Growth patterns and ages of tropical forest trees Chapter 3

Lifetime growth patterns and ages of Bolivian rainforest trees obtained by tree ring analysis

With Pieter A. Zuidema Journal of Ecology: accepted

Abstract Growth patterns and ages of tropical forest trees are strongly governed by temporal variation in light availability. Periods of high growth after canopy disturbances ("releases") are necessary for successful canopy regeneration. To study the importance of growth releases, lifetime data are required. The recent detection of annual rings in tropical forest trees offers the possibility to do so. We studied lifetime growth patterns and age variation in six Bolivian rainforest species, using tree ring analysis. Our aims were (1) to evaluate the magnitude and sources of age variation of canopy trees, (2) to analyze the frequency of suppression and release events, and (3) to analyze the relation between temporal growth changes and tree age. The average age of trees of 60 cm diameter differed three-fold between species. Within species, the age variation of these large trees was remarkably high, with maximum ages 2-3 times the minimum. This variation was mainly explained by variation in passage time through the juvenile categories. We used strong relative growth changes to detect release and suppression events. Average canopy trees experienced 0.8-1.4 releases, with a maximum of 4. We identified ways in which trees have attained the canopy (canopy accession patterns): (a) growth without major growth changes, (b) one release event, (c) one suppression event, or (d) several release and suppression events. The time required to attain the canopy differed among these four categories, in increasing fashion. Thus, the distribution of trees over categories of canopy accession is closely related to the average age of canopy trees and its variation. There were clear differences among species in how trees attained the canopy and in the length of slow-growth periods they experienced, suggesting differences in shade tolerance and growth responses to gaps, and is thus indicative for life-history differences among nonpioneer tree species. Canopy attainment of tropical rainforest trees does not occur by steady growth, but rather by irregular patterns of growth spurts and stand-stills, probably mostly caused by temporal variation in light. Differences in these patterns may largely explain differences in the ages of large tropical rainforest trees. Key-words: growth patterns, growth release, growth suppression, tree age, tree ring analysis, tropical rain forest.

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Chapter 3

Introduction
A large share of trees in the understorey of tropical rainforests grows at very low rates due to limiting light availability (Chazdon et al. 1996). Canopy disturbances caused by tree and branch falls may release these trees from low-light conditions (Canham 1985; Canham et al. 1990; vanderMeer & Bongers 1996b). Many non-pioneer tree species in tropical forests are thought to require such releases from understorey light levels to be able to reach the canopy (Denslow 1980; Brokaw 1985), particularly those species that attain large stature (canopy and emergent trees). For species requiring canopy openings, the size of gaps, the frequency of gap formation and the growth response of species to high-light levels, determines the age at which individuals reach the canopy. This age is an important lifehistory characteristic, as it usually coincides with the onset of reproduction (Zuidema & Boot 2002). Information on ages of adult trees is also essential for forest management, as canopy trees are usually logged for timber and their age represents the time required to replace the harvested tree. The size and number of gaps that is required for trees to attain the canopy is thought to vary among species due to differences in response to high-light conditions and shade tolerance (Hartshorn 1978; Chazdon et al. 1996; Canham et al. 1999). Thus, the average growth trajectory of trees towards the canopy probably differs between species (cf. Canham 1985b; Poulson & Platt 1989). Information on these trajectories, including the presence and frequency of periods of high growth (releases) and low growth (suppressions), is essential to understand differences in life histories among species. Within one species, variation among individual trees in the occurrence of releases and suppressions may have important consequences for the variation in age of canopy trees and thus determine the age of individual canopy trees. Clearly, the analysis of growth trajectories towards the canopy requires long-term information on tree growth. Such information is lacking for tropical forests, as most growth data are obtained in permanent sample plots and cover less than 20 years (Condit 1995; Clark & Clark 1992, 2001). As a result, long-term growth patterns of tropical forests trees have been evaluated using short-term data (Lieberman et al. 1985a; Clark & Clark 2001). Similarly, age estimates have been obtained from projections using short-term data (Clark & Clark 1992, 2001) that are poorly validated (cf. Martinez-Ramos & Alvarez-Buylla 1998; Baker 2003). Such estimates may be biased, as successful trees may have grown at above-average growth rates (cf. Landis & Peart 2005). In temperate forests, tree ring analysis has been used to obtain insight in lifetime growth patterns, suppression and release cycles and historical growth rates of canopy trees (Canham 1985; Lorimer & Frelich 1989; Lusk & Smith 1998; Landis & Peart 2005). Over the last decade it has become clear that annual tree rings are formed in many tropical forest trees (Worbes 1999; Fichtler et al. 2003, 2004; chapter 2), thus providing an opportunity to study lifetime growth and age in a direct and more reliable way. Here, we report on a study in which tree rings were used to reconstruct lifetime growth patterns of six rainforest tree species. Specifically, we addressed the following questions: (1) What is the magnitude of variation in age of large conspecific trees, and what causes this variation? Does this differ among species? (2) What is the frequency of suppression and release events in growth trajectories of individual trees? And do these frequencies vary among species and size categories? (3) To what extent do differences in individual growth trajectories influence the time required to reach the canopy?

