Colonización y persistencia de Acacia pennatula en bosques ... · al. 1995, Pennington et al....
153
Colonization and Persistence of Acacia pennatula in Transformed Tropical Dry Forests The Role of Disturbances and Biotic Interactions Colonización y persistencia de Acacia pennatula en bosques tropicales secos transformados El rol de las perturbaciones y las interacciones bióticas
Transcript of Colonización y persistencia de Acacia pennatula en bosques ... · al. 1995, Pennington et al....
Colonization and Persistence of Acacia
pennatula in Transformed Tropical Dry Forests
The Role of Disturbances and Biotic Interactions
Colonización y persistencia de Acacia pennatula en
bosques tropicales secos transformados
El rol de las perturbaciones y las interacciones bióticas
Colonization and Persistence of Acacia pennatula in
Transformed Tropical Dry Forests
The Role of Disturbances and Biotic Interactions
Colonización y persistencia de Acacia pennatula en
bosques tropicales secos transformados
El rol de las perturbaciones y las interacciones bióticas
----------
Memoria presentada por:
Guillermo Peguero Gutiérrez
Para optar al grado de doctor.
Con la aprobación del director:
Dr. Josep Maria Espelta Morral
Bellaterra, junio del 2012
Peguero, G. (2012)
Tesis doctoral (Universitat Autònoma de Barcelona), Bellaterra, Catalunya (España)
Palabras clave: alelopatía, bosque secundario, bosque tropical seco, depredación de semillas,
dispersión, establecimiento de plántulas, frugivoría, fuego, germinación, perturbaciones,
rebrote, regeneración/restauración forestal, Nicaragua, Mesoamérica.
Keywords: allelopathy, secondary forest, tropical dry forest, seed predation, dispersal, seedling
establishment, frugivory, fire, germination, disturbances, resprouting, forest regeneration and
restoration, Nicaragua, Mesoamerica.
Todo el material gráfico es del autor.
Esta tesis se ha llevado a cabo en el ‘Centre de Recerca Ecològica i Aplicacions Forestals’
(CREAF), en el programa de doctorado de Ecología Terrestre de la Universidad Autónoma de
Barcelona y en colaboración con la Facultad Regional Multidisciplinaria de Estelí perteneciente
a la Universidad Nacional Autónoma de Nicaragua – Managua (FAREM-Estelí / UNAN-
Managua).
El autor ha recibido financiamiento procedente de una beca FI para estudios doctorales
concedida por la ‘Agència de Gestió d’Ajuts Universitaris i de Recerca’ (AGAUR / Generalitat de
Catalunya) y a través del proyecto D/026276/09 concedido por la Agencia Española de
Cooperación para el Desarrollo (AECID / Ministerio de Asuntos Exteriores y de Cooperación).
Carne de yugo, ha nacido
más humillado que bello,
con el cuello perseguido
por el yugo para el cuello.
[…]
¿Quién salvará este chiquillo
menor que un grano de avena?
¿De donde saldrá el martillo
verdugo de esta cadena?
[…]
Miguel Hernández, 1936-1937
Cuando te vayás octubre
voy a quedar lleno de invierno
como quien tiene
una gran reserva de lágrimas
para seguir llorando
Cuando llovés
lloro
y ya después lo veo todo limpio
porque es en tu llovida
que el paisaje se despeja.
Fernando Antonio Silva, Octubre 1979
Índice
Resumen
Introducción: Bosques Secos Mesoamericanos - Canción urgente para Nicaragua
Capítulo 1. La aptitud frugívora del ganado y la quema de pastos - Los primeros
ingredientes para una receta de éxito
Capítulo 2. Rebrota o muere – La inevitable presencia de perturbaciones repetidas
Capítulo 3. “Al cerro vengo subiendo…” – Depredación de semillas a lo largo de un
gradiente altitudinal
Capítulo 4. Demasiados depredadores para una misma semilla – ¿Una coexistencia
mediada por los frugívoros?
Capítulo 5. Una oportunidad o una barrera – Inhibición o facilitación del establecimiento
de plántulas
Resumen de las conclusiones principales
Retorno a Nicaragua - Implicaciones para la gestión
Publicaciones
Apéndice fotográfico
Agradecimientos
Resumen
El bosque tropical seco es uno de los biomas más ricos en biodiversidad y a la vez el sistema forestal más amenazado del planeta. Tras la masiva transformación de estos bosques en sistemas silvo-pastoriles para uso ganadero, muy pocas son las especies forestales que consiguen colonizar y persistir en estos nuevos ambientes. Mejorar el conocimiento del efecto de los principales impactos resultantes de esta transformación puede ayudar a mejorar la gestión actual del sistema y a proponer alternativas de manejo, ecológicamente razonables, encaminadas a la recuperación forestal. Esta tesis tiene por objetivo investigar qué papel juegan el cambio en el régimen de perturbaciones y en el conjunto de interacciones bióticas sobre el éxito colonizador de Acacia pennatula, una especie común en sistemas silvo-pastoriles de toda Mesoamérica. En el primer capítulo se investiga su capacidad de persistencia por rebrote tras perturbaciones de diversa intensidad (corte y fuego) aplicadas antes y después de la época seca y de manera repetida. Los resultados muestran que los individuos quemados sobreviven y rebrotan menos que los cortados y que al final de la estación seca es más difícil la recuperación, probablemente por la falta de recursos (N y especialmente P) almacenados en la raíz principal. En el segundo capítulo se estudia el papel que puede jugar el ganado como agente dispersor de semillas y la posible interacción entre la endozoocória y el fuego como factores desencadenantes de la germinación. El ganado es un eficaz agente dispersor de las semillas de diversas especies forestales, no obstante el paso por el tracto digestivo no estimuló la germinación de las especies testadas a diferencia del fuego el cual de manera general liberó las semillas de su latencia. En el tercer capítulo se investiga la variación en los mecanismos de defensa de semillas ante la depredación pre-dispersiva por parte de insectos (Bruchidae) a lo largo del rango de distribución altitudinal de A. pennatula. El saciado del predador mediante producciones masivas de frutos y el aborto de semillas que aumenta la mortalidad de las larvas, son mecanismos de defensa que actúan simultáneamente aunque su contribución relativa varía a lo largo del gradiente. En el cuarto capítulo se explora el rol que los frugívoros pueden tener controlando las poblaciones de insectos depredadores de semillas. La presencia de frugívoros reduce la proporción de semillas depredadas e incluso podría promover la coexistencia de varias especies de depredadores sobre la misma planta huésped. En el quinto se estudia el potencial de interferencia alelopática de A. pennatula sobre otras especies competidoras. Esta especie muestra indicios de interferir el desarrollo de las raíces de las plántulas que se establecen bajo su copa poniendo así en duda su capacidad de nucleación de la sucesión tras un eventual abandono de los sistemas silvo-pastoriles en los cuales es dominante. En conjunto A. pennatula es capaz de colonizar y persistir tras la transformación del bosque tropical seco gracias a: i) es eficazmente dispersada por el ganado y germina rápidamente tras el fuego en los pastos, ii) persiste tras perturbaciones repetidas (corte y fuego) mediante sucesivos rebrotes, iii) tiene mecanismos de defensa eficaces ante la depredación pre-dispersiva de sus semillas y es favorecida por la aptitud frugívora del ganado, y iv) es capaz de invadir los pastos e interferir alelopáticamente el establecimiento de plántulas bajo su copa. En la última sección de la presente tesis se proponen diversas alternativas de manejo para mejorar la gestión actual de los sistemas silvo-pastoriles en los cuales esta especie es dominante, y a fin de promover la recuperación forestal y el valor de conservación de la biodiversidad de los mismos.
Summary
Tropical Dry Forest (TDF) is one of the most biodiversity-rich biome and the most threatened forest ecosystem of the world. After the pervasive transformation of these forests into wooded rangelands, there are very few species able to colonize and to persist in this new environment. Improving the knowledge of the major impacts resulting from this land-use change may aid the current management practices and may provide ecologically sound alternatives aimed to the forest recovery. The general objective of this thesis is then to investigate the role played by the new disturbance regime and biotic interactions in colonization and persistence of Acacia pennatula, a tree species common in wooded rangelands throughout Mesoamerica. In the first chapter it is investigated its ability to resprout after disturbances (clipping and fire) applied before and after the dry season and repeatedly. The results show that those individuals burned had lower survival and resprouting vigor than those individuals only clipped. Additionally, recovering from a disturbance applied after the dry season was more difficult, and this was likely due to the lack of resources (N and especially P) stored in the main root. In the second chapter it is studied the role that cattle may play as a seed dispersal agent and the potential interaction between endozoochory and fire as triggers of germination. Cattle is currently an effective dispersal agent of several forest species, however, gut passage did not stimulate germination unlike fire which generally broke seeds’ physical dormancy. In the third chapter it is investigated the variation in seed defense mechanisms against pre-dispersal seed predators by insects (Bruchidae) along the altitudinal range of A. pennatula. Predator satiation by means of massive fruit crops and seed abortion which increases larval mortality, are both defense mechanisms that act simultaneously although its relative contribution vary along the altitudinal gradient. In the fourth chapter it is examined the role that frugivores may have in controlling seed predator populations. Frugivores reduced the proportion of seeds preyed upon by seed beetles and the results suggest that frugivores may promote coexistence of different predator species on the same plant host. In the fifth chapter it is studied the allelopathic interference of A. pennatula over other competitor species. The results show that this species may impair seedling establishment under its canopy by reducing root development. This warns about the ability of this species as a succession nuclei after an eventual abandonment of the wooded rangelands in which dominate. Overall, A. pennatula is able to colonize and to persist after TDF transformation thanks to: i) is effectively dispersed by cattle and germinate after pasture fires, ii) persists after repeated disturbances by successive resprouting, iii) has defense mechanisms against pre-dispersal seed predation and moreover is favored by cattle frugivory, and iv) is able to encroach pastures impairing seedling establishment under its canopy by means of an allelopathic interference. In the last section management proposals are provided in order to ameliorate current practices and to promote forest recovery in those wooded rangelands in which this species dominate.
IntroducciónGeneral:
Bosques Secos Mesoamericanos –
Canción urgente para Nicaragua
¿Por qué una tesis sobre Bosque Tropical Seco?
De acuerdo con la clasificación climática ya clásica de Holdridge (1967), los
bosques tropicales secos son aquellos que tienen lugar en áreas libres de heladas, con
temperaturas anuales medias mayores de 17ºC, precipitaciones de entre 250 hasta 2000
mm y con tasas anuales de evapo-transpiración potencial sobre precipitación que
exceden, a veces largamente, la unidad. Esta última característica, quizá la más
definitoria, es en parte resultado de la elevada estacionalidad de las precipitaciones que
resulta en un estricto déficit hídrico durante la estación seca que puede tener una
duración de 2 hasta 6 meses según aumenta la latitud.
No obstante, dentro de estas amplias categorías climáticas caben un gran número
de formaciones forestales cuyas características estructurales van desde ‘prados’ más o
menos densamente arbolados hasta bosques cerrados con dos o incluso tres estratos en
el dosel (Murphy & Lugo 1986, Pennington et al. 2009), de manera que la
diferenciación entre ‘bosque tropical seco’ y ‘sabana’ no ha sido siempre del todo clara
(Ratnam et al. 2011). Este hecho se refleja en las múltiples maneras por las que ha sido
y es denominado este bioma, a saber, bosque tropical estacionalmente seco (Bullock et
al. 1995, Pennington et al. 2009, Dirzo et al. 2011), bosques secos tropicales o
subtropicales de hoja ancha y de monzón (Olson & Dinerstein 1998), o mediante
nombres propios como “caatinga” en Brasil –formación colindante con el polimórfico
“cerrado” de discutida clasificación-, “bosque seco tumbesino” en Ecuador y Perú o
“bosque seco chiquitano” en Bolivia. Esta relativa indefinición no solo ha dificultado
las estimas de su distribución y grado de conservación actuales sino que también ha
complicado el estudio de su distribución potencial (Miles et al. 2006) y más aún, la
definición de los atributos y características funcionales que de manera general definen
las especies arbóreas que habitan estos ecosistemas forestales (Murphy & Lugo 1986,
Pennington et al. 2009).
Si sabemos sin embargo, que la distribución extremadamente disyunta de los
bosques tropicales secos ha producido una elevada β-diversidad entre áreas así como
notables tasas de endemismo que a su vez han conferido características casi únicas a
cada uno de sus núcleos biogeográficos (Prado & Gibbs 1993, Trejo & Dirzo 2002,
Pennington et al. 2009, Linares-Palomino et al. 2011). Desafortunadamente sabemos
también que la conservación de esta biodiversidad tan característica, pasa hoy en día por
la revalorización y la gestión de los paisajes altamente fragmentados y modificados en
los que se encuentran prácticamente todos los bosques tropicales secos del planeta
(Janzen 1988, Miles et al. 2006, DeClerck et al. 2010). Así las cosas, parece que el
futuro del bosque tropical seco está íntimamente unido a los esfuerzos de restauración
ecológica que además no pueden más que partir de aquellos elementos forestales,
árboles dispersos, bosques secundarios y rodales remanentes, que aún persisten en estos
paisajes altamente humanizados (Manning et al. 2006, Chazdon et al. 2009, DeClerck et
al. 2010, Griscom & Ashton 2011).
En conclusión podemos apreciar que entre los ecosistemas con mayor
biodiversidad, el bosque tropical seco destaca especialmente por ser el sistema forestal
más amenazado y transformado del planeta, y tal vez también, el menos estudiado
(Janzen 1988, Sanchez-Azofeifa et al. 2005, Miles et al. 2006). Con todo, además de su
elevado valor ecológico, es también proveedor de bienes y servicios ambientales claves
para el sustento de millones de personas (e.g. bienes directos como agua dulce, madera
para construcción y como fuente energética, forraje, medicinas naturales, o servicios de
regulación como el mantenimiento de la fertilidad del suelo o el control de las
inundaciones etc., Maass et al. 2005). Por otro lado, también destaca el elevado
potencial de secuestro de carbono que podría resultar de la reducción de las emisiones
procedentes de la deforestación y la degradación forestal de los bosques tropicales secos
(Angelsen 2010). Un almacenamiento de carbono que sería incluso mayor si se llegara
revertir esta tendencia en pro de una recuperación forestal generalizada (Silver et al.
2000, Angelsen 2010). Cabe señalar además, que bajo las incertidumbres derivadas del
actual cambio climático (IPCC 2007) esta función de almacenamiento cobra una
especial relevancia y sentido de oportunidad a escala mundial (Angelsen 2010).
¿Por qué Mesoamérica? El caso de Nicaragua.
La región Mesoamericana, que comprende desde la península de Yucatán hasta el istmo
de Panamá, es una unidad biogeográfica propia con un valor ecológico único (Flora
Mesoamericana 1994, Pennnington et al. 2009). Gracias a su singular condición de
corredor biológico natural, su biota se ha visto enriquecida por el intercambio entre los
dos grandes sub-continentes americanos y muy especialmente por haber actuado como
refugio durante la última glaciación (Gentry, 1982, Cody et al. 2010).
Por otra parte, la presencia humana en Mesoamérica ha sido constante desde su
llegada a finales del Pleistoceno, hace aproximadamente 11000 años, y por tanto
también ha sido continua su influencia sobre los ecosistemas (Denevan 1992, Cooke
2005, Griscom & Ashton 2011). El sistema de agricultura itinerante tradicional,
conocido por el descriptivo sobrenombre de “roza tumba y quema”, se basaba en el
aclareo del bosque y el cultivo siguiendo un patrón rotacional muy dinámico. No
obstante, con el advenimiento de las sucesivas civilizaciones precolombinas, la
modificación del paisaje llegó a ser tan profunda que lejos de ser un bosque prístino, lo
que encontraron los primeros conquistadores españoles fueron vastas extensiones de
cultivos y plantaciones de frutales que por otro lado eran las necesarias para alimentar
una población estimada de varios millones de habitantes (Denevan, 1992). Así en 1544,
Fray Bartolomé de las Casas sostenía que en la “provincia de Nicaragua […] era cosa
verdaderamente de admiración ver cuán poblada de pueblos, que cuasi duraban tres y
cuatro leguas en luengo, llenos de admirables frutales que causaba ser inmensa en la
gente […] porque era la tierra llana y rasa, que no podían esconderse en los montes, y
deleitosa, que con mucha angustia y dificultad osaban dejarla…” (de las Casas 1544).
Incluso siendo la anterior una valoración un tanto exagerada, parece indiscutible
que roturar el bosque mediante la tala y la quema es una práctica que se remonta miles
de años atrás en Mesoamérica (Dull 2004). Sin embargo, los colonizadores españoles
aportaron ciertas innovaciones como la introducción del ganado doméstico, cuya
función en términos ecológicos había estado ausente del sistema desde la extinción
masiva de la megafauna herbívora pleistocénica (Janzen & Martin 1982). Este último
enfoque productivo, eminentemente silvo-pastoril y de carácter extensivo, ha sido el que
ha predominado hasta la actualidad y particularmente en Nicaragua, donde ciertas
políticas de desarrollo llevadas a cabo desde mediados del siglo XX bajo el auspicio de
determinadas instituciones financieras internacionales, impulsaron enormemente la
deforestación y la expansión de la llamada “frontera agrícola” hasta los preocupantes
límites actuales (Kaimowitz 1996, Larson 2001, Griscom & Ashton 2011).
Ante este escenario parece necesario conjugar los actuales usos productivos con
la conservación de la biodiversidad y los bienes y servicios ambientales que proporciona
el bosque tropical seco. Así, es oportuna aquella investigación que tenga por fin último
profundizar en el conocimiento básico de este ecosistema así como aquella que analice
los efectos de los principales impactos derivados de su transformación en sistemas
silvo-pastoriles. La información obtenida puede ser por tanto, de utilidad para mejorar
su actual gestión e incluso para proponer alternativas de manejo, ecológicamente
razonables, ante un eventual y urgente marco favorable a la restauración forestal.
Cambios en el régimen de perturbaciones y en las interacciones bióticas
tras la transformación del bosque - Acacia pennatula como caso de
estudio.
La transformación del bosque en un sistema silvo-pastoril, es decir la conversión
del bosque cerrado en un pasto arbolado, conlleva un profundo cambio en el régimen de
perturbaciones que a menudo impide o dificulta la recuperación del sistema anterior a la
transformación. El ejemplo más evidente es el aumento de la frecuencia e intensidad de
las perturbaciones de origen antropogénico, normalmente aplicadas éstas como
herramientas de control del establecimiento de especies leñosas en el pasto. Estas
medidas generalmente pasan por la quema de los pastos durante la época seca, a veces
incluso precedida y/o seguida por el corte a mata rasa o chapia manual de aquellos
individuos ya establecidos y que por tanto solo pueden persistir a merced de su
capacidad de rebrote reiterado.
A diferencia de otros ecosistemas en los cuales la respuesta “rebrotadora” post-
perturbación ha sido extensamente investigada (e.g. áreas mediterráneas, sabana
africana etc., Bond & Keeley 2005), en el ámbito del bosque tropical seco son todavía
pocos los estudios sobre este extendido mecanismo de persistencia (no obstante ver,
Swaine 1992, Gould et al. 2001, McLaren & McDonald 2003, Otterstrom et al. 2006).
Por ejemplo, la movilización de reservas almacenadas (e.g. almidón, nitrógeno, fósforo)
parece ser un factor clave para rebrotar tras una perturbación (Chapin et al. 1990), sin
embargo, no hay un solo estudio que aborde esta cuestión en el ámbito del trópico seco
mesoamericano ni que analice la posible interacción entre la marcada estacionalidad
(i.e. sequía prolongada) y la disponibilidad y movilización de reservas para rebrotar tras
una perturbación. Qué duda cabe que obtener información detallada sobre la variación
estacional en la supervivencia y en el vigor del rebrote tras una perturbación, bien sea
fuego o chapia como medidas de control, puede ser de gran utilidad a fin de proponer
alternativas de manejo que mejoren la gestión de las especies leñosas en los pastos.
Por otro lado, la transformación del bosque en un sistema silvo-pastoril también
provoca profundos cambios en el conjunto de interacciones bióticas. Por ejemplo, en
condiciones de bosque cerrado, una plántula estableciéndose típicamente debe competir
con otras plántulas y con los individuos ya establecidos por unos recursos limitados
(e.g. luz y nutrientes). Sin embargo, estas relaciones altamente competitivas entre
plantas pueden tornarse en relaciones de facilitación neta bajo condiciones de elevado
estrés ambiental, como por ejemplo elevados déficits hídricos (Bertness & Callaway
1994, Maestre et al. 2009). De ser así, las especies forestales pioneras, capaces de
establecer individuos aislados en los potreros, tendrían una importancia capital como
“nucleadoras” de la sucesión al facilitar el establecimiento de plántulas de otras especies
tras un eventual abandono del uso ganadero (Slocum 2001). No obstante, también se ha
descrito que algunas de estas especies pioneras, tras el abandono de los pastos
rápidamente invaden e incluso impiden el establecimiento de otras especies bajo sus
copas, bloqueando así la sucesión (“encorachment”) durante décadas (Burgos & Maass
2004, Álvarez-Yépiz et al. 2010) de manera que no todas las especies pioneras serían
igual de “buenas nucleadoras” a medio o largo plazo (Slocum 2001).
Otro de los factores limitantes para la regeneración del bosque como resultado
del cambio en las interacciones bióticas que tiene lugar tras su transformación, es la
falta de dispersión de semillas dentro del pasto (Holl et al. 2000). Muchas de las
especies de árboles del bosque tropical seco presentan síndromes de dispersión por
zoocória de modo que son animales frugívoros (e.g. aves y murciélagos) los que
habitualmente dispersan sus semillas según patrones característicamente agregados
alrededor de “perchas” de alimentación y descanso (Holl et al. 2000). No obstante, la
falta de árboles aislados dentro del pasto, supone una ausencia casi total de estos
“núcleos” de dispersión de semillas reduciéndose así la capacidad de regeneración del
bosque. A pesar de esto, la dispersión de un número considerable de especies forestales
puede ser efectuada por el propio ganado doméstico a raíz de haber conservado éstas
especies diversos atributos “anacrónicos” en frutos y semillas, como la indehiscencia
del fruto o la dormición física de las semillas, los cuales probablemente fueron
seleccionados en el pasado para promover la dispersión de las semillas por la ya extinta
mega-fauna pleistocénica (Janzen & Martin 1982). No obstante, el ganado podría tener
ciertas preferencias de consumo de manera que fueran agentes dispersores
cuantitativamente más efectivos (i.e. mayor número de visitas y mayor número de frutos
consumidos por visita; sensu Schupp 1993) para unas determinadas especies que otras,
lo cual tendría consecuencias en los patrones de regeneración a nivel de paisaje (Eycott
et al. 2007). Por otro lado, se ha sugerido que el paso por el tracto intestinal del agente
dispersor (i.e. endozoocória) podría estimular la germinación de las semillas al romper
su latencia por escarificación de la cubierta (Traveset 1998) de manera similar al golpe
de calor producido por el fuego, cuyo rol estimulante de la germinación ya ha sido
ampliamente documentado en diversas especies y ecosistemas (Keeley & Fotheringam
2000). Sin embargo hasta la fecha no hay estudios que exploren una posible interacción
entre ambos factores: si la germinación es resultado directo del nivel de escarificación
de la cubierta de las semillas (Traveset et al. 2008), entonces el fuego podría tener un
efecto aditivo sobre el desgaste producido en la cubierta de la semilla tras el paso por el
tracto intestinal del agente dispersor de manera que ambos factores, endozoocória y
fuego, se reforzarían mutuamente y gestionados adecuadamente podrían llegar a ser
netos promotores de la regeneración forestal.
Por último, otra interacción biótica que puede tener un gran impacto en la
dinámica poblacional de las plantas y por tanto limitar su reclutamiento de plántulas, es
la depredación de semillas (Louda, 1982, Crawley, 2000, Kolbe et al. 2007, Vaz-
Ferreira et al. 2011). En consecuencia, las plantas han desarrollado diversos
mecanismos de defensa o bien oponiendo “resistencia” a la depredación mediante
barreras físicas o químicas (Hulme & Benkman 2002) o bien “tolerándola” mediante el
saciado de los depredadores (Janzen 1971, Kelly & Sork 2002). Además, el aborto de
semillas, tanto si es resultado directo de la infestación por un depredador como si no,
también puede producir incrementos en la mortalidad de los depredadores actuando por
tanto como mecanismo de defensa del resto de semillas maduras (Stephenson 1981,
Holland et al. 2004, Östergård et al. 2007). Teniendo todo esto en cuenta, en el actual
escenario del bosque seco mesoamericano se pueden formular una serie de preguntas
aún muy poco exploradas y de interés tanto básico como aplicado. Por ejemplo, ¿la
depredación pre-dispersiva de semillas puede condicionar la capacidad de colonización
del pasto de una especie dada? Y de ser así, ¿varia esta presión de depredación a lo
largo del rango de distribución altitudinal de esta misma especie? Una respuesta
afirmativa a ambas preguntas podría tener implicaciones a la luz de una posible
migración en altura resultado del cambio climático (Colwell et al. 2008, Chen et al.
2011). Expansiones que ya han sido descritas para diversas especies de árboles
tropicales (Feeley et al. 2011) y en las que las interacciones bióticas como la
depredación de semillas, probablemente jueguen un papel destacado (Davis et al. 1998,
Hillyer & Silman 2011).
En esta misma línea de interacciones antagónicas entre especies forestales y sus
depredadores de semillas, cabe preguntarse además sobre el posible rol que puede jugar
el ganado cuando es el agente dispersor de estas mismas especies. Es bien sabido que a
menudo los agentes dispersores también antagonizan con los depredadores pre-
dispersivos, especialmente si éstos últimos son insectos (Sallabanks & Courtney 1992).
Por un lado por el simple hecho de que dispersan su recurso clave, pero también porque
al alimentarse de los frutos, los agentes dispersores pueden depredarlos a ellos mismos
(accidentalmente o no) en caso de que aún se encuentren dentro del fruto o semilla
(Herrera 1989, Sallabanks & Courtney 1992). Por extensión, es fácil imaginar que
tiempos de permanencia dentro del fruto o semilla más largos quizá permiten un mejor
aprovechamiento del recurso pero a su vez conllevan mayores riesgos de ser
accidentalmente depredados por parte del agente dispersor. De ser así, la coexistencia de
diversas especies de depredadores pre-dispersivos explotando la misma planta huésped
podría venir en parte mediada por distintas vulnerabilidades ante mayores o menores
tasas de dispersión de frutos en caso que diverjan en sus tiempos de permanencia dentro
de los frutos o semillas.
En este marco de cambios dramáticos tanto en el régimen de perturbaciones
como en el conjunto de interacciones bióticas, una gran parte de las especies forestales
características del bosque seco mesoamericano no consiguen ni persistir ni propagarse
mientras que hay otras cuya abundancia y distribución se ha visto altamente favorecida
(Esquivel et al. 2008, Tarrasón et al. 2010). Este es el caso de Acacia pennatula Benth.,
una leguminosa mimosoide común como árbol disperso en potreros y en bosques
secundarios desde México hasta Ecuador (Ebinger et al. 2000). Esta especie pionera y
colonizadora de pastos está particularmente extendida por todo el centro Norte de
Nicaragua, principalmente en la frontera entre el bosque seco de tierras bajas y el
bosque nublado de montaña (Stevens et al. 2001), donde además de proporcionar
diversos bienes directos para pobladores y productores locales (por ejemplo, madera
para postes y construcción, leña, forraje para el ganado, etc., Purata et al. 1999, Nieto
2000) también actúa de refugio para la biodiversidad (Greenberg et al. 1997).
Así, por su ubicuidad en nuestra zona de estudio en el centro norte de Nicaragua
(ver descripciones más detalladas en cada capítulo) como por su importancia social y
ecológica, Acacia pennatula es un modelo adecuado a partir de la cual investigar qué
papel juega el régimen de perturbaciones y las interacciones bióticas en la capacidad de
colonización y persistencia de esta especie tras la transformación del bosque seco en un
sistema silvo-pastoril. ¿Se trata solo de una gran capacidad de persistencia tras
perturbaciones intensas y frecuentes o también son el conjunto de interacciones bióticas
las que favorecen a esta especie en detrimento de otras tantas? Una respuesta a estas
preguntas, aún siendo ésta incompleta y preliminar, podría dar información valiosa
sobre los principales impactos y factores limitantes resultantes de la transformación del
bosque. Además ayudaría a vislumbrar si en último término esta capacidad de
colonización del espacio abierto que presenta tanto A. pennatula como otras especies de
características ecológicas similares, podría ser una oportunidad para la recuperación del
bosque seco mesoamericano mediante una gestión orientada a ello.
