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., Vicca S., Janssens I.A., Carnicer J., Martín-Vide J., Peñuelas J. (2018) The consecutive disparity index, D: a measure of temporal variability in ecological studies. Ecosphere. 9: 0-0.EnlaceDoi: 10.1002/ecs2.2527
Temporal variability in ecological processes has attracted the attention of many disciplines in ecology, which has resulted in the development of several quantitative indices. The coefficient of variation (CV = standard deviation × mean−1) is still one of the most commonly used indices to assess temporal variability, despite being known to present several problems on its assessment (e.g., mean dependence or high sensitivity to rare events). The proportional variability (PV) index was developed to solve some of the CV's drawbacks, but, so far, no variability index takes into account the chronological order of the values in time series. In this paper, we introduce the consecutive disparity index (D), a temporal variability index that takes into account the chronological order of the values, assessing the average rate of change between consecutive values. We used computer simulations and empirical data for fruit production in trees, bird counts, and rodent captures to compare the behavior of D, PV, and CV under different scenarios. D was sensitive to changes in temporal autocorrelation in the negative autocorrelation range, and CV and PV were sensitive in the positive autocorrelation range despite not considering the chronological order of the values. The CV, however, was highly dependent on the mean of the time series, while D and PV were not. Our results demonstrate that, like PV, D solves many of the problems of the CV index while taking into account the chronological order of values in time series. The mathematical and statistical features of D make it a suitable index for analyzing temporal variability in a wide range of ecological studies. © 2018 The Authors.
Sardans J., Alonso R., Carnicer J., Fernández-Martínez M., Vivanco M.G., Peñuelas J. (2016) Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain. Perspectives in Plant Ecology, Evolution and Systematics. 18: 52-69.EnlaceDoi: 10.1016/j.ppees.2016.01.001
Concentrations of nutrient elements in organisms and in the abiotic environment are key factors influencing ecosystem structure and function. We studied how concentrations and stoichiometries of nitrogen (N), phosphorus (P) and potassium (K) in leaves of forest trees are related to phylogeny and to environmental factors (mean annual precipitation, mean annual temperature, forest type, and nitrogen deposition). Using data for 4691 forest plots from across Spain, we tested the following hypotheses: (i) that foliar stoichiometries of forest trees are strongly influenced by phylogeny, (ii) that climate, as an important driver of plant uptake and nutrient use efficiency, affects foliar stoichiometry, (iii) that long-term loads of N influence N, P and K concentrations and ratios in natural vegetation, and (iv) that sympatric species are differentiated according to their foliar stoichiometry, thereby reducing the intensity of resource competition. Our analyses revealed that several factors contributed to interspecific variation in elemental composition and stoichiometry. These included phylogeny, forest type, climate, N deposition, and competitive neighborhood relationships (probably related to niche segregation effect).These findings support the notion that foliar elemental composition reflects adaptation both to regional factors such as climate and to local factors such as competition with co-occurring species. © 2016 Elsevier GmbH.
