Elizabeth Del Carmen Gusman Montalvan
Elizabeth Del Carmen Gusman Montalvan
Elizabeth Del Carmen Gusman Montalvan
TESIS DOCTORAL
ELIZABETH GUSMÁN MONTALVÁN
UNIVERSIDAD POLITÉCNICA DE MADRID
TESIS DOCTORAL
1
Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja. Ecuador.
2
Área de Biodiversidad y Conservación. Departamento de Biología y Geología, ESCET,
Madrid, 2015
Marcelino de la Cruz Rot, y Adrián Escudero Alcántara, Profesores Titulares del
CERTIFICAN:
“Diversidad funcional y Diversidad filogenética en los Bosques Secos del Sur del
Ecuador”, son aptos para ser presentados por Elizabeth Gusmán Montalván ante el tribunal
que en su día se consigne, para aspirar al Grado de Doctor por la Universidad Politécnica de
Madrid.
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II
Tribunal nombrado por el Mgfco. y Exmo. Sr. Rector de la Universidad Politécnica de
Madrid, el día ………………. de ……………………………………………….2015.
Presidente: ……………………………………………………………………………………
Secretario: ……………………………………………………………………………………
Vocal: …………………………………………………………………………………………
Vocal: …………………………………………………………………………………………
Vocal: …………………………………………………………………………………………
Suplente: ……………………………………………………………………………………...
Suplente: ……………………………………………………………………………………...
Calificación …………………………………………………………………………………...
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EL PRESIDENTE
………………………………..
LOS VOCALES
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EL SECRETARIO
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A mis Padres y hermanos por ser la razón de mi vida.
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VI
ÍNDICE
RESUMEN ........................................................................................................... 1
ABSTRACT....................................................................................................... 7
INTRODUCCIÓN GENERAL........................................................................ 11
2.1. REGLAS DE ENSAMBLAJE EN LA COMUNIDAD .........................13
2.2. OBJETIVOS ............................................................................................20
2.3. ÁREA DE ESTUDIO Y METODOLOGÍA GENERAL .......................23
CAPÍTULO 1..................................................................................................... 36
Environmental variation mediates habitat filtering and limiting similarity in a
Dry Neotropical forest. ....................................................................................36
CAPÍTULO 2..................................................................................................... 66
Linking functional and phylogenetic diversities with assembly processes in a
dry neo tropical forest ......................................................................................66
CAPÍTULO 3..................................................................................................... 95
¿Actúan los mecanismos de ensamblaje a diferentes escalas espaciales en un
Bosque Seco? ...................................................................................................95
CAPÍTULO 4................................................................................................... 121
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2
El concepto tradicional de reglas de ensamblaje refleja la idea de que las especies no co-
concentración de bosques secos tropicales bien conservados del sur de Ecuador, y que
constituyen una de las áreas de endemismo más importantes del mundo. El clima se
caracteriza por una estación seca que va desde mayo a diciembre y una estación lluviosa de
enero a abril, su temperatura anual varía entre 20°C y 26°C y una precipitación promedio
Mi primer tema fue orientado a evaluar si la distribución de los rasgos funcionales a nivel
comunitario es compatible con la existencia de un filtro ambiental (filtrado del hábitat) o con
(10x50m). Para ello, se analizó la distribución de los valores de cinco rasgos funcionales
(altura máxima, densidad de la madera, área foliar específica, tamaño de la hoja y de masa de
con la distribución esperada bajo un modelo nulo con ausencia de competencia. Los
resultados obtenidos apoyan que tanto el filtrado ambiental como la limitación a la semejanza
Un segundo tema fue identificar si la diversidad funcional está condicionada por los
competencia se vuelve más importante, teniendo en cuenta las posibles modificaciones a este
patrón general a causa de las interacciones de facilitación. Para abordar este estudio
analizamos tanto las variaciones en la diversidad funcional (respecto a los de los cinco rasgos
Los análisis mostraron que tan sólo la diversidad de tamaños foliares siguió el patrón de
variación esperado, disminuyendo a medida que aumentó el estrés abiótico mientras que ni el
Un tercer tema fue evaluar si los procesos que organizan la estructura funcional de la
comunidad operan a diferentes escalas espaciales. Para ello cartografié todos los árboles y
funcionalmente todas las especies. Dicha parcela fue dividida en subparcelas de diferente
tamaño, obteniéndose subparcelas a seis escalas espaciales distintas. Los resultados muestran
existencia bien de filtros ambientales actuando a escala fina o bien de procesos competitivos
diversidad taxonómica, funcional y filogenética. Para ello utilicé tres funciones sumario
espaciales: ISAR- para el nivel taxonómico, IFDAR para el nivel funcional y IPSVAR para
4
el nivel filogenética y las contrastamos frente a modelos nulos que describen la distribución
espacial de las especies individuales. Los resultados mostraron que en todas las escalas
comportaron como neutras, es decir, que están rodeados por la riqueza de diversidad
proceso de filtrado de hábitat. En este estudio pone de relieve cómo el análisis de las
comunidad.
Todos los resultados de este estudio aportan nuevas evidencias de los procesos de ensamblaje
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6
ABSTRACT
The traditional concept of the rules assembly for species communities reflects the idea that
species do not co-occur at random but are restricted in their co-occurrence by interspecific
processes in the assembly of plant communities in the dry forests of southern Ecuador.
This study was conducted in the biogeographic region of Tumbesina has the largest
as one of the most important areas of endemism in the world. The climate is characterized by
a dry season from May to December and a rainy season from January to April. The annual
temperature varies between 20 ° C and 26 ° C and an average annual rainfall between 300
I first assessed whether the distribution of functional traits at the level of the community is
compatible with the existence of an environmental filter (imposed by habitat) or the existence
was conducted for 58 species of woody plants spread over 109 plots of 10 x 50 m.
Specifically, I compared the distribution of values of five functional traits (maximum height,
wood density, specific leaf area, leaf size and mass of the seed), via selected statistical
properties (range, variance, kurtosis and analyzed the standard deviation of the distribution of
the closest functional species) distances and compared with a expected distribution under a
null model of no competition. The results support that both environmental filtering and a
limitation on trait similarity affect the assembly of plant communities in dry forests
Tumbesina.
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My second chapter evaluated whether variation in functional diversity is conditioned by
(notwithstanding possible changes to this general pattern due to facilitation). To address this
theme I analyzed changes in both the functional diversity (maximum height, wood density,
specific leaf area, leaf size and mass of the seed) and the phylogenetic diversity, along a
gradient of climatic stress in Tumbes forests. The observed patterns of variation were
contrasted against the diversity expected under a completely random null model of
community assembly.
Only the diversity of leaf sizes followed the hypothesis decreasing in as trait variation abiotic
stress increased, while the other functional traits multivariate functional diversity and
The third theme assess whether the processes that organize the functional structure of the
community operate at different spatial scales. To do this I mapped all the trees and shrubs of
more than 5 cm in diameter within a plot of 9 hectares of dry forest and functionally
classified each species. The plot was divided into subplots of different sizes, obtaining
subplots of six different spatial scales. I found aggregation of similar functional strategies at
small scales, which may indicate the existence of environmental filters or competitive
processes that correspond to the optimal strategy for these fine scales.
Finally, with the same information from the permanent plot of 9 ha, I evaluated the effect and
phylogenetic diversity. The analysis comprised three spatial summary functions: ISAR- for
taxonomic level analysis, IFDAR for functional level analysis, and IPSVAR for phylogenetic
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level analysis, in each case the pattern of diversity was contrasted against null models that
randomly reallocate describe the spatial distribution of individual species and their traits. For
all spatial scales considering ISAR, IFDAR and IPSVAR, most species behaved as neutral,
i.e. they are surrounded by the diversity of other traits similar to that expected under a null
diversity, suggesting that they may play a role in competitive processes that limiting
functional and phylogenetic diversity, can help us understand the co-occurrence of species in
All results of this study provide further evidence of the processes of assembly of the
community of the seasonally dry forests as environmental variables and competition play an
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
INTRODUCCIÓN GENERAL
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
central en la ecología vegetal (Crawley 1986), los científicos han buscado reglas o normas
generales que expliquen la distribución de las especies en todas las regiones biogeográficas
(Götzenberger et al 2012). La teoría de biogeografía de islas fue una de las primeras teorías
controladas por normas ecológicas (MacArthur and Wilson 1967). Sin embargo, el término
"regla o norma de ensamblaje" fue presentado por primera vez por Jared Diamond (1975) que
entonces el concepto de estás normas de ensamblaje han sido un tema central en la ecología y
análisis de cómo los rasgos funcionales se distribuyen, generalmente los rasgos funcionales
reproducción y supervivencia del individuo (Lavorel and Garnier 2002; Cornelissen et ál.
2003; McGill et al. 2006; Violle et al. 2007). Dentro de este enfoque se han propuesto dos
mecanismos principales para explicar el papel de los rasgos funcionales de las plantas,
similares este proceso de filtrado conduce a una escasa dispersión en los valores de los rasgos
dentro de las comunidades, es decir, estos filtros abióticos llevan a una distribución de
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
caracteres convergentes o de 'baja dispersión' (Weiher et al. 1995; Cornwell et al. 2006;
Grime 2006).
Segundo el Límite de similitud o diferenciación de nicho impide que las especies que
los valores de los rasgos dentro de las comunidades (MacArthur y Levin 1967; Weiher y
Keddy 1.995; Grime 2006). Se espera que la competencia pueda crear una distribución
divergente o 'sobre dispersión' de los valores del rasgo entre las especies localmente
De acuerdo con una está línea de razonamiento, se espera que los patrones más fuertes de
filtrado en los rasgos funcionales se de en condiciones muy duras (por ejemplo frío o seco),
debido a la fuerte filtrado abiótico (Weiher and Keddy 1995; Cornwell et al. 2006), mientras
que la alta divergencia del rasgo se espera en los hábitats más competitivos y productivos de
acuerdo a la hipótesis de limite de similitud (MacArthur and Levin 1967; Wilson and Stubbs
2012).
Entre la gran cantidad de rasgos medibles sobre un individuo, los de interés para la ecología
funcional deben cumplir al menos cuatro condiciones (Lavorel et al., 2007). Ellos deben: (i)
tener alguna relación con la función de la planta; (ii) ser relativamente fáciles de observar y
rápidos de cuantificar, (iii) ser medibles utilizando protocolos estandarizados; y (iv) tener una
clasificación coherente (Garnier et al, 2001a; Cornelissen et al, 2003a; Mokany et al. 2008).
La mayoría de los rasgos medidos en esta tesis están directamente relacionados con procesos
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Debido a los vínculos directos entre los rasgos y el funcionamiento de los organismos, la
distribución de rasgos ofrecen una visión de gran alcance en cómo las comunidades se
ensamblan y cómo influyen en los procesos de los ecosistemas (Cornwell y Ackerly 2009,
Díaz et al. 2001). Dado que los rasgos fundamentales que determinan el ensamble de la
comunidad y los procesos de los ecosistemas pueden ser compartidos entre las comunidades
de todo el mundo (Díaz et al. 2004). Entre los más utilizados en los estudios del ensamble de
Desde una perspectiva basada en el rasgo, una comunidad puede estar caracterizada por la
distribución de los rasgos funcionales de los individuos que la componen (Ackerly 2003).
Debido a los vínculos directos entre los rasgos y el funcionamiento de los organismos, la
distribución de caracteres ofrecen una visión a gran alcance en ¿cómo las comunidades se
ensamblan y cómo influyen en los procesos de los ecosistemas? (Cornwell y Ackerly 2009,
Díaz et al. 2001). Dado que los rasgos fundamentales que determinan el ensamble de la
comunidad y procesos de los ecosistemas pueden ser compartidos entre las comunidades de
todo el mundo (Díaz et al. 2004), el conocimiento obtenido a través de los enfoques basados
en los rasgos puede ayudar a entender y (McGill et al. 2006), de mejor manera la ecología de
las comunidades.
los últimos 15 años, y se han hecho muchos progresos como el desarrollo de listas de rasgos
funcionales claves que definen aspectos independientes de las estrategias de las plantas
compilación de bases de datos de rasgos globales (Kattge et al. 2011), que documentan los
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
espacio y el tiempo (Fonseca et al. 2000; Wright et al. 2004; Garnier et al. 2004; Kraft et al.
2008).
A pesar del interés de los estudios basados en los rasgos funcionales en la ecología, la
mayoría de los estos hacen hincapié en los patrones de rasgos en los ecosistemas de bosques
húmedos templados o tropicales. Existiendo pocos estudios relacionados con los patrones de
secos (BTES) u otros ecosistemas limitados por la disponibilidad agua (Chaturvedi et al.
2011, Hulshof et al 2013). La disponibilidad de agua sin lugar a dudas es uno de los factores
limitantes más importantes en los BTES, siendo crítica para el establecimiento, supervivencia
y desarrollo de las plantas (Ruthemberg 1980), condicionando tanto los gradientes espaciales
(Balvanera et al. 2011, Espinosa et al. 2011), procesos ecológicos básicos y las interacciones
bióticas que se establecen en cada bosque (Martínez-Yrizar et al. 1992; Mooney et al. 1993).
los estos bosques secos (Blain and Kellman 1991; Murphy and Lugo 1995; Sampaio 1995).
