on health, fitness and long-term persistence

136
of primates are therefore needed to help in the design of appropriate management strategies
for primate populations in the Lacandona region and other disturbed tropical forests.
Acknowledgements This research was supported by grants from the Consejo Nacional de
Ciencia y Tecnología (CONACyT Grant CB2005-C01-51043 and CB2006-56799). OMC
obtained a scholarship from the Dirección General de Estudios de Posgrado, UNAM, as
part of the Programa de Posgrado en Ciencias Biológicas and from Secretaría de Relaciones
Exteriores (SRE) of Mexico. A postdoctoral fellowship given to VAR by the Consejo
Técnico de la Investigación Científica (UNAM) is gratefully acknowledged. The Instituto
para la Conservación y el Desarrollo Sostenible, Costa Rica (INCODESO) provided
logistical support. This study would not have been possible without the collaboration of A.
M. González Di-Pierro and the local people in Loma Bonita, Chajul, Reforma Agraria and
Zamora Pico de Oro ejidos. We thank C. Hauglustaine, C. Balderas, K. Amato, S.
Martínez, J. Herrera, and R. Lombera for field assistance. A. Estrada and J. Benítez-
Malvido made useful suggestions during the design of this research. J. M. Lobato and G.
Sánchez provided technical support. We also thank two anonymous reviewers for valuable
criticism and suggestions that improved the manuscript.
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Table 1 Activity budgets for 7 frugivorous atelids in different forest types.
Activity pattern
Primate species
Feed Rest Travel Other
Sitea Forest type
(vegetation type)b
Season
(study length)c Ref.d
Lagothrix lagotricha 36 36 24 4 TNP C (TWF) Annual (13, 672) 1
L. lagotricha 26 30 39 6 EBC C (TWF) Annual (12, 720) 2
L. lugens 36 36 24 4 TNP C (TWF) Annual (12, 624) 3
Ateles chamek 19 45 30 6 NKM C (TDF) Annual (11, ─ ) 4
A. chamek 29 45 26 0 MNP C (TMF) Annual (21, 1360) 5
A. hybridus 23 27 42 8 SJC F (TWF) Annual (8, ─) 6
A. paniscus 35 41 23 ─ VOL C (TMF) Annual (12, ─) 7
A. belzebuth 17 58 25 0 YNP C (TWF) Annual (12, 1268) 8
A. belzebuth 50 24 18 8 TAW C (TDF) Annual (12, ─) 9
A. belzebuth 22 63 15 ─ TNP C (TWF) Annual (12, ─) 10
A. belzebuth 18 45 36 ─ MES C (TWF) Annual (─,─) 11
A. geoffroyi 26 45 29 0 SNP C (TDF) Rainy (24, 335) 12
A. geoffroyi 19 55 27 0 SNP C (TDF) Dry (24, 335) 12
A. geoffroyi 35 43 22 0 PUL F (TDF) Annual (47, ─) 13
A. geoffroyi 26 54 16 4 BCI C (TWF) Rainy (10, ─) 14
A. geoffroyi 51 29 10 10 LAC C, F (TWF) Rainy (15, 1010) 15
A. geoffroyi 37 38 14 11 LAC C, F (TWF) Dry (15, 1010) 15
aSite: TNP, Tinugua National Park, Colombia; EBC, Estación Biológica Caparú, Colombia;
NKM, Noel Kempff Mercado National Park, Bolivia; MNP, Manú National Park, Peru;
SJC, San Juan del Carare, Colombia; VOL, Voltzberg, Surinam; YNP, Yasuní National
Park, Ecuador; TAW, Tawadu, Venezuela; MES, Maraca Ecological Station, Brazil; SNP,

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Santa Rosa National Park, Costa Rica; PUL, Punta Laguna, Mexico; BCI, Barro Colorado
Island, Panama; LAC, Lacandona rainforest, Mexico
bC, continuous forest; F, fragmented forest; TWF, tropical wet forest; TMF, tropical moist
forest; TDF, tropical dry forest
cNumber of months and observation hours
dReferences: 1. Stevenson et al. (2000); 2. Defler (1995); 3. Stevenson et al. (1994); 4.
Wallace (2001); 5. McFarland Symington (1988); 6. Aldana (2009); 7. van Roosmalen
(1980); 8. Suarez (2006); 9. Castellanos (1995); 10. Klein and Klein (1977); 11. Nunes
(1995); 12. Chapman (1988); 13. Ramos-Fernández and Ayala-Orozco (2003); 14. Milton
(1981a); 15. this study

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Table 2 Characteristics of the sites and groups of Ateles geoffroyi studied in Lacandona, Chiapas,
Mexico (Modified from Chaves et al., in press).
Sites Size (ha) Location
Elevation
(m a.s.l.)a
DNF
(m)
DCF
(m)
YSF
Group
size
Home
range
(ha)b
Continuous forest 331000
Montes Azules Biosphere
Reserve
C1 ─ 16°06'58.2"N, 90°56'18.4"W 125–170 ─ ─ ─ 40 29.7
C2 ─ 16°09'32.0"N, 90°54'06.6"W 130–180 ─ ─ ─ 36 47.3
C3 ─ 16°09'40.0"N, 90°54'04.5"W 130–210 ─ ─ ─ 44 89.6
Forest fragments
Marqués de Comillas
Municipality
F1 14.4
Zamora Pico de Oro
16°19'52.0"N, 90°51'06.1"W 125–140 450 200 29 35
14.4
F2 31
Zamora Pico de Oro
16°19'24.5"N, 90°50'43.7"W 130–145 150 1200 24 39
31.0
F3 1125
Reforma Agraria
16°15'12.2"N, 90°49'59.5"W 150–250 100 1100 26 41
63.1
Abbreviations: DNF, distance to nearest forest fragments; DCF, distance to continuous forest;
YSF, years since fragmentation
aMeters above sea level. Range is indicated
bHome range was determined for monkey communities in continuous forest and in the fragment
F3. In the other two fragments, monkeys used the entire fragment area (see further details on
Chaves et al. in press).

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Table 3. Percent time spent by spider monkeys in different activities according to study site
per season.
Site Season Activity patterns
Feeding Resting Traveling Others
Continuous forest
C1 Rainy 59.2 18.2 13.2 9.4
Dry 42.6 26.7 20.6 10.1
C2 Rainy 38.8 40.3 9.7 11.2
Dry 33.9 37.2 10.8 18.1
C3 Rainy 43.4 32.8 15.9 7.9
Dry 20.2 48.4 19.9 11.5
Forest fragments
F1 Rainy 60.7 21.4 6.9 11.1
Dry 51.3 31.6 9.4 7.7
F2 Rainy 56.9 26.9 8.1 8.1
Dry 43.3 43.2 7.7 5.7
F3 Rainy 42.7 36.7 8.5 12.1
Dry 30.9 42.3 14.5 12.3

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Figure legends
Fig. 1 Percent time (average ± SD) spent by spider monkeys in different activities
according to forest type (A), and season (B). Different letters indicate significant
differences between forest types or seasons (p < 0.05).
Fig. 2 Seasonal diet composition of spider monkeys. The percentages of total feeding time
(average ± SD) consuming different plant items are indicated: mature fruits (MF),
immature fruits (IF), mature leaves (ML), immature leaves (IL), young branch piths (BR),
flowers (FW), and other plant items (OT, decayed wood, plant secretions, moss, and
epiphyte roots). Different letters above bars indicate significant differences (p < 0.05).

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Fig. 1
A
a
a
a
a
a
b
ba
0
10
20
30
40
50
60
Feeding Resting Traveling Others
Continuous forest
Forest fragments
Activity
B
a
a
a
a
a
a
b
b
0
10
20
30
40
50
60
70
Feeding Resting Traveling Others
Rainy season
Dry season
Percentage of time

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Fig. 2
a
a
a
a
a
a
a
a
a
b
b
a
a
a
0
10
20
30
40
50
60
MF IF ML IL BR FW OT
Diet composition
Percentage of time
Rainy season
Dry season

152
CAPÍTULO IV

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Running title: Absence of spider monkeys affects seedling composition
Absence of spider monkeys in small forest fragments affects the composition of
seedlings in Southern Mexico
(manuscript in preparation, Biological Conservation, IF= 3.16)
Oscar M. Chaves,a,*, Katrhyn Ea. Stoner, Víctor Arroyo-Rodrígueza, Julieta Benítez-
Malvidoa, Alejandro Estradab, Miguel Martínez-Ramosa
a Centro de Investigaciones en Ecología, Sistema de Estudios de Posgrado, Universidad
Nacional Autónoma de México. Apartado Postal 27-3 (Xangari), Morelia, Michocán.
b Laboratorio de Primates, Instituto de Biología, Universidad Nacional Autónoma de
México. Apartado Postal 176, San AndrésTuxtla, Veracruz, Mexico
3
ABSTRACT
*Corresponding author at: Centro de Investigaciones en Ecología, Sistema de Estudios de
Posgrado, Universidad Nacional Autónoma de México. Apartado Postal 27-3 (Xangari),
Morelia, Michocán.
E-mail address: ochaba@gmail.com (O.M. Chaves)

154
Seed dispersal by arboreal vertebrates is a critical process for successful recruitment of
many tropical tree species and hence for the maintenance of tropical plant diversity. We
evaluated the richness, diversity and abundance of seedling species in forest fragments
where spider monkeys (Ateles geoffroyi) have disappeared in Lacandona rainforest, Mexico
We identified, counted and marked seedlings in three areas of continuous forest and six
fragments (three fragments with monkeys and three fragments without monkeys). We
classified the seedling species into four categories according to their dispersal mode: (1)
primate-dispersed species, (2) small and medium vertebrate-dispersed species, (3) wind-
dispersed species, and (4) gravity-dispersed species. Abundance and diversity of primate-
dispersed seedling species were higher in continuous forest and fragments with monkeys
than in fragments without monkeys. In contrast, overall species richness, richness of small
and medium vertebrate-dispersed species, and abundance of abiotic-dispersed species were
higher in the latter habitats. Species-rank abundance curves showed that primate-dispersed
species and small and medium vertebrate-dispersed species were dominant in continuous
forest and fragments with monkeys, whereas in fragments without monkeys the seedling
community was dominated by small and medium vertebrate-dispersed species and abiotic-
dispersed species. Canonical Correspondence Analysis showed that seedling composition
was best correlated (positively) with spider monkey abundance and to a lesser degree large-
bodied frugivore richness, and that it was poorly correlated with adult tree community
structure, canopy openness, fragment size, fragment age, and isolation level. Our results
suggest that the disappearance of spider monkeys could ultimately affect tree composition,
favoring small and medium seed-size vertebrate-dispersed species and abiotic-dispersed
species in fragments.
Keywords: forest fragmentation, tropical rain forest, seedling recruitment, seed dispersal,
spider monkey disappearance

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1. Introduction
Fragmentation and other human disturbances have negative effects on the reproduction and
survival of many species of plants and animals worldwide (Brook et al., 2003; Vellend et
al., 2006). However, tropical forests are likely the most affected ecosystems due to their
rapid continued degradation (FAO, 2007; Malhi et al., 2008). For instance, tropical
rainforest clearing, fragmentation, hunting, and other disturbances have resulted in the great
reduction and/or extirpation of many frugivorous vertebrates (Moran et al., 2009; Terborgh
et al., 2008). This is a serious conservation problem because the lower abundance or local
extinction of many frugivorous dispersers may affect the population dynamics of plant
species (Stoner et al., 2007).
Since vertebrates are the main seed dispersers of 70–95 percent of woody plants in
tropical forests (Fleming et al., 1987; Jordano, 2000), regeneration of these plant
communities largely depends on these animals (Terborgh et al., 2008; Wright et al., 2007).
However, dispersal services, and hence their effect on seedling recruitment, depends on
both vertebrate and fruit species´ characteristics. There is an inverse relationship between
the number of dispersers and fruit and seed size, due to the mechanical and physical
constrains derived from fruit and seed handling (Donatti et al., 2007; Jordano, 1995). Thus,
plant species with small fruits and seeds (e.g. Ficus spp. and Miconia spp.) can be handled
and potentially swallowed and dispersed by a wide assemblage of vertebrate dispersers, but
large-seeded plant species (e.g. Spondias spp., Virola spp., and Pouteria spp.) depend on
large-bodied specialized dispersers (Donatti et al., 2007; Wright et al., 2007). In spite of the
overlap in fruit species exploited by primates and other arboreal frugivores (e.g. birds, bats,
kinkajou, coati-mundis) there are several examples of plants that primarily depend on

