482 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

Effects of nutrient (N, P, K) fertilization on the dynamics

of fine roots in tropical rain forests with different soil texture

in the Colombian Pacific region

Harley Quinto Mosquera1*; https://orcid.org/0000-0001-5989-4334

Flavio H. Moreno Hurtado2; https://orcid.org/0000-0002-4634-5042

1. Programa de Biología, Facultad de Ciencias Naturales, Universidad Tecnológica del Chocó Diego Luis Córdoba,

Quibdó, Colombia; d-harley.quinto@utch.edu.co (*Correspondencia)

2. Departamento de Ciencias Forestales, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Sede

Medellín, Medellín, Colombia.; fhmoreno@unal.edu.co

Received 08-VII-2021. Corrected 25-IV-2022. Accepted 01-VII-2022.

ABSTRACT

Introduction: Fine root dynamics include production, turnover and decomposition; they are crucial to forest

health, affect the entire biogeochemical complex of the ecosystem, and consequently, they substantially affect

carbon balance. However, the influence of environmental factors and soil nutrient limitation on fine roots pres-

ents considerable uncertainties and has not been studied in tropical forests with more than 7 000 mm annual

rainfall.

Objective: To measure the effect of fertilization on fine roots in the high precipitation Chocó forest.

Methods: We worked in two sites of the Chocó region, Colombia (August 2014-May 2015), where rainfall

exceeds 10 000 mm per year. We applied five fertilization treatments (N, P, K, NPK and Control) to two soil

type plots. Soil cylinders were removed at pre-established intervals to measure roots.

Results: Phosphorus applications increased fined roots; and more fine roots were produced in sandy than in

loam soil. The effects of fertilization were related, but not clearly determined by edaphic conditions.

Conclusions: In this Chocó forest, the production of fine roots was higher in sandy and nutrient-rich soils but

belowground net primary productivity was limited by the content of edaphic Phosphorus.

Key words: nutrient limitation; fine root production; fine root decomposition; fine root residence time; tropical

soils.

https://doi.org/10.15517/rev.biol.trop.2022.47351

TERRESTRIAL ECOLOGY

Fine roots are a fundamental component of

forest ecosystems because they are necessary

for the acquisition of water and nutrients from

soil (Jackson et al., 1997). Fine root dynamics

include processes such as the production, turn-

over, and decomposition of fine roots (Green

et al., 2005; Jiménez et al., 2009; Violita et al.,

2016; Wang et al., 2019a). They are crucial to

forest health, affect the entire biogeochemical

complex of the ecosystem, and consequently,

they substantially affect the carbon balance of

forests (Jiménez et al., 2009). Particularly, fine

root production represents between 30 and 40

% of net primary productivity (NPP) in tropi-

cal forests (Aragão et al., 2009; Jackson et al.,

1997; Saugier et al., 2001). For this reason,

fine root production plays an important role in

global carbon dynamics, in the biogeochemical

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cycle of nutrients, and in mitigating climate

change (Jackson et al., 1997; Vitousek &

Sanford, 1986); it is strongly influenced by

the conditions of the site, both biological (i.e.

biome and species), atmospheric (temperature,

humidity, and rainfall), and edaphic (soil pH,

texture, and nutrient content) (Finér et al.,

2011; Metcalfe et al., 2008; Silver et al., 2005).

On the other hand, fine root decomposition

is a key process for regulating carbon and nutri-

ent cycling in soils; it is controlled by multiple

factors, including climate, temperature, water

availability, moisture, and soil properties, such

as nutrients, biota (diversity and microbial

activity), and oxygen (Chapin III et al., 2002;

Zhang & Wang, 2015). If there were no decom-

position, ecosystems would quickly accumulate

large quantities of detritus, leading to seques-

tration of nutrients in forms unavailable to

plants (Chapin III et al., 2002); therefore, fine

root turnover is a critical component of ecosys-

tem nutrient dynamics and carbon sequestra-

tion (Gill & Jackson, 2000; Matamala et al.,

2003). Different studies have demonstrated that

fine root residence time is controlled mainly by

soil temperature, moisture status, and nutrient

availability (Cordeiro et al., 2020; Hendrick &

Pregitzer, 1997; Nadelhoffer, 2000). Despite

the importance of fine root dynamics in tropical

ecosystems, most of the studies have been done

in the temperate regions; therefore, the influ-

ence of environmental factors, and specifically

the soil nutrients, on the functioning of fine

roots in tropical forests is debated and presents

considerable uncertainties. This study aims to

help filling that knowledge gap.

The availability and release rate of nutri-

ents from the soil limit fine root dynamics of

tropical forests (Kochsiek et al., 2013; Yuan

& Chen 2012); therefore, evaluating its nutri-

ent limitation is essential to understand the

role of these forests as carbon sinks; it is also

important to predict how they will respond

to various anticipated environmental changes,

including increasing N deposition, atmospheric

CO2, drought, and warming (Alvarez-Clare &

Mack, 2015; Thornton et al., 2007). It has been

hypothesized that lowland tropical rainforests

are limited mainly by the low availability of

soil P, due to the high rates of parent mate-

rial weathering that facilitate mineral losses

by leaching, and by its fixation, e.g. in oxides

of Fe and Al (Miller et al., 2001; Vitousek,

1984). In contrast, soil N, when biologically

fixed, is usually less limiting than P in old soils

(Vitousek, 1984; Walker & Syers 1976).

To determine how soil nutrients limit fine

root dynamics in tropical forest ecosystems,

various methodological approaches have been

used. Fertilization with minerals (N, P, K) has

been considered as one of the most effective

and reliable ways to determine nutritional limi-

tation in tropical forests (Sullivan et al., 2014).

Even though, plants develop more fine roots

to increase nutrient uptake when nutrients are

scarce, the response to the addition of nutrients

needed by plants is the increase of fine root

growth (Yuan & Chen, 2012); in areas enriched

with nutrients whose availability is adequate

or excessive, the growth response should be

null or even negative (Sullivan et al., 2014).

Consequently, higher fine root dynamics are

expected when limiting nutrients are added in

infertile soils.