El éxito de las especies en ocupar diferentes nichos dependerá de la capacidad para tolerar el
estrés hídrico y competir por el agua durante la sequía (Engelbrecht and Kursar 2003).
basados en rasgos funcionales en los Bosques Secos del Sur del Ecuador, con el fin principal
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
El primer capítulo fue orientado a la teoría del ensamble de la comunidad que considera que
la distribución de los valores de los rasgos funcionales dentro de una comunidad están
condicionados por un “Filtrado” dado por las condiciones ambientales que restringe el rango
de estrategias viables en una comunidad, y que puede también estar dado por un reparto de
especies coexistentes (Cornwell y Ackerly 2009). Nosotros nos hemos propuesto responder si
la distribución de los valores de los rasgos funcionales en los Bosques Secos del Sur del
Ecuador puede tomarse como evidencia de un rango limitado (filtrado por el hábitat) y/o de
un espaciado regular (limite a la semejanza) predicho por la teoría del ensamblaje de las
mismo género) son funcionalmente y ecológicamente más similares que especies alejadas
(Webb 2002). Si el filtrado de hábitat es el proceso comunitario las especies deberían ser
filogenéticamente mas relacionadas de lo esperado por azar (Webb et al. 2002; Cavender-
Bares et al. 2004; Losos 2008). Sin embargo, si la divergencia del rasgo es debido a los
procesos de limite de similitud entre las plantas, esto conduce a la predicción de una
estructura filogenético más dispersas, es decir especies que interactúan deben ser menos
al. 2004; Kraft et al. 2007). Se espera que la importancia de estos procesos opuestos, filtrado
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Con base en estos supuestos, una expectativa generalizada es que la diversidad funcional
disminuye bajo fuerte estrés biótico y aumenta en los habitas más leves (por ejemplo Weither
y Keddy 1995), y que filogenéticamente estén mas agrupado bajo fuerte estrés (por ejemplo
Webb 2000). Aunque estos dos son uno de los principales procesos de la asamblea de la
comunidad hay otros procesos que también puede afectar a la diversidad funcional de la
Levine 2010; Weiher et al. 2011) Por un parte tenemos la facilitación a menudo permite la
coexistencia de especies (Callaway et al. 2002; Brooker et al. 2008; Butterfield 2009) con
Banuet et al. 2006) aumento la diversidad funcional y la dispersión filogenético. Y por otra la
competencia puede aumentar la similitud de los rasgos entre las especies ocasionando que
pueden competir relativamente igual (Chesson 2000). Este proceso puede reducir la
diversidad funcional (Chesson 2000; Spasojevic and Suding 2012) y aumentar la dispersión
Bajo estas premisas hemos explorado la diversidad de los bosques tropicales secos del sur de
El tercer capítulo fue orientado a cuantificar la dispersión de los rasgo funcionales a lo largo
de una escala espacial a nivel funcional y filogenético. Swenson and Enquist (2009) aplicaron
del rasgo y los análisis filogenéticos para cuantificar patrones en múltiples escalas espaciales
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
ecológicos y evolutivos que operan en los rasgos de las especies a través del espacio y el
tiempo.
que hemos cartografiado e identificado todos los individuos arbóreos y arbustivos. Esto nos
permitirá conocer como actúan los procesos de ensamblaje de la comunidad a escala espacial
fina y determinar que escalas espaciales resultan más importantes (Kraft y Ackerly 2010). En
Westoby et al. 2002; Westoby and Wright 2006) cuantificamos la relación entre la dispersión
hectáreas, con un enfoque espacialmente explícito. Recientemente, los ecologistas han pasado
especies con el fin de probar las hipótesis del ensamble de la comunidad (Swenson 2013).
mediante el uso de patrones espaciales, como es el uso del ISAR (Su relación individual de
especies-área) propuesto por Wiegand et al. (2007), donde calcula la riqueza de especies en
los barrios locales alrededor de los individuos de una especie clave dentro de una comunidad.
Como consecuencia de ello una especie en particular pueden ser identificada como
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
acumulador o repelente de diversidad, o como neutral. A pesar del claro impacto del enfoque
desarrollado por Wiegand et al. 2007, es limitado, ya que trata a todas las especies
ecológicamente idéntico y evolutivamente independiente (CO Webb et al. 2002, Yang et al.
multi-escala de Wiegand et al. 2007) donde se incluya a otros ejes de la biodiversidad, como
el funcional (DF) y filogenético (PD). porque están convencidos de que pueden ser mejores
Cadotte et al. 2009; Flynn et al. 2011; Helmus and Ives 2012). El objetivo de este capitulo
diversidad taxonómica usamos ISAR, IFDAR para el nivel funcional y IPSVAR para la
estudios han demostrado que en este ecosistema, la facilitación es más fuerte en condiciones
de estrés y se reduce cuando las condiciones mejoran (por ejemplo, Espinosa et al. 2014,
2011).
2.2. OBJETIVOS
- Está tesis ha sido estructurada en cuatro capítulos que cubren aspectos como: la estructura
los Bosques Secos del Sur del Ecuador, un tipo de ecosistema de gran diversidad.
con la existencia del filtrado del hábitat o el límite de similitud en un bosque neotropical
seco.
Se considera que la distribución de los valores que pueden tomar los rasgos funcionales
dentro de una comunidad está condicionada por dos tipos principales de procesos de
ensamblaje. En primer lugar un “Filtrado por el hábitat” que restringe el rango de estrategias
viables en una comunidad .En segundo lugar el reparto de micro-sitios y recursos, que
magnitud de ambos procesos puede depender de las condiciones de una localidad y puede
Hoy en día, algunas investigaciones en ecología implican además de los métodos basados en
estructuración de la comunidad.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
la co-ocurrencia de las especies en el ensamble de las comunidades. Con fin de obtener una
Los ecologistas han pasado de medir la diversidad de especies solo con la riqueza y la
Seco, a nivel taxonómico, funcional y filogenético, para conocer si en una comunidad hay
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Área de estudio
La presente tesis se llevó a cabo en los bosques estacionalmente secos del suroccidente de
Ecuador, ubicados en la región Pacífico Ecuatorial (Espinosa et al. 2012). Estos bosques
forman parte de la región biogeográfica Tumbesina, que abarca territorios del suroeste de
Ecuador y noroeste de Perú, en un rango altitudinal que va desde el nivel del mar hasta los
2000 m s.n.m., aproximadamente (Best and Kessler 1995; Espinosa et al. 2011). Estos
bosques son muy ricos en especies y refugio de una extraordinaria diversidad de endemismos
de muy diferentes grupos taxonómicos (Best and Kessler 1995). La región Tumbesina abarca
una gran variedad de climas, como resultado de la posición geográfica y la topografía variada
(Best y Kessler 1995). La precipitación es el factor climático más variable, y por ende, el más
Esta región es reconocida como un centro de endemismo para diferentes taxones (Best y
Kessler 1995), así como por ser uno de los hotspots más amenazados del mundo (Dinerstein
et al. 1995, Espinosa et al. 2012). El clima se caracteriza por una estación seca que va de
mayo a noviembre y una estación lluviosa que se extiende desde diciembre a abril (Aguirre
and Kvist 2005). Para toda esta zona se estima una temperatura promedio anual entre 20° y
26°C y una precipitación promedio anual entre 300 y 700 mm (Aguirre y Kvist 2005).
Zapotillo, Macará, Celica; 120-2640 m s.n.m.) en uno de los remanentes más grandes y mejor
conservados de los bosques secos Tumbesinos (Aguirre y Kvist 2005), entre las latitudes
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
temperatura media anual en la región de unos 24°C (rango: 10-33°C) y con una precipitación
localizada en el extremo sur del Ecuador, provincia de El Oro, entre las ciudades de Arenillas
y Huaquillas, y cubre un área de 131,7 Km2 (Decreto Ejecutivo No. 787) (03° 34’ 15,44’’S;
80° 08’ 46,15’’E, altitud 30 m). La REA fue incluida dentro del Patrimonio de Áreas
caracteriza por una estación de lluvias de cuatro meses con una precipitación media anual de
515 mm a partir de enero a abril y de 152 mm durante la estación seca. La temperatura media
es de 25.2°C tienen una variación máxima de 3.4 º C entre los meses más fríos y más cálidos.
Metodología general
Para realizar los capítulos 1y 2 utilizamos las 109 parcelas (10x50m) previamente
establecidas en el sur del Ecuador en el área de estudio. Estas parcelas estuvieron establecidas
en 48 parches de bosque seco con un diseño estratificado, tratando de cubrir el rango total de
Para cumplir con los objetivos planteados en los capítulos 3 y 4, se estableció una parcela
las zonas mejor conservadas de la REA, que posee una formación vegetal de transición entre
bosque tropical seco y matorral seco de tierras bajas. Todas las plantas leñosas con DAP >5
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Para colectar los rasgos funcionales dentro de nuestra investigación, tomamos en cuenta los
La Altura máxima de la planta como se la conoce en varios estudios, se asocia con el vigor
es la distancia más corta entre el límite superior de los principales tejidos fotosintéticos
(excluyendo inflorescencias) en una planta y el nivel del suelo, expresada en metros (Pérez-
vida de las especies. Las especies con un baja densidad cuenta con altas tasas de crecimiento
de diámetro y altura (Poorter 2008, Chave et al. 2009) mientras que las especies con una alta
densidad de la madera tiene tasas de crecimiento lento, pero sobreviven mejor a la sequía
hidráulico, hojas más pequeñas por lo general se encuentran en hábitats más secos y más
expuestas (Ackerly et al. 2002; Cornwell and Ackerly 2009). Se conoce como tamaño de la
hoja, al área de la superficie proyectada de un solo lado (envés) correspondiente a una sola
hoja, expresada en mm2 (Cornelissen et al. 2003). El tamaño de la hoja es importante para el
2009). En el caso del Área foliar específica está definida como el área superficial de captura
de luz por unidad de biomasa seca, refleja un compromiso entre la captura y conservación de
los recursos (Poorter et al. 2009) tiene una fuerte relación positiva con la concentración de
nutrientes en la hoja, conductancia en los estomas, la tasa de fotosíntesis, el uso eficiente del
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
agua (Hoffmann et al., 2005), longevidad de la hoja, tasa relativa de crecimiento, densidad de
la madera, y la capacidad competitiva (Reich et al. 1997). Área foliar específica se cree que
variará con la fenología de la hoja, especies caducifolias tienen mayor área foliar específica,
especies de hoja perenne tienen valores más bajos de Área foliar específica (Reich et al.
1997). Finalmente la Masa seca de la semilla esta relacionada con todos los aspectos de la
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Referencias
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and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and
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Ackerly, D. D. (2003). Community assembly, niche conservatism, and adaptive evolution in changing
environments. International Journal of Plant Sciences, 164(S3), S165-S184.
Aguirre, Z. and L. P. Kvist. (2005). Composición florística y estado de conservación de los bosques
secos del sur-occidente del Ecuador. Lyonia 8(2):41-67.
Aguirre, Z., Kvist, L. P., and Sánchez, O. (2006). Bosques secos en Ecuador y su diversidad. Botánica
Económica de los Andes Centrales, 162-187.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
CAPÍTULO 1
36
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
37
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Abstract
According to Community Assembly Theory (sensu Diamond) abiotic constraints and biotic
interactions combine to form assembly rules that determine which species from the local pool
will coexist. Although, this theory has generally been studied with data on taxonomic
diversity, it may be more informative to consider the functional traits of species. Two main
mechanisms have been proposed to explain the role of functional traits in the assembly of
plant communities; a habitat filter that restricts the range of viable strategies and second, a
We compare the distribution of values for five traits (maximum height, wood density,
specific leaf area, leaf size and seed mass) in 58 woody plant species from 109 dry forest
plots. Specifically, we examined the within-community mean, range, variance, kurtosis and
the standard deviation of this distribution of neighbor distances (sdND). The range and
variance of maximum height, specific leaf area and seed mass were smaller than would be
expected from a lottery model of community assembly in most plots. We also found evidence
of limiting similarity for leaf size in the kurtosis, and seed mass in sdND.
These results support the existence of both habitat filtering and a limiting similarity affect in
assembly of plant communities of Tumbesian dry forests. Habitat filtering is evident along
the precipitation gradient with functional trait configurations in drier sites of high specific
leaf size, high wood density, high maximum height, and low seed mass. We also confirmed
that the climate gradient modifies the strength of the limiting similarity with a shortage of the
allowed functional strategies and an increase of the effects of competition (a more even
distribution of trait values), for most traits, as the conditions become harder (i.e., drier).
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Introduction
Detection of patterns in the ecosystems and inference of their causal processes were basic
topics in the development of community ecology [1,2]. One of the most impacting theoretical
contributions in this context was formulated by Diamond [3] as the Community Assembly
Theory. In a very synthetic way it points out that coexistence is possible due to differences in
resource use among species. According to this theory, the combined effect of abiotic
constraints (environmental conditions) and biotic interactions conform certain assembly rules
determining which species from the local pool will coexist at fine spatial and time scales in
the realized assemblages. Tests for this theory have traditionally focused on the taxonomic
identity and diversity, but a complementary and more informative approach is to consider the
functional features of species (functional traits) inhabiting these communities [4]. Plant
functional traits, i.e., any morphological, physiological or phenological feature that affects
plant growth, reproduction or survival, constitute a direct link between plant fitness and the
environment and are useful for answering relevant questions in ecology [5]. Indeed, plant
functional traits offer the best available approach for achieve a general predictive
Two main mechanisms have been proposed to explain the role of plant functional traits in the
construction of realized assemblages: i) habitat filtering, which implies that the environment
selects (i.e., "filters") the range of suitable trait values within a community and, ii) limiting
similarity, which means that only species differing in their traits and therefore having
competition [4]. Thus it is reasonable to test whether variation in the traits of coexisting
species is larger than expected by chance, with trait divergence being interpreted as evidence
of limiting similarity [8]. On the contrary, if habitat filtering were operating we would expect
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
a convergence of species trait values, i.e. less variation at the community level than expected
by chance [4].
