Bruno Moreira

Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora.

BACKGROUND AND AIMS The role of fire as a germination cue for Mediterranean Basin (MB) plants is still unclear. The current idea is that heat stimulates germination mainly in Cistaceae and Fabaceae and that smoke has a limited role as a post-fire germination cue, in comparison with other Mediterranean-type ecosystems (MTEs), suggesting that fire-stimulated germination is less relevant in the MB than in other MTEs. However, recent studies showed that the assembly of Mediterranean plant communities is strongly driven by post-fire germination, suggesting an important role for fire as a germination cue. We hypothesize that both heat and smoke have important effects on the different post-fire recruitment processes of MB species (e.g. level and rate of germination and initial seedling growth). METHODS To ascertain the role of heat and smoke in the post-fire germination response of MB woody plants, a germination experiment was performed with seven heat and two smoke treatments on 30 MB woody species from seven different families, including species with water-permeable seeds and species with water-impermeable seeds. KEY RESULTS Heat stimulated the germination (probability and rate) of 21 species and smoke in eight species, out of the 30 species studied. In addition, six species showed enhanced initial seedling growth after the smoke treatments. CONCLUSIONS The results suggest that both heat and smoke are important germination cues in a wide range of MB woody species and that fire-cued germination in woody plants of the MB may be as important as in other MTEs.

Fires enhance flammability in Ulex parviflorus

Wildfires have been occurring in terrestrial ecosystems since the early evolution of plants (Bowman et al., 2009; Pausas & Keeley, 2009; Bond & Scott, 2010) and have shaped many species and ecosystems worldwide (Keeley et al., 2011). Plant flammability is an important driver of fire in terrestrial ecosystems and thus has a fundamental role in ecosystem dynamics and species evolution (Belcher et al., 2010; Bond & Scott, 2010; He et al., 2011). Many traits enhance plant flammability (Cornelissen et al., 2003), including structural traits such as high surface area to volume ratio and retention of standing dead biomass (Papió & Trabaud, 1990, 1991; van Wilgen et al., 1990; Schwilk, 2003), and chemical traits, such as high cellulose : lignin ratio and high levels of volatile compounds and waxes (Philpot, 1970; Rundel, 1981; Dimitrakopoulos & Panov, 2001; Alessio et al., 2008). Indeed, it has been suggested that flammability-enhancing traits have evolved to maintain fire-prone ecosystems. This hypothesis was first proposed at the community level, where it was stated that ‘fire-dependent plant communities burn more readily than nonfire-dependent communities because natural selection has favoured development of characteristics that make them more flammable’ (Mutch, 1970). However, this hypothesis was criticized, mainly for being group selectionist and for lacking an explanation on how increased flammability of an individual would increase its fitness (Snyder, 1984; Christensen, 1985; Troumbis & Trabaud, 1989). Later, the hypothesis on the evolution of flammability was reformulated at the individual level within the framework of inclusive fitness theory (Bond & Midgley, 1995). It suggested that flammability-enhancing traits could be favoured in individuals if the elevated flammability resulted in increased mortality of neighbours, and thus opened up space for recruitment opportunities of the flammable individual offspring (‘kill thy neighbour’ hypothesis, Bond & Midgley, 1995; also called ‘born-to-burn’ hypothesis, Zedler, 1995). More recent modelling studies have suggested different genetic mechanisms for the evolution of flammability (Kerr et al., 1999; Schwilk & Kerr, 2002). Indeed, the correlation between post-fire regeneration strategy and flammability across different species provides some evidence for the ‘kill thy neighbour’ hypothesis (Keeley & Zedler, 1998; Schwilk & Ackerly, 2001; Cowan & Ackerly, 2010; Saura-Mas et al., 2010; He et al., 2011). However, rigorous field evidence on whether fire enhances plant flammability within populations of a particular species is lacking. If natural selection enhances flammability traits in fire-prone ecosystems through an increase in opportunities for post-fire recruitment (Bond & Midgley, 1995), the hypothesis should be better tested in obligate seeder species, that is, in species that lack resprouting ability and for whom post-fire regeneration relies only on germination from the seed bank (Bond & Van Wilgen, 1996; Pausas et al., 2004). This is because obligate seeders have shorter and nonoverlapping generations and higher population turnover than resprouters (Verdú et al., 2007), and thus should be more sensitive to fire regime changes. Previous experimental studies on plant flammability in fire-prone ecosystems have focused on differences between species and, in particular, between regeneration strategies (e.g. Cowan & Ackerly, 2010; Saura-Mas et al., 2010), but none has studied the intraspecific variability and its relation to fire regime. In this study, we predict that individuals of seeder species growing in populations subject to recurrent fires will be more flammable than individuals of the same species growing in populations that rarely burn. In addition, because of this directional selection and the different population dynamics in contrasted fire regimes, we also predict that seeder species living in different fire regimes should differ in the variance structure of flammabilityenhancing traits (Endler, 1986). We tested these predictions in Ulex parviflorus (Mediterranean gorse, Fabaceae), a shrub species of the Mediterranean Basin lacking the ability to resprout and whose germination is triggered by fire. We quantified, at the individual level, flammability-enhancing traits in populations with contrasted fire regimes.