Sardans J., Alonso R., Janssens I.A., Carnicer J., Vereseglou S., Rillig M.C., Fernández-Martínez M., Sanders T.G.M., Peñuelas J. (2015) Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestris forests: Relationships with climate, N deposition and tree growth. Functional Ecology. : 0-0.EnlaceDoi: 10.1111/1365-2435.12541
This study investigated the factors underlying the variability of needle and soil elemental composition and stoichiometry and their relationships with growth in Pinus sylvestris forests throughout the species' distribution in Europe by analysing data from 2245 forest stands. Needle N concentrations and N:P ratios were positively correlated with total atmospheric N deposition, whereas needle P concentrations were negatively correlated. These relationships were especially pronounced at sites where high levels of N deposition coincided with both higher mean annual temperature and higher mean annual precipitation. Trends towards foliar P deficiency were thus more marked when high N deposition coincided with climatic conditions favourable to plant production. Atmospheric N deposition was positively correlated with soil solution NO3- , SO42- , K+, P and Ca2+ concentrations, the soil solution NO3-:P ratio, total soil N and the total soil N:Olsen P ratio and was negatively correlated with soil Olsen P concentration. Despite these nutrient imbalances, during the period studied (1990-2006), N deposition was positively related with Pinus sylvestris absolute basal diameter (BD) growth, although only accounting for the 10% of the total variance. However, neither N deposition nor needle N concentration was related with relative annual BD growth. In contrast, needle P concentration was positively related with both absolute and relative annual BD growth. These results thus indicate a tendency of European P. sylvestris forests to store N in trees and soil in response to N deposition and unveil a trend towards increased nutrient losses in run-off as a consequence of higher soil solution N concentrations. Overall, the data show increasing ecosystem nutrient imbalances with increasingly limiting roles of P and other nutrients such as K in European P. sylvestris forests, especially in the centre of their distribution where higher levels of N deposition are observed. Thus, although the data show that N deposition has had an overall positive effect on P. sylvestris growth, the effect of continuous N deposition, associated with decreasing P and K and increasing N:P in leaves and in soil, may in the future become detrimental for the growth and competitive ability of P. sylvestris trees. © 2015 British Ecological Society.
Sardans J., Janssens I.A., Alonso R., Veresoglou S.D., Rillig M.C., Sanders T.G.M., Carnicer J., Filella I., Farre-Armengol G., Penuelas J. (2015) Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Global Ecology and Biogeography. 24: 240-255.EnlaceDoi: 10.1111/geb.12253
Aim: Plant elemental composition and stoichiometry are crucial for plant structure and function. We studied to what extent elemental stoichiometry in plants might be strongly related to environmental drivers and competition from coexisting species. Location: Europe. Methods: We analysed foliar N, P, K, Ca and Mg concentrations and their ratios among 50 species of European forest trees sampled in 5284 plots across Europe and their relationships with phylogeny, forest type, current climate and N deposition. Results: Phylogeny is strongly related to overall foliar elemental composition in European tree species. Species identity explained 56.7% of the overall foliar elemental composition and stoichiometry. Forest type and current climatic conditions also partially explained the differences in foliar elemental composition among species. In the same genus co-occurring species had overall higher differences in foliar elemental composition and stoichiometry than the non-co-occurring species. Main conclusions: The different foliar elemental compositions among species are related to phylogenetic distances, but they are also related to current climatic conditions, forest types, drivers of global change such as atmospheric N deposition, and to differences among co-occurring species as a probable consequence of niche specialization to reduce direct competition for the same resources. Different species have their own 'fixed' foliar elemental compositions but retain some degree of plasticity to the current climatic and competitive conditions. A wider set of elements beyond N and P better represent the biogeochemical niche and are highly sensitive to plant function. Foliar elemental composition can thus be useful for representing important aspects of plant species niches. © 2014 John Wiley & Sons Ltd.
Carnicer J., Coll M., Pons X., Ninyerola M., Vayreda J., Penuelas J. (2014) Large-scale recruitment limitation in Mediterranean pines: The role of Quercus ilex and forest successional advance as key regional drivers. Global Ecology and Biogeography. 23: 371-384.EnlaceDoi: 10.1111/geb.12111
Aim: Large-scale patterns of limitations in tree recruitment remain poorly described in the Mediterranean Basin, and this information is required to assess the impacts of global warming on forests. Here, we unveil the existence of opposite trends of recruitment limitation between the dominant genera Quercus and Pinus on a large scale and identify the key ecological drivers of these diverging trends. Location: Spain Methods: We gathered data from the Spanish National Forest inventory to assess recruitment trends for the dominant species (Pinus halepensis, Pinus pinea, Pinus pinaster, Pinus nigra, Pinus sylvestris, Pinus uncinata, Quercus suber, Quercus ilex, Quercus petraea, Quercus robur, Quercus faginea and Quercus pyrenaica). We assessed the direct and indirect drivers of recruitment by applying Bayesian structural equation modelling techniques. Results: Severe limitations in recruitment were observed across extensive areas for all Pinus species studied, with recruitment failure affecting 54-71% of the surveyed plots. In striking contrast, Quercus species expanded into 41% of the plots surveyed compared to only 10% for Pinus and had a lower local recruitment failure (29% of Quercus localities compared to 63% for Pinus species). Bayesian structural equation models highlighted the key role of the presence of Q.ilex saplings and the increase in the basal area of Q.ilex in limiting recruitment in five Pinus species. The recruitment of P.sylvestris and P.nigra showed the most negative trends and was negatively associated with the impacts of fire. Main conclusions: This study identified Q.ilex, the most widespread species in this area, as a key driver of recruitment shifts on a large scale, negatively affecting most pine species with the advance of forest succession. These results highlight that the future expansion/contraction of Q.ilex stands with ongoing climate change will be a key process indirectly controlling the demographic responses of Pinus species in the Mediterranean Basin. © 2013 John Wiley & Sons Ltd.