36

Growth patterns and ages of tropical forest trees We collected tree ring data from six rainforest tree species in northern Bolivia, all of which produce clear annual rings, caused by the occurrence of a distinct dry season (chapter 2). All study species are non-pioneers (sensu Swaine & Whitmore 1988), but they differ in shade tolerance. We identified relative growth increases and decreases in ring trajectories, which may indicate releases and suppressions due to canopy dynamics (e.g. Nowacki & Abrams 1997), although other causes are also possible. We then classified trees according to their growth pattern into the canopy and compared these among species. Our study provides reliable information on ages of tropical rainforest trees and is one of the first to unravel the causes of intra-specific variation in tree age.

Materials and Methods

Study areas and species The study areas are situated in the northern part of the Bolivian Amazon in the departments of Pando and Beni. The vegetation in both areas is tropical lowland moist forest with a canopy of 25-35 m height. The average basal area (DBH>20 cm) is 15 m2ha-1 with 103 trees per hectare (Superintendencia Forestal 1999). The total precipitation is 1760 mm (Cobija, Pando) and 1690 mm (Riberalta, Beni), with a distinct dry season from May until September with less than 100 mm of rain per month. In the department of Pando, we collected samples of Amburana cearensis and Cedrela odorata from the private property Purisima (11o24S, 68o43W), 50 km south of the town of Cobija. This area consists of 850 ha mainly undisturbed tropical moist forest, on undulating terrain. Samples of Bertholletia excelsa, Cedrelinga catenaeformis, Tachigali vasquezii and Peltogyne cf. heterophylla were collected from several adjacent logging concessions or private areas (10o55S, 65o40W), approximately 40 km east of the town of Riberalta, consisting of mainly undisturbed tropical moist forest. We selected the six study species, because all grew clear annual rings (chapter 2; see Table 1 for names, in the text all species will be named by genus only). None of the species is a classical pioneer (sensu Swaine & Whitmore 1988), but species do differ in shadetolerance or successional status. Amburana, Bertholletia, Cedrela, and Tachigali were all characterized as relatively light-demanding species, occurring in earlier stages of regeneration and being intermediate in their shade-tolerance as a seedling (Poorter 1999; Pea-Claros 2001) and Cedrelinga has previously been characterized as shade-tolerant (Poorter 1999). Peltogyne is a shade-tolerant species with a relatively high
Table 1 Adult stature, growth potential, largest observed diameter (R.J.W.Brienen, unpublished data) and sample size for the six study species. Growth potential is the mean of the five highest annual growth rates observed in different trees (cf. Clark & Clark 1999). Growth potential Largest observed Sample Species (cm/year) diameter (cm) size Amburana cearensis Bertholletia excelsa Cedrela odorata. Cedrelinga catenaeformis Peltogyne cf. heterophylla Tachigali vasquezii 1.8 1.9 3.2 3.7 1.8 4.8 119 210 179 201 100 80 35 12 60 33 17 29

37

Chapter 3 abundance of saplings in the dark understory (R. Brienen, personal observations). The six species clearly differ in diameter growth potential (Table 1). Amburana, Bertholletia and Peltogyne showed relatively low maximum growth rates, while Cedrela and Cedrelinga had high maxima and Tachigali showed a very high growth potential. Sample collection and ring measurements Between October 2002 and September 2003 we took samples from trees that were felled for timber or from trees that had died recently by natural causes. Minimum diameter of the sampled trees was 50 cm at breast height (DBH). From each tree a cross-sectional wood disc or segment was taken with a chain saw. Most samples (>90%) were taken from a height between 0.4 and 1.5 m, in exceptional cases up to 3.4 m. When buttresses were present, we tried to take samples above the buttresses, but this was not possible for all trees. Especially in trees of Cedrela and Cedrelinga buttresses more than 3 m high were common and a relatively large proportion of discs contained buttresses. For each disc, we calculated its surface area from pictures of the complete disc and, based on this, the average diameter. Average diameter (D, cm) was calculated as D = SQRT(A/)*2, where A is the disc area (cm2). After air-drying, we polished the discs mechanically with sandpaper up to grit 600. We chose two to four radii for ring counting and measuring of ring widths. These radii were chosen such that the average of the radii best corresponded to the calculated average diameter of the disc. For trees with buttresses, we counted and measured the rings both in buttresses and in parts in-between buttresses. Tree-rings were marked and every tenth ring was interconnected between radii to identify errors in ring marking. The ring widths were measured to the nearest 0.001 mm using a computer-compatible tree-ring measuring system (Velmex Inc. Bloomfield N.Y. USA) and a 40x10 stereomicroscope. Ring measurements were performed along each of the radii in a straight line, and generally perpendicular to growth boundaries. Tree ring formation in the six study species was proven to be annual by correlations between ring width and rainfall, by counting tree rings on discs of known ages or by radiocarbon dating (chapter 2). This confirms annual ring formation in the adult categories, but for the juvenile categories there is some uncertainty to which degree rings are formed annually; rings were not cross-dated in the juvenile categories and only for Cedrela has annual ring formation been proven (Dnisch et al. 2002). Tachigali showed no ring formation in the juvenile wood and was thus excluded for analysis of the juvenile categories. We expect ring formation in the other species to be predominantly annual, but missing rings or false rings are a potential bias. Missing rings during periods of suppression is a known problem and could yield underestimations of ages and overestimates of early growth (Lorimer et al. 1999). In Peltogyne, some rings may have been missing and ages may therefore be underestimated in this species (chapter 2). We expect that these potential biases do not influence the outcome of the results substantially. Calculation of age-diameter relationships and passage time We calculated the annual diameter increments of each tree by averaging ring-widths along the different radii and multiplying this value by two. Subsequently, we corrected for the difference of this calculated diameter value with the actual diameter at sample height (obtained from the disc area) to correct for over- or under-estimation of growth rates due to irregular growth patterns around the trunk (buttresses and depressions). The size of the correction of each annual increment value was based on the maximum difference between 38