However, research evaluating the effects

of soil fertilization on fine root production in

tropical forests shows contrasting patterns. For

example, Cuevas and Medina (1988) observed

increases in fine root production with the

addition of NH4Cl in Amazonian forests of

Tall Caatinga and Low Bana (spodosols poor

in N), and with KH2PO4 in forests of Tierra

Firme (oxisols) and Low Bana. Yuan and Chen

(2012), showed in a meta-analysis that fine root

production increased with the application of N

and P in low altitude tropical forests, whereas

in acrisols (ultisols and oxisols) the fine root

production responded negatively to the appli-

cation of N and positively to the addition of P.

Alvarez-Clare et al. (2013) did not find effects

of the addition of N and P on fine root produc-

tion in clayey tropical soils, poor in P and rich

in N. The application of N and P had little

effect on the dynamics of fine roots in young,

N-limited soils, while conversely, the applica-

tion of N and P in old, P-poor soils increased

484 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

the decomposition and turnover of fine roots

(Ostertag, 2001). Guo et al. (2020) found that

N addition largely increased shoot growth

but had a limited effect in root growth in two

tree species in China and root mass fraction

decreased significantly with high N fertiliza-

tion. Wurzburger and Wright (2015) reported

that the addition of N, P, and K together

reduced fine-root biomass in a lowland forest

in Panama. Yavitt et al. (2011) reported that

fine root production and turnover responded to

the addition of K rather than P, and that after

2 years, the K added increased the turnover

of fine roots in moderately fertile soils. The

addition of N, P, and K together reduced fine-

root biomass in a lowland forest in Panama

(Wurzburger & Wright, 2015). These results

show that the response of fine root dynamics

to fertilization is variable and seems to be sig-

nificantly determined by other edaphic factors,

including topography, soil type, texture, and

nutrient content.

Evaluations of fertilization effects on fine

root dynamics in the tropics have been car-

ried out in forests with average annual rainfall

less than 7 000 mm (Alvarez-Clare et al.,

2013; Cuevas & Medina, 1988; Yuan & Chen,

2012). As a consequence of global climate

change significant increases of rainfall are

expected in different tropical regions (Inter-

governmental Panel on Climate Change, 2014),

which could affect the availability of nutrients

and the function of these ecosystems as CO2

sinks. Consequently, it is crucial to understand

how fine root dynamics are affected by nutri-

ent limitation in highly rainy tropical forests,

which has not been studied before. Likewise,

it is also important answering to which extent

edaphic conditions, such as texture and nutri-

ent availability, affect the response of fine root

dynamics to fertilization.

The objective of this study is to evalu-

ate the effects of soil fertilization on fine root

dynamics in tropical rain forests with topog-

raphies and soils of different textures (sandy

and loam) in the Chocó biogeographic region,

where rainfall exceeds 10 000 mm per year

(Poveda et al., 2004). We expect that responses

of fine root dynamics to fertilization (N, P, K)

vary with edaphic conditions, such as texture

and nutrient content in these forests. In par-

ticular, the application of N, P, K and NPK

is expected to increase fine root dynamics

(production and turnover), especially in soils

with sandy textures because their lower capac-

ity of nutrient retention in the soil matrix by

their coarse particles makes them more prone

to nutrient limitation; contrarily, in loam soils

the response to nutrient application is expected

to be lower. We also expect that the responses

to each nutrient (N, P, K, NPK) applied is dif-

ferent, with a greater influence of P applica-

tion on fine root dynamics because of the low

P contents of soil in these forests (Quinto &

Moreno, 2016).

MATERIALS AND METHODS

Study area: the present study was con-

ducted in tropical rain forests of the towns of

Pacurita (municipality of Quibdó) and Opo-

godó (municipality of Condoto), department

of Chocó, Colombia. These two forest sites

are part of the Chocó region located in the

Central North ecogeographic subregion, which

includes the upper basins of the Atrato and San

Juan rivers (Poveda et al., 2004); the mean

temperature is 26 °C and annual precipitation

is 8 000 mm. The localities are within the

geomorphological unit of Sedimentary Hills of

the Tertiary, which are formed by sedimentary

rocks of low altitude, composed of sandy clay-

stones, sandstones and limestones. The soils

of both sites are ultisols, extremely acidic (pH

between 3.7 and 5.5), with very low values of

P (0.5-3.5 ppm), Mg (0.06-1.85 cmol kg-1), Ca

(0.06-0.96 cmol kg-1) and ECEC (0.56-2.64

cmol kg-1), and intermediate values of K (0.03-

0.48 cmol kg-1). Particularly in Opogodó, soils

are less steep, with higher contents of sand

(62-96 %), organic matter, and total N; while in

Pacurita they have greater Al saturation and are

loam, with lower contents of sand and higher

of clay (Table 1).

In both locations the sampling was car-

ried out in well-conserved primary forests; in

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Opogodó, three permanent plots of one hectare

were established inside the facility of the Uni-

versidad Tecnológica del Chocó “Diego Luis

Córdoba” in 2 013. In Pacurita, two permanent

plots were established in the forest reserve area

called Estación Biológica Pacurita.

Methods: o evaluate the effect of fertiliza-

tion on the dynamics of fine roots, a random-

ized complete block design was established

(Shieh & Jan, 2004) with five fertilization

treatments (N, P, K, NPK and Control) and five

repetitions (blocks), three of them in Opogodó

and two in Pacurita. The blocks consisted of

permanent plots of 1 ha. For the application

of the fertilization treatments, each plot was

divided into five experimental units of 20 x 100

m (0.2 ha), where the fertilization treatments

were applied randomly. Likewise, to evaluate

the variability within each experimental unit,

they were divided into 20 x 20 m record-

ing units, where the dynamics of fine roots

were monitored.

The fertilizers were applied to each experi-

mental unit by broadcast; two-meter perimetric

strips were left unfertilized inside each experi-

mental unit to reduce the risk of nutrient

contamination from adjacent plots due to the

effects of runoff and leaching. In order to

reduce the influence of topography on the con-

tamination and losses of nutrients of neighbor-

ing units, the longest side of the experimental

units in Pacurita was arranged parallel to the

slope of the terrain.

