Science of the Total Environment 631–632 (2018) 1600–1610

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Science of the Total Environment

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Impact of potato cultivation and cattle farming on physicochemical

parameters and enzymatic activities of Neotropical high Andean Páramo
ecosystem soils
Lizeth Manuela Avellaneda-Torres a,b,c,⁎, Tomás Enrique León Sicard d, Esperanza Torres Rojas b,e
a
Programa de Doctorado en Agroecología, Departamento de Desarrollo Rural, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Bogotá D. C., Colombia
b
Colombian Center for Genomics and Bioinformatics of Extreme Environments (GEBIX), Bogotá D. C., Colombia
c
Programa de Ingeniería Ambiental, Grupo de Investigación TECNOAMBIENTAL, Facultad de Ingeniería, Universidad Libre, Bogotá D.C., Colombia
d
Instituto de Estudios Ambientales (IDEA), Universidad Nacional de Colombia, Bogotá D.C., Colombia
e
Laboratorio de Agrobiotecnología, Departamento de Agronomía, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Bogotá, D.C., Colombia

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Potato crop and livestock decreased β-

glucosidase, phosphodiesterase and
urease.
• Potato crop and livestock increased acid
phosphatase and protease on Páramo
soils.
• Drought increased organic carbon, cat-
ion exchange capacity and enzymatic
activities.
• Potato crop and livestock decreased car-
bon and cation exchange capaci\ty on
Páramo.
• Enzymatic activities indicated impacts
of potato crop and livestock on Páramo
soils.

a r t i c l e i n f o a b s t r a c t

Article history: The Andean Páramos are high mountain ecosystems whose soils are essential for the management of South
Received 19 September 2017 American water resources, but research on anthropic impacts to these soils is currently minimal and insufficient.
Received in revised form 12 February 2018 The objective of this study was to evaluate the impacts of potato (Solanum tuberosum) cultivation and livestock
Accepted 13 March 2018
on the physicochemical parameters and enzymatic activities that determine the soil quality of the Neotropical
Available online xxxx
high Andean Páramo ecosystem in the Nevados National Natural Park (Nevados NNP) in Colombia. It was
Keywords:
hypothesised that sites with potato crops and livestock farming would exhibit significant changes in soil physi-
Protected areas cochemical parameters and enzymatic activities compared with Páramo sites that have been conserved without
Páramo agriculture. Samples were collected from soils under potato cultivation, livestock and Páramo (subject to the low-
Land use impact est degree of human intervention possible), on three farms in the El Bosque District at three different altitudes
Soil enzymes (Buenos Aires, El Edén and La Secreta) during two seasons (dry and rainy). The results showed that none of
Soil quality indicators the physical parameters under study presented statistically significant differences due to the type of use (live-
stock, potato crop or Páramo), season of sampling (dry or rainy season) or altitude (different farms). The chemical
parameters that statistically significantly differed due to land use were organic carbon, cation exchange capacity,
calcium, potassium, and ammonium and those that showed statistically significant differences associated with
the sampling timing were organic carbon, nitrogen, cation exchange capacity, total carbon, C/N and nitrate.

⁎ Corresponding author at: Programa de Doctorado en Agroecología, Departamento de Desarrollo Rural, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Bogotá D. C.,
Colombia.
E-mail address: lmavellanedat@unal.edu.co (L.M. Avellaneda-Torres).

https://doi.org/10.1016/j.scitotenv.2018.03.137
0048-9697/© 2018 Elsevier B.V. All rights reserved.
 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610 1601

Additionally, there were differences in organic carbon due to the altitude of the farms. With respect to enzymatic
activities, those of β-glucosidase, phosphodiesterase and urease significantly decreased in soils under potato cul-
tivation and livestock relative to those of Páramo, but those of acid phosphatase and protease increased signifi-
cantly under potato cropping and livestock. The activities of β-glucosidase, acid phosphatase, alkaline
phosphatase, phosphodiesterase and protease were higher during the dry season than the rainy season, and
the activities of β-glucosidase, acid phosphatase and urease decreased statistically in the lower-altitude farm
(La Secreta). These decreases in enzymatic activities are attributable to changes in the organic carbon of the
soil. This study provides a novel insight on the relationships between land use and the physicochemical param-
eters and enzymatic activities of Páramo soils (which have been minimally studied to date) at different altitudes
and during different seasons. The results suggest that changes in agricultural practices should be implemented to
maintain the organic carbon of soil and, therefore, its enzymatic activities.
© 2018 Elsevier B.V. All rights reserved.

1. Introduction
The Andean Páramos are unique Neotropical high mountain ecosys-
tems that are essential for the management of South American water re-
sources as they perform fundamental ecological functions related to the
collection, regulation and supply of water (de Groot et al., 2002; Otero
et al., 2011). The Páramos are mainly located in Colombia, Venezuela,
Ecuador and northern Peru, and they extend from the boundaries of
the Andean Forest (3200 and 3500 m in altitude) to the limit of perma-
nent snow (4500 and 5000 m in altitude) (Buytaert et al., 2007;
Poulenard et al., 2001).
The Nevados National Natural Park (Nevados NNP) is in the central
high Andes Mountains and is one of the most important protected
areas in Colombia, covering 58,300 ha. The most representative ecosys-
tem is the Páramo, which covers nearly 38,600 ha (66.21% of the total
area of the Nevados NNP) (PNNN, 2010). However, there is a strong
conflict over land use between the Nevados NNP and the resident
farmers, especially in the El Bosque District, where farmers engage in
subsistence agriculture involving potato (Solanum tuberosum) cultiva-
tion and raising cattle, applying traditional, inherited farming practices
in combination with techniques from the Green Revolution. Therefore,
the El Bosque District embodies the conflicts of interests between sub-
sistence agricultural practices and conservation goals in the Páramo
that are particularly important because agricultural and livestock activ-
ity is prohibited inside the Nevados NNP.
A series of physical, chemical and biological indicator parameters are
used to assess soil health and quality. Physicochemical parameters can
indicate soil degradation and erosion (Xu et al., 2016; Yusong et al.,
2017) and desertification (Li et al., 2018) as well as changes in soil
due to systems of use (Moghimian et al., 2017; Singh et al., 2016),
land use and cover (Liu et al., n.d.; Moghimian et al., 2017), soil manage-
ment and climate changes (Bojko and Kabala, 2016). Additionally, they
can serve as indicators of soil reclamation (Xie et al., 2017) and changes
in ecosystem sustainability (Zhu et al., 2016). Similarly, enzymatic activ-
ities are involved in the transfer of energy, soil biochemical processes
and environmental quality (Dick, 1994; Tabatabai, 1994) and are fre-
quently used as indicators of microbial activity (Garcia et al., 1993;
Gispert et al., 2013; Salazar et al., 2011). At an ecosystem scale, soil en-
zymatic activity is a function of the microbial activity associated with
roots, and it regulates the humidity, temperature and quality of the sub-
strate (nutrient availability) (Salazar et al., 2011; Tabatabai, 1994).
Therefore, enzymatic activities can be used as a parameter to describe
changes associated with alterations to soil use and cover associated
with agricultural practices and to interpret the functions of soil within
the ecosystem (Acosta-Martínez et al., 2007). Furthermore, enzymatic
activities are considered important factors for edaphic fertility and sen-
sitive indicators of agricultural, ecological and anthropogenic influences
on the soil (Marcinkeviciene et al., 2013; Svirskene, 2003), so they are
important for measuring the degree of soil degradation in agricultural
and natural ecosystems (Gianfreda and Rao, 2011; Trasar-Cepeda
et al., 2000; van Beelen and Doelman, 1997). Soil enzymes are tightly
linked to nutrient cycles, and they respond quickly to changes due to an-
thropogenic factors, such as the presence of xenobiotic substances
(Gianfreda et al., 2005; Gianfreda and Rao, 2011). Hydrolases are partic-
ularly important because they are closely linked to the carbon, nitrogen
and phosphorus nutrient cycles (Yuan et al., 2012).
Despite the importance of Páramo ecosystems, specifically those lo-
cated within the Nevados NNP, research on the impacts of potato culti-
vation and livestock on Páramo soils, especially on the enzymatic
activities, is currently minimal and insufficient, so the objective of this
study was to (1) evaluate if potato cultivation and livestock impact
the physicochemical parameters and enzymatic activities that deter-
mine the soil quality of the Neotropical high Andean Páramo ecosystem
in the Nevados NNP in Colombia and (2) evaluate if these changes are
affected by altitude and the sampling season. Additionally, the soils
were taxonomically characterised and used as reference tools for com-
parisons. It was hypothesised that the sites with potato cultivation
and livestock rearing would exhibit significant changes in soil physico-
chemical parameters and enzymatic activities compared with Páramo
sites that have been conserved without agricultural activities.
2. Materials and methods
2.1. Description of the study site
The present study was performed within the Nevados NNP in the El
Bosque District, Risaralda Department, Colombia. Access to the El
Bosque District is difficult because it is in the centre of the Nevados
NNP in the western range of the Andes mountains in the municipality
of Pereira (Risaralda), approximately 300 km from Bogotá. Reaching
the study area requires between five and seven hours on foot or by
mule from El Cedral (Risaralda), two hours from the city of Pereira, or
four to six hours, also on foot or by mule, by horse trails from the Potosí
site in the city of Villamaría, Caldas.
The following agroecosystems were examined: Buenos Aires (04°44′
58.3′′ N - 075°26′40.4′′ W; 3769 m a.s.l.), El Edén (04°44′32.3′′ N -
075°26′37.9′′ W; 3590 m a.s.l.) and La Secreta (04°44′08.5′′ N -
075°26′34.7′′ W; 3432 m a.s.l.) (Fig. 1-A and B). According to the gen-
eral study of soils from the Instituto Geográfico Agustín Codazzi
(IGAC) (2004), the sampled agroecosystems are within two climatic
units. The Buenos Aires agroecosystem has a pluvial cold climate, is lo-
cated near Otun Lake between 3600 and 4000 m a.s.l., and has daily av-
erage temperatures of 6 to 9 °C and average annual precipitation
between 2000 and 4000 mm. In this region, microclimates are created
by intense circulation of local winds resulting from proximity to the
Santa Isabel volcano (IGAC, 2004). The El Edén and La Secreta
agroecosystems have a cold and humid climate, altitudes between
3000 and 3600 m a.s.l., average daily temperatures between 9 and
12 °C and average annual precipitation between 1000 and 2000 mm.
In the study areas, potato fields and pastures (for cattle raising) have
been rotated in cycles with fields lying fallow biannually for N80 years.
Potato farming is primarily performed manually without any
1602 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610

