氮磷添加对树木生长和森林生产力影响的研究进展

人为活动所导致的氮、磷输入和大气氮、磷沉降使生态系统中的氮、磷可利用性大幅提高, 对陆地生态系统的碳循环过程产生了显著影响。树木生长和森林生产力在全球碳循环中发挥着重要作用, 它决定着陆地碳固存的大小和方向。目前, 在全球范围内开展了很多氮、磷添加调控树木生长和森林生产力的野外控制实验, 但是研究结果并不一致, 受到多种生物、环境和实验处理条件等因素的影响。该文从野外氮添加和磷添加实验的文献数量、实验数量及其全球空间分布三个方面概述了氮、磷添加对树木生长和森林生产力影响的研究现状, 并总结了氮、磷添加实验中树木生长和森林生产力的评估方法, 包括相对生长速率和绝对增长量。基于相关的研究结果, 阐述了氮、磷添加影响树木生长和森林生产力的调控因素及其潜在影响机制, 包括气候、树木径级与林龄、植物功能性状(共生菌根类型、树木固氮属性和保守性与获得性性状)、植物和微生物相互作用关系、区域养分沉降速率和实验处理条件等。最后, 基于当前的研究进行了系统总结, 并指出今后需要加强的几个方面的研究, 以期为后续研究提供参考: 树木生长响应氮、磷添加的生理学机制, 树木各部分生长对氮、磷添加响应的权衡与分配, 植物功能性状在调节与预测树木生长响应氮、磷添加中的作用, 树木之间的竞争关系如何调控氮、磷添加对树木生长的影响, 以及开展长期的和联网的氮、磷添加对树木生长和森林生产力影响的野外控制实验。     

A review on the effects of nitrogen and phosphorus addition on tree growth and productivity in forest ecosystems

Nitrogen (N) and phosphorus (P) inputs induced by anthropogenic activities and atmospheric N and P deposition have largely increased the availability of soil N and P in terrestrial ecosystems, which have considerably affected terrestrial carbon cycling processes. Tree growth and productivity in forest ecosystems play an important role in global carbon cycling, and determine the magnitude and direction of terrestrial carbon sequestration. Currently, a large number of field manipulation experiments have been conducted to investigate the effects of N and/or P addition on tree growth and forest productivity, but the results from these studies were inconsistent. Such inconsistent results might be affected by multiple factors, including biological, environmental and experimental variables. Here, we reviewed the present research status of the effects of N and P addition on tree growth and forest productivity in forest ecosystems based on three aspects, including the number of publications and experiments with field N and P addition, and the global distributions of these experiments. Then, we summarized the methods for assessing tree growth and forest productivity at ecosystem level in forest ecosystems, including relative growth rate and absolute increment. According to the related results, we reviewed the regulating factors that affect tree growth and productivity, and the potential mechanisms for such factors, including climate, tree size and stand age, plant functional traits (including type of tree-associated mycorrhizal fungi, N-fixation property of trees, and conservative and acquisitive functional traits), plant-microbe interaction, ambient nutrient (i.e., N and P) deposition rate, and experimental variables. Finally, we summarized the current studies, and pointed out five aspects that are urgently needed to provide further insights in future studies, including the physiological mechanism of how tree growth responds to N and P addition, the tradeoff and allocation among growth of various parts of tree under N and P addition, the role of plant functional traits in regulating and predicting the responses of tree growth to N and P addition, how the competition among trees regulates the responses of tree growth to N and P addition, and conducting long-term and coordinated distributed field experiments investigating the effects of N and P addition on tree growth and forest productivity at the global scale.     

Interpreting tree responses to thinning and fertilization using tree-ring stable isotopes

? Carbon sequestration has focused renewed interest in understanding how forest management affects forest carbon gain over timescales of decades, and yet details of the physiological mechanisms over decades are often lacking for understanding long-term growth responses to management. ? Here, we examined tree-ring growth patterns and stable isotopes of cellulose (δ(13)C(cell) and δ(18)O(cell)) in a thinning and fertilization controlled experiment where growth increased substantially in response to treatments to elucidate physiological data and to test the dual isotope approach for uses in other locations. ? δ(13)C(cell) and δ(18)O(cell) results indicated that fertilization caused an increase in intrinsic water-use efficiency through increases in photosynthesis (A) for the first 3 yr. The combination treatment caused a much larger increase in A and water-use efficiency. Only the thinning treatments showed consistent significant increases in δ(18)O(cell) above controls. Changes in canopy microclimate are the likely drivers for δ(18)O(cell) increases with decreases in relative humidity and increases in leaf temperature associated with thinning being the most probable causes. ? Tree-ring isotopic records, particularly δ(13)C(cell), remain a viable way to reconstruct long-term physiological mechanisms affecting tree carbon gain in response to management and climate fluctuations.     