The doses and timing of fertilizer applica-

tion were similar to those reported in experi-

ments carried out in other low altitude tropical

forests (Mirmanto et al., 1999; Wright et al.,

2011). Thus, along one year, four equal doses

were applied starting in August 2014 and fin-

ishing in May 2015 (in the months of August,

November, February and May) in the following

amounts and formulations: for the N treatment,

125 kg N ha-1 year-1 were applied in the form

of urea ((NH2)2CO), distributed in four doses,

each one of 2.72 kg of Urea per recording unit;

for the P treatment, 50 kg P ha-1 year-1 were

added in the form of phosphoric rock (H3PO4)

distributed in four doses of 1 kg of H3PO4 per

recording unit; for the K treatment, 50 kg K

TABLE 1

Parameters of edaphic fertility in the studied forests. Data are means ± standard deviation

Parameters Opogodó Range Pacurita Range Mann-Whitney test

pH 4.97 4.22-5.51 4.03 3.68-4.37 -1 869.0*

Aluminum (Al cmol kg-1)0.12 ± 0.05 0.1-0.3 0.94 ± 0.21 0.2-1.4 1 790.0*

Al saturation (%) 12.65 ± 5.25 3.78-31.57 57.21 ± 9.61 15.6-71.06 1 786.0*

Organic matter (OM %) 11.94 ± 3.85 4.61-24.74 4.06 ± 1.27 1.95-5.85 -1 816.0*

Nitrogen (N %) 0.61 ± 0.22 0.23-1.68 0.20 ± 0.06 0.1-0.29 -1 815.0*

Phosporous (P ppm) 1.32 ± 0.60 0.63-3.5 1.36 ± 0.64 0.49-3.2 43.5 NS

Potasium (K cmol kg-1)0.23 ± 0.08 0.06-0.48 0.17 ± 0.09 0.03-0.47 -796.0*

Magnesium (Mg cmol kg-1)0.28 ± 0.21 0.12-1.85 0.18 ± 0.05 0.06-0.35 -964.0*

Calcium (Ca cmol kg-1)0.38 ± 0.22 0.06-0.96 0.35 ± 0.10 0.17-0.79 -89.0 NS

ECEC1 (cmol kg-1)1.03 ± 0.38 0.56-2.64 1.64 ± 0.26 0.77-2.19 1 474.5*

Clay (%) 1.04 ± 2.31 0.0-12.0 18.52 ± 3.69 10.0-28.0 1 772.5*

Silt (%) 13.23 ± 4.97 4.0-28.0 28.12 ± 6.21 8.0-40.0 1 626.0*

Sand (%) 85.71 ± 6.57 62.0-96.0 53.36 ± 6.73 42.0-70.0 -1 763.5*

Carbon (C %) 6.93 2.65-14.35 2.35 1.13-3.39 -1 816.0*

C/N 11.35 2.49-11.7 11.77 11.17-11.98 35.0 NS

N/P 0.46 0.10-2.0 0.15 0.03-0.59 -1 541.0*

Number of samples 75 50

1 Effective cation exchange capacity. The asterisks (*) indicate significant differences P < 0.05. NS: Non-Significant.

486 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

ha-1 year-1 were applied in the form of potas-

sium chloride (KCl)) distributed in four doses

of 1 kg of KCl per recording unit; for the NPK

treatment, each of the doses mentioned in the

previous treatments were applied together; and

for the control no fertilizers were applied.

Measurement of the production and

residence time of fine roots: to measure the

production of fine roots, a modification of the

growth cylinder method (ingrowth cores) was

used (Moreno, 2004). In essence, the method

consists of extracting a soil core from which

roots are removed; then, the soil is returned

to the same hole and left for a time period to

allow the growth of fine roots. Soil cylinders

are removed at pre-established intervals, roots

are extracted, and fine root production are

determined (Hendricks et al., 2006). To control

that the volume of soil deposited and removed

was the same, three thick metal wires were

vertically installed in the walls and left in each

hole (Moreno, 2004); these wires were used

as guides to fill the hole with soil and to align

the core during subsequent sample collection.

Another advantage of this modification is that

the soil deposited back into the hole is not

packed in any container, in such a way that it

is completely in contact with the surrounding

environment and there are no obstacles that

could limit the root growth as happens with the

traditional method, in which the deposited soil

is packed in a mesh-made container.

Each 20 x 20 m recording unit was sub-

divided into 4 (10 x 10 m squares). Then, the

modified growth cylinders were placed in the

center of each 10 x 10 m square, where two

samples were extracted (0-10 cm and 10-20 cm

deep) with an Eijkelkamp® soil core sampler

(8 cm in diameter and 15 cm deep). Standing

stocks of fine roots were sampled in the first

sampling campaign before the application of

fertilization treatments, and fine root produc-

tion were sampled every three months in all the

holes, which were filled again with root-free

soil previously collected and prepared of the

respective soil depth. Subsequently, the separa-

tion and manual extraction of fine roots (with

diameters ≤ 5 mm) was carried out using plas-

tic trays and sieves of different calibers. After

extracting fine roots, the soil was introduced

back into the respective hole, while roots were

transported to the Botany and Ecology labora-

tory of the Technological University of Chocó

for processing. This procedure was performed

quarterly for one year. In each sampling cam-

paign, 100 soil cylinders were evaluated at each

of the two depths per plot; therefore, a total

of 1 000 fine root samples were taken in each

sampling in the five plots evaluated. Fine-root

sampling began six months after the first appli-

cation of fertilization treatments to allow time

for their effects.

In the laboratory, a final cleaning of fine

roots was made with sieves of different cali-

bers and water under pressure. Subsequently,

fine root biomass was obtained by weighing

in an analytical balance (0.001 g) after drying

at 70 ºC in a forced ventilation oven for 72 h

(Acequilab Ltda®); the fine root production

was determined as the accumulated value over

time of fine root biomass in the ingrowth cores.

By using appropriate expansion factors, the

values obtained for fine root biomass (stand-

ing stock as measured in the first sampling

campaign) and fine root production in the first

20 cm of soil (as measured through the pro-

cedure described above in the ingrowth cores

and after adding values found in 0-10 and

10-20 cm) were expressed in t ha-1 and t ha-1

year-1, respectively. The residence time of fine

roots (years) was estimated as the division of

fine root biomass by its production; the above,

based on the fact that ecosystems are in a stable

dynamic state (Olson, 1963).

