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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 763-771, April-June 2021 (Published June 30, 2021)

Limited evidence of coupling between above and belowground

functional traits in tropical dry forest seedlings

Rosa Arrieta-González

1,2

; https://orcid.org/0000-0002-3169-5015

Juan Paez

; https://orcid.org/0000-0002-0774-8391

Yamileth Dominguez-Haydar

; https://orcid.org/0000-0002-3103-9878

Beatriz Salgado-Negret

2,3

*; https://orcid.org/0000-0002-3103-9878

1. Departamento de Biología, Universidad del Atlántico, Puerto Colombia-Atlántico, Barranquilla, Colombia;

rarrieta@unal.edu.co, yamilethdominguez@mail.uniatlantico.edu.co

2. Departamento de Biología, Universidad Nacional de Colombia, Bogotá, Colombia;

bsalgadon@unal.edu.co (*Correspondence)

3. Grupo de Investigación en Química y Biología, Universidad del Norte, Barranquilla, Colombia;

jpaezg93@gmail.com, bsalgadon@unal.edu.co

Received 06-IV-2021. Corrected 15-VI-2021. Accepted 28-VI-2021.

ABSTRACT

Introduction: Water availability is one of the main factors determining the distribution of woody species in

the tropics. Although the functional mechanisms that determine the species tolerance to water deficit have been

extensively studied in adult individuals, the responses of early ontogenetic stages have been less explored.

Objective: To identify functional strategies and trait correlations between different seedlings’ dimensions (leaf,

stem, and root). We expect limited coordination between above and below-ground functional traits due to a

single conservation-acquisition trade-off cannot capture the variability of functions and environmental pressures

to which the root system is subjected.

Methods: We measured 12 functional traits belonging to 38 seedling species in a tropical dry forest in Colombia.

We explored the relationships between pairs of traits using Pearson correlations, and to obtain an integrated view

of the functional traits, a principal component analysis (PCA) was performed.

Results: The results showed limited evidence of linkage between above- and below-ground traits, but we did

find significant correlations between traits for the continuum of conservative and acquisitive strategies. Root

traits related to water and nutrient take capacity formed an orthogonal axis to the acquisitive-conservative

continuum.

Conclusions: Our results showed that dry forest seedlings have different functional strategies to cope with water

deficit. The incorporation of root traits helps to explain new functional strategies not reported for leaf and stem

traits. This study contributes to understanding the mechanisms that explain species coexistence and is particu-

larly relevant for predicting future forest trajectories.

Key words: acquisitive strategy; Colombia; conservative strategy; functional traits; water deficit; water storage.

Arrieta-González, R., Paez, J., Dominguez-Haydar, Y., &

Salgado-Negret, B. (2021). Limited evidence of coupling

between above and belowground functional traits in

tropical dry forest seedlings. Revista de Biología Tropical,

69(2), 763-771. https://doi.org/10.15517/rbt.v69i2.46549

https://doi.org/10.15517/rbt.v69i2.46549

Water availability is one of the main envi-

ronmental factors determining the establish-

ment and distribution of tree species at local

and regional scales (Engelbrecht et al., 2007;

Markesteijn et al., 2011; Méndez-Alonzo et

al., 2012). Different studies have shown that

the performance of species varies in response

to water availability, and this is explained

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through their functional traits (Engelbrecht

et al., 2007; Poorter & Markesteijn, 2008;

Markesteijn et al., 2011; González-M et al.,

2020). For instance, species adapted to drought

have developed functional traits that allow

them to maintain growth despite low soil water

potentials. Among the most studied traits are

stomatal closure and leaf deciduousness, which

allows plants to avoid dehydration during the

driest periods of the day or year (Markes-

teijn et al., 2011; Méndez-Alonzo et al., 2012).

Water storage in tissues to maintain xylem

water transport and low levels of dehydration

(Borchert, 1994; Scholz et al., 2007; Pineda-

García et al., 2013), investment in deep roots to

access more humid soils (Paz et al., 2015), or

the presence of dense tissues that do not dehy-

drate and promote high resistance to cavitation

(Bonal & Guehl, 2001; Comita & Engelbrecht,

2014). Despite this knowledge, studies are

still needed that incorporate traits associated

with other plant structures and functions, such

as root traits.

