Environmental and physiological drivers of tree growth : a pan-tropical study of stable isotopes in tree rings

Forests in the wet tropics harbour an incredible biodiversity, provide many ecosystem services and regulate climatic conditions on regional scales. Tropical forests are also a major component of the global carbon cycle, storing 25% of the total terrestrial carbon and accounting for a third of net primary production. This means that changes in forest structure and forest cover in the wet tropics will not only affect biodiversity and ecosystem services, but also have implications for the global carbon cycle and – as a result – may speed up or slow down global warming. Deforestation rates are still high in the tropics and have profoundly affected the extent of forests in many countries. Additionally, there are indications that undisturbed and pristine tropical forests are changing. The most notable changes found by the monitoring of permanent forest plots are an increase of tree growth and forest biomass per unit of surface area over the last decades. If this is indeed the case, it would entail that the world’s tropical forests are potentially absorbing a significant fraction of human caused CO2emissions and as such are mitigating global warming. However, increased tree growth and forest biomass have not been found in all studies. Furthermore, it is unknown whether the observed changes in intact forests are part of a long-term change, or merely reflect decadal scale fluctuations. These uncertainties lead to an ongoing debate on whether tree growth and forest biomass have increased in tropical forests and – if so – to what extent. In addition, there is also a scientific discussion on the factor(s) that could underlie the potential changes in tree growth and forest biomass. Possibly, they are caused by an internal driver, like the lasting effect of large scale disturbances in the past, or by external drivers. Possible external factors affecting tropical forest dynamics are (1) climate change (temperature and precipitation), (2) increased nutrient depositions and (3) increased atmospheric CO2concentration. In this thesis, I investigated the environmental changes that could have formed the basis for changes in tropical tree growth. I used two relatively new tools in tropical forest ecology: tree-ring measurements and stable isotope analyses. Tree-ring widths were measured to obtain long-term information on tree growth. Stable isotopes in the wood of tree rings were analysed to provide information on the environmental and physiological drivers of tree growth changes. This thesis is part of a larger project on the long-term changes in intact forests in the wet tropics (the TroFoClim project, led by Pieter Zuidema) and also includes the PhD theses of Mart Vlam and Peter Groenendijk. In this project, ~1400 trees of 15 species were examined that were collected in three forest sites distributed across the tropics (in Bolivia, Cameroon and Thailand). For the assessment of long-term changes in growth and stable isotopes, it is important to understand shorter term fluctuations due to forest dynamics (i.e. gap formation), because these interfere with changes on a longer temporal scale. The formation of a gap in a closed canopy forest, after the death of a tree, can cause considerable environmental changes in the surrounding area, e.g. in light, nutrient and water availability. This can strongly affect the growth rates of the remaining trees. However, in most studies the environmental drivers of changes in tree growth after gap formation are not considered. In CHAPTER 2 I measured carbon isotope discrimination (Δ13C) in annual growth rings of Peltogyne cf.heterophylla, from a moist forest in North-eastern Bolivia, and evaluated the environmental drivers of growth responses after gap formation. Growth and Δ13C was compared between the seven years before and after gap formation. Forty-two trees of different sizes were studied, half of which grew close (13C suggesting that this response was driven by increased light availability and not by improved water availability. Interestingly, most small trees did not show a growth stimulation after gap formation. This result was hypothesized to be caused by an increased drought stress. However, the measurement of Δ13C showed that increased water stress is unlikely the cause for the absence of increased growth, but rather suggested that light conditions had not improved after gap formation. These results show that combining growth rates with changes in Δ13Cis a valuable tool to better understand the causes of temporal variation in tree growth. An important potential driver of long-term changes in tree growth is climate change, e.g. global warming and altered annual precipitation. To understand the effect of climate change on tree growth, the availability of reliable data on historical climate is off course crucial. For the study areas in Bolivia and Thailand, previous studies have investigated the occurrence of temporal trends in temperature and precipitation. For the study area in Cameroon however, as well as for West and Central Africa in general, the availability of instrumental climate data is very restricted. This limits the possibility to relate past climatic variation to changes in tree growth and calls for proxies that allow reconstruction of past climatic conditions. In CHAPTER 3 I assessed the potential use of stable isotopes of oxygen (δ18O) in tree rings as a tool for the reconstruction of precipitation in tropical Africa. I measured δ18O in tree rings of five large Entandrophragmautiletreesfrom North-western Cameroon. A significant negative correlation was found between annual tree-ring δ18O values (averaged over the five individuals) and annual precipitation amount during 1930-2009 in large areas of West and Central Africa. I also found tree-ring δ18O to track sea surface temperatures (SST) in the Gulf of Guinea (1930-2009). These two results are related because rainfall variabilityin West and Central Africa is profoundly influenced by the SST of the tropical AtlanticOcean. Thus a high SST in the Gulf of Guinea is associated with high precipitation over large parts of West and Central Africa and recorded in tree rings by a relatively low δ18O value. On the other hand, dry years when SST is low, are recorded by relatively high tree-ring δ18O values. I also found a significant long-term increase of tree-ring δ18O values. This trend seems to be caused by lowered precipitation from 1970 to 1990 (the Sahel drought period). From 1860 to 1970, no significant long-term trend was observed in tree-ring δ18O values, suggesting no substantial change in precipitation amount occurred over this period. Another potential driver of altered tree growth and biomass in intact tropical forests is the