Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

Litterfall and nutrient transfer dynamics in a successional

gradient of tropical dry forest in Colombia

Angie Montañez-S*1; https://orcid.org/0000-0001-8994-9287

Andrés Avella-M1; https://orcid.org/0000-0002-1595-1154

René López Camacho1; https://orcid.org/0000-0003-2026-0371

1. Universidad Distrital Francisco José de Caldas, Bogotá, Colombia; avmontanezs@correo.udistrital.edu.co

(*Correspondence), aavellam@udistrital.edu.co, rlopezc@udistrital.edu.co

Received 05-X-2022. Corrected 23-V-2023. Accepted 16-VIII-2023.

ABSTRACT

Introduction: The litterfall production, foliar nutrient dynamics and decomposition are essential to maintain

nutrient cycling, soil fertility, and carbon regulation in terrestrial ecosystems. With several studies addressing

the variation of these processes, their dynamics in tropical dry forests (TDFs) remain unclear, due to its complex

interaction of biotic and abiotic factors.

Objective: To evaluate litterfall, nutrient potential return and use efficiency, and decomposition variation in a

TDF successional gradient in Tolima, Colombia.

Methods: We quantified litterfall from November 2017 to October 2019 in 12 plots distributed in four succes-

sional stages: initial, early, intermediate, and late forests. We identified key tree species in foliar litter production

and characterized the foliar decomposition of these species. At the community level, we quantified the C, N and

P potential return, the N and P use efficiency, and the C:N and N:P ratio. Subsequently, we analyze relationships

between vegetation characteristics and some soil chemical properties with these ecological processes.

Results: We found that total litterfall in late forests (8.46 Mg ha-1 y-1) was double that found in initial forests (4.45

Mg ha-1 y-1). Decomposition was higher in initial (k = 1.28) compared to intermediate (k = 0.97) and late forests

(k = 0.87). The nutrient potential return didn’t change along succession, but it did show differences between study

sites. The structural development and species richness favored litterfall, while soil chemical conditions influenced

nutrient returns and decomposition.

Conclusions: TDFs could recover key ecosystem function related to litterfall and nutrient dynamics after distur-

bances cessation; however, the soil quality is fundamental in return and release of nutrients.

Key words: biogeochemical cycles; plant succession; ecological indicators; forests recovery; key species.

RESUMEN

Dinámica de la hojarasca y transferencia de nutrientes en un gradiente sucesional

de bosque seco tropical en Colombia

Introducción: La producción de hojarasca, la dinámica de nutrientes foliares y la descomposición son esenciales

para mantener el ciclo de nutrientes, la fertilidad del suelo y la regulación del carbono en ecosistemas terrestres.

Con diversos estudios que abordan estos procesos, su variación en los bosques secos tropicales (BSTs) permanece

incierta, por su compleja interacción de factores bióticos y abióticos.

Objetivo: Evaluar la caída de hojarasca, el retorno potencial de nutrientes y eficiencia de uso, y la variación en

descomposición en un gradiente sucesional de un BST en Tolima, Colombia.

https://doi.org/10.15517/rev.biol.trop..v71i1.52278

TERRESTRIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

INTRODUCTION

Tropical dry forests (TDFs) are strategic

ecosystems with great biological diversity and

multiple ecosystem services such as soil sta-

bilization, water and climate regulation, car-

bon storage, among others (Gei & Powers,

2014; Murphy & Lugo, 1986). However, due

to the historical loss of more than 60 % of

their original coverage, they are among the

most threatened ecosystems in the Neotropics

(Portillo-Quintero & Sánchez-Azofeifa, 2010).

The main causes of loss and TDFs transforma-

tion have been the livestock expansion, mining,

urban development, and tourism (González-

M et al., 2019; Pizano & García, 2014). This

situation puts at risk the biodiversity, ecologi-

cal processes, and ecosystem services in TDFs

(Fernandez-Mendez et al., 2014; Quesada et

al., 2009). Within the ecological processes that

can be affected by land use change, are litterfall,

nutrient returns, and decomposition (Gei &

Powers, 2014; Meister et al., 2012).

Litterfall, nutrient return and decompo-

sition are fundamental ecological processes

for organic matter return and nutrient real

return to soils (Vitousek, 1984). These eco-

logical processes represent the ability to trans-

form biomass and supply or retain nutrients

depending on the availability of resources

(Aerts & Chapin, 1999; Coleman et al., 2018;

Vitousek & Sanford, 1986). In this way, in the

dry season when resources are scarce, plants in

TDFs could reabsorb nutrients before litterfall,

as an adaptation mechanism that allows them

to be more energy efficient (Gei & Powers,

2014; Vitousek, 1984). Additionally, depend-

ing on the degradation level and the ecosystem

resilience, these ecological processes can vary

widely in different successional stages (Aryal et

al., 2015; Sánchez-Silva et al., 2018; Souza et al.,

2019; Xuluc-Tolosa et al., 2003).

