Correlating δ13C and δ18O in cellulose of trees

We measured the carbon and oxygen isotopic composition of stem cellulose of Pinus sylvestris, Picea abies, Fagus sylvatica and Fraxinus excelsior. Several sites along a transect of a small valley in Switzerland were selected which differ in soil moisture conditions. At every site, six trees per species were sampled, and a sample representing a mean value for the period from 1940 to 1990 was analysed. For all species, the mean site δ¹³C and δ¹⁸O of stem cellulose are related to the soil moisture availability, whereby higher isotope ratios are found at drier sites. This result is consistent with isotope fractionation models when assuming enhanced stomatal resistance (thus higher δ¹³C of incorporated carbon) and increased oxygen isotope enrichment in the leaf water (thus higher δ¹⁸O) at the dry sites. δ¹⁸ O-δ¹³C plots reveal a linear relationship between the carbon and oxygen isotopes in cellulose. To interpret this relationship we developed an equation which combines the above-mentioned fractionation models. An important new parameter is the degree to which the leaf water enrichment is reflected in the stem cellulose. In the combined model the slope of the δ¹⁸O-δ¹³C plot is related to the sensitivity of the p_i/p_a of a plant to changing relative humidity.     

Annual cyclicity in high-resolution stable carbon and oxygen isotope ratios in the wood of the mangrove tree Rhizophora mucronata

In the present study, the high‐resolution stable carbon (¹³C/¹²C) and oxygen (¹⁸O/¹⁶O) isotope ratio profiles in the wood of the mangrove Rhizophora mucronata Lam., a tropical tree species lacking distinct growth rings, were investigated. Variations of both isotope ratios revealed a remarkable annual cyclicity with lowest values occurring at the latewood/earlywood boundary (April–May) and highest values during the transition from earlywood to latewood (October–November). Based on the current knowledge of the physiology of this mangrove species, as well as on the current literature available on high‐resolution profiles of stable isotope ratios in tree rings, possible driving forces responsible for this seasonal pattern are discussed. The annual cyclicity, together with a conspicuous isotope pattern appearing in the El‐Niño year 1997, promises great potential for tropical dendrochronology.     

Stable isotope composition of organic compounds transported in the phloem of European beech--evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport

The analysis of stable isotope composition (delta13C, delta15N, delta18O) of phloem-transported organic matter is a useful tool for assessing short-term carbon and water balance of trees. A major constraint of the general application of this method to trees at natural field sites is that the collection of phloem sap with the "phloem bleeding" technique is restricted to particular species and plant parts. To overcome this restriction, we compared the contents (amino compounds and sugars) and isotope signatures (delta13C, delta15N, delta18O) of phloem sap directly obtained from incisions in the bark (bleeding technique) with phloem exudates where bark pieces were incubated in aqueous solutions (phloem exudation technique with and without chelating agents [EDTA, polyphosphate] in the initial sampling solution, which prevent blocking of sieve tubes). A comparable spectrum of amino compounds and sugars was detected using the different techniques. O, C, or N compounds in the initial sampling solution originating from the chelating agents always decreased precision of determination of the respective isotopic signatures, as indicated by higher standard deviation, and/or led to a significant difference of mean delta as compared to the phloem bleeding technique. Hence, depending on the element from which the ratio of heavy to light isotope is determined, compounds lacking C, N, and/or O should be used as chelating agents in the exudation solution. In applying the different techniques, delta13C of organic compounds transported in the phloem of the twig (exudation technique with polyphosphate as chelating agent) were compared with those in the phloem of the main stem (phloem bleeding technique) in order to assess possible differences in carbon isotope composition of phloem carbohydrates along the tree axis. In July, organic compounds in the stem phloem were significantly enriched in 13C by > 1.3 per thousand as compared to the twig phloem, whereas this effect was not observed in September. Correlation analysis between delta13C and stomatal conductance (Gs) revealed the gradient from the twigs to the stem observed in July may be attributed to temporal differences rather than to spatial differences in carbon isotope composition of sugars. As various authors have produced conflicting results regarding the enrichment/depletion of 13C in organic compounds in the leaf-to-stem transition, the different techniques presented in this paper can be used to provide further insight into fractionation processes associated with transport of C compounds from leaves to branches and down the main stem.     

Carbon and oxygen isotope composition of organic compounds in the phloem sap provides a short-term measure for stomatal conductance of European beech (Fagus sylvatica L.)

At eight different dates during the 2000 growing season, δ¹³C and δ¹⁸O were determined in the phloem of adult beech trees growing in natural beech stands in south‐west Germany differing in stand density and local climate. In addition, stand transpiration, precipitation, photosynthetic active radiation, relative air humidity, water pressure deficit of the air, air and soil temperature, soil water potential, and sugar concentration of the phloem sap were determined directly and evaporation and canopy stomatal conductance were modelled. All parameters were related to δ¹³C. The study aimed to identify the time integral within which the δ¹³C of organic compounds transported in the phloem is an indicative measure of these environmental influences. δ¹³C of soluble carbon transported in the phloem was well correlated with mean stomatal conductance in a two‐day integral prior to phloem sampling but did not depend on either light intensity or soil water availability. A strong positive relationship between δ¹³C and δ¹⁸O pointed to observed variation in δ¹³C of phloem sap being a result of variation in stomatal conductance. Bulk leaf δ¹³C was a poor indicator of changes in environmental conditions during the growing season. From these results we conclude that the analysis of δ¹³C in soluble carbon transported in the phloem is a reliable indicator of short‐term changes in C_i/C_a. In contrast, the δ¹³C of structural carbon in beech foliage represents an integration of a range of factors that mask short‐term influences responsible for C_i/C_a.     