Growth patterns and ages of tropical forest trees the increments along the radii for that particular year. Thus, no correction was applied if the different radii showed equal increments in a particular year, while large corrections were applied for those years with relatively high differences between the increments along the radii (e.g. in buttresses versus depressions). Corrected growth values were validated by comparing them with growth curves calculated from area measurements of 10-year increment periods. The sum of corrections was less than 10% for over 75% of the trees, and amounted to more than 25% for a few (3%) trees. For each tree we established age-diameter relationships for its complete lifetime. When rings were lacking in the tree centre, we estimated the distance to the pith and used the average number of rings of the other samples of that species to estimate the age of the first visible ring. In Cedrelinga this was done for a substantial number of samples due to the frequent occurrence of hollow trees. For this species the number of rings to 5 cm diameter was estimated for 20 out of 33 samples. In the other species relatively few samples relied on such estimates (i.e., 2 samples in Amburana, 5 samples in Bertholletia, 6 samples in Cedrela and never in Peltogyne). Note that the ages presented here are calculated from stem discs obtained at > 40 cm above the ground and do not include the time required to grow from seedling to sampling height. This means that both average age and its variation are underestimated. The time to reach the minimum sampling height is probably less than two to three years for five of the study species (Amburana, Bertholletia, Cedrela and Cedrelinga; Poorter 1999). For each size class of 10 cm width between 0 and 60 cm diameter the median, minimum and maximum passage time was calculated, being the number of years spent in a size class. A Kruskal-Wallis test with the Dunn-test was used to test for differences between species in passage times in each size class. In order to assess the contribution of each size class to the eventual variation in ages at 60 cm diameter, we analysed the effect of passage time in each class on age at 60 cm diameter by a multiple regression analysis. In this regression model, all size classes were included, except for those causing a high colinearity. Analysis of temporal growth patterns Lifetime growth patterns of individual trees were analysed for two purposes; first, to test whether the frequency of growth changes differs between different size classes. And secondly, to test whether and how species differ in the way they grow to the canopy (or to canopy size), we analysed "canopy accession patterns". We did these analyses only for Amburana, Cedrela, Cedrelinga and Peltogyne. For Bertholletia we had insufficient complete growth trajectories and for Tachigali we had no ring data for the smaller size classes. As we had no information on the relationship between light environment and growth, we defined the criteria of suppression and release as proportional decreases or increases in growth, instead of using an absolute threshold (e.g. Canham 1985; Landis 1999). Such proportional criteria have been used in other studies and proven to be reliable for detecting canopy disturbances in temperate forest trees (Lorimer & Frelich 1989; Nowacki & Abrams 1997; Lusk & Smith 1998; Rentch et al. 2003). We used moving averages to remove longterm age-size relations and very short-term variation in growth rates caused by variation in weather (Nowacki & Abrams 1997). As canopy closure in tropical forest gaps takes on average some 15 years to take place (vanderMeer & Bongers 1996b), a window of 10 years is considered to be sufficiently short to capture release and suppression effects brought about by canopy opening and closing.

39

Chapter 3 We used the formula of Nowacki and Abrams (1997) to derive the percentage growth change: %GCi = [(M2-M1)/M1] x 100 (1) ,

where %GCi = percentage of growth change for year i, M1 = the preceding 10-year mean diameter growth (including the year of change), and M2 = the subsequent 10-year mean diameter growth. Hence, if M1 is the mean over the period 1960- 1969, the mean for M2 was calculated over the years 1970-1979. In our analysis, we regarded a growth increase of more than 100% as a growth release, and a growth suppression was defined by a growth decrease of at least 50%. For each growth release or suppression the year of strongest growth change was regarded as the year of the event. A growth release is called a sustained growth-release when it lasts for more than 5 years. These operational definitions are used throughout this paper, regardless of the actual cause of the growth change (e.g. canopy disturbance, physical damage, or other factors influencing tree growth). For each tree, we calculated the frequency of growth releases and suppressions in each size class and tested for differences in the frequency of events between understory (<30 cm in diameter) and canopy trees (>30 cm in diameter) using a Wilcoxon signed ranked test. Most trees in our study reached the canopy at around 30 cm in diameter and received full or nearly full light above this, while only few trees below this diameter received full light levels (unpublished data, Zuidema & Boot 2002). Four patterns of canopy accession were distinguished and each individual tree was assigned to one of these patterns. (1) No sustained release. Canopy accession without the occurrence of major growth changes. A single temporary growth release (< 5 years) is allowed, as light climates generally improve when trees grow higher into the canopy even in the absence of a canopy opening (Montgomery & Chazdon 2001). Note that this pattern also includes trees that have been in high light conditions since the start of the ring data. (2) One sustained release. Canopy accession through at least one clear release event. This pattern is distinguished to identify trees showing a clear growth increase, which is most likely due to the opening of the canopy. Trees belong to this type if they show one release event, which is either preceded by growth suppression or which is sustained for more than 5 years. (3) One suppression; canopy accession takes place after the occurrence of one suppression event. Trees of this type usually have a high initial growth rate, followed by a strong growth decrease and no subsequent growth releases. (4) Multiple releases and suppressions; canopy accession takes place through multiple growth releases and suppressions. Any growth release must always be followed by a growth suppression and/or separated from a new growth release by more than 5 years. For trees of this type, successful growth into the canopy involved repeated growth shifts, most probably due to canopy dynamics. For each of the four species, we calculated the proportion of trees belonging to each canopy accession pattern and we calculated the time to reach 30 cm diameter for each combination of species and pattern. Differences between species in the distribution of trees in each of the canopy accession patterns and in the average number of releases were tested by a Fisher exact test. We tested for differences in time to reach 30 cm diameter between species and

