Evidence of current impact of climate change on life: A walk from genes to the biosphere

Penuelas J., Sardans J., Estiarte M., Ogaya R., Carnicer J., Coll M., Barbeta A., Rivas-Ubach A., Llusia J., Garbulsky M., Filella I., Jump A.S. (2013) Evidence of current impact of climate change on life: A walk from genes to the biosphere. Global Change Biology. 19: 2303-2338.
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Doi: 10.1111/gcb.12143

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We review the evidence of how organisms and populations are currently responding to climate change through phenotypic plasticity, genotypic evolution, changes in distribution and, in some cases, local extinction. Organisms alter their gene expression and metabolism to increase the concentrations of several antistress compounds and to change their physiology, phenology, growth and reproduction in response to climate change. Rapid adaptation and microevolution occur at the population level. Together with these phenotypic and genotypic adaptations, the movement of organisms and the turnover of populations can lead to migration toward habitats with better conditions unless hindered by barriers. Both migration and local extinction of populations have occurred. However, many unknowns for all these processes remain. The roles of phenotypic plasticity and genotypic evolution and their possible trade-offs and links with population structure warrant further research. The application of omic techniques to ecological studies will greatly favor this research. It remains poorly understood how climate change will result in asymmetrical responses of species and how it will interact with other increasing global impacts, such as N eutrophication, changes in environmental N : P ratios and species invasion, among many others. The biogeochemical and biophysical feedbacks on climate of all these changes in vegetation are also poorly understood. We here review the evidence of responses to climate change and discuss the perspectives for increasing our knowledge of the interactions between climate change and life. © 2013 John Wiley & Sons Ltd.

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Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest

Peñuelas J., Rico L., Ogaya R., Jump A.S., Terradas J. (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biology. 14: 565-575.
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Doi: 10.1111/j.1438-8677.2011.00532.x

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We explored the changes in richness, diversity and evenness of epiphytic (on the leaf surface) and endophytic (within leaf tissues) bacteria and fungi in the foliar phyllosphere of Quercus ilex, the dominant tree species of Mediterranean forests. Bacteria and fungi were assessed during ontogenic development of the leaves, from the wet spring to the dry summer season in control plots and in plots subjected to drought conditions mimicking those projected for future decades. Our aim was to monitor succession in microbiota during the colonisation of plant leaves and its response to climate change. Ontogeny and seasonality exerted a strong influence on richness and diversity of the microbial phyllosphere community, which decreased in summer in the whole leaf and increased in summer in the epiphytic phyllosphere. Drought precluded the decrease in whole leaf phyllosphere diversity and increased the rise in the epiphytic phyllosphere. Both whole leaf bacterial and fungal richness decreased with the decrease in physiological activity and productivity of the summer season in control trees. As expected, the richness of epiphytic bacteria and fungi increased in summer after increasing time of colonisation. Under summer dry conditions, there was a positive relationship between TRF (terminal restriction fragments) richness and drought, both for whole leaf and epiphytic phyllosphere, and especially for fungal communities. These results demonstrate that changes in climate are likely to significantly alter microbial abundance and composition of the phyllosphere. Given the diverse functions and large number of phyllospheric microbes, the potential functional implications of such community shifts warrant exploration. © 2012 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Reduced tree health and seedling production in fragmented Fagus sylvatica forest patches in the Montseny Mountains (NE Spain)

Barbeta A., Peñuelas J., Ogaya R., Jump A.S. (2011) Reduced tree health and seedling production in fragmented Fagus sylvatica forest patches in the Montseny Mountains (NE Spain). Forest Ecology and Management. 261: 2029-2037.
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Doi: 10.1016/j.foreco.2011.02.029

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Habitat fragmentation results in smaller and more isolated populations that may be at higher risk of extirpation or further decline in comparison with their more continuously distributed progenitors. Risks to fragmented populations have frequently been considered from the perspective of population genetics, however, disruption of normal plant demography may be an equal or greater threat to population persistence. We compared demographic performance and tree health in continuous and fragmented forest plots with similar tree size structure and local climatic and physiographic conditions in order to determine if fragments are characterized by poor health and reproduction. We found that beech forest fragments showed lower seedling density, more tree crown damage and also higher percentage of dead trees. However, mortality of juveniles in the youngest age class was substantially lower in fragments such that long-term population structure remained similar between the two forest types. If reduced mortality compensates for reduced seedling establishment, as our data suggest, then fragmented populations should show greater long-term persistence than would be predicted based on comparison of young age cohorts alone. However, despite such demographic compensation, the decreased health of adult trees may pose an increasing future threat to the fragmented populations. Our results demonstrate the importance of integrating demographic patterns over long time periods and not relying on single year or cohort comparisons and may partly explain population genetic differences previously reported for the same populations. © 2011 Elsevier B.V.