Functional traits can be coupled to define

functional strategies, and tree species exposed

to water deficit are distributed along a con-

tinuum of traits related to tissue investment

and a hydraulic safety-efficiency trade-off

(Méndez-Alonzo et al., 2012; Pineda-García

et al., 2015; González-M et al., 2020). At one

extreme, there are species with high invest-

ment in dense tissues, dense stems with narrow

xylem vessels, high leaf dry matter content,

and leaf longevity. These species with dense

and hydraulically safe tissues, known as “con-

servative” species, have low growth rates but

high survival (Poorter et al., 2008). The other

extreme are the “acquisitive” species charac-

terized by thin, short-lived leaves with high

investment in nutrients and less dense stems

with wide xylem vessels. These soft tissues

and their high hydraulic efficiency result in

high growth rates but low survival (Poorter et

al., 2008). Root trait dimension has been less

explored. One hypothesis postulate that roots

follow the “acquisition-conservation” trade-off

analogous to leaf economic spectrum (Weems-

tra et al., 2016). However, recent studies have

found mixed evidence (Valverde-Barrantes et

al., 2015; Withington et al., 2006; Weemstra et

al., 2016), showing decoupling between above

and below ground traits (Withington et al.,

2006; Weemstra et al., 2016; Freschet et al.,

2020). Recent work showed a trade-off in C

investment between deep roots and water stor-

age tissues associated with successional and

old-growth forest species, respectively (Paz

et al., 2015). These studies invite to discuss

the correlations between functional traits and

whether coordination between traits reported

in adults develops from the first stages of

plant development.

Understanding the response mechanisms

to drought is particularly relevant in seedlings

because regeneration allows for the inference

of forest successional trajectories and ulti-

mately is key to determining forest resilience

(Osuri et al., 2017). Additionally, seedlings are

the most sensitive to environmental changes as

they have poorly developed roots that do not

reach deep soil layers (Engelbrecht & Kursar,

2003) and must compete for water and nutri-

ents with established adult individuals (Lewis

& Tanner, 2000). Furthermore, seedlings face

light limitations in the understory that reduces

their photosynthetic and growth rates (Romo,

2005); and in turn, they have limited carbo-

hydrate reserves to invest in organs such as

leaves or roots (Poorter & Markesteijn, 2008).

These characteristics, added to the fact that

many tropical species can spend decades under

understory (Hubbell et al., 1999), make this

ontogenetic state the bottleneck for establishing

individuals and forests of the future.

Tropical dry forest is an ideal model for

understanding how tree species cope with

drought. First, it presents a strong dry season

where soil water deficit limits tree species’

growth and establishment (Murphy & Lugo,

1986; González-M et al., 2019). Second, strate-

gies to cope with water deficit have been well-

studied in adult individuals, but it is unclear

whether these strategies are fully developed

from the seedling ontogenetic stage. And third,

high fragmentation rates in this ecosystem can

amplify the climatic severity due to the edge

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effects with effects on its structure and diver-

sity (González-M et al., 2019). Understanding

the functional mechanisms that determine seed-

ling establishment will strengthen our ability

to predict and understand these forests’ future

under climate change scenarios in which great-

er seasonality and reductions in rainfall are

expected (Dai, 2013; Feng et al., 2013).

This study evaluated the variation of 12

functional traits above and belowground in 38

species of dry forest seedlings. The selected

traits are related to the different strategies of

plants to cope with drought, such as investment

in dense tissues, efficiency in root foraging

of water and nutrients, and the water stor-

age capacity (Markesteijn & Poorter, 2009;

Méndez-Alonzo et al., 2012; Pineda-García et

al., 2013; Paz et al., 2015; Salgado-Negret et

al., 2016). The main objective was to identify

the functional strategies and the correlation

among pairs of traits belonging to different

plant dimensions (leaf, stem, and root). We

expected species are distributed along with two

extreme strategies, acquisitive and conserva-

tive. However, we expect low coordination

between above and below-ground functional

traits due to a single conservation-acquisition

trade-off cannot capture the variability of func-

tions and environmental pressures to which the

root system is subjected (Valverde-Barrantes et

al., 2015; Weemstra et al., 2016).

