Annual Tree Rings in The Rainiest Forests of The Americas: Jorge Andrés Giraldo Jiménez

Annual Tree Rings in the Rainiest
Forests of the Americas
Jorge Andrés Giraldo Jiménez
Universidad Nacional de Colombia

Facultad Ciencias Agrarias, Área Curricular en Bosques y Conservación Ambiental
Medellín, Colombia
2021
Annual Tree Rings in the Rainiest
Forests of the Americas
Jorge Andrés Giraldo Jiménez
Tesis o trabajo de investigación presentada(o) como requisito parcial para optar al título
de:
Doctorado en Ecología
Director:
Maestro Universitario, Jorge Ignacio del Valle
Línea de Investigación:
Dendrocronología tropical
Grupo de Investigación:
Bosques y Cambio Climático
Universidad Nacional de Colombia

Facultad Ciencias Agrarias, Área Curricular en Bosques y Conservación Ambiental
Medellín, Colombia
2021
A Catalina, con amor, por su paciencia y apoyo
en este largo proceso.
Agradecimientos
Quiero expresar mi agradecimiento al profesor Jorge Ignacio del Vale, quien propició esta
investigación y me permitió participar de ella. A él agradezco haberme presentado el
sendero de la ciencia. Aprecio enormemente la ayuda brindada por los miembros del
Centro Forestal Tropical Pedro Antonio Pineda de la Universidad del Tolima, por abrirnos
sus puertas y su hospitalidad, facilitando el acceso a los bosques del Bajo Calima: Nelson
Albarán, Faber Hernández, Luz Amalia Forero, Omar Melo, Silvio Soliz, Héctor Palacio,
Nilson Murillo (Juaco), Oscar Murillo, Sebastián Moreno. Agradezco a la Comunidad de las
Brisas (Bajo Calima), particularmente a Sixto Cáceres y Iris Valencia por apoyar los
muestreos de campo, su apoyo fue vital durante todas las campañas de campo.
Gracias a Carlos A. Sierra, por sus constructivos comentarios, por gestionar y aceptar mi
pasantía en el Instituto Max Planck para la Biogeoquímica. A David Herrera, agradezco su
hospitalidad y apoyo durante mi estancia en Jena.
Gracias al Herbario Medel de la Universidad Nacional de Colombia y a Jorge Mario Vélez

por la ardua labor de identificación botánica. Agradezco a todas las personas que nos
apoyaron en diferentes etapas de la investigación: Andrés Caro, Diego David, Marileny
Vásquez, Alejandro Torres, Mauricio Herrera, Mario Santa, Alejandro Gómez, Wilmar
López, Juan Luis Posada, Alejandro Castaño, Wilson Lara, Alejandro Gómez, Sebastián
González.
Esta investigación fue apoyada por el proyecto 4083 de la Universidad Nacional de

Colombia, proyecto 1118-714-51372 de Colciencias, por el Instituto Max Planck para la
Biogeoquímica y por la beca para estudiantes de doctorado Nacionales de COLCIENCIAS
(Convocatoria 785).
Abstract IX
Abstract
In this dissertation, I explore the dendrochronological potential of trees from a lowlands
tropical wet forest (Precipitation over 7,200 mm y-1), without seasonal water deficit or
flooding. I study the causes and sensitivity of annual growth rings to climate variables in
several tree species by different methods. I analyzed the anatomical features of 81 tree
species (~ 45% showed well-defined tree rings) (Chapter 1). Then I present results of tree
ring frequency and possible causes of tree ring formation. I observed both positive and
negative growth answers to water and light availability, depending on the tree species,
suggesting that either excess or deficit of growth factors may explain seasonal growth
rhythms in some trees (Chapter 2). This fact is also observed by the intra-annual variability
of stable isotopes in tree rings (Chapter 3). As a study case, I present a practical application
of dendroecology as an effective tool for resolving disputes in forensic sciences, the first
carried in the biogeographic Chocó region (Chapter 4). This research opens a new frontier
for tree rings science, the ever-wet tropical forests without water deficit.
Keywords: dendrochronology, Chocó region, radiocarbon, stable isotopes, tropical trees.

X Annual Tree Rings in the Rainiest Forests of the Americas
Anillos de crecimiento anuales en la región más

lluviosa de las Americas
Resumen
En esta disertación, exploro el potencial dendrocronológico de los árboles de los bosques

siempre húmedos tropicales (Precipitación superior a 7,200 mm año-1), que no presentan
déficit hídrico o inundaciones periódicas. Se estudian las causas y la sensibilidad de los
anillos de crecimiento anuales a variables climáticas en muchas especies de árboles, a
través de diferentes métodos. Son analizadas las características anatómicas de la madera
en 81 especies de árboles (~ 45% presentan anillos de crecimiento bien definidos)
(Capítulo 1). En el Capítulo 2, se presentan los resultados de la frecuencia de anillos en
muchas especies y se exploran los posibles detonantes ambientes de su formación. Se
obtienen observaciones tanto positivas como negativas entre el crecimiento, el agua y la
disponibilidad de luz, dependiendo de la especie; lo cual sugiere que tanto el déficit como
el exceso del crecimiento pueden ser factores que determinan el crecimiento rítmico en
algunas especies de árboles. Dicha evidencia También es observada a través de la
variabilidad intra anual de las proporciones isotópicas del oxígeno en la celulosa
(δ18Ocelulosa) (Capítulo 3). Como un caso de estudio, se presenta una aplicación práctica de
la dendrocronología como una herramienta efectiva para resolver disputas legales, siendo
ese el primer ejemplo de dicha aplicación, llevado a cabo en la región biogeográfica del
Chocó (Capítulo 4). Esta investigación abre una nueva frontera en la ciencia de los anillos
de crecimiento, los bosques siempre húmedos tropicales carentes de déficit hídrico.
Palabras clave: dendrocronología, Región del Chocó Biogeográfico, radiocarbono,

isótopos estables, árboles tropicales.
Contents XI
Contents
Pág.
Introduction ....................................................................................................................... 1
1. Chapter 1. Dendrochronological potential of trees from America's rainiest

region ................................................................................................................................. 5
1.1 Introduction ....................................................................................................... 6
1.2 Materials and methods ...................................................................................... 7
1.2.1 Study area .............................................................................................. 7
1.2.2 Dry month analysis in study area ........................................................... 8
1.2.3 Sampling ................................................................................................ 9
1.2.4 Processing of wood samples .................................................................. 9
1.2.5 Observable anatomical characteristics ................................................. 10
1.2.6 Growth ring periodicity .......................................................................... 10
1.2.7 Pantropical growth ring potential .......................................................... 11
1.3 Results and discussion ................................................................................... 11
1.3.1 Biodiversity of the Chocó Region ......................................................... 26
1.3.2 About tree-rings formation in tropical hyper-humid regions .................. 27
1.3.3 Dendrochronological potential studies around tropics: Unclear pattern28
1.3.4 Species in this chapter with annual rings reported in other regions ..... 37
1.4 Conclusions..................................................................................................... 47
2. Chapter 2: Growth rhythms of trees from the rainiest neotropical region ......... 49
2.1 Introduction ..................................................................................................... 50
2.2 Materials and methods .................................................................................... 52
2.2.1 Study area ............................................................................................ 52
2.2.2 Tree-ring samples and dating ............................................................... 54
2.2.3 Environmental data .............................................................................. 55
2.2.4 Field measurements ............................................................................. 55
2.2.5 Data analyses ....................................................................................... 56
2.3 Results ............................................................................................................ 57
2.4 Discussion ....................................................................................................... 64
2.5 Conclusions..................................................................................................... 66
3. Chapter 3: Isotope signatures in tree rings reveal growth rhythms occurring in

the least rainy season in a hyper-humid neotropical forest ....................................... 67
3.1 Introduction ..................................................................................................... 68
3.2.1 Study area ............................................................................................ 70
3.2.2 Sampled species .................................................................................. 71
3.2.3 Preparation of the Wood samples ........................................................ 72
XII Título de la tesis o trabajo de investigación
3.2.4 Stable isotope analysis ........................................................................ 74

3.2.5 Oxygen isotopes in rain ........................................................................ 74
3.2.6 Statistical analysis ................................................................................ 75
3.3 Results ............................................................................................................ 75
3.4 Discussion ....................................................................................................... 81
3.5 Conclusions .................................................................................................... 84
4. Chapter 4. Radiocarbon and dendrochronology applied in a legal dispute: A

case from Colombia ........................................................................................................ 87
4.1 Introduction ..................................................................................................... 88
4.2.1 Study area ............................................................................................ 90
4.2.2 Field sampling ...................................................................................... 90
4.2.3 Sample preparation .............................................................................. 90
4.2.4 Tree ring analysis ................................................................................. 91
4.2.5 Radiocarbon analysis ........................................................................... 92
4.3 Results ............................................................................................................ 93
4.4 Discussion ....................................................................................................... 96
4.5 Conclusion ...................................................................................................... 98
5. General conclusions ............................................................................................... 99
A. Appendix: Age determination by post-bomb 14C and by tree rings .................. 103
Bibliography .................................................................................................................. 111

Introduction
Tree growth rhythms are seasonal events observed on different plant tissues and organs
such as vascular cambium, leaves, branches, and reproductive structures (Albert et al.
2019), genetically determined but modulated by environmental conditions (Lüttge and
Hertel 2009; Fyllas et al. 2017). Vascular cambium rhythm is related to tree size increment
(i.e., tree growth), commonly observed as wood anatomy changes due to variation in growth
rate. Such wood anatomy changes appear as an accumulation of layers, also known as
tree rings (Fritts 1976).
In the last century, the belief that tropical trees had no growth rings because of a lack of
thermal or photoperiod seasonality, compared with temperate and boreal regions (Jacoby
1989; Whitmore 1990; McCarroll and Loader 2004; Turner 2004; Begon et al. 2006), led to
the slow development of the tropical dendrochronology. However, when considering
different triggering factors, tree-rings research in the tropics increased nearly exponentially.
Over the last two decades, many studies have demonstrated the occurrence of annual tree
rings in diverse tropical ecosystems such as semi-arid, dry, semi-deciduous, humid, and
wet forests, savannahs, floodplains, estuaries, mangroves, and high mountains trees
(Schöngart et al. 2002, 2017; Worbes 2002; Brienen and Zuidema 2005; Zuidema et al.
2012; Brienen et al. 2016). While temperature, water availability, and light availability may
control tropical trees growth, varying across species and ecosystems (Rozendaal and
Zuidema 2011); rainfall seasonality and flooding are considered the main dominant triggers
to explain annual growth rings in lowland tropical trees (Brienen et al. 2016; Schöngart et
al. 2017).
The booming of dendrochronology in tropics has allowed answering several questions

about ecology, conservation, climatology, hydrology, growth modeling to sustained forest
management, modeling the ontogenetic growth to obtain significant population traits as life
span, mean life, and life expectancy, the phases of release and suppression of tree growth
in forests, among others (Schöngart 2008; Rozendaal 2010; Ballantyne et al. 2011; Giraldo
2 Introduc
and del Valle 2011; Inga and del Valle 2017; Stahle et al. 2020). But most studies still focus
on studying tree growth patterns, wood anatomy, and the causes and sensitivity of tree ring
to climate variables (Schöngart et al. 2017; Marcelo-Peña et al. 2020; Pearl et al. 2020),
probably due to the highly diverse ecosystems in which tree species develop different
growth strategies.
Even though annual growth rings in many tropical tree species could be explained mainly
by the seasonal water availability paradigm (Wagner et al. 2012; Brienen et al. 2016;
Mendivelso et al. 2016; Schöngart et al. 2017); the environmental triggers of the growth
ring in trees of the lowlands tropical rainforests (Precipitation over 7,200 mm y-1), without
seasonal water deficit or flooding, remain unexplored. This probably has been occurred by
sampling difficulties or because scientists were unaware of the existence of such
ecosystems.
Tropical tree diversity tends to increases with precipitations. Wetter tropical forests sustain
the most diverse plant communities on Earth (Gentry 1988; Givnish 1999). Along the Pacific
coast of South America, from Northern Ecuador to the Colombian–Panamanian Darien
Gap, the Biogeographic Chocó Region is found, the rainiest on all American continents.
This Region includes, according to recent research (Mesa and Rojo 2020), the rainiest
place on Earth located at López de Micay village, which exceeds the 13,000 mm mean
annual rainfall, is about 120 km South far from the study area. The Chocó Region is home
to one of the greatest biological diversity on Earth, including many endemic species (Gentry
1988, 1989; Faber-Langendoen and Gentry 1991; Myers et al. 2000). The low-level jet
stream (tropopause air current) centered around 5°N, known as the Chocó Jet, explains
the high regional precipitation (Mesa and Rojo 2020). However, this region of the American
Pacific is poor on instrumental records. Therefore, paleoclimatic records with an annual
resolution are urgent to help determine with less uncertainty the trends of global change in
the region.
Through this dissertation, I study the cambial growth rhythms (tree rings) and their
frequency of the Chocó region. I explore possible causes and sensitivity of the growth rings
to climate variables in several species from a lowland wet non-seasonal tropical forest with mean
annual rainfall over 7,200 mm.
Introduc 3
Hypothesis
According to Liebig's law, the growth of an organism is not controlled by all the available
resources (light, temperature, water, nutrients, etc.); but by the scarcest resource in the
environment, the limiting factor (Taylor 1934). This law is a simplification of the physiological
response of plants to environmental pressure (Jones 1997). The limiting factor that controls
annual tree growth each year represents the main variable recorded in the tree-rings
thickness (Speer 2010; Stine 2019). Under this view, light availability, mainly
photosynthetically active radiation, could be a limiting factor in high cloud cover regions
such as non-seasonal hyper-humid forests. In particular, the light limitation could be
extreme in the rainiest months in which cloud cover increases, inducing an annual pattern
on tree growth (Restrepo-Coupe et al. 2013; Green et al. 2020). Then, the interaction
between light and water availability may drive tree growth rhythms in tropical hyper-humid
forests.
In ecology is well established that both deficit and excess of a growth factor produce stress
limiting the plant growth (Schulze et al. 2019). Therefore, a law of the minimum and a law
of the maximum should exist as limiting growth factors. These two laws are involved in
Shelford's tolerance law (Niinemets and Valladares 2008): If other factors are not limiting,
as the magnitude of a limiting factor increases, organisms respond by increasing their
growth, up to a limit at which the response saturates. Subsequent increases in this factor
produce less and less growth because the organism is growing under incremental stresses.
So, in ever wet forests, the availability of water, measured as rainfall, should be close to
the maximum tolerance threshold for some species. Hypothetically, too much precipitation
maintains high water saturation in the soil, which reduces its aeration and favors hypoxic
conditions in the roots limiting tree growth. I hypothesize that, in some species, light
availability, soil moisture, and slight variation in rainfall exert control on cambial growth
rhythms in hyper-humid tropical forests.
Throughout this dissertation, I try to contribute to the understanding of the causes of annual
tree-rings formation, as a consequence of rhythmic growth, in several tree species from the
biogeographic Chocó Region in Colombia. Classification of tree-ring structures in 82
species is contrasted with tropical literature. The dendrochronological potential of species,
according to tree-ring visibility, is inferred from radiocarbon dating, dendrometers, cross-
dating, or the stable isotopes 13C and 18O. I use these data to determine the sensitivity to
4 Introduc
climate variables as a surrogate of growth drivers. In a less rainy area of the same
biogeographic region, I present a practical application of both annual tree rings and
radiocarbon dating as an effective tool for resolving disputes in forensic sciences.
This dissertation probably contains the first dendroecological studies carried out in tropical
hyper-humid forests, without an evident hydric seasonality, due to water deficit or flooding.
The objectives of this study are

▪ to determine the occurrence of tree rings structures in tropical tree species from the
Biogeographic Chocó Region;
▪ to determine the promising species for dendrochronology according to an
anatomical classification;
▪ to determine growth rings frequency in tree species by different methods
(radiocarbon, cross-dating, and dendrometer observations);
▪ to assess possible environmental drivers of tree-rings formation;
▪ to establish the intra-annual variability of δ13C and δ18O in tree rings in two species
and to explore their relationships with environmental variables;
▪ to evaluate the use of annual tree rings and radiocarbon dating as tools to resolves
disputes in forensic sciences.
1. Chapter 1. Dendrochronological potential of
trees from America's rainiest region
With Jorge I. del Valle, Carlos A. Sierra, Omar Melo
Published in Pompa-García M., Camarero J. (eds) Latin American Dendroecology.

Springer. https://doi.org/10.1007/978-3-030-36930-9_5
Abstract: Hydric seasonality, dry or flooding periods, has been the explanation given by
dendrochronologists for the formation of growth rings in tropical trees. However, under
tropical hyper-humid conditions, there are species with growth periodicity and, therefore,
with visible growth rings useful for dendrochronology. We classify, for the first time, the
anatomical structures of the growth rings of the tropical trees from the Biogeographic Chocó
Region. An annual rainfall >7,200 mm without hydric seasonality characterizes the studied
forest. We classify the tree rings as present (well or poorly defined), or absent. We also
considered the feasibility of tree-rings dating (dendrochronological potential). We
characterized 81 species of trees belonging to 38 families. About 82% of species with
growth rings, 46% well defined, and 36% poorly defined. Absent rings in only 18%.
Dendrochronological potential was high (14%), medium (25%), low (43%), and null (18%).
We contrast our results with vast literature around tropics. Our results suggest that still
without any hydric seasonality, many tropical tree species develop growth rings. Our
findings drive to new questions: What is the periodicity of tree rings in these non-seasonal
hyper-humid environments? What other subtle seasonality could be involved in the growth
periodicity of these species, or are they genetic?
Keywords: Tree rings, Non-seasonal rainfall, Biogeographic Chocó Region, Colombia

6 Annual Tree Rings in the Rainiest Forests of the Americas
1.1 Introduction
In dendrochronology, the current paradigm states that exists a more likelihood of growth-
rings formation in these cases: (1) in seasonally dry climates - water deficit- (Détienne and
Barbier 1988; Vetter and Botosso 1989; Worbes 1995, 1999; Bullock 1997; Jalil et al. 1998;
Borchert 1999; Enquist and Leffler 2001; Schöngart et al. 2002, 2017; Marcati et al. 2006;
Brienen et al. 2009, 2016; Morel 2013; Groenendijk et al. 2014; Silva et al. 2019; Granato-
Souza et al. 2019), (2) in periodically flooded environments which produce anoxic
conditions for the root system (Worbes and Junk 1989; Schöngart et al. 2002, 2017;
Worbes and Fichtler 2010; Brienen et al. 2016; Parolin et al. 2016), (3) in estuaries, due to
variability in salt concentration (Menezes et al. 2003; Chowdhury et al. 2016; Phan et al.
2019), (4) in deciduous or semi-deciduous species (Borchert 1999; Lisi et al. 2008; Nath et
al. 2016; Shimamoto et al. 2016), and (5) under seasonal variations in irradiance, time of
sunrise or sunset, or sunlight intensity (Breitsprecher and Bethel 1990; Clark and Clark
1994; O´Brien et al. 2008; Marcati et al. 2016; Shimamoto et al. 2016; Lotfiomran and Köhl
2017). According to literature cited, hydric seasonality, dry periods, or periodic floods, are
the dominant triggering variables for the formation of growth rings in tropical trees.
Because of high cloud cover limits the availability of photosynthetically active radiation
(Clark and Clark 1994), even in non-seasonal tropical forests, light appears to be the most
limiting factor during the rainy season. Cloudiness induces a reduction in photosynthetic
photon flux density (PPFD): the higher the cloud cover, the greater is the reduction in PPFD
(Graham et al. 2003). Besides, seasonal water highlighted the predominant role of water
availability that determined seasonal variation in tree growth (Wagner et al. 2012). The
availability of water in the soil could be more determinative than rainfall in the formation of
annual rings (Détienne and Barbier 1988; Falcon-Lang 1999; Silva et al. 2019). On the
other hand, the excess of water in the soil, cloudiness, and low solar radiation in wet tropical
climates could result in reduced photosynthesis, lower rates of tree growth, and low aerial
biomass in the forests (Álvarez et al. 2017).
Some researchers have found that trees of boreal origin (Laurasia) tend to form growth
rings more frequently than those of tropical origin (Fahn 1967; Tomlinson and Craichead
1972; Aguilar-Rodríguez and Barajas-Morales 2005). This type of growth rings, like a
fingerprint of its phytogeographic origin, implied that their formation is from the genetic
Chapter 1 7
background. The variables that trigger the formation of growth rings in tropical trees can
affect species in the same forest differently. For instance, species with annual growth rings
from the Atlantic rainforests in Brazil responded to four different triggering variables: the
period of leaves abscission, flooding, photoperiod, and endogenous periodicity (Callado et
al. 2001).
Although information on growth periodicity of trees species in tropical hyper-humid, non-

seasonal climates is scarce, there are species where periodic growth observed through
annual measurements of diameter (Clark and Clark 1994), phenological observations
(Frankie et al. 1974), cambial activity (Breitsprecher and Bethel 1990; O´Brien et al. 2008;
Bräuning et al. 2009), and annual rings (Fichtler et al. 2003; Moreno and del Valle 2014).
All of these measurements suggested the existence of a possible triggering of growth rates
associated with rainfall, the duration of the day, the angle of insolation, or a combined
response between rain and light levels. The evaluation of species with growth rings is the
first step in selecting those potentially useful in dendrochronological studies (Tarhule and
Hughes 2002; Tanaka 2005; Groenendijk et al. 2014; Silva et al. 2016; Islam et al. 2018).
The presence of growth rings suggests the existence of growth periodicity, which is
probably regulated by some environmental factor. In this study, for the first time, we perform
an anatomical classification of the tree-ring structure in the rainiest region of the Americas,
the Colombian Pacific, in a lowland, wet, non-seasonal tropical forest with mean annual
rainfall >7200 mm. The discovery of species with dendrochronological potential in a tropical
hyper-humid and non-seasonal region would open a new frontier in dendrochronology.
1.2 Materials and methods
1.2.1 Study area