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Environmental change and the option value of genetic diversity

Jump A.S., Marchant R., Peñuelas J. (2009) Environmental change and the option value of genetic diversity. Trends in Plant Science. 14: 51-58.
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Doi: 10.1016/j.tplants.2008.10.002

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Rapid anthropogenic environmental change is altering selection pressures on natural plant populations. However, it is difficult to predict easily the novel selection pressures to which populations will be exposed. There is heavy reliance on plant genetic diversity for future crop security in agriculture and industry, but the implications of genetic diversity for natural populations receives less attention. Here, we examine the links between the genetic diversity of natural populations and aspects of plant performance and fitness. We argue that accumulating evidence demonstrates the future benefit or 'option value' of genetic diversity within natural populations when subject to anthropogenic environmental changes. Consequently, the loss of that diversity will hinder their ability to adapt to changing environments and is, therefore, of serious concern. Crown Copyright © 2008.

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The altitude-for-latitude disparity in the range retractions of woody species

Jump A.S., Mátyás C., Peñuelas J. (2009) The altitude-for-latitude disparity in the range retractions of woody species. Trends in Ecology and Evolution. 24: 694-701.
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Doi: 10.1016/j.tree.2009.06.007

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Increasing temperatures are driving rapid upward range shifts of species in mountains. An altitudinal range retreat of 10 m is predicted to translate into a ∼10-km latitudinal retreat based on the rate at which temperatures decline with increasing altitude and latitude, yet reports of latitudinal range retractions are sparse. Here, we examine potential climatic, biological, anthropogenic and methodological explanations for this disparity. We argue that the lack of reported latitudinal range retractions stems more from a lack of research effort, compounded by methodological difficulties, rather than from their absence. Given the predicted negative impacts of increasing temperatures on wide areas of the latitudinal distributions of species, the investigation of range retractions should become a priority in biogeographical research. © 2009 Elsevier Ltd. All rights reserved.

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Microspatial population genetic structure of the Mediterranean shrub Fumana thymifolia

Jump A.S., Rico L., Lloret F., Peñuelas J. (2009) Microspatial population genetic structure of the Mediterranean shrub Fumana thymifolia. Plant Biology. 11: 152-160.
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Doi: 10.1111/j.1438-8677.2008.00109.x

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Fumana thymifolia (Cistaceae) is an insect-pollinated, gravity-dispersed evergreen shrub, which is a common component of fire-prone Mediterranean shrubland ecosystems. Despite the availability of basic knowledge on its ecology, little is known of its breeding system and no information is available on its population genetic structure. We explored the within-population genetic structure of this species using amplified fragment length polymorphism (AFLP) molecular markers and related this to predictions based on its breeding system, pollen and seed dispersal. Existing information on the reproductive ecology of F. thymifolia was supplemented by artificial pollination experiments. We determined that self-fertilisation can occur in F. thymifolia but results in reduced fruit set. Significant genetic structuring was detected within the population, a likely consequence of localised seed dispersal in combination with a mixed mating system. In a study site covering approximately 0.5 ha, amova revealed that approximately 9% of genetic variability was distributed among population subsamples. Significant spatial genetic structure was detected, with kinship coefficients being significantly elevated above the null expectation in the first six distance classes (maximum 5 m), and a value of Sp of up to 0.0342, comparable with species having similar ecological characteristics. Weak isolation by distance at the plot scale was detected, suggesting that insect-mediated pollen flow is non-random, despite being more extensive than seed dispersal. Fumana thymifolia provides a promising model for the investigation of both short- and long-term population dynamics in relation to fire frequency within this plant community. © 2008 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia

Jump A.S., Peñuelas J., Rico L., Ramallo E., Estiarte M., Martínez-Izquierdo J.A., Lloret F. (2008) Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia. Global Change Biology. 14: 637-643.
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Doi: 10.1111/j.1365-2486.2007.01521.x

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Rapid climate change will impose strong directional selection pressures on natural plant populations. Climate-linked genetic variation in natural populations indicates that an evolutionary response is possible. We investigated such a response by comparing individuals subjected to elevated drought and warming treatments with individuals establishing in an unmanipulated climate within the same population. We report that reduction in seedling establishment in response to climate manipulations is nonrandom and results from the selection pressure imposed by artificially warmed and droughted conditions. When compared against control samples, high single-locus genetic divergence occurred in drought and warming treatment samples, with genetic differentiation up to 37 times higher than background (mean neutral locus) genetic differentiation. These loci violate assumptions of selective neutrality, indicating the signature of natural selection by drought. Our results demonstrate that rapid evolution in response to climate change may be widespread in natural populations, based on genetic variation already present within the population. © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd.