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primates for seed dispersal (see Nunez-Iturri & Howe 2007). Peres and Van Roosmalen
(2002) propose that large-bodied Atelinae primates in the Amazon Basin are practically
exclusive dispersers of large-seeded plants (> 1 cm width). Similarly, in French Guiana
Julliot (1997) found that howler monkeys (Alouatta seniculus) are the main disperser of
some large-seeded plants (e.g. Chrysophyllum lucentifolium, Pouteria torta). Large-bodied
primates are a highly vulnerable group due to their dependence on well-preserved tropical
forest (Mittermeier and Cheney, 1987), hunting pressures (de Thoisy et al., 2009), and
drastic population declines reported in different primate species living in fragments
(reviewed by Isabirye-Basuta and Lwanga, 2008).
Loss or severe population decline of key frugivores (e.g. primates and birds) can lead
to a reduction in seed dispersal and seedling recruitment, particularly in the case of large-
seeded plants (Melo et al., 2010; Sethi and Howe, 2009; Terborgh et al., 2008). The
disappearance of primates may alter considerably plant population dynamics because it is
unlikely that dispersal services provided by them can be compensated for by other
frugivorous vertebrates. Nevertheless, our ability to understand this phenomenon in forest
fragments is seriously limited by the fact that most primate studies have been conducted in
large protected areas (e.g. Southeastern Peru: Nuñez-Iturri & Howe 2007). Furthermore,
results may be confounded with changes in other ecological variables in fragments (e.g.
large bodied-frugivore richness, vegetation structure, canopy openness, isolation level, and
fragment size and age: Saunders et al. 1991; Laurance 2005) and therefore, not a direct
result of changes in disperser abundance. For this reason, it is necessary to take into
consideration these variables in order to determine the relative impact of disappearance of a
specific seed disperser on seedling recruitment. .

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In Mesoamerica the assessment of potential effects of local disappearance of large-
bodied frugivores in forest fragments on seedling recruitment and composition remain
practically unexplored (but see Melo et al. 2010, Gonzalez-Di Pierro et al. unpublished
data). Based on the available evidence, we hypothesize that in forest fragments the lack of
spider monkeys (Ateles geoffroyi vellerosus) deprive large-seeded plants of efficient
dispersers and hence limit community-wide recruitment of primate-dispersed species in
comparison with forests containing monkeys. To address this hypothesis we: (1) compare
the abundance, dominance, richness and diversity of seedlings according to their dispersal
mode in continuous forest, and in fragments with and without spider monkeys, (2)
determine the relative dominance of seedling species with different dispersal modes in each
habitat; and (3) determine the relative contribution of spider monkeys abundance, large-
bodied frugivore richness, adult tree composition, canopy openness, and fragment size, age
and isolation level to the observed patterns. Finally, we discuss the conservation
implications of local disappearance of large-bodied primates on regeneration of tropical
rainforest fragments and suggest directions for future research.
2. Methods
2.1. Study area
We conducted this study during a 17-mo period in 2007 (January-June, August-November)
and 2008 (February-May, July-September) in the Lacandona rainforest, southern Chiapas,
Mexico (16°05'58" N, 90º52'36" W). Covering parts of Mexico, Guatemala, and Belize,
this region encompasses the largest portion of tropical rainforest in the Neotropics (Dirzo,

158
1994). The average annual temperature in the region is 23.9°C and the average annual
rainfall is 2881. Greatest rainfall concentration is found in June–September (range: 423–
511 mm/month), and lowest in February-April (46–60.6 mm/month) (Comisión Federal de
Electricidad, Mexico, unpublished data).
The study sites were located in two adjacent areas separated by the Lacantún river:
the fragmented region of Marqués de Comillas (MCR, eastern side of the river), and the
undisturbed Montes Azules Biosphere Reserve (MABR, western side). In contrast to
MABR, MCR was colonized and deforested in the sixties, and today, most of the original
forest cover has been modified (Marquez-Rosano, 2006). Approximately 50% of the land
surface of MCR is nowadays used for agricultural purposes, but small (0.5–30 ha) and large
(> 1000 ha) forest fragments still remain in the area. The protected area of MABR was
created in 1978 and consists of approximately 300,000 ha of undisturbed forest, and
contains approximately 4314 species of vascular plants (Martínez et al., 1994).
2.2. Study sites
We carried out this study in 9 sites: 3 areas within the MABR (hereafter continuous forest,
CF) separated by at least 4 km from each other, 3 forest fragments with monkeys (hereafter
occupied fragments, OF), and 3 forest fragments without monkeys (hereafter unoccupied
fragments, UF). In CF and OF spider monkey groups ranged from 35 to 44 individuals in
size (Supplementary Table 1). All OF and UF fragments were isolated ≥ 17 years ago, and
their sizes ranged from 6.4 to 1125 ha (Supplementary Table 1). Despite the large size of
the latter fragment, we considered it as a fragment due to the distance from the continuous
forest (1100 m), the surrounding anthropogenic matrix (cattle ranches, pastures, and human

159
settlements), the vegetation structure, and the high perturbation level (O.M. Chaves et al.,
unpublished data). Contrasting to CF and OF, in UF sites howler monkeys (Alouatta pigra)
and most large-bodied frugivores are absent (Supplementary Table 2). Furthermore, a
Principal Component Analysis grouped the adult tree (> 10 cm DBH) structure of
fragments without monkeys (UF) and forests with monkeys (OF and CF) in two separate
groups (KW = 5.7, df = 2, p < 0.05).
2.3. Primates in the study area
Two sympatric primate species are present in the study area: the black-handed spider
monkey (Ateles geoffroyi) and the black howler monkey (Alouatta pigra). The former
species is distributed from the state of Veracruz, Mexico, throughout most of Central
America and the Choco Region of the Pacific coast of South America to northern Ecuador.
The latter species is endemic to southern Mexico, Belize, and Guatemala (Rylands et al.,
2006). In Mexico there are two subspecies of spider monkeys: A. geoffroyi vellerosus
(present in most of southern Mexico, including our study area) and A. g. yucatanensis
(restricted to the Yucatán peninsula) (Watts & Rico-Gray 1987). In MABR the population
density of A. geoffroyi is estimated as 2.9 ind/km2, while that for A. pigra is 14.4 ind/km2
(Estrada et al., 2004). Alouatta pigra is considered primarily folivorous, but may devote as
much as 50% of their feeding time to consuming fruits (Pavelka and Knopff, 2004).
Conversely, A. geoffroyi is well-recognized as a fruit specialist and ripe fruits can account
for more than 70% of its feeding time (González-Zamora et al., 2009; van Roosmalen and
Klein, 1988). Further details about spider monkey ecology are provided by Di Fiore &
Campbell (2007).

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2.4. The seedling community
Before establishing the sampling plots within each study site, we conducted systematic
troop follows for 6 spider monkey groups (3 groups in CF and 3 groups in OF), as part of a
larger ecological study focused on collecting foraging data. We used this information to
place the seedling sampling areas along foraging route of spider monkeys at the OF and CF,
whilst in UF sites these areas were selected randomly.
To evaluate seedling recruitment we implemented an experimental design similar to
that in Benítez-Malvido (1998). In each CF, OF and UF site, we located three 50 x 50 m
blocks separated by at least 30 m from each other. Within each block, we located three 50
m-linear transects and fifteen 1-m2 plots, for a total of 45 1-m2 plots in each one of the nine
study sites, totaling 405 1-m2 plots in all sites. In each 1-m2 plot we marked (with
individually numbered aluminum tags), identified and counted all woody seedlings and
palms 5–100 cm tall. The only climbers considered were a few large-seeded (seeds > 1.5
cm in length) fleshy-fruited vines that were highly consumed by spider monkeys (e.g.
Abuta panamensis, and Paullinia costata: González-Zamora et al., 2009). The sampling
plots were surveyed every 3-mo during a 16-mo period to record new recruitments.
Seedling identification was achieved with the collaboration of an experienced local
para-taxonomist. Plant nomenclature was used according to the Missouri Botanical Garden
nomenclatural update database (http://mobot.org/W3T/ search/ vast.html). Individuals not
identified in the field were assigned to morphospecies, and collected for later identification
using the Lacandona reference collection located at the Centro de Investigaciones en
Ecosistemas (UNAM, Morelia, Mexico).

161
2.5. Dispersal mode
Following Nuñez-Iturri and Howe (2007) we classified seedlings according to their seed
dispersal mode into four categories which include abiotic and biotic vectors: (1) primate-
dispersed species (PD)–fleshy fruit species with seeds 1.5–5 cm in length, which are mainly
consumed by large primates such as A. geoffroyi; (2) small and medium vertebrate-
dispersed species (SMD)–fleshy fruit species with seeds <0.1– < 1.5 cm in length, which
are dispersed by bats, small mammals, and birds, among others; (3) wind-dispersed species
(WD)–all species having winged seeds/fruits, and (4) gravity-dispersed species (GD)—
those lacking any obvious dispersal mechanism or disperser reward. Dispersal mode of
each species was assigned to one of these four categories based on fruit and seed traits (e.g.
morphology, size, type of pulp/aril), complemented with recent reviews on spider monkey
diet (Di Fiore et al., 2008; González-Zamora et al., 2009).
2.6. Ecological variables
In order to determine if any differences in seedling community structure among CF, OF and
UF may be attributed to the presence/absence of spider monkeys, we evaluated a variety of
ecological variables that have been recognized as important factors influencing seedling
community structure and composition. These variables include: (1) spider monkey
abundance, (2) large-bodied frugivore richness (3) vegetation structure, (4) canopy
openness, (5) fragment age, (6) fragment size. Furthermore, as an indicator of isolation we
measured (7) distance to the nearest fragment, and (8) distance to the continuous forest.

162
Further methodological details on these variables are provided in the Supporting
Information.
2.7. Data analysis
For each study site we pooled data from all seedlings sampled, and then we estimated
seedling species richness using four nonparametric estimators provided by EstimateS 7.5
(Colwell, 2005). After 1000 randomizations of sample order we estimated the: incidence-
based coverage estimator (ICE), abundance-based coverage estimator (ACE), Chao2, and
bootstrap. To test for differences in species richness and diversity among habitat types (CF,
OF and UF), we standardized the number of individuals sampled to control for differences
in individual density using the rarefaction approach and calculated the Shannon index
(EcoSim; Gotelli and Entsminger, 2001). To test for differences in abundance, species
richness, diversity and evenness among habitat types we used Kruskal-Wallis tests
considering each of the three sites as replicas within each habitat. To identify which
habitats were statistically different among each other we used Nemenyi post-hoc
comparisons. To evaluate whether seedling composition was affected by dispersal mode,
we constructed species rank-abundance curves for each study site within each habitat. We
plotted the relative abundance of seedling species against the rank of the species, from the
most abundant to the rarest species (Magurran, 2004). These analyses were carried out
using SYSTAT software (version 11.0, SPSS Institute Inc, Chicago).
To evaluate the relationship between seedling composition of PD-species and the
different ecological variables for each site, we used Canonical Correspondence Analysis
(CCA) processed by the program PC-ORD 4.0 (McCune and Mefford, 1997). The CCA is a

163
direct gradient analysis technique that relates species composition to measured
environmental or ecological variables (ter Braak, 1987). The main CCA matrix consisted of
seedling abundances of PD-species, whereas the secondary CCA matrix consisted of the 8
ecological variables measured in each one of the 9 study sites. Finally, a Monte Carlo
permutation test was performed to assess the significance of the correlations found.
3. Results
3.1. Seedling community structure
Overall, after 16 months we registered 6879 seedlings (2087 seedlings in CF, 1472 in OF,
and 3320 in UF) comprised of 90 species (and an additional 43 morphospecies), 59 genera
and 37 families in the 405 1-m2 plots. Of these species, 78.9% were trees, 15.6% were
shrubs, 4.4% were vines and 1.1% were palms. When assigned to dispersal mode, 68.9%
were SMD-species, 12.2% were WD-species, 11.1% were PD-species, and 7.8% were GD-
species. Of the top ten seedling species in CF, four were PD-species, compared to three
species in OF and one species in UF (Supplementary Table 3). The three most abundant
seedling species in CF were Ampelocera hottlei (33%) followed by Castilla elastica (15%)
and Brosimum aliscastrum (12%), in OF they were Inga punctata (22%), B. alicastrum
(18%) and C. elastica (11%), and in UF they were Licania hypoleuca (21%), B. alicastrum
(17%) and Vochysia guatemalensis (16%) (Supplementary Table 3). In general, sampling
completeness ranged from 60 to 80% in most cases, indicating that the inventories were
reasonably complete (Supplementary Table 4).