increase of anthropogenic nutrient depositions, especially nitrogen. The deposition of nitrogen has likely risen due to an increased industrialization and use of artificial N fertilizers in most tropical countries. Nitrogen can stimulate plant growth, as is well known from the positive effect of N fertilizer application on crop yields. Previous studies have shown that the stable isotope ratio of nitrogen (δ15N) increased during the last decennia in the wood of trees from Brazil and Thailand as well as in tree leaves from Panama. This increased δ15N has been interpreted as a signal that tropical nitrogen cycles have become more ‘open’ and ‘leaky’ during the last decades in response to increased anthropogenic nitrogen depositions. The underlying mechanism is that high rates of nitrogen deposition and high ambient nitrogen availability lead to an increased nitrification. This process can cause a gradual 15N-enrichment of soil nitrogen. In CHAPTER 4 I analysed changes in tree-ring δ15N values of 400 trees of six species from the three study sites. In the trees from Cameroon no long-term change of tree-ring δ15N values was found (1850-2005), even though NH3and NOxemissions seem to have increased strongly around the study area since 1970. Possibly, the very high precipitation at that site causes the local nitrogen cycle to be already very ‘leaky’, limiting the effect of additional nitrogen input on the δ15N signature of soil nitrogen. Alternatively, nitrogen input in this forest might be much lower than reconstructed NH3and NOxemissions suggest. For the study site in Bolivia, no significant change of tree-ring δ15N values was found (1875-2005), which is in line with the expected result for areas with a low anthropogenic nitrogen input. I found a marginally significant increased of δ15N values since 1950 in trees from Thailand, which confirms previous observations. This points to an effect of increased anthropogenic nitrogen deposition, which could have stimulated photosynthetic rates, if indeed nitrogen was limiting tree growth. The most often hypothesized factor to cause a long-term increase of tree growth is the rise of atmospheric CO2. Since the onset of the industrial revolution (~1850) global atmospheric CO2concentration has increased by 40%. Elevated CO2can directly affect plants by increasing the activity, as well as the efficiency, of the CO2fixing enzyme rubisco and thereby increase photosynthetic rates. Potentially more important in plant communities subjected to periods of limited water availability (like a dry season) is that elevated CO2 can cause a reduction of stomatal conductance, which lowers evapo-transpiration and hence reduces water losses.This increases water-use efficiency (i.e. the amount of carbon gained through photosynthesis divided by the amount of water loss through transpiration) and might allow plants to extend their growth season and/or increase their photosynthetic activity during the hottest hours of the day when water-stress might be severe. Elevated atmospheric CO2is thus a very likely candidate to have stimulated tropical tree growth (also referred to as CO2fertilization), provided at least that plant growth was either carbon or water limited. In CHAPTER 5 I tested the CO2fertilization hypothesis by analysing growth-ring data of 1100 trees from the three study sites. The measurement of tree-ring widths allowed an assessment of historical growth rates, whereas stable carbon isotopes (δ13C) in the wood of the trees were used to obtain an estimate of the CO2concentration in the intercellular spaces in leaves (Ci) and of water-use efficiency (intrinsic water-use efficiency; iWUE). I used a sampling method that controls for ontogenetic (i.e. size developmental) changes in growth and δ13C. With this method, trees were compared across a fixed diameter (i.e. same ontogenetic stage). I chose two diameters: 8 cm (referring to small understorey trees) and 27 cm (referring to larger canopy trees). A mixed-effect model revealeda highly significant and exponential increase of Ciat each of the three sites, and in both understorey and canopy trees. Over the last 150 years Ciincreased by 43% and 53% for understorey and canopy trees respectively. Yet, the rate of increase in Ciwas consistently lower than that of atmospheric CO2. This ‘active’ response to elevated atmospheric CO2resulted in a significant and large increase of iWUE. Over the last 150 years, iWUE increased by 30% and 35% for understorey and canopy trees.A long-term increase of iWUE indicates either a proportional increase of net photosynthesis and/or a decrease of stomatal conductance and thus transpiration, both of which could have stimulated biomass growth. However, I found no increase of tree growth over the last 150 years in any of the sites. Although there are several possible explanations for these findings, I argue that it is most likely that tropical tree growth is generally not limited by water and carbon, but by a persistent nutrient limitation (e.g. of phosphates) and that this has prevented tropical trees to use the extra CO2for an acceleration of growth. In this thesis I have studied environmental and physiological drivers of tree growth changes. I found evidence of decreased precipitation over the last decades at the study site in Cameroon (CHAPTER 3), a changed nitrogen cycle at the study site in Thailand (CHAPTER 4) and an overall change in the physiology of all tree species studied (increased iWUE; CHAPTER 5). One of the main findings of this thesis is however, that these changes have not led to a net change of tree growth over the last 150 years (CHAPTER 5). This is an important finding that could have two major implications. Firstly, the absence of a long-term growth stimulation suggests that the increase of iWUE is mainly driven by a reduced stomatal conductance, which likely leads to a reduced evaporative water loss. If trees across the tropics are reducing evapo-transpiration, this will change affect hydrological cycles, e.g. leading to a lower humidity, higher air temperatures and a reduced precipitation. Secondly, the absence of a growth stimulation over the last 150 years suggests that the carbon sink capacity of tropical forests is currently overestimated, e.g. by Dynamic Global Vegetation Models, which assume strong CO2fertilization effects and as such a high capacity of tropical forests to mitigate global warming. I anticipate that the planned Free Air Concentration Enrichment (FACE) experiments in the tropics will shed light on the reasons why increased CO2does not stimulate the growth rates of tropical trees. Furthermore, I argue that combining tree-ring measurements and stable isotope analyses together with permanent plot research is the most promising way to increase our understanding of the changes in tropical forests.</p

