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TESIS DOCTORAL 2015

RESPUESTA ADAPTATIVA DE ESPECIES LEÑOSASA LAS VARIACIONES CLIMÁTICAS Y AMBIENTALES

EN EL NOROESTE DE SENEGAL

Joseph Saturnin DIEME

2015

Diseño de la portada: Pierre Laclais ([email protected]). Illustrations & Graphisme; www.aquarelle-de-

savoie.com, France.

mailto:[email protected]

http://www.aquarelle-de-savoie.com/

http://www.aquarelle-de-savoie.com/

Departamento de Biología y Geología Universidad de Almería

Respuesta adaptativa de especies leñosas a las

variaciones climáticas y ambientales en el noroeste de

Senegal

Memoria presentada por el Licenciado Joseph Saturnin Diémé para optar al título de Doctor por la Universidad de Almería, dirigida por el Dr. Francisco I. Pugnaire de Iraola y la Dra. Cristina Armas Kulik.

Mayo de 2015 El Doctorando

VoBo de los Directores

Joseph Saturnin Diémé Francisco I. Pugnaire de Iraola Cristina Armas Kulik

En vérité, en vérité, je vous le dis, si le grain de blé tombé en terre ne meurt pas, il

demeure seul; Mais s'il meurt, il porte beaucoup de fruit.

Jean 12, 24

A mi esposa Madeleine

A mis hijos Edmond Pascal y Jean François

En la vida hace falta: paciencia para aceptar las cosas que no podemos cambiar,

fuerza para cambiarlas e inteligencia para distinguirlas.

Anónimo

Agradecimientos

La Presente Tesis Doctoral forma parte de los estudios realizados bajo el soporte económico del

proyecto FUNCITREE financiado por la Unión Europea, 7th Framework Programme (grant

KBBE-2272657FP) y MICINN (grant CGL2010-17081) y ha sido desarrollada en la Estación

Experimental de Zonas Áridas en Almería, instituto perteneciente al Consejo Superior de

Investigaciones Científicas (EEZA-CSIC). También he sido beneficiario de una beca predoctoral

MAEC-AECID (Agencia Española de Cooperación Internacional para el Desarrollo) para

ciudadanos extranjeros.

En la fase final de esta “aventura” de ir a otro país a estudiar, de dejar a la familia, trabajo,

amigos… en fin, de abandonar una vida que comienza a ser estable y aventurarse en un nuevo

sueño, una nueva meta por cumplir tanto a nivel personal como profesional, es preciso hacer un

balance de todo ello. Al mirar hacia atrás y ver todo lo dejado, al poner la mirada en el presente y

ver todo lo aprendido y disfrutado de esta experiencia y al mirar hacia el futuro y ver las

posibilidades que hay en mi camino, es preciso agradecer a quienes han participado en cada

una de la etapas de esta aventura. Sin estas personas no habría sido posible cumplir esta meta.

Así gracias a Dios, por estar conmigo en cada paso que doy, por fortalecer mi corazón e iluminar

mi mente y por haber puesto en mi camino a aquellas personas que han sido mi soporte de esta

aventura.

Desde estas líneas quisiera, especialmente mostrar mi gratitud y más sincero cariño a mi director

de tesis Paco Pugnaire. Primero por creer en mí, aceptándome bajo su dirección, lo que me trajo

un sinnúmero de enseñanzas, tanto personales como profesionales. Le agradezco que me haya

abierto hace ya cuatro años las puertas de su grupo de investigación, dándome la oportunidad

de tener una visión más amplia del mundo de la investigación y descubrir cuánto me motiva.

Además le agradezco todo el tiempo invertido en lo personal, siempre apoyándome en

momentos difíciles, escuchándome cada vez que fue necesario y enseñándome que las cosas

son más sencillas de lo que aparentan. Su apoyo y optimismo han sido decisivos para seguir

adelante y llegar a buen puerto. Y cómo no, no podré olvidar sus ricas paellas…. Quiero que

sepa que en todo sentido usted es un ejemplo para mí.

Quiero expresar también mis más sinceros agradecimientos y con especial cariño a mi co-

directora de tesis Cristina Armas. Gracias por tu acogida, apoyo y enseñanzas en investigación

desde los trabajos de campo en Senegal, por tu entusiasmo por la ciencia y por esa alegría

contagiosa. Sin tu ayuda más de un capítulo (¡y futuros manuscritos!) de este trabajo no habría

visto su luz. Merci beaucoup je t’attend au Senegal. Y gracias a tu marido Barlo, por su alegría y

mejor humor.

Gracias al Consejo Superior de Investigaciones Científicas, EEZA-CSIC, por permitir desarrollar

mi actividad investigadora en este centro y a todo el personal administrativo, técnico, de servicio

y de laboratorio, que han contribuido en ello. Gracias también a la Universidad de Almería, por

acogerme en su programa de doctorado en Ciencias.

Quisiera expresar mi agradecimiento al Ministerio de l’enseignement superieur et de la recherche

de Senegal que ha autorizado mi estancia de tesis, muchas gracias a mis colegas.

Muchas gracias al Dr Mayecor Diouf del Centre National de Recherches Forestieres del Institut

Senegalais de Recherches Agricoles (CNRF/ISRA) y los becarios, por su apoyo, consejos y

ayuda en el campo.

Ahora me gustaría agradecer a todos los miembros de la EEZA por su acogida, consejos y

apoyo que me han permitido sentirme a gusto, en casa. No olvidaré jamás la ayuda y consejos

de Alfredo con los tubos de PVC….del experimento de invernadero, Teresa por sus historias,

apoyo, sonrisas,…, Myriam por su mejor humor. Al grupo de Ecología Funcional (EFUN),

Christian, Petr y su familia, Carme, Sara, Yudy, por el apoyo, discusiones, reuniones….,

especialmente a Nuria por la acogida en tu casa en mis primeras semanas en Almería, tu apoyo

en los análisis de filogenia…Javier por su ayuda en las medidas en el invernadero y la foto de su

baobab del capítulo 2. Muchas gracias. Y, por supuesto, quiero agredecer a mis preferid@s

chumber@s Oriol, Ana, Fran, Meire, Elisa, Alejandro, Cristina, Monica, Olga, Laura, Luisa,

Miguel, Gustavo, Sonia, Lourdes, Eva, Loli, Maite, Martin, Andreas, Iñaki, Juan, Jaime, Sandro

todas las charlas, discusiones, tapas, celebraciones, cenas……Gracias especial a Angela (eres

especial, una angela) y Saher.

Gracias a Fernando Casanoves del Centro Agronómico Tropical de Investigación y Enseñanza

(CATIE) en Costa Rica por su indispensable ayuda con los análisis estadísticos, y a Jordi Moya y

José María Gómez por atender mis múltiples solicitudes sobre los análisis de filogenia.

A mis queridos amigos de la UAL, el grupo internacional, Saher, Soraya, Carretero, Marín,

Gregorio, Miguel, Argelia, Cesar, Tere por las discusiones, ayudas, consejos, tapas, rutas,

comidas, celebraciones, tiempo pasado en la universidad hasta los domingos, muchas gracias.

Al cura Paco, el equipo misionero y todos los fieles de la Parroquia San Pio X de Zapillo muchas

gracias, vuestra acogida y compañía reanimaba mi espíritu domingo tras domingo. Y muchas

gracias a Alfonso y su esposa Concha por su acogida, consejos y apoyo para mejorar mi

castellano.

A todo los senegaleses de Almería especialmente Bassirou, El Hadj, Bouba, Marie, Anta,

Sokhna, Anta y su familia, Ndongo por las discusiones….Muchas gracias

Gracias en especial a esas personas tan importantes en mi vida. A mi mujer Madeleine (su

familia) por su paciencia y nuestros queridos hijos Edmond Pascal y Jean François que verán la

tesis para comprender lo que les espera.

A mis padres Edmond y Eliane a pesar de no estar presentes físicamente, sé que procuran mi

bienestar desde mi país Senegal, y está claro que si no fuese por el esfuerzo realizado por ellos,

mis estudios de tercer ciclo no hubiesen sido posibles. A mi abuelita Christine, mis hermanos

Rufin (su mujer Luisa y niña Rose Christine), Chimére, Richard, Constantin, mi hermanita

Honorine y su familia (Pierre los niños Clementine y Sylvain porque a pesar de la distancia, el

ánimo, apoyo y alegría que me brindan me dan la fortaleza necesaria para seguir adelante).

A mis tios Abbé Camille, Jean Christophe, Omer, Pierre y Paul, Gilles por todo su amor y

comprensión, muchas gracias.

A mi mejor amigo y hermano Ampa que conocí en Almería, que Dios te bendiga con tu familia.

A mi querida Dra. Lucie Awa Thione del ministerio, por tu presencia diaria en mi vida tan

personal como profesional, le agradezco mucho.

A mis amigos Marc, Frere Luc Brunette, Henri Noel, Joseph Coly Diouf, Evariste, Mahé…muchas

gracias por todo.

A mis queridos primos y primas especialmente a Madeleine Bassene, Marguerite, Khardiata

Michelle, Ken, Steven, El Hadj, Nicolas los miembros de las largas familias DIEME (padre) y

COLY (madre) muchas gracias.

A aquellas personas que han estado presentes en mi camino y, aunque ya no están,

especialmente mis tios Kadialy, Gustave, Cesar, Monseigneur Maixent Coly todos han puesto su

granito de arena para que hoy sea quién y cómo soy.

Mes remerciements vont enfin à toute personne qui a contribué de près ou de loin à l’élaboration

de ce travail. Due Dieu vous le rende en grâces infinies et fasse descendre sur vos familles

toutes les belles prévenances que vous êtes en droit d'espérer de sa magnificence. AMEN

RESPUESTA ADAPTATIVA DE ESPECIES

LEÑOSAS A LAS VARACIONES CLIMATICAS

Y AMBIENTALES EN EL NOROESTE DE

SENEGAL

Índice

RESUMEN GENERAL .................................................................................................................. 1

INTRODUCCIÓN GENERAL ......................................................................................................... 3

OBJETIVOS GENERALES ........................................................................................................... 7

CHAPTER 1: FUNCTIONAL GROUPS OF SAHELIAN TREES IN A SEMIARID

AGROFORESTRY SYSTEM OF SENEGAL ................................................................................. 9

Summary ...................................................................................................................... 11

1. Introduction .......................................................................................................... 13

2. Materials and methods ......................................................................................... 15

2.1. Study site and species ................................................................................. 15

2.2. Plant traits .................................................................................................... 18

2.3. Data analysis ............................................................................................... 19

3. Results ................................................................................................................. 20

4. Discussion ............................................................................................................ 25

5. Conclusion ........................................................................................................... 29

Appendices ................................................................................................................... 30

CHAPTER 2: FUNCTIONAL RESPONSES OF FOUR SAHELIAN TREE SPECIES TO

RESOURCE AVAILABILITY ....................................................................................................... 33

Summary ...................................................................................................................... 35

1. Introduction .......................................................................................................... 37

2. Material and methods .......................................................................................... 39

3. Results ................................................................................................................. 43

4. Discussion ............................................................................................................ 50

5. Conclusion ........................................................................................................... 53

CHAPTER 3: TRAITS ASSOCIATED TO DROUGHT STRATEGIES AFFECT THE EVOLUTION

OF LEAF THICKNESS AND HABIT OF MAIN WOODY SPECIES OF A SEMIARID SAHELIAN

AGROFORESTRY ECOSYSTEM ............................................................................................... 55

Summary ....................................................................................................................... 57

1. Introduction .......................................................................................................... 59

2. Material and methods .......................................................................................... 61

2.1. Tree community data ....................................................................................... 61

2.2. Phylogeny ........................................................................................................ 63

2.3. Statistical analysis ....................................................................................... 65

3. Results ..................................................................................................................... 66

4. Discussion ................................................................................................................ 68

5 Conclusion ................................................................................................................ 71

Appendices .................................................................................................................. 72

CONCLUSIONES GENERALES ................................................................................................. 75

BIBLIOGRAFÍA ........................................................................................................................... 77

Aspectos generales

1

RESUMEN GENERAL

Tanto estudiar las respuestas de las plantas a la sequía para comprender la estructura y

composición de las comunidades vegetales, como analizar las respuestas de las plantas a la

disponibilidad de recursos y su evolución, son aspectos importantes para predecir su resistencia

a los cambios futuros en el clima. Así, en esta tesis pretendemos comprobar las estrategias de

adaptación a la sequía de las especies leñosas sahelianas, sus respuestas a la disponibilidad de

recursos a través de las variaciones del crecimiento y la asignación de biomasa a los distintos

órganos de la planta y, finalmente, al efecto de la filogenia en sus estrategias adaptativas a la

sequía. Para evaluar esto recogimos datos de rasgos funcionales de 20 especies leñosas en

campo apoyados de un experimento en invernadero.

En el primer capítulo de esta tesis intentamos establecerlos grupos funcionales que

corresponden a las distintas estrategias adaptativas de las plantas a la sequía analizando 9

especies leñosas de gran importancia socio-económica y ecológica den el Noroeste de Senegal.

Para ello, en la aldea de Leona recogimos datos en dos épocas distintas (seca y húmeda) de

cuatro rasgos funcionales relacionados con la estrategia de adquisición de recursos y de dos

rasgos morfológicos de las distintas especies. Identificamos dos clases funcionales principales,

que se identifican con especies de hoja perenne y hoja caduca y, posteriormente, los

subdivididos en cuatro grupos funcionales (2 grupos por clase funcional).

Con base a estos resultados, en el segundo capítulo buscábamos indagar en mayor

profundidad como estos grupos funcionales que corresponden a estrategias adaptativas a la

sequía se traducen en crecimiento y asignación de biomasa según la disponibilidad de recursos,

principalmente agua y nutrientes en el suelo. Establecimos un experimento en invernadero con

las 9 especies descritas en el primer capítulo usando plántulas que crecieron bajo distintos

tratamientos con un diseño factorial de agua y nutrientes, con dos niveles de cada factor. Hemos

tenido problemas con la germinación en cinco especies: las semillas de dos especies no

germinaron, otras dos especies germinaron pero las plántulas murieron pronto y una germinó al

final del experimento. Al final, seguimos el experimento con cuatro especies, la mayoría de hoja

caduca. Estimamos la tasa relativa de crecimiento (RGR), la relación raíz:tallo (R/S) y el área

específica de hoja (SLA), que mostraron diferencias entre especies, los regímenes de agua y la

disponibilidad de nutrientes. RGR varió entre especies y fue muy sensible al agua y la

disponibilidad de nutrientes; las especies de hoja caduca mostraron valores globales altos en

condiciones fértiles, con valores altos de RGR apoyados por valores altos de SLA. En general,

nuestras especies asignan más biomasa a las raíces, sobre todo en régimen de bajos recursos,

reflejando estrategias de adaptación relacionadas con el agua y los nutrientes. Las distintas

especies mostraron un nivel distinto de plasticidad fenotípica.