Objetivos y estructuración de la tesis.
El objetivo general de esta tesis es por tanto investigar qué papel juegan las
perturbaciones y las interacciones bióticas (e.g. dispersión y depredación de semillas,
alelopatía) en el éxito colonizador de Acacia pennatula tras la transformación del
bosque seco mesoamericano en sistemas silvo-pastoriles. A tal fin, esta tesis está
organizada en 5 capítulos en los que se abordan distintos aspectos del cambio en el
régimen de perturbaciones y en el conjunto de interacciones bióticas, que tienen lugar
tras la transformación del bosque y que pueden ayudar a comprender porqué
determinadas especies forestales persisten e incluso prosperan en las actuales (aunque
quizá no tan nuevas) condiciones.
Así, en el primer capítulo se estudia experimentalmente la capacidad de
persistencia de A. pennatula en el pasto tras perturbaciones de distinta intensidad (i.e.
corta y fuego), estacionalidad y frecuencia (antes o después de la estación seca y en
ambos casos), con especial atención al papel que puede jugar la marcada estacionalidad
(i.e. sequía prolongada) en la disponibilidad de recursos almacenados en la raíz
principal (almidón, nitrógeno y fósforo) para la supervivencia y vigor del rebrote post-
perturbación.
En el segundo se aborda la importancia que tiene el ganado doméstico como
agente dispersor de semillas. En concreto se analiza de manera experimental si puede
ser un agente dispersor cuantitativamente más efectivo para algunas especies del bosque
tropical seco, si las semillas de determinadas especies resisten mejor el paso por su
tracto digestivo y/o germinan mejor ante el fuego y si puede existir alguna interacción
entre estos dos factores (endozoocória y fuego) en la germinación. Para responder a
estos objetivos comparamos Acacia pennatula con otras dos especies nativas y tambien
presentes en la zona de estudio, Guazuma ulmifolia (Malvaceae) y Enterolobium
cyclocarpum (Fabaceae), las cuales tienen tamaños de fruto, de semilla y de numero de
semillas/fruto muy contrastantes.
En el tercer capítulo se investiga la variación en la depredación pre-dispersiva de
semillas de A. pennatula por parte de insectos especialistas (Bruchidae, Mimosestes
sp.) a lo largo de su rango de distribución altitudinal. Se analiza concretamente el papel
que juega el saciado de los depredadores y el aborto de semillas como medidas
defensivas así como su variación relativa a lo largo del gradiente. Se explora por último
si la depredación puede condicionar el reclutamiento de plántulas en el pasto y por
tanto, en último término, limitar o favorecer una posible expansión poblacional en altura
de esta especie en nuevos escenarios ecológicos (e.g. cambio climático).
En el cuarto se explora de manera preliminar el papel que pueden jugar los
frugívoros dispersores de semillas (en este caso el ganado) en la reducción de la presión
por depredación pre-dispersiva de semillas y en la posible mediación de la coexistencia
de distintas especies de depredadores explotando el mismo recurso o planta huésped.
Para explorar estas hipótesis se investigaron dos especies de árboles (A. pennatula y G.
ulmifolia) y sus respectivos gremios de insectos depredadores pre-dispersivos de
semillas (Bruchidae: Mimosestes anomalus/Mimosestes humeralis, y Amblycerus
cistelinus/Acanthoscelides guazumae respectivamente) en dos zonas contrastadas por la
presencia y la ausencia de larga duración de ganado.
En el quinto y último capítulo se investiga de manera experimental, en
laboratorio y en campo, el potencial de interferencia alelopática de A. pennatula en la
germinación y establecimiento de plántulas bajo su copa, explorando por extensión si
puede facilitar o más bien inhibir el establecimiento de plántulas bajos su copa y por
tanto nuclear o bien bloquear la sucesión tras un eventual cambio de uso de los pastos.
Finalmente en la última sección se proporciona un resumen de los principales
resultados obtenidos, junto con una breve síntesis subrayando las principales
implicaciones para la gestión de esta especie y del sistema en conjunto.
Nota Taxonómica:
Seigler & Ebinger en un artículo publicado el año 2006 apoyaron el origen polifilético
del género Acacia y propusieron nuevas combinaciones para los representantes
neotropicales del género. Así, Acacia pennatula junto con sus subsp. pennatula y
subsp. parvicephala fueron propuestas como Vachellia pennatula y V. pennatula var.
parvicephala respectivamente. Actualmente, A. pennatula y V. pennatula son
consideradas sinónimos aceptados e intercambiables (Tropicos.org/MOBOT). En la
presente tesis se mantiene la notación original siguiendo por tanto la nomenclatura
propuesta por Rico Arce (2007).
Referencias
Angelsen, A., ed. (2010) La implementación de REDD+. Center for International Forestry Research,
Bogor, Indonesia.
Bullock, S.H., Mooney, H.A., & Medina, E. (1995) Seasonally dry tropical forests Cambridge University
Press, Cambridge, UK.
Chazdon, R.L., Harvey, C.A., Komar, O., Griffith, D.M., Ferguson, B.G., Martínez-Ramos, M., Morales,
H., Nigh, R., Soto-Pinto, L., & Van Breugel, M. (2009) Beyond reserves: A research agenda for
conserving biodiversity in human-modified tropical landscapes. Biotropica, 41, 142-153.
Chen, I., Hill, J.K., Ohlemüller, R., Roy, D.B., & Thomas, C.D. (2011) Rapid range shifts of species
associated with high levels of climate warming. Science, 333, 1024-1026.
Cody, S., Richardson, J.E., Rull, V., Ellis, C., & Pennington, R.T. (2010) The great American biotic
interchange revisited. Ecography, 33, 326-332.
Colwell, R.K., Brehm, G., Cardelús, C.L., Gilman, A.C., & Longino, J.T. (2008) Global warming,
elevational range shifts, and lowland biotic attrition in the wet tropics. Science, 322, 258-261.
Cooke, R. (2005) Prehistory of Native Americans on the Central American land bridge: colonization,
dispersal, and divergence. Journal of Archaeological Research, 13, 129-187.
Davis, A.J., Jenkinson, L.S., Lawton, J.H., Shorrocks, B., & Wood, S. (1998) Making mistakes when
predicting shifts in species range in response to global warming. Nature, 391, 783-786.
de Las Casas, B. (1544 ) Brevísima relación de la destruición de las Indias. Cátedra, Madrid, España.
DeClerck, F.A.J., Chazdon, R., Holl, K.D., Milder, J.C., Finegan, B., Martinez-Salinas, A., Imbach, P.,
Canet, L., & Ramos, Z. (2010) Biodiversity conservation in human-modified landscapes of
Mesoamerica: Past, present and future. Biological Conservation, 143, 2301-2313.
Denevan, W.M. (1992) The pristine myth: the landscape of the Americas in 1492. Annals of the
Association of American Geographers, 82, 369-385.
Dirzo, R., Young, H.S., Mooney, H.A., & Ceballos, G. (2011) Seasonally Dry Tropical Forests: Ecology
and Conservation Island Press, Washington, USA.
Dull, R.A. (2004) An 8000-year record of vegetation, climate, and human disturbance from the Sierra de
Apaneca, El Salvador. Quaternary Research, 61, 159-167.
Ebinger, J.E., Seigler, D.S., & Clarke, H.D. (2000) Taxonomic revision of South American species of the
genus Acacia subgenus Acacia (Fabaceae: Mimosoideae). Systematic Botany, 25, 588-617.
Esquivel, M.J., Harvey, C.A., Finegan, B., Casanoves, F., & Skarpe, C. (2008) Effects of pasture
management on the natural regeneration of neotropical trees. Journal of applied ecology, 45,
371-380.
Feeley, K.J., Silman, M.R., Bush, M.B., Farfan, W., Cabrera, K.G., Malhi, Y., Meir, P., Revilla, N.S.,
Quisiyupanqui, M.N.R., & Saatchi, S. (2011) Upslope migration of Andean trees. Journal of
Biogeography, 38, 783-791.
Gentry, A.H. (1982) Neotropical floristic diversity: phytogeographical connections between Central and
South America, Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals
of the Missouri Botanical Garden, 69, 557-593.
Greenberg, R., Bichier, P., & Sterling, J. (1997) Acacia, cattle and migratory birds in southeastern
Mexico. Biological Conservation, 80, 235-247.
Griscom, H.P. & Ashton, M.S. (2011) Restoration of dry tropical forests in Central America: a review of
pattern and process. Forest Ecology and Management, 261, 1564-1579.
Herrera, C.M. (1989) Vertebrate frugivores and their interaction with invertebrate fruit predators:
supporting evidence from a Costa Rican dry forest. Oikos, 185-188.
Hillyer, R. & Silman, M.R. (2011) Changes in species interactions across a 2.5 km elevation gradient:
effects on plant migration in response to climate change. Global Change Biology, 16, 3205-
3214.
Holdridge, L.R. (1967) Life zone ecology Tropical Science Center, San José, CR.
IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change IPCC, Geneva,
Switzerland.
Janzen, D.H. (1988). Tropical dry forests. In Biodiversity (ed E.O. Wilson), pp. 130-137. National
Academy Press, Washington, USA.
Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science,
215, 19-27.
Kaimowitz, D. (1996) Livestock and deforestation: Central America in the 1980s and 1990s: a policy
perspective. Center for International Forestry Research, Jakarta, Indonesia.
Larson, A. (2001) Recursos forestales y gobiernos municipales en Nicaragua: Hacia una gestión efectiva.
Universidad Centroamericana-Nitlapán Managua, Nicaragua.
Linares-Palomino, R., Oliveira-Filho, A.T., & Pennington, R.T. (2011). Neotropical seasonally dry
forests: Diversity, endemism, and biogeography of woody plants. In Seasonally Dry Tropical
Forests (eds R. Dirzo, H.S. Young, H.A. Mooney & G. Ceballos), pp. 3-21. Island Press,
Washington, USA.
Maass, J.M., Balvanera, P., Castillo, A., Daily, G.C., Mooney, H.A., Ehrlich, P., Quesada, M., Miranda,
A., Jaramillo, V.J., & García-Oliva, F. (2005) Ecosystem services of tropical dry forests: insights
from long-term ecological and social research on the Pacific Coast of Mexico. Ecology and
Society, 10, 17.
Manning, A.D., Fischer, J., & Lindenmayer, D.B. (2006) Scattered trees are keystone structures-
implications for conservation. Biological Conservation, 132, 311-321.
Miles, L., Newton, A.C., DeFries, R.S., Ravilious, C., May, I., Blyth, S., Kapos, V., & Gordon, J.E.
(2006) A global overview of the conservation status of tropical dry forests. Journal of
Biogeography, 33, 491-505.
Murphy, P.G. & Lugo, A.E. (1986) Ecology of tropical dry forest. Annual review of ecology and
systematics, 17, 67-88.
Nieto, H. (2000) Contribución de Acacia pennatula (Carbón) a la productividad agroforestal sostenible de
la reserva natural Miraflor-Moropotente, Estelí, Nicaragua, Centro Agronómico Tropical de
Investigación y Enseñanza, Turrialba, Costa Rica.
Olson, D.M. & Dinerstein, E. (1998) The Global 200: a representation approach to conserving the Earth's
most biologically valuable ecoregions. Conservation Biology, 12, 502-515.
Pennington, R.T., Lavin, M., & Oliveira-Filho, A. (2009) Woody plant diversity, evolution, and ecology
in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology,
Evolution, and Systematics, 40, 437-457.
Prado, D.E. & Gibbs, P.E. (1993) Patterns of species distributions in the dry seasonal forests of South
America. Annals of the Missouri Botanical Garden, 80, 902-927.
Purata, S.E., Greenberg, R., Barrientos, V., & López-Portillo, J. (1999) Economic potential of the
huizache, Acacia pennatula (Mimosoideae) in central Veracruz, Mexico. Economic botany, 53,
15-29.
Ratnam, J., Bond, W.J., Fensham, R.J., Hoffmann, W.A., Archibald, S., Lehmann, C.E.R., Anderson,
M.T., Higgins, S.I., & Sankaran, M. (2011) When is a 'forest' a savanna, and why does it matter?
Global Ecology and Biogeography, 20, 653-660.
Rico Arce, M.L. (2007) A checklist and synopsis of American species of Acacia (Leguminosae:
Mimosoideae) Comision Nacional para el Conocimiento y Uso de la Biodiversidad, Tlalpan,
Mexico.
Sallabanks, R. & Courtney, S.P. (1992) Frugivory, seed predation, and insect-vertebrate interactions.
Annual Review of Entomology, 37, 377-400.
Sánchez-Azofeifa, G.A., Quesada, M., Rodríguez, J.P., Nassar, J.M., Stoner, K.E., Castillo, A., Garvin,
T., Zent, E.L., Calvo-Alvarado, J.C., & Kalacska, M.E.R. (2005) Research Priorities for
Neotropical Dry Forests. Biotropica, 37, 477-485.
Seigler, D.S. & Ebinger, J.E. (2006) New combinations in the genus Vachellia (Fabaceae: Mimosoideae)
from the New World. Phytologia, 87, 139-178.
Silver, W.L., Ostertag, R., & Lugo, A.E. (2000) The potential for carbon sequestration through
reforestation of abandoned tropical agricultural and pasture lands. Restoration ecology, 8, 394-
407.
Stevens, W.D., Pool, A., Montiel, O.M., Ulloa, C.U., & Garden, M.B. (2001) Flora de Nicaragua
Missouri Botanical Garden Press St. Louis, USA.
Tarrasón, D., Urrutia, J.T., Ravera, F., Herrera, E., Andrés, P., & Espelta, J.M. (2010) Conservation status
of tropical dry forest remnants in Nicaragua: Do ecological indicators and social perception
tally? Biodiversity and Conservation, 19, 813-827.
Trejo, I. & Dirzo, R. (2002) Floristic diversity of Mexican seasonally dry tropical forests. Biodiversity
and Conservation, 11, 2063-2084.
Capítulo1
Rebrota o muere –
La inevitable presencia de perturbaciones
repetidas
Resumen
Diversas especies de plantas propias del bosque tropical seco, persisten tras las
perturbaciones (por ejemplo tras la chapia o el fuego) en parte gracias al rebrote. No
obstante se sabe muy poco sobre si esta capacidad se ve afectada por la severidad de las
perturbaciones y especialmente por el momento de la estación durante la cual se
producen, y aun más, sobre la importancia que juegan los recursos almacenados
(almidón, N y P). Investigamos la capacidad de rebrote tras la chapia y la quema
aplicados ambos tratamientos de forma experimental antes y después de la estación seca
en individuos de Acacia pennatula en sistemas silvopastoriles del Noroeste de
Nicaragua. Cada tratamiento se aplicó en 12 individuos y fue replicado en 6 parcelas.
Un año después del inicio del experimento, tanto la supervivencia como la recuperación
de biomasa fueron significativamente menores en los individuos quemados que en los
podados (78% % y 75.3 8.0 g versus 94% % y 79.1 6.8 g; Media Error
Estándar). Cualquiera que fuera el tipo de perturbación aplicada, los individuos
perturbados después de la estación seca mostraron la menor supervivencia, crecimiento
y concentración de N y P. Estos resultados sugieren que el rebrote en la especies del
trópico seco pueden estar limitado tras perturbaciones intensas (por ejemplo el fuego)
pero especialmente si éstas ocurren hacia el final de la estación seca. Esta restricción
fenológica podría ser debida a una reducción de la disponibilidad de N y P a medida que
la estación seca progresa.
Chapter1
Resprout or die ‐ The inevitable presence of repeated
disturbances
Abstract
Many plant species in tropical dry forests partly base their ability to persist after
disturbance on resprouting. Yet little is known if this ability can be affected by the
intensity and seasonality of disturbance and whether the amount of resources (starch, N,
P) stored in the taproot may constrain this response. We investigated resprouting after
experimental clipping or burning, applied before or after the dry season and repeatedly
in Acacia pennatula individuals in wooded rangelands of North-West Nicaragua. Each
treatment was applied to 12 trees and replicated in six plots. One year after the onset of
the experiment, survival and biomass recovery were significantly lower in burned than
in clipped individuals (78% % and 75.3 8.0 g vs. 94% % and 79.1 6.8 g;
mean SE). Whatever the disturbance applied, trees disturbed after the dry season
significantly showed the lowest survival, growth and concentration of N and P. These
results suggest that resprouting in dry tropical species may be constrained by intense
disturbances (e.g. burning) but especially if they occur towards the end of the dry
season. This phenological constraint could be due to the reduced availability of N and P
as this dry season progresses.
Introduction
Many plant species in tropical dry forests base their ability to persist partly on
resprouting after disturbance (Vieira & Scariot 2006). This ability is due both to the
presence of a protected bud bank (Klimešová & Klimeš 2007) and on the maintenance
of stored reserves to sustain regrowth (Chapin et al. 1990). Yet the relative importance
of stored resources in driving resprouting remains elusive. Thus, while certain studies
have proven carbohydrates to be mobilised during resprouting and to constrain regrowth
(Bowen & Pate 1993), others have suggested nitrogen and phosphorus to be the most
limiting resources (Canadell & López-Soria 1998, Miyanishi & Kellman 1986). What’s
more, a third group has observed no correlation between stored resources and
resprouting vigour (Cruz et al. 2003a). Resprouting may also be conditioned by the
interaction between the phenological dynamics of resource mobilisation within the plant
and the time when disturbance occurs (Castell et al. 1994, Cruz et al. 2002, Hodgkinson
1992). Thus, species-specific differences in resprouting may arise from differences in
bud bank size, ability to store and mobilise reserves, and phenological differences when
disturbances take place (Bonfil et al. 2004, Canadell & López-Soria 1998, Espelta et al.
1999).
Acacia sensu lato is a large circumtropical genus. Some of these species act as
pioneers, successfully persisting in highly disturbed areas thanks to their drought
resistance and resprouting ability. Numerous studies have reported the high resprouting
ability of Acacia spp. in fire-prone ecosystems such as African savannas, as well as in
Australian and North American grasslands (Meyer et al. 2005, Schutz et al. 2009,
Wright & Clarke 2007). Yet little is known about this response in the Neotropical
species from dry forests, although they may behave differently due to the lower
importance of fire as a natural ecological driver in this area compared to other
disturbance types (i.e. grazing exerted by megaherbivores in Janzen & Martin 1982, see
also Vieira & Scariot 2006). Moreover, despite the harsh dry season undergone by
plants in tropical dry areas, and the potential increase in drought intensity as a result of
the climate change (IPCC 2007), not a single study addresses the effects of the time of
disturbance on the resprouting ability in plants of tropical dry forest and the role played
by stored resources (e.g. starch, nutrients) in this response.
The main aim of this study was to experimentally investigate the resprouting
response of Acacia pennatula to different disturbance regimes. We assessed survival,
resprouting vigour and resource concentration (starch, N and P) in individuals, after two
types of disturbance of differing intensity (clipping, burning) applied before or after the
dry season and repeatedly. We hypothesise that: (1) if resprouting ability in A.
pennatula has been selected by fire, we should find few differences in resprouting
between clipped and burned individuals (for Mediterranean-type species, see Bonfil et
al. 2004); (2) if the dry season involves a reduction in the levels of stored reserves so as
to support the plant metabolism (Sardans & Peñuelas 2007), individuals disturbed at the
end of this season should show lower resprouting ability (Bonfil et al. 2004); and (3) if
resprouting ability critically depends on the amount of stored resources, resprouting
should be reduced in repeatedly disturbed individuals.
Materials and Methods
Study area and species
The study was conducted in the Miraflor-Moropotente Terrestrial Protected Landscape
in the Estelí Department, north-west Nicaragua (13º19’30”-13º60’30”N, 86º11’00”-
86º22’00”W). This protected area covers 290 km2 of wooded rangelands with isolated
tropical dry-forest remnants. The mean annual temperature ranges from 16ºC to 30ºC
with a mean rainfall of 804 mm y-1 (data from Condega weather station, 1983-2009).
Most rainfall episodes (90%) take place between May and November (wet season) and
the rest in a dry season from December to April. Soils are ultisols and vertisols
developed from an ancient (i.e. Pliocene) volcanic parent material (D. Tarrasón, unpubl.
data). According to Tarrasón et al. (2010), most of the protected area is occupied by
wooded rangelands with scattered A. pennatula trees. Acacia pennatula Benth. is a
spiny leguminous tree (up to 8 m), native to Central America, and common in secondary
tropical dry forests and disturbed areas from South-East Mexico to Ecuador (Ebinger et
al. 2000). The indehiscent protein-rich pods of this species are used by local people for
cattle-raising (Casassola 2000). Thanks to this type of management, livestock enhance
both the spread of A. pennatula seeds and their germination ability (G. Peguero, unpubl.
data).
Experimental design and sampling
In order to analyse the resprouting ability of A. pennatula under different disturbance
regimes, we designed a factorial experiment, combining two types of disturbance
applied at different times of the year. Disturbance treatments consisted of: (1) clipping
all above-ground biomass and (2) burning. Comparison of these two treatments was
done in light of the different disturbance intensities they represent: i.e. clipping does not
affect the bud bank located in the root collar whereas burning may (Espelta et al. 1999).
The burning treatment was performed by applying the flame of an acetylene hand torch
directly to the base of the stump until reaching a mean temperature of 300ºC for an
average of 2 min (Lloret & López-Soria 1993). Temperature was continuously
monitored with a thermometric probe (Anritherm Thermometer HL600 Type K).
According to the description of wildfire intensity in similar ecosystems (Gibson et al.
1990), this experimental treatment simulates the low-intensity wildfires that affect
savanna-like landscapes. To test disturbance-date effects on resprouting, both treatments
were applied: at the start of the dry season (December 2007), at the end of the dry
season (June 2008) or at both times (before and after the dry season). Each experimental
treatment was applied on 12 individuals randomly selected and replicated on six
different sites subjected to similar management practices (hereinafter plots). To check
the size of individuals at the start of the experiment, the initial number of stems was
counted and the fresh weight of all stems in those individuals clipped or burned was
estimated, once cut down, with a field scale. To estimate the initial biomass of
individuals assigned to the ‘after dry season’ treatment (i.e. not initially disturbed), we
measured the diameter and height of all stems and used allometric equations relating
basal diameter with dry biomass (80ºC, 48 h) obtained from a subsample of 30 resprouts
(dry biomass = 125.3 basal diameter – 82.1; n = 30; P < 0.0001, R2 = 0.72). At the onset
of the experiment, A. pennatula individuals had a height ranging from 0.4 to 1.2 m, an
average of eight stems per individual and an above-ground dry biomass of 858 49 g
(mean SE).
The experiment finished in October 2008 (12 months after disturbance was
applied in the ‘before the dry season’ treatments and 6 months following the ‘after the
dry season’ treatments), when we revisited all individuals and identified them as living
or dead (i.e. resprouted or non-resprouted). Even though a different period of time had
passed for individuals disturbed before or after the dry season, it is highly improbable
that non-resprouted individuals from the later treatment could further resprout after 6
months, according to the fast resprouting behaviour of this species (personal
observation) and other Acacia spp. (e.g. Acacia karoo, Schutz et al. 2009). In those
individuals that survived, we counted and cut down all resprouts to estimate the final
biomass produced. To control for the different time individuals disturbed before and
after the dry season had for growing before the experiment ended, we calculated a
mean growth rate per individual at a monthly basis, as: final biomass divided by 12
months in individuals disturbed before the dry season and by 6 months in those
disturbed after the dry season.
To assess the effects of the different types and dates of disturbance in the below-
ground reserves of starch, N and P, we excavated and collected the first 30 cm of the
taproot of 12 individuals per experimental treatment (two per plot) at the end of the
experiment. We also took an equivalent sample of taproots from a group of untouched
plants designated as controls (12 individuals, two per plot). The protected status of the
area precluded the possibility of excavating (destroying) a larger number of plants.
Taproots were transported to the lab where they were dried (60ºC, until a constant
weight was reached) and ground into fine powder. Starch was extracted with a 90%
DMSO solution at 120ºC for 1 h and concentration was determined colourimetrically at
620 nm after reaction with acidic iodine solution (0.06% KI and 0.003% I2 in 0.05N
HCl). Nitrogen was analysed by complete combustion according to the Dumas
principle, whereas phosphorus was analysed through conventional wet acid digestion
and inductively coupled plasma optical emission spectrometry (ICP-OES).
Data analysis
Differences in survival and in the number of resprouts produced according to the
experimental treatments were analysed by means of generalized linear mixed models
(GLIMMIX procedure; SAS 9.1, SAS Institute), using a binomial error and a logit link
function for survival and a Poisson error and a log link function for the number of
resprouts. Differences in final biomass and growth rate per individual were analysed by
means of general linear mixed models (Statistica 6.0 software, StatSoft Inc.), after
dependent variables were log-transformed to meet the assumption of normality. In all of
these analyses, disturbance (clipping, burning) and disturbance date (before or after the
dry season and repeatedly) were included as fixed factors whereas plot was included as
a random factor. To account for the potential effect of the size of individuals in their
response to the experimental treatments, initial biomass was also included in all
analyses as a covariate.
The effects of type and disturbance date on the concentration of starch, nitrogen
and phosphorus (log-transformed) in the taproot were analysed using two separate
general linear models, including initial biomass as a covariate. Two separate models for
type and disturbance date had to be conducted due to restrictions imposed by the
sampling design. Because taproot samples were obtained at the end of the experiment
we lacked control individuals for each disturbance date and thus the potential interaction
between type and disturbance date could not be tested. Because of the low number of
taproots excavated per plot, we did not include plot as a random factor in these analyses.
Results
Survival of A. pennatula individuals was significantly affected by the type of
disturbance and the date it was applied, but not by the interaction between these two
factors (Table 1). Survival was lower in burned than in clipped individuals
(respectively, 78% 4% and 94% 2%; mean SE), and whatever the type of
disturbance undergone, survival was higher in individuals disturbed before the dry
season, slightly lower in those repeatedly disturbed, and much lower in those disturbed
only at the end of the dry season (respectively 96% 2%, 89% 4% and 72% 7%).
In surviving individuals, resprouting vigour (number of resprouts, growth rate
and final biomass) was also affected by the experimental treatments applied (Table 1).
Interaction between the type and disturbance date revealed that individuals clipped and
burned before the dry season produced a similar number of resprouts, while resprout
production was much lower in those burned after the dry season (Figure 1). Moreover,
burned individuals exhibited a lower growth rate and attained a lower final biomass than
those clipped (Table 1; respectively, 13.3 1.2 g mo-1 vs 14.8 1.2 g mo-1 and 75.3
8.0 g vs 79.1 6.8 g). Not only the type of disturbance, but also the date it was applied,
affected the growth rate (Table 1). Curiously, the growth rate of twice-disturbed
individuals was similar to that of those disturbed once before the dry season and both
were significantly higher than individuals disturbed after the dry season (Figure 2). The
positive effect of the initial biomass on resprouting vigour (i.e. number of resprouts,
growth rate and final biomass) was greater on burned than on clipped individuals
(interaction disturbance type × initial biomass in Table 1), while in terms of disturbance
date, the positive effect of size was only observed in individuals disturbed before the
dry season (interaction disturbance date × initial biomass in Table 1).
At the end of the experiment, individuals that had been most severely disturbed
(burned) had lower starch and N concentrations in their taproots than clipped or control
ones (Figure 3, F2,32 = 7.0, P = 0.003 for starch and F2,32 = 12.7, P = 0.0001 for N). As
for the date when disturbance was applied, no differences were seen in the concentration
of starch; while concentration of N, and especially P, were significantly lower in
individuals disturbed after the dry season (Figure 4, F3,71 = 5.0, P = 0.004 for N and F3,71
= 5.3, P = 0.002 for P). Whatever the type and disturbance date, the significance of the
covariate effect in these analyses indicated that both starch and P concentration in the
taproot were negatively related to the initial biomass of individuals (F1,71 = 14.2, P =
0.0003 for starch and F1,71 = 8.2, P = 0.005 for P).
