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.
Enlace
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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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.
Enlace
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.
Enlace
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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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.
Enlace
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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Global biodiversity, stoichiometry and ecosystem function responses to human-induced C-N-P imbalances

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.
Enlace
Doi: 10.1016/j.jplph.2014.07.022

Resumen:

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.

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A unified framework for diversity gradients: The adaptive trait continuum

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.
Enlace
Doi: 10.1111/j.1466-8238.2012.00762.x

Resumen:

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.

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Multi-generational long-distance migration of insects: Studying the painted lady butterfly in the Western Palaearctic

Stefanescu C., Páramo F., Åkesson S., Alarcón M., Ávila A., Brereton T., Carnicer J., Cassar L.F., Fox R., Heliölä J., Hill J.K., Hirneisen N., Kjellén N., Kühn E., Kuussaari M., Leskinen M., Liechti F., Musche M., Regan E.C., Reynolds D.R., Roy D.B., Ryrholm N., Schmaljohann H., Settele J., Thomas C.D., van Swaay C., Chapman J.W. (2013) Multi-generational long-distance migration of insects: Studying the painted lady butterfly in the Western Palaearctic. Ecography. 36: 474-486.
Enlace
Doi: 10.1111/j.1600-0587.2012.07738.x

Resumen:

Long-range, seasonal migration is a widespread phenomenon among insects, allowing them to track and exploit abundant but ephemeral resources over vast geographical areas. However, the basic patterns of how species shift across multiple locations and seasons are unknown in most cases, even though migrant species comprise an important component of the temperate-zone biota. The painted lady butterfly Vanessa cardui is such an example; a cosmopolitan continuously-brooded species which migrates each year between Africa and Europe, sometimes in enormous numbers. The migration of 2009 was one of the most impressive recorded, and thousands of observations were collected through citizen science programmes and systematic entomological surveys, such as high altitude insect-monitoring radar and ground-based butterfly monitoring schemes. Here we use V. cardui as a model species to better understand insect migration in the Western Palaearctic, and we capitalise on the complementary data sources available for this iconic butterfly. The migratory cycle in this species involves six generations, encompassing a latitudinal shift of thousands of kilometres (up to 60 degrees of latitude). The cycle comprises an annual poleward advance of the populations in spring followed by an equatorward return movement in autumn, with returning individuals potentially flying thousands of kilometres. We show that many long-distance migrants take advantage of favourable winds, moving downwind at high elevation (from some tens of metres from the ground to altitudes over 1000 m), pointing at strong similarities in the flight strategies used by V. cardui and other migrant Lepidoptera. Our results reveal the highly successful strategy that has evolved in these insects, and provide a useful framework for a better understanding of long-distance seasonal migration in the temperate regions worldwide. © 2012 The Authors. Journal compilation © 2012 Nordic Society Oikos.

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Biogeography of species richness gradients: Linking adaptive traits, demography and diversification

Carnicer J., Brotons L., Stefanescu C., Peñuelas J. (2012) Biogeography of species richness gradients: Linking adaptive traits, demography and diversification. Biological Reviews. 87: 457-479.
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Doi: 10.1111/j.1469-185X.2011.00210.x

Resumen:

Here we review how adaptive traits contribute to the emergence and maintenance of species richness gradients through their influence on demographic and diversification processes. We start by reviewing how demographic dynamics change along species richness gradients. Empirical studies show that geographical clines in population parameters and measures of demographic variability are frequent along latitudinal and altitudinal gradients. Demographic variability often increases at the extremes of regional species richness gradients and contributes to shape these gradients. Available studies suggest that adaptive traits significantly influence demographic dynamics, and set the limits of species distributions. Traits related to thermal tolerance, resource use, phenology and dispersal seem to play a significant role. For many traits affecting demography and/or diversification processes, complex mechanistic approaches linking genotype, phenotype and fitness are becoming progressively available. In several taxa, species can be distributed along adaptive trait continuums, i.e. a main axis accounting for the bulk of inter-specific variation in some correlated adaptive traits. It is shown that adaptive trait continuums can provide useful mechanistic frameworks to explain demographic dynamics and diversification in species richness gradients. Finally, we review the existence of sequences of adaptive traits in phylogenies, the interactions of adaptive traits and community context, the clinal variation of traits across geographical gradients, and the role of adaptive traits in determining the history of dispersal and diversification of clades. Overall, we show that the study of demographic and evolutionary mechanisms that shape species richness gradients clearly requires the explicit consideration of adaptive traits. To conclude, future research lines and trends in the field are briefly outlined. © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society.

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Llebot E. (ed). Impactes, vulnerabilitat i retroalimentacions climàtiques als ecosistemes terrestres catalans. Segon informe sobre el canvi climàtic a Catalunya.

Peñuelas J, Filella I, Estiarte M, Ogaya R, Llusià J, Sardans J, Jump A, Curiel J, Carnicer J, Rutishauser T, Rico L, Keenan T, Garbulsky M, Coll M, Diaz de Quijano M, Seco R, Rivas-Ubach A, Silva J, Boada M, Stefanescu C, Lloret F, Terradas J (2011) Llebot E. (ed). Impactes, vulnerabilitat i retroalimentacions climàtiques als ecosistemes terrestres catalans. Segon informe sobre el canvi climàtic a Catalunya. Institut d'Estudis Catalans i Generalitat de Catalunya. Barcelona, pp. 373-407.

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