Carnicer J., Stefanescu C., Vives-Ingla M., López C., Cortizas S., Wheat C., Vila R., Llusià J., Peñuelas J. (2019) Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics. Journal of Animal Ecology. : 0-0.EnlaceDoi: 10.1111/1365-2656.12933
Widespread population declines have been reported for diverse Mediterranean butterflies over the last three decades, and have been significantly associated with increased global change impacts. The specific landscape and climatic drivers of these declines remain uncertain for most declining species. Here, we analyse whether plastic phenotypic traits of a model butterfly species (Pieris napi) perform as reliable biomarkers of vulnerability to extreme temperature impacts in natural populations, showing contrasting trends in thermally exposed and thermally buffered populations. We also examine whether improved descriptions of thermal exposure of insect populations can be achieved by combining multiple information sources (i.e., integrating measurements of habitat thermal buffering, habitat thermal amplification, host plant transpiration, and experimental assessments of thermal death time (TDT), thermal avoidance behaviour (TAB) and thermally induced trait plasticity). These integrative analyses are conducted in two demographically declining and two non-declining populations of P. napi. The results show that plastic phenotypic traits (butterfly body mass and wing size) are reliable biomarkers of population vulnerability to extreme thermal conditions. Butterfly wing size is strongly reduced only in thermally exposed populations during summer drought periods. Laboratory rearing of these populations documented reduced wing size due to significant negative effects of increased temperatures affecting larval growth. We conclude that these thermal biomarkers are indicative of the population vulnerability to increasing global warming impacts, showing contrasting trends in thermally exposed and buffered populations. Thermal effects in host plant microsites significantly differ between populations, with stressful thermal conditions only effectively ameliorated in mid-elevation populations. In lowland populations, we observe a sixfold reduction in vegetation thermal buffering effects, and larval growth occurs in these populations at significantly higher temperatures. Lowland populations show reduced host plant quality (C/N ratio), reduced leaf transpiration rates and complete above-ground plant senescence during the peak of summer drought. Amplified host plant temperatures are observed in open microsites, reaching thermal thresholds that can affect larval survival. Overall, our results suggest that butterfly population vulnerability to long-term drought periods is associated with multiple co-occurring and interrelated ecological factors, including limited vegetation thermal buffering effects at lowland sites, significant drought impacts on host plant transpiration and amplified leaf surface temperature, as well as reduced leaf quality linked to the seasonal advance of plant phenology. Our results also identify multiannual summer droughts affecting larval growing periods as a key driver of the recently reported butterfly population declines in the Mediterranean biome. © 2018 The Authors. Journal of Animal Ecology © 2018 British Ecological Society
Fernández-Martínez M., Llusià J., Filella I., Niinemets Ü., Arneth A., Wright I.J., Loreto F., Peñuelas J. (2018) Nutrient-rich plants emit a less intense blend of volatile isoprenoids. New Phytologist. 220: 773-784.EnlaceDoi: 10.1111/nph.14889
The emission of isoprenoids (e.g. isoprene and monoterpenes) by plants plays an important defensive role against biotic and abiotic stresses. Little is known, however, about the functional traits linked to species-specific variability in the types and rates of isoprenoids emitted and about possible co-evolution of functional traits with isoprenoid emission type (isoprene emitter, monoterpene emitter or both). We combined data for isoprene and monoterpene emission rates per unit dry mass with key functional traits (foliar nitrogen (N) and phosphorus (P) concentrations, and leaf mass per area) and climate for 113 plant species, covering the boreal, wet temperate, Mediterranean and tropical biomes. Foliar N was positively correlated with isoprene emission, and foliar P was negatively correlated with both isoprene and monoterpene emission rate. Nonemitting plants generally had the highest nutrient concentrations, and those storing monoterpenes had the lowest concentrations. Our phylogenetic analyses found that the type of isoprenoid emission followed an adaptive, rather than a random model of evolution. Evolution of isoprenoids may be linked to nutrient availability. Foliar N and P are good predictors of the type of isoprenoid emission and the rate at which monoterpenes, and to a lesser extent isoprene, are emitted. © 2017 The Authors. New Phytologist © 2017 New Phytologist Trust
Mu Z., Llusià J., Liu D., Ogaya R., Asensio D., Zhang C., Peñuelas J. (2018) Seasonal and diurnal variations of plant isoprenoid emissions from two dominant species in Mediterranean shrubland and forest submitted to experimental drought. Atmospheric Environment. 191: 105-115.EnlaceDoi: 10.1016/j.atmosenv.2018.08.010
We tested the effect of increasing drought conditions in the Mediterranean Basin on isoprenoid emissions for the coming decades by analyzing their effect experimentally on the dominant Mediterranean species Erica multiflora in a Garraf shrubland and Quercus ilex in a Prades forest in Catalonia (Spain). Drought was simulated in Garraf using automatically sliding curtains to decrease the amount of soil moisture by 5% and in Prades by partial rainfall exclusion and runoff exclusion for a 25% decrease. We measured photosynthetic rates (A), stomatal conductance (gs) and rates of isoprenoid emission in the morning and at midday for four seasons and determined the relationship of emission rates with environmental conditions. Terpenes were emitted by both species, but only E. multiflora emitted isoprene. α-Pinene and limonene were the most abundant terpenes. Isoprenoid emissions increased with air temperature and generally decreased as the amount of soil moisture increased. The results of this study suggest that higher isoprenoid emissions can be expected in the warmer and drier conditions predicted for the coming decades in the Mediterranean region. © 2018
Preece C., Farré-Armengol G., Llusià J., Peñuelas J. (2018) Thirsty tree roots exude more carbon. Tree Physiology. 38: 690-695.EnlaceDoi: 10.1093/treephys/tpx163
Root exudation is an important input of carbon into soils and affects plant and soil communities, but little is known about the effect of climatic factors such as drought on exudation, and its ability to recover. We studied the impact of increasing drought on root exudation and its subsequent recovery in the Mediterranean tree species Quercus ilex L. in a greenhouse study by measuring the amount of total organic carbon in exudates. The amount of exudation per unit root area increased with drought duration and was 21% higher under the most extreme drought scenario compared with the non-droughted control. The amount of root exudation did not differ between the treatments following 6 weeks of re-watering, indicating a strong capacity for recovery in this species. We concluded that drought could affect the amount of root exudation, which could in turn have a large impact on microbial activity in the rhizosphere, and alter these microbial communities, at least in the short term. This tree species may be able to return to normal levels of root exudation after a drought event, but long-term exudate-mediated impacts on Mediterranean forest soils may be an unforeseen effect of drought. © The Author(s) 2018. Published by Oxford University Press. All rights reserved.