Las estrategias de las especies que forman una comunidad vegetal son el resultado de

adaptaciones previas en ancestros comunes, y para entender y predecir sus respuestas a

cambios ambientales es importante conocer su historia evolutiva. En el tercer capítulo

pretendíamos entender la evolución de las especies leñosas analizando su señal filogenética.

Para esto, usamos rasgos funcionales de 20 especies leñosas obtenidos en la zona saheliana de

estudio en Senegal. Encontramos bajos valores de la k de Blomberg para todos los rasgos

estudiados, con rangos que van de 0.204 a 0.995, lo que indica que tienen baja señal

filogenética; es decir, están poco relacionados filogenéticamente. Se observó una señal

filogenética significativa sólo para el grosor de hojas y tipo de hoja (caduca o perene). Los

resultados sugieren que estos rasgos evolucionaron como con un movimiento browniano,

experimentando una radiación tardía y una evolución gradual desde entonces. El carácter de

hoja caduca es la forma que ha divergido más recientemente. Estos datos implican que el

carácter caducifolio encontrado en ambientes semiáridos es una estrategia para escapar de la

sequía de reciente adquisición, en consonancia con los datos que sugieren que la sequía es un

factor relativamente reciente en el mundo.

Aspectos generales

3

INTRODUCCIÓN GENERAL

La diversidad biológica, o biodiversidad, es una medida de la variedad y la variabilidad

(capacidad para variar), de todos los organismos vivos. Incluye la diversidad genética de las

especies y sus poblaciones, la diversidad de especies y formas de vida, la compleja diversidad

de las especies asociadas y sus interacciones, así como los procesos ecológicos (XVIIIe

Assemblée Générale de l'IUCN, "The World Conservation Union", Costa Rica, 1988). En otras

palabras, la biodiversidad se refiere a la diversidad de la vida en todas sus formas e incluye una

amplia gama de escalas, desde genes hasta ecosistemas a través de individuos y especies

(Secretariat of the Convention on Biological Diversity 2003). La flora y la fauna están sujetas a

extinciones y renovaciones que son consecuencia de procesos evolutivos y la acción de los

cambios ambientales, pero también más recientemente, de la acción del hombre. Los seres

humanos han alterado profundamente el medio ambiente, alterando los ciclos biogeoquímicos

globales, transformando la tierra y mejorando la movilidad de la biota (Chapin et al., 2000).

Estos cambios conducen a una pérdida mundial de diversidad con un ritmo sin

precedentes a nivel geológico (Wood et al., 2000, Maskell et al., 2010, Harley, 2011). Como las

propiedades funcionales de los ecosistemas están determinadas por la diversidad de especies y

la estructura de la vegetación, el cambio de estructura de la vegetación causada por la pérdida

de especies podría tener efectos negativos en el funcionamiento de los ecosistemas (Symstad et

al., 1998, Naeem et al., 2009). La pérdida de biodiversidad amenaza importantes procesos de los

ecosistemas y los servicios ambientales que los seres humanos obtienen de ellos (Chapin et al.,

2000), especialmente en las zonas áridas (Perrings and Walker, 1995, Duffy, 2003).

Trabajos científicos han identificado en el último decenio una serie de atributos

fisiológicos de las plantas que corresponden a funciones tales como crecimiento (Cornelissen et

al., 1999), la capacidad de adaptación (Grime et al., 1997), tolerancia a los ambientes hostiles

(Wright and Westoby, 1999) y la palatabilidad de los pastos para pastoreo (Díaz et al., 2004). Se

ha propuesto también que los rasgos de las plantas pueden servir como un vínculo entre el

cambio ambiental y los cambios en el ecosistema (Díaz et al., 2004), y que estos rasgos -y las

especies que los presentan- afectan a los ecosistemas en función de su abundancia.

Estudios recientes indican que la diversidad funcional, y no el número de unidades

taxonómicas, impulsa en última instancia el funcionamiento de los ecosistemas (Cadotte et al.,

2009, Flynn et al., 2011), por lo que la diversidad funcional y filogenética han demostrado ser los

mejores predictores de la productividad primaria (Cadotte et al., 2009, Clark et al., 2012).

La diversidad funcional “el valor y la variedad de las especies y rasgos de los

organismos (Tilman et al., 1997, Tilman et al., 2001, Mouchet et al., 2010)” es un componente de

la diversidad biológica que influye la dinámica de los ecosistemas, su estabilidad, la

productividad, el balance de nutrientes, y otros aspectos del funcionamiento de los ecosistemas

(Petchey and Gaston, 2006). El concepto de diversidad de rasgos funcionales se basa en el

supuesto de que con el aumento de disimilitud de rasgos entre especies, la diversidad de

estrategias en el uso de recursos aumenta y las especies que se superponen a lo largo de los

ejes de disponibilidad de recursos disminuye (Tilman, 1997). Un rasgo es cualquier característica

morfológica, bioquímica, de comportamiento y fenológica de un individuo que potencialmente

afecta a su rendimiento y aptitud (Petchey and Gaston, 2002). Por lo tanto, medir la diversidad

funcional es medir la diversidad de rasgos funcionales, donde los rasgos funcionales son

componentes del fenotipo de un organismo que influyen en los procesos a nivel de ecosistemas

(Petchey and Gaston, 2006) y refleja el ensamblaje de especies de una comunidad (Clark et al.,

2012).

Sin embargo, las diferencias actuales entre las especies que se encuentran en una

comunidad ecológica son el resultado de las modificaciones de un ancestro común (Webb et al.,

2002). Así, la conservación de la biodiversidad requiere conocimientos de su historia, como la

Aspectos generales

5

conservación del potencial evolutivo requiere la integración de la diversidad filogenética

(Posadas et al., 2001).

El agua es el recurso ecológico más limitante para la mayoría de árboles y masas

forestales, porque a medida que disminuye el contenido de agua del suelo los árboles se vuelven

más estresados y comienzan a reaccionar a los cambios de disponibilidad de recursos. El

informe de IPCC (2007) indica una clara tendencia a la disminución de las precipitaciones y al

aumento de las temperaturas en las regiones áridas del Sahel y el sur de África. Además, indica

que la zona afectada por la sequía ha aumentado a nivel mundial desde la década de 1970 y

predice que el aumento de las temperaturas y la menor precipitación en los trópicos áridos y

semiáridos pueden conducir a una reducción general de los pastizales y de la producción

ganadera, amenazando la seguridad alimentaria, así como los valores culturales y sociales.

En el África subsahariana los agricultores dependen en gran medida de los sistemas

agroforestales que les proporcionan una variedad de servicios como la producción de forraje, la

provisión de sombra, la estabilización del suelo, la fertilización del suelo, alimentos y la

producción de combustible. Sin embargo, la mayoría de estos sistemas agroforestales se basan

en un pequeño número de especies de árboles dispersos, lo que reduce la estabilidad y la

capacidad de adaptación de estos sistemas a los cambios climáticos y la incertidumbre.

Se pueden definir los sistemas agroforestales como los sistemas y prácticas de uso de la

tierra en la que las plantas leñosas se integran con los cultivos y/o ganado para obtener una

variedad de beneficios y servicios (Wight, 1998). La integración puede hacerse ya sea en una

asociación espacial (por ejemplo, cultivos con árboles) o de acuerdo con una secuencia de

tiempo (por ejemplo, barbechos mejorados, rotaciones).

Pero el papel de los sistemas agroforestales está evolucionando. Considerando que los

sistemas agroforestales dominantes de los años 1980 y 1990 se centraron en la productividad

agrícola y la mejora de los medios de vida, los actuales en un contexto de preocupación

creciente sobre el cambio global, se caracterizan por la rápida pérdida de la biodiversidad,

acentuando la persistencia de la pobreza en África (Garrity et al., 2006, Mbow et al., 2014).

En efecto, los agricultores continúan luchando para aumentar de manera sostenible los

objetivos de producción aunque la continua degradación de la tierra, los bajos precios del

mercado, y la falta de instituciones capaces de prestar apoyo técnico y apoyo financiero hacen

que este desafío cada vez es más difícil (Bishaw et al., 2013). Así, las combinaciones de gestión

de las múltiples necesidades que deben cumplirse en las diversas escalas exigen una

modernización de los sistemas agroforestales que cumplan con los requisitos específicos de los

agricultores locales.

Para cumplir con este objetivo, y para aumentar la capacidad de adaptación de sistemas

agroforestales, es necesario conocer mejor una serie de especies arbóreas y arbustivas

disponibles a nivel regional cuya funcional cultural, ecológica y productiva se pueda usar para

mejorar la funcionalidad de estos sistemas. Por lo tanto, el diseño de sistemas agroforestales

modernizados con una función de resiliencia al cambio climático requiere una sólida

comprensión no sólo de las necesidades de producción de los agricultores, sino también un gran

conocimiento práctico de la relación entre los atributos o características de las especies de

plantas individuales y la capacidad de estas especies para proporcionar funciones agroforestales

específicos como la resistencia a la sequía.

Aspectos generales

7

OBJETIVOS GENERALES

Contribuir a entender cómo mejorar la productividad y la resistencia a la sequía de los

sistemas agroforestales de la zona semiárida de Senegal (Fig. 1) mediante el estudio de los

rasgos funcionales de un conjunto de especies leñosas socio-económicamente importantes.

Los objetivos que se abordarán específicamente en los diferentes capítulos de esta tesis

son:

Entender las respuestas fisiológicas de las especies leñosas en ambientes semiáridos

de la zona saheliana de Senegal respecto a las condiciones de suelo y clima, y

clasificarlos en diferentes grupos funcionales (capítulo 1).

Estudiar el efecto de la disponibilidad de agua y nutrientes en el suelo en el crecimiento

y la asignación de biomasa a las partes aérea y radicular de las especies seleccionadas

de la zona saheliana de Senegal (capítulo 2).

Estudiar la señal filogenética de distintas estrategias adaptativas a la sequía de las

especies leñosas seleccionadas de la zona saheliana de Senegal (capítulo 3).

(a)

(b)

Figura 1. Zona de estudio (marcada con un cuadrado rojo en el mapa b). Zona saheliana en el

mapa (a) y Senegal y sus regiones climáticas en el mapa (b).

Field site location. All tree trait measurements were performed in the agroforestry systems in

Louga region, Senegal (Chapter 1 and 3 in this Thesis). (a) Map of Africa highlighting the

Sahelian area in orange; (b) Senegal climatic regions (Adapted from IRD – Cartographie A. LE

FUR-AFDEC).

Sahelian

Sahelian-Sudanese

Sudanese

Sudanese-Guinean

Sub-Guinean

Climatic regions Cities, number of residents Limits

Main roads

Rail road

More than 500 000

From 100 000 to 500 000

From 50 000 to 100 000

Low than 50 000

9

CHAPTER 1: FUNCTIONAL GROUPS OF SAHELIAN TREES IN A

SEMIARID AGROFORESTRY SYSTEM OF SENEGAL

11

Summary

Addressing plant responses to drought is important to understand the structure and

composition of plant communities in water-limited environments and to forecast their resilience to

future changes in climate. In a semiarid agroforestry system in the Sahelian steppe of Leona

(Senegal) we selected nine tree species of great environmental and socio-economic importance

and explored their drought-resistance mechanisms. We hypothesized that these tree species will

show different suites of traits regarding responses to drought, and expected to identify functional

groups of species differing in their strategies to withstand water shortage. Over two seasons (dry

and wet) we monitored four traits reflecting above- and below-ground strategies of resource

acquisition such as predawn leaf water potential (pd), specific leaf area (SLA), leaf thickness,

and leaf area index (LAI), and two morphological traits, trunk diameter and tree height. LAI and

pd were measured six times during the dry and rainy seasons, and the other traits were

measured once. We identified two functional classes, evergreen and deciduous species,

subdivided into four functional groups. The first class included deciduous and semideciduous

species in 2 functional groups which generally had large SLA, low leaf thickness, and small to

intermediate inter-seasonal variations in pd. The second class included evergreen species and

was also divided into 2 groups with low SLA, high thickness and large inter-seasonal variations of

pd throughout the year. These groups represent strategies which differ in their response to

changing environmental conditions and should help forecast community composition under future

scenarios of climate change.

Capítulo 1

13

1. Introduction

Tropical seasonally-dry forests and savannahs occur under rainfall regimes that vary

greatly in frequency and intensity, with rainfall unevenly distributed among seasons.

Consequently, water availability is one of the most limiting factors for plant growth in these

tropical ecosystems, influencing plant functioning and community structure across both, large-

scale rainfall gradients and small-scale, topographic gradients (Ogle and Reynolds, 2004). The

relative success of tree species along these gradients and their fate under potential changes in

water availability will depend on how well they are adapted to cope with drought (Markesteijn,

2010). Research on plant responses to water stress is becoming increasingly important as most

climate-change scenarios suggest an increase in aridity in many areas of the globe, including the

tropics (Petit et al., 1999) which may result in shifts in the composition of current plant

communities and in their distribution ranges.

Plants have developed several strategies at different levels to cope with soil water

shortage, including phenological adjustments, control of tissue water status, and morphological

and anatomical traits that vary almost as much within species as among species (Brendel and

Cochard, 2011). Therefore species-specific differences in the ability to deal with drought may be

a major factor influencing plant community structure (Engelbrecht and Kursar, 2003).