The Chocó Biogeographic Region extends across the Pacific of South America, from
northern Ecuador to the Colombian-Panamanian Darien Gap. Most of this region, the
rainiest in the New World (Poveda and Mesa 2000), is located along the Colombian Pacific
coast, on the western flank of the Western Cordillera of the Andes. In some sites, mean
annual precipitation exceeds 12,000 mm, with extremes of 18,449 mm in 1953 and 19,839
mm in 1936 (Mesa et al. 1997). The study was conducted in a wet tropical forest in the
Holdridge system (Holdridge 1967) with 4,000 - 8,000 mm mean annual precipitation.
Specifically, the study area belongs to the Low Calima River Basin, where the Tropical
Forest Centre Pedro Antonio Pineda of the University of Tolima (3°55Ń, 77°07´W) is
located there (Figure 1-1), which includes an area of influence of 66,700 ha of forest that
belongs to the Community Council of the Low Calima River Basin.
Figure 1-1: Study area in the Biogeographic Chocó Region, located both in the wet tropical
forest and tropical rain forest life zones (Holdridge 1967). Walter and Lieth' ombrothermic
climate diagram (Walter et al. 1975) of the Low Calima Climatic Station (triangle), which
belongs to the Institute of Hydrology, Meteorology and Environmental Studies (IDEAM).
The dark area indicates an excess of water year around (all months are hyper-humid)
1.2.2 Dry month analysis in study area

The climatic diagram (Figure 1-1) used widely by dendrochronologists incorporates the
xerothermic index for intertropical climates of Gaussen (Bagnouls and Gaussen 1957).
According to this criterion, a month is dry if rainfall is less than twice the mean monthly
temperature expressed in millimeters of rain. For our case, that would be approximately
25.9 (2) = 51.8 mm. Even in February, the least rainy month, rainfall exceeded the dry
month criterion by 7-fold: 350 mm compared with 51.8 mm. The North American
climatologist (Thornthwaite 1948) incorporated the concept of Potential Evapotranspiration
(PET) calculated from air temperature and day length. Under this concept, a month was dry
Chapter 1 9
if the precipitation was lower than the PET. (Holdridge 1967) developed an approximate
formula based only on the mean monthly temperature to calculate the monthly PET. This
formula, which is near the thermic tropic where our area of study is located, calculates
Thornthwaite´s PET very well. As in the study area, the mean annual temperature and the
mean temperature for each month were almost the same (Figure 1-1). If we assume that
every month had 30.4 days, the Holdridge (1967) formula allowed us to estimate the
monthly PET = (58.93) (25.9) / 12 = 127 mm. That is to say, the xerothermic index of
Gaussen underestimated PET by about 2.4- times. However, even using the PET criterion,
which is much more demanding than Gaussen's xerothermic index, rainfall in February still
exceeded PET by about 2.7-times
1.2.3 Sampling
In the study area, a local Afro-Colombian ethnic group that inhabits these forests belonging
to the Community Council of the Low Calima River Basin, among the subsistence,
economic, and cultural activities they carry out, there is a sporadically felling of trees in
small areas of the forest. As virtually all the species of trees existing there has some use in
the wood market, from these trees, we collected complete cross-sectional discs. Then, this
sampling was reasonably at random as recommend (Speer 2010) to represent a landscape.
We also collected fifteen species existing in the region, but that did not appear in the
sampling. They were found within the experimental area and arboretum of the Pedro
Antonio Pineda Tropical Forest Center of the University of Tolima, most of them with
increment borers because of restrictions of the University. For this purpose, we extracted
2-3 cores 5 mm in diameter from the trees at 1.3 m above the ground approximately. The
holes produced by the increment borer were filled with wax, and antibacterial and healing
products, to avoid penetration by insects and pathogens. From each tree, we also collected
leaves, flowers, and fruits, whenever present, to aid in taxonomic identification.
1.2.4 Processing of wood samples

Wood samples were taken to the Tropical Dendroecology Laboratory of the National
University of Colombia, Medellín, and dried to a constant weight at 28°C. Then, to highlight
the growth rings, the samples were polished successively with abrasive sandpapers, from
60 to 600 grains. Samples were scanned at a resolution of 1,800 - 2,400 dpi in an Epson
Expression 10,000XL Scanner. The high-resolution images allowed macroscopic
characteristics to be observable up to 10-15µm. All images were processed with ImageJ
11.52i Software (Schindelin et al. 2012).
1.2.5 Observable anatomical characteristics

We identified the growth rings according to their type: (A) density changes due to an
increase in the wall thickness of the fibers, (B) presence of marginal bands of axial
parenchyma, or (C) differences in the diameter, distribution, and grouping of the pores: ring-
porous, semi-ring-porous, and diffuse-porous. One or several types of these anatomical
structures can be present in the same sample. We classified the presence of growth rings
according to Silva et al. (2016) as well defined (+), poorly defined (±), or absent (-).
The analysis considers the difficulty or impossibility of dating the growth rings when are
many anomalies such as false rings, wedging rings, tangential discontinuity, or lost rings.
The analysis included the visual dating possibility of growth rings that is an essential
procedure in dendrochronology. We made this classification by visual inspection using
different degrees of magnification, granting these qualitative classifications: (1) null: there
were no growth rings; (2) low: several poorly defined growth rings, difficult to mark, lost
rings, too many together, or frequent tangential discontinuity; (3) medium: false or lost rings
were evident and not frequent; or (4) high: growth rings were clearly defined with tangential
continuity, and few false rings.
1.2.6 Growth ring periodicity

We determined the growth periodicity in some sampled species by using the bomb-peak
dating method (Worbes and Junk 1989; Fichtler et al. 2003). Samples were prepared
according to Steinhof et al. (2017) and were analyzed in an accelerator mass spectrometry
(AMS) at the radiocarbon laboratory of Max Planck Institute for Biogeochemistry in Jena,
Germany. To obtain chronological dates from the radiocarbon values, we used the
calibration software Cali-Bomb (Reimer et al. 2004).
Chapter 1 11
1.2.7 Pantropical growth ring potential

An exhaustive pantropical literature review was made on the dendrochronological potential
of trees covering from Northern Subtropic to Southern subtropic and from sea level to high
mountains. All types of known seasonality affecting the growth rings are included:
temperature, droughts, and floods. We compare our results with the pantropical revision in
terms of the number of studied species and percent of species with growth rings. We also
determined which species in our study were reported with annual rings in studies carried
out in seasonally climates from other neotropical regions.
1.3 Results and discussion

According to Gaussen xerothermic index (Bagnouls and Gaussen 1957) and the monthly
potential evapotranspiration (Holdridge 1967), in the study area (Figure 1-1), on average,
there are not ecologically dry months. However, because it is soil water-holding capacity
and not precipitation that is the crucial factor for tree growth, water limitation in some
species cannot be ruled out. Trees from wet environments are more water-demanding than
those from dry climates which is a species-specific trait (Silva et al. 2019).
Eighty-one species were sampled from 38 plant families after a month of sampling. From
the sampling, basically at random, it was found that 58% of the species were only
represented by a single tree, which shows the high richness and diversity of trees existing
in the study area. The families with the most number of species included Sapotaceae (7),
Fabaceae (7), Malvaceae (5), Chrysobalanaceae (4), Moraceae (4), Myristicaceae (4), and
Vochysiaceae (4). Of the total, 17 endemic species (21%) were recorded from Colombia:
Jacaranda hesperia, Dacryodes frangens, Marila macrophylla, Clusia leptanthera, Vismia
rufa, Quararibea foenigraeca, Sterculia aerisperma, Qualea lineata, and Vochysia artantha,
which included eight species endemic to the Low Calima River Basin Region: Licania
caldasiana, Tapura costata, Tachigali colombiana, Magnolia calimaensis, Pterandra
ultramontana, Henriettea maguirei, Coussapoa valaria, and Vochysia pacifica. In addition
to these, we sampled 14 endemic species of the Biogeographic Chocó Region (18%):
Campnosperma panamensis, Licania sp, Dipteryx oleifera, Humiriastrum procerum,
Gustavia occidentalis, Huberodendron patinoi, Phragmotheca siderosa, Otoba latialata,
Virola dixonii, Otoba lehmannii, Isertia pittieri, Pouteria buenaventurensis, Pouteria collina,
and Cecropia virgusa. The other species (not mentioned) have a much wider distribution
(Table 1-1).
The macroscopic structures observed in the analyzed species (Table 1-1, Figure 1-2,
Figure 1-3, Figure 1-4) can be seen with the naked eye or with only a few zooms as changes
in the form of alternate bands of light and dark areas. This was interpreted as increases in
wood density that were attributed to the thickening of the fiber cell walls (A), which may be
gradual or abrupt (Figure 1-2). This ring pattern was dominant in the sampled species (52%)
(Figure 1-4a). It sometimes occurred together with bands of marginal parenchyma (B)
(Figure 1-3), which was present in 36% of the species (Figure 1-4a).
In 82% of the studied species, we found growth rings; 46% were well defined (distinct rings),
and 36% were poorly defined with visible although faint rings. Only 18% of the species had
no growth rings or discontinuous bands, where it is difficult to establish if growth rings were
present (Figure 1-4b, Table 1-1).
The semi-ring-porous pattern (C), that is a characteristic generally reported in species that
grow in dry environments, or at least, with a dry season (Worbes and Junk 1999), was
exhibited by 13% of the species in combination with the other anatomical characteristics:
The combination A-C occurred in 9% of the species, the combination A-B-C occurred in
2%, and the B-C pattern only occurred in 1% (Figure 1-4a, Figure 1-5). Although the growth
rings were well defined, the possibility of dating them was not necessarily high, as occurred
in Symphonia globulifera, T. costata, Cedrela odorata, and other species, where the
possibility of dating them was only medium (Table 1-1). On the other hand, in species with
poorly defined rings, the possibility of dating them was null as in Hebepetalum humiriifolium,
low as in Cespedezia spathulata, or medium as in Pourouma bicolor; but never high.
Chapter 1 13
(a) (b) (c)
Figure 1-2: Species of trees sampled in the Low Calima River Basin, Biogeographic Chocó
Region, with growth rings that were defined by increases in fiber wall thickness (A): (a)
Apeiba macropetala, (b) Phragmotheca siderosa, (c) Posoqueria latifolia. The arrows
indicate the growth rings
(a) (b) (c)
Figure 1-3: Species of trees sampled in the Low Calima River Basin, Biogeographic Chocó
Region, with (A) growth rings defined by increases in fiber wall thickness and (B)
parenchyma bands: (a) Clarisia racemosa, (b) Zanthoxylum riedelianum, (c) Coussapoa
valaria. The arrows indicate growth rings
Table 1-1: Tree species sampled in the Low Calima River Basin, Biogeographic Chocó Region, characterized according to their growth
rings. Visibility: well defined (+), poorly defined (±), absent (-). Anatomical structure: density changes due to increased fiber wall
thickness (A), the presence of marginal bands of axial parenchyma (B), differences in diameter, distribution, and grouping of pores that
delimited the ring (C). Porosity: diffuse-porous, semi-ring-porous or ring-porous. The possibility of dating: high, medium, low
Potential in Numbe
Tree-ring Wood Vessel Type of
Family Species Dendrochrono r of Distribution
visibility anatomy antomy samples
logy trees
Campnosperma Biogeographic
Anacardiaceae - A Diffuse-porous None 2 Core
panamensis Standl. Chocó
Aspidosperma Cross-
Apocynaceae + A Diffuse-porous Low 1 Wide distribution
excelsum Benth. section
Aspidosperma
Cross-
Apocynaceae desmanthum Benth. + A Diffuse-porous Low 2 Wide distribution
section
ex Müll. Arg.
Jacaranda hesperia
Bignoniaceae + A Diffuse-porous High 2 Core Endemic
Dugand.
Bourreria
Semi-ring-
Boraginaceae costaricensis ± A,C Low 1 Core Wide distribution
porous
(Standl.) A.H Gentry
Dacryodes frangens
Cross-
Burseraceae Daly & M. C. - A Diffuse-porous None 1 Endemic
section
Martínez
Cross-
Burseraceae Protium sp. + A Diffuse-porous Medium 1 Wide distribution
section
Cross-
Calophyllum
Calophyllaceae ± A,B Diffuse-porous Low 14 section (5) - Wide distribution
longifolium Willd.
Core (9)
Marila macrophylla Cross-

Calophyllaceae ± A Diffuse-porous Low 1 Endemic
Benth. section
Potential in Numbe
logy trees
Cross-
Chrysobalanaceae Hirtella americana L. ± A Diffuse-porous Low 1 Wide distribution
section
Cross-
Chrysobalanaceae Hirtella sp. ± A,B Diffuse-porous Low 1 Wide distribution
section
Licania caldasiana Cross-

Chrysobalanaceae ± A,B Diffuse-porous Low 1 Endemic
Cuatrec. section
Cross- Biogeographic
Chrysobalanaceae Licania sp. - A Diffuse-porous None 1
section Chocó
Clusia leptanthera Semi-ring- Cross-

Clusiaceae ± A,C Low 1 Endemic
Cuatrec porous section
Symphonia Cross-
Clusiaceae + A,B Diffuse-porous Medium 1 Wide distribution
globulifera L. f. section
Tapura costata Semi-ring- Cross-

Dichapetalaceae + B,C Low 1 Endemic
Cuatrec. porous section
Cross-
Dichapetalaceae Sloanea sp. ± A Diffuse-porous Low 1 Wide distribution
section
Cross-
Erythroxylaceae NN + A Diffuse-porous Low 1 Wide distribution
section
Cross-
Euphorbiaceae Mabea sp. Aubl. + A Diffuse-porous High 2 section (1) - Wide distribution
Core (1)
Hevea brasiliensis
Cross-
Euphorbiaceae (Willd. ex A. Juss.) + A,B Diffuse-porous Medium 1 Wide distribution
section
Müll. Arg.
Dipteryx oleifera Cross- Biogeographic

Fabaceae ± A,B Diffuse-porous Medium 1
Benth. section Chocó
Chapter 1 17
Potential in Numbe
logy trees
Cross-
Fabaceae Inga acreana Harms + A,B Diffuse-porous Medium 1 Wide distribution
section
Inga rubiginosa Cross-

Fabaceae + A,B Diffuse-porous Medium 1 Wide distribution
(Rich.) DC. section
Schizolobium
Fabaceae parahyba (Vell.) S.F. + A,B Diffuse-porous Medium 1 Core Wide distribution
Blake
Pentaclethra
Fabaceae macroloba (Willd.) + A,B Diffuse-porous Medium 2 Core Wide distribution
Kuntze
Tachigali colombiana Cross-

Fabaceae + A Diffuse-porous High 3 Endemic
Dwyer section
Fabaceae Abarema sp. ± A,B Diffuse-porous Low 1 Core Wide distribution
Cross-
Goupiaceae Goupia glabra Aubl. + A Diffuse-porous High 21 Wide distribution
section
Humiriastrum
Humiriaceae procerum (Little) + A Diffuse-porous High 8
section Chocó
Cuatrec.
Cross-
Humiriaceae Sacoglottis sp. ± A Diffuse-porous Low 3 Wide distribution
section
Cross-
Hypericaceae Vismia rufa Cuatrec. - A Diffuse-porous None 1 Endemic
section
Cross-
Lauraceae Nectandra sp. + A Diffuse-porous Low 1 Wide distribution
section
Cross-
Lauraceae Ocotea sp. + A Diffuse-porous Low 1 Wide distribution
section
Potential in Numbe
logy trees
Couratari guianensis Cross-

Lecythidaceae + A Diffuse-porous Low 1 Wide distribution
Aubl. section
Cariniana pyriformis Cross-

Lecythidaceae + A Diffuse-porous High 14 Wide distribution
Miers. section
Gustavia occidentalis Cross- Biogeographic

Lecythidaceae + A,B Diffuse-porous Low 1
Cuatrec. section Chocó
Hebepetalum
Cross-
Linaceae humiriifolium ± A Diffuse-porous Low 7 Wide distribution
section
(Planch.) Benth.
Magnolia calimaensis
Magnoliaceae + A,B Diffuse-porous Medium 1 Core Endemic
(Lozano) Govaerts
Pterandra
Semi-ring- Cross-
Malpighiaceae ultramontana H.P. + A,C Low 2 Endemic
porous section
Riley ex Cuatrec.
Huberodendron Biogeographic
Malvaceae + A,B Diffuse-porous High 1 Core
patinoi Cuatrec. Chocó
Apeiba macropetala Semi-ring- Cross-

Malvaceae + A,C High 6 Wide distribution
Ducke porous section
Quararibea Cross-
Malvaceae ± A,B Diffuse-porous Low 1 Endemic
foenigraeca Cuatrec. section
Phragmotheca Cross- Biogeographic

Malvaceae + A Diffuse-porous Medium 2
siderosa Cuatrec. section Chocó
Sterculia aerisperma Semi-ring- Cross-

Malvaceae ± A,B,C Low 3 Endemic
Cuatrec. porous section
Cross-
Melastomataceae Henriettea maguirei - A,B Diffuse-porous None 1 Endemic
section
(Wurdack) Penneys,
Chapter 1 19
Potential in Numbe
logy trees
Michelang., Judd &

Almeda
Cross-
Melastomataceae Miconia sp. - A,B Diffuse-porous None 1 Wide distribution
section
Semi-ring- Cross-
Meliaceae Cedrela odorata L.1 + A,B,C High 1 Wide distribution
porous section
Dendrobangia Cross-
Metteniusaceae - A Diffuse-porous Low 2 Wide distribution
boliviana Rusby section
Castilla elastica var.

Cross-
Moraceae costaricana (Liebm.) + A Diffuse-porous Medium 1 Wide distribution
section
C.C. Berg
Clarisia racemosa Cross-

Moraceae + A,B Diffuse-porous Medium 1 Wide distribution
Ruiz & Pav section
Cross-
Moraceae Sorocea sp. ± A Diffuse-porous Low 1 Wide distribution
section
Moraceae Ficus sp. - A,B Diffuse-porous None 1 Core Wide distribution
Osteophloeum
platyspermum Cross-
Myristicaceae ± A Diffuse-porous Medium 2 Wide distribution
(Spruce ex A. DC.) section
Warb.
Otoba latialata Cross- Biogeographic

Myristicaceae + A Diffuse-porous High 11
(Pittier) A.H. Gentry section Chocó
Myristicaceae Virola dixonii Little + A Diffuse-porous High 4
section Chocó
Otoba lehmannii
Biogeographic
Myristicaceae (A.C.Sm.) ± A,B Diffuse-porous Medium 2 Core
Chocó
A.H.Gentry
Potential in Numbe
logy trees
Cross-
Myrtaceae Myrcia sp. - A Diffuse-porous None 1 Wide distribution
section
Syzygium
Myrtaceae malaccense (L.) - A Diffuse-porous None 1 Core Wide distribution
Merr. & L.M. Perry
Cespedesia
Semi-ring- Cross-
Ochnaceae spathulata (Ruiz & ± A,C Low 1 Wide distribution
porous section
Pav.) Planch.
Minquartia Cross-
Olacaceae - A Diffuse-porous Low 1 Wide distribution
guianensis Aubl. section
Hieronyma
Semi-ring-
Phyllantaceae alchorneoides + A,C Medium 3 Core Wide distribution
porous
ALLEMAO
Semi-ring- Cross-
Rhizophoraceae Cassipourea sp. + A,C Low 1 Wide distribution
porous section
Isertia pittieri Cross- Biogeographic

Rubiaceae - A Diffuse-porous None 1
(Standl.) Standl. section Chocó
Posoqueria latifolia Cross-

Rubiaceae + A Diffuse-porous Medium 1 Wide distribution
(Rudge) Schult. section
Zanthoxylum
Cross-
riedelianum subsp.
Rutaceae ± A,B Diffuse-porous Low 7 section (1) - Wide distribution
hygrophilum
Core (6)
(Cuatrec.) Reynel
Casearia arborea Cross-

Salicaceae ± A Diffuse-porous Low 1 Wide distribution
(Rich.) Urb. section
Cross-
Sapotaceae Manilkara sp. ± A Diffuse-porous Low 1 Wide distribution
section
Chapter 1 21
Potential in Numbe
logy trees
Pouteria
Sapotaceae buenaventurensis ± A Diffuse-porous Low 2
section Chocó
(Aubrév.) Pilz
Pouteria engleri Cross-

Sapotaceae + A Diffuse-porous Medium 1 Wide distribution
Eyma section
Pouteria collina Cross- Biogeographic

Sapotaceae + A,B Diffuse-porous Medium 1
(Little) T.D. Penn. section Chocó
Pouteria eugeniifolia Cross-

Sapotaceae - A Diffuse-porous None 3 Wide distribution
(Pierre) Baehni section
Cross-
Sapotaceae Pouteria sp. - A,B Diffuse-porous None 1 Wide distribution
section
Cross-
Sapotaceae Pouteria sp. ± A,B Diffuse-porous Low 2 Wide distribution
section
Simarouba amara Cross-

Simaroubaceae ± A,B Diffuse-porous Low 13 Wide distribution
Aubl. section
Cecropia virgusa Cross- Biogeographic

Urticaceae ± A Diffuse-porous Medium 15
Cuatrec. section Chocó
Coussapoa valaria Cross-

Urticaceae ± A,B Diffuse-porous Low 1 Endemic
C.C. Berg section
Pourouma bicolor Cross-

Urticaceae ± A,B Diffuse-porous Low 5 Wide distribution
subsp. bicolor Mart. section
Qualea lineata Cross-

Vochysiaceae + A Diffuse-porous Medium 7 Endemic
Stafleu section
Vochysia artantha Cross-

Vochysiaceae - A Diffuse-porous None 5 Endemic
Stafleu section
Potential in Numbe
logy trees
Vochysia pacifica Cross-

