Ages and long-term growth patterns of four threatened Vietnamese tree species
Conservation of threatened tree species requires basic information on growth rates and ages. This information is lacking for many species, but can be obtained relatively easily from tree ring analysis. We studied four threatened Vietnamese species: three conifers from high-elevation forests (Calocedrus macrolepis, Dacrydium elatum and Pinuskwangtungensis) and one broad-leaved species from lowland forest (Annamocarya sinensis). We collected increment cores from remnant populations in protected areas and measured ring width. We built chronologies and found significant correlations with rainfall (all species) and temperature (two species), indicating that rings were formed annually. Diameter-age trajectories showed that species reached reproductive size at 60–80 years. Maximum observed ages were 128–229 years. Some species showed large variation in long-term growth rates among individuals, which was partially explained by strong persistence of growth differences. We also assessed whether growth rates changed over time. For certain size categories in some species, we found higher recent growth rates of juvenile trees compared to those in the distant past. This shift requires a cautious interpretation, but is consistent with a CO2 fertilization effect. For other size categories, we found contrasting results: extant large trees had higher growth rates as small juveniles compared to extant small trees. Such correlations, which we found for all species, suggest a ‘juvenile selection effect’: the preferential survival of fast-growing juveniles to the canopy. Information on ages, historical growth rates and juvenile selection effect is relevant for the planning of conservation actions.
KeywordsAutocorrelated growth Dendroecology Juvenile selection effect Threatened species Tree age Vietnam
Deforestation, overexploitation and forest fragmentation in southeast Asia have led to dramatic population declines of thousands of tree species (Sodhi et al. 2004). As a consequence, a large number of tropical Asian tree species has now been included in the IUCN red list (IUCN 2009). To design effective conservation measures for these species, basic knowledge on their ecology and life history is required (Schemske et al. 1994). For instance, information is required on the ages at which they reach reproductive size, maximum ages, long-term growth rates and responses to climatic variability and changes. Tree ring analysis can assist in obtaining such basic information, as it allows the lifetime reconstruction of growth rates of individual trees (Roig et al. 2005; Brienen and Zuidema 2006; Newton 2007; Soliz-Gamboa et al. 2010). Tree ring data obtained from increment cores can be obtained without harming trees, and is therefore particularly suitable for the study of threatened tree species (e.g., Buckley et al. 2007). Compared to permanent plot studies, tree ring analysis is a low-cost tool that requires much less investment of research time. Yet, surprisingly few dendro-ecological studies have been conducted on threatened tree species (Devall et al. 1998; Roig et al. 2005; Lisi et al. 2008).
Although the field of tropical dendro-ecology is relatively young, recent studies have yielded interesting ecological insights that are relevant to understanding the dynamics of threatened tree species (Rozendaal and Zuidema 2010). For instance, it was shown that individual growth trajectories might differ strongly and persistently among individuals (Brienen et al. 2006, 2010), suggesting that variation in environmental conditions of trees (perhaps in combination with genetic differences) may have a lasting impact on growth. Such persistent growth differences may have important consequences for population dynamics and conservation (e.g., Zuidema et al. 2009). A study by Rozendaal et al. (2010a) found that extant large individuals (that have reached the canopy) were the relatively faster growers in the past as a juvenile, a finding that had been observed earlier in temperate forest species (Landis and Peart 2005). A final recent finding is that growth rates in some Bolivian tree species have increased over the last one to two centuries, perhaps as a result of climatic changes (Rozendaal et al. 2010a). Such long-term growth patterns are of importance in understanding the drivers of tree growth in (threatened) tree species.
In this study, we investigated the ages and long-term growth patterns of four threatened tree species in Vietnam (Chien et al. 2008). As a result of large-scale deforestation and unsustainable forest exploitation, over 300 tree species in Vietnam are threatened (Chien 2006). Relict populations often occur in national parks or in remote, hilly areas. We were specifically interested in obtaining relevant information on ages and long-term growth rates of threatened tree species. To this end, we determined the maximum observed age and age at first reproduction of our study species. Furthermore, we reconstructed individual growth trajectories and analyzed to what extent growth rates were autocorrelated over time, meaning that fast growers remained fast growers and slow growers remained slow growers. Next, we checked for gradual changes in diameter growth over time, and compared diameter growth rates obtained from ring analysis with values from permanent sample plots (Chien et al. 2008). To our knowledge, this is one of the first dendro-ecological studies for tropical Asian species (Baker et al. 2005; Buckley et al. 2007) and the first of its kind on threatened tree species.