40

Growth patterns and ages of tropical forest trees patterns, using a two-way ANOVA with a Bonferroni post-hoc test for contrasts between species and patterns. Median and maximum of longest consecutive periods of low growth (i.e. <2 mm/year) were calculated for each species. The length of such periods can be interpreted as an indicator of the ability of species to survive periods of suppressed growth (Canham 1985; Orwig & Abrams 1994; Landis 1999). We are aware that the choice of the growth threshold influences the lengths of the periods, but we used the results only for comparisons between species and these did not change when using lower thresholds. In many studies different thresholds were applied for different species based on the occurrence of extant juveniles in different microsites and their growth rates at different light levels (Lorimer et al. 1988; Landis 1999). We could not do this for our species, due to lack of such data. The application of one threshold probably yields equal ranking of species, as shown by Landis (1999).

Results
Age-diameter relationships We observed large differences in growth trajectories both among species and within species (Figs. 1 and 2). Bertholletia trees may become over 400 years old (427 years), while Tachigali usually dies before the age of 60 (when adding a projected 25 years to reach 10 cm in diameter; Poorter et al. 2005b). Maximum ages observed for Amburana and Peltogyne were 243 and 254 years, and the oldest tree of Cedrela was 308 years. Although large trees were sampled for Cedrelinga, their ages did not exceed 123 years. Species differed strongly in mean age-size relations (Fig. 1). Mean ages at 60 cm in diameter varied from 49 years (Tachigali) to more than 150 years (Bertholletia and Peltogyne). Around 15 cm in diameter, mean ages did not vary much among Amburana, Cedrela, Cedrelinga and Tachigali, but at larger diameters age-differences increased. The average age-size relations of Bertholletia and Peltogyne were nearly equal, showing the highest average ages at any diameter.
120

100

Cedrela Cedrelinga Bertholletia Amburana

Diameter (cm)

80

Tachigali
60

40

Peltogyne

20

0 0 50 100 150 200 250

Age (y)

Figure 1 Mean age-diameter relations for the six study species.

41

Chapter 3
200 200

(a) Amburana caerensis

(b) Cedrela odorata

150

150

100

100

50

50

0 0 200 50 100 150 200 250

0 0 50 100 150 200 250

(c) Bertholletia excelsa

200

(d) Tachigali vasquezii

150

150

Diameter (cm)

100

100

50

50

0 0 200 50 100 150 200 age 250 200 300 350 400

0 0 25 50 75

(e) Cedrelinga catenaeformis

(f) Peltogyne cf. heterophylla

150

150

100

100

50

50

0 0 50 100 150 200 250

0 0 50 100 150 200 250

Age (y)

Figure 2 Age-diameter relations for the six study species. Each line represents one individual tree. The dashed lines indicate constant diameter growth of 1 cm per year. Note that in Tachigali the trajectories are plotted from 10 cm diameter onwards.

42

Growth patterns and ages of tropical forest trees

80

Diameter class:

Median passage time (years)

70 60 50 40 30 20 10 0 a de h k n q ab e gh k n q a d f j m p ab c g i l op b e gh jk n q

0-10 cm >10-20 >20-30 >30-40 >40-50 >50-60

c f i l o

Amburana

Bertholletia

Cedrela

Cedrelinga

Peltogyne

Tachigali

Figure 3 Median passage time through 10-cm diameter classes for the six study species. Error bars represent the absolute maximum and minimum passage time. Sample sizes vary from 5 to 60 trees per class. Passage time differed (P< 0.001) between species in each of the size categories (Kruskal-Wallis tests). Different superscript letters under the bars indicate differences between species (P <0.05) using Dunn-tests. Samples sizes the species are: Amburana 2235, Bertholletia 5-11, Cedrela 51-60, Cedrelinga 6-33,Peltogyne 17, Tachigali 17-26.