Functional traits are plant attributes that are partly the result of evolutionary processes

(Flores et al., 2014) and which may be used as indicators of plant responses to environmental

factors (Cornelissen et al., 2003a, Lavorel and Garnier, 2002). As functional traits are related to

plant persistence (Knevel et al., 2005), they can be used to assess tolerance to stress. The

combination of functional traits can therefore be a way to characterize plant functioning and to

highlight the adaptive strategies of a species (Grime, 2001). Interspecific analyses of functional

traits and their correlations among a large number of species may expand the understanding of

Plant functional groups

plant resource-use strategies and thus help explain species responses and functions, and their

effects at ecosystem level (Vendramini et al., 2002, Wright et al., 2005). It is well-known that

species differ in drought tolerance, and a number of traits have been associated with this function

(Valladares and Sánchez-Gómez, 2006). For example, plant sensitivity to drought may be

evaluated through different indicators of plant physiological status, such as leaf water potential,

stomatal conductance, or chlorophyll fluorescence (Armas and Pugnaire, 2005, Armas and

Pugnaire, 2009, Gómez-Aparicio et al., 2006, Pugnaire et al., 1996, Quero et al., 2011).

Therefore, an integrative measure of key drought resistance traits under contrasting water

availabilities may provide a powerful tool to examine inter-specific responses to drought

(Engelbrecht and Kursar, 2003).

Drought is the shortage of water availability experienced by the plant when soil moisture

is depleted as a consequence of relatively higher evaporation rates compared to rainfall. Plants

may experience drought as stress, which is tolerated or avoided thanks to a suite of

morphological, physiological and phenological mechanisms (Parolin et al., 2010). Trade-offs in

resource allocation are typically associated to the different strategies (Flores et al., 2014). The

avoidance strategy usually leads to escape from water deficits for instance by maximizing deep-

root water uptake or by decreasing water loss by different means. Species with the avoidance

strategy can be water savers or water spenders. The savers, have little osmotic and stomatal

adjustment (stomatal control, leaf movements, decreasing leaf size, shedding leaves), minimize

water loss at early stages of drought and keep high values of leaf water potential (Ludlow, 1989).

Water spenders keep high rates of transpiration, photosynthesis, and growth. Water spenders

species may as well tolerate the loss of relatively high amounts of xylem hydraulic conductivity by

embolism. Instead, drought-tolerant species have the ability to survive desiccation while

minimizing reductions in growth and fitness (Engelbrecht and Kursar, 2003).

Capítulo 1

15

Plant species segregate along natural gradients of water availability according to their

capacity to withstand drought. However, species with contrasting ecological requirements coexist

(Valladares and Sánchez-Gómez, 2006), as in the Sahelian zone of Senegal, where evergreen

and deciduous species co-occur. Such contrasted patterns certainly reflect very different

physiological adaptations of sahelian species to the ruling water shortage conditions (Fournier,

1995). Drought tolerant species in these habitats usually have a high degree of sclerophylly (Piot

and Diaite, 1993), being deciduous species less sclerophyllous than evergreen species (Medina,

1984). Here we focus on the mechanisms related to drought resistance of nine sahelian tree

species, evergreen and deciduous, ubiquitous in the Sahelian region, and of high socio-economic

importance for the local populations. We hypothesized that 1) different tree species will show

different suites of traits regarding responses to drought, and 2) functional traits will allow us to

identify different strategies depending on the mechanisms to withstand drought.

2. Materials and methods

2.1. Study site and species

The study was conducted in the sahelian savannah of Leona, northwest Senegal, a

semiarid environment with sub-canarian climate (Wade, 1997). It is under the influence of oceanic

winds and currents that reduce the extreme seasonal contrasts of the Sudano-Sahelian climate.

Therefore this region has a smooth, atypical climate whose influence diminishes away from the

coast. Between February and May the area is dominated by the Harmattan (hot and dry winds)

with huge sand storms and high desiccating capacity. The wet monsoon season occurs between

June and October with an average annual rainfall that varies between 220 and 350 mm (Gaye

and Edmunds, 1996) mainly from July to September followed by a dry season between

November and June. Temperatures are high during most of the year. The hottest period generally


corresponds to the months of May and October. Minimum temperatures range between 22.5 and

28° C and maximum temperatures between 31 and 37° C (Wade, 1997).

Photo 1.- Continental Sahelian Agroforestry landscape (Leona, Senegal).

Photo 2.- Coastal Sahelian Agroforestry landscape (Leona, Senegal).

Capítulo 1

17

Soils are mostly sandy, little-leached ferruginous tropical soils with poor structure and

usually occupied by peanut, cowpea, millet crops and grassland. There is an intensive cropping

system and lands are generally not left uncultivated in any season/year, leading to impoverished

soils that require large inputs of fertilizer before new sowing. Being sandy soils, they have low

water holding capacity, low organic matter content and are often subject to wind erosion.

Photo 3.- Dry season (Leona, Senegal).

Photo 4.- Rainy season (Leona, Senegal).


The natural landscape is a savannah with scattered big trees and shrubs in a matrix of a

continuous herbaceous/grass species layer that thrives during the rainy season. Most of the

woody species of this Sahelian savannah ecosystem are thorny. Harvesting of trees and shrubs,

grazing, cropping and rainfall all contribute to shape the vegetation regionally (Konate, 2010).

We selected nine dominant and ecologically and socio-economically important tree species with

multiple uses in these areas, Acacia tortilis subsp. raddiana (Savi) Brenan, Adansonia digitata L.

(baobab), Balanites aegyptiaca (L.) Del., Celtis integrifolia Lam., Combretum glutinosum Perr. Ex

DC., Faidherbia albida (Del.) Chev., Neocarya macrophyla (Sabine) Prance, Sclerocarya birrea

(A. Rich) Hochst and Tamarindus indica L. (Table 1).

2.2. Plant traits

We selected three plant traits indicators of different functions related to resource use by

the plant, complementary in representing water use strategies such as predawn leaf water

potential (pd), specific leaf area (SLA) and leaf area index (Niinemets, 2001) plus leaf

thickness. Predawn leaf water potential (pd) provides information on the water status of the

plant as well as on its capacity to take up soil water. Its value range is species-specific and

depends, among others, on rooting depth, root architecture, and root physiological properties

(Pérez-Harguindeguy et al., 2013). Leaf traits are commonly associated to life history, range

distribution, and resource requirements of the species. Specific leaf area is one of the most

widely used leaf traits as an indicator of plant responses to the environment. SLA is strongly

linked to relative growth rate and the resource-use strategy of the plant (Poorter and Garnier,

2007) and can be used to estimate resource availability (Pérez-Harguindeguy et al., 2013). A

related trait is leaf-thickness, linked to leaf construction costs, leaf lifespan and gas exchange

(Loranger and Shipley, 2010).

Capítulo 1

19

We also measured the leaf area index (LAI), or the total leaf area of the plant per unit

ground area (Jonckheere et al., 2004). LAI is a dimensionless index (m²/m²) and reflects the

capacity of the plant to intercept radiation. Predawn leaf water potential and LAI may be inversely

related (Bréda et al., 1995), as higher LAI means higher evaporative surface which may lead to a

decrease in pd. These three traits thus reflect strategies in resource capture and use.

We measured these traits in six healthy, mature trees of each of nine species, all growing

in the field. Leaf water potential and LAI measurements were carried out six times, 3 during the

dry season (November 2010, February and April 2011) and 3 during the rainy season (July 2010,

August and September 2011), whereas SLA and leaf thickness were measured once during the

rainy season for all species except for Faidherbia (leaves were collected in the dry season, as it is

a rainy-season deciduous species) when leaves are at their best.

Two tree-level morphological traits, diameter at breast height (DBH) and plant height

were additionally measured to control for variability associated to tree size. Trait data were

collected following the protocols in Cornelissen et al. (2003b), Knevel et al. (2005) and Pérez-

Harguindeguy et al. (2013).

2.3. Data analysis

Differences in plant traits among species, seasons, and months were analysed with

General Linear Mixed Models. Main fixed factors were species, season/month and the interaction

between them. Tree individual’s identity was included as a random factor. We assumed a

correlation between species and seasons/months and included a compound symmetry temporal

correlation among measurements. We also tested several variance structures to avoid

heteroscedasticity and selected the best model according to the Akaike information criterion

(Akaike, 1974). In the case of pd and LAI we selected varExp, which represents an exponential

structure of a variance covariate. For the others traits (SLA, thickness, DBH and height) we used


varIdent, which represents a variance structure with different variances for different strata

(Galecki and Burzykowski, 2013). Post-hoc differences were tested with Fisher LSD test. We also

performed multivariate analyses (Principal Component and Cluster Analyses) of all functional

traits in order to identify groups of individuals with common functional characteristics.

Statistical analyses were performed with Infostat (Di-Rienzo et al., 2013). Reported

values throughout the text and figures are means ± 1 standard error (SE).

3. Results

There were significant changes in the seasonal course of pd in most species (Fig. 1a).

It was highest (i.e., less negative) for all species in July 2011, after the onset of the rainy season,

when values ranged -0.24 to -0.65 MPa. Adansonia, Sclerocarya and Neocarya showed rather

steady pd during both the rainy and dry seasons. In most species, however, there was a

decrease in pd during the dry season and remained low in this period (Fig. 1b). We observed

relatively important intra-specific variability in November 2010 and particularly, in April 2011 (dry

season) especially in Acacia, Balanites and Tamarindus.

Similarly, LAI changed significantly along seasons (Fig. 1c), being lowest in the driest

months for all species except for Faidherbia. Most species had relatively high LAI in the wet

season (Fig. 1d). Faidherbia was the only rain-season deciduous species in the dataset and

showed higher LAI values during the dry season compared to the rainy season (Fig. 2d). During

the dry season Neocarya and Combretum had the highest LAI. Large intra-specific variation was

observed in Adansonia (April 2011), Combretum and Celtis in August 2010, and also in Neocarya

(November 2010 and August 2011) (Fig. 1c).

Capítulo 1

21

(a)

(b)

(c) (d)

Figure 1. Seasonal change in predawn leaf water potential (pd) (a) and leaf area index (LAI) (c), and mean pd (b) and LAI (d) during the rainy and dry seasons of 9 tree species in the Sahelian region of Senegal: Acacia tortilis (Acto), Adansonia digitata (Addi), Balanites aegyptiaca (Baae), Celtis integrifolia (Cein), Combretum glutinosum (Cogl), Faidherbia albida (Faal), Neocarya macrophylla (Nema), Sclerocarya birrea (Scbi) and Tamarindus indica (Tain). Data are mean values ± SE, n=6. Post-hoc letters are not included to improve clarity (see Appendix S1and S2 for post-hoc tests).

Acacia tortilis Adansonia digitata Balanites aegyptiaca Celtis integrifolia Combretum glutinosum Faidherbia albida Neocarya macrophylla Sclerocarya birrea Tamarindus indica

Wet seasonDry season

Aug'10 Nov'10 Apr'11 Jul'11 Sep'11

p

d (M

Pa)

-4

-3

-2

-1

0

Act

o

Add

i

Baa

e

Cei

n

Cog

l

Faa

l

Nem

a

Scb

i

Tai

n

p

d (M

Pa)

-4

-3

-2

-1

0

ef

bc

igh

de

a

fg

ab

c

ab

e

cd

hiefg

i i

ef

ab

Aug'10 Nov'10 Apr'11 Jul'11 Sep'11

LA

I

0

1

2

3

4

5

Act

o

Ad

di

Baa

e

Ce

in

Co

gl

Faa

l

Ne

ma

Scb

i

Ta

in

LAI

0

1

2

3

4

d

bcd

d d dcd

abcabc

abab

e

abcdabc

a

d

abcabc

abc


Specific leaf area (SLA) differed across species, being smallest in Balanites, Combretum

and Neocarya and highest in Faidherbia (Fig. 2a). SLA changed between the rain and dry

seasons, being smaller in the latter (data not shown).

Leaf thickness (Fig. 2b) also differed among species, and not surprisingly was highest in

the evergreen Balanites, Neocarya and Combretum, and it was low in the deciduous and

semideciduous Faidherbia and Tamarindus, the other species displaying intermediate values.

Regarding tree height (Fig. 2c), individuals of Celtis and Adansonia were tallest and there

was large intra-specific variation in Balanites and Celtis.

Figure 2. Specific Leaf Area (SLA) (a), thickness (b), plant height (c) and Diameter at Breast Height (DBH) (d) of tree species in the Sahelian region of Senegal, Acacia tortilis (Acto), Adansonia digitata (Addi), Balanites aegyptiaca (Baae), Celtis integrifolia (Cein), Combretum glutinosum (Cogl), Faidherbia albida (Faal), Neocarya macrophylla (Nema), Sclerocarya birrea (Scbi) and Tamarindus indica (Tain). Data are mean values ± SE, n=6. Bars with different letters are significantly different (Fisher LSD post-hoc tests).

a

Species

Acto AddiBaaeCein Cogl FaalNemaScbi Tain

SLA

(m

2 kg

-1)

0

2

4

6

8

10

abab

cd

abc

cd

a

d

bcbc

b

Species

Addi Baae Cein Cogl Faal Nema Scbi Tain

Th

ickn

ess

(mm

)

0.0

0.2

0.4

0.6

0.8

b

a

b

ab

c

a

bc

c

Species


Hei

gh

t (m

)

0

2

4

6

8

10

12

14

b

a

b

a

b

ab

b

bb

d

Species


DB

H (

m)

0

1

2

3

4

d

bcd

dcd cd d

a

bc ab

Capítulo 1

23

We aimed to identify functional groups according to variations in traits by principal

component analysis (PCA) and performed a hierarchical clustering of three physiological traits

(pd, LAI, SLA) and height of all species. We excluded leaf thickness as we had no values for

one species. The PCA showed that the absolute value of pd (i.e., without sign) was positively

correlated with LAI and inversely correlated with SLA and tree height (Fig. 3); i.e., the lower the

SLA and tree height, the lower (more negative) the pd and LAI. Thus, Balanites and

Combretum which had low pd had also low SLA. Species like Acacia and Adansonia were

characterized by high SLA, while Neocarya, Celtis and Tamarindus showed comparatively higher

LAI.

Figure 3. Principal Component Analysis (PCA) of SLA, absolute value (with no sign) of predawn

leaf water potential (pd), LAI and height of the 9 sahelian tree species.