Although the prevalence of these two mechanisms in natural communities is far from being
known, it has been hypothesized that the prevailing assembly mechanism in realized
assemblages could shift along environmental gradients from limiting similarity (and
functional divergence) at more productive and milder sites to habitat filtering (and
convergence) at the more stressful conditions [9]. In fact, the effect of environmental
gradients on the strength and direction of plant-plant interactions has been extensively
documented and has confirmed these expectations in many cases [10,11,12,13]. The shifts in
trait values across sites along and environmental gradient is usually related to species
Keeping this in mind, we have evaluated the role of habitat filtering and limiting similarity on
the assembly of neotropical Tumbesian dry forests, one of the less studied tropical forest
ecosystems in the world, despite evidences of extreme threats and forest losses are
assembly in these forests is critical for their proper management and conservation [17] and
also to complete the knowledge about the prevalence of these functional mechanisms in
In previous works we found that both the composition and the structure of Tumbesian forests
greatly shift as climatic conditions (mainly annual precipitation) change along its distribution
area [19]. Our main objective here is to test whether the paradigm about the prevalence of
these assembly mechanisms remains valid in the Tumbesian forest, with e.g., limiting
similarity prevailing in the wetter and milder places occupied by the Tumbesian forest, close
to montane forests, and habitat filtering prevailing in the harsh full areas in contact with the
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
dry shrublands [20]. More specifically we intended to answer the following questions: (1) Is
there any evidence for a restricted distribution (habitat filtering) or even spacing (limitation
of similarity) of trait values in the Tumbesian forests? (2) Does the relative importance of
habitat similarity or habitat filtering with respect to different traits change across the climatic
gradient?
Methods
Natural history of the Tumbesian dry forests
Tumbesian dry forests extend on a narrow fringe territory comprising 87,000 km2 along the
Pacific coast from the southwestern tip of Ecuador, to the northwestern of Peru [21]. Our
study area covers nearly 2000 km2 in the province of Loja (Zapotillo, Macará and Celica
districts) in the southernmost tip of Ecuador, covering an altitude range from 120 to 2,600 m.
This territory encompasses one of the largest and best conserved remnants of the Tumbesian
dry forests in Ecuador [22,19]. We surveyed only well-conserved stands without evidences of
recent anthropogenic perturbations. All survey and collection was authorized under the
is ca 24 ºC (range: 10–33 ºC). Mean annual precipitation is ca 500 mm/yr (range: 270–1284
mm/yr).
These forests are very rich in tree and shrub species [19] and are dominated by Bursera
graveolens, Acacia macracantha and Capparis scabrida. It is also the habitat of several
Field data
stratified sampling design based on the available preliminary landscape maps in the territory.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
In each plot we counted the number of individuals of all standing perennial species see details
[19]. From the Worldclim database [25], we annotated for each plot the value of the mean
annual precipitation, as this variable has been shown to be one the main predictor of species
turnover and is correlated to the variation of community composition and structure in the area
[19].
We selected a set of plant functional traits, which are known for being tightly related to
important processes in trees and shrubs [26]. Leaf size (LS) plays a particularly important
role in carbon assimilation, water relations and energy balance [27]. Plant growth and
survival are strongly connected to specific leaf area (SLA, leaf area per unit mass). This trait
represents an "economic" axis of variation that ranges from species typical of resource-rich
habitats, which have a rapid tissue turnover and high metabolic rates and whose attributes
enhance the rapid acquisition of photosynthetic carbon (high SLA), to species tolerating
resource-limited habitats which tend to show opposite attributes [28]. SLA and LS decrease
LS is important for energy balance and hydraulic functioning, with smaller leaves generally
found in drier and more exposed habitats [36]. WD is related to water efficiency and
transport [36]. Although the variation of this trait is considered to be orthogonal to the leaf
economic one [37], it is also related to growth and survival. Low WD is usually a surrogate
of high stem growth rates [38], whereas high WD are related to low growth rates and to the
development of thick cell walls [39], which makes stems more resistant to breakage [40] and
to fungi and pathogen attacks [41]. Hmax is related to access to light [42,43]. Higher plants
intercept on average more light and therefore have potentially faster growth rates [44]. SM is
a crucial feature for dispersion and regeneration and is related to the competition-colonization
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
trade-off [45]. Large seeds provide reserves for successful seedling establishment in poor
light or intense competitive conditions [46]. By contrast, small-seeded species produce more
seeds per unit of reproductive effort [47] and are better colonizers [48].
We selected all woody species appearing in at least 4 of the studied plots. Three traits (LS,
SLA and SM) were measured in the field and/or the laboratory, following standardized
protocols [26]. In the case Hmax were taken from the literature [49,50,51,52] and WD [S2]
For each species, we collected 10 leaves from each of 10 randomly chosen trees, covering all
the environmental range of each species in our data set. LS, was measured with the program
Image J [53] from scanned (300 dpi) fresh leafs. Leaf mass (for calculation of SLA) was
measured after 3 days drying at 60 ºC. Seeds were also collected from at least 10 fruits taken
from different individuals of each species. We also used seed accessions from the Germplasm
Bank of Universidad Técnica Particular de Loja. Seed mass was obtained after 48 hours
drying at 80 °C [26]. SM of ten species, which could not be collected in the field, were
Data analysis
We first calculated the Spearman rank correlation coefficients between trait values of species
and between mean species trait values by plot. For subsequent analyses, we log-transformed
Hmax, LS, SLA and MS values. WD showed a normal distribution and was not transformed.
The effects of habitat filtering can be seen as a reduction in the variety of successful trait
values that occur within a community [2,55,56]. To detect such a reduction, we measured the
range and the variance of trait values within each community. If habitat filtering is operating
on a specific plant trait, then the observed range of values for the plant trait should be lower
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
than expected if communities were assembled independently with respect to that trait. As the
range is susceptible to extreme values that could be due to mass effects [57] or measurement
error, we measured also the variance of trait values in these communities as a more efficient
metric of convergence [36]. In fact, these two metrics have been shown as good predictors of
three complementary approaches. First, we computed the kurtosis of the distribution of trait
values within plots, since it has been suggested that platykurtic distributions (i.e., low
kurtosis values) are expected when a process (i.e., limiting similarity) spreads species traits
within a realized community [36]. Secondly, we checked for large variances in the
distribution of trait values, as this is also a robust indicator of character divergence [58].
Additionally, we quantified the even distribution of trait values within plots. For this, within
each plot, we ordered species with respect to their trait values and computed differences in
trait values among neighbor species ("neighbor distances"). The standard deviation of this
limiting similarity process would be ruling the assembly process, sdND should be low or, in
any case, lower than the sdND of a completely random process [36].
Inference about the significance of the observed range, variance and kurtosis was based on a
lottery null model, with equal probability of assembling any of the recorded species in each
null community [36]. As we considered each of the surveyed plots as a community unit, we
conducted 9999 random draws for each plot with the same richness as the observed plot. We
compared the range, and kurtosis of observed trait values in the plot to the median of the
range and kurtosis of traits in the simulated communities with one-tailed Wilcoxon paired-
sample tests. In the case of variance we compared observed and expected values with two-
44
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
tailed tests. As the presence of a strong habitat filter effect could generate false positives
when testing for even spacing with lottery models (due to the existence of extreme trait
values in the species pool, [36], inference about the distribution of sdND's was based on a
two-step null model which accounts for possible habitat filtering [36]. In a first step, for each
plot, we identified among the 58 species those species whose niche breadth (relative to
annual precipitation) comprised the abiotic conditions found in the plot (i.e., "potential
community members").
Niche breadth was estimated as the range of annual precipitation values among the plots
where the species appeared in the whole study. In the second step, we conducted 9999
random draws with the same richness of each plot choosing among the set of potential
community members. We computed the sdND's of each random community and built a
distribution of sdND's under our null model. We then compared the observed sdND's with the
In order to test whether species turnover along the gradient has any effect on the distribution
of traits, we also computed correlations between the mean value of each trait in each plot and
Finally, to test whether assembly mechanisms shift along the precipitation gradient, we
calculated Spearman rank correlations between the annual precipitation and the range,
variance, kurtosis and sdND's for each trait in each plot. All analyses including null models
Result
We found 102 species (73 trees and 29 shrubs). Maximum richness per plot was 14 species,
with a median of 4 species per plot. We selected the 58 species (30 deciduous, 13 semi–
45
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
deciduous and 15 evergreens) that appeared in at least four of the studied plots (S1).
Plant functional traits showed appreciable variation between species. Hmax varied from 4 m
(Annona sp, LS ranged between 287.00 ± 60.22 cm2 in Piscidia carthaginensis and 8.46 ±
2.52 cm2 in Prosopis juliflora. SLA values varied between 46.63 cm2/g and 2.9 cm2/g in
Urera sp. and Fulcaldea laurifolia, respectively. WD ranged between 1.00 g.cm–3 (Tabebuia
chrysantha) and 0.19 g.cm–3 (Erythroxylum glaucum). Finally, SM ranged from 0.01 g in
We did not find intraspecific trait correlations except for the case of Hmax and LS (Table 1).
Table 1. Spearman rank correlation coefficients for 58 species trait values. Significant correlations (p
< 0.05) are shown in bold.
WD LS SLA SM
LS –0.23
WD – wood density; LS – leaf size; SLA – specific leaf area; SM – seed mass; Hmax – maximum height.
The mean trait values, per plot were significantly correlated for some traits. LS was positive
correlated with SLA and Hmax, and negative correlated with SM; whereas WD showed
positive correlation with SLA and SM. Finally SLA had a positive correlation with Hmax
(Table 2).
46
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Table 2. Spearman rank correlation coefficients for mean trait values, in 109 plots. Significant
correlations (p < 0.05) are shown in bold.
WD LS SLA SM
LS 0.02
WD – wood density; LS – leaf size; SLA – specific leaf area; SM – seed mass; Hmax – maximum height
The range and variance of Hmax, SLA and SM were smaller than expected for the lottery
47
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
1.5 0.6
1.0 0.4
0.5 0.2
0.0 0.0
3.0
range in trait values
2.0
2.5
1.5
2.0
1.5 1.0
1.0
0.5
0.5
0.0 0.0Observed values
☐
2 4 6 8 10 12 14
Null expectation
log(seed mass)
Species richness
8
2 4 6 8 10 12 14
Species richness
Figure 1. The community–wide range of values of five traits at different levels of species richness.
Open circles show the observed values for 109 plots; solid squares show the mean of 9999 null model
trials at each of the corresponding levels of species richness. See Table 3 for a description of the traits
and a synthesis of results; note that data have been log–transformed except for wood density. Wood
density showed an approximately normal distribution and was not transformed.
48
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Table 3: The range and variance of trait values within a site: deviations from the lottery model of
habitat filtering. Figures show the number of plots where the range or variance observed for the
distribution of values of each trait was smaller than the range or variance expected according to the
lottery null model.
Range Variance
expectation expectation
Hmax – maximum height; WD – wood density; LS – leaf size; SLA – specific leaf area; SM – seed mass. P – p-
value
On the other hand, the kurtosis of trait values within plots was significantly lower than
expected only for LS (Table 4). The standard deviation of the distribution of neighbor
distances among trait values within plots (sdND) was significantly lower than expected only
for SM (Table 4). Remarkably, the variance of WD was smaller than expected only in a few
Table 4: The kurtosis of trait values per plot, and the standard deviation of the distribution per plot of
"neighbor distances" (sdND), i.e., functional distances among neighbors in the list of species ordered
according to their trait values. Figures show the number of plots where the kurtosis or sdND observed
for the values of each trait was smaller than the kurtosis or sdND expected according to a lottery null
model (kurtosis) or to a two–step model accounting for habitat filtering (sdND).
49
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Kurtosis sdND
expectation P Expectation P
Hmax – maximum height; WD – wood density; LS – leaf size; SLA – specific leaf area; SM – seed mass. P – p-
value
Average values (per plot) for four traits showed correlation with annual precipitation.
Average Hmax, WD and SLA decreased as annual precipitation increased, while SM increased
with precipitation (Table 5). In parallel, range and variance of Hmax, SM and SLA values per
plot increased with precipitation. Kurtosis of Hmax and SM were also positively correlated
with annual precipitation (Table 5). The sdND of LS and WD showed respectively positive
Table 5: Spearman rank correlation coefficients between plot value, range, variance, kurtosis,
standard deviation of nearest distance (sdND) and mean for plant functional traits and annual
precipitation. Bold values indicate correlations with p<0.05
Hmax – maximum height; WD – wood density; LS – leaf size; SLA – specific leaf area; SM – seed mass.
50
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Discussion
Although numerous functional trait-based studies have shown functional patterns from
temperate to Mediterranean and tropical moist forest ecosystems, there are relatively few
studies addressing patterns of functional trait diversity in tropical dry forests (TDFs) or other
The distributions of trait values within the Tumbesian TDFs were clearly nonrandom,
suggesting that the studied plant traits play an important role in determining the success or
failure of each species in each particular site. We did not find intra-specific trait correlations
(except for the case of Hmax and LS, Table 1), which implies that the potential response of
the studied traits to habitat filtering and competition could be considered independent.
We found signal of habitat filtering (smaller than expected range and variance of trait values)
for three traits: SLA, Hmax, and SM (Table 3). We found also evidence for limiting
similarity (lower kurtosis or lower sdND values than expected, respectively) for LS and SM,
and a lower variance for WD (Table 4). These results support the idea that both habitat
filtering and limiting similarity, which are considered sometimes as competing models of
community assembly, act simultaneously in the South Ecuadorian dry forests and,
sometimes, even act over the same trait (e.g., over SM).
The platykurtic distribution of LS and the trend towards large variance of WD within
communities are probably related to competition for water. Being water the main limiting
resource in the Tumbesian forests [19], a niche partition around water use efficiency, which
is closely related to LS [27,63, 64] and WD [65], would promote coexistence within the
community.