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Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: Increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes

Peñuelas J., Hunt J.M., Ogaya R., Jump A.S. (2008) Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: Increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Global Change Biology. 14: 1076-1088.
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Doi: 10.1111/j.1365-2486.2008.01563.x

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We aimed to gain knowledge on the changes in intrinsic water use efficiency (iWUE) in response to increasing atmospheric CO2 concentrations and climate change over the last century. We investigated the variation in the iWUE of mature Fagus sylvatica trees located in the higher, central and lower altitudinal forest limits (HFL, CFA and LFL) of one of the southernmost sites of beech distribution in Europe, the Montseny Mountains in Catalonia (northeast Spain), during the last century by analysing the δ13C of their tree rings. Pre- and post-maturation phases of the trees presented different trends in δ13C, Δ13C, Ci (internal CO2 concentration), iWUE and basal area increment (BAI). Moreover, these variables showed different trends and absolute values in the LFL than in the other altitudinal sites, CFA and HFL. Our results show the existence of an age effect on δ13C in the CFA and HFL (values increased by ca. 1.25‰ coinciding with the BAI suppression and release phases, previous to maturation). These age-related changes were not found in the LFL, whose beech trees arrived to maturation earlier and experienced drier conditions during the suppression phase. In the last 26 years of comparable mature trees, the increase of iWUE deduced from the Δ13C analyses was ca. 10% in LFL, ca. 6% in CFA and not significant in HFL. These results show that climate change towards more arid conditions accounted for these higher Δ13C-values and increases in the LFL more than the continuous increase in atmospheric CO2 concentrations. This increased iWUE in the LFL did not avoid a decline in growth in these lowest altitudes of this beech southern range-edge as a result of warming. Furthermore, since there was no apparent change in iWUE and growth in the beech forests growing in the more standard-adequate environments of higher altitudes in the last 26 years, the rate of sequestration of C into temperate ecosystems may not increase with increasing atmospheric CO2 concentrations as predicted by most models based on short-term small scale experiments. © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd.

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Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny Mountains, northeast Spain

Jump A.S., Hunt J.M., Peñuelas J. (2007) Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny Mountains, northeast Spain. Ecoscience. 14: 507-518.
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Doi: 10.2980/1195-6860(2007)14[507:CROGAE]2.0.CO;2

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A rise in elevation of the temperate biome has been reported in the mountains of northeast Spain. We aimed to determine the principal climatic factors limiting growth and establishment of the dominant temperate tree, Fagus sylvatica, across its altitudinal range and how its climate-response has varied over time. We determined the climate-response of the growth of adult trees and the establishment of juveniles using dendroecological methods at 3 sites along an elevational gradient spanning this species' full altitudinal distribution of approximately 1000-1650 in above sea level. We found strong altitudinal variation in growth and establishment responses to climate. The most common growth response was to high spring and summer temperature (April-July), which promoted growth and establishment at the upper treeline but had the opposite effect at low altitudes. Precipitation was strongly limiting for adult growth at the lower limit of F. sylvatica and declined in importance with increasing altitude. Sensitivity of growth to summer temperature increased over the second half of the 20th century. Future increases in summer temperature are likely to have negative consequences for growth and establishment at this species' low altitude, low latitude range-edge, particularly if temperature increase is not matched by increasing precipitation.

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Extensive spatial genetic structure revealed by AFLP but not SSR molecular markers in the wind-pollinated tree, Fagus sylvatica

Jump A.S., Peñuelas J. (2007) Extensive spatial genetic structure revealed by AFLP but not SSR molecular markers in the wind-pollinated tree, Fagus sylvatica. Molecular Ecology. 16: 925-936.
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Doi: 10.1111/j.1365-294X.2006.03203.x

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Studies of fine-scale spatial genetic structure (SGS) in wind-pollinated trees have shown that SGS is generally weak and extends over relatively short distances (less than 30-40 m) from individual trees. However, recent simulations have shown that detection of SGS is heavily dependent on both the choice of molecular markers and the strategy used to sample the studied population. Published studies may not always have used sufficient markers and/or individuals for the accurate estimation of SGS. To assess the extent of SGS within a population of the wind-pollinated tree Fagus sylvatica, we genotyped 200 trees at six microsatellite or simple sequence repeat (SSR) loci and 250 amplified fragment length polymorphisms (AFLP) and conducted spatial analyses of pairwise kinship coefficients. We re-sampled our data set over individuals and over loci to determine the effect of reducing the sample size and number of loci used for SGS estimation. We found that SGS estimated from AFLP markers extended nearly four times further than has been estimated before using other molecular markers in this species, indicating a persistent effect of restricted gene flow at small spatial scales. However, our SSR-based estimate was in agreement with other published studies. Spatial genetic structure in F. sylvatica and similar wind-pollinated trees may therefore be substantially larger than has been estimated previously. Although 100-150 AFLP loci and 150-200 individuals appear sufficient for adequately estimating SGS in our analysis, 150-200 individuals and six SSR loci may still be too few to provide a good estimation of SGS in this species. Journal compilation © 2006 Blackwell Publishing Ltd.

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