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Tree Physiology
GuillermoGoldstein
Louis S. Santiago Editors
Tropical
Tree
Physiology
Adaptations and Responses in a
Changing Environment
Tree Physiology
Volume 6
Series editors
Frederick C. Meinzer, Corvallis, USA
Ülo Niinemets, Tartu, Estonia
r.brienen@leeds.ac.uk
Guillermo Goldstein •Louis S. Santiago
Editors
Tropical Tree Physiology
Adaptations and Responses in a Changing
Environment
123
r.brienen@leeds.ac.uk
Tree Rings in the Tropics: Insights
into the Ecology and Climate Sensitivity
of Tropical Trees
Roel J.W. Brienen, Jochen Schöngart and Pieter A. Zuidema
Abstract Tree-ring studies provide important contributions to understanding the
climate sensitivity of tropical trees and the effects of global change on tropical
forests. This chapter reviews recent advances in tropical tree-ring research. In
tropical lowlands, tree ring formation is mainly driven by seasonal variation in
precipitation or flooding, and not in temperature. Annual ring formation has now
been confirmed for 230 tropical tree species across continents and climate zones.
Tree-ring studies indicate that lifespans of tropical tree species average c. 200 years
and only few species live >500 years; these values are considerably lower than
those based on indirect age estimates. Size-age trajectories show large and persis-
tent growth variation among trees of the same species, due to variation in light,
water and nutrient availability. Climate-growth analyses suggest that tropical tree
growth is moderately sensitive to rainfall (dry years reduce growth) and temperature
(hot years reduce growth). Tree-ring studies can assist in evaluating the effects of
gradual changes in climatic conditions on tree growth and physiology but this
requires that sampling biases are dealt with and ontogenetic changes are disen-
tangled from temporal changes. This remains challenging, but studies have reported
increases in intrinsic water use efficiency based on δ
13
C measurements in tree rings,
most likely due to increasing atmospheric CO
2
. We conclude that tree-ring studies
offer important insights to global change effects on tropical trees and will
increasingly do so as new techniques become available and research efforts
intensify.
R.J.W. Brienen (&)
School of Geography, Leeds University, Woodhouse Lane, Leeds LS2 9JT, UK
e-mail: r.brienen@leeds.ac.uk
J. Schöngart
Instituto Nacional de Pesquisas da Amazônia (INPA), Av. AndréAraújo 2936,
P.O. Box 478, Manaus, AM 69011-970, Brazil
P.A. Zuidema
Forest Ecology and Forest Management, Centre for Ecosystems,
Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands
©Springer International Publishing Switzerland 2016
G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_20
439
r.brienen@leeds.ac.uk
Introduction
Tropical trees are an important element of the global biosphere. Tropical forests and
woody savannas cover 12–15 % of the Earth’s terrestrial surface (FAO 2006), and
host more than 40,000 tree species (Slik et al. 2015), they store about 60 % of total
global forest biomass (Pan et al. 2011), and play a significant role in the water,
carbon and nutrient cycles of the earth (Bonan 2008; Spracklen et al. 2012). Given
these important roles, it is essential to understand how tropical forests respond to
changing climatic conditions. This requires information about the climate sensi-
tivity of tropical trees and the long-term dynamics of tropical forests. For instance,
to project the effects of future climate change, it is pertinent to obtain insights into
the responses of tropical trees to variation in climate and CO
2
(Zuidema et al.
2013), while long-term information on tree ages and forest disturbance history are
important to infer residence times of carbon in forests as well as the interactive
effects of disturbance and climate change on forest dynamics (Babst et al. 2014;
Gebrekirstos et al. 2014).
Tree ring analysis (or dendrochronology) can importantly contribute to the study
of tropical forest responses to changing climate. However, in the tropics it has
lagged behind studies in temperate and boreal trees, where tree rings provided
detailed insights into tree growth and functioning, and trees’responses to past
climate (Fritts 1976; Speer 2010). While the occurrence of clearly defined annual
rings in tropical trees is less common than in temperate trees, a substantial number
of tropical species is known to form annual rings. One of the first documented
observations on tree rings in a tropical tree species was by Brandis in 1856, who
noticed that Teak (Tectona grandis) in Indonesia produced distinct rings which he
assumed to be formed in response to an annually recurring dry season. This was
confirmed in 1881 by Gamble by counting rings on plantation trees with known
age, and much later by the publication of the first tropical tree ring chronology on
Teak from Java by Berlage (1931). The research field of tropical dendrochronology
has made some important advances since then. Two workshops specifically dedi-
cated to this research field (1980 and 1989) summarized the advances and con-
cluded that it has been clearly demonstrated that many tropical tree species in
regions with seasonality in rainfall or flooding form distinct annual rings (Bormann
and Berlyn 1981; Baas 1989). In 2002, Worbes evaluated 139 species from
neotropical floodplains and terra firme, showing the occurrence of growth bands in
at least a third of the listed species. In the last decade the number of species with
proven annual rings has increased strongly (Zuidema et al. 2012) due to increased
research efforts throughout the tropics. Despite these recent advances, even today
the Berlage teak chronology (1514–1929) published in 1931 remains one of the
longest tree ring chronologies in the tropics. The apparent lack of success in
reconstructing long climate sensitive ring width chronologies, as witnessed for
example in the paucity of tropical chronologies in the International Tree Ring
Database (Grissino-Mayer and Fritts 1997), highlights undeniable problems in
detecting tree rings for a large number of species, but is also partially due to
440 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
insufficient efforts, and long-standing skepticism towards the occurrence of ring
formation in tropical trees.
