Fire effects on pollination and plant reproduction: a quantitative review.

BACKGROUND AND AIMS: Fire may favour plant flowering by opening the vegetation and increasing abiotic resource availability. Increased floral display size can attract more pollinators and increase the absolute fruit and seed production immediately after the fire. However, anthropogenic increases in fire frequency may alter these responses. We aim to assess the effects of fire on pollination and reproductive success of plants at the global scale. METHODS: We performed a systematic literature review and meta-analyses to examine overall fire effects as well as different fire parameters on pollination and on plant reproduction. We also explored to what extent the responses vary among pollinators, pollination vectors, plant regeneration strategies, compatibility systems, vegetation types and biomes. KEY RESULTS: Most studies were conducted in fire-prone ecosystems. Overall, single fires increased pollination and plant reproduction but this effect was overridden by recurrent fires. Floral visitation rates of pollinators were enhanced immediately following a wildfire, and especially in bee-pollinated plants. Fire increased the absolute production of fruits or seeds but not the fruit or seed set. The reproductive benefits were mostly observed in wind-pollinated (graminoids), herbaceous and resprouter species. Finally, fire effects on pollination were positively correlated with fire effects on plant reproductive success. CONCLUSIONS: Fire has a central role in pollination and plant sexual reproduction in fire-prone ecosystems. The increase in the absolute production of fruits and seeds suggests that fire benefits on plant reproduction are likely driven by increased abiotic resources and the consequent floral display size. However, reproduction efficiency, as measured by fruit or seed set, does not increase with fire. In contrast, when assessed on the same plant simultaneously, fire effects on pollination are translated into reproduction. Increased fire frequency due to anthropogenic changes can alter the nature of the response to fire.

Reptile responses to fire across the western Mediterranean Basin.

Effects of anthropogenic activities, including climate change, are modifying fire regimes, and the dynamic nature of these modifications requires identification of general patterns of organisms' responses to fire. This is a challenging task because of the high complexity of factors involved (including climate, geography, land use, and species-specific ecology). We aimed to describe the responses of the reptile community to fire across a range of environmental and fire-history conditions in the western Mediterranean Basin. We sampled 8 sites that spanned 4 Mediterranean countries. We recorded 6064 reptile sightings of 36 species in 1620 transects and modeled 3 community metrics (total number of individuals, species richness, and Shannon diversity) as responses to environmental and fire-history variables. Reptile community composition was also analyzed. Habitat type (natural vs. afforestation), fire age class (time since the last fire), rainfall, and temperature were important factors in explaining these metrics. The total number of individuals varied according to fire age class, reaching a peak at 15-40 years after the last fire. Species richness and Shannon diversity were more stable during postfire years. The 3 community metrics were higher under postfire conditions than in unburned forest plots. This pattern was particularly prevalent in afforested plots, indicating that the negative effect of fire on reptiles was lower than the negative effect of afforestation. Community composition varied by fire age class, indicating the existence of early- and late-successional species (xeric and saxicolous vs. mesic reptiles, respectively). Species richness was 46% higher in areas with a single fire age class relative to those with a mixture of fire age classes, which indicates pyrodiverse landscapes promoted reptile diversity. An expected shift to more frequent fires will bias fire age distribution toward a predominance of early stages, and this will be harmful to reptile communities.