Fig. 1. Geographic location of the study sites. A. Labels showing the study sites inside the Nevados NNP in Colombia, South America. B. The “Buenos Aires”, “El Edén” and “La Secreta” farms
in the village of “El Bosque”, Pereira Municipality, Risaralda, Colombia, with coordinates (Google Inc.) and altitudes in metres above sea level (m a.s.l.). C. Diagram of the experimental
design and soil sampling, including the taxonomic classification of the soils.

specialised machinery, but conventional agro-chemicals are applied in-
cluding carbofuran, parathion, methamidophos, chlorpyrifos, profeno-
fos, mancozen, propineb, mefenoxam, phenothrin and N:P:K
fertilisers. Grasses cultivated in the area include Dactylis glomerate
and ryegrass (Lolium sp. and Lachemilla sp.), and the adjacent con-
served areas (Páramo) are predominantly covered with Cortaderia
selloana, Pernettya prostrata, Buddleia sp., Lupinus albus, Dendropanax
sp. and Chusquea sp. Below, we use Páramo to refer to the area with
the least possible anthropic intervention.
2.2. Taxonomic characterisation of soil in the El Bosque District
Sampling was performed in Nevados NNP in the El Bosque District,
Colombia to identify the modal profile. Soils were evaluated from
three agroecosystems at different altitudes: Buenos Aires, El Edén and
La Secreta. In each agroecosystem, three soil samples were obtained
with box corers that corresponded to soil under potato fields, cattle pas-
ture and conserved Páramo, and 2 × 2 × 1.2-m trenches were opened on
each farm to identify the soil type according to IGAC soil guidelines
(IGAC, 2007). In each trench, representative samples were collected
from each horizon and analysed based on IGAC (2007) lab protocols,
and the taxonomic classification was performed to the subgroup level
using a soil taxonomy key (SSS, 2010).
2.3. Experimental design and soil sampling
To identify the effects of potato cultivation and livestock on the
physicochemical parameters and enzymatic activities of Páramo soil,
samples were collected from three agroecosystems at different eleva-
tions and evaluated simultaneously: Buenos Aires (3769 m a.s.l.), El
Edén (3590 m a.s.l.) and La Secreta (3432 m a.s.l.) of the village of El
Bosque in the Nevados NNP, Colombia. The first 20 cm of the soils was
collected after removing the layer of plant material on the surface, and
in each agroecosystem (different altitudes), three types of land use
were simultaneously evaluated: Páramo (with the lowest degree of
human intervention possible), potato cultivation and livestock. Within
each land use in each agroecosystem, three 10-m × 10-m windows or
observation quadrants were evaluated, and soil samples composed of
10 subsamples were collected along a zigzag transect in each. Sampling
was conducted in both the dry and rainy seasons. An experimental de-
sign was implemented that consisted of three factors, soil use, altitude
and season, and each factor included a nested factor of the observation
 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610
window or quadrant. Each combination of factors was evaluated at the
three different sites for a total of 54 samples: 3 land uses × 3 altitudes
× 2 seasons × 3 observation windows or quadrants; each sample was
analysed in three replicates (Fig. 1-C). The minimum distance between
each land use type was 500 m, and the sampling plots were verified as
not continuous to avoid possible errors due to contamination of one
sample with another. Sampling was performed in the same way for
the different land uses, farms and seasons.
2.4. Physicochemical parameters of the soil
The physicochemical parameters of the soil were determined ac-
cording to IGAC methods (2006) as follows: humidity according to the
gravimetric method; apparent density (D) according to the cylinder
method; structural stability according to Yoder's mechanical sieving
method; texture according to the Bouyoucos method; pH in water ac-
cording to the potentiometric method with soil:water (w/v) ratio of
1:1; percentage of organic carbon (OC) according to Walkley and Black's
method; cation exchange capacity (CEC), calcium (Ca), magnesium
(Mg), potassium (K) and sodium chloride (NaCl) through extraction
with 1 N ammonium (NH4) acetate; exchangeable acidity through ex-
traction with 1 M potassium chloride (KCl); assimilable P by the Bray
II method; total N (TN) with the micro-Kjeldahl method; N-NH4 and ni-
trate (N-NO3) through extraction with 2 M KCl; and distillation with
magnesium oxide (MgO) and Devarda's alloy. In addition, the total car-
bon content (TC), total hydrogen (TH) and TN contents were analysed
with a LECO 1000 elemental analyser (Model CHN–1000, LECO Corp.,
St Joseph, MI) (IGAC, 2006). The TC, TH and TN contents were only de-
termined in the higher- and lower-altitude farm, that is, Buenos Aires
and La Secreta, respectively.
2.5. Soil enzymatic activity
Urease activity (EC 3.5.1.5) was determined using urea as a substrate
and based on the method described by (Alef and Nannipieri, 1995). Pro-
tease activity (EC 3.4.2.21-24) was determined using casein as substrate
(Ladd and Butler, 1972). Acid and alkaline phosphatase activity (EC
3.1.3.2 and 3.1.3.1, respectively) were determined using sodium p-
nitrophenyl phosphate as a substrate (Eivazi and Tabatabai, 1988;
Tabatabai and Bremner, 1969). Phosphodiesterase activity (EC 3.1.4.1)
was determined using sodium bis-p-nitrophenyl phosphate as a sub-
strate (Browman and Tabatabai, 1978). β-glucosidase activity (EC
3.2.1.21) was determined using p-nitrophenyl-β-D-glycoside as a sub-
strate (Eivazi and Tabatabai, 1988). Dehydrogenase activity (EC
3.1.4.1) was determined using triphenyltetrazolium chloride as a sub-
strate (Öhlinger, 1996). To determine the urease, protease and dehydro-
genase activities (EC 1.1.1.1), 0.1 g of soil was collected, and 0.2 g was
collected to determine the acid phosphatase, alkaline phosphatase,
phosphodiesterase and β-glucosidase activities. The quantities of the re-
agents and substrates were modified according to the quantity of the
soil used. Urease activity is expressed as μg N g−1 dw 2 h−1; protease ac-
tivity is expressed as μg tyr g−1 dm 2 h−1; acid phosphatase, alkaline
phosphatase, phosphodiesterase and β-glucosidase activities are
expressed as μg pNP g−1 dw h−1; and dehydrogenase activity is
expressed as μg TPF g−1 dm 16 h−1. All the enzymatic activities were
determined in triplicate.
2.6. Statistical analysis
The assumptions of homogeneity of variance and normality were
analysed with a Bartlett and Shapiro-Wilk test. However, because the
data did not satisfy the normality assumption, non-parametric
Kruskal-Wallis and Wilcoxon tests were performed with a significance
level of P ≤ 0.05 to assess any statistically significant differences. The
above tests were performed with the free software R 2.10.0. Subsequent
1603
multivariate analyses (MVA) were applied, including a principal com-
ponent analysis (PCA), using SPAD v.7 software.
3. Results and discussion
3.1. Taxonomic classification of soils
The soils described for the Nevados NNP in the El Bosque District cor-
respond to screes at the bottom of the slope, where materials from ad-
jacent steep slopes accumulated through the force of gravity. These
deposits lie on top of thick mantles of volcanic ashes. Old scree buried
by pyroclastic materials can be observed in the study area.
The soils belong to the order Andisol, with Typic Haplocryands found
at the Buenos Aires farm and Thaptic Hapludands found at the La
Secreta and El Edén farms (Fig. 1-C). These soils have andic properties
in 60% or more of their depths, so they have low D, high phosphate re-
tention and variable fertility (SSS, 2010). Their P fixation capacities are
high because they are derived from volcanic ashes (Van Reeuwijk,
1989; Wada, 1980). The observed soils partially match the results of
the general soil study performed by the IGAC (2004) in which Typic
Haplocryands were found in areas with Lithic Cryandept soils, and
Thaptic Hapludand soils were found in areas with Fluventic
Humitropept soils. These results are explained by the lower level of de-
tail in the general IGAC (2004) soil study, whereas the present study
was performed at the farm level and shows greater detail.
The combination of a humid and cold climate causes a low rate of or-
ganic matter (OM) decomposition in these soils (Cleef, 1981; Hofstede,
1995; Luteyn, 1992; Monasterio and Sarmiento, 1991), and stable com-
pounds form with inorganic non-crystalline materials, which further
slows degradation (Jaramillo and Daniel, 2002; Van Reeuwijk, 1989;
Wada, 1980). In addition, Andean Andisols have a high C content and
are vulnerable to erosion because of farming and deforestation (Henry
et al., 2013). The OC held in these soils is important because it mitigates
increases in atmospheric C associated with climate change (Henry et al.,
2013).
3.2. Soil physicochemical parameters
None of the physical parameters under study showed statistically
significant differences between land uses (potato, livestock or Páramo),
season or farm (altitude differences) (Table 1), indicating that the im-
pact of potato and cattle farming within El Bosque has not been great
enough to significantly change these parameters. This result could be at-
tributed to the established resting periods between each potato-
planting event (N7 years fallow) and the low-intensity cattle rearing,
which is measured as livestock density ha−1 (0.24–0.36).
The chemical parameters that differed statistically between the
three land-use types were OC, CEC, Ca, K and NH4 (Tables 1 and 2).
The properties with statistically significant seasonal differences were
OC, N, and CEC, % C, C/N and NO3, with only OC differing among the
three evaluated factors (land use, season and altitude). The remaining
parameters (pH, P, Na, AI and Mg) did not significantly differ among
any of the evaluated factors.
The behaviour of OC (easily oxidised OC) showed a trend of Páramo
N potato farms N cattle farms. The differences between Páramo and cat-
tle farming soils were statistically significant, but those between potato
and cattle farming were not. Otero et al. (2011) reported the same be-
haviour of OM in soils under potato cultivation and cattle farming in
Páramo ecosystems. Similar results were found in Chingaza NNP and
Nevados NNP, where the TC was lower in the soil profiles of conserved
highland ecosystems than in non-conserved ecosystems.
The decrease in easily oxidised OC in soils under potato and cattle
farming in the present study might have been caused by the loss of na-
tive vegetation cover due to cattle farming relative to the Páramo, which
exposed the soil to environmental factors such as water, air and solar ra-
diation and likely increased erosion (Otero et al., 2011). The loss of soil
1604 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610