The species also differed in the shape of individual growth trajectories (Fig. 2); most trees of Amburana and Bertholletia showed rather straight curves, with little variation (i.e., constant growth rates over time). Many trees of Cedrela, Cedrelinga and Peltogyne showed sigmoid curves, with slow initial growth, which gradually increased at larger diameters and then again slowed down towards the largest sizes. The highest variation in growth trajectories was observed in Peltogyne and Cedrela (Table 2); the coefficient of variation (CV) of ages at 60 cm diameter for these species was more than twice as high as the value of Cedrelinga. Amburana and Bertholletia showed intermediate values of coefficient of variation. Passage time and its significance for age variation In all study species, we found the highest median passage time in the size class of 0 to 10 cm in diameter and a decrease in subsequent size classes (Fig. 3). In Cedrela, Cedrelinga and Peltogyne, this decrease was more marked than in Amburana. For Bertholletia, the passage times increased again after 40 cm in diameter. Ring data for diameters <10 cm were lacking for Tachigali, but estimated passage time from repeated diameter measurements is relatively high (i.e. 25 years; Poorter et al, 2005) compared to that of subsequent classes. Differences between the maximum and minimum passage time were large for all species, except for Tachigali. Generally, the largest differences were found in the first size class and decreased towards larger size classes. This pattern is mainly caused by decreasing maximum passage time, as the minimum passage time varied little among the size classes. In Amburana and Peltogyne, the highest maximum passage time was found in the second and third size classes, respectively. Of all species and size classes, the largest absolute

43

Chapter 3
Table 2 Part correlation coefficients indicating the effect of passage time through size categories on age at 60 cm in diameter, obtained by multiple regression analysis. The last columns show the mean, minimum and maximum ages at reaching 60 cm diameter and the coefficient of variation (CV, %) and the sample size (N). Categories for which part correlations had a high colinearity were excluded from the analysis (shown in table with -). All regression models were highly significant (p<0.001). Significance indications for each of the part correlation coefficients are: ns: not significant, **:p<0.01,***:p<0.001. Tachigali and the first classes of Bertholletia and Cedrelinga were not included in the analysis, because of low sample size (<10; shown with x). Size categories (cm, diameter) Age at 60 cm diameter (y) 0-10 10-20 20-30 30-40 40-50 50-60 Mean (Min. Max.) CV (%) N 0.30*** 0.27*** 0.12*** 0.11*** 0.10*** 0.17*** 112.4 (77-159) 18.7 22-35 x 0.39*** 0.52*** 0.27*** x 0.46*** 0.26*** 0.25*** x x ns 0.18** 0.26*** 0.12*** ns 0.32** 0.16*** 0.19*** x x 0.35*** 0.06*** ns x 166.41 (121-239) 0.13*** 94.9 (42-172) ns 68.4 (55-95) 0.13*** 140.81 (88-230) x 22.8 (20-31) (+252) 21.1 28.7 11.7 27.0 5-12 51-60 6-33 16-17 9-26

Species Amburana Bertholletia Cedrela Cedrelinga Peltogyne Tachigali

1 For Bertholletia and Peltogyne the passage times and age calculations start at 1.5 cm diameter, as the rings in this trajectory were missing or invisible in most samples. 2 Ages expressed here for Tachigali, are ages from 10 cm diameter. For comparison with other species add 25 years as indicated in parenthesis, which is the projected time to grow to 10 cm diameter (Poorter et al. 2005b).

difference in passage time was found in the first size class of Cedrela; trees can grow 10 cm in diameter within 8 years, but this may also take over 70 years. The contribution of passage time through each size class to age at 60 cm diameter was assessed by part correlation coefficients (Table 2). For all species, the highest part correlation coefficients were found in the smallest size classes (0-20 cm diameter). In Amburana, Cedrela and Peltogyne correlation coefficients strongly decreased with size. In Bertholletia and Cedrelinga such clear size-dependent pattern was not found. These results indicated that the smallest size classes are most important in determining ages at 60 cm trees. Temporal variation in growth patterns Growth trajectories of individual trees are highly variable, as is shown by the examples of eight of our study trees (Fig. 4). These eight growth trajectories show high levels of variation in growth rate, both for individual trees over time and among individuals. The arrows indicate the suppressions and releases as defined by proportional growth changes. Strong growth changes in the trajectories are mostly classified as suppressions and releases. Some trees show no growth releases or suppressions, while others show one or more such events. Remarkable are the long periods of very low growth rates that some trees experienced (e.g. Fig. 4f-Cedrela; 50 years of very low growth rates before the first release event occurred). The frequencies of growth releases and suppressions differed among size classes (Fig. 5). Generally, we observed high frequencies of growth releases in the smaller size classes and substantially lower frequencies or no events at all in trees > 40 cm diameter. In Amburana, Cedrela and Peltogyne, the highest frequency of growth releases is observed in the smallest class with a clear decrease for larger size classes. The average frequency of growth releases in the smallest size class was approximately one out of the five or six trees every decade. The highest frequency of release events in Cedrelinga occurred between 10 and 20 cm in diameter, and was two to six times higher than the frequencies observed in other species in

44

Growth patterns and ages of tropical forest trees

(a) Amburana cearensis 2 1.6 1.2 0.8 1 0.4 0 2 1.6 1.2 0.8 1 0.4 0 (e) Peltogyne cf. heterophylla 2 1.6 No sustained release 3 2.5 0.5 0 (f) Cedrela odorata Multiple releases (c) Amburana cearensis One sustained release 3 0.5 0 (d) Cedrela odorata No sustained release One suppression 3 (b) Cedrela odorata One sustained release