Respuestas de reptiles al fuego en la Cuenca Mediterránea occidental Resumen Los efectos de actividades antropogénicas, incluyendo el cambio climático, están modificando los regímenes de fuego, y la naturaleza dinámica de estas modificaciones requiere la identificación de patrones generales de las respuestas de los organismos al fuego. Esta es una tarea desafiante debido a la gran complejidad de los factores involucrados (incluyendo clima, geografía, uso de suelo y la ecología de cada especie). Nuestro objetivo fue describir las respuestas de la comunidad de reptiles al fuego bajo diversas condiciones ambientales e historias de fuego en la Cuenca Mediterránea occidental. Muestreamos ocho sitios en cuatro países mediterráneos. Registramos 6064 avistamientos de reptiles de 36 especies en 1620 transectos y modelamos tres métricas comunitarias (número total de individuos, riqueza de especies y diversidad de Shannon) como respuestas a las variables ambientales y de historia de fuego. También analizamos la composición de la comunidad de reptiles. El tipo de hábitat (natural versus forestación), la clase de edad del fuego (tiempo transcurrido desde el último incendio), la precipitación pluvial y la temperatura fueron factores importantes en la explicación de estas métricas. El número total de individuos varió de acuerdo con la clase de edad del fuego, alcanzando un pico a los 15­40 años después del último incendio. La riqueza de especies y la diversidad de Shannon fueron más estables durante los años posteriores a incendios. Las tres métricas de la comunidad fueron más altas bajo condiciones post incendio que en las parcelas sin historial de fuego. Este patrón fue particularmente prevalente en parcelas forestadas, lo cual indica que el efecto negativo del fuego sobre los reptiles fue menor que el efecto negativo de la forestación. La composición de la comunidad varió por clase de edad del fuego, indicando la existencia de especies sucesionales tempranas y tardías (reptiles xéricos y saxícolas, respectivamente). La riqueza de especie fue 46% mas alta en áreas con una sola clase de edad del fuego que en aquellas con una mezcla de clases de edad del fuego, lo cual indica que los paisajes pirodiversos promovieron la diversidad de reptiles. Un cambio esperado hacia incendios más frecuentes sesgará la distribución de la edad del fuego hacia una predominancia de etapas tempranas, y esto será perjudicial para las comunidades de reptiles.

Quantitative genetic analysis of floral traits shows current limits but potential evolution in the wild.

The vast variation in floral traits across angiosperms is often interpreted as the result of adaptation to pollinators. However, studies in wild populations often find no evidence of pollinator-mediated selection on flowers. Evolutionary theory predicts this could be the outcome of periods of stasis under stable conditions, followed by shorter periods of pollinator change that provide selection for innovative phenotypes. We asked if periods of stasis are caused by stabilizing selection, absence of other forms of selection or by low trait ability to respond even if selection is present. We studied a plant predominantly pollinated by one bee species across its range. We measured heritability and evolvability of traits, using genome-wide relatedness in a large wild population, and combined this with estimates of selection on the same individuals. We found evidence for both stabilizing selection and low trait heritability as potential explanations for stasis in flowers. The area of the standard petal is under stabilizing selection, but the variability is not heritable. A separate trait, floral weight, presents high heritability, but is not currently under selection. We show how a simple pollination environment coincides with the absence of current prerequisites for adaptive evolutionary change, while heritable variation remains to respond to future selection pressures.

Evolutionary fire ecology: An historical account and future directions.

The idea that fire acts as an evolutionary force contributing to shaping species traits started a century ago, but had not been widely recognized until very recently. Among the first to realize this force were Edward B. Poulton, R. Dale Guthrie, and Edwin V. Komarek in animals and Willis L. Jepson, Walter W. Hough, Tom M. Harris, Philip V. Wells, and Robert W. Mutch in plants. They were all ahead of their time in their evolutionary thinking. Since then, evolutionary fire ecology has percolated very slowly into the mainstream ecology and evolutionary biology; in fact, this topic is still seldom mentioned in textbooks of ecology or evolution. Currently, there is plenty of evidence suggesting that we cannot understand the biodiversity of our planet without considering the key evolutionary role of fire. But there is still research to be done in order to fully understand fire's contribution to species evolution and to predicting species responses to rapid global changes.

Development and characterization of microsatellite loci in Ulex parviflorus Pourr. And its cross-transferability to other Genisteae.