164
3.2. Species richness and diversity
We found that abundance of individuals of PD-species differed among habitat types
(Kruskal-Wallis: H = 9.3, df = 2, p = 0.04), being higher in CF and OF than in UF (p < 0.05
in both cases), but it was similar between CF and OF (p > 0.1). Similarly, rarefied diversity
of PD-species was higher in CF and OF than in UF (mean, 1.5, 1.4 and 1, respectively;
Kruskal-Wallis: H = 7.1, df = 2, p < 0.05; Table 1). By contrast, overall species richness
was greater in UF than in OF or CF (49, 40 and 37 species, respectively; Kruskal-Wallis: H
= 6.8, df = 2, p < 0.05; Table 1). Similarly, SMD-species richness also was greater in UF
than in OF or CF (31, 20 and 23 species, respectively; Kruskal-Wallis: H = 7.6, df = 2, p <
0.05; Table 1). Finally, the abundance of individuals of both WD-species and GD-species
differed significantly among habitat types (Table 1), being greater in UF than in OF or CF
(p < 0.05 in both cases) and similar between OF and CF (p > 0.1 in both cases). However,
we did not detect other significant differences among habitat types for species richness,
diversity and evenness (Table 1).
3.3. Species-rank curves
Assemblage structure differed among habitat types, depending on the seed dispersal mode
(Fig. 1). In the continuous forest areas, SMD-species and PD-species were clearly dominant
species (Fig. 1a). Similarly, in occupied fragments, dominancy of SMD-species and PD-
species were also observed, but the number of PD-species in the top ten ranked species
tended to decrease (Fig. 1b). By contrast, in unoccupied fragments the seedling community

165
was dominated by SMD-, WD- and GD-species, and the number of PD-species in the top
ten ranked species was negligible (Fig. 1c).
3.4. Seedling composition and ecological variables
According to the CCA analysis axis 1, 2 and 3 together explained 95.6% of the variance in
species data (69.8%, 18.6% and 7.2%, respectively). Pearson correlations for species-
environment for each axis (1.0, 0.9 and 0.9, respectively) were significant for the three
canonical axes (Monte Carlo test, p < 0.02 in all cases). Eigenvalues were relatively high
for species (> 0.3) indicating considerable species turnover along the gradients summarized
in axis 1 and 2 (Fig. 2a). Axis 1 and 2 separated seedling species assemblages of forests
with monkeys (CF and OF) and unoccupied fragments (Fig. 2b). Spider monkey abundance
was the most important ecological variable in axis 1, followed by large-bodied frugivore
richness (Table 2). Spider monkey abundance was positively correlated with large-bodied
frugivore richness (r = 0.77), adult tree community structure (r = 0.52) and fragment age (r
= 0.61). Similarly, large-bodied frugivore richness was positively related to adult tree
community structure and fragment age, but negatively correlated to canopy openness and
distance to nearest fragments (Table 2). Finally, adult tree community structure was
negatively correlated to canopy openness and positively correlated to fragment age (Table
2).

166
4. Discussion
As we hypothesized, higher abundance, diversity and dominance of PD-species was found
in CF and OF compared to UF. Overall species richness, SMD-species richness, and
abundance and dominance of individuals of abiotic-dispersed species were higher in UF
than in CF and OF, suggesting that the disappearance of spider monkeys (as well as the
disappearance of other large-bodied vertebrates, Supplementary Table 2) altered the
community seedling structure in these habitats.
4.1. Shifts in seedling composition in fragments without monkeys
Our findings support results of different studies in fragmented forests of the Neotropics and
Paleotropics. For instance, detrimental effects on PD-species recruitment and an increase in
abiotic-dispersed species recently have been reported in sites with intensive hunting
pressures on large-bodied primates in southeastern Peru (Nunez-Iturri et al., 2008). In
fragments with howler monkeys (Alouatta pigra) in Community Baboon Sanctuary, Belize
(Marsh and Loiselle 2003) and in Lacandona (González-Di Pierro et al. unpublished data),
howler monkey-dispersed seed species had lower abundances in fragments without
howlers, which presumably reflects increased recruitment of howler fruit trees in fragments
that contain howlers. In fragments of La Macarena, Colombia, the absence of Ateles
belzebuth and Lagothrix lagotricha results in the low representation of seedlings and
saplings of large-seeded species compared with the undisturbed continuous forest of
Tinigua, Colombia, but the proportion of small and medium-seeded species was similar
between continuous and fragmented forests (Stevenson and Aldana 2008). Finally, in

167
Yucatán Peninsula, Mexico, the absence of A. geoffroyi in logged sites results in a greater
accumulation of Manilkara zapota saplings under tree canopies than in the unlogged sites
(all of which present communities of spider monkeys), whilst sapling species richness is
greater in the unlogged than in the logged sites (Gutiérrez-Granados and Dirzo, 2010).
Similar results have also been reported for the Paleotroics. In Kibale National Park,
Uganda, Chapman and Onderdonk (1998) found that in contrast with intact forest, which
presented healthy populations of large-bodied primates, twenty studied fragments had
lower density and richness of seedling species, particularly for large-seeded species. In
fragments of the tropical dry forest of western Madagascar, the presence of the brown
lemur (Eulemur fulvus) results in a higher regeneration of lemur-dispersed species (seeds >
1 cm width) than in fragments without lemurs, suggesting that the regeneration of a
complete set of primary forest tree species depend upon the presence of lemurs (Ganzhorn
et al., 1999). Despite the methodological differences among the studies mentioned above
and our study, all studies consistently demonstrate that the disappearance of large-bodied
monkeys has a remarkable negative effect on the regeneration of large-seeded species.
4.2. Large-seeded species assemblage and ecological variables
We found that spider monkey abundance was the most important ecological variable
explaining the large-seeded seedling assemblages in the different habitat types (r = 0.65),
followed by large-bodied frugivore richness (r = 0.55), whereas none of the other
ecological variables showed high correlations with seedling assemblages (Table 2). These
findings reinforce our hypothesis that spider monkeys function as non-redundant
specialized dispersers and hence their absence in fragments alters seedling assemblages.

168
Similar conclusions also have been highlighted by other studies with large-bodied primates
in southeastern Peru (Nunez-Iturri et al., 2008), Colombia (Stevenson and Aldana, 2008), in
our same study area (Gonzalez-Di Pierro et al., unpublished data), and in fragments with a
poor large-bodied frugivore richness in Yucatan Peninsula, southern Mexico (Melo et al.,
2010).
Conversely, some authors suggest that secondary seed dispersal, low post-dispersal
survivorship of seeds and seedlings, and the overlap in fruit resources used by primates and
non-primate dispersers, dilute the influence that any primate species can have on recruiting
the next generation of adult trees (Lambert and Chapman, 2005; Lambert and Garber,
1998). Some studies on Neotropical primates have shown that an important percentage of
seeds defecated by monkeys are predated or removed and relocated by the action dung
beetles (e.g. A. seniculus, Ateles paniscus: Andresen, 1999) and scatter-hoarding rodents
(e.g. Ateles paniscus: Forget and Cuiljpers, 2008). Nevertheless, in our study we assume
that primary dispersal by spider monkey is highly associated with recruitment of defecated
seeds due to several reasons. First, most secondary dispersal by animals results in moving
seeds relatively short distances (e.g. < 1m in dung-beetles: Andresen 2002; ca. 5 m in
scatterhoarding rodents: Forget & Cuijpers 2008). Second, recent studies have shown that
secondary seed dispersal is not a critical process for recruitment, but rather a process that
contributes to higher survival of cached seeds in comparison with uncached seeds (Forget
and Cuijpers, 2008). Third, spider monkeys are capable of memorizing and following
specific foraging routes over time (Valero and Byrne, 2007), directly affecting recruitment
and plant structure and composition across many generations (Di Fiore and Suarez, 2007),
with or without the intervention of secondary dispersers or predators. Finally, some
alternate primary and secondary dispersers, other than spider monkeys, of large-seeded

169
species in Lacandona (e.g. howler monkeys, tapirs, deer, Supplementary Table 2) are also
capable of moving seeds several hundred meters. Nevertheless, it is reasonable to expect
that their relative contribution to seedling recruitment is low compared to spider monkeys,
because most seeds are commonly deposited in large clumps at feeding roosts, latrines and
sleeping trees (e.g. howler monkeys: Howe 1989; Pouvelle et al. 2009; tapir: Fragoso 1997)
and hence seeds are more vulnerable to density/distance-dependent mortality predicted by
the Janzen-Connell model (Howe, 1989).
4.3. Conservation implications
Our findings highlight the importance of spider monkeys on plant population dynamics.
Local extinction of this large-bodied primate in fragments, results in important structural
changes in seedling assemblages, including a reduction in recruitment and diversity of PD-
species and the prevalence of SMD-species and abiotic dispersed species (WD and GD-
species). Our results also indicate that these changes are mainly related to abundance of
spider monkeys and to a lesser degree large-bodied frugivore richness. Similar results also
have been found in Lacandona for the composition of seedlings and seedbank in small
fragments without howler monkeys (Alouatta pigra) and fragments and continuous forest
with this primate (González-Di Pierro et al., unpublished data). These findings suggest that
in the Lacandona region (and probably other Mesoamerican forest fragments), forest
management strategies and conservation efforts should take into consideration the key role
of large-bodied primates in forest regeneration and ecosystem function. Evidence suggests
that relationships among angiosperms and their animal dispersers are generally best
described as diffuse networks rather than close coevolutionary relationships (see Herrera

170
1985). Under this scenario, local extinctions of large-bodied frugivores is rarely followed
by extinction of the large-seeded species they disperse (Donatti et al., 2007). Certainly
ecological redundant seed dispersers (e.g. most small frugivorous birds, rodents, and
opportunistic frugivoruous-carnivorous animals) may play an important role in the
recruitment of small and medium-seeded species in both continuous and fragmented
forests, but apparently they are unable to compensate for the specialized services provide
by large-bodied frugivores (Babweteera and Brown, 2009; Cramer et al., 2007; Melo et al.,
2010). However, more studies evaluating the effect of large-bodied Neotropical primates
(and other similar frugivores) on regeneration in fragmented tropical forests are needed to
develop a better understanding of this phenomenon.
Acknowledgments
This research was supported by grants from the Consejo Nacional de Ciencia y Tecnología,
Mexico (CONACyT Grant CB2005-C01-51043 and CB2006-56799). O.M.C. obtained a
scholarship from the Dirección General de Estudios de Posgrado (UNAM), as part of the
Programa de Posgrado en Ciencias Biológicas, UNAM, Mexico. The Instituto para la
Conservación y el Desarrollo Sostenible, Costa Rica (INCODESO) provided logistical
support. This study would not have been possible without the collaboration of the local
people in Loma Bonita, Chajul, Reforma Agraria and Zamora Pico de Oro ejidos. We are
grateful to C. Hauglustaine, C. Balderas, S. Martínez, J. Herrera, and R. Lombera for field
assistance during monkey follows and seedling samplings. M. Quesada provided useful
comments and suggestions in early drafts of this paper. J. Rodriguez collaborated with the
identification of seedlings. We are grateful for technical support provided by J. M. Lobato
Garcia and G. Sánchez Montoya.