Data analysis: to evaluate the effect of

soil fertilization on the dynamics of fine roots,

first, the assumptions of normality and homo-

geneity of variances were evaluated with the

Bartlett, Hartley and Kurtosis statistics. Ini-

tially, mean values of root biomass, production

and residence time were compared between

soil types (sandy and loam) with the T-student

test when data had normal statistical distribu-

tion; otherwise, we used the Mann-Whitney

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(W) test (Hoshmand, 1998). When possible,

data were log transformed to reach normal

distribution. Subsequently, the variation of

the dynamics (production and residence time)

of fine roots as a function of the fertilization

treatments, localities, and their interactions

(localities x treatments) were evaluated using

a two-way analysis of variance (ANOVA)

with mixed effects, Tukey’s Multiple Range

Test, and General Linear Models (Hoshmand,

1998). Statistical analyses were performed

in the R programming environment (R Core

Team, 2017).

RESULTS

The production of fine roots in these tropi-

cal rain forests in the 0-20 cm layer was (mean

± standard deviation) 4.16 ± 1.38 t ha-1 year-1 in

sandy-textured soils in in forests of Opogodó,

and 3.45 ± 1.05 t ha-1 year- 1 in loam-textured

soils in forests of Pacurita (Table 2); with sig-

nificant differences between them. Values of

fine root biomass and production were higher

in the 0-10 cm than in the 10-20 cm soil layer

(Table 3). The interaction between factors

(texture type * fertilization treatment) was also

significant (Table 4), which means that at least

one fertilization treatment had different effect

between locations. Indeed, the production of

fine roots was significantly higher in sandy

soils (but not in loamy soils) in response to the

application of P, with respect to the Control

(Fig. 1). Results of fine root production in each

soil layer show that the effects described above

occurred only in the 0-10 cm layer, while the

effect of soil texture, fertilization treatment

and interactions were not significant in the

10-20 cm layer (Table 5). The residence time

of fine roots was 1.56 ± 0.76 years in soils with

a sandy texture, and 1.96 ± 0.76 years in soils

with a loam texture (Table 2); with significant

differences between localities (Table 4). The

interaction between factors also showed signif-

icant effects on the residence time of fine roots

(Table 4, Fig. 1), which means that fertilization

treatments did not have the same effect in the

two texture types (Fig. 1).

DISCUSSION

Fine root dynamics of tropical forests

of Chocó in soils of different texture: In the

tropical rainforests of the biogeographic Chocó

region, the dynamics (productivity and resi-

dence time) of fine roots were greater in sandy

textured soils, compared to soils with loam

texture; i.e., in sandy soils, fine roots grew

faster and had shorter life span. These results

are in line with Aragão et al. (2009), who found

TABLE 2

Production and residence time of fine roots in tropical rain forests with different soil texture of Chocó, Colombia

Fine root biomass (t ha-1)

Soil texture Mean S.D. C.V. (%) S.E. Min. Max. Kurtosis Mann-Whitney

Sandy 5.90 1.84 31.19 0.21 2.22 12.07 0.97 1.1676 ns

Loam 6.28 1.65 26.37 0.23 2.52 11.53 1.36

Fine root production (t ha-1 year-1)

Soil texture Mean S.D. C.V. (%) S.E. Min. Max. Kurtosis Mann-Whitney

Sandy 4.16 1.38 33.09 0.16 1.81 9.27 1.12 1 283**

Loam 3.45 1.05 30.56 0.15 2.10 6.90 2.62

Fine root residence time (years)

Soil texture Mean S.D. C.V. (%) S.E. Min. Max. Kurtosis Mann-Whitney

Sandy 1.56 0.72 45.86 0.08 0.44 4.32 3.69 1 222***

Loam 1.96 0.76 38.65 0.11 0.96 3.79 0.03

S.D. standard deviation, C.V. coefficient of variation, E.E. standard error, Min minimum value, Max maximum value. In

the Mann-Whitney test, asterisks indicate significant differences (*) P < 0.05; (**) P < 0.01; (***) P < 0.001; ns P > 0.05.

488 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

that allocation of NPP to below-ground shows

no relationship to soil fertility but appears to

decrease with the increase of soil clay content.

Higher sand content favors soil aeration (oxy-

gen content) and macroporosity, and promotes

growth and productivity of fine roots, as has

been evidenced in previous research carried

out in tropical rainforests (Jiménez et al.,

2009; Kochsiek et al., 2013; Metcalfe et al.,

2008; Quinto et al., 2016). In summary, these

results bring strong evidence that differences of

edaphic conditions generate significant effects

on the dynamics of fine roots in low altitude

tropical rainforests.

Effect of soil fertilization on the dynam-

ics of fine roots: In these tropical rain forests

of the biogeographical Chocó, the effect of

soil fertilization on the dynamics of fine roots

apparently was determined by the edaphic

conditions, in terms of texture, specific to each

locality. In particular, it was found that fine

Fig. 1. Effect of soil fertilization treatments with N, P, K

and NPK on the rates of production (t ha-1 year-1), and

residence time (years) of fine roots in two tropical rain

forests with differences in soil texture (sandy and loam)

in Chocó, Colombia. The asterisks (*) indicate significant

differences between the fertilization treatments and the

Control. The letters (a, b, c) indicate significant differences

between fertilization treatments.

