Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics

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.
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Doi: 10.1111/1365-2656.12933

Resumen:

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

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The consecutive disparity index, D: a measure of temporal variability in ecological studies

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.
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Doi: 10.1002/ecs2.2527

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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.

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Shifting from a fertilization-dominated to a warming-dominated period

Peñuelas, J., Ciais, P., Canadell, J.G., Janssens, I.A., Fernández-Martínez, M., Carnicer, J., Obersteiner, M., Piao, S., Vautard, R., Sardans, J. (2017) Shifting from a fertilization-dominated to a warming-dominated period. Nature Ecology and Evolution. 1: 1438-1445.
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Doi: 10.1038/s41559-017-0274-8

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Impacts of global change on Mediterranean forests and their services

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.
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Doi: 10.3390/f8120463

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Evolutionary responses of invertebrates to global climate change: The role of life-history trade-offs and multidecadal climate shifts

Carnicer, J., Wheat, C., Vives, M., Ubach, A., Domingo, C., Nylin, S., Stefanescu, C., Vila, R., Wiklund, C., Peñuelas, J. (2016) Evolutionary responses of invertebrates to global climate change: The role of life-history trade-offs and multidecadal climate shifts. Global Climate Change and Terrestrial Invertebrates. : 319-348.
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Doi: 10.1002/9781119070894.ch16

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Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia

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., Rico, L., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino, M., Vives, M., Nadal-Sala, D., Sabaté, S., Gracia, C., Terradas, J. (2016) Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environmental and Experimental Botany. : 0-0.
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Doi: 10.1016/j.envexpbot.2017.05.012

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Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain

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.
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Doi: 10.1016/j.ppees.2016.01.001

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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.

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A regionally informed abundance index for supporting integrative analyses across butterfly monitoring schemes

Schmucki R., Pe'er G., Roy D.B., Stefanescu C., Van Swaay C.A.M., Oliver T.H., Kuussaari M., Van Strien A.J., Ries L., Settele J., Musche M., Carnicer J., Schweiger O., Brereton T.M., Harpke A., Heliölä J., Kühn E., Julliard R. (2016) A regionally informed abundance index for supporting integrative analyses across butterfly monitoring schemes. Journal of Applied Ecology. 53: 501-510.
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Doi: 10.1111/1365-2664.12561

Resumen:

The rapid expansion of systematic monitoring schemes necessitates robust methods to reliably assess species' status and trends. Insect monitoring poses a challenge where there are strong seasonal patterns, requiring repeated counts to reliably assess abundance. Butterfly monitoring schemes (BMSs) operate in an increasing number of countries with broadly the same methodology, yet they differ in their observation frequency and in the methods used to compute annual abundance indices. Using simulated and observed data, we performed an extensive comparison of two approaches used to derive abundance indices from count data collected via BMS, under a range of sampling frequencies. Linear interpolation is most commonly used to estimate abundance indices from seasonal count series. A second method, hereafter the regional generalized additive model (GAM), fits a GAM to repeated counts within sites across a climatic region. For the two methods, we estimated bias in abundance indices and the statistical power for detecting trends, given different proportions of missing counts. We also compared the accuracy of trend estimates using systematically degraded observed counts of the Gatekeeper Pyronia tithonus (Linnaeus 1767). The regional GAM method generally outperforms the linear interpolation method. When the proportion of missing counts increased beyond 50%, indices derived via the linear interpolation method showed substantially higher estimation error as well as clear biases, in comparison to the regional GAM method. The regional GAM method also showed higher power to detect trends when the proportion of missing counts was substantial. Synthesis and applications. Monitoring offers invaluable data to support conservation policy and management, but requires robust analysis approaches and guidance for new and expanding schemes. Based on our findings, we recommend the regional generalized additive model approach when conducting integrative analyses across schemes, or when analysing scheme data with reduced sampling efforts. This method enables existing schemes to be expanded or new schemes to be developed with reduced within-year sampling frequency, as well as affording options to adapt protocols to more efficiently assess species status and trends across large geographical scales. Monitoring offers invaluable data to support conservation policy and management, but requires robust analysis approaches and guidance for new and expanding schemes. Based on our findings, we recommend the regional generalized additive model approach when conducting integrative analyses across schemes, or when analysing scheme data with reduced sampling efforts. This method enables existing schemes to be expanded or new schemes to be developed with reduced within-year sampling frequency, as well as affording options to adapt protocols to more efficiently assess species status and trends across large geographical scales. Journal of Applied Ecology © 2016 British Ecological Society.

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Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestris forests: Relationships with climate, N deposition and tree growth

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.
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Doi: 10.1111/1365-2435.12541

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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.

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Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions

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.
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Doi: 10.1111/geb.12253

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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.

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