2.5 2 1.5

Diameter growth (cm/y)

2.5

2 1.5

s
1.2 0.8

2 1.5 1

r s s r s

0.4 0 (g) Peltogyne cf. heterophylla 2 1.6 1.2 0.8 0.4 0 0 25 50 75 100 125 150 Multiple releases

0.5 0

(h) Cedrelinga catenaeformis

4 3.5 3 2.5 2

One sustained release

1.5 1 0.5 0 0

25

50

75

100

125

150

Age (y)

Figure 4 Examples of growth trajectories of individual trees and classification into canopy accession patterns (underlined). Growth suppressions (s) and releases (r) are marked. These events were defined by relative growth changes. Vertical lines mark the years of reaching 30 cm in diameter. Trees were assigned to a canopy accession pattern, based on the presence, absence, severity and frequency of growth suppressions and releases. Note different scales on Y- axes.

45

Chapter 3 this size class. The frequency of suppression events did not show a clear pattern, and species showed both lower (e.g. Amburana) and higher frequencies (e.g. Peltogyne) in the larger size classes. Cedrelinga trees that reached the canopy experienced few or no suppressions The average frequency of release events for all species was significantly higher for understory trees (<30 cm in diameter) compared to canopy individuals (30-70 cm in diameter). The frequency of suppressions was only significantly higher for understory trees in Cedrela (Wilcoxon sign rank test, P<0.05). Canopy accession patterns Table 3 shows the proportion of trees assigned to each of four canopy accession patterns that we distinguished. The proportions of trees in each of the canopy accession pattern types differed significantly between species (Fisher exact test, p<0.05), except between Cedrela and Peltogyne. It is remarkable that most trees of Amburana (> 40 %) grew into the canopy without sustained releases. In Cedrela, three canopy accession patterns (no sustained release, one sustained release, and multiple releases) were encountered in comparable proportions, while in Cedrelinga nearly 80% of the trees showed one sustained release. Nearly half the Peltogyne trees showed multiple releases, but others grew into the canopy without releases or through one sustained release. Thus, both between and within species there are differences in the way in which trees attain the canopy.

0.25

(a) Amburana cearensis Release events

0.25 0.2

(b) Cedrela odorata

Mean frequency of events per 10 years

0.2

Suppression events
0.15 0.1 0.05 0 0.15 0.1 0.05 0

(c) Cedrelinga catenaeformis

0.5 0.4 0.3 0.2 0.1 0
0 10 20 30 40 50 60 70 80

(d) Peltogyne cf. heterophylla

0.25 0.2 0.15 0.1 0.05 0
0 10 20 30 40 50 60 70 80

Diameter (cm)
Figure 5 Mean frequency of release and suppression events per decade for diameter classes. Release and suppression events are based on relative growth changes. Note that the scale of the Y-axis for Cedrelinga is different.

46

Growth patterns and ages of tropical forest trees

Table 3 Proportions of trees in each of four canopy accession pattern; mean time required to reach 30 cm diameter and average and maximum number of releases to reach 30 cm in diameter. The last two columns show the mean and maximum of longest consecutive periods of slow growth (<2 mm/year) before reaching 30 cm in diameter. The distribution over canopy accession patterns differed between all species (pairwise comparisons; Fisher exact tests, p<0.05), except for the comparison of Cedrela and Peltogyne. Both species and patterns had a significant effect on the time to reach 30 cm in diameter (two-way ANOVA, p<0.001; Cedrelinga excluded due to missing data). Significant differences are indicated by different capital letters for species and different lower case letters for patterns (Bonferroni post-hoc tests, p<0.05). Median period of slow growth (< 2 mm/y) differed among species (Kruskal-Wallis tests, p<0.05). Different letters indicate differences between species (P <0.05) using Dunn-tests. Species Canopy accession pattern Percentage of Time to reach 30 cm Number of releases Period with growth diameter (y) trees until 30cm < 2 mm/y (y) Mean Amburana (N=35) No sustained release One sustained release One suppression Multiple releases Cedrela (N=56) No sustained release One sustained release One suppression Multiple releases Cedrelinga1 (N=14) No sustained release One sustained release One suppression Multiple releases Peltogyne (N=17) No sustained release One sustained release One suppression 24% 29% 0% 14% 79% 0% 7% 32% 36% 0% 32% 43% 23% 17% 17% 63.1
A

Range

Mean 0.8

Max 3

Median 2
b

Max 16

58.8 a 62.5 b 59.8 ab 77.8 c 60.6 A 43.1 60.0 78.8 c 34.2 28.5 35.5 32 102.2B 74 a a b

38-78 55-79 36-89 56-94 1.2 26-59 27-89 31-119 1.1 23-50 1.4 57-105 68-106 4 15 a 41 2 3ab 8 4 4ab 47

91b

Multiple releases 47% 124c 87-187 1 The time to reach 30 cm and the number of releases in Cedrelinga only cover the growth trajectory from 5 cm diameter to 30 cm.