In advanced successional stages that are

distinguished by structural and species com-

position development (Chazdon, 2014), it

has been reported that litterfall and nutri-

ent returns is higher (Barreto da Silva et al.,

2018; Castellanos-Barliza et al., 2019; Huang

et al., 2017; Sánchez-Silva et al., 2018; Souza

et al., 2019). Likewise, the decomposition and

nutrients release could be superior and more

efficient, due to better soil conditions, greater

water efficiency and microbial activity (Schil-

ling et al., 2016). In contrast, other studies

have shown that in early and intermediate

stages, litterfall, nutrient returns and release

may be greater due to fast-growing species with

higher photosynthetic rates and efficient nutri-

ent returns (Castellanos-Barliza, León-Peláez,

Armenta-Martínez, et al., 2018; Sánchez-Silva

Métodos: Cuantificamos la caída de hojarasca entre noviembre 2017 y octubre 2019 en 12 parcelas distribuidas

en cuatro estados sucesionales: bosque inicial, temprano, intermedio y tardío. Identificamos las especies arbó-

reas clave en la producción de hojarasca y caracterizamos la descomposición foliar de estas especies. A nivel

comunitario, cuantificamos el retorno potencial de C, N y P, la eficiencia de uso de N y P y la relación C:N y N:P.

Posteriormente, analizamos las relaciones entre las características de la vegetación y algunas propiedades quími-

cas del suelo con estos procesos ecológicos.

Resultados: Encontramos que la caída total de hojarasca en los bosques tardíos (8.46 Mg ha-1 año-1) fue el doble

de la hallada en bosques iniciales (4.45 Mg ha-1 año-1). La descomposición fue mayor en bosques iniciales (k =

1.28) en comparación con bosques intermedios (k = 0.97) y tardíos (k = 0.87). El retorno potencial de nutrientes

no cambió con el avance de la sucesión vegetal, pero exhibió diferencias entre los sitios de estudio. El desarrollo

estructural y la riqueza de especies favorecieron la caída de hojarasca, mientras que las condiciones químicas del

suelo influyeron en el retorno de nutrientes y descomposición.

Conclusiones: Los BSTs tienen la capacidad de recuperar la función ecosistémica de aporte de hojarasca fina,

retorno y liberación de nutrientes después del cese de alteraciones antrópicas; sin embargo, la calidad del suelo es

fundamental en el retorno y liberación de nutrientes.

Palabras clave: ciclos biogeoquímicos; sucesión vegetal; indicadores ecológicos; recuperación de bosques; espe-

cies clave.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

et al., 2018; Valdespino et al., 2009; Xuluc-

Tolosa et al., 2003). These ecological processes

respond to the interaction of multiple biotic

factors such as structure and species richness,

morphological and physiological traits varia-

tion, and microbial activity (Coleman et al.,

2018; Steidinger et al., 2019); and abiotic factors

such as soil type and microclimatic conditions

(Ostertag et al., 2008; Sánchez-Silva et al., 2018;

Schilling et al., 2016).

In relation to the N and P foliar nutrients

dynamics in TDFs, it has been reported that

the P content decreases, and its use efficiency

increases with the forest age (Read & Lawrence,

2003); while N returns recovered in the first

successional stages (Gei & Powers, 2014). In

dry forests of La Guajira in Colombia affect-

ed by coal mining, Castellanos-Barliza León-

Peláez and Campo (2018) found that after 21

years of active restoration, the flow of N and

P recovered, but the rate of P mineralization

didn’t change. Meanwhile, in dry forests of the

Yucatan Peninsula that historically had corn

crops, Read and Lawrence (2003) found that

N concentration didn’t change along plant suc-

cession, while the P concentration decreased in

mature forests. The P and N flux variation is

mainly attributed to its origin nature (Campo

et al., 2001; Gei & Powers, 2014); and other

factors such as land use history, soil type, cli-

mate, and vegetation (Gei & Powers, 2014);

but the influence of various abiotic and biotic

factors on N and P returns remains uncertain

(Souza et al., 2019).

The main objective of this study was to

evaluate the litterfall, nutrient potential return

and use efficiency, and decomposition variation

in a TDF successional gradient. Specifically,

we ask the following questions: i) How does

the litterfall, nutrient potential return and use

efficiency, and decomposition change in dif-

ferent successional stages in a TDF? ii) How is

the relationship between some soils chemical

properties and vegetation with respect to these

ecological process? To answer these questions,

we quantified litterfall production for two years

(November 2017-October 2019) in four suc-

cessional stages: initial (3-5 years), early (10-15

years), intermediate, (20-30 years) and late (>

40 years); we identified tree species with the

greatest litterfall contribution and quantified

the rate decomposition of these species. At

the community level we measured C, N and

P potential return, N and P use efficiency,

C:N and N:P ratios. Finally, we analyzed the

relationship of some vegetation characteristics

and soil chemical properties with litterfall, the

nutrient potential return and use efficiency,

and decomposition.

Considering that studies of these ecologi-

cal processes in TDFs are contrasting due to

the biotic and abiotic interactions mentioned

above, we expect that: i) Litterfall and decom-

position will increase along plant succession,

due to the structure development, species rich-

ness and better soil conditions, which favor

litterfall contribution and nutrients release. ii)

Second, we expect N return to be higher in

initial and early forests, and P return to increase

along succession; in this way N use efficiency

and C:N will be higher in late forests, and P use

efficiency and N:P will have higher values in the

early stages of succession. iii) Third, we believe

that soil chemical properties will have a stron-

ger effect on nutrient return and use efficiency,

and decomposition; meanwhile the structure

and species richness will strongly influence lit-

terfall contribution.