Materials and methods
Study site and species
Characteristics of study species and field sites
Maximum height (m)
Maximum DBH (cm)
Maximum age (year)
Reproductive age (year)
Canopy height (m)
Annamocarya sinensis (Dode) Leroy (Juglandaceae)
Cuc Phuong (21°N–105°E)
Calocedrus macrolepis Kurz (Cupressaceae)
Ba Vi (21°N–105° E)
Dacrydium elatum (Roxb) Wall ex Hook (Podocarpaceae)
Bach Ma (16°N–107°E)
Pinus kwangtungensis Chun ex Tsiang (Pinaceae)
Hang Kia –Pa Co (20°N–104°E)
The precipitation is high in the four study areas: around 2,000 mm year−1 in Ba Vi, Cuc Phuong and Hang kia-Pa Co, and more than 3,000 mm year−1 in Bach Ma. In all four areas, rainfall is not evenly distributed over the year. The dry season is rather pronounced in all areas with 5 dry months (<100 mm mo−1) in Ba Vi, 6 in Cuc Phuong and Hang Kia-Pa Co and 3 in Bach Ma.
We studied four Vietnamese tree species: Annamocarya sinensis, Calocedrus macrolepis, Dacrydium elatum and Pinus kwangtungensis (hereafter referred to by their genus names). All four species are long-lived and reach the forest canopy when mature. Three species (Calocedrus, Dacrydium and Pinus) are conifers, while Annamocarya is a broad-leaved deciduous species. The coniferous species grow in subtropical forests in high mountains, while the broad-leaved Annamocarya occurs in lowland tropical forests. Several characteristics of the four species and their field sites are described in Table 1.
For the demographic study, we established permanent plots at the study sites in 2003. The following measurements were taken for all individuals >1 diameter at breast height (DBH), total height and signs of reproduction (flowers, fruits). These measurements were repeated in 2004 and 2005 (Chien et al. 2008). The relation between reproductive status and DBH was analyzed using logistic regression; this yielded the probability of reproduction for each DBH (results presented in Chien et al. 2008).
Descriptive statistics of the tree ring chronology of four Vietnamese tree species
No. of radii in chronology (total no. of radii)
Mean ring width (mm)
Variance first eigenvector (%)
All cores were sanded until we could clearly identify the rings. Ring boundaries were identified visually by a magnifier. Ring widths were measured to the nearest 0.1 mm. When the cores did not include the tree pith, the distance to the pith was estimated using the average number of rings of the other samples of the same species. In this way, we obtained an estimate of the number of missing rings. However, often cores taken from hollow trees or cores that deviated far from the pith were eliminated. For the trees having two cores, the average values of these cores were taken to describe average diameter increment. In total, we obtained and measured 30 cores for Annamocarya, 28 for Calocedrus, 42 for Dacrydium and 26 for Pinus (Table 2).
To examine the relationship between climate of the study sites and tree growth for the four species, meteorological data were collected. Annual rainfall data were obtained from the following meteorological stations: Nho Quan for Annamocarya, Son Tay for Calocedrus, Nam Dong for Dacrydium, and Mai Chau for Pinus. Annual temperature data were collected from Lang station for Anamocarya and Calocedrus, Hue station for Dacrydium and Hoa Bihn station for Pinus.
Dendrochronological data analysis
For each species, we first checked ring series of all trees for measurement errors (wedging or missing rings) by correlating the series in COFECHA (Grissino-Mayer 2001). Tree ring series that showed strong correlation with each other were selected to establish a chronology. For this purpose, the raw ring series were standardized with a negative exponential curve or negative linear function using ARSTAN (Cook and Holmes 1985). These standardized series were then correlated to the total annual rainfall and average annual temperature (Pearson correlations).