The hierarchical classification (Fig. 4) allowed us to group species into 2 classes with 4

functional groups. The first class included deciduous and semideciduous species split into 2

functional groups, and generally had large SLA and low leaf thickness, showing small to

intermediate inter-seasonal variations in pd. The first group was formed by two evergreen

species, Combretum and Neocarya, and the second included the deciduous Adansonia,

Faidherbia and Sclerocarya. The second class included evergreen species with overall low SLA,

high thickness and large inter-seasonal variations of pd throughout the year, and was also

subdivided into 2 groups, one formed only by Balanites and the last one by Acacia, Celtis and

Tamarindus.

Figure 4. Cluster analysis of three physiological traits (predawn leaf water potential (pd),

specific leaf area (SLA) and Leaf Area Index (LAI)) of the 9 tree species (Cophenetic correlation =

0.925).

Capítulo 1

25

4. Discussion

A combination of physiological and morphological traits enabled the grouping of tree

species into different functional types which, given the significant association between traits and

plant responses to environmental factors, implies that species in the same functional group will

likely display similar responses to the environment (Garnier and Navas, 2012) i.e., “functional

response groups” sensu Lavorel et al. (1997). We used traits easy to monitor and quantify

(Garnier et al., 2004), measured using standardised protocols (Cornelissen et al., 2003b, Knevel

et al., 2005, Pérez-Harguindeguy et al., 2013), and which are indicators of the mechanisms by

which plants make use of water and tolerate drought.

Tropical savannahs are important biomes across the world (Williams et al., 1997) with a

high diversity of species and life forms in both the herbaceous and woody layers (Wilson et al.,

1996). Numerous woody species in savannahs, dominant and subdominant, are drought-

deciduous but have developed additional strategies to cope with seasonal, chronic and erratic

drought spells. There are two groups that appear to display the avoider and tolerant strategies

described by Valladares et al. (2004), showing that plant water strategies rely on the analysis of

several variables from the cellular level to gas exchange, to cavitation vulnerability.

Tree species in our study avoid drought by different means; one group included

Adansonia, Faidherbia and Sclerocarya, all deciduous species, and another group of avoiders

included Acacia (deciduous), Celtis and Tamarindus (semideciduous). The decrease in

evaporative surfaces by leaf shedding contributes to preserve water within the plant, but these

species are also deep rooted, which suggests increased water uptake as a complementary

measure to avoid drought (Logan et al., 2010). These two functional groups share large SLA and

generally low leaf thickness, both traits associated with lower leaf longevity and construction

costs (Westoby et al., 2002, Flores et al., 2014).


The main characteristic of the three species in the functional group containing Acacia is

that they display intermediate inter-seasonal variations in pd. Maintaining such levels of water

potential depends on the plant’s ability to extract soil water and to limit water loss through

transpiration. Many authors have characterized water relations in Acacia. Its wide spatial

distribution is indicative of a remarkable adaptability which can be attributed to three basic

elements, water uptake from deep soil layers, low water consumption, and optimization of the

ratio between assimilation and transpiration (i.e., high water use efficiency); in addition, the bulk

of gas exchange does occur in the rainy season where the potential water losses are lower (Do et

al., 1996). Water stress avoidance in Acacia is thus based on two mechanisms, maximization of

water absorption by deep root systems and minimization of water loss (small leaves,

deciduousness). Both mechanisms keep turgor and relatively high water potential. Then, when

water stress increases, expender species (which maximize water uptake but show low water use

efficiency) cannot maintain high rates of transpiration. Tamarindus and Celtis have intermediate-

to-high SLA values. Although they also have high LAI, water loss is minimized by losing

progressively their leaves as drought intensity progresses (Bourou, 2012, Maes et al., 2009).

Indeed, Tamarindus shows the highest inter-seasonal variation in pd in our dataset, but when

drought becomes long and severe, Tamarindus reduces transpiration through a gradual loss of

leaves to almost total defoliation, but maintains its water potential (Bourou, 2012). Overall, this

first functional group of drought avoiders include species that avoid water stress first by

maximizing water uptake (deep root systems) and, when water stress accentuate, by minimizing

water loss by progressively shedding their leaves.

The other functional group of drought avoiders included the deciduous Adansonia,

Faidherbia and Sclerocarya characterized by small-to-intermediate inter-seasonal variations in

water potential, suggesting that they have access to permanent water sources. The unique

character of Faidherbia is that it loses its leaves in the wet season, most likely to avoid

Capítulo 1

27

competition with herbs (Roupsard, 1997), and thrives in the dry season based on the efficiency of

its root system, able to take up water from deep soil layers (Roupsard, 1997). As the taproots of

adult Faidherbia plants reach the water table, they ensure water supply all year round.

Regarding Adansonia and Sclerocarya, in addition to losing their leaves under water

stress they have relatively short taproots, reaching depths of 2.4 m in Sclerocarya (Orwa et al.,

2009) and robust lateral roots which produce tubers in Adansonia. Roots of Adansonia are

relatively shallow (down to ca. 1.8 m), but spread out to a distance greater than the height of the

tree (Fenner, 1980 ). Robust lateral roots allow these species to explore the upper soil horizons

and thus, have the capacity to extract the maximum amount of rainwater before deep infiltration.

Such an extensive shallow root system is probably best adapted to exploiting erratic rainfall.

Water may be stored in the trunk and, together with the loss of leaves during the dry season,

enable the tree to have access to enough water supplies. Storage organs in Adansonia are large

woody stems more or less lignified, with succulent tissue. Baobab trees have long been assumed

to depend on water stored in their large, swollen stems (Wickens, 1983) but recent reports

indicate that only a limited amount of stored water is used for physiological processes buffering

daily water deficits (Chapotin et al., 2006b). By contrast, stem water reserves are used by the tree

to support new leaf growth and cuticular transpiration, but not to support stomatal opening in the

dry season (Chapotin et al., 2006a) since leaves are present only during the rainy season.

Two functional groups showed a water-stress tolerance strategy by being able to

maintain low leaf water potentials (Valladares et al., 2004). Tolerant species have tissues

resistant to dehydration and xylem cavitation, show osmotic adjustment and high cell wall

elasticity. Species of the first group (Combretum and Neocarya) and the group formed solely by

Balanites are all evergreen, maintain high LAI all the year round and show low pd (except

Neocarya) even during the rainy season and most of the dry season. Leaf area index is an


indirect measure of canopy structure which governs the flow of water from the plant to the

atmosphere (Bréda et al., 1995). According to Blum (2011), the ability of plants to meet water

demands and thus tolerate water deficit depends on their hydraulic machinery that involves the

reduction of net radiation by canopy albedo (reflecting part of the energy load on the plant). With

a high LAI the efficiency of light interception increases (Kool and Lenssen, 1997) increasing as

well photosynthetic rate and the efficiency of water use (Waring and Landsberg, 2011).

Maintaining a higher LAI, however, increases transpiration, leading to higher inter-seasonal

variations in pd.

During the dry season, with pronounced decrease of soil water content, leaf water

potential decreases (as in all evergreen species in our study except Neocarya) thereby reducing

their ability to properly pump water to cells. Such an imbalance between water provision and

needs is generally explained by a very high resistance to the passage of water in the soil-plant

interface (Sobrado, 1986). Evergreen species lose their turgor pressure at a total water potential

much lower than deciduous species (Fournier, 1995). Thereby, the leaf tissue of evergreen

species is adapted to stand higher turgor pressure than deciduous species when the water

potential decreases, although there is variability (e.g., Balanites and Combretum) (Fournier,

1995).

Neocarya and Combretum are evergreen species with high LAI, high leaf thickness and

low SLA. However, while Neocarya experienced small variations of pd throughout the year,

these variations were important in Combretum. Low SLA tend to correspond with relatively high

investments in leaf “defences” (particularly structural ones) and long leaf lifespan, which

correlates to leaf thickness and cuticular sclerophylly (Cornelissen et al., 2003b). Neocarya has

leathery and hairy leaves that decrease transpiration and allow coping with drought. In arid

environments, Combretum only grows near reliable water sources and only has active

Capítulo 1

29

photosynthesis during the rainy season (Berger et al., 1996). However, it is the existence of a

very deep root system what explains the physiological behaviour of Combretum (Fournier, 1995).

The last functional group included only Balanites, an evergreen species whose range

includes the Sahelian climate and the Saharan area (Grouzis et al., 1996); it is a species that

develops a deep taproot and grows at a very slow rate (Hall and Walker, 1991). It is one of

Sahelian trees with higher tolerance to drought (Depierre and Gillet, 1991), showing high inter-

seasonal variation in pd, long spines, and low SLA (e.g., sclerophyllous leaves).

5. Conclusion

In conclusion, our data show that different tree species display different suites of traits

reflecting mechanisms to cope with drought. These functional traits allowed us to identify different

strategies and group them into four different functional groups depending on how the species

withstand drought. We distinguished two functional groups of deciduous and semi-deciduous

species with generally large SLA and low leaf thickness, and small to intermediate inter-seasonal

variations of pd. Evergreen species were also divided into two functional groups showing low

SLA, thick leaves and high inter-seasonal variations in pd. These groups represent strategies

which differ in their response to changing environmental conditions and should help forecast

community composition under future scenarios of climate change.


Appendices

Acacia tortilis Adansonia

digitata

Balanites

aegyptiaca

Celtis

integrifolia

Combretum

glutinosum

Faidherbia

albida

Neocarya

macrophylla

Sclerocarya

birrea

Tamarindus

indica

Rainy_Aug10 1.14±0.17fghij 0.55±0.1nop 1.47±0.21defgh 1.07±0.14ghij 1.69±0.13cde 1.04±0.14ghijkl 0.74±0.12jklmn 0.6±0.12mnop 1.51±0.23defg

Dry_Nov10 1.79±0.22cde 1.01±0.1hijkl 2.77±0.39ab 2.48±0.18abc 2.52±0.14abc 1.28±0.15efghi 1.04±0.13ghijk 0.67±0.12lmno 2.55±0.41abc

Dry_April11 1.94±0.23bcd 0.53±0.1nop 2.93±0.42a 1.85±0.16cd 2.33±0.14abc 1.69±0.17cde 0.89±0.13ijklm 0.41±0.12nop 2.38±0.37abc

Rainy_Jul11 0.46±0.13nop 0.37±0.11op 0.65±0.15lmno 0.51±0.12nop 0.56±0.12mnop 0.38±0.13op 0.24±0.11p 0.35±0.11op 0.46±0.13nop

Dry_Sep11 1.66±0.21cdef 0.73±0.1klmn 1.47±0.22defgh 1.03±0.13ghijkl 2.27±0.14abc 2.24±0.22abc 0.74±0.12jklmn 0.49±0.12nop 1.29±0.2efghi

Appendix S1. Predawn leaf water potential (- MPa) of 9 tree species in the Sahelian region of Senegal. Data are mean ± SE, n=6; (a) in different months;

(b) mean values per dry and rainy season. Values with different letters are significantly different (Post-hoc tests, P<0.05).

Capítulo 1

31

Acacia tortilis Adansonia

digitata

Balanites

aegyptiaca

Celtis

integrifolia

Combretum

glutinosum

Faidherbia

albida

Neocarya

macrophylla

Sclerocarya

birrea

Tamarindus

indica

Rainy_Aug10 1.34±0.26def 1.7±0.33bcdef 1.3±0.17def 3.22±0.58a 3.09±0.47a 0.58±0.19f 1.64±0.23cdef 1.67±0.29cdef 2.2±0.22abc

Dry_Nov10 1.82±0.35abcde 1.52±0.3cdef 1.87±0.19abcde 2.74±0.45ab 3.11±0.48a 2.05±0.56abcd 3.45±0.47a 2.42±0.45abc 2.33±0.23abc

Dry_April11 1.36±0.26def 0.17±0.36f 1.35±0.17def 1.78±0.27abcde 1.38±0.27def 1.77±0.44abcde 2.41±0.3abc 1.71±0.85abcde 1.69±0.19cdef

Rainy_Jul11 1.8±0.37abcde 1.1±0.23def 1.57±0.18cdef 1.79±0.28abcde 2.89±0.43a 1.97±0.63abcde 3.3±0.44a 1.23±0.23def 2.45±0.24ab

Dry_Sep11 0.83±0.2ef 1.14±0.24def 1.11±0.17def 1.6±0.25cdef 1.29±0.21def 0.28±0.16f 1.47±0.21cdef 1.33±0.24def 1.7±0.19cdef

Appendix S2. Mean LAI values of 9 tree species in the Sahelian region of Senegal. Data are mean ± SE, n=6; (a) in different months; (b) mean values

per dry and rainy season. Values with different letters are significantly different (Post-hoc tests, P<0.05).

33

CHAPTER 2: FUNCTIONAL RESPONSES OF FOUR SAHELIAN TREE

SPECIES TO RESOURCE AVAILABILITY

35

Summary

Plants experience a fluctuating environment in time and space. It is therefore important to

address plant responses to resource supply, as global change will impact resource availability

hence ecosystem productivity. We applied several treatments to four Sahelian tree species to

check for responses to resource availability, hypothesizing that it will change growth and

allocation patterns under different water and nutrient availability regimes. We selected four

species of great environmental and socio-economic importance in the Sahel, and grew seedlings

under a factorial design of water and nutrients, each with two levels. Our results showed

differences in RGR, R/S and SLA among species, water regimes and nutrient availability. Indeed,

RGR varied among species and was very responsive to water and nutrient availability, the

deciduous species showing overall high values under fertile conditions; with large RGR values

supported by large SLA values. Overall, our species allocated more biomass to roots, particularly

under low resource supply, reflecting adaptive strategies related to water and nutrient limitation.

Not all species showed similar phenotypic plasticity, however. Acacia tortilis and Faidherbia

albida showed the greatest responses, which reflect their greater spatial distribution in Africa. Our

data suggest that the different Sahelian species may respond differently to future environmental

changes, which likely will affect their spatial distribution and therefore the structure of plant

communities.

Capítulo 2

37

1. Introduction

Ecological systems show variability of their main characteristics, such as biodiversity and

productivity, in space and time (Ollier, 2004). They are also subjected to environmental variability,

for instance in the amount and seasonality of rainfall, which may have a critical influence on

ecosystem structure and productivity, particularly in water-limited ecosystems (Engelbrecht et al.,

2006, Clark et al., 2001, Gonzalez et al., 2012). Plant species respond to such variability by

occupying different habitats based on their stress tolerance strategy. It is well-known that water

shortage is one of the main factors limiting plant establishment and growth in arid ecosystems

(Armas and Pugnaire, 2005), ultimately shaping plant community structure (Padilla and Pugnaire,

2007) and productivity.