MATERIALS AND METHODS

Study area and species selection: This

study was carried out in a tropical dry forest

located in Caribbean region in Colombia (Bras-

ilar, municipality of San Jacinto, department of

Bolívar - 9°53’40” N, 75°10’57” W), located at

an altitude between 352 and 602 m a.s.l.

We selected 38 seedling species belonging

to 32 genera and 21 families (14 deciduous

and 24 evergreen species; Digital appendix

1). The species selection was based on their

high abundance in the study area, and together

they represented more than 80 % of the total

abundance of seedlings registered in 96 plots

of 1 m

previously established for the area

(Salgado-Negret, data unpublished). For abun-

dant species, between 4 and 15 individuals

(57.8 %) and rare species, between 1 and 3

individuals (42.1 %), were sampled. All indi-

viduals were located in similar light conditions

(canopy cover varied between 72.1 % and 98.4

%) and similar relative soil humidity (6.36 and

21.1 %). The individuals had a height between

40 and 70 cm. Harvest of each seedling was

carried out by digging with a shovel 50 cm

around the stem to avoid losing the fine roots.

The sampled seedlings were stored in plastic

bags, labeled, and transported to the field

station for processing.

Functional traits: In total, 12 functional

traits belonging to the leaf, stem, and root

dimensions were measured, following the

protocols of Poorter and Markesteijn (2008),

Pérez-Harguindeguy et al. (2013), Paz et

al. (2015) and Salgado-Negret et al. (2016).

Leaf traits were estimated for five leaves per

individual. Each leaf was weighed fresh and

scanned (Canon Canoscan LiDE 220) to esti-

mate the leaf area (LA, mm

). Leaf thickness

(LT, µm) was measured for each fresh leaf

with a digital micrometer (Mitutoyo reference

293-240-30) in three different sections of the

leaf, and avoiding the main veins. The leaves

were dried at 70 ºC for 48 hours to estimate the

dry weight, and from which the specific leaf

area (SLA, cm

/g) and leaf dry matter content

(LDMC, mg/g) were calculated.

Stem density (SD, g/cm

) was estimated

by dividing the dry mass (dried at 70 ºC for 48

hours) and the green volume calculated by the

water displacement method (Salgado-Negret

et al., 2016). The stem water content (SWC,

mg/g) was estimated by dividing the weight of

the fresh water-saturated stem sample by the

oven-dry weight. With the hydrated roots, the

fresh weight of the whole root was estimated,

then they were dried at 70 ºC for 48 hours to

estimate the dry weight. Using an architectural

criterion, the roots were separated into primary

and secondary roots. The root dry matter con-

tent (RDMC, mg/g) was calculated as the

relationship between the dry weight and the

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fresh weight of the secondary roots. The root

water content (RWC, g/g) was determined as

the relationship between the fresh weight and

the dry weight of the primary root. The sec-

ondary-to-primary-root-mass ratio (SPRMR,

g/g), was calculated as the secondary root mass

per unit primary root mass (Markesteijn &

Poorter, 2009). The aboveground-to- below-

ground -length ratio (AUL, cm) was calculated

as the ratio between seedling height (cm) and

maximum root depth (MRD, cm), both traits

were estimated with a tape measure. Finally,

leaf, stem and root mass fractions (LMF, SMF,

RMF, g/g) were calculated as dry mass of each

organ per unit dry plant mass). At the end, the

LMF and SMF (LSMF, g/g) were summed as

an indicator of the aboveground biomass of

the plant.

To explore the relationships between pairs

of traits, Pearson correlations using the Bon-

ferroni correction were performed. In order

to obtain an integrated view of the functional

traits, a principal component analysis (PCA)

was performed using the 38 species and the

12 functional traits to identify the functional

strategies of the species. All analysis were

performed using R statistical language (R Core

Team, 2015).

RESULTS

Significant correlations were reported

between traits of different seedlings’ dimen-

sions (Fig. 1). Functional strategies were

observed in the PCA (Fig. 1, Table 1), and the

first two ordering axes explained 61.4 % of the

species’ variation as a function of the function-

al traits. PCA reported two functional continua;

the first was dominated by the “trade-off”

between resource conservation and acquisition.