TABLE 3

Fine root biomass and production in tropical rain forests with different soil texture and fertilization treatments of Chocó, Colombia

Fine Root Biomass (0-10 cm) Texture soil N Min Max Mean S.E. Variance S.D. Median Kurtosis C.V. t-student tests

Sandy 75 1.08 7.97 3.53 0.17 2.04 1.43 3.21 0.98 40.44 1.601 ns

Loam 50 1.19 9.13 3.96 0.21 2.24 1.50 4.07 1.48 37.75

Fine Root Biomass (10-20 cm) Texture soil N Min Max Mean S.E. Variance S.D. Median Kurtosis C.V. Mann-Whitney tests

Sandy 75 0.79 6.54 2.37 0.11 0.94 0.97 2.32 3.52 41.01 0.047 ns

Loam 50 1.07 4.37 2.32 0.11 0.63 0.79 2.33 -0.08 34.08

Fine Root Production (0-10 cm) Texture soil N Min Max Mean S.E. Variance S.D. Median Kurtosis C.V. Mann-Whitney tests

Sandy 75 1.03 5.29 2.65 a0.10 0.82 0.91 2.59 -0.15 34.13 3.4145***

Loam 50 1.09 5.32 2.13 b0.11 0.58 0.76 2.07 5.70 35.64

Fine Root Production (10-20 cm) Texture soil N Min Max Mean S.E. Variance S.D. Median Kurtosis C.V. Mann-Whitney tests

Sandy 75 0.58 6.15 1.51 0.09 0.65 0.81 1.28 14.00 53.52 0.816 ns

Loam 50 0.50 2.50 1.31 0.06 0.20 0.45 1.33 0.24 34.36

N: number of subplots, S.D.: standard deviation, C.V.: coefficient of variation, S.E.: standard error, Min is the minimum value, Max is the maximum value. In the Mann-Whitney

test, asterisks indicate significant differences (*) P < 0.05; (**) P < 0.01; (***) P < 0.001; ns P > 0.05.

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root production increased with the application

of P in sandy soils. Therefore, a limitation of

the underground net primary productivity was

evidenced by the edaphic availability of P in

these soils, which is in line with the hypoth-

esis of P limitation proposed by Vitousek

(1984), Vitousek et al. (2010), Yuan and Chen

(2012), and Dalling et al. (2016), among oth-

ers. However, the addition of N, P, and K did

not have the same effect in promoting fine root

production, which is in line with results report-

ed by Wurzburger and Wright (2015), who

found that the addition of these three nutrients

actually reduced standing fine-root biomass

and mycorrhizal colonization of fine roots; they

also found that fertilization with these three

nutrients shifted allocation away from fine

roots to aboveground biomass. It seems that

the effect of nutrient application varies depend-

ing on complex interactions among nutrients

TABLE 4

Two-way ANOVA with interactions and fixed effects of soil texture (sandy and loam) and fertilization treatments (control,

N, P, K and NPK) on the production and residence time of fine roots in tropical rain forests of Chocó, Colombia

Fine root production (t ha-1 year-1)

Sum of squares Degrees of freedom Mean square FP - value

Texture type 15.28 1 15.28 10.64 0.00145

Treatments 10.16 4 2.54 1.769 0.139

Interaction 19.43 4 4.86 3.383 0.0117

within 165.12 115 1.44

Total 210.00 124

Fine root residence time (years)

Sum of squares Degrees of freedom Mean square FP - value

Texture type 4.75 1 4.75 9.44 0.0026

Treatments 2.55 4 0.64 1.27 0.287

Interaction 5.89 4 1.47 2.93 0.0238

within 57.83 115 0.50

Total 71.02 124

TABLE 5

Two-way ANOVA with interactions and fixed effects of soil texture (sandy and loam) and fertilization treatments (control,

N, P, K and NPK) on fine root production at 0-10 and 10-20 cm-depth in tropical rain forests of Chocó, Colombia

Fine root production (t ha-1 year-1) (0-10 cm)

Sum of squares Degrees of freedom Mean square FP - value

Texture 8.02 1 8.019 12.33 0.0006373

Treatment 7.77 4 1.941 2.986 0.02185

Interaction 6.62 4 1.656 2.547 0.04313

Within 74.78 115 0.650

Total 97.19 124

Fine root production (t ha-1 year-1) (10-20 cm)

Sum of squares Degrees of freedom Mean square FP - value

Texture 1.15 1 1.150 2.457 0.1197

Treatment 0.58 4 0.145 0.3103 0.8706

Interaction 3.66 4 0.915 1.955 0.1061

Within 53.82 115 0.468

Total 59.21 124

490 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

applied, mycorrhizae, and allocation responses

of plants. On the other hand, fertilization did

not have significant effects on residence time;

it appears that the effects of soil fertilization on

the dynamics of fine roots are more evident in

the production than in the residence time.

However, the results of fine root produc-

tion described above for the 0-20 cm soil-layer

were not recorded in the 10-20 layer, where

the effect of soil texture or fertilization treat-

ments were not significant. It has been widely

reported that fine root biomass, production,

decomposition, and turnover are all higher in

the superficial layers of soil than in the deeper

ones (Cordeiro et al., 2020; Cusack & Turner,

2021; Pries et al., 2018), which also was found

in this study. Although the nutrient addition has

been less studied, the effect of nutrient appli-

cation also has been more pronounced in the

surface than in the deeper soil layers (Wang et

al., 2019b), in line with our results.

The fact that the responses to fertilization

were so different between localities differing in

edaphic and topographic characteristics, sug-

gests that the particular conditions of the site

explain such variation. Other authors reported

similar results to ours in the sandy soils and

flat topography of Opogodó, where fertiliza-

tion with P increased the production of fine

roots; for example, Cuevas and Medina (1988)

in Amazonian forests of Tierra Firme (Oxisols)

and Low Bana, with sandy soils. In a meta-

analysis, Yuan and Chen (2012), also found

that fine root production increased with the

application of P in low altitude tropical forests.

Based on these observations, it seems that in

tropical sandy soils, the greater availability (or

addition) of edaphic P increases the production

of fine roots.

Likewise, results of the present study for

the sandy soils of Opogodó are similar to those

reported by Jiménez et al. (2009) and Kochsiek

et al. (2013), who found higher production of

fine roots in tropical sandy soils, which could

be attributed to at least two causes: 1) given

that sandy soils have lower mineral retention

capacity (P, K, Ca, Mg) than loam soils (Jimé-

nez et al., 2009; Silver et al., 2000), as well

as higher release rate of NH4

+, PO4

3- and K+

(Kochsiek et al., 2013), the higher production

of fine roots probably constitutes a response

of plants to capture more nutrients and reduce

their losses due to leaching and runoff, espe-

cially in high-rainfall forests, such as these of

Chocó; 2) in fine-textured tropical soils, the

higher nutrient fixation in addition to the lower

volume of macropores probably limits the pro-

duction of fine roots.