The even spacing of SM values could be interpreted under the same framework of niche
partition, i.e., as the result of the dispersion of different regeneration strategies associated to
microsite variability within plots (i.e., very fine spatial scale). This is congruent with the
51
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
known relationship between seed size and the competition-colonization trade-off [47,66] and
similar results have been found in other ecosystems, such as the Great Basin pine
Another sign of the mediation of the environment in trait-based community assembly is the
variation of average community trait values through the environmental gradient. In fact,
environmental gradients can generate species turnover [68] caused by the gradient filtering
community mean trait values along the gradient. We confirmed the existence of shifts in
mean community values along the precipitation gradient for most traits. For example,
community SLA increased as the climate became drier. Although this finding may seem
counterintuitive and contrary to what has been found in a number of studies [36,69,70], SLA
was not significantly related to climatic parameters in a global study reported by Ordoñez
[71]. The usual decline of SLA along gradients of decreasing moisture is usually mediated by
a transition from thin, large-leaved, deciduous plants to thick, small-leaved, perennial species
[36]. In the Tumbesian forests however, most species are deciduous [19,72], and must build a
new foliar system each wet season. As the duration of the wet season is related to annual
precipitation in the Tumbesian region [73], faster foliar development (and therefore higher
The variation of WD along the precipitation gradient was consistent with the lower stem-
growth rates expected in the drier sites. High WD are related to low growth rates and to the
development of thick cell walls [39], which additionally enable stems to resist embolism
The average Hmax per plot increased with declining annual precipitation. This is surprising
as the dispersion of Hmax values within plots showed symptoms of habitat filtering (i.e.,
lower range and variance than expected according to null models), which suggest that drier
52
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
conditions favor the establishment of species with potentially larger height. We think that in
this case the convergence in trait values is not caused by habitat filtering but instead is the
result of the competitive processes for light [78]. In fact, larger Hmax is positively related to
faster growth rates in tropical trees [44], as access to light increases exponentially with height
in forest canopies [43]. This, in combination with their larger LS (LS is correlated with Hmax
at species level; Table 1) would make Tumbesian species with larger potential height grow
faster than the smaller ones. In the drier sites, where the growing season is shorter, a faster
Average SM per plot decreased with declining annual precipitation. This is not surprising as
high SM provides a competitive advantage for seedlings in the most competitive extreme
(i.e., the humid extreme) of the precipitation gradient [47,79,80,81]. In fact, larger seeds
provide the emerging seedlings with larger reserves and make them succeed size-dependent
competition, and to recover easily from damage caused, e.g., by herbivory or falling debris
[82], processes more important in the most productive (i.e., humid) extreme of the gradient.
On the contrary, small seed species are better colonizers of sites where conditions for
Finally, the influence of the environment on the processes mediating community assembly
could be confirmed by assessing the existence of shifts in the distribution of trait values
within communities along the environmental gradient. We confirmed that the distributions of
some traits shifted also along the gradient of precipitation. For example, the range and
variance of SLA, Hmax and SM decreased with declining precipitation. This means a
shortage of the allowed functional strategies for these traits as the environmental conditions
become harder. This result is contrary to recent views that expect convergence to occur in
more productive sites [76,78,84], and instead agrees with the traditional niche differentiation
theory, which expects these convergences to occur in the more stressful sites [85]
53
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
The kurtosis of Hmax and SM decreased with declining precipitation, as did the sdND of LS.
This means that, within communities, the spread of values for these traits increased as
precipitation decreased. This result points to an increase of the effects of competition, as the
In the case of wood density, we found that sdND increased as precipitation declined, which
means that the spread of WD values was less even in dry sites, i.e., that the effects of
competition (or limiting similarity) on this trait decrease as the climate becomes harder. This
shows that the selective pressures for this trait and those for Hmax and SM are operating
In conclusion, we confirmed the influence of both habitat filtering and limiting similarity on
the assembly of the Tumbesian forests. The existence of a neat trend for plot mean trait
values across the precipitation gradient is consistent with the idea of habitat filtering: within
each sampled habitat, only species inside of the viable range of trait values will be included.
The results of the correlation analysis suggest that in the drier sites, the successful functional
strategy consist of high SLA, high WD, high Hmax and low SM (Table 5). We confirmed
that the gradient also modifies the strength of the limiting similarity and the habitat filtering
processes, with a shortage of the allowed functional strategies (i.e., a decrease of the range of
trait values) and an increase of the effects of competition (a more even distribution of trait
54
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
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APPENDIX 1.
S1 Table: Mean trait values for 58 species of tropical dry forest. The letters a,b,c, mean the base literature of each trait. Hmax – maximum height; WD –
wood density; LA – leaf area; SLA – specific leaf area; SM – seed mass.
a b d
Family Species Hmax (m) WD (g. cm–3) LS (cm2 ) SLA(cm2. g–1) SM (g)
Mimosaceae Acacia macracantha Humb. and Bonpl. ex Willd. 12 0.73 28.16±4.6 6.93 3.12
Burseraceae Bursera graveolens (Kunth) Triana and Planch 10 0.32 129.97±28.9 7.44 2.28
Caesalpinaceae Caesalpinia glabrata Kunth, Karl (Carl) Segismundo 8 0.95 42.83±9.4 9.95 10.63
Bombacaceae Ceiba trischistandra (A. Gray) Bakh. 22 0.32 123.21±24.5 11.86 8.29
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Boraginaceae Cordia alliodora (Ruiz and Pav.) Oken. 10 0.52 60.17±13.5 7.25 1.65
Bombacaceae Eriotheca ruizii (K. Schum.) A. Robyns. 15 0.39 177.26±45.8 19.59 1.14
Moraceae Maclura tinctoria (L.) D. Don ex Steud. 15 0.79 22.14±4.5 16.65 1.92
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Caesalpinaceae Senna mollissima (Humb. and Bonpl. ex Willd.) H.S. Irwin 6 0.56 152.48 7.18 3.6
and Barneby
Caesalpinaceae Senna spectabilis (DC.) H.S. Irwin and Barneby 8 0.56 268.34 24.99 1.62
63
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Symbol shows the averages of values the data for wood density and seed mass of the genus for each species
Symbol shows the averages of values the data for wood density and seed mass of the family for each species.
a
Whaley OQ, Orellana A, Pérez E, Tenorio M, Quinteros F, et al. Plantas y Vegetación de Ica, Perú – Un recurso para su restauración y conservación. Royal Botanic
Gardens, Kew. 2010.
a
Aguirre Z, Cueva E, Merino E, Quizhpe W, Valverde A. Evaluación ecológica rápida de la vegetación en los bosques secos de La Ceiba y Cordillera Arañitas, provincia de
Loja, Ecuador. Pp. 15-35. En M.A. Vásquez, M. Larrea, L. Suárez and P. Ojeda (eds.). Biodiversidad en los Bosques Secos del Sur-Occidente de la Provincia de Loja.
EcoCiencia, Ministerio del Ambiente, Herbario LOJA y Proyecto Bosque Seco. 2001; Quito. Ecuador.
a
Aguirre Z, Zofhre H. Especies forestales de los bosques secos del Ecuador. Guia dendrológica. 2012; 392.
b
Zanne AE., Lopez-Gonzalez G*, Coomes DA, Ilic J, Jansen S, et al. Global wood density database. 2009; Dryad. Identifier: http://hdl.handle.net/10255/dryad.235.
b
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. Towards a worldwide wood economics spectrum. Ecology letters. 2009; 12: 351–366.
c
Royal Botanic Gardens Kew. Seed Information Database (SID). Versión 7.1. Available from. October 2013; http://data.kew.org/sid/
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65
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
CAPÍTULO 2
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
67
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
ABSTRACT
One of the most important challenges for ecologist is to understand the assemblage
mechanisms of plant communities. One compelling community assembly model predicts that
These focus ignores the importance of other assembly processes such as equalizing fitness
We intended to determine whether facilitation under the highest level of stress modifies the
expected response for habitat filtering and limiting similarity by adding phylogenetically and
functionally distinct species to the community. In the present work we evaluated the
functional structure of five important plant functional traits along a climatic stress gradient.
We compared the observed trait distribution in the community with a null model that assumes
Our results suggest evidences of habitat filtering in the values taken by most traits along the
stress gradient (measured as CWN), no evidence that functional diversity shifted along the
environmental gradient was found for any trait except for leaf size. The usual decline of LS at
along gradients of decreasing moisture is usually mediated by a transition from thin, large-
leaved, deciduous plants to thick, small-leaved, perennial species. Other factor is the
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
INTRODUCTION
One of the most important challenges for ecologist is to understand the assemblage
mechanisms of plant communities (Keddy 1992; Weiher and Keddy 1995; Chesson 2000;
Ackerly 2003; Götzenberger et al. 2012; Price et al. 2012). A promising approach for
disentangle these mechanisms is the use of functional and phylogenetic diversities (McGill et
al. 2006; Kraft et al. 2008; Mayfield and Levine 2010; Wiens et al. 2011; Paine et al. 2011;
Katabuchi et al. 2012; Shipley et al. 2012). A complete theoretical framework has been built
to describe how the environmental conditions affect the values taken by these two community
attributes during the assemblage of plant communities (Lavorel and Garnier, 2002; McGill et
Two potentially opposing processes can structure the distribution of functional diversity
along environmental gradients. Firstly, abiotic limitations increase the species functional
similarity, because the co-occurring species needs to be functionally adapted to the same
abiotic envelope (May et al. 2013). This process is known as "habitat filtering" (Cornwell and
would predict a limit in the similarity of coexisting species (MacArthur and Levins 1967;
Pacala and Tilman 1994). Since that species with similar functional traits may have a
substantial overlap niche, it is expected that co-occurring species show divergence of traits
(MacArthur and Levins 1967; Stubbs and Wilson 2004; Kraft et al. 2008). This process is
known as “limiting similarity” (Cornwell and Ackerly 2009). Thus, while the habitat filtering
reduces the functional diversity (Weiher and Keddy 1995; Weiher et al. 2011), the limiting
similarity increases the functional diversity among coexisting species (Cornwell and Ackerly
2009; Weiher et al. 2011). If these niche and functional differences matter they should shift
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
along gradients simply because their prevalence appears associated to stressful conditions
The relationship between functional and phylogenetic diversity is rooted in the reasonable
assumption that evolutionary diversification has generated traits diversification, which in turn
may result in greater niche complementarity and similarity associated to relatedness (Webb
2000). Thus, related species (i.e. same genus) are functionally and ecologically more similar
than distantly related species (Webb et al. 2002). This framework allows inferring the
with null expectation generated by drawing species at random from a regional pool of
potential colonists (Webb 2000; Cornwell et al. 2006). In the same way that functional
diversity, the phylogenetic diversity can be affected for “habitat filtering” and “limiting
similarity” (i.e. competitive exclusion). If the habitat filtering is the assembly community
process and plants exhibit evolutionary niche conservatism, then closely related species with
similar traits should coexist within a community more commonly than expected and the
species would be clustered in the phylogeny (Webb et al. 2002; Cavender-Bares et al. 2004;
composition, this should limit coexistence of closely related species with similar niches, and
species would be overdispersed in the phylogeny (Webb et al. 2002; Cavender-Bares et al.
It is expected that the importance of these opposing processes, habitat filtering and limiting
(Freschet et al. 2011; Violle et al. 2012). Based on these assumptions, a widespread
expectation is that functional diversity decreases under strong biotic stress and it increases in
milder habitats (e.g. Weither and Keddy 1995; Spasojevic and Suding 2012) and that
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
phylogenetic diversity is clustered under strong biotic stress and shows overdispersion in
mesic habitats (e.g. Webb et al. 2002; Swenson and Enquist 2009).
Although these two are among the main processes in the community assembly there other
processes that can also affect the functional diversity of community and phylogenetic
structure (Valiente-Banuet and Verdú 2007, Mayfield and Levine 2010; Weiher et al. 2011).
Even if niche differentiation prevents coexisting of similar species (i.e. limiting similarity)
competition may increases similarity among species (Chesson 2000). Under some conditions
species with similar traits may compete relatively equally, thus excluding competitors with
unfit traits (i.e. equalizing fitness processes Chesson 2000; Grime 2006). This process may
reduce functional diversity (Chesson 2000, Spasojevic and Suding 2012) and increase species
dispersion in the phylogeny. On the other hand, in stressful environments, facilitation often
allows the coexistence of species (Callaway et al 2002; Brooker et al. 2008; Butterfield 2009)
with different functional traits (Callaway 2007) and/or phylogenetically distant (Valiente-
Under these limitations to know when and where both diversities run in parallel remains as a
challenge. In order to build a more general framework for disentangling the signatures of
habitat filtering and limiting similarity in community assembly left on functional and
phylogenetic diversities we have explored the diversities of dry tropical forests of southern
Ecuador along a large environmental gradient. Some works carried out in this ecosystem
have recognized the prevalence of facilitation and have shown that the strength of this
interaction increases with stress (Espinosa et al. 2011; 2013). We intended to determine
whether facilitation under the highest level of stress modifies the expected response for
habitat filtering and limiting similarity by adding phylogenetically and functionally distinct
71
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
In the present work we evaluated the functional structure of five important plant functional
traits along a climatic stress gradient. We compared the observed trait distribution in the
community with a null model that assumes random community assembly. Based on this
approach, we want to answer the following specific questions: i) does functional and
phylogenetic diversity shift along abiotic stress gradients from lower values at the stressful
conditions to higher values at the more benign habitats?., and ii) does facilitation increase
Methods
Tumbesian dry forests extend on a narrow fringe territory comprising 87,000 km2 along the
Pacific coast from the southwestern tip of Ecuador, to the northwestern of Peru (Dinerstein et
al. 1995). Our study area covers nearly 2000 km2 in the province of Loja (Zapotillo, Macará
and Celica districts) in the southernmost fringe of Ecuador, covering an altitude range from
120 to 2600 m. This territory encompasses one of the largest and best conserved remnants of
the Tumbesian dry forests in Ecuador (Aguirre and Kvist 2005; Espinosa et al. 2011). We
perturbations. Average annual temperature in the region is ca 24 ºC (range: 10–33 ºC). Mean
These forests are very rich in tree and shrub species (Espinosa et al. 2011) and are dominated
by Bursera graveolens, Acacia macracantha and Capparis scabrida. It is also the habitat of
several endangered tree species including Juglans neotropica, Siparuna eggersii (Joergensen
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Field data
stratified sampling design based on the available preliminary landscape maps in the territory.