The relative growth rate (RGR), i.e, the increase in plant biomass over a given period of

time proportionally to the biomass present at the beginning of the period, is a prominent indicator

of plant strategies regarding productivity in relation to environmental stress and disturbance

(Pérez-Harguindeguy et al., 2013). Relative growth rates can be compared among species and

individuals that differ widely in size. Good insights into plant strategies can be obtained easily by

separating the components underlying growth variation, e.g., leaf, stem and root mass as well as

leaf area (LA). These underlying parameters are related to allocation (e.g., leaf-mass fraction, the

fraction of plant mass allocated to leaf), leaf morphology, and physiology (unit leaf rate, the rate of

increase in plant mass per unit LA, a variable closely related to the daily rate of photosynthesis

per unit LA; also known as net assimilation rate) (Pérez-Harguindeguy et al., 2013).

Plant species with different growth rates frequently occupy different habitats (Brendel and

Cochard, 2011) so that species that typically occur in “fertile” environments tend to have higher

RGRmax (maximum relative growth rate) than those typically occurring in “infertile” habitats

(Clarkson, 1967, AbdElRahman and Krzywinski, 2008, Grime, 1979, Ludlow, 1989, Chapin, 1980,

Plant responses to resource availability

Roupsard, 1997). In general, deciduous species show higher potential growth rates and higher

specific leaf areas (SLA) than perennials (Reich and Walters, 1992, Cornelissen et al., 1996,

Cornelissen et al., 1998, Reich et al., 1997, Reich, 1998), although it cannot be generalized

(Antúnez et al., 2001). Nonetheless, species with high RGRmax usually do not occupy infertile

habitats because their physiology is more sensitive to suboptimal resource levels and their RGR

decrease rapidly as fertility decreases (Meziane and Shipley, 1999).

Species changes in response to the environment is known as the reaction norm, an

important parameter to understand the process of plant species adaptation and evolution

(Gotthard and Nylin, 1995, Schlichting and Pigliucci, 1998) which has become a unifying concept

in evolutionary biology (Stearns, 1989). Species responses evolve by natural selection when

there are spatial heterogeneity in the selection pressures and extensive gene flow between sites

with different selection regimes (Gomulkiewicz and Kirkpatrick, 1992). Reaction norms have been

based on the assumption that tradeoffs (a linkage between two traits that affects the relative

fitness of genotypes and thereby prevents the traits from evolving independently) influence the

trajectory of evolution according to different behavioral and physiological processes that operate

within the lifetime of an individual (Angilletta et al., 2003). Allocation patterns in response to

resource availability are one such tradeoff.

We explored species responses to environmental severity by analyzing the reaction norm

and tradeoffs regarding RGR and water and nutrient availability in a greenhouse experiment with

four Sahelian tree species. The Sahel is a transition zone between the arid Sahara desert in the

north and (sub-) humid tropical savannas in the south. During the second half of the 20th century

the Sahel has experienced an important decrease in precipitation, causing severe droughts that

are having dramatic impacts on ecosystems and human population, most of which rely on the

natural resources of the region (Gardelle et al., 2010, Gonzalez, 2001, Nicholson, 2001).

Increased aridity and larger human populations, in addition to heterogeneity of environmental

Capítulo 2

39

conditions, have led to uneven changes and pressures on tree cover in the Sahel (Gonzalez et

al., 2012). As future climate projections predict more severe droughts in the African savanna

(Boko et al., 2007, Brooks, 2004), it seems important to identify species tolerant to drought (Cuni-

Sanchez et al., 2011) to design mitigation programs. Knowledge of native species could allow to

diversify agroforestry systems and mitigate environmental degradation (Dawson et al., 2009,

Leakey et al., 2006) and play an important role in environmental conservation and improvement

of productivity (Duru et al., 2000).

Here we aim to investigate the differences in seedling growth and morphology of four

Sahelian tree species testing the hypothesis that 1) plant species differ in their relative growth

rate (RGR) caused by habitat-related variation in abiotic factors, like water and nutrients; 2) plants

will preferentially allocate biomass to the organ harvesting the resource that is limiting growth ;

and, finally 3) in deciduous species the reaction norm will be stronger than in evergreen species

regarding water and/or nutrient availability.

2. Material and methods

A greenhouse experiment was established between November 2012 and August 2013 at

the University of Almería greenhouses (36º50'N, 2º27'W), Spain using two dry-deciduous

species, Acacia tortilis (Savi) Brenan and Adansonia digitata L., one wet-season deciduous

species (Faidherbia albida (Del.) Chev.), and one evergreen species, Tamarindus indica L. Seeds

of these four Sahelian species were acquired in Senegal (PRONASEF, Senegal National Project

of Forestry Seeds, Dakar) and subjected to a pre-germination treatment based on concentrated

sulfuric acid for 10 min (T. indica), 60 min (A. tortilis and F. albida) and 12 h (A. digitata).


Two seeds per species were sown in a sand and vermiculite mixture (1:1 in volume) in 50

cm long, 10 cm wide PVC tubes and thinned to one after germination. Plants were watered every

morning and received fertilizer once a month between November 2012 and March 2013. A

commercial fertilizer (NPK [Mg-S]; 19-19-19 [2-8]) was applied, using a nutrient solution of 0.5 g

fertilizer per liter of water (N+) to half of the plants per species. A second, low nutrient solution (N)

was prepared by diluting 1 L of N+ in 10 L. Two water regimes were designed to keep substrate

moisture at certain levels; one was low (W-), using 100 ml per week (i.e., one watering per week)

for half the plants, and one high (W+) using 200 ml per week (2 waterings per week, 100 ml each)

to the other half in a factorial design with water and nutrient as fixed factors. So, four treatments

were established in March 2013 according to nutrient and water regime, W+N+, W+N-, W-N+,

and W-N-. Each treatment included 6 to 9 replicates.

Capítulo 2

41

Fadherbia albida

Acacia tortilis

Tamarindus indica

Adansonia digitata

At harvest, nine months after sowing, plants were separated into above- and below-

ground parts, and the above-ground into leaves and stem. Plant parts were dried at 70ºC for 48 h

and weighed. We also recorded taproot length (measured with a ruler to 0.1 cm), largest stem

diameter (using an electronic caliper), and number of leaves. Six leaves per plant were scanned

with a flatbed scanner to determine specific leaf area (SLA). Total plant biomass (TPB) was

calculated by adding the dry mass of the different plant parts. Root-to-shoot ratio (R/S) was

calculated by dividing root mass by shoot mass. Relative growth rate (RGR) was estimated as

RGR = (ln TPB2 −ln TPB1)/(t2 −t1), where t is the elapsed time in days between sowing (T1) and

harvest (T2). In order to calculate TPB1 we selected 10 seeds per species, extracted the

embryos, dried them in an oven for at least 72 h at 70ºC, and weighted them with a precision

balance (to 10-6 g). Thus we use the mean TPB1 value per species.


We tested the ability of plants to alter their morphology in response to a change in

environmental conditions by measuring their reaction norms (RN). The reaction norm is a function

relating an environmental variable to the phenotype expressed by a genotype. So, RN measure

phenotypic plasticity, and can explain plant life-history (Day and Rowe, 2002). Seeds for each

species in this study were harvested in the same area so that their mother plants were subject to

the same soil and climatic conditions. We plotted RN regarding RGR and R/S vs. water and

nutrient supply.

The effects of water and soil nutrients in the growth of our woody species were analyzed

with linear mixed models. Main fixed factors were species, nutrient and water. No correction of

heterogeneity of variances or transformation of variables for normality was made. We also tested

the ability of plants to alter their morphology in response to a change in the environmental

conditions by measuring the reaction norms. We plotted RSR differences (amplitude) between

the highest and the lowest values per factor (nutrient and water). We calculated species age by

constructing a phylogeny of these four species with Phylomatic (Webb and Donoghue, 2005) and

used the “bladj” procedure to fix the root node at a specified age and then get the age of other

nodes (Webb and Donoghue, 2005).

Statistical analyses were performed with the Infostat software package (Di-Rienzo et al.,

2013). Reported values throughout the text and figures are means +/- 1 standard error.

Capítulo 2

43

3. Results

There were differences in RGR, R/S and SLA among species, water regime and nutrient

availability (Table 1). RGR was greater in Acacia tortilis and lowest in Tamarindus indica (Fig. 1).

All species reacted to water supply except T. indica, which showed a steady RGR independently

of the water and nutrient regime. The other 3 species reacted to both water and nutrients

availability as RGR at the two extreme treatments (W+N+ vs W-N-) were always different (higher

with higher resource supply) regardless the species. RGR at intermediate resource supply (W+N-

or W-N+) was in between the two extremes and was dependent on species identity (Fig. 1).

Figure 1. Relative growth rate (RGR) of Acacia tortilis, Adansonia digitata, Faidherbia albida and

Tamarindus indica individuals growing at two levels of nutrient availability (high, N+ and low, N-)

and two water regimes (W+ and W-). Data are mean ±1SE (n= 6-9). Different letters show

significant differences among species and treatments (post-hoc comparisons among species x

water x nutrient levels).

Treatments

W+N+ W+N- W-N+ W-N-

RG

R (

da

y-1

)

0.000

0.005

0.010

0.015

0.020

0.025

Acacia tortilis

Adansonia digitata

Faidherbia albida

Tamarindus indica

a

a a

b

d

e

b

cc c

f

f

ff

dede


SLA varied according to species as well (Fig. 2). It was greatest in Adansonia digitata,

and in general, all species increased their SLA with higher water and nutrient supply (Table 1).

SLA of A. tortilis was responsive to nutrient supply under low water availability, while SLA of F.

albida was more responsive to differences in water supply. The other two species had similar

SLA across treatments (Fig. 2).

Figure 2. Specific leaf area (SLA) of Acacia tortilis, Adansonia digitata, Faidherbia albida and

Tamarindus indica individuals growing at two levels of nutrient availability (high, N+ and low, N-)

and two water regimes (W+ and W-). Data are mean ±1SE (n= 6-9). Different letters show

significant differences (post-hoc comparisons among species x water x nutrient levels).

All species had R/S values above 1 (Fig. 3, Table 1; except A. tortilis in the W+ and A.

digitata in the W+N+ treatments), meaning they allocated relatively more biomass to roots than to

aboveground parts (Fig. 4). R/S increased as resources were limiting (Fig. 3) except in T. indica,

reaching extremely high values in Faidherbia albida. Overall, A. tortilis and F. albida were more

responsive to differences in water supply (i.e., differences in R/S were greatest between W- vs

W+ treatments).

Treatments

W+N+ W+N- W-N+ W-N-

SL

A (

m2

/kg

)

0

5

10

15

20

25

Acacia tortilis

Adansonia digitata

Faidherbia albida

Tamarindus indica

cdecde

e

bcd

a

abab

abcdabab

cdede

e

cde

e

abc

Capítulo 2

45

Figure 3. Root shoot ratio (R/S) of Acacia tortilis, Adansonia digitata, Faidherbia albida and Tamarindus indica individuals growing at two levels of nutrient availability (high, N+ and low, N-) and two water regimes (W+ and W-). Data are mean ±1SE (n= 6-9). Different letters show significant differences (post-hoc comparisons among species x water x nutrient levels).

d.f.

RGR R/S SLA

F-value p-value F-value p-value F-value p-value

(Intercept) 1 6832.59 <0.0001 1001.79 <0.0001 503.3 <0.0001

Species (S) 3 463.65 <0.0001 53.24 <0.0001 4.01 0.0094

Nutrient (N) 1 12.37 0.0006 7.39 0.0076 4.16 0.0437

Water (W) 1 12.34 0.0007 36.42 <0.0001 6.38 0.0129

S x N 3 0.47 0.7020 2.81 0.0428 1.78 0.1557

S x W 3 2.87 0.0398 8.58 <0.0001 0.71 0.5472

N x W 1 0.31 0.5804 8.58 <0.0001 0.71 0.5472

S x N x W 3 0.38 0.7709 1.2 0.3136 0.64 0.5934

Table 1. Results of linear models analysing differences in relative growth rate (RGR), root to

shoot ratio (R/S) and specific leaf area (SLA) of four Sahelian tree species growing under

different soil water and nutrient regimes (n=6-9). Species, level of fertilizer or water treatments

were included in the model as fixed factors with a full-factorial design. Significant p values are

highlighted in bold.

Treatments

W+N+ W+N- W-N+ W-N-

R/S

0

1

2

3

4

5

6

Acacia tortilis

Adansonia digitata

Faidherbia albida

Tamarindus indica

cd

c

b

a

cd

def defcde

ghh

fgef

h

ef

de

def


Acacia tortilis

Adansonia digitata

Faidherbia albida

Tamarindus indica

Figure 4. Mean relative biomass allocation (%) to roots, shoots and leaves of Acacia tortilis,

Adansonia digitata, Faidherbia albida and Tamarindus indica plants grown at two levels of

nutrient availability (high: N+, and low: N-) and two water regimes (W+ and W-).

Plants in the high nutrient treatment were taller than plants in the low nutrient treatment

except T. indica (Table 2). Shoot and leaf mass were greater in the high-nutrient treatment than in

the low-nutrient treatment (Table 2) except again in T. indica, but there was no effect of nutrient

regime on root mass of the different species (Table 2). Therefore, plant size (TPB) was much

higher in the high-nutrient treatment (Table 2) except T. indica, again. Water also had a

significant effect on plant growth (Table 1).