In this chapter, we present important findings obtained in tropical tree ring
research relevant to the general theme of this book, the adaptation of tropical trees
to changing climate. We first describe the different mechanisms of tree ring for-
mation in tropical trees, relate this to tree phenology, and provide an overview of
tropical tree species with proven annual rings. The following sections present
results on ages, growth patterns and regeneration strategies of tropical trees, and a
review of the sensitivity of tropical trees to inter-annual variation in climate and
long-term tree responses to CO
2
increase. We end with a section on insights from
isotope techniques and a summary of our main conclusions.
In our review, we included all studies from tropical latitudes (i.e., between 23.4°
North and South) thus including both wet forests and savannas, very wet and dry
areas, and flooded and non-flooded areas. We excluded studies in mountain systems
(>1500 m a.s.l), and mangroves, where environmental conditions and cues are very
different.
Tree Ring Formation in the Tropics
Tree-ring boundaries are formed when cambium cells in tree trunks are dormant. In
mid- and high-latitude regions, the principal trigger behind cambial dormancy and
the formation of anatomically distinct tree rings is seasonal variation in day length
hours and temperature (Fritts 1976). In the tropics, there is no (or very limited)
seasonality in these climatic variables. This notion was the basis for the long-held
belief that tropical trees show relative constant growth throughout the year and
would not form annual rings (cf. Lieberman and Lieberman 1985; Whitmore 1998).
Nevertheless, many tropical trees do show annually recurring phenological patterns
(van Schaik et al. 1993), which may slow down cambial activity or induce complete
cambial dormancy, and result in an anatomically distinct layer of wood i.e., a tree
ring boundary. Seasonality in leaf phenology in tropical trees is thought to be an
adaptation to variation in external (abiotic) stress. Rainfall seasonality is by far the
most common stressor for tropical trees (Worbes 1995,1999). Over large areas of
the tropics, especially further away from the equator, evapotranspiration exceeds
rainfall for at least several weeks per year. This causes seasonal water-stress
especially for shallow rooted species in dry sites (Borchert 1994), and may result in
complete leaf shedding (deciduous), or exchange of leaves within a very short
period (brevi-deciduous). When trees are leafless, cambial activity stops, and a
distinct layer of wood is formed. While this behavior is most likely a plastic or
evolutionary adaptation to reduce leaf cover during periods of prolonged water
stress, the actual trigger to which trees respond may be different. For instance, in
some deciduous species of seasonally dry forests, it has been observed that trees
drop their leaves before water stress has developed and that bud break often occurs
before the onset of the wet season and is triggered by variation in day length
Tree Rings in the Tropics: Insights into the Ecology …441
r.brienen@leeds.ac.uk
(Rivera et al. 2002; Elliott et al. 2006). Another abiotic stress factor leading to the
formation of annual rings is seasonal flooding. During flooding, anoxic conditions
of the roots induce leaf fall, cambial dormancy and the formation of annual rings in
many tree species (Worbes 1985; Schöngart et al. 2002).
Whether trees form annually distinct rings depends both on the species-specific
physiology and wood anatomy, but also on exogenous factors like the seasonality
of the rainfall or flooding. Trees showing strictly annual cycles of leaf fall and
flushes are more likely to form annual rings, and the percentage of species with
annual rings is expected to be higher in sites with strong annually recurring sea-
sonality (Borchert 1999). Several studies demonstrated the importance of season-
ality in environmental conditions by showing that some species may form clear
annual rings in seasonal sites, but lack rings in very wet sites with low precipitation
seasonality or in very dry sites with highly irregular precipitation (Geiger 1915;
Coster 1927; Borchert 1999; Pearson et al. 2011). Hence, tree ring formation can be
strictly annual, bi-annual (Jacoby 1989; Gourlay 1995) or irregular with false
(non-annual) rings occurring every few years (Wils et al. 2011). Formation of
annual rings can also differ between life stages with clear and annual rings in the
adult phases, but absent, vague, or non-annual rings formed during the juvenile
phases (Dünisch et al. 2002; Brienen and Zuidema 2005; Soliz-Gamboa et al.
2011). These issues call for cautious interpretation of tree-ring measurements in
new species or in the same species at different sites.
A global dicot wood anatomy database with 5663 anatomical descriptions,
indicates that ca. 23 % of the tropical woody dicots present distinct growth
boundaries, somewhat lower than the global average of 34 % and the 76 % in
temperate regions in the northern hemisphere (Wheeler et al. 2007). Considering
the very high diversity of tropical tree species (Slik et al. 2015) and the propor-
tionally low number of studied species, this lower occurrence of tree rings in the
tropics still yields a potentially very large number of species forming anatomically
distinct ring boundaries. As anatomic records do not indicate whether rings are
formed annually, we provide a review of 130 studies on tree rings in tropical trees
(see also Zuidema et al. 2012; Schöngart 2013) for which annual formation of tree
rings has been verified using various methods (e.g. cambial marking, climate cor-
relations, bomb-peak dating, trees of known age, etc., see Worbes 1995). This
review shows that 230 different tropical tree species from 46 different families form
annual rings (see summary Table 1). These studies cover all continents and climates
(see Fig. 1), and also include some very wet sites (4000 mm annual precipitation)
with limited seasonality in rainfall (Fichtler et al. 2003; Groenendijk et al. 2014).