MATERIALS AND METHODS

Study area: The study was conducted

at three locations in the upper basin of the

Magdalena River, North Tolima department,

Colombia. The Civil Society Nature Reserve

(CSNR) “Tambor” (5°12’25’’ N & 74°44’12’’

W) in Honda municipality; the CSNR “Jabiru”

(5°01’50’’ N & 74°53’04’’ W) in Armero-Guay-

abal municipality and Hacienda San Felipe

(5°07’25’’ N & 74°57’06’’ W) in Falan munici-

pality (Fig. 1). These forests correspond to TDF

remnants in inter Andean valleys Magdalena

River. Historically, this zone has been charac-

terized by the establishment of extensive and

intensive cattle ranching (Fernandez-Mendez

et al., 2014). The geomorphological landscape

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

includes piedmont and low and intermediate

hills geoforms. Typic Ustorthents and Lithic

Ustorthents are dominant soils, which have

developed from sandstone, tuff, and clay

(IGAC, 2004). Soil texture is loam to clay loam,

with 58.1 % ± 12.9 sand, 25.1 % ± 7.55 silt, and

16.8 % ± 6.12 clay in average. Soils are charac-

terized by medium fertility and moderate pH

(García Villalobos, 2020). The climate is hot

dry, with a bimodal precipitation, the annual

average precipitation is 1 876 ± 258 mm with

dry season from January to March and June to

September, while the rainy season is from April

to May and October to November (Fernandez-

Mendez et al., 2014).

A total of 12 permanent monitoring plots

(PMP) were established (three plots in each

successional stage). Since age is not a pre-

cise succession metric (Chazdon, 2014), we

assigned an approximate age from forest/no

forest thematic layers corresponding to 1990,

2000, 2005, 2010 and 2013 years (Salgado-

Negret et al., 2017). Additionally, we consider

local communities’ knowledge regarding age

abandonment, in this way age ranges were

defined for each successional stage: initial (3-5

years); early (10-15 years); intermediate (20-

30); and late (> 40 years). Initial corresponds

to sites that have lost their original coverage,

which historically were agricultural crops and

pastures that were abandoned in the last 5

years. Early characterized by an open canopy,

with arboreal and shrubby elements that origi-

nated from plant succession in the last 10 to 15

years. Intermediate forests were distinguished

by regularly distributed tree elements, forming

a discontinuous canopy with trees that reach

heights of up to 25 m, tree cover between 30-70

% and an age of abandonment greater than 20

years. Finally, late forests constitute little inter-

vening vegetal formations (sporadic presence of

cattle), which are characterized by high natural

regeneration, closed canopy and differentiated

strata with coverage greater than 70 % (Table 1).

Litterfall production: Litterfall was moni-

tored in 96 circular collectors (0.5 m2) along

successional gradient. In each PMP, eight

Fig. 1. Study area in North Tolima. Colombia. Permanent monitoring plots (0.18 ha) per successional stage are represented

by asterisks for initial (3-5), triangles for early (10-15), circles for intermediate (20-30) and squares for late (> 40).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

collectors were installed so that 24 collectors

per successional state were established follow-

ing the Biodiversity and Ecosystem Services

TDFs Evaluation Protocol (Salgado-Negret et

al., 2017). Collectors were permanently exposed

and every month for two years litterfall was

collected (November 2017-October 2019). To

obtain the dry weight, the samples were dried

at 60 °C for 24-72 h depending on moisture

content (in rainy periods were dried for 48-72

h) until a constant weight was obtained. After

drying, the biomass obtained was separated

into leaves (refer to foliar litter in this study),

branches (< 2 cm) and reproductive material

(flowers, fruits). Miscellaneous unidentified

material was not considered because it repre-

sented less than 5 % of total contribution. Sub-

sequently, the dry weight of each component

was obtained in a precision digital scale 0.01 g.

Total litterfall was obtained from the monthly

production sum of all collectors by successional

state, adapting the equation of Honorio and

Baker (2010).

To estimate foliar litter contribution by

species, every three months in the first year

of study (November 2017-October 2018), four

collectors per PMP were randomly selected.

Subsequently, foliar litter was separated accord-

ing to their shape and texture, including the leaf

blade and the petiole. For foliar litter palms,

only the rachis and the pinnae contained in

the collector were considered, excluding the

petiole and the foliar parts outside the collector

(Ribeiro et al., 2020). To estimate contribu-

tion by species, foliar litter was weighed on

a digital scale with a precision of 0.01, and it

Table 1

Structural characteristics vegetation and floristic composition of study sites of four successional stages in a TDF, North

Tolima. Colombia.