Treatments

W+N+ W+N- W-N+ W-N-

Bio

mass a

llocation (

%)

0

20

40

60

80

100

de d ee

b bc a a

cd cd dede

Leaf

Shoot

Root

Treatments

W+N+ W+N- W-N+ W-N-

Bio

mass a

llocation (

%)

0

20

40

60

80

100

cde f fef

b a a a

c cd defdef

Leaf

Shoot

Root

Treatments

W+N+ W+N- W-N+ W-N-

Bio

mass a

llocation (

%)

0

20

40

60

80

100

d ef

fgef

c b a a

de de gg

Root

Shoot

Leaf

Treatments

W+N+ W+N- W-N+ W-N-

Bio

mass a

llocation (

%)

0

20

40

60

80

100

c bc cbc

a a a a

bc bc bcb Leaf

Shoot

Root

Capítulo 2

47

Acacia tortilis Adansonia digitata Faidherbia albida Tamarindus indica

High Low High Low High Low High Low

Shoot mass (g) 1.61±0.22a 0.73±0.06b 1.34±0.23a 0.55±0.05c 1.22±0.12a 0.66±0.04bc 0.19±0.02d 0.18±0.02d

Root mass (g) 2.17±0.3b 1.6±0.19b 2.12±0.42b 1.46±0.21b 4.58±0.29a 4.18±0.27b 0.71±0.09c 0.76±0.09c

Leaf mass (g) 1.27±0.14a 0.56±0.05bc 0.97±0.25ab 0.44±0.06c 1.19±0.13a 0.47±0.04c 0.22±0.03d 0.26±0.03d

Total plant mass (g) 5.05±0.56b 2.86±0.26cd 4.44±0.76bc 2.44±0.32d 6.99±0.47a 5.3±0.31b 1.12±0.13e 1.2±0.13e

Plant height (cm) 44.67±3.16a 29.97±1.7c 24.45±2.85c 14.62±1.43d 46.96±2.33a 35.55±1.57b 10.22±0.78e 9.23±0.74e

Table 2. Responses of our four target tree species to nutrient addition. Data are mean ±1SE (n= 6-9); different letters in a row show significant differences

between species (p˂0.05).


High Low High Low High Low High Low

Shoot mass (g/plant) 1.44±0.21a 0.89±0.09b 1.15±0.22ab 0.74±0.09bc 1.19±0.12a 0.69±0.05c 0.21±0.02d 0.16±0.02d

Root mass (g/plant) 2.18±0.3b 1.58±0.2b 1.79±0.3b 1.79±0.36b 4.73±0.3a 4.03±0.26a 0.82±0.1c 0.65±0.09c

Leaf mass (g/plant) 1.07±0.12a 0.76±0.08bc 0.92±0.25ab 0.49±0.07d 0.98±0.12ab 0.68±0.06c 0.26±0.04d 0.22±0.03d

Total plant mass (g/plant) 4.7±0.52bc 3.21±0.32d 3.86±0.67cd 3.02±0.47d 6.9±0.47a 5.4±0.31b 1.29±0.14e 1.04±0.12e

Plant height (cm) 38.14±2.4b 36.49±2.67b 22.86±2.73c 16.21±1.66d 45.33±2.26a 37.17±1.68b 10.16±0.8e 9.29±0.71e

Table 3. Responses of our four target tree species to water addition. Data are mean ±1SE (n= 6-9); different letters in a row show significant differences

between species (p˂0.05).


Low water availability in general reduced plant height and shoot, leaves, and root mass

(Table 3). Total plant mass was much higher in the high-water regime (Table 3), except in A.

tortilis and T. indica. Overall Tamarindus indica was the only species that did not have a

significant response in biomass or allocation patterns in response to nutrient or water addition.

Reaction norms

The different species had different reaction norms regarding RGR and R/S (Fig. 5).

Under high water and high nutrient treatment, our species tended to increase RGR and allocated

more to aboveground parts. Water supply did affect RN of A. tortilis regarding RGR and R/S, and

R/S of F. albida, while nutrient supply changed RGR of A. tortilis and R/S in F. albida. The others

species showed less plasticity for these traits in this environmental set.

Capítulo 2

49

a)

b)

c)

d)

e)

f)

Figure 5. Reaction norms (RGR and R/S) of our four target woody species growing under high or low resource supply (water + nutrient). Different letters show significant differences among treatments (post-hoc comparisons).

Treatments

W+N+ W-N-

RG

R (

da

y-1

)

2

4

6

8

10

12

14

16

18

20

22

24


a

bb

c

d

e

ff

W+N+ W-N-

RG

R (

da

y-1

)

2

4

6

8

10

12

14

16

18

20

22

24 a

bb

c

d

e

ff

W+N+ W-N-

R/S

0

1

2

3

4

5

6

cd

a

cde

de

efgh

h

W+N- W-N-

RG

R (

da

y-1

)

0.002

0.004

0.006

0.008

0.010

0.012

0.014

0.016

0.018

0.020

0.022

0.024a

b

de

e

c c

f f

W+N- W-N-

R/S

0

1

2

3

4

5

6

a

c

h

efef

dedef

cde

Treatments

W-N+ W-N-

RG

R (

da

y-1

)

0.002

0.004

0.006

0.008

0.010

0.012

0.014

0.016

0.018

0.020

0.022

0.024a

b

c c

de e

ff

Treatments

W-N+ W-N-

R/S

0

1

2

3

4

5

6

b

a

cde

def de

fgef


4. Discussion

Our different tree species responded differently to resource availability, reacting to water

and nutrient supply. As expected, we found a positive relation between RGR and nutrient

availability (Cornelissen et al., 1998), showing higher RGR when resources were higher (Poorter,

1989). A notable exception is Tamarindus indica, which did not respond at all to different resource

supply.

Given adequate resources, high RGR is critical for plants to grow and occupy space,

both below- and above-ground, allowing them to acquire a larger share of limiting resources

(Grime 1999, Ruiz-Robleto and Villar, 2005). All our species except T. indica, which is evergreen,

are deciduous and show RGR values between 0.005 and 0.023 gxg-1xd-1, quite high compared

with other tree species growing in dry environments (Lamers et al., 2006, Atta et al., 2012,

Hoffmann and Franco, 2003). Deciduous species are characterized by RGR higher than

evergreen species (Sobrado, 1991, Antúnez et al., 2001, Wright et al., 2004, Ruiz-Robleto and

Villar, 2005) which is linked to a greater capacity to acquire nutrients (Lambers and Poorter,

1992). They show also higher phenotypic plasticity (Roupsard, 1997). Overall, species with high

growth rate generally have as well high rates of photosynthesis and respiration per unit mass,

requiring high concentrations of nitrogen and other nutrients to sustain such physiological activity

along with a high leaf turnover. Slow-growing species show opposite patterns (Reich et al., 1997,

Wright et al., 2004). In contrast to deciduous species, the evergreen T. indica did not respond to

resource addition. It is a species characterized by slow growth (El-Siddig et al., 2006, Diallo et al.,

2008) and its seedlings depend heavily on mycorrhiza (Ba et al., 2001, Bourou et al., 2010),

which most likely were absent in our seedlings. This species is in addition very high sensitive to

cold (Morton, 1987). It is native to dry, subtropical environments so it may have, over

Capítulo 2

51

evolutionary time, adjusted a low demand to a low supply to avoid exhaust limiting resources and

having their RGR functions closer to its optimum growth rate (Grime and Hunt, 1975, Chapin,

1980), patterns which enable this species to thrive in arid environments (Park et al., 2012).

RGR is the product of net assimilation rate (NAR) and leaf area ratio (LAR) (Evans,

1972). LAR in turn could be partitioned into specific leaf area (SLA) and leaf mass ratio (LMR).

Most studies concluded that LAR is the factor that the best explains differences in RGR, and the

most important component of which is SLA (Antúnez et al., 2001, Hoffmann and Franco, 2003,

Ruiz-Robleto and Villar, 2005) which reflects a trade-off in plant resource-use strategy which is

tightly coupled to resource availability. SLA increases from low to high soil resource availability

(Coley et al., 1985, Lavorel and Garnier, 2002, Evans, 1972) and in our experiment all species

increased SLA with higher water and nutrient supply (Fernández et al., 2002). Therefore, RGR

increase in our experiment was parallel to variations in SLA, supporting the view that SLA is the

most important factor sustaining RGR.

Biomass allocation patterns vary among species and are also sensitive to environmental

clues (Atkin et al., 2006). The relative amount of biomass allocated to the different plant organs

(leaves, stem and roots) is not fixed but may vary over time and across environments (Poorter et

al., 2012). Many studies have shown that drought stress influences allocation patterns (Liu and

Stützel, 2004, Spollen et al., 1993) particularly R/S values, which is one of the mechanisms

involved in the adaptation of plants to drought stress (Turner, 1997, Poorter et al., 2012). In our

experiment, R/S values were generally well above 1 irrespective of the species, suggesting a

genetically-fixed higher biomass allocation to roots when species are adapted to infertile

environments (Chapin, 1980, Aerts and Chapin, 2000, Lambers et al., 2008). R/S was highest in

Faidherbia albida, reaching a value of 4 under low water and nutrient levels and reflecting its

ability to strongly alter allocation patterns. It fact, F. albida is a species very sensitive to drought

(Roupsard, 1997) and its ability to quickly reach deeper, moister soil horizons may be critical in


coping with water stress at such an early stage to become established, as has also been shown

for other woody species in semiarid conditions (Padilla and Pugnaire, 2007). Opposite to its

dramatic response concerning R/S, RGR did not change much in F. albida, and SLA decreased

significantly only under reduced water availability. Faidherbia albida is a singular species in

several ways, as one of the few cases of species shedding leaves in the wet season (Roupsard

et al., 1996).

In our experiment, baobab (A. digitata) responded more to N addition than to water

addition. This may be because, while adult baobab trees accumulate water in their stem, baobab

seedlings use the taproot as main storage organ (Wickens and Lowe, 2008) allocating more

resources to belowground structures than adults (Cuni-Sanchez et al., 2011). As a consequence,

their ability to store water explains the different responses found. A similar strategy has also been

observed in other tropical tree species (Poorter and Markesteijn, 2008). Given the importance of

the taproot for seedling survival under dry spells (Padilla and Pugnaire, 2007, Poorter and

Markesteijn, 2008), seedlings with relatively larger taproots have a higher chance of survival in

drought-prone regions than seedlings with relatively smaller taproots, because they can store

both more water and more carbohydrates.

A characteristic of vegetation in arid environments such as the sahelian savanna is to

show high temporal and spatial variation in growth patterns, which depends on environmental

variability particularly in soil moisture (AbdElRahman and Krzywinski, 2008). In general, woody

plants in African savannas grow on nutrient-poor soils and they are slow-growing (Ward et al.,

2012). They are also adapted to high temperature variations and long droughts (Baumer, 1983),

in addition to low rainfall, high water variability, and high potential evapotranspiration

(Thornthwaite, 1948). This highlights the importance of water as a selection pressure (Noy-Meir,

1973) to which plants may respond through plasticity or evolution (Franks et al., 2014). An

increase in water availability causes great plastic responses in plant traits (Ward et al., 2012)

Capítulo 2

53

reflecting environmental effects on plant growth and development (Ackerly et al., 2000), since the

emergence of a phenotype is consequence of the interaction of a genotype with the environment

(AbdElRahman and Krzywinski, 2008). Spatial heterogeneity in the environment affects the

degree of phenotypic plasticity displayed by a plant population (Van-Kleunen and Fischer, 2005,

Volis et al., 2005) and serves as a selection driver.

Within our species, F. albida and A. tortilis showed high phenotypic plasticity -and

probably genotypic plasticity as well- which allows them to cope with water and nutrient variability

and explains their large geographical spread in Africa. In fact, a significant genetic diversity for F.

albida was showed by Roupsard (1997).

5. Conclusion

In conclusion, our data show that RGR varied among species and was very responsive to

water and nutrient availability, deciduous species showing overall high values under fertile

conditions, and large RGR being supported by large SLA. RGR was largest in Acacia tortilis and

smallest in Tamarindus indica. Overall, our species allocated more biomass to roots, reaching 4-

fold at times, reflecting adaptive strategies related to water and nutrient limitation. Our Sahelian

species responded more to nutrient than to water addition, and two species, Acacia tortilis and

Faidherbia albida, showed high phenotypic plasticity which supports their large distribution area.

Our data suggest that the different Sahelian species may respond differently to future

environmental changes, which likely will affect their spatial distribution and therefore the structure

of plant communities.

55

CHAPTER 3: TRAITS ASSOCIATED TO DROUGHT STRATEGIES

AFFECT THE EVOLUTION OF LEAF THICKNESS AND HABIT OF

MAIN WOODY SPECIES OF A SEMIARID SAHELIAN AGROFORESTRY

ECOSYSTEM

57

Summary

Drought is the main constraint in semi-arid environment as the Sahel savanna, so it is

important to understand the evolution of species to predict and mitigate the effects of

anthropogenic global change in this ecosystem. Utilizing functional traits of 20 sahelian woody

species collected in FUNCITREE project, we examined the hypothesis that sahelian woody

species phylogeny will show a low phylogeny diversity and favors high resource use efficiency.

Over two seasons (dry and wet) we monitored six traits reflecting above- and below-ground

strategies of resource acquisition such as predawn leaf water potential (pd), specific leaf area

(SLA), leaf thickness, and leaf area index (LAI), leaf nitrogen and carbone, and one

morphological trait, tree height. LAI and pd were measured six times during the dry and rainy

seasons, and the other traits were measured once. We add the foliage on the analisis.

We found a low Blomberg’s k value for all studied traits ranging 0.204 to 0.995, indicating

that they have low phylogenetic signal. But, significant phylogenetic signal was observed only on

leaf thickness and foliage. Thus, leaf thickness and foliage evolve in a Brownian motion,

experiencing a late radiation and a gradualism evolutionary mode where deciduous character is

the recent diverged. These data imply that deciduous character believes in semi-arid environment

as escape strategy favored by drought. So, it will be relevant to introduce evergreen woody

species in reforestation programs to diminish competition between deciduous species for water

use.

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1. Introduction

Climate change scenarios suggest an increase in aridity in many areas of the globe (Petit et

al., 1999). Since drought, along with temperature and radiation, is the most important constraint

to plant survival (Boyer, 1982), climate change in semiarid regions is expected to trigger

desertification processes (Peters et al., 2015) with serious consequences as semiarid

ecosystems sustain a considerable part of the world’s terrestrial biomass, net primary productivity

and biodiversity (Atjay et al., 1979). Changes in community composition induced by drought can

lead also to decrease phylogenetic diversity in plant communities (Knapp et al., 2008, Dinnage,

2009, Thuiller et al., 2011).

Higher plants respond to drought either by escaping, avoiding or tolerating water

shortage (Levitt, 1972, Turner, 1986). Escaping drought entails the completion of the life cycle

before the onset of drought (Bazzaz, 1979, Heschel and Riginos, 2005, Wu et al., 2010), a

strategy that follow annual species.