The majority of the studies however, are located in zones away from the equator
that have at least one distinct dry season (cf. Fig. 1).
The existence of growth rings is closely related to the wood anatomical structure,
and therefore—at least partially—genetically determined (Wheeler et al. 2007, but
see; Fichtler and Worbes 2012). Variation in wood anatomy of tropical trees that
defines ring boundaries is distinctly different from temperate northern hemisphere
woods (Worbes 1995), thus requiring a separate classification. A useful and widely
used anatomical classification of growth ring boundaries in tropical woods is that of
442 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
Coster (1927) adopted by Worbes (1995,2002). It distinguishes four different types
of growth zones: (1) density variations; (2) marginal parenchyma bands; (3) repeated
patterns of alternating parenchyma and fibre bands; (4) variations in vessel distri-
bution and/or vessel size (i.e., ring-porosity) (Fig. 2). As currently no large-scale
classification of wood anatomy of growth zones exists for tropical tree species, it is
Table 1 Summary table of
literature review of 130
studies showing the number
of species with annual rings
per vegetation type, the
top-five species used for tree
ring studies, and top five
families with ring forming
species
Vegetation type #studies
Wet forest 76
Moist forest 117
Dry forest 18
Open savannah and desert 15
Floodplain 21
Top five species used in the tropics
Tectona grandis
Terminalia superba
Cedrela odorata
Triplochiton scleroxylon
Macrolobium acaciifolium
Top five families with ring forming species # species
Fabaceae 95
Meliaceae 17
Malvaceae 11
Bignoniaceae 7
Combretaceae 7
A total of 230 species with annual formation of tree rings was
found. The annual character of rings in these studies was verified
using various methods (e.g. cambial marking, climate
correlations, bomb-peak dating, trees of known age, etc.).
A comprehensive list of these studies can be found in Zuidema
et al. (2012) and Schöngart (2013). Studies in mountain systems
(>1500 m a.s.l) or mangroves are excluded from this review
0
500
1000
1500
2000
Fig. 1 Map with locations of tree-ring studies in the tropics. The background color shows the
precipitation in the driest quarter (data: WorldClim, Hijmans et al. 2005) with blue areas marking
areas that receive more than 300 mm during the driest quarter
Tree Rings in the Tropics: Insights into the Ecology …443
r.brienen@leeds.ac.uk
hard to make generalizations about relations between wood anatomy or the occur-
rence of growth zones and taxonomy. Nevertheless, the top families with
ring-forming species are Fabaceae, Meliaceae and Malvaceae (see Table 1). Growth
zones in Fabaceae and Meliaceae often show marginal parenchyma bands (Worbes
1989; Groenendijk et al. 2014), while alternating parenchyma and fibre bands are a
common feature in Lecythidaceae, Sapotaceae, and Moraceae (Worbes 1989).
Density variations and vessel size variation can occur in concurrence with the pre-
vious features, or delineate an annual growth zone by itself. The best example of a
“ring-porous”species with wide vessels delineating the start of a new ring, is Teak
(Tectona grandis), one of the most widely used tropical species for climate recon-
struction in the tropics (cf. Fig. 2f). Examples of families with species with variations
in wood-density include Annonaceae, Lauraceae and Euphorbiaceae (Worbes 1989).
Despite the advances in tropical tree ring analysis, tropical trees commonly
present problems in the form of vague growth boundaries, false rings (Fig. 2h) and
wedging rings (Fig. 2i) or discontinuous (locally absent) rings (Fig. 2g). For those
interested in performing tree-ring studies in the tropics, please refer to Stahle (1999)
and Worbes (1995,2002) for practical guidance.
Inferences from Trees Rings on Tree Longevity, Growth
Patterns and Regeneration
Tree rings allow detailed reconstruction of growth curves for individual trees over
the full length of their life, thereby providing profound ecological insights that
cannot be obtained using for example relative short-term growth measurements. We
will highlight a few important ecological inferences that have been made from
growth rings of tropical trees.
Tree rings provide accurate information on tree ages. The question of how old
tropical trees become has occupied scientists for a long time, and has been the
subject of fierce scientific debate. Ages in trees can be measured directly only by
means of radiocarbon dating or tree ring analysis (Martinez-Ramos and
Alvarez-Buylla 1998). Some radiocarbon dating methods revealed ages for tropical
trees in excess of 1000 years (Chambers et al. 1998; Vieira et al. 2005), but given
the controversy on these reported ages (Martinez-Ramos and Alvarez-Buylla 1998,
1999; Worbes and Junk 1999) and the focus of this chapter, we here report on the
outcome of ages obtained by tree ring analysis only.
Figure 3shows the range of maximum observed ages for 71 tropical tree species.