Discussion
The high survival rate of A. pennatula after experimental disturbances is similar to other
Acacia sp. (Meyer et al. 2005, Schutz et al. 2009, Wright & Clarke 2007) and may help
explain the persistence of this species in highly disturbed areas. However, burned
individuals showed higher mortality and lower resprouting vigour compared to the
clipped ones. Sensitivity to fire was also evident in the greater positive effect of the
initial size on the number of resprouts produced after disturbance for burned than for
clipped individuals (interaction disturbance type × initial biomass in Table 1). In light of
these results, and taking into account that certain authors have suggested that wildfires
have not been a natural ecological driver in tropical dry forests (Janzen 2002, Vieira &
Scariot 2006), the resprouting behaviour of A. pennatula cannot be assumed to be a fire
adaptation (sensu Bond & Keeley 2005). Alternatively, resprouting ability in these
Neotropical species may be a pre-adaptive trait of damage tolerance to the grazing
pressure exerted by extinct megaherbivores (Janzen & Martin 1982).
The lower survival and resprouting vigour in individuals disturbed at the end of
the dry season has been noticed in other species living in seasonal climates and
attributed to the worsening of the plant water status and the consumption of stored
reserves so as to sustain metabolic activity during a harsh dry season (Bonfil et al. 2004,
Bowen & Pate 1993, Cruz et al. 2002, Hodgkinson 1992). However, twice-disturbed
plants (before and after the dry season) showed a higher survival likelihood and
resprouting vigour than those disturbed only at the end of the season. The improvement
in resprouting ability with an increasing frequency of disturbance has been observed for
some Mediterranean species (e.g. Erica arborea, Riba 1998) but, as far as we know, this
is the first report of such a compensatory response (sensu McNaughton 1983) for an
Acacia sp. This higher performance of twice-disturbed individuals may be due to the
combination of two factors. First, after being disturbed at the start of the dry season, A.
pennatula individuals were able to resprout and quickly develop well-expanded leaves
within a few weeks (G Peguero, pers. obs; for A. karoo, Schutz et al. 2009). This
contrasts with species that exhibit a far more delayed resprouting onset (e.g.
Mediterranean evergreen oaks, Bonfil et al. 2004) and it could be due to the lower leaf
construction costs of the thin leaves of Acacia pennatula in comparison to those of
sclerophyllous-evergreen species (Wright et al. 2004). Second, in these fast-resprouting
individuals of A. pennatula, an oversized root-shoot ratio in comparison to undisturbed
plants may help to enhance resource availability and thus improve water status and
photosynthetic activity during the dry season (Castell et al. 1994, Schutz et al. 2009).
Actually, the similar levels of starch concentration of individuals disturbed just before
the dry season and those twice disturbed, suggest that the latter were quickly able to
replenish part of the starch consumed after their initial resprouting process.
Our results indicate that burn recovery required the mobilisation of a greater
amount of starch and N than recovery from clipping. As Vesk & Westoby (2004) have
suggested, this could be due to the reconstruction costs of the bud bank (i.e. meristems)
and their protective structures (e.g. bark) after more intense disturbances (e.g. burning).
Yet the lack of significant differences in starch concentration in plants disturbed before
and after the dry season and, especially between once- and twice-disturbed individuals,
backs the idea of a minor role of carbon reserves in resprouting under moderate
disturbance regimes (Cruz et al. 2003a, b). Conversely, the lower N and P levels in
individuals disturbed at the end of the dry season, and also lower P levels in those twice
disturbed, suggests that, rather than starch, N and especially P availability may constrain
the resprouting ability of plants (Canadell & López-Soria 1998, Chapin et al. 1990,
Miyanishi & Kellman 1988, Saura-Mas & Lloret 2009). The key role of P as a limiting
nutrient in tropical areas has been widely suggested (Lugo & Murphy 1986) usually
associated with a depletion-driven P limitation in old volcanic soils (Vitousek et al.
2010, see also Herbert & Fownes 1995, Vitousek & Farrington 1997). Indeed, soils in
our study area have developed from ancient volcanic parent material and show very low
P levels (9.5 1.7 ppm, D. Tarrasón, unpubl. data). In addition to soil characteristics, P
limitation for resprouting could also arise from a phenological constraint: i.e. the need
to carry out a massive mobilisation of this nutrient from woody reservoirs towards
leaves to improve water-use efficiency during drought conditions (Sardans & Peñuelas
2007). Moreover, it must be highlighted that A. pennatula as a N2-fixing species
(Cervantes et al. 1998) may have high P demands (Nguyen et al. 2006, Ribet & Drevon
1996, Vitousek 1999). Thus, low P levels may limit regrowth not only directly but also
indirectly through constraining N-fixation. To the best of our knowledge, this is the first
contribution to the hypothesis of a limitation of resprouting response in tropical dry
forests mediated by a phenological constraint in nutrient availability (N, P).
Nevertheless, given the relatively moderate disturbance intensity we applied, further
research should be carried out under more intense disturbance regimes, different
watering levels or fertilising with P. In addition, the significance of the factor ‘plot’ in
all traits describing the resprouting success and the effects of initial biomass in the final
concentration of starch and N in disturbed plants, indicates resprouting may also be
influenced by heterogeneous resources across the site not quantified and other inter-
individual differences.
As with other Acacia spp. worldwide, scattered individuals of A. pennatula may
be a keystone structure (sensu Manning et al. 2006) in highly disturbed areas in Central
America, playing a dual, contrasting role. On the one hand, they may help the early
successional recovery of other late-successional tree species through a process of
facilitation during seedling establishment (Tarrasón et al. 2010). On the other, A.
pennatula is often an early coloniser during woody succession in grassland (Purata et al.
1999) which can create problems for maintaining and managing pasture. Hence the
results obtained in this study can be used to design ecologically sound management
alternatives (i.e. protection or control) of A. pennatula, depending on the management
goals (Bond & Archibald 2003). Furthermore, our results suggest that A. pennatula
plants would perform poorly under some climate-change scenarios which predict a
lengthening of the dry seasons in some tropical-dry areas, which may also result in more
frequent fires.
References
Bond, W.J. & Archibald, S. (2003) Confronting complexity: fire policy choices in South African savanna
parks. International Journal of Wildland Fire 12, 381-389.
Bond, W.J. & Keeley, J.E. (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable
ecosystems. Trends in Ecology and Evolution 20, 387-394.
Bonfil, C., Cortés, P., Espelta, J.M. & Retana, J. (2004) The role of disturbance in the co-existence of the
evergreen Quercus ilex and the deciduous Quercus cerrioides. Journal of Vegetation Science 15,
423-430.
Bowen, B.J. & Pate, J.S. (1993) The significance of root starch in post-fire shoot recovery of the
resprouter Stirlingia latifolia R. Br. (Proteaceae). Annals of Botany 72, 7-16.
Canadell, J. & López-Soria, L. (1998) Lignotuber reserves support regrowth following clipping of two
Mediterranean shrubs. Functional Ecology 12, 31-38.
Casasola, F. (2000) Productividad de los sistemas silvopastoriles tradicionales en Moropotente, Estelí,
Nicaragua. M.Sc. thesis, CATIE, Turrialba, Costa Rica.
Castell, C., Terradas, J. & Tenhunen, J.D. (1994) Water relations, gas exchange, and growth of resprouts
in mature plant shoots of Arbutus unedo L. and Quercus ilex L. Oecologia 98, 201-211.
Cervantes, V., Arriaga, V., Meave, J. & Carabias, J. (1998) Growth analysis of nine multipurpose woody
legumes native from southern Mexico. Forest Ecology & Management 110, 329-341.
Chapin, F.S., Schultze, E.D., & Mooney, H.A. (1990) The ecology and economics of storage in plants.
Annual Review of Ecology, Evolution and Systematics 21, 423-447.
Cruz, A., Pérez, B., Quintana, J.R. & Moreno, J.M. (2002) Resprouting in the Mediterranean type shrub
Erica australis affected by soil resource availability. Journal of Vegetation Science 13, 641-650.
Cruz, A., Pérez, B. & Moreno, J.M. (2003a) Plant stored reserves do not drive resprouting of the
lignotuberous shrub Erica australis. New Phytologist 157, 251-261.
Cruz, A., Pérez, B. & Moreno, J.M. (2003b). Resprouting of the Mediterranean-type shrub Erica australis
with modified lignotuber carbohydrate content. Journal of Ecology 91, 348-356.
Ebinger, J.E., Seigler, D.S. & Clarke, H.D. (2000) Taxonomic revision of South American species of the
genus Acacia subgenus Acacia (Fabaceae: Mimosoideae). Systematic Botany 25, 588-617.
Espelta, J.M., Sabaté, S. & Retana, J. (1999) Resprouting dynamics. Pp. 61-73 in Rodà, F., Retana, J.,
Gracia, C. A. & Bellot, J. (eds.). Ecology of Mediterranean evergreen oak forests. Springer,
Berlin.
Gibson, D.J., Hartnett, D.C. & Merill, G.L.S. (1990) Fire temperature heterogeneity in contrasting fire
prone habitats – Kansas tallgrass prairie and Florida sandhill. Bulletin of the Torrey Botanical
Club 117, 349-356.
Hodgkinson, K.C. (1992) Water relations and growth of shrubs before and after fire in a semi-arid
woodland. Oecologia 90, 467-473.
IPCC (2007) Climate Change 2007: The physical science basis. Contribution of working group I to the
fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge
University Press, Cambridge. 996 pp.
Janzen, D.H. (2002) Tropical dry forest: Area de Conservación de Guanacaste, Northwestern Costa Rica.
Pp. 559-583 in Perrow, M. & Davy, A. J. (eds.). Handbook of ecological restoration, volume II.
Cambridge University Press, Cambridge.
Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the Gomphotheres ate. Science
215, 19-27.
Klimešova, J. & Klimeš, L. (2007). Bud banks and their role in vegetative regeneration – a literature
review and proposal for simple classification and assessment. Perspectives in Plant Ecology,
Evolution and Systematics 8, 115-129.
Lloret, F. & López-Soria, L. (1993) Resprouting of Erica multiflora after experimental fire treatments.
Journal of Vegetation Science 4, 367-374.
Lugo, A.E. & Murphy, P.G. (1986) Nutrient dynamics of a Puerto Rican subtropical dry forest. Journal of
Tropical Ecology 2, 55-72.
Manning, A.D., Fischer, J. & Lindenmayer, D.B. (2006) Scattered trees are keystone structures –
implications for conservation. Biological Conservation 132, 311-321.
McNaughton, S.J.C. (1983) Compensatory plant growth as a response to herbivory. Oikos 40, 329-336.
Meyer, K.M., Ward, D., Moustakas, A. & Wiegand, K. (2005) Big is not better: small Acacia mellifera
shrubs are more vital after fire. African Journal of Ecology 43, 31-136.
Miyanishi, K. & Kellman, M. (1986) The role of root nutrient reserves in regrowth of two savanna
shrubs. Canadian Journal of Botany 64, 1244-1248.
Nguyen, N.T., Mohapatra, P.K. & Fujita, K. (2006) Elevated CO2 alleviates the effects of low P on the
growth of N2-fixing Acacia auriculiformis and Acacia mangium, Plant and Soil 285, 369-379.
Purata, S.E., Greenberg, R., Barrientos, V. & Lópe-Portillo, J. (1999) Economic potential of the
Huizache, Acacia pennatula (Mimosoideae) in Central Veracruz, Mexico. Economic Botany 53,
15-29.
Riba, M. (1998) Effects of intensity and frequency of crown damage on resprouting Erica arborea L.
(Ericaceae). Acta Oecologica 19, 9-16.
Ribet, J. & Drevon, J.J. (1996) The phosphorus requirement of N2-fixing and urea-fed Acacia mangium.
New Phytologist 132, 383-390.
Sardans, J. & Peñuelas, J. (2007) Drought changes phosphorus and potassium accumulation patterns in an
Evergreen Mediterranean forest. Functional Ecology 21, 191-201.
Saura-Mas, S. & Lloret, F. (2009) Linking post-fire regenerative strategy and leaf nutrient content in
Mediterranean woody plants. Perspectives in Plant Ecology, Evolution and Systematics 11, 219-
229.
Schutz, A.E.N, Bond, W.J. & Cramer, M.D. (2009) Juggling carbon: allocation patterns of a dominant
tree in a fire-prone savanna. Oecologia 160, 235-246.
Tarrasón, D., Urrutia, J.T., Ravera, F., Herrera, E., Andrés, P. & Espelta, J.M. (2010) Conservation status
of tropical dry forests remnants in Nicaragua: Do ecological indicators and social perception
tally? Biodiversity and Conservation 19, 813-827.
Vesk, P.A. & Westoby, M. (2004) Funding the bud bank: a review of the costs of buds. Oikos 106, 200-
208.
Vieira, D.L. & Scariot, A. (2006) Principles of natural regeneration of tropical dry forests for restoration.
Restoration Ecology 14, 11-20.
Vitousek, P.M. (1999) Nutrient limitation to nitrogen fixation in young volcanic sites. Ecosystems 2, 505-
510.
Vitousek, P.M. & Farrington H. (1997) Nutrient limitation and soil development: experimental test of a
biogeochemical theory. Biogeochemistry 37, 63-75.
Vitousek, P.M., Porder, S., Houlton, B.Z. & Chadwick, O.A. (2010) Terrestrial phosphorus limitation:
mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications (20),
5-15.
Wright, B.R. & Clatke, P.J. (2007) Resprouting responses of Acacia shrubs in the Western desert of
Australia – fire severity, interval and season influence survival. International Journal of
Wildland Fire 16, 317-323.
Wright, I.J., Reich, P.B, Westoby, M., Ackerly, D.A., et al. (2004) The worldwide leaf economics
spectrum. Nature 428, 821-827.
Table 1. Results of the effects of disturbance type (clipping, burning), disturbance date (before and after the dry season and repeatedly), initial
biomass (Bi) and their interaction on survival, number of resprouts, final biomass and individual growth rate of Acacia pennatula individuals in
tropical dry forests in north-west Nicaragua. Effects on survival and number of resprouts were tested by means of generalized linear mixed
models (GLMM), while effects on the other variables were analysed by means of a general linear mixed model. For GLMM models the
covariance parameter estimate ± SE is shown.
Survival Number of resprouts Biomass Individual growth rate
df F P df F P df F P df F P
Disturbance type (D) 1, 417 8.62 0.0035 1, 344 22.8 <0.0001 1, 344 8.11 0.0047 1, 344 8.17 0.0045
Disturbance date (Dt) 2, 417 10.8 <0.0001 2, 344 16.5 <0.0001 2, 344 2.37 0.0951 2, 344 3.61 0.0281
Initial biomass (Bi) 1, 417 3.73 0.0540 1, 344 192 <0.0001 1, 344 33.6 <0.0001 1, 344 33.9 <0.0001
D × Dt 2, 417 3.73 0.246 2, 344 4.49 0.0119 2, 344 2.90 0.0562 2, 344 2.94 0.0541
D × Bi 1, 417 0.97 0.326 1, 344 24.4 <0.0001 1, 344 4.96 0.0266 1, 344 4.99 0.0261
Dt × Bi 2, 417 0.73 0.482 2 ,344 2.56 0.0786 2, 344 7.05 0.0010 2, 344 5.76 0.0035
Plot --- --- --- --- --- --- 5, 344 32.4 <0.0001 5, 344 33.7 <0.0001
Covariance parameter 0.492 ± 0.467 0.028 ± 0.019 --- ---
0
2
4
6
8
10
12
Clipping Burning
Re
spro
uts
(n
um
be
r p
er in
divi
dua
l)
Disturbance type
AaAa
Aa
Aa
Aa
Bb
after dry season
before dry season before and after
Figure 1. Mean ± SE number of resprouts in Acacia pennatula individuals subjected to
burning or clipping before dry season, after dry season and on the two dates (before and
after dry season). Different letters indicate significant differences between disturbance
treatments for a given season (upper case letters) and between the different seasons
within the same disturbance treatment (lower case letters), according to LS means tests.
0
5
10
15
20G
R in
bio
mas
s (g
mo-1
)
a a
b
before and after
after dry season
before dry season
Figure 2. Mean ± SE growth rate in biomass in Acacia pennatula individuals disturbed
before dry season, after dry season and on the two dates (before and after dry season).
Different letters indicate significant differences among the experimental treatments
according to Fisher-LSD test.
0
5
10
15
20
25
30
35
40a
b
aS
tarc
h (
mg
g -1
)
a)
0
2
4
6
8
10
a
a
b
Nitr
oge
n (
mg
g-1
)
b)
Pho
sph
oru
s (m
g g
-1)
0.5
0.4
0.3
0.2
0.1
0
0.6
a
a
a
c)
Control Clipping Burning
Figure 3. . Mean ± SE concentration of starch (a), nitrogen (b) and phosphorus (c) in
the taproot of Acacia pennatula individuals undisturbed (control), clipped and burned.
Different letters indicate significant differences according to Fisher-LSD test.
0
5
10
15
20
25
30
35
40
a)
Sta
rch
(mg
g-1)
a
a
a
a
0
1
2
3
4
5
6
7
8
Nitr
ogen
(m
g g
-1)
a a a
b
b)
Pho
spho
rus
(mg
g-1)
a a
b b
c)0.5
0.4
0.3
0.2
0.1
0control
before dry season
before and after
afterdry season
Figure 4. Mean ± SE concentration of starch (a), nitrogen (b) and phosphorus (c) in the
taproot of Acacia pennatula individuals undisturbed (control), disturbed before dry
season, disturbed after dry season and disturbed on the two dates (before and after dry
season). Different letters indicate significant differences according to Fisher-LSD test.
Capítulo2
La aptitud frugívora del ganado y la
quema de pastos –
Los primeros ingredientes para una receta
de éxito
Resumen
Tras la transformación masiva del bosque tropical seco en pastos arbolados de uso
ganadero, la falta de dispersión de semillas ha sido sugerida como una de las mayores
barreras para la regeneración forestal. Sin embargo, la dispersión de semillas mediante
endozoocória por parte del ganado junto con la capacidad del fuego para liberar a las
semillas de su latencia puede jugar un papel crucial aumentando la germinación y
finalmente el reclutamiento de plántulas. En tres especies comunes del bosque seco
Mesoamericano, evaluamos la efectividad del ganado como agente dispersor mediante
un experimento de cafetería. Además testamos la posible interacción entre endozoocória
y fuego como factores desencadenantes de la germinación, mediante un experimento en
el cual el tránsito intestinal de las semillas fue reproducido experimentalmente y
seguido de diversos tratamientos consistentes en golpes de calor a distintas temperaturas
y tiempos de exposición. Los frutos de las tres especies fueron consumidos ávidamente
por el ganado pero la gran diferencia entre especies en el número de semillas por fruto
produjo aún más acusadas diferencias en la efectividad del ganado como agente
dispersor en términos de carga de semillas por cada evento de forrajeo. No hubo
interacción entre el tránsito intestinal y el fuego sugiriendo así que la germinación de las
semillas con latencia física no es solo una cuestión del nivel de escarificación de la
cubierta. No obstante, mientras que el tránsito intestinal no produjo ningún efecto, el
fuego estimuló consistentemente la germinación a medida que la temperatura y el
tiempo de exposición de los golpes de calor aumentaron. En conjunto nuestros
resultados sugieren que la dispersión de semillas por parte del ganado junto con la
capacidad de las semillas de resistir su paso por el tracto intestinal y el fuego en
liberarlas de su latencia, pueden ser procesos clave a fin de promover la regeneración de
los bosques tropicales secos Mesoamericanos.
Chapter2
Cattle frugivory and pasture fires ‐ The first ingredients
for a successful recipe
Abstract
After the massive transformation of tropical dry forests into cattle-ranching savannas,
the lack of seed dispersal has been suggested as a major barrier to forest regeneration.
However, seed dispersal through endozoochory by cattle along with fire-induced release
of seed dormancy may play a crucial role enhancing germination and ultimately plant
recruitment in pastures. In three common Mesoamerican dry-tropical tree species, we
assessed the effectiveness of cattle as dispersal agent by means of cafeteria tests. We
also tested the potential interaction between endozoochory and fire as triggers of
germination through an experiment in which gut passage was experimentally
reproduced and followed by heat-shock treatments differing in temperature and time.
The fruits of the three species were avidly eaten by cattle but the great difference on the
number of seeds per fruit led to striking differences between species on the
effectiveness of cattle as dispersal agent in terms of seed load per foraging event. There
was no interaction between gut passage and fire: whereas gut passage did not have any
effect, fire consistently stimulated germination with increasing heat-shock temperature
and time of exposition. Overall our results suggest that seed dispersal by cattle along
with the ability of seeds to resist gut passage and the capacity of fire to release seeds
from their physical dormancy may be key processes in order to foster Mesoamerican
dry forest regeneration.
Introduction
After the pervasive transformation of Mesoamerican Dry Forests (MDF) into cattle-
ranching savannas (Griscom & Ashton 2011), the lack of seed dispersal into pastures
has been widely suggested as a major barrier to forest regeneration (Holl et al. 2000,
Griscom & Ashton 2011). Notwithstanding, several MDF species retain a suite of fruit
and seed traits that enable endozoochory (e.g., edible indehiscent fruits with hard-coated
seeds that resist scarification during gut passage), these being most likely the result of
the adaptation to the seed dispersal provided by the now extinct megaherbivores (Janzen
& Martin 1982). Therefore cattle may in turn be a key factor to overcome this dispersal
limitation by means of acting as a surrogate dispersal agent for many MDF tree species
(Janzen 1981, 1982, Gardener et al. 1993).
However fruit traits such as size, shape, number of seeds per fruit, chemical
composition or nutritional value, may result on specific preferences of frugivores
(Traveset 1998, Kitamura et al. 2002) that may affect the quantity component of their
effectiveness as seed dispersal agents, i.e., the number of visits and the number of seeds
dispersed per visit (Schupp 1993). This potential foraging choice can favour some
species and have consequences on seed dispersal into pastures and so on forest
regeneration patterns at a landscape level (Eycott et al. 2007). Although there is a
remarkable knowledge of cattle preferences between the foliages of some MDF tree
species currently used as alternative forage options (Sandoval-Castro et al. 2005), little
is yet known about cattle preferences between the fruits of the tree species they usually
feed on. Additionally, a particular animal species can have significantly different effects
on germination (i.e. positive, neutral or negative) after the seeds’ passage through its
digestive tract, and this may depend on a variety of seed traits such as seed coat
thickness, sculpture or seed size, which are intrinsic to the plant species (Traveset
1998). Consequently, different plant species may perform differently to the same
dispersal agent, for instance as a result of differences on their gut passage resistance
(Benítez-Malvido et al. 2003), but concerning MDF there are still few studies assessing
these potential differences (but see Gardener et al. 1993, Benítez-Malvido et al. 2003).
Another feature of the current conversion of MDF into cattle-ranching savannas
is the recurrent usage of fire as a pasture management strategy (Miles et al. 2006,
Peguero & Espelta 2011, Griscom & Ashton 2011). Indeed, human-induced fire has
been pervasive during the last century in MDF (Griscom & Ashton 2011) but further
there is now clear evidence that its use for forest clearance has been widespread during
the several millennia of pre-Columbian human settlement (Denevan 1992, Dull 2004,
Cooke 2005, Avnery et al. 2011). However, in spite that fire is widely known to release
physical seed dormancy and trigger germination in a variety of species and ecosystems
(Keeley & Fotheringam 2000) to the best of our knowledge there are no studies
addressing this topic on MDF tree species so that there is a surprising lack of knowledge
on their germination responses after fire (Otterstrom et al. 2006, but see Zuloaga-
Aguilar et al. 2010 for cloud forest tree species). In addition, both endozoochory and
fire have been reported to induce germination in seeds with physical dormancy (i.e.,
water impermeable coat, Baskin & Baskin 2000) by means of coat scarification
(Traveset 1998, Keeley & Fotheringam 2000) but so far it has not been explored the
relationship between both factors. Namely, if germination patterns are a function of the
level of seed coat scarification (Traveset et al. 2008), then a given seed that survives gut
passage with an abraded seed coat but remains dormant, could be released of its
physical dormancy by shorter heat-shocks at lower temperatures, thus having fire an
additive effect over the chemical and bacterial scarification produced during gut
passage.
So, the main goals of the present study were: (i) to confirm cattle as surrogate
seed dispersal agent on MDF while to assess its potential preference among fruits and
differences on its effectiveness as dispersal agent, and (ii) to investigate the germination
response after gut passage and subsequent fire in MDF tree species which are usually
dispersed by cattle into pastures. To this intent, we carried out cafeteria trials and a
germination experiment with three common MDF tree species which share
endozoochory and physical dormancy as dispersal and germination syndromes
respectively. Besides for the first time, we empirically tested whether pasture fire,
which was estimated through heat-shocks differing in temperature and exposition time
(Gashaw & Michelsen 2002), may have an additive effect over the scarification of seeds
produced during gut passage, which was simulated following a standardized in vivo-in
vitro procedure (Gardener et al. 1993). The results obtained may provide further insights
on the role that cattle and fire may have, if properly managed, in fostering MDF
regeneration in human-induced savannas.
Materials and Methods
Study area and species
This study was conducted in the Miraflor-Moropotente plateau (800-1200 m a.s.l) in
Northwest Nicaragua, which is a protected landscape characterised by a dry tropical
climate, i.e., monthly temperatures range from 16 to 33ºC and 90% of the 830 mm mean
annual precipitation falls during a 6-month wet season (May-October). The 290 km2 of
the area are a mosaic of savannah-like pastures surrounded by secondary and remnant
MDF patches with different conservation status (Tarrasón et al. 2010). Prescribed fires
during the dry season are a common practice in order to control woody species
regeneration in pastures yet there are several forest species colonizing pastures (Peguero
& Espelta 2011). This community of pasture pioneers is widely dominated by Acacia
pennatula Benth. (Fabaceae), a spiny tree that is common in secondary MDF and
disturbed areas from Central to South America. This species produces protein-rich
indehiscent flat dry pods of an average weight of 4.5 gr (±0.24 SE) with a mean of 11
(±0.21 SE) hard-coated seeds of 0.06-0.1 gr that present physical dormancy (Baskin &
Baskin 2000). Once ripen at the beginning of the dry season, these fruits are actively fed
by cattle so that their seeds are spread into pastures by dunging. After gut passage, seeds
appear to survive and apparently germinate immediately after the first rains of the next
wet season (Peguero personal observation). This fruiting phenology and dispersal
syndrome are shared by many other tree species common in the study area such as
Guazuma ulmifolia Lam. (Malvaceae) and Enterolobium cyclocarpum Jacq. Griseb.
(Fabaceae). G. ulmifolia, a 2-15 m Neotropical tree, is also common regenerating in
pastures as well as in secondary or remnant forests (Esquivel et al. 2008). Its fruits are
spheroidal nuts with a hard woody core and a sweet outer coat, and they also are
valuable dry-season forage for cattle (Janzen 1982). They have an average weight of 2.6
gr (±0.17 SE) and a mean of 51 (±0.67 SE) tiny seeds within of 0.004-0.01 gr. E.
cyclocarpum is also a dry forest tree species of Central and South America, whose
canopy of up to 50 m height represents a conspicuous landscape element. Its indehiscent
rounded dry pods are also eaten by cattle (Janzen 1981) and have an average weight of
22 gr (±0.92 SE) and a mean of 11 very hard-coated seeds (±0.58 SE) of 0.8-1.1 gr.
Both latter species also have physical seed dormancy according to Baskin & Baskin
(2000). All previous fruit trait data come from a sample of at least 30 fruits collected
from 5 individuals of each tree species.
Fruit preference experiment
In order to assess fruit preference by cattle we conducted a cafeteria experiment during
August 2009 in the farm of an extensive cattle-rancher of the study area. We habituated
seven 6-month cow calves (Brown Swiss x Brahman) to feed in individual troughs
under the researchers presence. This habituation consisted in 5 days of offering a grain-
bran based concentrate ad libitum during 5 minutes each morning. After this habituation
period we started 5 consecutive days of preference trials that consisted in offering fruits
of A. pennatula, G. ulmifolia and E. cyclocarpum in separate amounts of 0.3 kg per
species within individual troughs. During 5 minutes, which was enough time to observe
the onset of a potential fruit selection but not enough to any of the offerings became
exhausted, we recorded the number of bites to each kind of fruit and finally we
weighted the final fruit intake. During the preference trials, the calves were fasted
overnight and all trials were done from 6 to 7 am to ensure a high and equivalent
feeding motivation during the whole experimentation period. Remarkably, all
individuals were naive with the fruits offered before the experiment and to avoid
conditioned learning (association) the position of fruits within the troughs was changed
each day.
