Efectos del estrés abiótico y factores bióticos en las interacciones planta planta: implicaciones para el funcionamiento y la restauración de los ecosistemas semiáridos
Autor: Santiago Soliveres Codina 1,2
Directores: Fernando T. Maestre Gil 1, Adrián Escudero Alcántara 1 y Fernando Valladares Ros 2
1Área de Biodiversidad y Conservación. Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos. 2 Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, Consejo Superior de Investigaciones Científicas.
Madrid, 2010
Dr. Fernando T. Maestre Gil y Dr. Adrián Escudero Alcántara, Profesor Titular y Catedrático de Universidad del Departamento de Biología y Geología de la Universidad Rey Juan Carlos, respectivamente, y Fernando Valladares Ros, Profesor de Investigación del Instituto de Recursos Naturales (Centro de Ciencias Medioambientales) del Consejo Superior de Investigaciones Científicas,
CERTIFICAN:
Que los trabajos de investigación desarrollados en la memoria de tesis doctoral: “ Efectos del estrés abiótico y factores bióticos en las interacciones planta planta: implicaciones para el funcionamiento y la restauración de los ecosistemas semiáridos ”, son aptos para ser presentados por el Ldo. Santiago Soliveres Codina ante el Tribunal que en su día se consigne, para aspirar al Grado de Doctor en Ciencias Ambientales por la Universidad Rey Juan Carlos de Madrid.
VºBº Director Tesis VºBº Director de Tesis
Dr. Fernando T. Maestre Gil Dr. Adrián Escudero Alcántara
VºBº Director Tesis
Dr. Fernando Valladares Ros
A mi madre, por ser mi inspiración
A Soraya, por ser mi Todo.
La transición de los datos a la teoría requiere imaginación creativa. Las hipótesis y teorías científicas no se “derivan” de los hechos observados, sino que se “inventan” para dar cuenta de ellos.
Carl Hempel
AGRADECIMIENTOS
“Joer, que cuatro años más largos” es lo primero que me viene a la mente al empezar a escribir estos agradecimientos. Pero después echo la vista atrás y me doy cuenta que he vivido un montón de experiencias, muchas más buenas que malas, y que he aprendido mucho en este proceso que es la tesis, he disfrutado muchísimo y me he formado como científico, y aún más importante, como persona (nunca es tarde para esto último, jeje). Todo esto se lo tengo que agradecer a la gente que me ha rodeado, apoyado y ayudado durante toda esta importante etapa de mi vida, a ellos va dedicada esta sección.
En primer lugar les quiero agradecer a mis directores de tesis el haberme brindado esta oportunidad, el haber trabajado mucho y muy duro para que pudiera colaborar con un montón de gente distinta, aprender cuanto necesitara en el camino y no tener que preocuparme por problemas de financiación, algo básico para poder hacer ciencia. Muy especialmente te quería agradecer a ti, Fernando (Maestre), por tu apoyo continuo y por ser un director inmejorable. Sin tu ayuda y apoyo, tus innumerables ideas y la inmensa cantidad de horas que has invertido, mirando y revisando cada uno de los capítulos de esta tesis en cada una de sus fases, esto no habría sido posible. Pero te quiero agradecer mucho más, el haberme enseñado una forma de trabajar que no tiene precio, y el haberme dado un ejemplo a seguir como profesional y como persona. A ti, Adrián, te tengo que agradecer tu infinita paciencia y todos los comentarios y aportaciones que has hecho a muchos de los trabajos que aquí se presentan. Me has ayudado muchísimo a entender la ecología de comunidades y muchas otras ecologías. Las discusiones científicas que hemos tenido y todos tus comentarios al respecto, han sido todo un placer y un aprendizaje estupendo, sin mencionar la estadística! Y sobre todo me has enseñado a ser crítico con todo lo que leo y escribo, y a aprender a formarme un criterio propio, lo cual sin duda me ayudará a ser mejor científico. Fernando (Valladares) es sin duda el responsable de que yo pudiera tener una beca para poder hacer la tesis. Te agradezco también que siempre hayas conseguido sacar un rato para ayudarme en muchas etapas de esta tesis, tus continuas aportaciones a muchos de estos trabajos sin duda han mejorado su calidad. Dudo que pocas personas sepan más del efecto de la sombra y de ecofisiología en general que tú, sólo espero haber sido un buen alumno.
A Pablo decirte que has sido un compañero de tesis excepcional, no tengo palabras para agradecerte tu continuo apoyo a lo largo de toda esta etapa de mi vida. He aprendido muchísimo de ti y, para mí, eres todo un ejemplo a seguir por muchas cosas. Por tu inmensa capacidad de trabajo, por no dejarte caer nunca y tirar siempre adelante, fueran cuales fueran las circunstancias y porque tienes unos coj… como no los tiene nadie. Muchísimas gracias también por todos los buenos momentos que he pasado contigo, en la uni, en los taludes, en las fieldtrips, en las roadtrips, y en las trips callejeras y camperas nocturnas y diurnas, y por acogerme en tu casa siempre que lo he necesitado. También por ser sin duda el maestro de ceremonias del grupo, por las Aranjuez summer festival, las fiestas en tu casa, por enseñarme las jam sessions madrileñas, por las cenas y por todo lo demás, mi experiencia madrileña hubiera sido mucho peor si no hubieras estado. Espero que nos encontremos muchas veces más en el camino. Andrea, a ti también te quería agradecer el ser una compañera estupenda, y tu ayuda en muchas fases de esta tesis. No te creas que me olvidé de quien se quedó conmigo aquellos primeros días hasta las 10 de la noche cortando los p… protectores para los conejos. Espero que te vaya muy bien en lo que emprendas en el futuro. Los tres hemos vivido muchos momentos juntos que recordaré siempre con cariño (eso de subir garrafas monte arriba es que une mucho, jeje), y que espero que se repitan en el futuro. Me gustaría agradecer a Jorgito (alias Piruan) por ser un compañero estupendo durante mis primeros pasos en el mundillo de la ecología, por tu incontenible curiosidad y tus ganas de aprender siempre cosas nuevas. Tampoco me olvido de que me has apoyado siempre, y has confiado en mí como pocos. Espero que te esté yendo genial allá por la Puna.
Tengo que decir que estoy tremendamente orgulloso de pertenecer y haber trabajado en el departamento de Biología y Geología de la URJC. El nivel científico de los Biodiversos es incuestionable, pero aún es mucho mayor el nivel humano, el buen ambiente que se respira y lo fácil que es trabajar con todos vosotros. Desde luego hacéis que ir a trabajar cada día sea más un placer que una obligación. Muchísimas gracias por haberme aceptado y acogido, y sobre todo, por haberme soportado. Recuerdo cómo Rubén y yo hablábamos en susurros el primer día, cuando me estaba enseñando los despachos y presentándome a la gente…aquella fue la única vez que hablé flojo en ese departamento, y sin embargo, todos los biodiversos han sabido perdonarme (o eso espero)… También espero que sepáis perdonarme mi sentido del humor algo “brusco” y no siempre acertado, espero que sepáis que siempre fue sin mala intención. En especial quería agradecerles a mis compis de despacho todos los buenos momentos que he vivido con vosotros durante estos años. A Cris Escolar, la pequeña del
grupo fernandiano, por tu eterna alegría contagiosa y por ser una compañera genial. A Edu, aquel señor bajito, con el pelo de dudosa procedencia, y oriundo de “un país chiquito, al ladito del cielo”. Simplemente, personas como tú hacen que el mundo sea un lugar mejor. Muchas gracias por preocuparte por todos nosotros siempre, por ser el alma de Biodispersos (Úbeda queda como testigo) y por no parar de organizar cosas para que, aquellos que estuviéramos fuera y añoráramos a nuestra gente, nos sintiéramos siempre como en casa. A todos los demás, Ares, Sonia, Mari Carmen, Samu, Pablo, Alberto, Rubén Milla y Alf (si, si…os escapasteis, pero para mí seguís siendo de mi despacho), muchas gracias por vuestra paciencia y ayuda, por todo lo que nos hemos reído y por los buenos recuerdos que me llevo de todos vosotros. Gracias a todos por hacer de ese despacho un lugar cálido donde diera gusto trabajar. También quería agradecer a toda la gente que me ayudó en algún momento con el trabajo de esta tesis, a Kike, Cristina Alcalá, Vicky, Patri, Dolo, Becky, Yoli, Chele, los Rubenes (Milla y Torices), Mariajo, José Margalet, Luis Giménez, Ozeluí y muchos otros que seguro que se me olvidan, pido perdón por ello. A Luisiño, por su optimismo y simpatía, y por ser un gran amigo y compañero. También porque sin él los eventos lúdico deportivos de este departamento serían inexistentes. Me gustaría también agradecerles a todos mis otros compañeros biodispersos el que me hayan ayudado cada vez que los he necesitado, y por todos los buenos momentos que hemos vivido juntos. A Rocío, María y Mónica, que junto con Andrea (Javi, Samu y Rubén Torices eran, supuestamente, la parte sensata) han sido el terror de vigilantes de metro y porteros de discoteca, me lo he pasado genial con todos vosotros cada vez que nos hemos juntado y espero que nos sigamos juntando muchas veces más…sea en el país que sea. También a Isa, Ana Millanes, Cris Fernández, Raúl, Javi, Sonja, Luis Giménez y Julián porque, sin duda, habéis ayudado a pasar estos años en la distancia de una forma mucho más agradable. No quiero olvidar a los nuevos, Peska, Carlos, Gema, Sonia (la otra) y los demás, me voy bien tranquilo sabiendo que las nuevas generaciones seguirán formando un departamento cojonudo donde trabajar y que pasarán muchos años antes de que haya un cochinillo aburrido en Navidad, espero eso sí, que mejoréis el nivel futbolístico actual.
Resulta que a las pocas horas de llegar a Móstoles me vi metido en un coche con un tipo asturiano con barba y pelo largo que me llevaba a ver un piso en la c/ Camino de Humanes, 12. Allí esperaba una andaluza, fumando como un carretero, y con un tembleque extraño en la pierna. Resulta que Rubén y Mariajo eran esa gente, y que fueron mi familia durante más de 2 años. No puedo dejar de agradeceros que hicierais de esa casa un hogar en el que poder
desahogarme y estar completamente a gusto, vuestro continuo apoyo y el que hayáis sido mis “hermanos mayores”, lo bien que lo hemos pasado y todo lo que he aprendido y disfrutado con vosotros. Me alegro mucho de poder teneros como amigos. A la familia tengo que sumar a Lucia y Horta, ha sido un gustazo conoceros y he disfrutado de cada momento que hemos pasado juntos.
A toda la gente que ha colaborado en algún capítulo de esta tesis, a Lucia por ayudarme con toda la parte de dendro y carbohidratos, y por enseñarme lo poco que se, sin tu ayuda el capítulo 2 no habría sido posible. A Chemi Olano, que con sus ideas y participación hizo que éste capítulo fuera mucho mejor. David Eldridge (alias Mr. Fantastic), the aussie guy with italian accent, thanks for all your help and your extraordinary sense of humour; and especially for completing the aussie gradient!!!. It has been a pleasure to meet and work with you. Matt Bowker, thanks for a lot of things, it has been wonderful everytime I worked with you and also the time we spent outside the job. Thanks also for an excellent feedback in our scientific discussions, for your patience and for introducing me in the causal correlation world. I´m very grateful because it was you who showed me that stop and think is the first thing you should do to start doing good science. To the aussie team, Nick Reid and Matt Tighe, for hosting me in Armidale and helping me with all the logistics during my stay. I especially thank Nick Schultz for helping me during all the fieldwork in Australia. A Rubén, porque sin él el capítulo 5 no existiría, por ser tan rápido y eficiente currando y porque ha sido un gustazo descubrir que, además de un buen amigo, eres muy buen científico. A Estrella, por iniciarme con el mundillo R y por ayudarme a buscar parcelas en Alicante, y a Bea Amat por echarme un cable con los árboles de regresión.
A mi gente de Alicante. Pero sobretodo al “Kanutet Vilero”, sin Jorge, Curro, Juande, Joanmi (gràcies per lo de la portada, rei), Raúl y Juanito mi vida en general, y los cuatro años de la tesis en particular, no serían lo mismo (no sé si mejor o peor, pero desde luego, mucho más aburrida). Sólo decir que tengo mucha suerte de teneros como amigos. Muchas gracias por estar siempre ahí, por perdonarme mis repetidas ausencias, y por estar siempre dispuestos a pasar conmigo el poco tiempo libre que he podido sacar, por las risas que nos hemos echado, y por ayudarme en todo cuanto os he pedido. Lo de ayudarme a plantar 2300 árboles el plena navidad no se me olvidará nunca…aunque con todo el alcohol que me habéis hecho filtrar, cabrones, ni siquiera puedo entender cómo es que aún recuerdo mi propio nombre! Tampoco me quiero olvidar de los alicantinos expatriados, Jorgito, JM (ex expatriados), el Cuñao,
Kiket, Vicen, Carla, Paula y Aitana, gracias por hacer que me sintiera en Madrid como en casa, o mejor dicho, que me sintiera acompañado fuera de ella.
Sin mi madre nada de esto (ni muchísimas otras cosas) nunca hubiera sido posible, tinc que agraírte moltes coses, pero sobretot que sempre hages estat ahí, que sigues una lluitadora i tot un exemple a seguir, i que ho hages donat tot per uns fills que no et mereixen, gràcies mare PER TOT. También me gustaría agradecerle al resto de mi familia, A Benilde, Juan Antonio, Jorge y Katia, porque sin su apoyo uno muchas veces no podría seguir adelante. Y como no, a mi recua de mascotas, las que siguen y las que se fueron, a Stick, Peluso, Lluna, Mac, y a mis últimos “compañeros de despacho”, a Acho y Legaña. Por estar siempre dispuestos a hacerme compañía y darme cariño sin pedir nada a cambio, por lo que me habéis hecho reír y disfrutar, y por enseñarme cosas tan útiles como que, si te echas al suelo en verano, se está más fresquito que en el sofá. No sabéis leer (creo), pero valéis un imperio.
Y uno siempre se deja lo mejor para el final. A Soraya, por ser mi continuo apoyo y por estar siempre junto a mí. Por soportar 3 años y medio de distancia y por acompañarme al final del mundo cuando te lo pedí (11 vuelos en 13 días, y eso que te da miedo volar!). Por dejarte robar horas por ese infame ordenador, unas horas que me gustaría, y debería, haber pasado contigo, y nunca reprochármelo (yo sí que lo hago, créeme). Por ayudarme en todo , siempre. Porque sin tí nada tiene mucho sentido y contigo y tu eterna sonrisa los problemas parecen unos puntitos lejanos en el horizonte. Y porque no recuerdo haber vivido mejores momentos en mi vida que los que paso junto a ti, es imposible pensar que haya alguien mejor con quien uno podría estar.
Seguro que me he dejado a mucha gente, y espero que sepan perdonarme…
A TODOS, GRACIAS POR TODO
ÍNDICE
Resumen Antecedentes 3 Objetivos 26 Metodología general y área de estudio 29 Estructura general de la tesis 35
Capítulo 1 Predicted climate change effects in rainfall regime modulate the outcome of grass shrub interactions in two semiarid communities. 39
Capítulo 2 Spatio temporal heterogeneity in abiotic factors modulate multiple ontogenetic shifts between competition and facilitation. 65
Capítulo 3 Temporal dynamics of herbivory and water availability interactively modulate the outcome of a grass shrub interaction in a semiarid ecosystem . 89
Capítulo 4 On the relative importance of climate and biotic non trophic interactions as drivers of local plant species richness 111
Capítulo 5 On the relative importance of environmental conditions, biotic interactions and evolutionary relationships as drivers of the structure of semiarid communities. 153
Discusión y conclusiones general es 185
Bibliografía y afiliación de los coautores 218
RESUMEN
RESUMEN
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ANTECEDENTES
Las llamadas “tierras secas” (drylands) engloban todos aquellos ecosistemas de ambientes desde hiperáridos a secos subhúmedas; representando en total un 41% de la superficie emergida del planeta (Millenium Ecosystem Assessment [en adelante MEA] 2005, Reynolds et al. 2007a,b; Fig. A1). Las tierras secas se caracterizan generalmente por tener precipitaciones escasas y variables, temperaturas aéreas extremas y una evapotranspiración potencial elevada (Noy Meir et al. 1973, Whitford 2002, Reynolds et al. 2007b). Estas características ambientales hacen que estos sistemas tengan una baja productividad, que es altamente variable dependiendo de las condiciones de cada año y de una alta heterogeneidad espacial en la disponibilidad de nutrientes y la productividad vegetal (Whitford 2002). Pese a ello, las tierras secas representan una parte importante de la biodiversidad global (Convención para la Lucha contra la Desertificación 2005; en adelante CLD), y son el hogar y la fuente de sustento del 38% de la población mundial (Reynolds et al. 2007a,b). Los impactos antropogénicos (i.e. cambios en el uso del suelo, sobre explotación de recursos, aumento de las infraestructuras) y el aumento de la aridez provocado por el cambio climático son algunas de las causas más importantes de la degradación de las tierras secas, comúnmente llamada desertificación (MEA 2005, Reynolds et al. 2005, 2007b). Un aumento del nivel de degradación implica una pérdida del funcionamiento y de los servicios ecosistémicos, afectando directamente al bienestar de una parte importante de la población humana (MEA 2005, Reynolds et al. 2007a). Una vez que una zona ha sido degradada, revertir estos cambios es difícil, ya que se requieren profundas transformaciones socio económicas que afecten al desarrollo y manejo de estas áreas, inversiones sustanciales de recursos externos, y un profundo conocimiento de los factores que condujeron a la merma de la productividad y de funcionamiento ecosistémico (MEA 2005, Reynolds et al. 2007a,b). Un alto porcentaje de las tierras secas, hasta el 70% según la CLD, están amenazadas de degradación, mientras que un 10 20% de ellas ya están degradadas en mayor o menor grado (MEA 2005). Más de las dos terceras partes del territorio español pertenecen a lo que se define como tierras secas, y hasta el 36% de su territorio está amenazado por la desertificación, concentrándose la mayoría de este área en la mitad sur Peninsular (Ministerio de Medio Ambiente, Rural y Marino; Fig A1). Aunque no es la única condición, un mejor conocimiento sobre cómo funcionan los ecosistemas en las tierras secas, sobre los factores que afectan a su
3 RESUMEN biodiversidad, y sobre cómo están respondiendo estos ecosistemas al cambio climático o a incrementos en las perturbaciones que les afectan, y que están asociados con motores de cambio global (i.e. herbivoría, incendios), nos permitirá desarrollar herramientas para prevenir y combatir la desertificación (MEA 2005, Reynolds et al. 2005, 2007a). Los ecosistemas naturales presentan un cierto nivel de resiliencia, de forma que pueden resistir cierto nivel de perturbación o incremento de estrés sin verse severamente afectados, y pudiendo recuperarse bajo condiciones ambientales promedio (Noy Meir 1975, Westoby et al. 1989, Briske et al. 2003); el problema es que, una vez alcanzados los umbrales de resistencia de estos ecosistemas, éstos pueden sufrir cambios repentinos a estados severamente degradados, desde donde el retorno puede ser imposible pese a que las condiciones ambientales que provocaron el tránsito del umbral se modifiquen (Briske et al. 2003, Cortina et al. 2005, Kefi et al. 2007, Scheffer et al. 2009). Por tanto, es fundamental establecer cuales son los diferentes umbrales (i.e. niveles de perturbación, aridez) que hacen colapsar los mecanismos de resiliencia de estos ecosistemas a estados más degradados; como por ejemplo cambios en la disponibilidad de hábitats (Bascompte y Rodríguez 2001), el colapso de la expansión de nicho promovida por las plantas nodriza (Michalet et al. 2006), o cambios en el patrón espacial y tamaño de los parches de vegetación que afecten a la captura y redistribución de los recursos (Schlesinger et al. 1990, Tongway y Hindley 1995, Kefi et al. 2007). Esta tesis doctoral se centra en los sistemas semiáridos, y por tanto, es sobre ellos en concreto sobre los que hablaremos a partir de ahora.
LA DINÁMICA Y EL FUNCIONAMIENTO DE LOS SISTEMAS SEMIÁRIDOS
La principal característica de los ambientes áridos y semiáridos es que llueve poco (índices de aridez [precipitación anual/evapotranspiración potencial] de entre 0,5 0,05), que esta lluvia es generalmente impredecible, y que normalmente se produce en pulsos más o menos extensos seguidos de temporadas secas prolongadas (Noy Meir 1973, Whitford 2002). Por consiguiente, el reclutamiento de nuevas plántulas sólo se produce durante pulsos de elevada disponibilidad de agua, que son poco frecuentes e irregulares a lo largo del tiempo; estos pulsos suelen corresponder con años particularmente benignos desde el punto de vista climático (p. ej. Eldridge et al. 1991, Escudero et al. 1999, Kitzberger et al. 2000, Whitford 2002, Holmgren et al. 2006). Aunque los pulsos de agua más abundantes y continuos existen, son los pulsos de agua cortos y de escasa intensidad (<5mm) los que predominan (Whitford 2002, Huxman et al. 2004). La diferente frecuencia entre los distintos tipos de pulsos, y cómo
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los distintos componentes del ecosistema (i.e. microorganismos del suelo, costra biológica y distintos tipos funcionales de plantas) aprovechan estos pulsos de agua, son la razón de que los ecosistemas áridos y semiáridos sustenten niveles de diversidad relativamente altos pese a su escasa productividad (Sala y Lauenroth 1982, Fowler 1986, Ogle y Reynolds 2004, Schwinning et al. 2004).
Figura A1 Distribución global de las tierras secas (arriba; Fuente: MEA 2005), y áreas amenazadas de desertificación en España (de verde a amarillo representa de menor a mayor grado de amenaza, imagen de abajo. Fuente: Ministerio de Medio Ambiente, Rural y Marino: http://www.mma.es/portal/secciones/biodiversidad/desertificacion/desertificacion_espni a/index.htm ).
La cobertura vegetal discontinua, organizada en manchas discretas de vegetación embebidas en una matriz de suelo desnudo, con escasa cobertura vegetal (Fig. A2),
5 RESUMEN característica de muchos ambientes áridos y semiáridos es el origen de la dinámica fuente sumidero que define el funcionamiento de estos ecosistemas (Ludwig y Tongway 1995, Aguiar y Sala 1999, Puigdefábregas et al. 1999). La dinámica fuente sumidero consiste en el arrastre de agua, nutrientes y semillas durante los eventos lluviosos de cierta magnitud desde la matriz de suelo desnudo o de muy escasa cobertura (fuente) hasta las manchas de vegetación existente (sumideros). Aunque la costra biológica del suelo y los microorganismos presentes en la matriz de suelo desnudo tienen un papel importante en la captura de carbono y el reciclado de nutrientes de estos ecosistemas (Belnap y Lange 2003, Huxman et al. 2004, Castillo Monroy et al. 2010); la mayor parte de la productividad, reciclado de nutrientes y captura de carbono ocurre en las manchas de vegetación, dominadas en su mayoría por arbustos y herbáceas graminoides perennes, que actúan como islas de recursos en un ambiente mucho más pobre (Franco y Nobel 1987, Schlesinger y Pilmanis 1998, Aguiar y Sala 1999). La concentración de los recursos en dichas manchas conlleva generalmente un aumento de la productividad, heterogeneidad ambiental y diversidad a nivel local (Noy Meir 1973, Huxman et al. 2004, Schwinning et al. 2004), algo que sería más difícil de alcanzar si los recursos se repartieran de forma homogénea en el ecosistema (Noy Meir 1973, Aguiar y Sala 1999). A su vez, es precisamente esta concentración de los recursos la que mantiene la estructura discontinua, con la presencia de manchas discretas de vegetación, a largo plazo, ya sea en áreas donde esta estructura existía de por sí (Ludwig y Tongway 1995, Puigdefábregas et al. 1999, Rietkerk y Van der Koppel 2008), o bien en lugares donde cambios en la composición vegetal han generado una distribución heterogénea de los recursos (Schlesinger et al 1990, Archer 1994). La dinámica fuente sumidero mantiene esta estructura heterogénea mediante procesos de retro alimentación positivos a escala de mancha (más recursos, más productividad en las manchas de vegetación, más captura de recursos), y negativos a mayores escalas (concentración de recursos y semillas en las manchas de vegetación dificulta el reclutamiento en sitios libres de vegetación, y por tanto, el desarrollo de patrones espaciales uniformes a nivel del ecosistema; Schlesinger et al. 1990, Archer 1994, Rietkerk y Van de Koppel 2008). Las diferencias en las condiciones ambientales (sombra, fertilidad del suelo, infiltración), junto con una mayor cantidad de semillas concentradas al quedar atrapadas en las manchas de vegetación por el efecto de la escorrentía o por la deposición de aves y mamíferos, hace que sea en estos lugares donde se concentra una gran parte del reclutamiento de nuevas plántulas (Aguiar y Sala 1999), aunque esto dependerá de los requerimientos ecológicos de cada especie (p. ej. Miriti et al. 1998, 2007, Caballero et al. 2008). El efecto
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positivo que tienen unas plantas sobre otras mediante la mejora de las condiciones ambientales (p. ej. reducción de temperatura y viento, mejora de las condiciones hídricas mediante sombreo, mayor fertilidad del suelo) y/o la defensa frente a la herbivoría recibe el nombre de “facilitación” (Callaway 1995; Figura A2), siendo uno de los factores fundamentales que interviene en el reclutamiento de nuevas plántulas en estas manchas de vegetación (Niering et al. 1963, McAuliffe 1988, Eccles et al. 1999). Sin embargo, la intercepción del agua de lluvia por los doseles de las plantas adultas y la mayor competencia por agua, luz y nutrientes debajo de estos manchas de vegetación, junto con los efectos negativos de la caída hojarasca, tanto físicos como químicos, relacionados con la liberación de compuestos alelopáticos, producen efectos negativos que pueden llegar a superar a los efectos beneficiosos según las especies implicadas y las condiciones ambientales reinantes (revisado en Fowler 1986, Callaway 2007). Además de esto, las mismas condiciones ambientales que son beneficiosas para las plántulas (i.e. poca radiación incidente) pueden resultar negativas para plantas más adultas (Schupp 1995), lo que hace que las interacciones positivas o facilitativas puedan volverse competitivas a medida que las plantas facilitadas avanzan en su desarrollo (Fowler 1986, Callaway y Walker 1007, Miriti 2006). Además, lo que puede ser beneficioso para una plántula en un determinado momento y condiciones puede ser pernicioso en otros, sin necesidad de cambios ontogenéticos (De la Cruz et al. 2008). El equilibrio entre facilitación/neutralidad/competencia es un determinante fundamental de la dinámica de las comunidades vegetales en los ecosistemas semiáridos (Fowler 1986, Aguiar y Sala 1999). Por tanto, un mayor conocimiento sobre la importancia relativa de las interacciones positivas frente a las negativas en distintos procesos y atributos ecosistémicos (i.e. composición, estructura), así como un entendimiento de los condicionantes para que se de uno u otro signo en la interacción, son fundamentales para poder entender el ensamblaje de las especies, la dinámica y funcionamiento de estos ecosistemas y mejorar su restauración (Fowler 1986, Cortina et al. 2005, Callaway 2007, Brooker et al. 2008, Gómez Aparicio 2009).
7 RESUMEN
Figura A2 Estructura espacial heterogénea con parches de vegetación herbácea y arbustiva en un espartal de Stipa tenacissima en Zorita, España (arriba). Individuos de Austrostipa scabra reclutando bajo un arbusto adulto en un bosque abierto de Eucalyptus populnea en Nyngan, Australia (abajo).
8
LA HIPÓTESIS DEL GRADIENTE DE ESTRÉS Y LA INTRODUCCIÓN DE LA FACILITACIÓN EN LA TEORÍA
ECOLÓGICA
Aunque las interacciones positivas entre plantas son conocidas desde hace tiempo (Clements 1916, Shreve 1931, Niering et al. 1963), han sido ampliamente ignoradas en ecología hasta hace 25 años (Callaway 1995). Durante los años previos enfatizó el papel de procesos como la competencia entre plantas, el efecto de las perturbaciones o el estrés abiótico en el ensamblaje de comunidades (p. ej. Grime 1973, Huston 1979, 1999, Tilman 1988), ignorando la importancia de la facilitación en este proceso (ver revisión en Callaway 2007). Prueba de ello es que sólo 27 artículos científicos versaron sobre facilitación en el período 1900 1989, mientras que el número de artículos sobre este tema en los últimos 20 años asciende hasta 1252 (Pakeman et al. 2009). Además, la facilitación ha sido introducida como un proceso importante en el ensamblaje de especies en comunidades, especialmente en medios “estresantes” (i.e. medios áridos y semiáridos, alta montaña, ecosistemas salobres, comunidades intermareales), ganándose un sitio en el marco de la teoría general ecológica (Callaway 1997, Hacker y Gaines 1997, Stachowicz 2001, Bruno et al 2003, Lortie et al. 2004, Michalet et al. 2006, Callaway 2007). Gran parte de este “viraje” en la atención prestada a la facilitación en ecología se la debemos a Mark Bertness y Ragan Callaway, que en 1994 publicaron su Hipótesis del Gradiente de Estrés (en adelante SGH, del inglés “Stress Gradient hipótesis”). Estos autores propusieron un modelo teórico sencillo y biológicamente muy plausible, en el cual predecían un aumento de la importancia y la frecuencia de las interacciones facilitativas frente a las competitivas a medida que el estrés abiótico o las perturbaciones aumentan. A partir de ese momento, las interacciones positivas pasaron a ser un mecanismo a tener en cuenta a la hora de estudiar la dinámica de las poblaciones, y luego las comunidades vegetales en todo el mundo (Callaway 2007). Bajo el paraguas de la SGH, numerosos ecólogos han fijado su atención en estas interacciones positivas y su efecto en la dinámica de ciertos pares de especies en particular (p. ej. Valiente Banuet et al. 1991, Maestre et al. 2001, Gómez Aparicio et al. 2004, Sthultz et al. 2007), en el efecto de ciertas especies clave sobre las demás especies (p. ej. Holzapfel y Mahall 1999, Pugnaire y Luque 2001, Maestre y Cortina 2005, Badano y Cavieres 2006), o, más raramente, en la importancia de la facilitación a nivel de comunidades enteras (p. ej. Hacker y Bertness 1999, Kikvidze et al. 2005, Maestre et al. 2010). Además, esta hipótesis no solo ha sido evaluada en plantas, sino que existen estudios sobre su aplicabilidad a comunidades intermareales (p. ej. Stachowicz 2001, Kawai y Tokeshi 2007,
9 RESUMEN
Daleo y Iribarne 2009), costra biológica del suelo (Mulder et al. 2001, Maestre et al. 2008, Bowker et al. 2010) e incluso entre herbívoros de diferente tamaño ( Arsenault y Owen Smith 2002 ). Prueba de su importancia son las más de 830 citas que ha recibido el artículo de Bertness y Callaway (1994) hasta la fecha. A pesar de constituir un punto de partida inmejorable para las investigaciones sobre facilitación, la SGH ha encontrado numerosas excepciones que hacen poner en duda la generalidad de sus predicciones. Así, resultados obtenidos cuando se evalúa la actividad vegetal con diferentes parámetros (Goldberg y Novoplansky 1997, Maestre et al. 2005, Gómez Aparicio 2009), se estudian niveles extremadamente altos de estrés (Kitzberger et al. 2000, Tielbörger y Kadmon 2000a, Maestre y Cortina 2004), o se consideran de forma simultánea distintos factores de estrés (Ibañez y Schupp 2001, Kaway y Tokeshi 2007, LeRoux and McGeoch 2010) contradicen las predicciones de la SGH. Además, las interacciones planta planta son altamente específicas, independientemente del nivel de estrés en el que ocurran (Callaway 2007). Esto hace pensar que los diferentes rasgos ecológicos de las especies que interactúan (Choler et al. 2001, Liancourt et al. 2005, Gross et al. 2009, Maestre et al. 2009a, Gómez Aparicio 2009) o sus relaciones evolutivas (Valiente Banuet et al. 2006, Valiente Banuet y Verdú 2007, Castillo et al. 2010) son factores fundamentales que afectan al resultado de estas interacciones. Estos resultados contradictorios han sido el punto de partida de numerosos debates y redefiniciones de la SGH, que han tratado de incorporar el efecto de la identidad y características ecológicas de las especies implicadas, los distintos niveles y tipos de estrés o las distintas medidas de rendimiento vegetal utilizadas (Holmgren et al 1997, Maestre et al. 2005, 2006, 2009a, Lortie y Callaway 2006, Callaway 2007, Malkinson y Tielbörger 2010, Holmgren y Scheffer 2010). De todas estas aportaciones se puede concluir que: a) la facilitación será especialmente intensa y frecuente a niveles intermedios de estrés; esto puede deberse a que, bajo niveles elevados de estrés, el efecto negativo de la competencia supera al efecto positivo; o bien a que las plantas nodriza no son capaces de mejorar suficientemente las condiciones ambientales bajo condiciones tan extremas (Maestre y Cortina 2004, Michalet et al. 2006, Holmgren y Scheffer 2010), b) el resultado de las interacciones dependerá de las características ecológicas de las especies implicadas (competidoras o tolerantes al estrés, sensu Grime 2001) y de si el tipo de estrés está directamente relacionado con un recurso (p. ej. agua o luz), o no (p. ej. temperatura o salinidad; Maestre et al. 2009a), c) el resultado de las interacciones dependerá del efecto de la nodriza sobre la disponibilidad de recursos (p. ej. luz, agua o temperatura), y las tolerancias relativas de las especies facilitadas (p. ej. tolerancia a la sombra, a la sequía o al frío;
10
Holmgren et al. 1997, Choler et al. 2001, Liancourt et al. 2005, Malkinson y Tielbörger 2010, Holmgren y Scheffer 2010), d) el resultado de las interacciones bajo distintos tipos de estrés puede ser de muy diferente naturaleza, pudiendo darse jerarquías entre los distintos tipos de estrés presentes (Baumeister y Callaway 2006), sinergias o anulaciones de sus efectos (Kawai y Tokeshi 2007) o bien, simplemente que éstos sean aditivos (Riginos et al. 2005), y e) las interacciones entre plantas tenderán a ser más positivas cuanto menos relacionadas (i.e. más distantes en la evolución) estén las especies que interactúan (Valiente Banuet et al. 2006, Valiente Banuet y Verdú 2007, Castillo et al. 2010). Además de estas complicaciones añadidas a la simplicidad excesiva de la SGH, hemos de tener en cuenta que, en medios áridos y semiáridos la disponibilidad hídrica y de nutrientes se produce en pulsos, seguidos de largos períodos de tiempo con una disponibilidad de agua o nutrientes muy limitada (inter pulsos; Goldberg y Novoplansky 1997, Whitford 2002), lo que complica aún más la predicción sobre el resultado de las interacciones planta planta. Por ejemplo, Goldberg y Novoplansky (1997) desarrollaron un modelo en el que predecían un efecto negativo de las nodrizas sobre el crecimiento durante los pulsos o épocas benignas, mientras que este efecto cambiaría a positivo, aumentando la supervivencia, durante los inter pulsos o épocas más secas. El resultado final de la interacción dependería de: 1) el efecto relativo de la competencia con la nodriza frente a los factores abióticos en el agotamiento de los nutrientes durante los inter pulsos, y 2) del efecto de la reducción en el crecimiento durante los pulsos sobre la supervivencia posterior en los inter pulsos (Goldberg y Novoplansky 1997). A pesar de su importancia, esta variabilidad intra anual en los recursos y su importancia relativa sobre el resultado final de las interacciones planta planta ha sido poco estudiada (Barchuk et al. 2005, Kikvidze et al. 2006, Sthultz et al. 2007, de la Cruz et al. 2008). Los diversos modelos existentes sobre los efectos del cambio climático para la región Mediterránea semiárida predicen, además de una reducción de la cantidad anual en las precipitaciones, un cambio sustancial en su patrón temporal (IPCC 2007). En el futuro es esperable que las épocas secas o inter pulsos sean más largos, las lluvias durante los pulsos menos abundantes, y los eventos de lluvias torrenciales más frecuentes (IPCC 2007, Knapp et al. 2008, Miranda et al. 2009). Es muy probable que estos cambios tengan efectos profundos sobre la vegetación de los ecosistemas semiáridos (Ogle y Reynolds 2004, Holmgren et al. 2006, López et al. 2008, Heisler White et al. 2009, Miranda et al. 2009, Pías et al. 2010). Por consiguiente, es fundamental estudiar cómo las interacciones planta planta van a verse afectadas por estos cambios, o cómo pueden mitigar estos cambios aumentando la resiliencia
11 RESUMEN del ecosistema ante el incremento de aridez y el cambio en el patrón temporal de las precipitaciones (Brooker et al. 2008). Sin embargo, son muy pocos los estudios que han evaluado el efecto de estos cambios en la frecuencia y abundancia de los eventos de lluvia sobre las interacciones planta planta (Zavaleta 2006, Knapp et al. 2008, Matías 2010). Ya se ha comentado anteriormente que los cambios en los requerimientos ecológicos de las distintas especies durante la ontogenia pueden modificar los resultados de sus interacciones con otras plantas (Callaway y Walker 1997, Miriti 2006). Estos cambios han sido relacionados con la existencia de interacciones positivas durante la germinación y el desarrollo de plántula, debido a una mayor vulnerabilidad a la sequía o a la herbivoría (Schupp 1995, Cavender Bares y Bazzaz 2000, Ibañez y Schupp 2001) y con el incremento de la competencia por la luz y el agua a medida que las plántulas crecen y se convierten en individuos reproductivos (Miriti 2006, 2007, Schiffers y Tielbörger 2006, Armas y Pugnaire 2009). Sin embargo, esta relación no siempre es tan evidente, y parece depender del nivel de estrés ambiental reinante en cada estado ontogenético y del estado fisiológico (Ibañez y Schupp 2001, Sthultz et al. 2007, Butterfield et al. 2010), de las diferencias en la forma de crecimiento de las especies que interactúan (Gómez Aparicio 2009), o de las relaciones evolutivas que definen las diferencias entre los rasgos ecológicos entre estas especies (Valiente Banuet y Verdú 2008). La inmensa mayoría de los estudios que evalúan cambios ontogenéticos en las interacciones planta planta se centran en ventanas temporales concretas a lo largo del desarrollo de las especies facilitadas (Armas y Pugnaire 2005, 2009, Miriti 2006, 2007, Valiente Banuet y Verdú 2008). Sin embargo, estas aproximaciones no dan una visión global del tema, ya que no tienen en cuenta el efecto de arrastre que las condiciones ambientales de años anteriores pueden tener en el presente. El efecto de las condiciones del año anterior sobre el crecimiento presente es fundamental en medios semiáridos (Whitford 2002). Por consiguiente, el no tener en cuenta dicho efecto puede confundir la relación entre el resultado de una interacción planta planta dada y las condiciones ambientales reinantes en un año concreto. Estudios que sigan el desarrollo de estas interacciones durante el tiempo necesario para que estas especies de vida larga pasen de plántula a adulto son logísticamente prohibitivos, por lo que el uso de medidas indirectas (i.e. estudios dendrocronológicos) podrían ser una solución adecuada para evaluar la interacción clima ontogenia en estas especies (véase Armas y Pugnaire 2005, Sthultz et al. 2007, Aragón et al. 2008, Pías et al. 2010 para otras aproximaciones). Además, es fundamental que estos estudios a lo largo de distintos estados ontogenéticos se realicen con distintas combinaciones de formas de crecimiento que
12
interactúen entre ellas (Gómez Aparicio 2009). Aunque muchas plántulas tienen escasa tolerancia a la sequía y pueden estar menos estresadas bajo el dosel de una planta adulta (Schupp 1995 pero ver Caballero et al. 2008, Matías 2010), las diferencias en los requerimientos ecológicos de individuos adultos entre tipos funcionales o formas de crecimiento diferentes pueden ser muy importantes. Por ejemplo, distintas tolerancias a la sombra o la sequía (Holmgren et al. 1997, Hastwell y Facelli 2003) o diferentes profundidades de enraizamiento (Sala y Lauenroth 1982, Schwinning et al. 2001, Ogle y Reynolds 2004) pueden ser clave a la hora de definir el resultado de las interacciones entre adultos de distintas especies. Los estudios sobre cambios de facilitación a competencia a lo largo de la ontogenia se centran en interacciones arbusto arbusto, con ambas especies teniendo características morfológicas y funcionales parecidas, por lo que es esperable que compartan sus nichos ecológicos de explotación de agua, luz y nutrientes (p. ej. Miriti 2006, Armas y Pugnaire 2009). Sin embargo, estudios centrados en otro tipo de interacciones (i.e. herbácea arbusto o entre arbustos con estrategias y formas contrastadas), muy abundantes por otro lado en medios semiáridos (Aguiar y Sala 1999), pueden arrojar resultados muy diferentes. Ello es así debido a que ambas formas de crecimiento difieren en la toma de agua y nutrientes por sus distintas profundidades de enraizamiento (Sala y Lauenroth 1982, Fowler 1986) y a que tienen alturas contrastadas, lo que puede reducir la competencia entre ambos grupos por la luz. Por ejemplo, Armas y Pugnaire (2005) encontraron que los individuos juveniles de la gramínea perenne Stipa tenacissima tenían efectos neutros o negativos sobre el arbusto Cistus clusii , dependiendo del clima; pero que este efecto negativo se volvía neutro (o incluso positivo, en condiciones más secas) cuando individuos adultos de ambas especies interactuaban. En otro estudio, Gasque y García Fayos (2004) encontraron que tanto las plántulas como los adultos de Pinus halepensis se desarrollaban mejor cuando crecían cerca de una macolla de S. tenacissima , sin encontrar cambios en estas interacciones positivas en distintos momentos del desarrollo de P. halepensis, aunque los efectos positivos de S. tenacissima sobre las plántulas de P. halepensis desaparecieron durante la sequía estival, ya que ninguna plántula sobrevivió. Resultados que contrastan con una relación monotónica entre el paso de facilitación a competencia con la edad (p. ej. Miriti 2006, Valiente Banuet y Verdú 2008) no se han encontrado sólo en interacciones leñosa herbácea, si no que también son comunes en otro tipo de interacciones. Tirado y Pugnaire (2003) encontraron efectos facilitativos, independientemente del momento ontogenético, al estudiar la interacción entre dos arbustos ( Asparagus albus y Ziziphus lotus ). Sthultz et al. (2007) también encontraron que el efecto del arbusto Fallugia paradoxa sobre el árbol Pinus edulis era positivo en sitios
13 RESUMEN de elevado estrés, independientemente de la edad de P. edulis , aunque el efecto positivo de F. paradoxa se tornaba negativo a medida que P. edulis crecía en sitios menos estresantes. Las interacciones entre especies herbáceas parecen estar normalmente dominadas por la competencia (Gómez Aparicio 2009), aunque esto depende en un grado importante de las condiciones ambientales reinantes (Graff et al. 2007, Veblen 2008), y con toda probabilidad de los rasgos funcionales de las herbáceas que interactúen (Cahill et al. 2008, Gómez Aparicio 2009). En consecuencia, la relación entre el signo de las interacciones planta planta, la ontogenia y las condiciones climáticas parece ser altamente específica de cada especie, o por lo menos para cada forma de crecimiento (Gómez Aparicio 2009), por lo que no sirve un modelo simple para predecir la evolución de las interacciones. Sin duda, estudios destinados a entender mejor estas relaciones son fundamentales para entender la dinámica de las comunidades vegetales en los escenarios climáticos presentes y futuros (Fowler 1986, Butterfield 2009).
EL PAPEL DE LA HERBIVORÍA Y SU INTERACCIÓN CON EL CLIMA EN LAS INTERACCIONES PLANTA -
PLANTA
La herbivoría es un factor fundamental que afecta al desarrollo de las plantas en condiciones semiáridas (McNaughton 1978, Milchunas et al. 1989, Fowler 2002, Kefi et al. 2007). Sabemos que la presencia de herbívoros y su preferencia por ciertas especies pueden influir en la dinámica competitiva entre las plantas (Gurevitch et al. 2000, Fowler 2002), con profundos efectos en la diversidad y abundancia relativa de las especies vegetales (Westoby et al. 1989, Fuhlendorf et al. 2001, Briske et al. 2003). También se conoce el efecto que algunas especies no palatables pueden ejercer en el mantenimiento de la diversidad en las comunidades vegetales mediante su papel protector/facilitador sobre otras (Hay et al. 1986, Callaway et al. 2000, Rebollo et al. 2002, Baraza et al. 2006, Veblen 2008). De hecho, este efecto protector puede compensar el efecto negativo derivado de la competencia por agua o nutrientes, dando como resultado neto una asociación positiva entre pares de especies (Graff et al. 2007). La herbivoría es, por tanto, un factor determinante de las interacciones planta planta en ambientes semiáridos (Rebollo et al. 2002, Baraza et al. 2006, Graff et al. 2007, Veblen 2008). Sin embargo, al igual que pasa con la mejora microclimática, el efecto protector de estas plantas nodriza tiene límites, y bajo niveles extremadamente altos de herbivoría u otras perturbaciones, este efecto positivo puede llegar a desaparecer (Brooker et al. 2006, Smit et
14
al. 2007, 2009, Graff et al. 2007, Forey et al. 2009). En medios semiáridos, la presión de los herbívoros puede aumentar a medida que la disponibilidad de forraje se reduce con menores disponibilidades hídricas (Illius y O´Connor 1999, Chase et al. 2000) o por aumento de cargas de estos herbívoros por dinámicas endógenas; a su vez, las condiciones abióticas pueden acelerar o retrasar la recuperación de las comunidades vegetales después de la perturbación (Fuhlendorf et al. 2001). Es lógico pensar que ambos factores, herbivoría y aridez, interactúan a la hora de definir el resultado de las interacciones planta planta y la dinámica de las comunidades vegetales (Van Auken 2000, Roques et al. 2001, Smit et al. 2009). Sin embargo, a pesar de los numerosos estudios realizados para evaluar las interacciones planta planta bajo niveles diferentes de estrés abiótico o herbivoría de forma separada (revisados en Callaway 2007), muy pocos trabajos han evaluado el efecto conjunto que la interacción entre ambos tipos de estrés produce sobre estas interacciones (Ibañez y Schupp 2001, Veblen 2008, Anthelme et al. 2009). La co ocurrencia de ambos tipos de estrés puede afectar de forma importante a las interacciones planta planta, provocando profundos efectos en la dinámica de las comunidades, que son difíciles de predecir si sólo consideramos ambos factores de estrés por separado (Smit et al. 2009). Además del efecto protector descrito anteriormente, las plantas nodriza pueden incrementar la tolerancia de las plantas facilitadas a la herbivoría (Rand 2004, Acuña Rodríguez et al. 2006). Las mejores condiciones hídricas y la mayor concentración de nutrientes presentes frecuentemente bajo el dosel de las plantas nodriza pueden ayudar a la recuperación de ciertas especies después de la pérdida de biomasa producida por la herbivoría (Crawley et al. 1998). Sin embargo esto no es tan sencillo, ya que el efecto que unas mejores condiciones hídricas o nutricionales, pero una menor radiación solar, tengan sobre la tolerancia a la herbivoría dependerá de cual es el recurso limitante en cada caso, y de cómo la pérdida de biomasa producida por la herbivoría afecte a la toma de este recurso. Wise y Abrahamson (2005, 2007) propusieron el Modelo de Recursos Limitados (“Limited Resource Model”), que predice correctamente la inmensa mayoría de relaciones entre tolerancia a la herbivoría y disponibilidad de recursos. Este modelo sugiere que la tolerancia a la herbivoría será mayor en condiciones más húmedas cuando el agua es el factor más limitante (algo común en sistemas semiáridos), ya que estas condiciones más húmedas favorecen mayores tasas de fotosíntesis, permitiendo compensar las pérdidas de biomasa ocasionadas por los herbívoros (Crawley et al. 1998). Sin embargo, en los casos en los que la luz es también un factor limitante (p. ej. Marañón y Bartolomé 1993, Seifan et al. 2010a), la tolerancia a la herbivoría será más baja conforme aumente la humedad (Baraza et al. 2004, Wise y
15 RESUMEN
Abrahamson 2005, 2007; Fig. A3). Esto se debe a que la fotosíntesis de estas plantas es potencialmente más alta bajo condiciones más húmedas, lo que hace que la pérdida relativa de rendimiento sea mayor cuando la fotosíntesis se ve limitada por la baja disponibilidad de luz producida por la pérdida de biomasa causada por la herbivoría. En cambio, en condiciones más secas, el crecimiento vegetal ya está limitado por la baja disponibilidad hídrica, por lo que el efecto relativo que tiene una menor disponibilidad lumínica en la fotosíntesis es mucho menor y la tolerancia es más alta (Fig. A3). Por consiguiente, tanto el efecto que las plantas nodriza tendrán sobre la tolerancia de las plantas facilitadas a la herbivoría, como las variaciones de este efecto bajo distintos niveles de disponibilidad hídrica son difíciles de predecir.
Figura A3 Predicciones del Modelo de Recursos Limitados en el caso de que la herbivoría afecte a la toma del recurso principal (Hrp; en nuestro caso el recurso principal sería agua) o a la toma de un recurso alternativo (Hra; en nuestro caso luz). Estas predicciones varían si el nivel inicial del recurso principal es bajo (panel de la izquierda) o alto (panel de la derecha). Modificado de Wise y Abrahamson 2007.
Debido a la gran importancia de ambos factores (herbivoría y agua) en ambientes semiáridos, parece prioritario llevar a cabo estudios destinados a resolver como las interacciones planta planta afectan a la incidencia de los herbívoros sobre las plantas facilitadas, y a la tolerancia a la herbivoría de estas plantas bajo distintas disponibilidades hídricas. Esto trabajos son fundamentales para entender la dinámica de las comunidades vegetales semiáridas (Smit et al. 2009). Este conocimiento puede ayudar a desarrollar estrategias de manejo adecuadas, que mantengan unos niveles razonables de pastoreo dependiendo de las condiciones de cada año, permitiendo un desarrollo sostenible en ambientes semiáridos (el 55% del área ocupada por estos ambientes se destina a la ganadería;
16
MEA 2005). Particularmente, aquellos estudios enfocados en las interacciones leñosa herbácea pueden ayudar a predecir el efecto de la herbivoría y el incremento de la aridez en ecosistemas afectados por procesos de matorralización.