These results provide an indication of tree longevities, although it should be noted
that in most cases, the purpose was not to sample the largest individuals of the study
species. The mean of the maximum observed age across all tropical tree species is
208 years (median = 200 years). In line with the high diversity in life-history
strategies among tropical trees, ages vary from a few decades for pioneer species
(Schöngart 2008; Brienen et al. 2009; Vlam 2014) to several centuries. Taxodium
mucronatum trees show the highest longevity reaching ages of more than 1500 years
444 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
in swamp forests in central Mexico (Stahle et al. 2012). However, such long-lived
conifers can be regarded an exception, as most broadleaved trees in lowland areas are
substantially younger. The oldest broadleaved tree with confirmed ages in excess of
1000 years using a combination of tree rings and radiocarbon dating are Baobab
trees from Africa (Robertson et al. 2006; Patrut et al. 2007), while few studies report
ages over 500 years old (Fichtler et al. 2003; Borgaonkar et al. 2010). This outcome
(a)
(d)
(f)
(h)
(j)
(c)
(e)
(g)
(i)
(b)
Fig. 2 Wood anatomical features of tropical tree rings showing the most common ring boundaries
(panels a–f) and some common problems encountered in tree ring studies (g–j). Growth direction
in panels a–fis from left to right.Filled white triangles indicate annual growth boundaries; open
triangles in panel hindicate false rings
Tree Rings in the Tropics: Insights into the Ecology …445
r.brienen@leeds.ac.uk
of the studies reviewed here are close to estimates of tree longevity derived from
growth rates from rainforests of central Amazon (median of 296 years, Laurance
et al. 2004) and Costa Rica (mean of 230 years from 10 cm DBH, Lieberman et al.
1985), and shows that life-spans of broadleaf tropical tree species are not different
from those of temperate broadleaf tree species (cf. Loehle 1988). However, the
results contrast with life-spans of several millennia for trees (mainly gymnosperms)
growing in extreme environments (Brown 1996). Reliable estimates of tree
longevities are an important basis for calculations of carbon residence times.
Reconstructions of age-size relationships show a large variation both within
(Fig. 4a, b) and between species (Fig. 4d–f). Within species several magnitudes of
variation in ages exist between trees of a similar size, even at the youngest stages.
For example, within the same population the ages of Cedrela odorata trees of
10 cm in diameter range from 9 to 75 years (cf. Fig. 4a), and a similar magnitude of
variation exists among Macrolobium acaciifolium trees from floodplain forests (cf.
Fig. 4b). Hence, young juvenile trees may be as old as large canopy trees. Such
large variation in growth rates between trees of the same species seems very
common in tropical trees (Worbes et al. 2003;López et al. 2013; Groenendijk et al.
2014), reaffirming that size is a poor predictor for tree age. This variation between
trees arises due to differences between individuals in light and water availability,
and soil fertility (Schöngart et al. 2005; Baker and Bunyavejchewin 2006; Brienen
et al. 2010a). The relative importance of these factors may vary between sites and
species. Comparison of two Cedrela populations showed that in moist forest with a
relatively dark understory, variation in juvenile growth was mainly governed by
fluctuations in light availability, while at a dry site spatial variation in water
availability was more important (Brienen et al. 2010a). In the Amazonian floodplain
species M. acaciifolium the effect of differences in nutrient availability seemed to
dominate variation in growth rates, with much slower growth in the nutrient poor,
black-water floodplains (Igapó), compared to the nutrient rich white-water flood-
plains (Várzea) (Schöngart et al. 2005). Remarkably, this growth variation is
associated with tree longevities, with slow growers at the nutrient poor sites
Fig. 3 Histogram of
observed maximum ages of
71 tropical tree species by use
of counting of annual tree
rings
446 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
attaining much higher ages (i.e., 403 years) compared fast growers at the richer sites
(i.e., 157 years). Such trade-offs between growth and longevity have been observed
in temperate trees (Bigler and Veblen 2009) and may have important implications
for future responses of forests to increased levels of CO
2
and temperature (cf.
Bugmann and Bigler 2011).
Comparison of mean age-size relationships between species shows a comparable
variation to that observed within a species (Fig. 4c–f) indicating that microsite and
stochastic difference between individual trees may be as important as its taxonomy
in shaping growth trajectories. Mean age of similarly-sized trees varies by a factor
of four to five across species and across vegetation types (wet to dry terra firme and
floodplain forests and savannas).