BACKGROUND: The genus Ulex is composed by 15 species distributed in Europe and Africa, but the majority of them are restricted to the Iberian Peninsula and Northwest Africa. Some of these species are common elements at the landscape level, and others contribute to global biodiversity as narrow endemics. Assayed nuclear and plastid Sanger-sequenced regions do not provide enough resolution to perform evolutionary studies on the genus, neither at the intraspecific population level nor at the interspecific phylogenetic level. Thus, we have developed and characterized a set of nuclear microsatellite loci in U. parviflorus to provide new highly polymorphic molecular markers for the genus Ulex. METHODS AND RESULTS: Genomic DNA enriched in microsatellite motifs using streptavidin-coated M-280 magnetic beads attached to 5'-biotinylated oligonucleotides was sequenced in a 454GS Junior System. After primer design, fluorescent-dyed amplicons were analyzed through capillary sequencing (ABI3730XL). Here we present twelve new high polimorphic SSRs markers developed in U. parviflorus specimens and tested in 120 individuals. The 12 SSR loci amplified a total of 152 alleles, and detected expected heterozygosities that ranged from 0.674 to 0.725 in the genotyped populations. Successful cross-species transferability of the 12 SSR loci to the rest of species included in the genus Ulex and three other representative Genisteae was achieved. CONCLUSIONS: The 12 novel proposed SSRs loci will contribute to perform evolutionary studies and genetic research on the genus Ulex and in other Genisteae.

Fire and summer temperatures interact to shape seed dormancy thresholds.

BACKGROUND AND AIMS: In Mediterranean ecosystems, the heat shock of wildfire disrupts physical seed dormancy in many plant species. This triggers germination in the post-fire environment where seedling establishment is optimal due to decreased competition and increased resource availability. However, to maintain the soil seed bank until a fire occurs, the minimum heat capable of breaking seed dormancy (i.e. the lower heat threshold) must be above the maximum temperatures typically observed in the soil during the summer. We therefore hypothesized that summer temperatures have shaped heat requirements for physical dormancy release. Specifically, we predicted that seeds from populations growing under warmer summers will have higher values of the lower heat threshold. METHODS: To evaluate this prediction, we collected seeds from two Cistus species in 31 populations (20 Cistus albidus and 11 Cistus salviifolius) along a climate gradient of summer temperatures on the eastern coast of Spain. For each population, seeds were treated to 10 min heat shocks, from 30 to 120 °C in 5 °C increments (19 treatments), to simulate increasing heat doses from summer to fire-related temperatures. Seeds were then germinated in the lab. KEY RESULTS: For all populations, maximum germination was observed when applying temperatures associated with fire. Lower heat thresholds varied among populations, with a positive relationship between summer temperatures at seed population origin and the heat dose required to break dormancy. CONCLUSIONS: Our results suggest that fire drives maximum dormancy release for successful post-fire germination, while summer temperatures determine lower heat thresholds for ensuring inter-fire seed bank persistence. Significant among-population variation of thresholds also suggests that post-fire seeder species have some potential to modify their dormancy release requirements in response to changing climate.

Resilience of reptiles to megafires.

Extreme climate events, together with anthropogenic land-use changes, have led to the rise of megafires (i.e., fires at the top of the frequency size distribution) in many world regions. Megafires imply that the center of the burnt area is far from the unburnt; therefore, recolonization may be critical for species with low dispersal abilities such as reptiles. We aimed to evaluate the effect of megafires on a reptile community, exploring to what extent reptile responses are spatially shaped by the distance to the unburnt area. We examined the short-term spatiotemporal response of a Mediterranean reptile community after two megafires (>20,000 ha) that occurred in summer 2012 in eastern Spain. Reptiles were sampled over 4 years after the fire in burnt plots located at different distances from the fire perimeter (edge, middle, and center), and in adjacent unburnt plots. Reptile responses were modeled with fire history, as well as climate and remotely sensed environmental variables. In total, we recorded 522 reptiles from 12 species (11 species in the burnt plots and nine in the unburnt plots). Reptile abundance decreased in burnt compared with unburnt plots. The community composition and species richness did not vary either spatially (unburnt and burnt plots) or temporally (during the 4 years). The persistence of reptiles in the burnt area supported their resilience to megafires. The most common lizard species was Psammodromus algirus; both adults and juveniles were found in all unburnt and burnt plots. This species showed lower abundances in burnt areas compared with the unburnt and a slow short-term abundance recovery. The lizard Psammodromus edwarsianus was much less abundant and showed a tendency to increase its abundance in burnt plots compared with unburnt plots. Within the megafire area, P. algirus and P. edwarsianus abundances correlated with the thermal-moisture environment and vegetation recovery regardless of the distance from the fire edge. These results indicated the absence of a short-term reptile recolonization from the unburnt zone, demonstrating that reptiles are resilient (in situ persistence) to megafires when environmental conditions are favorable.