171
Appendix A. Supplementary material
Supplementary data associated with this article can be found in the online version, at doi:
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Table 1
Observed and rarefied species richness and diversity for the unoccupied fragments (UF), occupied fragments (OF), and continuous
forest (CF) by dispersal mode. Mean and standard error are indicated. Abundance represents the total number seedling recruitment
during the 16-mo study period in the 45 1-m2 plots in each site. For comparisons, p is the probability for the two-tailed Kruskal-Wallis
statistic. Significant differences are indicated in bold.
Seed dispersal modea Unoccupied fragments Occupied fragments Continuous forest
UF1 UF2 UF3 Average SE OF1 OF2 OF3 Average SE CF1 CF2 CF3 Average SE p
All dispersal modes
abundance 1070 1230 1020 1107 63.5 277 724 471 490.7 129.3 445 665 977 695.7 154.1 0.061
species richness 51 47 49 49 1.2 41 37 40 39.3 1.8 39 36 37 37.3 1.2 0.043
species richness rarefied 36.4 24.7 25.6 28.9 3.8 42 25.8 32.3 33.4 4.7 32.0 30.8 26.7 29.8 1.6 0.5
H’ 3.3 1.9 2.4 2.5 0.4 3.1 2.3 2.7 2.7 0.2 2.8 2.6 2.2 2.5 0.2 0.87
H" rarefied 3.2 1.8 2.3 2.4 0.4 3.1 2.3 2.6 2.7 0.2 2.7 2.6 2.1 2.5 0.2 0.83
evenness 0.9 0.6 0.7 0.7 0.1 0.8 0.7 0.7 0.8 0.04 0.8 0.8 0.6 0.7 0.04 0.9
PD-species
abundance 73 30 46 49.7 12.5 63 93 74 76.7 8.8 118 123 484 241.7 121.2 0.039
species richness 9 4 5 6.0 1.5 8 9 6 7.7 0.9 8 8 7 7.7 0.3 0.64
species richness rarefied 6.8 3.9 5 5.23 0.85 7 6.5 5.2 6.2 0.5 6.5 6.6 4.3 5.8 0.7 0.62
H’ 1.5 0.6 1.6 1.2 0.3 1.4 1.6 1.4 1.5 0.07 1.6 1.5 1.6 1.6 0.03 0.47
H" rarefied 1.1 0.9 1.1 1.0 0.01 1.4 1.5 1.3 1.4 0.06 1.5 1.4 1.5 1.5 0.03 0.046
evenness 0.7 0.4 0.7 0.6 0.1 0.7 0.8 0.8 0.8 0.03 0.8 0.7 1.0 0.9 0.1 0.44
SMD-species

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abundance 569 201 759 509.67 163.79 105 393 248 248.67 83.14 211 180 374 255.00 60.17 0.43
species richness 31 32 30 31.0 0.6 19 18 24 20.3 1.9 24 19 25 22.7 2.6 0.048
species richness rarefied 15.4 25.4 14.9 18.6 3.4 18.3 11.2 18.6 16.03 2.42 18.9 14.1 16.6 16.5 1.39 0.96
H’ 2.2 2.8 1.9 2.3 0.3 2.4 1.6 2.1 2.0 0.2 2.1 1.6 2.1 1.9 0.2 0.56
H" rarefied 2 2.7 1.8 2.2 0.3 2.4 1.5 2 2.0 0.3 2.0 1.5 2 1.8 0.2 0.86
evenness 0.7 0.8 0.7 0.7 0.05 0.8 0.6 0.7 0.7 0.06 0.7 0.6 0.7 0.6 0.04 0.57
WD-species
abundance 108 98 298 168.0 65.1 1 12 11 8.0 3.5 16 12 12 13.3 1.3 0.035
species richness 2 3 5 3.3 0.9 1 5 4 3.3 1.2 2 4 2 2.7 0.7 0.8
species richness rarefied 1.9 1.2 1.2 1.4 0.2 ─ 4.7 3.9 4.3 0.3 2 3.9 2 2.6 0.6 0.3
H’ 0.7 0.1 0.1 0.3 0.2 ─ 1.3 1.3 1.3 0.01 0.7 1.3 0.4 0.8 0.3 0.57
H" rarefied 0.6 0.08 0.06 0.2 0.2 ─ 1.3 1.2 1.3 0.02 0.7 1.3 0.4 0.8 0.2 0.41
evenness 0.9 0.4 0.3 0.6 0.2 ─ 0.8 0.9 0.9 0.03 0.9 0.9 0.6 0.8 0.10 0.3
GD-species
abundance 58 491 90 213 139.3 10 18 9 12.3 4.0 20 31 10 20.3 6.1 0.044
species richness 5 4 6 5 0.6 5 3 3 3.7 0.7 2 4 4 3.3 0.7 0.22
species richness rarefied 2.9 1.2 1.9 2 0.5 3.9 2.3 2.9 3.0 0.5 1.3 2.2 3.4 2.3 0.6 0.31
H’ 1.2 0.1 0.6 0.7 0.3 1.5 0.9 0.4 0.9 0.3 0.2 0.7 1.3 0.7 0.3 0.67
H" rarefied 1.0 0.08 0.4 0.50 0.3 1.3 0.7 0.4 0.8 0.2 0.1 0.5 1.1 0.6 0.3 0.67
evenness 0.9 0.4 0.7 0.7 0.1 0.9 0.8 0.4 0.7 0.2 0.5 0.7 0.9 0.7 0.1 0.99

Chaves et al.
180
Table 2
CCA intra-set and inter-set correlations for the first and second ordination axes for seedlings of PD-species and weighted correlation
matrix for ecological variables. Correlations with absolute values > 0.5 are enhanced in bold. Abbreviations: SA, spider monkey
abundance; LF, large-bodied frugivore richness; AT, adult tree community structure; CO: canopy openness; DC, distance to
continuous forest; FA, fragment age; FS, fragment size; DF, distance to nearest fragment.
Intra-set
correlations
Inter-set
correlations Ecological variables
Ecological
variable Axis 1 Axis 2 Axis 1 Axis 2 SA LF AT CO DC FA FS DF
SA 0.65 0.25 0.65 0.25 ─ 0.77 0.52 -0.41 -0.32 0.61 0.33 -0.32
LF 0.55 -0.02 0.55 -0.02 ─ 0.56 -0.64 -0.42 0.80 0.19 -0.61
AT -0.41 0.21 -0.41 0.21 ─ -0.50 -0.28 0.49 0.11 -0.18
CO 0.40 0.27 0.40 0.27 ─ 0.67 -0.79
0.04 0.66
DC 0.35 -0.23 0.35 -0.23 ─ -0.75 0.40 0.62
FA -0.27 -0.04 -0.27 -0.04 ─ 0.03 -0.83
FS -0.26 -0.27 -0.26 -0.27 ─ -0.27
DF 0.06 0.11 0.06 0.11 ─

181
Figure legends
Figure 1.
Species/ rank abundance plots for the top 25 seedling species according to seed dispersal
mode in each area of continuous forest (a), occupied (b), and unoccupied (c) fragments.
Species rank is ordered from the most to the least abundant species.
Figure 2.
Canonical correspondence analyses ordination of (a) seedling species assemblages and (b)
study sites. Species: Ah, Ampelocera hottlei; Dg, Dialium guianense; Gg, Guarea glabra;
Ip, Inga pavoniana; Pc, Pouteria campechiana; Pl, Posoqueria latifolia; Sm, Spondias
mombin; and Sr, S. radlkoferi.

182
Figure 1.
0.1
1
10
100
0.1
1
10
100
0.1
1
10
100
Log (total percentual abundance)
Specices rank
CF1
CF2
CF3
OF1 OF2 OF3
UF1 UF2 UF3
Seed dispersal mode
(a) Continuous forest
(b) Occupied fragments
(c) Unoccupied fragments

183
Figure 2.
-0.4
-0.9
-1.3
-1.7
0.0
0.4
0.9
1.3
1.7
2.1
-0.4-0.9-1.3-1.7 0.0 0.4 0.9 1.3 1.7 2.1
Fragment size
Fragment age
Distance to continuous forest
Adult tree composition
Canopy openness
Spider monkeys abundance
Vector scalin
g
: 2.53
-1.1
-2.2
-3.3
-4.4
-5.5
0.0
1.1
2.2
3.3
4.4
5.5
-1.1-2.2-3.3-4.4-5.5 0.0 1.1 2.2 3.3 4.4 5.5
Fragment size
Fragment age
Distance to continuous forest
Adult tree composition
Canopy openness
Spider monkeys abundance
Vector scalin
g
: 7.7
4
Pl
Dg
Gg
Sr
Sm
Ip
Ah
Pc
UF3
UF2
UF1
OF1
CF1
CF3
OF2 OF3
CF2
Axis 1
Axis 1
Axis 2
Axis 2
(a)
(b)
Large frugivore richness
Large frugivore richness

184
Methodological Details on Ecological Variables
Abundance of spider monkeys in each CF and OF was estimated by visual counts during
the preliminary follows complemented with our data from a15-mo period of systematic
spider monkey follows (see Chaves et al., 2010). Richness of large-bodied frugivores was
focused on: (1) terrestrial mammals weighing >1.5 kg and (2) large-bodied birds common
in Lacandona (e.g., toucans, guans, and trogons). For the first group we estimated richness
by two methods: direct observation along trails and water holes during day and night and
looking for and identifying tracks and signs (Reid, 1997), whilst richness of birds was
determined via direct observations using high resolution binoculars (Swarovski SLC 10 x
42). These samplings were carried out weekly during a 10-mo period (March-July 2007 and
June-October 2008). Furthermore, we complemented our censuses by conducting
interviews with local people working in tourism and/or those who regularly hunted in the
region.
To determine the vegetation structure in each CF, OF and UF sites we fixed ten 50 ×
2 m linear transects randomly (Gentry, 1982), for a total of 90 transects. We recorded all
trees and shrubs with diameter at breast height (DBH) ≥10 cm. With this information, we
conducted a Principal Component Analysis (PCA) for PD-species and used component
scores of the most important axes as ecological variables in subsequent analysis. We
quantified the percentage of canopy openness with a spherical concave densiometer (Model
C, Forest Densiometers, Oklahoma). We carried out brief interviews with land-owners to
determine fragment age. Finally, to determine fragment size, distance to the nearest
fragment/continuous forest we used recent LANDSAT satellite images (Instituto Nacional
de Estadística y Geografía, México,
http://mapserver.inegi.org.mx/rni/index.cfm?s=geo&c=1311) of the study area
complemented with direct field-measures using a GPS (Garmin 76 CSX).

185
Supplementary Table 1. Description of study sites in Lacandona, Chiapas, Mexico.
Sites Size (ha) Location
Distance to
nearest
fragment(m)
Distance to
continuous
forest (m)
Years since
fragmentation
Spider
monkey
abundance
Years since
disappearance
of monkeys
Continuous Forest 331,000 Montes Azules Biosphere Reserve
CF1 ─ 16°06'58.2"N, 90°56'18.4"W ─ ─ ─ 40 ─
CF2 ─ 16°09'32.0"N, 90°54'06.6"W ─ ─ ─ 36 ─
CF3 ─ 16°09'40.0"N, 90°54'04.5"W ─ ─ ─ 44 ─
Occupied fragments Marqués de Comillas region
OF1 14.4
Zamora Pico de Oro ejido
(16°19'52.0"N, 90°51'06.1"W) 450 200 29
35 ─
OF2 31
Zamora Pico de Oro ejido
(16°19'24.5"N, 90°50'43.7"W) 150 1200 24
39 ─
OF3 1125
Reforma Agraria ejido
(16°15'12.2"N, 90°49'59.5"W) 100 1100 26
41 ─
Unoccupied fragments Marqués de Comillas region
UF1 6.4
Chajul ejido
(16°06'39.5"N, 90°56'04.6"W) 200 150 19
0 15

186
Supplementary Table 2. Large-bodied frugivore composition of continuous and fragmented forests.
Animal taxon Common name Continuous forest Occupied fragments Unoccupied fragments
CF1 CF2 CF3 OF1 OF2 OF3 UF1 UF2 UF3
Mammalia
Rodentia
Agoutidae
Agouti paca Paca + +
Primates
Atelinidae
Alouatta pigra Black howler monkey + + + + + +
Ateles geoffroyi vellerosus Black-handled spider monkey + + + + + +
Artiodactyla
Tayassuidae
Dicotyles pecari White-lipped peccary + + +
Tayassu tajacu Collared peccary + + + +
Cervidae
Manzama americana Red brocket + + +
Odocoileus virginianus White-tailed deer + + + + + + +
Perissodactyla
Tapiridae
Tapirus bairdii Baird’s tapir + + + + +
Carnivora
Procyonidae
Potos flavus Kinkajou + + + +
Aves

187
Cracidae
Crax rubra Great curassow + + + + +
Ortalis vetula Plain chachalaca + + + + + + + +
Penelope purpurascens Crested guan + + + + + +
Ramphastidae
Pteroglossus torquatus Collared aracari + + + +
Ramphastos sulfuratus Keel-billed tucan + + + + + + + +
Trogonidae
Trogon elegans Elegant trogon + + + + + + + +
Trogon massena Slaty-tailed trogon + + + + + + + +
Total number of species 13 16 16 6 11 11 4 2 8
Presence is indicated with plus (+) signs.