Successional

stage

Initial

(3-5)

Early

(10-15)

Intermediate

(20-30)

Late

(> 40)

Individuals/0.18 ha 69 ± 33 187 ± 105 196 ± 67 182 ± 56

Individuals /ha 383 ± 181 1 041 ± 585 1 087 ± 374 1 013 ± 311

Species/0.18 ha 17 ± 7 22 ± 8 25 ± 7 31 ± 7

Species /ha 93 ± 39 120 ± 42 139 ± 39 174 ± 37

Basal area m2 0.18 ha-1 4.6 ± 1.9 21.6 ± 16.9 26.7 ± 15.4 25.8 ± 14.9

Basal area m2 ha-1 25.9 ± 10.7 119.7 ± 93.9 148.1 ± 85.5 143.5 ± 82.6

CWM foliar area (cm2)* 79.5 ± 40.7 64.1 ± 26.7 109.3 ± 68.7 97.8 ± 33.6

Shannon-Wiener

Diversity Index 2.1 ± 0.3 2.2 ± 0.3 2.1 ± 0.5 2.7 ± 0.4

Species with higher IVI

values

Attalea butyracea

(Kunth) (28.7 %),

Guazuma ulmifolia

Lam (24.8 %), Cordia

alliodora (Ruiz &

Pav.) Oken (22.7 %),

Coccoloba coronata

Jacq. (20.4 %), y

Centrolobium paraense

Tul. (17.8 %).

Attalea butyracea

(Kunth) (59.1

%), Calliandra

tergemina (L.)

Benth. (22.3 %),

Cordia alliodora

(Ruiz & Pav.) Oken

(11.1 %) y Eugenia

sp. (8.6 %).

Guadua angustifolia

Kunth (49 %),

Anacardium excelsum

(Kunth) Skeels (24

%), Erythroxylum ulei

O.E.Schulz (21.7 %),

Oxandra espintana

(Benth.) Baill. (19.7 %),

Attalea butyracea (L.f.)

Wess.Boer (19.2 %) y

Machaerium tolimense

Rudd (10.5 %).

Oxandra espintana

(Benth.) Baill. (27.6

%), Anacardium

excelsum (Kunth)

Skeels (20.1 %),

Trichilia oligofoliolata

M.E. Morales (|9.2

%), Sorocea cf. sprucei

(18.7 %) y Astronium

graveolens Jacq. (15.3

%).

All individuals with DBH ≥ 2.5 cm were included. The values correspond to the mean ± 1 SD of the three study sites. Adapted

from Polania, (2019). *Data provided by the IAvH (González-M et al., 2019). CWM: community-weighted mean.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

was summed by successional stage and by site

to selected species that contributed the most

foliar litter.

Leaf nutrient potential return and nutri-

ent use efficiency: To evaluate nutrient poten-

tial return, four of the eight collectors per

PMP were selected, who gathered the quarterly

contribution of foliar litter during the first year

of study. In total, 192 samples were evaluated

(12 plots × 4 collectors × 4 periods in the year).

The foliar litter samples were sent to National

Laboratory in Bogotá, for carbon (C), nitrogen

(N) and phosphorus (P) content quantification.

Nutrient potential return was estimated as aver-

age annual fluxes (kg ha-1 y-1) multiplying foliar

litter production by nutrients concentration in

each plot and successional stage (Read & Law-

rence, 2003). Additionally, we quantified C:N,

N:P ratios and the nitrogen use efficiency index

(NUE) and phosphorus use efficiency index

(PUE) considering the nutrient efficiency used

per unit of dry mass produced in foliar litter,

that is equivalent to inverse of foliar litter nutri-

ent concentration (1/[nutrient concentration])

(Vitousek, 1984).

Leaf litter decomposition: To estimate

decomposition rates by species and community

level, litter bags were built considering the spe-

cies that contributed the most foliar litter (iden-

tified in the previous phase). These species

exhibited high IVI values (Table 1) and higher

foliar litter contributions, so ecologically they

also represented the community level (weighted

average of k value). According to Graca et al.

(2005); Salgado-Negret et al. (2017), 5 g foliar

litter were deposited in 20×20 cm nylon-type

bags, with a 5 mm diameter mesh eye. 18 litter

bags by individual/species were constructed

(522 in total; 22 species and 29 individuals, due

to some species were repeated by successional

stage). The distribution of litter bags per plot

varied between 36 (2 species) to 72 (4 species)

according to species selection with the highest

foliar litter contribution. The litter bags were

installed at the end of May 2019 and were

collected at 30, 63, 92, 120, 153 and 189 days.

The 18 litter bags per species were installed

with a rope that held all the bags to facilitate

their collection and avoid their loss; therefore,

a separation between the bags was not guar-

anteed so that they were exposed to the same

microclimatic conditions (Salgado-Negret et

al., 2017). In the laboratory, the litter bags

were carefully cleaned to remove soil particles,

emerging fine roots, and other adhering mate-

rials. Subsequently, they were dried at 60 °C for

48 to 72 h until reaching a constant weight to

estimate the dry weight on a digital scale with

0.01 g precision.