Germination experiment
In order to assess the potential additive effects of endozoochory and fire over the
germination response of the three studied species, we conducted a germination
experiment in which we combined the experimental simulation of gut passage (i.e.
endozoochory) with different thermal shock treatments (i.e. fire) in a balanced factorial
design. To simulate the effects of gut passage on the seeds we developed a three-step (1.
rumen; 2. abomasum-duodenum; 3. intestine) in vivo-in vitro standardized procedure in
the facilities of the Ruminants Research Group (Autonomous University of Barcelona)
during July 2010 (see Gardener et al. 1993 for a similar procedure). During March 2010
fruits from 5 individuals of each species were hand-harvested and manually dehisced to
obtain their seeds. Once in the lab, the seeds of each species coming from different
individuals were pooled and introduced in separate groups into sealed nylon bags
(Ankom Technology, Fairport, NY) and then into the rumen of a cannulated cow. After
48 hours of rumen suspension, the bags were placed into glass incubation bottles
containing 2 L of 0.1 N HCl adjusted to pH 1.9 with 1 g/L of pepsin (P-7000, Sigma, St.
Louis, MO) for 2h with constant rotation at 39ºC in DaisyII incubators (Ankom
Technology). After incubation the bags were rinsed with tap water and introduced in
incubation bottles containing 2 L of a pancreatin solution (0.5 M KH2PO4 buffer
adjusted to pH 7.75, containing 50 ppm of thymol and 3 g/L of pancreatin, P-7545,
Sigma) and incubated during 24 h with constant rotation at 39ºC (adapted from Gargallo
et al. 2006). Finally, to reproduce the anaerobic intestinal environment we collected
samples of rectum faeces from three different cows into plastic bags saturated with CO2
and they were immediately placed in a water-bath with a buffer solution of salt minerals
(NaCl, KCl, NaPO4, KPO4) at 39ºC. The faeces were manually crumbled in order to re-
suspend fibre associated bacteria and the solution was filtered through a 250 μm mesh
screen and completed with a buffer solution of salt minerals until reaching a dilution of
0.2 g faecal sample per ml-1 of buffer (adapted from Bindelle et al. 2006). The bags
within the intestinal bacterial inoculum were incubated 24 h more with constant rotation
at 39ºC in anaerobic conditions. Although it must be noted that retention times within a
ruminant may vary depending on the size and specific gravities of the particles (i.e.,
seeds; Murphy et al. 1989), the incubation times applied followed those suggested by
Warner (1981) and applied by Gardener et al. (1993) with which this latter authors did
not find differences compared with natural passage rates of seeds in cattle. Once the
simulation of gut passage was done, we reproduced the effects of a pasture fire by
means of exposing sets of seeds after ‘gut passage’ and without ‘gut passage’ (i.e., just
dispersed seeds versus seeds stored in a putative soil bank) to different thermal shocks
differing in temperature (60, 90 and 120ºC, and ‘no heat-shock group’ hereafter referred
as control) and with two exposition times (2 and 6 minutes) with an electric heater.
According to Gashaw & Michelsen (2002), this range of temperature and exposition
time reliably reproduces the conditions of the upper soil layers or the soil surface during
fires in tropical grasslands. After all ‘pre-germination’ treatments were applied (2 levels
of ‘gut passage’ × 4 temperatures × 2 exposition times = 16 treatments), we set 10
seeds of each species in 8.5-cm Petri dishes with moistened filter paper obtaining 10
replicates (i.e. 1 Petri dish) per treatment. All dishes were set in a germination chamber
with a constant environment of 21ºC, 70% RH and 300 μmol photons m-2 s-1 in 16/8
hours of light/dark photoperiod. During the next 14 days (Gardener et al. 1993) all
dishes were kept moistened with distilled water and germination (i.e. radicle protrusion)
was recorded daily.
Data analysis
Fruit preference by cattle was assessed as differences on the number of bites done to
each kind of fruit and on the total fruit intake (grams ingested) of each plant species
during preference trials. Additionally, we also estimated the number of ingested seeds
from the total fruit intake of each species through the species-specific ratio of seed
number per gram of fruit. Although fruit intake and number of ingested seeds were not
formally count variables, they largely depended on the number of bites given so they
equally fitted a negative binomial distribution. Therefore in order to deal with non
normality and over-dispersion of data in these three variables, negative binomial
regressions were done using GLIMMIX procedure with SAS software (SAS Institute
Inc., Cary, NC) including fruit (i.e., 3 plant species) as fixed factor and day (i.e., 5
consecutive days of feeding trials) as a continuous variable. To control for the
autocorrelation between the repeated measures carried out on the same individuals,
these (i.e., the 7 calves) were included as a residual random factor with an
autoregressive covariance structure since the measures were evenly spaced on time
(SAS 2009). The final differences on the proportions of germinated seeds per treatment
were assessed by means of a generalized linear model with a binomial error distribution
with untransformed data (Warton & Hui 2011) using GLIMMIX procedure with SAS
(SAS Institute). In this latter analysis, plant species, gut passage, temperature and
exposition time along with their interactions were included as fixed factors and the
minimum adequate model was selected according to the lower AIC.
Results
The fruits of the three species tested were avidly eaten by all naïve calves in all feeding
trials thus confirming their innate tendency to act as seed dispersal agents of these
species into pastures. However, the significant among species differences observed on
the number of bites done as well as on the fruit intake per trial (respectively, F2, 12 =
6.67; P = 0.0113 and F2, 12 = 7.26; P = 0.0086) suggested a pattern of fruit preference in
which G. ulmifolia and E. cyclocarpum were selected over A. pennatula fruits (Figure
1a-b). Interestingly, the great among species differences on the ratio of seeds per gram
of fruit led to strong differences on the mean number of seeds ingested by a calf on a
single foraging trial (F2, 12 = 35.6; P < 0.0001). This fact was specially striking in G.
ulmifolia which has great amounts of tiny seeds packed on small fruits, but further due
to this reason, the initial differences on fruit intake between E. cyclocarpum and A.
pennatula were finally equalized in terms of numbers of seed ingested (Figure 1c).
Although there were significant individual-level variation on the number of bites, on the
total fruit intake and consequently, on the number of ingested seeds (respective
covariance parameters: 0.7809 ± 0.1183; 1.0117 ± 0.1467; 3.2553 ± 1.3269), these
response variables did not change along the consecutive feeding trials (day, F1, 95 =
0.16; P = 0.6892 and F1, 95 = 0.00; P = 0.9950 F1, 95 = 0.00; P = 0.9982).
Concerning the germination experiment, there were no differences among
species on the final germination percentages (species, F2, 406 = 0.92; P = 0.3991).
However, fire consistently triggered germination of the three species tested which
reached higher germination percentages as heat-shock temperature increased
(temperature, F3, 406 = 5.41; P = 0.0012; Figure 2). Besides, the duration of fire also had
a significant effect to the extent that six minutes of heat exposition produced an overall
germination increase of 7.5 % relative to only two minutes (exposition time, F3, 406 =
5.41; P = 0.0012; respectively 10.2±3 versus 2.7±1, Mean ± SE significant differences
according to LS Means tests). By contrast, gut passage did not have significant effects
on germination (gut passage, F1, 406 = 2.57; P = 0.1097), and although gut passage
reduced between a 5-15% the germination percentage achieved by both legume species,
these species-specific differences had only marginal significance (species × gut passage,
F2, 406 = 2.64; P = 0.0727). Additionally, gut passage did not modified seeds’ response
neither to heat-shock temperature (gut passage × temperature, F3, 406 = 0.66; P = 0.5766)
nor to exposition time (gut passage × exposition time, F1, 406 = 0.1; P = 0.7538) thus
rejecting the hypothesized additive effects between gut passage and fire.
Discussion
Fruit preference and seed disperser effectiveness
The results obtained in the cafeteria trials allow us to confirm the role that cattle has as a
surrogate seed dispersal agent in MDF, at least for the species tested. This key function
however, can be extensive to a greater number of MDF tree species that retain
endozoochory traits (Janzen & Martin 1982) and it could be essential for the eventual
forest regeneration based on passive strategies (Mouissie et al. 2005, Holl & Aide 2011,
Griscom & Ashton 2011). Nonetheless, differences on fruit traits such as the content of
anti-nutritional components, e.g., tannins and phenols which are in very low
concentrations in the fruits of G. ulmifolia and E. cyclocarpum (Pinto-Ruiz et al. 2009),
may underlie the observed cattle preferences on these fruits thus suggesting that some
tree species may become (or even may have been) especially favoured. Due to the great
levels of defaunation in the heavily fragmented MDF (Melo et al. 2010) cattle is
nowadays the main seed dispersal agent for several animal-dispersed tree species into
pastures, so that the quantity component of its effectiveness as seed disperser, i.e., the
number of foraging visits and the number of seeds dispersed per visit (Schupp 1993) can
be of special relevance for forest regeneration at a landscape level (Eycott et al. 2007).
Thus, our results suggest that many tiny seeds packed within highly desired small fruits
led to greater dispersal efficiency in terms of higher potential seed loads per foraging
event (fig. 1c). The greater the number of seeds ingested by the disperser, the greater
would be the seeding into pastures therefore the chance for seedling establishment. On
the other hand, it is widely known that species with larger seeds tend to retain larger
reserves in storage cotyledons (Green & Juniper 2004) and are thus more likely to resist
drought conditions (Leishman & Westoby 1994) and also to resprout after severe
seedling damage (Harms & Dalling 1997, Green & Juniper 2004). Hence, their
hypothetical numerical disadvantage in pastures may be in part counterbalanced by their
higher seedling survival in high-stress nutrient-poor conditions (Muller-Landau 2010).
However, this potential colonization-related trade-off that involves fecundity and seed
size as well as seed dispersal and seedling tolerance deserve further field research
(Muller-Landau 2010).
Endozoochory and fire: two consecutive events fostering pasture colonization
Concerning the germination experiment, our results pointed out that the seeds of the
species tested can resist gut passage remaining viable thereby suggesting that those
traits for endozoochory may be of key importance in order to overcome forest fragments
and colonize pastures. In addition, our results also support that the adaptive significance
of large mammals to trees with endozoochory traits appear to be exclusively linked with
dispersing their seeds rather than scarifying them to trigger germination after dunging
(Janzen 1981, Janzen et al. 1985). Certainly, a given seed dispersed through
endozoochory by a large mammal not only must avoid germinating inside its dispersal
agent, which invariably leads to seed’s digestion (Janzen et al. 1985, Gardener et al.
1993), but also it should resist the scarification during gut passage sufficiently to do not
germinate immediately in the moist dung but just in the middle of the dry season.
Rather, the surviving seeds are those that become incorporated into a putative soil seed
bank as the dung is decomposed and at some later time have their dormancy broken up
in the soil by other(s) environmental cue(s) (Janzen et al. 1985, Baskin & Baskin 2000).
Interestingly, to break seed dormancy is precisely what a pasture fire has been
proved to do in the species tested in this study. Indeed fire, which was estimated by
means of heat shocks within the range described for low intensity pasture fires (Gashaw
& Michelsen 2002), showed a consistent pattern promoting germination in the three
species (fig.2). This fire-induced dormancy release may have special relevance taking
into account the high seasonality of the MDF which has been suggested to have
promoted early germination at the onset of the rainy season especially on those species
dispersed during the dry season (Garwood 1983). Despite that heat-shock triggered
germination is known to be produced on a variety of species with physical dormancy
(Keeley & Fotheringham 2000), including several African and Australian Acacia sp.
(Hanna 1984, Sabiiti & Wein 1987, Bradstock & Auld 1995, Mbalo & Witkowski
1997), this result is novel since so far it has not been assessed previously in MDF and
further it may help to explain the pasture colonizing success of the species tested
(Esquivel et al. 2008, Peguero & Espelta 2011).
Finally, concerning the lack of additive effects of fire over gut passage
scarification, it seems that physical dormancy breakage may be rather an all-or-nothing
response instead of a function of the level of seed scarification (Traveset et al. 2008). In
fact, this heat-induced dormancy breakdown is usually based initially on the rupture of
the strophiole testa cells which may occur from a certain temperature threshold (Hanna
1984, Serrato-Valenti et al. 1995). Nevertheless, the remarkable variation in
germination observed here agrees with other structural and histochemical studies
stressing that physical dormancy release is a more complex process than previously
thought (Serrato-Valenti et al. 1995, Morrison et al. 1998).
Physical Dormancy: adaptation to endozoochory and exaptation to fire?
Bradshaw et al. (2011) have pointed out that physical dormancy may display selective
advantages in highly seasonal environments where episodic seedling recruitment is
favoured. However, since physical dormancy has multiple phylogenetic origins (it is
present in 16 families) and further it is not restricted to fire-prone ecosystems, these
authors conclude that this trait should be viewed as an exaptation to fire. Being so,
physical dormancy in the species present in this study could have been selected to allow
endozoochory by those large mammals with which these species interacted during
several millions of years before their Pleistocene extinction (Janzen & Martin 1982).
Moreover, physical dormancy is likely to have evolved during this Miocene-Eocene
period (Bradshaw et al. 2011). Notwithstanding this, anthropogenic fires may also drive
the rapid evolution of seed traits such as seed coat thickness (Gómez-González et al.
2011) and in spite of there is some uncertainty around natural fire regimes in MDF
before human settlement, it is now clear that for several millennia anthropogenic fires
have been present recurrently allowing forest clearance into more open landscapes
(Denevan 1992, Dull 2004, Cooke 2005, Avnery et al. 2011). Hence, although the
origin of physical dormancy could be related to allow endozoochory, it is also likely
that anthropogenic fire has been playing an important role favouring the retention of this
trait despite the absence of seed dispersal vectors.
Conclusions
Altogether, our results suggest that the colonizing success of some MDF tree species
may in part be explained by their ability to be dispersed by cattle, by their seeds to resist
gut passage, and by pasture fires ultimately breaking their seeds’ physical dormancy
thus allowing them to match germination with the onset of the rainy season. However
nowadays in Mesoamerica, the full profile of a pasture colonist or even that of a pasture
encroacher, should include a strong resprouting ability in order to withstand the high
frequency regime of perturbations of varying severity, namely great herbivory pressure
as well as repeated clipping and burning (Peguero & Espelta 2011). Taking this into
account, if MDF regeneration in human-induced pastures is to be fostered, it seems
reasonable to maintain the seed dispersal function of cattle while relaxing both
herbivory pressure and fire regime whose frequency should be remarkably reduced and
even applied only selectively in order to ensure progressive seedling establishment.
References
Avnery, S., Dull, R.A., & Keitt, T.H. (2011) Human versus climatic influences on late-Holocene fire
regimes in southwestern Nicaragua. The Holocene, 21, 699-706.
Baskin, C.C. & Baskin, J.M. (2000) Seeds: ecology, biogeography, and evolution of dormancy and
germination Academic Press, San Diego.
Benítez-Malvido, J., Tapia, E., Suazo, I., Villaseñor, E., & Alvarado, J. (2003) Germination and seed
damage in tropical dry forest plants ingested by iguanas. Journal of Herpetology, 37, 301-308.
Bindelle, J., Buldgen, A., Boudry, C., & Leterme, P. (2007) Effect of inoculum and pepsin-pancreatin
hydrolysis on fibre fermentation measured by the gas production technique in pigs. Animal Feed
Science and Technology, 132, 111-122.
Bradshaw, S.D., Dixon, K.W., Hopper, S.D., Lambers, H., & Turner, S.R. (2011) Little evidence for fire-
adapted plant traits in Mediterranean climate regions. Trends in Plant Science, 16, 69-76.
Bradstock, R.A. & Auld, T.D. (1995) Soil temperatures during experimental bushfires in relation to fire
intensity: consequences for legume germination and fire management in south-eastern Australia.
Journal of Applied Ecology, 76-84.
Cooke, R. (2005) Prehistory of Native Americans on the Central American land bridge: colonization,
dispersal, and divergence. Journal of Archaeological Research, 13, 129-187.
Denevan, W.M. (1992) The pristine myth: the landscape of the Americas in 1492. Annals of the
Association of American Geographers, 82, 369-385.
Dull, R.A. (2004) A Holocene record of Neotropical savanna dynamics from El Salvador. Journal of
Paleolimnology, 32, 219-231.
Esquivel, M.J., Harvey, C.A., Finegan, B., Casanoves, F., & Skarpe, C. (2008) Effects of pasture
management on the natural regeneration of neotropical trees. Journal of Applied Ecology, 45,
371-380.
Eycott, A.E., Watkinson, A.R., Hemami, M.R., & Dolman, P.M. (2007) The dispersal of vascular plants
in a forest mosaic by a guild of mammalian herbivores. Oecologia, 154, 107-118.
Gardener, C.J., McIvor, J.G., & Jansen, A. (1993) Survival of seeds of tropical grassland species
subjected to bovine digestion. Journal of Applied Ecology, 30, 75-85.
Gargallo, S., Calsamiglia, S., & Ferret, A. (2006) Technical note: A modified three-step in vitro
procedure to determine intestinal digestion of proteins. Journal of Animal Science, 84, 2163-
2167.
Garwood, N.C. (1983) Seed germination in a seasonal tropical forest in Panama: a community study.
Ecological Monographs, 53, 159-181.
Gashaw, M. & Michelsen, A. (2002) Influence of heat shock on seed germination of plants from regularly
burnt savanna woodlands and grasslands in Ethiopia. Plant Ecology, 159, 83-93.
Gómez-González, S., Torres-Díaz, C., Bustos-Schindler, C., & Gianoli, E. (2011) Anthropogenic fire
drives the evolution of seed traits. Proceedings of the National Academy of Sciences, 108,
18743-18747.
Green, P.T. & Juniper, P.A. (2004) Seed mass, seedling herbivory and the reserve effect in tropical
rainforest seedlings. Functional Ecology, 18, 539-547.
Griscom, H.P. & Ashton, M.S. (2011) Restoration of dry tropical forests in Central America: a review of
pattern and process. Forest Ecology and Management, 261, 1564-1579.
Hanna, P.J. (1984) Anatomical features of the seed coat of Acacia kempeana (Mueller) which relate to
increased germination rate induced by heat treatment. New Phytologist, 96, 23-29.
Harms, K.E. & Dalling, J.W. (1997) Damage and herbivory tolerance through resprouting as an
advantage of large seed size in tropical trees and lianas. Journal of Tropical Ecology, 13, 617-
621.
Holl, K.D. & Aide, T.M. (2011) When and where to actively restore ecosystems? Forest Ecology and
Management, 261, 1558-1563.
Holl, K.D., Loik, M.E., Lin, E.H.V., & Samuels, I.A. (2000) Tropical montane forest restoration in Costa
Rica: overcoming barriers to dispersal and establishment. Restoration ecology, 8, 339-349.
Janzen, D.H. (1981) Enterolobium cyclocarpum seed passage rate and survival in horses, Costa Rican
Pleistocene seed dispersal agents. Ecology, 62, 593-601.
Janzen, D.H. (1982) Natural history of guacimo fruits (Sterculiaceae: Guazuma ulmifolia) with respect to
consumption by large mammals. American Journal of Botany, 69, 1240-1250.
Janzen, D.H., Demment, M.W., & Robertson, J.B. (1985) How fast and why do germinating guanacaste
seeds (Enterolobium cyclocarpum) die inside cows and horses? Biotropica, 17, 322-325.
Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science,
215, 19-27.
Keeley, J.E. & Fotheringham, C.J. (2000). Role of fire in regeneration from seed. In Seeds: The ecology
of regeneration in plant communities (ed M. Fenner), pp. 311-330. CABI, Wallingford.
Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Maruhashi, T., & Noma, N. (2002)
Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand.
Oecologia, 133, 559-572.
Leishman, M.R. & Westoby, M. (1994) The role of seed size in seedling establishment in dry soil
conditions--experimental evidence from semi-arid species. Journal of Ecology, 82, 249-258.
Mbalo, B.A. & Witkowski, E.T.F. (1997) Tolerance to soil temperatures experienced during and after the
passage of fire in seeds of Acacia karroo, A. tortilis and Chromolaena odorata: a laboratory
study. South African Journal of Botany, 63, 421-425.
Melo, F.P.L., Martínez-Salas, E., Benítez-Malvido, J., & Ceballos, G. (2010) Forest fragmentation
reduces recruitment of large-seeded tree species in a semi-deciduous tropical forest of southern
Mexico. Journal of Tropical Ecology, 26, 35-43.
Miles, L., Newton, A.C., DeFries, R.S., Ravilious, C., May, I., Blyth, S., Kapos, V., & Gordon, J.E.
(2006) A global overview of the conservation status of tropical dry forests. Journal of
Biogeography, 33, 491-505.
Morrison, D.A., McClay, K., Porter, C., & Rish, S. (1998) The role of the lens in controlling heat-induced
breakdown of testa-imposed dormancy in native Australian legumes. Annals of Botany, 82, 35-
40.
Mouissie, A.M., Vos, P., Verhagen, H.M.C., & Bakker, J.P. (2005) Endozoochory by free-ranging, large
herbivores: ecological correlates and perspectives for restoration. Basic and Applied Ecology, 6,
547-558.
Muller-Landau, H.C. (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed
size. Proceedings of the National Academy of Sciences, 107, 4242-4247.
Murphy, M.R., Kennedy, P.M., & Welch, J.G. (1989) Passage and rumination of inert particles varying in
size and specific gravity as determined from analysis of faecal appearance using
multicompartment models. Britih Journal of Nutrition, 62, 481-492.
Otterstrom, S.M., Schwartz, M.W., & Velázquez-Rocha, I. (2006) Responses to Fire in Selected Tropical
Dry Forest Trees. Biotropica, 38, 592-598.
Peguero, G. & Espelta, J.M. (2011) Disturbance intensity and seasonality affect the resprouting ability of
the neotropical dry-forest tree Acacia pennatula: do resources stored below-ground matter?
Journal of Tropical Ecology, 27, 539-546.
Pinto-Ruiz, R., Hernández-Sánchez, D., Ramírez-Avilés, L., Sandoval-Castro, C.A., Cobos-Peralta, M.,
& Gómez-Castro, H. (2009) Tannins and phenols on in vitro fermentation of tropical fodder
trees. Agronomía Mesoamericana, 20, 81-89.
Sabiiti, E.N. & Wein, R.W. (1987) Fire and Acacia seeds: a hypothesis of colonization success. Journal
of Ecology, 937-946.
Sandoval-Castro, C.A., Lizarraga-Sanchez, H.L., & Solorio-Sanchez, F.J. (2005) Assessment of tree
fodder preference by cattle using chemical composition, in vitro gas production and in situ
degradability. Animal Feed Science and Technology, 123, 277-289.
SAS (2009) SAS/STAT 9.2 User's Guide, 2nd edn. SAS Institute Inc., Cary.
Schupp, E.W. (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Plant Ecology,
107, 15-29.
Serrato-Valenti, G., De Vries, M., & Cornara, L. (1995) The hilar region in Leucaena leucocephala
Lam.(De Wit) seed: structure, histochemistry and the role of the lens in germination. Annals of
Botany, 75, 569-574.
Tarrasón, D., Urrutia, J.T., Ravera, F., Herrera, E., Andrés, P., & Espelta, J.M. (2010) Conservation status
of tropical dry forest remnants in Nicaragua: Do ecological indicators and social perception
tally? Biodiversity and Conservation, 19, 813-827.
Traveset, A. (1998) Effect of seed passage through vertebrate frugivores' guts on germination: a review.
Perspectives in Plant ecology, Evolution and Systematics, 1, 151-190.
Traveset, A., Rodríguez-Pérez, J., & Pías, B. (2008) Seed trait changes in dispersers' gut and
consequences for germination and seedling growth. Ecology, 89, 95-106.
Warner, A.C.I. (1981) Rate of passage of digesta through the gut of mammals and birds. Nutrition
Abstracts and Reviews, 51, 789-820.
Warton, D.I. & Hui, F.K.C. (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology,
92, 3-10.
Zuloaga-Aguilar, S., Briones, O., & Orozco-Segovia, A. (2010) Effect of heat shock on germination of 23
plant species in pine-oak and montane cloud forests in western Mexico. International Journal of
Wildland Fire, 19, 759-773.
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
(a)
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
(a)
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
(a)
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
0
2
4
6
8
10
12
No.
of
bite
s
a
b
b
(a)
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a
0
20
40
60
80
100
Fru
itin
take
(gr)
b
a
a(b)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)
0
50
100
150800
1200
1600
2000
G. ulmifolia E. cyclocarpum A. pennatula
No
. o
fin
gest
ed
seed
s
a
b
b
(c)
Figure 1. Among species differences on fruit preferences and seed ingestion by cattle
assessed by means of cafeteria feeding trials (see methods): (a) No. of bites, (b) Fruit
intake (gr), and (c) No. of ingested seeds. Values are Means ± 1SE. Different letters
show significant differences according to Least Square means tests.
0
5
10
15
20
25
Control 60 90 120
Ger
min
atio
n(%
)
Temperature (ºC)
a a
b
c
0
5
10
15
20
25
Control 60 90 120
Ger
min
atio
n(%
)
Temperature (ºC)
a a
b
c
Figure 2. Effect of heat-shock temperatures on the final germination percentages
achieved. Values are Means ± 1SE. Different letters show significant differences among
treatments differing in heat-shock temperature according to Least Square means tests.
Capítulo3
Al cerro vengo subiendo… ‐
Depredación de semillas a lo largo de un
gradiente altitudinal
Resumen
El saciado del predador y el aborto de semillas han sido reportados como mecanismos
efectivos para reducir la depredación pre-dispersiva de semillas, no obstante, si pueden
actuar simultáneamente y si su contribución en la defensa de semillas puede variar
espacialmente ha sido escasamente investigado. A lo largo del rango altitudinal del
árbol del trópico seco Acacia pennatula investigamos la relación entre la producción de
frutos y el aborto de semillas con la depredación pre-dispersiva y el éxito de infestación
por brúquidos (Mimosestes sp.). Además, evaluamos la hipotética relación entre el
número de semillas maduras que escaparon a la depredación y el reclutamiento de
plántulas a nivel de sitio durante la siguiente estación húmeda. El saciado del predador
fue efectivo dado que cuanto mayor fue la producción de frutos menor fue la proporción
de semillas depredadas, y las altas tasas de aborto estuvieron relacionadas con aumentos
en la mortalidad larval. No obstante, aunque ambos mecanismos actuaron
simultáneamente, su contribución relativa varió considerablemente a lo largo del
gradiente altitudinal, i.e., el saciado del predador fue más importante en las partes
medias del rango mientras que el aborto de semillas fue relevante en la parte periférica y
especialmente importante en el margen superior. De manera destacable, el número de
semillas maduras que escapó a la depredación estuvo relacionado con la densidad de
plántulas a nivel de sitio durante la siguiente estación húmeda subrayando la
importancia demográfica que pueden tener los mecanismos de defensa de las semillas.
En conjunto, estos resultados destacan la importancia de considerar la variabilidad
espacial cuando se analizan los mecanismos de defensa y previenen sobre considerar el
saciado o el aborto de semillas como alternativas separadas para reducir la pérdida de
semillas. Además, estos resultados pueden ser de especial relevancia ante la potencial
expansion en altura de esta especie promovida por el cambio climático.
Chapter3
Moving upwards? – Seed predation variability along an
altitudinal gradient
Abstract
Predator satiation and seed abortion have been reported as effective mechanisms
reducing pre-dispersal seed predation, however, whether they may act simultaneously
and whether their contribution to seed defence may spatially vary has been barely
addressed. Along the altitudinal range of the dry-tropical tree Acacia pennatula we
investigated the importance of fruit production and seed abortion for pre-dispersal seed
predation and infestation success by the bruchid beetles (Mimosestes sp.). Additionally,
we measured the potential relationship between the sound seed output with plant
recruitment at site level. Predator satiation was effective since the greater the fruit
production the lower the proportion of preyed seeds while high seed abortion rates were
related with increases in larval mortality. However, although both mechanisms act
simultaneously, their relative contribution vary considerably along the altitudinal range,
i.e., predator satiation was mainly present in the middle parts of the range where seed
production is much higher and seed abortion was relevant at the peripheral sites and
especially high at the upper margin. The number of sound seeds that escaped predation
was related with seedling density at site level pointing out the demographic significance
of seed defence mechanisms against pre-dispersal seed predation. Overall, these results
highlight the importance of considering spatial variability when analyzing seed defence
mechanisms and they warn about considering predator satiation or seed abortion as two
separate alternatives for plants to reduce seed loss. Moreover, these results may be of
special relevance in light of the potential climate-driven upward shift on the distribution
range of this plant species
Introduction
Seed predation by specialized insects can have major impacts on the distribution and
dynamics of plants by reducing the effective number of sound seeds and hence seedling
recruitment (Louda 1982, Crawley 2000, Kolb et al. 2007, Espelta et al. 2009, Vaz
Ferreira et al. 2011). Consequently, plants have evolved a wide array of resistance
mechanisms to preclude seed consumption based on physical and chemical barriers
(Hulme & Benkman 2002). In addition, similar to what has been defined as “tolerance”
against herbivory (see Mauricio et al. 1997, Stowe et al. 2000), other seed defence
strategies may not prevent seed predation but help “tolerate” the negative consequences
of seed loss by controlling the population of predators. Interestingly, the two
mechanisms so far described are based on the number of seed available to predators, yet
in two opposite ways: either producing extraordinary large or reducing the size of seed
crops. On the one hand, the production of large seed crops may assure some seeds to
escape predation owing to the impossibility of predators to consume all seeds (“predator
satiation” in Janzen 1971, Kelly & Sork 2002). On the other hand, a reduction on the
number of seed available, mediated by seed abortion, may constrain insect success by
killing larvae located in aborted seeds and increasing larval competition over sound
ones (Stephenson 1981, Traveset 1993, Holland et al. 2004, Östergård et al. 2007). In
both cases, the advantage of reducing seed predators’ performance must offset the cost
of the resources invested on the seeds lost (see examples for seed satiation in Espelta et
al. 2008, 2009 and for seed abortion in Holland & DeAngelis 2002).