Vochysiaceae ± A,B Diffuse-porous None 2 Endemic
Cuatrec. section
Cross-
Vochysiaceae Vochysia sp. ± A,B Diffuse-porous None 4 Wide distribution
section
(a) A,C B,C (b)
9% 1% Absent
A,B,C 18%
Poorly
2%
defined
36%
A
A,B 52%
36% Well
defined
46%
(c) (d)
Chocó region None High
17% 18% 14%
Wide Endemic
distributi 21% Medium
on 25% Low
62% 43%
Figure 1-4: (a) Percentage of growth rings according to their type: changes in density due
to an increase in fiber wall thickness (A), the presence of marginal bands of axial
parenchyma (B), differences in diameter, distribution, and grouping of pores that delimited
the ring (C), and combinations of the above, (b) Percentage of tree species sampled in the
Low Calima River Basin, Biogeographic Chocó Region, with growth rings absent or present,
(c) Percentage of species with growth rings classified according to their distribution range,
(d) Classification of species with growth rings that could be dated
(a) (b) (c)
Figure 1-5: Semi-ring-porous trees species sampled in the Lower Calima River Basin,
Biogeographic Chocó Region, (Type C) or combined with another anatomical trait. a Clusia
leptanthera, b Tapura costata, c Pterandra ultramonanta. Arrows indicate growth rings
The possibility of dating the rings depends both on their presence and on their continuity,
which is sometimes limited by competition (Figure 1-6a), traumatic rings produced by
injuries in the cambium (Figure 1-6b), or other difficulties such as the anomalous
architecture of the stems (Figure 1-6c, d). In these cases, the rings can be identified using
complete cross-sectional discs, which are recommended in tropical dendrochronology
(Détienne 1995; Worbes 2002; Brienen and Zuidema 2005). Undoubtedly, the minimal
observation area when corers from increment borers are used makes dating difficult. In
general, in 39% of the species, the dating of growth rings was feasible. These included both
medium (25%) and high (14%) dating percentages (Figure 1-4d). Species such as Goupia
glabra with visible growth rings (Table 1-1) may present areas with tangential discontinuity
that can only be detected with complete cross-sectional discs (Figure 1-7a).
Figure 1-6: Irregularities in growth rings due to competition and architecture that was
present in some tree species sampled in the Lower Calima River Basin, Biogeographic
Chocó Region: (a) Irregular very eccentric discs with the pith very displaced in Couratari
guianenesis, (b) Tangential discontinuity of the growth rings, and wedging rings (fused),
followed by traumatic tissue in Couratari guianenesis; (c) Irregular wooden disc typical of
Aspidosperma excelsum; (d) Faint growth rings in Aspidosperma excelsum.
Chapter 1 25
Figure 1-7: Growth rings of Goupia glabra. (a) Complete cross-sectional disc with growth
rings as seen with the naked eye. (b) Growth rings in a rectangular cross-section of 1.5 cm
x 2.3 cm
The results of this study show that, in contrast to the pessimistic opinion of many
dendrochronologists and ecologists about the existence of growth rings in the tropics
(Whitmore 1975; Schweingruber 1988; Evans and Schrag 2004; Poussart et al. 2004;
Vaganov et al. 2006; Anchukaitis et al. 2008; Speer 2010; Hughes et al. 2011; Thomas
2014; Hu and Riveros 2016; Hirons and Thomas 2018; Nakai et al. 2018), in this non-
seasonal hyper-humid tropical environment, many tree species have growth rings.
Surprisingly, 66 species out of 81 sampled species (82%) showed growth rings that were
visible with the naked eye (Table 1-1). Also, these species occurred in a rainier, non-
seasonal environment than that in which any other researchers had previously attempted
to study tropical growth rings (Table 1-2).
Among the 60 pantropical study areas cited in Table 1-2, which included trees that grew
from the lowlands to high tropical mountains, and with all types of seasonality including
droughts, floods, variation in temperature, and various combinations of those variables;
these study areas included a broad latitudinal gradient going from the subtropics of the
Northern Hemisphere to the subtropics of the Southern Hemisphere. In all of them, the
percentage of trees with growth rings ranged from 3% to 100%. Our study ranked 17th in
percentage of tree species with growth rings, surpassing most of the studies cited in Table
1-2. Nevertheless, the results of this chapter are one of only two without any seasonality.
Although 16 studies reviewed in Table 1-2 exceeded the percentage of trees with growth
rings report here (Table 1-2), the real potential of trees with growth rings in the Low Calima
River Basin is even more considerable as discussed below.
1.3.1 Biodiversity of the Chocó Region

The study area of this dissertation is known for a very high richness and species diversity
of tree species. Faber-Langendoen and Gentry (1991) found in this same area 241 dicot
tree species with a diameter at breast height (dbh) ≥10 cm in only 1 ha of forest sampling,
and only 2.4 individuals per each-one tree species sampled. In the sample from our study
area, we found 2.9 individuals per species. If the the Faber-Langendoen and Gentry (1991)
sampling was random and representative for our study area, we estimate that in just one
hectare of forest in the Lower Calima River Basin, would be about 113 tree species with
well-defined rings (0.47 x 241). If only a small fraction of these tree species have annual
growth rings, or with any other constant periodicity, we would have discovered a gold mine
of potential dendrochronological species in the non-seasonal tropical wet forests of the
Biogeographical Chocó Region. Colombia, which contains 5,746 tree species, has more
species of trees than any country in the world after Brazil. However, on a per square
kilometer basis, Colombia has many more species than Brazil (Beech et al. 2017).
The Chocó Biogeographical Region is one of the most crucial tree diversity and endemism
hot spots in the world (Prance 1982). Among the species with great dendrochronological
potential, the following stand out due to the clarity of their rings: Huberodendron patinoi,
Cariniana pyriformis, Mabea sp. Inga acreana, Tachigali colombiana, Goupia glabra,
Apeiba macropetala, Humiriastrum procerum, Nectrandra sp., Ocotea sp, Clarisia
racemosa, Otoba latialata, Virola dixonii, Posoqueria latifolia, Pouteria englerii, Pouteria
collina, and Qualea lineata. Nevertheless, the high diversity of tree species found in our
study area has an Achilles heel: necessarily, the populations are very small, which difficult
to obtain enough replicas for most species
Chapter 1 27
1.3.2 About tree-rings formation in tropical hyper-humid regions

Based on the data in Table 1-2, and contrary to the prevailing hypothesis that periodic
droughts or floods condition growth rings formation in tropical trees, the percentage of trees
with growth rings does not seem to depend only on these environmental variables. For
instance, Tarelkin et al. (2016) found no differences in the percentages of trees with distinct,
indistinct, or absent growth rings between two forests with contrasting in both precipitation
as seasonality in Central Africa (Democratic Republic of Congo). See more differ strikingly
cases in Table 1-2.
In our study, the hypothesis of the existence of growth rings in deciduous or semi-deciduous
tree species (Borchert 1999; Lisi et al. 2008; Nath et al. 2016; Shimamoto et al. 2016)
applied only to C. odorata, S. parahyba, D. panamensis, Goupia glabra, Couratari
guianensis, Tachigali colombiana and, Humiriastrum procerum, which are deciduous, and
for C. pyriformis, which is a brevi-deciduous species. Together represent less than 12% of
the studied species that exhibited growth rings in this study (Table 1-1). On the contrary,
our results were more in agreement with other authors (Worbes 1999; Callado et al. 2001;
Carlquist 2001; Fichtler et al. 2003; Aguilar-Rodríguez and Barajas-Morales 2005; Evert
2006; Tarelkin et al. 2016), who did not find an association between deciduousness and
the formation of growth rings in tropical trees. In fact, according to these authors, neither
do all deciduous trees have growth rings nor do all evergreens lack growth rings.
Based on the hypothesis related to phytogeographic origin, in which growth rings are more
common in species from a boreal origin (Laurasia) (Fahn 1967; Aguilar-Rodríguez and
Barajas-Morales 2005; Ramírez-Martínez et al. 2017), we found that all species of plant
families with an assigned origin, except for two, were from Gondwana and centered on the
Amazonian region. The two families from Laurasia were Lineaceae and Salicaceae (Gentry
1982).
1.3.3 Dendrochronological potential studies around tropics:

Unclear pattern
We show a comparison from our study results with other studies from pantropical regions
in Table 1-2 and Table 1-3. Some examples illustrate the inexplicable differences found by
the authors cited in Table 1-2. The only other case in wet tropical forests without any
seasonality was that of Araya (2012), who reported 22% with growth rings, almost four
times less than in our study.
Some results emerge from Table 1-2: (1) There are growth rings in trees in all tropical
forests around the world, (2) There were no clear trends for ring formation in terms of dry,
moist, or wet climates, seasonality of rainfall, flooding, temperature, or any combination of
these variables, (3) There was no trend with the latitudinal distance from the Equatorial line
to the North and South subtropics. It is very striking that Miller and Détienne (2001) did not
find growth rings in many tree species in French Guiana; by contrast, other researchers
working in the same region, and other areas of the Neotropics, have reported annual growth
rings in these same species. To cite a few examples, growth rings were found by several
authors for Himenaea courbaril, Carapa guianensis, Couratari guianensis, Dipteryx oleifera,
Goupia glabra, Jacaranda copaia, Simarouba amara, Symphonia globulifera, and many
other species as cited by Brienen et al. (2016) and by Schöngart et al. (Schöngart et al.
2017). Curiously, when we analyzed the disciplinary background of investigators, a pattern
emerged. Most studies in Table 1-2 that reported >70% of trees with growth rings were
tropical dendrochronologists who did not follow the IAWA Committee (1989) classification
of growth rings. In sharp contrast, all studies that reported <50% were performed by wood
anatomists who followed this classification. Silva et al. (2019) compiled many proposals for
the classification of the growth rings. But, the one most used by wood anatomists appeared
to be that of the IAWA Committee, although they usually made modifications to it.
The IAWA Committee (1989) classifies the growth rings from dicot wood into two types: (1)
distinct growth ring boundaries, (2) indistinct or absent growth ring boundaries. The limits
of the rings are distinct if "there is an abrupt structural change in the limits between them,
usually including a change in the thickness of the cell wall of the fibers and/or in the radial
diameter of the fibers.” The separation between these two groups is highly subjective, but
the creation of a single group for indistinct and absent and the emphasis on density changes
can lead to classifying species with growth rings, even annual rings, within the second
Chapter 1 29
group. But, also, the emphasis given to increased fiber density tends to classify tropical
species that have subtle, though perceptible rings, boundaries into the second group, as is
the case in the very narrow parenchyma bands typical in the wood of tropical legumes
(Worbes 1995). This family of plants has the highest number of species with annual rings
(Brienen et al. 2016).
Most of the wood anatomists cited in Table 1-2 and Table 1-3 followed the IAWA
Committee's standards, but in reality, few followed them literally, and they modified them to
create three groups: (1) distinct, (2) indistinct, or (3) absent, although they may have used
other terms that are roughly equivalent (Vásquez and Ramírez 2005; Marcati et al. 2006;
Baguinon et al. 2008; Santini 2013; Silva et al. 2016; Tarelkin et al. 2016; Islam et al. 2018).
Most tropical dendrochronologists follow the classification of Worbes (1995), which covers
four basic types of rings: (1) reduction in diameter and increase in fiber density, (2) one or
more marginal parenchyma bands, (3) parenchyma bands and fibers of different diameters,
or (4) varying frequency and width of vessels within the rings. Combinations among these
types often occur.
Dendrochronologists have found annual rings in virtually all dicot trees from temperate and
cold regions (Schweingruber 1988, 2007; Speer 2010; DÁrrigo et al. 2014; Schweingruber
and Börner 2018), except in the Mediterranean where many irregularities occur (Silva et al.
2019). However, Wheeler et al. (2007) who used the IAWA Committee´s standards, report
for the regions of Europe (excluding the Mediterranean), Temperate Asia, and for North
America, 85, 84, and 81 percent of trees, respectively, with distinct rings. The remaining
species were in that sort of black box: indistinct or absent. Note that similar and even higher
percentages there are in Table 1-2 in the tropics. It seems, therefore, that even in temperate
and cold regions, the IAWA Committee’s criteria tend to underestimate the presence of
growth rings in dicot species.
Table 1-2: Percentage of growth rings in tropical trees that grow in diverse environments with seasonality. In bold are the results of
this chapter
Species Total
with species Mean Mean
growth studied Rainfall temperature Type of
Code rings (%)1 (n) Site (mm) (°C) seasonality Reference
Rainfall,
Pantanal, Brazilian Mato Grosso, 2 Schöngart et al.
1 100 58 1,150 23–26 temperature.
South America (2011)
flooding
Amazonian Terra Firme forests, 2,000– Vetter and

2 100 29 26–27 Rainfall
South America 3,000 Botosso (1989)
Rainfall,
Pantanal, Brazilian Mato Grosso, Póvoa de
3 100 28 1,182 20–312 temperature,
South America Mattos (1999)
flooding
Terra Firme, flooded and

2,100- Cintra et al.
4 100 17 swampy Amazonian forests, 27 Rainfall
2,810 (2013)
Brazil, South America
Rainfall,
Brazilian Cerrado, São Paulo, Marcati et al.
5 94 48 1,450 20–262 temperature,
South America (2006)
flooding
Seasonaly semi-deciduous
Rainfall, Lisi et al.
6 92 24 forests Saoutheast Brazil, South 1,370 15–232
temperature (2008)
America
Chapter 1 31
Rainfall,
Pantanal, Brazilian Mato Grosso, 2 de Arruda et
7 94 67 1,150 21–31 temperature,
South America al. (2017)
flooding
Rema-Kalenga Wildlife
Rainfall, Islam et al.
8 93 27 Sanctuary, Bangladesh, South 2,370 25
temperature (2018)
Asia
Diverse ecosystems, Colombia, 1,500– Vásquez and

9 90 57 <24 Rainfall
South America 4,000 Ramírez (2005)
Arid and dry savanna trees, 500– Fahn et al.

10 90 27 28 Rainfall
Africa 1,000 (1981)
11 89 19 Tana River, Kenya, Africa 370 28 Flooding Maingi (2006)
Floodplain forests, Amazon, 1,500– Worbes and

12 88 78 26 Flooding
Brazil, South America 3,000 Fichtler (2010)
Seasonal deciduous forests of 730– Marcelo

13 86 183 16–263 Rainfall
the north and center of Peru 2,6803 (2017)
Roig et al.
14 87 52 Yucatan, Mexico, North America 1,036 25 Rainfall
(2005)
Amazonian Terra firme forests, 2,000– Trevizor

Pará, South America 3,000 (2011)
Central and South Brazil, South 1,500– Rainfall,

16 85 177 24–27 Alvim (1964)
America 2,000 temperature
Biogeographic Chocó Region,

17 82 81 7,219 25.9 None This chapter
Colombia, South América
Groenendijk
18 82 22 South East Cameroon, Africa 4,082 27 Rainfall
et al. (2014)
Kodagu, Karnacata, India, South Nath et al.

19 82 38 2,725 14–292 temperature
Asia (2016)
Eastern Amazon Forests, Brazil, Campos et

20 81 26 1,973 23 Rainfall
South America al. (2008)
Central Amazonian Forests, Tanaka

21 79 226 3,400 26 Rainfall
Brazil, South America (2005)
North Minas Gerais, Brazil, South Rainfall, Barbosa et.

22 79 24 814 22–262
America temperature al. (2018)
Moist forests (Atlantic Forest), Rainfall, dos Santos et

23 79 111 1,278 15–252
Brazil, South America temperature al. (2016)
Central Amazon, Brazil, South Tanaka

24 79 179 3439 26 Rainfall
America (2005)
1,500– Rainfall, Baguinon et

25 78 239 All Philippines, Southeast Asia 26–282
3,500 temperature al. (2008)
Caparo Forest Reserve, Worbes

26 78 37 1,700 25 Rainfall
Venezuela, South America (1999)
Amazonian forests, Brazil, South 1,500– Santini

America 3,000 (2013)
900– Baguinon et
28 77 65 All Sri Lanka, South Asia 26–282 Rainfall
5.000 al. (2008)
Misiones, North Argentina, Bognisegna

29 77 13 1,700 15–252
Subtropics, South America Temperature et al. (1989)
Chapter 1 33
Lowland dry forests, Oaxaca, Brienen et al.

30 76 21 930 26 Rainfall
South of Mexico, North America (2009)
Moist forests, Los Tuxtlas

1,300– Rainfall, Gutiérrez
31 75 79 Biosphere Reserve, Mexico, 24–272
4,200 temperature (2014)
North America
1,000– MAE-FAO
32 70 56 All Ecuador, South America > 12 Rainfall
3,000 (2014)
Central Kalimantan, (Indonesia) Worbes et al.

33 70 27 2,572 27 Rainfall, flooding
South Borneo, Southeast Asia (2017)
2,000– Fahn et al.

34 71 24 Moist forests from Africa 27 Rainfall
3,000 (1981)
1,000– Rainfall, Alves and

35 66 61 South Brazil, South America 14–232 Angyalossy-
1,500 temperature
Alfonso (2000)
1,000– Gutiérrez et
65 64 135 Bolivia, South America <20 -
4,000 al. (2002)
1,800– Abdul-Azim
37 61 26 Malaysia, Southwest Asia 26–272 Rainfall and Okada
3,000
(2014)
Florida, USA, Sub tropical North Tomlinson

38 59 97 1,500 10–262 Temperature and Craichead
America
(1972)
Lotfiomran
39 58 38 Suriname, South America 2,209 26 Rainfall and Köhl
(2017)
Amazon rain forests from Brazil, 2,000 –

40 57 60 27 Rainfall Alvim (1964)
South America 3,000
Democratic Republic of Congo, 1,200 – Tarelkin et al.

41 56 103 24 – 262 Rainfall
Africa 1,700 (2016)
1,000 – Rainfall, Baguinon et

42 54 91 All Thailand, Southeast Asia 26 – 312
2,200 temperature al. (2008)
Southeastern Brazil, South 1,500 – Raifall, Alves and

43 53 176 14 – 232 Angyalossy-
America 2,000 temperature
Alfonso (2000)
500 –
44 53 108 Venezuela, South America >12 Rainfall León (2014)
4,000
North Brazil (Amazonia), South 2,000 – Alves and

45 52 217 26 Flooding Angyalossy-
America 3,000
Alfonso (2000)
Lowland moist,fores, Java Island, 2,000 – Fahn et al.

Indonesia, tropical Asia 4,000 (1981)
Moist forests of Chiapas, Mexico, Brienen et al.

47 52 50 2,800 23 Rainfall
North America (2009)
Ramirez et
Lowland deciduous forest, 700 – Rainfall, al. Ramírez-
48 52 21 22 – 26 2
Mexico, North America 1,000 temperature Martínez et al.
(2017)
Peru, Moist Central Forest, South 2,325 24 – 272 Rainfall, Beltrán and
49 50 80 Valencia
America 2,250 15 – 192 temperature
(2013)
Chapter 1 35
Rainfall,
temperature
500 – Alves and

50 47 38 Northeast Brazil, South America 26 Rainfall, flooding Angyalossy-
1,500
Alfonso (2000)
Premontane and lowland forests, 1,500 – Arévalo and

51 43 43 >18 - Londoño
Colombia, South America 4,000
(2005)
Central-western Brazil, Cerrado, 1,000 – Raifall, Alves and

52 40 25 20 – 262 Angyalossy-
South America 2,000 temperature
Alfonso (2000)
Pakistan, India, Sri Lanka, and Wheeler et

53 38 541 - - -
Burma al. (2007)
Aguilar-
Dicot trees of a mountain moist 1,200 – Rodríguez and
forest, Mexico, North America 1,700 Barajas-
Morales (2005)
Wheeler et
55 28 708 Dicot trees tropical Africa - -
al. (2007)
Dicot trees Southeast Asia and Wheeler et

56 24 1273 - - -
the Pacific al. (2007)
Wet non-seasonal forests, Costa

57 22 110 6,000 25 No one Araya (2012)
Rica, Central America
Wheeler et
58 17 1695 Dicot trees Neotropics - - -
al. (2007)
250 – Tarhule and

59 10 70 Sahel Savannah, Sudan, Africa 28 Rainfall,
1,100 Hughes (2002)
French Guiana (Guyana), South Miller and

60 3 107 3,200 29 Rainfall Détienne
America
(2001)
1
When two or more studies have the same percentage, the one with the largest sample (n) is presented first
2
The mean monthly temperatures of the coldest and warmest months, respectively
3
Data taken in seven seasonal deciduous forests between 230 and 2200 m asl with average annual temperatures between 26°C and 16°C, respectively. The mean annual rainfalls
vary from 730 to 2680 mm
Some researchers who have studied the growth rates of tropical trees and their climatic
relationships using stable isotopes of 13C and 18O justified their use for the lack of growth
rings in these species (Evans and Schrag 2004; Poussart et al. 2004; Hietz et al. 2005;
Pons and Helle 2011; Hu and Riveros 2016; Nakai et al. 2018). However, most species
studied by these authors were repeatedly reported by several tropical dendrochronologists
to have annual growth rings. Such is the case for Cordia alliodora, Carapa guianensis, S.
amara, C. odorata, and Swietenia macrophylla (Brienen et al. 2016; Schöngart et al. 2017),
or at least they had growth rings as in Samanea saman (Skolmen 1974; de Arruda et al.
2017); and Hieronyma alchorneoides (León 2014), and this chapter in Table 1-1.
1.3.4 Species in this chapter with annual rings reported in other

regions
Table 1-3 presents the species of this chapter with annual rings and their visibility reported
by different authors. Thirty percent of the species from this chapter have been reported
previously with annual growth rings in other regions. It suggests that they probably also
form annual growth rings in the area of our study in Colombia. At the time of writing this
chapter, we had only received radiocarbon analyses of the growth rings of six species, all
with annual rings; these species were Cariniana pyriformis (171 y), G. glabra (70 y),
Pourouma bicolor (36 y), Inga sp (62 y), Mabea sp (80 y) and, Inga acreana (100 y). Growth
rings of the last three species had not reported before. Additionally, C. odorata, one of the
trees sampled, had a known planting date where the number of rings coincided with the
years since planting (9 y). That is, we found numerous species with dendrochronological
potential in the rainiest region of the Americas where there is not hydric seasonality, which
marks a milestone that contradicts the long-held prejudice of many dendrochronologists
and wood anatomists that there are no growth rings in trees from these environments. This
finding opens the frontiers of dendrochronology to these tropical environments that closed
until now because of hypothetical and unjustified causalities, which had not been
substantiated by empirical observations in situ, as prescribed by science.
Table 1-3: Species of this chapter reported with annual rings in other regions and in this
chapter (in bold).
Visibility
Annual
Species References rings and References
This Other visibility
chapter studies
Vásquez and
Apeiba ± Cintra et al.
+ Ramírez (2005) +
macropetala1 (2013)
- Araya (2012)
Arévalo and Moreno and del

+ +
Londoño (2005) Valle (2014)
Cariniana Sudworth and

+ -
pyriformis Mell (1911)
+ This chapter
Vásquez and
+
Ramírez (2005)
Brienen et al.
Castilla elastica + - Araya (2012) +
(2009)
Alves and
Baker et al.
+ Angyalossy- +
(2017)
Alfonso (2000)
Miller and
+ + Köhl et al. (2017)
Détienne (2001)
Arévalo and Lotfiomran and

Cedrela odorata ± + +
Londoño (2005) Köhl (2017)
Rozendaal
+
(2010)
Vásquez and
+
Ramírez (2005) ± This chapter
+ Worbes (2002)
Alves and
Rozendaal
- Angyalossy- +
(2010)
Alfonso (2000)
Clarisia
+
racemosa Beltrán and Soliz-Gamboa et
+ +
Valencia (2013) al. (2011)
± Gutiérrez (2014) + Tanaka (2005)

Chapter 1 39
Nahuz et al.
+
(2013)
+ Santini (2013)
Alves and
- Angyalossy-
Alfonso (2000)
León (2008,
+
2014)
Miller and
+
Couratari Détienne (2001)
+ + Morel (2013)
guianensis
Nahuz et al.
-
(2013)
+ Santini (2013)
± Trevizor (2011)
Vásquez and
±
Ramírez (2005)
Miller and
-
Détienne (2001)
± Rojas (2000)
Dipteryx Fichtler et al.
+ Vásquez and +
panamensis + (2003)
Ramírez (2005)
Wiedenhoeft
+
(2011)
Vetter and Détienne and

+ ±
Botosso (1989) Baribier (1988)
Vetter and
Miller and
- + Botosso (1989)
Détienne (2001)
This chapter
Goupia glabra + Vásquez and

+ + Köhl et al. (2017)
Ramírez (2005)
Lotfiomran and
± Trevizor (2011) +
Köhl (2017)
Pons and Helle Lopes de Oliveira

- +
(2011) (2010)
Nahuz et al. Cintra et al.