15N in tree rings as a bio-indicator of changing nitrogen cycling in tropical forests: an evaluation at three sites using two sampling methods

Anthropogenic nitrogen deposition is currently causing a more than twofold increase of reactive nitrogen input over large areas in the tropics. Elevated N-15 abundance (delta N-15) in the growth rings of some tropical trees has been hypothesized to reflect an increased leaching of N-15-depleted nitrate from the soil, following anthropogenic nitrogen deposition over the last decades. To find further evidence for altered nitrogen cycling in tropical forests, we measured long-term delta N-15 values in trees from Bolivia, Cameroon, and Thailand. We used two different sampling methods. In the first, wood samples were taken in a conventional way: from the pith to the bark across the stem of 28 large trees (the "radial" method). In the second, delta N-15 values were compared across a fixed diameter (the "fixed-diameter" method). We sampled 400 trees that differed widely in size, but measured delta N-15 in the stem around the same diameter (20 cm dbh) in all trees. As a result, the growth rings formed around this diameter differed in age and allowed a comparison of delta N-15 values over time with an explicit control for potential size-effects on delta N-15 values. We found a significant increase of tree-ring delta N-15 across the stem radius of large trees from Bolivia and Cameroon, but no change in tree-ring delta N-15 values over time was found in any of the study sites when controlling for tree size. This suggests that radial trends of delta N-15 values within trees reflect tree ontogeny (size development). However, for the trees from Cameroon and Thailand, a low statistical power in the fixed-diameter method prevents to conclude this with high certainty. For the trees from Bolivia, statistical power in the fixed-diameter method was high, showing that the temporal trend in tree-ring delta N-15 values in the radial method is primarily caused by tree ontogeny and unlikely by a change in nitrogen cycling. We therefore stress to account for tree size before tree-ring delta N-15 values can be properly interpreted

Environmental and physiological drivers of tree growth : a pan-tropical study of stable isotopes in tree rings