Table 1
Mean physical and chemical properties for the evaluated factors (land use, season and farm) in Nevados NNP in the El Bosque District.

Factor Ɵg D WAD pH OC N P Ca K Mg Na AI CEC

% g cm−3 Mm % % cmol kg−1

Land use n = 54 Páramo 79.6a 0.7a 12.4a 5.3a 8.0a 0.65a 6.9 a 7.5a 0.5a 2.2a 0.1a 1.0a 44.3a
Crop 48.1 a 0.7a 11.6a 5.3a 6.3ab 0.52a 34.5a 4.1b 0.2b 0.8a 0.3a 1.1a 32.4b
Cattle farming 53.8 a 0.9a 12.0a 5.5a 6.0b 0.51a 21.3a 3.5b 0.4ab 0.9a 0.2a 0.6a 31.8b
Season n = 54 Rainy 62.4 a 0.7a 12.3a 5.3a 5.8a 0.52a 21.1a 4.9a 0.4a 1.3a 0.3a 1.0a 32.3a
Dry 58.6 a 0.8a 11.7a 5.4a 7.7b 0.60b 21.3a 5.1a 0.4a 1.2a 0.1a 0.8a 40.0b
FARM n = 54 Buenos Aires 59.8 a 0.8a 10.4a 5.2a 7.2a 0.52a 16.8a 4.5a 0.4 a 1.4a 0.1a 1.2a 36.7a
El Edén 59.6 a 0.7 a 12.8a 5.4a 7.4a 0.64a 26.2a 6.9b 0.4 a 1.5a 0.1a 0.9a 37.1a
La Secreta 62.7 a 0.8 a 12.7a 5.4a 5.7b 0.52a 20.9a 3.7a 0.4 a 1.0a 0.4a 0.7a 34.5a
Standard deviation 0.18 0.14 1.68 0.33 2.03 0.14 21.7 0.30 0.02 0.08 0.01 0.05 9.9

Ɵg, gravimetric moisture; D, apparent density; WAD, mean weighted diameter; OC, organic carbon; CEC, cation exchange capacity; and n, number of replicates.