Tree growth analyses
To assess to the extent which growth differences among individuals persisted over time, we correlated the ranks of growth rates across diameter categories. For this purpose, we first calculated the average growth rate of 5-cm diameter categories for each individual (i.e., for 0−5, 5−10, 10−15 cm, etc.) to obtain a data set of average growth in 5-cm categories. Using this data set, we calculated the extent to which the ranks of individuals in terms of growth rates in a particular size category were correlated with those in the successive categories. We performed Spearman correlations among all size categories that contained >10 individuals.
The second analysis of growth patterns involved a test for historical changes in growth rates. To this end, we calculated the average growth rate per 2-cm diameter category and for each section we also determined the average diameter and the average year of ring formation. The latter was transformed to year before present (YBP), with 2005 as the reference year. We then correlated average growth in each category to the year before present (YBP) to test for historical changes in growth rates. Negative correlations are an indication for a historical growth increase (Rozendaal et al. 2010a).
Similar correlations were performed between average growth rate per 2-cm diameter category and the present-day diameter of trees. For example, average growth in the 0–2 cm diameter category for all individuals was correlated with extant diameter of these individuals. Positive correlations between growth rate and extant diameter were indications that a tree with a high extant DBH had a higher growth rate in the specific diameter category. Repeating the analyses with 5-cm diameter categories instead of 2-cm categories yielded very similar results.
A third analysis involved the comparison of diameter growth obtained from tree ring data with those from permanent plots (Chien et al. 2008). We only used tree ring data from trees >30-cm diameter, as these are mostly well-established adult trees. In this way, we were able to check whether juvenile growth rates of extant large trees were higher than those of present-day juvenile trees. The differences in the way the data were obtained did not allow to statistically test for differences as tree ring data are repeated over size categories while plot data are not. However, a qualitative comparison could be made.
Results of tree ring analysis
Rings of the four study species were found to be sufficiently clear for marking and counting. For each of the four study species a standardized tree ring chronology was created using ARSTAN. Descriptive statistics of the chronology are included in Table 2.
Year-to-year variation in ring width of all species significantly correlated with total annual rainfall in the year of ring formation: Annamocarya (R2 = 0.57, P < 0.01), Calocedrus (R2 = 0.15, P < 0.05), Dacrydium (R2 = 0.21, P < 0.05) and Pinus (R2 = 0.23, P < 0.01). We also found significant negative correlations between ring width and average annual temperature for Calocedrus (R2 = 0.12, P < 0.05) and Pinus (R2 = 0.27, P < 0.01), but not for Anamocarya and Dacrydium. In all, clarity of the rings produced and the correlation of ring widths with annual climate data provides support for the annual nature of the growth rings.
Age-diameter relationships and autocorrelated growth
Growth trajectories were very similar for Calocedrus individuals, leading to a low degree of variation in ages on reaching reproductive diameter. A contrasting pattern was observed for Annamocarya for which individual growth trajectories strongly varied, resulting in high age variability on reaching reproductive size and the typical fan-shaped figure (see Fig. 1a). Pinus and Dacrydium showed an intermediate degree of variation across individuals. Another observation that can be made based on these growth trajectories is that for Annamocarya and Dacrydium, fast-growing trees tend to remain the faster growers over several decades, while in the other two species, individual growth curves tend to show more crossing over.
The results of these autocorrelation analyses show that ranks in growth rate are very often maintained over one or two 5-cm diameter categories (Fig. 2). Thus, growth differences persisted at least for one or two decades for all species. In Annamocarya and Dacrydium, growth differences persisted over more diameter categories, with positive rank correlations extending from the 5–10 cm category onwards. Such correlations imply that growth differences were persistent for many decades.
Historical versus recent growth rates
Age estimates and climate-growth relations
Maximum observed ages of our study species ranged from 130 to 230 years, while estimated maximum ages based on growth trajectories and the largest observed diameter were >200 years for all species and >300 years for Calocedrus. These maximum ages are within the range of published ages based on ring counts for (sub)tropical tree species (Martinez-Ramos and Alvarez-Buylla 1998, Rozendaal et al. 2010).