Forests in the wet tropics harbour an incredible biodiversity, provide many ecosystem services and regulate climatic conditions on regional scales. Tropical forests are also a major component of the global carbon cycle, storing 25% of the total terrestrial carbon and accounting for a third of net primary production. This means that changes in forest structure and forest cover in the wet tropics will not only affect biodiversity and ecosystem services, but also have implications for the global carbon cycle and – as a result – may speed up or slow down global warming. Deforestation rates are still high in the tropics and have profoundly affected the extent of forests in many countries. Additionally, there are indications that undisturbed and pristine tropical forests are changing. The most notable changes found by the monitoring of permanent forest plots are an increase of tree growth and forest biomass per unit of surface area over the last decades. If this is indeed the case, it would entail that the world’s tropical forests are potentially absorbing a significant fraction of human caused CO2emissions and as such are mitigating global warming. However, increased tree growth and forest biomass have not been found in all studies. Furthermore, it is unknown whether the observed changes in intact forests are part of a long-term change, or merely reflect decadal scale fluctuations. These uncertainties lead to an ongoing debate on whether tree growth and forest biomass have increased in tropical forests and – if so – to what extent. In addition, there is also a scientific discussion on the factor(s) that could underlie the potential changes in tree growth and forest biomass. Possibly, they are caused by an internal driver, like the lasting effect of large scale disturbances in the past, or by external drivers. Possible external factors affecting tropical forest dynamics are (1) climate change (temperature and precipitation), (2) increased nutrient depositions and (3) increased atmospheric CO2concentration. In this thesis, I investigated the environmental changes that could have formed the basis for changes in tropical tree growth. I used two relatively new tools in tropical forest ecology: tree-ring measurements and stable isotope analyses. Tree-ring widths were measured to obtain long-term information on tree growth. Stable isotopes in the wood of tree rings were analysed to provide information on the environmental and physiological drivers of tree growth changes. This thesis is part of a larger project on the long-term changes in intact forests in the wet tropics (the TroFoClim project, led by Pieter Zuidema) and also includes the PhD theses of Mart Vlam and Peter Groenendijk. In this project, ~1400 trees of 15 species were examined that were collected in three forest sites distributed across the tropics (in Bolivia, Cameroon and Thailand). For the assessment of long-term changes in growth and stable isotopes, it is important to understand shorter term fluctuations due to forest dynamics (i.e. gap formation), because these interfere with changes on a longer temporal scale. The formation of a gap in a closed canopy forest, after the death of a tree, can cause considerable environmental changes in the surrounding area, e.g. in light, nutrient and water availability. This can strongly affect the growth rates of the remaining trees. However, in most studies the environmental drivers of changes in tree growth after gap formation are not considered. In CHAPTER 2 I measured carbon isotope discrimination (Δ13C) in annual growth rings of Peltogyne cf.heterophylla, from a moist forest in North-eastern Bolivia, and evaluated the environmental drivers of growth responses after gap formation. Growth and Δ13C was compared between the seven years before and after gap formation. Forty-two trees of different sizes were studied, half of which grew close (<10m) to single tree-fall gaps; the other half grew more than 40 m away from gaps (control trees). I found that increased growth was mainly associated with decreased Δ13C suggesting that this response was driven by increased light availability and not by improved water availability. Interestingly, most small trees did not show a growth stimulation after gap formation. This result was hypothesized to be caused by an increased drought stress. However, the measurement of Δ13C showed that increased water stress is unlikely the cause for the absence of increased growth, but rather suggested that light conditions had not improved after gap formation. These results show that combining