The avoidance strategy is common to both annual and perennial species while tolerance

occurs in plants able to endure low tissue water potential through suites of traits involving e.g.,

osmotic adjustment and the formation of more compact and stiff tissues (Lambers et al., 2008).

Evergreen species have lower maximum photosynthetic capacity, leaf nitrogen, and specific leaf

area than corresponding deciduous species.

Drought avoidance or escape can lead either to plastic or evolutionary changes (Franks,

2011). To determine the evolutionary history of a group of plants, morphological, biochemical,

physiological, structural, phenological, or behavioral characteristics (i.e., functional traits) are

often used, as they influence plant performance in a given environment (McGill et al., 2006).

Functional traits involved in the fitness of a species are subject to natural selection (Bernard-

Verdier, 2012); therefore the distribution of current trait values result from contemporary and past

Phylogeny and plant drought strategies

processes, and can be adaptive (through natural selection) or non-adaptive. Since these traits are

the product of evolution (Blomberg and Garland, 2002, Hansen and Orzack, 2005) they may have

evolved differently along different branches of the phylogeny. The footprint of this evolutionary

heritage in the current distribution of a trait is called phylogenetic signal, or the tendency of

phylogenetically close species to be more similar than distant species (Blomberg and Garland,

2002). However, according the Brownian model of evolution, species are assumed to diverge

over time in a manner analogous to a random walk, with variance increasing in proportion to the

square root of the sum of the evolutionary distance separating taxa (Felsenstein, 1985).

Trait evolution phenomena such as adaptive radiation, species specialization, and

punctuated change can all be tested using trait evolution models. These models use a variety of

indices to measure, and test for, phylogenetic signal in a quantitative trait. One can also quantify

the rate of evolution of different traits, or a single trait in different clades. Blomberg’s K (Blomberg

et al., 2003) and Pagel’s k (Pagel, 1999) assume a Brownian Motion model (BM) of trait

evolution. The Ornstein-Uhlenbeck (OU) is an evolutionary process with selection that differs from

BM, it possesses a selective optimum (Butler and King, 2004).

In addition, Coyle et al. (2014) showed that phylogenetic diversity should be low in

stressful environments because only certain clades have evolved the adaptations needed to

tolerate such conditions.

Using traits related to drought resistance of 20 woody species from the Sahel, we

explored species adaptation to drought and their potential responses to drying climate, expecting

that phylogenetic analysis would help distinguish escape and avoidance strategies. The Sahel is

a semi-arid, stressful environment, south of the Sahara desert where water is a main limiting

factor (Tucker et al., 1985, Hein et al., 2011). We hypothesized that Sahelian woody species will

show low phylogenetic diversity due to a long selection period for drought-resistant traits,

including those favoring high resource use efficiency.

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2. Material and methods

2.1. Tree community data

This study was conducted using the FUNCITREE Project database of vegetation in semi-

arid areas of Africa and South America (Mulder et al., 2013). We selected data from the Sahelian

area of Senegal, a tropical dry savannah characterized by periodic and prolonged droughts with

high temperatures during most of the year, dominated by the Harmattan (hot and dry winds with

huge sand storms and high desiccating capacity).

We selected plant traits as indicators of different functions related to resource capture

and use by plants (leaf nitrogen and carbon), water use strategies such as predawn leaf water

potential (pd), growth rate such as specific leaf area (SLA), in addition to leaf area index and

leaf thickness (Niinemets, 2001). pd provides information on plant water status as well as on its

capacity to take up soil water. Its value range is species-specific and depends, among others, on

rooting depth, root architecture, and root physiological properties (Pérez-Harguindeguy et al.,

2013). Leaf traits are commonly associated to life history, range distribution, and the species’

resource requirements. Specific leaf area is one of the most widely used leaf traits as an indicator

of plant responses to the environment. SLA is strongly linked to relative growth rate and the

resource-use strategy of the plant (Poorter and Garnier, 2007) and can be used to estimate

resource availability (Pérez-Harguindeguy et al., 2013). A related trait is leaf thickness, linked to

leaf construction costs, leaf lifespan and gas exchange (Loranger and Shipley, 2010). Finally, the

leaf area index (LAI; leaf area per unit ground area reflects the capacity of the plant to intercept

radiation (Jonckheere et al., 2004). pd and LAI may be inversely related (Bréda et al., 1995), as

higher LAI means higher evaporative surface which may lead to a decrease in pd. These four

traits thus reflect strategies in resource capture and use.


We measured these traits in six healthy, mature trees of each of 20 species, all growing

in the field (Table 1). pd and LAI measurements were carried out six times, 3 during the dry

season (November 2010, February and April 2011) and 3 during the rainy season (July 2010,

August and September 2011), whereas SLA and leaf thickness were measured once during the

rainy season, when leaves were at their best, for all species except for Faidherbia (which leaves

were collected in the dry season, as it is a rainy-season deciduous species). Finally, leaf C and N

contents (%) were analyzed with a Finnigan Delta Plus isotope mass spectrometer (Thermo

Fisher Scientific Inc., USA) with an associated elemental analyzer at SIRFER lab (Utah, USA;

http://sirfer.utah.edu/). Plant height was used to control for variability associated to tree size. Trait

data were collected following the protocols in Cornelissen et al. (2003b), Knevel et al. (2005) and

Pérez-Harguindeguy et al. (2013). Detailed information can be found in Chapter 1.

We compiled species-level means of all these traits (Appendix S1) also taking into

account their leaf habit in the analysis. Thus, we coded leaf phenology as 1 for evergreen and

semi-deciduous and 0 for deciduous species.

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63

Species Family Leaf habit

Acacia_nilotica (L.) Delile Fabaceae Deciduous

Acacia Senegal (L.) Willd Fabaceae Deciduous

Acacia seyal Del. Fabaceae Deciduous

Acacia tortilis subsp. raddiana (Savi) Brenan Fabaceae Deciduous

Adansonia digitata L. Malvaceae Deciduous

Annona senegalensis Pers. Annonaceae Deciduous

Aphania senegalensis (Juss. Ex poir.) Radlk. Sapindaceae Evergreen

Balanites aegyptiaca (L.) Del. Balanitaceae Evergreen

Bauhinia_rufescens Lam Fabaceae Deciduous

Celtis integrifolia Lam. Ulmaceae Evergreen to semi deciduous

Combretum glutinosum Perr. Ex DC. Combretaceae Evergreen

Cordia sinensis Lam Boraginaceae Evergreen

Faidherbia albida (Del.) Chev. Fabaceae Deciduous

Maytenus senegalensis (Lam.) Exell Celastraceae Evergreen

Neocarya macrophyla (Sabine) Prance Chrysobalanaceae Evergreen

Piliostigma reticulatum (DC.) Hochst. Fabaceae Evergreen

Prosopis juliflora (Sw.) DC. Fabaceae Deciduous

Sclerocarya birrea (A. Rich) Hochst Anacardiaceae Deciduous

Tamarindus indica L. Fabaceae Evergreen to semi deciduous

Ziziphus mauritiana Lam Rhamnaceae Deciduous

Table1. List of the Sahelian tree species analyzed their habit.

2.2. Phylogeny

Since species are related phylogenetically, species data points are not statistically

independent and phylogenetic distances should be taken into account in the statistical analysis

(Felsenstein, 1985, Paradis, 2006). We constructed a phylogeny of our species with 20 tips and

15 internal nodes (Fig. 1, Appendix S2) using the Phylomatic online software v.2 (Webb et al.,


2008), which provides a dendrogram resolved to the genus level based on the Angiosperm

Phylogeny Group III (Stevens, 2012). Branch lengths were assigned using the BladJ function of

the Phylocom software, which assigned nodal ages down to the family-level (Wikström et al.,

2001). Where node ages were unavailable, the software split known distances evenly between

ageless nodes and branch tips occurring between or after known nodes. Similar phylogenies

have been useful in evaluating ecological hypotheses about the phylogenetic relationships among

species in natural communities (Cavender-Bares et al., 2009, Kembel and Hubbell, 2006, Kraft

and Ackerly, 2010).

Figure 1. Phylogenetic tree of 20 Sahelian woody species. Branch lengths were assigned using

the BladJ function which assign nodal ages down to the family-level. Newick file in Appendix S2.

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65

2.3. Statistical analysis

We tested for phylogenetic relatedness in trait values, or “phylogenetic signal” for each

trait using Blomberg’s K (Blomberg et al., 2003). K measures the extent to which related species

retain similar trait values due to their shared ancestry. In the absence of phylogenetic signal K=0,

while K=1 when trait values evolve by Brownian Motion Model (BM) along the phylogeny. Finally,

K values ˃1 suggest stronger phylogenetic structure, i.e., trait similarity among phylogenetically

related species stronger than expected under the null model. The phylogenetic signal, however,

is a pattern that can arise from a diversity of underlying evolutionary processes (Revell et al.,

2008). It is common to equate low phylogenetic signal with evolutionary lability (Blomberg et al.,

2003), whereas strong phylogenetic signal has been interpreted as a sign of niche or evolutionary

conservatism (Swenson et al., 2007).

The statistical significance of K was estimated by calculating the variance of

phylogenetically independent contrasts (PICs). These analyses were performed using the Picante

package in R (Kembel et al., 2010).

A Phylogenetic Least Squares model (PGLS) was used to test if phylogenetic signal

through leaf thickness and leaf habit would help us distinguish escape and avoidance strategies.

First we used the lowest-AIC criterion to determine which of the three most-common models of

evolution, Brownian, Pagel or Ornstein-Uhlenbeck (Paradis, 2006), better described the evolution

of leaf thickness and leaf habit. We then set the most appropriate evolutionary model to test

significant relationship between these traits that had significant phylogenetic signal and the others

traits by adding interactions and/or covariates.

All phylogenetic analyses were performed using R using phylogenetic packages “ape”,

“mvtnorm”, “MASS”, “nlme”, “geiger”, “car”, “effects” and “phytools”.


3. Results

Our results showed a significant phylogenetic signal (P >0.05 for PIC variance results) for

some traits, such as leaf thickness and leaf lifespan (Table 2), with Blomberg’s k value close to 1,

suggesting late radiation followed by gradual evolution. Nonetheless, Blomberg’s k values were

low for all traits, ranging 0.204 to 0.995. As low phylogenetic signal limited the ability to infer

patterns of character evolution, we focused only on traits that had a significant phylogenetic

signal.

PIC

K Z P

Plant height 0.693 -1.141 0.088

LAI 0.274 0.032 0.665

C 0.204 0.661 0.719

N 0.260 0.129 0.635

Leaf thickness 0.751 -1.830 0.011

pd 0.446 -1.079 0.163

SLA 0.197 1.162 0.845

Leaf /habit 0.995 -3.224 0.022

Table 2. Results of phylogenic signal analysis using Blomberg’s K for 20 sahelian woody species,

and PIC (Phylogenetic Independent Contrast) analysis (?)Phylogenetic signal significantly

different (p < 0.05) is showed in bold.

The PGLS analysis of leaf thickness and phenology showed that the Brownian motion

model applied better to leaf thickness while the Pagel model suited leaf habit better (Table 3).

Leaf thickness and leaf lifespan had positive coefficient value, indicating that low thickness and

deciduous character are more recent. We found significant e relation between leaf thickness and

SLA, LAI and leaf N whereas there were any significant phylogenetic relation between leaf habit

Capítulo 3

67

and the others traits (Table 4). So, species with high leaf thickness had low SLA, high LAI and

leaf N while species with low leaf thickness had high SLA, low LAI and leaf N (Table 4).

Evolutionary models

Brownian Pagel Ornstein-Uhlenbeck

AIC Coef.value SE AIC Coef.value SE AIC Coef.value SE

Leaf thickness

-23.742* 0.339 0.083 -22.621 0.338 0.072 -17.144 0.304 0.027

Leaf habit 24.363 0.536 0.293 -53.192* 0.536 0.307 37.359 0.450 0.114

* Model with the lowest AIC shows the best evolutionary model.

Table 3. Selection of the best evolutionary model using the lowest-AIC criterion, with its

coefficient value and standard error.

Estimate t-test P

(Intercept) 0.8928177 1.6747637 0.1198

pd 0.1083302 1.1408591 0.2762

Height 0.0025182 0.2190194 0.8303

LAI 0.1987341 2.3283185 0.0382

C -0.0165353 -1.5698450 0.1424

N 0.0862596 2.0597078 0.0618

SLA -0.0429561 -2.4598034 0.0300

Leaf habit 0.0774269 1.2962063 0.2193

Table 4.- Phylogenetic Generalized Least Squares predictors and their estimated effects for the

best evolutionary model for testing the relationship between leaf thickness and the others traits.


4. Discussion

We expected that Sahelian woody species would show low phylogenetic diversity as having

evolved under conditions favoring high resource use efficiency. In addition, we expected that

phylogenetic analysis would tell apart species with the escape and avoidance strategies to

drought.

Our data showed a significant phylogenetic signal only for leaf thickness and leaf

lifespan, which were positively correlated. This involves phylogenetic niche conservatism (Diniz-

Filho et al., 2012). But the fact that these traits had a Blomberg’s K value close to 1 shows they

evolved in a Brownian motion manner, i.e., the more closely related the species, the less

phenotypic difference between them (Blomberg and Garland, 2002). In a Brownian-type

evolution, the amount of change in any given interval is generally small and random in direction;

such a pattern of evolution could emerge either from genetic drift or from natural selection that

randomly fluctuated through time in direction and magnitude (Losos, 2008). Under the Brownian

motion model, evolutionary changes are simply added to values present in the previous

generation or at the previous node in a phylogenetic tree. Thus, members of lineages that have

only recently diverged will necessarily (on average) tend to be similar, as compared with more

distantly related lineages (Blomberg et al., 2003). This is our case, leaf thickness and habit had a

Blomberg’s K value close to 1, suggesting late radiation followed by gradual evolution. As their

coefficient value are positive, evergreen character and high leaf thickness are respectively more

ancient than deciduous character and low thickness that seem diverged recently indicating that,

abiotic factors selected for distinct leaf traits (Pringle et al., 2011).