Conservative species showed high leaf and

root dry matter contents (LDMC and RDMC)

and high stem density (SD), while acquisitive

species were related with high water content

in roots (RWC) and stems (SWC) (Fig. 1). The

traits that defined each of these strategies were

negatively correlated (i.e., decoupled; Table 2).

The second continuum separated the species

with high investment in belowground biomass

(RMF) and deep roots (MRD) from the species

with tall height above ground (AUL), shallow

roots, and high investment in secondary roots

(Fig. 1, Table 2). Leaf traits such as SLA and

LT were not correlated with other functional

traits (Table 2).

TABLE 1

Loadings and proportion of variance of the principal

component analysis of leaf, root and stem traits of 38

species of seedlings from a dry forest in Colombia

Functional traits Comp.1 Comp.2

LDMC 0.29 0.225

SLA -0.133

LT -0.198

SD 0.319 0.359

RMF 0.307 -0.353

RWC -0.353 -0.264

SPRMR -0.323 0.255

RDMC 0.253 0.342

AUL -0.337 0.225

SWC -0.281 -0.368

MRD 0.339 -0.305

LSMF -0.307 0.353

Proportion of variance 38.6 22.8

Trait abbreviations: leaf dry matter content (LDMC),

specific leaf area (SLA), leaf thickness (LT), stem density

(SD), root mass fraction (RMF), root water content (RWC),

econdary-to-primary-root-mass ratio (SPRMR), root dry

matter content (RDMC), aboveground-to belowground

length ratio (AUL), stem water content (SWC), maximum

root depth (MRD) and leaf-stem mass fraction (LSMF).

DISCUSSION

Using 12 functional traits measured in

38 seedling species from a tropical dry for-

est, we found limited evidence of coupling

between above and belowground traits, with

the exception of tissue density (conservative

strategy) and storage capacity of stems and

roots (acquisitive strategy). Furthermore, roots’

traits relating to the ability to forage water

and nutrients formed an orthogonal axis to

the acquisitive-conservative continuum. These

results show that root traits cannot be reduced

to a single axis of variation, which is probably

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Fig. 1. Principal component analysis (PCA) of the average values of functional traits by species. Above-ground (green) and

below-ground functional traits (red). The percentages of variation explained by the first two axes of the ACP are included

in the graph. See trait abbreviations in Table 1.

TABLE 2

Pearson correlations with Bonferroni correction between leaf, root and stem traits of 38 species

of seedlings from a dry forest in Colombia

LDMC SLA LT SD RMF RWC SPRMR RDMC AUL SWC MRD LSMF

LDMC 1 -0.46 -0.31 0.59** 0.05 -0.55* -0.42 0.4 -0.33 -0.4 0.28 -0.05

SLA 1 -0.43 -0.15 -0.01 0.23 0.23 -0.01 0.23 0.06 -0.23 0.01

LT 1 -0.31 0.04 0.13 0.21 -0.31 0.06 0.11 0.05 -0.04

SD 1 0.07 -0.74*** -0.27 0.58** -0.35 -0.79*** 0.19 -0.07

RMF 1 -0.30 -0.60** 0.2 -0.49 -0.11 0.68*** -1***

RWC 1 0.19 -0.64*** 0.32 0.74*** -0.36 0.30

SPRMR 1 -0.05 0.71*** 0.07 -0.61*** 0.60**

RDMC 1 -0.05 -0.67*** 0.05 -0.2

AUL 1 0.2 -0.79*** 0.49

SWC 1 -0.14 0.11

MRD 1 -0.68***

*P <0.05, **P < 0.01, ***P < 0.0001. Trait abbreviations: specific leaf area (SLA), leaf dry matter content (LDMC), leaf

thickness (LT), leaf-stem mass fraction (LSMF), stem density (SD), stem water content (SWC), root water content (RWC),

root dry matter content (RDMC), root mass fraction (RMF), secondary-to-primary-root-mass ratio (SPRMR), aboveground-

to belowground length ratio (AUL) and maximum root depth (MRD).

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related to the multiple functions that they fulfill

in the individual. Plants have different combi-

nations of traits that enable them to deal with

water limitations in these ecosystems.