OC has also been proposed to occur with reduced OM contributions, in- The increases in OC, TC, C/N and NO3 were significantly greater dur-
creased decomposition rates or reduced physical protection of C in soils, ing the dry season than the rainy season, which might have been due to
such as with destructive tillage processes (Henry et al., 2013; Post and certain environmental factors, such as the higher humidity, that in-
Kwon, 2000). Similarly, it has been noted that tillage decreases OM be- crease soil erosion and cause a subsequent loss of OC (Otero et al.,
cause of higher mineralisation of crop residues, alteration of soil aggre- 2011). The consistency of the results regarding the effects of potato
gates and increased aeration (Sainju et al., 2003). However, and cattle farming obtained with the Walkley-Black method and the
conservation tillage (reduced and no-tillage) increases the OC in the LECO analyser may indicate that weather conditions have a greater im-
topsoil layer (López-Bellido et al., 2010; Melero et al., 2011; Sainju pact on easily oxidised OM as well as complex and molecularly stable
et al., 2003; Six et al., 1998), improves aggregation and preserves soil re- compounds.
sources better than conventional tillage practices (Melero et al., 2011). A statistically significant decrease in OC was observed in the La
Changes in soil use have been reported to increase erosion through Secreta agroecosystem relative to the other ecosystems because of its
changes in vegetation cover and tillage, but the fate of C in eroded lower altitude, which might explain the increased average temperature
soils is still a debated subject. Soil erosion processes have been de- of this agroecosystem and OM degradation that are reflected in the soil
scribed as the partial redistribution of buried C by erosion and emission taxonomy (Cryand vs Udand). However, the OC values of the studied
into the atmosphere (Henry et al., 2013; Lal, 2004). soils were between 5.7 and 8.0%, so all the evaluated soils were classi-
Decreases in soil TC, TN and C/N (as determined with a LECO ele- fied as having high OC (ICA, 1992).
mental analyser) were caused by potato and cattle farming (Table 2), The CEC and NH4 were significantly lower in soils under potato and
but these differences were not statistically significant. Although potato cattle farming. The CEC significant increased during the dry season com-
and cattle farming remove vegetation cover, this does not affect the pared with the wet season, and this might have been associated with
above indicators. However, the OC determined by the Walkley-Black the previously discussed loss of OM generated by changes in the vegeta-
dry combustion method (easily oxidised C) expresses the total contents tion cover and subsequent exposure of the soil to environmental factors
of C, H and N, and performing a maximum of two potato harvests on the such as water, air and solar radiation. Moreover, the lower NH+ 4 content
same parcel with a subsequent resting period (with cattle farming) was in the soils of the La Secreta agroecosystem relative to Buenos Aires
shown to have contributed to the decreased impact of farming practices could be explained by the lower OM contents in the former. The CEC
over the most complex and molecularly stable C (humic substances). was between 31.8 and 44.3 cmol kg−1, which corresponds to the
The C/N ratio is an estimator of the availability of OM as a nutrient high-CEC category (Galiano, 1991; ICA, 1992) and is well-correlated
source for plants, which indicates favourable mineralisation processes, with the high OM contents and andic characteristic of the studied soils.
so a high C/N value indicates lower rates of mineralisation The Ca and K contents significantly decreased due to potato and cat-
(Avellaneda et al., 2005). Thus, it is evident that soils under Páramo ex- tle farming, and this might have been caused by the successive nutrient
hibit lower mineralisation (greater humification) than soils under po- extraction by the crops and simultaneous nutrient fixation caused by
tato and cattle farming, but these differences were not statistically the organic-mineral complexes of the andosols (Hofstede, 1995).
significant, which suggests that the described farming processes do The P content showed a trend of potato cultivation N cattle farming N
not significantly affect the mineralisation and humification of soil OM Páramo, which might indicate the use of N:P:K fertiliser, but these differ-
with high molecular complexity. ences were not statistically significant, indicating that these practices
were not intensive in the area. The P content did not change with vari-
ations in altitude or sampling time, and the values were within the 6.9
to 34.5 cmol kg−1 range, indicating a low-to-medium content (Hanke,
Table 2
1991; ICA, 1992) that is characteristic of andic soils, which are known
Mean chemical properties for the evaluated factors (land use, season and farm) in Nevados
NNP in the El Bosque District.
for high phosphate fixation.
The MVA of the physicochemical variables (Fig. 2) showed an accu-
Factors TC TH TN C/N NH4 NO3 mulated variance of 63% for the first two axes. In this analysis, differ-
−1
% mg kg ences were observed in the behaviour of Páramo relative to potato
Land use n = 36 Páramo 9.4a 1.5a 0.5a 26.1a 36.7a 18.6a and cattle farming, which indicated land use-related differences in
Crop 7.7a 1.3a 0.4a 20.6a 15.1ab 17.7a physicochemical properties. According to the normalised eigenvector
Cattle farming 6.9a 1.3a 0.3a 20.0a 13.2b 15.6a 1, the most informative variables were Mg (−0.39), CEC (−0.37), OC
Season n = 36 Rainy 7.5a 1.2a 0.4a 23.3a 29.0a 22.1a
(−0.34), N (−0.34) and Ca (−0.34), and greater values were observed
Dry 8.7b 1.6b 0.4a 20.0b 14.3a 12.5b
Farm n = 36 Buenos Aires 9.0a 1.4a 0.4a 23.3a 28.6a 15.4a in Páramo soils relative to soils under potato and cattle farming. This re-
La Secreta 7.0a 1.4a 0.4a 20.0a 14.7b 19.2a sult is consistent with the greater conservation of OM, increased natural
Standard deviation 2.38 0.33 0.14 12.4 1.30 1.04 vegetation cover and lower disturbance in Páramo soils, all of which in-
TC, total carbon; TH, total hydrogen; TN, total nitrogen; and n, number of replicates. Differ- crease the stability of OM cycling and provide greater OC, CEC, N and
ent letters for each factor indicate statistically significant differences. gravimetric moisture content (Ɵg) compared to soils under potato
 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610 1605

Fig. 2. Principal component analysis of the physicochemical parameters of the studied soils from Nevados NNP in the El Bosque District. M, gravimetric moisture (Ɵg); D, bulk density;
WAD, mean weighted diameter; OC, organic carbon; and CEC, cation exchange capacity.

and cattle farming. The increased OM in soils may improve their physi-
cal and chemical properties, such as humidity, TN, CEC and aggregate
stability (López-Piñeiro et al., 2013), but soils under potato crops had
higher P contents (eigenvector 1:0.20), indicating the effect of chemical
fertilisation with P. Greater soil densities were observed with cattle
farming (eigenvector 1:0.25), which might indicate compaction pro-
cesses caused by trampling.
An analysis of the changes related to sampling season showed that
greater values of Mg, CEC, OC, N and Ca were observed during the dry
season, which is consistent with the results of the univariate analysis,
where greater erosion and nutrient leaching were evident during the
rainy season. The PCA did not indicate a specific trend in physicochem-
ical parameters as a function of the altitude of the farms.
The variables that highly correlated with each other were CEC and OC
(0.90), OC and N (0.86), Mg and Ca (0.86), Ɵg and Mg (0.85), CEC and N
(0.83) and CEC and Mg (0.83). However, inversely proportional relation-
ships were reported between OC and N and the P contents in soils, and
these might have been caused by increases in the use of fertiliser with
high P content and different levels of allophane, which reduces P avail-
ability through the increased formation of OM complexes that increase
P fixation (Henry et al., 2013). Moreover, overturning soil with a plough
dries out the soil surface and liberates many of the immobilised nutrients
in the edaphic environment (FEDEPAPA, MAVDT, CORPOBOYACÁ, and
HUMBOLDT, 2004) such as P, which might be encapsulated within the
organic-mineral complex of allophane and OM.
3.3. Enzymatic activity
β-glucosidase, phosphodiesterase and urease activities significantly
decreased in soils under potato and cattle farming relative to the Páramo
soil, but acid phosphatase and protease activities significantly increased
(Table 3). Alkaline phosphatase and dehydrogenase activities did not
show statistically significant differences.
The reduction in β-glucosidase activity associated with potato and
cattle farming is relevant because this enzyme is involved in catalysing
the hydrolysis and biodegradation of several glycosides in vegetable
residues (Ajwa and Tabatabai, 1994; Bakshi and Varma, 2011;
Martinez and Tabatabai, 1997), of which the final product is glucose,
an important source of energy for soil microorganisms (Bakshi and
Varma, 2011; Esen, 1993). Therefore, a decrease in β-glucosidase activ-
ity can indicate lower glucose liberation caused by the application of ag-
rochemicals, which might inhibit microbial activity. Such conditions
restrict the degradation of cellulosic compounds that are part of the
OM in the soil. In addition, lower enzymatic activity might be consid-
ered a slower process of C metabolism and indicate the rupture of glu-
cose dimers and decreased OM in the potato and cattle fields relative
to that of the Páramo. Such findings confirm reports that β-
glucosidase enzyme activity is sensitive to soil management practices
(V. Acosta-Martínez and Tabatabai, 2000; Bakshi and Varma, 2011; Li
et al., 2018; Madejón et al., 2001; Moghimian et al., 2017; Xie et al.,
2017).

Table 3
Mean enzymatic activity for the studied soils for the evaluated factors (land use, season and farm) in Nevados NNP in the El Bosque District.

Factors β-gluc Pac Palk Pd Ure Pro Deh

μg pNP g−1 ss h−1 μg N-NH+

4 g
−1
ss 2 μg tyr g−1 ss 2 h−1 μg TPF g−1 ss 16 h−1
h−1

Land Use n = 54 Páramo 299.6a 752.4a 86.4a 18.0a 53.4a 732.2a 218.3a
Crop 220.4b 788.9ab 80.6a 12.4b 36.8a 886.8b 219.3a
Cattle farming 215.6b 851.5b 66.0a 12.9b 0.9b 866.2b 5.3a
Season n = 54 Rainy 234.2a 785.3a 74.3a 13.3a 34.0a 749.4a 337.2a
Dry 256.1a 805.2a 81.2a 15.5b 26.9a 904.2b 44.2a
Farm n = 54 Buenos Aires 248.4b 907.0a 70.5a 13.8a 43.5a 785.5a 2.3a
El Edén 302.3a 852.6a 84.4a 15.0a 39.8a 853.2a 147.8a
La Secreta 184.7c 626.2b 78.4a 14.3a 8.0b 841.6a 289.5a
Standard deviation 12.3 39.8 3.89 0.72 1.52 41.3 7.33