In each plot we counted the number of individuals of all standing perennial species (see
details in Espinosa et al. 2011). From the Worldclim database (Hijmans et al. 2005), we
annotated for each plot the value of the mean annual precipitation, as this variable has been
shown to be one the main predictor of species turnover and is correlated to the variation of
We selected a set of plant functional traits, which are known for being tightly related to
important processes in trees and shrubs. Leaf size (LS) plays a particularly important role in
carbon assimilation, water relations and energy balance (Ackerly et al. 2002). Plant growth
and survival are strongly connected to specific leaf area (SLA, leaf area per unit mass). This
trait represents an "economic" axis of variation that ranges from species typical of resource-
rich habitats, which have a rapid tissue turnover and high metabolic rates and whose
attributes enhance the rapid acquisition of photosynthetic carbon (high SLA), to species
tolerating resource-limited habitats which tend to show opposite attributes (Poorter and
Bongers 2006). SLA and LS decrease along gradients of declining moisture and/or nutrient
availability (Schimper et al. 1903; Hamann 1979; Dolph and Dilcher 1980; Givnish 1984;
Skarpe 1996; Cunningham et al. 1999; Fonseca et al. 2000; Ackerly et al. 2002).
LS is important for energy balance and hydraulic functioning, with smaller leaves generally
found in drier and more exposed habitats (Cornwell and Ackerly 2009). Wood density (WD)
is related to water efficiency and transport (Cornwell and Ackerly 2009). Although the
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
variation of this trait is considered to be orthogonal to the leaf economic one (Ackerly 2004),
it is also related to growth and survival. Low WD is usually a surrogate of high stem growth
rates (King et al. 2006), whereas high WD are related to low growth rates and to the
development of thick cell walls (Castro-Díez et al. 1998), which makes stems more resistant
to breakage (van Gelder et al. 2006) and to fungi and pathogen attacks (Augspurger 1984).
Height maximum (Hmax) is related to access to light (Westoby 1998; Poorter et al. 2005).
Higher plants intercept on average more light and therefore have potentially faster growth
rates (Poorter et al. 2008). Seed mass (SM) is a crucial feature for dispersion and regeneration
and is related to the competition-colonization trade-off (Coomes and Grubb 2003). Large
seeds provide reserves for successful seedling establishment in poor light or intense
seeds per unit of reproductive effort (Moles and Westoby 2006) and are better colonizers
We selected all woody species appearing in at least 4 of the studied plots. Three traits (LS,
SLA and SM) were measured in the field and/or the laboratory, following standardized
protocols (Cornelissen et al. 2003). The rest (wood density and maximum height) were taken
For each species, we collected 10 leaves from each of 10 randomly chosen trees, covering all
the environmental range of each species in our data set. LS was measured with the program
Image J (Kraft et al. 2010) from scanned (300 dpi) fresh leafs. Leaf mass (for calculation of
SLA) was measured after 3 days drying at 60 ºC. Seeds were also collected from at least 10
fruits taken from different individuals of each species. We also used seed accessions from the
Germplasm Bank of Universidad Técnica Particular de Loja. SM was obtained after 48 hours
drying at 80 °C (Cornelissen et al. 2003). SM of ten species, which could not be collected in
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
the field, were approximated by the average SM of congeneric species recorded in the Kew
STATISTICAL ANALYSIS
We conducted a principal components analysis (PCA) with all the recorded climatic and soil
variables using function rda of package vegan (Oksanen et al. 2013. The first PCA axis (PC1)
accounted for 51 % of the environmental variation and was highly correlated to variation in
climatic conditions, so we use plot scores in this axis as a measure of the mean environmental
Species richness and Simpson’s diversity index was measured in each plot.
of trait values (CWM, Garnier et al. 2004). In addition, we computed functional dispersion
(FDis, Laliberté and Legendre 2010) as a measure of functional diversity, using function
fdisp in the package FD (Laliberté and Legendre 2010). We computed CWM and FDis both
for each individual trait and for all the traits in combination. In addition, to describe
(CVFDis) or each individual trait and for all the traits in combination. To make the
classification, we calculated the Euclidean distance among plots on the basis of their PC1
scores and computed a hierarchical clustering (Ward's minimum variance method) with the
function hclust of package stats (R Core et al. 2013). We partitioned the hierarchical
clustering into nine groups (varying in size from 9 to 15 plots; Spasojevic and Sunding 2012).
To calculate phylogenetic diversity, we first generated a phylogenetic tree for the 58-recorded
taxa using the program Phylomatic and the megatree version R20130707 (Webb and
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Donoghue 2005). Branch lengths were calibrated according to Wikström et al. (2001) using
the bladj algorithm of Phylocom (Webb et al. 2008). We then calculated phylogenetic
diversity for each plot as the mean pairwise distance (MPD) among co-occurring species with
function mpd in package picante (kembel 2010). As is usual in this kind of studies (e.g.,
Kembel and Hubbell, 2006; Kraft and Ackerly 2010, Spasojevic and Sunding 2012), to
quantify overall clustering of taxa on the phylogenetic tree, we computed the standardized
version of MPD, net relatedness index (NRI), comparing the observed MPD for each plot
with the expectations (mean and standard deviation) of a null model of community assembly.
A NRI of zero indicates no difference between observed and null values, values greater than
zero indicate phylogenetic overdispersion and values less than zero indicate phylogenetic
Inference about FDis and NRI was based on the values of FDis and MPD computed for
communities simulated according to a null model based on GLM with fixed abundance and
richness
To determine how the measured variables (e.g. species diversity, mean Bray–Curtis
dissimilarity trait CWM's, difference in FDis, NRI and CV FDis) changed along the
environmental gradient, we fitted OLS regressions, testing both linear and quadratic
responses to plot scores in the PC1.We selected the best-fit using Akaike Information Criteria
(Crawley 2007). All computations were made in the R environment (R Core Team 2014).
RESULTS
Environmental gradient
The first principal component axis (PC1) accounted for 51 % of the variation in the
76
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
the driest month, annual precipitation, soil moisture and also others like pH and slope were
negatively correlated with the PC1 score. Variation in soil organic matter, total nitrogen and
organic carbon were mostly related to PC2, which accounted for an additional 19 % of
Species richness
We recorded 58 species in the 109 plots. The most abundant species were Simira
(Malvaceae) and Caesalpinia glabrata (Fabaceae), which appeared in >40 percent of the
plots. On the other hand, most species (54%) appeared in <5 percent of the plots. Maximum
richness per plot was 14 species, with a median of 4 species per plot.
We did not find intraspecific trait correlations except for the case of Hmax and LS (r = 0.3, p =
0.02).
Communities at the stressful end of the abiotic gradient (higher PC1 scores) tended to be
significantly higher in stature, with higher wood density. LS and SLA were largest at medium
environmental conditions and decreased to wards both ends of the environmental gradient
(quadratic relationship). Seed mass did not varied along the environmental gradient (Fig. 1).
77
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0
200 20
150 15
100
10
50
5
-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0
Less stressful More stressful
Enviromental gradiente
Seed mass
50
40
30
20
10
0
-1.0 -0.5 0.0 0.5 1.0
Less stressful More stressful
Enviromental gradiente
Figure.1. Community-weighted mean (CWM) trait values along the stress–resource environmental gradient
(principal components analysis component 1. Community- weighted Maximum height (m) (a: F11,107 = 6.88, R2
= 0.05, P = 0.01), Wood density (g. cm–3) (e: F1,107 = 19.81, R2 = 0.15, P<0.001), leaf size (cm2) (b: F2,106= 5.96,
R2 = 0.08, P = 0.004) Specific leaf area (cm2. g–1) (d: F1,106 = 6.83, R2 = 0.10, P = 0.002).
For all traits, most communities showed functional diversity concordant with the expectations
of the null model of community assembly considered. In some cases, however, some plots
showed overdispersion or underdispersion for some traits. The trait for which most plots
deviated from the expected null FDis was wood density, for which 9% and 15 % of plots
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
(n=10 and n=16) showed respectively over- and under-dispersion. Maximum height was the
trait for which there were the least deviations (only six over-dispersed and one under-
-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0
0.06
0.1
0.04
0.0 0.02
0.00
-0.1
-0.02
-0.2 -0.04
-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0
Less stressful More stressful
Enviromental gradiente
Seed Mass
0.3
0.2
0.1
0.0
Figure. 2. Functional diversity (FDis) for individual traits along a stress–resource environmental gradient
(principal components analysis component. We represent for each plot the difference between observed
(FDisobs) and the expected (FDisnull) functional diversity according to null model based on GLM with fixed
abundance and richness of community. The dashed line represents the expected difference whereas values larger
79
Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
and smaller than 0 indicate respectively over- and under-dispersion of FDis in respect to the null model.1).
Functional diversity significantly increased with increasing water stress only for leaf area (a: F 1,106 = 3.87, R2 =
0.03, P < 0.05). Black symbols represent communities where functional diversity significantly differed (p <
0.05) from the null expectation; white symbols represent communities where the observed functional diversity
was not significantly different from the null expectation.
When FDis was computed from all traits combined, only five plots showed overdispersion
and eleven underdispersion (Fig. 3). The deviations from the expected FDisNULL occurred
uniformly along the whole environmental gradient for al traits except for leaf size, for which
functional diversity decreased towards the stressful end of the environmental gradient (Fig.2).
As in the case of the combined FDis, there were more underdispersed (14) than overdispersed
(5) cases among the plots that deviated from the expected phylogenetic diversity (as
estimated by NRI; Fig 3). Similarly, these deviations occurred along the whole environmental
gradient.
0.05 4
3
FDIS obs - Fdis null
Functional diversity
0.00 2
NRI
0
-0.05
-1
-2
-0.10
-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0
Fig. 3. Multivariate functional diversity (FDis) (principal components analysis component 1) and phylogenetic
diversity [net relatedness index (NRI)] did not change along the stress–resource environmental gradient than
null model. Black points represent plots where functional or phylogenetic diversity were significantly different
from the null model. The dashed line represents null functional diversity where negatives values indicate greater
functional diversity than null and positive values indicate less functional diversity than null.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Functional diversity of all traits was highly variable among communities (CVFDis F2,7 = 10.3,
R2 = 0.67, P = 0.008) at the stressful end of the environmental gradient. Variability among
communities diminished (lower CVFDis) towards the less stressful end of the gradient for SLA
(F2,7 = 7.49, R2 = 0.59, P = 0.01). CVFDis did not change over the environmental gradient for
leaf area (F1,9 = 4.14, R2 = 0.24, P = 0.07), wood density (F1,9 = 0.99, R2 = <-0.001, P = 0.42),
maximum height (F2,8 = 7.49, R2 = 1.39, P = 0.30) and seed mass (F2,8 = 0.22, R2 = -0.18, P =
0.80).
DISCUSSION
The study of shifting patterns in functional and phylogenetic diversity along environmental
gradients has been used to understand the mechanisms ruling community assembly and in
particular, the role of habitat filtering and limiting similarity (e.g. Spasojevic and Suding
2011; May et al. 2013; Kraft and Ackerly 2010). Robust evidence shows that both functional
diversity and phylogenetic dispersion are usually low under strong abiotic stress, and that
they increase in regions with mesic conditions and more competitive interactions (e.g.
Weiher and Keddy 1995; Corwell and Ackerly 2009). However, some processes such as
facilitation can modify this pattern due to the fact that positive interactions tend to occur
between phylogenetic and functional distant species (Valiente-Banuet and Verdú 2007)
increasing the functional diversity and phylogenetic dispersion and therefore shifting the
expected pattern under the more general theoretical framework. In our tropical dry forest we
found evidences of the more general pattern only with respect to the diversity of leaf size,
On the other hand, when multivariate functional and phylogenetic diversity were evaluated
they did not showed significant variation along the environmental gradient..
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Interesantly, although functional and phylogenetic diversity showed no variation, the CWM's
for most traits were affected by the environmental gradient. CWM quantifies the dominant
trait values in a community and is consequently closely related to the ‘‘mass ratio
hypothesis’’ (Grime, 1998), which propose that ecosystem processes are mainly determined
by the functional traits of dominant species in a community (i.e. functional identity). The sign
of the CWM-environment relationship for some traits (e.g., Hmax and WD) is the same to the
sign found for the relationship between the unweighted community averages and annual
precipitation in another study (Gusmán et al. in revision) and points to habitat filtering as the
main process governing community assembly around these traits. In the case of SLA, we
found that the CWM decreased with favorable environmental conditions, as in the
unweighted analysis, but was better described by a quadratic relationship, i.e., CWM for SLA
were higher for intermediate environmental conditions and decreased towards both the
stressful and the favorable extremes of the gradient. The same relationship was found for the
CWM of leaf size. In our analyses, the CWM for seed mass was not significantly related to
environmental variation, but excluding two-outlier plots from the analysis, we found the
same relationship that we have reported to the unweighted case. The changes in the CWM
could be due stress tolerance of plants as response to habitat filtering (Weiher and Keddy
1995; Cornwell and Ackerly 2009; Lebrija-Trejos et al. 2010) and/or the equalizing fitness
In the stressfull habitats, leaf size and SLA are reduced probably as a response to low water
availability (Hulshof et al. 2013), i.e, as a consequence of habitat filtering. Although the
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
more competitive small LS and SLA values, this should be accompanied by a decrease in
functional diversity of these traits, which does not happen (in fact there is a significant
increase of FDis for leaf size towards the more benign end of the environmental gradient). A
more plausible explanation for this decrease of CWM values for LS and SLA at the less
stressful in the case of leaf area our results showed effects of habitat filtering, the functional
diversity was low in the stressful habitats and the mean leaf area was smaller in drier sites, a
result consistent with other studies at local and regional scales (Parsons 1976; Wilf et al.