Tree-ring responses in Araucaria araucana to two major eruptions of Lonquimay Volcano (Chile)

Palaeoclimate proxies have demonstrated links between climate changes and volcanic activity. However, not much is known about the impact of volcanic eruptions on forest productivity. Here we used tree-ring width and annually resolved carbon and oxygen isotopic records from tree rings of Araucaria araucana (Molina) K. Koch, providing a centennial-scale reconstruction of tree ecophysiological processes in forest stands nearby the Lonquimay Volcano (Chile). We observed a mean decrease in tree-ring width following the major eruption of 1988–1990 (with aerosol emission), most probably caused by the modified ecological conditions due to acid rain and ash deposition, while a generally negative relationship between δ¹³C and δ¹⁸O would point to a decline in humidity and precipitation. More negative δ¹³C and lower δ¹⁸O values (positive correlation) following the major eruption of 1887–1890 (without aerosol emission) would suggest high stomatal conductance and moisture availability, though tree-ring width (and probably photosynthetic rate) was unaltered. At least for this sample of trees, in the case of eruption with large tephra emission, the beneficial effect of aerosol light scattering on tree productivity appears to be outweighed by the detrimental effect of eruption-induced toxic deposition. Signals of the two major eruptions of the past 200?years at Lonquimay were present in tree rings of nearby A. araucana. No unique response of tree functions to volcanic eruptions can be expected, but rather (1) the variable volcanic properties and (2) the complex interplay of diffuse light increase (aerosol scattering), air temperature decrease (cloud shading), and toxic deposition impact (volcanic ash), makes any prediction of tree growth and ecophysiological response very challenging.     

Linking drought legacy effects across scales: From leaves to tree rings to ecosystems

Severe drought can cause lagged effects on tree physiology that negatively impact forest functioning for years. These “drought legacy effects” have been widely documented in tree‐ring records and could have important implications for our understanding of broader scale forest carbon cycling. However, legacy effects in tree‐ring increments may be decoupled from ecosystem fluxes due to (a) postdrought alterations in carbon allocation patterns; (b) temporal asynchrony between radial growth and carbon uptake; and (c) dendrochronological sampling biases. In order to link legacy effects from tree rings to whole forests, we leveraged a rich dataset from a Midwestern US forest that was severely impacted by a drought in 2012. At this site, we compiled tree‐ring records, leaf‐level gas exchange, eddy flux measurements, dendrometer band data, and satellite remote sensing estimates of greenness and leaf area before, during, and after the 2012 drought. After accounting for the relative abundance of tree species in the stand, we estimate that legacy effects led to ~10% reductions in tree‐ring width increments in the year following the severe drought. Despite this stand‐scale reduction in radial growth, we found that leaf‐level photosynthesis, gross primary productivity (GPP), and vegetation greenness were not suppressed in the year following the 2012 drought. Neither temporal asynchrony between radial growth and carbon uptake nor sampling biases could explain our observations of legacy effects in tree rings but not in GPP. Instead, elevated leaf‐level photosynthesis co‐occurred with reduced leaf area in early 2013, indicating that resources may have been allocated away from radial growth in conjunction with postdrought upregulation of photosynthesis and repair of canopy damage. Collectively, our results indicate that tree‐ring legacy effects were not observed in other canopy processes, and that postdrought canopy allocation could be an important mechanism that decouples tree‐ring signals from GPP.     