In this study, soil fertilization with N,

P, K and NPK had little effect in loam soils.

Apparently, the greater fixation of mineral

ions that occurs in these tropical soils tends

to cause immobilization of multiple nutrients,

which probably makes it difficult to show the

limitation of each particular mineral nutrient

(Alvarez-Clare et al., 2013). In addition to the

fixation and occlusion of cations, other factors

may have contributed to the lack of response of

fine root production to treatments of N, P and

K application; among them, the lower porosity

that reduces the penetration of nutrients applied

through fertilization, the high rainfall, and the

steep topography, which cause easy washing by

runoff and leaching of added ions (Quinto &

Moreno, 2016; Silver et al., 2000). In addition

to the above reasons, Sayer and Banin (2016),

in an analysis of fertilization experiments

found that one of the main effects of nutrient

application to the soil in tropical forests is the

increase of added nutrients in plant tissues such

as leaves and fine roots, without affecting other

parameters such as the variables of fine root

dynamics measured in the present study.

Another reason that would explain the

little effect of the N and K addition on fine root

dynamics in the studied forests is the fact that

these forests have soils rich in N with moder-

ate K contents (Table 1), which would have

prevented significant effects of the application

of these nutrients on the fine root dynamics.

Apparently, the high levels of total edaphic N,

added to the high rates of biological fixation

of N that regularly occur in this type of eco-

systems (Cleveland et al., 1999), generate an

adequate supply of N and therefore, no limita-

tion of underground net primary productivity

491

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 482-494, January-December 2022 (Published Jul. 12. 30, 2022)

by this nutrient (Vitousek, 1984; Vitousek et

al., 2010; Walker & Syers 1976). Likewise, K

may not be limiting the dynamics of fine roots

because it is a highly mobile nutrient, and its

concentrations remain high due to the input

to the soil from forest canopy (Osorio, 2014),

which would explain the little effect of its

application on the dynamics of fine roots.

In the tropical rain forests of the biogeo-

graphic Chocó, the production of fine roots

was higher in sandy and nutrient-rich soils. The

effects of soil fertilization on the production of

fine roots were associated with the particular

edaphic conditions of each locality. Likewise,

the production of fine roots increased with the

application of P in sandy soils; therefore, a

limitation of underground net primary produc-

tivity was evidenced by the content of edaphic

P in such soils.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict 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

This research was funded through the

Project “Evaluación del efecto de la fertil-

ización del suelo sobre la producción neta del

ecosistema en áreas degradadas por minería,

como estrategia para potenciar la captura de

carbono y la venta de servicios ambientales

en el Chocó biogeográfico”, code 1128 -852-

72243, contract 494-2020. signed between the

Universidad Tecnológica del Chocó Diego Luis

Córdoba, Universidad Nacional de Colombia

sede Medellín and Ministerio de Ciencia, Tec-

nología e Innovación de Colombia. We appre-

ciate the hospitality and collaboration of the

inhabitants of the locality of Opogodó (munici-

pality of Condoto) and Pacurita (municipality

of Quibdó). We thank Jefferson Córdoba Mena

for his support in the project’s field activities.

RESUMEN

Efectos de la fertilización con nutrientes (N, P, K)

sobre la dinámica de raíces finas en bosques húmedos

tropicales con diferente textura del suelo en la región

del Pacífico colombiano

Introducción: La dinámica de las raíces finas incluye pro-

ducción, rotación y descomposición; son cruciales para la

salud de los bosques, afectan todo el complejo biogeoquí-

mico del ecosistema y, en consecuencia, afectan sustancial-

mente el balance de carbono. Sin embargo, la influencia de

los factores ambientales y la limitación de nutrientes del

suelo en las raíces finas presenta incertidumbres considera-

bles y no se ha estudiado en bosques tropicales con más de

7 000 mm de precipitación anual.

Objetivo: Medir el efecto de la fertilización en las raíces

finas en el bosque chocoano de alta precipitación.

Métodos: Se trabajó en dos sitios de la región del Chocó,

Colombia (agosto 2014-mayo 2015), donde las precipita-

ciones superan los 10 000 mm anuales. Se aplicaron cinco

tratamientos de fertilización (N, P, K, NPK y Control) a

dos parcelas por tipo de suelo. Los cilindros de suelo se

retiraron a intervalos preestablecidos para medir las raíces.

Resultados: Las aplicaciones de fósforo aumentaron las

raíces finas; y se produjeron más raíces finas en suelos

arenosos que en francos. Los efectos de la fertilización

estuvieron relacionados, pero no claramente determinados

por las condiciones edáficas.

Conclusiones: En este bosque chocoano, la producción

de raíces finas fue mayor en suelos arenosos y ricos en

nutrientes, pero la productividad primaria neta subterránea

estuvo limitada por el contenido de fósforo edáfico.

Palabras clave: limitación de nutrientes; producción de

raíces finas; descomposición de raíces finas; recambio de

raíces finas; suelos tropicales.

REFERENCES

Alvarez-Clare, S., & Mack, M. C. (2015). Do foliar, litter,

and root nitrogen and phosphorus concentrations

reflect nutrient limitation in a lowland tropical wet

forest? PLoS ONE, 10(4), e0123796.

Alvarez-Clare, S., Mack, M. C., & Brooks, M. (2013). A

direct test of nitrogen and phosphorus limitation to

net primary productivity in a lowland tropical wet

forest. Ecology, 94(7), 1540–1551.

Aragão, L. E. O. C., Malhi, Y., Metcalfe, D. B., & Silva-

Espejo, J. E. (2009). Above- and below-ground net

primary productivity across ten Amazonian forests

492 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

on contrasting soils. Biogeosciences Discussions,

6(1), 2441–2488.

Chapin III, F. S., Matson, P. A., & Mooney, H. A. (2002).

Principles of Terrestrial Ecosystem Ecology. Sprin-

ger-Verlag New York, Inc.

Cleveland, C. C., Townsend, A. R., Schimel, D. S., Fisher,

H., Howarth, R. W., Hedin, L. O., Perakis, S. S.,

Latty, E. F., Von Fischer, J. C., Elseroad, A., & Was-

son, M. F. (1999). Global patterns of terrestrial bio-

logical nitrogen (N2) fixation in natural ecosystems.