A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin Eudyptes chrysocome

The rockhopper penguin (Eudyptes chrysocome) is a conspicuous apex marine predator that has experienced marked population declines throughout most of its circumpolar breeding distribution. The cause(s) for the declines remain elusive, but the relatively large spatio‐temporal scale over which population decreases have occurred implies that ecosystem‐scale, at‐sea factors are likely to be involved. We employ stable isotope analyses of carbon (¹³C/¹²C, expressed as δ¹³C) and nitrogen (¹⁵N/¹⁴N, δ¹⁵N) in time‐series of rockhopper penguin feather samples, dating back to 1861, in order to reconstruct the species' ecological history. Specifically, we examine whether rockhopper penguin population decline has been associated with a shift towards lower primary productivity in the ecosystem in which they feed, or with a shift to a diet of lower trophic status and lower quality, and we use long‐term temperature records to evaluate whether shifts in isotope ratios are associated with annual variations in sea surface temperature. Having controlled temporally for the Suess Effect and for increases in CO₂ concentrations in seawater, we found that overall, δ¹³C signatures decreased significantly over time in rockhopper penguins from seven breeding sites, supporting the hypothesis that decreases in primary productivity, and hence, carrying capacity, for which δ¹³C signature is a proxy, have been associated with the decline of penguin populations. There was some evidence of a long‐term decline in δ¹⁵N at some sites, and strong evidence that δ¹⁵N signatures were negatively related to sea surface temperatures across sites, indicative of a shift in diet to prey of lower trophic status over time and in warm years. However, a site‐by‐site analysis revealed divergent isotopic trends among sites: five of seven sites exhibited significant temporal or temperature‐related trends in isotope signatures. This study highlights the utility of stable isotope analyses when applied over relatively long timescales to apex predators.     

Increasing carbon discrimination rates and depth of water uptake favor the growth of Mediterranean evergreen trees in the ecotone with temperate deciduous forests

Tree populations at the low‐altitudinal or ‐latitudinal limits of species' distributional ranges are predicted to retreat toward higher altitudes and latitudes to track the ongoing changes in climate. Studies have focused on the climatic sensitivity of the retreating species, whereas little is known about the potential replacements. Competition between tree species in forest ecotones will likely be strongly influenced by the ecophysiological responses to heat and drought. We used tree‐ring widths and δ¹³C and δ¹⁸O chronologies to compare the growth rates and long‐term ecophysiological responses to climate in the temperate‐Mediterranean ecotone formed by the deciduous Fagus sylvatica and the evergreen Quercus ilex at the low altitudinal and southern latitudinal limit of F. sylvatica (NE Iberian Peninsula). F. sylvatica growth rates were similar to those of other southern populations and were surprisingly not higher than those of Q. ilex, which were an order of magnitude higher than those in nearby drier sites. Higher Q. ilex growth rates were associated with high temperatures, which have increased carbon discrimination rates in the last 25 years. In contrast, stomatal regulation in F. sylvatica was proportional to the increase in atmospheric CO₂. Tree‐ring δ¹⁸O for both species were mostly correlated with δ¹⁸O in the source water. In contrast to many previous studies, relative humidity was not negatively correlated with tree‐ring δ¹⁸O but had a positive effect on Q. ilex tree‐ring δ¹⁸O. Furthermore, tree‐ring δ¹⁸O decreased in Q. ilex over time. The sensitivity of Q. ilex to climate likely reflects the uptake of deep water that allowed it to benefit from the effect of CO₂ fertilization, in contrast to the water‐limited F. sylvatica. Consequently, Q. ilex is a strong competitor at sites currently dominated by F. sylvatica and could be favored by increasingly warmer conditions.     

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

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.     

Bulk leaf δ18O and δ13C reflect the intensity of intraspecific competition for water in a semi-arid tussock grassland

We investigated the extent to which plant water and nutrient status are affected by intraspecific competition intensity and microsite quality in a monodominant tussock grassland. Leaf gas exchange and stable isotope measurements were used to assess the water relations of Stipa tenacissima tussocks growing along a gradient of plant cover and soil depth in a semi-arid catchment of Southeast Spain. Stomatal conductance and photosynthetic rate decreased with increasing intensity of competition during the wet growing season, leading to foliar δ ¹⁸O and δ ¹³C enrichment. A high potential for runoff interception by upslope neighbours exerted strong detrimental effects on the water and phosphorus status of downslope S. tenacissima tussocks. Foliar δ ¹⁵N values became more enriched with increasing soil depth. Multiple stepwise regression showed that competition potential and/or rhizosphere soil depth accounted for large proportions of variance in foliar δ ¹³C, δ ¹⁸O and δ ¹⁵N among target tussocks (57, 37 and 64%, respectively). The results presented here highlight the key role that spatial redistribution of resources (water and nutrients) by runoff plays in semi-arid ecosystems. It is concluded that combined measurement of δ ¹³C, δ ¹⁸O and nutrient concentrations in bulk leaf tissue can provide insight into the intensity of competitive interactions occurring in natural plant communities.     