Afinal contribution of tree ages to tropical forest ecology is in evaluating
changes in forest dynamics and reconstructing past disturbances. Distinct peaks in
the age distribution of light-demanding tree species may indicate periods of dis-
turbances if these have resulted in elevated recruitment rates of these species (Baker
0
20
40
60
80
100
120
140
050100150200250
Dry forest (1100 mm)
Moist forest
(1750 mm)
0 50 100 150 200 250 300 350 400 450
Igapó, nutrient poor
Várzea, nutrient rich
0 50 100 150 200 250 300 350
(a) (b)
(c) (d)
(e) (f)
Cedrela odorata,Terra firme Macrolobium acaciifolium, Floodplain
Central Amazonian floodplain forests
Moist to wet tropical forest (1750-4000 mm precipitation)
Seasonally dry tropical forest (1470-1530 mm precipitation) Dry forest-savanna mosaic (1200 mm precipitation)
Fig. 4 Growth trajectories of tropical trees derived from tree ring analysis. Panels a–bshow
trajectories of individual trees for Cedrela odorata from two terra firme forests (Bolivia and
Mexico; Brienen et al. 2010a) and for Macrolobium acaciifolium from Brazilian floodplains
(Schöngart et al. 2005). Panels c–fshow mean trajectories for different species from (c) moist to
wet tropical forests (6 spp. northern Bolivia; Brienen and Zuidema 2006); 4 spp. Cameroon
(Groenendijk et al. 2014), dCentral Amazonian Várzea floodplain forests (14 spp.; Schöngart
2008), eseasonally dry tropical forests (5 spp. southern Bolivia; van der Sleen 2014), 5
spp. Thailand; (Vlam 2014), and fdry forest-savannah mosaics (6 spp. west Africa, Schöngart
et al. 2006)
Tree Rings in the Tropics: Insights into the Ecology …447
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et al. 2005; Vlam et al. 2014b). The spatial configuration of tree ages of such
light-demanding species may provide important additional information on the
extent of these disturbances (Middendorp et al. 2013). Another indication of
changes in forest dynamics can be obtained from the analysis of ‘releases’, periods
of elevated growth rates, which can be caused by increased light levels. In forests
where tree mortality is gradually increasing over time, more gaps are formed, which
may lead to an increase in the incidence of such growth releases. The interpretation
of the causes of growth releases is not straightforward though, as individuals and
species may strongly differ in responses to gap formation (Brienen and Zuidema
2006; Soliz‐Gamboa et al. 2012) and releases may be induced by climatic vari-
ability (Brienen et al. 2010a; Vlam 2014). So far, the few analyses of release
frequency for tropical tree species have shown no or minor shifts in the rate of
releases during the last century, suggesting that gap dynamics have remained rather
stable over the last century (Rozendaal et al. 2011; Vlam 2014). It should be noted
however, that retrospective tree ring studies miss a significant and possibly
non-random proportion of the original historical tree population (Landis and Peart
2005; Rozendaal et al. 2010), which may lead to biases in reconstructions of
historical growth rates and release frequencies (Brienen et al. 2012a).
Climate Sensitivity of Tree Rings
Temperature, water-availability, and incoming solar radiation all affect tree growth.
The responses of tropical trees to these controls may be complex and non-linear,
and may vary across species and ecosystems. Tree ring analysis is an ideal tool to
evaluate growth responses to climatic fluctuations, as it yields long series of growth
rates at annual resolution. Here we review growth responses of tropical trees to
climatic variation based on 45 studies reporting climate growth relations (Table 2).
The studies generally adopt standard dendrochronological techniques (Speer 2010)
to develop a climate sensitive tree-ring chronology. A chronology is a time series of
averaged growth for individuals that shows comparable growth fluctuations
Table 2 Summary table of the climate-growth relationships for different vegetation types
(excluding floodplains)
Vegetation type Correlation ring
width-rainfall, mean (max)
n Correlation ring
width-temperature, mean (min)
n
Wet forest
(>2000 mm)
0.49 (0.75) 6 ––
Moist forest (1000–
1500 mm)
0.44 (0.66) 39 −0.44 (−0.6) 8
Dry forest
(<1000 mm)
0.57 (0.89) 7 −0.42 (−0.57) 5
Open savannah 0.49 (0.65) 7 −0.3 (−0.40) 2
448 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
(cf. Fig. 5a). It should be noted that a straightforward comparison of the results of
climate-growth relations is hampered by variation in the selection of trees to be
included, the procedures to remove ontogenetic trends from the growth data, the
length of the growth series and the statistical analyses applied.
(a)
(b)
(c)
(d)
(e) (f) (g)
Fig. 5 Example of time series of growth (a,b), leaf intercellular CO
2
derived from tree ring
carbon isotopes (c), and tree ring oxygen isotopes (d) for a dry forest tree species, Mimosa
acatholoba from southern Mexico. Panels e,f, and gshow the relationship of the ring width and
isotope derived data to external variables. Growth and internal CO
2
(derived from δ
13
C in tree
rings) are most strongly related to annual rainfall, while oxygen isotopes related strongly to
variation in isotopes in rainfall from a distant station in San Salvador and was also negatively
correlated to local precipitation (r = −0.72). All relations are significant at p < 0.001. Data-sources
Brienen et al. (2010a,2011,2013)
Tree Rings in the Tropics: Insights into the Ecology …449
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Our analysis shows that annual variation in tropical tree growth is often asso-
ciated with fluctuations in precipitation: in nearly 60 species, growth rates increased
with rainfall (Table 2). This sensitivity to rainfall fluctuations was similar for dry,
moist and wet forests (Table 2), although one would expect a higher sensitivity in
drier forest sites. The lack of a clear relation of growth responses with underlying
climate is at least partially due to methodological differences across studies, but also
due to differences between species in their sensitivity to rainfall fluctuations, even
when they occur in the same area (e.g., Schöngart et al. 2006; Mendivelso et al.