Although numerous studies have reported evidences of the benefits of “predator
satiation” or “seed abortion” to reduce seed predation, whether these two mechanisms
may act simultaneously in a given species and whether their contribution to seed
defence may vary spatially has been barely addressed. Indeed, some studies have
suggested that local environmental conditions (e.g. local water availability in Espelta et
al. 2008, see also Kelly and Sork 2002) may influence the amount of seeds produced
and, ultimately, result in spatial differences in the success of seed predator satiation in
Mediterranean oaks. Concerning seed abortion, it has been observed that it may also
spatially vary and, specially, increase at the boundaries of a plant distribution gradient
owing to adverse climate conditions or inbreeding (Garcia et al. 2000). To some extent,
it could be hypothesised that in a resource availability gradient seed predator satiation
would easily occur in those situations where it is possible to produce large seed crops
while seed abortion would be more efficient in reducing seed predation in poorer sites.
The potential interactions and conflicts between these different seed defence
mechanisms may be of special ecological interest regarding the spatial variation of seed
predation (Louda 1982, Giménez-Benavides et al. 2007) and the environmental
conditions plants must face (Giménez-Benavides et al. 2007, Kolb et al. 2007).
The main aim of the present study has been to investigate the spatial variability of
predator satiation and seed abortion as seed defence mechanisms in the dry-forest tree
Acacia pennatula along an altitudinal gradient in NW Nicaragua. This species offers an
interesting study model for the purposes of our research as: i) it is one of the most
predominant tree species in Mesoamerica (Ebinger et al. 2000, Stevens et al. 2001), ii) it
produces large crops of fruits (pods) with multiple seeds that are conspicuously preyed
upon by several Mimosestes (bruchid) species (Janzen 1980, Traveset 1991, Peguero &
Espelta unpublished results). Moreover, there are increasing evidences of a recent
altitudinal expansion of A. pennatula in some dry-tropical regions of Nicaragua (see
Ravera 2011). In light of the potential shifts on plant distribution boundaries owing to
climate warming, studies comparing plant-animal interactions in the centre vs.
peripheral ranges have become of major interest to identify possible mechanisms
underlying these migrations (Hillyer & Silman 2010). These studies are particularly
interesting in the tropics, where upslope altitudinal shifts are far more likely than
poleward (Colwell et al. 2008, Feeley et al. 2011).
We hypothesize that the contribution of predator satiation and seed abortion to seed
escape in A. pennatula will vary along the altitudinal gradient. Specifically, massive
seed productions (i.e. predator satiation) will be the most important mechanism in the
mid-parts of the range where climate is milder and reproduction costs may be lower.
Conversely, seed abortion will be the main mechanism involved in reducing seed
predator performance at the edges of A. pennatula distribution range. In order to test this
hypothesis we assessed along an altitudinal gradient of A. pennatula presence: (i) the
variability in fruit (pods) crop size, seed production and seed abortion rates, (ii) the
infestation success of Mimosestes spp. and seed predation rates, and (iii) the final
outcome of seed predation in terms of sound seed output and seedling recruitment along
the altitudinal gradient.
Materials and methods
Study area and species
This study was conducted along an altitudinal gradient (600-1450m a.s.l) in the Estelí
valley in Northwest Nicaragua. This region is characterised by a dry tropical climate at
the low and mid-part of the gradient (up to 1000m) where the minimum and maximum
average monthly temperatures are 16 and 33ºC and the mean annual rainfall is 830mm
year-1. This gradient is characterised by increasing moisture (i.e. greater annual
precipitation and shorter dry seasons) and lower minimum temperatures with altitude as
in other similar tropical areas (Vázquez & Givnish 1998).
Along the whole gradient the landscape is a mosaic of savannah-like pastures and
sparse forest remnants where one of the dominant tree species is the pioneer Acacia
pennatula. This species is common in secondary forests and disturbed areas from
México down to Ecuador (Ebinger et al. 2000) and in our study area usually occurs
from 600 up to 1400 m a.s.l being extremely rare above and below this range (according
to exsiccatae from Stevens et al. 2001 and Peguero personal observation). Like many
other dry tropical trees (Janzen 1971), A. pennatula blooms at the beginning of the dry
season. The initiated fruits remain immature until the last rains when they suddenly
increase to full size and shape and start darkening. Once in the ground they are actively
searched by cattle that nowadays are the main dispersal agents (Peguero & Espelta
unpublished results).
The most important pre-dispersal seed predators in our study area are two beetles
(Bruchidae): Mimosestes anomalus the most common, and the rarer Mimosestes
humeralis (JM Maes personal communication). The females of both species lay their
eggs (c. 1 mm) on the surface of ripe fruits during the dry season. After hatching, the
first instar larva bore the pod wall in search of a seed from which to feed. Each larva
needs one seed to successfully complete its development hence seed multi-infestation is
not allowed (Janzen 1980, Traveset 1991). The adult beetles emerge 3-4 weeks later and
as multivoltine species, the just emerged adults can mate and several adult generations
occur in a single fruiting season (cf. Traveset 1991). In our study area parasitism
appears to be low to the extent that less than 2% of a sample of 1800 ripe fruits
contained parasitoid wasps (G. Peguero, unpublished data).
Sampling design
In order to investigate the role of predator satiation and seed abortion as seed defence
mechanisms in A. pennatula along an altitudinal gradient, five sampling areas were
selected in the Estelí valley (Table 1). All sites were flat wooded rangelands almost
dominated by A. pennatula and representative in terms of density, structure and tree
species composition of the vegetation in the study area according to Tarrasón et al.
(2010). In each site, we randomly selected 3 plots in which we measured dbh and
projected crown area of 6 trees (5 sites x 3 plots x 6 trees=90 trees). During March 2009
(the peak of the fruiting season), we made an estimation of the total fruit crop size by
means of counting the number of hanging fruits during 30 seconds by two independent
observers (see Koenig et al. 1994). Then, we collected 20 ripe fruits from the crown of
each selected tree per site (n=1800 fruits). After counting the number of eggs laid by
bruchid females, each fruit was suitably tagged and tightly packed into a thin-walled
plastic bag which was tied shut and then hung inside a large inflated and closed plastic-
bag (after Janzen 1980). During the next 4 weeks all emerged adult beetles were
removed and we recorded the number of adult emergences. In order to determine seed
abortion, seed predation and sound seed output we dissected each fruit and counted the
number of aborted seeds, preyed seeds (i.e. having a characteristic round hole) and
sound seeds.
The information gathered enabled us to calculate: i) the proportion of preyed seeds
upon mature seeds (number of preyed seeds/total seeds excluding aborted seeds), ii) the
proportion of aborted seeds (number of aborted seeds/total seeds), iii) the total seed
production per tree (number of seeds per fruit × fruit crop size) and iv) the sound seed
output per tree (number of sound seeds per fruit × fruit crop size). Infestation success
(i.e. larval survival from egg to adult stage) was inferred by means of (cf. Traveset
1991). To the calculation of this mean ratio at tree level, all fruits with emergence holes
before packing and those fruits without eggs and adult emergences were excluded. Even
though some eggs can die before larvae bore into the fruit, the ratio of adult emergences
per eggs laid has been observed to be a consistent of larval survival within fruits (Janzen
1971, see also Traveset 1990).
Finally, to explore whether there may be a relationship between the number of seeds
that escape predation and the recruitment success of seedlings along the altitudinal
gradient we measured the number of A. pennatula seedlings at each site level during the
following wet season (July 2009). We carried out 5 samplings per site in which we
counted the seedlings of less than 1-year-old in 100m2 transects (500m2 per site).
Data analysis
We used general linear mixed models to test for the effect of altitude in fruit crop size
per tree, seed number per fruit, proportion of aborted seeds per fruit, proportion of
preyed seeds per tree, and seed predator performance (i.e. the number of eggs laid per
fruit and the ratio of adult emergences per egg laid). In these models altitude (i.e. site)
was included as a fixed factor and plot as a random factor nested within altitude to
control for spatial heterogeneity within sites (Giménez-Benavides et al. 2007). In
several of these models we included covariates: i) projected crown area in the analysis
of fruit crop size to account for differences linked with individual tree sizes, ii) fruit
crop size in the analysis of the proportion of aborted to control for a potential effect of
competition among fruits matured in a tree(Stephenson 1981) and iii) total number of
seeds produced per tree in the analysis of the proportion of preyed seeds at tree level to
investigate a potential effect of predator satiation (Bonal et al. 2007, Espelta et al.
2009). In all models response variables were logarithmically transformed, if required, to
meet the assumption of normality, so that all response variables were able to be
modelled by means of general linear mixed models with restricted maximum likelihood
parameterization (Bolker et al. 2009) using SAS software (PROC MIXED, Littell et al.
2006). The effect of the random factor was analysed using Wald Z-statistic test whereas
fixed factors (i.e. altitude and covariate effects) were analysed with F-tests. Degrees of
freedom were estimated by the Satterthwaite’s method (Littell et al. 2006).
Seed predator (Mimosestes spp.) performance along the altitudinal gradient was
explored through two different analyses: (1) differences in the mean number of eggs
laid per fruit among sites were analysed including fruit crop size as a covariate that
could influence the female oviposition patterns (Östergård et al. 2007); and (2)
differences among sites on infestation success (i.e. ratio of the number of adult beetles
emerged per number of egg laid) were analysed including the proportion of aborted
seeds per fruit as a covariate to assess whether seed abortion can directly increase larval
mortality (Holland et al. 2004, Östergård et al. 2007). Best model was selected
according to Akaike Information Criterion (Bolker et al. 2009).
The relevance of seed predation for seedling recruitment was assessed by means of
running two regression analyses: i) number of mature seeds produced with seedling
density and ii) number of seeds that escaped and seedling density. If escaping predation
is a relevant process for seedling recruitment we should find a better relationship
between the density of seedlings established when compared to the number of seeds that
escaped predation, than when compared to the total number of sound seeds produced.
Finally, to test for the relevance of sound seed output in the recruitment of A. pennatula
along the altitudinal gradient, differences on seedling density were analysed by means
of a general linear model including altitude as a fixed factor.
Results
Fruit crop size in A. pennatula changed with altitude (site effect: F 4, 84= 27, P <
0.0001): it was highest at mid-high altitudes and tended to decrease in the lowest and
highest sites (Fig. 1a). This spatial variability in the number of pods produced was not
related with individual tree size (crown area effect: F 1, 84= 1.9, P = 0.17). Conversely to
fruit crop size, the number of seeds per pod was very similar among all sites except at
the highest locality where it was significantly lower (site effect: F 4, 11.7= 5.2, P =
0.0116; Fig.1b, open blocks). Although the mean number of seeds per fruit did not
change remarkably with altitude, the proportion of aborted seeds per pod clearly
differed among sites (site effect: F 4, 11.9= 15.9, P < 0.0001) being significantly greater
in the higher sites of the altitudinal gradient (Fig. 1b, filled blocks). Interestingly, fruit
crop size did not affect neither the number of seeds per fruit (covariate effect: F 1, 78.6=
2.2, P = 0.14) nor the proportion of aborted seeds per fruit (covariate effect: F 1, 80.9=
0.1, P = 0.71) suggesting there was no trade-off involved between the number of fruits,
seed number and seed abortion.
Large seed crops were effective to satiate seed predators as the larger the seed
production in a tree the lower the proportion of preyed seeds along the entire altitudinal
gradient (GLM, crop size effect: d.f. = 1, 81.1, F = 7.2, P = 0.009). Nevertheless there
were significant variations among sites in the proportion of preyed seeds (GLM, factor
site: d.f. = 4, 12.3, F = 9.8, P < 0.001, Fig. 1c).
The mean number of eggs laid by bruchid females in each fruit was not influenced
by the number of ripe fruits present in the crown (GLM, covariate effect: d.f. = 1, 84, F
= 3.1, P = 0.082) but there were significant differences along the altitudinal gradient
(GLM, site effect: d.f. = 4, 84, F = 5.1, P = 0.001). Specifically these differences arose
between the mid parts of the gradient with higher mean number of eggs laid per pod
(900 and 1100m with 7.11.4a and 6.21.2ab respectively) with the extreme parts of the
gradient (600 and 1300m with 2.91.2c and 3.91.2c respectively), although the very
highest site reached an intermediate value (4.61.1bc; values refer mean eggs per fruit
1 SE; different letters indicate significant differences according to least square means
tests). Interestingly, larval mortality estimated through the ratio of adult beetles emerged
per egg laid was markedly different among sites (GLM, factor site: d.f. = 4, 11.3, F = 5,
P = 0.015) depicting an almost inverse pattern to seed abortion (Fig. 2a vs Fig. 1b).
Actually, larval mortality increased with abortion rate per fruit (GLM, covariate effect:
d.f. = 1, 81.8, F = 6.2, P = 0.015), so that if all trees are plotted together (Fig. 2b) the
rate of seed abortion alone is able to explain the 25% of the observed variability in the
number of adult emergences per egg laid (linear regression: d.f. = 1, 85, r2 = 0.25, P <
0.0001).
Concerning the effects of within site variability (plot), it must be noticed that with two
of the previous response variables (namely, fruit crop size and number of eggs laid per
pod) the random factor could not be estimated correctly in the corresponding analyses.
Nevertheless, the lack of significance of the factor “plot” in the analyles of the number
of seeds per fruit (0.180.2, Z = 0.91, prob. Z = 0.2), the proportion of aborted seeds per
fruit (0.00010.001, Z = 0.08, prob. Z = 0.47), the proportion of preyed seeds
(0.0030.004, Z = 0.74, prob. Z = 0.23) and the number of adult beetles emerged per
egg laid (0.0010.002, Z = 0.27, prob. Z = 0.4), allows us to assume that the effects of
within site variability were also not significant in these two previous cases.
Seedling recruitment differed significantly between sites (GLM, site effect: d.f. = 4, 20,
F = 12.3, P < 0.0001, see Fig. 3a). Interestingly, the number of seedlings was not related
with the number of mature seeds produced (p = 0.1006) but with the number of mature
seeds that escaped predation (r2 = 0.93, p < 0.05, Fig. 3b).
Discussion
The present study shows that predator satiation and seed abortion can co-occur in a
given species as seed defence against predators. However they may show large spatial
variations on their relative contribution to the seed defence strategy. Indeed, predator
satiation and seed abortion varied considerably along the altitudinal gradient: i.e. in the
centre of the range massive fruit and seed production in A. pennatula trees allowed a
predominant role of predator satiation (see also Janzen 1971), whereas on the peripheral
locations, specially at the upper margin of the altitudinal range, it was mainly seed
abortion what impaired seed predator performance and reduced the infestation success
(Holland et al. 2004, Östergård et al. 2007). Overall, these results highlight the
importance of considering spatial variability when analyzing seed defence mechanisms
and they warn about considering predator satiation or seed abortion as two separate
alternatives for plants to reduce seed loss. Indeed, seed defence, in terms of large seed
productions with certain levels of seed abortion, was positively related with the success
of seedling recruitment as pointed out by the close relationship among the number of
seeds that escaped predation and the density of seedlings. However, we must handle
with some care these results, because: i) the positive relationship among seed number
and seedling density is based on a reduced number of sites and ii) other factors such as
microsite limitation and particularly competition with grasses might be other major
barriers for seedling establishment (Holl et al. 2000).
Influence of altitude in fruit/seed production and predation rates
Declining environmental suitability is expected to result in a decrease in plant
reproduction toward species’ range boundaries (Parsons 1991, García et al. 2000, Jump
& Woodward 2003). Indeed, total fruit/seed production of A. pennatula was
significantly higher at mid-parts of the altitudinal gradient (Figure 1a). This may be
mainly related with proximal ecological causes such as water availability or temperature
stress (Stephenson 1981) since those trees that experience lower water shortages (e.g.
owing to shorter dry seasons) or milder temperatures can produce greater fruit crops
(Lee & Bazzaz 1982, Jump & Woodward 2003). Conversely to fruit/seed production,
seed abortion rates increased at the peripheral sites and especially at the upper range
margin of A. pennatula which can also be related with adverse weather conditions: e.g.
greater water stress on the lowlands (Lee & Bazzaz 1986) or lower temperatures with
altitude (García et al. 2000, Jump & Woodward 2003). In addition, the highest seed
abortion in the upper point of the transect could also be due to inbreeding owing to the
lower number of trees (see Table 1, see also García et al. 2000). Interestingly, the lack
of a trade-off between fruit production and seed set reinforces the idea that seed
abortion was not mainly driven by resource competition.
Is predator satiation and seed abortion alternative or complementary seed
defence mechanisms?
Predator satiation and bruchid larval mortality owing to seed abortion acted
simultaneously along the altitudinal gradient studied. On the one hand, predator
satiation by means of large fruit crops probed to be effective along the whole altitudinal
gradient since in all trees the proportion of preyed seeds was inversely related with the
number of seeds produced (see also Janzen 1971). Although this tolerance mechanism
to predation has been suggested to be especially efficient in species with a large inter-
annual variability in seed crop size (masting species in Kelly & Sork 2002) it has also
been described in species that regularly produce large seed crops (e.g. Cassia grandis in
Janzen 1971). On the other hand, seed abortion reduced seed predator performance to
the extent that infestation success was lower in those sites in which abortion rates were
higher. Indeed, as previously suggested by other studies, seed abortion may impose
density-dependent mechanisms that control seed predators’ populations (Stephenson
1981, Holland & DeAngelis 2002) by means of an increase in larval competition and
larval mortality (Holland et al. 2004, Östergård et al. 2007), which are two of the main
factors that have been suggested to set bruchid density (Janzen 1971, Traveset 1991).
Additionally, a low seed to ovule ratio has been suggested as a bet-hedging strategy
against environmental stochasticity, giving opportunities to rapidly adjust seed set when
conditions are favourable and enhancing the quality of offsprings through a better
resource matching (de Jong & Klinkhamer 2005). Indeed, all these adaptive
explanations for the advantage of a certain level of seed abortion rather than mutually
exclusive might mutually reinforce.
The relative contribution of predator satiation and seed abortion to seed defence varied
along the altitudinal gradient. Since predator satiation depends on large fruiting efforts
(Janzen 1971, Bonal et al. 2007, Espelta et al. 2009), it seems reasonable it will occur
most likely where the environmental conditions are suitable to the reproductive
function, i.e. at the centre part of the altitudinal or latitudinal distribution range of a
given plant species (García et al. 2000, Jump & Woodward 2003). But in fact, along the
whole altitudinal gradient studied those A. pennatula trees with larger seed productions
lost lower proportions of their seeds despite the substantial differences among sites on
total fruit crops, so that the costs of satiation may be different among sites. We suggest
that this may be related with the reduction of infestation success that seed abortion
imposes to seed predators which may result in a greater effectiveness of satiation. This
hypothetical complementarity could imply a modification of the fitness gain curve of
predator satiation, i.e. with less investment there is a greater reproductive success in
terms of greater sound seed outputs (de Jong & Klinkhamer 2005). In fact as discussed
above there is no evidence for a trade-off between fruit production, seed set and seed
abortion rates which could have led to disruptive selections between these two
mechanisms of seed defence (see Mauricio et al. 1997 for defences against herbivory).
Moreover, different defence traits may be redundant but not mutually exclusive
(Mauricio et al. 1997) and so mixed patterns of defence allocation may lead to
evolutionary stable strategies (Núñez-Farfán et al. 2007) for instance when their costs
are significantly variable between populations (Fornoni et al. 2004). From our point of
view, this rationale could also be applicable to different strategies of seed defence
mechanisms as they jointly benefit plants against seed predation (Siemens et al. 1992,
Xiao et al. 2007) and the reproductive components implied (i.e. seed production and
abortion) spatially vary (García et al. 2000, Jump & Woodward 2003, Giménez-
Benavides et al. 2007).
Perspectives: Seed predator tolerance and the potential upward migration of A.
pennatula under new climatic scenarios
There is an increasing evidence of rapid range boundaries shifts in many plant species in
response to climate warming (Chen et al. 2011). Particularly in tropical systems, it is
expected that upslope shifts will be far more likely than poleward migrations (Colwell
et al. 2008, Feeley et al. 2011). Interestingly, it has been suggested that these shifts may
be brought about not only by a direct tracking of the changes in climate but also by
indirect changes in species’ interactions (Davis et al. 1998, Thomas 2010). All these
things being considered, we can question how climate change will modify the current
seed defence mechanisms observed in A. pennatula and how it will influence the
suggested upward range expansion of this species (Ravera 2011). In our study area, the
presence of bruchid eggs along the whole altitudinal range discards the possibility of an
“enemy release” effect leading to a relaxation of the seed predation pressure on the
upper range margin in this case (see Menéndez et al. 2008). Conversely, it seems that
seed abortion is currently contributing to reduce seed predation and thus favouring
seedling recruitment in the upper sites. To what extent climate warming might result in
a shift from seed abortion to seed predator satiation as the main seed defence
mechanisms against pre-dispersal seed predators requires further attention to discern
whether lower seed predation at higher elevations may be one of the causes of upslope
migration facing climate change in tropical forests (Hillyer & Silman 2010).
References
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J.S.S.
(2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in
Ecology & Evolution 24, 127-135.
Bonal, R., Munoz, A. & Diaz, M. (2007) Satiation of predispersal seed predators: the importance of
considering both plant and seed levels. Evolutionary Ecology 21, 367-380.
Chen, I., Hill, J.K., Ohlemüller, R., Roy, D.B. & Thomas, C.D. (2011) Rapid Range Shifts of Species
Associated with High Levels of Climate Warming. Science 333, 1024-1026.
Colwell, R.K., Brehm, G., Cardelús, C.L., Gilman, A.C. & Longino, J.T. (2008) Global warming,
elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258.
Crawley, M.J. (2000) Seed predators and plant population dynamics. - In: Fenner, M. (ed.) Seeds: The
Ecology of Regeneration in Plant Communities. CAB International, pp. 157-191.
Davis, A.J., Jenkinson, L.S., Lawton, J.H., Shorrocks, B. & Wood, S. (1998) Making mistakes when
predicting shifts in species range in response to global warming. Nature 391, 783-786.
de Jong, T.J. & Klinkhamer, P.G.L. (2005) Evolutionary ecology of plant reproductive strategies.
Cambridge University Press.
Ebinger, J.E., Seigler, D.S. & Clarke, H.D. (2000) Taxonomic revision of South American species of the
genus Acacia subgenus Acacia (Fabaceae: Mimosoideae). Systematic Botany 25, 588-617.
Espelta, J.M., Cortés, P., Molowny-Horas, R. & Retana, J. (2009) Acorn crop size and pre-dispersal
predation determine inter-specific differences in the recruitment of co-occurring oaks. Oecologia
161, 559-568.
Espelta, J.M., Cortés, P., Molowny-Horas, R., Sánchez-Humanes, B. & Retana, J. (2008) Masting
mediated by summer drought reduces acorn predation in Mediterranean oak forests. Ecology 89,
805-817.
Feeley, K. J., Silman, M. R., Bush, M. B., Farfan, W., Cabrera, K. G., Malhi, Y., Meir, P., Revilla, N. S.,
Quisiyupanqui, M. N. R. & Saatchi, S. 2011. Upslope migration of Andean trees. Journal of
Biogeography 38, 783-791.
Fornoni, J., Núñez-Farfán, J., Valverde, P.L. & Rausher, M.D. (2004) Evolution of mixed strategies of
plant defense allocation against natural enemies. Evolution 58, 1685-1695.
García, D., Zamora, R., Gómez, J.M., Jordano, P. & Hódar, J.A. (2000) Geographical variation in seed
production, predation and abortion in Juniperus communis throughout its range in Europe.
Journal of Ecology 88, 435-446.
Giménez Benavides, L., Escudero, A. & Iriondo, J.M. (2007) Reproductive limits of a late flowering high
mountain Mediterranean plant along an elevational climate gradient. New Phytologist 173, 367-
382.
Hillyer, R. & Silman, M.R. (2010) Changes in species interactions across a 2.5 km elevation gradient:
effects on plant migration in response to climate change. Global Change Biology 16, 3205-3214.
Holl, K.D., Loik, M.E., Lin, E.H.V. & Samuels, I.A. (2000) Tropical montane forest restoration in Costa
Rica: overcoming barriers to dispersal and establishment. Restoration Ecology 8, 339-349.
Holland, J.N., Bronstein, J.L. & DeAngelis, D.L. (2004) Testing hypotheses for excess flower production
and low fruit to flower ratios in a pollinating seed consuming mutualism. Oikos 105, 633-640.
Holland, N.J. & DeAngelis, D.L. (2002) Ecological and evolutionary conditions for fruit abortion to
regulate pollinating seed-eaters and increase plant reproduction. Theoretical Population Biology
61, 251-263.
Hulme, P.E. & Benkman, C.W. (2002) Granivory. - In: Herrera, C. M. and Pellmyr, O. (eds.), Plant–
animal interactions: An evolutionary approach. Blackwell Publishing, pp. 132-54.
Janzen, D.H. (1971) Escape of Cassia grandis L. beans from predators in time and space. Ecology 52,
964-979.
Janzen, D.H. (1980) Specificity of seed-attacking beetles in a Costa Rican deciduous forest. Journal of
Ecology 68, 929-952.
Jump, A.S. & Woodward, F.I. (2003) Seed production and population density decline approaching the
range edge of Cirsium species. New Phytologist 160, 349-358.
Kelly, D. & Sork, V.L. (2002) Mast seeding in perennial plants: why, how, where? Annual Review of
Ecology and Systematics 33, 427-447.
Koenig, W.D., Mumme, R.L., Carmen, W.J. & Stanback, M.T. (1994) Acorn production by oaks in
central coastal California: variation within and among years. Ecology 75, 99-109.
Kolb, A., Ehrlén, J. & Eriksson, O. (2007) Ecological and evolutionary consequences of spatial and
temporal variation in pre-dispersal seed predation. Perspectives in Plant Ecology, Evolution and
Systematics 9, 79-100.
Lee, T.D. & Bazzaz, F.A. (1982) Regulation of fruit and seed production in an annual legume, Cassia
fasciculata. Ecology 63, 1363-1373.
Lee, T.D. & Bazzaz, F.A. (1986) Maternal regulation of fecundity: non-random ovule abortion in Cassia
fasciculata Michx. Oecologia 68, 459-465.
Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O. 2006. SAS for mixed
models. SAS Institute Publishing.
Louda, S.M. (1982) Distribution Ecology - Variation in Plant Recruitment over a Gradient in Relation to
Insect Seed Predation. Ecological Monographs 52, 25-41.
Mauricio, R., Rausher, M.D. & Burdick, D.S. (1997) Variation in the defense strategies of plants: are
resistance and tolerance mutually exclusive? Ecology 78, 1301-1311.
Menéndez, R., González-Megías, A., Lewis, O.T., Shaw, M.R. & Thomas, C.D. (2008) Escape from
natural enemies during climate-driven range expansion: a case study. Ecological Entomology 33,
413-421.
Núñez-Farfán, J., Fornoni, J. & Valverde, P.L. (2007) The evolution of resistance and tolerance to
herbivores. - Annual Review of Ecology, Evolution and Systematics 38, 541-566.