Global Biogeochemical Cycles, 13(2), 623–645.

Cordeiro, A. L., Norby, R. J., Andersen, K. M., Valverde-

Barrantes, O., Fuchslueger, L., Oblitas, E., Hartley,

I. P., Iversen, C. M., Gonçalves, N. B., Takeshi, B.,

Lapola, D. M., & Quesada, C. A. (2020). Fine-root

dynamics vary with soil depth and precipitation in a

low-nutrient tropical forest in the Central Amazonia.

Plant Environment Interactions, 1(1), 1–14.

Cuevas, E., & Medina, E. (1988). Nutrient dynamics within

Amazonian forests. II. Fine root growth, nutrient

availability and leaf litter decomposition. Acta Oeco-

logia, 76(1), 222–235.

Cusack, D. F., & Turner, B. L. (2021). Fine root and soil

organic carbon depth distributions are inversely rela-

ted across fertility and rainfall gradients in lowland

tropical forests. Ecosystems, 24, 1075–1092.

Dalling, J. W., Heineman, K., Lopez, O. R., Wright, S. J., &

Turner, B. L. (2016). Nutrient availability in tropical

rain forests: The paradigm of Phosphorus limitation.

In G. Goldstein, & L. S. Santiago (Eds.), Tropical tree

physiology. Adaptations and responses in a changing

environment (pp. 261–273). Springer International

Publishing Switzerland.

Finér, L., Ohashi, M., Noguchi, K., & Hirano, Y. (2011).

Fine root production and turnover in forest ecosys-

tems in relation to stand and environmental charac-

teristics. Forest Ecology and Management, 262(1),

2008–2023.

Gill, R. A., & Jackson, R. B. (2000). Global patterns of

root turnover for terrestrial ecosystems. The New

Phytologist, 147, 13–31.

Green, J. J., Dawson, L. A., Proctor, J., Duff, E. I., & Els-

ton, D. A. (2005). Fine root dynamics in a tropical

rain forest is influenced by rainfall. Plant and Soil,

276(1), 23–32.

Guo, J., Gao, Y. Z., Eissenstat, D. M., He, C. G., & Sheng,

L. X. (2020). Belowground responses of woody

plants to nitrogen addition in a phosphorus-rich

region of northeast China. Trees, 34, 143–154.

Hendrick, R. L., & Pregitzer, K. S. (1997). The relationship

between fine root demography and the soil environ-

ment in northern hardwood forests. Ecoscience, 4(1),

99–105.

Hendricks, J. J., Hendrick, R. L., Wilson, C. A., Mitchell,

R. J., Pecot, S. D., & Guo, D. (2006). Assessing

the patterns and controls of fine root dynamics: an

empirical test and methodological review. Journal of

Ecology, 94(1), 40–57.

Hoshmand, A. R. (1998). Statistical Methods for Environ-

mental and Agricultural Sciences. CRC Press LLC.

Intergovernmental Panel on Climate Change. (2014). Cam-

bio climático 2014: Informe de síntesis. Contribución

de los Grupos de trabajo I, II y III al Quinto Infor-

me de Evaluación del Grupo Intergubernamental

de Expertos sobre el Cambio Climático. IPCC.

https://www.ipcc.ch/site/assets/uploads/2018/02/

SYR_AR5_FINAL_full_es.pdf

Jackson, R. B., Mooney, H. A., & Schulze, E. D. (1997).

A global budget for fine root biomass, surface area,

and nutrient contents. Proceedings of the National

Academy of Sciences of the United States of America,

94(1), 7362–7366.

Jiménez, E., Moreno, F., Peñuela, M., Patiño, S., & Lloyd,

J. (2009). Fine root dynamics for forests on contras-

ting soils in the Colombian Amazon. Biogeosciences,

6, 2809–2827.

Kochsiek, A., Tan, S., & Russo, S. E. (2013). Fine root

dynamics in relation to nutrients in oligotrophic

Bornean rain forest soils. Plant Ecology, 214(5),

869–882.

Matamala, R., González-Meler, M. A., Jastrow, J. D.,

Norby, R. J., & Schlesinger, W. H. (2003). Impacts of

fine root turnover on forest NPP and soil C sequestra-

tion potential. Science, 302, 1385–1387.

Metcalfe, D. B., Meir, P., Aragao, L. E., Da Costa, A. C. L.,

Braga, A. P., GonḈalves, P. H. L., de Athaydes Silva

Jr., J., de Almeida, S. S., Dawson, L. A., Malhi, Y., &

Williams, M. (2008). The effects of water availability

on root growth and morphology in an Amazon rain-

forest. Plant and Soil, 311(1), 189–199.

Miller, A. J., Schuur, E. A. G., & Chadwick, O. A. (2001).

Redox control of phosphorus pools in Hawaiian mon-

tane forest soils. Geoderma, 102(1), 219–237.

Mirmanto, E., Proctor, J., Green, J., Nagy, L., & Suriantata.

(1999). Effects of nitrogen and phosphorus fertiliza-

tion in a lowland evergreen rainforest. Philosophical

Transactions of the Royal Society B, 354, 1825–1829.

Moreno, F. (2004). Soil Carbon Dynamics in Primary and

Secondary Tropical Forests in Colombia (Doctoral

dissertation). Florida International University, United

States of America.

Nadelhoffer, K. J. (2000). The potential effects of nitrogen

deposition on fine-root production in forest ecosys-

tems. The New Phytologist, 147, 131–139.

493

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 482-494, January-December 2022 (Published Jul. 12. 30, 2022)

Olson, J. S. (1963). Energy storage and the balance of

producers and decomposers in ecological systems.

Ecology, 44(2), 322–331.

Osorio, N. W. (2014). Manejo de nutrientes en suelos del

Trópico. Editorial L. Vieco S.A.S.

Ostertag, R. (2001). Effects of nitrogen and phosphorus

availability on fine-root dynamics in Hawaiian mon-

tane forests. Ecology, 82(2), 485–499.

