Fire persistence mechanisms in Mediterranean plants: ecological and evolutionary consequences Bruno Ricardo Jesus Moreira Fire persistence mechanisms in Mediterranean plants: ecological and evolutionary consequences Memoria presentada por: Bruno Ricardo Jesus Moreira Para optar al grado de doctor en Ciencias Biológicas Departamento de Ecología, Universidad de Alicante Director de tesis: Dr. Juli G. Pausas Alicante, Diciembre de 2012. Acknowledgments Numerous people were involved and contributed in many ways to the completion of this thesis. Firstly I would like to thank to Juli, my scientific advisor. He is sincerely thanked for his good advices, the encouragement and help in this thesis. This thesis was definitively a starting point where first steps towards the realisation of my future career were taken. As I have written elsewhere, “I was supervised by an outstanding researcher which inculcated me independent thinking and encouraged to openly question his opinions and suggestions with scientific arguments (…) Although, under the careful supervision of my supervisor, I was expected to lead my research, define the project goals, methodologies and main milestones to achieve.” I am really glad and proud that all of this is true. Susana has been of utmost importance for my Ph.D. She has been my role model since from the beginning; a model for friendship, dedication, scientific rigour, suffering capacity and perseverance. I know I always could count on her and that I will always can. I would also like to thank the people at CEAM and CIDE for their company and support, especially to my office mates and all the students and research assistants that passed by and which help was invaluable. Particularly to the ones who had to work with me for endless hours in the field and/or laboratory. I am perfectly aware of the harsh conditions we went through. The list of people who deserve thanks based on their friendship gets long at this point, and it extends far back in time. To the “Portuguese friends”, obrigado for the crazy time and very good moments, to the “not Portuguese friends” thanks for making my stay abroad easier to support (although making it difficult to return) and for the multicultural teachings. I do not need to say names, you know who you are!! I would also like to thank my family for the support they provided me through my entire life and in particular, I must acknowledge my girlfriend and best friend, Sandra, without whose love, encouragement and editing assistance, I would not have finished this thesis. A minha sincera gratidão em especial também para os meus pais, irmão, tios e primos que me apoiaram de todas as formas possíveis. A melhor maneira que tenho de lhes agradecer é esta: concluir o doutoramento e voltar para Portugal. Espero que se possa ver ao longe. The work has been financed by projects from the Spanish Government PERSIST (CGL2006- 07126/BOS) and VIRRA (CGL2009-12048/BOS) and from Generalitat Valenciana RESERBROT (GVPRE/2008/360). I would also like to thank the authorities from the Parque Natural de la Serra Calderona, the Alzira City Council (Paraje Natural Municipal de la Murta y la Casella), the Parque Natural del Carrascal de la Font Roja and Fundación Caja Castellón-Bancaja (Barranc dels Horts, Ares del Maestrat) for permission to collect seeds and/or work in these areas. This thesis was supported by a “Bolsa de Investigação com a referência SFRH/BD/41343/ 2007, financiada pelo POPH - QREN - Tipologia 4.1 - Formação Avançada, comparticipado pelo Fundo Social Europeu e por fundos nacionais do MCTES”. I hope they will also support my posdoc. “Life is not easy for any of us. But what of that? We must have perseverance and above all confidence in ourselves. We must believe that we are gifted for something and that this thing must be attained.” Marie Curie Index Chapter 1 General Introduction …………………………………...... 11 Chapter 2 To resprout or not to resprout: factors driving intraspecific variability in resprouting …………………... 21 Chapter 3 Tanned or burned: The role of fire in shaping physical seed dormancy …………………………………………... 39 Chapter 4 Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora ………………………. 63 Chapter 5 Field evidence of smoke-stimulated seedling emergence and establishment in Mediterranean Basin flora ………… 83 Chapter 6 Combined effect of heat and smoke on the germination of Mediterranean Basin flora ……………………………….. 99 Chapter 7 Heat and smoke stimulated germination: two mechanisms for plant coexistence in fire-prone ecosystems ………….. 113 Chapter 8 Local versus regional intraspecific variability in regeneration traits ………………………………………... 129 Chapter 9 Fires enhance flammability in Ulex parviflorus ………… 145 Chapter 10 Flammability as a biological concept …………………… 159 Chapter 11 Discussion ……………………………………………….. 