EL PAPEL DE LA FACILITACIÓN EN EL ENSAMBLAJE DE COMUNIDADES
Uno de los debates que más ha fascinado a los ecólogos a lo largo de su historia (ver Gotelli y Graves 1996, Callaway 1997, 2007, Hubbell 2001, Alonso et al. 2006 para revisiones sobre este debate) es el iniciado a partir de los trabajos de Clements (1916) y Gleason (1926), los cuales proponen modelos opuestos sobre la concepción de las comunidades vegetales: un superorganismo en el cual las interacciones bióticas juegan un papel fundamental (Clements 1916), o bien una coincidencia de especies que coexisten debido a sus adaptaciones independientes a las condiciones ambientales de cada lugar (Gleason 1926). Resolver este debate no sólo tiene un atractivo teórico, también tiene implicaciones fundamentales para la conservación de los ecosistemas naturales. Comprender la naturaleza de una comunidad y ver las distintas especies como entidades reemplazables y sustituibles, o como organismos con fuertes relaciones de interdependencia puede conllevar cambios drásticos en como entendemos y gestionamos la biodiversidad (discutido en Callaway 2007). Existen numerosos estudios que apoyan ambas teorías, siendo clave la escala temporal, y sobretodo espacial, a la que estos estudios se realizan (Hubbell 2001, Stokes y Archer 2010). Estudios conducidos en áreas extensas, a niveles biogeográficos o regionales, parecen indicar que las interacciones bióticas no son importantes, y que las comunidades por tanto, no son estables, sino que cambian con el tiempo debido a procesos estocásticos de especiación, dispersión y extinción (Hubbell 2001, pero ver Gotelli et al. 2010). Sin embargo, estudios a escalas locales advierten sobre la suma importancia que las interacciones bióticas tienen en el mantenimiento de estas especies en un lugar dado, así, procesos como la exclusión competitiva, la segregación de nicho o los mutualismos entre numerosos organismos (p. ej. insectos polinizadores y plantas) han sido demostrados como clave para mantener el conjunto concreto de especies que coexisten en una comunidad dada (Levin 1970, Diamond 1975, Huston 1979, 1999, Rezende et al. 2007), especialmente en aquellas más consolidadas o menos pioneras (Stokes y Archer 2010). Por otro lado, sabemos que las interacciones facilitativas son claves para mantener la diversidad en las comunidades naturales (Bruno et al. 2003, Callaway 2007). Así, muchas de las especies nodriza han sido catalogadas como ingenieros del ecosistema ( sensu Jones et al. 1996) en numerosos ecosistemas de todo el
17 RESUMEN mundo (Hacker y Bertness 1999, Stachowicz 2001, Maestre y Cortina 2005, Badano y Cavieres 2006). Como ya se ha comentado anteriormente, estas especies modifican las condiciones microambientales en sus cercanías, lo que permite la existencia de especies menos adaptadas a las condiciones ambientales particulares de ese sitio, ya que sin la presencia de estas especies nodriza no podrían sobrevivir (expansión de nicho; Bruno et al. 2003). Así pues, parece claro que ambas visiones de lo que es una comunidad son complementarias, y que la escala espacial que consideremos (no tanto la temporal, como se discutirá en la siguiente sección) es fundamental para entender la importancia de los procesos estocásticos frente a las interacciones bióticas para el ensamblaje de las comunidades. De hecho, Hubbell (2001) reconoce que “ aunque la asunción de neutralidad completa es, sin duda, falsa, pocos ecólogos negaran que las poblaciones y comunidades reales no están sujetas sólo a los factores físicos y las interacciones bióticas, sino también a la estocasticidad demográfica…Las comunidades ecológicas están indudablemente gobernadas por reglas de ensamblaje de nicho y dispersión, junto con la estocasticidad demográfica, pero la pregunta importante es: ¿Cuál es la importancia relativa y cuantitativa de estos procesos? ”. Bien, han pasado casi diez años desde que se hizo esta pregunta, y algo hemos aprendido en el camino. Tanto las aproximaciones teóricas como empíricas parecen apuntar al mismo sitio: mientras que son los procesos estocásticos a gran escala (especiación y dispersión) los que determinan que especies de plantas “aparecen” en una comunidad dada, son los factores físicos (también estocásticos en algún grado) y las interacciones bióticas los que determinan en mayor parte cuales de estas especies permanecen (Huston 1999, Lortie et al. 2004a, Rajaniemi et al. 2006, Rezende et al. 2007, pero ver Gotelli et al. 2010). Si bien se presupone que tanto los factores ambientales (i.e. clima, perturbaciones) como las interacciones bióticas condicionan el ensamblaje de comunidades a escalas locales, poco se sabe sobre la importancia relativa de ambos factores como determinantes de dicho ensamblaje (Butterfield et al. 2010). Callaway (2007) advierte sobre el efecto tampón que algunas plantas nodriza pueden tener sobre la variabilidad inter anual en las precipitaciones (que podemos considerar estocástica) de algunos desiertos y zonas semiáridas, promoviendo ambientes más estables en estos ecosistemas. Esta revisión sugiere, por tanto, que las posibles interacciones entre las condiciones abióticas y las interacciones planta planta son clave a la hora de definir la dinámica de las comunidades naturales, ya que pueden modificar los efectos de la estocasticidad climática en estas poblaciones.
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Algunos estudios evaluaron la hipótesis de que las interacciones bióticas (fundamentalmente la competencia) eran clave en los sistemas más productivos, mientras que las condiciones ambientales, y la falta de adaptaciones fisiológicas de la mayoría de especies a estas condiciones, determinaban la caída en la riqueza de especies observada en los ambientes menos productivos (Grime 1973, Huston 1979). De estos estudios se deriva una relación unimodal entre la riqueza y la productividad de las comunidades naturales, donde en ambos extremos se vería una caída de la diversidad de especies respecto a niveles intermedios de productividad, donde los niveles de diversidad serían máximos (Grime 1973). Tanto Hacker y Gaines (1997) como Michalet et al. (2006) discutieron el papel que podrían jugar las interacciones facilitativas en esta relación unimodal entre productividad y diversidad. Ambos trabajos afirman que las plantas nodriza, mediante modificación del microambiente bajo su dosel, pueden reducir el filtro abiótico que se da en las condiciones menos productivas, aumentando así la diversidad en niveles medios altos de “estrés”. Estos trabajos difieren en que Hacker y Gaines (1997) asumen que la relación entre las interacciones positivas y el incremento de estrés es positiva y monotónica, mientras que Michalet et al. (2006) apuntan a un colapso de estos efectos facilitativos bajo niveles extremadamente altos de estrés, donde incluso el crecimiento de las plantas nodriza, y por tanto su capacidad de modificación del microambiente, estaría limitado. Aunque estos modelos sencillos fueron un punto de partida excelente para empezar a evaluar el papel relativo de los factores físicos y las interacciones bióticas en el ensamblaje de las especies a nivel local, son insuficientes. Por un lado, se basan en una relación diversidad productividad unimodal, la cual no es, ni mucho menos, tan general como se esperaba (Grace 1999, Waide et al. 1999, Gillman y Wright 2006, sólo en 2010 se han publicado en la revista Ecology cinco estudios discutiendo la generalidad de esta relación). Por otro lado, presuponen la existencia de un gradiente de “estrés” que afecta de forma general todas las especies de una comunidad, y que este nivel de estrés aumenta a medida que se reduce la productividad, lo cual tampoco tiene por qué ser cierto (ver discusión en Körner 2003, 2004, Lortie et al. 2004b). Cada especie presenta unas características propias que le permitirán tener un óptimo ambiental en unas condiciones particulares (sean estas más o menos productivas); por tanto, a medida que nos alejamos de estas condiciones ambientales óptimas, esta especie en particular verá aumentado su nivel de estrés (Chapin et al. 1987, Körner 2003). Sin embargo, las distintas especies que coexisten en una comunidad difieren en mayor o menor grado en sus óptimos ambientales y, por tanto, es incorrecto considerar que todas ellas se verán afectadas de la misma manera a medida que cambien las condiciones ambientales (Chapin et al. 1987,
19 RESUMEN
Lortie et al. 2004b). Por lo tanto, el uso de aproximaciones basadas en el papel de las especies “tolerantes al estrés” facilitando la existencia de las especies más “competidoras” a medida que el estrés aumenta (p. ej. Travis et al. 2005) es inadecuado porque estas estrategias ecológicas cambian con las condiciones ambientales (una especie tolerante a un determinado factor de estrés no tiene porque ser tolerante a otros tipos de estrés; y una especie competidora verá modificadas sus habilidades competitivas dependiendo de las condiciones ambientales en las que se desarrolle). La revisión y cuestionamiento de estos tres supuestos (la existencia de una relación unimodal entre riqueza y productividad, de un nivel de estrés único que afecte a comunidades naturales enteras y de estrategias ecológicas que permanecen estables a lo largo de gradientes ambientales amplios), permitirá explorar alternativas más realistas sobre el papel que juega la expansión de nicho y las modificaciones microclimáticas promovidas por las plantas nodriza a lo largo de gradientes ambientales. Sería de esperar, entonces, que el efecto positivo de las plantas nodriza sobre la diversidad local se extienda con igual importancia a lo largo de gradientes ambientales amplios, ya que este efecto positivo afectará al mismo número de especies, aunque su identidad (tanto de las nodrizas como de las facilitadas) vaya cambiando a medida que cambien las condiciones ambientales y unas especies u otras se alejen de su óptimo ambiental (Greiner la Peyre 2001, Choler et al. 2001, Liancourt et al. 2005, Chu et al. 2008, Holmgren y Scheffer 2010). La superación de los supuestos aludidos debería tener profundas implicaciones en nuestra forma de ver la importancia relativa de las interacciones positivas a lo largo de gradientes ambientales, haciendo innecesario hablar de un nivel de estrés único a nivel de comunidad, ya que este nivel cambiará con cada especie y condición ambiental. Esta es quizás, la razón fundamental de los resultados contradictorios sobre los cambios en el signo y la intensidad de las interacciones planta planta a lo largo de gradientes ambientales (Maestre et al. 2005, 2006, Lortie y Callaway 2006). Asimismo, la frecuencia e importancia de las interacciones positivas a nivel de comunidad deberían mantenerse estables a lo largo de gradientes ambientales amplios, ya que la identidad, pero no la cantidad, de las especies facilitadas es lo que cambiará a lo largo de estos gradientes. Sin duda, estudios diseñados para evaluar estas predicciones serán de ayuda para finalmente entender tanto el papel relativo de los factores físicos y las interacciones bióticas en el mantenimiento de la diversidad local, como la relación de esta diversidad con la productividad (Mulder et al. 2001, Callaway 2007). La inmensa mayoría de las aproximaciones que versan sobre el efecto de la facilitación en las comunidades naturales, tanto teóricas como empíricas, se centran en los niveles medios altos de “estrés” (Hacker y Gaines 1997, Lortie et al. 2004a, Travis et al.
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2005, Michalet et al. 2006, Callaway 2007), otros estudios revelan que los efectos de ciertas plantas sobre sus vecinas pueden extenderse en condiciones muy productivas (Levine 1999, Laird y Schwamp 2006, 2009, Brooker et al. 2008), donde cabría esperar que la exclusión competitiva jugara un papel fundamental (Grime 1973, 2001). Uno de los mecanismos propuestos (la complementariedad de nicho, descrito a continuación) no puede considerase como facilitación, ya que no implica que una determinada especie se beneficie por la presencia de otra. En ambientes heterogéneos, una mayor diversidad de especies, o grupos funcionales distintos, puede llevar a una mayor y más eficiente explotación de los recursos, aumentando la productividad de la comunidad a mayores niveles de diversidad debido a la complementariedad de nicho (p. ej. Hector et al. 1999).
Figura A4 Quizás el ejemplo más conocido de redes de competencia intransitiva es el juego de “Piedra, papel o tijeras”. Podemos observar como la complejidad de las redes intransitivas aumenta a medida que añadimos más actores (especies) al juego. Este tipo de redes de competencia intransitiva es más probable que ocurran en las manchas de vegetación cuanto mayor sean la riqueza de especies y la heterogeneidad en los recursos por los que compiten. Esto puede encontrarse a medida que nos movemos desde áreas de suelo desnudo hacia las manchas de vegetación de mayor complejidad (imágenes de la parte de debajo de la figura).
Sin embargo, otros mecanismos sí que están directamente relacionados con las interacciones positivas entre plantas. Entre ellos destacan la facilitación indirecta, es decir el efecto positivo de una especie determinada sobre otra, mediado por el efecto negativo de la primera sobre una tercera especie (Levine 1999, Callaway 2007, Brooker et al. 2008, Cuesta
21 RESUMEN et al. 2010). Si imaginamos una sencilla comunidad de tres especies (A, B y C), donde hay una jerarquía competitiva marcada (A>B>C), entonces, es fácil de imaginar que A puede facilitar a C mediante su efecto negativo sobre B. Otro mecanismo que atañe a las interacciones positivas de una manera indirecta es la competencia intransitiva, esto es, la inexistencia de una jerarquía marcada en las habilidades competitivas de las especies que coexisten (Gilpin 1975). Si volvemos a nuestra comunidad de tres especies, será fácil de entender que si A>B>C>A entonces el balance competitivo está más equilibrado y se pueden mantener mayores niveles de diversidad (Laird y Schwamp 2006, 2009, Bowker et al. 2010; Fig. A4). Esta competencia intransitiva sólo puede existir cuando la heterogeneidad en los recursos y en los grupos funcionales que coexisten permite un equilibrio en las habilidades competitivas de las especies en una comunidad (Grace 1993, Huston 1999). Ya hemos dicho anteriormente que las plantas nodriza, y los parches que estas forman, son una de las mayores fuentes de heterogeneidad en ecosistemas semiáridos (p. ej. Pugnaire et al. 1996a, Tracol et al. 2010). Bajo el dosel de estas plantas se dan condiciones heterogéneas de luz, agua, nutrientes o redes micorrícicas (Pugnaire et al. 1996a, Holmgren et al. 1997, Wolfe et al. 2009 y referencias en ese texto) que pueden generar las condiciones necesarias de heterogeneidad para que se de competencia intransitiva o, alternativamente, segregación de nicho. Ambos mecanismos pueden promover un aumento de la diversidad de especies que coexisten bajo su dosel (Grace 1993, Pugnaire et al. 1996a, Hastwell y Facelli 2003, Silvertown 2004, Maestre y Cortina 2005, Badano y Cavieres 2006, Laird y Schwamp 2006). Así pues, es probable que se den procesos de retroalimentación positiva entre ambos procesos (más heterogeneidad y más diversidad generan competencia intransitiva o segregación de nicho, que a su vez aumentan la diversidad) que aumenten de forma desproporcionada la diversidad local de las comunidades vegetales. No obstante, hasta la fecha sólo hay un estudio que evalúe el efecto de las plantas nodriza sobre la dinámica competitiva de sus especies facilitadas (Tielbörger y Kadmon 2000b), y no se ha evaluado este efecto conjuntamente con otros mecanismos como la mejora microambiental y expansión de nicho. Estudios que evalúen los efectos de las plantas nodriza sobre la riqueza de especies local, teniendo en cuenta en un mismo marco general todos los posibles mecanismos por los que estas plantas pueden aumentar la diversidad (expansión de nicho, competencia intransitiva o segregación de nicho), son necesarios para entender finalmente el papel de las interacciones planta planta en la diversidad local y, por tanto, en la productividad y el funcionamiento ecosistémico (Mulder et al. 2001, Hooper et al. 2005) a lo largo de gradientes ambientales (Callaway 2007).
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EL PAPEL DE LA FACILITACIÓN EN LA EVOLUCIÓN DE LAS COMUNIDADES VEGETALES
Aunque se ha sugerido que las interacciones bióticas no son importantes en comparación con los procesos estocásticos de especiación y dispersión a lo largo de escalas de tiempo evolutivas (Hubbell 2001), numerosos estudios indican lo contrario (p. ej. Bascompte 2009). Ejemplos clásicos de ello son los procesos de coevolución que pueden existir entre diferentes especies de plantas y sus animales asociados, ya sean polinizadores o herbívoros (Darwin 1859). Rezende et al. (2007) encontraron una señal filogenética clara en redes de interacciones animal planta. Sus resultados indican que las interdependencias entre ambos tipos de organismos pueden llevar a procesos de coextinción cuando una de las especies desaparece, mostrando un alto grado de dependencia interespecífica que parece extenderse durante toda la historia evolutiva de las especies que forman las comunidades naturales. Estos procesos de coevolución han sido demostrados también en las interacciones entre plantas. Por ejemplo, Callaway y Aschehoug (2000) evaluaron las interacciones entre Centaurea diffusa , una planta nativa de Asia, e invasora en Estados Unidos, y sus vecinas en ambas regiones. En este estudio vieron como, al añadir carbón activo para secuestrar los compuestos alelopáticos, no se encontró ninguna diferencia entre las vecinas asiáticas (que por otro lado eran menos sensibles a la competencia con C. diffusa ). Sin embargo, las vecinas americanas experimentaron un menor efecto competitivo de C. diffusa al añadir carbón activo, lo que demuestra que estas especies estaban menos adaptadas a los compuestos alelopáticos. Estos resultados sugieren que las vecinas asiáticas habían experimentado algún grado de adaptación a estos compuestos debido a la coexistencia con C. diffusa . Pero sin duda, el mejor ejemplo de interdependencia entre plantas a lo largo de escalas de tiempo evolutivas lo encontramos en Valiente Banuet et al. (2006). Estos autores encontraron que las especies de origen Terciario (condiciones más húmedas que las actuales) dependen de la presencia de especies originadas durante el Cuaternario (condiciones más áridas) para mantener su nicho de regeneración en diversos ecosistemas Mediterráneos. La conclusión de estos autores fue que la mejora microclimática promovida por las especies del Cuaternario ha sido clave para mantener a las especies del Terciario en ambientes a los que no estaban adaptadas, lo que indica que las interacciones planta planta son fundamentales para mantener la diversidad de las comunidades naturales a lo largo de escalas de tiempo evolutivas. El reciente desarrollo de las filogenias moleculares ha permitido a los ecólogos evaluar el efecto de distintos mecanismos (i.e. interacciones bióticas, factores físicos) en el ensamblaje de las comunidades a lo largo de estas escalas de tiempo evolutivas (Webb et al.
23 RESUMEN
2002, Cavender Bares et al. 2009). Si asumimos que muchos rasgos ecológicos están bien conservados a lo largo de la evolución (Herrera 1984, 1992, Ackerly 2003, Valiente Banuet et al. 2006), una dominancia de las interacciones competitivas producirá la coexistencia de especies con rasgos marcadamente diferentes, que permitan cierta segregación de nichos ecológicos para su coexistencia; por tanto, el patrón filogenético de esa comunidad será más disperso o equitativo de lo que sería esperable por azar (Webb et al. 2002). En cambio, si los filtros abióticos son de mayor importancia para esa comunidad, el conjunto de especies que la formen se caracterizará por una cierta homogeneidad en sus rasgos ecológicos, que corresponde con sus adaptaciones morfológicas y fisiológicas a esas condiciones ambientales; por tanto, el patrón filogenético de esa comunidad será más agregado de lo que sería esperable por azar (Webb et al. 2002, Pausas y Verdú 2007). Esta asunción sencilla fue el punto de partida de la explosión de estudios que durante los últimos diez años han tratado de inferir los mecanismos dominantes en el ensamblaje de una comunidad dada a partir su patrón filogenético (revisado en Cavender Bares et al. 2009, Vamosi et al. 2009). Estudios recientes advierten sobre otros posibles mecanismos que pueden afectar al patrón filogenético de una comunidad y que antes no habían sido considerados. Por citar algunos ejemplos, la preferencia de herbívoros o polinizadores por taxones filogenéticamente relacionados (Webb et al. 2006, Sargent y Ackerly 2008), la escala a la que se realice el estudio (Cavender Bares et al. 2006, Kraft et al. 2007, Kraft y Ackerly 2010), diferencias en el nicho de regeneración o las habilidades competitivas entre las especies que coexisten (Myfield y Levine 2010), o las interacciones positivas entre plantas (Valiente Banuet y Verdú 2007, Verdú et al. 2009), son algunos de los mecanismos que pueden afectar a la estructura filogenética de las comunidades. Es por ello que, para inferir los mecanismos de ensamblaje a partir de patrones filogenéticos se recomiendan medidas complementarias de otros procesos, como patrones de co ocurrencia (indicador de interacciones bióticas positivas y negativas; Tirado y Pugnaire 2005), variables físicas (filtros abióticos) o la conservación de rasgos ecológicos importantes a lo largo de la evolución (Cavender Bares et al. 2009, Pausas y Verdú 2010). Sin embargo, estudios que incluyan las medidas de estos otros mecanismos y las posibles interacciones entre ellos, tanto a nivel de comunidad como a nivel de especie, son aún muy escasos pese a que las interacciones entre algunos de esos procesos son clave para el ensamblaje de las comunidades semiáridas (Holmgren y Scheffer 2010, Butterfield et al. 2010). La idea de Darwin (1859) en relación a que las especies más parecidas necesariamente tenían que competir de una forma más intensa ha permeado en la teoría ecológica durante 150
24
años (Webb et al. 2002, Cahill et al. 2008). Sin embargo, a pesar de sus profundas implicaciones para la diversidad local y el ensamblaje de las comunidades naturales, esta idea ha sido pobremente estudiada experimentalmente (Valiente Banuet et al. 2006, Valiente Banuet y Verdú 2007, 2008, Cahill et al. 2008, Castillo et al. 2010). Cahill et al. (2008) no encontraron ninguna relación entre la distancia filogenética y el efecto de la competencia al evaluar una base de datos amplia que incluía la relación entre 50 especies objetivo y 92 especies competidoras distintas. Ellos atribuyeron esta falta de relación a la diferencia entre las interacciones entre mono y dicotelodóneas, ya que la intensidad de la competencia aumentaba con la distancia filogenética para las monocotiledóneas, ocurriendo lo contrario con las dicotiledóneas. Los trabajos de Valiente Banuet y colaboradores (2006, 2007, 2008) y Castillo et al. (2010), conducidos en su mayoría con especies dicotiledóneas, concluyen que la competencia disminuye también con la distancia filogenética entre dos especies, siendo más probable que se den interacciones positivas entre especies distanciadas en la evolución. Por tanto, la idea de Darwin parece confirmarse en la mayoría de casos estudiados, al menos para plantas dicotiledóneas. De estos estudios se concluye, por tanto, que la relación evolutiva es clave para decidir el resultado de la interacción entre dos especies. Sin embargo, se ha discutido con anterioridad en este texto, y durante 20 años en la literatura ecológica en general, que las condiciones ambientales son fundamentales para definir el resultado de estas interacciones. Entonces, ¿cuál es la importancia relativa de las condiciones ambientales frente a las relaciones evolutivas a la hora de definir el resultado de las interacciones planta planta?, ¿interactúan ambos factores a la hora de definir estos resultados? Hasta la fecha ningún estudio se ha planteado responder a estas preguntas, las cuales son clave para establecer la importancia de las relaciones planta planta en el ensamblaje de las comunidades bajo distintas condiciones ambientales y a lo largo de escalas de tiempo amplias. Asimismo, estudios enfocados en la interacción entre la distancia filogenética entre las especies implicadas y el clima en el que se dan estas interacciones nos pueden ayudar a mejorar nuestras inferencias sobre los procesos reinantes en el ensamblaje de una comunidad a partir del estudio de los patrones filogenéticos.
25 RESUMEN
26
OBJETIVOS
El objetivo general de esta tesis es evaluar el efecto de distintos niveles de estrés, tanto biótico como abiótico, en el resultado de las interacciones entre pares de especies vegetales, estudiando también cómo estas interacciones y los factores climáticos afectan a la diversidad local de especies y a la estructura filogenética de las comunidades vegetales en medios semiáridos. Para poder conseguir este objetivo general se han desarrollado siete objetivos específicos, que se describen a continuación y se abordarán en los cinco capítulos que conforman el cuerpo de esta tesis doctoral.
OBJETIVOS A NIVEL DE PAR DE ESPECIES
• Evaluar el efecto del cambio en el patrón temporal de las precipitaciones predicho por diversos modelos de cambio climático en el resultado de la interacción entre Retama sphaerocarpa (planta facilitada) y distintas especies herbáceas (plantas nodriza) en un ecosistema natural (espartal dominado por Stipa tenacissima ) y uno emergente (herbazal de talud de carretera; Capítulo 1).
• Evaluar el efecto de la variabilidad espacio temporal en la disponibilidad de agua sobre la interacción entre el arbusto gipsófilo Lepidium subulatum (planta facilitada) y la herbácea perenne S. tenacissima (planta nodriza) a lo largo de diferentes estados ontogenéticos de L. subulatum (Capítulo 2).
• Determinar el efecto simultáneo de dos factores distintos de estrés (herbivoría y aridez), así como de su dinámica temporal, en el resultado de la interacción entre R. sphaerocarpa (planta facilitada) y la herbácea S. tenacissima (planta nodriza; Capítulo 3).
• Evaluar la generalidad de los modelos teóricos existentes para predecir el signo de las interacciones planta planta a lo largo de gradientes ambientales en dos regiones semiáridas contrastadas (Capítulo 4).
27 RESUMEN
• Definir la importancia relativa de las relaciones filogenéticas y las condiciones ambientales a la hora de definir el signo de las interacciones entre pares de especies vegetales presentes en espartales de S. tenacissima a lo largo de un gradiente ambiental amplio (Capítulo 5).
OBJETIVOS A NIVEL DE COMUNIDAD
• Estudiar la importancia relativa de distintos mecanismos de facilitación/competencia (expansión de nicho, mejora microambiental, competencia intransitiva y segregación de nicho) y de los factores climáticos, así como la interacción entre ambos, a la hora de determinar la riqueza local de especies en dos comunidades semiáridas de características contrastadas a lo largo de gradientes ambientales amplios (Capítulo 4).
• Evaluar la extensión del efecto de las interacciones bióticas, los factores climáticos, y su interacción, sobre el patrón filogenético en espartales de Stipa tenacissima a lo largo de un gradiente ambiental amplio (Capítulo 5).
28
METODOLOGÍA GENERAL Y ÁREA DE ESTUDIO
REA DE ESTUDIO
Salvo dos excepciones (parte de los capítulos 1 y 4), esta tesis doctoral se centra en su totalidad en los espartales de Stipa tenacissima situados en el centro y sudeste Peninsular. Este ecosistema es uno de los más representativos de las zonas semiáridas de España y el Norte de África (LeHoureu 2001). Los espartales se extienden sobre suelos pedregosos, limosos, arcillosos, calizos o yesosos, en zonas desde el nivel del mar hasta 2000 m de altitud, y con precipitaciones que pueden llegar hasta los 700 mm, aunque preferentemente se dan en la franja entre 200 400 mm (revisado en Maestre et al. 2007). Los espartales son formaciones vegetales abiertas, con coberturas que oscilan entre el 18% y el 60% (Maestre 2002, Ramírez 2006), de estructura y composición heterogéneas (Puigdefábregas y Sánchez 1996, Puigdefábregas et al. 1999, Maestre et al. 2007). Al igual que otros sistemas semiáridos, la estructura espacial de la vegetación en los espartales, caracterizada por la presencia de manchas de vegetación discreta embebidos en una matriz de suelo desprovisto de plantas vasculares, generan una dinámica fuente sumidero que resulta clave en la dinámica hídrica y ecológica de estas comunidades (Puigdefábregas et al. 1999, Maestre y Cortina 2004c, Ramírez y Bellot 2009). Los espartales han sido intensamente manejados por el hombre desde hace no menos de 4000 años, principalmente para la explotación de fibras vegetales (Barber et al. 1997). Sin embargo, la llegada de las fibras sintéticas y el abandono general del campo que ocurrió en España a partir de los 1960s, promovió el cese del manejo humano de estos ecosistemas (Maestre et al. 2007). Este cese ha provocado la recolonización, aunque muy lenta y poco abundante, de los arbustos rebrotadores típicos de estos climas, que anteriormente eran eliminados por su posible efecto negativo sobre el crecimiento del esparto (Cortina y Maestre 2005, Maestre et al. 2007, Maestre et al. 2009b). Así, arbustos como Pistacia lentiscus , Quercus coccifera , Rhamnus lycioides o Ephedra fragilis , entre otros, han aumentado levemente su cobertura en estos ecosistemas desde el abandono de su explotación (Maestre et
29 RESUMEN al. 2007). Estos arbustos, a pesar de representar una parte pequeña en cuanto a cobertura en estos ecosistemas, juegan un papel fundamental, ya que incrementan la heterogeneidad y diversidad local (Cortina y Maestre 2005, Maestre y Cortina 2005), y afectan positivamente a la fertilidad y el funcionamiento ecosistémico (Pugnaire et al. 1996a, Caravaca et al. 2003, Maestre et al. 2009b). A diferencia de estos arbustos, que extienden su sistema radicular no sólo bajo su dosel, si no también en las áreas de suelo desnudo circundantes, el esparto centra sus raíces exclusivamente bajo su dosel, y a profundidades inferiores a 40 cm de profundidad, dependiendo su rendimiento en gran parte de su capacidad para recoger el agua de escorrentía generada durante los eventos de lluvia (Puigdefábregas et al. 1999; pero véase Ramírez et al. 2007 para una visión alternativa). Esta capacidad de capturar el agua de escorrentía, junto con los efectos que su dosel produce sobre la reducción de la radiación incidente y la demanda evaporativa, son claves para entender el efecto positivo que el esparto produce sobre otras especies y su papel como “islas de recursos” (Maestre et al. 2001, 2003, Gasque y García Fayos 2004, Armas y Pugnaire 2005, Barberá et al. 2006, Navarro et al. 2008). Los capítulos 1, 2 y 3 de esta tesis se centran en espartales del centro de la Península Ibérica que crecen en suelos gipsícolas. Estos suelos presentan características químicas (exceso de iones de sulfato o Calcio, baja retención de agua; Meyer 1986, Escudero et al. 1999, 2000) y físicas (costra superficial dura; Romao y Escudero 2005) que hacen que la colonización vegetal difícil para muchas especies, siendo su composición florística particularmente abundante en especialistas de estos sustratos (revisado en Caballero 2006, Matesanz 2008). Esto, junto con la combinación de características climáticas adversas (estos suelos se desarrollan sobretodo en medios semiáridos) hace que estos suelos yesosos presenten una gran cantidad de endemismos, adaptados a las condiciones particulares de estos suelos y climas. Estas características hacen de los ecosistemas Mediterráneos yesíferos hábitats de interés para su conservación por la particularidad de las especies que los conforman (Caballero 2006, Matesanz 2008 y referencias en esos textos). Por tanto, en los espartales escogidos para el desarrollo de los capítulos 1, 2 y 3 pueden encontrarse especies propias de los matorrales gipsófilos (especialistas de suelos yesíferos; Helianthemum squamatum , Lepidium subulatum , Centaurea hyssopifolia ) y “gipsovags” (generalistas que pueden vivir en suelos yesíferos; Retama sphaerocarpa , Rosmarinus officinalis o Thymus vulgaris ). En cambio, los capítulos 4 y 5 se centran en los espartales presentes en los suelos calcáreos desde Guadalajara a Murcia (ver Fig. A5). La amplia zona de distribución de estos espartales sobre un suelo relativamente homogéneo hace posible la realización de experimentos observacionales a lo largo de un gradiente climático amplio, que oscila entre
30
13 17 ºC de temperatura media, y 273 488 mm de precipitación media anual, con mucha mayor cantidad y frecuencia de heladas en el extremo occidental (Guadalajara Madrid) que en el oriental (Alicante Murcia) del gradiente. Alternativamente, parte de los experimentos de esta tesis doctoral (Capítulo 1) se han desarrollado sobre herbazales de talud de carretera, un tipo de ecosistema emergente que está aumentando su importancia a nivel global año a año (García Palacios et al. 2010). Estos sistemas se caracterizan por una cobertura herbácea dominada por especies anuales, generalmente ruderales que presentarán mayor o menor cobertura dependiendo del tipo de talud (desmonte o terraplén; Matesanz et al. 2006) o de la disponibilidad de agua durante la germinación y desarrollo de las plántulas (Bochet y García Fayos 2004; ver García Palacios 2010 para una revisión extensa sobre la dinámica de estos sistemas emergentes). En estos herbazales, es común que la sucesión secundaria se vea ralentizada, bien por la escasa disponibilidad de agua o nutrientes (Bolling y Walker 2000), o bien porque coberturas herbáceas muy desarrolladas no dejan huecos libres para la colonización de nuevas especies (Burke y Grime 1996). La introducción de especies leñosas en estos sistemas ha sido recomendada para acelerar la sucesión secundaría (Booth et al. 1999); sin embargo, sabemos muy poco sobre como las herbáceas dominantes en este tipo de sistemas afectan al éxito de estas plantaciones, especialmente bajo diferentes niveles de disponibilidad hídrica. Un mejor entendimiento de la interacción entre ambos grupos vegetales (herbáceas y leñosas) nos permitirá conciliar los dos mayores retos en la restauración de estos taludes de carretera: el establecimiento de una cobertura herbácea suficientemente densa como para prevenir procesos de erosión (Andrés y Jorba 2000), y el establecimiento de especies leñosas para acelerar su sucesión secundaria (Jorba y Vallejo 2008). Por otro lado, en el Capítulo 4 se evalúa el efecto de las interacciones bióticas y el clima en la diversidad local, no sólo de espartales, si no de ecosistemas semiáridos australianos. Concretamente se han muestreado comunidades pertenecientes a las alianza de Eucalyptus populnea y Callitris glaucophylla y de Casuarina pauper y Alectyron oleifolius (Beadle 1948), comúnmente encontradas en las llamadas “tierras rojas” de este continente. Estas tierras rojas se caracterizan por tener textura arenosa, suelos profundos y con contenidos bajos en nutrientes (Isbell 1996). Estos ecosistemas se caracterizaban originalmente por presentar coberturas herbáceas continuas, con individuos dispersos de Eucalyptus spp. y algunos arbustos. Sin embargo, la elevada presión ganadera a la que han sido sometidas estas áreas (Keith 1998) ha incrementado notablemente el reclutamiento de estos arbustos (p. ej. Geijera parviflora , Eremophylla spp. , Callitris glaucophylla , etc.) y ha reducido la cobertura
31 RESUMEN herbácea. Lo que finalmente ha generado una estructura discontinua, de manchas discretas de vegetación embebidas en una matriz de suelo desnudo, equivalentes a las de los espartales anteriormente descritos (Tongway y Hindley 1995). Estas comunidades ocupan una amplia superficie en el este de Australia, que permitió seleccionar 10 parcelas con vegetación perteneciente a estas comunidades a lo largo de un gradiente climático amplio ( 16º–19º C y 280–630 mm) con el objetivo de complementar el muestreo realizado en España para el Capítulo 4 (descrito con más detalle en la siguiente sección).
Figura A5. Distribución aproximada de las parcelas utilizadas a lo largo del gradiente ambiental referido en los capítulos 4 y 5. El diagrama ombroclimático (Fuente: www.globalbioclimatics.org) y una imagen general de los dos extremos del gradiente junto a una posición intermedia aparecen mostrados en la figura.
El clima de todas las áreas de estudio escogidas para esta tesis es Mediterráneo semiárido, difiriendo en su grado de continentalidad y en sus precipitaciones medias. En las parcelas situadas en el centro Peninsular, las temperaturas en invierno son mucho más frías y las precipitaciones anuales son algo mayores. La lluvia sigue una distribución bimodal, con máximos marcados en primavera (Abril Mayo) y otoño (Septiembre Octubre). La variabilidad interanual de la precipitación es muy grande, siendo impredecibles tanto la
32
cantidad como el patrón temporal de las lluvias de cada año (revisado en Puigdefábregas et al. 1999; ver figuras con precipitaciones registradas durante el período de estudio en los capítulos 1 y 3). En las parcelas situadas en el sudeste peninsular, las temperaturas son más suaves en invierno y las precipitaciones medias algo menores. La distribución temporal de los eventos de lluvia en estas parcelas es más unimodal, centrándose las precipitaciones hacia finales del verano y comienzos del otoño (Fig. A5). Las precipitaciones en el gradiente australiano siguen una distribución relativamente homogénea a lo largo del año, con una ligera predominancia de eventos de lluvia durante el verano (el 60% de estos eventos se concentra en verano).
METODOLOGÍA GENERAL
En esta tesis doctoral se han realizado experimentos tanto manipulativos como observacionales, en los que se incluyen distintos niveles de estrés abiótico (generalmente aridez) y biótico (herbivoría). Todos ellos han sido llevados a cabo bajo condiciones naturales. Los diferentes niveles de aridez se han conseguido mediante riegos en los experimentos manipulativos, o mediante el uso de gradientes ambientales amplios en las aproximaciones observacionales. En éstas últimas se han homogeneizado, tanto como ha sido posible, la pendiente, orientación, tipo de suelo e historia de manejo previo de las parcelas seleccionadas, con la intención de evitar la influencia de otros factores que no estuvieran considerados en el experimento y que pudieran confundir la interpretación de sus resultados. Los únicos herbívoros considerados han sido los conejos, que eran especialmente abundantes en las parcelas seleccionadas (véanse los tres primeros capítulos). Su nivel de herbivoría ha sido controlado mediante mallas de exclusión, combinado con el seguimiento de plantones no protegidos a lo largo de un año. Los experimentos manipulativos se centran en interacciones a nivel de par de especies. Las aproximaciones observacionales, en cambio, han sido utilizadas para evaluar el efecto de estas interacciones tanto a nivel de especie como a nivel de comunidad. La complejidad de las interacciones bióticas se ha evaluado mediante análisis de co ocurrencia (Gotelli 2000) o utilizando distintos indicadores del desarrollo vegetal (crecimiento, supervivencia y eficiencia fotosintética en los manipulativos, crecimiento o cobertura en los observacionales) en individuos que crecían bajo el dosel de la planta nodriza escogida y en áreas libres de vegetación para cada estudio. La metodología utilizada en cada caso se detalla en la sección dedicada a ese fin en los distintos capítulos de esta tesis doctoral (ver siguiente sección).
33 RESUMEN
34
ESTRUCTURA GENERAL DE LA TESIS
Los cinco capítulos que conforman el cuerpo de esta tesis han sido escritos en inglés, para su publicación en revistas científicas de ámbito internacional. A continuación se da una breve descripción de estos capítulos y de la metodología utilizada en cada uno de ellos.
Capítulo 1. Las modificaciones en el régimen de lluvias predichas con el cambio climático modulan las interacciones herbácea-arbusto en dos comunidades semiáridas.
Pese al gran interés que ha suscitado en los últimos 20 años la relación entre las interacciones planta planta y el nivel de estrés, muy pocos estudios han evaluado cómo los cambios en el patrón temporal de las precipitaciones dentro del mismo año afectan al resultado de las interacciones planta planta. Este patrón temporal es incluso más importante que la cantidad de lluvia que cae durante un año determinado para el funcionamiento de los medios semiáridos. El objetivo de este capítulo es evaluar el efecto de las modificaciones en la abundancia y frecuencia de los eventos de lluvia predichos con el cambio climático en la interacción entre plantones de R. sphaerocarpa y diversas especies herbáceas. Para ello aumentamos experimentalmente la cantidad de agua disponible entre abril y julio, imitando a la inversa la reducción de las precipitaciones durante este período (el tratamiento control, sin riego, sería el futuro escenario de cambio climático y los tratamientos de riego serían los escenarios actuales). El riego fue distribuido en dos o cuatro pulsos de lluvia, imitando el incremento en la frecuencia de eventos torrenciales. El estudio se llevó a cabo durante tres años en dos sistemas marcadamente diferentes situados sobre sustratos ricos en yeso: un espartal y un herbazal de terraplén de carretera, dominados por S. tenacissima y diversas anuales nitrófilas, respectivamente. Para evaluar el efecto de las herbáceas sobre R. sphaerocarpa , se midió la supervivencia, crecimiento y eficiencia fotosintética durante estos tres años. Los objetivos de este capítulo eran evaluar las diferencias entre 1) diferentes vecinas herbáceas, 2) el efecto de las vecinas a lo largo de pulsos e interpulsos y 3) el cambio en el efecto de las vecinas bajo diferentes abundancias o frecuencias de eventos lluviosos.
35 RESUMEN
Capítulo 2. La heterogeneidad espacio-temporal en los factores abióticos modula los cambios entre competencia y facilitación que ocurren a lo largo de la ontogenia.
Las interacciones planta planta están determinadas, en parte, por las condiciones ambientales y la ontogenia de las especies implicadas. Pese a que el efecto de ambos factores en el resultado de estas interacciones ha sido evaluado de forma separada, muy pocos estudios han investigado su efecto conjunto. El objetivo de este capítulo era testar este efecto, así como su variabilidad espacio temporal. Para ello se evaluó la interacción entre el arbusto gipsófilo Lepidium subulatum y la herbácea perenne S. tenacissima en tres zonas del centro Peninsular. Dentro de estas tres zonas evaluamos el resultado neto de la interacción entre ambas especies usando análisis de co ocurrencia en laderas con orientación norte (menos estrés) y sur (más estrés). En una de las tres zonas (Aranjuez) se evaluaron cambios en el signo de la interacción a lo largo de distintas etapas ontogenéticas de L. subulatum en las dos orientaciones mediante una combinación de experimentos de siembra y medidas dendrocronológicas, de floración y de acumulación de carbohidratos. Este conjunto de técnicas nos permitió estudiar en detalle el efecto de la ontogenia y de la variabilidad espacial en la disponibilidad hídrica, así como su interacción en la relación entre L. subulatum y S. tenacissima . Las hipótesis principales fueron: 1) la interacción entre ambas especies pasará de fuertemente positiva a fuertemente negativa a lo largo del desarrollo de L. subulatum ; 2) dado que ambas especies son tolerantes al estrés, es de esperar que las interacciones positivas dominen a niveles intermedios de estrés hídrico; y 3) un mayor nivel de estrés hídrico debería reducir el efecto negativo de S. tenacissima en individuos adultos de L. subulatum .
Capítulo 3. Las dinámicas temporales de la herbivoría y la disponibilidad hídrica interactúan modulando el resultado de una interacción herbácea-arbusto en un ecosistema semiárido.
La herbivoría y la aridez son dos factores de estrés que comúnmente coinciden en los medios semiáridos, jugando ambos un papel fundamental en el resultado de las interacciones planta planta. Sin embargo, su efecto conjunto ha sido pobremente estudiado. En este capítulo se estudia el efecto conjunto de ambos tipos de estrés, y su variabilidad temporal a lo largo del año, en el resultado de la interacción entre S. tenacissima y plantones del arbusto R. sphaerocarpa . Para ello se utilizó una combinación de aproximaciones observacionales y
36
experimentales. Estas aproximaciones incluyen el seguimiento de la supervivencia y el nivel de daño provocado por conejo en plantones sin protección a lo largo de un año, y el efecto de la manipulación del nivel de aridez y el daño por herbivoría en el signo de la interacción entre ambas especies. Las hipótesis iniciales de este estudio fueron: 1) S. tenacissima reducirá el daño por conejo sobre R. sphaerocarpa mediante su papel de ocultadora frente a los herbívoros; 2) las mejores condiciones hídricas, pero menores niveles de luz, reducirán la tolerancia de R. sphaerocarpa bajo el dosel de S. tenacissima ; y 3) el efecto conjunto de niveles altos de ambos tipos de estrés (herbivoría y aridez) anularán el efecto positivo derivado de la protección y la mejora microclimática de S. tenacissima .
Capitulo 4. Sobre la importancia relativa del clima y las interacciones bióticas no tróficas como determinantes de la riqueza local de especies vegetales.
En este capítulo se pretende evaluar el efecto relativo de las condiciones climáticas y distintos componentes de las interacciones bióticas (expansión de nicho y efecto sobre la dinámica competitiva de las especies vecinas –intransitividad en la competencia o segregación de nicho), así como la interacción entre ambos factores, a la hora de definir la riqueza local de especies vegetales en comunidades semiáridas a lo largo de gradientes ambientales amplios. Para ello se llevo a cabo un estudio observacional a diversas escalas en comunidades semiáridas de España y Australia. Se evaluó el efecto de ocho variables climáticas, resumidas mediante análisis de componentes principales, sobre la riqueza específica de cada localidad, así como sobre diversos indicadores del signo, intensidad e importancia de las interacciones bióticas a nivel de especie y de comunidad. Además, se estudió el efecto de estas interacciones sobre la riqueza específica, y la variación de dicho efecto a lo largo del gradiente climático escogido en cada región. Se midió la intensidad y la importancia de estas interacciones, tanto a nivel de par de especies como de comunidad, utilizando índices disponibles en la literatura. La frecuencia de las interacciones facilitativas a nivel de comunidad fue cuantificada calculando el porcentaje de especies, con respecto al número total de especies en la localidad, que se desarrollaron mejor (beneficiarias), o dependían directamente (obligadas) de la presencia de dos especies nodrizas distintas en cada región. La expansión de nicho fue evaluada mediante el número de especies obligadas, y también utilizando un índice de similaridad entre las poblaciones de los microambientes nodriza (bajo una de las dos especies nodriza seleccionadas en cada región) y claro (en suelo desnudo). Los cambios en la dinámica competitiva de las vecinas fueron analizados mediante una
37 RESUMEN aproximación observacional a escala de mancha, y utilizando modelos nulos de estructura agrupada (“guild structure null models”) para medir los patrones de co ocurrencia. Nuestras hipótesis iniciales predecían una igual importancia de las interacciones bióticas para la diversidad a lo largo de los gradientes ambientales, provocada porque la expansión de nicho afecta al mismo número de especies, aunque su identidad cambie, a lo largo de estos gradientes. Alternativamente, proponemos que los cambios en la dinámica competitiva (segregación de nicho o competencia intransitiva), junto con el aumento de la riqueza de especies debido a la expansión de nicho, conducen a efectos positivos desproporcionados sobre la riqueza local de especies debido a procesos de retroalimentación positiva.
Capitulo 5. Sobre la importancia relativa de las condiciones ambientales, las interacciones bióticas y las relaciones evolutivas como determinantes de la estructura de las comunidades semiáridas.
En este capítulo se evalúa el efecto relativo de las condiciones ambientales y las interacciones bióticas (competencia/facilitación a nivel de comunidad) sobre el patrón filogenético de espartales semiáridos dominados por S. tenacissima . En el mismo se estudia también cómo interactúan estos dos factores a la hora de determinar dicho patrón, así como la variación en sus efectos relativos a lo largo de un gradiente ambiental amplio. Para ello se utilizan parte de las zonas de estudio e indicadores de interacciones bióticas descritos para el capítulo 4, junto con medidas de co ocurrencia a nivel de parcela. También se determinó el patrón filogenético de cada una de las localidades muestreadas y se evaluó el efecto sobre este patrón de los distintos mecanismos derivados de las condiciones climáticas, las interacciones bióticas, y la interacción entre ambos factores, mediante regresiones lineares y correlaciones parciales. Asimismo, se analizó el efecto de la distancia filogenética entre la planta facilitada y su nodriza, de las condiciones climáticas de cada lugar, y de la interacción entre ambos factores, como moduladores de la relación entre un total de 200 pares de especies a lo largo de este gradiente ambiental mediante árboles de regresión. Las hipótesis principales de este capítulo fueron: 1) la importancia relativa de las condiciones climáticas y las interacciones bióticas para el ensamblaje de las comunidades, y por tanto para su patrón filogenético, varía a lo largo del gradiente ambiental, y 2) la distancia filogenética y las condiciones climáticas interactúan a la hora de definir el signo de las interacciones planta planta.
38
Predicted climate change effects in rainfall regime modulate the 1 outcome of grass-shrub interactions in two semi-arid communities
Santiago Soliveres, Fernando T. Maestre, Pablo García-Palacios, Adrián Escudero, and Fernando Valladares. Manuscrito inédito
CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
40 CHAPTER 1
ABSTRACT
Much research has been devoted to understand how plant plant interactions behave along water stress gradients in drylands. However, few studies have evaluated how changes in the magnitude and frequency of rainfall events, which are an important component of ongoing climate change, modulate the outcome of such interactions. We evaluated the response of the interaction between seedlings of the shrub Retama sphaerocarpa (L.) Boiss., our target plant, and different herbaceous neighbours to those changes in rainfall availability during three years. The experiment was conducted in natural and anthropogenic grasslands dominated by a perennial stress tolerator and ruderal annual species, respectively. Competition between herbaceous plants and Retama seedlings prevailed, and increased with water stress. These negative effects were reduced through time, suggesting niche segregation between the interacting plants. Less frequent, but more intense rainfall events, accelerated this niche segregation in the natural grassland, where the stress tolerator grass took more advantage of light rainfall events than Retama and competition was stronger. Thus, increases in the frequency of heavy rains could counteract the negative effects of the increased competition between grasses and shrubs expected under higher water stress conditions. However, in the anthropogenic grassland the phenology of the annuals made more frequent and lighter rainfall events more useful to avoid competition by water, being heavy rains uneffective in this case. Our findings suggest the existence of a trade off between the shade tolerance of protégée plants and the effects of nurses on light and water availability that defines the outcome of a given plant plant interaction. Our results challenge current predictions on the outcome of these interactions under climate change, and could be used to further refine our forecasts on how plant plant interactions, and therefore plant communities, will respond to such change in ecosystems where grass shrubs interactions are prevalent.