± +
(2013) (2013)
Oliveira et al.
+
- Santini (2013) (2014)
+ This chapter
Beltrán and
+ + Jalil et al. (1998)
Hevea Valencia (2013)
+
brasiliensis Ohashi et al.
± Gutiérrez (2014) +
(2001)
Wiedenhoeft
Inga acreana + + + This chapter
(2011)
Alves and
Inga rubiginosa + + Angyalossy- + Tanaka (2005)
Alfonso (2000)
Osteophloeum + Marcelo (2017) Lopes de Oliveira

+ +
platyspermum - MAE-FAO (2014) (2010)
+ León (2008) Hazlett (1987)2

Pentaclethra
+ + Fichtler et al.
macroloba + Araya (2012)
(2010)
Pourouma ± Tanaka (2005)

± ± Tanaka (2005)
bicolor
± This chapter
Brienen et al.
+ Gutiérrez (2014) +
(2009)
Schizolobium
+ + Lisi et al. (2008)
parahyba Vásquez and
+ Marcati et al.
Ramírez (2005)
+
(2008)
Miller and Détienne et al.

- ±
Détienne (2001) (1988)
Gutiérrez et al. Fichtler et al.

+ ±
Simarouba (2002) (2003)
±
amara
- Araya (2012)
López-Ayala et
- MAE-FAO (2014) +
al. (2006)
± Santini (2013)
Chapter 1 41
± Trevizor (2011)
Vásquez and
+
Ramírez (2005))
Arévalo and Détienne et al.

+ ±
Londoño (2005) (1988)
Miller and
- ± Détienne (1995)
Symphonia Détienne (2001)
+
globulifera
- Araya (2012)
Callado et al.
+ Santini (2013) +
(2001)
± Trevizor (2011)
Using dendrometer bands in a non-seasonal wet forest at La Selva, Costa Rica, with an
annual precipitation of about 4000 mm, O´Brien et al. (2008) found an annual diameter
growth periodicity in both a deciduous (D. panamensis) and an evergreen species (S.
amara), although not in the evergreen species P. macroloba (Table 1-1, Table 1-3). These
three species had been reported to have annual rings in the same forest (Fichtler et al.
2003). Perhaps the growth periodicity of P. macroloba was so subtle that it is undetected
by the instrument used by O´Brien et al. (2008).
The evergreen H. alchorneoides did not show annual periodicity in the diameter growth by
O´Brien et al. (2008) but, in this chapter and also in León (2014), this species exhibited
growth rings (Table 1-1). Something similar could have happened with P. macroloba, but it
seems that, until now, the periodicity of its growth rings had never studied. O´Brien et al.
(2008) could not identify a single triggering factor for the seasonal periodicity, phenology,
and stem increments observed at La Selva. Hypothetically, they thought that
deciduousness and periodic growth of species such as D. panamensis might have resulted
from phylogenetic inertia in species that have their center of diversity in the Central and
Northern Amazon, where the climate is more seasonal.
In sharp contrast to O´Brien et al. (2008), Hazlett (1987) and Breitsprecher and Bethel
(1990) found evidence of periodic growth in P. macroloba in the same study area. Hazlett
(1987) used dendrometer bands, and Breitsprecher and Bethel (1990) used radial
dendrometers with data loggers that stored hourly measurements. Hazlett (1987) reported
that P. macroloba grew at faster rates during the less rainy season of the year. But
Breitsprecher and Bethel (1990) found that during these months, P. macroloba went into
dormancy both in well-drained and in swamp forests. Perhaps because they used more
precise instruments with a much higher temporal resolution, Breitsprecher and Bethel
(1990) found a dormancy period in this species. D. panamensis was dormant during the
less rainy season in two successive years, but only one tree was studied (Breitsprecher
and Bethel 1990). This dormancy was undetected by O´Brien et al. (2008). Breitsprecher
and Bethel (1990) suggested that variation in the daily amount of incoming solar radiation
may be an environmental trigger of the annual growth periodicity at La Selva. Hazlett
(1987), although not ruling out the annual endogenous growth control in P. macroloba,
emphasized that during the less rainy period there was more illumination and higher
temperatures, increasing growth rates that depended mainly on current photosynthesis.
In French Guiana, under a marked annual drought and 2,700 mm mean annual rainfall,
Détienne et al. (1988) studied the diameter growth for five consecutive years using
dendrometer bands and by marking the cambium with Mariaux windows to determine the
periodicity of the growth rings in S. amara, G. glabra, and S. globulifera. They found a high
correspondence between the monthly precipitation through the years and the monthly
growth rates in S. amara and G. glabra. The relationship was less evident in S. globulifera.
Growth rings were annual in all three species, but they were difficult to observe, especially
in G. glabra. The authors attributed the formation of annual rings to annual droughts. By
contrast, in flood-prone forests of the Mata Atlantica in Brazil, Callado et al. (2001) attributed
the formation of annual rings in S. globulifera to endogenous periodicity.
Considering that the four species discussed in the last three paragraphs (D. panamensis,
S. amara, P. macroloba, and S. globulifera) have been described previously as with annual
growth rings and for which several environmental factors responsible for their formation are
suggested in Table 1-3, how valid can these proposed variables for the study sites in Costa
Rica at 10°26Ń and in French Guiana at 5°04Ń be for our study area? Our area of study
is much closer to the Equatorial line (3°55Ń) and, therefore, the length of the day,
temperature, and sunshine irradiance are more constant throughout the year. Our study
area receives almost twice the precipitation of the site in Costa Rica and nearly triples that
of French Guiana. This last site also has a marked dry period, non-existent in our study
Chapter 1 43
area. However, all of those species have growth rings in our study area (Table 1-1, Table
1-3). Both these species, and the others in Table 1-1, respond to very subtle environmental
cues, or the hypothesis for the origin of their growth rings must be modified totally. If it has
accepted that the primary growth of some architectural models of tropical trees has
genetically determined periodicity, endogenous secondary growth periodicity could be an
alternative hypothesis for some species included in this chapter. Silva et al. (2019)
proposed this classification for the growth rings: (1) obligatorily with growth rings,
developing rings independently of environmental conditions; (2) facultative, growing rings
depending on the variation of one or more environmental factors; and (3) obligatorily without
growth rings, never forming growth rings, independently of environmental conditions. If the
trees species with growth rings in Table 1-1 are not sensitive to subtle environmental cues,
we must conclude that these species are obligatory with growth rings. Precise
measurements with dendrometer bands suggest that there are ever growing species that
form annual rings, and so, the cambium does not enter into dormancy. It is enough for tree-
ring formation in these species that the cambium reduces its activity substantially, but
without a complete halt (Silva et al. 2019). This seems to be the case in C. insignis, C.
obtusifolia, Minquartia guianensis, and S. amara (O´Brien et al. 2008), Schefflera
morototoni, G. glabra, S. globulifera, and S. amara (Détienne and Barbier 1988; Morel
2013), Shorea patoiensis, S. pinanga and S. dasyphylla (Fujii et al. 1999), S. leprosula, S.
acuminata, S. parvifolia, and Dryobalanops sumatrensis (Sass et al. 1995; Wang and
Hamzah 2018), and young trees of Terminalia superba (E de Faÿ 1992). Perhaps this is
one of the reasons why some of these species have faint rings. For this reason, a third
group of species with periodic growth, but without cambial dormancy, should exist.
In 11 of the 17 species found with annual rings by dendrochronologists (Table 1-3), and
with growth rings and annual growth rings in this chapter, some wood anatomists did not
find growth rings at all, or they grouped them as indistinct or absent. Two U.S. Forest
Service wood anatomists, who studied the anatomy of C. pyriformis and Swietenia
macrophylla, did not observe growth rings in these species (Sudworth and Mell 1911). Both
species have been described repeatedly by other anatomists as having growth rings (Table
1-3) and by dendrochronologists with annual growth rings marked by increased fiber density
(Brienen et al. 2016; Schöngart et al. 2017). Détienne and Barbier (1988) described as
annual the growth rings of G. glabra, S. amara, and S. globolifera in the French Guiana
forests, and Détienne (1995) also confirmed the annual rings of S. globulifera. But Miller
and (2001), with one author in common and in the same forest, did not find growth rings in
any of the three species. How do we explain such contradictory results?
A way to avoid subjectivity in the identification of growth rings is to develop computer vision
methods on high-resolution scanned images for the identification and measurement of
several growth ring variables. In this way, the types of rings could be determined
automatically, and their variables measured quickly and safely. Not without challenges, the
development of this technique would be the entrance to the fourth revolution of knowledge
for dendrochronology and wood anatomy.
Dendrochronology would learn a great deal thoroughly investigating the trees of these non-
seasonal, hyper-humid tropical climates. In highly complex tropical ecosystems there may
be emerging properties and nonlinearities that seem not contemplated in
dendrochronological studies of the temperate region.
Dendrochronology in the temperate region operates linearly according to Liebig´s law. This
law states that growth is dictated not by total resources available, but by the scarcest
resource (limiting factor). However, ecology teaches us that both the deficit of a growth
factor and its excess produce tension and limit growth. Therefore, a law of the minimum
and a law of the maximum should exist as limiting factors for growth. These two laws are
involved in Shelford's tolerance law (Niinemets and Valladares 2008): If other factors are
not limiting, as the magnitude of a limiting factor increases, organisms respond by
increasing their growth, up to a limit at which the response saturates. Subsequent increases
in this factor produce less and less growth because the organism is growing under
incremental stresses. Consequently, Shelford's law is non-linear and depicts a unimodal
curve (Figure 1-8). Under a non-seasonal, hyper-humid tropical climate, we cannot exclude
the possibility that soil moisture exerts tension on tree growth of some species. Then, the
correlation between tree growth rates and annual precipitation would be negative and not
positive as the law of the minimum stipulates. In fact, this has already been demonstrated
for temperature in tropical lowland trees where the correlation between rings width and
mean annual temperature is often negative (Herrera and del Valle 2011; Ramírez and del
Valle 2011; del Valle et al. 2012; Moreno and del Valle 2014), in line with what we might
call the law of the maximum.
Chapter 1 45
Figure 1-8: It shows a representation of Shelford's tolerance law for dendrochronological

applications. There is a limiting factor: by water deficit in the soil (left), and by an excess of
water in the soil that increasing the anoxic conditions for roots (right). Towards the center
of the curve, the rings should be complacent. Consequently, the response of ring widths to
soil moisture must be non-linear.
However, the range of tolerance to soil moisture is different for each species, and their
populations respond to the resources available depending on the assemblage of species
in which they are inserted (Niinemets and Valladares 2008). Thus, for a given soil moisture
content, different species may respond in different ways, and even the same species:
subsidy or stress. In temperate regions, the cambium of virtually all tree species
synchronously enters into dormancy during autumn and is activated during spring.
Therefore, there is minimal uncertainty about when trees grow or stop growing. Something
similar is assumed to occur when there is hydric stress in the tropics. The cambium of trees
in temperate regions responds to temperature and day length cues (Evert 2006). In
seasonal tropical climates trees respond to droughts or floods (Evert 2006; Brienen et al.
2016; Schöngart et al. 2017), although day length or irradiance may also be involved
(Callado et al. 2001; Silva et al. 2019). But, if in non-seasonal tropical wet climates trees
form growth rings, as proved in this chapter, will there be synchrony between the different
species? And, to what cue or cues will these trees respond when they are only at 3°55´
from the Equatorial line?
We should not rule out that genetically controlled periodicities that regulate their frequencies
may exist, at least in some species (Fahn 1967; Tomlinson and Craichead 1972; Tomlinson
and Longman 1981; Jacoby 1989; Mushove et al. 1995; Callado et al. 2001; Silva et al.
2019). In perennials, the molecular and genetic factors that influence these clocks are
gradually becoming disentangled with Populus as a prototype (Johansson 2010). Today it
is known that these periodicities are controlled genetically (Lüttge and Hertel 2009;
Johansson 2010). The input to the clock in Populus is mediated by the phytochrome-A
photoreceptor to detect the circa-annual clock (Johansson 2010). A large number of genes
have identified that expressed during the radial woody growth of plant stems (Liu et al.
2014). There are two types of periodicity: (1) synchronization of behavioral and
physiological processes to cyclic environmental factors, or extrinsic adaptive value, and (2)
coordination of internal metabolic processes, or intrinsic adaptive value (Sharma 2003).
These periodicities are also called exogenously and endogenously controlled, respectively,
by scientists who have developed the architectural models for trees (Hallé et al. 1978;
Barthélémy et al. 1995; De Reffye et al. 2008; Nicolini et al. 2012; Palubicki 2013). In our
opinion, tropical dendrochronology should devote to this task in the coming years.
Growth rings have both genetic and environmental origins, but little scientist knows about
the contribution of each of these factors in the growth ring formation (Schweingruber 2007).
In temperate regions, the sharp contrasts between temperatures and day lengths
throughout the year make it challenging to discriminate environment influence from genetic
factors. In non-seasonal, tropical hyper-humid climates that are very close to the Equatorial
line, such as in our study area, mean monthly temperatures and day lengths are nearly
constant the year round. Hypothetically, this circumstance suggests that, if any other subtle
environmental factor as cloudiness is not involved in these growth rings periodicities;
genetic factors are the principal causes of the growth rings formation in this environment.
Chapter 1 47
1.4 Conclusions
We report here the existence of growth rings for trees growing under an extreme humid
tropical environment without marked seasonality in precipitation, temperature or solar
irradiance. From a total of 81 trees studied, ~ 45% showed well-defined growth rings. The
percentage of trees with growth rings was even higher than in other tropical regions with
more seasonal climates. A survey of the literature suggests no clear relationship between
climate and ring formation, but curiously, an association with ring-detection criteria
developed by different research communities. The large proportion of growth ring in the
trees in this tropical non-seasonal region, suggests that other environmental factors, or
even from the genetic origin, may determine growth-rings development in trees.
Some questions to be answered by dendrochronology for non-seasonal hyper-humid

tropical environments would be (1), what are the periodicities of the growth rings? (2), what
is the relationship between high rainfall and growth rings? (3), what other subtle seasonality
or cues might be involved in these periodicities?
We believe that future researches in non-seasonal tropical regions such as those with
extreme precipitation would help to understand better the factors controlling growth ring
formation in tropical trees.
2. Chapter 2: Growth rhythms of trees from
the rainiest neotropical region
With Jorge I. del Valle, Diego A. David, Sebastián González-Caro, Conrado Tobón,
Carlos A. Sierra
Abstract: The occurrence of annual growth rings as a consequence of the seasonal activity
of vascular cambium in tropical trees has been explained, either by the annual water deficit
or annual floods. However, little is known about annual tree-ring drivers under tropical
hyper-humid conditions without evident yearly dry periods. Shelford's law states that both
the deficit and the excess of environmental resources limit plant growth. Accordingly, we
hypothesize that reduced solar radiation, excess soil moisture, and slight reduction of
precipitation control annual growth rings in tropical hyper-humid forests without annual dry
periods. We first test the occurrence of rhythmic growth in several tree species from the
Biogeographic Choco Region (annual rainfall 7,200 mm) using three different methods:
Radiocarbon (14C) dating, tree rings synchronization, and dendrometer bands. Then, we
assess the effect of some environmental drivers, namely rainfall, short wave radiation,
temperature, and soil moisture, on tree growth (tree rings and dendrometers). We observe
both positive and negative growth answers to water and light availability, depending on the
tree species. This fact suggests that both excess or deficit of growth factors may explain
seasonal cyclicity of growth rhythms in some trees, strengthening our hypothesis. We show,
for the first time, the occurrence of annual growth rhythms in several tropical tree species
under extreme ever wet conditions. A new frontier is here open for tree rings science,
transforming the long-held belief that there was no rhythmic tree growth in hyper humid
environments.
2.1 Introduction
Plant growth rhythms are seasonal or cyclic events occurring on different tissues and
organs such as meristems, roots, leaves, and reproductive structures (Lüttge and Hertel
2009; Albert et al. 2019). For tree species, growth rhythms are driven by environmental
conditions such as climate, light availability, and soil conditions (Lüttge and Hertel 2009;
Fyllas et al. 2017). In temperate and highly seasonal regions tree growth generally follows
an annual cycle expressed as cyclic tree ring formation driven by temperature seasonality
and water availability (Babst et al. 2019; Stine 2019; Pearl et al. 2020). In contrast, growth
rhythms in tropical trees and their drivers are less studied (García-Cervigón et al. 2020).
The occurrence of annual growth rings as a consequence of the seasonal activity of

vascular cambium in tropical trees has been an intriguing subject of study for ecologists,
silviculturists, and biologists (Worbes 2002; Yáñez-Espinosa et al. 2010; Shimamoto et al.
2016; Albert et al. 2019). Hence, establishing the exact age of tropical trees is a challenging
task, mainly when anatomical tree-ring structures are unclear, or even when they are well
defined, arises the question, what is the frequency of their formation? (Stahle 1999; Ricker
et al. 2020). Tropical tree-ring frequency is commonly determined using 14C of specific tree
rings (Bomb-peak-method) (Worbes and Junk 1989; Fichtler et al. 2003; del Valle et al.
2014; Andreu-Hayles et al. 2015), complemented by detailed observations of growth in
vascular cambium using dendrometers, microsections, and xylem wounds (Worbes 2002;
Lisi et al. 2008; Shimamoto et al. 2016; Hogan et al. 2019; Pumijumnong et al. 2019). Also,
successful cross-dating (i.e., tree-ring synchronization between samples) has been helpful
to analyze the environmental drivers of tropical tree-rings formation (Stahle 1999; Trouet et
al. 2006; Remane and Therrell 2014).
The tropical dendrochronology paradigm has evolved fast during the last 30 years. A few
decades ago, the common belief was that tropical trees had no rhythmic growth because
of a lack of thermal seasonality, compared with temperate and boreal regions (Whitmore
1990). However, the accumulation of evidence on annual rings in the tropics suggests that
Chapter 2 51
dry periods or periodic floods are the dominant triggering variables leading to tropical tree-
ring formation (Rozendaal and Zuidema 2011; Brienen et al. 2016; Schöngart et al. 2017).
But, pieces of evidence of annual tree rings in wet tropical climates, without water deficit or
flooding (Fichtler et al. 2003; Moreno and del Valle 2014; Giraldo et al. 2020), challenge
current assumptions about the factors inducing growth-ring formation in tropical trees. In
particular, Chapter 1 showed a high percent of tree-rings structures in several tree species
(82%, n = 81) from the Choco region, the rainiest in the New World (precipitation over 7,200
mm y-1). While it is not clear what factors rule periodic growth rhythms in tropical trees under
such conditions, slight variation in rainfall, soil moisture, solar irradiance, cloudiness,
sunrise and sunset time could be considered as possible drivers (Breitsprecher and Bethel
1990; Clark and Clark 1994; Borchert and Rivera 2001; O´Brien et al. 2008; Moreno and
del Valle 2014).
According to Liebig's law, the growth of an organism is not controlled by all the available
resources (light, temperature, water, nutrients, etc.) but by the scarcest environmental
resource (i.e., limiting factor) (Taylor 1934). The limiting factor that controls annual tree
growth is the main variable recorded in the tree-rings thickness (Speer 2010; Stine 2019).
Under this view, light availability, mainly photosynthetically active radiation, would be a
limiting factor in high cloud cover regions such as non-seasonal hyper-humid forests. In
particular, the light limitation would be extreme during the rainiest months in which cloud
cover increases, producing an annual pattern on tree growth. Indeed, tree growth in
seasonal tropical forests is limited by light availability during the rainy season (Graham et
al. 2003). Recent observations based on satellite information indicate an increase in canopy
photosynthetic activity during the less rainy period in the tropical wet forests without water
deficit (Green et al. 2020). It implies a reduction in growth and productivity during the rainiest
months as a consequence of water excess (Muller-Landau et al. 2021), or
photosynthetically limited for both high cloudiness and an excess of precipitation (Restrepo-
Coupe et al. 2013). Then, the interaction between light and water availability may drive tree-
growth rhythms in tropical hyper-humid forests.
In fact, according to Shelford´s law (Shelford 1913, 1931), all organisms have both
minimum and maximum thresholds for the different environmental factors that control their
population growth. Near these thresholds, organisms grow under stress and constrained
by both deficit and excess. So, in hyper-humid forests without any dry season, the
availability of water measured as rainfall should be close to the maximum tolerance

threshold for some species. Hypothetically, too much precipitation maintains high water
saturation in the soils, which reduces its aeration and favors hypoxic conditions in the roots,
limiting tree growth. Considering both Liebig´s and Shelford´s laws, we hypothesize that at
least in some species, light, soil moisture, and slight reductions in precipitation control tree
growth rhythm in hyper-humid tropical forests without evident dry periods. In contrast, we
expect to find negative correlations between rainiest months and tree growth. In this study
we aim: i) to determine the growth ring frequency in some species with well-defined tree
rings, growing in a hyper-humid tropical forest, ii) to describe intra-annual growth patterns
in some of these species, iii) to assess possible environmental drivers of tree growth in a
hyper-humid tropical forest. This information can provide new insights into the interaction
between physiology and environmental drivers of growth rhythms in the neotropical rainiest
region, little studied until now.
2.2.1 Study area