Poveda, I. C., Rojas, C., Rudas, A., & Rangel, O. (2004). El

Chocó biogeográfico: Ambiente Físico. In O. Rangel

(Ed.), Colombia Diversidad Biótica IV. El Chocó

biogeográfico/ Costa Pacífica. Instituto de Ciencias

Naturales, Universidad Nacional de Colombia.

Pries, C. E. H., Sulman, B. N., West, C., O’Neill, C.,

Poppleton, E., Porras, R. C., Castanha, C., Zhu, B.,

Wiedemeier, D. B., & Torn, M. S. (2018). Root litter

decomposition slows with soil depth. Soil Biology

and Biochemistry, 125, 103–14.

Quinto, H., Caicedo, H., Perez, M. T., & Moreno, F. H.

(2016). Dinámica de raíces finas y su relación con la

fertilidad edáfica en bosques pluviales tropicales del

Chocó biogeográfico colombiano. Revista de Biolo-

gía Tropical, 64(4), 1709–1719.

Quinto, H., & Moreno, F. H. (2016). Precipitation effects

on soil characteristics in tropical rain forests of

the Chocó biogeographical region. Revista Facultad

Nacional de Agronomía, 69(1), 7813–7823.

R Core Team. (2017). R: A language and environment for

statistical computing. R Foundation for Statistical

Computing. Vienna, Austria. https://www.R-project.

org/

Saugier, B., Roy, J., & Mooney, H. A. (2001). Estimations

of global terrestrial productivity: Converging toward

a single number? In J. Roy, B. Saugier, & H. A.

Mooney (Eds.), Terrestrial Global Productivity (pp.

401–426). Academic Press.

Sayer, E. J., & Banin, L. F. (2016). Tree nutrient status and

nutrient cycling in tropical forest. Lessons from ferti-

lization experiments. In G. Goldstein, & L. S. Santia-

go (Eds.), Tropical tree physiology. Adaptations and

responses in a changing environment (pp. 275–297).

Springer International Publishing Switzerland.

Shieh, G., & Jan, S. (2004). The effectiveness of randomi-

zed complete block design. Statistica Neerlandica,

58(1), 111–124.

Silver, W. L., Neff, J., Mcgroddy, M., Veldkamp, E.,

Keller, M., & Cosme, R. (2000). Effects of soil tex-

ture on belowground carbon and nutrient storage in

a lowland Amazonian forest ecosystem. Ecosystems,

3, 193–209.

Silver, W. L., Thompson, A. W., Mcgroddy, M. E., Varner,

R. K., Dias, J. D., Silva, H., Crill, P. M., & Keller,

M. (2005). Fine root dynamics and trace gas fluxes

in two lowland tropical forest soils. Global Change

Biology, 11, 290–306.

Sullivan, B. W., Alvarez-Clare, S., Castle, S. C., Porder,

S., Reed, S. C., Schreeg, L., Cleveland, C. C., &

Townsend, A. R. (2014). Assessing nutrient limita-

tion in complex forested ecosystems: alternatives to

large-scale fertilization experiments. Ecology, 95(3),

668–681.

Thornton, P. E., Lamarque, J. F., Rosenbloom, N. A.,

& Mahowald, N. M. (2007). Influence of carbon-

nitrogen cycle coupling on land model response

to CO2 fertilization and climate variability. Global

Biogeochemical Cycles, 21, GB4018. https://doi.

org/10.1029/2006GB002868.

Violita, V., Triadiati, T., Anas, I., & Miftahudin, M. (2016).

Fine root production and decomposition in lowland

rainforest and oil palm plantations in Sumatra, Indo-

nesia. HAYATI Journal of Biosciences, 23(2016),

7–12.

Vitousek, P. M. (1984). Litterfall, nutrient cycling and

nutrient limitation in tropical forests. Ecology, 65(1),

285–298.

Vitousek, P., Porder, S., Houlton, B. Z., & Chadwick, O.

A. (2010). Terrestrial phosphorus limitation: mecha-

nisms, implications, and nitrogen–phosphorus inte-

ractions. Ecological Applications, 20(1), 5–15.

Vitousek, P. M., & Sanford Jr., R. L. (1986). Nutrient

cycling in moist tropical forest. Annual Review of

Ecology and Systematics, 17, 137–167.

Walker, T. W., & Syers, J. K. (1976). The fate of phospho-

rus during pedogenesis. Geoderma, 15, 1–19.

Wang, C., Brunner, I., Zong, S., & Li, M. (2019a). The

dynamics of living and dead fine roots of forest

biomes across the Northern Hemisphere. Forests,

10(953), 1–15.

Wang, W. J., Mo, Q. F., Han, X. G., Hui, D. F., & Shen, W.

J. (2019b). Fine root dynamics responses to nitrogen

addition depend on root order, soil layer, and experi-

mental duration in a subtropical forest. Biology and

Fertility of Soils, 55, 723–736.

Wright, S. J., Yavitt, J. B., Wurzburger, N., Turner, B. L.,

Tanner, E. V. J., Sayer, E. J., Santiago, L. S., Kaspa-

ri, M., Hedin, L. O., Harms, K. E., Garcia, M. N.,

& Corre, M. D. (2011). Potassium, phosphorus, or

nitrogen limit root allocation, tree growth, or litter

production in a lowland tropical forest. Ecology,

92(8), 1616–1625.

Wurzburger, N., & Wright, S. J. (2015). Fine root responses

to fertilization reveal multiple nutrient limitation in a

lowland tropical forest. Ecology, 96(8), 2137–2146.

494 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 482-494, January-December 2022 (Published Jul. 12, 2022)

Yavitt, J. B., Harms, K. E., Garcia, M. N., Mirabello, M.

J., & Wright, S. J. (2011). Soil fertility and fine root

dynamics in response to four years of nutrient (N,

P, K) fertilization in a lowland tropical moist forest,

Panama. Austral Ecology, 36(4), 433–445.

Yuan, Z. Y., & Chen, H. Y. H. (2012). A global analysis

of fine root production as affected by soil nitrogen

and phosphorus. Proceedings of the Royal Society B,

279(1743), 3796–3802.

Zhang, X., & Wang, W. (2015). The decomposition of fine

and coarse roots: their global patterns and controlling

factors. Scientific Reports, 5(1), 1–10. https://doi.

org/10.1038/srep099400