41 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
INTRODUCTION he study of plant plant interaction should be considered when studying plant dynamics along water stress plant interactions and community dynamics Tgradients has been a major topic in water limited ecosystems (Goldberg and in dryland ecology during the last decade Novoplansky 1997, De la Cruz et al. 2008). (e.g. Pugnaire and Luque 2001, Maestre Understanding community responses to and Cortina 2004a). The seminal “stress water pulses in water limited ecosystems is gradient hypothesis” (SGH), which predicts particularly timing because current rainfall an increase in the frequency of facilitative events are likely to be extremer as a interactions as abiotic stress increases consequence of the ongoing climate change (Bertness and Callaway 1994), constitutes a (Knapp et al. 2008). For example, forecasts paradigmatic framework for these studies for the Mediterranean Basin predict a (see Callaway 2007 and Brooker et al. 2008 decrease in the amount of annual rainfall, for reviews). However, the generality of its the lengthening of drought periods and the predictions has been recently debated increase of the frequency of heavy storms (Maestre et al. 2005, 2006, Lortie and (IPCC 2007). Grass shrub interactions are Callaway 2006, Callaway 2007, Maestre et particularly instructive for studying the al. 2009a, Smit et al. 2009, Malkinson and effects of these climatic changes on the Tielbörger 2010). Furthermore, the outcome of plant plant interactions because relationship between plant plant of their contrasted water acquisition interactions and environmental gradients is strategies and their abundance in natural especially complex in arid and semiarid and anthropogenic ecosystems worldwide environments, where water availability is (e.g. Sala et al. 1989, Scholes and Archer highly pulsed, with erratic and typically 1997). While grasses tend to use more short periods of enough water availability efficiently the water derived from light and triggering ecosystem processes sparse rainfall events (Sala et al. 1989, (Schwinning and Sala 2004). Indeed, the Reynolds et al. 2004), shrubs generally size and frequency of individual rain events perform better after continuous rains, which registered in a given period may have more recharge deeper soil profiles (Sala et al. importance for the functioning of semiarid 1989, Schwinning and Ehleringer 2001, ecosystems than the total rainfall Schwinning and Sala 2004). These grass accumulated (Whitford 2002, Ogle and shrub interactions are likely to be Reynolds 2004). These temporal dynamics particularly sensitive to the changes in
42 CHAPTER 1 overall water availability and frequency of have evaluated the effects of shrubs on rainfall events predicted under future annuals (see Callaway 2007 for a review). climate change scenarios. For example, Thus, studies directed to clarify the effects shrub encroachment may be promoted by of grasses (both perennials and annuals) on the increase in the frequency of heavy shrubs across realistic water stress gradients storms (Ogle and Reynolds 2004), or are of crucial importance to understand reduced by the enlargement of summer plant community responses to ongoing drought (López et al. 2008), two features of climate change in those ecosystems where the ongoing climate change. Alternatively, grasses and shrubs coexist. In this study we grasses may foster shrub survival and aimed to test the response of grass shrub recruitment under moderate drought interactions to changes in the degree of conditions, but these positive effects may abiotic stress. The study was conducted in be overcome by the increase in competition two different semiarid Mediterranean registered under periods of very low water communities: a natural Stipa tenacissima L. availability (Kitzberger et al. 2000, Maestre steppe (hereafter called “natural grassland”) and Cortina 2004a, 2004b). The possible and an annual dominated grassland located responses of these interactions to changes in a motorway embankment (hereafter in rainfall amount and frequency seem very called “anthropogenic grassland”). complex and at times counter intuitive, and Degraded landscapes such as the latter are further complicated by the fact that the represent good examples of novel multiple responses described above are ecosystems, which are increasing in likely to occur simultaneously. importance worldwide because of the rise A particular case of grass shrub in anthropogenic disturbances (Hobbs et al. interaction, and also farily common in 2006). Given that the structure and semiarid environments worldwide, occurs functioning of these novel ecosystems often when annuals act as nurse plants for shrubs differs from that found in natural ones (e.g. Holzapfel and Mahall 1999 and (Hobbs et al. 2006), studies focusing on references therein). These annual shrub both natural and novel ecosystems may interactions are likely to behave help to further refine our predictions of the differentially along environmental gradients response of plant communities to climate because of the different life strategy of the change (Brooker 2006). Our focal species former. However, they have been largely were the leguminous shrub Retama ignored in the facilitation literature, as the sphaerocarpa (L.) Boiss. (hereafter bulk of studies on grass shrub interactions Retama ) and different grass species (the
43 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS stress tolerator tussock grass Stipa intense because they will be mainly derived tenacissima –hereafter Stipa – and several from the shade produced by their dry ruderal annual species), the latter acting as tissues (annuals die during summer), but potential nurse plants for Retama . Stipa will reduce Retama survival because The outcome of grass shrub of the increased competition by water will interactions in semiarid ecosystems, either outweight the positive environmental natural or anthropogenic, depends strongly buffering promoted by shade (Maestre and on soil water availability (Eliason and Allen Cortina 2004a); and iii) the increase in the 1997, Maestre and Cortina 2004a), and frequency of heavy storms will reduce therefore, both grassland types are excellent competition between Retama and both Stipa study systems to test changes in the and annual grasses by recharging deeper outcome of grass shrub interactions across soil layers and promoting niche segregation abiotic stress gradients. We obtained a (Sala et al. 1989, Ogle and Reynolds 2004). realistic water stress gradient by modifying the amount and timing of water availability METHODS separately, according to the most likely STUDY AREA climate change scenarios for the study area. Both the natural and anthropogenic We tested the following hypotheses: i) both grasslands selected for this study are Stipa and annual grasses will reduce located in the center of the Iberian Retama growth because of competition by Peninsula (natural grassland: 40º03´60´´N, water during wet seasons, when most of 3º54´91´´W, 545 m.a.s.l.; anthropogenic vegetation growth concentrates in semiarid grassland: 52º16´00´´N, 3º43´13´´W, 604 environments (Goldberg and Novoplansky m.a.s.l.) and share the same climate and soil 1997, Escudero et al. 1999); ii) Stipa and type. The climate is semiarid annuals will differ in their effect on Retama Mediterranean, with average annual survival. Although both Stipa and annuals precipitation and temperature of 388 mm will increase Retama survival during and 15 ºC, respectively, and with a strong summer drought, mainly via microclimate summer drought (Aranjuez weather station; amelioration and improvement of soil 1994 2005 period; Marqués et al. 2008). properties (Goldberg and Novoplansky Both communities are located on gypsum 1997, Maestre et al. 2003), these effects rich soils, classified as Xeric Haplogypsid will change with the lengthening of summer (Marqués et al. 2008), although in the drought. Under these conditions, the anthropogenic grassland the original positive effects of annuals will be more
44 CHAPTER 1 substrate has been altered by the mixture microsite types were defined differently in with gravels and components from external the two ecosystems. Nurse microsites were: sources during the construction of the 1) located upslope and adjacent to Stipa motorway. Vegetation in the natural tussocks (stress tolerator nurse) of ca. 1 m grassland is an open steppe dominated by width (< 15 cm from the edge of the north Stipa tenacissima , with a perennial plant face of the tussock, where facilitative cover of 24%. Vegetation in the effects of this species on target shrubs have anthropogenic grassland is dominated by been found, e.g. Maestre et al. 2003) in the annuals, with a mean cover of 75% and natural grassland, and 2) located in the with Bromus rubens L. , B. diandrus Roth., center of a multi specific 50 cm diameter and Medicago sativa L. as the most grass patch (ruderal nurse) of ca. 40 cm abundant species (16, 14 and 14% of the height and 75 100% cover (in spring) in the total cover, respectively; García Palacios et anthropogenic grassland. The rest of the al. 2010). Hereafter we refer to those seedlings were assigned to randomly herbaceous annuals as annual grasses for selected Open microsites. These were either simplicity. Both study sites hold a high located in bare ground areas at least 80 cm density of rabbits ( Oryctolagus cunniculus away from any perennial plant (natural L.), as suggested by visual contacts, and by grassland site), or placed in sites where all the high number of warrens and latrines aboveground vegetation within 80 cm found (S. Soliveres, pers. obs. ). diameter circles surrounding the target seedling was monthly clipped EXPERIMENTAL DESIGN (anthropogenic grassland site). In December 2006, 176 two year old The seedlings were randomly allocated Retama seedlings, with a mean height of of to establish two full factorial experiments 27 ± 2 cm, were planted in each site by with two factors each, which were run in using manually dug holes of 20×20×20 cm. parallel in the two grasslands studied. In the These seedlings came from a nursery in first experiment (hereafter Experiment 1) central Spain (viveros Bárbol, Madrid). We the two factors were Microsite ( Nurse vs. randomly assigned these seedlings to two Open ) and Irrigation. This irrigation different microsites: “Nurse” and “Open”. treatment consisted in three different Because of the heterogeneous patch amounts of water applied during eight interpatch structure of the natural steppe watering events (once every month between system, and the homogenous herbaceous April and July in both 2007 and 2008). In cover of the anthropogenic site, these each watering event, the 0%, 25% and 50%
45 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS of the median from the last 30 years for that studied of: i) an increase in summer drought particular month was applied to the control (summer drought was longer in less (hereafter +0%), amount 1 (hereafter watered plants [+0% > +25% > +50%] +25%), and amount 2 (hereafter +50%) because of the low rainfall levels typically treatments, respectively. In the second registered during June and July in the study experiment (hereafter Experiment 2) the area), ii) a reduction of rainfall during the factors were i) Microsite ( Nurse vs. Open ), wet season (spring rainfall was less and ii) Irrigation frequency. In this case we abundant in non watered plants [+0% < applied the same amount of water +25% < +50%]), and iii) changes in the employed in the +50% treatment, but with frequency of heavy showers (magnitude of two different frequencies: two and four individual events was higher in the 2x than pulses (hereafter named as 2x and 4x in the 4x treatment, despite both treatments treatments, respectively). The first received the same amount of water, Fig. frequency treatment (4x) was applied in 1.1). All these effects, i.e. the increase in four monthly pulses, from April to July, as summer drought, the reduction in the total explained above; the second frequency rainfall amount and the increase in the treatment (2x) was applied every two frequency of heavy showers are predicted months, in May and July. In each of the by future climate change scenarios for the watering events applied in the 2x treatment, Mediterranean Basin (IPCC, 2007; see the amounts of water added equaled the Table 1.1). Because of the high density of sum of April and May, and June and July rabbits observed, and to avoid seedling irrigations applied in the 4x treatment, predation, the seedlings were protected respectively (Fig. 1.1, Table 1.1). Both from browsing by using a thin wire mesh. irrigation treatments were applied This mesh did not shade the seedlings, and irrespectively of the rainfall registered in thus did not confound the effects of any of each month (Fig. 1.1). With these two the factors studied in the experiment. experiments we aimed to evaluate the effects on the outcome of the interaction
46 CHAPTER 1
Figure 1.1 Climatic data (mean monthly temperature, black circles; and monthly rainfall, black bars) obtained from a meteorological station (Onset, Pocasset, MA, USA) located in the natural grassland. The increment in monthly rainfall promoted by the irrigation treatments applied during 2007 and 2008 is represented by different colors: +25% (dark grey) = irrigation of 25% of the median of April-July rainfall in four pulses, +50 -4x (light grey) = irrigation of 50% of the median of April-July rainfall in four pulses, and +50 -2x (white) = irrigation of 50% of the median of April-July rainfall in two pulses).
Table 1.1 Details of the water amount added (l · m -2) in each irrigation treatment (Experiments 1 and 2) and the periods when these pulses took place. Last row explains the specific climate change effect that each irrigation treatment emulated.
Irrigation EXPERIMENT 1: EXPERIMENT 2: Pulses Amount treatment Frequency treatment +0% +25% +50% 4x 2x April 0 6 12 12 May 0 9.25 18.5 18.5 30.7 June 0 10.85 21.7 21.7 July 0 5.65 11.3 11.3 33 Total water applied 0 31.75 63.5 63.5 63.5
Simulated climate change effect
47 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
MONITORING OF SOIL MOSITURE on woody seedlings follows seasonal AND PLANT PERFORMANCE dynamics of water availability (Maestre et Soil moisture was measured by time al. 2003), the effects of herbaceous domain reflectometry (TDR; Topp and neighbours on soil moisture availability Davis 1985) using a Campbell TDR100 were tested considering different dry/wet system (Campbell Scientific Ltd, periods. To evaluate how the irrigation Loughborough, UK). In 10 randomly treatments and the presence of grasses selected planting holes per each of the eight affected soil moisture, the relative possible treatments combinations, 10 cm interaction index (RII; Armas et al. 2004) long TDR probes were vertically installed was calculated for each sampling date as:
(n = 80). This soil depth was chosen (TDR Nu – TDR Op )( (TDR Nu + TDR Op), because we expected the concentration of where TDR Nu and TDR Op are soil moisture most of the roots of the interacting species data obtained in Nurse and Open to be in the upper part of the soil during the microsites, respectively. To aid interpreting study period (herbs and young woody our results, RII data were grouped in seedlings should concentrate their roots in intervals with percentages in soil moisture the upper soil layers; Scholes and Archer, above and below 10% (wet and dry 1997). A strong relationship between TDR seasons, respectively). This limit values and soil gravimetric moisture has corresponds to the natural seasonal been found in the natural grassland (R 2 = dynamics in water availability; periods 0.84; P < 0.0001; Soliveres et al. unpubl. below and above 10% moisture occur data ); thus, this measurement can be mainly during summer drought and when considered as a good proxy for soil plant activity concentrates, respectively moisture availability. Soil moisture was (Schwinning and Sala 2004, Reynolds et al. measured every two months during the 2004). We randomly paired the samples by study period, starting and ending in April microsite ( Nurse vs. Open ) and between the 2007 and September 2009, respectively. As four irrigation treatments obtained with the summer drought is considered the two experiments (+0%, +25%, +50% 4x, bottleneck for plant recruitment in semiarid and +50% 2x; 10 pairs for each microsite × Mediterranean environments (Escudero et irrigation combination). Then, RII data of al. 1999), this sampling was conducted these paired samples were grouped for wet monthly during the summer (June and dry seasons separately. With these data, September). the average RII for all wet and dry seasons As the magnitude of the effect of Stipa was obtained for each of the four irrigation
48 CHAPTER 1 treatments. measuring it is important to understand its The outcome of plant plant interactions relative role in the interactions studied. varies widely depending on the Both plant growth and survival are performance measure used (Goldberg and integrative measurements that include the Novoplansky 1997, Maestre et al. 2005). effects of microsite or irrigation on plant Thus, as recommended when studying these performance during the whole year. interactions along stress gradients (Brooker Therefore, they are not appropriate to detect et al. 2008), we used several performance seasonal differences in the effect of the measurements to test the effect of assayed treatments on seedling neighbour grasses on Retama seedlings. performance. To assess for such Seedling height, root collar diameter and differences, we estimated the potential survival were measured after each summer, photochemical efficiency of Retama in September 2007, 2008 and 2009. A seedlings by measuring the maximum strong relationship between standing quantum yield of PSII (Fv/Fm) of dark biomass and root collar diameter has been adapted leaves (30 min, at midday) with a previously observed for Retama seedlings pulse modulated fluorometer (FMS2, (R 2 = 0.823, P < 0.0001; Soliveres et al. Hansatech Instruments, Norfolk, UK). This unpubl. data ), so this measure was used as parameter has been widely used as an our surrogate of seedling biomass in the indicator of plant stress in semiarid regions field. The relative growth rate (hereafter (e.g. Pugnaire et al. 1996b, Maestre et al. RGR) of Retama seedlings for each year 2003, Aragón et al. 2008); small changes in was obtained as: ln RCD 1 – ln RCD 0)/(T 1 – photochemical efficiency have been
To); being RCD 1 and RCD 0 the root collar associated with water limitations during diameter at the precedent (T 0) and current important stages of the lifecycle of woody
(T 1) sampling date, respectively. The plants in these environments (Aragón et al. slenderness coefficient, which is considered 2008), and have been found to match a good indicator of light competition results with other performance measures (Kurashige and Agrawal 2005), was also (e.g. survival) when evaluating the outcome calculated as the ratio between height and of plant plant interactions (e.g. Maestre et root collar diameter lnv H/ln RCD. Light al. 2003, 2004). Six seedlings per competition can be an important factor combination of treatments and grassland affecting plant plant interactions, even in type were randomly selected for these water limited environments (Seifan et al. measurements ( n = 48 per grassland). 2010a, Soliveres et al. 2010). Therefore, Different randomly selected plants were
49 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS measured in each sampling period, which Thus, we used multivariate analysis of took place on the same dates than TDR variance (MANOVA) to test the effects of surveys (see above). To test for differences microsite and irrigation on this variable at in the intensity of biotic interactions in each study site. These analyses were response to the treatments evaluated within conducted separately for Experiments 1 and dry or wet seasons, the RII index was 2. Slenderness coefficient data were calculated using Fv/Fm data as described squared root transformed to meet above for the TDR data. MANOVA assumptions. Damage derived from rabbit activity STATISTICAL ANALYSES (warrens and territory coverage) was an RII data (calculated from both TDR and important source of seedling death despite Fv/Fm measurements) were organized by of the grazing protection provided (see dry/wet seasons to test treatment effects results below). Thus, we separated the during seasons with contrasted rainfall survival status of Retama seedlings into availability during the year. We calculated three levels: alive, death by drought or 95% confidence intervals of this index for death by rabbit. We analyzed survival each level of irrigation amount or percentages of these seedlings separately frequency, and per each wet/dry period to for each year and study site by using a test for significant differences from zero hierarchical log linear analysis, with (which means neutral effect of the nurse on microsite and irrigation as fixed factors. To the response variable). If 95% confidence assess the effects of the factors assayed intervals did not overlap with zero or with during each year, only those seedlings that each other, we took as significant the survived the previous summer were taken differences of the RII from zero or between into account (for example, to analyze treatments, respectively. These differences survival of 2008, we only considered those were interpreted as increases (if seedlings alive after the summer of 2007). significantly higher) or decreases (if With this approach, we were able to assess significantly lower) of soil moisture or the consistency of the effect of the Fv/Fm under the canopy of the herbaceous treatments evaluated over the years. This neighbours in comparison with open areas. approach also avoids the potential Relative growth rate data obtained for “dragging” that an extremely strong effect root collar diameter and slenderness of a given treatment during a given year coefficient were correlated from one year to may have on the overall net results (e.g. if another (r > 0.375, P < 0.0001 in all cases). the +50% treatment would had strong
50 CHAPTER 1 effects in 2007, but not in the rest of years two pulses (2x treatment), a response not we could detect it with our approach; in observed in the 4x treatment (Fig. 1.2B). In contrast, taking into account survival the anthopogenic grassland, the increase in percentage from the beginning may produce water amount reduced monotonically the an overall net significant effect of this negative effect of annuals on soil moisture treatment over the study period). Survival (Fig. 1.2C). Annuals reduced soil moisture data from one year to another were not in the +0% treatment, but did not affect, or correlated (Pearson r < 0.4; P > 0.2 in all even increased, water availability the cases); thus, independency is expected. comparing to open microsites in the +25% As with growth data, separate analyses and the +50% treatments, respectively. The were performed for each experiment. latter had the same effect regardless of the Statistical analyses were conducted using frequency of watering pulses (Fig. 1.2D). SPSS 13.0 for Windows (Chicago, Illinois, These effects were consistent in both dry USA). and wet periods.
RESULTS PLANT PERFORMANCE
SOIL MOISTURE In Experiment 1, the irrigation treatments The different irrigation treatments produced modified the effect of grasses on the Fv/Fm contrasted results depending on the of Retama seedlings in a way that grassland considered. In the natural mimicked the effects of the former on soil grassland, the frequency, but not the moisture in the natural grassland (Fig. 1.3). amount, of water added modified the effect However, the amount of water applied did of Stipa on soil moisture; the opposite not affect the studied interaction in the response was found in the anthopogenic natural grassland, with the exception that grassland. In the natural grassland, Stipa Stipa effect shifted from neutral to slightly had a mostly neutral effect on soil moisture positive as water availability increased in both dry and wet periods, regardless of during wet seasons (neutral in the +0% the amount of water added (Fig. 1.2A). This treatment and slightly positive in the rest; neutral effect shifted to slightly positive Fig. 1.3A). Although the amount of water when the +50% treatment was applied in was not important affecting the outcome of
51 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
Figure 1.2 Relative effects of herbaceous nurse plants, as measured with the Relative Interaction Index (RII), on soil water availability during dry/wet seasons (periods with soil moisture above and below 10%, respectively). RII was calculated for the mean values of ten Nurse/Open pairs for each of the irrigation treatments assayed. Legend of the Experiment 1 (panels A and C) and Experiment 2 (panels B and D) treatments as follows: +0% = no irrigation, +25% = irrigation of 25% of the median of April-July, +50% = irrigation of 50% of the median of April-July in four pulses, 4x = irrigation of 50% of the median of April-July rainfall in four pulses, and 2x = irrigation of 50% of the median of April-July rainfall in two pulses. Data represent means ± 95% confidence interval ( n = 10) in the natural (A and B) and the anthropogenic (C and D) grassland, respectively. the studied interaction during dry seasons, but this treatment did not affect the studied less frequent but heavier water inputs (2x interaction during wet periods. Contrary to treatment) neutralized the negative effect of the results found in the natural grassland, Stipa on Retama found in dry periods (Fig. the 2x treatment did not affect the 1.3B). Alternatively, nurse annuals reduced interaction outcome neither in dry nor in monotonically their negative effect on wet seasons in the anthropogenic grassland Retama seedlings during dry seasons as the (Fig. 1.3D). water amount added increased (Fig 1.3C),
52 CHAPTER 1
Figure 1.3. Relative effects of herbaceous nurse plants, as measured with the Relative Interaction Index (RII), on seedling photochemical efficiency during dry/wet seasons (periods with soil moisture above and below 10%, respectively). RII was calculated for the mean values of six Nurse/Open pairs for each of the irrigation treatments assayed. Data represent means ± 95% confidence interval ( n = 6) in the natural (A and B) and the anthropogenic (C and D) grassland, respectively. Rest of legend as in Fig. 1.2.
Neither microsite nor irrigation natural grassland, and was negatively treatments affected the growth rate of affected by the presence of annuals
Retama in the natural grassland, which was (MANOVA Pillai´s Trace: F 2,53 = 4.6; P = almost nill in all the cases (Table 1.2; see 0.014). According to the results found with detailed statistics in Appendix A in the Fv/Fm measurements, increases in Supplementary Material). The 2x treatment, water availability (+50% treatment) but not the rest, slightly decreased the neutralized this negative effect of annuals, slenderness coefficient of Retama seedlings regardless of the frequency of its (Table 1.3). This trend was constant for the application. The slenderness coefficient was three years of study, but was significant no affected neither by microsite nor by any only in 2007 (F 3,53 = 3.63; P = 0.019). The of the irrigation treatments in the growth rate of Retama was much higher in anthropogenic grassland. the anthropogenic grassland than in the
53 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
Table 1.2. Relative growth rate (cm · cm -1 · year -1) of root collar diameter (RGR) of Retama sphaerocarpa seedlings in the different experiments and study sites. Values are means ± SE (n = 4-16, depending on the treatment and the sampling period). Open = areas without perennial vegetation, Nurse = areas under the canopy of annual plants (anthropogenic grassland) or Stipa tenacissima (natural grassland), +0% = unwatered seedlings, +25% = irrigation of 25% of the median of April-July rainfall in four pulses, 4X = irrigation of 50% of the median of April-July rainfall in four pulses, and 2X = irrigation of 50% of the median of April-July rainfall in two pulses. Different letters or asterisks indicate significant differences (MANOVA test; P < 0.05) between microsites or among irrigation treatments, respectively. See Appendix A in Supplementary Information for detailed statistical results.
Experiment 1: Amount treatment
Natural grassland Anthropogenic grassland Microsite Irrigation 2007 2008 2008 2009 2007 2008 2008 2009
a Open +0% 0.00 ± 0.02 0.02 ± 0.01 1.37 ± 0.13 1.66 ± 0.13
+25% 0.06 ± 0.01 0.00 ± 0.01 1.54 ± 0.08 1.83 ± 0.06 a
+50% 0.05 ± 0.01 0.00 ± 0.01 1.40 ± 0.08 1.63 ± 0.08 a
+0% 0.00 ± 0.02 0.01 ± 0.01 1.40 ± 0.09 1.70 ± 0.11 b Nurse +25% 0.02 ± 0.01 0.00 ± 0.01 1.59 ± 0.13 1.56 ± 0.12 b
+50% 0.03 ± 0.01 0.00 ± 0.01 1.56 ± 0.22 1.75 ± 0.13 b
Experiment 2: Frequency treatment
4X 0.05 ± 0.01 a 0.00 ± 0.01 1.40 ± 0.08 1.63 ± 0.08 Open 2X 0.04 ± 0.01 a 0.01 ± 0.02 1.41 ± 0.11 1.66 ± 0.11
4X 0.03 ± 0.01 b 0.00 ± 0.01 1.56 ± 0.22 1.75 ± 0.13 Nurse 2X 0.00 ± 0.01 b 0.00 ± 0.02 1.46 ± 0.09 1.60 ± 0.08
The presence of grasses reduced the negative effect of grasses on the ability of survival of Retama in the two grasslands Retama seedlings to resist summer drought studied during 2007 and 2008, a negative in 2007, but a positive effect was detected effect that disappeared in 2009 (Table 1.4, by the protection against rabbit damage see also Appendix B in Supplementary during this year, resulting in a net neutral Material for detailed statistical results). In effect (see Retama seedlings death by the anthropogenic grassland, we found a drought or by rabbits in Table 1.4).
54 CHAPTER 1
Table 1.3. Slenderness coefficient (unitless) of Retama sphaerocarpa seedlings in the different experiments and study sites. Values are means ± SE ( n = 4-16, depending on the treatment and the sampling period). Rest of legend as in Table 1.2
Experiment 1: Amount treatment
Natural grassland Anthropogenic grassland Microsite Irrigation 2007 2008 2009 2007 2008 2009
Open +0% 2.4 ± 0.3 2.2 ± 0.2 1.8 ± 0.1 2.7 ± 0.2 2.2 ± 0.1 1.7 ± 0.1
+25% 3.2 ± 0.2 2.2 ± 0.2 2 ± 0.2 3.5 ± 0.7 2.1 ± 0.2 1.8 ± 0.1
+50% 3.4 ± 0.4 2 ± 0.2 2 ± 0.1 4 ± 0.5 2.5 ± 0.2 1.6 ± 0.1
+0% 2.9 ± 0.6 3 ± 0.5 2.5 ± 0.5 2.7 ± 0.2 2.2 ± 0.1 1.7 ± 0.1 Nurse +25% 2.9 ± 0.2 2.4 ± 0.2 2.3 ± 0.2 3.1 ± 0.3 2.2 ± 0.2 2 ± 0.1
+50% 3.7 ± 0.5 2.7 ± 0.4 2.4 ± 0.2 3.4 ± 0.4 2.4 ± 0.2 1.9 ± 0.1
Experiment 2: Frequency treatment
4X 3.4 ± 0.4 2 ± 0.2 2 ± 0.1 4 ± 0.5 2.5 ± 0.2 1.6 ± 0.1 Open 2X 2.4 ± 0.2 * 1.9 ± 0.1 1.9 ± 0.2 4.1 ± 0.5 2.6 ± 0.2 1.7 ± 0.1
4X 3.7 ± 0.5 2.7 ± 0.4 2.4 ± 0.2 3.4 ± 0.4 2.4 ± 0.2 1.9 ± 0.1 Nurse 2X 2.3 ± 0* 2.2 ± 0.4 2.1 ± 0.2 3.7 ± 0.3 2.7 ± 0.1 2.4 ± 0.2
These negative effects were independent of on the survival of this species disappeared the irrigation treatments, with the exception in the +50% treatment (Table 1.4, of Experiment 1 in the anthropogenic Appendix B). Different irrigation grassland in 2008. During this year, the frequencies did not affect the survival of survival of Retama monotonically increased Retama seedlings neither in the natural nor with water availability (+0% < +25% < in the anthropogenic grassland. +50%), and the negative effects of annuals
55 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
Table 1.4. Percentage of Retama sphaerocarpa seedlings death by drought or by rabbit (separated by /) during the three years of study in the different experiments and study sites. Percentage were calculated taking as 100% those seedlings which had survived after the summer of the previous year. Initial n was 22 for each combination of treatments. Different letters or asterisks indicate significant differences (Log-linear test; P < 0.05) between microsites or among irrigation levels within each experiment, respectively. See Appendix B in Supplementary Information for detailed statistical results. Rest of legend as in Table 1.2.
Amount treatment
Natural grassland Anthropogenic grassland Microsite Irrigation 2007 2008 2009 2007 2008 2009
a a a Open +0% 4 / 0 10 / 3 33 / 3 0 / 12 12 / 12 33 / 15
+25% 4 / 8 18 / 0 a 33 / 0 0 / 9 a 10 / 19 a 38 / 8
+50% 0 / 4 21 / 0 a 44 / 0 0 / 13 a 4 / 13 a* 13 / 13
+0% 13 / 0 60 / 0 b 75 / 0 8 / 0 b 30 / 13 b 52 / 11 Nurse +25% 8 / 0 50 / 0 b 75 / 0 9 / 4 b 30 / 22 b 40 / 20
+50% 0 / 0 53 / 11 b 63 / 11 10 / 0 b 19 / 0 b* 38 / 5
Frequency treatment
4X 0 / 4 21 / 0 a 44 / 0 0 / 13 a 4 / 13 13 / 13 Open 2X 0 / 0 19 / 5 a 40 / 15 0 / 16 a 0 / 21 20 / 24
4X 0 / 0 53 / 11 b 63 / 11 10/ 0 b 19 / 0 38 / 5 Nurse 2X 17 / 4 53 / 5 b 74 / 5 12 / 4 b 21 / 4 55 / 3
DISCUSSION natural grassland, maybe due to the low
WATER STRESS INCREASES THE growth rates found in this ecosystem INTENSITY OF GRASS SHRUB regardless of the treatment applied. The COMPETITION negative effect of annuals found in the According to our first hypothesis, we found anthropogenic grassland seems to be mainly a negative effect of both Stipa and annuals caused by competition by water, an effect on the growth of Retama seedlings that increased with water stress. According (Goldberg and Novoplansky 1997). to previous studies (Knoop and Walker However, this effect was almost nill in the 1985, Davis et al. 1999, Maestre and
56 CHAPTER 1
Cortina 2004a), the highest competition our results do not fully support this intensities were found under the higher recommendation because of the inexistence water stress levels (both summer drought of positive effects of these herbaceous and non watered treatments in the plants during the entire study period (see Experiment 1), a response that contradicts also McDonald 1986, Eliason and Allen predictions of the SGH (Bertness and 1997). Interestingly, when considering the Callaway 1994). Both Stipa and the annuals impact of rabbit activity, which was negatively affected the growth, stress level considerable in the anthropogenic and survival of Retama seedlings. These grassland, the negative effect of annuals on results partially reject our second the ability of seedlings to overcome hypothesis, based on the model proposed by summer drought was compensated by the Goldberg and Novoplansky (1997), because protective role of these annuals (see Retama herbaceous neighbours reduced shrub seedlings death by drought/rabbit in Table survival and did not show any positive 1.4). This result illustrates how the effects effect during dry periods (Figs. 1.2 and that multiple stressors have on a particular 1.3). Also, and in contrast with our second nurse protégée interaction is a crucial factor hypothesis, this effect remained equal affecting the potential of this particular regardless of the water amount added in the nurse to have positive, neutral or negative natural grassland, but was more negative in effects on the protégée depending on the the anthropogenic grassland as water stress particular environment where this increased (see results of Experiment 1). The interaction occur (Smit et al. 2009, most plausible explanation for these results Soliveres et al. in press ). is that the negative effects of both Stipa and annuals on the stress experienced by DIFFERENT NURSE GRASSES HAVE Retama seedlings during wet periods UNEVEN EFFECTS ON RETAMA reduced growth and resource capture, SEEDLINGS compromising survival during summer Competition between Retama and annuals regardless of the environmental stress was clearly driven by water competition, experienced during this season. and therefore increases in soil moisture Ruderal plants have been suggested as reduced the negative effect of these species. possible nurse plants in degraded areas, However, the effects of Stipa on soil where other nurse plants are absent, and its moisture (neutral or positive) did not fully potential use as a restoration tool has been match those on seedling performance suggested (Brooker et al. 2008). However, (survival reduction and increased stress),
57 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS suggesting that competition by factors other availability (Malkinson and Tielbörger than water were also important drivers of 2010). This trade off should be taken into the final outcome of the interaction studied. account when studying specific plant plant The shade intolerance of Retama interactions along stress gradients because (Valladares and Pugnaire 1999, Valladares it will define the final outcome of a given et al. 2003), together with the trend to interaction and how it changes across increase slenderness coefficient underneath environmental gradients (Holmgren et al. Stipa canopy, seems to point to light 1997, Prider and Facelli 2004, Malkinson competition as a key factor defining the and Tielbörger 2010). outcome of the studied interaction in the natural, but not in the anthropogenic, CHANGES IN RAINFALL grassland, where Stipa canopies could FREQUENCY, HERBACEOUS shade Retama seedlings enough to limit PHENOLOGY AND POTENTIAL FOR carbon gain (Davis et al. 1999, Soliveres et NICHE SEGREGATION al. 2010, Seifan et al. 2010a). Light Niche segregation is among the most competition could explain the contrasting important factors fostering coexistence in results found between both grassland types, semiarid environments (Fowler 1986, Sala where a lack of influence of water amount et al. 1989, Scholes and Archer 1997). in the natural, but not in the anthropogenic Despite that our study only lasted three grassland was found. Our findings, and years, it seems enough time for Retama those from previous studies (Prider and seedlings to avoid competition by grasses, Facelli 2004, Seifan et al. 2010a), point to as demonstrated by the lack of effect of the existence of a trade off between the nurse herbs on Retama survival during shade and drought tolerances of the 2009 at both study sites. Retama seedlings protégée plant and how nurse plants affect are able to reach deep soil layers soon after water and light supply for their protégées. its establishment (Padilla and Pugnaire For example, although nurses may exert a 2007), and thus it is likely that they were positive effect on the availability of one able to reach deeper soil profiles than those resource (i.e. water), the overall effect of a achieved by its herbaceous neighbours in nurse on a particular target will be negative three years. These results agree with if shade provided by this nurse is deeper previous studies with other species (Brown than the physiological limits of this and Archer 1990), which found a high particular protégée plant can withstand, ability of woody seedlings to reach soil regardless of its positive effect on water
58 CHAPTER 1 resource partitioning with grasses very nurses caused it (Gómez Aparicio 2009). In early in their life cycle. the anthropogenic grassland more water Contrary to our expectations (Ogle and pulses (those of spring and early summer) Reynolds 2004, Knapp et al. 2008) and in the 4x than in the 2x treatment increased despite of the existence of niche the amount of water available for seedlings segregation described above, the assayed when the annual nurses were active. This differences in the frequency of heavy increase in water availability might storms (2x vs. 4x treatment in Experiment compensate competition by water between 2) did not increase seedling survival when annuals and Retama seedlings, as growing with grasses in any of the studied demonstrated by the significant reduction of sites. However, taking into account other negative effects on survival, growth or measurements (soil moisture and Fv/Fm), stress found. On the other hand, in the 2x the two assayed frequencies had differential treatment one of the two irrigation pulses effects depending on the site considered. was applied during summer, when most While more frequent water inputs (4x ruderal nurses were death. Therefore, treatment) promoted higher soil moisture negative effects of annuals on Retama and shrub performance in the anthropogenic seedlings were less important when the grassland, less frequent but heavier water plant received this irrigation, resulting in a inputs (2x treatment) had the same effects less effective compensation of water in the natural one. Following the inverse competition when compared to the same soil texture hypothesis proposed by Noy amount of water applied more frequently. Meir (1973), this could be caused by In contrast, Stipa is not only perennial and differences in soil depth between both therefore competitive during the entire year, grasslands, with deeper soils (i.e. the but also highly efficient taking water from natural grassland) allowing niche short and light rainfall inputs, even during segregation and shallow soils (i.e. summer (Pugnaire et al. 1996b, Balaguer et anthropogenic grassland) preventing it. al. 2002). Thus, the 4x treatment more However, both soil types had similar likely benefited Stipa than reduced geological basis and thus it is likely that competition between this species and both had similar textures and depths. Thus, Retama seedlings in the natural grassland. the most plausible explanation for this However, the less frequent but heavier differential response between grassland water pulses applied in the 2x treatment types is that differences on the life strategy could reach deeper soil profiles, where (annuals vs. perennials) of the herbaceous Stipa is not able to take water, and therefore
59 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS may enhance niche segregation, increasing within the same site, avoiding site to site shrub performance (Fv/Fm results; see also confounding factors, and with more than Sala et al. 1989, Schwinning and Ehleringer two points along stress gradients driven by 2001, Ogle and Reynolds 2004). In spite of water availability. We did so in two this competition was importantly affected contrasting ecosystems with different by light (see discussion above), an herbaceous potential nurses, and following improvement in water status could increase a four point realistic water stress gradient, the ability of Retama to compete for light derived from predictions for future climate (Fahey et al. 1998), as demonstrated by the change scenarios for the study areas, within significant increase in the slenderness each of the three study years. Our results coefficient and Fv/Fm observed in the 2x suggest that the expected increase in water treatment. Unfortunately, we did not stress under climate change will reduce measure root structural traits, but the shrub recruitment and performance in extremely low shoot growth rates of semiarid grasslands, but these effects will Retama seedlings found in this ecosystem, depend on the specific species involved and compared with those observed in the the suggested trade off between anthropogenic grassland (Table 1.2), shade/drought tolerances of protégée and suggests a major investment in root growth nurse effects on light and water availability. to promote this niche segregation. The However, the increase in the frequency of differential responses to different water heavy rains may counteract this effect by availabilities and frequencies found enhancing niche segregation among depending on the life strategy of the coexisting plants (Knapp et al. 2008), an herbaceous plants could help to reconcile effect that will be mediated by the life contrasting results observed in the strategy of the nurses involved. The results literature, which support or reject niche presented here challenge current predictions segregation between woody plants and of plant plant interactions in response to the grasses. ongoing climate change in Mediterranean ecosystems (Brooker 2006), and therefore CONCLUDING REMARKS raise caution on current generalizations on Despite the plethora of studies devoted to how grass shrub interactions will respond test facilitation/competition shifts along to climate change. stress gradients (see Callaway 2007 for a ACKNOWLEDGEMENTS review), to our knowledge none of them We thank Matthew Bowker for revising the English have experimentally tested these shifts of this manuscript. A.P. Castillo Monroy, M.
60 CHAPTER 1
Carpio, E. Pigem, C. Alcalá, P. Alonso, R. Milla, L. REMEDINAL2, INTERCAMBIO and EFITAL Gimenez and J. Margalet for their help during [B007/2007/3 10.2] projects, the latter funded by the fieldwork. We thank the Instituto Madrileño de Ministerio de Ciencia e Innovación (MICINN). FTM Investigación y Desarrollo Rural, Agrario y acknowledges support from the European Research Alimentario (IMIDRA) and CINTRA S.A. for Council under the European Community's Seventh allowing us to work in their sites. SS and PGP hold Framework Programme [(FP7/2007 2013)/ERC PhD fellowships from the EXPERTAL project, Grant agreement n° 242658]. funded by Fundación Biodiversidad and CINTRA S.A. This work was supported by the EXPERTAL,
61 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
Supplementary Material for Chapter 1.
Appendix A. Detailed statistical results of the MANOVA perfomed with growth rates and slenderness coefficients.
Statistical results of the MANOVA perfomed with growth rate and slenderness coefficient data in the natural (A, B; separate analyses for each variable) and the anthropogenic (C, D; separate analyses for each variable) grasslands. Significant ( P < 0.05) or marginally significant (0.05 < P < 0.1) are highlighted in bold and italics, respectively. RGR = relative annual growth of root collar diameter; SC = slenderness coefficient.
Table S1. MANOVA results showing the overall effect of the factors assayed (microsite and irrigation) on the 5 variables tested (RGR 2007-08 and 2008-09, and SC for 2007, 2008 and 2009) in the natural grassland. This analysis was performed separately for Experiments 1 (Amount treatment) and 2 (Frequency treatment).
Experiment 1: Amount treatment Factor Pillai´s trace F df P value Microsite (M) 0.574 4.859 5,18 0.005 Irrigation (I) 0.394 0.933 10,38 0.515 M x I 0.192 0.404 10,38 0.937 Experiment 2: Frecuency treatment Microsite (M) 0.386 2.518 5,20 0.063 Irrigation (I) 0.402 2.686 5,20 0.052 M x I 0.115 0.520 5,20 0.758
Table S2. Results from separate ANOVA analyses for each variable in the natural grassland. Analyses were conducted separately for Experiments 1 and 2 (Amount and Frequency treatments, respectively).
Experiment 1: Amount treatment Dependent Microsite (M) Irrigation (I) M x I variable F df P F df P F df P RGR 2007 08 3.9 1,42 0.06 0.4 2,42 0.66 0.1 2,42 0.91 RGR 2008 09 1.6 1,42 0.22 1.1 2,42 0.35 0.3 2,42 0.73 SC 2007 1.9 1,42 0.19 1.8 2,42 0.18 0.2 2,42 0.79 SC 2008 5.0 1,42 0.04 0.6 2,42 0.56 0.4 2,42 0.69 SC 2009 3.3 1,42 0.08 0.6 2,42 0.55 0.2 2,42 0.80 Experiment 2: Frecuency treatment RGR 2007 08 7.6 1,24 0.01 2.6 1,24 0.12 0.2 1,24 0.65 RGR 2008 09 0.5 1,24 0.48 0.9 1,24 0.77 0.0 1,24 0.93 SC 2007 0.7 1,24 0.80 9.1 1,24 0.01 0.5 1,24 0.48 SC 2008 3.4 1,24 0.08 1.8 1,24 0.20 0.5 1,24 0.49 SC 2009 2.9 1,24 0.1 0.9 1,24 0.36 0.5 1,24 0.48
62 CHAPTER 1
Table S3. MANOVA results showing the overall effect of the factors assayed (microsite and irrigation) on the 5 variables tested (RGR 2007-08 and 2008-09, and SC for 2007, 2008 and 2009) in the anthropogenic grassland. This analysis was performed separately for Experiments 1 (Amount treatment) and 2 (Frequency treatment).
Experiment 1: Amount treatment Hypothesis/error Factor Pillai´s trace F P value df Microsite (M) 0.286 5.056 5,63 0.001 Irrigation (I) 0.238 1.731 10,128 0.081 M x I 0.054 0.358 10,128 0.962 Experiment 2: Frecuency treatment Microsite (M) 0.341 4.653 5,45 0.002 Irrigation (I) 0.085 0.839 5,45 0.529 M x I 0.045 0.424 5,45 0.829
Table S4. Results from separate ANOVA analyses for each variable in the anthropogenic grassland. Analyses were conducted separately for Experiments 1 and 2 (Amount and Frequency treatments, respectively).
Experiment 1: Amount treatment Dependent Microsite (M) Irrigation (I) M x I variable F df P F df P F df P RGR 2007 08 3.3 1,67 0.07 0.3 2,67 0.73 0.0 2,67 0.97 RGR 2008 09 5.3 1,67 0.03 0.3 2,67 0.76 0.8 2,67 0.48 SC 2007 0.6 1,67 0.44 3.0 2,67 0.06 0.3 2,67 0.76 SC 2008 0.0 1,67 0.95 1.2 2,67 0.30 0.1 2,67 0.94 SC 2009 0.17 1,67 0.70 0.2 2,67 0.78 0.6 2,67 0.54 Experiment 2: Frecuency treatment RGR 2007 08 3.4 1,49 0.07 2.1 1,49 0.16 0.3 1,49 0.56 RGR 2008 09 3.4 1,49 0.07 3.7 1,49 0.06 1.8 1,49 0.19 SC 2007 1.0 1,49 0.31 0.4 1,49 0.55 0.1 1,49 0.80 SC 2008 0.7 1,49 0.79 1.0 1,49 0.33 0.2 1,49 0.70 SC 2009 0.3 1,49 0.62 2.7 1,49 0.10 1.6 1,49 0.22
63 CLIMATE CHANGE AFFECTS PLANT INTERACTIONS
Appendix B: Detailed statistical results of the log linear analyses performed with survival frequencies.
Hierarchical log linear results for the different models for both study sites and for each year of study (2007 2009). Table S5 shows the results of the analyses conducted with the three amount treatments evaluated (+0%, +25% and +50%; Experiment 1), without considering the frequency levels. Table S6 shows the results of the analyses conducted with the two frequency treatments evaluated (2x and 4x; Experiment 2), without introducing the amount levels. P-values < 0.05 are shown in bold Table S5
Anthropogenic grassland Natural grassland Factor df 2007 2008 2009 2007 2008 2009 G P G P G P G P G P G P
Microsite 2 14.5 0.0007 6.9 0.031 0.54 0.763 5.6 0.062 23.6 >0.001 2 0.365 Irrigation 6 0.06 0.999 11.9 0.018 2.4 0.655 8.8 0.065 1.6 0.813 0.1 0.999
Table S6
Anthropogenic grassland Natural grassland Factor df 2007 2008 2009 2007 2008 2009 G P G P G P G P G P G P
Microsite 2 12 0.0024 3.5 0.174 1.8 0.410 5.9 0.052 12.9 0.002 2.3 0.314 Irrigation 6 0.5 0.778 1.7 0.434 2.7 0.253 5.7 0.057 0.4 0.816 3.4 0.186
MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
Spatio-temporal heterogeneity in abiotic factors modulate multiple ontogenetic shifts between competition and facilitation 2
Santiago Soliveres, Lucía DeSoto, Fernando.T. Maestre and José Miguel Olano Manuscrito publicado en: Perspectives in Plant Ecology, Evolution and Systematics 12: 227-234.
MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
66 CHAPTER 2
ABSTRACT
Plant plant interactions are largely influenced by both environmental stress and ontogeny. Despite the effects of each of these factors on the overall outcome of these interactions has received considerable attention during the last years, the joint effects of both factors as drivers of such outcome are poorly understood. We used the combination of spatial pattern analysis, fruit production surveys, carbohydrate assays, sowing experiments and dendrochronological techniques to explore the interaction between Stipa tenacissima (nurse) and Lepidium subulatum (protégée) in two different slope aspects. This battery of techniques allows us to study the effects of the nurse plant during the whole life cycle of the protégée, and to assess the role of spatio temporal variability in abiotic stress as a modulator of ontogenetic shifts in plant plant interactions. Spatial pattern analyses suggested a net facilitative effect of S. tenacissima on L. subulatum . This effect was particularly important during the germination, shifting to competition (growth reduction) early after establishment. Competition was gradually reduced as the shrub aged, suggesting niche differentiation. The magnitude of competition was reduced under low rainfall levels in south facing slopes, whereas this response was observed due to other abiotic factors in north facing slopes. Our results highlight the crucial effect that positive interactions at early life stages have to determine the long term outcome of a given plant plant interaction, and the existence of multiple shifts between facilitation and competition along different life stages of the protégée. They also show how these ontogenetic shifts are modulated by abiotic factors, which differ among slope aspects. These findings may help to refine conceptual and theoretical models about shifts between facilitation and ontogeny under current climate change scenarios.
67 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
INTRODUCTION 2007).
he analysis of the spatio temporal The relationship between abiotic variation of facilitative and stress and the final outcome of plant plant competitive interactions along interactions is further complicated by the T ontogenetic changes that plants experience abiotic stress gradients has become a major research topic in community ecology throughout their life cycle, which can during the last two decades (Kikvidze strongly modulate facilitation/competition 1996, Maestre and Cortina 2004a, shifts (Miriti 2006, Schiffers and Kikvidze et al. 2006, Brooker et al. 2008). Tielbörger 2006, Armas and Pugnaire In arid and semiarid areas, such variations 2009). Short term studies, which form the are particularly important, as water, which core of facilitation/competition research is the most limiting factor, shows a strong (see Callaway 2007 for a review), are spatio temporal variability (Whitford 2002, insufficient to fully understand the Holmgren et al. 2006). These environments magnitude of ontogenetic shifts in plant are characterized by a high inter annual plant interactions, but long term studies are variability in rainfall distribution, and as a often logistically prohibitive because of result, plant recruitment is limited to economic and temporal constraints. Some particularly rainy years (Holmgren et al. studies have overcome these limitations by 2006). Furthermore, water availability also using annual plants (Schiffers and experiences a strong spatial variation Tielbörger 2006), or by sampling specific between slope aspects: radiation and temporal windows of the plant life cycle temperatures, and thus water stress, are (Armas and Pugnaire 2005, 2009, Miriti higher in south facing slopes, while in 2006, Valiente Banuet and Verdú 2008). north facing slopes water stress and These approaches in isolation are evapotranspiration are lower (Friedman et insufficient to test ontogenetically driven al. 1977, Bellot et al. 2004, Aragón et al. facilitation/competition shifts along the 2007, Pueyo and Alados 2007). These whole plant life, particularly in long lived spatio temporal changes in water perennial plants, and to assess the effects availability have been pointed as a major of spatio temporal changes in abiotic stress factor defining the final outcome of plant on such ontogenetic shifts. These problems plant interactions in drylands (Tielbörger can be circumvented using and Kadmon 2000a, Pugnaire and Luque dendrochronological techniques, assigning 2001, Gómez Aparicio et al. 2004, Miriti annual rings to calendar years (Schweingruber 1988). Since xylem acts as
68 CHAPTER 2
conductive area for water and nutrients tussock grass Stipa tenacissima L. within a plant (e.g. Dyer and Bailey 1987, (Poaceae; the nurse plant) and the shrub Bascietto and Scarascia Mugnozza 2004), Lepidium subulatum L. (Brassicaceae; the this technique can reconstruct investment protégée plant) in two slope aspects (north in secondary growth along plant life, and and south) with contrasting abiotic stress therefore, act as a measurement of plant environments. This combination of performance in each year during its whole approaches provides us with a continuous life. set of data, suitable for testing the presence Although it is known that the of ontogenetic facilitation/competition outcome of plant plant interactions may be shifts throughout the entire life cycle of the affected by the interaction between abiotic protégée. Furthermore, we aimed to assess stress and the ontogeny of the target the role of spatio temporal changes in species (Goldberg et al. 2001), there is a abiotic stress (differences between abiotic lack of studies evaluating the simultaneous factors controlling plant growth and effects of abiotic stress, both in space and survival among slope aspects, and in time, and ontogeny as drivers of on the differences between water availability outcome of plant plant interactions (but see among years) as a modulator of these Schiffers and Tielbörger 2006; Sthultz et shifts. We tested the following hypotheses: al. 2007). Improving our understanding on (i) the germination and survival of L. the interacting effects of these factors will subulatum seeds and seedlings will be allow us to further refine current higher under S. tenacissima than in conceptual and mathematical models adjacent bare ground zones because of the aiming to predict how plant plant improvement of environmental conditions interactions change along stress gradients under the canopy of this nurse plant (Michalet 2007), and to increase the (Maestre et al. 2001, 2003, Barberá et al. precision of our estimates about how plant 2006); (ii) the outcome of the interaction individuals and communities will respond will shift from facilitation to competition to ongoing climate change (Brooker 2006). with shrub age, resulting in less growth In this study, we combine spatial pattern and fruit production of L. subulatum when analyses, sowing experiments, growing under the canopy of S. dendrochronological and reproductive tenacissima (Miriti 2006); (iii) given that surveys, and carbohydrate assays to both S. tenacissima and L. subulatum are explore the relationship between the primarily stress tolerant species (Pugnaire
69 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS et al., 1996b, Palacio et al. 2007), and that range from 0.1% to 10%, with high water deficit (a resource related stress) is survivorship linked to especially the main limiting factor, we expect to find favourable years (Escudero et al. 2000, facilitative interactions mainly under J.M. Olano, unpubl. data ). Annual survival moderate abiotic stress levels, (Maestre et rates increase sharply afterwards, reaching al. 2009a). This will happen because the 71–95% for adults, depending mainly on positive effect of microclimatic autumn and spring conditions. amelioration is limited after a threshold Flowering starts at 2 4 years (M. under high levels of abiotic stress, where Eugenio, pers. com.). Primary growth competition, mainly for water, overcomes occurs in two pulses, from mid February to the positive effect of this amelioration and June, and from September to November, competition arises again (Maestre and respectively (Palacio and Montserrat Martí Cortina 2004a); and (iv) the magnitude of 2005, Palacio et al. 2007). Secondary facilitation and competition is modulated growth also occurs in spring. Flowering by spatio temporal changes in climatic and fruiting stages last from April to June. conditions. A detailed description on the natural history of S. tenacissima and the grasslands
METHODS it forms is given in Maestre et al. (2009b).
TARGET SPECIES STUDY AREA Lepidium subulatum is a dwarf summer Three sites were selected in central Spain deciduous shrub linked to gypsum for this study: Aranjuez (40º10´30´´N, 31º outcrops. It is distributed along the 54´09´´W; 545 m.a.s.l.); Tielmes (40º Western Mediterranean where it coexists 12´40´´N, 31º25´02´´W; 595 m.a.s.l.); and with S. tenacissima . Seeds are small, Noblejas (40º10´03´´N, 31º37´01´´W; 526 exhibiting atelechory (Escudero et al. m.a.s.l.). Their climate is Mediterranean 2000) and forming a small permanent seed semiarid, with average annual precipitation bank (Caballero et al. 2008). Emergence of 388 mm, characterized by a high inter concentrates in winter, but spans to June, annual variability and a characteristic with densities ranging from 19 to 700 strong summer drought. Mean annual seedlings m 2 (Escudero et al. 2000, J.M. temperature is 14.6 ºC, ranking from 25 ºC Olano, unpubl. data ). Plant recruitment in July to 5.6 ºC in January (Data from bottlenecks occur during the first summer National Meteorological Service, 1994– after germination, when survival rates 2005. Marqués et al. 2008). The three sites
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were located on gypsum rich soils, slopes (e.g. Friedman et al. 1977, classified as Typic Gypsiorthid (Tielmes Sternberg and Shoshany 2001, Bellot et al. and Noblejas) and Xeric Haplogypsid 2004; Aragón et al. 2008, Pueyo and (Aranjuez; Soil Survey Staff 1994). Alados 2007). Differences in perennial Vegetation was in all cases an open steppe cover between slope aspects were dominated by S. tenacissima , and particularly evident in the Aranjuez site contained shrub species like L. subulatum , (Appendix C in Supplementary Material), Retama sphaerocarpa (L.) Boiss . and so this site was selected to carry out the Helianthemum squamatum (L.) Dum. bulk of the fieldwork in this study. Cours . Perennial plant cover is below 45% in all cases. OBSERVATIONAL MEASUREMENTS In April 2008, five 25 m × 4 m transects EXPERIMENTAL DESIGN were randomly established in each of the At each site, experimental plots in north experimental plots (30 transects in total). and south aspect slopes were established, Every L. subulatum individual found along with slopes varying between 13º and 22º. the transect band was registered. Those Perennial cover was different depending on individuals located at distances shorter the slope aspect in all the studied areas: than 20 cm and larger than 50 cm from the 31% vs. 33%; 24% vs. 42%; and 32% vs. edge of a S. tenacissima tussock were 35% for south vs. north aspect slopes in considered as growing in association with Tielmes, Aranjuez and Noblejas, S. tenacissima and in isolation, respectively. Since cover can be a good respectively. These situations are hereafter surrogate of productivity in ecosystems called Tussock and Open microsites, such as those studied (Flombaum and Sala respectively. This distance has been used 2009), and productivity is a good proxy for as separation between microsites in other abiotic stress at the level of entire plant studies with S. tenacissima , detecting communities (Lortie and Callaway 2006), significant differences in both biotic and we assume that these differences are abiotic features between Tussock and Open related to higher levels of abiotic stress in microsites (e.g. Maestre et al. 2001, 2003, the south than in the north facing slopes. 2009b). L. subulatum individuals growing This agrees with many studies conducted at distances among 20–50 cm from the in arid and semiarid areas showing higher edge of a S. tenacissima tussock were not abiotic stress in south vs. north aspect considered for further analyses.