Comparison of whole wood and cellulose carbon and oxygen isotope series from Pinus nigra ssp. laricio (Corsica/France)

Stable isotopes in tree rings have widely been used for palaeoclimate reconstructions since tree rings record climatic information at annual resolution. However, various wood components or different parts of an annual tree-ring may differ in their isotopic compositions. Thus, sample preparation and subsequent laboratory analysis are crucial for the isotopic signal retained in the final tree-ring isotope series used for climate reconstruction and must therefore be considered for the interpretation of isotope–climate relationships. This study focuses on wood of Corsican Pine trees (Pinus nigra ssp. laricio) as this tree species allows to reconstruct the long-term climate evolution in the western Mediterranean. In a pilot study, we concentrated on methodological issues of sample preparation techniques in order to evaluate isotope records measured on pooled whole tree-ring cellulose and whole tree-ring bulk wood samples. We analysed 80-year long carbon and oxygen chronologies of Corsican Pine trees growing near the upper tree line on Corsica. Carbon and oxygen isotope records of whole tree-ring bulk wood and whole tree-ring cellulose from a pooled sample of 5 trees were correlated with the climate parameters monthly precipitation, temperature and the self-calibrating Palmer Drought Severity Index (sc-PDSI). Results show that the offsets in carbon and oxygen isotopes of bulk wood and cellulose are not constant over time. Both isotopes correlate with climate parameters from late winter and summer. The carbon and oxygen isotope ratios of cellulose are more sensitive to climatic variables than those of bulk wood. The results of this study imply that extraction of cellulose is a pre-requisite for the reconstruction of high-resolution climate records from stable isotope series of P. nigra ssp. laricio.     

北京东灵山辽东栎林树木生长对气候要素的响应特征

根据北京东灵山辽东栎(Quercus wutaishanica)的年轮宽度资料,分析了该地区树木生长在1951—2010年时段对气候要素的响应特征。相关分析表明,夏季干旱胁迫是限制东灵山辽东栎树木生长的最为重要的气候要素,主要体现在与夏季(7—9月)温度的负相关关系和夏季降雨(7月)的正相关关系,另外春季(5月)温度对树木生长也有一定的限制性影响;年表与生长季节干旱指数普遍呈正相关关系,进一步证实了干旱胁迫对树木生长的限制性作用。滑动相关分析表明,年表与夏季温度负相关关系及与夏季降雨的正相关关系在近期趋于增强,这表明夏季干旱胁迫对树木生长影响作用有不断加强的趋势。辽东栎林是北京东灵山温带落叶阔叶林的优势群落,在暖干化气候不断发展背景下,辽东栎林生长的干旱胁迫效应将更加突出,对北京东灵山地区森林的生产力及固碳能力产生负面影响。     

森林生态系统碳循环对全球氮沉降的响应

森林土壤和植被储存着全球陆地生态系统大约46%的碳,在全球碳平衡中起着非常重要的作用。过去几十年来,森林生态系统的碳循环和碳吸存受到了全球氮沉降的深刻影响,因为氮沉降改变了陆地生态系统的生产力和生物量积累。以欧洲和北美温带森林区域开展的研究为基础,综述了氮沉降对植物光合作用、土壤呼吸、土壤DOM及林木生长的影响特征和机理,探讨了森林生态系统碳动态对氮沉降响应的不确定性因素。热带森林C、N循环与大部分温带森林不同,人为输入的氮对热带生态系统过程的影响也可能不同,因此指出了在热带地区开展碳氮循环耦合研究的必要性和紧迫性。     

Toward consistent measurements of carbon accumulation: A multi-site assessment of biomass and basal area increment across Europe

The use of tree-ring data in carbon cycle research has so far been limited because traditional study designs are not geared toward quantifying forest carbon accumulation. Existing studies that assessed biomass increment from tree rings were often confined to individual sites and used inconsistent sampling schemes. We applied a consistent biomass-oriented sampling design at five managed forest sites located in different climate zones to assess the annual carbon accumulation in above-ground woody tissues (i.e. stems and branches) and its climate response. Radial growth and biometric measurements were combined to reconstruct the annual biomass increment in individual trees and upscaled to the site level. In addition to this, we estimated that 32–60 trees are required at these five sites to robustly quantify carbon accumulation rates. Tree dimensions and growth rates varied considerably among sites as a function of differing stand density, climatic limitations, and management interventions. Accordingly, mean site-level carbon accumulation rates between 65 g C m⁻² y⁻¹ and 225 g C m⁻² y⁻¹ were reconstructed for the 1970–2009 period. A comparison of biomass increment with the widely used basal area increment (BAI) revealed very similar growth trends but emphasized the merits of biomass assessments due to species-specific BAI/biomass relationship. Our study illustrates the benefits and challenges of combining tree-ring data with biometric measurements and promotes the consistent application of a standardized sampling protocol across large spatial scales. It is thus viewed as a conceptual basis for future use of tree-ring data to approach research questions related to forest productivity and the terrestrial carbon balance.     