This study was carried out at the low Calima River Basin (3°57´12.54´´ N, 76°59´27.96´´
W), which belongs to the Choco Biogeographic region, in northern South America, near the
Pacific coast of Colombia (Figure 2-1). This region is the rainiest in the New World. In some
places, mean annual precipitation is over 12,000 mm (Mesa et al. 1997; Poveda and Mesa
2000; Mesa and Rojo 2020). In the Yurumanguí village (120 km South from our study area),
recorded rainfall in 2018 was 26,987 mm (Mesa and Rojo 2020). The low-level jet stream
(tropopause air current) centered around 5°N, known as the Chocó Jet, explains the high
regional precipitation (Mesa and Rojo 2020). Furthermore, the high floristic richness,
endemism, and increasing deforestation place the Choco region as one of the most
biodiverse hotspots in the World with high priority for conservation (Myers et al. 2000;
Fagua and Ramsey 2019; Pérez-Escobar et al. 2019). Small hills with slopes up to 45° with
elevations ranging from 40 - 100 m above sea level characterize the study area. Soils are
mottled grey-yellow clay-loam, poor in soil nutrients and high iron and aluminum
concentration (Faber-Langendoen and Gentry 1991).
Chapter 2 53
Figure 2-1: The study area. (a) Calima River Basin (square), located in the Chocó Region,
with an area of explicit precipitation gradient (data from https://chelsa-climate.org/) (Karger
et al. 2017). Mean monthly precipitation (b) and temperature (c) data from Bajo Calima
meteorological station, which belongs to the Institute of Hydrology, Meteorology, and
Environmental Studies of Colombia (IDEAM). Mean monthly values of short-wave solar
radiation SWR (W m-2) (d), available from Clouds and the Earth’s Radiant Energy System
- CERES (https://ceres.larc.nasa.gov/) and mean monthly NDVI (Normalized Difference
Vegetation Index) (e), data from Modis/Terra vegetation indices
(https://lpdaac.usgs.gov/products/mod13q1v006/).
2.2.2 Tree-ring samples and dating

We obtained entire cross-sections for multiple tree species, taking advantage that Afro-
Colombian ethnic groups sporadically felling trees for their economic and cultural activities.
We choose 14 species with well-defined to poorly defined tree rings, but that could be dated
to establish their tree-ring frequency by the radiocarbon bomb-peak method (Worbes and
Junk 1989; Fichtler et al. 2003). A priori, we assumed the annual formation of tree rings.
Then, we assigned the calendar year to the last ring formed, either complete or incomplete:
2016 was the sampling year, and from there, we counted regressively to the pith. We
collected about 20 mg of the wood sampled in each tree ring for radiocarbon analyses from
specific rings dated by regressive counting between 1957-2010. Samples were prepared
following Steinhof et al. (2017) to extract alpha-cellulose and were analyzed at the
radiocarbon laboratory of Max Planck Institute for Biogeochemistry in Jena. We calibrated
the radiocarbon results using Cali-Bomb (Reimer et al. 2004) with Northern Hemisphere
Zone calibration data (NHZ2) to obtain calendar dates. Finally, such calibrated dates were
compared with the assumed calendar years (dendrochronological dates) and counting the
number of rings as the difference between dated rings, allowing us to establish the tree-
ring frequencies (del Valle et al. 2014).
Our study area bears an exceptional richness and diversity of tree species with many
endemic and rare species (Gentry 1989); but their populations tend to be small, and most
tree species are scattered on the landscape. Therefore, it is not easy to sample several
trees from most species. For these reasons, we used only four tree species with available
tree samples (n ≥ 4 trees) growing at similar sites and conditions (illumination and slope),
to check tree-ring synchronization. Samples were prepared according to standard
procedure as described by Speer (2010). In an Epson Expression 10000XL scanner, we
obtained high-resolution images (1800-2400 dpi), allowed us to observe macroscopic wood
features up to 10- 15 μm. Tree-ring measurements were obtained by combining ImageJ
(Fiji) 11.52i software (Schindelin et al. 2012) and R software (R Core Team 2020). Cross-
dating was carried out at the tree level first. Then, we gradually added other tree-ring series,
ensuring statistical and graphical synchronization. The quality control, series
synchronization, and generation of chronologies were carried out with the dplR package
(Bunn 2008, 2010).
Chapter 2 55
2.2.3 Environmental data

From the Bajo Calima Meteorological Station (IDEAM), mean monthly rainfall data (1947-
2017) and mean monthly temperature data (1957-2016) were available. Some lacking
records were estimated with the closest five meteorological stations also from the Bajo
Calima basin. Due to the lack of ground instrumental measurements of solar radiation, we
use the mean monthly short-wave solar radiation: SWR (W m-2) satellite-derived product
available from Clouds, and the Earth’s Radiant Energy System - CERES
(https://ceres.larc.nasa.gov/), as a surrogate of the incoming photosynthetically active
radiation between 2000-2019. The Normalized Difference Vegetation Index (NDVI) was
obtained from MODIS time series in the study region previously filtered to reduce
cloudiness and missing data. These data were extracted from the MODISTools R package
(Tuck et al. 2014). We used time series from ten points selected into the study area, in
which forest cover has been maintained in the last 20 years. For each point, we averaged
NDVI data for each month between 2000-2019.
2.2.4 Field measurements

We installed 20 automatic band dendrometers (Tree-Hugger®, Global Change Solutions)
at tree diameters 15- 30 cm and at tree heights from 1.3 to 3 m to avoid buttress.
Measurements were recorded hourly and data downloaded every five weeks. Before
installing the dendrometers, we cleaned the stem surfaces to avoid the proliferation of
epiphytes around them. The first ten dendrometers were installed in April 2018; after few
months, most of them stopped recorded measurements. Then, we installed a second group
in October 2019; most of them were still working until our last download in February 2021.
The malfunctions issues of devices, non-measurement periods, or damage must be
attributed to a permanently high relative humidity in the study area. For this study, we
selected four species with well-defined tree rings, but the recordings of just two (Goupia
glabra, n = 6 and Apeiba macropetala, n = 3) were used because they present the complete
records in different replicates, which is much more suitable for a better understanding of
growth rhythms along the year. These same two species were analyzed by the tree-rings
series. We also installed two soil moisture and soil temperature stations (Campbell Sci®)
at two depths, 10 and 30 cm. The frequency of measurements was 30 min. All these
measurements were carried between 2018 – 2020. For an accurate determination of soil
water content, we calibrated the measurements according to Frumau et al. (2006). We

carefully debugged the data by removing aberrant measurements, mainly present in
dendrometer data. Most of them related to irregular changes in the battery voltage of
devices.
As a first step, we transformed circumference increment data to radial increment data

assuming that stems were cylindrical. To standardize the measurements, we subtracted all
the first measurements in dendrometers allowing each dendrometer data to illustrate
similarities among the same species. This procedure allowed us to average the data
monthly and to eliminate short-term fluctuations of stem girth due both daily changes in soil
humidity and the effect of diurnal fluctuations of temperature and radiation. The mean
monthly, cumulative and standard deviation growth was obtained for an entire year. All filter
procedures and statistical analyses were performed using the R software (R Core Team
2020).
2.2.5 Data analyses

We considered some parameters to assess the suitability of tree-ring series: series
intercorrelation which measure the strength signal common in all sampled trees (Speer
2010). The mean correlation coefficient among tree-ring series (rbar) as an indicator of
common signal strength (Speer 2010; Cook and Pederson 2011). The expressed
population signal (EPS) measure of the common variability in a chronology, values below
0.85 suggest few trees dominate de level signal (Speer 2010). The Signal to noise ratio
(SNR) is a measure of the amount of desired signal is recorded in the chronology (Cook
and Kairiukstis; Speer 2010). Mean sensitivity as a measurement of variability in tree ring
width, values ranging between 0.2 and 0.4 are considered sensitive enough for climate
reconstruction (Speer 2010).
To assess the relationship between tree-ring frequency and environmental parameters, we

use the R-package treeclim (Zang and Biondi 2015) to perform bootstrapped correlation
analysis between tree-ring chronologies and mean monthly precipitation, mean monthly
temperature, and SWR (W m-2) from September of the previous year to August of the
current year. We choose such a period according to our field observations: in some species,
Chapter 2 57
leaf shedding and new leaves occur from September to February and flowering from
February-May. The selected period includes the probable growing season for the studied
species. We also, used the NDVI as complementary information to give us an idea of the
possible phenological changes of the vegetation in the study area.
To assess the effect of environmental drivers in the intra-annual tree growth, we used a
cross-correlation test between monthly dendrometer series from two species (G. glabra and
A. macropetala) and monthly data of precipitation, soil water content, short-wave radiation,
and NDVI. This analysis was run using the ccf function in the base R package.
2.3 Results
Tree-ring frequency was checked by calibrated dates of 14C in calendar years and
dendrochronological dates (Appendix A). According to this result in the 14 species tested,
tree-ring formation occurs annually. In 10 tree species, the accuracy of the results is much
more evident because the annual resolution is clear in different tree samples or adjacent
tree rings from the same tree sample. Four species with a single dated ring also allow
establishing annual periodicity in ring formation. The comparison between all radiocarbon
vs. dendrochronological dates matched extremely well and within one-year margin error
(mean = 0.05, Sd = 0.54) (Figure 2-2). The species phenology or growth season, which in
some cases start the previous year, are the attributable reasons for some small differences
(Figure 2-2). In just one radiocarbon sample of Tachigalii colombiana, we found a significant
difference between calibrated dates and dendrochronology dates (1.5 years), caused by
sampling error, probably including wood from an adjacent tree ring; however, the annual
tree ring annuity was confirmed by other samples from the same tree, and by other different
trees (discs).
Four species: (Humirastrum procerum, Qualea lineata, Apeiba macropetala, Goupia

glabra) with a sample size between 4 and 12 trees, growing under similar conditions, were
successfully cross-dated. Despite the small sample available, we confirmed tree-rings
synchronization (Table 2-1). Two species with the largest replicates Q. lineata and G.
glabra presented suitable values of serial correlation (0.42 – 0.46, p < 0.05, respectively),
running r-bar (0.36 – 0.31 respectively), and expressed population signal EPS (0.87 – 0.89
respectively) (Table 2-1). The other two species had the highest and the lowest mean series
correlation: A. macropetala (0.49, p < 0.05) and H. procerum (0.41, p < 0.05), respectively.
And both species reveal low EPS values (Table 2-1). H. procerum and G. glabra are prone
to form wedging rings close to wounds, where tree rings usually vanished. We carefully
avoid those sectors in the cross-sections when delineating and measuring growth rings.
Figure 2-2: Relationship between dendrochronology dates and calibrated radiocarbon

dates (n= 36) from 14 species, see Appendix A. The histogram represents the difference
between corresponding dates.
Chapter 2 59
Table 2-1: Descriptive statistics of four cross-dated tree species from low Calima River
Basin. rmean: mean series intercorrelation. rbar: running bar; EPS: Expressed population
signal; SNR: Signal noise to ratio. MS: mean sensitivity. *(p < 0.05).
Humirastrum Qualea Apeiba Goupia

procerum linneata macropetala glabra
Time-span
(years) 1943-2016 1960-2016 1984-2016 1869-2019
Sampled tres
(series) 6 7 5 12
Diameter
range (cm) 15 - 50 10 - 60 45 - 50 10 - 30
Ring width and

deviation (mm) 2.4 ±1.3 3.7 ± 2.1 8.3 ± 6.1 1.8 ± 1.1
Interseries
correlation 0.49* 0.46* 0.41* 0.42*
rbar 0.28 0.36 0.31 0.32
EPS 0.82 0.87 0.833 0.89
SNR 4.58 6.76 4.98 8.58
MS 0.35 0.36 0.45 0.31
The results of the bootstrapped chronologies-climate correlations are contrasting between

species (Figure 2-3). With H. procerum we observed negatively association with September
precipitation of the previous year (r = - 0.33, p < 0.05) and with mean precipitation from
September-October (r = - 0.35, p < 0.05) (Figure 2-3b), and that it was also significant
correlated with the shortwave radiation from October previous and current January
(October: r = -0.54, p < 0.05; January: r = 0.66, p < 0.05), also correlated with mean short
wave radiation from December previous to current April (r = 0.56, p < 0.05) (Figure 2-3c).
The growth of Q. lineata was significantly positively associated with January precipitation
of current year (r = 0.38, p < 0.05) and with mean precipitation from September previous to
current January (r = 0.28, p < 0.05) (Figure 2-3f), but negatively correlated with shortwave
radiation of previous December (r = -0.45, p < 0.05) (Figure 2-3g).
The A. macropetala growth is negative correlated with current year June and July
precipitation (June: r = -0.58, p < 0.05; July: r = -0.34, p < 0.05) (Figure 2-3j) and with mean
precipitation from current May to current September (r = -0.44, p < 0.05) as well as
significantly correlated with shortwave radiation of the previous October, previous
November, current March and current April (October: r = -0.65, p < 0.05; November: r = -
0.61, p < 0.05; March: r = 0. 68, p < 0.05; April: r = 0.59, p < 0.05) and with mean current
year shortwave radiation from January to May (r = 0.77, p < 0.05) (Figure 2-3k).
The tree-ring chronology of G. glabra was positively associated with May, July and August
precipitation of the current year (May: r = 0.23, p < 0.05; July r = 0.40, p < 0.05; August: r =
0.31, p < 0.05), also positively correlated with mean precipitation from May to October of
current year (r = 0.43, p < 0.05) (Figure 2-3n), also a negative correlation is observed with
shortwave radiation in March of current year (r = -0.42, p < 0.05) and with mean current
year shortwave radiation from January-June (r = -0.36, p < 0.05) (Figure 2-3o).
Temperature had not significant associations with the analyzed chronologies (Figure 2-3).
Chapter 2 61
Figure 2-3: Tree chronologies and bootstrapped correlations with environmental variables.
The first row of panels (a, e, i, m) represents the tree-ring chronologies, the second to the
fourth row of panels represent, respectively, the chronologies association with precipitation,
short-wave radiation (SWR) in W m-2, and temperature. Numerals a, b, c, d, represent
Humiriastrum procerum chronology and their correlation with precipitation, SWR and
temperature, respectively. Numerals e, f, g, h, represent Qualea lineata chronology and
their correlation with precipitation, SWR and temperature respectively. Numerals i, j, k, l,
represent Apeiba macropetala chronology and their correlation with precipitation, SWR,
and temperature respectively. Numerals m, n, o, p, represent Goupia glabra chronology
and their correlation with precipitation, SWR, and temperature, respectively. Lower case
months (previous year) and months in capitals (current year).
Dendrometer measurements provide evidence of intra-annual growth rhythms occurring

differently in the two studied species (uncoupled growth) (Figure 2-4a – 2-4b). A.
macropetala growth is evident during January - August followed by abrupt reduction of

growth (interpreted as dehydration of the stem) during August - October, before starting
growing again during November-December. Its observation suggests growing start in
November of the previous year and finishes in August of the current year. The G.
glabra dendrometer growth reveals no growth and slight dehydration between January –
March, followed by growth from April - October, then abrupt dehydration and no growth
between October - December. Which means the complete growing season start in March
of the current year and finish in February of the following year.
In Figure 2-4a – 2-4f, we present the graphical variation of tree growth and environmental
factors variation along the year. Figure 2-4g – 2-4p allows us to obtain a better interpretation
of the relationships based on cross-correlation comparisons. The comparison between both
species (Figure 2-4g, 2-4h). G. glabra shows a significant positive relation with precipitation
with zero lag (Figure 2-4i). Meanwhile, A macropetala presents a significant positive
correlation with two months lagged (Figure 2-4m). The relationship between SMC and both
species presents the highest significant correlation value with a lag of 2 months (Figure 2-
4j and Figure 2-4n).
A significant and negative relation with 2 and 3 months lagged is observed between G.
glabra and SWR (Figure 2-4k), but no relationship is observed between A. macropetala and
SWR (Figure 2-4o). Finally, comparisons between G. glabra and NDVI show significant
correlations with 1-2 months lag (Figure 2-4l). Moreover, A. macropetala comparisons with
NDVI were positive and significant with a zero lag and one lagged month (Figure 2-4p).
Chapter 2 63
Figure 2-4: Comparison between mean monthly growth and environmental factors. (a)
Mean monthly cumulative growth (mm). (b) Mean monthly growth rate (mm month-1), the
bars indicate the growth period. (c) Precipitation (PP) in millimeters (mm). (d) Mean monthly
soil moisture content (SMC) expressed in volumetric units (cm3 cm-3). (e) Mean monthly
short-wave radiation (SWR) in W m-2. (f) Mean monthly normalized difference vegetation
index (NDVI). (g-h) cross-correlation function between G. glabra and A. macropetala. (i-p)
Cross-correlation function between mean monthly growth and environmental factors. (i) G.
glabra vs. PP. (j) G. glabra vs. SMC. (k) G. glabra vs. SWR. (l) G. glabra vs. NDVI. (m) A.
macropetala vs. PP. (n) A. macropetala vs. SMC. (o) A. macropetala vs. SWR. (p) A.
macropetala vs. NDVI.
2.4 Discussion
We found evidence of annual growth rhythms on trees growing in a tropical hyper-humid
forest without water deficit. These rhythms are inferred on three independent facts: annual
growth rings synchronization (dendrochronological method) in several tree species,
dendrometer observations, and the high correlation between radiocarbon and tree-ring
estimated age in 14 tree species
This study is the first report of tree-ring annuity for 8 out of 14 tree species analyzed. The
other tree species were reported with annual rings in other seasonal tropical forests: C.
racemosa by bomb-peak method and cross-dating (Soliz-Gamboa et al. 2011); G. glabra
by cross-dating (Oliveira et al. 2014; Lotfiomran and Köhl 2017); S. globulifera and H.
brasiliensis by pinning method (cambium wounds), band dendrometers and phenology
(Callado et al. 2001; Ohashi et al. 2001). Or inferred by a marked dry season each year in
A. macropetala and C. elastica, (Brienen et al. 2009; Cintra et al. 2013). Curiously C.
elastica and C. racemosa had been repeatedly reported with absent tree ring boundaries
in descriptions performed by wood anatomists (Alves and Angyalossy-Alfonso 2000; Miller
and Détienne 2001; Araya 2012; Beltran and Valencia 2013). Then, our finding challenges
the generalized idea of a lack of tree growth rhythms and consequently tree rings in hyper-
humid regions such as the rainiest forest of the Americas due to continuum water supply.
According to our hypothesis, in some species we expected to find negative correlations