Östergård, H., Hambäck, P.A. & Ehrlén, J. (2007) Pre-dispersal seed predation: The role of fruit abortion
and selective oviposition. Ecology 88, 2959-2965.
Parsons, P.A. (1991) Evolutionary rates: stress and species boundaries. Annual Review of Ecology and
Systematics 22, 1-18.
Ravera, F. (2011) Which future for semi-arid socio-ecological systems? Anticipatory co-learning for
climate change adaptation in Northern Nicaragua. Institut de Ciència i Tecnologia Ambiental. -
Universitat Autònoma de Barcelona, p. 310.
Siemens, D. H., Johnson, C.D. & Ribardo, K.J. (1992) Alternative seed defense mechanisms in
congeneric plants. Ecology 73, 2152-2166.
Stephenson, A.G. (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annual
Review of Ecology and Systematics 12, 253-279.
Stevens, W.D., Ulloa, C.U., Pool, A. & Montiel, O.M. (2001) Flora de Nicaragua. Missouri Botanical
Garden.
Stowe, K.A., Marquis, R.J., Hochwender, C.G. & Simms, E.L. (2000) The evolutionary ecology of
tolerance to consumer damage. Annual Review of Ecology and Systematics 31, 565-595.
Tarrasón, D., Urrutia, J.T., Ravera, F., Herrera, E., Andrés, P. & Espelta, J.M. (2010) Conservation status
of tropical dry forest remnants in Nicaragua: Do ecological indicators and social perception tally?
Biodiversity and Conservation 19, 813-827.
Thomas, C.D. (2010) Climate, climate change and range boundaries. Diversity and Distributions 16, 488-
495.
Traveset, A. (1990) Bruchid egg mortality on Acacia farnesiana caused by ants and abiotic factors.
Ecological Entomology 15, 463-467.
Traveset, A. (1991) Pre-dispersal seed predation in Central American Acacia farnesiana: factors affecting
the abundance of co-occurring bruchid beetles. Oecologia 87, 570-576.
Traveset, A. (1993) Deceptive fruits reduce seed predation by insects in Pistacia terebinthus L.
(Anacardiaceae). Evolutionary Ecology 7, 357-361.
Vaz Ferreira, A., Bruna, E.M. & Vasconcelos, H.L. (2011) Seed predators limit plant recruitment in
Neotropical savannas. Oikos 120, 1013-1022.
Vázquez, G.J.A. & Givnish, T.J. (1998) Altitudinal gradients in tropical forest composition, structure, and
diversity in the Sierra de Manantlán. Journal of Ecology 86, 999-1020.
Xiao, Z., Harris, M.K. & Zhang, Z. (2007) Acorn defenses to herbivory from insects: implications for the
joint evolution of resistance, tolerance and escape. Forest Ecology and Management 238, 302-
308.
Local
Name
Site
Coordinates
Altitude
(m a.s.l)
Equivalent
Diameter
(cm)
Individual
Crown Area
(m2)
Tree
Density
(Ind/Ha)
Basal
Area
(m2/Ha)
Trinidad 12º56.22'N
86º13.10'W
600 101 38.23.8 700110 15.11.2
Limón 13º3.83'N
86º21.79'W
900 121 68.48 40678 10.92.2
Campana 13º09.10'N
86º19.12'W
1100 121 74.49 549126 17.74.7
Brasil 13º10.14'N
86º15.03'W
1300 181 122.110.5 680180 33.97.9
Miraflor 13º13.80'N
86º13.58'W
1450 191 119.210 26342 22.23
Table 1. Summary of A. pennatula forest characteristics in the different sites.
Equivalent diameter and individual crown area are the mean of 30 randomly selected A.
pennatula trees in each site (10 per plot) whereas tree density and basal area have been
calculated by sampling all trees in 3 circles (radius=20m) in each site. All values are
Mean SE.
0
20
40
60
80
100
600 900 1100 1300 1450
(c)
Pro
por
tion
of p
reye
d s
eed
s (%
)
Altitude (m)
a
b b
a
a
0
20
40
60
80
100
120
600 900 1100 1300 1450
(a)N
o.
frui
ts p
er t
ree
a
b
cc
b
0
2
4
6
8
10
12
14
0
20
40
60
80
100
600 900 1100 1300 1450
No.
see
ds p
er f
ruit
Pro
portio
n of ab
orted see
ds (%)
A A AA
B
c
bc
aa
ab
(b)
0
20
40
60
80
100
600 900 1100 1300 1450
(c)
Pro
por
tion
of p
reye
d s
eed
s (%
)
Altitude (m)
a
b b
a
a
0
20
40
60
80
100
120
600 900 1100 1300 1450
(a)N
o.
frui
ts p
er t
ree
a
b
cc
b
0
2
4
6
8
10
12
14
0
20
40
60
80
100
600 900 1100 1300 1450
No.
see
ds p
er f
ruit
Pro
portio
n of ab
orted see
ds (%)
A A AA
B
c
bc
aa
ab
(b)
Figure 1. Altitudinal differences in: (a) Number of fruits per tree, (b) Number of seeds
per fruit (open blocks) and proportion of aborted seeds per fruit (filled blocks) and (c)
Proportion of preyed seeds per tree of A. pennatula. Mean SE values are represented.
Different letters indicate significant differences between sites according to LS means
tests.
Figure 2. (a) Differences in number of adult beetles of Mimosestes sp. emerged per egg
laid on A. pennatula fruits along an altitudinal gradient. Mean SE values per tree are
represented. Different letters indicate significant differences between sites according to
LS means test. (b) Relationship between rate of seed abortion per fruit and the number
of adult beetles emerged per egg laid at tree level (d.f. = 1, 85, r2 = 0.25, P < 0.0001).
600 900 1100 1300 1450
(a)
Ad
ult
em
erg
ed p
er e
gg
laid
Altitude (m)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
a
bcc
ab
a
(b)(b)
0
0.2
0.4
0.6
0.8
1
0
0.2
0.4
0.6
0.8
1
0 0.1 0.2 0.3 0.4 0.5 0.6
Rate of seed abortion
Ad
ulte
me
rge
d p
ereg
gla
id
0 0.1 0.2 0.3 0.4 0.5 0.6
Ad
ulte
me
rge
d p
ereg
gla
id
Rate of seed abortion
Figure 3. (a) Differences in seedling density of A. pennatula along the altitudinal
gradient. Mean SE values are represented. Different letters indicate significant
differences between sites according to Tukey HSD test. (b) Significant relationship
between the sound seed output (number of escaped seeds) per tree and seedling density
at site level (d.f.= 1,5, r2=0.93, p < 0.05).
0 100 200 300 400 500 600 700No. escaped seeds
0
0.1
0.2
0.3
0.4
0.5
0.6
No
. se
edl
ing
sp
er
m2
600900
1450
1100
1300
(b)
0 100 200 300 400 500 600 700No. escaped seeds
0
0.1
0.2
0.3
0.4
0.5
0.6
No
. se
edl
ing
sp
er
m2
600900
1450
1100
1300
(b)
0 100 200 300 400 500 600 700No. escaped seeds
0
0.1
0.2
0.3
0.4
0.5
0.6
No
. se
edl
ing
sp
er
m2
600900
1450
1100
1300
(b)
No
. of s
ee
dlin
gs
pe
r m
2
aa
a
b
b
Altitude (m)600 900 1100 1300 1450
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7(a)
Capítol4
Demasiados depredadores para una
misma semilla –
¿Una coexistencia mediada por los
frugívoros?
Resumen
Se ha sugerido que los vertebrados frugivores reducen la depredación de semillas a
través del control de las poblaciones de insectos depredadores de semillas (IDS) a los
cuales matan accidentalmente cuando comen frutos. No obstante, no se ha explorado si
esta depredación ‘intra-gremio’ puede afectar de manera diferencial a distintas especies
de IDS de acuerdo a diferencias en la permanencia en los frutos debidas a notables
diferencias en el tiempo de desarrollo larvario. En los árboles del trópico seco Acacia
pennatula y Guazuma ulmifolia exploramos el rol que los frugívoros (a saber, el ganado
doméstico) pueden jugar reduciendo la depredación de semillas y promoviendo la
coexistencia de distintas especies de IDS (Bruchidae spp.) con distintos tiempos de
desarrollo larvario. Comparamos la depredación de semillas y las abundancias relativas
de las especies de brúquidos en dos localizaciones contrastadas por la presencia y la
ausencia de frugívoros (ganado). En presencia de ganado encontramos una significativa
reducción de la proporción de semillas depredadas y cambios en la comunidad de IDS:
hubo una menor abundancia de especies de brúquidos con un desarrollo larval más
prolongado. Nuestros resultados sugieren que la interacción entre procesos evolutivos
(que resultan en variaciones en los atributos del ciclo vital de los IDS) con procesos
ecológicos (por ejemplo, depredación ‘intra-gremio’) pueden contribuir a la
coexistencia de distintas especies de insectos alimentándose de las semillas de la misma
planta huésped.
Chapter4
Too much predators for the same seed ‐ A frugivore‐
mediated coexistence?
Abstract
Vertebrate frugivores have been suggested to reduce seed predation by controlling the
populations of insect seed predators (ISP) by means of killing them when feed on fruits.
However it has not been explored whether this intra-guild predation may differently
affect ISP according to differences in the time larvae spend in the fruit. In the dry-
tropical trees Acacia pennatula and Guazuma ulmifolia we explored the role that
frugivores may play in reducing seed predation and in the coexistence of the ISP
involved (Bruchidae spp.) with different larval development times. We compared seed
predation and the relative abundance of bruchid species in two sites contrasted by the
presence and absence of frugivores (cattle). In the presence of cattle we found a
significant reduction of the proportion of seeds preyed upon and changes in the ISP
community: i.e. a lower presence of the bruchid species with a longer larval
development time. Our results suggest that the interplay between evolutionary processes
(resulting in variation in ISP life-histories) with ecological interactions (e.g. frugivore
intra-guild predation) may contribute to the coexistence of different insect species
feeding upon the same host plant.
Introduction
How species exploiting the same resources can coexist is a basic theoretical question in
ecology. Concerning insect seed predators (ISP), coexistence of species sharing the
same host plant has been mainly explained through trait-mediated effects resulting from
ecological constraints based on differences in insects sizes (Espelta et al. 2009, Bonal et
al. 2011). However, ISP along with vertebrate frugivores and their common target plant
form evolutionary triads characterised by complex and dynamic interactions. Indeed, in
addition to direct two-way relationships with the plant –antagonistic with predators and
mutualistic with frugivores–, there may be indirect interactions between frugivores and
ISP benefiting the plant (Sallabanks & Courtney 1992). For example, once dispersed,
seeds are no longer available for pre-dispersal ISP so they may ‘escape’ in space
(Janzen 1971). Furthermore, frugivores can indirectly control the size of ISP
populations by killing insects (i.e. enclosed larvae or pupae) when feed on fruits
(Herrera 1989, Hauser 1994, Gómez & González-Mejías 2002, Bonal & Muñoz 2007).
Nonetheless, whether insects with different life-history traits may have different
vulnerabilities to frugivores has not yet been explored.
If insect infestation does not remarkably alter fruit characteristics deterring
frugivores (Herrera 1984), vertebrate-dispersed fruits may be seen as ‘risky places’ for
insects feeding inside them since the longer the time spent in the fruit the greater the
probability of being ingested. Therefore, the guild of insects that compete for seeds of
the same plant may experience different vulnerabilities to frugivory depending on their
fruit residence time which is often mediated by species-specific differences in larval
development time (LDT). Thus the presence of frugivores would not only reduce seed
predation but also may modify the community of insects involved: i.e. by reducing the
population of species with longer LDT.
In this study, conducted in the dry-tropical trees Guazuma ulmifolia and Acacia
pennatula, we observed that frugivores reduce the levels of pre-dispersal seed predation
and we provide, apparently for the first time, evidences suggesting that they may alter
the community of ISP (Bruchidae spp. in our study). Finally, we discuss these results in
light of how the interplay between ecological and evolutionary processes may allow the
coexistence of ISP that compete for the same resource.
Material and methods
Study area and species
This study was conducted at “El Limón Biological Field Station” (13º 03’ 44”N – 86º
21’ 57”W; National Autonomous University of Nicaragua-Managua) in the Estelí valley
(Northwest Nicaragua), a region characterised by a dry tropical climate, i.e., monthly
temperatures ranging from 16 to 33ºC and 90% of the 830 mm of mean annual
precipitation falling during a 6-month wet season (November-May). The landscape is a
mosaic of savannah-like pastures, secondary and remnant tropical dry forest patches
where the native Acacia pennatula (Fabaceae) and Guazuma ulmifolia (Malvaceae)
usually dominate (Tarrasón et al. 2010). Both species bloom during the dry season and
the initiated fruits remain immature until the last rains when they suddenly increase to
full size and gradually fall from February to May. In A. pennatula, fruits are indehiscent
dry flat pods of an average length of 8.5 (±0.06 SE), a width of 2 cm (±0.01 SE) and a
mean of 10 seeds (±0.14 SE) in each pod, while G. ulmifolia has hard spheroidal nuts of
an average maximum diameter of 2.3 cm (±0.01 SE) containing a mean of 44 tiny seeds
within (±0.67 SE; n=600 fruits of each species). Once on the ground, both types of
fruits are actively consumed by domestic cattle which nowadays, after the extinction of
Pleistocene mega-herbivores, are the main seed dispersal agents through endozoochory
(Janzen & Martin 1982).
Seeds of both species are conspicuously preyed upon by the larvae of several
bruchid species (figure 1): Mimosestes anomalus (Kingsolver & Johnson 1978) and
Mimosestes humeralis (Gyllenhal 1873) in A. pennatula; and Amblycerus cistelinus
(Gyllenhal 1833) and Acanthoscelides guazumae (Johnson & Kingsolver 1971) in G.
ulmifolia. It should be noticed that, while larvae of M. anomalus, M. humeralis and A.
guazumae require a single seed to complete their development, the larvae of A.
cistelinus must eat almost all seeds of a single fruit to become an adult (Janzen 1982,
Traveset 1992). Therefore in A. cistelinus only one adult can emerge from each infested
fruit after a time length of about 6 weeks after oviposition, whereas in the other species
in 3-4 weeks as many adults may emerge as sound seeds in the fruit (Janzen 1982,
Traveset 1992). Accordingly, A. cistelinus is considered to be a univoltine species
whereas Mimosestes spp. and A. guazumae are multivoltine and may produce several
generations during each fruiting season (Janzen 1982, Traveset 1992).
Sampling design
To test for the potential effect of frugivores on seed predation and on the relative
abundances of the abovementioned bruchid species on their specific hosts, we selected
two adjacent flat forests with identical management history (i.e. absence of
anthropogenic fires), fairly dominated by A. pennatula and G. ulmifolia, but contrasted
by the presence and the long absence of frugivores: i.e. a 15-ha wooded rangeland
where cattle eat all fallen fruits vs “El Limón Biological Field Station” that is an old
ranch with 17-ha of secondary forest where cattle have been excluded for 13 years and
there is no frugivory at all (G. Peguero personal observation). Although more replicates
would have been ideally desirable, in this as well as in other similar ecosystems it is
highly difficult to find such large herbivore exclosures extended on time (see for similar
experimental designs Cabin et al. 2000, González-Mejías et al. 2004, Bonal & Muñoz
2007). So, during March 2009 at the peak of the fruiting season, we randomly selected
10 trees of each species scattered within each site. We estimated their fruit crop size by
having two independent observers count the number of fruits for 30 seconds. Then, after
gently shaking the branches, we collected 30 fallen ripe fruits per tree in both sites (2
sites × 2 species × 10 trees × 30 fruits tree-1, n=1200 fruits). In the lab, each fruit was
tagged and packed into an inflated plastic-bag and for the next 6 weeks all emerged
adult beetles were collected for species determination. Finally, we dissected each fruit
and counted the number of preyed and sound seeds to calculate the proportion of preyed
seeds (preyed seed/total seeds).
Data analysis
Differences in fruit crop sizes and seed predation among sites were analysed by means
of general linear models after checking the normality of the response variables. For the
analysis of crop size we included the projected crown area as a covariate in order to
account for differences in tree size among populations while for the assessment of seed
predation we included fruit crop size to account for the potential effect of predator
satiation. Changes in the relative composition of the guild of ISP among sites were
tested at tree level (i.e. considering all sampled fruits per tree) by comparing the number
of emerged individuals of each species and the species proportion. These analyses were
performed by means of Kruskal-Wallis tests using site as the grouping variable.
Analyses were done for the two tree species separately owing to the differences in their
guild of ISP.
Results
There were no differences in fruit crop size per tree among sites for both A. pennatula
(F1,17 = 1.0, P = 0.3) as for G. ulmifolia (F1,17 = 1.2, P = 0.3) and in neither of the two
species was fruit production influenced by crown area (F1,17 = 1.9, P = 0.2 for A.
pennatula, and F1,17 = 0.07, P = 0.8 for G. ulmifolia). The trees of both species suffered
significantly higher seed predation in the site without frugivores (0.843±0.04 vs
0.695±0.04, F1,17 = 7.8, P = 0.01 for A. pennatula and 0.378±0.04 vs 0.115±0.04, F1,17 =
19.1, P = 0.0004 for G. ulmifolia) and these predation rates were not influenced by fruit
crop per tree (respectively, F1,17 = 0.26, P = 0.2 and F1,17 = 0.07, P = 0.8). Within the
guild of ISP preying on A. pennatula seeds there were no differences among sites either
in the numbers of adult beetles collected (χ21,20= 0.97, P = 0.32 for M. humeralis, and
χ21,20= 0.06, P = 0.94 for M. anomalus) or in the relative proportion of each species
(χ21,20= 0.57, P = 0.45; figure 2a). Conversely there were strong differences in the
relative abundance of G. ulmifolia’s ISP (figure 2b). In the site without frugivores
almost all collected beetles (98%) belonged to the larger Amblycerus cistelinus, whereas
this species hardly reached 28% in the presence of frugivores (χ21,20= 7.6, P = 0.006 for
the number of individuals and χ21,20= 12.9, P = 0.0003 for species proportion).
Discussion
The present study provides new evidences suggesting that beyond their role as seed
dispersal agents, frugivores may control the populations of insects feeding upon seeds
through incidental digestion (Herrera, 1989, Hauser 1994, Gómez & González Mejía
2002) leading to a significant reduction of the proportion of preyed seeds (Bonal &
Muñoz 2007). Moreover, to the best of our knowledge, we document for the first time
that this control effect may differ among the various species of ISP that exploit the same
host plant.
Certainly, we must acknowledge that to obtain our results only a large herbivory
exclosure (17-ha) could be used. As in other previous works (Cabin et al. 2000,
González-Mejías et al. 2004, Bonal & Muñoz 2007), the difficulty of finding such large
facilities preclude a complete spatially replicated design. Nevertheless, the consistency
of the reduction of seed predation in both A. pennatula and G. ulmifolia (i.e. a sort of
biological replicates) and the lower vulnerability of the multivoltine bruchid species (i.e.
with lower larval development time) suggest cattle frugivory as the most parsimonious
explanation to the differences observed in seed predation and the composition of insect
community.
As previously reported, the lack of grass during the dry season makes the fallen ripe
fruits of both tree species to be highly desired resources for cattle and thus they are
ingested irrespective of whether they are sound or insect infested (Janzen 1982,
Traveset 1992, Peguero personal observation). Thus, fruit ingestion directly mediates
‘seed escape’ but also results in the incidental digestion of any enclosed larvae or pupae
(Herrera 1989, Hauser 1994) and although fruits may be seen as risky places for ISP, in
light of our results the risks taken appear to be different for each species within the same
ecological guild. In the case of G. ulmifolia, there were striking differences among sites
concerning the relative abundances of each ISP species. After a long absence of
frugivores (e.g. cattle during 13 years) the larger A. cistelinus seems to exclude the tiny
A. guazumae, most likely because the larger larva of the former species devour the
single-seed infesting larvae of the latter when multi-infestation of a fruit occurs (Janzen
1982), and this competitive exclusion seems to be a common situation (Johnson &
Kingsolver 1971, Janzen 1982). However, in areas where fruits are regularly consumed
by cattle the population of A. cistelinus decreases while that of A. guazumae increases.
The lower vulnerability of A. guazumae to vertebrate frugivory could arise from its
multivoltine life-history strategy: a small body size involves a shorter LDT which
directly results in less time spent in a vulnerable state within the fruit. Conversely, in A.
pennatula neither the number of emerged adults nor the relative proportions of
Mimosestes species varied. In this case, the similar body size and multivoltinism of both
species may involve a similar LDT and thus, the same vulnerability to frugivores.
Larger body size generally confers several competitive advantages such as higher
adult fecundity (Honěk 1993) but also produces evolutionary conflicts like those
derived from the consequent greater resource requirements (Espelta et al. 2009, Bonal &
Muñoz 2009). In the general case in fact, when the favourable season is long enough, an
extra generation can appear only after an LDT reduction has been selected, and there is
some experimental evidence of a correlated reduction in body size in such shifts in
voltinism (Nylin & Gothard 1998). So far, the coexistence of ISP species that share the
same host plant has been mainly explained through niche partitioning based on
ecological constraints imposed by seed and insect sizes (e.g. resource availability vs.
resource requirements) (Espelta et al. 2009, Bonal et al. 2011). However our results
might expand this perspective and suggest that the interplay between ecological
interactions (e.g. frugivore intra-guild predation) and evolutionary processes resulting in
variations on ISP life-history traits and strategies may drive niche partitioning (Bonsall
et al. 2004) thus allowing multi-species coexistence within the same ecological guild.
References
Bonal, R., Espelta, J.M., & Vogler, A.P. (2011) Complex selection on life-history traits and the
maintenance of variation in exaggerated rostrum length in acorn weevils. Oecologia, 167, 1-9.
Bonal, R. & Muñoz, A. (2007) Multi-trophic effects of ungulate intraguild predation on acorn weevils.
Oecologia, 152, 533-540.
Bonal, R. & Muñoz, A. (2009) Seed weevils living on the edge: pressures and conflicts over body size in
the endoparasitic Curculio larvae. Ecological Entomology, 34, 304-309.
Bonsall, M.B., Jansen, V.A.A., & Hassell, M.P. (2004) Life history trade-offs assemble ecological guilds.
Science, 306, 111-114.
Cabin, R.J., Weller, S.G., Lorence, D.H., Flynn, T.W., Sakai, A.K., Sandquist, D., & Hadway, L.J. (2000)
Effects of long-term ungulate exclusion and recent alien species control on the preservation and
restoration of a Hawaiian tropical dry forest. Conservation Biology, 14, 439-453.
Espelta, J.M., Bonal, R., & Sánchez-Humanes, B. (2009) Pre-dispersal acorn predation in mixed oak
forests: interspecific differences are driven by the interplay among seed phenology, seed size and
predator size. Journal of Ecology, 97, 1416-1423.
Gómez, J.M. & González-Megías, A. (2002) Asymmetrical interactions between ungulates and
phytophagous insects: being different matters. Ecology, 83, 203-211.
González-Megías, A., Gómez, J.M., & Sánchez-Piñero, F. (2004) Effects of ungulates on epigeal
arthropods in Sierra Nevada National Park (southeast Spain). Biodiversity and Conservation, 13,
733-752.
Hauser, T.P. (1994) Germination, predation and dispersal of Acacia albida seeds. Oikos, 70, 421-426.
Herrera, C.M. (1984) Avian interference of insect frugivory: an exploration into the plant-bird-fruit pest
evolutionary triad. Oikos, 42, 203-210.
Herrera, C.M. (1989) Vertebrate frugivores and their interaction with invertebrate fruit predators:
supporting evidence from a Costa Rican dry forest. Oikos, 54, 185-188.
Honěk, A. (1993) Intraspecific variation in body size and fecundity in insects: a general relationship.
Oikos, 66, 483-492.
Janzen, D.H. (1971) Escape of Cassia grandis L. beans from predators in time and space. Ecology, 52,
964-979.
Janzen, D.H. (1980) Specificity of seed-attacking beetles in a Costa Rican deciduous forest. Journal of
Ecology, 68, 929-952.
Janzen, D.H. (1982) Natural history of guacimo fruits (Sterculiaceae: Guazuma ulmifolia) with respect to
consumption by large mammals. American Journal of Botany, 69, 1240-1250.
Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science,
215, 19-27.
Johnson, C.D. & Kingsolver, J.M. (1971) Descriptions, life histories, and ecology of two new species of
Bruchidae infesting guacima in Mexico. Journal of the Kansas Entomological Society, 44, 141-
152.
Nylin, S. & Gotthard, K. (1998) Plasticity in life-history traits. Annual Review of Entomology, 43, 63-83.
Sallabanks, R. & Courtney, S.P. (1992) Frugivory, seed predation, and insect-vertebrate interactions.
Annual Review of Entomology, 37, 377-400.
Tarrasón, D., Urrutia, J.T., Ravera, F., Herrera, E., Andrés, P., & Espelta, J.M. (2010) Conservation status
of tropical dry forest remnants in Nicaragua: Do ecological indicators and social perception tally?
Biodiversity and Conservation, 19, 813-827.
Traveset, A. (1992) Effect of vertebrate frugivores on bruchid beetles that prey on Acacia farnesiana
seeds. Oikos, 63, 200-206.
(a)
(b)
∼1 cm
∼1 cm
Figure 1. Insect seed predators of: (a) Acacia pennatula: Mimosestes humeralis (length,
i.e. pronotum-elytra, 3.6–6.0 mm) and M. anomalus (length, 3.0–3.6 mm); (b) Guazuma
ulmifolia: the larger Amblycerus cistelinus (length, 7.0–8.5 mm) and the smaller
Acanthoscelides guazumae (length, 1.7–2.2 mm). Notice the similar range of body size
of the species preying upon Acacia pennatula and the differences between those preying
upon Guazuma ulmifolia.
M. humeralis(a) M. anomalus
A. cistelinus(b) A. guazumae
M. humeralis(a) M. anomalus
A. cistelinus(b) A. guazumaeA. cistelinus(b) A. guazumae
Figure 2. Differences between sites (with and without cattle) on the relative abundances
of the corresponding guilds of insect seed predators at tree level (n=40). Numbers inside
columns indicate the absolute number of adults collected from each species. Significant
differences between sites were only found within the guild of Guazuma ulmifolia both
in relative proportions and number of adults collected.
Capítulo5
Una oportunidad o una barrera –
Inhibición o facilitación del establecimiento de
plántulas
Resumen
Se ha sugerido que la sucesión secundaria del bosque tropical seco tras el abandono de
tierras se ve favorecida por la facilitación al establecimiento de plántulas ejercida por
las especies pioneras. No obstante, algunas de estas especies pioneras pueden a veces
actuar como invasores de pastos bloqueando la sucesión por varias décadas.
Investigamos mediante ensayos de laboratorio y experimentos de campo si la alelopatía
puede jugar un papel en la detención de la sucesión al limitar el establecimiento de
plántulas de especies de árboles bajo la copa de Acacia pennatula. Los extractos de las
hojas de A. pennatula no afectaron la germinación pero redujeron el crecimiento de las
plántulas y especialmente el desarrollo de sus raíces, modificando su modelo de
asignación de biomasa hacia una reducción de la relación raíz/tallo. La supervivencia de
las plántulas fue un 20-30% menor bajo la copa de A. pennatula. Esta reducción de la
supervivencia fue particularmente pronunciada a medida que la estación seca avanzó a
pesar de las condiciones más favorables (por ejemplo, mayor humedad del suelo)
encontradas en las posiciones interiores bajo la copa. En conjunto nuestros resultados
sugieren que en lugar de facilitar, A. pennatula puede inhibir el establecimiento de
plántulas bajo su copa probablemente por medio de una interferencia alelopática en el
desarrollo del sistema radical con consecuencias negativas críticas para la supervivencia
de las plántulas durante la estación seca. Esta contribución previene acerca de
sobreestimar el efecto nucleador que los árboles aislados pueden tener a fin de facilitar
la sucesión secundaria en los altamente perturbados sistemas silvopastoriles procedentes
del bosque tropical seco.
Chapter5
An opportunity or a barrier ‐ Inhibition or facilitation of
seedling establishment
Abstract
Secondary succession after land abandonment in tropical dry forests has been suggested
to be favoured by the facilitation effects for seedling establishment exerted by pioneer
trees isolated in these savannah-like landscapes. However, it has also been noticed that
these pioneer species may sometimes have an encroaching effect and arrest succession
for several decades. We investigated whether allelopathy can play a role in limiting
seedling establishment of co-occurring tree species under the canopy of Acacia
pennatula by means of lab bioassays and field experiments in north-west Nicaragua.