growth rates with changes in Δ13Cis a valuable tool to better understand the causes of temporal variation in tree growth. An important potential driver of long-term changes in tree growth is climate change, e.g. global warming and altered annual precipitation. To understand the effect of climate change on tree growth, the availability of reliable data on historical climate is off course crucial. For the study areas in Bolivia and Thailand, previous studies have investigated the occurrence of temporal trends in temperature and precipitation. For the study area in Cameroon however, as well as for West and Central Africa in general, the availability of instrumental climate data is very restricted. This limits the possibility to relate past climatic variation to changes in tree growth and calls for proxies that allow reconstruction of past climatic conditions. In CHAPTER 3 I assessed the potential use of stable isotopes of oxygen (δ18O) in tree rings as a tool for the reconstruction of precipitation in tropical Africa. I measured δ18O in tree rings of five large Entandrophragmautiletreesfrom North-western Cameroon. A significant negative correlation was found between annual tree-ring δ18O values (averaged over the five individuals) and annual precipitation amount during 1930-2009 in large areas of West and Central Africa. I also found tree-ring δ18O to track sea surface temperatures (SST) in the Gulf of Guinea (1930-2009). These two results are related because rainfall variabilityin West and Central Africa is profoundly influenced by the SST of the tropical AtlanticOcean. Thus a high SST in the Gulf of Guinea is associated with high precipitation over large parts of West and Central Africa and recorded in tree rings by a relatively low δ18O value. On the other hand, dry years when SST is low, are recorded by relatively high tree-ring δ18O values. I also found a significant long-term increase of tree-ring δ18O values. This trend seems to be caused by lowered precipitation from 1970 to 1990 (the Sahel drought period). From 1860 to 1970, no significant long-term trend was observed in tree-ring δ18O values, suggesting no substantial change in precipitation amount occurred over this period. Another potential driver of altered tree growth and biomass in intact tropical forests is the increase of anthropogenic nutrient depositions, especially nitrogen. The deposition of nitrogen has likely risen due to an increased industrialization and use of artificial N fertilizers in most tropical countries. Nitrogen can stimulate plant growth, as is well known from the positive effect of N fertilizer application on crop yields. Previous studies have shown that the stable isotope ratio of nitrogen (δ15N) increased during the last decennia in the wood of trees from Brazil and Thailand as well as in tree leaves from Panama. This increased δ15N has been interpreted as a signal that tropical nitrogen cycles have become more ‘open’ and ‘leaky’ during the last decades in response to increased anthropogenic nitrogen depositions. The underlying mechanism is that high rates of nitrogen deposition and high ambient nitrogen availability lead to an increased nitrification. This process can cause a gradual 15N-enrichment of soil nitrogen. In CHAPTER 4 I analysed changes in tree-ring δ15N values of 400 trees of six species from the three study sites. In the trees from Cameroon no long-term change of tree-ring δ15N values was found (1850-2005), even though NH3and NOxemissions seem to have increased strongly around the study area since 1970. Possibly, the very high precipitation at that site causes the local nitrogen cycle to be already very ‘leaky’, limiting the effect of additional nitrogen input on the δ15N signature of soil nitrogen. Alternatively, nitrogen input in this forest might be much lower than reconstructed NH3and NOxemissions suggest. For the study site in Bolivia, no significant change of tree-ring δ15N values was found (1875-2005), which is in line with the expected result for areas with a low anthropogenic nitrogen input. I found a marginally significant increased of δ15N values since 1950 in trees from Thailand, which confirms previous observations. This points to an effect of increased anthropogenic nitrogen deposition, which could have stimulated photosynthetic rates, if indeed nitrogen was limiting tree growth. The most often hypothesized factor to cause a long-term increase of tree growth is the rise of atmospheric CO2. Since the onset of the industrial revolution (~1850) global atmospheric CO2concentration has