The time required to reach the canopy (i.e. 30 cm diameter) differed significantly between species and between different patterns (two-way ANOVA, Fspecies=17.0, Fpatterns=18.2, p<0.001; Table 3). Peltogyne needed more time to reach 30 cm diameter than Cedrela and Amburana. Time to reach the canopy for Cedrelinga could not be compared directly with the other species as it was calculated from 5 cm in diameter onwards. In Amburana, Cedrela, and Peltogyne the average time required to grow into the canopy was longest for trees with multiple releases, intermediate for trees with sustained releases and shortest for trees without sustained releases.

47

Chapter 3 The highest mean number of releases to grow into the canopy was found in Peltogyne and the lowest number in Amburana. No significant differences were found between species in the mean number of releases (Kruskal-Wallis tests). Among all trees the absolute maximum of observed releases were found in Cedrela and Peltogyne, with up to four releases before reaching 30 cm in diameter. An analysis of growth rates revealed that Peltogyne had significantly longer consecutive periods of growth < 2 mm/year compared to the other species (Table 3). The maximum period of slow growth was long for Cedrela and Peltogyne (i.e. 47 and 41 years), while it was much shorter for Amburana and Cedrelinga.

Discussion
Ages of tropical forest trees Tree ages obtained in this study (60 to over 400 years) resemble those obtained from tree ring studies in Costa Rica (Fichtler et al. 2003) and Cameroon (Worbes et al. 2003). For Cedrela, quite similar ages were found for a close congener (Cedrela lilloi) in subtropical Argentina (Grau 2000). Age determinations of Tachigali and Bertholletia are in accordance with estimates based on matrix models for these species (Zuidema & Boot 2002; Worbes et al. 2003; Poorter et al. 2005b) and with one radiocarbon dated Bertholletia tree in Brazil (440 60 years for a tree of 225 cm diameter: Camargo et al. 1994). Intra-specific variation in age-size relationships was very high. Among the six species, Cedrela showed the highest variation in age per size category. Understory trees of 10 cm of this species may be as old as adult trees of 60 cm in the canopy. Several studies have reported a similar magnitude of variation in age-size relations (cf. Enright & Hartshorn 1981; Villalba et al. 1985; Worbes et al. 2003), thus reaffirming that diameter is a poor indicator of tree age (Harper 1977; Sarukhan et al. 1984). The variation in ages at larger diameters (60 cm) was mainly caused by variation in passage time of trees through small size classes (<20 cm in diameter). Growth variation in these size categories is high due to large differences in light conditions among individuals (Chazdon & Fetcher 1984; Montgomery & Chazdon 2001). Thus, the ages of large canopy trees is strongly determined by the time they require to become 30 cm in diameter. Few estimates exist on passage time of juvenile tropical trees through the smallest size classes. Condit et al. (1993) present such data for a subsample of fast-growing species, making comparison with our results difficult. The only estimates appropriate for comparison with our study are projections based on short-term growth data for six nonpioneer, canopy and emergent species in Costa Rica (Clark and Clark 1992; 2001). The projected passage times to reach 30 cm in diameter (34-59 years) based on maximum growth rates are close to those observed by us. But projections based on median growth rates predict more than fourfold longer passage times (177-462 years). Partly, this difference could be explained by interspecific growth differences. But the fundamental difference between our sample and that of Clark & Clark (1992; 2001) is probably more important: our study trees represent a subset of successful trees that have reached the canopy, while the projections are based on all juvenile trees in the forest, including those that will not reach the canopy. This subset of successful trees may have had above-average growth rates, as has recently been shown for subalpine forest trees (Landis & Peart 2005). Slow growing juveniles accumulate more mortality chances as they stay longer in the understory (Swaine et al. 1987a; Terborgh et al. 1997; Arets 2005) and juvenile mortality is

48

Growth patterns and ages of tropical forest trees higher for suppressed trees (Kobe et al. 1995; Wyckoff & Clark 2002). Such selection of fast-growing trees may explain the discrepancy in passage time, but direct comparisons of age values obtained for the same species with different methods are required to confirm this (Bormann & Berlyn 1981; Martinez-Ramos & Alvarez-Buylla 1998; Baker 2003). To the extent that the above explanation holds, our results show that the use of median or mean growth rates tends to overestimate tree ages and that tropical forest canopy trees are younger than hitherto assumed. Temporal growth patterns We used relative growth changes to analyse temporal growth patterns of individual trees. This method has been successfully applied in the analysis of canopy disturbance in temperature forests (Lorimer & Frelich 1989; Orwig & Abrams 1995; Nowacki & Abrams 1997; Lusk & Smith 1998; Rentch et al. 2003), but had not been used for tropical forest trees before. As canopy dynamics similarly govern tree growth in temperate and tropical forests (Canham et al. 1990), we have applied a very comparable technique to that used before. We defined suppressions and releases based on strong and lasting growth differences, making our estimates of the frequency of these events rather conservative (cf. Lorimer & Frelich 1989; Nowacki & Abrams 1997; Rentch et al. 2003). For release events, the frequencies probably exclude causes other than canopy openings, as a doubling in growth rate over 10 years is expected to be related to a increase in light level. For suppression events, both canopy closure and crown damage (branch loss; Paciorek et al. 2000) may be responsible. For all study species, we consistently found that small trees experienced more releases than large trees per decade. This decreasing frequency may be caused by the larger temporal shifts in light levels for trees in the understorey and sub-canopy (Chazdon & Fetcher 1984; Montgomery & Chazdon 2001), but also by the weaker responses of large trees to increased light levels (Lorimer & Frelich 1989). Suppression frequencies, on the other hand, did not decrease with tree size and were also observed for large canopy trees. Crown damage and perhaps liana infestation are the most likely causes for suppressions in large trees (vanderMeer & Bongers 1996a). Among trees of the same species we observed a high diversity of growth trajectories through the juvenile categories, indicating that trees can reach the canopy in many ways. The classification into four canopy accession patterns allowed us to group trajectories. Trees with the canopy accession pattern no sustained release probably experienced rather stable or slightly changing light conditions while growing into the canopy. They required the shortest time to reach the canopy, as they did not experience suppressions. Growth into the canopy through one sustained release is most likely brought about by an abrupt and strong increase in light level by the formation of a gap. Trees that were classified in this category required more time than the previous group as they had experienced a suppression before the release, but still grew relatively fast. Quite different is the canopy accession pattern through one suppression. All trees classified as such belonged to Amburana and most showed high initial growth rates followed by a suppression event. These trees possibly were located in a canopy gap early in their life (Lorimer & Frelich 1989), and reached the canopy at relatively young age. Multiple release-patterns are an indication of repeated canopy openings often separated from each other by depressed growth rates due to canopy closure (or crown damage). Trees following this pattern took longest to reach the canopy, as they experienced several suppressed periods with slow growth.