The PCA did show that tissue density (SD,

RDMC, and LDMC) was coordinated across

plant dimensions, which has been reported

previously in seedlings (Poorter & Markesteijn,

2008; Markesteijn & Poorter, 2009; Pineda-

García et al., 2015; Weemstra et al., 2016).

The coordination of high tissue density is

an important strategy to cope with drought

because species with dense stems are gener-

ally associated with narrow xylem vessels that

allow them to reduce the risk of cavitation of

the xylem (Markesteijn et al., 2011; Méndez-

Alonzo et al., 2012). Additionally, a high den-

sity of fibers with thick cell walls may protect

the xylem from the strong negative pressures

generated by drought (Hacke et al., 2001).

Dense, smaller, and more rigid leaves, have

small transpiration surfaces that reduce the

plants’ wilting and water requirements (Poorter

et al., 2009). Examples of conservative species

are Trichilia carinata (Meliaceae), Machae-

rium lanceolatum (Fabaceae), and Chiococca

alba (Rubiaceae). Additionally, our results also

showed coordination between water storage

capacity in stems and roots. Water storage

plants have low stem density which do not

resist the xylem’s high tension during the dry

seasons, which could have acted as a selection

pressure promoting water storage in their tis-

sues (Méndez-Alonzo et al., 2012). The root

water storage is essential for the maintenance

of photosynthetic and growth rates during

dry seasons but also in the hours of greatest

daytime transpiration when there may be a

significant delay between the loss of water in

the leaves and the absorption of water by the

roots (Čermák et al., 2007). For the tropical

dry forest, seedlings can use the water stored

in the stems (SWC) to delay hydraulic failure

for months (Pineda-García et al., 2013), and

the high root water storage of seedlings (RWC)

allows them to function physiologically in

drought conditions (Poorter & Markesteijn,

2008). Piper piojoanum (Piperaceae), Piper

reticulatum (Piperaceae), and Anacardium

excelsum (Anacardiaceae) are examples of

water storage species.

The orthogonal axis to the acquisitive-

conservative continuum was related to the

roots’ ability to forage water and nutrients in

the soil. At one extreme, we found coordina-

tion in belowground traits related to explore

and forage deep soils (high RMF and MRD).

At the other end, species with shallow roots

(low MRD), high secondary root biomass (high

SPRMR), and high inversion on above ground

length (high AUL) were located. Plants in dry

forests have shown two main root strategies:

deep roots with high carbon investment to

explore the more humid soil horizons or invest-

ing in water-storing tissues (Paz et al., 2015;

Prieto et al., 2015). Because the two strategies

involve investing in the construction and main-

tenance of different types of tissues, the trade-

off is expected and has even been associated

with different successional stages (Paz et al.,

2015). Contrary to these studies, our results did

not show this dichotomy, and root water stor-

age (RWC) was decoupled from traits related

to water and nutrient foraging such as MRD,

RMF, and SPRMR. These results mean that

both species with deep roots and high invest-

ment in root biomass (high MRD and RMF)

and species with shallow roots with a high

proportion of secondary roots (high SPRMR)

can store water in their root tissues. Examples

of water storage species with shallow roots are:

Sorocea sprucei (Moraceae) and Ruellia mac-

rophylla (Acanthaceae), while Eugenia florida

(Myrtaceae) would be the species with deep and

water storage roots. Despite this orthogonality,

our results show that most of the acquisitive

species with water-storage roots had shallow

roots with high secondary roots investment.

These water-storage roots are associated with a

greater capacity for soil exploration, absorption

of nutrients and water (Eissenstat et al., 2000;

Roumet et al., 2006; Paz et al., 2015; Prieto et

al., 2015). Conversely, species with thick and

deep roots will have greater resistance to water

deficit because these provide more specialized

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functions for the transport of water and nutri-

ents (Paz et al., 2015; Prieto et al., 2015).