Farré-Armengol G., Filella I., Llusià J., Peñuelas J. (2017) β-Ocimene, a Key Floral and Foliar Volatile Involved in Multiple Interactions between Plants and Other Organisms. Molecules (Basel, Switzerland). 22: 0-0.EnlaceDoi: 10.3390/molecules22071148
β-Ocimene is a very common plant volatile released in important amounts from the leaves and flowers of many plant species. This acyclic monoterpene can play several biological functions in plants, by potentially affecting floral visitors and also by mediating defensive responses to herbivory. The ubiquity and high relative abundance of β-ocimene in the floral scents of species from most plant families and from different pollination syndromes (ranging from generalism to specialism) strongly suggest that this terpenoid may play an important role in the attraction of pollinators to flowers. We compiled abundant evidence from published studies that supports β-ocimene as a generalist attractant of a wide spectrum of pollinators. We found no studies testing behavioural responses of pollinators to β-ocimene, that could directly demonstrate or deny the function of β-ocimene in pollinator attraction; but several case studies support that the emissions of β-ocimene in flowers of different species follow marked temporal and spatial patterns of emission, which are typical from floral volatile organic compound (VOC) emissions that are involved in pollinator attraction. Furthermore, important β-ocimene emissions are induced from vegetative plant tissues after herbivory in many species, which have relevant functions in the establishment of tritrophic interactions. We thus conclude that β-ocimene is a key plant volatile with multiple relevant functions in plants, depending on the organ and the time of emission. Experimental behavioural studies on pure β-ocimene conducted with pollinating insects will be necessary to prove the assumptions made here.
Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino-Serrano, M., Vives-Ingla, M., Stocker, B.D., Balzarolo, M., Guerrieri, R., Peaucelle, M., Marañón-Jiménez, S., Bórnez-Mejías, K., Mu, Z., Descals, A., Castellanos, A., Terradas, J. (2017) Impacts of global change on Mediterranean forests and their services. Forests. 8: 0-0.EnlaceDoi: 10.3390/f8120463
Seco, R., Karl, T., Turnipseed, A., Greenberg, J., Guenther, A., Llusia, J., Peñuelas, J., Dicken, U., Rotenberg, E., Kim, S., Yakir, D. (2017) Springtime ecosystem-scale monoterpene fluxes from Mediterranean pine forests across a precipitation gradient. Agricultural and Forest Meteorology. 237-238: 150-159.EnlaceDoi: 10.1016/j.agrformet.2017.02.007
Zhang, C., Filella, I., Liu, D., Ogaya, R., Llusià, J., Asensio, D., Peñuelas, J. (2017) Photochemical Reflectance Index (PRI) for detecting responses of diurnal and seasonal photosynthetic activity to experimental drought and warming in a Mediterranean shrubland. Remote Sensing. 9: 0-0.EnlaceDoi: 10.3390/rs9111189
Achotegui-Castells A., Della Rocca G., Llusià J., Danti R., Barberini S., Bouneb M., Simoni S., Michelozzi M., Peñuelas J. (2016) Terpene arms race in the Seiridium cardinale - Cupressus sempervirens pathosystem. Scientific Reports. 6: 0-0.EnlaceDoi: 10.1038/srep18954
The canker-causing fungus Seiridium cardinale is the major threat to Cupressus sempervirens worldwide. We investigated the production of terpenes by canker-resistant and susceptible cypresses inoculated with S. cardinale, the effect of these terpenes on fungal growth, and the defensive biotransformation of the terpenes conducted by the fungus. All infected trees produced de novo terpenes and strongly induced terpenic responses, but the responses were stronger in the canker-resistant than the susceptible trees. In vitro tests for the inhibition of fungal growth indicated that the terpene concentrations of resistant trees were more inhibitory than those of susceptible trees. The highly induced and de novo terpenes exhibited substantial inhibition (more than a fungicide reference) and had a high concentration-dependent inhibition, whereas the most abundant terpenes had a low concentration-dependent inhibition. S. cardinale biotransformed three terpenes and was capable of detoxifying them even outside the fungal mycelium, in its immediate surrounding environment. Our results thus indicated that terpenes were key defences efficiently used by C. sempervirens, but also that S. cardinale is ready for the battle.
Farré-Armengol, G., Filella, I., Llusia, J., Peñuelas, J. (2016) Bidirectional Interaction between Phyllospheric Microbiotas and Plant Volatile Emissions. Trends in Plant Science. 21: 854-860.EnlaceDoi: 10.1016/j.tplants.2016.06.005
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