Highest drought sensitivity and lowest resistance to growth suppression are found in the range core of the tree Fagus sylvatica L. not the equatorial range edge

Biogeographical and ecological theory suggests that species distributions should be driven to higher altitudes and latitudes as global temperatures rise. Such changes occur as growth improves at the poleward edge of a species distribution and declines at the range edge in the opposite or equatorial direction, mirrored by changes in the establishment of new individuals. A substantial body of evidence demonstrates that such processes are underway for a wide variety of species. Case studies from populations at the equatorial range edge of a variety of woody species have led us to understand that widespread growth decline and distributional shifts are underway. However, in apparent contrast, other studies report high productivity and reproduction in some range edge populations. We sought to assess temporal trends in the growth of the widespread European beech tree (Fagus sylvatica) across its latitudinal range. We explored the stability of populations to major drought events and the implications for predicted widespread growth decline at its equatorial range edge. In contrast to expectations, we found greatest sensitivity and low resistance to drought in the core of the species range, whilst dry range edge populations showed particularly high resistance to drought and little evidence of drought‐linked growth decline. We hypothesize that this high range edge resistance to drought is driven primarily by local environmental factors that allow relict populations to persist despite regionally unfavourable climate. The persistence of such populations demonstrates that range‐edge decline is not ubiquitous and is likely to be driven by declining population density at the landscape scale rather than sudden and widespread range retraction.     

Long tree‐ring chronologies reveal 20th century increases in water‐use efficiency but no enhancement of tree growth at five Iberian pine forests

We investigated the tree growth and physiological response of five pine forest stands in relation to changes in atmospheric CO₂ concentration (c_a) and climate in the Iberian Peninsula using annually resolved width and δ¹³C tree‐ring chronologies since ad 1600. ¹³C discrimination (Δ≈c_i/c_a), leaf intercellular CO₂ concentration (c_i) and intrinsic water‐use efficiency (iWUE) were inferred from δ¹³C values. The most pronounced changes were observed during the second half of the 20th century, and differed between stands. Three sites kept a constant c_i/c_a ratio, leading to significant c_i and iWUE increases (active response to c_a); whereas a significant increase in c_i/c_a resulted in the lowest iWUE increase of all stands at a relict Pinus uncinata forest site (passive response to c_a). A significant decrease in c_i/c_a led to the greatest iWUE improvement at the northwestern site. We tested the climatic signal strength registered in the δ¹³C series after removing the low‐frequency trends due to the physiological responses to increasing c_a. We found stronger correlations with temperature during the growing season, demonstrating that the physiological response to c_a changes modulated δ¹³C and masked the climate signal. Since 1970 higher δ¹³C values revealed iWUE improvements at all the sites exceeding values expected by an active response to the c_a increase alone. These patterns were related to upward trends in temperatures, indicating that other factors are reinforcing stomatal closure in these forests. Narrower rings during the second half of the 20th century than in previous centuries were observed at four sites and after 1970 at all sites, providing no evidence for a possible CO₂‘fertilization’ effect on growth. The iWUE improvements found for all the forests, reflecting both a c_a rise and warmer conditions, seem to be insufficient to compensate for the negative effects of the increasing water limitation on growth.     

Stand structure modulates the long-term vulnerability of Pinus halepensis to climatic drought in a semiarid Mediterranean ecosystem

We investigated whether stand structure modulates the long-term physiological performance and growth of Pinus halepensis Mill. in a semiarid Mediterranean ecosystem. Tree radial growth and carbon and oxygen stable isotope composition of latewood (δ(13)C(LW) and δ(18)O(LW), respectively) from 1967 to 2007 were measured in P. halepensis trees from two sharply contrasting stand types: open woodlands with widely scattered trees versus dense afforested stands. In both stand types, tree radial growth, δ(13)C(LW) and δ(18)O(LW) were strongly correlated with annual rainfall, thus indicating that tree performance in this semiarid environment is largely determined by inter-annual changes in water availability. However, trees in dense afforested stands showed consistently higher δ(18)O(LW) and similar δ(13)C(LW) values compared with those in neighbouring open woodlands, indicating lower stomatal conductance and photosynthesis rates in the former, but little difference in water use efficiency between stand types. Trees in dense afforested stands were more water stressed and showed lower radial growth, overall suggesting greater vulnerability to drought and climate aridification compared with trees in open woodlands. In this semiarid ecosystem, the negative impacts of intense inter-tree competition for water on P. halepensis performance clearly outweigh potential benefits derived from enhanced infiltration and reduced run-off losses in dense afforested stands.