Tanned or Burned: The Role of Fire in Shaping Physical Seed Dormancy

Plant species with physical seed dormancy are common in mediterranean fire-prone ecosystems. Because fire breaks seed dormancy and enhances the recruitment of many species, this trait might be considered adaptive in fire-prone environments. However, to what extent the temperature thresholds that break physical seed dormancy have been shaped by fire (i.e., for post-fire recruitment) or by summer temperatures in the bare soil (i.e., for recruitment in fire-independent gaps) remains unknown. Our hypothesis is that the temperature thresholds that break physical seed dormancy have been shaped by fire and thus we predict higher dormancy lost in response to fire than in response to summer temperatures. We tested this hypothesis in six woody species with physical seed dormancy occurring in fire-prone areas across the Mediterranean Basin. Seeds from different populations of each species were subject to heat treatments simulating fire (i.e., a single high temperature peak of 100°C, 120°C or 150°C for 5 minutes) and heat treatments simulating summer (i.e., temperature fluctuations; 30 daily cycles of 3 hours at 31°C, 4 hours at 43°C, 3 hours at 33°C and 14 hours at 18°C). Fire treatments broke dormancy and stimulated germination in all populations of all species. In contrast, summer treatments had no effect over the seed dormancy for most species and only enhanced the germination in Ulex parviflorus, although less than the fire treatments. Our results suggest that in Mediterranean species with physical dormancy, the temperature thresholds necessary to trigger seed germination are better explained as a response to fire than as a response to summer temperatures. The high level of dormancy release by the heat produced by fire might enforce most recruitment to be capitalized into a single post-fire pulse when the most favorable conditions occur. This supports the important role of fire in shaping seed traits.

Local versus regional intraspecific variability in regeneration traits

Intraspecific trait variability has a fundamental contribution to the overall trait variability. However, little is known concerning the relative role of local (e.g. disturbances and species interaction) and regional (biogeographical) processes in generating this intraspecific trait variability. While biogeographical processes enhance plant trait variability between distant populations, in fire-prone ecosystems, recurrent fires may have a preponderant role in generating variability at a local scale. We hypothesize that plants respond to the local spatio-temporal heterogeneity generated by fire by having a relatively large local variability in regeneration traits in such a way that overrides the variability at a broader biogeographical scale. We test this hypothesis by assessing the intraspecific variability in fire-related regeneration traits of two species (Cistus salviifolius and Lavandula stoechas) growing in fire-prone ecosystems of the Mediterranean Basin. For each species, we selected six populations in two distant regions, three in the east (Anatolian Peninsula) and three in the west (Iberian Peninsula). For each species and population, we analysed the following regeneration traits: seed size, seed dormancy and stimulated germination by fire-related cues (heat and smoke). To evaluate the distribution of the variability in these traits, we decomposed the variability of trait values at each level, between regions (regional) and between population within region (local), using linear mixed-effect models. Despite the biogeographical and climatic differences between regions, for the two species, intraspecific variability in regeneration traits was higher at a local (within regions) than at a regional scale (between regions). Our results suggest that, in Mediterranean ecosystems, fire is an important source of intraspecific variability in regeneration traits. This supports the prominent role of fire as an ecological and evolutionary process, producing trait variability and shaping biodiversity in fire-prone ecosystems.