Leaf extracts of A. pennatula did not affect seed germination but reduced the general
growth and especially the development of the root compartment in seedlings, shifting
their biomass allocation model to a reduced root/shoot ratio. Survival of planted
seedlings under the canopy of A. pennatula was about 20-30% lower than outside, and
this reduction was particularly pronounced as the dry season progressed, despite the
milder conditions (e.g. higher soil moisture) experienced in the inner positions under the
canopy. Altogether, our results suggest that, rather than facilitating, A. pennatula may
inhibit the establishment of seedlings under its canopy probably by means of an
allelopathic interference in the development of the root system with critical negative
consequences for young seedlings in terms of overcoming the dry season. This
contribution warns about overemphasizing the nucleation effect that remnant and
isolated trees may have in order to facilitate secondary succession in these highly
disturbed savannah-like tropical dry forests.
Introduction
Tropical dry forests (TDF) have been extensively disturbed and are considered to be one
of the most threatened ecosystems worldwide (Janzen 1988). Specifically in
Mesoamerica, undisturbed dry forests now account for less than 2% of their original
surface (Olson & Dinerstein 2002) and most areas have changed into savannah-like
landscapes where a reduced group of early-successional tree species dominates (usually
Acacia and Mimosa spp.: see Burgos & Mass 2004, Álvarez-Yépiz et al. 2008). In this
ecological scenario pioneer species may act as successional nuclei, i.e. recruitment foci
for other plant species (Yarranton & Morrison 1974, Slocum 2001). Positive effects of
pioneer trees could start with an increased likelihood of seed dispersal of other species
under their canopies owing to their role as perching sites for birds and bats (Guevara et
al. 1986, Holl et al. 2000). In addition, other facilitating effects that would enhance
establishment success under tree canopies compared to open conditions may include: i)
improved water relations from a lower transpiration demand along with higher soil
moisture (Holmgren et al. 1997, Holmgren 2000), ii) shelter against extreme
temperatures (Nobel 1989), iii) better nutrient conditions from higher litter deposition
and mineralization rates (Callaway et al. 1991, Belsky 1994) and iv) protection against
herbivory (McAuliffe 1986, García & Obeso 2003).
Accordingly, secondary succession in TDF may depend largely on the
facilitation effects exerted by pioneer trees isolated in pastures (Slocum 2001). However
after land abandonment, the forest community composition is often dominated by a few
long-lived pioneer species resulting in very slow or non-existent structural and
compositional change for several decades (Chazdon 2008). Indeed, facilitation and
interference may act simultaneously in the field (Callaway & Walker 1997, Maestre et
al. 2003) and recruitment limitation can appear if direct competition for resources
between trees and young seedlings surpasses the abovementioned benefits (Putz &
Canham 1992, Holl 1998) or if the release of allelopathic substances occurs (Nilsson
1994, Ridenour & Callaway 2001). Whereas the role of direct competition (e.g. light,
water, nutrients) has been thoroughly explored and considered as a potential constraint
to succession in tropical forests (Peterson & Carson 2008), so far, the importance of
allelopathy has barely been suggested (Holl 1998). Thus, investigating whether pioneer
trees may inhibit rather than facilitate seedling establishment by means of an
allelopathic interference is a key point to understand the successional dynamics of
tropical forests.
Allelochemicals are released by plants through leaching, volatilization, root
exudation or litter incorporation into soil (Reigosa et al. 1999, Inderjit & Duke 2003)
and can interfere with several plant target processes (e.g. cell division, nutrient uptake,
stomatal conductance). Although these effects may vary depending on the identity of
the species occurring on the understory (Lorenzo et al. 2011), the overall effect usually
results in the delay and reduction of germination (Chou et al. 1998, Escudero et al.
2000) and also in constraints to seedling establishment (Orr et al. 2005) mainly through
reductions in root system development (Bais et al. 2003). Therefore, allelopathy has
been suggested to play a key role in community assemblage as well as species
replacement during succession (Hilhorst & Karssen 2000).
Hence, the main aim of the present study was to explore whether allelopathic
interference may exceed facilitation for the establishment of seedlings under the canopy
of pioneer species in secondary TDF. To achieve this objective we selected the dry-
tropical pioneer tree Acacia pennatula Benth. as a case study because it is a common
and dominant tree in disturbed areas and secondary TDF remnants from Mesoamerica
down to Ecuador (Ebinger et al. 2000, Tarrasón et al. 2010). Acacia sensu lato is a large
circumtropical genus with several species playing a dominant role in natural or
anthropogenic savannahs and providing important ecological and socio-economical key
functions (Purata et al. 1999, Munzbergova & Ward 2002). In Mesoamerica, the
abandonment of pastures and wooded rangelands usually leads to secondary forests
widely dominated by pioneer Acacia species that persist as almost mono-specific stands
for several decades (Álvarez-Yépiz 2008, Burgos & Mass 2004). Interestingly, several
species in this genus have provided examples of phytotoxic activity in leaves, flowers
and root extracts (González et al. 1995, Chou et al. 1998, Lorenzo et al. 2011), which
could partially explain this ability to arrest succession. Yet whether this effect exceeds
the benefits that seedlings may encounter under the canopy of isolated trees
(facilitation) has seldom been explored. To test the phytotoxic activity of A. pennatula,
we first performed a bioassay with aqueous extracts of leaves on seed germination and
early seedling growth. Second, we carried out a field experiment where we planted and
compared the success of germination and seedling survival in various positions under
the canopy of A. pennatula and outside. We hypothesize that, if A. pennatula has
allelopathic potential, it must decrease germination and seedling growth (lab
experiments) and the likelihood of germination and survival of seedlings planted under
the tree canopy. The results obtained can improve our understanding of the the potential
role that allelopathy may play in the successional dynamics in dry tropical forests.
Materials and methods
Study site and species
This study was conducted in the CIEA-El Limón a research field-station of the National
Autonomous University of Nicaragua-Managua (FAREM-UNAN/Managua) located at
a height of 890 m in Estelí (North-West Nicaragua 13.3676ºN 86.21967ºW). Mean
monthly temperature ranges from 16 to 33ºC and mean annual rainfall is 804 mm year-1,
with approximately 90% falling from May to November (INETER, data for the 1983-
2009 period). Forested areas in the field-station are predominated by sparse Acacia
pennatula Benth. (Fabaceae) trees in a savannah-like landscape typical of once
disturbed TDF in Mesoamerica. This species has traditionally been favoured by local
land-owners due to its protein-rich pods that are foraged by domestic livestock during
the dry season (Purata et al. 1999, Casasola 2000). When grazing and other management
pressures cease, A. pennatula seedlings and saplings rapidly grow and encroach on
pastures, leading to low diversity stands in which apparently no succession takes place
(G. Peguero personal observation in the study area; for a similar result with A.
cochliacantha see Álvarez-Yépiz et al. 2008).
To test whether A. pennatula trees may facilitate or inhibit the establishment of
other tree species under its canopy, we selected three native and common species that
are also present in these secondary TDF areas: Guazuma ulmifolia Lam. (Sterculiaceae),
Enterolobium cyclocarpum Griseb. (Fabaceae) and Cedrela odorata L. (Meliaceae).
These species were selected not only for their commonness both in secondary and
mature forests but also because they reflect contrasting characteristics in seed size,
dormancy and degree of protection found in tree species in dry tropical areas. G.
ulmifolia and E. cyclocarpum have hard-coated seeds and dormancy, yet they present
very different seed sizes (0.004 - 0.01 g seed-1 and 0.83 - 1.11 g seed-1 respectively). In
contrast, C. odorata has no dormancy and an intermediate seed size (0.017 - 0.025 g
seed-1).
Laboratory bioassay
In order to test whether chemical compounds in leaves of A. pennatula may have
phytotoxic activity on the germination response and early seedling growth of co-
occurring tree species, we designed a laboratory bioassay. These trials were conducted
only with C. odorata seeds because they do not have dormancy and germination takes
only 6 or 7 days in non-limiting water conditions (Baskin and Baskin 2001).
During the dry season of 2009, A. pennatula leaves were randomly collected
from trees growing in the field-station and taken to the lab where we obtained an
aqueous extract after incubating 1000 g of slightly trimmed fresh leaves in 3 L. of
distilled water (48 hours at 235ºC, see Escudero et al. 2000 for a similar extraction
method). The solution obtained was filtered with cheesecloth and diluted by adding
distilled water as required to produce treatment solutions of: 50, 25, 16, 8 and 4 percent
of the stock solution (see Escudero et al. 2000 for similar concentrations). The electrical
conductivity of the aqueous extracts was measured in order to assess for potential
osmotic effects which may be confused with phytotoxic activity. Electrical conductivity
of the treatment solutions 50, 25, 16, 8 and 4 percent were 1.9 dS m-1, 1.33 dS m-1, 1.12
dS m-1, 1.01 dS m-1 and 0.56 dS m-1 respectively. Since Escudero et al. (2000) did not
find osmotic effects within the same range of electrical conductivities, all lab trials were
conducted using only distilled water as control treatment.
For the assay on germination response, each treatment solution was applied to
ten replicates of 15 seeds of C. odorata. Each replicate consisted of a 7-cm Petri dish
where seeds were laid on a paper watered with 2 ml of the treatment dilution and set to
germinate in lab conditions (8 days, 235ºC, 12-hr photoperiod of natural light). In
order to ensure non-limiting water conditions we added 2 ml of the corresponding
dilution to each Petri dish on the third and sixth days. Germination success (i.e. radicle
emerging from testa) was recorded daily and was used to calculate the days required to
attain the 50% of the seeds germinated (henceforth “G50”) and the final germination
percentage. At the end of this germination experiment we randomly selected 50
germinated seeds from each treatment, which were sown in culture pots with a general
purpose growing medium (Pro-Mix PGX®/Premier Tech Ltd.). The pots were watered
regularly with 3 ml of the corresponding treatment solution every 48-hr for 15 days. At
the end of this period, the fresh mass of leaves, stems, and roots of all plants were
weighted separately and then all samples were oven-dried (60ºC/48h) in order to obtain
the corresponding dry mass which allowed us to calculate the relative weight ratio of
leaves (LWR), stems (SWR) and roots (RWR) of each seedling.
Field experiments
In order to test whether A. pennatula trees interfere with or facilitate the germination
and establishment of co-occurring tree species in natural conditions, we designed an
experiment in El Limon field-station. We randomly selected 31 isolated A. pennatula
trees and defined 4 positions from the trunk to outside of the canopy, trying to mimic
the natural gradient of light availability, soil moisture and accumulation of
allelochemicals by litter decomposition and/or leachates. So we established three
microsites under the canopy, namely, near the trunk (about to 0.3m), in the middle and
at the edge of the crown (henceforth referred to as Trunk, Crown and Edge), and finally
a control position was set outside of the crown (Outside). The rationale of this
experiment is that if the crown of A. pennatula provides shelter for the germination and
establishment of young seedlings especially helping them to cope with the harsh
environmental conditions occurring during the dry season (facilitation effect), we would
expect higher survival in the inner positions with respect to the edge or outside of the
canopy. On the other hand, if the leaves of A. pennatula have a relevant phytotoxic
activity (interference effect) we would expect survival to be higher in these positions
where accumulation of allelochemicals is lower (on the edge or outside of the canopy).
To test for these potential effects on seed germination, we buried a wire mesh
bag with 10 seeds of C. odorata in each of the abovementioned positions under 10 of
the randomly selected trees. Seeding was repeated twice, at the beginning and end of the
wet season in 2009, to test for the potential interaction of the effects of position under
the canopy of A. pennatula trees and the accumulation of allelochemicals (e.g. due to
higher litter deposition during the dry season). The number of germinated seeds was
checked after eight days. A second field experiment was also conducted with seedlings
of C. odorata, G. ulmifolia and E. cyclocarpum previously grown in culture trays in a
general purpose growing medium (Pro-Mix PGX®/Premier Tech Ltd.). At the end of
the wet season (October 2009), when seedlings had their first pair of true leaves they
were transplanted following the abovementioned positional scheme under the 31
randomly selected trees. In order to preclude above-ground competition, the understory
vegetation was completely removed as well as the grass cover in the ‘Outside’ position.
Seedling survival was monitored twice: after 2 and 4 months following transplant
(December 2009 and February 2010), to check for the influence of environmental
conditions (i.e. increasing drought as the dry season progressed).
To characterize light availability and soil moisture in the different microsites
where seedlings were planted, we measured the photosynthetically active radiation
(PAR) available at seedling level with a ceptometer (Decagon Devices, AccuPAR LP-
80®) and we gravimetrically measured the water content in a sample of topsoil (i.e. 20
cm deep) in each planting position of the 31 selected trees at the end of the experiment
(February 2010). Despite the fact that A. pennatula is partially deciduous and so light
limitation can be underestimated, it is at this time of the season when seedlings face
higher water shortage.
Data analysis
To test the effects of the different aqueous extracts of A. pennatula leaves in the
germination of C. odorata seeds, we used generalized linear models (GENMOD
procedure; SAS Institute) with a Poisson error distribution and a log link function and
including treatment dilution as a fixed factor and G50 and the total number of seeds
germinated as the dependent variables. Seedling growth and biomass allocation data
were analysed by means of univariate ANOVA tests (Statistica 6.0 software; StatSoft
Inc.). In these latter analyses, dependent variables were log-transformed, when
necessary, to meet the assumption of normality.
Differences in the germination success and seedling survival in the different
positions under the canopy of A. pennatula trees were analysed by means of generalized
linear mixed models (GLIMMIX procedure; SAS Institute) with a Poisson error
distribution and a log link function including: i) position (Trunk, Middle, Edge,
Outside) as a fixed factor, ii) season as fixed factor, iii) tree as a random factor and for
the analysis of seedling survival species (G. ulmifolia, E. cyclocarpum, C. odorata) as a
fixed factor. Finally, the data of PAR at the seedling level and topsoil water content
were log-transformed and analysed by means of a general linear mixed model including
position as fixed effect and tree as random (Statistica 6.0 software; StatSoft Inc.).
Results
Germination
In the lab experiment, the concentration of the A. pennatula leaf aqueous extract did not
affect the total germination of C. odorata seeds (df = 7, 72; Chi-square = 5.6; P = 0.58);
neither did the number of days needed to achieve 50% of total germination (df = 7, 72;
Chi-square = 5.2; P = 0.64). Across treatments, the final percentage of germination was
on average 95.3% ( 0.1 SE) and G50 was 5.4 ( 0.08 SE) days. Similarly, in the field
experiment, the number of germinated seeds was not affected by the relative position
where they were sown under the crown of A. pennatula trees (df = 3, 62; F = 1.9; P =
0.14). In this experiment, germination differences were only observed between the two
sowing dates (df = 1, 62; F = 16.5; P < 0.0001), i.e. more seeds germinated at the
beginning of the wet season than at the end (90 4% vs. 64 4%; Mean SE).
Seedling growth and survival
Despite the general lack of effects on germination, there were significant effects of A.
pennatula on growth and survival (Figure 1). Specifically, the extracts of A. pennatula
leaves had significant effects on the growth (total dry biomass) achieved by C. odorata
seedlings grown in the lab (df = 5, 293; F = 34.4; P < 0.0001). Total biomass of
seedlings was negatively related to the concentration of the aqueous extract, this
inhibitory effect being significant from the 8% treatment solution onwards. Considering
the root, stem and leaf compartments of seedlings, reduction of biomass accumulation
was especially relevant at the root level (df = 5, 293; F = 52.1; P < 0.0001) and also
significant at the stem level (df = 5, 293; F = 2.6; P < 0.05) whereas the leaf biomass
was similar between treatments (df = 5, 293; F = 0.8; P = 0.82). Consequently these
effects resulted in a strikingly different biomass allocation pattern of seedlings watered
with the different concentration of A. pennatula leaf extracts (RWR: df = 5, 293; F = 50;
P < 0.0001, SWR: df = 5, 293; F = 21.9; P < 0.0001 and LWR: df = 5, 293; F = 25; P <
0.0001). As Figure 2 shows, as the concentration of A. pennatula leaves extracts
increased, the seedlings exhibited lower RWR and higher SWR and LWR.
Concerning the field experiment, the statistical analysis revealed that for the
three species tested (G. ulmifolia, E. cyclocarpum, C. odorata) seedling mortality was
significantly higher under the canopy than outside (Time × Position: df = 3, 591; F =
2.8; P = 0.0421). Particularly during the middle of the dry season, when appeared a
clear gradient of increasing mortality from outside the canopy towards inner positions
(Figure 3). Also at this time and irrespective of the position in which the seedlings were
planted, appeared differences of mortality among the three species (Time × Species: df
= 2, 591; F = 3.8; P = 0.0233). Thereby, the seedlings of the large-seeded E.
cyclocarpum exhibited higher survival probability (0.5 0.05b vs. C. odorata 0.2
0.04a and G. ulmifolia 0.3 0.05a; Mean SE, different letters indicate significant
differences according to LS Means tests). As expected, soil water content and PAR
were significantly different depending on the position under the crown (respectively, df
= 3, 60; F = 6.6; P < 0.001 and df = 3, 120; F = 18.2; P < 0.0001). Soil water content
was remarkably lower outside of the canopy whereas the canopy PAR interception was
greater when closer to the trunk (Table 1).
Discussion
The results of our study suggest that isolated A. pennatula trees in savannah-like
tropical dry forests may inhibit rather than facilitate the establishment of other tree
species under their canopy through the release of allelopathic substances. Indeed, in
some semi-arid neotropical areas specific examples have been described of how after
the abandonment of croplands and rangelands there is usually a several decades phase
(sometimes more than 50 years) of secondary forests almost dominated by a single
leguminous species, usually belonging to Acacia or Mimosa genus (Burgos & Maass
2004, Romero-Duque et al. 2007, Álvarez-Yépiz et al. 2008, Lebrija-Trejos et al. 2008).
In addition, the combination of the results obtained in the lab and in the field suggest
that the phytotoxic effect of A. pennatula occurs mostly during the phase of seedling
establishment - rather than during germination - and it may be related to inducing a
biomass partitioning in the seedlings (i.e. lower RWR) unfavourable to face the severe
water shortage during the dry season.
In contrast to several studies that reported phytotoxic effects of Acacia species
on germination (González et al. 1995, Chou et al. 1998), the aqueous extracts of A.
pennatula leaves did not reduce or delay germination in C. odorata and the values
observed in the lab experiment were high and similar to those previously reported in
non-limiting water conditions (Baskin & Baskin 2001). This lack of differences between
treatments in both total germination percentage and in G50 excludes an osmotic effect
of the treatment dilutions. In fact, the electrical conductivities of the dilutions used in
our experiment were within the range tested by Escudero et al. (2000) in which these
authors did not find osmotic effects. Conversely to the lack of effects on germination,
the strong inhibitory effect observed on the early growth of C. odorata seedlings (Figure
1) suggests the presence of some water-soluble phytotoxic compounds in the treatment
solutions, active even at low concentrations. Interestingly, this inhibition produced an
imbalance in the biomass allocation among organs within seedlings (Figure 2) and
resulted in an undersized root compartment (see similar results in Bais et al. 2003, Orr
et al. 2005). This particular biomass allocation pattern may present an important
constraint when seedlings have to face severe water stress during the drought season
(for the negative effects of reduced RWR on overcoming water stress conditions, see
Espelta et al. 2005). Indeed, in our field experiment we found that seedling mortality
increased as the dry season progressed and there were species specific differences: i.e.
the larger-seeded species E. cyclocarpum showed a higher survival than C. odorata and
G. ulmifolia (see Moles & Westoby 2004, for a review on the relationship between seed
size and seedling performance). Concerning the potential substances reducing RWR,
recently Rios (2005) carried out an exhaustive analysis of the secondary metabolites
present in the leaves of A. pennatula and found considerable amounts of several
substances with reported allelopathic properties: lupenone and lupeol (see Macías-
Rubalcava 2007), daphnetin (see Schulz & Friebe 1999 in Inderjit & Duke 2003) and
especially catechin whose action as a suppressor of root growth has been thoroughly
described (Bais et al. 2003). This allelopathic potential of A. pennatula could be
analogous to other congeners with similar chemical profiles and described allelopathic
mechanisms (e.g. A. dealbata; Lorenzo et al. 2011).
The reported inhibitory effect of A. pennatula leaves in root growth and the
resulting imbalance in the root/shoot ratio of seedlings (Figure 2) may contribute to an
understanding of the pattern of seedling mortality observed in our field experiment.
Interestingly, in the three species mortality was more pronounced under the canopy of
A. pennatula closer to the trunk than outside the canopy, and this effect increased as the
dry season progressed (Figure 3). This suggests that seedlings grown under the canopy
may have experienced an unfavourable biomass partitioning among organs in order to
overcome water stress (e.g. reduced root/shoot ratio). Certainly this imbalance could
also be caused by a lower PAR availability under the canopy of A. pennatula (see
Holmgren et al. 1997 for a discussion on the trade-off between acclimation to shade and
to drought). However, it must be noticed that values of PAR recorded under the canopy
of A. pennatula trees in our study were much higher than light compensation points
reported for many tropical tree species (Larcher 2003), which suggests that seedlings
did not experience severe light limitation even when the canopy is full-leaved.
Moreover, in dry ecosystems the establishment of seedlings has often been reported to
be mostly restricted to shady sites (Guevara et al. 1992, Gerhardt 1996, Jurado et al.
2006). This ‘nurse effect’ occurs because the improvement of plant water status (i.e.
lower transpiration demands and enhanced soil moisture) under the canopy exceeds the
costs caused by lower light levels (Holmgren et al. 1997). All things considered, we
suggest that the presence of allelopathic substances in the litter under the canopy of A.
pennatula and their effect on preventing the proper development of roots and the
balance in resource allocation could worsen the seedlings’ vulnerability to water stress,
ultimately shifting the net effect of the canopy shelter from facilitative to competitive.
Furthermore, the observed pattern in which establishment conditions seem to worsen
almost linearly with the proximity to the trunk also suggests that leaching could be a
mode of release for allelochemicals, compatible with litter decomposition. Both
liberation methods have been previously suggested for Acacia species (Chou et al. 1998,
González et al. 1995, Lorenzo et al. 2011), and leaching especially is supposed to
produce such a gradient of decreasing concentrations from the base of the trunk to the
edge of the crown. Nonetheless, we must acknowledge that further research is needed in
order to detect effective concentrations of such allelopathic substances (e.g. lupenone,
lupeol, daphnetin or catechin) in the soil so as to investigate where the allelochemicals
are coming from (litter decomposition, leaching or root exudation).
Finally, if the ecological challenge is to manage pastures and secondary TDF in
order to achieve a composition of species and a structure similar to original forests,
research efforts must be made in order to find how to overcome successional barriers
(Aide et al. 2000). The lack of seed dispersal, germination, seedling resource
competition and herbivory have been described as major barriers to succession in TDF
(Holl et al. 2000). However our results warn that, in addition to the former constraints,
allelopathic interference may sometimes also play a role in shifting establishment
facilitation into interference and ultimately arresting succession. To the extent that tree
species differ in their ‘nursing’ ability, the early succession patterns may largely rely on
the kind of remnant tree species present in these pastures (Slocum 2001). Therefore, the
selection of a more passive or active restoration strategy may depend on the
composition of this initial community of isolated pioneer trees and its capacity to
nucleate succession or to arrest it through allelopathy (Holl & Aide 2011).
References
Aide T.M., Zimmerman J.K., Pascarella J.B., Rivera L. & Marcano-Vega H. (2000) Forest regeneration
in a chronosequence of tropical abandoned pastures: implications for restoration ecology.
Restoration Ecology 8, 328-338
Álvarez-Yépiz J.C., Martínez-Yrízar A., Búrquez A. & Lindquist C. (2008) Variation in vegetation
structure and soil properties related to land use history of old-growth and secondary tropical dry
forests in northwestern Mexico. Forest Ecology and Management 256, 355-366
Bais H.P., Vepachedu R., Gilroy S., Callaway R.M. & Vivanco J.M. (2003) Allelopathy and exotic plant
invasion: from molecules and genes to species interactions. Science 301:1377.
Baskin C.C. & Baskin J.M. (2001) Seeds: ecology, biogeography, and evolution of dormancy and
germination. Academic Press, USA
Belsky A.J. (1994) Influences of trees on savanna productivity: tests of shade, nutrients, and tree-grass
competition. Ecology 75, 922-932.
Burgos A., Maass J.M. (2004) Vegetation change associated with land-use in tropical dry forest areas of
Western Mexico. Agriculture, Ecosystems and Environment 104, 475-481
Callaway R.M., Nadkarni N.M., Mahall B.E. (1991) Facilitation and interference of Quercus douglasii on
understory productivity in central California. Ecology 72, 1484-1499.
Callaway R.M. & Walker L.R. (1997) Competition and facilitation: a synthetic approach to interactions in
plant communities. Ecology 78, 1958-1965.
Casasola F. (2000) Productividad de los sistemas silvopastoriles tradicionales en Moropotente, Estelí,
Nicaragua. CATIE, Turrialba, CR.
Chazdon R.L. (2008) Chance and determinism in tropical forest succession. In: Carson WP, Schnitzer SA
(eds) Tropical forest community ecology. Wiley-Blackwell, UK, pp. 384–408
Chou C.H., Fu C.Y., Li S.Y. & Wang Y.F. (1998) Allelopathic potential of Acacia confusa and related
species in Taiwan. Journal of Chemical Ecology 24, 2131-2150.
Ebinger J.E., Seigler D.S. & Clarke H.D. (2000) Taxonomic revision of South American species of the
genus Acacia subgenus Acacia (Fabaceae: Mimosoideae). Systematic Botany 25, 588-617.
Escudero A., Albert M.J., Pita J.M. & Pérez-García F. (2000) Inhibitory effects of Artemisia herba-alba
on the germination of the gypsophyte Helianthemum squamatum. Plant Ecology 148, 71-80.
Espelta J.M., Cortés P., Mangirón M., Retana J. (2005) Differences in biomass partitioning, leaf nitrogen
content, and water use efficiency (δ13C) result in similar performance of seedlings of two
Mediterranean oaks with contrasting leaf habit. Ecoscience 12, 447-454.
García D., Obeso J.R. (2003) Facilitation by herbivore mediated nurse plants in a threatened tree, Taxus
baccata: local effects and landscape level consistency. Ecography 26, 739-750.
Gerhardt K. (1996) Effects of root competition and canopy openness on survival and growth of tree
seedlings in a tropical seasonal dry forest. Forest Ecology and Management 82, 33-48.
González L., Souto X.C. & Reigosa M.J. (1995) Allelopathic effects of Acacia melanoxylon R. Br.
phyllodes during their decomposition. Forest Ecology and Management 77, 53-63.
Guevara S., Meave J., Moreno-Casasola P. & Laborde J. (1992) Floristic composition and structure of
vegetation under isolated trees in neotropical pastures. Journal of Vegetation Science 3, 655-664.
Guevara S., Purata S.E. & Maarel E. (1986) The role of remnant forest trees in tropical secondary
succession. Plant Ecology 66, 77-84.
Hilhorst H.W.M. & Karssen C.M. (2000) Effect of chemical environment on seed germination. In: Fenner
M (ed) Seeds: The ecology of regeneration in plant communities. CABI, New York, pp. 293–309
Holl K.D. (1998) Effects of above-and below-ground competition of shrubs and grass on Calophyllum
brasiliense (Camb.) seedling growth in abandoned tropical pasture. Forest Ecology and
Management 109, 187-195.
Holl K.D., Aide T.M. (2011) When and where to actively restore ecosystems? Forest Ecology and
Management 261, 1558–1563.
Holl K.D., Loik M.E., Lin E.H.V., Samuels I.A. (2000) Tropical montane forest restoration in Costa Rica:
overcoming barriers to dispersal and establishment. Restoration Ecology 8, 339-349.
Holmgren M. (2000) Combined effects of shade and drought on tulip poplar seedlings: trade-off in
tolerance or facilitation? Oikos 90, 67-78.
Holmgren M., Scheffer M. & Huston M.A. (1997) The interplay of facilitation and competition in plant
communities. Ecology 78,1966-1975.
Inderjit & Duke S.O. (2003) Ecophysiological aspects of allelopathy. Planta 217, 529-539.
Janzen D.H. (1988) Management of habitat fragments in a tropical dry forest: growth. Annals of Missouri
Botanical Garden 75,105-116.
Jurado E., Garcia J.F., Flores J. & Estrada E. (2006) Leguminous seedling establishment in Tamaulipan
thornscrub of northeastern Mexico. Forest Ecology and Management 221,133-139.