β-gluc, β-glucosidase; Pac, acid phosphatase; Palk, alkaline phosphatase; Pd, phosphodiesterase; Ure, urease; Pro, protease; Deh, dehydrogenase; and n, number of replicates. Different
letters for each factor indicate statistically significant differences.
1606 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610
The significant decrease in phosphodiesterase activity associated
with cattle farming and (non-significant) reduction in alkaline phos-
phatase indicates that the alkaline conditions during potato and cattle
farming decrease the conversion processes of organic phosphodiesters
and OM to their inorganic forms. The decreased availability of P in soil
is caused by this enzyme because phosphatases are capable of catalysing
the hydrolysis of esters and phosphoric acid anhydrides (Bakshi and
Varma, 2011). Additionally, the decrease in the activities of phosphodi-
esterase and alkaline phosphatase might be caused by the lower OM
content in soils under potato and cattle farming as well as by the re-
duced microbial activity caused by the application of agrochemicals.
Progressive declines in microbial activity have been reported with in-
creased incubation periods for phosphatase activity in the presence of
chlorpyrifos (Lorsban applied in potato cultivation). Similar responses
have been observed in the presence of methyl parathion, dichlorvos
and methomyl (Gianfreda and Rao, 2011; Madhuri and Rangaswamy,
2002; Rani et al., 2008). Decreases in alkaline phosphatase might indi-
cate less-efficient root-symbiotic colonisation processes because several
studies have shown that this enzyme is primarily produced in the roots
after mycorrhizae colonisation. Therefore, alkaline phosphatase has
been proposed as an indicator of the efficiency of root-symbiotic coloni-
sation (Bakshi and Varma, 2011; Tisserant et al., 1993). All the above re-
sults confirm that phosphatases differ according to soil coverage and
management practices (Bakshi and Varma, 2011; Li et al., 2018;
Moghimian et al., 2017; Ndakidemi, 2006; Wright and Reddy, 2001;
Xie et al., 2017).
The decrease in the activities of phosphodiesterase and alkaline
phosphatase is consistent with most of the studies in the literature.
However, an opposite behaviour was observed for acid phosphatase
(increased in potato and cattle fields), which is inconsistent with previ-
ous reports suggesting that an increase in the P content of potato fields
under rotation with cattle farming caused by the application of N:P:K
fertilisers elevates the P content in soil and inhibits phosphatase activity
(Das and Varma, 2011). In contrast, soil P deficiencies (in the Páramo
soils, which do not receive extra P) did not cause an increase in the se-
cretion of acid phosphatase by plant roots to improve the solubilisation
of fixed nutrients, as reported by (Das and Varma, 2011). Thus, it has
been proposed that an increase in phosphatase enzymes by plant
roots and microorganisms may be induced when P is limited. Conse-
quently, an increase in acid phosphatase activity may reflect high de-
mand for this macronutrient (Salazar et al., 2011) and may result from
potato and cattle farming through the increased microbial activity,
which promotes the growth of microorganisms under high nutrient
availability. However, the behaviour of this enzyme in the studied con-
ditions remains unclear.
The degradation of soil phosphodiester compounds (phosphodies-
terase) and organic P in alkaline conditions (alkaline phosphatase)
may be greater in OM that has suffered less disturbance (Páramo) and
may be inhibited under potato and cattle farming because of the addi-
tion of pesticides. However, in the case of organic P degradation under
acidic conditions (acid phosphatase), which is more common in acidic
soils, the activity of this enzyme is prioritised to produce organic P,
which is in high demand during potato and cattle farming. In this case,
fertiliser application might be used to promote microbial activity.
Urease activity showed a trend of Páramo N potato cultivation
N cattle farming, and significant differences were observed between cat-
tle farming and the other two land uses. This may have been caused by
the inhibition of microbes as result of agrochemical application during
potato cultivation in rotation with pastures. Soil enzymatic activities
have been reported to be inhibited by N fertilisation (Aon et al., 2001;
Karaca et al., 2011), and urease activities have been reported to decrease
due to high sensitivity to chlorpyrifos (Gianfreda and Rao, 2011).
The protease activity significantly increased in soils under potato
and cattle farming. This was a similar trend to that reported for acid
phosphatase activity and indicates that these agricultural practices pro-
mote the degradation of protein residues, which is most likely due to
the increase in microbial activity caused by fertilisation associated
with potato cultivation. However, protease activity exhibited an oppo-
site behaviour to that of urease. Similar results have been observed in
bacterial morphotype consortiums, where the production of
oligopeptides from proteins may have been greater than the hydrolysis
of urea or urea-type substrates and the production of their reaction
products, CO2 and NH3 (Avellaneda-Torres et al., 2012).
Statistically significant differences related to land use, sampling time
or farm altitude were not reported for dehydrogenase activity. The ac-
tivities of β-glucosidase, acid phosphatase, alkaline phosphatase, phos-
phodiesterase and protease were greater in the dry season than in
rainy season, which is consistent with the higher OC content reported
for the dry season. However, these differences were statistically signifi-
cant only for phosphodiesterase and protease. In addition, β-
glucosidase, acid phosphatase and urease activities statistically signifi-
cantly decreased on the La Secreta farm compared to the other two
farms, a behaviour that is attributable to differences in OM (higher-alti-
tude farms showed greater OC content).
The MVA of enzymatic activities showed an accumulated variance of
54.2% for the first two axes and a variance of 71.8% for the first three
axes. Therefore, graphic representations of axes 1 and 2 (Fig. 3-A) as
well as 1 and 3 (Fig. 3-B) were analysed, and differences were observed
among the enzymatic behaviours in soil from the Páramo and potato
and cattle fields. Fig. 3-A (axes 1 and 2) shows that phosphodiesterase
and alkaline phosphatase activities were greater in the Páramo soil, a
trend that is confirmed in Fig. 3-B (axes 1 and 3). In addition, Fig. 3-A
and B show that the acid phosphatase and protease activities were
higher in soils under potato and cattle farming. This might indicate
that the activities of several enzymes involved in the same geochemical
cycle are not necessarily synergistic but have an inverse relationship, as
previously reported by Avellaneda-Torres et al. (2012). The contribu-
tions of the variables to the variance according to the normalised eigen-
vector 1 were as follows: phosphodiesterase (0.33), β-glucosidase
(0.33), acid phosphatase (0.43), alkaline phosphatase (0.33), urea (−
0.01 eigenvector 1 and 0.60 eigenvector 2), protease (0.44) and dehy-
drogenase (−0.52).
An analysis of the changes associated with season in Fig. 3-A and B
shows that acid and alkaline phosphatase, β-glucosidase, protease and
phosphodiesterase activities were increased during the dry season.
This may have been caused by microbial activity being stimulated by
the increase in OM. The activity of multiple enzymes is correlated with
the amount of OM because this parameter affects soil microbial mass
and moisture. Additionally, positive correlations have been reported be-
tween OM and the activity of β-glucosidase, proteases and phospha-
tases (Gispert et al., 2013), and seasonal changes in enzymatic
activities have been observed, suggesting that fluctuations in enzymatic
activities occur as a function of seasonal changes and environmental
conditions, such as soil temperature and moisture content (Yuan et al.,
2012).
A PCA of the main enzymatic activities did not indicate a specific
trend related to altitude. In general, high correlations were reported be-
tween phosphodiesterase, alkaline phosphatase and β-glucosidase and
between protease and acid phosphatase.
3.4. Relationship between physicochemical parameters and enzymatic
activity
The MVA of enzymatic activity showed an accumulated variance of
50.3% for the first two axes and a variance of 62.1% for the first three,
so the graphic representations of axes 1 and 2 (Fig. 4-A) and 1 and 3
(Fig. 4-B) were analysed. The differences in the behaviour of physico-
chemical variables and enzymatic activity among the Páramo and po-
tato and cattle field soils were analysed (Fig. 4-B), and the results
confirmed the PCA results for the physicochemical parameters and en-
zymatic activities. A global analysis was performed according to the nor-
malised eigenvector 1, and the most informative variables were as
 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610 1607

Fig. 3. Principal component analysis of the enzymatic activity in the studied soils from Nevados NNP in the El Bosque District. Glu, β-glucosidase; AcP, acid phosphatase; AlP, alkaline
phosphatase; Pd, phosphodiesterase; Ure, urease; Pro, protease; and Deh, dehydrogenase. A. Axes 1 and 2. B. Axes 1 and 3.