increased by 40%. Elevated CO2can directly affect plants by increasing the activity, as well as the efficiency, of the CO2fixing enzyme rubisco and thereby increase photosynthetic rates. Potentially more important in plant communities subjected to periods of limited water availability (like a dry season) is that elevated CO2 can cause a reduction of stomatal conductance, which lowers evapo-transpiration and hence reduces water losses.This increases water-use efficiency (i.e. the amount of carbon gained through photosynthesis divided by the amount of water loss through transpiration) and might allow plants to extend their growth season and/or increase their photosynthetic activity during the hottest hours of the day when water-stress might be severe. Elevated atmospheric CO2is thus a very likely candidate to have stimulated tropical tree growth (also referred to as CO2fertilization), provided at least that plant growth was either carbon or water limited. In CHAPTER 5 I tested the CO2fertilization hypothesis by analysing growth-ring data of 1100 trees from the three study sites. The measurement of tree-ring widths allowed an assessment of historical growth rates, whereas stable carbon isotopes (δ13C) in the wood of the trees were used to obtain an estimate of the CO2concentration in the intercellular spaces in leaves (Ci) and of water-use efficiency (intrinsic water-use efficiency; iWUE). I used a sampling method that controls for ontogenetic (i.e. size developmental) changes in growth and δ13C. With this method, trees were compared across a fixed diameter (i.e. same ontogenetic stage). I chose two diameters: 8 cm (referring to small understorey trees) and 27 cm (referring to larger canopy trees). A mixed-effect model revealeda highly significant and exponential increase of Ciat each of the three sites, and in both understorey and canopy trees. Over the last 150 years Ciincreased by 43% and 53% for understorey and canopy trees respectively. Yet, the rate of increase in Ciwas consistently lower than that of atmospheric CO2. This ‘active’ response to elevated atmospheric CO2resulted in a significant and large increase of iWUE. Over the last 150 years, iWUE increased by 30% and 35% for understorey and canopy trees.A long-term increase of iWUE indicates either a proportional increase of net photosynthesis and/or a decrease of stomatal conductance and thus transpiration, both of which could have stimulated biomass growth. However, I found no increase of tree growth over the last 150 years in any of the sites. Although there are several possible explanations for these findings, I argue that it is most likely that tropical tree growth is generally not limited by water and carbon, but by a persistent nutrient limitation (e.g. of phosphates) and that this has prevented tropical trees to use the extra CO2for an acceleration of growth. In this thesis I have studied environmental and physiological drivers of tree growth changes. I found evidence of decreased precipitation over the last decades at the study site in Cameroon (CHAPTER 3), a changed nitrogen cycle at the study site in Thailand (CHAPTER 4) and an overall change in the physiology of all tree species studied (increased iWUE; CHAPTER 5). One of the main findings of this thesis is however, that these changes have not led to a net change of tree growth over the last 150 years (CHAPTER 5). This is an important finding that could have two major implications. Firstly, the absence of a long-term growth stimulation suggests that the increase of iWUE is mainly driven by a reduced stomatal conductance, which likely leads to a reduced evaporative water loss. If trees across the tropics are reducing evapo-transpiration, this will change affect hydrological cycles, e.g. leading to a lower humidity, higher air temperatures and a reduced precipitation. Secondly, the absence of a growth stimulation over the last 150 years suggests that the carbon sink capacity of tropical forests is currently overestimated, e.g. by Dynamic Global Vegetation Models, which assume strong CO2fertilization effects and as such a high capacity of tropical forests to mitigate global warming. I anticipate that the planned Free Air Concentration Enrichment (FACE) experiments in the tropics will shed light on the reasons why increased CO2does not stimulate the growth rates of tropical trees. Furthermore, I argue that combining tree-ring measurements and stable isotope analyses together with permanent plot research is the most promising way to increase our understanding of the changes in tropical forests