Carnicer J., Sardans J., Stefanescu C., Ubach A., Bartons M., Asensio D., Penuelas J. (2014) Global biodiversity, stoichiometry and ecosystem function responses to human-induced C-N-P imbalances. Journal of Plant Physiology. : 0-0.EnlaceDoi: 10.1016/j.jplph.2014.07.022
Global change analyses usually consider biodiversity as a global asset that needs to be preserved. Biodiversity is frequently analysed mainly as a response variable affected by diverse environmental drivers. However, recent studies highlight that gradients of biodiversity are associated with gradual changes in the distribution of key dominant functional groups characterized by distinctive traits and stoichiometry, which in turn often define the rates of ecosystem processes and nutrient cycling. Moreover, pervasive links have been reported between biodiversity, food web structure, ecosystem function and species stoichiometry. Here we review current global stoichiometric gradients and how future distributional shifts in key functional groups may in turn influence basic ecosystem functions (production, nutrient cycling, decomposition) and therefore could exert a feedback effect on stoichiometric gradients. The C-N-P stoichiometry of most primary producers (phytoplankton, algae, plants) has been linked to functional trait continua (i.e. to major axes of phenotypic variation observed in inter-specific analyses of multiple traits). In contrast, the C-N-P stoichiometry of higher-level consumers remains less precisely quantified in many taxonomic groups. We show that significant links are observed between trait continua across trophic levels. In spite of recent advances, the future reciprocal feedbacks between key functional groups, biodiversity and ecosystem functions remain largely uncertain. The reported evidence, however, highlights the key role of stoichiometric traits and suggests the need of a progressive shift towards an ecosystemic and stoichiometric perspective in global biodiversity analyses.
Carnicer J., Barbeta A., Sperlich D., Coll M., Penuelas J. (2013) Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale. Frontiers in Plant Science. 4: 0-0.EnlaceDoi: 10.3389/fpls.2013.00409
Recent large-scale studies of tree growth in the Iberian Peninsula reported contrasting positive and negative effects of temperature in Mediterranean angiosperms and conifers. Here we review the different hypotheses that may explain these trends and propose that the observed contrasting responses of tree growth to temperature in this region could be associated with a continuum of trait differences between angiosperms and conifers. Angiosperm and conifer trees differ in the effects of phenology in their productivity, in their growth allometry, and in their sensitivity to competition. Moreover, angiosperms and conifers significantly differ in hydraulic safety margins, sensitivity of stomatal conductance to vapor-pressure deficit (VPD), xylem recovery capacity or the rate of carbon transfer. These differences could be explained by key features of the xylem such as non-structural carbohydrate content (NSC), wood parenchymal fraction or wood capacitance. We suggest that the reviewed trait differences define two contrasting ecophysiological strategies that may determine qualitatively different growth responses to increased temperature and drought. Improved reciprocal common garden experiments along altitudinal or latitudinal gradients would be key to quantify the relative importance of the different hypotheses reviewed. Finally, we show that warming impacts in this area occur in an ecological context characterized by the advance of forest succession and increased dominance of angiosperm trees over extensive areas. In this context, we examined the empirical relationships between the responses of tree growth to temperature and hydraulic safety margins in angiosperm and coniferous trees. Our findings suggest a future scenario in Mediterranean forests characterized by contrasting demographic responses in conifer and angiosperm trees to both temperature and forest succession, with increased dominance of angiosperm trees, and particularly negative impacts in pines. © 2013 Carnicer, Barbeta, Sperlich, Coll and Peñuelas.