follows: Mg (0.36), CEC (0.34), Ca (0.32), TN (0.31), OC (0.30), phospho-
diesterase (0.24) and β-glucosidase (0.21). These variables increased in
the Páramo soils relative to those under potato and cattle farming,
which might be related to the loss of OM resulting from the loss of
plant cover and cultural labour associated with the potato-pasture sys-
tem. Several studies have confirmed correlations between the activities
of these enzymes and OC (Dick et al., 1988; Eivazi and Tabatabai, 1990;
Frankenberger and Tabatabai, 1991; Santrucková et al., 2004) (Li et al.,
2018; Moghimian et al., 2017; Xie et al., 2017).
When natural systems are converted to agricultural systems, the bi-
ological properties of the soil are modified, resulting in higher enzy-
matic activities (β-glucosidase, β-glucosaminidase, arylamidase, acid
and alkaline phosphatase, phosphodiesterase and arylsulfatase) in con-
served areas compared to agricultural areas (Karaca et al., 2011). These
results are consistent with those of several studies that found a decrease
in enzymatic activities in cultivated soils compared with non-cultivated
or less-disturbed soils (Acosta-Martínez et al., 2008; Bonanomi et al.,
2011; Gianfreda et al., 2005). Cultivation systems also differentially af-
fect the behaviour of soil enzymes, and dehydrogenase, acid and alka-
line phosphatase activities, microbial C biomass, and N levels have
been found to be lower under a monoculture system than an organic
and a crop rotation system (Benintende et al., 2008; Gajda and
Martyniuk, 2005; Karaca et al., 2011). Moreover, it has been reported
that plots fertilised with compost showed increased enzymatic activity
(dehydrogenase, protease, β-glucosidase, and alkaline phosphatase)
(Melero et al., 2007).
However, differences in the patterns of physicochemical parameters
and enzymatic activities related to climatic conditions were also ob-
served. (Nearing et al., 2005) reported changes in precipitation patterns
and extreme climatic events over the last century in Colombia, and
Otero et al. (2011) indicated that regional climatic change may have a
significant influence and cause an increase in the rate of soil erosion
globally if conservation measures are not implemented to mitigate
damage caused by disturbances to the soil.
The greatest correlations between enzymatic activity and physico-
chemical parameters were between β-glucosidase and Ca (0.67), phos-
phodiesterase and Ca (0.56), phosphodiesterase and K (0.58) and
phosphodiesterase and CEC (0.68), although the highest correlations
have been proposed to be between OC and different enzymatic activities
(Bonanomi et al., 2011; Gispert et al., 2013; Yuan et al., 2012). Similar
correlations were detected in the present study (0.50 on average).
4. Conclusions
Five (CO, Ca, K, CEC and NH4) of the 16 chemical parameters
analysed showed statistically significant differences related to potato
cultivation and cattle farming in the Páramo, and OC was the main indi-
cator. Five (β-glucosidase, phosphodiesterase, urease, acid phosphatase
1608 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610

Fig. 4. Principal component analysis of the enzymatic activity and physicochemical parameters of the studied soils from Nevados NNP in the El Bosque District. Glu, β-glucosidase; AcP, acid
phosphatase; AlP, alkaline phosphatase; Pd, phosphodiesterase; Ure, urease; Pro, protease; and Deh, dehydrogenase. M, gravimetric moisture (Ɵg); D, bulk density; WAD, mean weighted
diameter; OC, organic carbon; and CEC, cation exchange capacity. A. Axes 1 and 2. B. Axes 1 and 3.