Flammability as a biological concept

Studies examining plant flammability descriptors as fire-adaptive traits (e.g., Schwilk, 2003; Scarff & Westoby, 2006; Cowan & Ackerly, 2010; Saura-Mas et al., 2010; Pausas et al., 2012) are normally formulated within the framework of inclusive fitness theory. In such framework, flammabilityenhancing traits are considered to favour individuals if the elevated flammability confers fitness benefits. In post-fire seeder species (i.e., those with fire-stimulated germination from a persistent seed bank), 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 & Midgley, 1995). This might be specially relevant in non-resprouting (obligate) seeders with strong spatial population structure (e.g., with short-distance dispersal). Because there is some evidence of heritability for both seed dormancy (e.g., Baskin et al., 2000; Huang et al., 2010) and flammability-enhancing traits (e.g. Sampedro et al., 2010), we would expect a selection for higher flammability with repeated fires.

Genetic component of flammability variation in a Mediterranean shrub

Recurrent fires impose a strong selection pressure in many ecosystems worldwide. In such ecosystems, plant flammability is of paramount importance because it enhances population persistence, particularly in non‐resprouting species. Indeed, there is evidence of phenotypic divergence of flammability under different fire regimes. Our general hypothesis is that flammability‐enhancing traits are adaptive; here, we test whether they have a genetic component. To test this hypothesis, we used the postfire obligate seeder Ulex parviflorus from sites historically exposed to different fire recurrence. We associated molecular variation in potentially adaptive loci detected with a genomic scan (using AFLP markers) with individual phenotypic variability in flammability across fire regimes. We found that at least 42% of the phenotypic variation in flammability was explained by the genetic divergence in a subset of AFLP loci. In spite of generalized gene flow, the genetic variability was structured by differences in fire recurrence. Our results provide the first field evidence supporting that traits enhancing plant flammability have a genetic component and thus can be responding to natural selection driven by fire. These results highlight the importance of flammability as an adaptive trait in fire‐prone ecosystems.

Secondary compounds enhance flammability in a Mediterranean plant

Some plant secondary compounds, such as terpenes, are very flammable; however, their role in enhancing plant flammability is poorly understood and often neglected in reviews on plant chemical ecology. This is relevant as there is growing evidence that flammability-enhancing traits are adaptive in fire-prone ecosystems. We analyzed the content of monoterpenes and sesquiterpenes, performed flammability tests and genotyped microsatellite markers, all in the same individuals of Rosmarinus officinalis, to evaluate the link between the content of terpenes, flammability and the genetic similarity among individuals. The results suggest that terpenes enhance flammability in R. officinalis, and that variability in flammability among individuals is likely to have a genetic basis. Overall our results suggest that the capacity to produce and store terpenes can be considered a flammability-enhancing trait and could have an adaptive value in fire-prone ecosystems.

Nitrogen-fixing bacteria in Eucalyptus globulus plantations.

Eucalypt cultivation is an important economic activity worldwide. In Portugal, Eucalyptus globulus plantations account for one-third of the total forested area. The nutritional requirements of this crop have been well studied, and nitrogen (N) is one of the most important elements required for vegetal growth. N dynamics in soils are influenced by microorganisms, such as diazotrophic bacteria (DB) that are responsible for biological nitrogen fixation (BNF), so the aim of this study was to evaluate and identity the main groups of DB in E. globulus plantations. Samples of soil and root systems were collected in winter and summer from three different Portuguese regions (Penafiel, Gavião and Odemira). We observed that DB communities were affected by season, N fertilization and moisture. Furthermore Bradyrhizobium and Burkholderia were the most prevalent genera in these three regions. This is the first study describing the dynamic of these bacteria in E. globulus plantations, and these data will likely contribute to a better understanding of the nutritional requirements of eucalypt cultivation and associated organic matter turnover.

Preschoolers and the Endowment Effect

We show that preschoolers exhibit the endowment effect as evidenced by experiments where children generally chose to keep their own toys rather than trading them for similar ones. Furthermore, we relate the emergence of this effect to childrens innate psychobiological traits—emotional state, gender, handedness, and digit ratio. The trials were conducted with 141 children across 6 kindergartens. We also found support that children, like adults, exhibit a preference for physical possession as opposed to ownership. As with adults, emotions also seem to matter, as children who were described as quiet and calm were more likely to present the endowment effect. Also of note, right-handed children described as quiet were more likely to exhibit the phenomenon. Furthermore, female children were generally found to be calmer than males, while males tended to be more fearful than females. This result was also previously found in teenagers.