Carnicer J., Stefanescu C., Vila R., Dincǎ V., Font X., Peñuelas J. (2013) A unified framework for diversity gradients: The adaptive trait continuum. Global Ecology and Biogeography. 22: 6-18.EnlaceDoi: 10.1111/j.1466-8238.2012.00762.x
Aim Adaptive trait continua are axes of covariation observed in multivariate trait data for a given taxonomic group. These continua quantify and summarize life-history variation at the inter-specific level in multi-specific assemblages. Here we examine whether trait continua can provide a useful framework to link life-history variation with demographic and evolutionary processes in species richness gradients. Taking an altitudinal species richness gradient for Mediterranean butterflies as a study case, we examined a suite of traits (larval diet breadth, adult phenology, dispersal capacity and wing length) and species-specific habitat measures (temperature and aridity breadth). We tested whether traits and species-specific habitat measures tend to co-vary, whether they are phylogenetically conserved, and whether they are able to explain species distributions and spatial genetic variation in a large number of butterfly assemblages. Location Catalonia, Spain. Methods We formulated predictions associated with species richness gradients and adaptive trait continua. We applied principal components analyses (PCAs), structural equation modelling and phylogenetic generalized least squares models. Results We found that traits and species-specific habitat measures covaried along a main PCA axis, ranging from multivoltine trophic generalists with high dispersal capacity to univoltine (i.e. one generation per year), trophic specialist species with low dispersal capacity. This trait continuum was closely associated with the observed distributions along the altitudinal gradient and predicted inter-specific differences in patterns of spatial genetic variability (FST and genetic distances), population responses to the impacts of global change and local turnover dynamics. Main conclusions The adaptive trait continuum of Mediterranean butterflies provides an integrative and mechanistic framework to: (1) analyse geographical gradients in species richness, (2) explain inter-specific differences in population abundances, spatial distributions and demographic trends, (3) explain inter-specific differences in patterns of genetic variation (FST and genetic distances), and (4) study specialist-generalist life-history transitions frequently involved in butterfly diversification processes. © 2012 Blackwell Publishing Ltd.
Coll M., Penuelas J., Ninyerola M., Pons X., Carnicer J. (2013) Multivariate effect gradients driving forest demographic responses in the Iberian Peninsula. Forest Ecology and Management. 303: 195-209.EnlaceDoi: 10.1016/j.foreco.2013.04.010
A precise knowledge of forest demographic gradients in the Mediterranean area is essential to assess future impacts of climate change and extreme drought events. Here we studied the geographical patterns of forest demography variables (tree recruitment, growth and mortality) of the main species in Spain and assessed their multiple ecological drivers (climate, topography, soil, forest stand attributes and tree-specific traits) as well as the geographical variability of their effects and interactions. Quantile modeling analyses allowed a synthetic description of the gradients of multiple covariates influencing forest demography in this area. These multivariate effect gradients showed significantly stronger interactions at the extremes of the rainfall gradient. Remarkably, in all demographic variables, qualitatively different levels of effects and interactions were observed across tree-size classes. In addition, significant differences in demographic responses and effect gradients were also evident between the dominant genus Quercus and Pinus. Quercus species presented significantly higher percentage of plots colonized by new recruits, whereas in Pinus recruitment limitation was significantly higher. Contrasting positive and negative growth responses to temperature were also observed in Quercus and Pinus, respectively. Overall, our results synthesize forest demographic responses across climatic gradients in Spain, and unveil the interactions between driving factors operating in the drier and wetter edges. © 2013 Elsevier B.V.
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