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.LinkDoi: 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.LinkDoi: 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.LinkDoi: 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.LinkDoi: 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.LinkDoi: 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.
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.LinkDoi: 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.
Gargallo-Garriga A., Sardans J., Pérez-Trujillo M., Guenther A., Llusià J., Rico L., Terradas J., Farré-Armengol G., Filella I., Parella T., Peñuelas J. (2016) Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota. BMC Plant Biology. 16: 0-0.LinkDoi: 10.1186/s12870-016-0767-7
Background: The phyllospheric microbiota is assumed to play a key role in the metabolism of host plants. Its role in determining the epiphytic and internal plant metabolome, however, remains to be investigated. We analyzed the Liquid Chromatography-Mass Spectrometry (LC-MS) profiles of the epiphytic and internal metabolomes of the leaves and flowers of Sambucus nigra with and without external antibiotic treatment application. Results: The epiphytic metabolism showed a degree of complexity similar to that of the plant organs. The suppression of microbial communities by topical applications of antibiotics had a greater impact on the epiphytic metabolome than on the internal metabolomes of the plant organs, although even the latter changed significantly both in leaves and flowers. The application of antibiotics decreased the concentration of lactate in both epiphytic and organ metabolomes, and the concentrations of citraconic acid, acetyl-CoA, isoleucine, and several secondary compounds such as terpenes and phenols in the epiphytic extracts. The metabolite pyrogallol appeared in the floral epiphytic community only after the treatment. The concentrations of the amino acid precursors of the ketoglutarate-synthesis pathway tended to decrease in the leaves and to increase in the foliar epiphytic extracts. Conclusions: These results suggest that anaerobic and/or facultative anaerobic bacteria were present in high numbers in the phyllosphere and in the apoplasts of S. nigra. The results also show that microbial communities play a significant role in the metabolomes of plant organs and could have more complex and frequent mutualistic, saprophytic, and/or parasitic relationships with internal plant metabolism than currently assumed. © 2016 Gargallo-Garriga et al.
Liu D., Llusia J., Ogaya R., Estiarte M., Llorens L., Yang X., Peñuelas J. (2016) Physiological adjustments of a Mediterranean shrub to long-term experimental warming and drought treatments. Plant Science. 252: 53-61.LinkDoi: 10.1016/j.plantsci.2016.07.004
Warmer temperatures and extended drought in the Mediterranean Basin are becoming increasingly important in determining plant physiological processes and affecting the regional carbon budget. The responses of plant physiological variables such as shoot water potential (Ψ), carbon-assimilation rates (A), stomatal conductance (gs) and intrinsic water-use efficiency (iWUE) to these climatic regimes, however, are not well understood. We conducted long-term (16 years) field experiments with mild nocturnal warming (+0.6 °C) and drought (−20% soil moisture) in a Mediterranean early-successional shrubland. Warming treatment moderately influenced Ψ, A and gs throughout the sampling periods, whereas drought treatment strongly influenced these variables, especially during the summer. The combination of a natural drought in summer 2003 and the treatments significantly decreased A and iWUE. Foliar δ13C increased in the treatments relative to control, but not significantly. The values of Ψ, A and gs were correlated negatively with vapor-pressure deficit (VPD) and positively with soil moisture and tended to be more dependent on the availability of soil water. The plant, however, also improved the acclimation to drier and hotter conditions by physiological adjustments (gs and iWUE). Understanding these physiological processes in Mediterranean shrubs is crucial for assessing further climate change impacts on ecosystemic functions and services. © 2016 Elsevier Ireland Ltd
Achotegui-Castells A., Danti R., Llusia J., Rocca G.D., Barberini S., Penuelas J. (2015) Strong Induction of Minor Terpenes in Italian Cypress, Cupressus sempervirens, in Response to Infection by the Fungus Seiridium cardinale. Journal of Chemical Ecology. : 0-0.LinkDoi: 10.1007/s10886-015-0554-1
Seiridium cardinale, the main fungal pathogen responsible for cypress bark canker, is the largest threat to cypresses worldwide. The terpene response of canker-resistant clones of Italian cypress, Cupressus sempervirens, to two differently aggressive isolates of S. cardinale was studied. Phloem terpene concentrations, foliar terpene concentrations, as well as foliar terpene emission rates were analyzed 1, 10, 30, and 90 days after artificial inoculation with fungal isolates. The phloem surrounding the inoculation point exhibited de novo production of four oxygenated monoterpenes and two unidentified terpenes. The concentrations of several constitutive mono- and diterpenes increased strongly (especially α-thujene, sabinene, terpinolene, terpinen-4-ol, oxygenated monoterpenes, manool, and two unidentified diterpenes) as the infection progressed. The proportion of minor terpenes in the infected cypresses increased markedly from the first day after inoculation (from 10 % in the control to 30–50 % in the infected treatments). Foliar concentrations showed no clear trend, but emission rates peaked at day 10 in infected trees, with higher δ-3-carene (15-fold) and total monoterpene (10-fold) emissions than the control. No substantial differences were found among cypresses infected by the two fungal isolates. These results suggest that cypresses activate several direct and indirect chemical defense mechanisms after infection by S. cardinale. © 2015 Springer Science+Business Media New York
Bernal M., Verdaguer D., Badosa J., Abadia A., Llusia J., Penuelas J., Nunez-Olivera E., Llorens L. (2015) Effects of enhanced UV radiation and water availability on performance, biomass production and photoprotective mechanisms of Laurus nobilis seedlings. Environmental and Experimental Botany. 109: 264-275.LinkDoi: 10.1016/j.envexpbot.2014.06.016
Climate models predict an increase in ultraviolet (UV) radiation and a reduction in precipitation in the Mediterranean region in the coming decades. High levels of UV radiation and water shortage can both cause photo-oxidative stress in plants. The aim of this study was to investigate the effects of enhanced UV radiation and its interaction with low water availability on seedling performance, biomass production, and photoprotective mechanisms of the sclerophyllous evergreen species Laurus nobilis L. (laurel). To achieve this goal, one-year-old seedlings of L. nobilis were grown outdoors under three UV conditions (ambient UV, enhanced UV-A, and enhanced UV-A. +. UV-B) and under two watering regimes (watered to field capacity and reduced water supply). The results show that plants produced more biomass when exposed to above ambient levels of UV-A or UV-A. +. UV-B radiation, especially under low water availability. This was probably related to a UV-induced increase in leaf relative water content and in leaf water use efficiency under water shortage. Even though our results suggest that UV-A supplementation may play an important role in the stimulation of biomass production, plants grown under enhanced UV-A plots showed higher levels of energy dissipation as heat (measured as NPQ) and a higher de-epoxidation state of the violaxanthin cycle. This suggests a greater excess of light energy under UV-A supplementation, in accordance with the observed reduction in the foliar content of light-absorbing pigments in these plants. Strikingly, the addition of UV-B radiation mitigated these effects. In conclusion, UV enhancement might benefit water status and growth of L. nobilis seedlings, especially under low water availability. The results also indicate the activation of different plant response mechanisms to UV-A and UV-B radiation, which would interact to produce the overall plant response. © 2014 Elsevier B.V.
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