between the rainiest months and trees growth. Based on Shelford´s law, H. procerum and
A. macropetala are close at their maximum thresholds for water excess and their minimum
thresholds for light availability. Also, the high rainfall period is characterized by high cloud
cover that may limit light availability for tree growth, which may explain the positive
correlations between rainfall and photosynthetically active radiation. Then, rainfall can exert
a direct negative effect by saturation the soil porosity with water, leading to hypoxia, and
an indirect effect by reducing light due to increasing cloudiness. In these both species, tree-
rings´ indices are negatively correlated with the rainiest season of the year, and positively
correlated with the solar radiation during the less rainy months of the year (Figure 2-3).
Based on dendrometer data for A. macropetala, the maximum growth rates occur during
the less rainy months, and growth stops during September - October, the rainiest months,
and is poorly related to solar radiation (Figure 2-4). These results suggest that the direct
Chapter 2 65
effect of rainfall on tree growth could be higher than the indirect. Few negative correlations
between growth and rainfall have been reported in tropical rain forests (Clark and Clark
1994; Soliz-Gamboa et al. 2011). However, to separate the direct and indirect effect of
rainfall on tree growth needs additional experiments to assess the effect of hypoxia, detailed
field data of cloudiness, and of photosynthetically active radiation.
In contrast, both Q. lineata and G. glabra showed a positive relationship with water
availability. In these species, the tree-rings´ indices are positively correlated to precipitation
during the rainiest months (Figure 2-3). On the other hand, negative correlations between
tree-rings´ indices and solar radiation during the less rainy months were found when light
availability is high. These results suggest that water excess and low solar radiation could
be limiting growth factors for some tree species but not for the entire tree community.
Moreover, G. glabra is a widely distributed species across precipitation gradients from
seasonal dry forests to hyper humid forests. This species could be considered as a long-
lived pioneer tree species with broad physiological tolerances to water and light availability
(Huc et al. 1994; Santos et al. 2012). Then, G. glabra can be strongly influenced by
precipitation rather than solar radiation. G. glabra defoliates under dry periods (Lacoste and
Alexandre 1991); it indeed defoliates during the less rainy month in our study area (personal
observations), indicating a strong affiliation to precipitation regimes. Q. lineata is a shade-
tolerant species distributed through most of the Choco region. The genus Qualea is broadly
distributed in South American forests, from dry to wet forests. Then, some tree species that
recently colonize hyper-humid forest retain their positive affiliation to precipitation regimes,
while tree species that evolved during long evolutionary periods under hyper-humid
conditions are better adapted to high rainfall to maximize their growth in less rainy months
(Esquivel-Muelbert et al. 2017).
Given the abundance of one resource, it is probable that another one operates as limiting
to growth. For this reason, it is plausible to find positive associations between the tree
growths and the increasing of a limiting resource to (growth factor) when it begins to be
gradually available, and null or negative associations when the same resource exceeds its
abundance and another begins to be scarce. The growth answer with this new resource
would begin to be positive as it increases.
Some environmental predictors used in this study can be unreliable indicators for our
hypotheses. Soil moisture content follow the rainfall pattern; however, it presents little
variation throughout the year (0.59 ± 0.003 cm3 cm-3) compared to other tropical regions
(Solander et al. 2020). This is due to the round-the-year soil wet condition that induces
almost permanent soil saturation. Probably most rainfall is evacuated by surface runoff
rather than infiltration. Then, an experimental assessment will be required to test roots
hypoxia as a limiting factor. NDVI is a good proxy for photosynthetically active radiation
absorbed by the canopy, plant growth, and forest productivity (Glenn et al. 2008; Soudani
et al. 2012). We observed two periods characterized by a decline in NDVI values during
February (less rainy) and October (the rainiest), the months with the highest and the lowest
light availability, respectively. Although dendrometer data from G. glabra tend to match
NDVI variation, much more species and ground data should be included, validating
phenological interpretations and forest productivity due to the exceptional richness of tree
species and the different growth strategies.
2.5 Conclusions
In this study we show for the first time the occurrence of annual growth rhythms in several
trees from a tropical forest with extremely wet conditions. It suggests that bot excess or
deficit of growth factors may explain seasonal cyclicity of growth rhythms in tropical trees,
strengthening our hypothesis. Although there are some limitations and problems in working
with tree rings in hyper-humid forests, is not impossible. A new frontier its open for tree
rings science, it means to extend the application of dendrochronology to hyper humid
environments where it was believed that there was no rhythmic growth.
3. Chapter 3: Isotope signatures in tree rings
reveal growth rhythms occurring in the
least rainy season in a hyper-humid
neotropical forest
With Jorge I. del Valle, Sebastián González-Caro, Carlos A. Sierra
Trees: submitted
Abstract: It is well known that growth-limiting factors such as periodic droughts can induce
periodicities in woody tissue formation in tropical trees. In regions without seasonal
droughts and with sufficient water for photosynthesis, periodicities in secondary growth
have been previously reported but, it is not well-known what factors may induce these
periodic growth rhythms. We obtained woody samples of two tree species, two individuals
per species, from the Biogeographic Chocó region in Colombia, which is one of the rainiest
on the planet, located close to the Pacific Ocean at the equatorial latitude. We measured
stable isotopes of oxygen and carbon (18O and 13C) in wood samples across the last five
growth rings in each species to obtain intra-annual variation in isotopes. We assessed
whether isotope variation correlated with climatic variables, in particular, the pattern of
precipitation regime. We found that both isotopes are correlated between them and with
the ring widths. We also found that the δ18O significantly correlated with the pattern of
precipitation regime. Our results suggest that isotope variation could be considered a
surrogate of tree growth in these hyper-humid and non-seasonal forests. They challenge
previous ideas about the dominant effect of the dry season on tropical tree-growth
periodicities, suggesting water excess as an additional limiting factor controlling growth
rhythms in some tropical trees.
3.1 Introduction
Despite the high variability of plant growth rates among different species and environmental
conditions, the climate is frequently suggested as the main driver for tree growth
(Dannenberg et al. 2019). In trees, some studies have shown the effect of seasonal water
availability or rainfall amount as the main limiting factor for growth and productivity in
neotropical forests (Wagner et al. 2012). These studies usually compare individual tree
species growing across rainfall and seasonality gradients (e.g., space for time substitution
approach). However, the effect of climatic fluctuations over time in the same tree individuals
is not entirely understood, particularly for tropical trees (Rahman et al. 2019). Therefore,
improving our understanding of how tropical trees grow and respond to environmental
drivers, and produce growth rhythms, are essential issues to predict tropical forests
dynamics, their management, conservation, and adaptation to climate change.
The seasonality of environmental variables triggers tree growth rhythms and annual ring
formation (Fritts 1976; Schweingruber 1988, 2007). Annual seasonal flooding, droughts, or
salinity changes, as in estuarine ecosystems, can induce tropical trees to form annual rings
(Callado et al. 2001; Schöngart et al. 2002; Menezes et al. 2003; del Valle et al. 2012;
Parolin et al. 2016). Then, annual growth rings in many tropical tree species could be
explained by the water as a limiting paradigm (Lisi et al. 2008; Groenendijk et al. 2014;
Brienen et al. 2016; Silva et al. 2016; Schöngart et al. 2017). However, in Chapter 1, we
showed that a high proportion of tree species (82% of sampled tree species, n=81) in a
hyper-humid Neotropical forest in the Choco region of Colombia (precipitation >7000 mm
y-1) have tree rings structures. The presence of tree rings in such ecosystems without
evident climatic seasonality suggests the existence of a regular growth periodicity (Fichtler
et al. 2003; Moreno and del Valle 2014; Giraldo et al. 2020) challenge the current
assumptions about the factors inducing growth ring formation in tropical trees. While little
is known about growth rhythms in trees from ever wet tropical forests (without dry periods),
slight variation in rainfall, soil moisture, solar irradiance, cloudiness, sunrise, and sunset
time, have been considered as possible drivers of these rhythms (Breitsprecher and Bethel
1990; Clark and Clark 1994; Borchert and Rivera 2001; O´Brien et al. 2008; Moreno and
del Valle 2014).
Chapter 3 69
Stable isotopes of oxygen, hydrogen, and carbon in tree rings are a complement to
conventional dendrochronological techniques. They can provide information on the
physiological mechanisms that regulate wood growth (Evans and Schrag 2004; McCarroll
and Loader 2004; Anchukaitis et al. 2008; van der Sleen et al. 2017). Plants take up carbon
dioxide (CO2) from the atmosphere and water (H2O) from soils needed to form tissues and
to maintain their metabolism (McCarroll and Loader 2004). Any change in environmental
conditions as relative humidity, soil moisture, radiation, temperature, etc., is captured by
plants and stored as chemical messages in their tissues in different proportions of stable
isotopes (13C/12C, 18O/16O, 2H/1H) (Farquhar et al. 1982; Roden et al. 2000). Depending on
environmental conditions, plants discriminate the relative proportions of isotopes taken up
from the external environment and incorporate them accordingly in their tissues (Managave
and Ramesh 2012). These isotope properties have been useful to study tree growth
patterns. In particular, high-resolution isotope sampling (intra-annual or intra-ring sampling)
has been useful to study the growth rhythms in tropical tree species (Evans and Schrag
2004; Hietz et al. 2005; Anchukaitis et al. 2008; Ballantyne et al. 2011; Managave and
Ramesh 2012; Ohashi et al. 2016). Even in trees that lack growth rings, this method allows
the detection of rhythms in woody tissue formation (Poussart et al. 2006; Pons and Helle
2011; Nakai et al. 2018). Thus, analyses of intra-annual variation of tree rings based on
isotopes and high-resolution environmental data could improve our understanding of
drivers of tree growth.
In the tropics, the higher the amount of annual precipitation, the greater the depletion of the
heavy isotopes of oxygen and hydrogen in rainwater (Kurita et al. 2009). This phenomenon
is known as the amount effect. It is caused by the early removal of heavy isotopes from
clouds by rain so that further rain progressively becomes isotopically depleted (Dansgaard
1964; Rozanski et al. 1993; Risi et al. 2008; Wang et al. 2020). The amount effect leads to
lower δ18O values in plant cellulose that coincide with the growing season (Managave and
Ramesh 2012; Brienen et al. 2016; van der Sleen et al. 2017). In trees growing in areas
where rainfall is very high all months of the year, water deficit is not a limiting factor for
growth. For these areas, we hypothesize that trees record the variability of the water source
in cellulose δ18O variability differently: Low values of δ18O in the cellulose during slow or no
growing periods (at ring boundaries). And higher values of δ18O in the cellulose during the
growing season (at the beginning or near the middle of the ring width), representing high
and low precipitation, respectively. Furthermore, we expect to find higher values, or greater
discrimination of δ13C, during growing periods with low rainfall, or higher incidence of solar
radiation due to cloudiness dispersion (i.e., more negative values of δ13C). In contrast,
during the period of lower radiation (higher cloudiness and higher precipitation), both lower
CO2 fixation and lower discrimination of the heavier carbon isotope (13C) is expected.
In this study, we aim to establish the intra-annual variability of δ13C and δ18O, in tree rings
of Humiriastrum procerum and Virola dixonii, sampled in a non-seasonal tropical hyper-
humid forest. Also, we aim to explore the relationships between isotope composition in tree
rings with environmental variables. To our knowledge, this is the first study on isotope
signatures in tree rings under such wet environments. So, we expect this analysis provides
new insights about tree growth factors acting under extreme rainfall amounts in tropical
forests.
3.2.1 Study area

The Chocó Region extends along the Pacific coast of South America, from the north of
Ecuador to the Colombia-Panama border (Darién Gap). This region is considered the
rainiest in the New World (Poveda and Mesa 2000). In some places, the mean annual
rainfall is over 12,000 mm y-1 (Mesa and Rojo 2020). In the study area, small hills with
slopes up to 45° are frequent, with elevations ranging from 40 - 100 m above sea level. The
soils are mottled grey-yellow clay loam, poor in soil nutrients, and with high iron and
aluminum concentration (Faber-Langendoen and Gentry 1991). We sampled the studied
tree species in the forests belonging to the Community Council of the Low Calima River
Basin, around the Pedro Antonio Pineda Tropical Forest Center of the University of Tolima
(3 ° 57´12.54´´ N, 76 °59´27.96´´ W). In the meteorological station, located within the study
area, the mean annual precipitation exceeds 7200 mm y-1. According to the Gaussen
xerothermic index (Bagnouls and Gaussen 1957) and the monthly potential
evapotranspiration (Holdridge 1967), on average, in the study area, there are no dry months
(Walter et al. 1976). The least rainy month of the year is February, with an average of 370
mm, which almost triples the potential evapotranspiration (127 mm). The mean annual
temperature of 25.9°C is almost constant during all months (Figure 3-1).
Chapter 3 71
Figure 3-1: a. Study area within the Chocó Region with explicit precipitation gradient
(Karger et al. 2017). b. Walter and Lieth’s ombrothermic climate diagram (Walter et al.
1975) of the Bajo Calima Climatic Station (square), which belongs to the Institute of
Hydrology, Meteorology, and Environmental Studies of Colombia (IDEAM). The dark area
indicates an excess of water (all months are hyper-humid).
3.2.2 Sampled species

We sampled four cross-sectional disks of two tree species collected in the study area: two
from Humiastrum procerum (Humiriaceae) and two from Virola dixonii (Myristicaceae). All
trees sampled were growing under similar conditions as dominant trees (15-20 meters of
height) of a closed canopy non-flooded secondary forest (about 70 years of secondary
succession). A very high richness and species diversity characterize this forest, but their
trees´ populations size is small (See Chapter 1 – 2). Individuals from the same species
usually are 50 to 400 m spaced among them. Both sampled species shed their leaves
between August to October (V. dixonii is a partially deciduous tree). Leaf flushing and new
leaves are common between November to February. Little is known about flowering and
fruit production of V. dixonii, but H procerum flowering occurs from February-March. Both
species are wet-forest specialists, and their distribution range goes from Costa Rica to
Ecuador.
3.2.3 Preparation of the Wood samples

Growth rings of these two species are well defined (Figure 3-2), easy to measure, and date,
characterized by the increase in cell wall thickness of fibers, producing a darker area at the
edge of the rings. In both species, vessels are diffuse-porous (Chapter 1). For each species,
we measured their tree-rings width (three radii for each cross-section). We compared ring
widths among individuals to ensure a good cross-dating. We test the tree-rings formation
frequency by the radiocarbon bomb-peak method sampling one or two particular rings in
the cross-sections (Figure 3-2a) (Fichtler et al. 2003; del Valle et al. 2014). We used the
software Cali-Bomb (Reimer et al. 2004) to obtain calendar dates from the radiocarbon
values.
For stable isotope analysis, we cut a radial block of wood approximately 5 mm thick and 10
mm deep from each cross-section, containing the last five tree rings closest to the bark
(Figure 3-2b). After a clear identification of the boundaries of the rings, we cut each tree
ring with a scalpel in several longitudinal slices with a thickness between 0.6-0.8 mm
(Figure 3-2b). This method allowed us to divide each growth ring into a different number of
slices. Each slice was packaged and labeled in Eppendorf tubes for the individual cellulose
extraction process.
Chapter 3 73
Figure 3-2: Wood samples for radiocarbon and stable isotopes analysis. a Sampled tree-
rings for radiocarbon analysis in one cross-section of Humiriastrum procerum. b
Rectangular section used for cellulose extraction and the analyses of stable isotopes in one
cross-section of Virola dixonii. L is the length of the section in mm (the value of L is variable
among trees, depending on the last five tree-rings widths). The width of the rectangular
section was 5 mm. The depth (d) of rectangular sections was 10 mm. We obtained the
slices with a scalpel and a stereomicroscope. The arrows on the edge of the images indicate
the growth-rings boundaries.
We extracted cellulose in each wood sample (both from sampled rings for radiocarbon
analysis as each split slice for stable isotope analysis), following the protocol described by
Steinhof et al. (2017). The first and last step of the procedure involves washing the samples
in a Soxhlet extractor for 12 hours with toluene-isopropanol (1:1) and H2O, respectively.
The intermediate steps include the application of different concentrations of acid (NaClO2,
CH3COOH) and base (NaOH) in micro-filter funnels held in a multiport (temperature 65-
70°C), which facilitated the bleaching of the samples and transforming them into pure α-
cellulose.
3.2.4 Stable isotope analysis

We carried out the mass-spectrometric analysis of stable isotopes of carbon and oxygen at
the BGC-IsoLab (Laboratory of Stable Isotopes of the Max Planck Institute for
Biogeochemistry, Jena, Germany). Both isotope measurements were performed on wood
from the same slice. Stable isotope ratios were measured using a Thermo Fisher TC/EA
oven coupled to a Delta + XL mass spectrometer. The BGC-IsoLab uses three internal
standards calibrated with Vienna Middle Standard Ocean Water (VSMOW) and the
Standard Light Antarctic Precipitation (SLAP); so, all measurement results are presented
on the VSMOW/SLAP references. Both samples and standards were placed in silver
capsules and subsequently analyzed and standardized as described by Gehre et al. (2004).
The proportion of isotopes is expressed in delta (δ) notation, using as international
standards, VSMOW for oxygen and Vienna Pee Dee Belemnite (VPDB) for carbon. Isotopic
ratios are reported as
𝑅𝑠𝑎𝑚𝑝𝑙𝑒
𝛿𝑠𝑎𝑚𝑝𝑙𝑒 = ( ) 𝑥1000,
𝑅𝑠𝑡𝑎𝑛𝑑𝑎𝑟𝑑 −1
where Rsample and Rstandard are the proportions of the heavy isotope versus the light isotope,
for the sample and the standard, respectively. Given the low abundance of isotopes in the
samples, they are expressed in values of per thousand (‰, per mil) (van der Sleen et al.
2017).
3.2.5 Oxygen isotopes in rain

Currently, there is no isotopic information on rainwater for the study site despite its
ecological importance. This fact limits the possibility of directly comparing δ18O values in
wood and δ18O in the rain. However, we use the database of the Global Network of Isotopes
in Precipitation (GNIP) of the International Atomic Energy Agency (IAEA), whose database
extends from 1961 to the present, providing the monthly composition of 18O, 2H, 3H isotopes
in the rain. Although in this network there are few data points for the Chocó region, to
determine the relationship between the contents of δ18O and monthly rainfall, we used data
from lowland tropical areas around the world, characterized by high rainfall (over 2300 mm
y-1). We excluded isotopic data from islands because wind and precipitation regimes may
not be analogous to continental patterns in our study area. Also, we ran the same
Chapter 3 75
correlation only for the site ‘Tulenapa’ (Urabá, Colombia), which is the nearest site with
information in the GNIP dataset.
3.2.6 Statistical analysis

To assess the relationship between isotope measurements (δ18Ocellulose, δ13Ccellulose), tree-
ring width, and climate, we ordered the isotope data from the most internal ring to the
external one (close to bark) of the tree samples. We assigned monthly values of
precipitation, temperature, relative humidity, cloudiness, solar brightness for each year,
under the assumption that the most external ring corresponds to the year of sampling. We
obtained the climatic variables from IDEAM, Colombia, and NASA Ges Disc-Earthdata
(https://disc.gsfc.nasa.gov/). We ran correlation analyses among all variables and using the
lme4 package in R (Bates et al. 2015). We employed generalized linear mixed-effects
models (GLMMs) to assess the relationship between isotope data, tree-ring widths, and
selected climatic variables. All variables were scaled (mean equals zero, and the standard
deviation equals one), allowing comparison among model results. We ran the GLMMs with
all the variables that showed significant cross-correlations. All models included an individual
tree as a random factor controlling for repeated measurements in the same individual.
Finally, we obtained the marginal and conditional R2 for each model.
3.3 Results
Due to a lack of data on the isotopic composition of rain in our study area, we established
a separate relationship with data from the GNIP database. This separate dataset showed
a negative correlation between δ18O in the rain and the monthly rainfall for the humid
lowland tropics (r = -0.39, p–value < 0.05, n = 96). For a different area, less rainy, but in the
same biogeographical region, we also observed a negative correlation between these
variables (r= -0.77, p-value <0.05, n =12) (Figure 3-3). Precipitation at the area for which
we have δ18O data (Tulenapa) follows the same intra-annual pattern as our st1udy area.
Therefore, we assume that δ18O in rainfall for our site follows a similar pattern, which we
use to explain the variation in our observations of δ18Ocellulose.
Figure 3-3: Relationship between δ18O in the rainwater and the monthly rainfall for the
humid lowland tropics. rall uses 96 pairs of values (grey points and black line), and rTulenapa
use 12 values from January to December (red points and dashed line) from Tulenapa,
Colombia, a place with isotopic data of rain within the Choco Region. * significance (95%).
Data are available in Table S2.
The 14C results in the F14C metric and their calibrations in the calendar years are presented
in Table 3-1. We tested the isotopic signature of 14C of different tree rings in all cross-
sections. The number of years between calibrated dates was the same as the tree-ring
number between radiocarbon sampled rings (Table 3-1), which confirms the annual nature
of sampled species. According to this result, tree rings marked and counted allow us to
know the real age of trees. Furthermore, the tree-ring width series match by crossdating
between the two sampled trees of each species. We found mean significant serial
intercorrelation values (p-value <0.05); in H procerum was 0.57, and 0.40 for V. dixonii. The
series intercorrelation represents the common-level signal recorded in tree-ring for the
available tree samples; few for developing a chronology, but enough to complement our
stable isotope observations.
Chapter 3 77
Table 3-1: Results of 14C dating and calibration in calendar dates of the samples. Values
in parentheses indicate the probability percent given by CALIBomb (Reimer et al. 2004)
and mean calibrated date rounded to the first integer calendar year. DBH: diameter at
breast height, (*) years difference estimated with the last ring.
Years Tree-
differen ring
DB CALIBomb Mean ce number
H Radioca Calibrated CALIBomb calibrat between between Tree
Sample (cm Heigh rbon age range (1 Calibrated age ed dated dated age
Especies ID ) t (m) Sample F14C σ) range (2 σ) date samples samples (years)
[1990.7-
1.1482 ± 1991.96] [1990.38+1992.
A 0.0019 (1.0) 63] (0.94) 1991
[2000.75- [2000.28-
1.0881 ± 2001.94] 2002.61]
Hpro65 56.5 20 B 0.0016 (1.0) (0.942) 2001 10 10 36
Humuriastr [2006.98-
um 1.0578 ± 2008.87] [2005.88-
procerum Hpro82 29.9 18 A 0.0020 (0.96) 2009.24] (0.89) 2008 8(*) 8(*) 43
[2000.75- [2000.26-
1.088 ± 2001.98] 2002.66]
A 0.00180 (1.0) (0.941) 2001
[2003.02- [2002.34-
1.0749 ± 2004.65] 2005.16]
Vdix43 13.4 15 B 0.0021 (1.0) (0.926) 2004 2 2 36
[1988.46- [1988.06-
1.1717 ± 1989.54] 1990.00]
A 0.0021 (1.0) (0.924) 1989
[1991.85- [1991.08-
Virola 22.9 1.1395 ± 1993.16] 1993.55]
dixonii Vdix199 8 18 B 0.0020 (1.0) (0.950) 1992 3 3 36
We observed a cyclic pattern in δ18Ocellulose values in the tree rings, which coincides with the
beginning and the end of the tree-ring boundaries (Figure 3-4). Such seasonal variation is
similar in the two radial sections of H. procerum; but not so clear in V. dixonii (Figure 3-4).
Within rings of H. procerum, low values of δ13Ccellulose appear (greater discrimination of
δ13C), but there is no obvious pattern. The intra-annual variation of δ18Ocellulose for H.
procerum was from 20.7 to 29.5‰ and from 21.8 to 28.3‰ for V. dixonii. The δ13Ccellulose
values were less conspicuous and ranged from -29.5 to -28.1‰ in H. procerum and from -
30.6 to -27.2‰ in V. dixonii (Figure 3-4). The local minimum values of δ18Ocellulose coincided
with the end and the beginning of the rings´ boundaries. These facts suggest non-random
patterns that match the tree rings of H. procerum with their isotopic composition (Figure 3-
4).
Figure 3-4: The radial variation of δ18Ocellulose (blue) and δ13Ccellulose (red) of two individuals
of Humiriastrum procerum: sample code 65 (a, b) and 82 (c, d). The same for two individuals
of Virola dixonii: sample code 199 (e, f) and 43 (g, h). Values at the top panels indicate tree-
ring widths in mm. The vertical lines indicate the limits of the annual rings. The year
corresponding to each ring appears at the bottom of each chart.
We found significant negative correlations (p-value <0.05) between carbon and oxygen
isotopic values in cellulose both at the borders and inside the rings with some environmental
variables. We observed a negative correlation (r= -0.46) between the δ18O at the border of
the rings (δ 18Orb) and the mean precipitation during the quarter of January-February-March
(PmeanJFM), and with precipitation of the driest month (Pmin) (r= -0.49, n = 20). Other
Chapter 3 79
variables that correlate with δ 18Orb are ring width (Rw) (r= -0.58, n =20), mean cloudiness
during the quarter of February-March-April (CmeanFMA) (r= -0.47, n =20). We obtained a
negative correlation between δ13C, at the border of the rings (δ13Crb), and Rw (r= -0.75, n
=20). We also found significant correlations between isotopes: δ 13Crb versus the maximum
value of δ13Ccellulose within the ring (δ 13Cwr) (r= 0.66, n = 20, the only positive), and δ 13Cwr
versus the maximum value of δ18Ocellulose within the ring (δ 18Owr) (r= -0.54, n = 20) (Figure
3-5). We did not find significant correlations with other variables.
Figure 3-5: Pearson´s correlation matrix of the δ18O and δ13C values observed in the tree
rings versus environmental variables (p-value <0.05). White cells lack statistical
significance. δ18Orb: δ18Ocellulose value at the ring boundary, δ13Crb: δ13Ccellulose value at the
ring boundary, δ13Cwr: the maximum value of δ13Ccellulose within the ring, δ18Owr: the maximum
value of δ18Ocellulose within the ring, PmeanJFM: mean rainfall during the January - February -
March quarter, Pmin: rainfall of driest month, CmeanJFM: mean cloudiness during the January
- February - March quarter, CmeanFMA: mean cloudiness during the February - March – April
quarter, RW: ring width.
We found similar results for the relationships among the variables depicted in Figure 3-5
using linear mixed-effect models and cross-correlation analysis. All models showed
differences between marginal and conditional R2 underlying the effect of the autocorrelation
of woody tissue data within individuals rather than climatic effects. Our mixed effect models
confirmed that these relationships are not an artifact of the sampling design (Table 3-2).
We found that marginal R2 duplicates the conditional R2 (Table 3-2). This result means that
the individual effects (random factors) exceed the effect of the precipitation surrogates
(fixed factors) in the isotope variation. Also, δ13Crb had a higher individual variation than
δ18Orb relative to ring width, based on the difference between marginal and conditional R2.
This result suggests that δ13Crb variation is affected differently among individuals, while
δ18Orb depends on the wood accumulation rate. Finally, precipitation surrogates are related
to δ18O potentially as a product of tree growth.
Table 3-2: Generalized linear mixed-effects models to assess the relationship with some
significant variables observed in cross-correlation analysis. δ18Orb: δ18Ocellulose value at the
ring boundary, PmeanJFM: average rainfall during the January - February - March quarter,
Pmin: precipitation during the driest month, CmeanJFM: average cloudiness during the
January - February - March quarter, CmeanFMA: average cloudiness during the February -
March – April quarter, RW: ring width. (p-value <0.05).
Model Estimate t-value p-value R2 Marginal R2 Conditional
Intercept 1.3x10-15 0.0 1.0
δ18Orb ~ PmeanJFM -4.8x10-1 -2.94 0.01 0.20 0.54
Intercept 1.2x10-15 0.0 1.0
δ18Orb ~ Pmin -4.8x10-1 -2.65 0.018 0.20 0.47
Intercept 2.13x10-15 0.0 1.0
δ18Orb ~CmeanFMA -4.04x10-1 -2.06 0.05 0.16 0.34
Intercept 1.24x10-15 0.0 1.0
δ18Orb ~ Rw -5.84x10-1 -3.05 0.0067 0.32 0.32
Intercept 2.3x10-16 0.0 1.0
δ13Crb ~ Rw -3.86x10-1 -2.49 0.023 0.18 0.68