71 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
SOWING EXPERIMENT in Open sites, sapling survival data In October 2007, a seed germination analyses cannot be provided. experiment was conducted in the Aranjuez site. It was designed as a fully factorial DENDROCHRONOLOGICAL experiment with two treatments: slope SURVEYS aspect (north vs. south) and microsite In June 2007, adult individuals of L. (open areas devoid of vascular vegetation, subulatum were randomly selected in the north and south face of S. tenacissima Aranjuez site for dendrochronological tussocks). Ten replicates were established measurements. These individuals were per treatment combination (each consisting chosen among those naturally growing in a 25 cm × 25 cm plot), and 75 under four different conditions, resulting commercial seeds of L. subulatum were from the combination of two microsites seeded in each replicate (25 holes, 3 seeds (Tussock vs. Open ) and slope aspects per hole). We chose this approach over the (north vs. south); 16 individuals were alternative neighbor removal approach, selected for each combination (64 in total). because neighbor removal does not erase After harvesting, a section of the stem the facilitative legacy effects of a nurse including the root collar was selected to plant upon soil infiltration and fertility. measure the annual growth ring widths as Seeds were buried at 0.5 cm to avoid ant an indicator of plant growth over the depredation, irrigated with 40 ml of water course of its life. Annual rings were dated and protected from rabbits (Oryctolagus and measured following standard cuniculus L.) by using a metallic mesh that denchronological techniques as detailed in did not shade the seeding site. A Appendix D in Supplementary Material. A germination test conducted under section of the main root of the same plants controlled conditions revealed that the total was also collected to measure the content germination rate of the pool of seeds of non structural carbohydrates using the employed was 89% after one month in a anthrone method (see Olano et al. 2006 for growth chamber (16 light hours at 20ºC a full account of the methodology). Two and 8 dark hours at 10ºC). Seed emergence different fractions of non structural and seedling survival were monitored carbohydrates were measured in this study: monthly until July 2008, when all nonsoluble and soluble carbohydrates. In germinated seedlings died during the L. subulatum , non soluble carbohydrates summer drought. Because of this extreme are used to overcome respiration rates in mortality event and the lack of germination the leafless plant during summer drought
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(Palacio et al. 2007). Therefore, low of two slope aspects (north vs. south) and contents in non soluble carbohydrates may microsites (Tussock vs. Open ) were compromise the ability of this species to randomly selected in the Aranjuez site. Ten survive this critical moment. We interpret infructescences per plant were randomly differences in this variable between chosen, and the number of fruits in each microsites or slope aspects as differences infructescence was registered. The canopy in the ability of L. subulatum to respond to area of each sampled individual was summer drought stress. On the other hand, calculated using the ellipse formula with soluble carbohydrates provide a surplus of the diameters parallel and perpendicular to sugars that can be stored for use under slope. This measurement was introduced in favourable conditions (Chapin et al. 1990), the analysis as covariate to control for and that are susceptible to be immediately plant size. allocated to functions such as growth. Thus, higher contents of soluble STATISTICAL ANALYSES carbohydrates in a given combination of The frequency of naturally occurring L. microsite/slope aspect may indicate that subulatum individuals in the surveyed plots the plant experiences more benign was analyzed by using a Chi square conditions there. Both soluble and non goodness of fit test. Our null hypothesis soluble carbohydrates inform us about the was that L. subulatum individuals have a status of the reserves of the plant, and thus random spatial pattern (depending directly are an integrative measurement of plant on the cover of each microsite). Data were performance during the whole year. These tested for independence in 6 separate one variables were measured in June, just way tables (resulting from each before summer drought, and in the main combination of site and slope aspect) root because this organ and date match including only the microsite factor with the maximum starch content organ (Tussock vs. Open ). A joint analysis that and period of the year for L. subulatum, would permit testing the interaction respectively (Palacio et al. 2007). between the factors included in the model was not possible because the relative FRUIT/INFRUCTESCENCE RATIO Tussock /Open microsites cover (and SURVEYS therefore the expected frequencies) in the In June 2008, ten reproductive L. different site × slope aspect combinations subulatum individuals in each combination were not equiprobable, a general
73 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS assumption of the null hypothesis used complementary approaches. First, the ring when analyzing contingency tables with width data of all individuals measured in a multiple factors. To calculate the expected given combination of microsite and slope frequencies, the number of total plants aspect were grouped according to L. found in each transect were multiplied per subulatum age, independently of the percentage of cover of each microsite. recruitment year, and averaged. The The sum of predicted/observed frequencies average ring width of each of these four of the five transects per each site × slope groups was used to estimate the effect of S. aspect combination was used to run the tenacissima on the growth of L. subulatum Chi square test. To adjust for the increase throughout the ontogeny of the later by in Type I error because of multiple testing, using the relative interaction index (RII; the Bonferroni correction was used Armas et al. 2004). This index was (corrected a: 0.05/6 = 0.0083). calculated as (Gst – Go)/(Gst + Go), where The effects of slope aspect (north Gst and Go are the average ring widths of vs. south) and microsite (open areas, north L. subulatum individuals growing in face of S. tenacissima tussocks and south Tussock and Open microsites, respectively. face of S. tenacissima tussocks) on the RII values were obtained from 1 to 12 cumulative number of germinated seeds year old individuals to maintain enough were tested by using generalized linear sample size along the whole age range ( n = models (GLMs). GLMs were run with a 12–16 individuals in all the groups for all Poisson error distribution combined with a the ages analyzed; sample size log link function; Type I log likelihood dramatically decreased for older ratios were used to analyze main effects. individuals). This 12 year period recovers As recommended to counteract data over different ontogenetic stages of the protégée dispersion and to adjust the statistics plant: seedling (first year), juvenile (from 2 properly, the scale parameter was to 4 years) and adult stage (from 5 years estimated by dividing the square root of the onward). Therefore, it is sufficient to test Pearson’s Chi square statistic by the possible ontogenetic shifts in the sign of degrees of freedom (McCullagh and the interaction studied. To remove Nelder, 1989). Differences between potential autocorrelation derived from microsites were tested using a post hoc test repeated measures of ring width, a Prais– based on least square means. Growth data Winsten autoregression was performed to obtained from dendrochronological test the relationship between the values of measurements were analyzed using two the RII index and L. subulatum age. This
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analysis takes into account the non spring (March May), and the cumulative independence of the samples by estimating rainfall of the two annual pulses of L. a regression equation whose errors follow subulatum growth (February June and a first order autoregressive process (SPSS, September November). Of all these 2004). Second, ring width data were correlations, only March rainfall, which is averaged for each calendar year, without prior to the main pulse of L. subulatum taking into account the age of each L. primary growth (Palacio et al. 2008), was subulatum individual, to evaluate the effect statistically correlated with the width of climate inter annual variability on growth of L. subulatum rings (Appendix E annual growth rates. The RII index was in Supplementary Material). Therefore, we calculated with these data as described selected rainfall in this month as our above, evaluating the relationship between surrogate of abiotic stress. Separate this index and the rainfall registered in regression and autoregression analyses March by using linear regression. March were conducted for north and south slopes. rainfall was selected as the best possible This approach allowed us to test rainfall predictor of abiotic stress because differences in the effects of rainfall on the it was highly correlated with the final outcome of the interaction depending standardized ring width series of L. on the variability in the abiotic conditions subulatum (Pearson’s correlation index: among the two slope aspects considered. 0.78 and 0.62, P < 0.05 for ring widths The relative importance of both ontogeny growth of L. subulatum in Open microsites and abiotic stress as drivers of the outcome in south and north aspect slopes, of the interaction studied was also respectively, see Appendix E in explored. For doing this, three sequential Supplementary Material). To ensure that analyses were run. First, the effects of no other important rainfall variable was microsite ( Tussock vs. Open) and slope ruled out without the proper test, we aspect (north vs. south) on the growth of L. evaluated the bivariate correlations subulatum were evaluated using repeated between the width growth of L. subulatum measures ANOVA. For doing this, ring rings and the rest of possible rainfall width data were grouped according to L. indicators of abiotic stress: rainfall of the subulatum age, independently of the rest of the months, total annual rainfall, calendar year when they were formed. As monthly rainfall of September–December abiotic conditions are different in north and of the previous year, cumulative rainfall of south slopes due to different irradiation,
75 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS temperature and water stress levels same analysis was performed but changing (Friedman et al. 1977, Bellot et al. 2004, the covariate to the median of March Aragón et al. 2008), separated analyses rainfall during the lifetime of each were run for each slope aspect. This individual included in the analysis. March procedure allowed us to test potential rainfall is a key driver of L. subulatum differences in the nature of abiotic factors growth (Palacio and Montserrat Martí controlling the final outcome of the 2005, Palacio et al. 2007; Appendix E in interaction at each slope aspect. The Supplementary Material), and its median second step was to introduce the would be a good estimator of the water recruitment year as covariate in this stress level suffered by each individual analysis to assess the specific weight of during its entire life. With this analysis we climatic variability. L. subulatum aimed to differentiate the effects of rainfall individuals were of contrasting ages from those of unmeasured abiotic factors (recruitment dates of individuals analyzed characterizing each year as modulators of vary from 1981 to 2000), so the ring width ontogenetic shifts in plant–plant corresponding to each individual age may interactions. The effects of microsite be influenced by the particular abiotic (Tussock vs. Open ) and slope aspect (north conditions in the period they grew, and vs. south) on the mean therefore a high intra group variability was fruits/infructescence ratio and on soluble expected to be found. As abiotic factors and non soluble carbohydrates content can produce non random differences were evaluated with a two way ANCOVA, between individuals, and these differences where the size of L. subulatum individuals could mask the effect of an experimental was used as a covariate. GLM analyses treatment, its inclusion as a covariate has were carried out using the GENMOD been recommended to gain power when procedure of SAS 9.0 (SAS Institute, Cary, testing the effects of the factors of interest, NC, USA). The remaining statistical particularly when a high intra group analyses were conducted using SPSS 13.0 variability is found (see Engqvist 2005 and for Windows (Chicago, IL, USA). The references therein). If the effect of this non soluble carbohydrates content did not covariate is significant, and changes that of meet the ANOVA assumptions (normality S. tenacissima , this would suggest that and homocedasticity), and was transformed abiotic stress is modulating the net effects by using the arcsin transformation. The rest of S. tenacissima on the growth of L. of the data met these assumptions, and subulatum during ontogeny. Lastly, the were not transformed.
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RESULTS suggesting that the magnitude of the
Lepidium subulatum was more frequent differences between microsites varied with than expected under S. tenacissima the slope aspect considered. More canopies than in open microsites in five of germination events occurred in the north the six site × slope aspect combinations than in the south face of S. tenacissima 2 studied (Table 2.1). The overall cumulative canopies in the south slope (χ = 9.2; P = germination rate was very low due to the 0.002), but no differences between the drought conditions of the study year (Fig. north and south face of the canopy were 2 2.1). However, it was higher under the found in the north slope (χ = 1.2; P = canopy of S. tenacissima than in Open 0.277). microsites. A significant microsite × slope aspect interaction was also found,
Table 2.1. Expected and observed frequency of Lepidium subulatum individuals found under the canopy of Stipa tenacissima (Stipa) and in bare ground areas (Open) in north- and south-facing slope aspects at the three studied sites. Data represent the sum of the number of individuals of the five transects measured in each site × slope aspect combination. Chi-square test results evaluate the effects of microsite ( χ2 and P-value) in the various site and slope aspect combinations. Significant results (Bonferroni-corrected α) are in bold .
Expected Observed Slope Site frequencies frequencies χ2 P value Aspect Open Stipa Open Stipa Tielmes South 75.5 29.5 40 26 17.1 <0.0001 North 63.62 23.38 52 9 10.97 0.009 Aranjuez South 176.95 28.05 137 29 9.05 0.002 North 63.56 33.44 24 34 24.63 <0.0001 Noblejas South 99.44 33.56 89 17 9.27 0.002 North 146.42 63.58 119 49 8.48 0.004
77 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
Figure 2.1. Cumulative germinations registered in bare ground areas (Open), north face of Stipa tenacissima tussocks (Stipa north) and south face of S. tenacissima tussocks (Stipa south). Data represent mean + SE; n = 10. Different letters indicate significant differences between microsites in each slope aspect (post-hoc test based on the differences of least-square means).
A significant positive relationship between which was particularly evident in the north the RII values and L. subulatum age was slope (north: F1,32 = 5.54, P = 0.025; south: found, suggesting that the negative effect F1,27 = 3.88, P = 0.059). When recruitment of S. tenacissima on the growth of L. year was introduced as a covariate in this subulatum decreased as individuals aged analysis, the effects of microsite became (Fig. 2.2A). This relationship was found in non significant in both the south 2 both slope aspects (R = 0.83 and 0.51 for (recruitment year: F1,26 = 6.71, P = 0.015; south and north slopes, respectively). A microsite: F1,26 = 0.46, P = 0.503) and negative linear relationship between the north (recruitment year: F1,31 = 4.24, P =
RII values and March rainfall was found in 0.048; microsite: F1,31 = 3.22, P = 0.082) the south slope, suggesting that negative slopes. When the median of March interactions dominated in years of high precipitation was used as a covariate, it did March rainfall (Fig. 2.2B). No significant not change substantially the effects of S. relationships were found in the north slope. tenacissima on the growth of L. subulatum Repeated measures ANOVA showed a in the north slope (median March negative effect of S. tenacissima on the precipitation: F1,31 = 0.89, P = 0.35; growth of L. subulatum individuals microsite F1,31 = 4.66, P = 0.039), but it did (Appendix D in Supplementary Material), so in the south slope (median March
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precipitation: F1,26 = 3.63, P = 0.068; 4.44; P = 0.039 and F1,58 = 4.71; P = 0.034, microsite: F1,26 = 0.58, P = 0.454). Non for soluble and non soluble carbohydrates, structural carbohydrate content was higher respectively; Fig. 2.3). in Open than in Tussock microsites (F1,58 =
A
B
Figure 2.2. (A) Relationships between the effect size of Stipa tenacissima on the growth of Lepidium subulatum , as measured by the RII index, and the age of L. subulatum . (B) Relationships between values of this index and the median of rainfall registered in March during the period 1995–2007. Results of significant autoregressions (A) and linear regressions (B) are shown. Each RII value is obtained by averaging growth data from 12 to 16 L. subulatum individuals.
79 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
Figure 2.3. Soluble and non-soluble root carbohydrates content (black and grey bars, respectively) of Lepidium subulatum individuals harvested into two different slope aspects (north vs. south) and growing underneath Stipa tenacissima canopy (Stipa) or in areas without perennial vegetation (Open). Data represent means ± SE; n = 16. Asterisks mark significant differences in root carbohydrates content between microsites within each slope aspect. Different letters mark significant differences among slope aspects for soluble (normal letters) and non-soluble carbohydrates (capital letters).
Figure 2.4. Number of fruits per infructescence (mean ± SE; n = 10) of Lepidium subulatum individuals growing into two different slope aspects (north vs. south) and microsites (underneath Stipa tenacissima canopy, Stipa, or in areas without perennial vegetation, Open).
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A higher content of soluble carbohydrates spatial scales, and their interaction with was found in north than in south aspect ontogeny determine the final outcome of slopes (F1,58 = 28.82; P < 0.001), but non plant–plant interactions. significant effects of slope aspect were As expected, we found higher found when analyzing non soluble germination rates under the canopy of S. carbohydrates. The average number of tenacissima than in bare ground areas in fruits/infrutescence ratio was affected by both slope aspects (Barberá et al. 2006, the size of L. subulatum individuals (F1,35 = Schiffers and Tielbörger 2006). This effect 10.70, P = 0.002), as larger plants had seems crucial to define the final outcome more fruits. However, no significant of the interaction studied, as indicated by effects of slope aspect and microsite were the strong net positive effect of S. found (slope aspect: F1,35 = 0.91, P=0.346; tenacissima on the abundance of L. microsite: F1,35 = 0.04, P = 0.845. Fig. 2.4). subulatum individuals in most of the situations and sites studied. It is interesting DISCUSSION to note, however, that if only two In contrast to studies showing a single microsites (e.g. open vs. north face of S. facilitation/competition shift throughout tenacissima tussocks) would had been the ontogeny of perennial plants (Miriti considered, as it has been done by most 2006, Valiente Banuet and Verdú 2008, facilitation studies (see Callaway 2007), Armas and Pugnaire 2009), our results the higher positive effect of S. tenacissima provide evidence of multiple ontogenetic on the germination of L. subulatum found shifts between facilitation/competition in the south aspect slope would point to a during the life cycle of the protégée. We higher facilitative effect with increases in also found that spatio temporal changes in abiotic stress (Bertness and Callaway abiotic stress modulated these ontogenetic 1994). However, the contrasting results shifts. To our knowledge, these responses found between slope aspects when have not been described before. While the evaluating the germination of L. subulatum importance of studying different abiotic in the north and south faces of S. stressors and their interaction has been tenacissima tussocks suggest a complex highlighted (Holmgren et al. 1997, Riginos interplay between abiotic stress and et al. 2005, Baumeister and Callaway facilitation, which is strongly influenced 2006), our study illustrates how the spatial by spatial variability in these abiotic variability of these stressors, even at small stressors (e.g. light availability; Parker and
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Muller 1982, Marañón and Bartolome we grouped our data by the four possible 1993; S. Soliveres, unpubl. data ). One treatments combinations and averaged possible explanation for these results is them to calculate RII), there is a clear that in south aspect slopes, where water reduction trend on the strength of the stress is higher than in north aspect slopes negative effect on growth as L. subulatum (Bellot et al. 2004, Aragón et al. 2008), individuals aged. This effect, together with seeds predominantly germinate under the the positive effect found on germination, north face of tussocks, where the points to multiple facilitation/competition improvement in microclimate by S. shifts along the life cycle of L. subulatum . tenacissima is maximal due to water inputs Differences between our results and those coming from run off and to the shadow from previous studies (Miriti 2006, provided by the canopy of this species Valiente Banuet and Verdú 2008, Armas (Maestre et al. 2001, 2003). This microsite and Pugnaire 2009) can be explained preference is not so evident in the north because our study focuses on a grass– aspect slope, as seed germination in both woody plant interaction, while previous faces of S. tenacissima tussocks was studies have focused on woody–woody similar. These results seems to suggest a plant interactions. In a grass–woody trade off between microclimatic interaction, the growth of the woody amelioration in the north face of S. individuals as they age helps to avoid tenacissima tussocks (Maestre et al. 2003) water and light competition from the and the increase in interference grasses (Fowler 1986, Van Auken 2000), competition with other neighboring plants whereas the benefits of shade and (Goldberg et al. 2001, Miriti 2006), as they increased soil resources under the canopy are less abundant under the south face of of the later still exist (Maestre et al. 2003). the tussocks (S. Soliveres, pers. obs.). This may render competition less Stipa tenacissima had a negative important, as effective nicheseparation is effect on the growth and carbohydrate likely to occur with increasing age (Fowler content of L. subulatum, suggesting that 1986, Van Auken 2000, Armas and not only sink activity (growth), but also Pugnaire 2005). This is less likely to occur resource levels (carbohydrate content) are when the nurse and protégée share the lower in this microsite. Although we same ecological traits (e.g. annuals: cannot statistically differentiate the effect Goldberg et al. 2001; Schiffers and found on L. subulatum growth from a Tielbörger 2006; or shrubs: Miriti 2006), neutral one (we do not have error bars as as they are likely exhibiting greater niche
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overlap (Maestre et al. 2009a) and the the interaction were found in the north increase of standing biomass can lead to an slope. The relationship with rainfall increase in resource competition (Schiffers observed in the south slope can be and Tielbörger 2006). This difference explained by the compensation of the suggests that differentiation in the traits of negative effect of shade on growth with the the plants involved are likely to play an reduction in the water stress experienced important role in determining ontogenetic by L. subulatum , particularly in dry years facilitation/competition shifts (Armas and (Fig. 2.2B; Holmgren et al. 1997, Hastwell Pugnaire 2009), and thus should be and Facelli 2003). In our case, it seems that explicitly taken into account when trying rainfall modulated the trend toward to generalize the results of particular escaping light competition with age, being studies. shade less negative under dry years. This is Apart from the life story traits of suggested by the reduction observed in the the interacting species, differences in the negative effects of S. tenacissima on the tolerance to abiotic stress and the growth of L. subulatum when rainfall was competitive ability of the interacting introduced as a covariate. In the north species are crucial when studying plant– slope, the ontogenetic trend was the same, plant interactions (Liancourt et al. 2005, but abiotic factors other than rainfall Maestre et al. 2009a, Gross et al. 2010). In modulated this trend, as indicated by the our study, two stress tolerant species change in microsite effect along ontogeny coexist along a temporal stress gradient when recruitment year, but not rainfall, driven by water availability of each year. was introduced in the analysis. Our study As both species are stress tolerant, and shows how the same nurse effect, and its water is a resource related factor, positive interaction with ontogeny, depends on the interactions are expected to be dominant at spatio temporal changes in the overall intermediate levels of abiotic stress amount of abiotic stress experienced by the because of the existence of thresholds in interacting individuals, and on the both sides of the gradient (Maestre et al. resources driving such stress (Holmgren et 2009a). This prediction was not met, as we al. 1997, Hastwell and Facelli 2003). found less competition under more Moreover, we show how a longitudinal stressful (i.e. lower rainfall) conditions in track of competitive or facilitative the south slope, and no relationships interactions and its relationship with between abiotic stress and the outcome of climatic conditions can be easily obtained
83 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS using secondary growth data present in aspect slopes, other factors were more annual rings. important in north aspect slopes. Despite the mostly negative effect of the nurse CONCLUDING REMARKS plant on growth and reserve accumulation, In contrast with previous studies, which the positive effect found on early stages of found an increase in competition as the life cycle of the protégée (germination) prote´ge´e plants grew (Miriti 2006, may be driving the net positive sign of the Schiffers and Tielbörger 2006, Valiente interaction, as demonstrated by the spatial Banuet and Verdú 2008), we found a aggregation found between studied species. reduction of competition as plant aged. Given the implications of understanding This result may be influenced by how plant–plant interactions change along differences in ecological traits of species stress gradients for accurately predicting involved in our study comparing to the global change impacts on communities and previous studies, which can result in an ecosystems (Brooker 2006), future studies effective niche separation between grasses should pay special attention to the and shrubs, and therefore a reduction of interplay between abiotic stress and competition (e.g. Armas and Pugnaire ontogeny as joint drivers of 2005; our case) or in a niche overlap, facilitation/competition shifts, and more which together with the increase in specifically, on the effect of nurse plants in biomass can lead to higher competition key stages of the life cycle under different (e.g. Miriti 2006 for shrubs; Schiffers and environmental conditions (Goldberg et al. Tielbörger 2006 for annuals). Because 2001). This is particularly true when perennial grasses conform an important working with long lived species in component of many vegetation formations stressful environments. worldwide (Zimmermann et al. 2010), our ACKNOWLEDGMENTS results provide useful information to refine We thank M. Bowker for an early revision on a current theoretical models about previous version of this manuscript. E. Marcos, P. García Palacios, A.P. Castillo, E. Pigem, C. Alcalá, facilitation/competition shifts along J.C. Rubio (CESEFOR) and M. Méndez for their help during field and laboratory work. SS was ontogeny of perennial species. Our results supported by a fellowship from Fundación Biodiversidad CINTRA (EXPERTAL project). also provide important insights on how LDS was supported by a fellowship from Junta de Castilla y León. FTM was supported by a ‘‘Ramón spatio temporal changes in abiotic stress y Cajal’’ contract from the Spanish Ministerio de can modulate multiple Ciencia e Innovación (MICINN), cofunded by the European Social Fund, by the British Ecological facilitation/competition shifts. As rainfall Society (Studentship 231/1975), and by the MICCIN project CGL2008 00986 E/BOS. JMO increased competition escape in south was supported by Junta de Castilla y León
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VA069A07 project. This research was supported by Biodiversidad CINTRA and Fundación BBVA, the EXPERTAL and INTERCAMBIO respectively. (BIOCON06/105) projects, funded by Fundación
85 MULTIPLE ONTOGENETIC SHIFTS IN PLANT INTERACTIONS
Supplementary material for Chapter 2
Appendix C. Pictures showing differences among perennial cover in north (picture above) vs. south (picture below) aspect slopes in the Aranjuez study site.
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Appendix D. Detailed description of growth measurements and ring width growth data used
After manually polishing Lepidium disc surfaces until the xylem cellular structure was clearly visible, ring widths were visually dated by assigning calendar years (Stokes and Smiley 1968) and measured to the nearest 0.001 mm using a sliding stage micrometer (Velmex, Bloomfield INC., NY, US) interfaced with a computer. The COFECHA software (Grissino Mayer 2001) was used to quantitatively check for cross dating errors. The synchronised and highly inter correlated ring width chronologies for each combination of microsite and slope were selected from the pool of raw chronologies and used to build a master chronology. The master chronologies represent the common ring width growth for each combination of factors (Figure S1). Master chronologies were standardized with the ARSTAN computer program (Cook and Holmes 1996) by fitting to a spline function with a 50% frequency response of 32 yr, which was flexible enough to reduce the non climatic variance by preserving high frequency climatic information.
Figure S1. Ring-width growth data in north and south slopes as Lepidium subulatum individuals aged. Stipa and Open indicate individuals located less than 20 cm and further away than 50 cm from the canopy of a Stipa tenacissima tussock. Most individuals from the Stipa microsite were located under its canopy. These data were used to calculate Relative Interaction Indexes (RII) shown in Figure 2.2 of the main text. Data represent means ± SE ( n = 12- 16).
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Appendix E. Climate Response of Lepidium subulatum growth
The obtained residual chronologies were correlated against monthly rainfall during the growing season (September of the previous year to June) to assess which months determined plant growth and can be used as indicators of stress level. Precipitation data were obtained from the nearest meteorological station (period 1995–2007; Dosbarrios Meteorological Station, located 11 km SE from Noblejas site).
Table S7. Pearson two-tailed correlations (r) between the standardized ring width growth data of Lepidium subulatum for the four slope aspect × microsite combinations and rainfall registered at the nearest weather station (39º53’04’’N, 3º28’33’’W. 714 m.a.s.l.). We consider each month separately and also the sum of the rainfall registered during February-June, September-November and March-May, which match with the growth pulses of L. subulatum . In all cases, n = 12. Stipa and Open indicate individuals located less than 20 cm and further away than 50 cm from the canopy of a Stipa tenacissima tussock, respectively. Most individuals from the Stipa microsite were located under its canopy. Correlations with P < 0.05 are in bold.
North -aspect slope South -aspect slope
Open Stipa Open Stipa r P r P r P r P Sep prev. 0.12 0.71 0.23 0.47 0.12 0.71 0.01 0.97 Oct. prev. 0.59 0.04 0.09 0.78 0.41 0.19 0.01 0.97 Nov. prev. -0.46 0.13 -0.09 0.78 -0.08 0.81 0.33 0.30 Dec. prev. -0.48 0.15 -0.19 0.56 -0.12 0.7 0.42 0.17 January -0.42 0.17 -0.21 0.51 0.06 0.85 0.33 0.29 February 0.22 0.49 -0.3 0.34 -0.1 0.82 -0.12 0.70 March 0.77 <0.01 -0.24 0.45 0.62 0.03 0.43 0.17 April -0.02 0.94 -0.03 0.92 -0.01 0.99 -0.04 0.91 May -0.31 0.34 -0.04 0.91 0.09 0.78 0.5 0.10 June -0.13 0.69 -0.27 0.39 0.18 0.58 -0.21 0.51 September -0.22 0.48 0.31 0.33 -0.06 0.86 0.46 0.13 October 0.33 0.29 0.18 0.58 -0.1 0.76 -0.4 0.20 November -0.25 0.44 -0.19 0.56 -0.07 0.83 0.06 0.86 December -0.23 0.48 -0.09 0.78 0.02 0.96 0.41 0.19 Annual -0.15 0.64 -0.34 0.29 0.14 0.67 0.46 0.13 Feb-June 0.17 0.61 -0.29 0.37 0.32 0.32 0.37 0.24 Sep-Nov. 0.26 0.42 0.14 0.67 0.39 0.21 0.28 0.38 March-May 0.15 0.65 -0.16 0.63 0.36 0.25 0.54 0.07
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Temporal dynamics of herbivory and water availability interactively modulate the outcome of a grass-shrub interaction 3 in a semiarid ecosystem
Santiago Soliveres, Pablo García Palacios, Andrea P. Castillo Monroy, Fernando T. Maestre,
Adrián Escudero and Fernando Valladares
Manuscrito publicado en: Oikos (en prensa). D.O.I. 10.1111/j.1600-0706.2010.18993.x
BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS
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ABSTRACT
The study of plant plant interactions along grazing and abiotic stress gradients is a major research topic in plant ecology, but the joint effects of both stressors on the outcome of plant plant interactions remains poorly understood. We used two different factorial experiments conducted in a semiarid Mediterranean steppe to assess: 1) the role of the perennial grass Stipa tenacissima , a low palatability species, providing protection from rabbit herbivory to the shrub Retama sphaerocarpa (Experiment 1), and 2) the effects of environmental amelioration provided by Stipa on the recovery of Retama after rabbit damage under two contrasted levels of water availability (Experiment 2). In the Experiment 1, water stress worked as an indirect modulator of herbivore protection by Stipa. This species protected Retama seedlings from rabbit herbivory during the wetter conditions of spring and winter, but this effect dissapeared when rabbit pressure on Retama increased during summer drought due to the decrease in alternative food resources. In the Experiment 2, Stipa exerted a negative effect on the survival of Retama seedlings during the three years of the experiment, regardless of inter annual differences in rainfall or the watering level applied. This negative effect was mainly due to excessive shading. However, Stipa increased Retama recovery after initial rabbit impact, overriding in part this negative shade effect. Conversely, Stipa impact on the Fv/Fm of Retama seedlings depended on the intra annual water dynamics and its experimental manipulation, overall contradicting predictions from the Stress Gradient Hypothesis. The complex interactions found between herbivory, microclimatic amelioration from Stipa, and water availability as drivers of Retama performance illustrate the importance of considering the temporal dynamics of both biotic and abiotic stressors to fully understand the outcome of plant plant interactions.
91 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS
INTRODUCTION nteractions among plants can be a continuous increase in the frequency of negative, neutral, or positive, positive interactions with increases in either Idepending their direction and consumer pressure or abiotic stress. magnitude on the level and type of the However, several studies suggest that stressors governing a given community (see positive plant plant interactions may Callaway 2007 for a review). Important collapse under extremely high levels of efforts have been devoted during the past both consumer pressure and abiotic two decades to understand the dynamics of stressors directly related to resources, such plant plant interactions along abiotic stress as water or light (e.g. Graff et al. 2007, or herbivory gradients, highlighting how Maestre et al. 2009a). These studies caused the presence of multiple abiotic stressors or the generality of SGH predictions to be different levels of consumer pressure challenged (Maestre et al. 2005, 2006, importantly affect the outcome of plant Lortie and Callaway 2006). As a result of plant interactions (e.g. Baumeister and this debate, predictions from the SGH have Callaway 2006, Graff et al. 2007). been refined to consider the effect of However, and despite their common co different abiotic stressors and the ecological occurrence in nature, the joint effects of strategy of the species involved, and to both herbivory and water stress on the introduce consumer pressure as a major outcome of these interactions remain factor affecting plant plant interactions largely ignored (Ibañez and Schupp 2001, along abiotic stress gradients (Maestre et al. Veblen 2008, Smit et al. 2009). Considering 2009a, Smit et al. 2009). Furthermore, in both abiotic stress and herbivory together is arid and semiarid areas water availability is crucial to understand the role of plant plant characterized by a strong inter and intra interactions in dryland ecosystems, where annual variability, with marked temporal these stressors are major factors influencing dynamics that profoundly affect ecosystem plant community dynamics (Fischer and functioning (Whitford 2002). These Turner 1976, Whitford 2002). temporal dynamics add complexity to the The Stress Gradient Hypothesis response of plant plant interactions to (SGH; Bertness and Callaway 1994), a abiotic stress (Goldberg and Novoplansky framework in which most studies focused 1997, Pugnaire and Luque 2001, de la Cruz on plant plant interactions rely on, predicts et al. 2008), and may also modulate the
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effect of herbivores on vegetation (Veblen relative importance of water and light as 2008). Thus, they must be specifically limiting factors for plant performance and considered when studying the relationship how herbivory affects their uptake (Wise between plant plant interactions and and Abrahamson 2005, 2007). Hence, the different environmental biotic and abiotic final outcome on the protégée plants stressors in arid ecosystems. response to herbivory is difficult to Herbivory is also a major driver of generalize and predict, so more studies plant plant interactions in these regions along these lines are needed to refine (Baraza et al. 2006, Graff et al. 2007, predictions on how plant communities Veblen 2008). Unpalatable nurse plants respond to different levels of abiotic and may protect their understorey vegetation biotic stressors (Graff et al. 2007, Smit et from herbivory damage by hiding more al. 2009). palatable plants under their canopies, or by We conducted two simultaneous field sharing their defenses against herbivores experiments to test the effects of rabbit (Baraza et al. 2006, Veblen 2008), a process herbivory and water availability on the commonly refered to as “associational interaction between the tussock grass Stipa resistance” ( sensu Hay 1986). This tenacissima L. (the nurse) and seedlings of protection against herbivory can strongly the leguminous resprouter shrub Retama affect vegetation dynamics and biodiversity sphaerocarpa (L.) Boiss. (the protégée) in a in grazed systems (Veblen 2008). semiarid Mediterranean steppe. Stipa has an Alternatively, the improvement on water overall low palatability (Ben Salem et al. status that nurse plants usually provide to 1994), and therefore could provide their target plants may also positively affect herbivory protection for shrub seedlings by target plant recovery from herbivory associational resistance. Furthermore, the damage (Rand 2004, Acuña Rodriguez et positive effect that microclimatic al. 2006). However, even in dry amelioration provided by Stipa has on the environments, shade casted by nurse plants survival of Mediterranean shrub seedlings can lead to light limitation for the protégée is well known (e.g. Maestre et al. 2001, plants (Seifan et al. 2010a, Soliveres et al. 2003). Since water stress and the impact of 2010). The joint effect that both shade and herbivores can prevent Retama an improved water status provided by nurse establishment in these environments plants have on the recovery from herbivory (Espigares et al. 2004, Rueda et al. 2008), it of the protégée plants will depend on the is likely that the protection from herbivores
93 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS and the microclimatic amelioration Supplementary Material). The soil is provided by Stipa canopies can play a key classified as Xeric Haplogypsid (Marqués role improving Retama colonization in et al . 2008). Vegetation is an open steppe semiarid grasslands. We tested the dominated by Stipa (this species accounts following hypotheses: i) Stipa provides up to 90% of the total perennial cover), protection from rabbit herbivory to Retama , with a perennial plant cover of 24%. Sparse enhancing its survival when rabbits are adult individuals of Retama and small present; ii) Shade provided by the Stipa shrubs such as Lepidium subulatum L. and canopy enhances Retama water status Helianthemum squamatum (L.) Dum. Cours increasing its survival, but this positive are also present. The study site has a high effect wane during extremely dry years due diversity of annual plants, which reach their to the overwhelming effect of competition production peak in spring and constitute an for water, iii) Regardless of plant water important part of plant productivity during status, light reduction produced by Stipa this period (Peco et al. 2009). will decrease Retama seedling recovery The study area harbours a high from rabbit herbivory; and iv) Facilitation density of rabbits ( Oryctolagus Cunniculus of Retama seedlings by Stipa will collapse L.), as suggested by the high number of under extreme levels of stress produced by visual contacts and the number of warrens the joint action of herbivore damage and and latrines found (S. Soliveres, pers. obs. ). drought stress. Domestic livestock or other large herbivores are absent, and thus rabbits are METHODS the only herbivores affecting vegetation
STUDY AREA there. Rabbit activity tracks seasonal We conducted the study in the Aranjuez variation in vegetation productivity. These Experimental Station, located in the center animals feed near their burrows to avoid of the Iberian Peninsula (40º03´60´´N, predation during spring and winter, when 3º54´91´´W). The climate is semiarid their prefered food –mainly annuals– is Mediterranean, characterized by cold abundant; however, during summer drought − − winters and a strong summer drought, with when annuals dry out and food is scarcer , average annual precipitation and rabbits increase their exploration to obtain temperature of 388 mm and 15 ºC, enough food to survive (Rueda et al. 2008). respectively (1994 2005; Marqués et al. The selection of woody seedlings as a food 2008, see also Appendix F in resource by rabbits increases during summer (Maestre et al. 2001). Rabbit
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browsing, in the case of Retama seedlings, were located in bare ground areas, > 50 cm may suppose the virtual removal of all the away from any perennial plant. One month aboveground biomass. after planting, rabbits browsed some of the seedlings, and we set up two parallel EXPERIMENTAL DESIGN experiments then. In the first experiment In December 2006, we planted 371 two (hereafter Experiment 1) we did not give year old Retama seedlings, with a mean the seedlings any protection from further height of 27 ± 2 cm (mean ± SE, n = 20), by grazing. This allowed us to test the using manually dug holes of 20×20×20 cm. protection against herbivores provided by The planted seedlings came from central Stipa canopy. In the second experiment Spain (viveros Bárbol, Madrid, Spain), and (hereafter Experiment 2) we evaluated the were maintained in the original nursery joint effects of contrasted levels of water until the week prior to planting. In the availability and Stipa environmental nursery, seedlings were grown under amelioration on the recovery of Retama optimal conditions (full sunlight, fertilized seedlings after rabbit browsing. 1:1 peat:coco peat substrate, watering to field capacity each week). We selected Experiment 1: Nurse plant protection these two year old seedlings to ensure they against herbivores had enough size and reserves to resist rabbit From the 371 Retama seedlings planted, we damage at least once (see Experiment 2 left a total of 195 seedlings without any below). The selection of these two year old protection from herbivores (the remaining seedlings does not underestimate potential plants after Experiment 2 was set up, see facilitative effects of Stipa because Retama below). From these seedlings, 103 and 92 seedlings were grown under optimal were located in Tussock (refuge) and Open conditions prior to their plantation, and thus (control) microsites, respectively. We they were still sensitive to water stress and scored which of these plants had been to the environmental amelioration provided browsed by rabbits and which of them were by Stipa. We randomly planted these able to resprout and survive after the virtual seedlings on two different microsites: removal of their aboveground biomass (i.e. “Tussock ” and “ Open ”. The former the effect of rabbit damage) during January, microsite was located < 15 cm from the March and September 2007. Because of the upslope face of an Stipa tussock (ca. 1 m high number of rabbits present in the study width and 80 cm height). Open microsites area and their repeated browsing, no plants
95 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS remained alive after September 2007, so we We conducted a spatial analysis of stopped monitoring then. browsed seedlings using the Spatial Analysis by Distance Indices (SADIE) Experiment 2: Joint effects of herbivory methodology (see Perry 1998 for details). and abiotic stress on the outcome of the The spatial pattern of herbivory damage by interaction rabbits was random (SADIE’s Aggregation
This experiment had three factors: i) Index [ Ia] = 0.95; P = 0.56; n = 176). Thus, Microsite ( Tussock vs. Open ), ii) Herbivory we do not expect unmeasured variables (Retama seedlings whose aboveground with spatial structure (e.g. soil depth, biomass was completely eaten by rabbits distance to a rabbit burrow or slope during the first month in the field vs. position) to influence seedling response to unbrowsed seedlings), and iii) Irrigation the assayed treatments. We did not measure (watered vs. non watered seedlings). Since seedling attributes that could influence inter annual variability is of crucial rabbit behaviour (e.g. plant C/N ratio, initial importance in dry environments, and it may plant height). However, the large number of strongly affect the results found and our seedlings randomly assigned to each conclusions (Ibañez and Schupp 2001), we treatment, and the fact that rabbit damage conducted this experiment during a three was equally intense (i.e. complete removal year period (and therefore under three of aboveground biomass) regardless of the contrasted environmental conditions) to add microsite considered, should control for the confidence to the results found. We set up experimental noise that any unmeasured 22 replicates per each combination of factors potentially affecting rabbit behavior treatments (176 seedlings in total). All the could have on the results of this seedlings from this experiment were experiment. protected from further herbivory after the The irrigation treatment consisted in first month in the field using a metallic eight supplementary pulses of water, once mesh. The diameter of the openings in the every month, between April and July in mesh was 5 cm, which casted no detectable both 2007 and 2008. The wettest and driest shade to the seedlings, and did not periods of the study area are spring (from confound the effects of any of the factors in March to May) and summer (from June to the experiment. In this experiment we September), respectively. Thus, the monitored the variables described below irrigation treatment affected both wet and (see Field monitoring section below). dry periods. In each monthly watering, we applied an amount of water equivalent to
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the 50% of the median rainfall registered fluorescence parameter Fv/Fm; it is during the past 30 years for this month, calculated from photosystem II (PSII) irrespectively of the rainfall registered (i.e. fluorescence signals as the ratio between 6, 9.3, 10.9 and 5.7 mm for April, May, the variable (Fv) and the maximum (Fm) June and July, respectively; see Appendix 1 fluorescence signal, which are obtained in Supplementary material). With this from a short light pulse after 20 minutes of irrigation scheme we aimed to evaluate the dark adaptation. Fv is the difference joint effects of reducing the summer between Fm and the minimal fluorescence drought (summer drought was longer in signal right before the saturating light pulse, unwatered plants because of the lack of being Fm the light that plant cannot absorb rainfall in June and July) and increasing when its absortion capability has been precipitation during the wet season (spring collapsed by a previous pulse. Fv/Fm was rainfall was less abundant in unwatered determined with a pulse modulated plants) on the outcome of the interaction fluorometer (FMS2, Hansatech Instruments, studied . Norfolk, UK). This variable is an estimator of the overall plant stress (Maxwell and Field monitoring of Experiment 2 Johnson 2000), and has been widely used as -Plant performance measurements an indicator of plant stress in numerous We monitored seedling height and survival studies in semiarid areas (e.g. Pugnaire et after each summer, which is the most al. 1996b, Maestre et al. 2001, 2003, critical season for seedling survival in Aragón et al. 2008). Furthermore, small Mediterranean semiarid regions (e.g., changes in the concentration of chlorophyll Maestre et al. 2001, 2003). We measured in leaf tissues associated with water these variables in September 2007, 2008 limitation, which can be tracked by and 2009. Height was well correlated with measuring Fv/Fm, can be crucial during aboveground biomass, as demonstrated by important stages of plant life (Aragón et al. an allometric relationship performed with 2008). Although the use of Fv/Fm can be seedlings of contrasted sizes and ages problematic for the detection of water stress (Spearman correlation: ρ = 0.65, P < in some species (Resco et al. 2008), it is a 0.0001; n = 45), and thus was used as our good proxy for plant stress in our case surrogate for seedling biomass in the field. because the canopy structure, lack of leaves We measured photochemical and the high tolerance of Retama to solar efficiency by using the in situ chlorophyll radiation minimizes photoinactivation and
97 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS downregulation in this species (Valladares gravimetric soil moisture (R 2 = 0.84; P < and Pugnaire 1999), a confounding factor 0.0001; n = 68) to assess for the validity of that could mask the relationship between these measurements in gypsum soils and to Fv/Fm and water stress. We randomly convert them in soil gravimetric moisture selected eight seedlings per treatment ( n = data. We measured soil moisture in the 64) for Fv/Fm measurements. We measured same plants in all the samplings, and in the Fv/Fm in four key moments for seedling same sampling periods as Fv/Fm surveys performance in Mediterranean semiarid (see above). When these measurements environments: during the wettest period of coincided with irrigation pulses, soil spring (April May), in the middle and at the moisture was measured at least one week end of the summer drought (July and after the irrigation. With this approach we September, respectively) and during the avoided giving too much importance to the coldest month (December January). Fv/Fm occasional influence of irrigation in our was measured in the same plants from May measurements, and assessed more 2007 to September 2009. realistically the soil moisture available for Retama seedlings during a given period. In Soil moisture measurements addition to these measurements, and to We measured soil moisture by time domain further evaluate the effects of irrigation on reflectometry (TDR; Topp and Davis 1985) soil water availability, we measured soil using a Campbell TDR100 system moisture one day after the irrigation pulse (Campbell Scientific Ltd, Loughborough, was applied on June 2007 in the planting UK). In eight randomly selected planting holes of 10 undamaged plants (the eight holes per treatment, we vertically installed replicates selected for the previously 10 cm long probes ( n = 64). We chose this described soil moisture measurements plus soil depth because the vast majority of root two extra replicates) of each of the four biomass of the planted seedlings combinations between microsite and concentrates near the soil surface (the pots irrigation ( n = 40). We measured soil where Retama seedlings were grown had moisture only in unbrowsed plants because ca. 15 cm. depth), and because Stipa we were only interested in assessing for tussocks also concentrate the majority of differences in soil moisture between the their roots in the upper layers of the soil irrigation treatments applied and the (Puigdefábregas et al. 1999). We conducted microsites tested. a site specific calibration between Time Domain Reflectometry measurements and
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STATISTICAL ANALYSES all the cases) and thus independency is As all Retama seedlings used in Experiment expected. Since browsing by rabbits 1 died at the end of the monitoring, we did removed most aerial biomass of planted not perform any statistical comparison with seedlings, and initial seedling height after the survival data at this period. However, rabbit impact was not measured, we did not we used the log rank statistic of the Kaplan consider such height as a covariate in Meyer procedure to compare the shape of further statistical analysis. the survivorship and number of browsed 100 plants curves between Tussock and Open A microsites. We analyzed the survival of 80
Retama seedlings from Experiment 2 60 OPEN TUSSOCK separately for each year by using a 40 hierarchical log linear analysis, with microsite, irrigation and herbivory as fixed 20 unbrowsedseedlings (%) factors. To assess for the effects of the 0 0 2 4 6 8 10 factors assayed during the different Months after planting environmental conditions characterizing
each year, only those seedlings that 100 B survived the previous summer were taken 80 OPEN into account for this analysis (for example, TUSSOCK to analyze survival of 2008, we only 60 considered those seedlings alive after the 40 summer of 2007). With this approach, we 20 seedlingsurvival (%) were able to assess the consistency of
0 treatment effects over the years. It also 0 2 4 6 8 10 Months after planting avoids the potential “dragging” that an extremely strong effect of a particular Figure 3.1. Dynamics of herbivore damage (A) treatment during a given year may have on and overall survivorship (B) of unprotected Retama sphaerocarpa seedlings growing under the overall net results (i.e. we could detect the canopy of Stipa tenacissima (Tussock) and if herbivory had strong effects in 2007, but in bare ground areas (Open) from December 2006 to September 2007. not in the rest of years). Survival data from one year to another were not correlated We analyzed gravimetric soil (Spearman correlation: ρ < 0.4; P > 0.2 in moisture (obtained from TDR data), Fv/Fm
99 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS and seedling height data by using repeated independent from those coming from wet measures ANOVA, with microsite, periods. However, by pooling the data from irrigation and herbivory as fixed factors. the three study years together (we Data were square root transformed to reach conducted two separate RM ANOVA, one normality and homocedasticity assumptions with dry and another for wet periods data when necessary. We found significant from the three study years) only consistent interactions between time and the results for the three years may result treatments evaluated when analyzing soil significant and this lack of independency moisture and Fv/Fm data (data not shown). disappears. Furthermore, with this approach These interactions can lead to the we removed the interactions with the misinterpretation of the effects of the fixed assayed treatments and time, avoiding the factors (Quinn and Keough 2002), and are confounding effect that the strong temporal of biological importance, as intra annual variability in water availability could have dynamics in water availability can strongly on the interpretation of the main treatment affect the effects of nurse plants (Goldberg effects (Quinn and Keough 2002). and Novoplansky 1997, De la Cruz et al. We evaluated differences in soil 2008). To properly assess the effect of the moisture between watered vs. unwatered assayed treatments, and to explore how the plants (soil moisture measures after the intra annual dynamics in water availability irrigation pulse of June 2007) using a two modulates them, we grouped both soil factor (microsite and irrigation) ANOVA. moisture and Fv/Fm data for the three study These data followed the assumptions of this years in wet/dry periods (periods with soil analysis, and thus were not transformed. moisture values above and below 10%, We conducted all statistical analyses using respectively) and analyzed them separately SPSS 13.0 for Windows (Chicago, Illinois, using repeated measures ANOVA. We USA). established this 10% value to separate wet/dry periods because it corresponds to a RESULTS biological threshold that separates periods EXPERIMENT 1: NURSE PLANT when most plant activity concentrates PROTECTION AGAINST HERBIVORES (those with soil moisture > 10%) in Survival and herbivore damage of semiarid environments (Noy Meir 1973, unprotected plants Valladares et al. 2005). These analyses Fewer plants were browsed by rabbits when could lack independency because results growing under Stipa canopies than in Open obtained in dry periods were not completely
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microsites during spring (Fig. 3.1A; Log I ; P < 0.0005 100 M ; P < 0.0005 rank test, P < 0.0001). Rabbit predation 2007 M x H ; P = 0.005 intensity on Retama seedlings increased 80 during summer drought. This, together with 60
the removal of most aboveground biomass 40 produced after each browsing impact, 20 caused the depletion of the resprouting 0 ability of Retama seedlings, and all the 100 2008 M ; P < 0.005 plants died during summer regardless of the 80 OPEN microsite where they were planted (Fig. TUSSOCK 60 3.1B). Thus, we did not find differences in 40
survival among microsites during the study Survival (%) period (Log rank test, P = 0.466). 20
0 100 M ; P = 0.06 EXPERIMENT 2: JOINT EFFECTS OF 2009 I x H ; P < 0.005 80 HERBIVORY AND ABIOTIC STRESS Plant performance 60
Stipa tenacissima reduced significantly the 40 survival of Retama seedlings during the 20 three years of study (2007: G2 = 12.7, df = 0 1, P = 0.005; 2008: G2 = 9.3, df = 1, P = H- H+ H- H+ G2 P I- I+ 0.002 and 2009: = 3.6, df = 1, < 0.06, Figure 3.2. Survival of Retama sphaerocarpa Fig. 3.3. 2). Survival was 17%, 27% and seedlings during the three years of study in the eight combinations of treatments evaluated. 15% lower in Tussock than in Open Open = bare ground areas, Tussock = Stipa tenacissima canopies, I- = no irrigation, I+ = microsites for 2007, 2008 and 2009, irrigation of 50% of the median of April-July period rainfall in four pulses, H- = no herbivore respectively. Irrigation increased the damage, and H+ = seedlings partially eaten by survival of Retama seedlings during the rabbits. Initial n = 22.
2 first summer by 27% ( G = 10.29, df = 1, P G2 = 7.7, df = 1, P = 0.005, Fig. 3.2). We = 0.001), but did not affect the negative found a significant interaction between effect of Stipa . Browsing damage did not prior herbivory damage and water affect mortality rates per se in this availability in 2009 ( G2 = 8.85, df = 1, P = experiment, but reduced the negative effect 0.003), being the survival of unbrowsed of Stipa on Retama (Microsite × Herbivory: seedlings higher than that of browsed
101 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS
seedlings when these were unwatered. × herbivory interaction was found (F 1,56 = When watered, seedlings that were browsed 5.35; P = 0.024), with more water available showed a higher survival rate than those under Stipa canopies and Open microsites that were not browsed (Fig. 3.2). for browsed and unbrowsed plants, Herbivory decreased seedling height respectively (Fig. 3.5). Although irrigation during the three years of study (RM increased soil moisture values by an
ANOVA: F 1,171 = 4.6; P = 0.036), an effect average of 35% after watering (Two way that was especially evident in 2008 (Fig. ANOVA, F 1,36 = 8.05; P < 0.001), it did not 3.3). We did not detect any microsite or affect soil moisture at the long term, as this watering effect, neither any interaction treatment had no significant effects on this between the treatments evaluated or with variable when analyzing the data gathered time, when analyzing seedling height. Stipa during the whole year (Repeated Measures tenacissima reduced the Fv/Fm ratio of ANOVA; P = 0.929). Retama seedlings during dry seasons (RM
ANOVA: F 1,56 = 9.6; P = 0.003), but this DISCUSSION effect decreased when plants were watered The results of our study highlight the (Microsite x Irrigation: F 1,56 = 3.9; P = importance of herbivory as a major factor 0.05). This Microsite x Irrigation affecting the relationship between plant interaction was also found in wet periods, plant interactions and abiotic stress. The when irrigation reduced the positive effects increase in rabbit pressure during summer of Stipa on Retama Fv/Fm (Fig. 3.4; drought, indirectly caused by the lack of Appendix G.A). alternative food resources during this season, overrided the herbivory protection Soil moisture provided by Stipa during wetter periods, 2007 was the wettest year of the studied when rabbit pressure upon Retama period, with soil moisture levels well above seedlings was lower. Conversely, the initial 20% during spring (Appendix G.2B). loss of biomass produced by rabbit Conversely, 2009 was the driest year, with browsing shifted the interaction between soil moisture levels below 10% in three of Stipa and Retama from negative to neutral. the four periods sampled (Appendix G.2B). Stipa tenacissima slightly (< 2%) reduced soil water availability during dry periods
(RM ANOVA: F 1,56 = 5.02; P = 0.029). During wet periods, a significant microsite
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interactions between herbivory, abiotic 2007 stress and their temporal dynamics as 40 drivers of the outcome of plant plant interactions highlight the importance of 30 considering these stressors together to fully
20 understand the outcome of plant plant interactions along environmental gradients
10 (Goldberg and Novoplansky 1997, de la 2008 40 OPEN Cruz et al. 2008, Anthelme and Michalet TUSSOCK 2009).