188
Supplementary Table 3. Top ten seedling species found in continuous forest and fragments in Lacandona.
Habitat type
Seedling species
Family
Growth form
Dispersal
Modea
%Total seedling
abundance
Continuous forest Ampelocera hottlei Ulmaceae Tree PD 32.8
Castilla elastica Moraceae Tree SMD 15.1
Brosimum alicastrum Moraceae Tree SMD 12.3
Virola guatemalensis Myristicaceae Tree SMD 6.7
Guarea glabra Meliaceae Tree SMD 5.6
Acacia usumacintensis Fabaceae Tree GD 3.0
Dialium guianense Fabaceae Tree PD 2.3
Celtis iguanaea Vitaceae Vine SMD 2.2
Abuta panamensis Menispermaceae Vine PD 1.8
Inga pavoniana Fabaceae Tree PD 1.4
Occupied fragments Inga punctata Fabaceae Tree SMD 22.1
Brosimum alicastrum Moraceae Tree SMD 17.7
Castilla elastica Moraceae Tree SMD 11.1
Guarea glabra Meliaceae Tree SMD 10.4

189
Dialium guianense Fabaceae Tree PD 6.3
Brosimum lactescens Moraceae Tree SMD 3.4
Nectandra reticulata Lauraceae Tree SMD 2.4
Paullinia costata Sapindaceae Vine SMD 2.2
Spondias radlkoferi Anacardiaceae Tree PD 1.9
Posoqueria latifolia Rubiaceae Tree PD 1.8
Unoccupied fragments Licania hypoleuca Chrysobalanaceae Tree GD 20.8
Brosimum alicastrum Moraceae Tree SMD 17.1
Vochysia guatemalensis Vochisiaceae Tree WD 16.2
Brosimum lactescens Moraceae Tree SMD 12.6
Xylopia frutescens Annonaceae Shrub SMD 4.6
Inga vera Fabaceae Tree SMD 3.7
Ampelocera hottlei Ulmaceae Tree PD 2.1
Hirtella americana Chrysobalanaceae Tree SMD 1.9
Pseudolmedia oxyphyllaria Moraceae Tree SMD 1.9
Vatairea lundellii Ulmaceae Tree WD 1.8
aDispersal mode: PD, primate-dispersed; SMD, small and medium vertebrates-dipserded; GD, gravity-dispersed; WD, wind-dispersed.

190
Supplementary Table 4. Observed and expected species richness in seedling communities
in continuous and fragmented forests in Lacandona, Chiapas, Mexico.
Seed dispersal mode by
Habitat typea
Number of
observed species ACEb ICEc Chao 2 Bootstrap Completenessd
All dispersal modes
UF1 51 77 71 84 86 71-86
UF2 47 78 76 87 86 76-87
UF3 49 66 60 49 86 49-86
OF1 42 69 72 79 84 69-84
OF2 36 74 60 74 85 60-85
OF3 40 80 73 78 86 73-86
CF1 37 81 75 71 87 71-87
CF2 35 91 84 93 89 84-93
CF3 45 72 70 67 86 67-86
Primate Dispersed Species
UF1 9 94 95 100 92 92-100
UF2 4 84 84 100 87 84-100
UF3 5 100 100 100 100 100
OF1 8 100 100 100 93 93-100
OF2 9 92 85 97 90 85-97
OF3 6 90 90 100 92 90-100
CF1 8 95 96 100 95 95-100
CF2 8 100 100 100 98 98-100
CF3 7 100 100 100 100 100
Small and Medium Vertebrate
Dispersed Species
UF1 31 79 73 89 86 73-89
UF2 32 84 84 93 88 84-93
UF3 30 75 69 89 87 69-89
OF1 19 80 86 93 88 80-93
OF2 17 76 62 77 85 62-85

191
OF3 26 70 65 66 85 66-85
CF1 25 75 65 70 84 65-84
CF2 17 79 78 92 87 78-92
CF3 27 68 62 55 85 55-85
Wind Dispersed Species
UF1 2 100 100 100 100 100
UF2 3 75 76 76 81 75-81
UF3 5 45 46 46 77 45-77
OF1 1 ─ ─ ─ ─ ─
OF2 5 51 41 48 78 41-78
OF3 4 100 100 100 94 94-100
CF1 2 100 100 100 100 100
CF2 4 100 87 100 87 87-100
CF3 2 100 100 100 95 95-100
Gravity Dispersed Species
UF1 5 85 59 84 87 59-87
UF2 4 80 55 80 85 55-85
UF3 6 50 36 50 81 36-81
OF1 5 77 78 100 85 77-100
OF2 3 85 86 100 88 85-100
OF3 3 100 97 100 100 97-100
CF1 2 100 65 100 85 65-100
CF2 4 85 85 100 87 85-100
CF3 4 90 89 100 89 89-100
a Abbreviations: UF, unoccupied fragments; OF, occupied fragments; CF, continuous
forest areas of the MABR (for further details see methods).
b Abundance-based coverage nonparametric richness estimator.
c Incidence-based coverage nonparametric richness estimator.
d Percentage of expected richness covered by sampling effort (range).

192
References
Chaves, O.M., Stoner, K.E., Arroyo-Rodríguez, V., Benítez-Malvido, J., Estrada, A., 2010.
Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in
continuous and fragmented rainforests in Southern Mexico. International Journal of
Primatology (in press).
Gentry, A.H., 1982. Patterns of neotropical plant species diversity. Evolutionary Biology
15, 1-84.
Reid, F., 1997. A field guide to the mammals of Central America and Southeast Mexico.
Oxford University Press, Oxford.

193
DISCUSIÓN GENERAL
Influencia de la disponibilidad de alimento en la dieta
Diferentes estudios en primates tropicales han demostrado que su dieta es más
diversa en fragmentos de bosque que en bosque continuo (e.g., Alouatta pigra: Rivera &
Calmé 2006, A. palliata: Cristóbal-Azkarate & Arroyo-Rodríguez 2007), lo cual se ha
relacionado con una menor disponibilidad de alimento en fragmentos (Arroyo-Rodríguez &
Mandujano 2006, Dunn et al. 2009). Por ejemplo, en África, Asia y América se ha
reportado que en fragmentos y/o periodos de escasez de frutos, los primates se alimentan de
partes vegetales alternativas (e.g., frutos inmaduros, hojas, corteza: Chapman 1987,
Fairgrieve & Muhumuza 2003, Cristóbal-Azkarate & Arroyo-Rodríguez 2007) y de formas
de crecimiento no arbóreas (e.g., trepadoras, hierbas, palmas: Onderdonk & Chapman
2000, Silver & Marsh 2003). De forma similar, los resultados de esta tesis sugieren que
debido a la reducción de alimento en fragmentos (e.g., menor densidad de árboles grandes
de las principales especies en la dieta), el mono araña se ve forzado a realizar importantes
ajustes en su dieta. Así, en fragmentos los monos araña: (1) consumieron módulos de una
mayor cantidad de especies de plantas; (2) incrementaron el consumo de hojas; y (3)
incrementaron el consumo de formas de hemiepífitas y palmas. En general, la evidencia
disponible indica que cuando los primates frugívoros se ven forzados a reducir el consumo
de frutos e incrementar el consumo de otros módulos vegetales de menor contenido
energético (como ocurrió en este estudio), tienden a diversificar su dieta. Este
comportamiento les permite diluir el posible efecto que pueden tener los metabolitos
secundarios en la salud (Freeland & Janzen 1974, Glander 1982) y a la vez incrementa la
probabilidad de que los animales puedan satisfacer sus necesidades nutricionales, ya que

194
ningún módulo vegetal en particular contiene todos los nutrientes que requiere un primate
(Lambert 2007). Esto es especialmente cierto en sitios con una baja disponibilidad de
alimentos con alto contenido energético (e.g., frutos), como es el caso de los fragmentos
boscosos de la Selva Lacandona.
El mayor consumo de material foliar en fragmentos podría afectar negativamente tanto la
salud del mono araña como la dinámica de la comunidad de plantas. Por ejemplo, los
monos araña podrían estar limitados en cuanto a la cantidad de material foliar que pueden
consumir debido a que su sistema digestivo está especializado para una dieta compuesta
principalmente de frutos maduros (Milton 1981, 1993, Lambert 1998). Como consecuencia
de una dieta más folívora, en algunas especies de atelinidos se ha reportado una reducción
abrupta del peso corporal (e.g., Alouatta palliata: Glander 2006; Ateles chamek: Karesh et
al. 1998), lo cual a largo plazo puede afectar la fertilidad y sobrevivencia de los animales.
Además, en estos mismos grupos de monos, nuestros datos sugieren que la eficiencia de A.
geoffroyi como dispersor de semillas podría ser menor en fragmentos que en bosque
continuo ya que en fragmentos se reduce tanto el porcentaje de excretas con semillas como
el porcentaje de semillas ingeridas (ver capítulo II).
Pese a la diversidad de la dieta en cuanto a especies de plantas y formas de vida (ver
Anexo), en ambos hábitats el mono concentró su tiempo de alimentación (≥ 80% del
tiempo total de alimentación) en un grupo relativamente pequeño de especies (Ficus spp.,
Spondias spp., Brosimum spp., Dialium guianense, y Licania platypus), las cuales también
han sido reportadas como ‘top’ especies en la dieta de A. geoffroyi a lo largo de
Mesoamérica (González-Zamora et al. 2009). Este comportamiento puede estar relacionado
con una mayor abundancia de especies, el gran tamaño de los árboles y la consecuente
mayor producción de alimento. Además, en el caso particular de Ficus spp., los ciclos

195
fenológicos asincrónicos de estas especies (Ibarra-Manríquez & Oyama 1992), permiten
que el mono araña consuma sus síconos a lo largo de todo el año (Weghorst 2007, Felton et
al. 2008). Por tanto, la abundancia de estas especies debe considerarse un factor
fundamental a la hora de evaluar la calidad del hábitat para los monos araña ya que puede
influir directamente en su dinámica poblacional y sobrevivencia a largo plazo.
Eficiencia en la dispersión de semillas
Como se predijo, los monos araña fueron dispersores eficientes en términos
cuantitativos y cualitativos tanto en bosque continuo como en fragmentos, lo cual es
consistente con otros estudios en monos araña que han demostrado que éstos son eficientes
en términos de la diversidad de frutos en la dieta, la manipulación de las semillas, la riqueza
de semillas defecadas y el patrón de defecación (e.g., Ateles spp.: Russo et al. 2005, A.
belzebuth: Link & Di Fiore 2006, Dew 2008). No obstante, los servicios de dispersión
brindados por el mono araña en Lacandona probablemente sean más importantes para
especies con semilla grande (>1 cm de diámetro) como Ampelocera hottlei (Ulmaceae),
Spondias spp. (Anacardiaceae) y Attalea butyracea (Arecaceae) debido a que existe una
relación inversa entre el tamaño de la semilla y el número potencial de dispersores (Jordano
1995).
Las relaciones entre las angiospermas y sus dispersores generalmente son descritas
como un tipo de coevolución “difusa” y no como una coevolución estrecha entre pares
(Herrera 1985, Ericksson 2008), lo cual implica que la desaparición de cualquiera de los
interactuantes muy rara vez conduciría a la desaparición del otro. Pese a esta realidad, los
servicios de los dispersores legítimos (como es el caso del mono araña) indudablemente

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pueden favorecer el flujo génico y el reclutamiento de las especies de frutos más
importantes en sus dietas (Stevenson & Aldana 2008, Gutiérrez-Granados & Dirzo 2010).
Los resultados también sugieren que la eficiencia del mono araña como dispersor
podría ser menor en fragmentos debido a que en comparación con el bosque continuo: 1) se
redujo la proporción de semillas tragadas y se incrementó la proporción de semillas
escupidas bajo el árbol parental, y 2) se redujo considerablemente el porcentaje de excretas
que contenían semillas, lo cual es reflejo de la mayor folivoría de los monos araña en los
fragmentos. Este resultado puede tener importantes implicaciones ecológicas, ya que la
regeneración de la comunidad de plantas podría ser más lenta (particularmente en el caso de
especies con semilla grande) en los fragmentos en comparación con el bosque continuo, tal
y como se ha encontrado en estudios recientes con monos araña y otras especies
emparentadas (e.g., Ateles belzebuth y Lagothrix lagotricha: Stevenson & Aldana 2008, A.
geoffroyi).
Influencia de la disponibilidad de recursos sobre los patrones de actividad
Los resultados también indicaron que como probable respuesta a la menor
disponibilidad de recursos alimenticios para los monos en fragmentos y durante la estación
seca (ver capítulo III de esta tesis), éstos fueron capaces de realizar importantes ajustes en
el tiempo dedicado a actividades vitales como la alimentación, la locomoción y el descanso.
Los datos sugieren que para compensar la menor disponibilidad y calidad de alimento en
fragmentos, los monos dedicaron más tiempo a la alimentación, lo cual también ha sido
reportado en diferentes poblaciones de A. geoffroyi en fragmentos de Punta Laguna,
México (Ramos-Fernández & Ayala-Orozco 2003). Debido a que el sistema digestivo de
los monos araña está diseñado para una dieta basada en módulos vegetales con un bajo