1998; Fonseca et al. 2000). The functional significance of leaf area is not entirely clear
(Corwell and Ackerly 2009). Leaf area can influence the thermal conductance of the leaf.
High leaf area serve to keep leaves with low temperature through evaporative cooling, this
mechanism is efficient under high water availability (Corwell and Ackerly 2009). At dry
sites, where limited soil water may lead to stomatal closure on a daily basis, closed stomata
and large leaves could lead to high and potentially damaging leaf temperatures (Givnish and
Vermeij 1976).
response to environmental stress (Norberg et al. 2001; Suding et al. 2008; Cadotte et al. 2009;
Flynn et al. 2011). Although we found evidences for habitat filtering in the average values
taken by most traits along the stress gradient (measured as CWN), no evidence that functional
diversity shifted along the environmental gradient was found for any trait except for leaf size.
functional diversity (Mouchet et al. 2010) and phylogenetic clustering (this one in case that
traits related to abiotic stress are phylogenetically conserved, as is usually assumed (Webb et
al. 2002, Kembel 2009). This hypothesis ignores facilitation or assumes that its effects will be
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
(Mason et al. 2013). However, there exists evidence about the dominant role played by in
structuring communities in stressful habitats (McAuliffe 1988; Tirado and Pugnaire 2005;
Valiente-Banuet et al. 2006). Espinosa et al. (2013, 2015) showed that in the interandean dry
shrublands and tropical dry forest facilitation shifts along environmental gradients, with an
increase of its effects towards more stressful conditions. Facilitation often allows the
coexistence of species (Callaway et al 2002; Brooker et al. 2008; Butterfield 2009) with
et al. 2006), which can increase phylogenetic dispersion and the functional diversity in the
CONCLUSIONS
The assumption that habitat filtering reduced the functional diversity (Weiher and Keddy
1995; Cornwell and Ackerly 2009) and phylogenetic dispersion (Webb et al. 2002; Cavender-
Bares et al. 2004; Kraft et al. 2007) in stressful environments, and that limiting similarity
(MacArthur and Levins 1967; Chesson 2000) ignores the importance of other alternative
found evidences of habitat filtering in the values taken by most traits along the stress gradient
(measured as CWN), no evidence that functional diversity shifted along the environmental
gradient was found for any trait except for leaf size. The usual decline of LS at along
deciduous plants to thick, small-leaved, perennial species (Corwell and Ackerly 2009). Other
factor is the increased leaf nitrogen in arid environments, as an adaptation to prevent water
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
loss by allowing stomata to remain closed for longer periods of time (Wright et al. 2001,
2005).
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
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CAPÍTULO 3
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RESUMEN
Una aproximación que ha resultado ser eficaz para cuantificar la influencia de los procesos
espaciales. Hemos encontrado que a escalas espaciales pequeñas, las especies que coexisten
son funcionalmente mas agrupadas, además existe una relación positiva entre la dispersión
indique existe una conservación de los rasgos funcionales en este tipo de bosque.
Nuestros hallazgos sugieren que la co-ocurrencia de especies fue impulsada por el filtrado de
hábitat a escalas pequeñas donde hubo mayor agrupación de lo esperado por el azar. Es decir
la piscina de especie.
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INTRODUCCIÓN
al. 2012). Algunos autores argumentan que una aproximación efectiva para cuantificar la
Los rasgos funcionales y la filogenia de las especies deberían ser aleatorios en la comunidad,
estructura de la comunidad (Hubbell 2001). Por otro lado, modelos deterministas afirman la
esta forma la estructura de la comunidad debe ser no-aleatoria con respecto a los rasgos
funcionales y a su filogenia (por ejemplo, Swenson y Enquist 2009; Kraft y Ackerly 2010;
tanto por condicionantes bióticos como abióticos. Mientras las interacciones bióticas (como
funcionales, las interacciones abióticas (por ejemplo el filtrado ambiental) conducen a la baja
2009). Bajo este mismo enfoque cuando analizamos la diversidad filogenética de una
comunidad se espera que las especies estrechamente relacionadas puedan ser ecológica y
2009). Por ejemplo, si los rasgos funcionales se conservan filogenéticamente, las especies co-
ocurrentes estarán más relacionadas de lo esperado por el azar (Webb et al. 2002). Sin
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funcional y filogenética.
2013). Por ejemplo en bosques tropicales el filtrado de hábitat parece ser más importante a
predecibles (Shipley et al. 2012), por otra parte, el límite de similitud, es a menudo más
importante a escalas más pequeñas donde las interacciones competitivas entre los vecinos
Con fin de obtener una visión más profunda de los mecanismos que promueven el ensamble
de las comunidades, nosotros evaluamos si el rol de los rasgos funcionales de las plantas en
Específicamente nos interesa entender (1) ¿Cómo influye la escala espacial en la relación
positiva entre estas dos medidas y que se torne negativa en escalas espaciales más grandes.
espacial?. Esperamos que el ensamble de las comunidades de bosque seco sea diferente a un
ensamble aleatorio de las especies del territorio, como consecuencia de filtrados bióticos o
abióticos. Así, a escalas cortas esperamos una mayor dispersión de caracteres como efecto de
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filtrado del ambiente. Finalmente, queremos entender. (3) ¿En qué medida la dispersión de
MÉTODOS
Área de Estudio
Arenillas y Huaquillas y cubre 131,7 Km2 (Decreto Ejecutivo No. 787) con una altitud que va
de 0 a 300 m. Esta zona pertenece a la región biogeográfica Tumbesina, una de las zonas más
amenazados (Best y Kessler 1995). El clima se caracteriza por una temporada de lluvias
(enero a abril), con una precipitación media de 515 mm y sólo 152 mm de promedio durante
máxima de 3.4 ºC entre los meses más fríos y más cálidos. La temperatura más baja se da
Dentro de una zona muy bien conservada en el centro de la REA conocida como 'Pintag
Nuevo' instalamos una parcela permanente en 2009. Esta área se caracteriza por una
formación de transición entre los bosques secos caducifolios y matorrales secos de tierras
bajas. Las especies de árboles más conspicuos de la zona son; Tabebuia chrysantha y
Tabebuia bilbergii (Bignoniaceae), junto con otras especies como Colicodendron scabridum
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(Capparaceae) y Croton sp. (Euphorbiaceae). De enero de 2010 a mayo del 2011 delimitamos
una parcela cuadrada de 9 hectáreas, subdivida en 225 subparcelas de 20x20 metros (400 m2).
Todos los individuos arbóreos con un diámetro a la altura del pecho (DAP) igual o mayor a
5cm fueron registrados. Cada individuo fue identificado y determinada su posición espacial.
Altura máxima de la planta está relacionada con el acceso a la luz (Westoby 1998; Poorter et
al 2005). Las plantas más altas interceptan en promedio más luz y por lo tanto tienen tasas de
encuentra relacionada con la eficiencia y el transporte del agua (Cornwell y Ackerly 2009) y
con el crecimiento y la supervivencia del individuo. Baja densidad de la madera suele estar
relacionada con altas tasas de crecimiento del tallo (King et al., 2005), mientras que altas
Díez et al. 1998) mejorando la resistencia de los tallos a la rotura (van Gelder et al. 2006) y a
están fuertemente conectados con el área foliar específica (SLA, siglas en ingles). Esta
característica representa un eje "económico" de variación que va desde las especies típicas de
los hábitats ricos en recursos, con altas tasas metabólicas y cuyos atributos mejoran la rápida
adquisición de carbono fotosintético (alta SLA), a las especies que toleran hábitats y recursos
limitados que tienden a mostrar atributos opuestos (Walters y Reich 1999; Poorter y Bongers
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2006). La Masa seca de la semilla (MSS, siglas en ingles) es una característica crucial para la
(Kitajima 2002). Por el contrario, las especies con semillas pequeñas son mejores
arbustos. El área foliar se midió con el programa Image J (Abramoff et al. 2004; Kraft and
Ackerly. 2010). El área foliar específica se calculó como el área de lámina de la hoja dividida
por la masa seca de la hoja (48 horas de secado a 80 ºC), para las especies de hojas
desplazamiento de agua que consiste en secar las muestras a 80 °C, hasta que las muestras
m/v: donde m= masa seca y v= al volumen). Para las especies que no fue posible calcular la
densidad de la madera directamente, se utilizó la base de datos de Chave et al. (2009). Para la
obtención de los datos de masa de las semillas recogimos muestras de al menos 10 individuos
de cada especie. Las semillas fueron secadas durante 48 horas a 80 °C, luego de lo cual
fueron pesadas según lo propuesto por Cornelissen et al (2003). La masa seca de la semilla de
algunas especies que no pudieron ser recogidas en el campo, se aproximó su valor en base a
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Análisis estadístico
(Ripley 1976; Illian et al. 2008). Nuestro ajuste de modelo se basa en minimizar una medida
presentada en Wiegand et al. 2012. Nosotros calculamos el patrón espacial de cada especie
con el patrón esperado en base a cuatro modelos (Poisson homogéneo (HPP), Poisson
inhomogéneo (IPCP)) (Shen et al. 2009, Lin et al. 2011). Una descripción detallada de los
Para seleccionar el modelo que mejor se ajustó a cada especie usamos el ajuste de bondad de
espaciales (20, 50, 500, 2000 y 10000 m2). Dentro de cada cuadrante se cuantificó la riqueza
de especies (SR siglas en ingles), dispersión funcional (FDis siglas en ingles) que es la
filogenética de especies (PSV siglas en ingles ). El PSV resume el grado en que las especies
cada escala espacial. Utilizamos el modelo espacial con mejor ajuste para cada especie
(Apéndice 2) para construir los modelos nulos. Para cada uno de estos conjuntos calculamos
la dispersión funcional generando una distribución nula. Esta distribución nula se utilizó para
testamos si la mediana de Ztd para todos los cuadrantes REA era diferente de una expectativa
Todos cálculos se efectuaron utilizando el entorno R (R Core Team 2013) y los paquetes
“spatstat” (Baddeley y Turner 2005), “ecespa” (de la Cruz 2008a), “FD” (Laliberté et al.
RESULTADOS
Inicialmente encontramos una relación positiva entre la dispersión funcional de los rasgos y
escalas espaciales mayores. En el caso de Masa seca de la semilla la relación fue positiva en
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todas las escalas espaciales (Fig. 1). Nosotros encontramos que existió una relación positiva
significativa en escalas cortas (0-100m2) para casi todos los rasgos funcionales excepto para
altura máxima. En el caso de Masa seca de la semilla fue significativo en casi todas las
1.0
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comunidad en cada escala espacial. Círculos negros indican correlaciones significativas (P ≤ 0.05).
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Spearman's rho
Área en m2
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mayor agrupamiento con respecto a lo esperada por el azar (Fig.2). Para la riqueza de
especies encontramos que la desviación fue significativo en escalas entre 0-1000 m2. En el
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
tamaño de la hoja fueron significativos también a escalas espaciales de 40-100m2, para SLA
FDIs PSVs SR
1.0
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area area
Figura 2. Desviación de las comunidades al modelo nulo a diferentes escalas espaciales. Los valores
por encima de la línea indican desviaciones positivas (dispersión de rasgos) y los valores por debajo
de la línea desviaciones negativas (agrupamiento de rasgos). Círculos negros indican desviaciones
significativas del modelo nulo mediante una prueba de Wilcoxon. (P ≤ 0.05), área en m2
Finalmente encontramos que existió una relación positiva significativa entre la dispersión
negativa significativa a escalas espaciales mayores (Fig. 3). En cuanto a la relación entre la
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
1.0
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Spearman's rho
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area area
DISCUSIÓN
conjunto en escalas cortas muestran agrupación funcional (Fig. 2), sugiriendo que las
subconjunto funcional en la piscina de especies (Webb et al., 2002). La filtración del medio
ambiente ocurra cuando las especies comparten tolerancias similares (Cavender-Bares et al.
2004, 2006), es decir ocupan el mismo tipo de entornos (Donoghue 2008), como por ejemplo
comunidades, y por lo tanto, las especies concurrentes deben ser funcionalmente más
similares.
En el caso de la diversidad filogenética encontramos que las especies fueron mas similares
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
comparten rasgos similares (Kraft et al. 2007; Losos et al. 2008), mientras que las especies
relacionadas lejanamente difieren en sus rasgos funcionales (Webb et al. 2002; Swenson and
Enquist 2009). Sin embargo este patrón puede cambiar a escalas espaciales mayores donde la
diversidad filogenética es mas dispersa, es decir que las especies que se encuentran en estos
donde las especies que se encuentran en estas escalas deben ser menos similares.
filogenético (Srivastava et al. 2012; Mouquet et al. 2012; Losos et al. 2008). Desde una
cambios ambientales (Mouquet et al. 2012; Sgro, et al. 2011). Esta relación entre la
diversificación evolutiva ha generado la diversificación del rasgo, que a su vez puede dar
Conclusión
En las 9-ha de la REA, nuestros resultados demuestran que funcionalmente las especies son
funcional en la piscina de especie. Los resultados también apoyan la hipótesis de que las
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En este proceso se define por su intensidad λ que normalmente se aproxima como λ = n / A, es decir,
denota la intensidad del patrón y describe el número medio de los puntos localizados en una unidad de
superficie, es decir, la densidad media de árboles por unidad de área para cada especie (Plotkin et al.