Stable isotopes in tropical tree rings: theory, methods and applications

1. The notion that many tropical tree species form annual growth rings has triggered research on their growth and its environmental drivers over long periods of time. Even more recently, a large number of studies have also analysed the natural abundance of stable isotopes in tropical tree rings. The rapid developments in this young field call for a review. Here, we focus on stable isotopes of carbon (13C), oxygen (18O) and nitrogen (15N).2. We start by explaining how environmental and physiological effects define the isotopic composition of wood in tropical trees. Abundance of 13C is mainly driven by water, light and nutrient availability. Here 18O values are chiefly determined by those of rainwater and additionally by rooting depth and factors determining leaf water evaporation. The 15N levels are determined by the 15N signature of nitrogen uptake, which in turn depends in complex ways on various processes in the nitrogen cycle.3. We then discuss methodological aspects of isotopes studies in tropical tree rings. An important requirement is that rings are reliably dated. Furthermore, a key methodological concern is that temporal changes in isotopic values can be confounded by tree-size driven changes, which can be avoided by sampling from a fixed diameter range or accounted for statistically.4. Next, 50 studies are reviewed that measured stable isotopes of C, O, and/or N in tree rings of a total of 85 tropical tree species. Temporal variation in both δ13C and δ18O was correlated with precipitation and El Niño Southern Oscillation variability. Seasonality in δ13C and δ18O was successfully used for delimiting visually non-distinct annual rings. Tropical tree responses to increasing atmospheric [CO2] were effectively quantified, using δ13C as a measure of intrinsic water use efficiency. And finally, anthropogenic changes in the nitrogen cycle in tropical forests have been inferred from δ15N.5. We conclude with methodological and ecophysiological recommendations for isotope studies in tropical tree rings. Future perspectives include the analysis of intramolecular isotopic distributions of isotopes in glucose that can advance our understanding of environmental effects on tropical tree physiology. Finally, we recommend that tropical tree ring isotope data are deposited in open access databases

Stable isotopes in tropical tree rings: theory, methods and applications

1. The notion that many tropical tree species form annual growth rings has triggered research on their growth and its environmental drivers over long periods of time. Even more recently, a large number of studies have also analysed the natural abundance of stable isotopes in tropical tree rings. The rapid developments in this young field call for a review. Here, we focus on stable isotopes of carbon (13C), oxygen (18O) and nitrogen (15N).2. We start by explaining how environmental and physiological effects define the isotopic composition of wood in tropical trees. Abundance of 13C is mainly driven by water, light and nutrient availability. Here 18O values are chiefly determined by those of rainwater and additionally by rooting depth and factors determining leaf water evaporation. The 15N levels are determined by the 15N signature of nitrogen uptake, which in turn depends in complex ways on various processes in the nitrogen cycle.3. We then discuss methodological aspects of isotopes studies in tropical tree rings. An important requirement is that rings are reliably dated. Furthermore, a key methodological concern is that temporal changes in isotopic values can be confounded by tree-size driven changes, which can be avoided by sampling from a fixed diameter range or accounted for statistically.4. Next, 50 studies are reviewed that measured stable isotopes of C, O, and/or N in tree rings of a total of 85 tropical tree species. Temporal variation in both δ13C and δ18O was correlated with precipitation and El Niño Southern Oscillation variability. Seasonality in δ13C and δ18O was successfully used for delimiting visually non-distinct annual rings. Tropical tree responses to increasing atmospheric [CO2] were effectively quantified, using δ13C as a measure of intrinsic water use efficiency. And finally, anthropogenic changes in the nitrogen cycle in tropical forests have been inferred from δ15N.5. We conclude with methodological and ecophysiological recommendations for isotope studies in tropical tree rings. Future perspectives include the analysis of intramolecular isotopic distributions of isotopes in glucose that can advance our understanding of environmental effects on tropical tree physiology. Finally, we recommend that tropical tree ring isotope data are deposited in open access databases

Tree-ring d18O in African mahogany (Entandrophragma utile) records regional precipitation and can be used for climate reconstructions