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contenido de fibra (Milton 1981, Lambert 1998), cuando aumenta el consumo de hojas
(como ocurrió en Lacandona, ver capítulo I), los monos deben invertir más tiempo en
alimentación para poder obtener suficiente cantidad de energía y nutrientes. Resultados
similares también se han reportado para babuinos (Iwamoto & Dunbar 1983) y gorilas de
montaña (Watts 1988). Sin embargo, en contraste con lo esperado, el tiempo dedicado a la
alimentación fue mayor en la época lluviosa y no en la seca. Este resultado podría
explicarse por el hecho de que durante la estación lluviosa la disponibilidad de frutos es
mayor y el mono araña tiende a alimentarse más durante este periodo con el fin de ingerir
energía y almacenarla en forma de grasa que utilizará para sobrevivir durante los periodos
de escasez (Felton et al. 2009). Adicionalmente, estudios recientes sugieren que el
incremento en la temperatura durante la estación seca, obliga a muchas especies de
primates (incluyendo a los monos araña) a reducir el tiempo dedicado a actividades como la
alimentación para minimizar los costos energéticos relacionados con la termoregulación
(Campos & Fedigan 2009, Dunbar et al. 2009, Korstjens et al. 2010).
Como resultado de la escasez de frutos, el mayor consumo de hojas y un menor
tiempo de alimentación durante la estación seca en Lacandona, los monos se vieron
obligados a descansar más tiempo, lo cual puede representar una estrategia no solamente
para minimizar los costos del sobrecalentamiento como ya se mencionó, sino también
porque el descanso es una demanda fisiológica de una dieta más folívora (Milton 1981,
Korstjens et al. 2010). En general, en la mayoría de primates el tiempo de descanso es una
función directa de la estacionalidad, la temperatura promedio, y el porcentaje de hojas en la
dieta (Korstjens et al. 2010). Además, el hecho de que el tiempo dedicado al descaso fuera
similar en bosque continuo y en fragmentos, sugiere que esta actividad está más afectada
por los cambios en temperatura (como sugieren Korstjens et al. 2010) y/o disponibilidad de

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alimento entre estaciones que por cambios en la disponibilidad de alimento entre estos dos
hábitats. Sin embargo, debido a que no existen datos climatológicos para todos los sitios de
estudio, no es posible confirmar esta hipótesis.
De acuerdo con la teoría de forrajeo óptimo, el tiempo que invierten los animales en
sus movimientos de forrajeo es una función de la cantidad y la calidad de parches de
alimentación disponibles en su hábitat (MacArthur & Pianka 1966). Por tanto en aquellos
animales que se alimentan de recursos con un alto grado de agregación espacial y temporal
(e.g., frutos maduros: Zimmerman et al.2007), es de esperarse que el tiempo invertido en
desplazamiento entre parches de alimentación esté directamente relacionado con la
disponibilidad de los mismos (Charnov & Orians 1973). Esta hipótesis puede ser
particularmente cierta en el caso de Ateles spp., ya que estos primates prefieren alimentarse
en parches de alimentación (i.e., conglomerados de plantas que producen frutos importantes
en la dieta de los monos araña) de frutos carnosos que están muy espaciados entre sí, lo
cual los obliga a moverse constantemente de un lugar a otro (Chapman & Chapman 2000).
Los datos de la tesis apoyan esta idea ya que en bosque continuo los monos araña
invirtieron más tiempo en locomoción que en fragmentos, probablemente porque estos
primeros hábitats presentaron una mayor disponibilidad de recursos alimenticios
importantes para los monos araña (ver capítulo I de esta tesis).
No obstante, en contraste con la predicción, durante la estación seca los monos
tendieron a invertir más tiempo moviéndose, lo cual también se ha reportado en primates de
Madagascar (Eulemur spp.: Overdorff 1993) e Indonesia (Tarsius spectrum: Gursky 2000).
Esto sugiere que para compensar la menor disponibilidad y el mayor espaciamiento de los
parches de frutos durante la estación seca (Zimmerman et al. 2007), los monos requieren
invertir más tiempo moviéndose para incrementar la probabilidad de encontrar suficiente

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alimento para satisfacer sus necesidades nutricionales. Pese a que los resultados muestran
que el mono araña tiene la capacidad de realizar ajustes conductuales en respuesta a la
limitación de recursos en fragmentos y durante la estación seca, no se sabe si esta
flexibilidad es suficiente como para garantizar la sobrevivencia de los monos a largo plazo.
Reducción en la abundancia de especies de semilla grande en fragmentos sin monos
Finalmente, los resultados indicaron que la ausencia de primates alteró la
composición de plántulas, reduciendo la abundancia y riqueza de especies de semilla
grande y favoreciendo tanto la riqueza de especies dispersadas por vertebrados pequeños
como la abundancia de especies dispersadas por medios abióticos (ver capítulo IV, Anexo).
Estos resultados concuerdan con lo que se ha encontrado en sitios sometidos a una alta
presión de cacería de primates grandes en el sureste de Perú (Nuñez-Iturri & Howe 2007,
Nuñez-Iturri et al. 2008). Estos estudios demuestran que la reducción de las poblaciones de
primates ha tenido afectos negativos sobre el reclutamiento de especies de semilla grande y
ha favorecido el reclutamiento de especies dispersadas por medios abióticos. Resultados
similares también se han encontrado en poblaciones de primates en fragmentos de la Selva
Lacandona (González-Di Pierro et al. datos no publicados), en Uganda (Chapman &
Onderdonk 1998), en Madagascar (Ganzhorn et al. 1999), en Belize (Marsh & Loiselle
2003), y en Colombia (Stevenson & Aldana 2008). Por ejemplo, en este último país la
desaparición de Ateles belzebuth y Lagothrix lagotricha en fragmentos de La Macarena se
ha traducido en una baja representación de especies de semilla grande en comparación con
el bosque continuo de Tinigua, el cual presenta poblaciones protegidas de ambas especies
de primates (Stevenson & Aldana 2008). De igual forma, en sitios sometidos a tala
selectiva, en la Península de Yucatán, México, la desaparición de A. geoffroyi propició un

200
incremento en la densidad y la dominancia de plántulas de Manilkara zapota (una especie
con semilla >1.5 cm de largo) bajo los parentales y una reducción de la diversidad de
plántulas de sotobosque en comparación con los sitios no talados que contenían monos
araña (Gutiérrez-Granados & Dirzo 2010). A pesar de las diferencias metodológicas entre
todos estos estudios y el mío, todos consistentemente muestran que la desaparición de los
primates frugívoros tiene profundas repercusiones sobre la composición de la comunidad
de plántulas, limitando el reclutamiento de las especies que producen frutos carnosos con
semillas grandes (las cuales son principalmente dispersadas por este tipo de primates).
Además, como se menciona en el capítulo IV de esta tesis, de ocho diferentes
variables ecológicas analizadas, la abundancia de monos araña junto con la riqueza de
animales frugívoros grandes son las que están más correlacionadas con la composición de
plántulas en cada tipo de bosque. Resultados similares también han sido observados
recientemente para diferentes primates en Sudamérica (Ateles belzebuth: Stevenson &
Aldana 2008) y en la Selva Lacandona (Alouatta pigra: Gonzalez-Di Pierro et al., datos no
publicados).
Todo lo anterior sugiere que las estrategias de manejo y los esfuerzos de
conservación del bosque en la Selva Lacandona (y probablemente en otras regiones de
Mesoamérica) deben tomar en consideración el papel clave que juegan los monos araña
como dispersores no redundantes de especies con semilla grande. Debido a que los datos de
esta tesis sugieren que la eficiencia del mono araña como dispersor podría ser menor en
fragmentos (ver capítulo II), es importante que las futuras estrategias de conservación
consideren el establecimiento de corredores biológicos que conecten los fragmentos más
pequeños con los fragmentos grandes y/o bosques continuos. Esto contribuiría tanto a una
dispersión más eficiente de las semillas (especialmente de las semillas más grandes), como

201
a mejorar el estado de salud de las poblaciones de monos presentes en los diferentes
fragmentos. Es de esperarse que al conectar los fragmentos más pequeños en los cuales
habitan los monos con los fragmentos grandes, también aumentará la disponibilidad de
recursos para los monos (e.g., frutos, dormideros, acceso a parejas), lo cual podría
minimizar la aparición de los problemas de salud relacionados con el estrés (e.g., pérdida
de peso, baja fertilidad, mayor vulnerabilidad al parasitismo) que se presenta en los monos
araña que habitan en fragmentos (Rangel-Negrín et al. 2009).

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CONCLUSIONES GENERALES
1) En comparación con el bosque continuo, los fragmentos presentaron una menor
disponibilidad de recursos alimenticios para A. geofroyi, lo cual se tradujo en cambios
considerables en su dieta, en su papel como dispersores de semillas, y en el tiempo que
invierten en alimentación, locomoción y descanso en ambos tipos de hábitat.
2) En Lacandona, Ficus spp., Spondias spp., Brosimum spp., Dialium guianense, y Licania
platypus representan las especies más importantes en la dieta del mono araña en bosque
continuo y en fragmentos. Por tanto, la densidad de árboles grandes de estas especies se
podría usar como un importante indicador de calidad de hábitat para el mono en
fragmentos. Así, el tamaño de las poblaciones de monos que un determinado fragmento
boscoso puede tolerar podría estar en función no sólo del tamaño del fragmento, sino de la
densidad de árboles adultos de estas especies, tal y como se ha encontrado para los monos
aulladores en Los Tuxtlas (Arroyo-Rodríguez & Mandujano 2006) y en la Lacandona
(González-Di Pierro et al. datos no publicados). Esto se debe tener en consideración a la
hora de realizar cualquier programa de conservación y/o reintroducción de esta especie.
3) Debido a la menor disponibilidad de recursos alimenticios para los monos araña en los
fragmentos en comparación con el bosque continuo, éstos se ven forzados a realizar
cambios conductuales que le permiten tolerar el estrés alimenticio. Entre estos cambios
destacaron el incremento en el consumo de hojas y formas de vida no arbóreas (e.g.,
hemiepífitas y palmas), el incremento del tiempo total de alimentación, y la reducción del
tiempo invertido en actividades energéticamente costosas (e.g., locomoción). De igual

203
forma, el estrés alimenticio durante la estación seca se tradujo en un mayor tiempo de
descanso en comparación con la estación seca. Probablemente estos cambios conductuales
representan una estrategia adaptativa para lidiar con una dieta de menor calidad (i.e., con
mayor contenido de fibra) y minimizar los costos energéticos relacionados con la
locomoción y la termoregulación tal y como sugieren los modelos socio-ecológicos de
primates (e.g., Korstjens et al. 2006, 2010, Dunbar 2009). Sin embargo, son indispensables
más estudios en fragmentos y bosques continuos para determinar si la plasticidad
conductual del mono araña (en la dieta y en los patrones de actividad) es suficiente como
para garantizar su sobrevivencia a largo plazo, particularmente en los fragmentos de bosque
más pequeños.
4) Debido a que la eficiencia del mono araña como dispersor tiende a ser menor en
fragmentos como resultado de cambios en la manipulación de las semillas y a un menor
porcentaje de excretas con semillas, es necesario que los esfuerzos de conservación en
Lacandona se enfoquen en incrementar la conectividad entre fragmentos, especialmente
entre los fragmentos pequeños y los fragmentos más grandes. Esto se traducirá en una
mayor disponibilidad de recursos alimenticios (particularmente frutos) para los monos
araña y por tanto, es razonable esperar que aumente su eficiencia como dispersores. A largo
plazo, y bajo el supuesto de que las alteraciones antropogénicas sean mínimas, la dispersión
de semillas por los monos podría contribuir considerablemente a la regeneración de la
selva.
5) La desaparición de los monos araña puede tener profundas repercusiones en la
composición de la comunidad plántulas y por ende en la futura comunidad de árboles.