2013; Vlam et al. 2014a). In addition, some species are more susceptible to rainfall
during the dry period, others to the wet period or transitional periods. And finally,
species may also show growth responses to rainfall during the previous growing
season (year). Such lagged responses are common, especially in strictly deciduous
species (e.g., Teak; Buckley et al. 2007, and several Meliaceae; Dünisch et al. 2003;
Brienen and Zuidema 2005; Heinrich et al. 2008; Vlam et al. 2014a), and may be
due to use of stored reserves at the beginning of the rainy season to support wood
formation (Dünisch and Puls 2003; Ohashi et al. 2009). These strong differences in
sensitivity to rainfall reflect species’differences in stem water storage, phenology,
rooting depth and use of reserves (Borchert 1994; Meinzer et al. 1999).
The strongest responses to precipitation are observed in dry sites in northern
Columbia and Peru and in southern Mexico, where >60 % of variation in ring width
is explained by year-to-year variation in rainfall totals (Rodríguez et al. 2005;
Brienen et al. 2010b; Ramírez and del Valle 2011,2012). In these dry to very dry
sites (50–900 mm annual precipitation), rainfall can be extremely variable among
years (partially due to ENSO), resulting in a strong control of precipitation on
growth (see Fig. 5e). Despite these exceptions, the overall effect of precipitation on
growth is relatively weak (mean correlation, r, across all species is 0.47, cf.
Table 2), suggesting that rainfall fluctuations have a limited impact on tree growth.
However, reserve storage in trees has a buffering effect and may reduce annual
fluctuations in tree growth. Work in a dry tropical forest shows that trees may be
relatively tolerant to annual fluctuations in rainfall, but sensitive to multi-annual
droughts (Mendivelso et al. 2014).
Temperature negatively affects growth in tropical trees (cf. Table 2), but the
number of studies reporting temperature growth relations is much lower than those
reporting precipitation influences. This is at least partially because fewer studies
included temperature explicitly in their climate growth relations, but also due to
lower responsiveness of tropical tree growth to temperature fluctuations. Especially,
in dry forests and savannas temperature influences were weaker than the influence
of rainfall, and in some cases temperature influences simply resulted from
co-linearity between inter-annual variation in rainfall and temperature (cf. Brienen
et al. 2010b). Several studies in moist forests show temperature effects that are of
comparable or slightly higher in magnitude compared to effects of precipitation
(Buckley et al. 2007;López and Villalba 2011; Ramírez and del Valle 2012;
Locosselli et al. 2013; Vlam et al. 2014a). These results along with findings of
temperature influences on tree growth from repeated tree diameter measurements in
several tropical forests (Clark et al. 2010; Dong et al. 2012) clearly show negative
450 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
influences of inter-annual variation in temperature on tropical tree growth. This
response is opposite to observed temperature responses of tree rings in cold cli-
mates (Fritts 1976), and consistent with negative effects of temperature on photo-
synthesis at high temperatures, above 30 °C (Doughty and Goulden 2008) and with
effects of temperature on respiration and evaporative demand (Lloyd and Farquhar
2008).
While there is a large uncertainty in climate models with regard to rainfall
predictions, there is a high degree of certainty for warming to occur throughout the
tropics (Stocker et al. 2013). This predicted warming may negatively affect tree
growth in the decades to come, but results of temperature sensitivity of tropical tree
growth based on annual fluctuations in temperature cannot be easily translated into
growth responses to a gradual rise in temperature, given possible acclimation of
photosynthesis and respiration to gradual temperature changes (Lloyd and Farquhar
2008). Also, the negative temperature effects may be offset by increases in atmo-
spheric CO
2
(Lloyd and Farquhar 2008). In all, our analysis indicates that tropical
tree growth is moderately to highly sensitive to rainfall fluctuations and less so to
temperature variation. Sensitivities to climatic fluctuations are highly
species-specific, which may contribute to an overall resilience of diverse tropical
forests to increased climatic variability in rainfall and temperature.
Global Change and Tropical Tree Growth
Future global climatic and atmospheric changes may affect the physiology and
growth of tropical tree species in various ways. Major atmospheric and climatic
drivers affecting tree growth include rising CO
2
levels, rising temperature, changes
in precipitation regimes and frequency of droughts, and increased atmospheric
deposition of nutrients. Tree-ring studies and analyses of stable isotopes in tree rings
can be used to quantify the effects of past climatic and atmospheric changes on tree
growth (Zuidema et al. 2013), and evaluate the performance of Earth system models
and improve their projections (Babst et al. 2014). Most importantly, the effects of
rising CO
2
levels on tree physiology and growth (CO
2
fertilization) can be studied
using stable carbon isotopes (
13
C) from tree rings and by changes in tree-ring width.
Analyses of carbon isotope ratios (δ
13
C) in tree rings over periods of time during
which atmospheric CO
2
levels have increased can be used to evaluate changes in the
intrinsic water use efficiency (iWUE), the ratio of carbon fixed (photosynthesis) to
water lost (stomatal conductance) (McCarroll and Loader 2004). In addition, stable
oxygen isotopes (
18
O) could potentially be used to infer changes in water fluxes
(e.g. evapotranspiration from forests, Brienen et al. 2012a,b), and stable nitrogen
isotopes (
15
N) can be used to evaluate changes in nitrogen cycling (Hietz et al.