Fire reduces parasite load in a Mediterranean lizard.

Wildfires are a natural disturbance in many ecosystems. However, their effect on biotic interactions has been poorly studied. Fire consumes the vegetation and the litter layer where many parasites spend part of their life cycles. We hypothesize that wildfires reduce habitat availability for parasites with consequent potential benefits for hosts. We tested this for the lizard Psammodromus algirus and its ectoparasites in a Mediterranean ecosystem. We predicted that lizards in recently burned areas would have lower parasite load (cleaning effect) than those in unburned areas and that this phenomenon implies that lizards spending their entire lives in postfire conditions experience a lower level of parasitism than those living in unburned areas. We compared the ectoparasite load of lizards between eight paired burned/unburned sites, including recent (less than 1 year postfire) and older fires (2-4 years). We found that lizards' ectoparasites prevalence was drastically reduced in recently burned areas. Likewise, lizards in older burned areas showed less evidence of past parasitic infections. Fire disrupted the host-parasite interaction, providing the opportunity for lizards to avoid the negative effects of ectoparasites. Our results suggest that wildfires probably fulfil a role in controlling vector-borne diseases and pathogens, and highlight ecological effects of wildfires that have been overlooked.

Variation in plant belowground resource allocation across heterogeneous landscapes: implications for post-fire resprouting.

PREMISE: Resource availability affects biomass allocation in ways that could influence plant responses to disturbance such as fire. This is important because fire also varies across landscapes in ways that are correlated to resource availability. We hypothesized that plants growing in landscape microsites with a shortage of nutrients and water allocate more biomass and resources to belowground structures (and thus promote traits that enhance post-fire resprouting ability) than plants in more mesic sites. METHODS: We selected sites in three contrasting topographies (3 gullies, 3 midslopes, and 3 ridges) that supported different vegetation types and fire regimes, in Jalisco, Mexico. At each site, we measured soil nutrient and water content and light availability. Then we sampled biomass and root starch allocation in three post-fire resprouting shrubs that grow across a wide range of microenvironmental conditions. RESULTS: The ridges showed the highest values of solar radiation and the lowest of soil N and water content. Overall, we found a significant tendency for higher root-to-shoot (R/S) ratios, greater fine root biomass, and higher root starch content, in individuals growing in ridges or midslopes compared to the values of the plants living in gullies. CONCLUSIONS: Plants located in open canopy sites, characterized by a shortage of nutrients and water, tend to allocate more biomass belowground than plants in wet and fertile sites. Thus, plants in wet and fertile forests should be more vulnerable to increased disturbance such as wildfires.

Fire and legume germination in a tropical savanna: ecological and historical factors.

BACKGROUND AND AIMS: In many flammable ecosystems, physically dormant seeds show dormancy-break patterns tied to fire, but the link between heat shock and germination in the tropical savannas of Africa and South America remains controversial. Seed heat tolerance is important, preventing seed mortality during fire passage, and is usually predicted by seed traits. This study investigated the role of fire frequency (ecological effects) and seed traits through phylogenetic comparison (historical effects), in determining post-fire germination and seed mortality in legume species of the Cerrado, a tropical savanna-forest mosaic. METHODS: Seeds of 46 legume species were collected from three vegetation types (grassy savannas, woody savannas and forests) with different fire frequencies. Heat shock experiments (100 °C for 1 min; 100 °C for 3 min; 200 °C for 1 min) were then performed, followed by germination and seed viability tests. Principal component analysis, generalized linear mixed models and phylogenetic comparisons were used in data analyses. KEY RESULTS: Heat shocks had little effect on germination, but seed mortality was variable across treatments and species. Seed mortality was lowest under the 100 °C 1 min treatment, and significantly higher under 100 °C 3 min and 200 °C 1 min; larger seed mass decreased seed mortality, especially at 200 °C. Tree species in Detarioideae had the largest seeds and were unaffected by heat. Small-seeded species (mostly shrubs from grassy savannas) were relatively sensitive to the hottest treatment. Nevertheless, the presence of physical dormancy helped to avoid seed mortality in small-seeded species under the hottest treatment. CONCLUSIONS: Physical dormancy-break is not tied to fire in the Cerrado mosaic. Heat tolerance appears in both forest and savanna species and is predicted by seed traits (seed mass and physical dormancy), which might have helped forest lineages to colonize the savannas. The results show seed fire responses are better explained by historical than ecological factors in the Cerrado, contrasting with different fire-prone ecosystems throughout the world.