Does Forest Continuity Enhance the Resilience of Trees to Environmental Change?

There is ample evidence that continuously existing forests and afforestations on previously agricultural land differ with regard to ecosystem functions and services such as carbon sequestration, nutrient cycling and biodiversity. However, no studies have so far been conducted on possible long-term (>100 years) impacts on tree growth caused by differences in the ecological continuity of forest stands. In the present study we analysed the variation in tree-ring width of sessile oak (Quercus petraea (Matt.) Liebl.) trees (mean age 115–136 years) due to different land-use histories (continuously existing forests, afforestations both on arable land and on heathland). We also analysed the relation of growth patterns to soil nutrient stores and to climatic parameters (temperature, precipitation). Tree rings formed between 1896 and 2005 were widest in trees afforested on arable land. This can be attributed to higher nitrogen and phosphorous availability and indicates that former fertilisation may continue to affect the nutritional status of forest soils for more than one century after those activities have ceased. Moreover, these trees responded more strongly to environmental changes – as shown by a higher mean sensitivity of the tree-ring widths – than trees of continuously existing forests. However, the impact of climatic parameters on the variability in tree-ring width was generally small, but trees on former arable land showed the highest susceptibility to annually changing climatic conditions. We assume that incompletely developed humus horizons as well as differences in the edaphon are responsible for the more sensitive response of oak trees of recent forests (former arable land and former heathland) to variation in environmental conditions. We conclude that forests characterised by a long ecological continuity may be better adapted to global change than recent forest ecosystems.     

Long-term growth decline in Toona ciliata in a moist tropical forest in Bangladesh: Impact of global warming

Tropical forests are carbon rich ecosystems and small changes in tropical forest tree growth substantially influence the global carbon cycle. Forest monitoring studies report inconsistent growth changes in tropical forest trees over the past decades. Most of the studies highlighted changes in the forest level carbon gain, neglecting the species-specific growth changes which ultimately determine community-level responses. Tree-ring analysis can provide historical data on species-specific tree growth with annual resolution. Such studies are inadequate in Bangladesh, which is one of the most climate sensitive regions in the tropics. In this study, we investigated long-term growth rates of Toona ciliata in a moist tropical forest of Bangladesh by using tree-ring analysis. We sampled 50 trees of varying size, obtained increment cores from these trees and measured tree-ring width. Analyses of growth patterns revealed size-dependent growth increments. After correcting for the effect of tree size on tree growth (ontogenetic changes) by two different methods we found declining growth rates in T. ciliata from 1960 to 2013. Standardized ring-width index (RWI) was strongly negatively correlated with annual mean and maximum temperatures suggesting that rising temperature might cause the observed growth decline in T. ciliata. Assuming that global temperatures will rise at the current rate, the observed growth decline is assumed to continue. The analysis of stable carbon and oxygen isotopes may reveal more insight on the physiological response of this species to future climatic changes.     

Cambial Growth Season of Brevi-Deciduous Brachystegia spiciformis Trees from South Central Africa Restricted to Less than Four Months

We investigate cambial growth periodicity in Brachystegia spiciformis, a dominant tree species in the seasonally dry miombo woodland of southern Africa. To better understand how the brevi-deciduous (experiencing a short, drought-induced leaf fall period) leaf phenology of this species can be linked to a distinct period of cambial activity, we applied a bi-weekly pinning to six trees in western Zambia over the course of one year. Our results show that the onset and end of cambial growth was synchronous between trees, but was not concurrent with the onset and end of the rainy season. The relatively short (three to four months maximum) cambial growth season corresponded to the core of the rainy season, when 75% of the annual precipitation fell, and to the period when the trees were at full photosynthetic capacity. Tree-ring studies of this species have found a significant relationship between annual tree growth and precipitation, but we did not observe such a correlation at intra-annual resolution in this study. Furthermore, a substantial rainfall event occurring after the end of the cambial growth season did not induce xylem initiation or false ring formation. Low sample replication should be taken into account when interpreting the results of this study, but our findings can be used to refine the carbon allocation component of process-based terrestrial ecosystem models and can thus contribute to a more detailed estimation of the role of the miombo woodland in the terrestrial carbon cycle. Furthermore, we provide a physiological foundation for the use of Brachystegia spiciformis tree-ring records in paleoclimate research.     