2011).
There are several advantages of using tree-ring analyses for studying global
change effects on tropical forests, compared to analyses based on plots: tree rings
cover longer periods of time, they yield growth rates at annual time resolution and
Tree Rings in the Tropics: Insights into the Ecology …451
r.brienen@leeds.ac.uk
additional measurements (stable isotopes, anatomy) can be obtained from tree rings
(Zuidema et al. 2013; Babst et al. 2014). On the other hand, limitations of tree-ring
analysis include that it cannot be conducted for full tree communities, and that it
requires well-trained researchers and more sophisticated materials. In addition,
there are a number of methodological issues (Brienen et al. 2012a) that need to be
accounted for in tree-ring analysis. First, sampling issues arise due to the fact that
alive trees sampled in tree-ring studies may be (and are likely) a non-random subset
of the population, which may affect the outcome of analyses of growth trends over
time (Briffa and Melvin 2011; Brienen et al. 2012a). Dealing with these biases
requires the sampling of trees of all sizes (Brienen et al. 2012a; Nehrbass‐Ahles
et al. 2014). Some biases cannot be prevented by adjusting sampling schemes in the
field, and need to be assessed by additional statistical analyses (Groenendijk et al.
2015) or simulations (Vlam 2014). Second, analyses of trends require that temporal
trends in growth, isotope values or derived variables (e.g., iWUE) are separated
from those occurring over the size range (or age range) of trees. Third, age dis-
tributions and recruitment waves of tree species may also affect the outcome of
analyses of trends (Vlam 2014). There is a need for critical methodological eval-
uations and the development of statistical and simulation tools to evaluate the
robustness of trends detected based on tree-ring analyses (Briffa and Melvin 2011;
Brienen et al. 2012a; Vlam 2014; Peters et al. 2015). We therefore call for a
cautious interpretation of published trends in growth, iWUE or isotope values for
which such robustness checks are lacking.
So far, trends in iWUE and tree-ring width have been evaluated for a small
number of tropical tree species. In several of these studies the abovementioned
methodological issues have not been (sufficiently) taken care of, potentially
affecting the sign and strength of trends in iWUE or growth. For instance, a number
of studies on trends in iWUE over time have not or insufficiently separated the
strong ontogenetic trend in iWUE from that occurring over time due to CO
2
rise
(Hietz et al. 2005; Nock et al. 2010; Brienen et al. 2011; Locosselli et al. 2013).
A recent study on 12 tree species across three tropical regions (Van der Sleen
et al. 2014) evaluated trends in iWUE for fixed diameter categories (8 and 27 cm
diameter), thus explicitly accounting for ontogenetic changes, and revealed a
30–35 % increase in iWUE over the last 150 years. A study on several Amazonian
species used the same approach to account for ontogenetic growth patterns and
reported increased growth rates for small individuals but not for large trees
(Rozendaal et al. 2010). These trends however may be confounded by differences
in survival of fast and slow growing trees (Brienen et al. 2012a). In a study on three
Thai species, decreasing growth trends were found (Nock et al. 2010) which may
partially have been generated by ontogenetic patterns and by effects of forest dis-
turbances. And finally, in the abovementioned pan-tropical study (Van der Sleen
et al. 2014) no growth increases were observed for 12 species over the past 100–
150 years. While these studies have explicitly addressed or discussed the effect of
several of the abovementioned biases, the reported trends may nonetheless have
been affected by forest disturbance and absence of tree regeneration (cf. Vlam
2014), and other biases (cf. Groenendijk et al. 2015).
452 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
In all, tree-ring studies in the tropics revealed (modest) increases in iWUE that
can be associated with the historical rise in atmospheric CO
2
levels. So far, the
contribution of tree-ring and isotope analyses to generating insights on responses of
tropical trees to global change has been small, in part due to the abovementioned
methodological issues (biases), but also a limited research effort in the tropics.
Nevertheless, this contribution can potentially be substantial if sampling designs
and statistical analyses are appropriate, biases are taken into consideration and
results are interpreted cautiously.
Advances in Stable Isotope Measurements in Tropical
Tree Rings
Analysis of stable isotopes (δ
18
O, δ
13
C) is increasingly being used in tropical tree
rings. Such measurements provide additional information: carbon isotopes mainly
provide a measure for plant physiology (i.e., the magnitude of isotope discrimi-
nation is related to the ratio between carbon fixed per water lost; McCarroll and
Loader 2004), while oxygen isotopes reflect variation in isotopic composition of the
source water, tree transpiration rates and relative humidity (Sternberg 2009). In the
section below, we will outline some recent advances on applications of isotope
analysis in tropical tree rings, and the main insights obtained.
Carbon isotopes in tree rings provide a good drought signal in sites where
moisture stress is limiting growth (Gebrekirstos et al. 2009; Fichtler et al. 2010;
Brienen et al. 2011; Schollaen et al. 2013). During dry years stomatal aperture
decreases, leading to reduced influx of CO
2
into leaf intercellular spaces, and thus a
lower intercellular [CO
2
](ci) and lower isotope discrimination (Δ). An example of
the effect of precipitation on intercellular CO
2
concentrations (derived from carbon
isotopes in tree rings) for a dry forest species from southern Mexico is shown in
Fig. 5f. At sites where trees experience less drought stress, the dominant factor
controlling tree ring δ
13
C may be the photosynthetic rate affected by irradiance (cf.