2000, Shen et al. 2009). K(r) es el número esperado de puntos en un círculo de radio r alrededor de
corrección de borde, y la función indicador I. El HPP tiene una intensidad constante a lo largo del área
de estudio y la distribución de los puntos es independiente, por lo que el valor esperado es K(r) = πr 2
Procesos Poisson clúster puntos no-independientes (agrupados) en un proceso de dos pasos. Primero,
se genera un HPP de puntos “padres” con intensidad. Luego cada “padre” produce un número
aleatorio de “descendientes” que se distribuyen de acuerdo a una ley de Poisson, con media =/,
isotrópica y normalmente distribuidos alrededor de cada árbol padre, con media cero y desviación
Los parámetros y son usualmente ajustados comparando la función K empírica con la función K
teórica, mediante el método de mínimo contraste (Stoyan y Stoyan 1994, Diggle 2003). De esta
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forma, la agregación del patrón es cuantificada por (número medio de grupos), y el tamaño medio
de los grupos está dado por . El PCP considera la distribución de descendientes como una función
de dispersión limitada y asume homogeneidad, sin embargo las características que conlleva esta
asociación de hábitat (Gunatilleke et al. 2006, Wiegand et al. 2007b, Morlon et al. 2008).
El IPP supone la formación del patrón en dos etapas, primero se genera un patrón de Poisson
homogéneo, luego los puntos del patrón son retenidos con una probabilidad proporcional a la
ambientales, esa superficie es estimada con una función kernel. Este proceso puede ser utilizado para
examinar los efectos de interacción entre la densidad de árboles y los factores ambientales (Shen et al.
(x) puede ser estimada en diferentes formas. Aquí utilizamos el método basado en “kernel
donde k(u) es una función kernel arbitraria y e(u) es término de corrección de borde. Utilizamos
Como una alternativa al IPP, es considerado también una extensión del HPCP, donde la distribución
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de los puntos además de ser agrupada es heterogénea. Waagepetersen (2007) considera un proceso
cluster X=XcY donde Xc son los cluster de los “descendientes” asociados a los puntos “padres” c en
un proceso de Poisson estacionario Y con intensidad > 0. La función de intensidad de X tiene forma
log-lineal, y el valor esperado para la función K heterogénea tiene la misma forma que para el HPCP.
Este proceso es adecuado para evaluar el efecto conjunto de heterogeneidad de hábitat y dispersión
limitada (Diggle 2003, Illian et al. 2008), de forma similar al HPCP, excepto por el número de
descendientes por padre, el cual ya no es una constante, sino que debe ser estimado a través de una
función de intensidad espacialmente heterogénea (Waagepetersen 2007, Yi-Ching Lin et al. 2011).
Los modelos fueron equipados con código basado en la spatstat paquetes R (Baddeley y Turner 2005)
y ecespa (De la Cruz, 2008). Proporcionamos este código y ejemplos de su uso en un nuevo paquete
Ripley (Ripley, 1978). Todas las funciones se estimaron hasta 75 m (es decir, r max = 75 m), con
pasos de 1 m.
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Appendice 2:
Tabla.1: valores de ajuste de bondad de u (gof-u) de los diferentes modelos adaptados a cada especie
IPCP: Proceso de agrupación de Poisson no homogénea; IPP: Procesos de Poisson no homogéneo
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Plotkin, J.B., Potts, M.D., Leslie, N., Manokaran, N., LaFrankie, J. y Ashton, P. 2000. Species-area
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explained by the joint effects of dispersal limitation and hábitat heterogeneity. Ecology 90(11):
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Stoyan, D. y Stoyan, H. 1994. Fractals, Random Shapes and Point Fields. Wiley, Chichester.
Wang, X., Wiegand, T., Wolf, A., Howe, R., Davies, S. J. y Hao, Z. 2011. Spatial patterns of tree
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CAPÍTULO 4
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ABSTRACT
Recently, ecologists have moved from measuring diversity as the species richness and
evenness, to using measures that reflect ecological differences as use of the functional and
species richness in local neighborhoods around the individuals of a focal species within a
dependent, local functional diversity structures around individual species, and individual
phylogenetic distance between species. We have used these tools in a dry forest in south of
Ecuador.
Our results showed that at all the spatial scales considered for ISAR, IFDAR and IPSVAR,
most species behaved as ‘neutral’, i.e. they are surrounded by the expected richness. Some
species in IFDAR (39%), IPSVAR (17%), were accumulator the functional and phylogenetic
diversity, suggesting the existence of a process of limiting similarity, i.e. the species are more
functionally different than expected. A small proportion of species was repeller of functional
and phylogenetic diversity than expected, suggesting the existence of an additional process
habitat filtering.
functional and phylogenetic diversity, may help us understand the co-occurrence of species in
diverse assemblages. These results suggest that some species showed a different behavior to
the plant-plant interactions, where the abiotic interactions and environment are important in
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INTRODUCTION
Historically, species richness has been the most common metric used to characterize local
can be achieved by studying simultaneous the three diversity, taxonomic, functional and
phylogenetic (Swenson 2011). For example, use of only the taxonomic diversity for
ecosystem processes (Hooper and Vitousek 1997; Tilman and Downing 1994; Tilman et al.
phylogenetic distance among species in a community (Faith 1992) and provides a measure of
hypotheses about the abiotic and biotic factors structuring communities (Helmus et al. 2007).
During the past decade ecologists have increasingly utilized phylogenetic and functional
traits information to estimate the ecological similarity of species in order to test mechanistic
consider functional traits to be better predictors of diversity (Tilman et al. 1997; Cadotte et al.
2009; Flynn et al. 2011; Helmus and Ives 2012). A common idea in the study of ecology is
that taxonomic, functional and phylogenetic diversity are positively correlated, that is,
accounting for one of these components also accounts for the others. However, recent studies
(Cadotte et al. 2013; Pavoine and Bonsall 2011; Pavoine et al. 2013) suggested that these
components might also represent independent aspects of community structure (Dainese et al.
2015).
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Have developed newfangled statistical analysis for the plant diversity study, by using spatial
patterns, as is the use of ISAR (His Individual Species–Area relationship) that computes
species richness in local neighborhoods around the individuals of a focal species within a
this must be done with caution and only after partialling out the possible existence of other
mechanisms, which can give also similar spatial signals (Espinosa et al.2015). Both
accumulators and repellers have been taken as evidence for non-neutral or niche- based
processes influencing the distribution and diversity of tree species in forest communities.
Conversely if the species diversity around a target individual does not deviate significantly
from that expected, this is taken as evidence for neutrality (Wiegand et al. 2007). The
proportion of these plant types and abundance within a community could shed light on the
aggregations of plants are often interpreted as a result of positive plant-plant interactions that
are generally considered to play a prominent role in semiarid plant community dynamics
because of harsh climate and scarce resources in these environments (Schlesinger et al. 1990;
Despite the clear impact of the approach developed by Wiegand et al. (2007). It has been
expanded this vision of spatial processes occurring in the community assembly, using tools
such measure of functional and phylogenetic diversity as the IFDAR (Individual functional-
Relationship).
The IFDAR quantifies the functional diversity and the IPSVAR the phylogenetic diversity of
species within circular areas around a target individual of a species. The IPSVAR is then
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compared with the expected random ratio taking into account the phylogenetic diversity of
species observed in the neighborhood, and IFDAR is compared with the expected random
ratio taking into account the traits diversity of species observed. The simultaneous
comparison of these functions and null models will give new insights of the process and
timing implied in the organization of the forests (Helmus and Ives 2012).
The aim of this study is to evaluate the species behavior in the three levels of diversity using
ISAR- for the level taxonomic, IFDAR for the level functional and IPSVAR for the level
phylogenetic. We test these patterns in the Neotropical dry forest, this ecosystem is especially
interesting because it is periodically subjected to a strong abiotic stress, which has led to
species develop patterns and morphofunctional adaptations. Some studies have showed that
in this ecosystem, the facilitation is stronger under stress conditions and it reduced when
conditions improve (e.g. Espinosa et al. 2014, 2011), additionally, to local scales Espinosa et
al. (2015) found interesting evidence that to local scales exist different processes acting such
plant-plant interactions define structure in our dry forest community and if it is mediated by
habitat filtering or limiting similarity, or both, and 2) to what extent the environmental
expected that species would present accumulator or repeller behavior at the taxonomic level.
interactions are mediated by limiting similarity at the same scale, we expected that the
species would present the same behavior at functional and phylogenetic levels. Conversely if
species show repeller behavior at taxonomic level, and this behavior is mediated by habitat
On the other hand, if environmental conditions rather than plant-plant interactions define the
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predominant.
Methods
Study Site
The study was conducted in the Arenillas Ecological Reserve (REA, from its Spanish name),
province, between the towns of Arenillas and Huaquillas. This reserve covers 131,7 Km2
(Decreto Ejecutivo No. 787), with an altitude ranging from 0 to 300 m. The climate is
characterized by a rainy season with an average annual rainfall of 515 mm from January to
April (wet season) and only 152 mm on average during the eight-month dry season (weather
station Huaquillas for a record period of 45 years (1969-2014)). The average temperature is
21-25 °C with a maximum variation of 3.4 ºC in the coldest and warmest reaching the lowest
temperature during the dry season. These dry forests are considered the most threatened
In the center of the REA in 2009, a permanent plot of 9 hectares was set up and marked all
trees and shrubs greater than 5 cm and identified. During the dry season (July to September
2010 and 2011) were mapped using a total station, Leica TS02-5 Power model with less than
5 cm accuracy.
The following functional traits were collected for 38 species between trees and shrubs that
growing in the permanent plot the traits were: maximum height (Hmax) (is the distance
between the top of photosynthetic tissue and the ground), leaf area (in square centimeters),
specific leaf area (SLA, in square centimeters of fresh leaf area per gram of dry leaf mass),
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wood density (in grams per square centimeter) and seed mass (in grams). The traits were
species, we randomly collected 10 leaves from each of 50 individuals. Leaf area was
measured with the program Image J (Abramoff et al. 2004; Kraft et al. 2010). Specific leaf
area was calculated, as the fresh leaf area divided by the leaf dry mass (48 hours drying at 80
ºC), for species of compound leaves the rachis was included. They were collected during the
phenologic peak. To estimate wood density secondary branches of three individuals were
collected with size in circumference ranging from 10 to 20 cm, fresh wood volume was
determined with the water displacement method (Chave 2006), after which samples were
oven-dried at 80ºC and weighed for species that we could not calculate the wood density, was
used the database of Chave et al (2009). Seed mass was recorded of the Kew Millennium
Phylogeny construction
A phylogenetic tree was constructed for these 38 species in the plot, using Phylomatic (Webb
and Donoghue 2005). Phylomatic utilizes the Angiosperm Phylogeny Group III (APG III
2010). Taxonomic relationships (family, genus and species) are pasted onto this backbone to
estimate the phylogenetic tree. Branch lengths were estimated for each tree using the BLADJ
algorithm implemented in Phylocom (Webb et al. 2008), to adjust the length of the branches
of the phylogeny with known ages of fossils of plants (Wikström et al. 2001). The ''ape”
library was used to import and manipulate the phylogeny, as required in R (Paradis 200, R
Development Core Team 2009). Our metric used for of phylogenetic analysis was
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To select appropriate null models for each species, we followed an approach conceptually
similar to the pattern reconstruction strategy of Wiegand et al. (2013) and implemented in
Chacón et al. (2013). We first fitted a battery of different spatial null models for each species:
(1) a homogeneous Poisson process (HPP) with constant intensity λ equal to the density of
the observed pattern; (2) a homogeneous Poisson cluster process (HPCP) with constant
intensity λ and parameters σ and ρ fitted by minimum contrast (Diggle 2003); (3)
heterogeneous Poisson processes (IPP) with an intensity function λ (x,y) estimated with a
Gaussian kernel (Wiegand et al. 2007) with 13 different σ values (bandwidths) from σ = 15 to
(IPCP) (Waagepetersen 2007) with sigma-values similar to IPP. A detailed description of the
the thesis. We performed 199 simulations for each null model. To avoid difficulties due to
small sample size we only calculated functions for species with at least 10 individuals.
Best model for each species was selected with the goodness-of-fit u statistic (Diggle 2003;
We analyzed our community in three dimensions: Taxonomic using the ISAR, functional by
For taxonomic diversity first, we computed ISAR for ‘adult’ individuals with DBH 10 cm,
which in our ecosystem is the dominant life stage (Linares-Palomino and Ponce-Alvarez
2009); these functions summarize how community richness is organized around individual
evaluated against the expectations of some assumed ecological processes and corresponding
null models, for example, if competitive effects were ruling the structure of a community, we
contrary, if only habitat filtering is affecting the assembly process, we should find that most
species have small values of FD in their neighborhoods. Even more if several processes were
simultaneously ruling the community assembly, IFDAR could detect there differential
effects, at least when these are occurring at contrasting spatial scales (De la Cruz in prep).
IFDAR is able to detect both positive and negative deviations of functional diversity from the
IPSVAR is then compared with the expected random ratio taking into account the
phylogenetic diversity of species observed in the neighborhood, closely related species might
have similar tolerances to similar environmental stressors and thus be more likely to occur
within the same community than with less related species (e.g., Webb 2000). Conversely,
closely related species might share the same resource requirements, and therefore
competition could prevent similar species in the same community (Elton 1946).
The goodness of fit of the models were evaluated in three ranges of radius 0 to 20 m; 21 to 40
m and 41 m- 60 m, to test for differences between the observed pattern and the null model
All calculations were done using the R statistical software, version 3.1.0 (R Development
Core Team, 2014). The ISAR analyses were implemented using the statistical package
‘‘idar’’ (De la Cruz, in prep.). The randomization process was simulated using the packages
‘‘spatstat’ (Baddeley and Turner 2005), ecespa (De la Cruz, 2008) and “picante” (Kembel et
al. 2010).