Chapter 3 81
3.4 Discussion
This chapter reports annual tree-rings and intra-annual isotopic signals of two species
growing in a hyper-wet and non-seasonal precipitation forest. Similar isotopic studies are
scarce in the tropics and exceptional in such rainy environments (precipitation over
4000mm) (Van der Sleen et al. 2015).
We provide evidence of intra-annual variation related to precipitation regimen based on

isotope variation of tree rings. In particular, isotope variation (δ18O) in cellulose follows
patterns coinciding with the ring boundaries of H. procerum but not for V. dixonii. There is
a correlation between the two isotopes, even if the surrogates of precipitation poorly
correlate to δ13C. Furthermore, we found a negative relationship between stable isotopes
in the cellulose and some precipitation variables; in particular, the mean precipitation during
the driest quarter (386 ± 87 mm). Moreover, the ring widths are negatively related to the
δ13Ccellulose (δ13Crb and δ13Cwr). The environmental response of δ13C is lower than that of
δ18O, and therefore, more difficult to detect. Thus, we provide evidence of intra-annual
variation related to precipitation regimen based on isotope variation in one of the most
humid regions of the world.
The variation in isotope concentration in the tree wood samples correlates with the tree-
ring boundaries. This pattern is clearer for δ18O but not for δ13C, probably because δ18O is
less affected by physiological discrimination processes. The highest values of δ18Ocellulose
occur within the rings (δ18Owr), i.e., during the growing period (Figure 3-4). Lower values of
δ18Ocellulose tend to occur close to ring boundaries (δ18Orb). This because of high precipitation
values or by leaf shedding. The studied trees develop their root systems in the first 40 cm
of soil. In such a case, probably soil water δ18O signature is the same as rainwater
(McCarroll and Loader 2004). The first and second third of the rings are produced with
water from the less rainy months, reflecting higher δ18O value. In contrast, during the rainy
months, at the end of growth rings (ring boundaries), rings reflect the low δ18O value of the
heavy rains (Figure 3-4). The δ18Ocellulose contains reliable information about local rainfall.
Their concentrations vary throughout the year, tightly coupled to rainfall. This result
suggests an environmental δ18O variation in the rainwater related to the water source:
monthly precipitation explained by the “amount effect” hypothesis or the inverse relationship
between monthly δ18O and precipitation amounts (Risi et al. 2008; Managave and Ramesh
2012).
High concentrations of δ18O during the less rainy season can be amplified in tree wood as
because of water evapotranspiration from the soil surface and leaves (Managave and
Ramesh 2012). Our results suggest that the growth of the two species occurs mainly during
the lowest rainy period of the year. An excess of humidity during that period (January,
February, March) drives a reduction in tree growth, evidenced by thinner growth rings
(Figure 3-4, Figure 3-5). This situation coincides with low δ18O values at the end of the ring,
at the same time that precipitation increases significantly. Simultaneously, radiation
decreases according to the relationship between δ18Orb and CmeanFMA. Therefore, an
increase in precipitation during the JFM quarter may be synergistically combined with a
reduction in solar radiation, contributing to reducing tree growth. Particularly, the H.
procerum tree-rings index is positively correlated with the solar radiation during the less
rainy months of the year and negatively correlated with the rainiest season of the year
(Chapter 2).
The δ18O signature in cellulose helps to identify the annual rings controlled by seasonal
changes in precipitation. It reflects low values during the highest rainy season. Identifying
annual growth increments is usually more effective with δ18O than with δ13C (Ohashi et al.
2016; van der Sleen et al. 2017). This fact is evident in our study (Figure 3-4). Some authors
claim that the growth ring delimitation through isotopic signatures is possible only if the
annual precipitation pattern is strongly marked (Managave and Ramesh 2012; Ohashi et
al. 2016; van der Sleen et al. 2017). They suggest few or no isotope signature in areas
where rainfall is even throughout the year. However, we found that small changes in
monthly rainfall amounts are enough to be expressed in the δ18O signature of tree-ring
cellulose. Although the effect of leaf shedding during the rainiest month could exert an effect
in such a season pattern.
The amplitude of the intra-annual variation of δ18O and δ13C in H. procerum are 8.7 ‰ and
1.41 ‰, respectively. The magnitude of this amplitude is similar to that reported, by other
authors, for species that grow in climates with high seasonal rainfall changes (Pons and
Helle 2011; Ohashi et al. 2016; Cintra et al. 2019). In V. dixonii, the amplitude of the isotopic
variation throughout the growth rings was smaller in δ18O (6.4 ‰) and larger in δ13C (3.3
Chapter 3 83
‰). Ohashi et al. (2016) found a mean amplitude of δ18O in the cellulose of the growth rings
of about 3 – 6 ‰ and a less distinct variation lower than 1‰ in δ13C. Pons and Helle (2011)
showed that Goupia glabra (a common species in our study area) has a mean δ18O
amplitude of around 2‰.
The evidence provided by correlations between the seasonal patterns of δ18O observed in
the cellulose supports our hypothesis, at least for H. procerum, which tends to register lower
δ18O values in its growth rings as precipitation increases. In climates where trees grow
during the rainy season, as water deficit is a limiting factor to growth, some researchers
have observed maximum δ18O values at ring boundaries when the precipitation is the
lowest during the year (Evans and Schrag 2004; Ballantyne et al. 2011; Ohashi et al. 2016).
In all these study areas, annual precipitation is substantially lower than in our study area;
and they suffer from seasonal droughts where the water deficit is limiting for tree growth,
which is not the case in our study area. Here, tree growth occurs during the less rainy
season, as occurs in forest episodically flooded, and water excess is a growth-limiting
factor. Consequently, low δ18O values at the ring’s boundaries and high values within the
ring (Cintra et al. 2019). Therefore, we concluded that rainwater excess is the most likely
limiting factor for tree growth in these two species. This conclusion is also supported by
observations presented in Chapter 2 for H. procerum and independent observations of band
dendrometers from two trees of the studied species (Figure 3-6).
Figure 3-6: Automatic band dendrometer observations vs. precipitation. Curves with bars
represent cumulative mean monthly growth of tree circumference (mm). The dashed line
corresponds to mean monthly precipitation (mm month-1).
In addition, studies on gross ecosystem productivity report high or increasing

photosynthetic activity during the less rainy season in the tropical wet forests (absent water
deficit), but photosynthetically limited due to high cloud coverage and rainfall (Restrepo-
Coupe et al. 2013; Green et al. 2020). This fact means slow or no growth in rainiest months
and high growth during less rainy months. In turn, the highest values of δ18O occur during
the first or second third of the rings corresponding to the earlywood, when the
environmental conditions are favorable for growth because of low rainfall. Apparently, up to
now, no previous research of this type has been carried out in such a highly humid
environment and without marked seasonal contrasts of rain or flooding. More precise
measurements (with large datasets) are critical for a broad understanding of tree growth
and the productivity of these forests.
3.5 Conclusions
We found that δ18Ocellulose is more robust than δ13Ccellulose for identifying annual rings and to
relate isotope composition to environmental variables. We believe that, the use of both
δ18Ocellulose as δ13Ccellulose provides, complementary information to the analysis of tree rings
Chapter 3 85
in non-seasonal tropical environments. However, additional research is needed to expand

this work to other species to obtain more information on isotope endmembers. In particular,
it would be useful to perform isotopic measurements of the meteoric water source, which
would allow us to pose new hypotheses about trees growing in nonseasonal hyper-humid
tropical climates. Our results, in concert, suggest that the intra-annual growth rhythms of
the studied trees are driven by water excess. In fact, according to Shelford´s law, all
organisms have both minimum and maximum thresholds for the different environmental
factors among which their population grows. Near these thresholds, organisms grow under
stress, limited to both deficit and excess (Shelford 1931; Niinemets and Valladares 2008).
So, in non-seasonal and hyper-humid forests (without dry periods), the availability of water,
measured as rainfall, is close to the maximum tolerance threshold for some species.
4. Chapter 4. Radiocarbon and
dendrochronology applied in a legal
dispute: A case from Colombia
With Jorge I. del Valle
Published: Radiocarbon https://doi.org/10.1017/RDC.2020.30
Abstract: In 2015 a dispute arose between an electricity company (EC) and smallholder of
a plantation teak when the company felled 80 trees (without consent of the owner) in a
linear transect under a rural power-line-corridor (PLC) fragmenting the teak stand in two
portions. EC stated that the area was no planted trees at the time of PLC establishing in
2008. The owner asserted he planted the stand in 2006 so in 2008 the company should
have seen planted trees. We used the bomb 14C signal of three felled trees and
dendrochronological dating five trees: three felled by the EC, and two felled by us in 2016
to do this study to determine the age. We found that the first growth rings were dated in
2005 both in the trees felled by EC in 2015 and felled by us in 2016, one year before to that
reported by the owner (2006). This year corresponds to the wood present in the cuttings at
stand planting year. These facts are in agreement with the owner´s testimony. The
plantation was 10 years old in 2015. Not seven or fewer years, as the EC alleges.
4.1 Introduction
The study of tree rings (dendrochronology) is a powerful tool to reconstruct the climatic
variations throughout the last centuries (Cook and Kairiukstis; Fritts 1976; Schweingruber
1988; Speer 2010; Hughes et al. 2011). Tree rings allow us to date the occurrence of
extreme climatic events such as maximum and minimum river flows, water levels in
reservoirs, among others. Another application has been in geomorphological research, in
which tree rings are useful to date and to study erosive processes such as landslides, rock,
and debris fall, volcanic events, tsunamis, etc., and that extend from a few years to
centuries (Haneca et al. 2006; Stoffel and Bollschweiler 2008; Speer 2010; Stoffel et al.
2011). In archaeology, tree rings have been employed to define the exact year in which the
trees were felled, altered or used for the construction of artifacts or buildings (Speer 2010;
Rubino and Baas 2019). In addition, dendrochronological methods have been useful to
prove the authenticity of some art pieces and musical instruments (Grissino-Mayer et al.
2004; Bernabei et al. 2017). In summary, dendrochronology is a useful and scientifically
accepted method to reconstruct the temporality of particular events.
In another context, the investigation and resolution of legal questions require the dating of
specific events to make decisions based on accepted scientific methods. For example, the
application of the dendrochronological methods focused on examining material related to
an alleged criminal act or legal dispute rests in forensic sciences. The application of
dendrochronology in criminalistics is called forensic dendrochronology (UNODC 2016). Its
use ranges from ecological studies up to dating wood pieces from illegal logging, the origin
of wood, dating of standing buildings, to dating wooden objects or objects that coincide with
crime scenes, through the characterization of wood anatomy or tree rings (Jozsa 1985;
Schweingruber 1988; Wolodarsky-Franke and Lara 2005; Ng et al. 2017; Köse et al. 2018;
Lehmann and Arruda 2019). This method is highly accepted in temperate regions in which
dendrochronology has been developed and widely used in many applications. In contrast,
in the tropics, dendrochronological applications are more recent.
Although there have been dendrochronological researches in the tropics for more than a
hundred years, only recently, the studies are growing exponential (Brienen et al. 2016).
These studies have confirmed the presence of annual growth rings in at least 220 tree
Chapter 4 89
species in the Neotropics (Brienen et al. 2016; Schöngart et al. 2017). The integration of
dendrochronological methods with radiocarbon dating has increased the accuracy and
certainty in determining the exact year of a growth ring in tropical trees. For this purpose,
tropical dendrochronologists frequently use the bomb-pulse radiocarbon, a term referring
to the sudden increase of 14C in the Earth's atmosphere due to hundreds of aboveground
nuclear bombs tests intensified between 1950 until 1963, when the Limited Test Ban Treaty
was signed (Worbes and Junk 1989). Here, we combined dendrochronology and the bomb-
pulse dating method to improve the resolution of temporal events in a legal dispute related
to land appropriation. In this case, we reconstruct the date of felling of some trees in a teak
(Tectona grandis) plantation. It is worth noting that teak has showed annual growth rings in
all places where this species has been studied (Pumijumnong et al. 1995; Deepak et al.
2010; D’Arrigo et al. 2011; Nocetti et al. 2011). Our hypothesis is that teak has annual rings
in our study area.
Dispute context
During September 2006, a smallholder planted three hectares of teak (Tectona grandis) in
Apartadó (Antioquia, Colombia). Teak is one of the most appreciated and valuable tropical
timbers of the world's timber trade (Kollert and Kleine 2017)). For the plantation with a
density of 1,233 trees/ha, the property owner (PO) used cuttings of about 50 cm in length
and about 1cm in diameter from new branches of another teak plantation. This method
allows an initial fast-growing and reduces tree mortality. In August 2015, nine years after
the teak plantation, the staff of an electricity company (EC) entered the property to check a
power-line-corridor (PLC) established in 2008 that crosses through the teak plantation.
Allegedly without the owner´s permission, the EC staff felled 80 trees growing under the
PLC, degrading and fragmenting the commercial area of the teak plantation in two stands.
After the owner´s complaints, the EC asserted that the area was not planted at the moment
of PLC establishment in 2008. According to the PO, he established the teak plantation in
2006, two years before that the PLC was constructed, and claimed that the EC officials
must have seen the planted trees in this place. We were asked to establish how the age of
both the stumps under the PLC and the living trees in the teak plantation surrounding the
PLC.
4.2.1 Study area

The teak plantation is located in Northern of Chocó Biogeographic Region, Colombia
(7°53′05″N - 76°38′06″W), close to Colombia-Panamanian border. The area is hilly, with
slopes ranging from slightly up to moderately inclined and an elevation ranging between 80
and 220 m altitudes. We obtained climate data from Tropical Rainfall Measuring Mission
(TRMM) (TRMM 2011) from 2000 - 2015. Mean annual precipitation and mean annual
temperature are 2,823 mm, and 26.7 °C, respectively. February, with about 65 mm, is the
month with the lowest rainfall. During the other months´ rainfall is over 100 mm. The mean
temperature is nearly the same all year round.
4.2.2 Field sampling

In 2016, we visited the study area to gather evidence that would support the facts (Figure
4-1). We measured the affected transect and counted the stumps of the felled trees under
PLC. To determine the age of trees felled, we cut three cross-sections at random from the
stumps felled in 2015 by the EC. To date the living trees from the plantation, we felled two
trees and obtained a cross-section of each one close to the ground. The use of complete
cross-sections is mandatory in this case because it is difficult to handle an increment borer
near ground level and reach the pith.
4.2.3 Sample preparation

The cross-sections were processed in the Tropical Dendroecology Laboratory of the
National University of Colombia at Medellin. The cross-sections were oven-dried at 28 °C,
up to reach a constant weight. To highlight the tree rings, we polished the cross-sections
with abrasive sandpaper, from 60 to 600 grains. The cross-sections were scanned at a
resolution of 1,800 dpi in an Epson Expression 10,000XL Scanner calibrated for
dendrochronological studies for Regent Instruments, Canada. The high-resolution images
allowed us to characterize the tree-rings width with a precision of about 10-15µm. All
images were processed with Image J11.52i software (Schindelin et al. 2012).
Chapter 4 91
4.2.4 Tree ring analysis

We marked and counted the tree rings from the bark to the pith of each cross-section. We
assigned calendar year 2016 to the last and still incomplete rings in the cross-sections of
the trees felled by us, because the sampling of the cross-sections was done in mid-July
2016 and growth season of teak in this place occurs from March - December. The same
procedure was performed for the cross-sections extracted from the stumps of the trees
apparently cut down by the EC (according to PO testimony), but assigning 2015 to the last
ring adjacent to the bark. In this way, all samples were dated, assuming an annual formation
frequency of the tree rings. By comparing the number of rings in the cross-sections of both
the trees felled by the EC in 2015 and by us in 2016, with the planting date provided by the
PO, it allowed us to determine the frequency of ring formation.
Figure 4-1: Photos of the felled area in the teak plantation (1166 m2): A) image of the
affected area taken in September 2015 by the property owner; B) the stump of one of the
felled trees; C) view of the felled area in July 2016, where some epicormic shoots of the
felled trees are visible.
4.2.5 Radiocarbon analysis

To validate the planting date obtained under the hypothesis of annual ring formation, we
used the modern radiocarbon fraction (F14C) (Stenström et al. 2011). We extracted about
4 to 6g of wood from the oldest part of the trees, the closest to the pith of three cross-
sections: One sample from a felled tree by the EC in 2015 (labeled TK2 in Table 4-1), and
two pieces from two trees felled by us in 2016 (labeled TK4 and TK5 in Table 4-1). The first
ring near the pith was the thinnest and came with the planted cuttings. The second ring was
also very thin since teak dedicates most of the photosynthetic products during this first
phase of the ontogenetic growth to roots, leaf production, and primary, not secondary
growth (Rao and Rajput 1999; Husen and Pal 2006) Then, most of the wood for radiocarbon
analysis by the conventional radiometric method had to be extracted from the third ring in
samples TK2 and TK5, to complete the amount of wood needed for the analysis: a mixture
of the 1st, 2nd and 3rd rings. In sample TK4, since all the initial growth rings were very thin,
the fourth ring contributed most of the wood mixture sample used for radiocarbon analysis.
The wood samples were sent to the Laboratory of Radiocarbon Analysis of the Institute of
Health and Medical Ecology, in Ukraine (Code IHME), for the determination of F14C by the
conventional radiometric method.
The wood samples were grinded to a fine powder. Then were submitted to solid-liquid
extraction in Soxhlet apparatus (6-7 hours). After extraction wood sample was dried at 105
°C about 3-5 hours to constant mass. Pre-treated wood samples were converted into
benzene, using of benzene line (http://benzene-line.com/). Benzene sample was counted
by liquid scintillation spectrometer (Quantulus 1220TM) using of Teflon vials (Skripkin and
Kovaliukh 1997; Skripkin and Buzynnyi 2017).
To calibrate the radiocarbon analysis in F14C, we used the bomb-pulse (post-bomb

calibration) and the CALIBomb program (Reimer et al. 2004), and the Northern Hemisphere
Zone 2 (NHZ2) calibration curve with one-year smoothing. The NHZ2 is the most
Chapter 4 93
appropriate calibration curve for the study site. This curve was extended from 1950 to 2010
with data from Hua et al. (2013).
4.3 Results
Our measurements made in the field indicated that the felled area was 1,166 m2 (11.6 m x
100 m; 3.88% of the planted area). We counted 80 stumps of the original teak plantation
as evidence of the felled trees (Figure 4-1). The results of the growth rings analysis are
presented in Table 4-1.
The cross-sections allowed us to characterize the anatomy of the wood in the transverse
plane (Figure 4-2). The teak growth rings can be observed by the naked eye; they are
defined by bands of terminal parenchyma (white arrows in Figure 4-2). Vessel distribution
is diffuse. The pores or vessels do not follow any clustering pattern. In all samples observed,
the heartwood occupies three-quarters of cross-sections, which is notable from an
economic point of view.
Table 4-1: Age determined in some trees cut down by the electric company and by us in
the teak plantation, by counting the number of growth rings from the bark (felled date) to
the pith.
Disc Tree
diameter height First Last Number of
Code (cm) (m) ring ring rings (age1) Annotations
2005 2015 11 Tree felled in 2015 by the
TK1 22.9 - company
TK2 22.8 - company
TK3 34.9 - company
TK4 34.7 17.4 2005 2016 12 Tree felled in 2016 to this study
TK5 23.2 16.6 2005 2016 12 Tree felled in 2016 to this study
1 Years old.
Tree-rings marked and counted allow us to know the real age of these trees (Table 4-1).
Because the trees whose cross-sections were examined by us from the felled area (TK1,
TK2, and TK3 in Table 1-4) were alive when cut down, we can assume all 80 felled trees
were alive when they fell under the PTL. Therefore, the last growth rings formed, or under
formation, present in these cross-sections were of the year 2015 (Figure 4-2A). Based on
these last rings formed in 2015, by counting the rings, we established the date of formation
of the previous rings up to the pith: The first tree rings correspond to 2005. Likewise, we
determined that, in the trees cut down by us in 2016 (TK4, and TK5 in Table 1-4), the first
rings dated from 2005, and by extension, the first rings of all planted trees were 2005.
Figure 4-2: Photos showing the retrospective dating of the growth rings in teak cross-
sections: A) cross-section from a tree felled in 2015 (TK2), absent bark probably due to
fungi decay; B) cross-section from a tree felled in 2016 (TK4). White arrows indicate the
growth ring boundaries.
Chapter 4 95
There are two main findings. The first one is that in all cross-sections sampled, the first
growth ring dated from 2005 (TK1 to TK5, in Table 4-1). This conflicts with the PO, who
claims he planted the trees in 2006. However, as the PO indicates they did not plant seeds
but cuttings, which already had one ring at time of planting. Therefore, the plantation in
2016 was 10 years old and trees were 11 years old. The other find is that the cross-sections
of trees felled by us and felled by the EC differ in only one ring (Table 4-1 and Figure 4-2).
These facts provide strong evidence of the annual nature of the growth rings in the study
teak trees, proving the hypothesis.
Table 4-2: Results of 14C dating and calibration in calendar dates of the samples TK2, TK4,
and TK5.
Mean
Sample Weigh Calibrated age Calibrated age calibrated
F14C
Code (g) range (1 Sigma) range (2 Sigma) date3
[2006.56 – [2005.21 - 2007