北亚热带马尾松年轮宽度与NDVI的关系

北亚热带地处暖温带向亚热带的过渡地区,对环境变化较为敏感。因此,研究北亚热带马尾松年轮宽度与森林NDVI的关系对于揭示陆地生态系统对全球气候变化的响应具有重要意义。以马尾松自然分布北界的南郑县和河南省鸡公山自然保护区为研究地点,利用北亚热带马尾松年轮宽度指数和1982-2006年逐月NOAA/AVHRR的归一化植被指数(NDVI)数据及气候数据,在分析年轮宽度及NDVI与气候因子关系的基础上,重点讨论了北亚热带马尾松径向生长与NDVI之间的关系。结果表明:北亚热带NDVI受水热条件的共同控制,其中与月均温相关性较强,且以正相关为主,与月降水量和干旱度指数多负相关;马尾松的径向生长与上一生长季的温度呈正相关,降水和干旱度指数为负相关,当年生长季内的温度和降水以促进作用为主,而与干旱度指数的关系在两地区内相反;南郑县和鸡公山地区年轮宽度与NDVI年值之间关系均不显著(P>0.05)。单月来讲,南郑县3、4、12月NDVI值与年表显著相关,鸡公山地区9月份的NDVI值与差值年表RES相关性最大;南郑县树木生长受温度影响最大,而鸡公山地区受温度和降水的综合作用。因此,在北亚热带地区,长时间序列的年轮宽度数据并不能很好反应NDVI的长期变化,利用树轮宽度指数来重建北亚热带地区NDVI需要进一步研究。     

Growth decline of Pinus Massoniana in response to warming induced drought and increasing intrinsic water use efficiency in humid subtropical China

Pinus Massoniana is the most widely distributed coniferous species in southern China and one of the most distributed species for plantation in China. It is not uncertain about the responses of tree growth to the combined effects of regional drying and the increase in the intrinsic water-use efficiency (iWUE) due to increased atmospheric CO₂. This study addressed this issue by comparing the tree growth patterns as represented by three tree-ring width chronologies with climate variables and three iWUE series derived from three tree-ring stable carbon isotope discrimination chronologies (Δ¹³C) from Pinus Massoniana in Daiyun Mountain, central Fujian province of China. Among these chronologies, we reported the first tree-ring carbon isotope discrimination chronologies (Δ¹³C) from Fuzhou area spanning last 210 years. It was found that tree radial growth is mainly limited by dry condition from May to October. Growth limitation by cold condition was only found in one high altitude site (780m) in early spring and late autumn. The tree-ring carbon discrimination was enhanced under conditions with low relative humidity and sufficient sunshine in late summer and autumn. In general, the iWUE showed a significantly increasing trend since the 1850s for all the sites in response to the increase in atmospheric CO₂. However, the growth promotion of the increased iWUE on tree growth could not compensate the growth limitation caused by drought. Especially since the 1960s, a growth decline was found at two drought stressed sites at low altitudes. On the other hand, the increase in temperature of spring and autumn and iWUE has most likely enhanced tree growth at the high altitude site.     

Drivers of aboveground wood production in a lowland tropical forest of West Africa: teasing apart the roles of tree density,tree diversity,soil phosphorus,and historical logging

Tropical forests currently play a key role in regulating the terrestrial carbon cycle and abating climate change by storing carbon in wood. However, there remains considerable uncertainty as to whether tropical forests will continue to act as carbon sinks in the face of increased pressure from expanding human activities. Consequently, understanding what drives productivity in tropical forests is critical. We used permanent forest plot data from the Gola Rainforest National Park (Sierra Leone) – one of the largest tracts of intact tropical moist forest in West Africa – to explore how (1) stand basal area and tree diversity, (2) past disturbance associated with past logging, and (3) underlying soil nutrient gradients interact to determine rates of aboveground wood production (AWP). We started by statistically modeling the diameter growth of individual trees and used these models to estimate AWP for 142 permanent forest plots. We then used structural equation modeling to explore the direct and indirect pathways which shape rates of AWP. Across the plot network, stand basal area emerged as the strongest determinant of AWP, with densely packed stands exhibiting the fastest rates of AWP. In addition to stand packing density, both tree diversity and soil phosphorus content were also positively related to productivity. By contrast, historical logging activities negatively impacted AWP through the removal of large trees, which contributed disproportionately to productivity. Understanding what determines variation in wood production across tropical forest landscapes requires accounting for multiple interacting drivers – with stand structure, tree diversity, and soil nutrients all playing a key role. Importantly, our results also indicate that logging activities can have a long‐lasting impact on a forest's ability to sequester and store carbon, emphasizing the importance of safeguarding old‐growth tropical forests.     