Data processing: To compare litterfall,

nutrient potential return - use efficiency, and

decomposition across successional stages, we

performed one-way Anovas, Welch’s robust

Anovas, and nonparametric Kruskal-Wal-

lis tests depending on data behavior. Subse-

quently, to confirm significant differences, we

performed Games-Howell post hoc tests or

Wilcoxon pairwise multiple comparison with

Bonferroni adjustment. Additionally, we per-

formed Principal Component Analysis (PCA)

to summarize vegetation characteristics, soil

chemical properties, and nutrient potential

return and use efficiency for the 12 PMP stud-

ied. Thus, we made three PCAs: (i) vegetation

characteristics: basal area, leaf area, height and

species richness; (ii) soil chemical properties:

pH, organic carbon (OC), N, P and cation

exchange capacity (CEC) and (iii) potential

nutrient return and use efficiency: C, N and P

returns, N:P, C:N, NUE and PUE. The scores

of the first dimensions (Dim1) of each PCA

were selected as a representation of vegetation

characteristics, soil chemical properties and

nutrients, because they summarized the data

and explained most data variance. Finally, to

analyze the relationship between the vegetation

characteristics and soil chemical properties

with litterfall, nutrient potential return and

use efficiency, and decomposition, we made

three mixed models with the lmer function of

the lme4 package. In these models the plot was

used as a random factor, and we included three

fixed effects: (i). The Dim1 of soil chemical

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

properties PCA; (ii). The Dim1 of vegetation

characteristics PCA; and (iii) the interaction

of both dimensions (soils×vegetation) (Bates et

al., 2015). All analyzes were performed in the

R software version 3.6.3 (R Core Team, 2020).

RESULTS

Litterfall production: Total annual lit-

terfall in a TDF range from 4.45 to 8.46 Mg

ha-1 y-1 and varied significantly among suc-

cessional stages. Total litterfall was highest in

late and intermediate (Welch, F3,50 = 13.0, P <

0.001) (Fig. 2). This trend was maintained for

foliar litter (Welch, F3,50 = 15.8, P < 0.001) and

branch fraction (Kruskal-Wallis, H3 = 25.36, P

< 0.05), meanwhile the reproductive structures

were lower in initial forests and didn’t change

between early, intermediate, and late forests

(Kruskal-Wallis, H3 = 17.04, P < 0.05).

Centrolobium paraense, Albizia guachapele

and Guazuma ulmifolia were the ones species

that contributed the most to leaf litter in ini-

tial (41.03 %). Calliandra tergemina, Spondias

mombin and Attalea butyracea represented the

greatest contribution in early (29.85 %). For its

part, Guadua angustifolia, Trichilia oligofoliola-

ta and Anacardium excelsum represented 49.16

% of the leaf litter in intermediate, while A.

excelsum, T. oligofoliolata and Oxandra espinti-

ana constituted 33.45 % in late forests (Table 2).

Leaf nutrient potential return and nutri-

ent use efficiency: The C, N and P poten-

tial return, N and P use efficiency, and C:N

didn’t change throughout succession (P > 0.05).

N:P was the only variable that exhibited dif-

ferences between initial and intermediate/late

forests (Kruskal-Wallis, H3 = 8.34, P < 0.05)

(Table 3). Even so, nutrient potential return and

Fig. 2. Total litterfall, foliar, branches and reproductive structures (flowers and fruits) in four successional stages in a TDF,

North Tolima. Error bars indicate ± 1 standard error. The values followed by the same letters are not significantly different

according to Welch and Kruskal-Wallis test.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

Table 2

Annual leaf litter (Mg ha-1 y-1 ± 1 standard deviation) of species with greatest contribution in four successional stages in a

TDF, North Tolima

Successional Stage Species Leaf litter %

Initial (3-5) Centrolobium paraense Tul. 0.53 ± 0.01 15.23

Albizia guachapele (Kunth) Dugand 0.50 ± 0.01 14.37

Guazuma ulmifolia Lam. 0.40 ± 0.01 11.49

Rondeletia pubescens Kunth 0.19 ± 0.01 5.46

Cupania latifolia Kunth 0.19 ± 0.002 5.46

Early (10-15) Calliandra tergemina (L.) Benth. 0.53 ± 0.02 12.59

Spondias mombin L. 0.38 ± 0.01 9,00

Attalea butyracea (L.f.) Wess.Boer 0.35 ± 0.01 8.27

Leguminosae 1 0.32 ± 0.01 7.76

Astronium graveolens Jacq. 0.23 ± 0.01 5.58

Guazuma ulmifolia Lam. 0.14 ± 0.004 3.36

Leguminosae 2 0.14 ± 0.01 3.35

Eugenia sp. 0.10 ± 0.003 2.49

Intermediate (20-30) Guadua angustifolia Kunth 1.68 ± 0.02 25.73

Trichilia oligofoliolata M.E. Morales 0.85 ± 0.03 13.02

Anacardium excelsum (Kunth) Skeels 0.68 ± 0.03 10.41

Machaerium tolimense Rudd 0.37 ± 0.03 5.67

Spondias mombin L. 0.30 ± 0.03 4.59

Bauhinia sp. 0.27 ± 0.03 4.13

Oxandra espintana (Benth.) Baill. 0.24 ± 0.03 3.68

Machaerium microphyllum (E.Mey.) Standl. 0.20 ± 0.03 3.06

Late (> 40) Anacardium excelsum (Kunth) Skeels 1.14 ± 0.01 17.43

Trichilia oligofoliolata M.E. Morales 0.65 ± 0.02 9.94

Oxandra espintana (Benth.) Baill. 0.39 ± 0.02 5.96

Ocotea longifolia Kunth 0.36 ± 0.02 5.5

Rutaceae 0.36 ± 0.02 5.5

Attalea butyracea (L.f.) Wess.Boer 0.30 ± 0.02 4.59

Ampelocera albertiae Todzia 0.26 ± 0.02 3.98

Machaerium tolimense Rudd 0.20 ± 0.01 3.06

Table 3

Carbon (C), nitrogen (N) and phosphorus (P) potential return (kg ha-1 y-1), nitrogen use efficiency (NUE) and phosphorus

use efficiency (PUE), C:N and N:P (mean ± 1 standard deviation) in four successional stages in a TDF, North Tolima