30
DRY SEASON M ; P < 0.005 0.8 20 M x I ; P = 0.005 Mean seedlingheight (cm) 10 0.6
2009 RM ANOVA: H ; P < 0.005 40
30 0.0 WET SEASON OPEN TUSSOCK 20 0.8 M x I ; P = 0.05
10 0.6
H- H+ H- H+ Photochemicalefficiency(Fv/Fm) I- I+
Figure 3.3. Height of Retama sphaerocarpa 0.0 seedlings during the three years of study in the H- H+ H- H+ eight combinations of treatments evaluated (mean ± SE; n depended on survival). Rest of I- I+ Legend as in Figure 3.2. Figure 3.4. Photochemical efficiency (Fv/Fm) of Retama sphaerocarpa seedlings during wet/dry Our results suggest that the negative effect periods (periods above/below 10% gravimetric soil moisture, respectively). Data are means ± of Stipa on the performance (Fv/Fm) of SE of the three years-study period data pooled Retama by wet/dry seasons; n = 8). Rest of Legend as was driven by water availability, in Figure 3.2. but that competition for other resources rather than water modulated the effect of Stipa on Retama survival. The complex
103 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS
corresponding increase in rabbit predation 10 DRY SEASON M ; P < 0.05 upon perennials due to changes in diet 8 produced by the lack of annuals during
6 summer (Rueda et al. 2008) can explain the suppression of this facilitative effect during 4 this season. Similar reductions of 2 facilitative effects under high herbivory 0 pressure have been previously reported 30 WET SEASON OPEN TUSSOCK (Graff et al. 2007, Smit et al. 2007), and 25 M x H ; P < 0.05 should be common when food resources are 20
Gravimetricsoil moisture (%) less abundant and the same number of 15 herbivores may exert higher pressure on the 10 remaining plants (but see Veblen 2008,
5 Anthelme and Michalet 2009).
0 H- H+ H- H+ I- I+ DOES SHADE INTOLERANCE OF THE
Figure 3.5. Gravimetric soil moisture (inferred PROTÉGÉE EXPLAIN THE NEGATIVE from time-domain reflectometry measurements) EFFECT OF THE NURSE PLANT? during wet/dry periods. Rest of Legend as in Figure 3.4. In contrast with previous studies using the
same nurse plant (e.g. Maestre et al. 2001, PROTECTION AGAINST HERBIVORES 2003), we found a net negative effect of BY STIPA TENACISSIMA Stipa on survival of Retama seedlings. Although Retama seedlings were protected Plant plant interactions depend up to a great from herbivore damage when Stipa was degree on the identity of the species present, this effect dissapeared during involved (Callaway 2007), and thus these summer drought, when the higher rabbit contrasting results are not fully surprising. impact upon Retama seedlings Plant competition in drylands is generally overshadowed the refuge effect of Stipa attributed to water or nutrients (Whitford (Fig. 3.1). Annual plants, which provide an 2002). Interestingly, most of the negative important fraction of plant productivity in effects of Stipa on Retama were not arid and semiarid systems (Fischer and influenced by increases in water Turner 1978), have completed their life availability, neither were explained by the cycle before the onset of summer drought in effect of Stipa on this variable. The reduced our study area (Peco et al. 2009). Thus, the light availability under the canopy of Stipa
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tussocks (which suppose >80% of incident Tielbörger 2010). The same may happen PAR reduction; see Maestre et al. 2003), with different life stages of a given species, has been identified as the major driver of as plants are often more shade tolerant early the positive effect of Stipa on shrub during their ontogeny than in later stages of seedlings (Maestre et al. 2003). However, development, and therefore are more likely this same shade could be also a key factor to benefit from nurse’s shade (Callaway and affecting the negative outcome of the Walker 1997, Miriti 2006). Our results studied interaction (Seifan et al. 2010a, highlight the species specific nature of such Soliveres et al. 2010). The lack of leaves of effects (Callaway 2007), since the same Retama and the concentration of the total shade that is beneficial for some species photosynthetic area on its cladodes, is (Maestre et al. 2001, 2003) could associated with the high light requirements conceivably be negative for Retama or of this species (Valladares and Pugnaire other shade intolerant plants (Marañón and 1999, Valladares et al. 2003, Espigares et Bartolomé 1993, Seifan et al. 2010a). Thus, al. 2004), and suggests that a reduction in more studies involving species with available light might underlie the outcome different ecological strategies and drought observed. and shade relative tolerances are needed to Most plant species adapted to improve our understanding on the responses drought are not able to cope with deep of plant plant interactions to abiotic stress shade (Niinemets and Valladares 2006), and and herbivory at the entire community therefore, it is likely that species that are level. more adapted to full sunlight and drought, which are abundant in dry environments, do THE ROLE OF FACILITATION AND not benefit from the presence of a nurse RESOURCE AVAILABILITY ON THE plant unless the positive effects of the nurse RECOVERY OF BROWSED PLANTS on the water status of the protégée Irrigation increased survival during part of overcome negative effects promoted by the studied period (Fig. 3.2) and also the light reduction (Holmgren et al. 1997). The degree of stress experienced by Retama more drought tolerant the protégée plant is, seedlings was lower during wet periods. the less positive the shade effect is expected Both results indicate that water was limiting to be, according to the general ideas the performance of this species, regardless discussed in recent revisions of the SGH of the microsite tested. However, light was (Maestre et al. 2009a, Malkinson and also an alternative limiting factor for plant
105 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS performance in Tussock but not in Open in watered plants, since plants growing microsites (discussed above). The Limited beneath the canopy of Stipa should be more Resource Model (LRM), which correctly limited by light, while plants growing in explains most of the relationships between Open microsites should be limited only by different resource levels and tolerance to water. However, our results did not fully herbivory, predicts a differential recovery match predictions from the LRM, maybe from tolerance depending on the nature of because our target plant was a resprouter, the limiting resources and the way and therefore its tolerance to herbivory herbivory damage affect their uptake (Wise might be affected not only by the amount of and Abrahamson 2005, 2007). Particularly, resources available, but also by the reserves this model foresees a higher tolerance to of each seedling might have (Vesk et al. herbivory under wetter conditions when 2004). In contrast, a higher survival in water is the only limiting factor (such as in browsed plants was found when they were Open microsites), but a lower tolerance watered, regardless of the microsite where under these same wet conditions when they were planted. This finding could herbivory exacerbates the limitation of an indicate an overcompensation of browsing alternative resource, light in our case (such damage by plants when environmental as in Tussock microsites). This latter conditions were more benign (Crawley et outcome is explained because plants al. 1998). Why the LRM predictions did not growing under drought are already at their correctly explain the effects of shade optimum light conditions, and are mainly provided by Stipa on Retama recovery after limited by water availability, while plants herbivory damage? Shade provided by growing under Stipa canopies are closer to Stipa might increase the water status of their optimum moisture conditions, but also Retama seedlings by a reduction in limited by light. Thus, the latter plants will transpiration (Holmgren et al. 1997). Thus, be much more sensitive to the reduced it is likely that this improvement in the uptake of light (their alternative limiting water status of Retama seedlings increased resource), and therefore to the loss of their tolerance to herbivory in a similar way biomass produced by herbivory, than the that watering did it in Open microsites. This former (Baraza et al. 2004, Wise and positive effect in the recovery from Abrahamson 2005, 2007). herbivory shifted the negative effect that Following these predictions, we may this same shade exerted on Retama survival expect lower tolerance to herbivory in on unbrowsed plants (we found a Tussock than in Open microsites, especially significant Microsite × Herbivory
106 CHAPTER 3
interaction when analyzing seedling pulses (our wet seasons) due to competition survival). The compensation of resource by resources, while increased survival competition due to herbivory protection has during periods with low nutrient availability been observed in previous studies in (our dry seasons). The final outcome would semiarid environments (Graff et al. 2007). depend on how much the negative effect on Our results suggest that this compensation growth during wet seasons affects survival also occurs when the nurse plant improves during dry periods, and on the relative recovery from herbivory, and highlight the importance of plant uptake or abiotic complex interaction between water stress factors affecting resource availability and herbivory as drivers of the outcome of during these dry periods (Goldberg and an interaction strongly influenced by shade. Novoplansky 1997, Hastwell and Facelli 2003). However, the effects of Stipa on the TEMPORAL DYNAMICS IN WATER Fv/Fm (our surrogate of plant stress) of AVAILABILITY MODULATE THE Retama seedlings during wet/dry seasons EFFECT OF STIPA ON RETAMA found differed from the expected responses In contrast with our initial hypothesis, Stipa arisen from the predictions of Goldberg and negatively affected Retama survival during Novoplansky (1997). Specifically, we the three years of study, regardless of the detected a trend towards facilitation and inter annual variation in rainfall availability competition during wet and dry seasons, among years. This may be explained respectively (although it must be considered because the studied interaction was mainly that we only measured the degree of stress driven by light competition, and therefore experienced by Retama and not its growth water availability only played a secondary or survival seasonally, which could be a role in its outcome. However, intra annual better test for this model). Differences dynamics in water availability and our produced in the outcome of the interaction irrigation treatment modulated the effect of studied within these seasonal dynamics Stipa on the stress level experienced by varied with irrigation, which overall Retama seedlings. Goldberg and suggest a reduction of competition intensity Novoplansky (1997) proposed a conceptual at intermediate levels of abiotic stress model to introduce the effect of intra annual (watered plants during summer or resource dynamics on plant plant unwatered plant during spring), but a interactions. In their model, nurse plants prevalence of competition in the rest of affected negatively protégée growth during assayed situations, as suggested by the
107 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS refined SGH when the two species involved how the complex interactions between are stress tolerators (Maestre et al. 2009a). herbivory and water stress jointly influence the outcome of plant plant interactions. CONCLUDING REMARKS They provide insights to fully understand Collectively, our experiments indicate the the interplay between facilitation and existence of a complex hierarchy of competition, and they can be used to further mechanisms affecting the interaction refine conceptual models aiming to predict studied (Baumeister and Callaway 2006). In the outcome of plant plant interactions our case, water shortage per se was along composite stress gradients. irrelevant under extremely high herbivory impacts (all seedlings died in Experiment 1 ACKNOWLEDGEMENTS but none of them due to drought), but We wish to thank E. Chaneton, D. Eldridge, M. Seifan and three anonymous referees for their useful indirectly modulated herbivory impacts by comments and corrections on a previous version of this manuscript. E. Pigem, C. Alcalá, S. Constán affecting alternative rabbit food resources. Nava, J. Papadopoulos and E. Barahona helped during the fieldwork. We thank the Instituto Conversely, the initial loss of biomass Madrileño de Investigación y Desarrollo Rural, Agrario y Alimentario (IMIDRA) for allowing us to produced by herbivory was a major factor work in the Finca de Sotomayor (Aranjuez). SS and affecting the outcome of the interaction PGP hold PhD fellowships from the EXPERTAL grant, funded by Fundación Biodiversidad and studied. Stipa exerted a negative effect on CINTRA S.A. APC was supported by a PhD fellowship from the INTERCAMBIO Retama seedlings mainly by light (BIOCON06/105) grant, funded by Fundación BBVA. FTM acknowledges support from the competition, but this shade improved European Research Council under the European Community's Seventh Framework Programme seedlings recovery after herbivory, (FP7/2007 2013)/ERC Grant agreement n° 242658. overriding the negative effects found on This research was funded by the EXPERTAL grant, and with additional funds from INTERCAMBIO unbrowsed plants. Our findings illustrate and REMEDINAL2 grants.
108 CHAPTER 3 .
Supplementary Material for Chapter 3
Appendix F. Climatic data (mean monthly temperature, black circles; and monthly rainfall, grey bars) obtained from a meteorological station (Onset, Pocasset, MA, USA) located at the study site. White bars represent the increment in monthly rainfall by the irrigation treatments applied during 2007 and 2008.
140 monthly rainfall 30 watering 120 25
100 20
80
15 60 Rainfall(mm) 10 40 Meantemperature (ºC)
5 20
0 0 S A Jl N O F S A Jl N D O Jn F S A Au D Jl My Jn Mc Ja Au My Jn Mc Ja Au My Mc 2007 2008 2009
109 BIOTIC AND ABIOTIC STRESSORS AFFECT PLANT PLANT INTERACTIONS
Appendix G. Photochemical efficiency of Retama sphaerocarpa seedlings (A) and gravimetric soil moisture (A) in the different sampling dates for the eight possible combinations of treatments. Open = bare ground areas, Stipa = Stipa tenacissima canopies, I = no irrigation, I+ = irrigation of 50% of the median of April July period rainfall in four pulses, H =no herbivore damage, and H+ = seedlings partially eaten by rabbits. Data represent means ± SE ( n = 8).
0.9 A
0.8
0.7
0.6
Open I- H- Open I- H+ 0.5 Open I+ H- Open I+ H+ Stipa I- H- Photochemical efficiency(Fv/Fm) 0.4 Stipa I- H+ Stipa I+ H- Stipa I+ H+ 0.3 y y t. y y y t. y il y t. a ul p ar a ul p ar pr ul p M J e u M J e u A J e S an S an S J J 2007 2008 2009
B 40 Open I- H- Open I- H+ Open I+ H- Open I+ H+ Stipa I- H- Stipa I- H+ Stipa I+ H- Stipa I+ H+ 20
10
Gravimetric soil moisture (%)
0 y y t. y y y t. y il y t. a ul p ar a ul p ar pr ul p M J e u M J e u A J e S an S an S J J 2007 2008 2009
110
On the relative importance of climate and biotic non-trophic
interactions as drivers of local plant species richness in semiarid 4 communities
Santiago Soliveres, David J. Eldridge, Fernando T. Maestre, Matthew A. Bowker, Matthew Tighe and Adrián Escudero. Manuscrito en revisión en Ecological Monographs
BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
112 CHAPTER 4 .
ABSTRACT
Most studies including the role of positive plant plant interactions as drivers of plant richness along environmental gradients assume an unimodal richness productivity relationship, which is not as general as previously thought, and the existence of an overarching stress gradient which affects equally the different species forming a community. We aimed to evaluate the relative roles of facilitation/competition and environmental conditions as drivers of local species richness without these assumptions, and to clarify their contribution to the richness productivity relationship. We conducted an observational experiment across wide environmental gradients in semiarid regions from Spain and Australia, assessing how the intensity, importance and frequency of positive interactions, and the degree of niche expansion provided by the nurse plants changed along these gradients. We also tested the particular mechanism (niche segregation, competitive exclusion or intransitivity) underlying the effects of nurses on their understorey vegetation. Nurse plants increased local richness by expanding the niche of the less adapted species both in Spain and Australia. The high variability of niches often found underneath their canopies may be the main reason why higher niche segregation and species coexistence was found under nurse than in open microsites. The outcome of the competition facilitation continuum changed depending on the type of stress gradient considered. When it was driven by both rainfall and temperature (Spanish sites), the community wide importance of nurse plants remained constant along the gradients. When the stress gradient was driven only by rainfall (Australian sites), the importance of nurses showed a unimodal relationship with the gradient, indicating a collapse of facilitation under both extremes of rainfall availability. Particular pairwise interactions outcomes were poorly predicted using abiotic measurements as an overarching stress level, and we propose to use each species distance to its environmental optimum as a better approach for this purpose. Our study provides a complete mechanistic understanding of the relative roles of plant plant interactions and environmental conditions shaping local species richness in semiarid environments. These results can also be used to refine our predictions of the response of plant communities to environmental gradients, and clarify the relative importance of biotic interactions as a driver of such responses.
113 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
INTRODUCTION
he study of the mechanisms 2007). Over the past decade, ecologists controlling the composition of have revisited the hump shaped richness Tcommunities has been a major productivity relationship to explore the topic in ecology since the early days of this potential effects of positive, non trophic science (see Gotelli and Graves 1996 for a interactions (hereafter ‘facilitation’; Hacker review). Recent research has highlighted and Gaines 1997, Michalet et al. 2006). the fact that local scale non random However, the relative effects of plant plant processes such as abiotic constraints and interactions and abiotic conditions on biotic interactions determine the species changes in species richness along that are able to successfully colonize a environmental gradients, and therefore their given environment (Huston 1999, Lortie et influence on the richness productivity al. 2004a, Rajaniemi et al. 2006). relationship, remain uncertain (Rajaniemi et Pioneering studies have suggested that, al. 2006). Studies aimed at clarifying the among local scale processes, competition roles of these factors can help to explain regulates richness at high levels of why several studies cast doubt on the productivity, while limited physiological generality of the hump shaped richness tolerances to abiotic stress or disturbance productivity relationship, particularly at reduce species recruitment, and thus both local and regional scales (Waide et al richness, at low levels of productivity 1999, Gillman and Wright 2006). (Grime 1973, Huston 1979). An inherent Many empirical studies (e.g. Hacker assumption of this observation is that and Bertness 1999, Kikvidze et al. 2005, competition is less important at the lower Valiente Banuet et al. 2006, Cavieres and productivity end of the gradient. Overall, Badano 2009) and theoretical models the joint effects of abiotic constraints and (Bertness and Callaway 1994, Bruno et al. competition should generate a hump shaped 2003, Lortie et al. 2004a) developed over relationship between species richness and the past two decades have emphasized the local productivity, which is reputed to be importance of facilitation for maintaining ubiquituous in nature (Grime 1973, 2001, community richness at low to moderate Huston 1979). However, plant plant levels of productivity (Hacker and Gaines interactions are key drivers of community 1997, Michalet et al. 2006). Environmental structure in both high and low productivity buffering (both microclimatic amelioration environments (Tilman 1988, Callaway and protection from herbivory) by nurse
114 CHAPTER 4 .
species can increase the realized niche of Most studies describing facilitatory less adapted species, and therefore increase mechanisms in relation to the diversity local richness (niche expansion; Bruno et productivity curve have tended to focus on al. 2003). Although the relationship unproductive to moderately unproductive between the importance and frequency of environments (Hacker and Gaines 1997, positive plant plant interactions and Michalet et al. 2006). Recent studies, abiotic/biotic stress was originally thought however, have revealed that ecological to be monotonic and positive (Bertness and processes such as niche segregation (Hector Callaway 1994), some studies have et al. 1999, Silvertown 2004), competition suggested a waning of positive interactions intransitivity (lack of hierarchy in under either extreme abiotic stress levels competition networks: Gilpin 1975, Laird (e.g. Kitzberger et al. 2000, Ibañez and and Schwamp 2006, Bowker et al. 2010), Schupp 2001, Maestre and Cortina 2004a) and indirect facilitation (Levine 1999, or intense disturbance (Ibañez and Schupp Brooker et al. 2008) may be key 2001, Smit et al. 2007, Forey et al. 2009), mechanisms enhancing species richness in thus obviating niche expansion (Michalet et more productive conditions. More benign al. 2006). Explanations invoked to explain conditions often found under nurse plants this lack of niche expansion under such (Franco and Nobel 1989) may increase the conditions are: 1) the competitive effects of local species pool and the heterogeneity of nurse plants may outweight the positive available niches, also allowing finer effects of environmental amelioration, partitioning of variable resources. Although particularly when abiotic stress is promoted largely ignored in facilitation research by a resource such as water (Maestre and (Brooker et al. 2008, but see Tielbörger and Cortina 2004a, Maestre et al. 2009a), and 2) Kadmon 2000b), these localized effects nurse plants may not be able to attain a size may potentially increase niche segregation large enough to ameliorate harsh abiotic (Pugnaire et al 1996,a Maestre and Cortina conditions in extremely stressful 2005) and competition intransitivity environments (Michalet et al. 2006). We beneath nurse plant canopies, enhancing henceforth refer to both of these potential overall local richness and productivity. mechanisms as facilitation waning models Despite the interest generated in the joint (see Fig. 4.1). effects of nurse plants on both niche expansion and changes in competition
115 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS outcomes, these mechanisms have largely with environmental conditions which it is been explored separately in the literature. maladapted therefore, intuitively it could be There is a clear need, therefore, to develop considered to be far from its environmental a unifying framework that integrates our optimum, and therefore limited or stressed understanding of the roles of niche (Lortie et al. 2004b). Since species forming expansion and competition in explaining a community do not need to be adapted to the role of plant plant interactions on local exactly the same environmental conditions, richness (Brooker et al. 2008). we can find, within a given community, Most conceptual models of species differing in their optima and facilitation developed to date are based on therefore differences in the degree of stress the notion that stress tolerant plants that they experience across environmental increase the performance of competitive gradients (Chapin et al. 1987, Greiner La plants under “ high levels of stress ”. Thus Peyre et al. 2001). We refer to this concept the underlying assumption of an henceforth as the individual-based stress overarching stress gradient affecting plant concept (Fig. 4.1). This may have profound communities has permeated the facilitation implications for our understanding on how literature (Lortie et al. 2004a, Travis et al. plant plant interactions affect local richness 2005, Michalet et al. 2006). However, and its relationship with productivity, since stress is a complex concept (see Körner niche expansion does not necessarily need 2003, Lortie et al. 2004b, Körner 2004, for to increase in the “ moderate to high stress a recent discussion) and is more direction ” (Lortie et al. 2004a, Travis et al. appropriately applied at the level of 2005, Michalet et al. 2006). Rather, a individual species than at the community general mechanism operating across the level. Individual species are adapted to entire environmental gradient should be that tolerate particular environmental better adapted plants increase the realized conditions, and under these particular niche of less adapted species to a given set conditions, a given species will experience of environmental conditions (Bruno et al. little or no stress (Körner 2003). However, 2003). Thus when dealing with natural the morphological and physiological plant communities, there is a clear need to adaptations to particular environmental question the existence of an overarching conditions constitute trade offs in a species´ stress gradient for the whole community, or ability to cope with different stressors of ecological strategies that remain constant (Tilman 1988, Niinemets and Valladares along these gradients (Greiner La Peyre et 2006). When a given species has to cope al. 2001, Prider and Facelli 2004, Holmgren
116 CHAPTER 4 .
and Scheffer 2010). A reassessment of the these two regions because they have assumptions underlying these notions will contrasting vegetation communities and pave the way for an improved management histories, and both exhibit a understanding of the relative roles of biotic relatively wide diversity in species richness interactions and abiotic conditions as across their respective environmental drivers of species diversity along gradients. Our main hypotheses were that: productivity gradients. 1) nurse plants will enhance local species In this study we aimed to develop a richness via niche expansion and changes in unifying framework that explains the the competitive networks (niche segregation relative effects of plant plant interactions and competition intransitivity) of their and environmental conditions on local understorey vegetation; 2) positive pairwise species richness across environmental interactions will wane at environmental gradients. Our framework includes the two conditions corresponding to levels of main processes by which plant plant extreme stress for involved plants (Michalet interactions may affect local diversity: 1) et al. 2006, Maestre et al. 2009a) and 3) niche expansion due to facilitation, and 2) since different species co ocurring in a changes in competitive outcomes beneath community differ in their relative tolerances nurse canopies. We have included in this to given environmental conditions, the framework an assessment of changes in the intensity, importance and frequency of intensity, importance and frequency of facilitation at the community level, and positive interactions on community level therefore niche expansion, will remain plant richness and productivity along an constant across stress gradients as the environmental gradient. We have also identity, but not the amount, of facilitated evaluated changes in the intensity and species changes along such gradients importance of a large number of pairwise (Greiner La Peyre et al. 2001). interactions along such gradients. To develop our framework we established plots METHODS across wide environmental gradients in STUDY AREA Spain and Australia, and assessed the Two semiarid regions were selected for this relative roles of plant plant interactions and study, one located in the Stipa tenacissima abiotic constraints as drivers of the local steppes of central and south eastern Spain, species richness at each plot. We chose and the other in the semiarid eucalypt
117 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS woodlands of eastern Australia. We (Eremophila mitchelii , E. sturtii , Dodonaea surveyed 10 (Australia) and 11 (Spain) sites viscosa, Acacia spp. and Senna spp.). along climatic gradients ranging from 13º– Details of the study sites and images of the 17º C mean annual temperature and 273– communities are given in Appendix H. 488 mm average annual rainfall in Spain, and from 16º–19º C and 280–630 mm in VEGETATION SURVEY Australia. Plot selection included the full At each site we established a 30 m × 30 m range of environmental conditions existing plot, containing the representative within the distribution of both vegetation vegetation of the surrounding area. This communities, as recommended to test the plot size permitted the inclusion of several relationship between plant plant shrub and tree patches within this area, interactions, community processes and enough to conduct the facilitation surveys environmental gradients (Brooker et al. described below. Within each plot we 2008, Lortie 2010). Within each country the centrally aligned three 30 m long transects, selected plots shared a common soil type, 8 m apart, down the slope for the vegetation management style and vegetation survey. Along each transect we placed 20 community type, and were selected with contiguous 1.5 m × 1.5 m quadrats, and similar orientation and slopes to minimize recorded the cover and abundance of all any experimental noise that could perennial plant species within the quadrat. potentially influence the effect of climatic These data provided us with a conditions on the stress experienced by the presence/absence matrix of 80 columns plant community. Stipa sites were located (four transects by 20 quadrats) for each on limestone soils. Vegetation was in all plot. The total cover of each plot, which has cases an open steppe (mean cover 35 to been shown to be a good surrogate of 68%) dominated by the perennial tussock productivity in semiarid environments grass Stipa , with sparse resprouting shrubs (Flombaum and Sala 2009), was derived such as Quercus coccifera , Pistacia from the average cover of perennial plants lentiscus and Rhamnus lycioides . Sites in across the 80 quadrats. This survey was south eastern Australia were open used to examine differences in community woodlands located on clay loam soils. composition derived from contrasting Canopy cover, which ranged from 18 70%, environmental optima of the different was dominated by Eucaliptus populnea , E. species forming each community across the intertexta , E. microtheca , Geijera parviflora and several shrub species
118 CHAPTER 4
Figure 4.1. Conceptual diagram synthesizing current facilitation models (upper panel) and our newly proposed model (lower panel). Current facilitation models are the Stress-Gradient Hypothesis (SGH), as originally presented by Bertness and Callaway (1994) and the Facilitation waning models , as a synthesis of new empirical data and several proposed modifications of the SGH (see main text). The SGH predicts an increase in positive interactions either under high consumer pressure or abiotic stress level (parts A, and E-F of the upper panel), being competition more important under moderate conditions (part C of the upper panel). Facilitation waning models propose that positive interactions dominate under high, but not extreme, levels of either abiotic stress or consumer pressure (parts B, D and E of the panel). In contrast with the SGH, these positive interactions collapse when consumer pressure reaches extreme high levels (e.g. Smit et al. 2007; part A in the upper panel) or when abiotic stress reaches this extreme levels (part F in the upper panel). Among facilitation waning models, some of them propose that negative interactions dominate again under such stressful conditions (e.g. Maestre et al. 2009a; discontinuous line), while others suggest that the sign of the interaction becomes neutral (e.g. Michalet et al. 2006). This differentiation is caused by the different explanations invoked to explain this facilitation waning (see main text). Our newly proposed model ( Individual-based stress concept ; lower panel) does not take into account if the “abiotic stress” or “consumer pressure” are extremely high, moderate or low, because their effects may differ depending on the physiological tolerances of the species involved, and thus are difficult to predict. Instead, we use the distance to the environmental optimum of each target species to predict the effects of nurse plants. As a given
119 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS particular species moves further away from its optimum, the effects of a nurse plant will become more positive (Greyner La Peyre et al. 2001, Holmgren and Scheffer 2010). This interaction will become more negative as the target species gets closer to its environmental optimum. This model also predicts a facilitation collapse when the given environmental conditions are so severe for a given target plants that the recruitment is impossible, even under the safe sites provided by the nurse plants (Kitzberger et al. 2000, Ibañez and Schupp 2001., Soliveres et al. in press ) gradient in each region (see Appendix I for under the canopies of five Quercus a detailed description of this analysis). coccifera (or another resprouting shrub species when Quercus was absent from the FACILITATION SURVEY plot; hereafter Shrub microsite). Because of differences in vegetation For the Australian plots, we sampled physiognomy, we conducted facilitation three different microsites; Open , Shrub and surveys using slightly different protocols in Tree . Shrub microsites were represented as Spain and Australia. In each plot located in inverse cone shaped (sensu Whitford 2002) Spain, ten Stipa tussocks (hereafter Stipa shrubs such as Eremophila mitchellii , microsite) were randomly selected, and the Dodonaea viscosa, Senna artemisioides or total area under their canopy sampled with juvenile Callitris glaucophylla , depending 0.5 m × 0.5 m quadrats. The abundance and on the species present in each plot. Our cover of all perennial plant species were sampling protocol changed slightly recorded within each quadrat. Since most of depending on the canopy size of shrubs. the species in the studied areas have Where the canopy was sufficiently large, canopies smaller than the 0.5 m × 0.5 m we sampled six 0.5 m × 0.5 m quadrats area, we believe that this is an appropriate under each of five shrubs. Where shrubs size to evaluate species co ocurrence on a were smaller, a larger number of shrubs distance closer enough to ensure that the were sampled in order to sample a total of species found were interacting someway. 30 quadrats. Paired Open microsites (> 1 m Ten paired open areas, located at least 1 m from any shrub or tree) were also sampled from any Stipa tussock or resprouting shrub adjacent to these shrubs to yield the same (hereafter Open microsite), were randomly sampling area. Finally, we sampled the selected adjacent to these tussocks. We same number of quadrats under the Tree balanced our sampling effort among microsites, which were represented by microsites by sampling the same area (i.e different species of eucalypts (E. populnea , the same number of 0.25 m 2 quadrats) of E. intertexta , E. microtheca ), Casuarina Open microsites as that sampled under pauper or Geijera parviflora . Because of Stipa . Finally, we sampled the same area the large area occupied by these tree species
120 CHAPTER 4 .
(up to 200 m 2 for some Eucalyptus trees), interactions and abiotic stress along we sampled only three trees in each plot. environmental gradients (Lortie 2010). We The canopy area of all shrubs and trees was used the first PCA axis as our surrogate for calculated based on the area of a circle. For the climatic gradient present at our sites in both Spain and Australia, plot level both countries (hereafter referred to as richness was calculated by summing up the Climate ). This axis explained 88.6% total number of different species found in (Eigenvalue = 8.08 10 3) and 86.2% the 30 0.5 m × 0.5 m, and eighty 1.5 m ×1.5 (Eigenvalue = 1.07 10 4) of the variance in m quadrats sampled. the climatic data for Spain and Australia, respectively. This axis was highly STATISTICAL ANALYSES correlated with rainfall and radiation in Reduction of climatic data Spain (Eigenvectors = 0.864 and 0.502 for Eight climatic variables (annual radiation, rainfall and radiation, respectively; the minimum, maximum and mean remainder of the eigenvectors were < 0.03 temperature, and rainfall, temperature range in all cases) but only with rainfall in [maximum minimum temperature], and Australia (Eigenvector = 0.996; the rest of minimum and maximum temperatures for eigenvectors were < 0.1 in all cases). the coldest and warmest month, Principal Component Analyses were carried respectively) were collected for each site out in Primer v. 6 statistical package for using available climatic models (Ninyerola Windows (PRIMER E Ltd., Plymouth et al. 2005) and data from the Bureau of Marine Laboratory, UK). Meteorology (www.bom.gov.au) in Spain We evaluated the relationships and Australia, respectively. We reduced between Climate and both cover and these climatic variables to a single synthetic species richness at the plot level, and the variable for each country using PCA. relationship between cover and richness, Summarizing environmental variables in a using both linear and quadratic regressions PCA allowed us to obtain a more general because either linear or unimodal assessment of the influence of all of our relationships between these variables are environmental variables at both community expected from previous studies (e.g. Grime and species specific levels. This approach is 1973, Whitford 2002). Regression analyses strongly recommended for testing were carried out using SPSS 13.0 for relationships between plant plant Windows (Chicago, Illinois, USA).
121 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Assessing biotic interactions To assess the importance of plant Because plant plant interactions cannot be plant interactions, i.e., the relative effect measured in a simple way (Maestre et al. that Stipa , shrubs and trees had on richness 2005, Brooker et al. 2005), we applied three and cover compared to that of other complementary indices to quantify their 1) environmental factors (Brooker et al. 2005), intensity, 2) importance and 3) frequency. we used the Interaction Importance Index
The intensity and importance of plant plant (I imp ; Seifan et al. 2010b), which has similar interactions were assessed using both plant statistical properties to RII and is therefore richness and cover. To measure the comparable among sites located across the intensity of the interactions, i.e., the effect environmental gradient sampled. This index that neighbours have on species richness is calculated as I imp = N imp /│N imp │+│E imp │, and cover regardless of other environmental where Nimp and E imp are the nurse plant and factors (Brooker et al. 2005), we used the environmental contributions to species
Relative Interaction Index (RII; Armas et richness or total cover, respectively. N imp is al. 2004). This index is calculated for each calculated as P Nurse – POpen , and E imp as P Open microsite pair as (P Nurse – POpen )/(P Nurse + – MP Open/Nurse , where MP Open/Nurse is the
POpen ), where PNurse is either mean cover or maximum value of species richness or mean species richness under the canopy of mean cover found in the entire gradient, a nurse plant ( Stipa , Shrub or Tree irrespective of the microsite sampled. microsites) and POpen is either mean cover Finally, the frequency of positive or mean species richness in the Open interactions was measured as the percentage microsite. This index has good statistical of either facilitation obligates and properties, which make it suitable for facilitation beneficiaries (sensu Butterfield comparing the intensity of plant plant 2009), as a percentage of the total species interactions across environmental gradients; pool of each plot. We considered as it has defined limits ( 1,+1), is symmetrical facilitation obligates those species found around zero, and has identical absolute only under the canopy of a given nurse values for competition and facilitation. It is plant but not in the Open microsites also linear, unbiased at low intensity (regardless of the identity of the nurse interactions, and has no discontinuities in plant), while facilitation beneficiaries were its range (Armas et al. 2004). For each plot species with more individuals growing we calculated the mean index obtained from under the canopy of a nurse than in the all the Nurse Open microsite pairs sampled. Open microsites. We used the number of recruited individuals because seedling
122 CHAPTER 4 .
germination and establishment, particularly battery of approaches provided us with a during the first year, are known to be the complete assessment of the relationships principal bottlenecks in plant recruitment in between plant plant interactions and abiotic semiarid environments, such as those stress. Furthermore, it allowed us to sampled (Eldridge et al. 1991, Escudero et evaluate the importance of nurse area as a al. 1999, Maestre et al. 2001). Thus, we driver of this relationship. This area believe that a higher number of individuals influences the effects of nurses on recruiting in a given microsite is indicative microclimatic amelioration and niche of superior environmental conditions availability, and thus affects the richness experienced in this microsite for a given and cover of understorey plants (Pugnaire et species, an approach followed by previous al. 1996a, Maestre and Cortina 2005, studies on the topic (Valiente Banuet et al. Michalet et al. 2006). 2006). Furthermore, to assess the relative The three attributes used to quantify role of abiotic stress and nurse size at the plant plant indicators (intensity, importance pairwise level, we selected for each country and frequency) were plotted against separately, those species present in at least Climate and mean nurse size for each plot three different sites across the sampled (i.e. the area occupied by the nurse plants). environmental gradient, which ensured that These relationships were tested with both we had at least three points with which to linear and quadratic regressions, following test the relationship between plant plant predictions from previous facilitation interactions and abiotic stress using climatic models (Bertness and Callaway 1994, features, as recommended (Lortie 2010). Michalet et al. 2006, Maestre et al. 2009a). With the selected species (16 and 13 for In the case of frequency, we calculated the Spain and Australia, respectively), we percentage of obligate and beneficiary calculated Iimp and RII for all the species species for each microsite and country using cover of the target species as our separately, and then for the whole proxy of plant performance. If the intensity community. For the whole community we or importance of facilitation increase with added together data for both nurse abiotic stress, as predicted by the “stress microsites ( Stipa and Shrub , Spain; or gradient hypothesis” (SGH; Bertness and Shrub and Tree , Australia) and also tested Callaway 1994, Callaway 2007), we would them separately for each country. This expect to detect an increasing trend of
123 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS positive interaction outcomes with model is another measurement of the fitness increasing stress. Alternatively, if of each model to our data. facilitative interactions collapse at extremely high stress levels (i.e. low Measuring changes in plant plant rainfall), we would expect to find a interaction outcomes depending on unimodal relationship between facilitation microsite indicators and climate, which may or may Nurse plants may affect the competitive not be related to nurse size (facilitation outcomes of their understorey plants by waning; Maestre and Cortina 2004a, increasing competitive intransitivity or by Michalet et al. 2006, Maestre et al. 2009a). niche segregation (Brooker et al. 2008). To test the generality and validity of these Both mechanisms are related to the three models (SGH, facilitation waning maintenance of higher species richness than because of smaller nurses, and facilitation if competitive exclusion alone dominates waning because of increasing competition), interactions among understorey plants we evaluated the relationships between RII, (Silvertown 2004, Laird and Schwamp Iimp obtained with all the pairwise 2006). Recent models have highlighted the interactions tested in each country, and the importance of competition intransitivity as climatic PCA axis or the nurse size using a key modulator of species richness (Laird Spearman correlations. To assist us in the and Schamp 2006, 2008, Bowker et al. interpretation of these analyses, the 2010). The degree of intransitivity can be percentage of pairwise interactions that defined as the absence of a competitive followed each model prediction was also hierarchy among the species coexisting in a calculated for each country and nurse plant. community (Gilpin 1975). However, this If the Spearman correlation with Climate is concept assumes that the competitive ability significant and negative, this will give of those species making up a given support to the SGH, if the relationship community are constant along the whole set between the interaction indices and Climate of possible environmental conditions. To is unimodal, this will give support to adequately test intransitivity it is necessary facilitation waning models. If the latter is to measure the competitive ability of every also related with nurse size, this will species against every other one (Grace et al. support the facilitation collapse derived 1993), making it exceptionally difficult to from nurse plant growth limitation. The test empirically. Alternatively, niche percentage of cases explained for a given segregation has been identified as a crucial mechanism increasing species richness (e.g.
124 CHAPTER 4 .
Silvertown 2004), and is more likely to explained below) independently for each of occur under the most heterogeneous the Stipa , Shrub and Tree microsites by conditions found beneath nurse plants, pooling all the sampled quadrats of these rather than in Open microsites (Pugnaire et microsites within each plot ( n = 30), al. 1996a, Maestre and Cortina 2005). obtaining a unique value per microsite and However, niche segregation may change per plot. Most of the species sampled in along environmental gradients (Huston Spain and Australia are small shrubs or 1999), and is also difficult to measure grasses, and therefore the quadrat size used empirically when considering the whole is particularly suitable to include plant community. interactions among them without including We attempted to measure changes in random co ocurrence or exclusions not competition intransitivity and niche related to competition among them. We segregation, and their relationship with the estimated species co occurrence with the C plot scale diversity of species found in each score index, a metric commonly used in this microsite, by using null models of guild kind of analyses (e.g. Dullinger et al. 2007, structure based on patterns of species co Maestre et al. 2008, Rooney et al. 2008). occurrence (Gotelli and Graves 1996, This index is calculated for each pair of
Gotelli et al. 2010). These null models are species as (R i S)(R j S), where R i and R j organized a priori by groups of ecological are the number of total occurrences for significance, such as different functional species i and j, and S is the number of groups or trophic levels (i.e. species guilds), quadrats in which both species occur. This and allow testing of the role of competition score is then averaged over all possible in structuring the community within each pairs of species in the matrix (Gotelli guild separately (Gotelli and Graves 1996). 2000). The C score is related to the This analysis is not limited to grouping by competitive exclusion concept of species guild. In reality, any type of a priori “checkerboardness” i.e., how many of the group could be examined. possible species pairs in a given community For co occurrence analyses, we never appear in the same quadrat together. organized our presence/absence data Thus, positive and large values of this index (obtained from the 0.5 m × 0.5 m quadrats) indicate that competition may be the by microsite guilds, that is, we calculated prevalent mechanism determining the co species co occurrence (C score index, occurrence patterns observed (Gotelli
125 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
2000). To determine the strength of co our conclusions. The results obtained with occurrence in a sample, the observed C this analysis were similar to those obtained score value is compared against a set of null with the ‘fixed rows–equiprobable models which serve as a baseline for what a columns’ null model, and thus are not community unstructured by species shown. interactions would look like (Connor and Standardized Effect Size (SES) Simberloff 1979). As the values of the C values of the C score less than or greater score are dependent on the number of than zero indicate prevailing spatial species and co occurrences observed within segregation and aggregation among the each plot, we obtained a standardized effect species within a community, respectively. size (SES) as (I obs Isim ) Ssim , where I obs is To assess the extent to which changes in the observed value of the C score, and I sim competitive outcomes affect local diversity, and S sim are the mean and standard we compared the SES obtained with the deviation, respectively, of this index plot level richness found in each microsite obtained from the n simulations performed (hereafter ‘plot richness’). The logic (Gotelli and Entsminger 2006). underlying the use of SES and plot richness We used ‘fixed rows–equiprobable values to measure competition intransitivity columns’ null models and 5000 or niche segregation is that we assume that simulations. With this approach, each SES will be higher when competitive species conserved its own abundance (rare exclusion is more important at the quadrat species remained rare and common species scale. High SES values can lead to two remained common) and each quadrat was different outcomes: 1) a reduction in plot assumed to have the same probability of richness because a few dominant species being colonized as the remainder, occupy all of the available space (i.e. when regardless of the number of species found the differences in competitive ability among in each quadrat, during the simulations. co existing species are high, competitive This null model has been recommended for transitivity leads to competitive exclusion standardized samples collected in and low diversity), or 2) an increase in plot homogenous habitats (Gotelli 2000), such richness, if there is a lack of a competitive as the ones gathered in this study. We also hierarchy and competitive dominants in used the “fixed rows fixed columns” each quadrat, depending on the algorithm (both species and quadrats microenvironmental conditions existing in conserved their relative abundance and each different quadrat. In this case, a high richness, respectively) to add confidence to quadrat scale competition will generate
126 CHAPTER 4 .
high turnover/heterogeneity in the quadrats, 4) Nurse plants do not affect SES, dominance of a given species, ultimately regardless of their effects on plot richness: leading to a high plot richness changes in the competitive outcomes are (intransitivity increases plot richness; Laird not an important factor modulating the and Schwamp 2006, 2008). Alternatively, effect of nurses on plot scale diversity. SES values will be lower if 1) the Differences in SES and plot competitive ability of co existing species is richness values obtained among microsites more equilibrated at the quadrat scale, and were compared using separate one way thus niche segregation prevails, or 2) spatial ANCOVAs for each variable. In these aggregation, and therefore positive effects models, microsite ( Open , Stipa and Shrub – of the nurse on their understorey species, Spain; Open , Shrub and Tree –Australia) prevail (Tirado and Pugnaire 2005). If we was introduced as a fixed factor, and mean analyze the effects of nurse plants on SES plot cover (our surrogate of overall site and plot richness separately, there are four productivity) was used as a covariate. possible responses: 1) Nurse plants have a Standardized Effect Size data were √(x+1) joint effect reducing SES and increasing transformed to meet assumption of plot richness compared to Open microsites: ANCOVA analyse (normal distribution of these plants promote the development of residuals and homoscedasticity). Tukey’s understorey/neighbour species via niche HSD post-hoc tests were used to assess for segregation and this has positive effects on differences among the three microsites of the overall plot scale richness, 2) Nurse each country. We tested for relationships plants increase both SES and plot richness: among the residuals of the ANCOVA and these plants increase quadrat scale nurse plant canopy area using Spearman competition, but species with competitive correlations. This was necessary in order to advantage vary among quadrats, generating assess the importance of nurse size, as we a high species turnover, and therefore could not use nurse size as a covariate in increasing plot scale richness our model because Open microsites do not (intransitivity), 3) Nurse plants increase have a size and the relationships between SES and reduce plot richness: competitive nurse area and their effect on SE and plot exclusion is the dominant interaction richness might not necessarily be linear. between understorey species and a smaller To add confidence to our results, set of competition winners dominate all we also developed an alternative approach
127 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
to detect the relative importance of (see Appendix J for methodological details competitive intransitivity and niche and results). Null model analyses were segregation based on a modification of conducted with Ecosim 7.22 (Gotelli and Whittaker´s beta diversity index (Whittaker Entsminger 2006). ANCOVA analyses 1972). Results from this approach were were carried out using SPSS 13.0 for very similar, and only suggested that it was Windows (Chicago, Illinois, USA). more sensible to detect niche segregation
SPAIN AUSTRALIA
50 60 A B
40 50
30 40
20 30 R2 = 0.66; P = 0.002 speciesrichness speciesrichness 10 20
0 10 30 40 50 60 10 20 30 40 50 60 70 80 mean plot cover (%) mean plot cover (%)
50 65 60 80 C D 60 70 40 50
55 60
30 40 50 50 cover: R 2 = 0.77; P = 0.003
45 20 40 30 Cover(%) Cover(%) 40 2 speciesrichness 30
species richness Cover: R = 0.4; P = 0.047 10 20 35 20 sp richness: R 2 = 0.64; P = 0.017 0 30 10 -200 -150 -100 -50 0 50 100 10 -200 -100 0 100 200 300 - RAINFALL + - RAINFALL +
+ MINIMUM TEMPERATURE/RADIATION -
Figure 4.2. Relationships between cover, our surrogate of standing biomass, and species richness at the community level in Spain (A) and Australia (B), respectively. The relationship between both cover (open dots, continuous line) and richness (black dots, dashed line) and the first axis of a PCA derived from climatic variables is shown for both Spain (C) and Australia (D), respectively. Significant relationships ( P < 0.05) are shown as bold lines.
128 CHAPTER 4
Assessment of niche expansion ANOVA, with microsite pair as fixed We calculated the Chao Jaccard abundance factor. Tukey’s post-hoc HSD tests were based similarity index (hereafter Chao used to assess significant differences among index ; Chao et al. 2005) to assess the pairs. After conducting the analysis, and to relative role of niche expansion by nurse assess the influence of climate in niche plants on community species richness. This segregation, we evaluated the relationship index is based on the probability that two between Climate and Chao index using randomly chosen individuals, one from both linear and quadratic regressions. With each of two samples (referred to as a both approaches we can correctly evaluate “pair”), belong to species shared by both the differences in the understorey samples. It takes into account not only the populations between each microsite (each number of shared species among different nurse type may have different effects on a microsites, but also differences in their given target plant, and this may translate in relative abundances (Chao et al. 2005). We a high dissimilarity not only between assume that, as the influence of niche Nurse/Open microsites, but also between expansion increases, more species should different nurses), and to account for the be present, or more abundant, under a given possible non linear relationships between nurse plant than in Open microsites. We Climate and the effects of the different calculated the Chao index at the community nurse plants tested on their understorey level by summing over the number of vegetation. The Chao index was calculated individuals and species recorded in all using EstimateS 8.2.0 for Windows quadrats for a given microsite within each (Colwell 2000; plot. Thus, the higher the dissimilarity http://viceroy.eeb.uconn.edu/estimates). among nurse microsites and open areas in a ANOVA and correlation analyses were given plot, the higher the effect of niche carried out using SPSS 13.0 for Windows expansion provided by nurse canopies on (Chicago, Illinois, USA). the overall community richness in this plot. Differences in the Chao index between microsite pairs (Stipa/Shrub vs. Open, Shrub/Tree vs. Open, Stipa/Shrub vs. Shrub/Tree for Spain and Australia, respectively) were compared with one way
129 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Table 4.1. Relationship between the indicators of interaction intensity (Relative Interaction Index, RII) and importance (Interaction Importance Index, Iimp) calculated for particular pairwise interactions and Climate . Particular pairwise interactions for both studied regions and the two different nurse microsites tested in each region are included (Stipa/Shrub and Shrub/Tree in Spain and Australia, respectively). The relationship between RII/Iimp and Climate can be nil (0), monotonically positive or negative (+ and -, respectively) or hump-shaped (hs). The last column indicates the number of sites along the gradient in which each species was present.
RII RII Iimp Iimp Spain Sites Stipa Shrub Stipa Shrub Asparragus horridus + + 0 3 Asphodelus ramosus hs Hs hs hs 4 Brachypodium retusum 0 0 0 + 6 Cistus clusii 0 6 Fumana ericoides 0 + 0 7 Fumana thymifolia 0 0 0 0 6 Helianthemum cinereum 0 0 6 Helianthemum violaceum 0 0 5 Rosmarinus officinalis 0 Hs 0 0 8 Sedum sediforme 0 0 6 Stahelina dubia + hs hs 4 Stipa offneri 0 + 0 hs 5 Teucrium capitatum 0 0 0 0 6 Teucrium pseudochamaepytis hs Hs 0 9 Thymus vulgaris 0 0 0 hs 11 Thymus zygis hs + 0 0 3 RII RII Iimp Iimp Australia Sites Shrub Tree Shrub Tree Austrodanthonia caespitosa 0 4 Austrostipa scabra 0 0 0 7 Boerhavia dominii 0 0 hs hs 4 Cenchrus ciliaris 0 4 Chenopodium desertorum hs 0 4 Einadia nutans 0 0 0 + 6 Enteropogon acicularis 0 0 0 6 Maireana enchylaenoides hs 0 0 0 3 Maireana sclerolaenoides hs hs + 4 Sclerolaena muricata + + 5 Sida corrugata 0 0 + 5 Sida cunninghamii 0 0 4 Vittadinia cuneata 0 + 0 + 4
130 CHAPTER 4
Table 4.2. Percentage of pairwise interaction outcomes, as measured with the Relative Interaction Index (RII) and the Interaction importance index (Iimp), explained by the two major current models tested in this work, the Stress-Gradient Hypothesis and the waning of facilitation under extremely high stress (Waning). As a special case in the facilitation waning model, the percentage of cases that are positively related with nurse size (compared with the total number of cases tested) are indicated below. st = Stipa tenacissima , sh = resprouting shrubs in Spain (SP) or inverse cone-shaped shrubs in Australia (AU), and tr = Eucalyptus or Geijera parviflora trees.