IncrementR: Analysing height growth of trees and shrubs in R

Dendrochronology mostly deals with secondary (radial) growth and attention to primary (height) growth has so far been limited. However, tree-ring widths might not adequately represent stem volume increments, net primary productivity and the size of the tree stem carbon sink. The main reason for the prevailing focus on radial growth is that establishing height growth chronologies requires time-consuming and destructive methods. However, for certain ecological applications, less laboriously acquired data on height growth averaged over several successive years are satisfactory. Here we present an R package that contains a set of tools for the analysis of height growth. The tools have been developed for input data of tree-ring widths extracted from series of successive stem height levels. Tree-ring widths ideally represent four directions in each cross section to capture potential changes in stem eccentricity between various height levels. The main computed parameters provided by the package include height growth along the stem, changes of stem eccentricity and stem taper. Accurate determination of average height growth depends on the correct estimation of the number of tree rings at different stem height levels, which might be complicated by missing rings in off-pith cores. The presented package therefore also contains functions implementing common procedures for the estimation of the number of missing tree rings near to the pith. Most outputs can be visualized graphically. The package is useful for estimating height growth in ecological and dendrogeomorphological studies, especially in situations where both primary and secondary growth is influenced by different environmental factors. It is also useful for analysing tree-ring chronologies assembled using serial sectioning, which typically applies to shrubs.     

Responses of radial growth and stable carbon isotopes to climate in the northern Tianshan Mountains

Climate change has profound effects on forest ecosystems. Schrenk spruce (P. schrenkiana) is a natural conifer species endemic to the arid inland areas of Asia. In this study, the relationship between tree-ring parameters of P. schrenkiana and major meteorological factors were analyzed, and the main limiting factors for tree radial growth and stable carbon isotope fractionation were explored. Our results indicate that moisture stress before and during the growing season have an important influence on radial growth of P. schrenkiana, especially, the correlation coefficient between tree-ring width and vapor pressure deficit (VPD) from previous August to current July is as high as −0.622 (n = 51, p < 0.01). Collinearity analysis further supports the conclusion that the limiting factor for the radial growth of P. schrenkiana is moisture. Although the correlation analysis results show that the tree-ring δ¹³C_corr is significantly positively correlated with sunshine duration (SD), additional analysis based on first order difference variables suggests that the climate factor may not be the only limiting factor for the stable carbon isotope fractionation of tree rings in the Sayram Lake Basin. This lays the foundation for the assessment of forest management practices and carbon sink capacity in light of future climate change.     

Evaluating the annual nature of juvenile rings in Bolivian tropical rainforest trees

Knowledge on juvenile tree growth is crucial to understand how trees reach the canopy in tropical forests. However, long-term data on juvenile tree growth are usually unavailable. Annual tree rings provide growth information for the entire life of trees and their analysis has become more popular in tropical forest regions over the past decades. Nonetheless, tree ring studies mainly deal with adult rings as the annual character of juvenile rings has been questioned. We evaluated whether juvenile tree rings can be used for three Bolivian rainforest species. First, we characterized the rings of juvenile and adult trees anatomically. We then evaluated the annual nature of tree rings by a combination of three indirect methods: evaluation of synchronous growth patterns in the tree- ring series, ¹⁴C bomb peak dating and correlations with rainfall. Our results indicate that rings of juvenile and adult trees are defined by similar ring-boundary elements. We built juvenile tree-ring chronologies and verified the ring age of several samples using ¹⁴C bomb peak dating. We found that ring width was correlated with rainfall in all species, but in different ways. In all, the chronology, rainfall correlations and ¹⁴C dating suggest that rings in our study species are formed annually.