Unearthing belowground bud banks in fire-prone ecosystems.

Despite long-time awareness of the importance of the location of buds in plant biology, research on belowground bud banks has been scant. Terms such as lignotuber, xylopodium and sobole, all referring to belowground bud-bearing structures, are used inconsistently in the literature. Because soil efficiently insulates meristems from the heat of fire, concealing buds below ground provides fitness benefits in fire-prone ecosystems. Thus, in these ecosystems, there is a remarkable diversity of bud-bearing structures. There are at least six locations where belowground buds are stored: roots, root crown, rhizomes, woody burls, fleshy swellings and belowground caudexes. These support many morphologically distinct organs. Given their history and function, these organs may be divided into three groups: those that originated in the early history of plants and that currently are widespread (bud-bearing roots and root crowns); those that also originated early and have spread mainly among ferns and monocots (nonwoody rhizomes and a wide range of fleshy underground swellings); and those that originated later in history and are strictly tied to fire-prone ecosystems (woody rhizomes, lignotubers and xylopodia). Recognizing the diversity of belowground bud banks is the starting point for understanding the many evolutionary pathways available for responding to severe recurrent disturbances.

Differential pollinator response underlies plant reproductive resilience after fires.

Background and aims: Assessing the resilience of plant-animal interactions is critical to understanding how plant communities respond to habitat disturbances. Most ecosystems experience some level of natural disturbance (e.g. wildfires) to which many organisms are adapted. Wildfires have structured biotic communities for millennia; however, the effects of fire on interactions such as pollination have only recently received attention. A few studies have shown that generalist plants can buffer the impact of fires by pollinator replacement, suggesting that the resilience to disturbance could depend on the level of specialization of the interactions. Here, we hypothesize that (1) fires could impose negative effects on plants with specialized pollination systems, and (2) in large wildfires, these negative effects will be stronger with increasing distance inside the burnt area because pollinators will need more time to recolonize. Methods: These questions were tested in the specialized pollination system of a widespread Mediterranean palm, Chamaerops humilis. The post-fire pollination resilience was assessed in replicated wildfires representing three post-fire ages by measuring the abundance of beetle pollinators and by estimating fruit set (i.e. the proportion of flowers setting fruits) in burnt and unburnt areas. To test for distance effects, plants were sampled along transects inside the burnt area. Key Results: Despite a marked post-fire decline in the specialist pollinator, exacerbated by the distance from the fire's edge, the palm's fruit set was barely affected. The temporary replacement by a sap beetle at burnt sites - an effective pollinator that had not been previously recognized - provided post-fire reproductive resilience. Conclusions: Differential pollinator responses to disturbance can ensure plant success even in plants with only two functionally similar pollinators. This highlights the importance of pollinator replacement and dynamics for the resilience of interactions and ultimately of plant reproduction in disturbance-prone ecosystems.

Increased fire frequency promotes stronger spatial genetic structure and natural selection at regional and local scales in Pinus halepensis Mill.