Succesional stage Initial (3-5) Early (10-15) Intermediate (20-30) Late (> 40)

C (kg ha-1 y-1)1 961.53 ± 830.92 1 841.53 ± 159.74 2 773.1 ± 317.53 2 758.37 ± 27.23

N (kg ha-1 y-1)85.77 ± 43.47 63.53 ± 11.46 94.83 ± 12.18 90.03 ± 12.56

P (kg ha-1 y-1)5.33 ± 3.61 4.73 ± 1.93 8.07 ± 1.13 6.13 ± 1.28

NUE 70.17 ± 16.11 70.13 ± 6.68 72.53 ± 11.24 78.27 ± 14.65

PUE 1 624.9 ± 556.07 1 576.23 ± 815.64 958.23 ± 279.99 1 166.43 ± 232.57

C:N 32.93 ± 7.86 30.97 ± 2.51 30.67 ± 3.52 33.3 ± 4.6

N:P 23.1 ± 4.8a22.17 ± 9.72 13.03 ± 2.18b14.4 ± 2.14b

Letters indicate significant differences between successional stages (P < 0.05).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

use efficiency presented an important variation

along succession conditioned by the site. C,

N and P return tended to be greater in inter-

mediate and late stages. This can be explained

because although Jabirú exhibited high nutrient

return in all successional stages, Tambor and

San Felipe presented lower values in initial and

early stages to induce a lower average value in

the first stages. For its part, PUE reached mean

higher values in initial and early successional

stages; meanwhile, NUE and C:N didn´t pres-

ent clear differences in succession (Table 3).

In this sense, nutrient potential return and

use efficiency exhibited a clear change between

study sites. Nutrients PCA confirmed it because

this allowed a clear site separation. Jabirú were

related to high nutrient potential return; while

San Felipe exhibited high N:P and PUE; and

Tambor associated with C:N and NUE. DIM1

explained 68.2 % variance, allowing to describe

the nutrient potential return and use efficiency.

Leaf litter decomposition: Decomposi-

tion rates are higher in initial and early com-

pared to intermediate and late forests (F2,9 =

1.62, P = 0.05). The residual dry mass-RDM

varied from 85.7 % (month 1) to 54.2 % (month

6) in initial forests; 88.2 to 45.4 % in early

forests; 90.9 to 61.7 % in intermediate forests;

and 92.1 to 63.4 % in late forests. At the species

level, R. pubescens and G. ulmifolia presented

the highest decomposition rates and the short-

est RDM in initial; Leguminosae 1 and A. gra-

veolens in early; S. mombin and O. espintiana in

intermediate; and Rutaceae and O. espintiana in

late (Table 4, Fig. 3). The R2 values ranged from

Fig. 3. Residual dry mass of foliar litter for the species with the highest litterfall contribution in four successional stages in a

TDF, North Tolima.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

0.83 to 1, indicating that the model appropri-

ately described the decomposition rates for all

species in all successional stages.

Relationship with vegetation character-

istics and soil chemical properties: Litterfall

exhibited a positive relationship with vegetation

characteristics (x2 = 28.96; P < 0.05) (Fig. 4A),

but no clear relationship was found with soil

chemical properties (x2 = 0.89; P > 0.05) (Fig.

4B). The interaction between soil chemical

properties and vegetation characteristics had

a slight relationship with litterfall (x2 = 3.14;

P = 0.076). In general, intermediate, and late

forests exhibited higher contributions of litter-

fall, better structural development of vegetation

and higher species richness, but not necessarily

better soil conditions.

In contrast, nutrient potential return and

use efficiency were not related to vegetation

characteristics (x2 = 2.82; P > 0.05) (Fig. 4C);

but showed a positive relationship with soil

chemical properties (x2 = 4.28; P = 0.04) (Fig.