RII Iimp Model SP SP AU AU SP SP AU AU (st) (sh) (sh) (tr) (st) (sh) (sh) (tr) Stress Gradient Hypothesis 23.5 29.4 38.5 61.5 17.6 29.4 15.4 7.7 Facilitation 23.5 17.7 23 0 11.8 23.5 15.4 7.7 Waning Nurse size 19 0 23 0 11.8 0 15.4 7.7
RESULTS reaching its maximum value in the more mesic plots. DIVERSITY BIOMASS RELATIONSHIP
AND THE EFFECT OF CLIMATE PLANT PLANT INTERACTIONS AND A total of 96 and 131 perennial species ABIOTIC STRESS were found in Spain and Australia, Contrasting results were found between the respectively, with a plot level richness studied regions. While neither intensity nor ranging from 9 to 47 in Spain, and from 16 importance of plant plant interactions were to 51 in Australia, respectively. The number related to abiotic stress in Spain, we of species found in each plot was linearly detected a hump shaped relationship and negatively related to mean plot cover in between most RII and Iimp values and Spain (Fig. 4.2A). This was particularly rainfall for the Australian sites (Fig. 4.3). evident near the centre of the climatic Both the percentage of facilitation gradient, under conditions of both moderate beneficiaries and obligates tended to drought and moderately low temperatures decrease with rainfall. This negative trend (Fig. 4.2C). In contrast, richness was was found to be significant for beneficiaries largely independent of either cover or in Spain and for obligates in Australia (Fig. climate in Australia (Figs. 4.2B and 4.2D). 4.4). The percentage of plants with more Mean cover at the plot level showed a individuals under the canopy of any nurse monotonic and positive increase with water plant than in Open microsites (facilitation availability in both Spain and Australia, beneficiaries) decreased from about 50% in
the drier and warmer sites to about 30% in
131 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
SPAIN AUSTRALIA
1.0 A 1.0 Stipa (richness) B 0.8 Shrub (richness) 0.8 Shrub (richness) Stipa (cover) Tree (richness) 0.6 Shrub (cover) 0.6 Shrub (cover) Tree (cover) 0.4 0.4
0.2 0.2
0.0 0.0
-0.2 -0.2 Interaction intensity (RII) 2 Tree (cover): R = 0.7; P = 0.005 2 Tree (richness): R = 0.49; P < 0.05 -0.4 -0.4 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 0.6 0.6 C D 0.4 0.4
0.2 0.2
0.0 0.0
-0.2 -0.2
Shrub (cover): R 2= 0.56; P = 0.055 -0.4 -0.4 2 Tree (cover): R = 0.57; P = 0.053
Interaction Interaction importance(Iimp) 2 Tree (richness): R = 0.7; P < 0.05 -0.6 -0.6 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 Climatic PCA axis values
Figure 4.3. Relationships between the indicators of interaction intensity (Relative Interaction Index, RII) and importance (Interaction importance index, Iimp), calculated for both community richness and cover, and the first axis of a PCA derived from climatic variables. Values are means ± SE per plot and microsite. Significant ( P < 0.05) relationships are shown with a bold line; marginally significant ones (0.05 < P < 0.10) are also showed in the figure. the wetter sites for Spain. This relationship positive interactions of each nurse plant and was different, however, for Australia, where climate separately, we found different facilitation obligate plants followed a results depending on the nurse plant unimodal relationship with climate. Only analyzed at both studied regions. We 10% of the species at the community level detected a similar relationship with climate required a nurse plant to occur at the wettest at the community level for Spanish Shrub sites, but this percentage increased up to microsites and Australian Tree microsites, 40% in the driest sites, and showed a but there were no significant relationships maximum ( ca. 60%) at the middle of the for Stipa (Spain) or Shrub (Australia) environmental gradient (Fig. 4.4). When we microsites. We found a marginally tested the relationship between frequency of significant linear relationship between nurse
132 CHAPTER 4
SPAIN AUSTRALIA
40 70 A B Stipa 60 2 30 Shrub Tree: R = 0.51; P = 0.02 Total 50 Total: R 2 = 0.61; P = 0.036 20 40
30 10
20
0 % % facilitation obligates 10
0 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 60 100
C Shrub: R 2 = 0.58; P < 0.005 D 50 Shrub 80 2 Tree Total: R = 0.61; P < 0.05 40 Total 60
30
40 20
20 10 % % facilitation beneficiaries
0 0 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 Climatic PCA axis values
+ RAINFALL -
Figure 4.4. Relationships between the percentage of facilitation beneficiaries (species with more individuals recruiting under nurse plants than in Open microsites) and facilitation obligates (species that only recruit under the canopy of nurse plants), regarding total species richness in each plot, and the first axis of a PCA derived from climatic variables. Significant ( P < 0.05) relationships are shown with a bold line. area and the percentage of the species to predict pairwise interaction outcomes, growing under Stipa (R 2 = 0.34; P = the Spearman correlations between 0.061); the same relationship for Shrub interaction indicators (RII and Iimp) and microsites was not significant. Climate showed that facilitation tended to Relationships among nurse size and decrease monotonically with rainfall in interaction indices were not significant for three of the four cases in Australia ( ρ any microsites in Australia. ranged from 0.27 to 0.46, P < 0.05 in all When testing the validity of the Stress the cases except Tree Iimp; see Fig. 4.5). Gradient hypothesis or alternative models However, these interaction indicators were
133 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS not significantly correlated with Climate in gradient ( Open : 1.03 ± 0.35; Stipa : 0.12 ±
Spain ( P > 0.6 in all cases). When we 0.14, Shrub : 0.03 ± 0.16; means ± SE; F 2,29 visually assessed each pairwise interaction, = 3.01; P = 0.008). Tukey’s HSD post-hoc RII values appeared to decline with rainfall tests revealed differences between Stipa in 38% of the total cases studied, according and Open (P = 0.028) and Shrub and Open to the SGH (Table 4.2). The relationship (P = 0.015) microsites, but not between between RII and Climate was more Stipa and Shrub microsites ( P = 0.961). common in Australia ( Shrub : 38.5%, Tree : Mean plot cover did not affect SES results, 61.5%) than in Spain ( Stipa: 23.5%; but when analyzing the effects of microsite Shrub : 29.4%), which adds confidence to on plot level richness, we found a the results obtained with the overall significant effect of cover (F 1,29 = 53.9; P < Spearman correlations. In contrast, the 0.0001) and a marginal positive effect of relationship between Iimp and Climate was microsite (F 2,29 = 3.01; P = 0.065). Overall, lower, in general. Iimp showed a these results suggest an effective niche decreasing trend with rainfall in 18% expansion by nurse plants, indicating an (Stipa ) and 29% ( Shrub ) of cases for increase in local richness under both Spain, and in 15% ( Shrub ) and 8% ( Tree ) nurses. However, this positive effect of cases for Australia, respectively. The decreased substantially with mean plot intensity and importance of the interactions cover (Spearman correlation between showed a hump shaped relationship when residuals of the ANOVA and mean plot plotted against Climate in 20% and 14% of cover = 0.78; P < 0.0001). Nurse size cases for Spain and Australia, respectively showed no relationship with the residuals (Table 4.2). These cases provided support of the ANCOVA models fitted with both for the facilitation waning model. SES and plot richness in Spain or in However, when we tested the relationships Australia. Differences in competitive between RII, Iimp and nurse size with exclusion among microsites, as measured Spearman correlations, none of these with SES, were not found for the indices was correlated with nurse size in Australian sites ( F2,27 = 2.4; P = 0.101). any of the nurse microsites tested in both countries (ρ < 0.2 in all cases). Competitive exclusion, as indicated by SES values, was lower under the canopy of both Stipa and Shrub than in Open microsites along the entire Spanish
134 CHAPTER 4
SPAIN AUSTRALIA
1.0 1.0 A B
0.5 0.5
0.0 0.0
Shrub: ρ = -0.46; P < 0.0001 -0.5 -0.5 Stipa Tree: ρ = -0.34; P = 0.003 Interaction intensity (RII) Shrub
-1.0 -1.0 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 1.0 1.0 C D Shrub: ρ = -0.27; P = 0.02
0.5 0.5
0.0 0.0
-0.5 -0.5 Shrub Tree Interaction importance (Iimp)
-1.0 -1.0 -200 -150 -100 -50 0 50 100 -200 -100 0 100 200 300 Climatic PCA axis values - RAINFALL +
Figure 4.5. Scatter plot showing the relationship between pairwise facilitation indicators (intensity [RII, panels A and B for Spain and Australia, respectively] and importance [Iimp, panels C and D for Spain and Australia, respectively]) and Climate . Spearman correlation coefficients and P values are shown in each case.
However, microsite significantly affected NICHE EXPANSION plot richness in this country (F 2,26 = 4.05; P Although the similarity index was slightly = 0.03). While the highest richness was lower for Shrub vs. Open microsites (0.64 ± found in Shrub microsites (plot richness = 0.08, mean ± SE, n = 11) than for Stipa vs. 17±1.7 and 11 ± 1.5 for Shrub and Open Open microsites (0.74 ± 0.08), we did not microsites, respectively; mean ± SE; Tukey find significant differences in the similarity HSD: P = 0.029), this effect was less index among nurse microsites in Spain marked in Tree microsites (plot richness = (Stipa vs. Shrub , 0.68 ± 0.06, n = 11;
15.8 ± 1.5; Tukey HSD: P = 0.093 for Tree ANOVA: F 2,29 = 0.622; P = 0.54). Shrub vs. Open microsites). In contrast to the and Stipa microsites shared about 70% of results found in Spain, mean plot cover did their understorey populations with Open not modify the effect of microsite on SES sites. Significant differences in similarity or plot richness. among microsite pairs were found,
135 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
however, in Australia ( F2,26 = 4.57; P = Overall, these results indicate that, while 0.02), suggesting some degree of niche Shrub microsites shared 60% of the expansion. Populations shared between populations beneath their canopies with Shrub Open or Shrub Tree pairs were close both Tree and Open microsites, the to 60%, though the similarity index for similarities between Tree and Open Tree Open microsites showed that they populations were lower ( ca. 40% shared). shared about 40% of the individuals (Tukey Similarity among the microsites tested did HSD post-hoc test; P = 0.034, 0.710 and not show any relationship with Climate in 0.171 for Open Shrub vs. Open Tree , Spain, but two of the three indices Open Shrub vs Shrub Tree , Open Tree vs calculated showed a quadratic relationship Shrub Tree pairs, respectively). with this variable in Australia (Fig. 4.6), suggesting a trend of increasing similarity 1.0 SPAIN
0.8 at both ends of the climatic gradient.
0.6
0.4 DISCUSSION
0.2 Open vs Stipa SPECIES RICHNESS PRODUCTIVITY
0.0 Open vs Shrub Stipa vs Shrub RELATIONSHIP AND THE CONCEPT -200 -150 -100 -50 0 50 100 OF STRESS AUSTRALIA 1.0 The results of our studies from both Spain 0.8 and Australia did not conform with the Chao-Jaccard similarityindex 0.6 hump shaped relationship between richness Open vs Tree: R 2 = 0.64; P = 0.028 2 0.4 Shrub vs Tree: R = 0.63; P = 0.032 and productivity predicted by pioneering Open vs Shrub 0.2 Open vs Tree studies (Grime 1973, Huston 1979). Several Shrub vs Tree 0.0 reviews and meta analyses have questioned -200 -100 0 100 200 300 Climatic PCA axis values the universality of this hump shaped - RAINFALL + relationship (Grace 1999, Waide et al.
1999, Gillman and Wright 2006). Although Figure 4.6. Relationships between Chao- Jaccard similarity index, our surrogate of niche the unimodal richness productivity expansion, and Climate in Spain and Australia. relationship is rarely proven empirically, it Data from the three different microsite pairs for each country (Open vs Stipa, Open vs Shrub, continues to be used to invoke the role of and Stipa vs Shrub for Spain; Open vs Shrub, Open vs Tree, and Tree vs Shrub for Australia) facilitative interactions on increasing plant are shown. Significant relationships ( P < 0.05) are shown as bold lines. community diversity (Hacker and Gaines 1997, Michalet et al. 2006). Previous
136 CHAPTER 4 .
studies have described the roles of stress given plot, but also promote the existence tolerant plants on niche expansion of more of a richer community because of greater competitive species (Lortie et al. 2004a, environmental heterogeneity (Pugnaire et Travis et al. 2005, Michalet et al. 2006). al. 1996a, Maestre and Cortina 2005). However, we argue that, as different species are adapted to different environmental PLANT PLANT INTERACTIONS conditions, their environmental optima will ALONG ENVIRONMENTAL occur at different points along any given GRADIENTS productivity gradient (Chapin et al. 1987, Community productivity in both Spain and Ibañez et al. 2007, Holmgren and Scheffer Australia was limited mainly by water 2010; see also Appendix I). A more general availability, consistent with the framework should consider the species expectations for arid and semiarid specific nature of ‘stress’ (Körner 2003) environments worldwide (Noy Meir 1973, and the ‘distance’ of each species from its Whitford 2002; Fig. 4.2). Thus, the ecological optimum, rather than the negative trend found in the frequency of ecological strategy that it employs. Given positive interactions with increasing rainfall the absence of a clear overarching stress in both areas provides strong support for the level affecting whole plant communities original predictions of the SGH (Bertness along environmental gradients (Chapin et and Callaway 1994). However, at the al. 1987), such a framework is clearly Australian sites, where environmental stress needed. Our results suggest that plant plant seemed to reach extremely high levels (plot interactions not only enhance diversity at cover declined to 17% in some cases; see mid to low productivity levels ( sensu Appendix H), positive effects of nurses on Hacker and Gaines 1997, Michalet et al. community richness decreased at the 2006), but that this effect extends to the highest stress levels, consistent with results entire productivity gradient via from other semiarid environments environmental amelioration by nurse plants (Kitzberger et al. 2000, Maestre and Cortina of the less adapted species to a given set of 2004a, Anthelme et al. 2007). We found environmental conditions (Holmgren and some evidence that increased nurse size Scheffer 2010). This positive effect is could explain increased facilitative effects reinforced because nurse plants not only of Stipa in the Spanish sites. Percentage of increase the available species pool in a facilitation obligate species and the
137 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS intensity of the positive effects on explanation for the positive effects of nurse community diversity increased with Stipa size found in pairwise interactions (Table size, suggesting an increased capacity to 4.2) could result from increased ameliorate harsh environmental conditions heterogeneity in microclimate (e.g. shade, by larger tussocks. However, in contrast to temperature, light) at different parts of the theoretical predictions (Michalet et al. canopy, which would be expected to 2006), nurse area was unrelated to either increase niche segregation (Pugnaire et al. importance, intensity or frequency of 1996a, Maestre and Cortina 2005). Thus, positive interactions at the community level the higher availability of different niches in the other microsites tested. The model and the associated decreases in inter developed by Michalet et al. (2006) was specific competition via niche segregation based on empirical data using mostly (Huston 1979, see discussion below) could tussock like nurses, plants similar to Stipa, enhance the performance of particular or cushion like plants (e.g. Choler et al. species more than any increase in the ability 2001, Callaway et al. 2002, Liancourt et al of the nurse to buffer environmental 2005, Anthelme et al. 2007). Small stressors per se. increases in the size of these nurses are Our results demonstrated likely to have relatively large facilitatory inconsistent relationships between effects on understorey species (Michalet et environmental stress and both interaction al. 2006, Anthelme et al. 2007). However, intensity and importance, contrary to relatively small changes in large nurse prevailing facilitation theory (Brooker et al. plants, such as the Australian eucalypt trees 2005, Callaway 2007). In Spain, neither (with canopy areas up to 200 m 2), would be interaction intensity nor importance were less likely to be influential. We suggest related to the environmental gradient we caution, therefore, in generalizing the evaluated, but a hump shaped relationship effects of nurse plants in semiarid for both facilitation/competition indicators environments without a consideration of was found in Australia. How can we their size. Even when the smallest nurse account for this difference? Environmental plants almost always exceed an area of 1.5 stress in the Spanish gradient was driven by m2, such as the microsites tested in this two negatively correlated and distinct studies (excepting Stipa ), we would not stressors; water and radiation/temperature. expect a strong relationship between nurse Thus, it is likely that in the coldest or size and their tendency to alleviate warmest extremes of this gradient, less environmental stress. An alternative cold or drought adapted plants would
138 CHAPTER 4 .
benefit from nurse canopies, respectively (Kitzberger et al. 2000, Soliveres et al. (Choler et al. 2001, Liancourt et al. 2005). 2010). This facilitative role collapsed at This may explain why the net positive extremely high stress levels. The most effects of nurse plants were equally intense parsimonious explanation for this is that or important at the community level along facilitation collapsed because species with the entire gradient (Tilman 1988). Indeed, low tolerances to drought and/or herbivory this is suggested by the fact that the were unable to overcome the environmental proportion of facilitation obligate species filters controlling their recruitment, was not significantly related to climate in regardless of the presence of nurse plants this region. The higher number of (Kitzberger et al. 2000, Ibañez and Schupp facilitation beneficiary species under drier 2001, Michalet et al. 2006, Soliveres et al. conditions could be related to the fact that, in press ), and therefore could not be regardless of their physiological adaptions included in our pairwise analyses. Thus, the or environmental optima, germination and positive effects on richness and productivity recruitment of most semiarid species are at the community level collapsed under limited by periods of adequate soil moisture these extremely stressful conditions (Forey (Westoby 1978/79). These periods are more et al. 2009). This is consistent with easily achieved under the more shaded observations of higher percentage of onditions beneath nurse plants than in Open facilitation obligate species and lower microsites (Franco and Nobel 1989). similarity at moderate levels of drought Therefore, under drier conditions we would stress, and with the breakdown of these likely record more individuals of most of effects under extremely high levels of species under the canopy of nurse plants drought (Fig. 4.4). than in Open microsites (Kitzberger et al. 2000). The environmental stress in the THE EFFECT OF PLANT PLANT eastern Australian gradient was INTERACTIONS ON DIVERSITY: predominantly driven by a single stressor, NICHE EXPANSION AND rainfall, through its influence on soil SEGREGATION moisture availability. Consequently, nurse The results from the Chao index of plants could conceivably have an important similarity, and the lack of relationship role in allowing recruitment and persistence between this index and Climate (Fig. 4.6), of taxa less adapted to low soil moisture suggest that facilitation from nurse plants
139 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS promotes niche expansion for the less ecological strategy (Prider and Facelli 2004, adapted species to the given environmental Maestre et al. 2009a). conditions present in a particular site across In contrast with previous studies the gradient, rather than increased niche (Tielbörger and Kadmon 2000b), our expansion of competitive species under results showed that nurse plants affected the harsh conditions . Our results partially competition outcomes of their understorey contrast with previous studies, which have vegetation in comparison with Open areas suggested that stress tolerant species through increases in niche segregation, but increase the realized niche of competitive not by increasing competition intransitivity. species on harsh (i.e. drier) environments While this was apparent in Spain, it was not (Travis et al. 2005, Michalet et al. 2006). in Australia. On the Spanish gradient, We argue that this is not caused by the competitive exclusion was significantly stress tolerator or competitor strategy of the lower under nurse canopies than in Open species involved, but rather the distance of microsites. This could be explained because each target species to its ecophysiological the more productive conditions found under optimum. It should be realized that about the nurse plants allowed more species to 20 30% of the sampled species recruited recruit. Since nurse plants provide some only under the canopies of nurse plants degree of microclimatic heterogeneity (Fig. 4.4), regardless of the environmental (Pugnaire et al. 1996a), the joint effect of conditions present in each plot. The total both processes (increase in species pool and percentage of facilitation obligate species variability in the resources that these (when considering both microsites together) species compete for) might increase niche was greater than those for separate segregation, and therefore local diversity microsites in both the Spanish and (Huston 1979, 1999, Silvertown 2004). We Australian gradients surveyed. These results found, however, that despite the relatively suggest that the identity of facilitation constant effect of nurse plants upon the obligate species changed according to the competitive outcome of their understorey particular nurse plant examined. These vegetation, the effect of nurses on local changes in the identity of facilitated species diversity decreased with productivity. It is depending on the nurse plants were, conceivable that the relative differences in perhaps, due to their different phylogenetic the microenvironmental conditions between relationships (Valiente Banuet and Verdú nurse and Open microsites that allowed 2007, 2008) or to differences in their more species to recruit under nurses than in the unvegetated interspaces declined under
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wetter conditions. In Australia, the lack of PAIRWISE INTERACTIONS AND THE nurse effects on competitive outcomes, but ABSENCE OF AN APPROPRIATE their positive effect on local diversity, may EXPLANATORY MODEL have resulted from environmental buffering None of the models we tested i.e. SGH (both microclimatic amelioration and (Bertness and Callaway 1994) or grazing protection), allowing fewer Facilitation waning model (Michalet et al. drought and herbivory tolerant species to 2006, Maestre et al. 2009a; see Fig. 4.1) recruit, and therefore increased diversity by predicted more than 60% of the pairwise direct facilitation. However, their relative interactions studied (see Tables 4.1 and homogeneous microenvironmental 4.2). The percentage of cases explained, conditions did not allow niche segregation however, varied strongly among microsites to occur (Huston 1979). In contrast with and regions, as well as with the identity of previous studies (Bowker et al. 2010), we the particular nurse plant (Callaway 2007, did not find an important contribution of Table 4.2). These results highlight the competition intransitivity to local species difficulties in establishing generalities when richness in any of the studied regions, even predicting how the outcome of plant plant in the more productive and heterogeneous interactions change along environmental environments beneath nurse plants. This gradients. Our results are not completely could be a matter of scale, since the unexpected, as plant plant interactions are availability of slightly different niches (i.e. driven by a complex set of factors including differences in shade or nutrients), even at the number and type of stressors considered the 0.5 m × 0.5 m scale, might prevent the (Baumeister and Callaway 2006, Maestre et changes in competitive dominance of al. 2009a, le Roux and McGeoch 2010), the different species depending on the different particular adaptations of species to cope conditions in each quadrat, causing the with current environmental conditions niche segregation, rather than competitive (Choler et al. 2001, Liancourt et al. 2005), exclusion at this scale. the relative effect of nurse shade on target plants (Holmgren et al. 1997, Prider and Facelli 2004, Soliveres et al. 2010), phylogenetic relationships (Valiente Banuet and Verdú 2007), and the ontogenetic stage of interacting plants (Callaway and Walker
141 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
1997, Miriti 2006, Soliveres et al. 2010). CONCLUDING REMARKS This complex array of mechanisms Our study has highlighted the fact that involved in the outcome of particular nurse plants increase local richness of plant pairwise interactions makes it extremely communities across broad environmental difficult to develop general predictions gradients. Nurses increase niche about the response of a given pairwise segregation and species coexistence by interaction to particular environmental providing a range of available niches conditions without a detailed knowledge of beneath their canopies, thereby allowing many of the attributes described above. species that are less adapted to a particular Extrapolation from a few pairwise position within the gradient to survive and comparisons to the broader community of recruit (niche expansion). Our results show species should only be made with extreme that the importance of nurse plants is caution. Future general models aimed at relatively constant along environmental predicting the outcomes of particular gradients when different independent pairwise interactions should therefore stressors (e.g. low temperature and rainfall, consider the complexities and multiplicity herbivory) have differential effects on the of mechanisms shaping such outcomes. We stress experienced by different species suggest here that this complexity could be within the community. However, the better integrated by using a surrogate of the importance of niche expansion increases distance of each target species from its along environmental gradients when a optimum, either from detailed knowledge given stressor, or a combination of of its physiological tolerances (i.e Choler et positively correlated stressors (e.g. high al. 2001, Liancourt et al. 2005) or by temperatures and salinity or drought), phylogenetic derived assumptions affects the stress level of different species (Valiente Banuet and Verdu 2007). The within the community (e.g. Callaway et al. outcomes of pairwise interactions could 2002). In the latter case, this positive effect therefore be better predicted by using a is likely to collapse under extremely high distance to optimum approach rather than levels of stress through several mechanisms an approach that considers all species in a previously discussed in the literature given community equally, by invoking the (Michalet et al. 2006, Smit et al. 2007, stress gradient model. Maestre et al. 2009a). Given the clumped nature of vegetation in arid and semiarid areas, and thus the tendency for plants to interact, it is
142 CHAPTER 4 .
not surprising to find that plant plant multiple models, such as that followed in interactions play a major role in shaping the this study, may provide important insights relationships between richness and into the mechanisms driving such productivity in these environments. outcomes, and on the community and However, our results indicate that the effect ecosystem level consequences of plant of these interactions on increasing or plant interactions. By using a multiplicity of decreasing richness along environmental conceptual and analytical approaches, and gradients is more complex than previously an appropriate dataset collected in two thought, and depends on the number of contrasted semiarid regions, our study stressors involved and their provides a more complete mechanistic interrelationships. Our findings also help to understanding of the relative role of biotic, explain why the unimodal relationship non trophic interactions and environmental between diversity and productivity is rarely conditions shaping local richness. It also found in arid and semiarid environments helps to refine our predictions of the (Waide et al. 1999). We maintain that the response of plant communities to outcome of particular pairwise interactions environmental gradients, and clarifies the is best predicted by the distance of a given relative importance of biotic interactions as plant to its environmental optimum rather a driver of such responses. than by an overarching stress gradient. This ACKNOWLEDGMENTS has profound implications for interpreting We thank David Tongway and Nick Reid for their previous studies evaluating the interplay help during plot selection and fieldwork in Australia. Nick Reid also hosted SS during a research stay in between facilitation and competition along his lab. Nick Schultz, Megan Good, María D. Puche, Pablo García Palacios, Erin Roger, Ian Telford, stress gradients, and should be considered James Val and Madeleine Rankin assisted with fieldwork and/or plant identification. Peter Weston, by future research on this important theme Anthony Gibson, Kevin Mitchell, Andrew Mosely and Patty Byrne allowed us access to their properties of community ecology. We highlight the and gave us valuable information on land fact that the complex array of mechanisms management issues in semiarid Australian woodlands. SS was supported by a PhD fellowship shaping the outcomes of pairwise plant from the EXPERTAL project, funded by Fundación Biodiversidad and CINTRA S.A. This research was plant interactions makes it difficult to funded by the CEFEMED, INTERCAMBIO (BIOCON 06/105) and REMEDINAL projects, develop a universal model that is able to funded by the Universidad Rey Juan Carlos Comunidad de Madrid, Fundación BBVA and successfully predict their outcome along Comunidad de Madrid, respectively. FTM environmental/productivity gradients. We acknowledges support from the European Research Council under the European Community's Seventh propose that approaches considering Framework Programme (FP7/2007 2013)/ERC
143 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Grant agreement n° 242658. DJE is supported by grant LP0882630 from the Australian Research Co
144 CHAPTER 4 .
Supplementary material for Chapter 4.
Appendix H. Characteristics of vegetation types and sites selected Stipa tenacissima grasslands, the vegetation type selected in Spain, constitute one of the more important European/North African ecosystem types, as they can be found from the semi desert steppes of Ukraine to the western Mediterranean (Izco 1984), with the greatest extensions being found in the Maghreb and the Iberian Peninsula (Le Houeróu 1986, 2001). In the semiarid parts of the Mediterranean Basin, these grasslands are distributed over 32,000 km 2 in a thin latitudinal fringe in North Africa, from Libya to Morocco, and in the southeastern Iberian Peninsula (Le Houérou 2001). See Maestre et al. (2009b) for a detailed account of the natural history of this ecosystem. Soils in the Spanish plots are Lithic calciorthid (Soil Survey Staff 1994) and characterized by a high CaCO 3 content, high pH values, low depth, and a stony surface. Sites in the semiarid woodlands in eastern Australia were located in the Bimble box (Eucalyptus populnea )–White cypress pine (Callitris glaucophylla ) alliance on the Cobar Pediplain, the Belah ( Casuarina pauper )–Rosewood ( Alectryon oleifolius ) woodlands in far western New South Wales (NSW), and woodlands dominated by White box ( Eucalyptus albens ) in central western NSW. While these communities have slightly different community dominants, physiognomically they are similar and characterized by an open woodland on clay loam soils with canopy cover ranging from 18 70% (Keith 1998). The midstorey shrub cover at all sites varied depending on grazing intensity and rainfall (Beadle 1948). Soils in the Australian plots were non sodic Kandosols to Demosols under the Australian classification (Isbell 1996), or a mixture of Luvisols, Yermosols and Ferrasols (FAO 1998) and are commonly grouped as Red earths (Stace et al 1968). They are characterized by deep clay loam to loamy surface textures with a gradual increase in clay content with depth. They have relatively low available nutrient and water holding capability (Isbell 1996).
145 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Table S7. Main charactertistics of the study sites. TSR = travelling stock reserve.
Mean Annual projected Site Latitude Longitude Land use Country rainfall Cover
(mm) (%)
Australia Cowra 33º50’41”S 148º36’12”E TSR 630 70
Australia Quandialla 33º53’19”S 147º51’27”E TSR 570 51 Australia Nevertire 31º51'27"S 147º42´28”E TSR 490 70
Australia Condobolin 33º07’15”S 142º24’44”E State Forest 455 18
Australia Nyngan1 31º10’00”S 142º24’44”E Grazing 406 31
Australia Nyngan2 31º10’00”S 142º24’44”E Grazing 406 43
Australia Florida 31º33’22”S 146º18’35”E Grazing 398 44
Australia Truganini 32º07’00”S 146º39’50”E property 375 44
Australia Etiwanda 32º09’40”S 145º53’40”E Grazing 360 21
Australia Buronga 34º07’35’’S 141º05’09”E Grazing 280 35
Spain Barrax 39º02’91’’N 2º13’82’’W Hunting area 433 46
Spain Camporreal 40º19’72’’N 3º25’36’’W Hunting area 457 54
Spain Carrascoy 37º48’02’’N 1º18’32’’W Hunting area 282 37
Spain Crevillente 38º14’15’’N 0º55’49’’W Hunting area 273 35
Spain El Ventós 38º28’14’’N 0º37’03’’W Hunting area 319 36
Spain Morata 40º27’62’’N 3º05’31’’W Hunting area 455 58
Spain Sierra Espuña 37º49’27’’N 1º40’41’’W Hunting area 364 49
Spain Titulcia 40º11’28’’N 3º30’13’’W Hunting area 440 57
Spain Villarrobledo 39º12’64’’N 2º30’77’’W Hunting area 446 63
Spain Yecla 38º35’40’’N 1º12’15’’W Hunting area 350 36
Spain Zorita 40º21’30’’N 2º52’62’’W Hunting area 434 45
146 CHAPTER 4 .
SPAIN AUSTRALIA
Figure S2. General appearance of the vegetation types studied in Spain and Australia.
147 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Appendix I. Measuring community composition changes across environmental gradients
To test for differences in community composition across the environmental gradient, we constructed for each country a data matrix comprising the relative frequency of each species in the 80 1.5 m by 1.5 m quadrats within each plot. Thus, a species occurring in all 80 quadrats at a given site received a relative frequency of 100%. We examined differences in community structure between the sites with Multi Dimensional Scaling (MDS) after applying a fourth root transformation to the data to downweight the influence of the most dominant species (Clarke and Warwick 2001). Extremely rare species (those appearing in less than the 1% of the sampled quadrats), were removed prior to analysis as recommended to improve the clarity in the analyses (Anderson et al. 2008). These rare species accounted for about half of the sampled species (46 of 96 for Spain, 57 of 131 for Australia). We used the Bray Curtis distance measure to construct the similarity matrix. This distance measure controls for the relative abundance of each species in a given matrix, and helps to avoid the undue influence of extremely abundant or extremely rare species (Clarke and Warwick 2001). We carried out these analyses using PRIMER v6 statistical package for Windows (PRIMER E Ltd., Plymouth Marine Laboratory, UK). We analysed the data in both two and three dimensions, and then chose the 2 D ordination, because it provided satisfactory results (i.e. low stress values) for both studied regions ( Stress = 0.10 and 0.12 for Spain and Australia, respectively). The stress value reflects how well the data can be represented in any given number of dimensions. Stress values < 0.05 indicate that the n axes provide an excellent representation of the relationships among samples, while values of > 0.20 are regarded as a poor representation. We performed the analyses with 25 random starts to reduce the risk of finding a local instead of the global minimum of this stress function. To identify the species or abiotic factors responsible for the ordination patterns found, the first two axes of the MDS biplot were correlated with the PCA axis obtained with climatic data (Climate ) and with the abundance of each species in each plot using Spearman correlation coefficients. For the latter analyses, only the species present in at least three of the 80 plots were considered. Variables with a correlation coefficient > 0.5 are represented in the MDS plot (Fig. B1). The ordination (see Figure below) showed a significant effect of rainfall on community composition in Spain, where different species were related both positively or
148 CHAPTER 4 .
negatively with this factor, depending on their ecophysiological tolerances. However, this effect was less clear in Australia, suggesting the existence of unmeasured factors affecting community composition. The relatively high density of domestic and native herbivores in the Australian semiarid zone (Noble and Tongway 1986) suggests that different levels of grazing pressure among plots could be one such factor.
1.5 A 1.0 Villarrobledo Yecla Camporreal 0.5
El Ventós Morata 0.0 Sierra Espuña MDS 2 MDS Carrascoy Barrax -0.5 Ch: 0.85 Tz: 0.70 Crevillente
-1.0 Titulcia Zorita
-1.5 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 MDS 1
Rainfall: 0.79 Hh: 0.70 Gs: 0.67
Ac: 0.69 Ar: 0.64 Br: 0.61 Ss: 0.67 Ft: 0.77 Hc: 0.87 Hv: 0.62
1.5 B Nevertire 1.0
Buronga 0.5 Etiwanda Truganini Gibson2 0.0 Al:0.75 Florida
MDS2 Quandialla -0.5 Gibson1 Cowra Rainfall:0.59 Me:0.81 Cal: 0.80
-1.0 Condobolin
-1.5 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0 MDS 1
Ed: 0.64 Des: 0.75 Cs: 0.65 Pd: 0.75 Scl: 0.66
Fig. S3 . MDS plot showing the dissimilarity distance among communities of the plots sampled along environmental gradients in Spain (A) and Australia (B). Spearman correlation coefficients >0.5 are showed in a box for each axis. Legends are: Rainfall = Climatic PCA, highly correlated with rainfall in both countries. Spain: Tz = Thymus zygis , Gs = Genista scorpius ; Ch = Carex humilis ; Ac = Anthyllis citisoides ; Ar = Asphodelus ramosus ; Br = Brachypodium retusum ; Ss = Sedum sediforme ; Ft = Fumana thymifolia ; Hh, Hc and Hv = Helianthemu hirtum , H. cinereum and H. violaceum , respectively. Australia: Al = Atriplex leptocarpa ; Me = Maireana enchylaenoides ; Cal = Calotis sp.; Ed = Eragrostys dielsii ; Des = Desmodium sp.; Cs = Cheilantes sieberi ; Scl = Sclerolaena sp.; Pd = Panicum decompositum.
149 BIOTIC INTERACTIONS DRIVE LOCAL SCALE RICHNESS
Appendix J. An alternative approach to measure changes in competitive outcomes depending on microsite As stated in the main text, three principal mechanisms may determine competitive outcomes in the vegetation in Open microsites and under nurse plants: competitive exclusion, intransitivity and niche segregation. While competitive exclusion is likely to cause low diversity at the plot scale, both intransitivity and niche segregation are likely to increase it. We aimed to to test for differences in the competitive outcomes among the three microsites tested in each country. As an alternative approach to that presented in the main text, we developed an index based on Whittaker´s beta diversity index (Whittaker 1972): A/(B 1), where A is the global species richness, and B the local species richness. In our case, A will be the species richness found under each microsite at the whole plot level, while B will be the species richness found in each one of the quadrats sampled for each microsite ( n = 30). To calculate B, those quadrats with no species occurring on them where not considered. The rationale behind this approach is similar to that described in the main text: 1) if competitive exclusion dominates, we will find a reduction of B causing a decrease in A (few dominant species will control all the space available; low B, low A = competitive exclusion); 2) if intransitivity dominates, we will find a low B but a high A because of few dominant species will dominate at the small scale (quadrat): however, the identity of these dominant species will change depending on the particular environmental conditions of each patch and the original species mixture that colonized it. This will generate a high turnover of species that will increase the plot scale richness (low B, high A = competition intransitivity); 3) if niche segregation dominates, both A and B will be high. At small spatial scales, the differential exploitation of resources (niche segregation) will enhance species coexistence, and therefore increase the chances of several species to recruit and coexist under a given microsite (high B, high A = niche segregation). We analyzed separately both A and B with univariate ANCOVA models, with microsite (three levels) as fixed factor and mean plot cover (a surrogate of productivity) as a covariate (Table S7).
150 CHAPTER 4 .
Table S8. ANCOVA results for both small-scale (B) and plot-scale (B) richness for studied region.
Underlying Variable Factor df F P value Effect mechanism Reduction of Higher niche Cover 1,29 53.9 <0.0001 A microsite effect segregation Microsite 2,29 3.0 0.65 Nurses increase A under nurse plants, this Reduction of difference Spain Cover 1,29 8.1 0.008 microsite effect B reduces with Microsite 2,29 4.7 0.017 Nurses increase B higher productivity Cover 1,26 0.2 0.628 None Higher niche A segregation Microsite 2,26 4.0 0.030 Nurses increase A under nurse Cover 1,26 2.7 0.113 None plants, regardless Australia B of ecosystem Microsite 2,26 4.0 0.030 Nurses increase B productivity
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152
On the relative importance of climate and biotic non-
trophic interactions as drivers of local plant species 5 richness in semiarid communities
Santiago Soliveres, Rubén Torices, Fernando T. Maestre. Manuscrito en revisión en Journal of Ecology
BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY
154 CHAPTER 5
ABSTRACT
Molecular phylogenies are being increasingly used to get new insights on the mechanisms structuring plant communities. However, the large number of factors potentially affecting the phylogenetic structure of plant communities cautions against the sole use of this information to properly infer the mechanisms shaping them. We jointly evaluated the effects of environmental conditions and biotic interactions on the phylogenetic structure of 11 semiarid Stipa tenacissima L. communities along an ample environmental gradient. We also assessed the relative importance of phylogenetic relatedness (PD) and abiotic conditions as drivers of pairwise interactions across such gradient. Habitat filtering and biotic interactions promoted a random phylogenetic structure in most of the communities studied. While positive biotic interactions increased phylogenetic evenness by niche expansion and habitat differentiation, more benign environmental conditions reduced this evenness indirectly by reducing the effects promoted by nurse plants. Phylogenetic relatedness was the primary factor affecting pairwise interactions. Values of this variable between 207 272.8 Myr led to competition, those outside this range led to neutral or positive interactions, depending on climate. Our study illustrates, for the first time, the relative importance of climate and biotic interactions on the phylogenetic structure of plant communities, and shows how the evolutionary relationships and environmental conditions interact to determine particular pairwise interactions. We also provide a comprehensive set of easy to measure and interpret tools for avoiding misleading interpretations when inferring mechanisms from phylogenetic structure data in observational studies.
155 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY
INTRODUCTION structure alone insufficient to properly
he recent development of infer the mechanisms shaping plant molecular phylogenies has communities (Cavender Bares et al. 2009, provided ecologists with a Myfield and Levine 2010). Thus, more T comprehensive approaches, including the powerful tool to get new insights on the mechanisms structuring plant communities study of environmental factors and co (Webb et al. 2002). The phylogenetic occurrence patterns, have been structure of a given community has been recommended to further refine the extensively used to assess the relative conclusions drawn from phylogenetic importance of environmental conditions methods (Pausas and Verdú 2010). (environmental filtering) or competition as Positive interactions among plants drivers of community structure (reviewed have been shown to largely influence the in Webb et al. 2002, Cavender Bares et al. structure and diversity of plant 2009, Vamosi et al. 2009). Biotic communities in virtually all terrestrial interactions and environmental conditions ecosystems (Callaway 2007, Brooker et al. are known to interactively affect plant 2008), and can even promote the expansion community structure and dynamics of realized species niches over (Butterfied et al. 2010). However, the evolutionary time frames (Valiente Banuet relative importance of both factors as et al. 2006). These interactions have been drivers of the phylogenetic structure of shown to depend up to a great degree on plant communities is still poorly the abiotic environment (Callaway 2007; understood (Cavender Bares et al. 2004, Maestre et al. 2009), and on the Verdú et al. 2009). Furthermore, the phylogenetic distance (hereafter PD) phylogenetic structure of a given between the interacting species (Valiente community may be strongly affected by Banuet et al. 2006, Castillo et al. 2010). other factors, including herbivore or Overall, these studies suggest that positive pollinator preference for closely related interactions are more likely to occur taxa (Webb et al. 2006), the scale among phylogenetically distant species considered (Kraft and Ackerly 2010), or pairs, or under harsh environmental differences in niche and competitive ability conditions (e.g. Callaway 2007, Valiente among co occurring species (Myfield and Banuet and Verdú 2007). In the same way Levine 2010). This complex array of that the different ontogenetic stages of factors makes the use of phylogenetic involved species interact with their PD in defining the outcome of pairwise plant
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plant interactions (Valiente Banuet and aimed to do so by simultaneously Verdú 2008, Castillo et al. 2010), both measuring the phylogenetic structure, environmental conditions and PD are likely different components of biotic interactions to jointly determine the outcome of these (co occurrence patterns, niche expansion interactions, and hence the structure of promoted by nurse plants, and differences plant communities. Although it is expected in the environmental filtering among that harsh environmental conditions cause facilitated/non facilitated species guilds), phylogenetic clustering (Webb et al. 2002), and a set of environmental conditions in 11 the prevalence of pairwise positive semiarid Stipa tenacissima communities interactions at the community level might located along an environmental gradient in lead to an even phylogenetic structure Spain. Additionally, we assessed how the (Valiente Banuet and Verdú 2007). abiotic conditions, the PD between the Therefore, knowing how PD and involved species, and the interaction environmental conditions jointly affect the between both factors modulated a large set outcome of pairwise species interactions of pairwise interactions outcomes along will provide additional insights to such gradient. We addressed the following understand the relative importances of questions: How do environmental filtering environmental filtering and biotic and biotic interactions jointly affect the interactions as drivers of the phylogenetic community phylogenetic structure across structure of entire plant communities environmental gradients?, and What is the (Cavender Bares et al. 2009). relative importance of PD and abiotic To our knowledge, no previous conditions in defining the outcome of study has evaluated the relative particular pairwise interactions? importances and joint effects of biotic interactions and environmental conditions as determinants of the phylogenetic structure of whole plant communities along wide environmental gradients, nor the joint effects and the relative roles of PD and environmental conditions as drivers of pairwise plant plant interactions. We
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Figure 5.1 Conceptual model synthesizing the unifying approach employed in this study at both community and pairwise levels. Arrows are the different processes considered affecting community assemblage and its phylogenetic structure. Circular boxes represent the surrogates of each process measured in this study. The phylogenetic structure of a given community will be affected by several factors such as abiotic conditions (i.e. environmental filtering) or biotic non-trophic interactions (i.e. facilitation/competition shifts, niche expansion or double environmental filtering [phylogenetic clustering among facilitated/non-facilitated species guilds, or differences in similarity among microsites]). However, these processes do not affect independently the community assemblage and they are likely to interact in many ways. We tested for shifts in the biotic interactions across a wide environmental gradient and how they affect the phylogenetic structure of the studied community. At the pairwise level, interaction outcomes should be more positive when these conditions represent higher stress (i.e. low rainfall, cold temperatures; Callaway 2007). A different line of inquiry highlights that the phylogenetic distance (PD) between involved species as a crucial factor affecting these interactions; the outcome will be more positive when higher the PD among the species involved
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(Valiente-Banuet et al. 2006, Valiente-Banuet and Verdú 2007, Castillo et al. 2010). We hypothesize that the PD distance between a nurse plant and a given beneficiary would need to increase for their interaction to be positive as abiotic conditions become less stressful.
MATERIALS AND METHODS the survey described below. In each site,
STUDY AREA we located four 30 m long transect We studied 11 Stipa tenacissima downslope for the vegetation survey, each communities along a climatic gradient 8 m apart across the slope. Along each × spanning from the center to the south east transect, we placed 20 contiguous 1.5 m of Spain (see Table S9). Our sites have 1.5 m quadrats, and recorded the annual precipitation and temperature presence/absence of each perennial plant values ranging from 273 mm to 488 mm, species within each quadrat. and from 13ºC to 17ºC, respectively. To To evaluate particular pairwise minimize the experimental noise produced interactions for both dominant nurse types by environmental factors other than in the study region (sprouting shrubs and S. climate, which could affect our tenacissima tussocks, hereafter Shrub and conclusions, all the sites shared the same Stipa microsites, respectively), and to general soil type ( Lithic Calciorthid , Soil assess the total number of facilitated Survey Staff 1994), and had similar species at each site, we established a orientation and slope values. Vegetation complementary sampling design. We was in all cases an open grassland randomly selected ten Stipa tussocks in dominated by S. tenacissima , with total each site, and sampled the total area under cover values ranging from 35% to 68%. their canopy using 0.5 m × 0.5 m quadrats Sparse resprouting shrubs like Quercus (~30 quadrats per site). Ten paired open coccifera , Pistacia lentiscus or Rhamnus areas (areas located at least 1 m away from lycioides were also present in all sites. any Stipa tussock or resprouting shrub, hereafter Open microsite), were randomly VEGETATION SURVEY selected adjacent to these tussocks. The At each site we established a 30 m × 30 m same number of 0.5 m × 0.5 m quadrats plot containing the representative sampled in each Stipa microsite was vegetation of the surrounding area. This sampled in each Open microsite selected, plot size allowed the inclusion of a number to balance the sampling effort. Finally, the of shrub patches large enough to conduct same area was also sampled under the
159 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY canopies of five sprouting shrubs (mostly This procedure resulted in the fixation of Q. coccifera , Appendix K). The abundance 48 nodes (representing more than 70% of (number of individuals) of all perennial internal nodes of our tree). plant species was recorded within each Once we assembled the sampled quadrat. phylogenetic tree for all the species surveyed (Fig. S8), we measured two ASSESSMENT OF PHYLOGENETIC different indicators of phylogenetic STRUCTURE relationships among co occurring plants at We assembled a phylogenetic tree for the each of our sites: the mean phylogenetic 86 species included in this study using distance (hereafter MPD; Webb et al. Phylomatic2 (Webb et al. 2008). All the 2002), and the pairwise PD among every families in our dataset matched the family possible pair of co occurring species in names of the angiosperm megatree used in each site. Since MPD is related to the Phylomatic (R20091110.new), which was species pool, we avoided this confounding based on the APG III phylogenetic factor by calculating its standardized effect classification of flowering plant orders and size (SES) with the Picante package for R families (Angiosperm Phylogeny Group (Kembel et al. 2010), version 2.10.1 (R 2009). Within family phylogenetic Development Core Team 2009). It was relationships were further resolved based calculated as (MPD obs MPD sim ) on data from various published molecular sdMPD sim , where MPD obs was the phylogenies (Appendix K, Table S10). observed value of MPD, and MPD sim and
After assembling the phylogenetic tree, we sdMPD sim were the mean and standard adjusted its branch lengths with the help of deviation, respectively, of this index the Phylocom BLADJ algorithm, which obtained from the 1000 simulations fixes the age of internal nodes based on performed under the null model. Positive clade age estimates, whereas undated SES, and with a P value > 0.95 indicate internal nodes in the phylogeny are spaced significant phylogenetic evenness in the evenly (Webb et al. 2008). According to sampled community, while negative SES Vamosi and Vamosi (2010), we used with P values < 0.05 indicate phylogenetic TimeTree (Hedges et al. 2006) to fix as clustering. many nodes in the tree as possible (see Appendix K for methodological details).
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Figure 5.2 Graphical synthesis of the results obtained. Different surrogates of biotic interactions (C-E), environmental filtering (A) and their interactions (B) are separated. Blue arrows indicate an increase in community phylogenetic evenness due to a given mechanism, while red arrows mean an increase in phylogenetic clustering (dashed lines indicate an indirect effect). Crossed-red circles indicate no effect (in the case of arrows) or no interaction with climate (in the case of variables). MPD = mean phylogenetic distance among all possible species pairs of a given site; MPDfac = mean phylogenetic distance among pairs of the cluster of facilitated species; C-score = standardised effect size of the C- score; Similarity = Chao-Jaccard abundance-based similarity index calculated for Stipa vs. Open or Shrub vs. Open microsites; % Obligates = percentage of species found only under a nurse plant comparing to the total species richness found in each site; Climate = values of the first axis of a PCA performed with eight environmental variables. Detailed statistical results from each relationship shown in this figure are in Fig. S10.