Larcher W. (2003) Physiological plant ecology: ecophysiology and stress physiology of functional
groups. Springer-Verlag, Berlin
Lebrija-Trejos E., Bongers F., Pérez-García E.A. & Meave J.A. (2008) Successional change and
resilience of a very dry tropical deciduous forest following shifting agriculture. Biotropica 40,
422-431.
Lorenzo P., Palomera-Pérez A., Reigosa M.J. & González L. (2011) Allelopathic interference of invasive
Acacia dealbata Link on the physiological parameters of native understory species. Plant
Ecology 212, 403-412.
Macías-Rubalcava M.L., Hernández-Bautista B.E., Jiménez-Estrada M., Cruz-Ortega R. & Anaya A.L.
(2007) Pentacyclic triterpenes with selective bioactivity from Sebastiania adenophora leaves,
Euphorbiaceae. Journal of Chemical Ecology 33, 147-156.
Maestre F.T., Bautista S. & Cortina J. (2003) Positive, negative, and net effects in grass-shrub
interactions in Mediterranean semiarid grasslands. Ecology 84, 3186-3197.
McAuliffe J.R. (1986) Herbivore-Limited Establishment of a Sonoran Desert Tree, Cercidium
microphyllum. Ecology 67, 276-280.
Moles A.T., Westoby M. (2004) Seedling survival and seed size: a synthesis of the literature. Journal of
Ecology 92, 372-383.
Munzbergova Z. & Ward D. (2002) Acacia trees as keystone species in Negev desert ecosystems. Journal
of Vegetation Science 13, 227-236.
Nilsson M.C. (1994) Separation of allelopathy and resource competition by the boreal dwarf shrub
Empetrum hermaphroditum, Hagerup. Oecologia 98, 1-7.
Nobel P.S. (1989) Temperature, Water Availability, and Nutrient Levels at Various Soil Depths--
Consequences for Shallow-Rooted Desert Succulents, Including Nurse Plant Effects. American
Journal of Botany 76, 1486-1492.
Olson D.M. & Dinerstein E. (2002) The Global 200: Priority ecoregions for global conservation. Annals
of Missouri Botanical Garden 89, 199-224.
Orr S.P., Rudgers J.A. & Clay K. (2005) Invasive plants can inhibit native tree seedlings: testing potential
allelopathic mechanisms. Plant Ecology 181, 153-165.
Peterson C.J. & Carson W.P. (2008) Processes Constraining Woody Species Succession on Abandoned
Pastures in the Tropics: On the Relevance of Temperate Models of Succession. In: Carson WP
and Schnitzer SA (eds) Tropical Forest Community Ecology. Wiley-Blackwell, UK, pp. 367-383
Purata S.E., Greenberg R., Barrientos V., López-Portillo J. (1999) Economic potential of the huizache,
Acacia pennatula (Mimosoideae) in central Veracruz, Mexico. Economic Botany 53, 15-29.
Putz F.E. & Canham C.D. (1992) Mechanisms of arrested succession in shrublands: root and shoot
competition between shrubs and tree seedlings. Forest Ecology and Management 49, 267-275.
Reigosa M.J., Sanchez-Moreiras A. & Gonzalez L. (1999) Ecophysiological approach in allelopathy.
Critical Reviews in Plant Science 18, 577-608.
Ridenour W.M. & Callaway R.M. (2001) The relative importance of allelopathy in interference: the
effects of an invasive weed on a native bunchgrass. Oecologia 126, 444-450.
Rios M.Y. (2005) Terpenes, coumarins, and flavones from Acacia pennatula. Chemistry of Natural
Compounds 41, 297-298.
Romero-Duque L.P., Jaramillo V.J. & Pérez-Jiménez A. (2007) Structure and diversity of secondary
tropical dry forests in Mexico, differing in their prior land-use history. Forest Ecology and
Management 253, 38-47.
Slocum M.G. (2001) How tree species differ as recruitment foci in a tropical pasture. Ecology 82, 2547-
2559.
Tarrasón D., Urrutia J.T., Ravera F., Herrera E., Andrés P. & Espelta J.M. (2010) Conservation status of
tropical dry forest remnants in Nicaragua: Do ecological indicators and social perception tally?
Biodiversity and Conservation 19, 813-827.
Yarranton G.A. & Morrison R.G. (1974) Spatial dynamics of a primary succession: nucleation. Journal of
Ecology 62, 417-428.
0 4 8 16 25 50
Treatment (%)
0.025
0.02
0.015
0.01
0.005
0
Bio
ma
ss (
gr)
a
cc
d
b
a
Figure 1. Effect of treatment solutions of A. pennatula leaves on the early growth of C.
odorata seedlings (Mean ± SE of total dry biomass). Different letters indicate
significant differences according to Fisher-LSD test.
Roots Stems Leaves
Treatment (%)
Re
lativ
e W
eig
ht
1
0.8
0.6
0.4
0.2
0
ab
ccd
d
ea a
bbc
c
daa
bc c
d
0 4 8 16 25 50
Figure 2. Effect of treatment solutions of A. pennatula leaves on the resource allocation
of C. odorata seedlings (mean values for the relative weights of roots, stems and leaves;
SE of each compartment are not shown). Different letters indicate significant
differences among treatment solutions according to Fisher-LSD test.
Sur
viva
l Pro
bab
ility
1
0.8
0.6
0.4
0.2
0
Aa
BaBab
Bb
Bc
AaAa
Ab
Trunk Crown Edge Outside
Figure 3. Seedling survival by position relative to the crown of A. pennatula trees two
and four months after transplant (open and closed blocks respectively). Different letters
indicate significant differences between the two sampling times in the same position
(upper case letters) and between positions within the same sampling time (lower case
letters), according to LS means tests.
Soil Water Content (%) PAR (μmol photons m-2 s-1)
Trunk 6.3 1.1 a 481 32 a
Crown 5.2 0.4 a 637 54 b
Edge 5.0 0.3 a 652 51 b
Out 3.5 0.3 b 892 64 c
Table 1. Differences in Soil Water Content (mean SE) and PAR at seedlings level
(mean SE) among different positions under trees of A. pennatula after four months of
seedling transplant. Different letters indicate significant differences according to Fisher-
LSD test.
Resumen de las conclusiones principales.
Capítulo1.
Rebrota o muere – La presencia inevitable de las perturbaciones repetidas.
• Los individuos de Acacia pennatula que fueron quemados sobrevivieron un
16% menos que aquellos que fueron cortados, mientras que la recuperación de
aquellos individuos perturbados de manera repetida no se vio más afectada
que la de aquellos individuos que fueron perturbados una sola vez. Esto pone
en duda por un lado que esta especie esté específicamente adaptada al fuego y
sin embargo subraya su capacidad para afrontar perturbaciones moderadas
frecuentes.
• El efecto de los tratamientos, tanto el corte como la quema, fueron
especialmente acusados justo después de la estación seca que fue cuando se
alcanzaron mayores mortalidades y una menor capacidad de recuperación
(menor número de rebrotes y menores tasas de crecimiento).
• La capacidad de rebrote tras la estación seca puede estar limitada por una
menor disponibilidad de nitrógeno y particularmente fósforo, tal y como
sugieren los menores valores almacenados en la raíz principal pero no por las
reservas de carbohidratos (almidón).
Capítulo2.
La aptitud frugívora del ganado y la quema de pastos ‐ Los primeros ingredientes
para una receta de éxito.
• El ganado ingirió ávidamente los frutos de las tres especies testadas (Acacia
pennatula, Guazuma ulmifolia, Enterolobium cyclocarpum). No obstante,
atributos específicos como un mayor número de semillas por fruto, convierten
• Las semillas de las tres especies fueron capaces de sobrevivir al paso por el
tracto digestivo el cual no incrementó los porcentajes de germinación. En
cambio el fuego estimuló la germinación especialmente cuando se aplicaron
golpes de calor de más de 90ºC y 6 minutos de exposición. No hubo
interacción entre endozoocória y fuego sobre la respuesta germinativa de las
tres especies testadas.
• El éxito colonizador de las especies testadas puede ser en parte explicado por
la aptitud del ganado para dispersar sus semillas (vector de dispersión), por la
capacidad de éstas para resistir el paso por el tracto digestivo, y por el fuego
que en última instancia es el factor responsable de romper la latencia de las
semillas favoreciendo su germinación
Capítulo3.
Al cerro vengo subiendo… – Depredación de semillas a lo largo de un gradiente
altitudinal.
• A nivel de individuo, cuanto mayor fue la producción de frutos menor fue la
proporción de semillas depredadas, y cuanto mayor fue la tasa de aborto de
semillas en los frutos mayor fue la mortalidad de las larvas de los
depredadores de semillas.
• Tanto el saciado de los insectos depredadores mediante producciones masivas
de frutos como el aumento de la mortalidad de sus larvas relacionado con el
aborto de semillas, actúan simultáneamente como mecanismos de defensa
aunque su contribución relativa varia a lo largo del rango de distribución
altitudinal de A. pennatula: mientras el saciado predomina en las partes
• A nivel de sitio, el número de semillas sanas que escaparon a la depredación
estuvo relacionado con el número de plántulas que encontramos durante la
siguiente estación húmeda lo cual subraya la importancia demográfica que
tienen los mecanismos de defensa de semillas.
Capítulo4.
Demasiados depredadores para una misma semilla – ¿Una coexistencia mediada por
los frugívoros?
• La proporción de semillas depredadas de Acacia pennatula y Guazuma
ulmifolia por parte de sus insectos depredadores especialistas (brúquidos) fue
significativamente mayor en ausencia de ganado, lo cual sugiere que al
alimentarse de sus frutos, las vacas pueden ejercer un cierto control sobre las
poblaciones de depredadores pre-dispersivos de ambas especies y por tanto
disminuir sus tasas de depredación de semillas.
• La especie de brúquido con mayor tiempo de permanencia en el fruto -y de
ciclo de vida univoltino- Amblycerus cistelinus, se vio más afectada por la
presencia de ganado lo cual sugiere que los frugívoros podrían facilitar la
coexistencia de varias especies de depredadores sobre la misma planta
huésped.
Capítulo5.
Una oportunidad o una barrera – Inhibición o facilitación del establecimiento de
plántulas.
• Los extractos acuosos de hojas de Acacia pennatula no disminuyeron la
capacidad de germinación de Cedrela odorata pero si redujeron sensiblemente
• Las plántulas de Cedrela odorata, Guazuma ulmifolia y Enterolobium
cyclocarpum plantadas bajo la copa de individuos de Acacia pennatula
sobrevivieron menos cuanto más cerca del tronco se encontraban y este efecto
fue más acusado a medida que la estación seca avanzó.
• En conjunto estos dos resultados ponen en duda la capacidad de A. pennatula
de nuclear la sucesión secundaria y alertan sobre la posibilidad que esta
especie bloquee la sucesión tras un eventual abandono de los sistemas silvo-
pastoriles en los cuales es dominante.
Retorno a Nicaragua: Implicaciones y perspectivas para la gestión.
Acacia pennatula es a todas luces una especie capaz de colonizar y persistir en los
pastos tras la transformación de los bosques tropicales secos en sistemas silvo-
pastoriles.
Para comprender en que radica esta capacidad, en primer lugar debemos apreciar
su capacidad para superar la barrera que supone la falta de dispersión de semillas en la
matriz paisajística que representa el pasto (capítulo 2). El ganado, atraído por el alto
valor nutritivo de sus frutos, actúa de agente dispersor eficaz de sus semillas durante la
época seca. Las semillas, viables pero mayoritariamente aún latentes tras su paso por el
tracto digestivo, encuentran en la quema de los pastos durante la época seca un factor
idóneo para liberarlas de la latencia impuesta por su cubierta impermeable
permitiéndoles por tanto germinar con las primeras lluvias y así aprovechar al máximo
la época favorable para el establecimiento. Estos atributos son compartidos por un
considerable número de especies forestales características del bosque seco
mesoamericano, las cuales muy probablemente fueron también dispersadas por la mega-
fauna herbívora pleistocénica. Este hecho notable permite al ganado ser actualmente un
eficaz sustituto de aquella fauna ya extinta y por tanto dispersar eficientemente las
semillas de diversas especies forestales, las cuales además tienen un comportamiento
germinativo similar en relación al fuego.
De todo esto se puede colegir que mediante una gestión adecuada, el ganado
gracias a su función dispersora junto con el fuego que estimula la germinación, pueden
promover la regeneración del bosque seco mesoamericano. Para lograr tal objetivo la
dieta del ganado podría enriquecerse con frutos de aquellas especies forestales cuyas
semillas son potencialmente dispersadas por el ganado como por ejemplo: además de las
3 especies aquí testadas como Leucaena sp., Pithecellobium sp. (Fabáceae), Crescentia
sp. (Bignoniaceae), Psidium sp. (Myrtaceae), Byrsonima sp. (Malpighiaceae), Anona sp.
(Annonaceae), etc. En relación al fuego es necesario señalar que si bien estimula
inicialmente la germinación, empleado de manera indiscriminada y recurrente también
puede dificultar el establecimiento de las especies forestales cuya regeneración se quiere
promover, de manera que su uso debería ser limitado o aplicado solo de manera puntual
o selectiva.
Ciertamente, teniendo en cuenta que la quema de pastos estimula la germinación
de A. pennatula, y que sus individuos una vez establecidos se comportan como
“rebrotadores” extraordinariamente recalcitrantes (capítulo 1), podemos llegar a la
conclusión un tanto paradójica de que el uso indiscriminado del fuego como medida de
control de leñosas podría haber favorecido la actual dominancia de esta especie en
sistemas silvo-pastoriles como los que aquí han sido estudiados en el centro-Norte de
Nicaragua. Así, si el objetivo es controlar o incluso eliminar esta especie de los pastos,
en base a los resultados presentados se puede recomendar la aplicación de las medidas
de control habituales, chapia y quema, al final o justo después de la época seca que es
cuando los individuos de A. pennatula encuentran más dificultades para sobrevivir y
rebrotar, quizá por haber movilizado sus reservas (nitrógeno y fosforo) hacia la parte
aérea a fin de afrontar la prolongada sequía. De manera particular el fuego, para ser una
medida más efectiva de control de A. pennatula, debiera de aplicarse de manera
selectiva, es decir solo sobre los individuos establecidos que se quieren eliminar y así
evitar el efecto estimulante de la germinación de un hipotético banco de semillas
remanente en el suelo (capítulo 2).
Por otro lado, para mantener poblaciones viables los individuos ya establecidos
de A. pennatula deben defender sus semillas de la depredación pre-dispersiva que
ejercen determinados insectos especialistas y que puede llegar a comprometer el
reclutamiento de plántulas (capítulo 3). A tal fin, el saciado de los depredadores
mediante la producción masiva de frutos es un mecanismo de defensa efectivo a lo largo
del rango de distribución altitudinal de esta especie aunque posiblemente requiere de
unas condiciones ambientales adecuadas para el esfuerzo reproductivo que significa
para los individuos. Condiciones éstas que progresivamente dejan de ser favorables a
medida que nos acercamos a los extremos del rango altitudinal y particularmente en la
parte superior del mismo. Simultáneamente, el aborto de semillas en los frutos se
relaciona con una mayor mortalidad de las larvas de los depredadores lo cual también
contribuye a la defensa de las semillas maduras. Este proceso es con toda probabilidad
desencadenado o bien por limitaciones por polen o bien por cuestiones ambientales
desfavorables a la reproducción de las plantas como el déficit hídrico o las bajas
temperaturas, condiciones climáticas por otra parte características de la periferia del
rango altitudinal de distribución de esta especie. No obstante, como mecanismo de
defensa solo puede ser efectivo dentro de un umbral por encima del cual la excesiva
pérdida de semillas abortadas, aún disminuyendo sensiblemente el éxito de infestación
de los insectos depredadores, no compensa los costos invertidos y la consecuente
disminución neta en el número de semillas maduras disponibles para la dispersión.
Ante el presente escenario de cambio climático, una de las más asentadas
respuestas, comprobada ya para diversas especies de plantas, es la migración de sus
poblaciones en altura en un proceso que se ha designado “rastreo climático” (ver
capítulo 3). Es decir que las plantas estarían ascendiendo siguiendo su óptimo
ambiental a medida que el clima cambia. Este proceso se espera que sea especialmente
acusado en el trópico y se cree que puede venir mediado o dificultado por los cambios
en las interacciones bióticas que el cambio climático puede suscitar. Así, teniendo en
cuenta que las condiciones ambientales en las partes más altas del rango de distribución
de A. pennatula se espera que se tornen progresivamente más favorables, es de esperar
también que las tasas de aborto se reduzcan y la capacidad de producir mayores
cosechas de frutos aumenten, de manera que en conjunto se posibilite una mejor defensa
de las semillas por saciado de sus depredadores pre-dispersivos mediando así una
expansión de esta especie en altura.
En relación a la defensa de las semillas ante la depredación pre-dispersiva por
parte de insectos cabe señalar también el efecto positivo que de manera indirecta el
ganado puede ejercer (capítulo 4). Al ingerir los frutos de A. pennatula y de G.
ulmifolia, el ganado no solo dispersa sus semillas si no que también depreda de manera
accidental aquellas larvas o pupas que aún permanecen dentro del fruto, de manera que
podrían llegar a ejercer un cierto control poblacional que en último término se tradujera
en una menor proporción de semillas depredadas. Aún siendo preliminares, estos
resultados también sugieren que las distintas especies que depredan sobre las semillas
de la misma planta huésped pueden experimentar distintas vulnerabilidades en función
de su tiempo de permanencia en el fruto, de manera que el ganado podría incluso tener
un papel importante como mediador de la coexistencia de estas especies de
depredadores especialistas.
Por último, la capacidad de colonización y persistencia en el pasto (capítulos 1 y
2), junto con los indicios presentados sobre interferencia alelopática (capítulo 5),
alertan sobre una posible invasión y bloqueo de la sucesión (o “encroachment”) de A.
pennatula tras un eventual abandono de los pastos en los que actualmente es una especie
dominante. De ser así la formación de rodales de elevada densidad y casi mono-
específicos (por ejemplo tacotales y latizales relativamente abundantes en la zona de
estudio) requeriría de labores de aclareo y enriquecimiento de especies a fin de
promover el avance de la sucesión secundaria hacia formaciones forestales más
desarrolladas. Para evitar este tipo de situaciones otra medida recomendable seria el
enriquecimiento de la comunidad de árboles dispersos en los potreros.
Publicaciones ‐ Publications
Versiones ligeramente modificadas de los presentes capítulos de esta tesis están
publicados o en vista de ser publicados como:
Slightly modified versions of the present chapters of this thesis are published or in view
to be published as:
Capítulo 1. Peguero, G. and Espelta, J.M. 2011. Disturbance intensity and seasonality
affect the resprouting ability of the neotropical dry-forest tree Acacia
pennatula: do resources stored below-ground matter? Journal of
Tropical Ecology 27:539-546.
Capítulo 2. Peguero, G. and Espelta, J.M. Oldies and newbies, but all goodies? No
interaction between endozoochory and fire in the germination ability of
tropical-dry tree species. Manuscript submitted.
Capítulo 3. Peguero, G., Bonal, R. and Espelta, J.M. Spatial variability in seed defence
mechanisms: Seed predator satiation and seed abortion vary along an
altitudinal gradient in Acacia pennatula. Manuscript submitted.
Capítulo 4. Peguero, G. and Espelta, J.M. Frugivores can mediate the coexistence of
insect seed predators depending on larval development time within the
fruit. Manuscript submitted.
Capítulo 5. Peguero, G., Lanuza, O.R., Savé, R. and Espelta, J.M. 2011. Allelopathic
potential of the neotropical dry-forest tree Acacia pennatula Benth.:
inhibition exceeds facilitation under tree canopies. Plant Ecology, in
press, DOI: 10.1007/s11258-011-0014-0
Apéndice fotográfico ‐ Photo Appendix
Foto 0.1 Cultivo de musáceas y frijol. Avance de la frontera agrícola en Jalapa (Nicaragua).
Foto 0.2 Sistema silvo-pastoril fruto de la transformación del bosque tropical seco. Miraflor-
Moropotente (Nicaragua).
Foto 0.3 Sistema silvo-pastoril dominado por Acacia pennatula durante la estación húmeda en
las Mesas de Moropotente (Nicaragua).
Foto 0.4 Sistema silvo-pastoril dominado por Acacia pennatula durante la estación seca en las
Mesas de Moropotente (Nicaragua).
Foto 0.5 Quema de potreros para el control de las especies leñosas en los pastos. Las Mesas
de Moropotente (Nicaragua).
Foto 1.1 Aplicación de tratamientos de corte en Acacia pennatula.
Foto 1.2 Aplicación de tratamientos de quema en Acacia pennatula.
Foto 1.3 Detalle de tocones de Acacia pennatula tras la aplicación de los tratamientos de corte
y de quema.
Foto 1.4 Detalle de rebrote de Acacia pennatula.
Foto 1.5 Obtención de raíces principales de Acacia pennatula para el análisis del contenido en
almidón, nitrógeno y fósforo.
Foto 2.1 Experimentos de cafetería con frutos de Acacia pennatula, Guazuma ulmifolia y
Enterolobium cyclocarpum.
Foto 2.2 Detalle del comedero tras una prueba de cafetería. Nótese en este caso la clara
preferencia mostrada.
Foto 2.3 Detalle del tratamiento de simulación del paso de las semillas de Acacia pennatula,
Guazuma ulmifolia y Enterolobium cyclocarpum (en bolsas de nylon) por el tracto digestivo del
ganado. Etapa ruminal realizada in situ en vaca canulada.
Foto 2.4 Adición del inóculo intestinal a las botellas de incubación. Etapa intestinal del tránsito
digestivo realizada ex situ en incubador rotacional Daisy.
Foto 2.5 Semillas en placas de Petri tras la aplicación de golpes de calor y previo paso por la
cámara de germinación.
Foto 3.1 Muestreo de vainas de Acacia pennatula en El Brasil – Mesas de Moropotente
(Nicaragua).
Foto 3.2 Detalle del embolsado de vainas para la recolección de insectos depredadores de
semillas (Mimosestes humeralis y Mimosestes anomalus).
Foto 3.3 Detalle de la depredación de las semillas por Mimosestes sp.
Foto 3.4 Medición de vainas y recuento de semillas abortadas, depredadas y sanas.
Foto 4.1 Aplicación de los extractos acuosos de hojas de Acacia pennatula en plántulas de
Cedrela odorata.
Foto 4.2 Detalle de individuo aislado de Acacia pennatula bajo la copa del cual se plantaron
plántulas de Cedrela odorata, Guazuma ulmifolia y Enterolobium cyclocarpum.
Foto 4.3 Detalle de plantula de Cedrela odorata.
Foto 4.4 Detalle de plántula de Guazuma ulmifolia.
Foto 4.5 Detalle de plántula de Enterolobium cyclocarpum.
Agradecimientos
Como en todas las tesis en esta también hay un conjunto de personas a las que tengo
mucho que agradecer.
En primer lugar debo mencionar a Pilar Andrés por brindarme la oportunidad de
trabajar en Nicaragua en un viaje que se encuentra en el origen de todo esto. A David
Tarrasón y Federica Rávera por acompañar allí mis primeros pasos y abrirme la puerta
de las Mesas de Moropotente. Y a Joan Franch por invitarme a conocer, en un viaje
iniciático inolvidable, la otra Nicaragua que se encuentra en el lado atlántico. Brisa
Delgado y Edurne Larracoetxea por su ejemplo y por hacerme reflexionar sobre qué
hacía yo en Nicaragua. Y también a Virginia García con quién he tenido el gusto de
compartir algunas de las alegrías e incertidumbres asociadas a llevar a cabo una tesis en
Nicaragua.
Mención especial merecen todas aquellas personas que en la FAREM-Estelí han
colaborado durante el desarrollo de esta tesis doctoral, sin la ayuda de las cuales ésta no
hubiera llegado a buen término. Aún a riesgo de olvidarme de alguien, no puedo dejar
de mencionar a: Oscar Rafael Lanuza, mi más voluntarioso compañero de fatigas el cual
siempre estuvo dispuesto a una hora más, una parcela más, unas cuantas muestras más.
Gracias por tu paciencia conmigo. Norman Gutiérrez quien más me ha ilustrado sobre
los pormenores de la revolución y sus secuelas contemporáneas. Keny López quien
“dobló el lomo” a mi lado desde el primer día y con quien compartí cervezas hasta
tomar la última, “la del estribo”. Josué Urrutia quien solidariamente me enseñó el ABC
de la flora del país. Don Bladimir Acuña, héroe nacional y referente en lo personal en
quien siempre confié ciegamente en llegar a donde hiciera falta y volver de una sola
pieza. Francisco Llanes cuyo discreto saber hacer facilitó enormemente toda la etapa
final de este trabajo. El resto del equipo “multicriterio”, a saber, Alejandrina Herrera,
Jaime Rocha y Abner Rivera con quienes aprendí a trabajar en las Mesas en aquellos
primeros días. Y algunos otros cuya colaboración en alguna de las investigaciones
también merece ser debidamente mencionada, como la de Jasser Obando, Francisco
“Lumumba” Mendoza y Orlando “Rambo” Rodríguez.
En el campo, allí en Nicaragua, también tengo muchas personas a las que
agradecer mucho. Por un lado Don Denis Rodríguez y Don “Chelao” Castillo (D.E.P)
que me brindaron la oportunidad de trabajar en sus potreros. Por otro, y de manera muy
especial, a Doña Corina y Don Andrés Rodríguez quienes me cuidaron maternal y
paternalmente, me abrieron las puertas de su casa, compartieron su maíz y sus frijoles
conmigo, y en concreto Don Andrés que me regaló su sabiduría durante largos
atardeceres, fumando Belmont y escuchando La Hora Ranchera.
En otro orden pero igualmente importante, se encuentran todas aquellas personas que
han compartido su conocimiento científico conmigo. En la facultad de Veterinaria, Jordi
Bartolomé, María Rodríguez y en especial Sara Cavini que me enseñó a trabajar con
vacas de una manera hasta entonces completamente insospechada por mi parte. En el
IRTA Robert Savé que siempre ha estado presto a colaborar y con quien compartí uno
de los momentos más duros de la tesis: un eterno viaje a oscuras y bajo la lluvia en la
pick up de una ranchera por inescrutables caminos en los que solo Bladimir, siempre
Bladimir, se orientaba. A Raúl Bonal quien, junto con Tete, me transmitió la pasión por
los gorgojos sensu latto y me enseñó en Royal City los principios del apasionante
mundo de la taxonomía molecular.
Y por supuesto Tete, quien como Stanley con Livingstone, me recuperó de la
selva, para luego confiar en mí y educarme científicamente (y como persona) a base de
amables sonrisas y pertinentes collejas. Aunque sea un tópico no puedo dejar de decir
que esta tesis no seria sin él y que de lo bueno lo mejor se debe también a él.
Y como no, todas aquellas personas que han convivido y compartido la
experiencia del doctorado en el CREAF. Becarios doctorales, técnicos, investigadores
futboleros et álii, todas ellas son responsables de hacer único este centro. Las del piso -1
(y algunas de otros pisos) y allegados de otros departamentos, sois demasiadas para
dejaros escritas en una lista pero vuestra alegría, las cenas, las fiestas, cualquier ocasión
que fuera buena y lo fueron todas, han ahuyentado día tras día el tedio y la monotonía.
No puedo sin embargo no mencionar a Josep Barba y Jara Andreu que me han
soportado pacientemente cada día en el despacho y que han jurado dejar de hacerlo sino
aparecen aquí sus nombres (Es-cán-da-lo, es un escándalo). También Xapa, Cela, Uli,
Roger y otros tantos amigos y amigas que me habéis ayudado a no pensar solo en esto y
recordarme que hay vida más allá de la tesis.
Gracias a mi padre Salvador y a mi madre Rafi por haber desarrollado y
estimulado en mí la curiosidad y las ganas de aprender. A mi hermana mayor Ana, por
ayudarme siempre desde que di mis primeros pasos de su mano hasta el doctorado. Y a
mi abuelo y abuela, yayo y yaya a quienes siempre tendré en el corazón al lado de mi
infancia.
Y por último a ti Laia por tu amor y por tu paciencia.
No tinc paraules per expressar-t’ho.
Esta tesis está dedicada a todas aquellas personas que allí en Nicaragua me enseñaron
con su humilde ejemplo, su mirada limpia y su corazón franco, a ser mejor persona.