The average diameter at which reproduction starts varied quite strongly among species, from 18 to 34 cm, but in all species this size was reached at comparable ages of 60–80 years. These observed ages are in accordance with previously published age estimates based on matrix models (Chien et al. 2008), but low compared to some other (sub)tropical tree species (e.g., Zuidema and Boot 2002). While the age at reaching reproductive size is low, very few seedlings reach that age. For our study species, the survival probability of a seedling to reach 60 years was estimated to be <0.1% for Calocedrus and <1% for the other three species (Chien et al. 2008). Therefore, conservation efforts that increase this success rate likely have a large impact on population growth.
The long reproductive period of our study species provides some security for long-term maintenance of the small relict populations of our study species. Yet, demographic analyses conducted so far suggest population decline for these and other threatened tree species in Vietnam (Chien et al. 2008; Zuidema et al. 2010). In this context, any conservation effort that prevents anthropogenic mortality of juvenile and adult trees will likely have a positive effect on the resilience of these populations.
Long-term growth patterns
We found that differences in growth rates among individuals tended to persist for one or several decades in most size categories for all species. Thus, fast growers tend to remain fast growers and slow growers tend to remain slow growers. For Annamocarya and Dacrydium, growth differences were often maintained over various size classes, implying that they persisted for several decades and probably for >60 years. These results are in accordance with those from a number of recent studies in which persistent growth differences were reported over short (<10 years, e.g., Grogan and Landis 2009) to long timescales (Brienen et al. 2006, 2010). It is likely that persistent growth differences are commonplace in (tropical) tree species, although the degree of growth differences and the degree of persistence likely differs across species and forest types. The occurrence of autocorrelated growth in tree species will have important implications for demographic studies and requires a different approach to demographic modeling (e.g., Van Mantgem and Stephenson 2005; Metcalf et al. 2009; Zuidema et al. 2009).
We found positive relations between diameter growth and extant diameter for all study species (Fig. 5). In three out of four species, such positive correlations were found for relatively small, juvenile trees (<20-cm diameter, all except Pinus). A similar result was obtained from the comparison of plot and ring data, in which extant large trees showed higher juvenile growth rates compared to extant juvenile trees (Fig. 6). In all, these results are consistent with the pattern that would be expected for a ‘juvenile selection effect’ (Rozendaal et al. 2010a). Such a ‘juvenile selection effect’ occurs if fast-growing juveniles have a higher chance to reach adult size as they accumulate less mortality risk while in the vulnerable juvenile stage, compared to slow-growing individuals. Such preferential survival of fast growers has now been reported for a number of species in both temperate and tropical forests (Landis and Peart 2005; Rozendaal et al. 2010a). The species studied here occur in distinct forest types: Annamocarya is a low-land forest tree of closed-canopy forests and fertile soils, while the three coniferous species occur in more open forests with a lower canopy but on rocky substrates. Thus, growth of Annamocarya juveniles is probably mostly light limited, and persistent fast juvenile growth likely increases the chance of reaching the canopy (cf. Rozendaal et al. 2010a). For the coniferous species, limited availability of water and nutrients or a limited rooting volume may lead to similar preferential survival of fast growers to adult size, but information on growth-limiting factors is required for a proper interpretation of these results.
In three of the four species, the correlations between growth and extant diameter were also present for adult trees of 30 to even 60-cm diameter (Fig. 5). It is unlikely that preferential survival of fast-growing individuals (the mechanism behind the ‘juvenile selection effect’) plays a role for trees of these sizes. Individuals of these sizes are well established and experience low mortality risks. An alternative explanation is related to strong and persistent growth differences that we observed (Fig. 2). If fast growers of the past remain fast growers in the present, they may be able to attain larger sizes compared to slow growers. This would be possible if the environmental conditions (e.g., light, water, nutrients) or tree characteristics (e.g., crown size) that allow trees to grow fast also provide the possibility to attain a large size. Another possible explanation of the results is that populations in which we sampled were recovering from previous disturbances and that historical growth conditions differed from present-day conditions (Rozendaal et al. 2010b). In the case of Annamocarya, the forest in the study area may have been more open before the Cuc Phuong National Park was established, allowing for faster growth of juveniles at that time, and gradually slower growth rates toward recent times as the forest became more dense and competition increased. The growth trajectories of Annamocarya presented in Fig. 1a, seem to support this idea. The individual trajectories show very little leveling off, i.e., the graphs are less sigmoid shaped than would be expected from a fully mature population. Therefore, the population may be recovering after a large-scale disturbance. Unfortunately, we did not possess information to evaluate if such changes had taken place and a visual inspection of the data did not reveal clear indications of concurrent recruitment peaks. We are aware that these explanations are rather speculative, but believe that it is important to use the results of this pilot study to formulate new hypotheses that can be tested in future work.