and protease) of the seven enzymes studied showed statistically signif-
icant differences due to potato cultivation and cattle ranching. Phospho-
diesterase, alkaline phosphatase and β-glucosidase activities decreased,
and protease and acid phosphatase activities increased.
An analysis of physicochemical characteristics and enzymatic activi-
ties with respect to season found statistically significant differences in 7
(CO, N, CEC, TC, TH, C/N and NO3) of 19 physicochemical characteristics
and 2 (phosphodiesterase and protease) of 7 enzyme activities. In gen-
eral, the highest OC content, CEC and enzymatic activity were detected
in the dry season. No unique trend related to the effect of altitude was
detected in the sampled farms. The evaluated physical parameters did
not show statistically significant differences among the studied factors
(land use, season and farm).
These results indicate the importance of participation among com-
munities, institutions and academia to implement processes that will
lead to changes in the agricultural practices of the El Bosque District
and improve the physicochemical properties and stabilise the enzy-
matic processes of the soil. Thus, implementing ecological models asso-
ciated with potato farming, agro-silvopastoral systems, no-tillage
systems, crop rotation, and ecological agriculture may lead to
improvements in soil physicochemical characteristics through the
management of OM and edaphic biodiversity. To implement these rec-
ommendations, issues recognised in previous studies must be acknowl-
edged, such as developing community management plans through state
funding, and agroecological research and agricultural models must be
developed (Avellaneda-Torres et al., 2014).
Acknowledgements
This research was funded by Colciencias (Contract 246-2011) and
developed under Contract No 15 of 2008 of the Ministerio de
Ambiente, Vivienda y Desarrollo Territorial (MAVDT), which
allowed access to genetic resources. Research permits were granted
by Unidad Administrativa Especial del Sistema de Parques
Nacionales Naturales (UAESPNN; DTNO-N-20/2007). We would also
like to thank the Colombian Center for the Genomics and Bioinfor-
matics of Extreme Environments (GEBIX) and the National Univer-
sity of Colombia for funding this research. Special thanks are
extended to the farmers from the El Bosque District, Rosita Mejía
and Luz Andrea Gordillo.
 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610
References
Acosta-Martínez, V., Tabatabai, M.A., 2000. Enzyme activities in a limed agricultural soil.
Biol. Fertil. Soils 31 (1), 85–91.
Acosta-Martínez, V., Cruz, L., Sotomayor-Ramírez, D., Pérez-Alegría, L., 2007. Enzyme ac-
tivities as affected by soil properties and land use in a tropical watershed. Appl. Soil
Ecol. 35 (1), 35–45.
Acosta-Martínez, V., Acosta-Mercado, D., Sotomayor-Ramírez, D., Cruz-Rodríguez, L.,
2008. Microbial communities and enzymatic activities under different management
in semiarid soils. Appl. Soil Ecol. 38 (3):249–260. https://doi.org/10.1016/j.
apsoil.2007.10.012.
Ajwa, H.A., Tabatabai, M.A., 1994. Decomposition of different organic materials in soils.
Biol. Fertil. Soils 18 (3):175–182. https://doi.org/10.1007/bf00647664.
Alef, K., Nannipieri, P., 1995. Methods in Applied Soil Microbiology and Biochemistry. Ac-
ademic Press. Harcourt & Company, London.
Aon, M.A., Cabello, M.N., Sarena, D.E., Colaneri, A.C., Franco, M.G., Burgos, J.L., Cortassa, S.,
2001. I. Spatio-temporal patterns of soil microbial and enzymatic activities in an ag-
ricultural soil. Appl. Soil Ecol. 18 (3):239–254. https://doi.org/10.1016/S0929-1393
(01)00153-6.
Avellaneda, L.M., Lozano de Yunda, A., Zamudio, A.M., 2005. Efecto del uso y la cobertura
del suelo sobre el perfil de polidispersidad de ácidos húmicos extraídos de un andisol
del departamento de Caldas, Colombia. Revista Colombiana de Química 34, 189–200.
Avellaneda-Torres, L.M., Melgarejo Muñoz, L.M., Narváez Cuenca, C.E., Sánchez Nieves, J.,
2012. Actividades Enzimáticas en Consorcios Bacterianos de Suelos Bajo Cultivo de
Papa con Manejo Convencional y Bajo Pastizal. Revista Facultad Nacional de
Agronomía, Medellín. 65, pp. 6349–6360.
Avellaneda-Torres, L.M., Torres, E., León, T., 2014. Agricultura y vida en el páramo: una
mirada desde la vereda El Bosque (Parque Nacional Natural de Los Nevados).
Cuadernos de Desarrollo Rural 11 (73), 105–128.
Bakshi, M., Varma, A., 2011. Soil enzyme: the state-of-art. In: Shukla, G., Varma, A. (Eds.),
Soil Enzymology. vol. 22. Springer, Berlin Heidelberg, pp. 1–23.
van Beelen, P., Doelman, P., 1997. Significance and application of microbial toxicity tests
in assessing ecotoxicological risks of contaminants in soil and sediment.
Chemosphere 34 (3):455–499. https://doi.org/10.1016/S0045-6535(96)00388-8.
Benintende, S.M., Benintende, M.C., Sterren, M.A., De Battista, J.J., 2008. Soil microbiolog-
ical indicators of soil quality in four rice rotations systems. Ecol. Indic. 8 (5), 704–708.
Bojko, O., Kabala, C., 2016. Transformation of physicochemical soil properties along a
mountain slope due to land management and climate changes — a case study from
the Karkonosze Mountains, SW Poland. Catena 140:43–54. https://doi.org/10.1016/
j.catena.2016.01.015.
Bonanomi, G., D'Ascoli, R., Antignani, V., Capodilupo, M., Cozzolino, L., Marzaioli, R., ...
Zoina, A., 2011. Assessing soil quality under intensive cultivation and tree orchards
in Southern Italy. Appl. Soil Ecol. 47 (3):184–194. https://doi.org/10.1016/j.
apsoil.2010.12.007.
Browman, M.G., Tabatabai, M.A., 1978. Phosphodiesterase activity of soils. Soil Sci. Soc.
Am. J. 42 (2):284–290. https://doi.org/10.2136/sssaj1978.03615995004200020016x.
Buytaert, W., Deckers, J., Wyseure, G., 2007. Regional variability of volcanic ash soils in
South Ecuador: the relation with parent material, climate and land use. Catena 70
(2):143–154. https://doi.org/10.1016/j.catena.2006.08.003.
Cleef, A.M., 1981. The vegetation of the páramos of the Colombian Cordillera Oriental.
Dissertationes Botanicae. Vaduz. J. Cramer 61, 320–321.
Das, S., Varma, A., 2011. Role of enzymes in maintaining soil health. In: Shukla, G., Varma,
A. (Eds.), Soil Enzymology. vol. 22. Springer, Berlin Heidelberg, pp. 25–42.
Dick, R.P., 1994. Soil enzyme activities as indicators of soil quality. In: Doran, J.W.,
Coleman, D.C., Bezdicek, D.F., Steward, B.A. (Eds.), Defining Soil Quality for a Sustain-
able Environment. American Society of Agronomy, Madison, WI, pp. 107–124.
Dick, R.P., Rasmussen, P.E., Kerle, E.A., 1988. Influence of long-term residue management
on soil enzyme activities in relation to soil chemical properties of a wheat-fallow sys-
tem. Biol. Fertil. Soils 6 (2), 159–164.
Eivazi, F., Tabatabai, M.A., 1988. Glucosidases and galactosidases in soils. Soil Biol.
Biochem. 20 (5), 601–606.
Eivazi, F., Tabatabai, M.A., 1990. Factors affecting glucosidase and galactosidase activities
in soils. Soil Biol. Biochem. 22 (7):891–897. https://doi.org/10.1016/0038-0717(90)
90126-K.
Esen, A., 1993. b-Glucosidases-biochemistry and Molecular Biology. Washington, DC: ACS
Symposium Series. 533. American Chemical Society.
FEDEPAPA, MAVDT, CORPOBOYACÁ, & HUMBOLDT, I, 2004. Guía ambiental para el cultivo
de papa. FEDEPAPA, MAVDT, Bogotá. Colombia.
Frankenberger, W., Tabatabai, M., 1991. Factors affecting L-glutaminase activity in soils.
Soil Biol. Biochem. 23.
Gajda, A., Martyniuk, S., 2005. Microbial biomass C and N and activity of enzymes in soil
under winter wheat grown in different crop management systems. Pol. J. Environ.
Stud. 14 (2), 159–163.
Galiano, F., 1991. Capacidad de intercambio catiónico y aniónico bases de cambio y
saturaciones. In: Silva, F. (Ed.), Fundamentos para la interpretación de análisis de
suelos, plantas y aguas para riego. Sociedad Colombiana de la Ciencia del Suelo,
Bogotá, pp. 164–185.
Garcia, C., Hernandez, T., Costa, F., Ceccanti, C., Gianni, A., 1993. Hydrolases in the organic
matter fractions of sewage sludge: chang es with composting. Bioresour. Technol. 45,
47–52.
Gianfreda, L., Rao, M., 2011. The influence of pesticides on soil enzymes. In: Shukla, G.,
Varma, A. (Eds.), Soil Enzymology. vol. 22. Springer, Berlin Heidelberg, pp. 293–312.
Gianfreda, L., Antonietta Rao, M., Piotrowska, A., Palumbo, G., Colombo, C., 2005. Soil en-
zyme activities as affected by anthropogenic alterations: intensive agricultural prac-
tices and organic pollution. Sci. Total Environ. 341 (1–3):265–279. https://doi.org/
10.1016/j.scitotenv.2004.10.005.
1609
Gispert, M., Emran, M., Pardini, G., Doni, S., Ceccanti, B., 2013. The impact of land manage-
ment and abandonment on soil enzymatic activity, glomalin content and aggregate sta-
bility. Geoderma 202–203 (0):51–61. https://doi.org/10.1016/j.geoderma.2013.03.012.
de Groot, R.S., Wilson, M.A., Boumans, R.M.J., 2002. A typology for the classification, de-
scription and valuation of ecosystem functions, goods and services. Ecol. Econ. 41
(3):393–408. https://doi.org/10.1016/S0921-8009(02)00089-7.
Hanke, F., 1991. Los elementos mayores N, P y k en el suelo. In: Silva, F. (Ed.),
Fundamentos para la interpretación de análisis de suelos, plantas y aguas para
riego. Sociedad Colombiana de la Ciencia del Suelo, Bogotá, pp. 186–196.
Henry, A., Mabit, L., Jaramillo, R.E., Cartagena, Y., Lynch, J.P., 2013. Land use effects on ero-
sion and carbon storage of the Río Chimbo watershed, Ecuador. Plant Soil 367 (1–2):
477–491. https://doi.org/10.1007/s11104-012-1478-y.
Hofstede, R.M., 1995. The effects of grazing and burning on soil and plant nutrient con-