49

Chapter 3 Thus, differences in canopy accession patterns among trees correspond to differences in the age at which they reach the canopy: low ages for trees that grew gradually to the canopy and high ages for trees that showed several periods of slow and fast growth. The distribution of trees of a given species over these four categories of canopy accession is probably related to the life history of the species, but also determines the average and variation in age of canopy trees. For instance, an even distribution of individuals over canopy accession patterns, such as in Cedrela and Peltogyne leads to high variation in ages. These latter species had twofold higher variation in ages at a certain size compared to Cedrelinga and Amburana, which predominantly followed one or two canopy accession patterns to grow into the canopy. Comparing species Our six study species were all non-pioneers (sensu Swaine & Whitmore 1988), but they differed strongly in longevity, age-size relationship and canopy accession patterns. Tree longevities differed more than sevenfold. The short maximum age of Cedrelinga and Tachigali (123 and 60 years) sharply contrast that of Bertholletia (427 years, Zuidema & Boot 2002). Especially in Tachigali, maximum age is low, only 60 years. This monocarpic species has very high growth rates and becomes reproductive at a young age (Poorter et al. 2005b) Among the six study species, mean ages at 60 cm diameter varied more than three-fold. For Amburana, Cedrela, Cedrelinga and Tachigali trees of <20 cm diameter had comparable size-age relations, but at larger diameter, ages differed strongly among species. This divergence was probably caused by differences in potential growth rate which became apparent at higher light availability (Clark & Clark 1999), or by differences in light availability among species (Poorter et al. 2005a). The differences between species in patterns of suppression and release suggest differences in life history, in spite of the fact that all study species were non-pioneers. These differences result from interspecific variation in shade tolerance (Kobe et al. 1995; Canham et al. 1999) and in response to increased light level (Denslow 1980b) and differences in light level (Poorter et al. 2005a). For instance, the absence of suppressions and the short periods of slow growth rates in Cedrelinga are most probably attributable to low survivorship in the shade. Juveniles of this species that have experienced longer periods of suppression may have died and are thus not present in our sample. In contrast, Cedrela and Peltogyne showed long periods of low growth (>47 and 41 years with < 2 mm/year) suggesting a higher ability to survive periods of suppression. Based on ring analysis alone, it is difficult to draw conclusions about the frequency and size of canopy openings that is required for successful regeneration into the canopy of our study species. Such figures could be obtained by combining our results with information on the proportion of juveniles that is present in various forest light environments and their growth rates in these sites. This has been successfully applied in temperate forests (cf. Canham 1985; Lorimer et al. 1988; Cao & Ohkubo 1999; Landis 1999). Our results show clear differences between non-pioneer species in lifetime growth patterns. In particular, the frequency of releases and the ability to withstand long periods of suppression, differ among species. Such differences are not detected using short-term growth data. This points out the relevance of lifetime growth data for the analysis of life histories of tropical forest trees.

50

Growth patterns and ages of tropical forest trees

Acknowledgements
We are very grateful to Adhemar Cassanova Arias, Merlijn Janssens, Henri Noordman, Jeanette Pacajes, Anneke Rijpkema, Jan Rodenburg, Vincent Vos and Oliver Yancke for their indispensable assistance with the ring measurements and to the staff of PROMAB and the field team of Purisima for their help with the fieldwork. We thank the Instituto de Geologa y Medio Ambiente (IGEMA) from the Universidad Mayor de San Andres (UMSA) in La Paz and Jaime Argollo for the use of their measurement equipment. Niels Anten, Ren Boot, Heinjo During, Matthew Landis, Francis Putz and Marinus Werger are acknowledged for constructive comments on earlier versions of this paper. This research is part of the Programa de Manejo de Bosques de la Amazona Boliviana (PROMAB) financed by grant BO 009703 from the Netherlands Development Assistence (DGIS).

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