We found negative correlations between diameter growth and year before present, for small diameter categories in two of our study species. This finding is consistent with recent results of a tree ring study in Bolivia (Rozendaal et al. 2010a), in which historical growth increases were observed for juvenile individuals pertaining to four tree species in moist forests. The interpretation of these patterns is not straightforward, as multiple factors may cause juvenile growth rates to increase over time, including CO2 fertilization, recovery from disturbances and sampling effects (Baker 2010; Rozendaal et al. 2010a). In our case, the interpretation was also hampered by the lack of small individuals among the cored trees, which contain growth rates of small trees from the recent past.
Only recently have ecologists started to relate tree growth rates to extant tree size and time before present. This has led to interesting but sometimes puzzling results. It is evident that such analyses need to be conducted on a larger set of species from various forest types to derive general patterns.
Tree ring analysis for conservation
Our study shows that with relatively simple means and in a low-cost study, it is possible to obtain information on ages and long-term tree growth patterns of tree species. Such basic information on ages is of direct relevance for conservation and management of threatened tree species.
The evaluation of historical growth patterns and the comparison of growth rates from tree rings and plot data allowed us to establish that fast-growing juveniles in our study species likely had a higher probability to reach reproductive size. Such persistently fast-growing individuals exhibit very different growth trajectories (Metcalf et al. 2009) and likely have a much larger contribution to population growth than slow growers (Zuidema et al. 2009). For conservation purposes, it will therefore be important to evaluate the factors that allow juvenile individuals to grow fast and maintain fast growth. Once such factors are identified, fast growers may be recognized and receive particular attention in conservation actions and the development of slower growing individuals may be stimulated.
We are grateful for the assistance in fieldwork and support from National Park agencies in Vietnam, as well as the Forest Science Institute of Vietnam. Danaë Rozendaal and Claudia Soliz kindly contributed to this study during the data analysis phase. This work has been supported by financial contributions from Tropenbos International (to P.D.C.).
This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
- Brienen RJW, Zuidema PA, Martinez-Ramos M (2010) Attaining the canopy in dry and moist tropical forests: strong differences in tree growth trajectories reflect variation in growing conditions. Oecologia. doi:10.1007/s00442-009-1540-5
- Chien PD (2006) Demography of threatened tree species in Vietnam. Dissertation, Utrecht UniversityGoogle Scholar
- Cook ER, Holmes RL (1985) Users manual for program ARSTAN. Lamont-Doherty Earth Observatory, Palisades, NYGoogle Scholar
- Grissino-Mayer HR (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree Ring Bull 57:205–221Google Scholar
- Grogan J, Landis RM (2009) Growth history and crown vine coverage are principal factors influencing growth and mortality rates of big-leaf mahogany Swietenia macrophylla in Brazil. J Appl Ecol 46:1283–1291Google Scholar
- IUCN (2009) IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 10 December 2009
- Lisi CS, Tomazello M, Botoss PC, Roig FA, Maria VRB, Ferreira-Fedele L, Voigt ARA (2008) Tree-ring formation, radial increment periodicity, and phenology of tree species from a seasonal semi-deciduous forest in southeast Brazil. IAWA J 29:189–207Google Scholar
- Rozendaal DMA, Zuidema PA (2010) Dendroecology in the tropics: a review. Trees (this issue). doi:10.1007/s00468-010-0480-3
- Rozendaal DMA, Soliz-Gamboa CC, Zuidema PA (2010b) Assessing long-term changes in tropical forest dynamics: a first test using tree-ring analysis. Trees (this issue). doi:10.1007/s00468-010-0478-x
- Soliz-Gamboa CC, Rozendaal DMA, Ceccantini G, Angyalossy V, van der Borg K, Zuidema PA (2010) Evaluating the annual nature of juvenile rings in Bolivian tropical rainforest trees. Trees Struct Funct (this issue). doi:10.1007/s00468-010-0468-z