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Como se ha reportado en otros trabajos similares (ver discusión), la desaparición de los
primates tropicales propicia una reducción en el reclutamiento de especies de semilla
grande (e.g., Spondias spp., Ampelocera hottlei y Virola spp.) y un incremento del
reclutamiento de especies dispersadas por vertebrados pequeños y por medios abióticos.
6) Todo lo anterior sugiere que las estrategias de manejo y los esfuerzos de conservación en
la Selva Lacandona deben tomar en consideración el papel clave que juegan los monos
araña como dispersores eficientes de muchas especies de árboles con semilla grande y su
capacidad relativa para realizar ajustes conductuales que le permitan lidiar con el aumento
de la deforestación, la pérdida de hábitat y el calentamiento global. En este sentido, la
pérdida de hábitat quizás sea la mayor amenaza para las poblaciones silvestres de A.
geoffroyi (Ramos-Fernández & Wallace 2008). No obstante, los modelos socio-ecológicos
(e.g., Korstjens et al. 2006) también indican que incrementos relativamente pequeños en la
temperatura ambiental (e.g., 2-5 °C) podrían comprometer seriamente la sobrevivencia de
los monos araña e incluso propiciar su extinción. Esto difícilmente conduciría a la
desaparición de sus especies de frutos preferidos (incluso en el caso de las plantas que
tienen semillas grandes como Spondias spp. y Attalea butyracea.) debido a que la relación
entre dispersores y plantas es generalmente una coevolución “difusa” (Herrera 1985). No
obstante, los resultados del capítulo IV sugieren que en ausencia de los monos la
composición y estructura de las comunidades de árboles de la Selva Lacandona podrían
cambiar considerablemente a largo plazo, dando origen a bosques dominados por especies
dispersadas por medios abióticos y/o vertebrados pequeños.

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Anexo
Listados de las especies de plantas en la dieta del mono araña y de las especies
de plántulas encontradas en los diferentes hábitats estudiados en la
Selva Lacandona

211
Cuadro 1. Lista de 152 especies de plantas consumidas por las comunidades de monos
araña estudiadas en bosque continuo y en fragmentos de la Selva Lacandona, Chiapas. 1=
frutos maduros, 2= frutos inmaduros, 3= hojas maduras, 4= hojas nuevas, 5= flores, 6=
madera podrida, 7= ramas, 8= zarcillos, 9= secreciones vegetales, 10= estípula terminal,
11= raíces, 12= semillas, % TTA= porcentaje del tiempo total de alimentación (n = 205 h
en bosque continuo y n = 243 h en fragmentos, ver más detalles en capítulo I).
Especie/Morfoespecie Familia Forma de vida Parte
consumida % TTA
Bosque Fragmentos
Licania platypus Chrysobalanaceae Árbol 1,4,6,7 31.2 4.9
Spondias radlkoferi Anacardiaceae Árbol 1,2,7 22.5 10.7
Spondias mombin Anacardiaceae Árbol 1,2,5 6.2 1.9
Ficus tecolutensis Moraceae Hemiepífita 1 4.6 12.2
Brosimum alicastrum Moraceae Árbol 1,2,4 4.4 9.7
Dialium guianense Fabaceae Árbol 1,2,4 3.8 18.3
Ampelocera hottlei Ulmaceae Árbol 1 3.6 0
Ficus obtusifolia Moraceae Hemiepífita 1,2 2.5 0.8
Strychnos tabascana Loganiaceae Bejuco 1,7 1.86 0.54
Ficus sp1 Moraceae Hemiepífita 1,2 1.6 8.2
Celtis iguanaea Ulmaceae Bejuco 1 1.6 0.5
Calatola laevigata Icacinaceae Árbol 1 1.5 2.2
Philodendron scandens Araceae Hemiepífita 4 1.25 0.64
Guarea glabra Meliaceae Árbol 1,2,7 1.1 1.31
Swietenia humilis Meliaceae Árbol 7 0.8 0
Ficus sp2 Moraceae Hemiepífita 1 0.8 2.2
Mortoniodendron guatemalense Malvaceae Árbol 1 0.68 0
Paullinia clavigera Sapindaceae Bejuco 4 0.71 0.023
Attalea butyracea Arecaceae Palma 1 0.63 0.22
Cecropia obtusifolia Cecropiaceae Árbol 1,4,10 0.53 0.14
Cissus verticillata Vitaceae Bejuco 1 0.45 0.041
Brosimum lactescens Moraceae Árbol 1 0.41 0.25
Abuta panamensis Menispermaceae Árbol 1,2 0.38 0.05
Pseudolmedia oxyphyllaria Moraceae Árbol 1 0.3 0.02

212
Cuadro 1. Continuación.
Especie/Morfoespecie Familia Forma de vida Parte
consumida % TTA
Bosque Fragmentos
Bejuco Msp8 (periquillo) Sapindaceae Bejuco 1,2 0.3 0.03
Syngonium chiapense Araceae Epífita 1 0.26 0.24
Alchornea latifolia Euphorbiaceae Árbol 1,2 0.26 0
Cecropia peltata Cecropiaceae Árbol 1,4 0.25 0.11
Manilkara sapota Sapotaceae Árbol 1,2 0.25 0.01
Machaeriumsp. Fabaceae Bejuco 4 0.23 0.11
Monstera acuminata Araceae Epífita 4 0.22 0.25
Ceiba pentandra Bombacaceae Árbol 4,5 0.21 0.24
Monstera sp1 Bromeliaceae Epífita 4 0.21 0.23
Nectandra ambingea Lauraceae Árbol 1,2 0.2 0.45
Ocotea dendrodaphne Lauraceae Árbol 1,2 0.2 1.1
Virola guatemalensis Myristicaceae Árbol 1 0.2 0.08
Pouteria campechiana Sapotacea Árbol 1,2,7 0.2 0.016
Ocotea sp. Lauraceae Árbol 1,5 0.19 0
Guarea grandifolia Meliaceae Árbol 1,2,7 0.18 0.45
Guarea sp. Meliaceae Árbol 1,2 0.14 0.17
Trophis racemosa Moraceae Árbol 1 0.14 0.45
Passiflora ambigua Pasifloraceae Bejuco 1 0.14 0
Philodendron radiatum Araceae Hemiepífita 4 0.13 0.32
Philodendron sp1 Araceae Hemiepífita 4 0.13 0.23
Cojoba arborea Fabaceae Árbol 1,4 0.13 0.51
Inga pavoniana Fabaceae Árbol 1,2 0.13 0.15
Paragonia pyramidata Bignoniaceae Bejuco 3,4 0.12 0.005
Combretum fructicosum Combretacea Bejuco 5 0.11 0.33
Orquidea Msp1 Orchidaceae Epífita 11 0.11 0.008
Hirtela sp. Chrysobalanaceae Árbol 1 0.1 0.007
Cupania dentata Meliaceae Arbusto 7 0.09 0
Castilla elastica Moraceae Árbol 1,7 0.09 0.14
Talauma mexicana Magnoliaceae Árbol 1 0.08 0
Brosimum costaricanum Moraceae Árbol 1,4,7 0.08 0
Bejuco Msp4 Bignoniaceae Bejuco 3,4 0.08 0
Combretum laxum Jacq. Combretacea Bejuco 5 0.07 0.39
Inga vera Fabaceae Árbol 1 0.07 0.02
Bravaisia integerrima Acanthaceae Árbol 3 0.06 0.85
Dioscorea mexicana Dioscoreaceae Bejuco 8 0.06 0

213
Cuadro 1. Continuación.
Especie/Morfoespecie Familia Forma de vida Parte
consumida % TTA
Bosque Fragmentos
Trichilia sp. Meliaceae Árbol 1 0.06 0
Árbol Msp3 — Árbol 4 0.06 0
Zanthoxylum kellermanii Rutaceae Árbol 4 0.05 0.72
Árbol Msp2 — Árbol 4 0.05 0.31
Orquidea Msp4 Orchidaceae Epífita 11 0.05 0
Thevetia ahouai Apocinaceae Arbusto 1 0.04 0.005
Protium copal Burseraceae Árbol 1,2 0.04 0
Inga punctata Fabaceae Árbol 1,2 0.04 1.08
Pterocarpus sp. Fabaceae Árbol 4 0.04 0
Brosimum sp. Moraceae Árbol 4 0.04 0.01
Bejuco Msp7 — Bejuco 4,7 0.04 0
Hirtella americana Chrysobalanaceae Árbol 1,7 0.03 0
Acacia sp1 Fabaceae Árbol 1,2 0.03 0.23
Ficus popenoei Moraceae Hemiepífita 1 0.03 0.2
Posoqueria latifolia Rubiaceae Árbol 1,7 0.03 0.08
Ramdia sp. Rubiaceae Arbusto 1 0.03 0.034
Astronium graveolens Anacardiaceae Árbol 4 0.02 0
Cymbopetalum mayanum Anonaceae Árbol 1 0.02 0.01
Mostera sp2 Bromeliaceae Epífita 4 0.02 0.015
Tetracera sp. Dilleniaceae Bejuco 1 0.02 0
Albizia leucocalyx Fabaceae Árbol 4 0.02 0.06
Inga sp1 Fabaceae Árbol 1,2 0.02 0.034
Acacia cornigera Fabaceae Arbusto 1 0.02 0.015
Lonchocarpus sp1 Fabaceae Bejuco 4,7 0.02 0.011
Lonchocarpus sp2 Fabaceae Bejuco 4 0.02 0
Calophyllum brasiliense Guttiferaceae Árbol 1,2 0.02 0
Licaria capitata Lauraceae Árbol 1 0.02 0
Luehea semanni Malvaceae Árbol 7 0.02 0.51
Quararibea funebris Malvaceae Árbol 1,2 0.02 0
Psidium sp. Myrtaceae Árbol 1,2 0.02 0
Passiflora sp. Pasifloraceae Bejuco 8 0.02 0.01
Bejuco Msp5 — Bejuco 4 0.02 0
Bejuco Msp9 Fabaceae Bejuco 4 0.02 0
Iresine sp. Amaranthaceae Bejuco 1 0.01 0
Stemmadenia donnel-smithii Apocinaceae Árbol 2 0.01 0

214
Cuadro 1. Continuación.
Especie/Morfoespecie Familia Forma de vida Parte
consumida % TTA
Bosque Fragmentos
Monstera sp. Araceae Epífita 4 0.01 0
Philodendron tripartitum Araceae Hemiepífita 4 0.01 0
Syngonium podophyllum Araceae Epífita 1,4 0.01 0
Capparis quiriguensis Caparidaceae Árbol 1,2 0.01 0.1
Schizolobium parahybum Fabaceae Árbol 2,5 0.01 0.71
Souroubea guianensis Marcgraviaceae Bejuco 1 0.01 0.1
Parathesis sp Myrsinaceae Arbusto 2 0.01 0
Epidendrum sp. Orchidaceae Epífita 11 0.01 0
Passiflora cookii Pasifloraceae Bejuco 1 0.01 0
Peperomia sp. Piperaceae Epífita 4 0.01 0
Paullinia fibrigera Sapindaceae Bejuco 4 0.01 0.03
Orquidea Msp5 Orchidaceae Epífita 4 0.01 0
Bejuco Msp2 Bignoniaceae Bejuco 4 0.01 0
Anthurium sp. Araceae Epífita 1 0.004 0
Nectandra reticulata Lauraceae Árbol 1,7 0.003 0.18
Reinhardtia gracilis Arecaceae Palma 1,2 0.001 0
Epiphyllum phyllanthus Cactaceae Epífita 1 0.001 0
Clusia sp. Clusiacae Árbol 4 0.001 0
Hibiscus sp. Malvaceae Árbol 5 0.001 0
Dendropanax arboreum Araliaceae Árbol 1,2 0 0.022
Bactris mexicana Arecaceae Palma 1 0 0.16
Bactris baduca Arecaceae Palma 1 0 0.15
Sabal mexicana Arecaceae Palma 1,9 0 2.2
Pithecoctenium crucigerum Bignoniaceae Árbol 5 0 0.016
Bromelia sp. Bromeliaceae Epífita 4 0 0.001
Tetracera volubilis Dilleniaceae Bejuco 1 0 0.1
Inga sp2 Fabaceae Árbol 1 0 0.031
Acacia farnesiana Fabaceae Árbol 1,2 0 0.17
Acacia sp2 Fabaceae Arbusto 1,2 0 0.28
Mucuna pruriens Fabaceae Bejuco 2 0 0.038
Semialarium sp. Hippocrateaceae Bejuco 12 0 0.19
Ochroma pyramidale Malvaceae Árbol 1 0 0.009
Pachira aquatica Malvaceae Árbol 5 0 0.013
Theobroma cacao Malvaceae Árbol 1,2 0 0.35
Mouriri mirtilloides Melastomataceae Arbusto 1,7 0 0.038