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Results
We tagged and georeferenced 9479 individuals with DBH greater than 5 cm in the 9-ha plot.
The best fit for spatial patterns were homogeneous Poisson cluster for fourteen species, and
homogeneous Poisson processes for nine species (Appendice 1). In all cases, the best models
included intensity surfaces estimated from their own patterns with Gaussian kernels.
Considering the ranges of radius r= 0–60 m, the most prevalent behavior for the 23 species
was neutral for ISAR with 57%, (13 species); IFDAR 60 % (14 species); and 70 % (16
100
100
neutrals
accumulators
repellers
80
80
80
Percentage of cases
Percentage of cases
Percentage of cases
60
60
60
neutrals neutrals
accumulators accumulators
repellers repellers
40
40
40
20
20
20
0
0 20 40 60 0 20 40 60 0 20 40 60
Figure1: Proportion of significant accumulator, repeller and neutral species for ISAR (Individual
Species-Area Relationships), IFDAR (Individual Functional-Diversity–Area Relationship) and
IPSVAR (Individual Phylogenetic Species Variability Area Relationship) in the REA, in a radius of
0-60 m.
For ISAR (taxonomic diversity) six species were accumulators (26%) in all spatial scales
(r=0-60 m), and Chloroleucon mangense was the only repeller of diversity in all-spatial
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
scales. In IFDAR (functional diversity) one species were accumulators (Jacquinia sprucei)
and one repeller (Armatocereus sp) of diversity (4%) in all-spatial scales (r=0-60 m). With
respect IPSVAR only was accumulator and repeller in certain spatial scales (Table 2).
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Table 2. p-values of the GoF u test for three spatial ranges: 0–20, 21–40 and 41–60 m. Grey background: species that behaved as accumulators in the
evaluated range. Black background: species that behaved as repellers in the evaluated range. Neutral behavior is showed as white cells and n.c. indicates that
ISAR, IFDAR and IPSVAR, were not calculated.
Achatocarpus pubescens 0.91 0.94 0.16 0.94 0.02 0.05 0.56 0.52 0.64
Armatocereus sp. 0.16 0.41 0.5 0.01 0.01 0.01 0.15 0.04 0.04
Bursera graveolens 0.24 0.07 0.1 0.56 0.85 0.9 0.1 0.11 0.16
Caesalpinia glabrata 0.01 0.01 0.03 0.42 0.38 0.66 0.95 0.48 0.1
Chloroleucon mangense 0.01 0.01 0.01 0.1 0.04 0.01 0.68 0.05 0.24
Coccoloba ruiziana 0.15 0.29 0.05 0.65 0.7 0.23 0.34 0.65 0.44
Cochlospermum vitifolium 0.2 0.07 0.11 0.72 0.29 0.69 0.48 0.13 0.04
Colicodendron scabridum 0.57 0.07 0.14 0.09 0.77 0.35 0.31 1 0.48
Croton sp 0.33 0.63 0.9 0.09 0.38 0.37 0.07 0.62 0.39
Cynophalla mollis 0.01 0.01 0.01 0.03 0.38 0.16 0.7 0.07 0.01
Eriotheca ruizii 0.01 0.01 0.02 0.05 0.48 0.67 0.69 0.45 0.91
Erythrina velutina 0.36 0.14 0.13 0.02 0.37 0.99 0.79 0.07 0.08
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Erythroxylum glaucum 0.02 0.39 0.43 0.33 0.76 0.59 0.51 0.8 0.7
Geoffroea.spinosa 0.01 0.01 0.01 0.13 0.42 0.84 0.53 0.84 0.11
Jacquinia sprucei 0.01 0.01 0.01 0.01 0.01 0.01 0.05 0.01 0.01
Leucaena trichodes 0.57 0.41 0.64 0.12 0.67 0.56 0.04 0.5 0.94
Malphigia emarginata 0.01 0.01 0.02 0.01 0.51 0.1 0.21 0.26 0.66
Piptadenia flava 0.27 0.19 0.42 0.20 0.07 0.59 0.04 0.59 0.82
Pisonia aculeata 0.05 0.54 0.71 0.46 0.78 0.68 0.43 0.15 0.52
Pithecellobium excelsum 0.28 0.02 0.01 0.5 0.04 0.05 0.21 0.09 0.08
Tabebuia billbergii 0.55 0.13 0.09 0.01 0.07 0.49 0.57 0.52 0.64
Tabebuia chrysantha 0.12 0.46 0.35 0.12 0.3 0.44 0.08 0.37 0.41
ISAR (Individual Species–Area Relationship), IFDAR (Individual Functional-Diversity–Area Relationship) and IPSVAR (Individual Phylogenetic Species Variability Area
Relationship).
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
In ISAR some species showed different spatial patterns depending on the proximity to the target
plant. For example, Erythroxylum glaucum accumulated diversity at short distances (r= 0-20 m)
and Pithecellobium excelsum, accumulated taxonomic diversity at large distances (r= 21-60 m)
(Table 2). For IFDAR five species (22%) accumulated diversity at short distances (r= 0-20 m),
and two species (9%) were accumulators in middle distances (r= 21- 40 m) (Table 2). Finally,
Chloroleucon mangense were repeller of diversity in greater distances (r= 21-60 m) (Table 2).
We found three species (13%) that behaved as accumulators in IPSVAR to large distances
Armatocereus sp. (r= 21- 60 m), Cynophalla mollis and Jacquinea sprucei (r= 41-60). Five
species (26%) behaved as repellers of phylogenetic diversity in the IPSVAR at short distances (4
species) and only one species at large distances (Cochlospermum vitifolium)(Table 2).
Cynophalla mollis showed an accumulator behavior so much for ISAR, IFDAR and IPSVAR in
0.14
30 i psvar ob s (r )
i psvar (r )
i psvar h i (r )
0.12 i psvar l o (r )
25 0.90
0.10
20
0.08
IPSVAR (r )
IFDAR (r )
ISAR (r )
15 0.85
0.06
10
0.04
0.80
5
i sar ob s (r ) 0.02 i f d ar ob s (r )
i sar (r ) i f d ar (r )
i sar h i (r ) i f d ar h i (r )
i sar l o (r ) i f d ar l o (r )
0 0.00
0 20 40 60 0 20 40 60 0 20 40 60
r r r
Figure 2: Proportion of significant accumulators for Cynophalla mollis (a) ISAR (Individual Species–
Area Relationship) in radius of 0-60 m, (b) IFDAR (Individual functional-diversity–area relationship) in
radius of 0-20 m, (c) IPSVAR (Individual Phylogenetic Species Variability Area Relationship) in radius
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
of 40-60 m.
Our results also showed that five out of eight species that showed an accumulator behavior in
ISAR showed the coincident behavior in IFDAR, however the accumulator effect in IFDAR was
Chloroleucon mangense was the only species that behaved as a repeller in the ISAR and IFDAR
(Fig. 3).
0.14
30
0.12
25
0.10
20
IFDAR (r )
ISAR (r )
0.08
15
0.06
10 i sar ob s (r ) i f d ar ob s (r )
i sar (r ) 0.04 i f d ar (r )
5 i sar h i (r ) 0.02 i f d ar h i (r )
i sar l o (r ) i f d ar l o (r )
0 0.00
0 20 40 60 0 20 40 60
r r
Figure 3. Proportion of significant repeller for Chloreucon mangense (a) ISAR (Individual Species–Area
Relationship) in radius of 0-60 m, and (b) IFDAR (Individual functional-diversity–area relationship) in
radius of 21-60 m.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
Discussion
Alternative dimensions of biodiversity as functional and phylogenetic diversity may have the
ability to convey species–area relationships and determining the degree to which processes as
random placement, habitat filtering and/or limiting similarity contribute to the spatial distribution
and assembly of communities (Webb 2000, Swenson et al. 2007, Kraft et al. 2008, Swenson and
Enquist 2009, Helmus and Ives 2012). Our results showed that at all the spatial scales considered
for ISAR, IFDAR and IPSVAR, most species behaved as ‘neutral’, i.e. they are surrounded by
the expected richness, under a null model that only accounts for environmental heterogeneity.
In the case of ISAR some species behaved as accumulators in all spatial scales. Several authors
(Maestre and Cortina 2005, Wiegand et al. 2007a, Brooker et al. 2008) suggest that in the
harshest environments some species tend to improve their surrounding environment, which
results in a strong spatial structuring of the community. Under these conditions the importance of
negative interactions is reduced and increases the importance of positive relationships (Callaway
2007), so it is expected that positive interactions such as facilitation would be more important
and consequently accumulator species would predominate over repeller ones. In particular with
IFDAR, some species were significant accumulators of diversity only on local spatial scales (0-
20 m) and generally behaved neutrally on larger spatial scales (Table 1), and this suggests that
some process limiting similarity is controlling community assembly at fine scales. If this were
the case, inter-specific competition would make that species avoid functionally similar species in
their close proximity (De la Cruz in prep). The frequent clustering of species accumulators on the
functional diversity may be also driven by facilitation, allowing different species around it. In the
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
case of Chloroleucon mangense was a repeller for ISAR and IFDAR, this repeller behavior could
be the consequence of a clumped spatial structure, where much of the living space surrounding
its individuals will be occupied by conspecifics, leaving less space for heterospecific species
(Yang et al, 2013) this process was generate for habitat filtering.
facilitation among distantly related species, while phylogenetic diversity repellers are
hypothesized to be target species where closely related species filter into the same neighboring
Finally observe some cases as Cynophalla mollis and Jacquinia sprucei that were accumulator
for ISAR-IFDAR and IPSVAR (Table 2), these species could be acting as community engineers,
conditions (Espinosa et al. 2015) allowing its around different functional species.
In this study highlights how analyzing alternative dimensions of biodiversity, such as functional
and phylogenetic diversity, may help us understand the co-occurrence of species in diverse
assemblages. These results suggest that some species showed a different behavior to the plant-
plant interactions, where the abiotic interactions and environment are also important in the
community assembly at functional and phylogenetic levels. In particular, we have shown that the
phylogenetic and functional distribution of some species are accumulators and repellers in this
dry forest is non-random indicating the importance of functional traits and past evolutionary
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
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Appendice 1
Table.1: Gof u values of the different models fitted to each species IPCP: inhomogeneous
Poisson cluster process; IPP: inhomogeneous Poisson process.
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
CONCLUSIONES GENERALES
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Diversidad funcional y filogenética en los Bosques Secos del Sur del Ecuador
encontraron que los valores de los rasgo a través del gradiente de precipitación es
correlación sugieren que en los sitios más secos, la estrategia funcional consiste en
alta SLA, alta WD, alta y baja Hmax SM. Se confirmó que el gradiente también
modifica la fuerza de la similitud limitante y los procesos de filtrado hábitat, con una
distribución de los valores de rasgo), para la mayoría de los rasgos, cuando las
condiciones se vuelven más seco. Estos hallazgos son muy interesantes desde el
punto de vista funcional de las interacciones de las especies, que pueden ser usados
Si bien estos resultados son consistentes con lo propuesto para los bosques
secos tropicales, donde se evidencia baja diversidad funcional en sitios que están
tomados por la mayoría de los rasgos a lo largo del gradiente de estrés (medido como
gradiente ambiental fue encontrado por cualquier rasgo excepto por el tamaño de la
hoja. Esta variación en el tamaño de la hoja es mediada por una transición del tamaño
de la hoja, es decir hojas grandes, tipico de hojas caducas, delgadas, y hojas pequeñas
especie. Los resultados también apoyan la hipótesis de que las especies se encuentran
mas similares y que a escalas superiores este comportamiento cambia siendo mas
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AGRADECIMIENTOS
Durante estos años tengo mucho que agradecer a mucha gente! Muchos han puesto su granito de
arena en esta tesis de manera muy distinta.
A mis Padres quienes han sido mi más grande fortaleza, a mis queridos herman@s Diani, Joha,
Pame, Angel, mis sobrinos Patricio y Angelito y a mi cuñada Jessenia que es como una hermana,
gracias por ese apoyo incondicional e invaluable en las largas jornadas de campo y laboratorio,
por todos los sacrificios que han hecho para que yo realice mis estudios.
A mis directores de tesis Adrián y Marcelino, sin ustedes esta tesis, nunca habría sido posible.
Adrian, mil gracias por apoyarme y dedicarle tanto tiempo e ilusión a esta tesis! Eres un
excelente investigador y sobre todo una persona increible.
Marcelino, muchas gracias por haberme permitido hacer la tesis contigo, por tu paciencia e
ilusión durante todos estos años eres lo máximo.
A mis compañeros del Departamento de Ciencias Naturales, especialmente a Carlos Iván quien
ha sido un pilar fundamental en el desarrollo de mi tesis, a Pablo Ramón y David Duncan
quienes me apoyaron en mis dudas estadísticas, Angel B., Anita A., Diego G, Dalton Q., Jorge
A., Andrea J., José R, Ramiro M, Bayo y Rosita quienes me apoyaron en alguna fase de mi tesis
153
y en mis estancias en Madrid … A Aran Luzuriga quien me ayudo como revisora de algunos
capítulos de mi tesis… A María Belen amiga incondicional.
La realización de esta tesis fue apoyada parcialmente por los proyectos A/024796/09 y
A/030244/10 de la Agencia Española de Cooperación Internacional y para el Desarrollo
(AECID) y el proyecto Islas-Espacio CGL2009-13190-C03-02 del Ministerio de Ciencia e
Innovación. A la beca doctoral SENESCYT 2009. A los proyectos internos de la UTPL,
PROY_CCNN 0030; PROY_CCNN 1260; PROY_CCNN 1054.
GRACIAS A TODOS
Eli Gusmán M.
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