TK21 4.7 1.058 ± 0.005
2009.12] (0.93) 2009.24] (0.88)
[2008.52 - [2007.43 - 2008
TK42 4.7 1.046 ± 0.005
2009.24] (0.42) 2009.24] (0.52)
[2005.35 - [2004.84 - 2007
TK52 5.7 1.062 ± 0.004
2007.84] (0.92) 2009.24] (0.90)
1Thisis a dead tree felled in 2015 by the electric company.
2Trees felled by us in 2016.
3Date rounded to the first integer calendar year. Values in parenthesis values indicate of
probability percent gives by CALIBomb.
The 14C results in F14C and their calibrations in calendar years are presented in Table 2-4
and Figure 3-4. As we explained in the methods, given the small amounts of wood supplied
for the 14C analysis by the first and second ring, closest to the piths of the cross-sections,
the third and fourth growth rings supplied most wood for the three 14C analysis. Then, the
14C isotopic signature of the year 2007 dominates in the TK2 and TK5 samples, and that of
2008 in the sample TK4 in the F14C analysis. Given that, in the cross-sections where the
TK2 and TK5 samples were extracted, the third rings from the pith to the bark were dated
by counting the rings as belonging to the year 2007, and the fourth ring of the TK4 sample
to the year 2008, the 14C dating also confirms the annual nature of the teak growth rings in
the study area.
4.4 Discussion
Teak have showed annual rings many other places around tropical region (Pumijumnong
et al. 1995; Deepak et al. 2010; D’Arrigo et al. 2011; Nocetti et al. 2011; Castaño 2016).
Here we also find annual growth rings in teak by counting retrospectively from the last
known date ring (Figure 4-2, and Table 4-2) to the pith and by bomb-pulse radiocarbon
dating (Table 4-2).
Our results show that when the trees were cut down by the electricity company in 2015, the
trees had 11 rings; that is, they were 11 years old (Table 4-2). The age of the trees does
not coincide with the planting date because, because the PO used cuttings of almost 1 year
old for planting. Therefore, the plantation was 10 years old in 2015.
It is evident that the cuttings were less than one year aged, and that their first rings were
barely forming. However, since all the leaves are removed from the cuttings before planting,
their growth stops. Only after the roots are formed with the energy supplied by the non-
structural carbohydrates stored in the parenchymal tissue of the cuttings wood, appear
primary growth´s shoots, and then the leaves, with which the first planting growth rings
begin to form. These rings and the subsequent rings tend to be tiny. Given that it is well
known that teak trees grow rapidly in height during the first years, but proportionally not so
much in diameter (de Camino and Morales 2013). Consequently, the isotopic signature of
the wood of the years 2007 and 2008 prevailed, given that most samples came from these
growth rings. The first two rings, closer to the pith, produced very few amounts of wood
useful for radiocarbon dating by the conventional radiometric method, which requires at
least 4g of wood. To dating exactly the first ring of the cuttings planted and dated 2005 by
rings count, we should have used the AMS (Accelerator Mass Spectrometer) radiocarbon
dating method, which requires approximately 400 times less mass of wood samples, but it
is much more expensive for a smallholder.
Chapter 4 97
Figure 4-3: Graphs showing the post-bomb 14C calibration dates with 2 σ of the samples
TK2, TK4, and TK5 using CALIBomb: A) sample TK2 dated the year 2007 after the bomb-
spike with an 88% probability, or the year 1957 with a 12% probability, before the spike; B)
sample TK4 dated the year 2008 with a 52% probability, or the year 1957 with a 48%
probability; C) sample TK5 dated the year 2007 with a 90% probability, or the year 1957
with 10% probability
The vessel distribution observed was diffuse (Figure 4-2A and 4-2B), in spite that wood
anatomists often describe the teak growth rings defined by circular to semicircular porosity
(pores grouped at the beginning of the ring), accompanied by a terminal parenchyma band
(Vásquez and Ramírez 2005; Richter and Dallwitz 2009). This suggests a kind of plasticity
of the hydraulic traits, under conditions with abundant irrigation or rain, this anatomy may
change as evidenced by recent work (Nocetti et al. 2011; Cardoso et al. 2015). It is
important to note that this study area over 2,823 mm a year in rainfall.
As shown in Table 4-2 and Figure 4-3, the probability of the dating with 2σ after the spike
of the bomb-pulse was 88% (2007), 52% (2008), and 90% (2007) for samples TK2, TK4,
and TK5, respectively. The reason why the radiocarbon dates were not 2005, as shows the
dendrochronological analysis, but 2007- 2008 (Table 4-2), is because the wood samples
used for dating are composed of a mixture of wood coming from 1th, 2th 3th tree rings in
TK2 and Tk5, and from 1tst to the 4th rings in TK4. However, radiocarbon results and the
tree-rings analysis validate the annual tree-rings frequency of tree rings in the teak of our
study area.
CALIBomb, as well as other programs to calibrate radiocarbon dating with the bomb-pulse,
systematically assign a higher probability to the dates after the bomb spike (del Valle et al.
2014). Therefore, more important than these probabilities are the knowledge we have about
the most likely dates. That is, are they before or after the bomb spike? In this study, there
is no doubt that they are after the bomb spike; all dates obtained in Table 4-2 are 100%
likely.
4.5 Conclusion
Dendrochronology and 14C dating combined emerge as a tool for effectively resolving some
disputes in forensic sciences related to tree cutting dating in tropical tree plantations. During
post-bomb years, the precise dating of the first growth ring around the pith of trees using
AMS 14C dating would be a great advantage.
5. General conclusions
Tropical dendrochronology has faced successfully several obstacles: The belief that
tropical trees had no annual growth rings, the complexity of wood anatomy, the lack of
knowledge on physiological processes or mechanisms of woody plant species to induce
annual tree rings formation, the variety of ecosystems with different climatic conditions, and
the vast plant diversity in the tropics. However, the colossal effort made by several scientists
in the past decades, teaches us that every obstacle is a research opportunity.
Most ecologists call tropical rain forests to several different ecosystems of the tropical
lowlands with annual rainfall over 2,000 mm. Only the Holdridge system discriminates
between moist forests (2,000 <4,000 mm), wet forests (4000 <8000 mm), and rainforest
(over 8000 mm) and explicitly recognize the existence of the hyper-humid tropical forests.
The existence of hyper-humid forests in the Chocó Biogeographic Region, with no apparent
water seasonality, as well as the observation of the wood of its trees that, at the naked eye,
revealed the existence of growth rings, were the opportunities we took advantage of.
The exceptional species richness of these forests in which, on average, there are only about
two trees of the same species in one hectare is also an Achilles heel for
dendrochronologists: As most trees are rare species, for dendrochronological studies is
very difficult to collect enough replicas. However, we found that, in these forests, there are
some relatively common species ubiquitously dispersed in the landscape with high
dendrochronological potential, such as Qualea lineata, Goupia glabra, Apeiba macropetala,
and Humiriastrum procerum, all except G. glabra, new for dendrochronology.
100 Título de la tesis o trabajo de investigación
We are aware that we have only opened a small window in the challenge of studying the
dendrochronology of tropical hyper-humid forests. But this first investigation invites other
researchers to explore this new mine of tree species for dendrochronological studies, to
use their rings as climate proxies. Therefore, new research should be carried out looking
for species with annual rings and dendrochronological potential. New researches should
focus on the most long-lived tree species to go back into the most remote past possible.
In this research, we found that, in contrast to the belief of many scientists, of 81 species
studied in Chapter 1, 82% had growth rings, 46% with well-defined rings, and 18% with
high dendrochronological potential. In chapters 1, 2, and 4, we show that 17 tree species
growing in the Biogeographic Chocó Region of Colombia have annual growth rings. Of
these trees, eight are new for dendrochronology. All 17 radiocarbon-dated species resulted
in annual growth rings (Chapter 2 and Chapter 4). Four species that had between four and
twelve replicates in Chapter 2 resulted in annual growth rings, dated both by
dendrochronological and radiocarbon methods. The tree rings widths were sensitive to
different environmental signals.
This research allowed answering several questions, extending the application of

dendrochronology to the little-explored hyper-humid environments. Our observations in
concert with Shelford law suggests that bot excess or a deficit of growth factors may explain
seasonal cyclicity of growth rhythms in tropical trees. In two species (H. procerum, A
macropetala) tree-rings index were negatively correlated with the rainiest season, and
positively correlated with the solar radiation during the less rainy season. However, other
two species (Q lineata, G. glabra) reveal a behavior typical of the species growing in zones
experience a dry season, or reduced precipitation for several months. In these two species,
the more water, the better the growth response, as suggested by the positive association
between tree-ring indices and precipitation. In such a case, it seems that some tree species
that colonize hyper-humid forest retain their positive affiliation to the original precipitation
regimes. Other tree species that evolved under hyper-humid conditions are better adapted
to high rainfall maximizing their growth during less rainy months.
The growth period of H. procerum occurs during the less rainy season, based on the
positive comparisons between the tree-rings index with the solar radiation during the less
¡Error! No se encuentra el origen de la referencia. 101
rainy months; and the negative correlation with the rainiest yearly season. The δ18O
concentrations we observed during the less rainy season can be amplified in the ring wood
because of water evapotranspiration. An excess of humidity during that period (January,
February, March) drives a reduction in tree growth, evidenced by thinner growth rings. This
situation coincides with low δ18O values at the end of the ring, at the same time that
precipitation increases significantly.
Given the abundance of one resource, it is probable that another one operates as limiting
to growth. For this reason, it is plausible to find positive associations between the tree
growths and the increasing of a limiting resource when it begins to be gradually available.
And null or negative associations when the same resource exceeds its abundance and
another begins to be scarce. The growth answer with this new resource would begin to be
positive as it increases.
Since the distant studies of Geiger in 1915, describing annual growth rings in Tectona
grandis from Indonesia, and of Coster, who in 1927 found annual rings in tropical tree
species also from Indonesia, of Alan Mariaux’s studies in 1967 discovering annual tree
rings in many tropical species from Africa. Since the revival of tropical dendrochronology
with Martin Worbes' studies in the Amazon during the 1980s, tropical hyper-humid forests
had been, with very few exceptions, practically avoided or unknown by
dendrochronologists. Until today, tropical dendrochronology has worked, in several
subdisciplines, with species from all environmental conditions in which trees can grow in
the tropics, except for hyper-humid lowland forests without evident hydric seasonality.
This research begins to fill a gap in knowledge in tropical dendrochronology. The claims of
many renowned scientists, based on prejudice rather than evidence, are beginning to fall.
The species with dendrochronological potential discovered here, and the many more that
must be in these forests, await some attention from the dendrochronological scientist's
community. This is the main conclusion of my dissertation.
A. Appendix: Age determination by
post-bomb 14 C and by tree rings
Appendix A. Age determination by post-bomb 14C and by tree rings in samples from 14
tree species. Calibrated ages were obtained by CaliBomb software (Reimer et al. 2004),
and with Northern Hemisphere Zone post-bomb calibration data (NHZ2). Pre-dated ring
(year): dendrochronological age; F14C: modern fraction of 14C (Postbomb); Calibrated date
1 σ and 2 σ (Prob): Mean calibrated age range with 1 sigma and two sigmas, values in
parentheses indicate of probability percent given by CALIBomb. The lowest probabilities
are not included. Cal AD: Mean calibrated age. Diff.: Difference between Cal AD and Pre-
dated ring (year). First ring: date of the first distinct ring in the sample, the pith or close to
it. Last ring: date of the last ring closets to the bark or sampling year.
Calibrated Calibrated
Sample Pre-dated date date Cal. First Last Age
Tree species Family code ring (year) F14C 1 σ (Prob.) 2 σ (Prob.) AD Diff. ring ring (years)
1.0998
± 1999.3 1999.2
Amac40_1 1999 1.9‰ (1.0) (0.95) 1999.2 0.2
Apeiba
Malvaceae
macropetala
1.072
± 2004.3 2004.4
Amac40-2 2005 2.4‰ (0.983) (0.914) 2004.3 -0.7 1995 2016 21
1.104
± 1998.3 1998.3
Amac42_1 1999 2.3‰ (1.0) (0.962) 1998.3 -0.7
1.0748
± 2003.9 2003.8
Amac42-2 2003 2.3‰ (1.0) (0.925) 2003.8 0.8 1985 2016 31
1.1105 1996.9 1997.0

Amac104_1 1997 ± 2‰ (1.0) (0.947) 1997.0 0.0 1978 2016 38
Castilla
Moraceae
elastica 1.0524
± 2008.6 2008.3
Cela183-1 2009 2.3‰ (0.882) (0.8) 2008.5 -0.5 1935 2016 81
Clarisia
Moraceae
racemosa 1.0496
± 2008.9 2008.5
Crac186-1 2009 2.2‰ (0.61) (0.65) 2008.7 -0.3 1997 2016 19
Goupia
Goupiaceae
glabra 1.1497
± 1991.2 1991.3
Ggla64-1 1991 1.9‰ (1.0) (0.93) 1991.3 0.3 1979 2016 37
Anexo B. Nombrar el anexo B de acuerdo con su contenido 105
1.0819
± 2002.4 2002.6
Ggla64-2 2003 1.5‰ (1.0) (0.931) 2002.5 -0.5
1.1188
± 1995.5 1995.3
Hbra130-1 1996 1.8‰ (1.0) (0.94) 1995.4 -0.6
Hevea
Euphorbiaceae
brasiliensis
1.1046
± 1998.2 1998.2
Hbra130-2 1998 1.8‰ (1.0) (0.964) 1998.2 0.2 1968 2016 48
1.4925 1971.8 1971.7

Hpro100-1 1972 ± 2‰ (1.0) (0.969) 1971.7 -0.3
Humiriastrum
Humiriaceae 1.3302
procerum
± 1978.0 1977.8
Hpro100-2 1978 2.3‰ (1.0) (0.927) 1977.9 -0.1 1922 2016 94
1.1482
± 1991.3 1991.5
Hpro65-1 1991 1.9‰ (1.0) (0.94) 1991.4 0.4 1980 2016 36
1.0881
± 2001.3 2001.4
Hpro65-2 2001 1.6‰ (1.0) (0.942) 2001.4 0.4
1.0578 2007.9 2007.6

Hpro82-1 2008 ± 2‰ (0.96) (0.889) 2007.7 -0.3 1947 2016 69
1.1832
± 1987.7 1987.5
Iacr20-1 1987 2.3‰ (1.0) (0.927) 1987.6 0.6
1.1633
± 1989.9 1989.8
Inga acreana Fabaceae Iacr20-2 1989 2.2‰ (1.0) (0.91) 1989.8 0.8 1916 2016 100
1.1934
± 1986.7 1986.6
Ing16-1 1987 1.9‰ (1.0) (0.915) 1986.7 -0.3
1.1455
± 1991.7 1991.7
Inga sp. Fabaceae Ing16-2 1992 1.8‰ (1.0) (0.948) 1991.7 -0.3 1954 2016 62
1.14 ± 1992.5 1992.3

Mabe25-1 1992 1.8‰ (1.0) (0.951) 1992.4 0.3
1.1181
± 1995.6 1995.4
Mabea sp Moraceae Mabe25-2 1995 1.8‰ (1.0) (0.931) 1995.5 0.5 1947 2016 69
1.0889
± 2001.2 2001.3
Olat12-1 2001 2.1‰ (1.0) (0.93) 2001.3 0.3 1968 2016 48
1.2677
± 1980.8 1980.9
Olat14-1 1980 2.7‰ (0.901) (0.89) 1980.8 0.8
1.1584 1990.3 1990.4

Olat14-2 1990 ± 2‰ (1.0) (0.907) 1990.3 0.3 1970 2016 46
1.0759
Otoba ± 2003.6 2003.7
latialata Myristicaceae Otat80 2004 2.9‰ (1.0) (0.923) 2003.6 -0.4 1963 2016 53
1.1868
Pterandra ± 1987.4 1987.2
ultramontana Malpighiaceae Pult88-1 1988 2.6‰ (1.0) (0.925) 1987.3 -0.7 1953 2016 63
1.0736
± 2004.0 2004.2
Qlin103-1 2004 2.6‰ (0.997) (0.917) 2004.1 0.1
1.0638
Qualea ± 2006.3 2006.7
lineata Vochysiaceae Qlin103-2 2007 3.1‰ (0.97) (0.898) 2006.5 -0.5 1956 2016 60
1.2655
Symphonia ± 1981.0 1981.0
globulifera Moraceae Sglo86-2 1981 2.1‰ (0.922) (0.904) 1981.0 0.0 1966 2016 50
1.1074
± 1997.5 1997.7
Tcol128-1 1996 1.8‰ (1.0) (0.972) 1997.6 1.6
Tachigalii
Fabaceae
colombiana
1.0516
± 2008.7 2008.4
Tcol128-2 2008 1.8‰ (0.806) (0.769) 2008.6 0.6 1974 2016 42
1.1012
± 1999.0 1998.9
Tcol51-1 1999 1.9‰ (1.0) (0.958) 1998.9 -0.1 1965 2016 51
1.1944
± 1986.6 1986.5
Tcol71-1 1987 1.9‰ (0.918) (0.907) 1986.6 -0.4
1.154
± 1990.7 1990.9
Tcol71-2 1990 1.8‰ (0.9) (0.9) 1990.8 0.8
1.1248
± 1994.5 1994.6
Tcol71-3 1995 1.8‰ (1.0) (0.94) 1994.6 -0.4 1953 2012 59
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Annual Tree Rings in The Rainiest Forests of The Americas: Jorge Andrés Giraldo Jiménez

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Annual Tree Rings in the Rainiest

Forests of the Americas

Jorge Andrés Giraldo Jiménez

Universidad Nacional de Colombia

Jorge Andrés Giraldo Jiménez

Universidad Nacional de Colombia

Gracias al Herbario Medel de la Universidad Nacional de Colombia y a Jorge Mario Vélez

Esta investigación fue apoyada por el proyecto 4083 de la Universidad Nacional de

Keywords: dendrochronology, Chocó region, radiocarbon, stable isotopes, tropical trees.

Anillos de crecimiento anuales en la región más

En esta disertación, exploro el potencial dendrocronológico de los árboles de los bosques

Palabras clave: dendrocronología, Región del Chocó Biogeográfico, radiocarbono,

1. Chapter 1. Dendrochronological potential of trees from America's rainiest

3. Chapter 3: Isotope signatures in tree rings reveal growth rhythms occurring in

3.2.4 Stable isotope analysis ........................................................................ 74

4. Chapter 4. Radiocarbon and dendrochronology applied in a legal dispute: A

5. General conclusions ............................................................................................... 99

Bibliography .................................................................................................................. 111

The booming of dendrochronology in tropics has allowed answering several questions

The objectives of this study are

Published in Pompa-García M., Camarero J. (eds) Latin American Dendroecology.

Keywords: Tree rings, Non-seasonal rainfall, Biogeographic Chocó Region, Colombia

Although information on growth periodicity of trees species in tropical hyper-humid, non-

1.2 Materials and methods

1.2.1 Study area

1.2.2 Dry month analysis in study area

1.2.4 Processing of wood samples

1.2.5 Observable anatomical characteristics

1.2.6 Growth ring periodicity

1.2.7 Pantropical growth ring potential

1.3 Results and discussion

(a) (b) (c)

(a) (b) (c)

Marila macrophylla Cross-

Licania caldasiana Cross-

Clusia leptanthera Semi-ring- Cross-

Tapura costata Semi-ring- Cross-

Dipteryx oleifera Cross- Biogeographic

Inga rubiginosa Cross-

Tachigali colombiana Cross-

Fabaceae Abarema sp. ± A,B Diffuse-porous Low 1 Core Wide distribution

Couratari guianensis Cross-

Cariniana pyriformis Cross-

Gustavia occidentalis Cross- Biogeographic

Apeiba macropetala Semi-ring- Cross-

Phragmotheca Cross- Biogeographic

Sterculia aerisperma Semi-ring- Cross-

Michelang., Judd &

Castilla elastica var.

Clarisia racemosa Cross-

Moraceae Ficus sp. - A,B Diffuse-porous None 1 Core Wide distribution

Otoba latialata Cross- Biogeographic

Isertia pittieri Cross- Biogeographic

Posoqueria latifolia Cross-

Casearia arborea Cross-

Pouteria engleri Cross-

Pouteria collina Cross- Biogeographic

Pouteria eugeniifolia Cross-

Simarouba amara Cross-