215
Cuadro 1. Continuación.
Especie/Morfoespecie Familia Forma de vida Parte
consumida % TTA
Bosque Fragmentos
Coussapoa oligocephala Moraceae Árbol 4 0 0.34
Maclura tinctoria Moraceae Árbol 1,2 0 1.66
Poulsenia armata Moraceae Árbol 1 0 1.61
Ficus insipida Moraceae Hemiepífita 1,6 0 3.2
Ficus yoponensis Moraceae Hemiepífita 4 0 0.31
Ficus sp3 Moraceae Hemiepífita 1,6 0 0.1
Ficus sp4 Moraceae Hemiepífita 1 0 1.4
Ficus sp5 Moraceae Hemiepífita 1 0 0.03
Blepharidium mexicanum Rubiaceae Árbol 7 0 0.18
Faramea occidentalis Rubiaceae Arbusto 1 0 0.08
Psychotria papantlensis Rubiaceae Arbusto 1,7 0 0.043
Zanthoxylum procerum Rutaceae Árbol 4 0 0.03
Paullinia costata Sapindaceae Bejuco 1,2 0 0.001
Serjania goniocarpa Sapindaceae Bejuco 4 0 0.027
Serjania mexicana Sapindaceae Bejuco 4 0 0.01
Árbol Msp1 (c.f. de Ocotea) Lauraceae Árbol 5 0 0.01
Árbol Msp4 Anonaceae Árbol 1 0 0.041
Árbol Msp5 Myrtaceae Árbol 4 0 0.2
Árbol Msp 6 (Palo blanco) — Árbol 3 0 0.39
Orquidea Msp2 Orchidaceae Epífita 11 0 0.034
Bejuco Msp1 (c.f. de
Bahuinia) Fabaceae Bejuco 4 0 0.18
Bejuco Msp3 Bignoniaceae Bejuco 4 0 0.13
Bejuco Msp6 — Bejuco 7 0 0.03

216
Cuadro 2. Lista de 88 especies de plántulas encontradas en bosque continuo (BC), fragmentos ocupados por monos (FO), y
fragmentos desocupados (FD). Para cada especie se indica el porcentaje de abundancia relativa en cada uno de los tres hábitats.
Especie/Morfoespecie Familia
Forma de
crecimiento Dispersor % de abundancia
BC FO FD
Abuta panamensis (Standl.) Krukoff & Barneby Menispermaceae Bejuco primates 1.8 0.87 0.29
Acacia cornigera (L.)Willd. Fabaceae Arbusto otros vertebrados 0.13 0.58 0
Acacia sp1 Fabaceae Arbusto otros vertebrados 0.22 0.87 0
Acacia sp2 Fabaceae Arbusto otros vertebrados 0.15 0 0
Acacia sp3 Fabaceae Arbusto otros vertebrados 0 0.27 0
Acacia usumacintensis Lundell Fabaceae Árbol otros vertebrados 2.97 0.97 0.81
Albizia leucocalyx Standley Fabaceae Árbol gravedad 0.26 1.26 0.11
Ampelocera hottlei (Standl.) Standl. Ulmaceae Árbol primates 32.8 0.87 2.1
Andira inermis(W. Wright) DC. Fabaceae Árbol otros vertebrados 0 0 0.1
Astronium graveolens Jacq. Anacardiaceae Árbol viento 0 0.29 0.07
Bravaisia integerrima Standl. Acanthaceae Árbol otros vertebrados 0.12 0.19 0
Brosimum alicastrum Sw. Moraceae Árbol otros vertebrados 12.28 17.67 17.06
Brosimum costaricanum Liebm. Moraceae Árbol otros vertebrados 0.12 0.25 0
Brosimum lactescens (S. Moore) C.C. Berg Moraceae Árbol otros vertebrados 0.42 3.39 1.81
Bursera simaruba (L.) Sarg. Burseraceae Árbol otros vertebrados 0 0 0.58

217
Cuadro 2. Continuación.
Especie/Morfoespecie Familia FC Dispersor % de abundancia
BC FO FN
Calatola laevigata Standley Icacinaceae Árbol otros vertebrados 0.19 0.19 0.47
Calatola sp. Icacinaceae Árbol otros vertebrados 0.01 0 0
Calophyllum brasiliense Cambess. Guttiferaceae Árbol otros vertebrados 0 0 0.38
Calophyllum sp. Guttiferaceae Árbol otros vertebrados 0 0 0.14
Casearia sp, Flacourtiaceae Arbusto otros vertebrados 0 0 0.11
Castilla elastica Sessé Moraceae Árbol otros vertebrados 15.13 11.07 1.19
Cecropia obtusifolia Bertol. Cecropiaceae Árbol otros vertebrados 0 0 0.1
Ceiba pentandra (L.) Gaertn. Bombacaceae Árbol viento 0.17 0.01 0
Celtis iguanaea (Jacq.) Sarg. Vitaceae Bejuco otros vertebrados 2.19 0.29 0.25
Cojoba arborea (L.)Britton & Rose Fabaceae Árbol otros vertebrados 0.29 1.07 0
Cordia alliodora(Ruiz. & Pav.) Oken Boraginaceae Árbol viento 0 0.29 0.57
Cordia sp. Boraginaceae Árbol viento 0 0.19 0.34
Croton schiedeanus Schlecht. Euphorbiaceae Árbol otros vertebrados 0 0.49 1.29
Croton sp. Euphorbiaceae Árbol otros vertebrados 0 0.58 0.15
Cupania dentata Sapindaceae Arbusto otros vertebrados 0.13 0.11 0.57
Cupania sp1 Sapindaceae Arbusto otros vertebrados 0 0.11 0.23

218
Cuadro 2. Continuación.
Especie/Morfoespecie Familia FC Dispersor % de abundancia
BC FO FN
Cupania sp2 Sapindaceae Arbusto otros vertebrados 0 0 0.09
Paullinia costata Sapindaceae Bejuco otros vertebrados 0.42 2.24 0.15
Cymbopetalum mayanum Lundell Annonaceae Árbol otros vertebrados 0.46 0.79 0.19
Cymbopetalum sp. Annonaceae Árbol otros vertebrados 0 0 0.18
Dendropanax arboreum Decne. & Planch. Araliaceae Árbol otros vertebrados 0 0 0.08
Dialium guianense (Aubl.)Sandwith Fabaceae Árbol primates 2.26 6.31 0.75
Eugenia sp1 Myrtaceae Árbol otros vertebrados 0 0.97 0.15
Eugenia sp2 Myrtaceae Árbol otros vertebrados 0 0.19 0.18
Garcinia intermedia (Pittier) Hammel Clusiaceae Árbol otros vertebrados 0.46 0.68 0
Guarea glabra Vahl Meliaceae Árbol primates 5.62 10.39 0.15
Guarea grandifolia DC. Meliaceae Árbol primates 0.09 0.19 0
Guarea sp. Meliaceae Árbol otros vertebrados 0 0.04 0
Hirtella americana L. Chrysobalanaceae Árbol otros vertebrados 0.39 0 1.92
Hirtella sp. Chrysobalanaceae Árbol otros vertebrados 0.23 0 0.36
Hirtella tiandra Swartz Chrysobalanaceae Árbol otros vertebrados 0.11 0 0
Inga pavoniana G. Don Fabaceae Árbol primates 1.42 0.39 0.37

219
Cuadro 2. Continuación.
Especie/Morfoespecie Familia FC Dispersor % de abundancia
BC FO FN
Inga punctata Willd. Fabaceae Árbol otros vertebrados 1.19 22.14 1.67
Inga sp1 Fabaceae Árbol otros vertebrados 0.19 0.19 0
Inga sp2 Fabaceae Árbol otros vertebrados 0.11 0 0
Inga sp3 Fabaceae Árbol otros vertebrados 0.21 0 0.07
Inga vera Willd. Fabaceae Árbol otros vertebrados 0.63 0 3.67
Licania hypoleucaBenth. Chrysobalanaceae Árbol gravedad 0 0.39 20.79
Licania platypus (Hemsl.) Fritsch Chrysobalanaceae Árbol gravedad 0.23 0.11 0
Lonchocarpus guatemalensis Benth. Fabaceae Árbol viento 0 0 0.29
Lonchocarpus sp. Fabaceae Árbol viento 0 0 0.13
Maclura tinctoria (L.) D. Don ex Steud. Moraceae Árbol otros vertebrados 0.12 0.29 0
Miconia sp1 Melastomataceae Árbol otros vertebrados 0 0 0.42
Miconia sp2 Melastomataceae Árbol otros vertebrados 0 0 0.17
Mouriri myrtilloides (Swartz) Melastomataceae Árbol otros vertebrados 0.22 0.17 0.41
Nectandra ambingea Lauraceae Árbol otros vertebrados 1.42 2.43 1.38
Nectandra reticulata (Ruiz & Pavón) Mez Lauraceae Árbol otros vertebrados 0.9 0.33 0
Ouratea lucens Ochnaceae Arbusto otros vertebrados 0.19 0 1.21

220
Cuadro 2. Continuación.
Especie/Morfoespecie Familia FC Dispersor % de abundancia
BC FO FN
Platymiscium yucatanum Standley Fabaceae Árbol viento 0 0.79 0.14
Porouma bicolor Cecropiaceae Árbol otros vertebrados 0 0 1.52
Posoqueria latifolia(Rudge) Roem. & Schult. Rubiaceae Árbol primates 0.93 1.85 0.39
Pouteria campechiana (Kunth) Baehni Sapotaceae Árbol primates 1.36 0.38 1.52
Protium copal (Schltdl. & Cham.) Engl. Burseraceae Árbol otros vertebrados 0.47 0.38 0
Pseudolmedia oxyphyllaria J. D. Smith Moraceae Árbol otros vertebrados 0.31 0 1.85
Pterocarpus sp Fabaceae Árbol viento 0.19 0.38 0.47
Quararibea funebris (Llave) Vischer Bombacaceae Árbol otros vertebrados 0.81 0.29 0
Quararibea guatemalteca (J.D. Smith) Standley & Steyerm Bombacaceae Árbol otros vertebrados 0.32 0 0
Roupala montana Aubl. Proteaceae Arbusto otros vertebrados 0 0 0.97
Sabal mexicana Mart. Arecaceae Palma otros vertebrados 0 0.01 0
Spondias mombin L. Anacardiaceae Árbol primates 0 0.61 0.21
Spondias radlkoferi Donn.Sm. Anacardiaceae Árbol primates 0.26 1.94 0
Stemmadenia donnel-smithii (Rose ex Donn. Sm.) Woodson Apocinaceae Árbol otros vertebrados 0.33 0.03 0
Tabebuia guayacan (Seem.) Hemsley Bignoniaceae Árbol viento 0 0 0.12
Teobroma cacao L. Sterculiaceae Arbusto gravedad 0.17 0.34 0

221
Cuadro 2. Continuación.
Especie/Morfoespecie Familia FC Dispersor % de abundancia
BC FO FN
Tetracera volubilis L. Dilleniaceae Bejuco otros vertebrados 0 0 0.12
Thevetia ahouai (L.) A. DC. Apocinaceae Árbol otros vertebrados 0 0.01 0
Trichilia martiana C. DC. Meliaceae Árbol otros vertebrados 0 0 0.02
Trophis racemosa (L.) Urban Moraceae Árbol otros vertebrados 1.05 1.46 0.42
Vatairea lundellii (Standley) Killip ex Record Ulmaceae Árbol viento 0.62 1.16 1.91
Virola guatemalensis Warb Myristicaceae Árbol otros vertebrados 6.72 0 0.75
Vochysia guatemalensis Donn. Sm. Vochisiaceae Árbol viento 0.12 0 16.22
Xylopia frutescens Aublet Annonaceae Arbusto otros vertebrados 0 0 4.61
Zanthoxylum procerum Donn. Sm. Rutaceae Árbol otros vertebrados 0 0.01 1.1