EVALUATING PLANT PLANT level by using the SES of the C score INTERACTIONS AT THE index (Gotelli et al. 2000). This metric is COMMUNITY LEVEL commonly used to assess the outcome of The 80 1.5 m 1.5 m quadrats surveyed at biotic interactions at the community level each site were used to examine the co (e.g. Rooney et al. 2008, Bowker et al. occurrence pattern at the whole community 2010), and was calculated as described
161 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY above for the MPD (see Appendix K for Stipa/Shrub and Open microsites will methodological details). indicate higher influence of niche To measure niche segregation or differentiation provided by nurse canopies. the “double habitat filtering” (see below) We calculated the CI by summing over the promoted by nurse plants we used two number of individuals and species recorded different measurements: 1) the Chao in all the 0.5 m × 0.5 m quadrats per Jaccard abundance based similarity index microsite and site ( n ~ 30) using EstimateS (hereafter CI; Chao et al. 2005), and 2) the 8.2.0 for Windows (Colwell 2000). We difference between MPD for the whole set also compared the MPDfac and MPDnf of species in a given community (described with the MPD index (see rationale in above), and the MPD for only the Assessing the effects of environmental facilitated/non facilitated species guilds filtering and biotic interactions on (MPDfac and MPDnf, respectively). We community phylogenetic structure below). refer here to “double environmental Finally, to evaluate the degree of filtering” to describe the effect of the the realized niche expansion ( sensu Bruno different environmental conditions found et al. 2003) provided by nurse plants, we in Open or nurse microsites, which calculated the percentage of facilitation generate different understorey species obligates (sensu Butterfield 2009), in guilds for each microsite (i.e., higher comparison to the total number of species dissimilarity among microsites; Badano found in each site. Facilitation obligates and Cavieres 2006). These guilds could be were those species with individuals phylogenetically clumped within each recruiting only under a nurse plant, and microsite because of their shared therefore, only able to colonize a given site adaptations to the same environmental under the microclimatic protection conditions, but can be phylogenetically provided by nurses. even at the whole community level because of the different environments EVALUATING PLANT PLANT existing at each site, i.e., MPD > MPDfac INTERACTIONS AT THE PAIRWISE or MPDnf. The CI is based on the LEVEL probability that two randomly chosen We measured facilitation intensity and individuals, one from each of two selected importance , i.e., the effect that neighbours microsites (Open, Stipa or Shrub), belong have on their target species regardless of to species shared by both microsites. A other environmental factors and the higher dissimilarity (lower CI) among relative effect of nurses on their target
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species compared to that of other species in each site were calculated using environmental factors, respectively the “cophenetic” command of R. The mean (Brooker et al. 2005), of each possible PD of facilitation beneficiaries (species Stipa and Shrub target species pairs at with more individuals recruiting under a each site. For doing this we used the nurse plant) and obligates (described Relative Interaction Intensity index (RII) above) at both Stipa and Shrub microsites and the Interaction Importance index was calculated in each site using these data (Iimp) provided by Armas et al. (2004) and (see Fig. 5.1). Seifan et al. (2010), respectively (see Appendix K for details). Both indices ASSESSING THE EFFECTS OF oscillate between 1 and 1 (relative units); ENVIRONMENTAL FILTERING AND positive and negative values indicate BIOTIC INTERACTIONS ON facilitation and competition, respectively. COMMUNITY PHYLOGENETIC The higher the index value, the higher the STRUCTURE intensity (RII) or importance (Iimp) of Prevalent climatic conditions (rainfall, such effect. For these analyses we used the radiation and a temperatures) for each site total number of individuals found in the were collected using available climatic ~30 0.5 m × 0.5 m quadrats sampled at models (Ninyerola et al. 2005) and reduced each site, and calculated a unique RII and to a single synthetic variable using PCA Iimp index for each species and site. We conducted with the Primer v. 6 statistical used the number of recruited individuals as package for Windows (PRIMER E Ltd., an indicator or each species performance to Plymouth Marine Laboratory, UK).We calculate these indices, because the number used the first axis of this PCA (hereafter of recruited individuals indicates superior Climate ) for the analyses explained below. environmental conditions for a given This axis explained 88.6% of the variance species in a given microsite, an approach and was inversely and positively correlated followed by previous studies (Valiente with radiation and rainfall, respectively Banuet et al. 2006, Valiente Banuet and (Appendix K). Verdú 2007). The relationships between the Alternatively, the pairwise surrogates of biotic interactions used (C phylogenetic distances among both nurses score, percentage of facilitation obligates , (Stipa and Shrub) and their co occurring and CI) and both MPD and Climate were
163 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY evaluated by using linear regressions. This interaction mechanism (depending on the set of analyses gives us an idea of the partial correlation that is non significant). relative importance of environmental Finally, as a second evaluation of conditions as drivers of biotic interactions, the degree of habitat differentiation, and and of the effects of these interactions on how abiotic conditions affected it, we the phylogenetic structure of the evaluated the effect of Climate on the community. Additionally, the relationship difference between MPD and both MPDfac between Climate and MPD was assessed and MPDnf, respectively. If this difference by using both linear regression (direct is significantly higher than 0, niche effect) and partial correlations (indirect differentiation is producing a phylogenetic effect, mediated by the effect of Climate clustering in facilitated or non facilitated on C score, percentage of facilitation species guilds, and thus the difference in obligates , CI and MPD MPDfac/nf, microclimatic conditions between nurse respectively). If C score, percentage of and Open microsites affect the facilitation obligates or CI increase MPD, phylogenetic structure of this particular this will mean that either competition, community. We first compared the MPD – niche expansion or niche differentiation MPDfac/nf difference from zero by using provided by nurse plants, respectively, t tests, with sites acting as replicates. Then, increase the phylogenetic evenness of the the relationship between Climate and this community. The relation between these difference was evaluated using linear biotic interactions indicators and Climate regressions to asses the effect of climatic will give us an idea on how climatic conditions on this “double habitat filtering” conditions influence such interactions. (Jones et al. 1997, Badano and Cavieres Finally, if both linear regression and partial 2006; Fig. 5.1) correlations between Climate and MPD are significant, this will mean that climatic ASSESSING THE EFFECTS OF conditions have a direct effect on the CLIMATIC CONDITIONS AND PD ON phylogenetic structure of the studied THE OUTCOME OF PAIRWISE communities. However, if only linear PLANT PLANT INTERACTIONS regressions, but not partial correlations, are To evaluate the existence of an interaction significant, this will mean that climatic between PD and abiotic conditions, we conditions are affecting MPD only via assessed the relationships between Climate their indirect effects on a particular biotic and the MPD obtained from all the nurse facilitated species pairs in each site by
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using linear regressions. These species Most of the studied sites showed a random pairs were divided according to the type of phylogenetic structure (Table S9). Climate facilitative relationship ( beneficiaries or was negatively related to MPD at the obligates ) and nurse plant ( Stipa or community level, but this relationship was shrubs). We also fitted the relationships only marginally significant (r = 0.53; P = between Climate , PD, RII and Iimp by 0.09). When we removed the indirect using Regression trees (De´ath and effect mediated by the relationship Fabricius 2000), as implemented in the between Climate and the MPD – MPDfac Tree package of R. We used 10 fold cross difference by using partial correlations, validation to fit the most parsimonious this relationship disappeared (ρ = 0.32; P = model to each dataset (De´ath and 0.4), suggesting the lack of a direct effect Fabricius 2000). Climate and the PD of Climate on MPD. In contrast, the between each target species and its nurse different measures of plant plant were used as predictor variables in the four interactions were all positively, but regression trees performed (RII and Iimp marginally, related to MPD at the indices for Stipa and shrub nurses). Despite community level (r = 0.60, 0.56 and 0.57; this low number of predictors, we used this P = 0.07, 0.09 and 0.07 for C score SES, procedure because of the heavily skewed CI between Open and Shrub microsites and nature of the PD values (Fig. S5), a percentage of facilitation obligates , characteristic commonly found with these respectively; Fig. 5.2, Fig. S6). The data (Castillo et al. 2010). Regression trees relationship between CI (Open vs. Stipa also allow detecting non linear microsites) and MPD was not significant (r relationships, and are insensible to the = 0.11; P = 0.44). Most of the surrogates distribution of either the predictor or of biotic interactions employed were not response variables (De´ath and Fabricius related to Climate (P > 0.35 in all cases; 2000). Fig. 5.2). However, the negative relationship between the MPD MPDfac RESULTS difference and Climate found (r = 0.82; P
EFFECTS OF ENVIRONMENTAL = 0.006) suggests a decrease in FILTERING AND BIOTIC phylogenetic clustering among facilitated INTERACTIONS ON COMMUNITY species with increased rainfall availability. PHYLOGENETIC STRUCTURE This difference was also significantly
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400 A
350
300 Total mean PD for Stipa
250 Total mean PD for Shrub Mean PD from facilitation beneficiaries 200 -200 -150 -100 -50 0 50 100
700 B 600
Stipa 500 Shrub
400
300 Total mean PD for Stipa
Mean PD from facilitation obligates 200 Total mean PD for Shrub
-200 -150 -100 -50 0 50 100 PCA climate - RAINFALL +
Figure 5.3 Relationship between the PCA axis obtained from climatic values (PCA climate) and mean phylogenetic distance (PD) between facilitation beneficiaries (A) or obligates (B) species and their nurses. No relationships were found for any of the assayed variables and climate (R 2 < 0.1 and P > 0.3 in all the cases).
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Figure 5.4 Regression trees conducted with both interaction intensity (RII; panel A) and importance (Iimp; panel B) indices. Split values for each predictor used (PD, in million years [Myr], or climatic PCA axis values) are shown in each branch. Terminal nodes show the mean value for each group of the response variable introduced and the number of cases in each node (between parenthesis; n = 200 cases for each tree). Positive and negative values indicate facilitative and competitive interactions, respectively. The higher the values, the more intense or important the effect of the nurse upon the target species. In each panel, the general fit of the model (D 2, percentage of variance explained by the model), extracted from the null deviance (Deviance root), and the deviance of the final chosen tree after 10-fold cross-validation (Deviance tree) are shown.
167 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY different from zero, but the MPD MPDnf interactions. When 207 Myr < PD < 272.8 difference was not (mean difference = 1.09 Myr, values of Climate higher than 47.7 ± 0.15 and 0.69 ± 0.20; t = 2.36 and 1.15; (the wettest sites) render negative RII P = 0.046 and 0.284 for facilitated and values, which were neutral otherwise. non facilitated species, respectively). When 207 Myr < PD > 272.8 Myr, RII These results suggest a phylogenetic values were positive in the dryer sites clustering, comparing with the general (Climate values < 127.2), but neutral in the species pool of each site, for the facilitated rest of climatic conditions (Fig. 5.4A). but not for the non facilitated species. Values of the Iimp index rendered slightly different results; when PD > 272.8 Myr EFFECTS OF CLIMATIC CONDITIONS and Climate values < 67 (dryer sites), AND PHYLOGENETIC DISTANCE ON shrubs were not important for the THE OUTCOME OF PAIRWISE performance of their target species; when INTERACTIONS Climate values where higher than 67 (mid The PD between nurse facilitated species to wet sites), shrubs exerted a negative remained constant across the entire effect upon their target species (Fig. 5.4B). environmental gradient sampled (Fig. 5.3). Climate and PD were poor predictors for DISCUSSION the RII and Iimp data calculated with the By jointly considering information on target species tested and Stipa as nurse abiotic conditions, state of the art 2 plant, respectively (Regression trees D = phylogenetic tools, and different aspects of 0.02 and 0 for RII and Iimp, respectively). biotic non trophic interactions Conversely, regression trees predicted 25% (competition/facilitation shifts, niche and 14% of the variance of the RII and expansion and niche differentiation), we Iimp indices for Shrub microsites and their were able to explore the relative target species (Fig. 5.4). Values of PD importances of plant plant interactions and between the shrubs and their target species the environment as drivers of the between 207 and 272.8 million years (Myr) phylogenetic structure of the studied rendered negative or neutral interactions, communities. Our results show that these while values of PD outside this values interactions are important to determine (<207 Myr or >272.8 Myr) indicated phylogenetic structure along a wide positive results for both RII and Iimp environmental gradient, but that the effect indices. Climate was a modulator of of climatic conditions on this structure is secondary importance for these pairwise
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indirectly mediated by its effects upon the variables measured. This does not mean “double environmental filtering” provided that plant plant interactions were not by the difference in microclimatic important at this level of organization, but conditions between nurse plants and Open rather that these interactions, mainly microsites. The phylogenetic evenness positive ones, importantly influenced promoted by biotic interactions and the community assemblage through niche phylogenetic clustering promoted by expansion and habitat differentiation climatic conditions, mediated by its effects across the entire environmental gradient on plant plant interactions, caused a studied (Fig. 5.2; Fig. S6). How does the random phylogenetic structure in most of equal importance of biotic interactions the studied communities. At the pairwise across wide environmental gradients affect level, we found that PD was a primary the relative roles of such interactions and modulator of plant plant interactions, with environmental filtering in determining the Climate playing a secondary role. PD phylogenetic structure of plant values between 207 278.2 Myr rendered communities? negative outcomes, while PD values When evaluating the effects of outside this range yielded positive or climatic conditions or biotic interactions on neutral outcomes, depending on the phylogenetic structure of the studied environmental conditions. communities separately, we found support for the patterns found by previous studies: DIRECT AND INDIRECT EFFECTS OF while competition increased the ENVIRONMENTAL FILTERING AND phylogenetic evenness of a given BIOTIC INTERACTIONS ON THE community, environmental filtering did the COMMUNITY PHYLOGENETIC contrary (Webb et al. 2002, Cavender STRUCTURE Bares et al. 2004). However, when In sharp contrast with previous studies considering both processes and their (Michalet et al. 2006, Callaway 2007), we interaction together, our results showed did not find any relationship between our that phylogenetic structure is determined surrogates of biotic interactions or niche by both direct and indirect effects mediated expansion at the community level (C score by climatic conditions and biotic non and percentage of facilitation obligates trophic interactions (Fig. 5.2), which species, respectively) and the climatic finally caused a random phylogenetic
169 BIOTIC AND ABIOTIC FILTERS FOR PHYLODIVERSITY pattern. To our knowledge, such Bruno et al. 2003), another important interaction has not been described before. surrogate of facilitation at the community These results are in the line of the most level, promoted phylogenetic evenness, in recent literature, which suggests that the agreement with previous findings phylogenetic structure alone, even with a (Valiente Banuet and Verdú 2007, Verdú perfect knowledge of the trait conservatism et al. 2009). This latter result highlights the of co occurring species, may not be necessity of measuring different indicators enough to infer the implied mechanisms in of plant plant interactions, and not only co the assemblage of a given community occurrence patterns, to correctly assess the (Pausas and Verdú 2010). Our study role of such interactions on the demonstrates that this is particularly true phylogenetic structure of plant when dealing with more than one communities. important mechanism shaping natural We were able to establish how an communities, something fairly common in increase in rainfall counter intuitively nature (Butterfield et al. 2010). In contrast acted as an environmental filtering, with previous studies (e.g. Valiente Banuet increasing community phylogenetic and Verdú 2007, Verdú et al. 2009), we did clustering, and how its effect was mediated not find any increase in phylogenetic by the reduction in the habitat evenness with the increase of facilitation differentiation provided by nurse plants importance, as shown by the C score (more rainfall reduced the difference measurements at the community level. between MPD and MPDfac; Fig. 5.2). Our This could be explained because of results also highlight the importance of contrasting ontogenetic stages comparing considering not only multiple processes, to those studies (more adult adult but also employing different proxies to interactions in our sampled sites than in the identify their direct and indirect effects on others; Valiente Banuet and Verdú 2008), community assemblage and its or because of some of the patchiness phylogenetic structure. Using only co registered with the C score may be more occurrence patterns, as previously related to a shared dispersion syndrome suggested (Pausas and Verdú 2010), would than to facilitation processes, and therefore not suffice to detect these indirect effects. this could lead to a phylogenetic clustering To take into account the whole set of (see additional discussion below). processes affecting phylogenetic structure However, the increase of the relative may also help to disentangle the importance of niche expansion ( sensu importance of phylogenetic diversity per se
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on ecosystem functioning or other The idea that a threshold in the PD important ecosystem services (e.g. Forest between the involved species may define et al. 2007, Maherali and Klironomos the outcome of their interaction is 2007, Cavender Bares et al. 2009), appealing, and fits surprisingly well – avoiding potential confounding effects although the authors did not discuss the produced by different processes causing a data in that way– results from a recent particular phylogenetic pattern (Mayfield study in the Mexican scrubland (Castillo et and Levine 2010). al. 2010). These authors found that lower PDs always indicate negative interactions, IS THE EVOLUTIONARY while higher PDs could mean either RELATIONSHIP MORE IMPORTANT positive or negative outcomes (see Figs 2 THAN ABIOTIC CONDITIONS and 3 in Castillo et al. 2010); in our case, DEFINING PAIRWISE INTERACTIONS this threshold would be PD < 272.8 Myr. OUTCOMES? Conversely, the lower PD threshold could A hierarchy between both PD and climatic be related not with a facilitatory effect of conditions modulated the outcome of the the nurse shrub, but with the role of the large set of pairwise interactions tested. In shrubs studied as a refuge for animals and our case, PD was the primary factor their perch effect (Pausas et al. 2006). This affecting such interactions, while climatic could promote an increase in the conditions played a secondary role (Fig. deposition of seeds by animals of other 5.4). We found a double threshold in PD Tertiary and animal dispersed shrubs, and values that defined the sign of the therefore foster the co occurrence of interactions, with PD values between 207 species phylogenetically related with the and 272.8 Myr always rendering studied shrubs by nucleation processes competition, and values outside these (Herrera 1992, Verdú and García Fayos thresholds always leading to facilitation. 1996). The fact that these results may be While results from the upper threshold (PD related mostly to a dispersion syndrome, > 272.8 Myr leading to facilitation) agree rather than to the facilitatory effect of the with current literature (Valiente Banuet shrubs themselves, could be a potential and Verdú 2007, 2008, Castillo et al. explanation of the contrasting results found 2010), those from the lower threshold in other studies regarding this low (facilitation with PD < 207 Myr) do not. threshold in PD values (Castillo et al.
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2010), and regarding the effect of Soliveres et al. in press ), since nor PD facilitation in the phylogenetic structure neither climatic conditions were good (we found an increase in phylogenetic predictors of such outcomes. clustering with lower SES C scores, but Valiente Banuet and Verdú [2007] or CONCLUDING REMARKS Verdú et al. [2009] found the contrary Inferring the mechanisms shaping plant using other measurements of co communities from their phylogenetic occurrence patterns). What factors, then, structure alone may drive to misleading determine the outcome of pairwise conclusions (Myfield and Levine 2010). interactions when PD is high enough to The use of manipulative experiments allow positive interactions to occur? Our including different communities under results show that environmental conditions contrasting environmental conditions, and play a major role once this threshold has the measurement of the direct and indirect been reached in some cases, with dryer effects of biotic interactions have been sites usually yielding more positive recommended to overcome these outcomes (Callaway 2007). However, we limitations (Cavender Bares et al. 2009, wish to highlight that only 25% of the Vamosi et al. 2009). However, such variance of the tested interaction outcomes experiments are often logistically were predicted by our regression trees. prohibitive. The observational and Therefore, other unmeasured factors, such analytical approach employed here may as different ontogenetic stages of the serve as an alternative to experimentation, involved plants (Valiente Banuet and and can help to avoid misleading Verdú 2008), differences in herbivory conclusions when inferring the several pressure among sites (Smit et al. 2009), or possible mechanisms underlying the ecophysiological traits labile through assemblage of natural communities. Our evolutionary time frames and therefore not study illustrates the complexity of direct detected with our phylogenetic approach and indirect effects of environmental (Cavender Bares et al. 2004, 2009), could filtering and biotic interactions as drivers be important factors affecting such of the phylogenetic structure of natural interactions (e.g. Liancourt et al. 2005). communities across environmental Such unmeasured factors could play a gradients. It also highlights the necessity of major role in defining the outcomes of the taking into account environmental interaction between Stipa and its target conditions and different components of the species (e.g. Soliveres et al. 2010; biotic non trophic interactions when
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studying the processes shaping plant these interactions only once PD reached communities and their phylogenetic this particular threshold. In contrast, other structure. unmeasured factors in the case of Stipa , This study also represents, to our such as herbivory, ontogenetic stage or knowledge, the first attempt to test the specific ecophysiological traits not relative importance and possible included in the PD relationships seemed interactions between the evolutionary more important drivers of such outcomes, relationships of two interacting species and illustrating the difficulties of predicting climate as drivers of the outcome of their pairwise interactions outcomes with simple interactions. Interactions between different models involving just one or few factors affecting plant plant interactions predictors. may lead to counterintuitive or antagonistic responses and should be studied jointly to ACKNOWLEDGMENTS Estrella Pastor, Beatriz Amat, Luis Cayuela, María properly infer their relative importances as D. Puche, Matt Bowker, and Pablo García Palacios assisted with fieldwork and/or statistical analyses. drivers of such interactions (Baumeister Adrián Escudero provided help with species and Callaway 2006, Soliveres et al. in identification. SS was supported by a PhD fellowship from the EXPERTAL project, funded by press ). Regression trees revealed as a Fundación Biodiversidad and CINTRA S.A. FTM acknowledges support from the European Research useful tool for detecting the hierarchy and Council under the European Community's Seventh Framework Programme (FP7/2007 2013)/ERC the non linear responses in the effect of Grant agreement n° 242658. This research was funded by the CEFEMED, and INTERCAMBIO climate and PD on such interactions. We (BIOCON 06/105) projects, funded by the found that PD was of primary importance Universidad Rey Juan Carlos Comunidad de Madrid, and Fundación BBVA, respectively. acting as a threshold, which could explain the species specific nature often found in plant plant interactions (Callaway 2007). Conversely, climatic conditions affected
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Supplementary material for Chapter 5.
Appendix K. Detailed materials and methods. SUITABILITY OF STIPA TENACISSIMA STEPPES Stipa tenacissima steppes are well suited ecosystems for testing the relative roles of biotic interactions and habitat filtering in the phylogenetic structure of plant communities, and to assess the relative importances and possible interactions between PD and climate as drivers of plant plant interactions outcomes for different reasons. Important ecophysiological traits are extremely well conserved through evolutionary time in the Mediterranean flora (Herrera 1992; Valiente Banuet et al. 2006), which avoid potential confounding factors in the interpretation of a given phylogenetic structure (Webb et al. 2002). Conversely, the PD between two interacting species is a good indicator of dissimilarity in their ecological niches and traits (Valiente Banuet et al. 2006, Valiente Banuet and Verdú 2007). Furthermore, S. tenacissima steppes are one of the most extended Mediterranean semiarid community types (Le Houreu 2001), and are strongly shaped by facilitation and its interaction with abiotic stress (e.g., Maestre and Cortina 2004a, Armas and Pugnaire 2005). See Maestre et al. (2009b) for additional details on the natural history of these communities.
SYNTHESIZING CLIMATIC CONDITIONS WITH PCA Eight climatic variables (annual radiation, minimum, maximum and mean temperature, annual rainfall, temperature range [maximum minimum], and minimum and maximum temperatures for the coldest and warmest month, respectively) were collected for each site using available climatic models (Ninyerola et al. 2005). We reduced them to a single synthetic variable using PCA to obtain a more general assessment of the influence of all of our environmental variables at both the community and pair of species levels. We used the first axis of this PCA (referred in the main text to as Climate ) as our surrogate of the climatic gradient present at our sites. This axis explained 88.6% (Eigenvalue = 8.08 10 3) of the variance in the climatic data, and was highly correlated with both rainfall and radiation (Eigenvectors = 0.864 and 0.502 for rainfall and radiation, respectively; the remainder of the eigenvectors were < 0.03 in all cases). PCA was carried out using the Primer v. 6 statistical package for Windows (PRIMER E Ltd., Plymouth Marine Laboratory, UK).
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METHODOLOGICAL DETAILS OF THE PHYLOGENETIC HYPOTHESIS The phylogenetic distances between species pairs were estimated by assembling a phylogenetic hypothesis for all the species included in this study using Phylomatic2 (avalaible at: http://www.phylodiversity.net/phylomatic/phylomatic.html). All the families in our data set matched the family names of the angiosperm megatree used in Phylomatic (R20091110.new), which was based on the Angiosperm Phylogeny Group III phylogenetic classification of flowering plant orders and families (APG 2009). Within family phylogenetic relationships were further resolved based on data from various published molecular phylogenies (Asteraceae: Funk et al. 2005; Susanna et al. 2006; Cistaceae: Guzmán and Vargas 2009; Guzmán et al. 2009; Fabaceae: Allan and Porter 2000, Allan et al. 2004, Wojciechowski et al. 2004; Poaceae: Bouchenak Khelladi et al. 2008, 2010; Rubiaceae: Bremer and Eriksson 2009). Once we had assembled the phylogenetic hypothesis, we adjusted its branch lengths with the help of the Phylocom BLADJ algorithm (Webb et al. 2008), which fixes the age of internal nodes based on clade age estimates, whereas undated internal nodes in the phylogeny are spaced evenly between dated nodes to minimize tree wide variance in branch length (Webb et al. 2008). Thus, BLADJ is a simple tool that fixes the root node of a phylogeny at a specified age and fixes the other nodes for which age estimates are available. It sets all other branch lengths by placing the nodes evenly between dated nodes, as well as between dated nodes and terminals (of Age 0). The Phylocom manual (Webb et al. 2008) suggests using the age estimates from Wikström et al. (2001); however, new analyses estimating divergence times for angiosperms have been published since the publication of this seminal work (e.g. Bremer et al. 2004, Anderson et al. 2005, Magallón and Castillo 2009, Smith et al. 2010, Wang et al. 2010). In addition, TimeTree (Hedges et al. 2006), a public knowledge base of divergence times among organism is publicly available online (http://www.timetree.net). This utility allows exploration of the thousands of divergence times among organisms in the published literature (Hedges et al. 2006). A tree based (hierarchical) system is used to identify all published molecular time estimates bearing on the divergence of two chosen taxa, such as species, compute summary statistics, and present the results. We mainly used this database to fix the ages of internal nodes on our phylogenetic hypothesis, completing TimeTree results with other published sources when this database did not provide any date (Cistaceae: Guzmán and Vargas 2009, Guzmán et al. 2009; Asteraceae: Kim et al. 2005, Torices 2010; Poaceae:
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Bouchenak Khelladi et al. 2010; Fabaceae: Lavin et al. 2005, Bello et al. 2009; Brassicaceae: Franzke et al. 2009; Caryophyllaceae: Valente et al. 2010). Eventually, we fixed the age of 48 internal nodes (see Table S2). Apart from the data showed in the text, we used this tree to calculate the mean nearest phylogenetic taxon index (MNTD; Webb et al. 2002), which measures the phylogenetic distance to the most closely related neighbor. This index was calculated using the Picante package for R (Kembel et al. 2010). Since MNTD was highly correlated with MPD (Pearson´s correlation: r = 0.87; P < 0.0001), and its results were very similar to those obtained with the MPD index, we only used results from the latter (presented in Table S1).
MEASURING CO OCCURRENCE PATTERNS AND PLANT PLANT INTERACTIONS OUTCOMES We measured co occurrence patterns in each community by using null models based on patterns of species co occurrence found with the 80 1.5 m × 1.5 m quadrats (Gotelli and Graves 1996). We estimated species co occurrence with the C score index, a metric commonly used by studies aiming to infer species interactions at the community level from co occurrence data (e.g. Rooney et al. 2008, Maestre et al. 2008, Bowker et al. 2010). This index is calculated for each pair of species as (R i S)(R j S), where R i and R j are the number of total occurrences for species i and j, and S is the number of quadrats in which both species occur. This score is then averaged over all possible pairs of species in the matrix (Gotelli 2000). The C score is related to the competitive exclusion concept of “ checkerboardness” i.e., how many of the possible species pairs in a given community never appear in the same quadrat together. Thus, positive and large values of this index indicate that competition may be a prevalent mechanism determining the co occurrence patterns observed (Gotelli 2000). As the values of the C score are dependent on the number of species and co occurrences observed within each plot, we obtained a standardized effect size (SES) as (I obs
Isim ) Ssim , where I obs is the observed value of the C score, and I sim and S sim are the mean and standard deviation, respectively, of this index obtained from the n simulations performed (Gotelli and Entsminger 2006). Standardized Effect Size (SES) values of the C score less than or greater than zero indicate prevailing spatial segregation (competition prevalence) and aggregation (facilitation dominance; Tirado and Pugnaire 2005) among the species within a community, respectively. We used ‘fixed rows–equiprobable columns’ null models and 5000 simulations. With this approach, each species conserved its own abundance (rare species remained rare and common species remained common) and each quadrat was assumed to
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have the same probability of being colonized as the remainder, regardless of the number of species found in each quadrat during the simulations. This null model has been recommended for standardized samples collected in homogenous habitats (Gotelli 2000), such as the ones gathered in this study. We also tried the “fixed rows fixed columns” algorithm (both species and quadrats conserved its relative abundance and richness, respectively) to add confidence to our conclusions. The results obtained with these analyses were similar than those obtained with the ‘fixed rows–equiprobable columns’ null model, and thus are not shown. We also calculated interaction intensity and importance indices (RII; Armas et al.
2004 and Iimp; Seifan et al. 2010, respectively). RII indices were calculated as (P Nurse –
POpen )/(P Nurse + POpen ), where PNurse was the number of individuals under the canopy of a nurse plant ( Stipa or Shrub) and POpen was the number or individuals recruited in the Open microsite. Alternatively, Iimp indices were calculated as Iimp = N imp /│N imp │+│E imp │, where
Nimp and E imp were the nurse plant and environmental contributions to the total number of individuals recruited for each species, respectively. N imp was calculated as P Nurse – POpen , and
Eimp as P Open – MP Open/Nurse , where MP Open/Nurse is the maximum number of recruited individuals for a given species found in the entire gradient, irrespective of the microsite sampled.
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Table S9. Main characteristics of the study sites. MPD = Mean phylogenetic distance and SES = Standardized effect size. The SES of the MPD was calculated as MPD obs – meanMPD null / sdMPD null ; where MPD obs is the observed phylogenetic distance in our sample, and meanMPD null and sdMPD null are the mean and standard deviation of the phylogenetic distances obtained from the n simulated communities under the null model. Positive SES, and with a P-value > 0.95 indicate significant phylogenetic evenness in the sampled community, while negative SES with P-values < 0.05 indicate phylogenetic clustering.* Indicates a significant phylogenetic clustering in this community. The dominant shrub species is Quercus coccifera in all sites excepting at Carrascoy, where it was Rhamnus lycioides .
Site Latitude Longitude Annual rainfall Species richness MPD (SES) P (MPD) (mm)
Barrax 39º02’91’’N 2º13’82’’W 433 24 0.88 0.22 Camporreal 40º19’72’’N 3º25’36’’W 457 9 0.77 0.16 Carrascoy 37º48’02’’N 1º18’32’’W 282 38 0.09 0.42 Crevillente 38º14’15’’N 0º55’49’’W 273 36 1.60 0.91 El Ventós 38º28’14’’N 0º37’03’’W 319 35 0.37 0.65 Morata 40º27’62’’N 3º05’31’’W 455 22 1.01 0.15 Sierra Espuña 37º49’27’’N 1º40’41’’W 364 32 1.49 0.04* Titulcia 40º11’28’’N 3º30’13’’W 440 21 0.84 0.24 Villarrobledo 39º12’64’’N 2º30’77’’W 446 18 0.83 0.18 Yecla 38º35’40’’N 1º12’15’’W 350 47 0.52 0.74 Zorita 40º21’30’’N 2º52’62’’W 434 38 1.52 0.91
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Table S10. Estimated age of branching events.
Node Estimated Reference label time (Myr) 1 334.5 Hedges et al. (2006) 2 298.0 Hedges et al. (2006) 3 150.1 Hedges et al. (2006) 4 147.8 Hedges et al. (2006) 5 122.0 Hedges et al. (2006) 6 101.0 Hedges et al. (2006) 7 67.0 Hedges et al. (2006) 8 112.0 Hedges et al. (2006) 9 57.0 Bouchenak Khelladi et al. (2010) 10 44.7 Bouchenak Khelladi et al. (2010) 11 28.0 Bouchenak Khelladi et al. (2010) 12 125.0 Hedges et al. (2006) 13 121.0 Hedges et al. (2006) 14 109.0 Hedges et al. (2006) 15 98.0 Hedges et al. (2006) 16 69.0 Hedges et al. (2006) 17 89.0 Hedges et al. (2006) 18 94.0 Hedges et al. (2006) 19 84.0 Bello et al. (2009) 20 55.0 Lavin et al. (2005) 21 24.6 Lavin et al. (2005) 22 97.5 Hedges et al. (2006) 23 84.8 Hedges et al. (2006) 24 39.0 Wikström et al. (2001) 25 19.0 Franzke et al. (2009) 26 51.0 Hedges et al. (2006) 27 14.5 Guzmán and Vargas (2009); Guzmán et al. (2009) 28 2.0 Guzmán and Vargas (2009); Guzmán et al. (2009) 29 1.6 Guzmán and Vargas (2009); Guzmán et al. (2009) 30 6.1 Guzmán and Vargas (2009); Guzmán et al. (2009) 31 122.0 Hedges et al. (2006) 32 122.0 Hedges et al. (2006) 33 55.8 Valente et al. (2010) 34 16.6 Valente et al. (2010) 35 73.5 Wikström et al. (2001) 36 113.0 Magallón and Castillo (2009); Anderson et al. (2005); Janssens et al. 2009) 37 111.9 Magallón and Castillo (2009); Anderson et al. (2005); Janssens et al. 2009) 38 96.6 Magallón and Castillo (2009); Janssens et al. (2009) 39 47.0 Kim et al. (2005) 40 35.5 Kim et al. (2005) 41 24.7 Torices (2010) 42 108.0 Hedges et al. (2006) 43 17.0 Bremer and Eriksson (2009) 44 106.0 Hedges et al. (2006) 45 90.0 Hedges et al. (2006) 46 76.0 Hedges et al. (2006) 47 23.0 Wikström et al. (2001) 48 8.5 Stevens (2010)
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Figure S4. Phylogenetic tree of the regional species pool. Phylogenetic hypothesis are developed in Appendix S1. Main nurse plants are highlighted in blue. Node labels are given in Table S9.
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180
160 A
140
120
100
80
60
numberof cases 40
20
0 0 100 200 300 400 500 600 700 800 120 B 100
80
60
40 numberofcases 20
0 100 200 300 400 500 600 700 800
Phylogenetic distance nurse-target species
Figure S5. Frequency histogram of the phylogenetic distances between the different target plants and their nurses, either Stipa tenacissima (A) or shrubs (B). Notice the discontinuous distribution and the skewness of the data.
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ENVIRONMENTAL CONDITIONS
2.0
1.5 Phylogenetic 1.0 evenness
0.5
0.0
-0.5 MPD (SES) -1.0 Phylogenetic clustering -1.5 R2= 0.30; P = 0.09
-2.0 -200 -150 -100 -50 0 50 100 Climatic PCA axis values
- RAINFALL +
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HABITAT × BIOTIC INTERACTIONS
3 1.0
2 0.9
1 0.8
0 0.7
C-score 2 -1 R = 0.13; P = 0.57 0.6 Similarityindex
-2 0.5 Open vs. Stipa: R 2 = 0.05; P = 0.54 Open vs. Shrub: R 2 = 0.01; P = 0.80 -3 0.4 -200 -150 -100 -50 0 50 100 -200 -150 -100 -50 0 50 100
40 4
35 3 Phylogenetic 30 2 clustering among facilitated/ 25 non-facilitated 1 species 20
2 0 15 R = 0.12; P = 0.30
% facilitation facilitation obligates % -1 10 MPDgen-MPDclust MPD facilitated : R2 = 0.68; P = 0.006 2 MPD non-facilitated : R = 0.05; P = 0.56 5 -2 -200 -150 -100 -50 0 50 100 -200 -150 -100 -50 0 50 100 Climatic PCA axis values Climatic PCA axis values Climatic PCA axis values - RAINFALL +
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BIOTIC INTERACTIONS
2.0 2.0
1.5 1.5 R2 = 0.36; P = 0.07 1.0 1.0
0.5 0.5
0.0 0.0 MPD -0.5 -0.5
-1.0 -1.0 Open vs. Stipa: R 2 = 0.01; P = 0.75 -1.5 -1.5 Open vs. Shrub: R 2 = 0.30; P = 0.09 -2.0 -2.0 -3 -2 -1 0 1 2 3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 C-score Similarity index 2.0 1.0
1.5 0.9 2 1.0 R = 0.01; P = 0.77 0.8 0.5
0.0 0.7 MPD -0.5 0.6 MPD fac vs Open-Stipa similarity
-1.0 Similarity index MPD fac vs Open-Shrub similarity 0.5 -1.5 MPD nf vs Open-Stipa similarity MPD nf vs Open-Shrub similarity -2.0 0.4 10 20 30 40 -2 -1 0 1 2 3 4 % facilitation obligates MPDgen - MPDclust
Figure S6. Detailed results of the conceptual diagram shown in Figure 5.2. Results are organized following sections provided in Figure 5.2 (effects of environmental conditions, biotic interactions and habitat × biotic interactions). In all cases, linear regressions results are shown in each plot.
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DISCUSIÓN Y CONCLUSIONES GENERALES
DISCUSIÓN GENERAL
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DISCUSIÓN GENERAL
Los trabajos presentados en esta tesis doctoral constituyen una de las evaluaciones más exhaustivas sobre la evolución de las interacciones planta planta a lo largo de gradientes ambientales realizadas hasta la fecha. Por un lado, se ha testado la evolución de la interacción entre Stipa tenacissima y Retama sphaerocarpa a lo largo de cuatro puntos contrastados de disponibilidad hídrica, derivados de predicciones realistas sobre futuros escenarios de cambio climático (IPCC 2007, capítulo 1). Por otro lado, se ha testado el efecto de la co ocurrencia de la aridez con distintos factores de importancia en la determinación del signo y la intensidad de las interacciones planta planta, como son la herbivoría (p. ej. Baraza et al. 2006), la ontogenia (p. ej. Miriti 2006) o la relación evolutiva entre las especies implicadas (p. ej. Castillo et al. 2010). Estas aproximaciones han revelado complejas interacciones y jerarquías existentes entre todos estos factores (capítulos 2, 3 y 5). Los experimentos realizados a nivel de comunidad han permitido evaluar la generalidad de los distintos modelos propuestos sobre la evolución de las interacciones planta planta a lo largo de gradientes ambientales (p. ej. Bertness y Callaway 1994, Michalet et al. 2006, Maestre et al. 2009a), tanto a nivel de par de especies como al de comunidades vegetales enteras (capítulo 4). Los resultados obtenidos apuntan a que –por orden de importancia– la herbivoría, las características ecológicas de las especies implicadas (deducidas tanto a partir de la tolerancia a distintos factores de estrés o fases ontogenéticas como de su historia evolutiva) y, por último, las condiciones climáticas y sus interacciones con los factores anteriormente mencionados, son los factores clave que definen el signo y la intensidad de las interacciones entre pares de especies vegetales. A pesar de que la mayoría de estudios sobre la dinámica de las interacciones planta planta en medios semiáridos se centran en la disponibilidad hídrica como factor abiótico clave (p. ej. Holzapfel y Mahall 1999, Tielbörger y Kadmon 2000, Pugnaire y Luque 2001, Maestre y Cortina 2004a), los trabajos presentados en esta tesis apuntan a la disponibilidad de luz y a la intolerancia a la sombra de las especies beneficiarias, o de sus distintas fases ontogenéticas, como un factor de gran importancia a la hora de definir dichas interacciones y su relación con la disponibilidad hídrica (Valladares y Pearcy 2002, Prider y Facelli 2004, Valladares et al. 2008, Seifan et al. 2010). Por otro lado, se ha demostrado que el patrón temporal, y no sólo la cantidad, de lluvia es algo importante a considerar si queremos entender la evolución de estas interacciones a lo largo de gradientes
189 DISCUSIÓN GENERAL ambientales, o su respuesta frente a futuros escenarios climáticos (Zavaleta 2006, Knapp et al. 2008). Los resultados obtenidos apuntan a que, mientras que el aumento de aridez puede conllevar un aumento de la competencia entre las especies estudiadas, el incremento de los eventos de lluvia torrencial puede acelerar la segregación de nicho entre las especies implicadas, reduciendo este efecto competitivo. Los efectos de ambos patrones (aumento de aridez y eventos torrenciales) dependerán de las tolerancias relativas a la sombra y a la sequía de la especie beneficiaria, y de la posibilidad de que se produzca una segregación de nicho efectiva entre la planta nodriza y su beneficiaria (Holmgren et al. 1997, Knapp et al. 2008, capítulos 1–3). Los múltiples factores que afectan de forma conjunta a las interacciones planta planta (herbivoría, aridez y diferentes características ecológicas), que comúnmente coexisten en los ecosistemas naturales, hacen que sea difícil desarrollar modelos generales que predigan la evolución de estas interacciones a lo largo de gradientes ambientales. Especialmente discutibles son aquellas aproximaciones que asumen un “gradiente de estrés” que afecta igualmente a todas las especies de una comunidad dada, ya que éstas difieren en sus adaptaciones ecofisiológicas y, por tanto, en sus tolerancias a los distintos factores de estrés que representan unas condiciones ambientales dadas (Chapin et al. 1987, Greiner la Peyre et al. 2001, Körner 2003). Los resultados presentados en el capítulo 4 apuntan a que los efectos positivos de las plantas nodriza sobre la riqueza de especies a nivel de comunidad están promovidos tanto por la expansión de nicho como por la reducción en la exclusión competitiva entre plantas vecinas. Estos efectos positivos se mantienen constantes a lo largo de gradientes ambientales donde coexisten distintos factores de estrés inversamente relacionados, o no relacionados entre sí (p. ej. aridez y bajas temperaturas), al contrario de lo que predicen los modelos teóricos actuales (p. ej. Lortie et al. 2004a, Michalet et al. 2006). Esta falta de variación de la importancia de las interacciones positivas a lo largo de estos gradientes ambientales deriva de la inexistencia de una gradiente de estrés único que afecta a todas las especies presentes en una comunidad. Las distintas condiciones microclimáticas que se encuentran bajo el dosel de las plantas nodriza beneficiarán a las especies menos adaptadas a las condiciones locales, sean éstas las que sean (Greyner la Peyre et al. 2001, Liancourt et al. 2005). Sin embargo, en gradientes ambientales gobernados por factores de estrés únicos o correlacionados entre sí (p. ej. aridez, bajas temperaturas), las interacciones entre plantas seguirán una relación unimodal, con predominio de las interacciones positivas a niveles medios altos de estrés y de las de
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competencia en ambos extremos del gradiente, tal como predicen los modelos teóricos en la actualidad (Michalet et al. 2006, Holmgren y Scheffer 2010). Por último, en esta tesis se muestran, por primera vez, los efectos conjuntos, directos e indirectos, de las condiciones climáticas (filtro de hábitat) e interacciones bióticas (distintos indicadores de competencia/facilitación) en el patrón filogenético de comunidades vegetales semiáridas (capítulo 5). El patrón filogenético encontrado fue aleatorio en la mayoría de casos, debido al efecto conjunto de un incremento de la dispersión filogenética promovida por las interacciones bióticas y del aumento de la agregación en este patrón causado por los efectos indirectos del clima sobre dichas interacciones. Los procesos de nucleación, derivados de la dispersión zoocora concentrada en arbustos y árboles remanentes que comúnmente se encuentra en ambientes Mediterráneos (Verdú y García Fayos 1996, Méndez et al. 2008), también parecen importantes en esta agregación del patrón filogenético. Los arbustos remanentes tienden a concentrar semillas de otros arbustos dispersados por animales, un síndrome de dispersión altamente conservado a lo largo de la evolución en la flora Mediterránea (Herrera 1992); por tanto, estos procesos de nucleación se dan entre especies evolutivamente próximas entre sí, causando agregación en el patrón filogenético. Se ofrecen en este último capítulo una serie de herramientas, fáciles de medir e interpretar, que pueden ayudar a evitar conclusiones erróneas derivadas de la inferencia de los mecanismos implicados en el ensamblaje de especies vegetales a partir del patrón filogenético de las comunidades en estudios observacionales (Cavender Bares et al. 2009, Mayfield y Levine 2010, Pausas y Verdú 2010).
HACIA UN NUEVO MODELO SOBRE LA EVOLUCIÓN DE LAS INTERACCIONES ENTRE PARES DE
ESPECIES A LO LARGO DE GRADIENTES BIÓTICOS Y ABIÓTICOS
Las numerosas excepciones a la Hipótesis del Gradiente de Estrés (Bertness y Callaway 1994) comúnmente encontradas en los sistemas naturales, han originado un debate sobre la generalidad de sus predicciones (Maestre et al. 2005, 2006, Lortie y Callaway 2006, Callaway 2007, Lortie 2010) que ha dado lugar a nuevas interpretaciones y revisiones del modelo inicial propuesto (Maestre et al. 2009a, Smit et al. 2009, Malkinson y Tielbörger 2010, Holmgren y Scheffer 2010). De estas nuevas aproximaciones se concluye que la naturaleza del estrés (si está relacionado o no con recursos directamente tomados por las plantas, p. ej. luz o agua frente a temperatura o salinidad), la co ocurrencia de distintos factores de estrés abiótico o de éstos con la herbivoría, o las respuestas no lineales derivadas de las distintas
191 DISCUSIÓN GENERAL tolerancias fisiológicas de las especies beneficiarias a los cambios microclimáticos promovidos por las plantas nodriza, son factores clave a considerar para entender la evolución de las interacciones planta planta a lo largo de gradientes ambientales. Sin embargo, incluir todos estos factores en un único modelo, que permita además inferir lo que ocurre en comunidades vegetales enteras a partir del estudio de las interacciones entre uno o pocos pares de especies es difícil. Incluso los modelos más recientes no son lo suficientemente generales a la hora de arrojar predicciones sobre la evolución de la frecuencia, intensidad e importancia de las interacciones planta planta en la estructura y composición de las comunidades vegetales a lo largo de distintos gradientes ambientales (pero véase Holmgren y Scheffer 2010 para una aproximación muy meritoria). Esto ocurre porque es extremadamente difícil que los modelos relativamente sencillos, que podrían ser extrapolables a numerosos ecosistemas y fácilmente evaluables, incluyan la gran variedad de factores que influyen en las interacciones planta planta. Y modelos que incluyan todos los factores serían extremadamente complejos y, por tanto, poco útiles. La dicotomía entre complejidad y utilidad se ilustra con un modelo conceptual que predice la evolución en las interacciones planta planta a lo largo de gradientes ambientales en zonas semiáridas a nivel de par de especies (Fig. B1). Para su elaboración se han tenido en cuenta algunas de las aportaciones más significativas de los últimos estudios publicados, así como los resultados presentados en esta tesis doctoral. En este modelo se evitan aspectos problemáticos a la hora de elaborar predicciones generales, como son la existencia de un gradiente general de estrés, que afecte a todas las especies de una comunidad por igual, o la existencia de estrategias ecológicas que permanecen constantes a lo largo de gradientes ambientales amplios (Travis et al. 2005, Michalet et al. 2006, Maestre et al. 2009a, Smit et al. 2009). Para ello, el modelo se basa en las tolerancias relativas de las especies implicadas a factores ambientales concretos (derivadas bien de sus rasgos ecofisiológicos o de su historia evolutiva), medibles y extrapolables a cualquier ambiente. El modelo presentado en la Figura B1 toma como base el modelo teórico presentado por Holmgren et al. (1997), que considera la eficacia biológica de las especies beneficiarias a lo largo de un gradiente, desde el centro del dosel de la planta nodriza hasta un claro libre de vegetación, bajo distintas condiciones de aridez. A este modelo se le ha añadido la respuesta diferencial, y no lineal, promovida por las distintas tolerancias ecofisiológicas de las especies implicadas o de sus distintas fases ontogenéticas, así como el efecto conjunto de distintos niveles de aridez con el impacto de la herbivoría. Por simplicidad se asume que la carga de herbívoros es constante a lo largo de las distintas condiciones ambientales (Smit et al. 2009).
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Esta asunción podría ser problemática, ya que se ha demostrado que ambos factores de estrés interactúan de diversas maneras y que, por tanto, no se puede considerar que varíen independientemente (Illius y O´Connor 1999, Ibañez y Schupp 2001, Silliman et al. 2005, Veblen 2008, capítulo 3). Además, el efecto de la herbivoría depende de la tolerancia a la misma de las especies beneficiarias así como de la palatabilidad de las especies nodriza (Baraza et al. 2006, Zamora et al. 2008). Ambos factores (tolerancia y palatabilidad) son directamente dependientes del nivel de recursos existente (Crawley 1998, Baraza et al. 2004, Wise y Abrahamson 2005, 2007, Smit et al. 2009). Las tolerancias ecofisiológicas han sido organizadas en tres grupos: 1) especies con una tolerancia media a la sequía y a la sombra, que constituyen la mayoría de especies existentes (Niinemets y Valladares 2006), 2) especies con una tolerancia a la sombra muy alta, pero intolerantes a la sequía (p. ej., Hedera helix , Rhagodia spinescens ), y 3) especies altamente tolerantes a la sequía, pero intolerantes a la sombra (p. ej., Retama sphaerocarpa , Helianthemum squamatum , Ambrosia dumosa ). Debido a la existencia de compromisos en las adaptaciones fisiológicas a ambos factores, no se considera la existencia de especies con una alta tolerancia conjunta a la sombra y a la sequía, ya que es poco probable que estas especies existan en la naturaleza (Niinemets y Valladares 2006). Por simplicidad, tampoco se pueden considerar en el modelo otras tolerancias fisiológicas que podrían ser relevantes en zonas áridas y semiáridas, como la tolerancia a suelos salinos o pobres en nutrientes (Pugnaire et al. 2004, Brady et al. 2005, Riginos et al. 2005, Armas y Pugnaire 2009), a bajas temperaturas (capítulo 4), o a vientos (Baumeister y Callaway 2006). Asimismo, las tolerancias a la aridez y a la sombra no se dividen en categorías discretas, ya que cada especie se localizará en un punto concreto dentro de un continuo de rasgos ecológicos que les permitirán una mayor o menor tolerancia a las condiciones ambientales (Kobe et al. 1995, Ackerly 2003, Niineemets y Valladares 2006). En el modelo que se introduce en la Figura B1 se consideran también tres fases ontogenéticas distintas: germinación y establecimiento temprano de las plántulas, juvenil, e individuos adultos reproductivos. Estas fases son claves a la hora de definir 1) el reclutamiento de nuevas especies en la comunidad (Escudero et al. 1999, Maestre et al. 2001, Holmgren et al. 2006), y 2) la demografía de estas especies (Escudero et al. 2000, Miriti et al. 2007), contribuyendo todos ellos de forma sustancial a la dinámica de las comunidades vegetales en las tierras secas (McAuliffe 1988, Eldridge et al. 1991, Eccles et al. 1999, Butterfield et al. 2010). Además, se considera la posibilidad de una segregación de nicho efectiva entre individuos adultos de las dos especies que interactúan, de forma que se predicen diferentes cambios en las interacciones entre adultos si existe dicha segregación (Fowler
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1986, Sala et al. 1989, Stokes y Archer 2010), o si por el contrario sus nichos ecológicos se solapan (Ludwig et al. 2004, Miriti 2006, Armas y Pugnaire 2009). Esta última separación puede tener implicaciones importantes en la respuesta de las comunidades vegetales a los cambios en el patrón de las precipitaciones predichos con el cambio climático (Schwinning y Sala 2004, Knapp et al. 2008, capítulo 1). Para hacer más entendibles los resultados de las interacciones derivados de este modelo, se han calculado también los resultados que serían esperables en la intensidad e importancia de las interacciones ( sensu Brooker et al. 2005, ver capítulo 4) para cada estrategia ecológica, cada fase ontogenética y cada uno de los tres niveles de aridez propuestos (Fig. B2).
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Figura B1. Modelo teórico donde se predice la evolución de la eficacia biológica (fitness) en un continuo dosel de planta nodriza-claro libre de vegetación a lo largo de un gradiente de aridez (modificado de Holmgren et al. 1997). Las estrategias ecológicas incluidas son tolerancia media a la sequía y a la sombra (en verde), intolerancia a la sequía (en azul), e intolerancia a la sombra (en rojo). Se indican variaciones en dicha evolución a lo largo de distintas fases ontogenéticas para cada estrategia: germinación y establecimiento inicial de plántulas (panel superior), crecimiento y supervivencia de individuos juveniles (2º panel) y coexistencia entre individuos adultos sin (3er panel) o con segregación de nicho (4º panel). Las flechas en el interior de cada panel indican el efecto de una carga constante de herbívoros a lo largo del gradiente de aridez, que es indiferente a las tolerancias a la sombra o a la sequía. Este efecto consiste en un aumento del fitness más cerca del dosel de la planta nodriza, que incrementará su importancia a niveles medios de aridez. A niveles más elevados de aridez, la escasez de fuentes alternativas de forraje hará que los herbívoros incrementen su esfuerzo de búsqueda y acaben perjudicando incluso a las plantas bajo el dosel (flecha diagonal en los paneles de la derecha). Este efecto será mucho más marcado en juveniles que en adultos, como muestran las flechas en los paneles.
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Figura B2. Intensidad e importancia de las interacciones planta-planta predichas a lo largo de un gradiente de aridez y en distintas fases ontogenéticas (germinación, juvenil y adulto; de arriba a abajo) predichos a partir del modelo teórico presentado en la Figura B1. Las distintas estrategias ecológicas incluidas siguen el mismo código de colores de dicha figura. La línea discontinua en medio de cada panel corresponde con el 0 (interacción neutra) de los indicadores tanto de intensidad como de importancia de las interacciones. Valores por encima o debajo de 0 implican facilitación o competencia, respectivamente. Las líneas continuas y discontinuas del panel inferior indican interacciones entre adultos con y sin segregación de nicho, respectivamente.
TRES ESTRATEGIAS, TRES RESPUESTAS Las especies tolerantes a la sombra se comportarán prácticamente del mismo modo a lo largo de su ontogenia (Fig. B1). Su elevada tolerancia a la sombra hace que sean capaces de aprovechar la mayor fertilidad en el suelo y disponibilidad hídrica comúnmente encontradas bajo el dosel de la planta nodriza (p. ej. Franco y Nobel 1989, Callaway 2007). Por tanto, su eficacia biológica siempre será mayor bajo una planta nodriza que en lugares libres de vegetación, independientemente de las condiciones de aridez. Un ejemplo clásico de este tipo de interacciones se da entre arbustos tolerantes a las altas temperaturas y los cactus columnares asociados en el sur de Estados Unidos y norte de Méjico. Así, los cactus columnares, como por ejemplo Carnegia gigantea (saguaro) o Neobuxbaumia tetetzo , ambos
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intolerantes a las altas temperaturas, crecen y sobreviven únicamente asociados a la sombra de plantas nodriza, que reducen la temperatura bajo su dosel (Shreve 1931, Niering et al. 1963, Valiente Banuet y Ezcurra 1991). Este comportamiento también se ha observado en la herbácea Brachypodium retusum a lo largo del gradiente ambiental estudiado en el capítulo 4 (Fig. B3; ver también Maestre y Cortina 2004b), o en las especies Enchylaena tomentosa y Rhagodia spinescens en el semiárido australiano (Hastwell y Facelli 2003, Prider y Facelli 2004). Especies intolerantes a altas radiaciones también se benefician de la presencia de especies nodriza en condiciones más mésicas. Por ejemplo, Gómez Aparicio et al. (2006) encontraron efectos muy positivos de la reducción de la luz incidente para las especies Acer opalus y Quercus pyrenaica en una zona seco subhúmeda (871 mm de lluvia anual), por lo que infirieron que el nicho de regeneración de estas especies se encontraría mayoritariamente bajo el dosel de especies nodriza, fundamentalmente arbustos (Castro et al. 2002, Gómez Aparicio et al. 2004, 2005). En todos los casos mencionados, estas especies mostraron una distribución restringida a la sombra de alguna especie nodriza bajo un amplio rango de condiciones de aridez. Esto da lugar a interacciones positivas muy intensas (al haber una eficacia biológica muy baja en los claros, cualquier índice que mida la intensidad de la interacción siempre será muy positivo). Sin embargo, a medida que aumente la aridez, algunas de estas especies se irán alejando de su óptimo ambiental, siendo más difícil su reclutamiento en medios muy áridos (nótese la bajada en la eficacia biológica de estas especies a medida que aumenta la aridez en la Fig. B1). Esta reducción de la eficacia biológica puede llegar incluso a la desaparición de esta especie bajo esas condiciones en particular, pese a la mejora microclimática promovida por la planta nodriza; esto provocaría un colapso de las interacciones positivas para estas especies (Michalet et al. 2006, Forey et al. 2009). Si se diera esta desaparición, obviamente la intensidad de la facilitación pasaría en un cambio brusco de muy positiva a cero (Fig. B2), ya que la especie ni siquiera estaría presente. Al contrario que la intensidad, la importancia de la facilitación para las especies intolerantes a la sequía se reducirá con el nivel de aridez. Esto ocurre porque la importancia es el efecto relativo de la planta nodriza con respecto a otras condiciones ambientales (Brooker et al. 2005) y, como se aprecia en la Fig. B1, la eficacia biológica de estas especies será mucho mayor en condiciones más húmedas, independientemente del efecto de la planta nodriza. Además, el efecto de esta planta nodriza no será tan positivo en condiciones más áridas, ya que el consumo de agua de esta nodriza puede llegar a superar a su mejora microclimática, dando lugar a condiciones de “sombra seca” y a efectos netos negativos sobre las especies vecinas (Valladares 2001, Valladares y Pearcy 2002).