4D). High C:N and N, P use efficiency were

related to low nutrients, OC % and CEC in

soils; while nutrient potential return (N, P)

Table 4

Decomposition factor k, decomposition time of 50 % and 99 % of foliar litter for species in in four successional stages in a

TDF, North Tolima

Successional Stage Species k t 0.5 (years) t 0.99 (years) R2adj

Initial (3-5) R. pubescens 1.51 0.58 3.84 0.9

G. ulmifolia 1.33 0.52 3.46 0.98

C. paraense 1.10 0.46 3.05 0.93

A. guachapele 1.02 0.68 4.51 0.96

C. latifolia 0.58 1.20 7.94 0.91

Early (10-15) Leguminosae 1 2.5 0.28 1.84 0.97

A. graveolens 1.97 0.35 2.34 0.92

S. mombin 1.79 0.39 2.57 0.97

C. tergemina 1.35 0.51 3.41 0.99

G. ulmifolia 1.31 0.53 3.52 0.99

Leguminosae 2 1.17 0.59 3.94 0.93

A. butyracea 0.98 0.71 4.70 0.83

Eugenia 0.69 1.00 6.67 0.93

Intermediate (20-30) S. mombin 1.66 0.65 4.34 0.99

O. espintiana 1.39 0.50 3.31 0.95

Bauhinia sp 1.01 0.69 4.56 0.94

G. angustifolia 0.87 0.80 5.29 0.87

M. microphyllum 0.75 0.92 6.14 0.95

M. tolimense 0.67 1.03 6.87 0.98

T. oligofoliolata 0.59 1.17 7.81 0.97

A. excelsum 0.51 1.17 7.81 1

Late (> 40) Rutaceae 1.55 0.45 2.97 0.96

O. espintiana 1.17 0.59 3.94 0.97

A. albertiae 1.05 0.66 4.39 0.98

O. longifolia 0.75 0.92 6.14 0.94

A. butyracea 0.68 1.02 6.77 0.92

M. tolimense 0.63 1.10 7.31 0.97

T. oligofoliolata 0.58 1.20 7.94 0.97

A. excelsum 0.45 1.54 10.23 0.93

The adjusted R2 indicates the coupling of the exponential model used for each species (P < 0.05).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

were related to high chemical soil properties

values. Jabirú presented the highest nutrient

potential return and better soil chemical condi-

tions, while San Felipe and Tambor exhibited

the highest use efficiency.

Finally, the decomposition rate presented a

relationship with the soil-vegetation interaction

(x2 = 4.27; P = 0.04). However, when evaluat-

ing only the structure and species richness,

there wasn’t relationship with decomposition

(x2 = 3.21; P > 0.05) (Fig. 4E); Likewise, the soil

chemical properties were not related to decom-

position (x2 = 0.14; P > 0.05) (Fig. 4F).

DISCUSSION

The plant succession favored the recovery

of litterfall and decomposition; while the site

conditions associated with soil chemical prop-

erties were determinant in nutrient dynamics.

Fig. 4. A. Annual litterfall (Mg ha-1 y-1) in relation to vegetation characteristics (vegetation PCA Dim1 score) and B. soil

chemical properties (soil PCA Dim1 score) (N = 96, litter collectors). C. Nutrient potential return and use efficiency in

relation to vegetation characteristics and D. soil chemical properties (N = 48, collectors for nutrient and soil analysis). E.

Decomposition rate (k) in relation to vegetation characteristics and F. soil chemical properties (N = 29, species).

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

Soil chemical properties, vegetation structure

and species richness of intermediate and late

forests favored a greater litterfall contribution.

Regardless of the successional stage, better soil

conditions favored foliar nutrient returns and

their release through decomposition. These

results suggest that tropical dry forests in dif-

ferent successional stages have the capacity

to recover key ecological processes related to

nutrient cycling and NPP, although the soil

quality conditioned by land use history has a

great influence on nutrients dynamics.

Litterfall recorded in this study (4.45-8.46

Mg ha-1 y-1) was within the range reported in

similar forest ecosystems (Aryal et al., 2015;

González-Rodríguez et al., 2011). In this regard,

litterfall was low in initial and early stages and

increased in intermediate and late forests, due

to the recovery of the structure and species

richness. In general, these results support our

first hypothesis and coincided with several

studies in TDFs in Mexico (Morffi-Mestre et

al., 2020; Sánchez-Silva et al., 2018), Costa Rica

(Schilling et al., 2016) and Brazil (Souza et al.,

2019), who’s attributed litterfall increase to the

biomass superiority and canopy development.

The high litterfall contribution in interme-

diate and late forests can also be explained by

the species composition and their morphologi-

cal and physiological traits (Becknell & Powers,

2014; Lopezaraiza-Mikel et al., 2014; Villalobos

et al., 2014). In this study we found a positive

effect of species richness and leaf area on lit-

terfall, which could be attributed to litterfall

would be mediated by significant contribution

of dominant individual trees (abundance and

basal area) with large leaves in more diverse

sites (Clark et al., 2001; Huang et al., 2017). In

this way, the role of the dominant species was

fundamental in litterfall contribution, particu-

larly in foliar litter, supported by the biomass

ratio hypothesis (Grime, 1998), which suggests

that ecosystem processes are determined by

dominant species (Conti & Díaz, 2013; Finegan

et al., 2015).

Nutrients from litterfall are key to main-

taining soil stability and supplying resources

to microorganisms and plants (Gei & Powers,

2014; Hulshof et al., 2014; Schilling et al., 2016).

In this study, the average C foliar return in late

forests was like that reported in primary dry

forests of Calakmul, Mexico (Aryal et al., 2015).