167 Chapter 12 Conclusions ……………………………………………… 175 Resumen …………………………………………………. 177 Chapter 1: General introduction 11 Chapter 1 General introduction Mediterranean ecosystems, including the Mediterranean Basin, have undergone a long history of fire (Pausas and Keeley 2009, Keeley et al. 2012). This recurrent pressure exerted by fire is a key factor in the evolution of plants and in the structure of plant communities. Many plant species have traits and mechanisms that allow them to persist and regenerate after fires. Thus, these traits have an adaptive value and are essential to understand the evolution and diversity of species in fire prone areas (Bond and van Wilgen 1996, Bond and Midgley 2001, Keeley et al. 2011, 2012). In Mediterranean shrublands and woodlands, which are typically composed of a relatively dense vegetation, fires are frequently crown fires; i.e., fire affects all the aboveground part of the vegetation (of the different strata; herbaceous, shrub and tree), including the canopies of the dominant growth forms. The intensity and, in general, the severity of these fires is high and much of the vegetation is greatly affected. The two main mechanisms that allow post-fire regeneration of plants, after these fires, are the ability to resprout (R) and the capacity of seedling recruitment (P) after fire. These two post-fire persistence mechanisms occur at two different hierarchical levels, at individual level and population level, respectively (Pausas and Lavorel 2003, Pausas et al. 2004) and allow the recovery of the ecosystem affected by fire. Individuals of a species persist after fire if they have the ability to resprout (R+). If individuals do not persist (R-), populations can persist if these have formed a seed bank with the capacity to withstand fire, allowing the recruitment of new individuals after fire (P+). These two post-fire regeneration mechanisms are not mutually exclusive, and thus species might be classified into four strategies: obligate resprouting species (R+P-), obligate seeding species (R-P+), facultative species (R+P+) and species without any post-fire regeneration mechanism (R-P-). Plant flammability is also an important mechanism for fire persistence. Flammability- enhancing traits are considered to favour individuals if the elevated flammability confers them fitness benefits. In seeder species, higher flammability could increase the recruitment opportunities for the offspring of the individual with enhanced flammability by increasing the chance of opening spaces and by producing the necessary cues for triggering germination from the seedbank (“kill thy neighbour” hypothesis; Bond and Midgley 1995). In addition, 12 Chapter 1: General introduction enhanced flammability (e.g., measured as enhanced fire spread rates) has also been suggested as a mechanism for fire protection in plants (Gagnon et al. 2010) and might be important, particularly for resprouting species. Despite the importance of these fire persistence mechanisms (post-fire resprouting and seedling recruitment and flammability), both for understanding species evolution and for predicting future ecosystem changes, the current level of knowledge still presents some gaps. Resprouting The ability to resprout after a fire, after the elimination of all aboveground biomass, characterizes the resprouting species and is important for persisting in fire-prone ecosystems. Resprouting consists of the production of new sprouts from protected buds (e.g., by the soil or by the plant bark). This mechanism confers persistence at individual level (and thus at population level) because part of the individual (at least the bellow ground part) resists fire and does not die. These species accumulate carbohydrate and nutrient reserves in the belowground organs (that are protected by the soil) and the presence of these reserves has been associated with the resprouting capacity (Bell et al. 1996, Canadell and López-Soria 1998, Bell and Ojeda 1999). Species have often been classified as resprouters (R+) or non resprouters (R-, e.g., Pausas et al. 2004, Vesk et al. 2004). However, there is evidence of a certain intraspecific variability in this mechanism (Paula et al. 2009). In addition, the information available on the factors driving the ability to resprout, the vigour of resprout, or the overall resprouting success is very low; such information is practically nonexistent for species that, although common, do not dominate the landscape. Seedling recruitment Post-fire seedling recruitment characterizes the seeder species and is also an important mechanism for persisting in fire-prone ecosystems. Seeder species have several traits that allow the success of this mechanism. Annual seed production