The decoupling between acquisitive-con-

servative continuum and the roots´ ability to

forage water and nutrients could have differ-

ent explanations. First, as the root system has

different functions, mechanical support, and

transport and storage of water and nutrients

(Eissenstat et al., 2000; Prieto et al., 2015), its

functional traits must be optimized to comply

with the three functions that could imply the

absence of a maximization of a trait associated

with a particular function. Second, the water

and the essential elements that plants acquire

from the soil have different properties, causing

the same trait to not be efficient in absorbing

all the elements (Weemstra et al., 2016). And

third, the physical properties of the soil exert

selective forces on the root system, which

could limit the maximum development of

traits for the acquisition of a specific limiting

resource (Weemstra et al., 2016). Under this

scenario, it seems likely that the roots have dif-

ferent strategic dimensions and that these vary

according to local conditions, which makes it

difficult to generate patterns in the correlations

between the above and belowground traits.

This study found limited trait coordina-

tion between above- and belowground traits

and novel trade-offs regarding belowground

trait correlation. A remarkable finding was the

decoupling between the acquisitive-conserva-

tive continuum from the ability to forage water

and nutrients of roots. Our results showed that

dry forest seedlings have multiple strategies to

cope with drought and highlight the importance

of incorporating root traits for a comprehen-

sive understanding of the responses of plants

to environmental conditions. This variety of

functional strategies, and, therefore, the parti-

tion of niche between species, could help to

explain the high diversity of species at the local

scale reported in tropical dry forests. However,

it is essential to recognize that traits may vary

with ontogeny, which is a variation source

rarely accounted. Additionally, these results

could help predict the species´ responses to

future climatic scenarios, to allow the selection

of species capable of establishing themselves

under different environmental conditions and

guide restoration actions in the most endan-

gered terrestrial ecosystem in the Neotropics.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We are grateful to the expert botanist

Álvaro Idárraga for his help identifying the

species. Natalia Norden, Hermes Cuadros, and

Ana Belén Hurtado provide helpful comments

on earlier versions of this manuscript. Finally,

without the generosity of Mr. Eduardo Torres,

Mrs. Reyna, and Eduardo Torres, who opened

the doors of their home, this work would not

have been possible.

RESUMEN

Evidencia limitada de acoplamiento entre rasgos

funcionales por encima y por debajo del suelo

en plántulas de bosque seco tropical

Introducción: La disponibilidad de agua es uno de los

principales factores que determina la distribución de las

especies leñosas en los trópicos. A pesar que los meca-

nismos funcionales que determinan la tolerancia de las

especies al déficit hídrico han sido ampliamente estudiados

en los individuos adultos, las respuestas de estados ontoge-

néticos tempranos han sido menos exploradas.

Objetivo: Identificar las estrategias funcionales y las

correlaciones de rasgos entre diferentes dimensiones de las

plántulas (hoja, tallo y raíz). Nosotros esperamos baja coor-

dinación entre los rasgos funcionales sobre y bajo el suelo

debido a que un único trade-off conservación-adquisición

de recursos, no puede capturar la variabilidad de funciones

y presiones ambientales a las que están expuestas las raíces.

Métodos: Medimos 12 rasgos funcionales pertenecientes a

38 plántulas en un bosque seco en Colombia. Exploramos

las relaciones entre pares de rasgos usando correlaciones

de Pearson, y para tener una visión integrada de los rasgos

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funcionales, usamos un análisis de componentes principa-

les (ACP).

Resultados: Reportamos limitada evidencia de acopla-

miento entre los rasgos sobre y bajo el suelo, pero

encontramos correlaciones significativas entre el continuo

de estrategias conservativas y adquisitivas. Los rasgos

de raíz relacionados con la capacidad de absorción de

agua y nutrientes formaron un eje ortogonal al continuo

adquisitivo-conservativo.

Conclusiones: Nuestros resultados mostraron que las

plántulas del bosque seco tienen diferentes estrategias

funcionales para lidiar con el déficit hídrico. La incorpo-

ración de los rasgos de la raíz ayuda a explicar nuevas

estrategias funcionales no reportadas por los rasgos de hoja

y tallo. Este estudio contribuye al entendimiento de los

mecanismos que explican la coexistencia de especies y es

particularmente relevante para predecir las trayectorias de

los bosques futuros.

Palabras clave: estrategia adquisitiva; Colombia; estra-

tegia conservadora; rasgos funcionales; déficit hídrico;

almacenamiento de agua.

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