The average N and P foliar return was higher

than that recorded in various TDFs of Meso-

america such as the Calakmul primary forests

(Aryal et al., 2015), Chamela, Mexico (Campo

et al., 2001) and secondary forests (7 years

old) in Santa Martha, Colombia (Castellanos-

Barliza, León-Peláez, Armenta-Martínez et al.,

2018). These differences can be attributed to

multiple factors at the regional scale like the cli-

mate variation, land use history and age forest,

topographic and soil conditions (Campo, 2016;

Gei & Powers, 2014; Waring et al., 2021); and

local variations in species composition and soil

microorganisms (Coleman et al., 2018; Schil-

ling et al., 2016).

Nutrient fluxes can vary widely due to cli-

matic seasonality, forest age, soil condition, and

species composition (Campo, 2016; Campo &

Merino, 2019; Gei & Powers, 2014; Saynes et

al., 2005). Similarly, to results of (Castellanos-

Barliza León-Peláez, Armenta-Martínez et al.,

2018; Valdespino et al., 2009) in Colombian

and Mexican TDFs respectively, we found that

nutrient potential return was mainly condi-

tioned by nutrients availability in soils, which

supports our third hypothesis and allowed a

differentiation between study sites. Meanwhile,

contrary to what we expected the variation of

nutrient potential return and use efficiency

didn’t change along plant succession. The N:P

was the only variable that changed in plant

succession, being higher in initial compared

to intermediate and late forests; however, this

result was conditioned by the site effect in the

early forests. In this respect, plants in TDFs

can supply their P requirement by the accu-

mulation of soil P bicarbonate and dissolved

P pools during the dry season (Valdespino et

al., 2009), and the presence of ectomycorrhizal

fungi (Meeds et al., 2021).

After litterfall, decomposition process

begins, which allows the gradual nutrients

release to the soil (Cornwell et al., 2008). We

found that rate decomposition was higher in

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

initial and early forests, and better soil chemi-

cal conditions, structure vegetation and spe-

cies richness favored decomposition. These

results partially support our hypothesis, since

the soil-vegetation interaction favored nutri-

ents release, but contrary to what we expected

(first hypothesis), decomposition was higher in

initial forests. This can be explained by species

composition with rapid nutrient return (e.g.,

G. ulmifolia, R. pubescens and S. mombin). This

coincides with what was reported in South-

west Mexico TDFs (Sánchez-Silva et al., 2018)

and the Yucatán Peninsula (Xuluc-Tolosa et

al., 2003), who found that early-stage species

exhibit high rates of decomposition due to high

N foliar concentration.

Decomposition rates can vary along plant

succession due to the interaction between

fauna, substrate, quality foliar litter and micro-

climatic conditions (Cornwell et al., 2008;

Schilling et al., 2016). Thus, higher decomposi-

tion rates in the initial and early forests can also

be explained by the microclimatic conditions

of sunlight and rain direct entry, which could

favor nutrients release of species adapted to

water deficit (Sánchez-Silva et al., 2018; Xuluc-

Tolosa et al., 2003). However, in this study we

don’t directly analyze microclimatic conditions,

but we found an effect of successional state.

In this way, we suggest that soil condition and

species composition of each successional stage

were determining factors in the differences

found in decomposition rates (Coleman et al.,

2018; Schilling et al., 2016).

The results of this study show that changes

in the litterfall contribution, nutrient potential

return and use efficiency, and decomposition

can be indicators of biogeochemical cycles

recovery in TDFs (Castellanos-Barliza, León-

Peláez, & Campo et al., 2018; Celentano et al.,

2011; Gei & Powers, 2014). These ecological

processes could be used in ecological resto-

ration monitoring programs, with emphasis

on the ecosystem functions recovery and soil

restoration (Celentano et al., 2011; Restrepo et

al., 2013). Another relevant aspect in ecological

restoration is the species selection according to

land degradation, landscape context, economic

and social factors (Lamb & Gilmour, 2003).

In this way, these ecological processes provide

valuable information for species selection that

facilitate biogeochemical cycles reestablishment

(Celentano et al., 2011).

Applied to ecological restoration, fast-

growing species with a high nutrient return

and high decomposition rates (e.g., G. ulmi-

folia, R. pubescens and C. paraense) could be

incorporated in degraded sites, which help to

recover the soil structure (Castellanos-Barliza

et al., 2019) In early stages, species such as A.

graveolens and S. mombin can favor the con-

tinuous supply of litterfall and rapid nutrient

release (associated with high decomposition),

promoting better microclimatic conditions for

the gradual species of advanced stages of suc-

cession establishment. On the other hand, in

intermediate and late forests, T. oligofoliolata

and A. excelsum are key species in net primary

productivity and carbon storage, due to their

high production and accumulation of litterfall.

Ethical statement: the 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 acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENTS

To the research project “Biodiversity and

ecosystem services evaluation in a Colom-

bian tropical dry forest” financed by Alexander

von Humboldt Biological Resources Research

Institute. To the research project 3-10-621-20

support by Research Center at the Universidad

Distrital (CIDC). The authors would like to

thank Gonzalo de las Salas and Angela Parrado

at the Universidad Distrital Francisco José Cal-

das for their help with revised former versions

of this manuscript. Many thanks to the entire

staff of the RNSC Jabiru, RNSC Tambor and

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52278, enero-diciembre 2023 (Publicado Ago. 24, 2023)

Hacienda San Felipe for their gracious support.

Walter García helped in data analysis.

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