McCarroll and Loader 2004). In line with this, a study on a moist tropical tree species
comparing δ
13
C in tree rings before and after gap formation shows a positive rela-
tionship between δ
13
C and growth, thus suggesting variation in growth was most
strongly driven by temporal changes in light availability (van der Sleen et al. 2014).
These studies show the potential for carbon isotope measurements in tree rings to
help interpret the causes of temporal growth rate variation in tropical trees.
Oxygen isotopes in tree rings reflect variation in source water δ
18
O and plant
physiological effects like leaf water enrichment due to transpiration (Sternberg
2009). Correlations of inter-annual variation in tree ring δ
18
O of tropical trees with
precipitation δ
18
O, suggest that plant physiological effects are not very pronounced
and that tree rings in these species mainly record source water influences (Brienen
et al. 2012b,2013; Schollaen et al. 2013). Figure 5g shows the relationship between
tree ring δ
18
O from southern Mexico and precipitation δ
18
O from San Salvador (ca.
700 km away). This shows that variation in source water δ
18
O (even from distant
Tree Rings in the Tropics: Insights into the Ecology …453
r.brienen@leeds.ac.uk
stations) explains more than 60 % of the variation in tree ring δ
18
O, but the degree
to which source water controls tree ring δ
18
O may vary between sites and species.
Variation in source water δ
18
O depends on local precipitation intensity (i.e., the
amount effect, cf. Dansgaard 1964), the origin of the water source, and rainout
processes during water vapour transport. For which of these processes tree ring
δ
18
O provides a proxy, depends on the location and geography of the site. In the
western Amazon, δ
18
O in tree rings proved to be a strong indicator of total
basin-wide precipitation and river discharge (Brienen et al. 2012b), while tree ring
δ
18
O at other (less continental) sites shows good correlations with more regional
precipitation amounts (Poussart and Schrag 2005; Xu et al. 2011; Brienen et al.
2013; Schollaen et al. 2013).
Recent technical developments in isotope techniques allow for very precise
dissection of small wood at high resolution (e.g., Schollaen et al. 2013). This has
permitted the detection of annual cycles in species that lack anatomically distinct
rings, which could subsequently be used to infer growth rates, determine tree ages,
or relate the isotope or growth signals to climate (Poussart et al. 2004; Anchukaitis
and Evans 2010; Schollaen et al. 2013; Xu et al. 2014). In addition, high-resolution
isotope series of δ
13
C has provided insights into differences between evergreen and
deciduous species in allocation of photosynthates to reserves versus wood (Ohashi
et al. 2009; Gulbranson and Ryberg 2013), and high-resolution oxygen isotopes
may allow for more detailed seasonal reconstructions of historical rainfall regimes.
For instance, it may allow studying differences in dry versus wet season precipi-
tation (Schollaen et al. 2013), and can be used to detect short-term climate events
caused by the El Niño-Southern Oscillation (ENSO) (Evans and Schrag 2004;
Anchukaitis and Evans 2010) or tropical cyclones (Li et al. 2011).
Finally, a few other useful techniques include the measurement of wood density
using gamma radiation, X-ray or high-frequency densitometry (Schinker et al.
2003; De Ridder et al. 2010). High-resolution densitometry measurements could
greatly assist ring boundaries detection, for those species presenting growth
boundaries defined by density variation (cf. Fig. 2d, e), and density variations
themselves may contain climate information. For example, Worbes et al. (1995)
found a significant relationship between density variations and the length of the
terrestrial phase in floodplains of Central Amazonia.
Conclusions
While the study of tropical tree rings started over a century ago, most advances in
this field have been made during recent decades. Important insights arising from
these recent tropical tree-ring studies in relation to the theme of this book include:
•Tree-ring analyses of 71 tropical species shows that tree longevity is shorter than
often believed (mean longevity ca. 200 years), suggesting relatively fast rates of
turnover and carbon cycling in tropical biomes.
454 R.J.W. Brienen et al.
r.brienen@leeds.ac.uk
•Individual tropical trees show incredibly strong and persistent variation in
long-term growth rates, resulting in a fourfold variation in the ages of similarly
sized trees. Interestingly, this intraspecific growth variation exceeds the
long-term growth variation between species.
•A review of the climate sensitivity of tropical trees shows that annual growth of
tropical tree species is more sensitive to fluctuations in rainfall than temperature.
While informative for tree sensitivity to climatic fluctuations, these results
cannot be directly used to predict growth responses to long-term and gradual
changes in temperature or rainfall.
•Long-term trends in water use and growth can be obtained from measurements
of stable isotopes and tree-ring width, but such analyses need to take sampling
biases and other methodological issues into account. So far, few long-term
studies have revealed evidence for century-long increases in intrinsic water use
efficiency of several tropical tree species. These results indicate that tropical tree
physiology is changing, most likely due to rising CO
2
.
•Combined studies on tree ring width and stable isotopes are promising to gain
new insights into the response of tropical vegetation to climate change, validate
coupled climate-vegetation models and diagnose large–scale changes in the
climate system.
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