Apart from leaf thickness and habit, the remaining traits showed Blomberg’s k values

lower than 1, indicating low phylogenetic signal. Leaf thickness was related with others leaf traits

such as SLA, LAI and leaf N. Such relation allowed us to distinguish life history strategies

Capítulo 3

69

regarding drought. Species with higher leaf thickness tend to be evergreen or semideciduous with

lower SLA, high LAI and leaf N while species with low leaf thickness are deciduous with high

SLA, low LAI and leaf N.

Phenotypic trait values of species in a community are shaped by their previous

evolutionary history (Harvey and Pagel, 1991). Thus, phylogenies contain signatures of past

evolutionary processes that led to contemporary biodiversity (Münkemüller et al., 2012), and the

phylogenetic signal is often interpreted as providing information about evolutionary processes or

rates of evolution (Revell et al., 2008). A low phylogenetic signal seems to imply rapid

evolutionary change, but does not specify a process that can be, for example, genetic drift or

natural selection (Gittleman et al., 1996, Blomberg et al., 2003). Our data showed a low

phylogenetic signal for most traits, suggesting rapid evolutionary change. For Revell et al. (2008))

a phylogenetic signal was low for conditions of strong stabilizing selection to a single optimum as

well as for conditions of strong, regular divergent selection; and phylogenetic signal was usually

uncorrelated with rate. Therefore, phylogenetic diversity should be low in the most stressful

environments (Coyle et al., 2014, Webb et al., 2002) such as semi-arid Sahelian savannahs.

Drought may act as a selection driver causing genetically-based evolutionary changes in

avoidance or escape (Fox, 1990, Ludwig et al., 2004); so plants can respond to drought through

evolution or plasticity (Franks, 2011). Therefore what we recorded suggests that our species may

respond to drought more for plasticity as they showed a lowed phylogenetic signal (closely

related species convergence not due to drought pressure).

In fact, plants have evolved a diversity of life history strategies to succeed in the varied

environments of the Earth (Adler et al., 2014). Leaf life span and SLA are often considered to be

the central traits under selection, as they are inferred to determine the position of the species

along this continuum (Westoby et al., 2002). For example, deciduous and evergreen trees that

have different leaf lifespans and frequently occupy different habitat types (Antúnez et al., 2001).


According to Antúnez et al. (2001), the only attribute consistently associated with the evergreen

habit was a low SLA. Leaves with higher SLA tend to have faster metabolic rates and shorter leaf

lifespan, and this strategy is favored in more fertile habitats (Wright et al., 2004). By contrary,

leaves with low SLA and evergreen habit (long leaf lifespan) are smaller, and small leaves are

often viewed as an adaptation to low water or high temperature environments (Ackerly, 2009).

Species with slow leaf economics traits (high leaf lifespans, low SLA), might also lead slow

growth rates (Poorter and Bongers, 2006). Such species can construct long-lived, well-defended

leaves that are often favored in low resource environments or build leaves that assimilate carbon

quickly under conditions of high resource availability but are prone to rapid tissue loss (Adler et

al., 2014).

These observations agree with our data that show that evergreen species with low SLA

have high leaf thickness, while the deciduous are characterized by high SLA and low leaf

thickness. In semi–arid environments such as the Sahelian savanna, where water shortage is the

main constraint for plant growth, these observations correspond with different plant drought

strategies. The adaptation mechanisms to withstand water shortage become more and more

developed and complex moving from wet areas towards arid areas, where the regularity of

drought events leads to the development of different strategies (Monneveux and Belhassen,

1996). It is well known that conservative water use can be adaptive, particularly in environments

that are consistently water limited (Ludlow, 1989, Bray, 1997, Taiz and Zeiger, 2006). Thus,

Franks (2011) considered that the reason why drought may favor a escape rather than avoidance

strategy in plants is probably a result of the interaction between environmental conditions and

plant life history in these environments. This would justify the recent diverged deciduous habit of

our study species. Moreover, in a drought-escape adaptive strategy, selection should favor plants

with high stomatal conductance, high photosynthetic rate, and low water use efficiency (Sherrard

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71

and Maherali, 2006), while it would favour conservative water use through stomatal closure in

species with drought avoidance strategy (Geber and Dawson, 1997, Arntz and Delph, 2001).

5 Conclusion

In conclusion, our data showed that leaf thickness and leaf habit (evergreen or

deciduous) had a significant phylogenetic signal. These traits evolved in our Sahelian species

following a Brownian motion model, which suggests late radiation and gradual evolutionary mode

and thus a recent divergence of the deciduous syndrome. Overall our data suggest that the

deciduous syndrome have been evolutionary favored in semi-arid environments as the Sahel

region. Deciduous and evergreen trees have different leaf life spans and frequently occupy

different habitat types related to different adaptive drought strategies; escape vs dehydration

avoidance strategy, respectively. Savanna environments are characterized by periodic and

intense drought events that favoured species with a escape rather than avoidance drought

strategy.

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Appendices

Appendix S1.- Mean trait values for the 20 woody Sahelian species analyzed

FAMILIES

SPECIES Height

(m)

LAI C (%) N (%) Thickness (mm)

Leaf Pot. (MPa)

SLA (m²/kg)

Leaf habit

Fabaceae Acacia nilotica 5.75 1.96 51.03 2.57 0.19 -1.21 6.28 0

Fabaceae Acacia senegal 7.25 2.45 44.98 4.5 0.28 -1.80 12.33 0

Fabaceae Acacia seyal 4.875 1.74 45.48 2.62 0.16 -1.48 7.76 0

Fabaceae Acacia tortilis 5.92 2.14 45.75 2.92 0.21 -1.33 9.94 0

Malvaceae Adansonia digitata 10.29 1.72 43.92 2.6 0.47 -0.66 5.07 0

Annonaceae Annona senegalensis 0.97 2.18 43.96 1.94 0.40 -1.17 6.90 0

Sapindaceae Aphania senegalensis 4.13 1.92 47.28 2.18 0.27 -0.88 8.65 1

Zygophyllaceae Balanites aegyptiaca 6.75 1.65 45.46 2.68 0.50 -1.64 5.28 1

Fabaceae Bauhinia rufescens 4.25 2.05 46.43 2.73 0.17 -1.40 8.80 0

Capparaceae Boscia senegalensis 1.71 2.27 43.56 3.23 0.35 -2.76 5.97 0

Ulmaceae Celtis integrifolia 11.42 1.89 39.85 2.33 0.32 -1.45 7.86 1

Combretaceae Combretum glutinosum 6.13 2.34 47.80 1.71 0.38 -1.57 5.66 1

Boraginaceae Cordia sinensis 6 1.01 45.8 4.2 0.13 -1.23 8.83 1

Capparaceae Crateva religiosa 8.08 1.98 41.90 2.78 0.25 -0.93 10.04 0

Fabaceae Faidherbia albida 8.67 1.45 47.10 2.33 0.27 -1.09 4.97 0

Celastraceae Maytenus senegalensis 2.39 2.07 46.66 1.64 0.39 -1.51 5.30 1

Chrysobalanaceae Neocarya macrophylla 6.08 2.15 47.05 1.38 0.44 -0.77 5.20 1

Fabaceae Pliostigma reticulatum 6 1.90 46.75 2 0.52 -0.85 7.31 1

Fabaceae Prosopis juliflora 8.17 2.27 43.93 2.87 0.14 -1.40 9.65 0

Anacardiaceae Sclerocarya birrea 8.58 1.88 45.44 1.52 0.24 -0.54 9.85 0

Fabaceae Tamarindus indica 7.18 2.05 46.54 1.82 0.26 -1.61 8.78 1

Rhamnaceae Ziziphus mauritiana 5.33 1.76 46.04 2.27 0.33 -1.75 5.37 0

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Appendix S2 Newick file format of 20 Sahelian woody species Phylogenetic tree with nodal ages

down to the family-level.

((((((((((((((((((((((((((((((((((((((((Acacia_senegal:15.853659,Acacia_seyal:15.853659,Acacia_tortilis

:15.853659,Acacia_nilotica:15.853659)acacia:15.853659,(((Faidherbia_albida:7.926829)faidherbi

a:7.926829):7.926828)ingeae:7.926830):7.926830):7.926826,((Prosopis_juliflora:15.853658)pros

opis:15.853658)prosopis_group:15.853659):7.926830):7.926830):7.926826):7.926834):7.926826

):7.926826)mimosoids:7.926834):7.926826):7.926826):7.926834):7.926834):7.926819):7.926834

):7.926834):7.926819,((Bauhinia_rufescens:55.487804)bauhinia:55.487804)cercideae:55.487801

,(Tamarindus_indica:83.231705)tamarindus:83.231705,(Piliostigma_reticulatum:83.231705)piliost

igma:83.231705)fabaceae:7.926834):7.926834)fabales:7.926819,((((((Celtis_integrifolia:35.67073

1)celtis:35.670731)ulmaceae:35.670731):35.670731,((((((((Ziziphus_mauritiana:15.853658)ziziph

us:15.853658):15.853659)paliureae:15.853657)ziziphoids:15.853657):15.853661)rhamnaceae:15

.853661):15.853653):15.853661):15.853653)rosales:15.853668):15.853653):7.926834,((((((((Neo

carya_macrophylla:22.018970)neocarya:22.018970)chrysobalanaceae:22.018967):22.018974):2

2.018967):22.018967)malpighiales:22.018982):22.018967,(((Maytenus_senegalensis:44.037941)

maytenus:44.037941)celastraceae:44.037949)celastrales:44.037933)celastrales_to_malpighiales

:22.018967):7.926834,(((Balanites_aegyptiaca:51.524391)balanites:51.524391)zygophyllaceae:5

1.524399)zygophyllales:51.524384)fabids:7.926819,(((((((((((Sclerocarya_birrea:17.835365)scler

ocarya:17.835365)anacardiaceae:17.835365):17.835365):17.835365,(((Aphania_senegalensis:2

2.294207)aphania:22.294207)sapindaceae:22.294209):22.294205):17.835365):17.835365)sapin

dales:17.835365,(((((((Adansonia_digitata:17.835365)adansonia:17.835365)malvaceae:17.83536

5):17.835365):17.835365)malvales:17.835365)malvales_to_brassicales:17.835365)huerteales_to

_brassicales:17.835365):17.835358):17.835373):17.835373,((((Combretum_glutinosum:39.2378

04)combretum:39.237804)combretaceae:39.237808)myrtales:39.237801):39.237808)malvids:17.

835358):7.926834)rosids:7.926834):7.926819,((((((((((Cordia_sinensis:21.618624)cordia:21.6186

24)boraginaceae:21.618626):21.618622)lamiids:21.618629):21.618622)ericales_to_asterales:21.

618622)asterids:21.618622,((((((Tamarix_senegalensis:24.706999)tamarix:24.706999)tamaricac

eae:24.706997):24.707001):24.707001):24.706993)caryophyllales:24.707001):21.618637):21.61

8622):21.618622):7.926834)core_eudicots:7.926834)trochodendrales_to_asterales:7.926819)sa

biales_to_asterales:7.926849)eudicots:7.926819)ceratophyllales_and_eudicots:7.926819)poales

_to_asterales:7.926849,(((((((((Annona_senegalensis:29.329269)annona:29.329269)annonaceae

:29.329269):29.329269):29.329269):29.329269)magnoliales:29.329269):29.329269)magnoliids:2

9.329285):29.329254)magnoliales_to_asterales:7.926819)austrobaileyales_to_asterales:7.92681

9)nymphaeales_to_asterales:7.926849)angiosperms:7.926829)seedplants:75.000000)euphylloph

yte:1.000000;

75

CONCLUSIONES GENERALES

Las diferentes especies leñosas sahelianas muestran distintos rangos de valores en

los rasgos funcionales que reflejan los mecanismos adaptativos a la sequía. Estos

rasgos funcionales nos permitieron identificar diferentes estrategias de las plantas y

agrupar a las especies en cuatro grupos funcionales diferentes:

Dos grupos funcionales de especies de hojas caducas y semi-deciduas,

caracterizadas por tener generalmente un área específica de hoja (SLA) alto

y hojas finas (menor grosor de hojas), con variaciones pequeñas a

intermedias del potencial hídrico según la época.

Las especies de hoja perene están divididas también en dos grupos en

función del SLA, grosor de la hoja y variaciones del potencial hídrico de

hoja al año según la época.

Estos grupos representan estrategias que difieren en su respuesta a las variaciones de

condiciones ambientales y deberían ayudar a predecir la composición de la

comunidad respecto a los escenarios futuros de cambio climático.

La razón de crecimiento relativo (RGR) varió entre especies y fue muy sensible a la

disponibilidad de agua y nutrientes. Las especies caducifolias mostraron valores

más altos en condiciones fértiles, con tasas importantes de RGR apoyadas por hojas

con un SLA alto. La RGR fue más alta en Acacia tortilis y más pequeña en

Tamarindus indica.

Las especies asignaron más biomasa a las raíces, llegando a asignar 4 veces más que

a los tallos, reflejando estrategias de adaptación relacionadas con el agua y los

nutrientes.

Conclusiones

Las especies Sahelianas respondieron más a la adición de nutrientes que a la de

agua. Dos especies, Acacia tortilis y Faidherbia albida, mostraron una alta

plasticidad fenotípica, que apoya su gran área de distribución geográfica.

Estos resultados sugieren que las distintas especies del Sahel pueden responder de

manera diferente a los cambios ambientales futuros, que probablemente afectarán a

su distribución espacial y, por tanto, la estructura de las comunidades vegetales.

El grosor de la hoja y el tipo de hojas tenían una señal filogenética significativa

mostrando que han evolucionado con un movimiento browniano, experimentando

una radiación tarde y un modo evolutivo gradual después. El carácter de hoja caduca

es el que ha divergido más recientemente. Las especies de hoja caduca se verán

favorecidos por la evolución futura del clima en un ambiente semiárido como el

Sahel.

Las especies de hoja caduca y de hoja perenne tienen diferente duración de vida de

la hoja y ocupan frecuentemente diferentes tipos de hábitat. Estas estrategias se

corresponden, respectivamente, a las de escapar y evitar la deshidratación, que son

las estrategias generales de adaptación a la sequía.

Como el Sahel presenta sequía a menudo, puede ser interesante utilizar especies de

hoja perenne y caducas en programas de reforestación, ya que especies cercanas

evolutivamente tienden a ser ecológicamente similares y muestran mayores tasas de

competencia.

77

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