The availability of instrumental climate data in West and Central Africa is very restricted, both in space and time. This limits the understanding of the regional climate system and the monitoring of climate change and causes a need for proxies that allow the reconstruction of paleoclimatic variability. Here we show that oxygen isotope values (d18O) in tree rings of Entandrophragma utile from North-western Cameroon correlate to precipitation on a regional to sub-continental scale (1930–2009). All found correlations were negative, following the proposed recording of the ‘amount effect’ by trees in the tropics. The capacity of E. utile to record the variability of regional precipitation is also confirmed by the significant correlation of tree-ring d18O with river discharge data (1944–1983), outgoing longwave radiation (a proxy for cloud cover; 1974–2011) and sea surface salinity in the Gulf of Guinea (1950–2011). Furthermore, the high values in the d18O chronology from 1970 onwards coincide with the Sahel drought period. Given that E. utile presents clear annual growth rings, has a wide-spread distribution in tropical Africa and is long lived (> 250 years), we argue that the analysis of oxygen isotopes in growth rings of this species is a promising tool for the study of paleoclimatic variability during the last centuries in West and Central Africa

Tree-ring d18O in African mahogany (Entandrophragma utile) records regional precipitation and can be used for climate reconstructions

The availability of instrumental climate data in West and Central Africa is very restricted, both in space and time. This limits the understanding of the regional climate system and the monitoring of climate change and causes a need for proxies that allow the reconstruction of paleoclimatic variability. Here we show that oxygen isotope values (d18O) in tree rings of Entandrophragma utile from North-western Cameroon correlate to precipitation on a regional to sub-continental scale (1930–2009). All found correlations were negative, following the proposed recording of the ‘amount effect’ by trees in the tropics. The capacity of E. utile to record the variability of regional precipitation is also confirmed by the significant correlation of tree-ring d18O with river discharge data (1944–1983), outgoing longwave radiation (a proxy for cloud cover; 1974–2011) and sea surface salinity in the Gulf of Guinea (1950–2011). Furthermore, the high values in the d18O chronology from 1970 onwards coincide with the Sahel drought period. Given that E. utile presents clear annual growth rings, has a wide-spread distribution in tropical Africa and is long lived (> 250 years), we argue that the analysis of oxygen isotopes in growth rings of this species is a promising tool for the study of paleoclimatic variability during the last centuries in West and Central Africa

No evidence for consistent long-term growth stimulation of 13 tropical tree species: results from tree-ring analysis

The important role of tropical forests in the global carbon cycle makes it imperative to assess changes in their carbon dynamics for accurate projections of future climate–vegetation feedbacks. Forest monitoring studies conducted over the past decades have found evidence for both increasing and decreasing growth rates of tropical forest trees. The limited duration of these studies restrained analyses to decadal scales, and it is still unclear whether growth changes occurred over longer time scales, as would be expected if CO2-fertilization stimulated tree growth. Furthermore, studies have so far dealt with changes in biomass gain at forest-stand level, but insights into species-specific growth changes – that ultimately determine community-level responses – are lacking. Here, we analyse species-specific growth changes on a centennial scale, using growth data from tree-ring analysis for 13 tree species (~1300 trees), from three sites distributed across the tropics. We used an established (regional curve standardization) and a new (size-class isolation) growth-trend detection method and explicitly assessed the influence of biases on the trend detection. In addition, we assessed whether aggregated trends were present within and across study sites. We found evidence for decreasing growth rates over time for 8–10 species, whereas increases were noted for two species and one showed no trend. Additionally, we found evidence for weak aggregated growth decreases at the site in Thailand and when analysing all sites simultaneously. The observed growth reductions suggest deteriorating growth conditions, perhaps due to warming. However, other causes cannot be excluded, such as recovery from large-scale disturbances or changing forest dynamics. Our findings contrast growth patterns that would be expected if elevated CO2 would stimulate tree growth. These results suggest that commonly assumed growth increases of tropical forests may not occur, which could lead to erroneous predictions of carbon dynamics of tropical forest under climate change