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1.0
0.5 FACILITACIÓN
0.0
RII ST -0.5 RII SH Iimp ST Índices deinteracción Índices Iimp SH COMPETENCIA
-1.0 -150 -100 -50 0 50 100 PCA climático - LLUVIA + Figura B3. Índices de intensidad (RII) e importancia (Iimp) de la interacción de Brachypodium retusum con sus especies nodriza Stipa tenacissima (ST) y arbustos rebrotadores (SH) a lo largo del gradiente climático estudiado en los capítulos 4 y 5. Nótese la nula relación con el clima, y los relativamente altos valores de los índices calculados.
Las especies con una tolerancia media a la sombra y a la sequía presentarán un comportamiento muy distinto a lo largo de su ontogenia. Por un lado, la germinación y establecimiento temprano de estas especies será mayor bajo las plantas nodriza, debido fundamentalmente a un suelo más fértil y a una menor radiación solar (p. ej. McAuliffe 1988, Barberá et al. 2006). Este efecto positivo puede colapsar a medida que aumente la aridez, ya que las plántulas de estas especies son más sensibles al estrés hídrico y pueden no germinar o morir bajo niveles muy elevados de aridez, incluso considerando los cambios microclimáticos de la planta nodriza (Kitzberger et al. 2000, Ibañez y Schupp 2001, Gasque y García Fayos 2004). Esto dará lugar a una relación unimodal de la importancia e intensidad de las interacciones a medida que aumente la aridez (Fig. B2). Los juveniles de estas especies, por otro lado, competirán con la nodriza en condiciones más húmedas, tal como predicen todos los modelos teóricos (p. ej. Bertness y Callaway 1994, Brooker y Callaghan 1998, Michalet et al. 2006, Maestre et al. 2009a). Sin embargo, estas especies aumentarán su eficacia biológica bajo el dosel de una planta nodriza en condiciones intermedias de aridez, fundamentalmente por el efecto positivo de la sombra sobre el estado hídrico de los juveniles (Valiente Banuet y Ezcurra 1991, Maestre et al. 2003, Callaway 2007). A medida que aumente la aridez, la
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intercepción de la escasa lluvia por el dosel de la planta nodriza (Tielbörger y Kadmon 2000a), o el incremento de la competencia entre ambas especies por el agua (Maestre y Cortina 2004a), generarán condiciones de “sombra seca” que reducirán la eficacia biológica de las especies beneficiarias bajo el dosel de la planta nodriza. Esto originará una relación unimodal a lo largo del gradiente de aridez, tanto de la intensidad como de la importancia de la facilitación sobre especies con una tolerancia media a la sombra y a la sequía (Tielbörger y Kadmon 2000a, Maestre y Cortina 2004, Barchuck et al. 2005). En individuos adultos, la competencia se extenderá hasta niveles medios de aridez cuando no haya separación de nicho, ya que las especies competirán por el agua y perderán parte de los beneficios de la sombra promovida por la planta nodriza al sobrepasar la altura de su dosel (Miriti 2006, Callaway 2007, Valiente Banuet y Verdú 2008). Sin embargo, en condiciones más áridas, procesos como el levantamiento hidráulico (hydraulic lift) o, simplemente, el efecto de la sombra sobre la humedad del suelo puede incrementar el efecto positivo de la nodriza (Callaway 2007). Esto generará una relación monotónica o unimodal entre la intensidad de la interacción y la aridez, dependiendo de los efectos relativos de la sombra o el levantamiento hidráulico y la competencia en el agua disponible para las plantas adultas facilitadas (podemos encontrar efectos contrastados en Dawson 1993, Maestre et al. 2003 y Ludwig et al. 2004, Maestre y Cortina 2004a). Sin embargo, si existe segregación de nicho, la intensidad (y la importancia) de la facilitación aumentará de forma lineal con la aridez, ya que la competencia entre ambas especies se verá reducida por la segregación de nicho a la vez que el efecto de la sombra y la mayor fertilidad del suelo continuarán, incluso en condiciones más áridas (Armas y Pugnaire 2005, Sthultz et al. 2007). Las especies intolerantes a la sombra, por otro lado, experimentarán mayores tasas de germinación y supervivencia temprana lejos de plantas adultas a niveles bajos e intermedios de aridez (p. ej. Veblen 1989, Baskin y Baskin 1998), pero pueden verse beneficiadas por cierto nivel de sombreo en lugares más áridos (Escudero et al. 2005, Pueyo et al. 2009, capítulo 2, pero ver Olano et al. 2005). Aunque esto puede depender de otros factores, como el momento en que emergen estas plántulas (de la Cruz et al. 2008). La relación entre juveniles de especies intolerantes a la sombra y una planta nodriza será casi siempre negativa, como se ha visto en numerosos sistemas semiáridos de todo el mundo (Parker y Müller 1982, Marañón y Bartolomé 1993, Escudero et al. 1999, Forseth et al. 2001, Prider y Facelli 2004, Seifan et al. 2010, capítulos 1–3). Este efecto negativo se incrementará con el nivel de aridez (Eliason y Allen 1997, Davis et al. 1999, Espigares et al. 2004, Valladares et al. 2008,
199 DISCUSIÓN GENERAL capítulos 1 y 3, Soliveres et al. en preparación ; Fig. B2), al contrario de lo que predice la Hipótesis del Gradiente de Estrés (Bertness y Callaway 1994). Por último, la interacción entre individuos adultos de una especie intolerante a la sombra y una planta nodriza dependerá en buena medida de si esta especie puede “escapar” de la competencia por la luz u otros recursos a medida que crece o no. En el primer caso se puede reducir el efecto negativo de la nodriza de forma gradual a medida que la especie beneficiaria crece (capítulo 2); mientras que en el segundo, incluso los individuos adultos van a seguir compitiendo por este recurso, manteniendo así la interacción negativa a lo largo de toda la vida del individuo (Miriti 2006, Miriti et al. 2007). En general, la herbivoría aumentará el efecto positivo de las nodrizas en todos los casos, sin importar las tolerancias relativas de las especies implicadas a otros factores ambientales. Se ha visto una reducción de las interacciones competitivas cuando los herbívoros están presentes en numerosos ecosistemas semiáridos de todo el mundo (McNaughton 1978, Gurevitch et al. 2000, Fowler 2002, Rebollo et al. 2002, Veblen 2008). De hecho, este cambio en las interacciones debido a la herbivoría puede llegar a compensar los efectos negativos de la competencia por recursos, generando efectos netos positivos (Graff et al. 2007). Sin embargo, bajo presiones muy elevadas de herbivoría, como las que se pueden dar si aumenta la carga de herbívoros con las mismas condiciones climáticas o se reduce la productividad vegetal con la misma carga de herbívoros (Illius y O´Connor 1999), el efecto protector de las plantas nodriza frente a la herbivoría puede colapsar, dando como producto interacciones ligeramente positivas o neutras (Graff et al. 2007, Smit et al. 2007, capítulo 3, Figs. B1 y B2). No obstante, esto dependerá de la palatabilidad de la planta beneficiaria y sus vecinas, el grado de tolerancia a la herbivoría de las especies implicadas y sus diferentes fases ontogenéticas, y el tipo de herbívoro presente en la zona de estudio (revisado en Zamora et al. 2008).
¿EXISTE UN MODELO SENCILLO Y GENERAL QUE PREDIGA LOS RESULTADOS DE LAS INTERACCIONES ENTRE PARES DE ESPECIES? Incluso evitando, por simplicidad, incluir en un mismo modelo algunos de los factores clave que modulan las interacciones planta planta –como la presencia de factores de estrés relacionados o no con recursos (Maestre et al. 2009a), la continuidad de rasgos ecológicos que definen la tolerancia de las especies a dichos factores (Kobe et al. 1995, Ackerly 2003, Liancourt et al. 2005), o la co ocurrencia de diversos tipos de estrés a la vez (Riginos et al. 2005, Baumeister y Callaway 2006, Kawai y Tokeshi 2007), por nombrar unos cuantos– el
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modelo presentado en la Figura B1 ha generado un total de 36 escenarios distintos, modulados a su vez por el nivel de herbivoría presente en cada sitio. Algo que la mayoría de ecólogos definirían quizás como un modelo demasiado complejo y poco útil. Este modelo, sin embargo, es el único que ilustra la gran complejidad existente y los numerosos factores que afectan al comportamiento de las interacciones planta planta en los sistemas semiáridos a lo largo de gradientes climáticos (en este caso de aridez). La gran cantidad de factores que intervienen en las interacciones planta planta haría necesario crear modelos de esta complejidad para cada bioma o sistema de estudio (p. ej. sistemas de alta montaña o ecosistemas salobres requerirían de modelos diferentes al presentado, pero igualmente complejos). Además, a la hora de aplicar estos modelos a nivel de comunidad, deberíamos incluir los efectos derivados de que las especies no están organizadas en pares de individuos aislados, sino que están organizadas en manchas discretas donde coexisten numerosos individuos de diversas especies (p. ej. Aguiar y Sala 1999). Esto podría generar fenómenos de facilitación indirecta (Levine et al. 1999, Cuesta et al. 2010), segregación o complementariedad de nicho (Hector et al. 1999, Silvertown 2004, Stokes y Archer 2010), o competencia intransitiva (Laird y Schwamp 2006, 2009), que podrían variar todos los resultados predichos en los 36 escenarios mostrados en el modelo. Se sugiere, por tanto, que el único modelo sencillo, que podría resultar útil para predecir los resultados de las interacciones entre pares de especies e inferir estos resultados a redes de interacciones más complejas, como las encontradas en las comunidades naturales, y en todos los sistemas de estudio de forma general, es el modelo basado en el estrés individual , descrito en el capítulo 4. Este modelo resume todos los posibles resultados de todos los posibles escenarios prediciendo que las interacciones planta planta se tornarán más positivas a medida que la especie beneficiaria se aleja de su óptimo ambiental (ya sean estas condiciones más o menos áridas, con o sin herbivoría, frío, salinidad, etc.), llegando a un colapso cuando las condiciones ambientales son tan duras para esta especie en concreto que ni siquiera puede reclutar bajo las plantas nodriza. Definir el óptimo ambiental de cada especie es una tarea ardua, pero sin embargo, es la única forma de predecir de forma general el resultado de la interacción de una especie en concreto con sus vecinas. Para inferir la distancia de una especie en concreto a su óptimo podría considerarse utilizar el número de individuos reclutados en áreas libres de vegetación como un indicador de la distancia al óptimo de esa especie (más individuos reclutados significarán mejores condiciones ambientales para esa especie [Valiente Banuet et al. 2006, Valiente Banuet y Verdú 2007]). También se pueden inferir las tolerancias relativas a cualesquiera que sean los factores de estrés dominantes en cada área de
201 DISCUSIÓN GENERAL estudio a partir de las bases de datos y publicaciones disponibles sobre rasgos ecológicos de las especies implicadas. Por ejemplo, podemos encontrar algunas bases de datos de libre acceso para especies mediterráneas (i.e. BROT [Paula et al. 2009] o BASECO [Gachet et al. 2005]) o artículos científicos que incluyen rasgos ecológicos de multitud de especies de todo el mundo (p. ej. Niinemets y Valladares 2006, Poorter et al. 2009, Wright et al. 2004). Un ejemplo de este tipo de inferencia lo podemos encontrar en Pavoine et al. (2010). Alternativamente, se podrían utilizar modelos de distribución potencial (p. ej. Guisan y Zimmermann 2000, Loiselle et al. 2003) de las especies beneficiarias. Según el modelo basado en el estrés individual, estas especies experimentarán un efecto más positivo de la presencia de una nodriza a medida que nos alejemos del centro de su área de distribución potencial.
FACILITACIÓN A NIVEL DE COMUNIDAD : IMPLICACIONES PARA LA ESTRUCTURA Y EVOLUCIÓN DE
LOS ECOSISTEMAS SEMIÁRIDOS
El modelo basado en el estrés individual soluciona algunos de los supuestos más problemáticos anteriormente mencionados (existencia de un gradiente de estrés general para todas las especies de una comunidad dada, y de estrategias ecológicas que se mantienen estables a lo largo de gradientes ambientales amplios) mediante el establecimiento de un gradiente de estrés único para cada especie. Este gradiente está basado en medidas de la tolerancia ecológica de cada especie a distintos factores ambientales, cuantitativas y extrapolables a cualquier sistema de estudio. Así pues, la ausencia de estos supuestos, junto con la consideración de la diferente naturaleza de los gradientes ambientales que podemos encontrar en la naturaleza (compuestos por factores de estrés independientes o correlacionados entre sí) y las diferencias en las tolerancias relativas entre las especies que coexisten en una comunidad dada, nos permitirá considerar finalmente la evolución de la importancia de las interacciones planta planta a nivel de comunidad bajo distintas condiciones ambientales. En la Figura B4 se muestra un modelo conceptual basado en una sencilla comunidad de tres especies (A, B y C). Cada especie difiere en su óptimo ambiental, y por tanto, tendrá una distribución diferente (basada en su eficacia biológica bajo distintas condiciones) a lo largo de un gradiente ambiental. Si no consideramos las interacciones positivas entre plantas, podemos observar un solapamiento mínimo en las distribuciones de estas tres especies, que vendría dado por: 1) las diferencias en sus tolerancias específicas a los distintos factores de
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estrés encontrados a lo largo de ese gradiente ambiental (Chapin et al. 1987), y 2) la exclusión competitiva que ejerce la especie más adaptada a las condiciones locales sobre las demás (Grime 1973; panel izquierdo de la Fig. B4). En cambio, si consideramos las interacciones facilitativas, se puede observar como la distribución espacial de cada especie aumenta (expansión de nicho; Bruno et al. 2003), ya que las especies más adaptadas a las condiciones locales aumentan las eficacia biológica de las menos adaptadas (panel derecho de la Fig. B4). Sin embargo, incluso teniendo en cuenta estas interacciones positivas, llega un momento en que las condiciones ambientales son demasiado duras para una especie dada, y el reclutamiento de esta especie en concreto es imposible, dando como resultado una eficacia biológica igual a cero, pese a la mejora microambiental que pudiera ejercer la especie nodriza (Kitzberger et al. 2000, Ibañez y Schupp 2001; flechas en el panel derecho de la Fig. B4). Sin embargo, el que el efecto positivo de la facilitación desaparezca para esa especie en concreto no significa que haga lo propio a nivel de la comunidad entera, ya que habrá otras especies capaces de reclutar bajo esas condiciones locales, pero lo suficientemente poco adaptadas como para verse beneficiadas por la presencia de una especie nodriza. Esto explicaría por qué en diversas comunidades se observa una reducción de la facilitación a escala de mancha, pero no un efecto significativo de esta reducción en la facilitación sobre la diversidad local (revisado en Michalet et al. 2006).
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Figura B4. Modelo teórico donde se predice la eficacia biológica de tres especies con rasgos ecológicos contrastados a lo largo de un gradiente ambiental. En el panel izquierdo se consideran sólo las tolerancias ecofisiológicas de cada especie y la exclusión competitiva. En el panel de la derecha se considera la expansión de nicho promovida por las especies nodriza (especies más adaptadas a las condiciones locales). Bajo condiciones demasiado severas para cada especie, su reclutamiento es imposible, incluso incluyendo la expansión de nicho, y la facilitación colapsa a nivel de esa especie (flechas en el panel). Cuando dejan de existir especies adaptadas a las condiciones locales a lo largo de este gradiente ambiental, la facilitación colapsa a nivel de comunidad (línea superior en el panel derecho). Hasta llegar a ese punto, la importancia de las interacciones positivas a nivel de comunidad permanece estable, ya que la identidad, pero no la cantidad, de especies facilitadas es lo que cambia a lo largo del gradiente.
Cuando el gradiente ambiental esté formado por diversos factores de estrés, independientes entre sí, la importancia de la facilitación a nivel de la comunidad entera se mantendrá constante hasta que ya no quede ninguna especie adaptada a las condiciones locales que pueda facilitar a las demás, lo que llevaría al colapso de la facilitación (Silliman et al. 2005, Michalet et al. 2006; línea superior del panel izquierdo de la Fig. B4). Casos en que el gradiente ambiental esté dominado por un solo factor de estrés, o varios correlacionados entre sí (p. ej. Bertness y Shumway 1993, Callaway et al. 2002), serían simplemente una fracción del escenario anteriormente descrito. Ambos casos están separados por la línea discontinua en la Figura B4. Este sencillo modelo conceptual resume el por qué las interacciones positivas son importantes en numerosos ecosistemas de todo el mundo, y no sólo en los considerados “estresantes” y el por qué las interacciones positivas serán más importantes bajo niveles “intermedios de estrés”, se trate del bioma que se trate (revisado en Holmgren y Scheffer 2010). También explica el colapso de las interacciones positivas bajo
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elevados niveles de estos factores de estrés a lo largo de gradientes ambientales, ya sea para especies concretas (Kitzberger et al. 2000, Ibañez y Schupp 2001), o en comunidades enteras (Silliman et al. 2005, Michalet et al. 2006). La Figura B4 ayuda a entender el papel de la facilitación en la evolución y resiliencia de las comunidades naturales. Estas interacciones positivas asegurarán el nicho de regeneración de las especies menos adaptadas a las condiciones locales (Valiente Banuet et al. 2006), sean estas las que sean, o el mantenimiento de la diversidad y el funcionamiento ecosistémico en condiciones ambientales menos productivas (Mulder et al. 2001, Kikvidze et al. 2005, Badano y Cavieres 2006), como las predichas con el cambio climático para la cuenca Mediterránea (Brooker 2006). Esto ocurrirá siempre y cuando queden especies que presenten tolerancias ecofisiológicas a las condiciones ambientales existentes y puedan suavizar estas condiciones para las especies menos adaptadas. Ahora bien, al igual que la mayoría de artículos relacionados con las interacciones entre plantas, el modelo propuesto en la Figura B4 no considera el hecho de que las especies de una comunidad no se relacionan par a par, si no que forman ensamblajes más o menos complejos que atañen a todas las especies que coexisten en esa comunidad (Maestre et al. 2010). Un ejemplo de ello serían las manchas de vegetación de las tierras secas, donde coexisten un elevado número de especies, y donde es probable que se den interacciones positivas y negativas entre multitud de ellas, dando lugar a complejas redes de interacción (Verdú et al. 2010). Como se ha mencionado antes, esto puede dar lugar a procesos de facilitación indirecta, competencia intransitiva, segregación o complementariedad de nicho (Grace et al. 1993, Hector et al. 1999, Levine et al. 1999, Silvertown 2004). El incremento de la diversidad mediante la expansión de nicho, junto con el aumento en la heterogeneidad en los recursos por el que estas especies compiten, promovidos ambos por la presencia de especies nodriza, puede dar lugar a aumentos desproporcionados en la diversidad local (Bowker et al. 2010). Aunque estos efectos ya se conocían y han sido estudiados por separado (revisado en Brooker et al. 2008), hasta ahora ningún modelo teórico ha incluido ambos mecanismos a la hora de predecir el papel de la facilitación en la diversidad de las comunidades naturales (Callaway 2007). Se pretende dar ese paso con el modelo mostrado en la Figura B5. Este modelo se basa en la distribución que podemos encontrar para cualquier especie a lo largo de un gradiente espacial o temporal en cualquier libro de ecología, esto es, una campana de Gauss más o menos apuntada. Como hemos explicado antes, los rasgos ecológicos de cada especie, y sus tolerancias relativas a los diferentes factores de estrés presentes a lo largo de ese gradiente, definirán su óptimo ambiental, que variará según la
205 DISCUSIÓN GENERAL especie. En este modelo, se utiliza un conjunto inicial de siete especies (de la A a la G). El nicho potencial de estas especies (panel superior izquierdo de todos los escenarios de la Fig. B5) vendrá indicado por los diversos filtros de establecimiento, esto es, llegada de propágulos (dispersión) y tolerancia a las condiciones locales. Una vez llegados a este punto es donde las interacciones bióticas adquieren mayor importancia (p. ej. Huston 1999, Rajaniemi et al. 2006, pero ver Mitchell et al. 2009, Gotelli et al. 2010).
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Figura B5. Modelo teórico donde se predicen los nichos potenciales y ocupados de distintas especies a lo largo de un gradiente ambiental, y como esto se refleja en la riqueza local de especies de una comunidad dada a partir de un conjunto inicial de siete especies (A–G). Las predicciones se realizan en cuatro escenarios distintos teniendo en cuenta: A) homogeneidad en los recursos por los que compiten las plantas, la cual hace imposible la intransitividad en la competencia o la segregación de nicho, B) heterogeneidad en los recursos, haciendo posible cierto grado de segregación de nicho o competencia intransitiva entre las especies existentes, C) expansión de nicho de las especies menos adaptadas a las condiciones locales promovida por especies nodriza, lo cual genera la llegada de nuevas especies que inicialmente no estaban en la comunidad, pero condiciones homogéneas en los recursos por los que estas especies compiten, y D) el doble efecto de las plantas nodriza (incrementar la heterogeneidad de nutrientes y aumentar el conjunto de especies mediante expansión de nicho) en un sistema ya de por sí heterogéneo. En los escenarios A y C se han sombreado los nichos ocupados por cada especie, para facilitar su comprensión. En los escenarios B y D esto no ha sido posible por el alto grado de solapamiento entre nichos que se predice. Nótese como la relación entre la riqueza de especies y la productividad (panel de abajo a la derecha en cada escenario) va cambiando según consideremos unos procesos u otros.
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En un primer escenario suponemos una disposición homogénea de los recursos por los que compiten estas siete especies (escenario A en la Fig. B5). En estas condiciones, es imposible que exista segregación de nicho o intransitividad en la competencia (Huston 1979, 1999). También obviamos aquí el efecto facilitador que pueden ejercer unas especies sobre otras. Por tanto, la exclusión competitiva es la única interacción planta planta que nos queda. En unas condiciones más o menos homogéneas, las especies más adaptadas a las condiciones locales (competitivas, sensu Grime 1979) pueden desplazar a las menos adaptadas, haciendo que su nicho real sea menor que el potencial. Poniendo como ejemplo las especies A, B y C, cumpliéndose que A>B>C tenemos que A excluirá a B y C en los lugares donde esté presente, reduciendo el nicho real de B y C. Y B hará lo mismo con C (áreas sombreadas del escenario A). En el escenario B se considera el efecto de la heterogeneidad ambiental, esto es, la variabilidad espacial o temporal en los recursos por los que compiten las especies presentes en una comunidad. Esto permitirá 1) que no haya una jerarquía marcada en la competencia (competencia intransitiva), si no que, dependiendo de las condiciones microambientales, la especie A pueda desplazar a las demás o pueda ser desplazada por otras (Gilpin 1975, Grace et al. 1993), y 2) que se pueda dar segregación de nicho, esto es, los nichos reales de diferentes especies pueden mantenerse aunque éstas compitan por el mismo recurso, ya que difieren en la toma de este recurso en el espacio o en el tiempo (Silvertown 2004). Ambos procesos son importantes, ya que pueden aumentar la diversidad a nivel local (Grace 1993, Huston 1999, Laird y Schwamp 2006; ver Tilman 1994 para una aproximación alternativa). En el escenario B de la Figura B5 podemos ver, por ejemplo, como A no excluye competitivamente a B de su nicho potencial (aunque reduce su nicho real considerablemente) pese a su superioridad competitiva. Esto ocurre debido al efecto indirecto de D, una especie que supera competitivamente a A. Por tanto, A, B y D coexisten (competencia intransitiva: A>B>D>A, que genera facilitación indirecta de D sobre B). Alternativamente, G y F pueden coexistir a pesar de que sus nichos potenciales se solapan. Esto se debe a que ambas especies no compiten exactamente entre ellas pese a necesitar los mismos recursos, ya que los toman en lugares o momentos diferentes (segregación de nicho, p. ej. Sala et al. 1989, capítulo 1). En sistemas heterogéneos y relativamente ricos en especies, estas especies pueden complementarse, de forma que toman los recursos disponibles de forma más eficiente, incrementando la productividad a nivel del ecosistema (Hector et al. 1999). Aunque esta complementariedad de nicho es clave para entender la relación entre diversidad y productividad, por lo que se ha incluido en el modelo, no afecta a la riqueza de especies, si no
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a la relación de la riqueza con la productividad total del sistema, por lo que no se discutirá ahora el papel de este proceso. El escenario C, por otro lado, es exactamente idéntico al A, salvo que se ha incluido la expansión de nicho ( sensu Bruno et al. 2003). Hasta el momento, este es el único efecto de las interacciones positivas que se había incluido en los modelos teóricos sobre el efecto de las interacciones planta planta en la riqueza local de especies (Hacker y Gaines 1997, Bruno et al. 2003, Lortie et al. 2004a, Michalet et al. 2006). Como predicen todos estos modelos, y se ha matizado en esta discusión, las especies más adaptadas a las condiciones locales incrementarán la eficacia biológica de las especies menos adaptadas, e incluso pueden permitir la colonización de otras especies, que no habían podido cruzar los filtros ambientales por ellas mismas (H e I, en el escenario C). Al haber ahora más especies en la comunidad, hay mayores posibilidades de que se de segregación o complementariedad de nicho. Sin embargo, este escenario sigue asumiendo unas condiciones homogéneas, que permiten la existencia de especies “competitivas” que excluyan a otras especies de sus nichos potenciales. Esto daría lugar al incremento de la riqueza, gracias a la expansión de nicho, predicho en condiciones más improductivas debido a que las especies “tolerantes al estrés” facilitan a las especies “competitivas” en condiciones improductivas (Hacker y Gaines 1997, Travis et al. 2005, Michalet et al. 2006; especie I en el escenario C). Aunque también puede incrementar la diversidad en situaciones mucho más productivas, donde la especie más adaptada a las condiciones locales (A en este caso), facilita la entrada de una especie menos adaptada (H). Este fenómeno ha sido observado en sistemas considerados muy productivos, como el bosque lluvioso tropical o bosques de ribera, entre otros (revisado en Holmgren y Scheffer 2010). Finalmente, en el escenario D se considera un medio de por sí heterogéneo, como la mayoría de medios naturales, donde además se incluye el doble efecto positivo que ejercen las especies nodrizas sobre la diversidad local en una comunidad dada. Estos efectos son: 1) incrementar el conjunto de especies disponibles por medio de la expansión de nicho (Bruno et al. 2003, Lortie et al. 2004a, Badano y Cavieres 2006), y 2) aumentar la heterogeneidad ambiental bajo su dosel, lo que incrementa aún más la heterogeneidad en los recursos por los que estas especies compiten (p. ej. Pugnaire et al. 1996a, Cuesta et al. 2010). Este escenario no había sido considerado hasta el momento para evaluar el efecto de la facilitación sobre la diversidad local (Callaway 2007). Sin embargo, es en este escenario donde las posibilidades de que se de competencia intransitiva y la segregación o complementariedad de nicho son máximas, lo que llevaría a un aumento de la diversidad desproporcionado provocado por procesos de retroalimentación entre ambos procesos (más especies disponibles y más
209 DISCUSIÓN GENERAL heterogeneidad en la competencia generan competencia intransitiva y/o segregación de nicho, que a su vez permiten que más especies puedan coexistir). Este proceso de retroalimentación positiva aumenta la diversidad local gracias a dos efectos fundamentales. Primero, porque aumenta el nicho potencial de la mayoría de las especies del conjunto, y segundo, porque se reducen las posibilidades de exclusión competitiva. Pocas especies son excluidas de sus nichos potenciales ya que, o bien difieren en el nicho de las especies con las que coexisten (H, D y A, en el escenario D), o bien, terceras especies evitan que estas sean excluidas (D permite que B no sea excluida por A). Este proceso de retroalimentación positiva, que lleva a la reducción de la exclusión competitiva para muchas especies, podría ser la causa del incremento de diversidad a lo largo de la sucesión en algunos ecosistemas (Johnston y Odum 1956, McKindsey y Bourget 2001), o de los resultados contrastados en la relación entre diversidad e invasibilidad de los ecosistemas (revisado en Bruno et al. 2003). Sistemas más diversos podrán atraer nuevas especies (sean estas invasoras o no) si las características del sistema de estudio (i.e. heterogeneidad en los recursos por los que compiten las especies) permiten que se den estos procesos de retroalimentación, pero evitarán la entrada de nuevas especies si estos procesos de retroalimentación no se dan y domina la exclusión competitiva. La coexistencia o no de todos estos factores (expansión, segregación y complementariedad de nicho, y competencia intransitiva) puede modificar de forma sustancial la relación entre la riqueza de especies y la productividad del ecosistema, incluso con las mismas especies, estudiadas a la misma escala y con la misma amplitud del gradiente estudiado (panel inferior derecho de todos los escenarios; ver Whitakker 2010, Mittlebach 2010 y referencias en estos textos para una discusión detallada sobre los efectos de la escala de estudio en la relación riqueza productividad). Esto podría ayudar a explicar la gran cantidad de excepciones que se han encontrado a esta relación unimodal entre riqueza y diversidad en numerosos ecosistemas de todo el mundo a nivel local (p. ej. Grace 1999, Waide et al. 1999, Gillman y Wright 2006). El modelo propuesto contradice no sólo la idea de que la facilitación es sólo importante en los sistemas más improductivos y estresantes (p. ej. Bertness y Callaway 1994), si no también que la facilitación sólo afecte a esta relación entre diversidad y productividad a niveles medios bajos de ésta última (Michalet et al. 2006). Se propone en esta discusión que evaluar el papel relativo de la expansión, complementariedad y segregación de nicho, junto con el grado de intransitividad de la competencia nos permitirá, por un lado, evaluar de una forma completa el papel de las interacciones planta planta en la diversidad local (Brooker et al. 2008), y por otro, definir la relación entre esta diversidad local y la productividad y el funcionamiento del ecosistema (Mulder et al. 2001, Callaway 2007,
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Maestre et al. 2010). Ambas cuestiones no son sólo atractivas desde el punto de vista teórico, ya que nos permiten arrojar algo de luz sobre los mecanismos implicados en la relación entre la diversidad y la productividad de los ecosistemas (Whitakker 2010), sino que también son cruciales para finalmente entender el papel de la biodiversidad en el funcionamiento de los ecosistemas y los servicios que éstos proveen (Hooper et al. 2005, Michalet et al. 2006) y, por tanto, en como entendemos y manejamos la naturaleza. Sin embargo, evaluar el papel de cada uno de los procesos mencionados a nivel de comunidad requeriría experimentos muy costosos y logísticamente inabordables, por lo que se ha sugerido el uso de estudios observacionales para evaluar la importancia relativa de las interacciones bióticas a nivel de comunidad (p. ej. Gotelli y Graves 1996, Brooker et al. 2008, Pausas y Verdú 2010). A pesar de que las herramientas existentes han permitido un mejor entendimiento de los mecanismos de ensamblaje de especies y el papel de las interacciones bióticas en este proceso (p. ej. Gotelli y Graves 1996, Dullinger et al. 2007, Maestre et al. 2008, 2010, Rooney 2008, Bowker et al. 2010, Gotelli et al 2010), éstas son insuficientes por el momento para discernir entre los procesos anteriormente mencionados. Aunque queda mucho por hacer en este aspecto, se ofrecen en los trabajos desarrollados en esta tesis doctoral (capítulos 4 y 5) una serie de herramientas para diferenciar entre los procesos de competencia intransitiva, expansión y segregación de nicho, y su efecto sobre la riqueza de especies y el patrón filogenético local, a partir de estudios observacionales. El refinamiento de estas técnicas ayudará a entender finalmente el papel de las interacciones bióticas no tróficas en el ensamblaje de las especies que forman las comunidades naturales, y la relación entre la diversidad de estas especies y la productividad de los ecosistemas.
IMPLICACIONES DE LA FACILITACIÓN EN LA RESTAURACIÓN DE LOS SISTEMAS SEMIÁRIDOS El papel que la facilitación puede jugar en la restauración de los ecosistemas Mediterráneos en general, y los semiáridos en particular, ya ha sido discutido ampliamente con anterioridad (Pugnaire et al. 1996, Maestre et al. 2001, Castro et al. 2002, Gómez Aparicio et al. 2004, Cortina y Maestre 2005, Padilla y Pugnaire 2006, Valladares y Gianoli 2007, Pueyo et al. 2009, Cortina et al. 2010). Sin embargo, en la inmensa mayoría de estos trabajos se trata el papel de las interacciones facilitativas en un contexto puramente climático, asumiendo que la importancia de estas interacciones para el éxito de la restauración aumentará con el nivel de aridez. Muy pocos trabajos han tenido en cuenta el colapso de estas interacciones facilitativas bajo niveles extremadamente altos de aridez o herbivoría (Valladares y Gianoli 2007, Pueyo
211 DISCUSIÓN GENERAL et al 2009, Cortina et al. 2010), o la importancia relativa de las interacciones facilitativas frente a otros múltiples procesos y herramientas importantes para la restauración (Méndez et al. 2008, Pueyo et al. 2009, Cortina et al. 2010). Se discute en esta sección la idoneidad de utilizar las interacciones facilitativas en restauración en sistemas semiáridos, con respecto a otras técnicas disponibles. También se discute como puede adaptarse el manejo de los ecosistemas semiáridos a las futuras condiciones ambientales que se esperan con el cambio climático, y el papel que la facilitación puede jugar en dicho proceso. El funcionamiento ecosistémico en la mayoría de ambientes semiáridos viene dado por la dinámica fuente sumidero, que permite a las manchas de vegetación retener el agua de escorrentía, recursos y semillas procedentes de las áreas de suelo desnudo. Esto favorece la captura y reciclaje de nutrientes y aumenta la colonización de nuevas especies en las manchas de vegetación (Ludwig y Tongway 1995, Aguiar y Sala 1999, Puigdefábregas et al. 1999). Como ya se ha comentado en la introducción general, la degradación de estos sistemas viene dada por la pérdida de esta estructura de la vegetación (reducción del tamaño y distanciamiento entre los parches [Maestre et al. 2006, Kefi et al. 2007], o reducción de la cobertura [Maestre y Escudero 2009]). La degradación de los sistemas semiáridos no es un proceso lineal, sino que experimenta distintos umbrales de degradación correspondientes con cambios drásticos en la estructura, composición y funcionamiento ecosistémicos (Van de Koppel et al. 1997; ver Fig. B6, modificado de Cortina et al. 2010). Aunque se ha visto que el funcionamiento ecosistémico no está necesariamente unido a su “restaurabilidad” (Cortina et al. 2005, Maestre et al. 2006), conocer en qué estado funcional se haya el ecosistema es básico para: 1) evaluar las medidas más adecuadas para su restauración, y 2) definir áreas prioritarias para la conservación o restauración (Cortina et al. 2005, 2010, Méndez et al. 2008). Así por ejemplo, en el caso de los espartales de Stipa tenacissima , aunque dependerá también de objetivos sociales, políticos y económicos, dos tipos de áreas prioritarias para la restauración de las estepas de Stipa tenacissima serían aquellas con niveles de funcionalidad intermedios (“estepas” y “estepas empobrecidas” sensu Cortina et al. 2010). En el caso de las estepas empobrecidas, para asegurarnos que la pérdida en la cobertura vegetal y la diversidad no alcanza estados de degradación severos (Maestre y Escudero 2009). En el caso de las estepas, en cambio, la prioridad se debería a que podemos ganar bastante en funcionalidad y servicios ecosistémicos con relativamente poca inversión.
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Figura B6. Esquema donde se resumen los cuatro posibles estados de degradación de una estepa de Stipa tenacissima : estepa con matorral (A), estepa sin matorral (B), estepa degradada o empobrecida (C) y área desertificada o “badland” (D). Se indican de forma esquemática las actuaciones prioritarias en cada etapa. La introducción de especies leñosas, prestando atención a la procedencia y calidad del material utilizado, es recomendable en todas las etapas, aunque el grosor de la flecha indica en cada caso el grado de prioridad de esta práctica. Se señalan las áreas prioritarias para la restauración con un círculo. EI = estructuras inertes para la captura y retención de escorrentía; ME = mallas de exclusión de herbívoros.
Hemos de tener en cuenta que el principal cuello de botella para el establecimiento de las plantas en medios semiáridos es el agua disponible (Eldridge et al. 1991, Whitford 2002, Holmgren et al. 2006). Por tanto, sea cual sea la herramienta que se utilice y el estado de degradación de la zona donde se actúe, un año seco dará un rendimiento menor del esfuerzo
213 DISCUSIÓN GENERAL invertido (Navarro et al. 2006 y referencias en dicho texto). Por tanto, predecir de alguna manera las condiciones climáticas venideras nos daría una información crucial sobre cuando actuar para maximizar el éxito de los esfuerzos de restauración (Cortina et al. 2010). La gran importancia de la alternancia de los eventos climáticos globales (El Niño/La Niña) para el patrón de precipitaciones de numerosas regiones de todo el mundo, incluida España (ver Holmgren et al. 2006), nos ofrece esta herramienta de predicción (Valladares y Gianoli 2007). Así, la alternancia entre las fases del Niño y la Niña nos ofrece ventanas temporales de vital importancia para predecir estos años lluviosos y centrar en ellos los proyectos de restauración. Si bien la alternancia de estos fenómenos no es predecible al 100%, presenta un tiempo de recurrencia aproximado de entre tres y seis años (Holmgren et al. 2006 y referencias en ese texto). Por tanto, mientras no se desarrollen mejores herramientas de predicción, cuando en un año en concreto se de la fase del Niño (condiciones más lluviosas para España), podemos inferir que los dos siguientes años serán igualmente benignos. Los esfuerzos destinados a la restauración de los sistemas semiáridos deberían centrarse exclusivamente en estos años, probablemente más lluviosos que la media, donde el éxito de los proyectos de restauración seguramente será mayor, sean cuales sean las herramientas que apliquemos. Una vez establecido el cuándo y el dónde es mejor actuar, podemos centrarnos en cómo es mejor hacerlo. Se utiliza aquí como base el diagrama modificado de Cortina et al. (2010) para ilustrar el papel relativo de las interacciones planta planta frente a otros procesos y herramientas útiles para asegurar el éxito de la restauración en los espartales de Stipa tenacissima (Fig. B6). En este diagrama se establecen cuatro estados alternativos en la degradación del funcionamiento ecosistémico en el caso de estos espartales que varían desde el suelo desnudo a la estepa con vegetación arbustiva. En las etapas menos degradadas (estepa con vegetación arbustiva, estepa y estepa empobrecida) interesaría incrementar la cobertura de vegetación arbustiva, lo cual se ha demostrado muy positivo para el funcionamiento y la diversidad de los espartales ibéricos (Maestre y Cortina 2005, Cortina y Maestre 2005, Maestre et al. 2009b). Para ello, en el caso de la estepa con vegetación arbustiva (no en el resto de etapas de degradación), podemos confiar en los procesos de nucleación que comúnmente suceden en sistemas Mediterráneos, donde los animales dispersan de forma natural propágulos de numerosas especies bajo los arbustos o árboles remanentes (efecto percha), que a su vez se establecerán con más éxito bajo estos arbustos debido a las condiciones de sombreo y mayor fertilidad del suelo (Verdú y García Fayos 1996, Pausas et al. 2006, Méndez et al. 2008). Si bien este proceso natural puede incrementar la diversidad y la cobertura de arbustos rebrotadores de forma natural en estos espartales y en numerosos
214
ecosistemas Mediterráneos (restauración pasiva), es poco probable que se aumente de forma significativa la colonización de estas especies en lugares donde no haya arbustos o árboles remanentes que atraigan a los animales dispersores. En otras palabras, la colonización natural sólo se dará en lugares donde previamente ya haya algún arbusto presente (los animales depositarán las semillas en esos lugares), no creándose nuevos parches de vegetación arbustiva en otros lugares (Cortina y Maestre 2005). Por tanto, incrementar la tasa de colonización y el número de parches formados por estos arbustos es deseable, especialmente en las estepas donde éstos no estén presentes (Cortina y Maestre 2005, Maestre y Cortina 2005). Para ello, utilizar las interacciones positivas del esparto con estas especies ha sido recomendado (p. ej. Maestre et al. 2001, Gasque y García Fayos 2004, Barberá et al. 2006, Navarro et al. 2008). Sin embargo, hay que considerar el hecho de que estas interacciones pueden colapsar bajo niveles extremos de aridez o herbivoría (Maestre y Cortina 2004a, capítulo 3). Bajo estas condiciones, el establecimiento de pilas de ramas u otras estructuras inertes (p. ej. microcuencas) que provean mejores condiciones hídricas y de fertilidad del suelo, o bien que reduzcan los efectos de la herbivoría (p. ej. mallas protectoras), para los plantones introducidos o para la colonización natural son recomendables (Tongway y Ludwig 1996, Ludwig y Tongway 1996, Holmgren et al. 2006, Soliveres et al. 2008, Pueyo et al. 2009). El uso de estructuras inertes destinadas a aumentar la retención del agua de escorrentía y otros recursos, también es recomendable en lugares muy degradados, independientemente de su nivel de aridez, debido a la ausencia de plantas que puedan ejercer como nodriza (estado más degradado en la Fig. B6). También en estas zonas más degradadas, donde con seguridad se ha perdido parte, o todo el horizonte orgánico del suelo, puede ser conveniente incrementar la fertilidad del suelo mediante el uso de enmiendas orgánicas. Si bien esto dependerá de las características físico químicas del sitio a restaurar y de las condiciones climáticas (Soliveres et al. en prensa y referencias en ese texto). Otra alternativa para incrementar la cobertura vegetal, especialmente en los sitios más áridos o degradados, es la introducción de especies más heliófilas (p. ej. Retama sphaerocarpa ; Moro et al. 1997, Caravaca et al 2003). Los capítulos 1 y 3 de esta tesis doctoral han demostrado que el uso de las interacciones facilitativas tampoco sería recomendable para la introducción de estas especies, siendo preferible introducir los plantones en lugares libres de vegetación. Las interacciones facilitativas, por tanto, aunque son una herramienta de restauración muy útil en determinados escenarios de restauración, no son recomendables en condiciones de aridez extrema o herbivoría muy intensa. En estas situaciones, otras medidas como las anteriormente
215 DISCUSIÓN GENERAL explicadas (y las discutidas más abajo) pueden dar mejores resultados en los proyectos de restauración. En algunas ocasiones, especialmente en los futuros escenarios predichos con el cambio climático, las condiciones ambientales pueden ser extremadamente adversas para la gran mayoría de especies de interés, de forma que su reclutamiento sea imposible, incluso bajo el dosel de una especie nodriza o con la presencia de las estructuras inertes mencionadas con anterioridad. En este caso, una cuidadosa selección de las poblaciones de donde se obtiene el material para la restauración, y el establecimiento de una calidad de planta adecuada para las condiciones ambientales puede mejorar el rendimiento de algunas especies (Cortina et al. 2006, Villar et al. en prensa ). Aunque esta selección y preparación del material es importante en cualquier proyecto de restauración, cobra especial importancia en sistemas particularmente áridos, donde la procedencia o la calidad de la planta pueden decidir el destino de las plántulas introducidas (Navarro et al. 2006, Trubat et al. 2008). La aplicación conjunta de la selección del material vegetal adecuado (especies y procedencias), en conjunto con una buena calidad de planta y el uso de estructuras inertes, puede llevarnos al éxito en la restauración bajo estas condiciones más áridas o degradadas (p. ej. proyecto FUNDIVFOR en el sureste ibérico, http://80.24.165.149/fundivfor/). A pesar de que se ha sugerido que los arbustos pueden ser la mejor opción posible como planta nodriza en ecosistemas Mediterráneos en las actuales condiciones climáticas (Gómez Aparicio et al. 2004, Gómez Aparicio 2009), se debería conceder un mayor crédito como especies nodriza a las herbáceas perennes como Stipa tenacissima en el futuro . Estas herbáceas es probable que ejerzan efectos más positivos sobre las especies leñosas de interés en las futuras condiciones predichas con el cambio climático, ya que el incremento en la frecuencia de eventos de lluvia torrenciales puede incrementar la segregación de nicho entre S. tenacissima y sus arbustos vecinos, pero no así en el caso de que la nodriza sea otro arbusto.
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CONCLUSIONES GENERALES
De los trabajos desarrollados en la presente tesis doctoral se extraen las siguientes conclusiones generales:
1) La tolerancia a la sombra es un factor clave a la hora de entender las interacciones planta planta en medios semiáridos. La sombra generada por Stipa tenacissima ejerció un efecto negativo sobre Retama sphaerocarpa y Lepidium subulatum , ambas especies intolerantes a la sombra.
2) Los efectos de los cambios en el patrón de las precipitaciones predichos con el cambio climático varían dependiendo de las especies implicadas. En general, la reducción en las lluvias de primavera aumentó los efectos negativos sobre las especies intolerantes a la sombra.
3) El efecto competitivo de las especies herbáceas sobre las leñosas se reduce con la edad de éstas últimas, lo que sugiere la existencia de procesos de segregación de nicho. El aumento de los eventos de lluvia torrencial, predicho con el cambio climático, puede acelerar la segregación de nicho entre especies leñosas y herbáceas.
4) Los factores climáticos que influyen en las interacciones planta planta a lo largo de su ontogenia presentan una heterogeneidad espacial marcada. Mientras que la lluvia fue el modulador fundamental de la interacción entre Lepidium y Stipa en la ladera de solana, otros factores climáticos fueron importantes en la ladera de umbría.
5) La herbivoría es un factor clave en las interacciones planta planta, que puede llegar a compensar los efectos negativos derivados de la competencia por nutrientes (i.e. luz o agua). La reducción del impacto de la herbivoría promovida por el efecto protector de Stipa sobre Retama redujo la competencia entre ambas especies, dando como resultado un efecto neto positivo de Stipa sobre Retama .
6) La herbivoría y el estrés hídrico presentan interacciones complejas, existiendo una jerarquía entre ambos factores. La aridez por sí misma no tuvo un efecto importante en la interacción entre Stipa y Retama bajo niveles muy altos de herbivoría. Sin embargo, la aridez moduló indirectamente la presión de herbivoría afectando a la productividad vegetal, y por tanto, a la cantidad de forraje disponible para los herbívoros y a su impacto sobre la especie estudiada.
7) Existe una jerarquía entre las condiciones climáticas y la distancia filogenética entre los arbustos rebrotadores y sus vecinas a la hora de definir la interacción entre ambas. Distancias filogenéticas entre 207 y 273 millones de años produjeron siempre interacciones competitivas. Mientras que valores fuera de este rango dieron lugar a interacciones neutras o facilitativas, dependiendo de las condiciones climáticas. Ni la distancia filogenética ni el clima fueron factores clave entre la interacción entre Stipa y sus especies vecinas.
217 CONCLUSIONES
8) El efecto positivo de Stipa sobre Lepidium durante la germinación de éste último fue clave a la hora de definir el resultado neto de la interacción entre ambas especies. Esto quedó demostrado por el elevado grado de co ocurrencia encontrado a pesar de la dominancia de interacciones negativas entre ambas especies a lo largo de la vida de Lepidium .
9) Las condiciones climáticas, interpretadas como un gradiente general de estrés, son predictores muy pobres del resultado de las interacciones entre pares de especies, ya que estas interacciones dependen de multitud de factores además del clima. Por tanto, ninguno de los modelos conceptuales dominantes en la actualidad predice una suficiente cantidad de estas interacciones como para ser aceptado de forma universal.
10) Las plantas nodriza aumentan la riqueza de especies y la diversidad filogenética a nivel local no sólo por la expansión de nicho, promovida por la mejora de las condiciones microclimáticas bajo su copa, sino también por un aumento de la segregación de nicho entre sus especies beneficiarias, derivado de una mayor heterogeneidad ambiental bajo su dosel.
11) La evolución del efecto positivo que las plantas nodriza ejercen sobre la riqueza local de especies a lo largo de gradientes ambientales depende de la naturaleza de dichos gradientes. Mientras que en España se mantuvo constante a lo largo de todo el gradiente estudiado (definido de forma opuesta por la aridez y las bajas temperaturas), este efecto aumentó con la aridez en Australia, donde la lluvia era el factor de estrés dominante en las comunidades estudiadas. En este último caso, se detectó un colapso del efecto positivo de las nodrizas bajo niveles extremos de aridez, como apuntan algunos modelos teóricos existentes.
12) Las condiciones climáticas y las interacciones bióticas interactúan a la hora de definir el patrón filogenético de las comunidades vegetales. Mientras que la facilitación aumentó la dispersión del patrón filogenético, condiciones climáticas “más benignas” (p. ej. más lluvia) incrementaron la agregación de este patrón mediante su efecto indirecto en la reducción de la diferenciación de nicho entre especies facilitadas y no facilitadas. El efecto conjunto de ambos factores generó un patrón filogenético aleatorio en la mayoría de comunidades estudiadas. Estos resultados advierten sobre la problemática derivada de inferir los mecanismos dominantes en el ensamblaje de una comunidad dada a partir únicamente de su patrón filogenético, aunque tengamos un conocimiento detallado del grado de conservación de importantes rasgos ecofisiológicos en las especies de esa comunidad a lo largo de la evolución.
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237 COAUTORES
AFILIACIÓN DE LOS COAUTORES
Fernando T. Maestre Gil Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain. E mail: [email protected]
Adrián Escudero Alcántara Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain. E mail: [email protected]
Fernando Valladares Ros Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, C.S.I.C., Serrano 115, E 28006 Madrid, Spain. E mail: [email protected]
Pablo García Palacios 1) Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain. 2) Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, C.S.I.C., Serrano 115, E 28006 Madrid, Spain. E mail: [email protected]
Andrea P. Castillo Monroy Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain. E mail: [email protected]
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Lucia DeSoto Suárez Centro de Ecogía Funcional, Departamento de Ciencias da Vida. Universidade de Coimbra 3001 – 455 Coimbra. Portugal. E mail: [email protected]
Jose Miguel Olano Área de Botánica, Departamento de Ciencias Agroforestales, E.U.I. Agrarias de Soria, Universidad de Valladolid, Campus de los Pajaritos, 42004 Soria, Spain. E mail: [email protected]
David Eldridge Department of Environment, Climate Change and Water, Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia. E mail: [email protected]
Matthew A. Bowker Colorado Plateau research Station, US Geological Survey, Flagstaff (USA). E mail: [email protected]
Matthew K. Tighe Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia. E mail: [email protected]
Rubén Torices Blanco Área de Botánica, Departamento de Ciencias Agroforestales, E.U.I. Agrarias de Soria, Universidad de Valladolid, Campus de los Pajaritos, 42004 Soria, Spain. E mail: [email protected]
239 COAUTORES
Diseño portada e imágenes: Joan Miquel Fuster Mollà y Santiago Soliveres Codina
Maquetación: Soraya Constán Nava y Santiago Soliveres Codina
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