Background and Aims: The recurrence of wildfires is predicted to increase due to global climate change, resulting in severe impacts on biodiversity and ecosystem functioning. Recurrent fires can drive plant adaptation and reduce genetic diversity; however, the underlying population genetic processes have not been studied in detail. In this study, the neutral and adaptive evolutionary effects of contrasting fire regimes were examined in the keystone tree species Pinus halepensis Mill. (Aleppo pine), a fire-adapted conifer. The genetic diversity, demographic history and spatial genetic structure were assessed at local (within-population) and regional scales for populations exposed to different crown fire frequencies. Methods: Eight natural P. halepensis stands were sampled in the east of the Iberian Peninsula, five of them in a region exposed to frequent crown fires (HiFi) and three of them in an adjacent region with a low frequency of crown fires (LoFi). Samples were genotyped at nine neutral simple sequence repeats (SSRs) and at 251 single nucleotide polymorphisms (SNPs) from coding regions, some of them potentially important for fire adaptation. Key Results: Fire regime had no effects on genetic diversity or demographic history. Three high-differentiation outlier SNPs were identified between HiFi and LoFi stands, suggesting fire-related selection at the regional scale. At the local scale, fine-scale spatial genetic structure (SGS) was overall weak as expected for a wind-pollinated and wind-dispersed tree species. HiFi stands displayed a stronger SGS than LoFi stands at SNPs, which probably reflected the simultaneous post-fire recruitment of co-dispersed related seeds. SNPs with exceptionally strong SGS, a proxy for microenvironmental selection, were only reliably identified under the HiFi regime. Conclusions: An increasing fire frequency as predicted due to global change can promote increased SGS with stronger family structures and alter natural selection in P. halepensis and in plants with similar life history traits.

Disturbance maintains alternative biome states.

Understanding the mechanisms controlling the distribution of biomes remains a challenge. Although tropical biome distribution has traditionally been explained by climate and soil, contrasting vegetation types often occur as mosaics with sharp boundaries under very similar environmental conditions. While evidence suggests that these biomes are alternative states, empirical broad-scale support to this hypothesis is still lacking. Using community-level field data and a novel resource-niche overlap approach, we show that, for a wide range of environmental conditions, fire feedbacks maintain savannas and forests as alternative biome states in both the Neotropics and the Afrotropics. In addition, wooded grasslands and savannas occurred as alternative grassy states in the Afrotropics, depending on the relative importance of fire and herbivory feedbacks. These results are consistent with landscape scale evidence and suggest that disturbance is a general factor driving and maintaining alternative biome states and vegetation mosaics in the tropics.

Towards understanding resprouting at the global scale.

Understanding and predicting plant response to disturbance is of paramount importance in our changing world. Resprouting ability is often considered a simple qualitative trait and used in many ecological studies. Our aim is to show some of the complexities of resprouting while highlighting cautions that need be taken in using resprouting ability to predict vegetation responses across disturbance types and biomes. There are marked differences in resprouting depending on the disturbance type, and fire is often the most severe disturbance because it includes both defoliation and lethal temperatures. In the Mediterranean biome, there are differences in functional strategies to cope with water deficit between resprouters (dehydration avoiders) and nonresprouters (dehydration tolerators); however, there is little research to unambiguously extrapolate these results to other biomes. Furthermore, predictions of vegetation responses to changes in disturbance regimes require consideration not only of resprouting, but also other relevant traits (e.g. seeding, bark thickness) and the different correlations among traits observed in different biomes; models lacking these details would behave poorly at the global scale. Overall, the lessons learned from a given disturbance regime and biome (e.g. crown-fire Mediterranean ecosystems) can guide research in other ecosystems but should not be extrapolated at the global scale.

Evolutionary ecology of resprouting and seeding in fire-prone ecosystems.

There are two broad mechanisms by which plant populations persist under recurrent disturbances: resprouting from surviving tissues, and seedling recruitment. Species can have one of these mechanisms or both. However, a coherent framework explaining the differential evolutionary pressures driving these regeneration mechanisms is lacking. We propose a bottom-up approach in addressing this question that considers the relative survivorship of adults and juveniles in an evolutionary context, based on two assumptions. First, resprouting and seeding can be interpreted by analogy with annual versus perennial life histories; that is, if we consider disturbance cycles to be analogous to annual cycles, then resprouting species are analogous to the perennial life history with iteroparous reproduction, and obligate seeding species that survive disturbances solely through seed banks are analogous to the annual life history with semelparous reproduction. Secondly, changes in the selective regimes differentially modify the survival rates of adults and juveniles and thus the relative costs and benefits of resprouting versus seeding. Our approach provides a framework for understanding temporal and spatial variation in resprouting and seeding under crown-fire regimes. It accounts for patterns of coexistence and environmental changes that contribute to the evolution of seeding from resprouting ancestors.