centrations in Colombian páramo grasslands. Plant Soil 173 (1):111–132. https://
doi.org/10.1007/bf00155524.
ICA, 1992. Fertilización en diversos cultivos. 5a ed. Instituto Colombiano Agropecuario,
Bogotá.
IGAC, 2004. Estudio General de Suelos del Departamento de Risaralda. Instituto
Geográfico Agustín Codazzi, Bogotá.
IGAC, 2006. Métodos analíticos del laboratorio de suelos. 6a ed. Instituto Geográfico
Agustin Codazzi, Bogotá.
IGAC, 2007. Manual de campo para levantamiento de suelos y tierras. Instituto Geográfico
Agustin Codazzi, Bogotá.
Jaramillo, J., Daniel, F., 2002. Introducción a la Ciencia del Suelo. Universidad Nacional de
Colombia Facultad de Ciencias, Medellín.
Karaca, A., Cetin, S., Turgay, O., Kizilkaya, R., 2011. Soil enzymes as indication of soil qual-
ity. In: Shukla, G., Varma, A. (Eds.), Soil Enzymology. vol. 22. Springer, Berlin Heidel-
berg, pp. 119–148.
Ladd, J.N., Butler, J.H.A., 1972. Short-term assays of soil proteolytic enzyme activities
using proteins and dipeptide derivatives as substrates. Soil Biol. Biochem. 4 (1),
19–30.
Lal, R., 2004. Soil carbon sequestration impacts on global climate change and food secu-
rity. Science 304 (5677):1623–1627. https://doi.org/10.1126/science.1097396.
Li, J., Tong, X., Awasthi, M.K., Wu, F., Ha, S., Ma, J., ... He, C., 2018. Dynamics of soil microbial
biomass and enzyme activities along a chronosequence of desertified land revegeta-
tion. Ecol. Eng. 111:22–30. https://doi.org/10.1016/j.ecoleng.2017.11.006.
Liu, D., Huang, Y., An, S., Sun, H., Bhople, P., & Chen, Z. Soil physicochemical and microbial
characteristics of contrasting land-use types along soil depth gradients. Catena doi:
https://doi.org/10.1016/j.catena.2017.10.028.
López-Bellido, R.J., Fontán, J.M., López-Bellido, F.J., López-Bellido, L., 2010. Carbon se-
questration by tillage, rotation, and nitrogen fertilization in a Mediterranean
vertisol All rights reserved. No part of this periodical may be reproduced or
transmitted in any form or by any means, electronic or mechanical, including
photocopying, recording, or any information storage and retrieval system, with-
out permission in writing from the publisher. Agron. J. 102 (1):310–318. https://
doi.org/10.2134/agronj2009.0165.
López-Piñeiro, A., Muñoz, A., Zamora, E., Ramírez, M., 2013. Influence of the man-
agement regime and phenological state of the vines on the physicochemical
properties and the seasonal fluctuations of the microorganisms in a vineyard
soil under semi-arid conditions. Soil Tillage Res. 126 (0):119–126. https://
doi.org/10.1016/j.still.2012.09.007.
Luteyn, J., 1992. Páramos, why study them? In: Balslev, H., Luteyn, J.L. (Eds.), Paramo; an
Andean Ecosystem under Human Influence. Academic Press, London, pp. 1–14
Madejón, E., Burgos, P., López, R., Cabrera, F., 2001. Soil enzymatic response to addition of
heavy metals with organic residues. Biol. Fertil. Soils 34 (3):144–150. https://doi.org/
10.1007/s003740100379.
Madhuri, R.J., Rangaswamy, V., 2002. Influence of selected insecticides on phosphatase ac-
tivity in groundnut (Arachis hypogeae L.) soils. J. Environ. Biol. 23 (4), 393–397.
Marcinkeviciene, A., Boguzas, V., Balnyte, S., Pupaliene, R., Velicka, R., 2013. Influence of
crop rotation, intermediate crops, and organic fertilizers on the soil enzymatic activ-
ity and humus content in organic farming systems. Eurasian Soil Sci. 46 (2):198–203.
https://doi.org/10.1134/s1064229313020105.
Martinez, C.E., Tabatabai, M.A., 1997. Decomposition of biotechnology by-
products in soils. J. Environ. Qual. 26 (3):625–632. https://doi.org/10.2134/
jeq1997.00472425002600030006x.
Melero, S., Madejón, E., Ruiz, J.C., Herencia, J.F., 2007. Chemical and biochemical properties
of a clay soil under dryland agriculture system as affected by organic fertilization. Eur.
J. Agron. 26 (3), 327–334.
Melero, S., López-Bellido, R.J., López-Bellido, L., Muñoz-Romero, V., Moreno, F., Murillo,
J.M., 2011. Long-term effect of tillage, rotation and nitrogen fertiliser on soil quality
in a Mediterranean vertisol. Soil Tillage Res. 114 (2):97–107. https://doi.org/
10.1016/j.still.2011.04.007.
Moghimian, N., Hosseini, S.M., Kooch, Y., Darki, B.Z., 2017. Impacts of changes in land use/
cover on soil microbial and enzyme activities. Catena 157 (Supplement C):407–414.
https://doi.org/10.1016/j.catena.2017.06.003.
Monasterio, M., Sarmiento, L., 1991. Adaptive radiation of Espeletia in the cold andean
tropics. Trends Ecol. Evol. 6, 387–391.
Ndakidemi, P.A., 2006. Manipulating legume/cereal mixtures to optimize the above and
below ground interactions in the traditional African cropping systems. Afr.
J. Biotechnol. 5, 2526–2533.
Nearing, M., Jetten, V., Baffaut, C., Cerdan, O., Couturier, A., Hernandez, M., ... Renschler, C.,
2005. Modeling response of soil erosion and runoff to changes in precipitation and
cover. Catena 61 (2), 131–154.
Öhlinger, R., 1996. Dehydrogenase activity with the substrate TTC. In: Schinner, F.,
Öhlinger, R., Kandeler, E., Margasin, R. (Eds.), Methods in Soil Biology. Springer, Ber-
lin, pp. 241–243.
1610 L.M. Avellaneda-Torres et al. / Science of the Total Environment 631–632 (2018) 1600–1610
Otero, J.D., Figueroa, A., Muñoz, F.A., Peña, M.R., 2011. Loss of soil and nutrients by surface
runoff in two agro-ecosystems within an Andean paramo area. Ecol. Eng. 37 (12):
2035–2043. https://doi.org/10.1016/j.ecoleng.2011.08.001.
PNNN, 2010. Restauración ecológica en páramos del Parque Nacional Natural de Los
Nevados. Editorial Andina.
Post, W.M., Kwon, K.C., 2000. Soil carbon sequestration and land-use change: processes
and potential. Glob. Chang. Biol. 6 (3):317–327. https://doi.org/10.1046/j.1365-
2486.2000.00308.x.
Poulenard, J., Podwojewski, P., Janeau, J.-L., Collinet, J., 2001. Runoff and soil erosion under
rainfall simulation of Andisols from the Ecuadorian Páramo: effect of tillage and burn-
ing. Catena 45 (3):185–207. https://doi.org/10.1016/S0341-8162(01)00148-5.
Rani, M., Lakshmi, K., Devi, P., Madhuri, R., Devi, S., Jyothi, K., 2008. Impact of chlorpyrifos
on soil enzyme activities in agricultural soil. Asian J. Microbiol. Biotechnol. Environ.
Sci. 10, 295–300.
Sainju, U.M., Whitehead, W.F., Singh, B.P., 2003. Agricultural management practices to
sustain crop yields and improve soil and environmental qualities. TheScientificWorld
Journal 3:768–789. https://doi.org/10.1100/tsw.2003.62.
Salazar, S., Sánchez, L.E., Alvarez, J., Valverde, A., Galindo, P., Igual, J.M., ... Santa-Regina, I., 2011.
Correlation among soil enzyme activities under different forest system management
practices. Ecol. Eng. 37 (8):1123–1131. https://doi.org/10.1016/j.ecoleng.2011.02.007.
Santrucková, H., Vrba, J., Picek, T., Kopácek, J., 2004. Soil biochemical activity and phos-
phorus transformations and losses from acidified forest soils. Soil Biol. Biochem. 36
(10), 1569–1576.
Singh, A.K., Rai, A., Singh, N., 2016. Effect of long term land use systems on fractions of
glomalin and soil organic carbon in the Indo-Gangetic plain. Geoderma 277 (Supple-
ment C):41–50. https://doi.org/10.1016/j.geoderma.2016.05.004.
Six, J., Elliott, E.T., Paustian, K., Doran, J.W., 1998. Aggregation and soil organic matter ac-
cumulation in cultivated and native grassland soils. Soil Sci. Soc. Am. J. 62 (5):
1367–1377. https://doi.org/10.2136/sssaj1998.03615995006200050032x.
SSS, 2010. Keys to Soil Taxonomy. 11a ed. United States Department of Agriculture Natu-
ral Resources Conservation Service.
Svirskene, A., 2003. Microbiological and biochemical indicators of anthropogenic impacts
on soils. Eurasian soil Sci 36 (2), 192–200.
Tabatabai, M., 1994. Enzymes. In: Weawer, R., Augle, S., Bottomly, P., Bezdicek, D., Smith,
S., Tabatabai, A., Wollum, A. (Eds.), Methods of Soil Analysis. Microbiological and
Biochemical Properties. Soil Science Society of America, Madison, pp. 775–833 (Part
772., N°775).
Tabatabai, M.A., Bremner, J.M., 1969. Use of p-nitrophenyl phosphate for assay of soil
phosphatase activity. Soil Biol. Biochem. 1 (4), 301–307.
Tisserant, B., Gianinazzi-Pearson, V., Gianinazzi, S., Gollotte, A., 1993. In planta histochem-
ical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular
mycorrhizal infections. Mycol. Res. 97 (2):245–250. https://doi.org/10.1016/S0953-
7562(09)80248-7.
Trasar-Cepeda, C., Leirós, M.C., Seoane, S., Gil-Sotres, F., 2000. Limitations of soil enzymes
as indicators of soil pollution. Soil Biol. Biochem. 32 (13):1867–1875. https://doi.org/
10.1016/S0038-0717(00)00160-7.
Van Reeuwijk, L.P., 1989. Andosols. In: Driessen, P.M., Dukdal, R. (Eds.), Lecture Notes on
the Major Soils of the World. Pudoc, Wageningen, pp. 47–54.
Wada, K., 1980. Mineral characteristics of andisols. In: Theng, B.K.G. (Ed.), Soils with Var-
iable Charge. Offset Publishers, Palmerston North, pp. 87–107.
Wright, A.L., Reddy, K.R., 2001. Phosphorus loading effects on extracellular enzyme activ-
ity in Everglades wetland soils. Soil Sci. Soc. Am. J. 65 (2):588–595. https://doi.org/
10.2136/sssaj2001.652588x.
Xie, X., Pu, L., Wang, Q., Zhu, M., Xu, Y., Zhang, M., 2017. Response of soil physicochemical
properties and enzyme activities to long-term reclamation of coastal saline soil, East-
ern China. Sci. Total Environ. 607–608:1419–1427. https://doi.org/10.1016/j.
scitotenv.2017.05.185.
Xu, M., Li, Q., Wilson, G., 2016. Degradation of soil physicochemical quality by ephemeral
gully erosion on sloping cropland of the hilly Loess Plateau, China. Soil Tillage Res.
155:9–18. https://doi.org/10.1016/j.still.2015.07.012.
Yuan, J., Ouyang, Z., Zheng, H., Xu, W., 2012. Effects of different grassland restoration ap-
proaches on soil properties in the southeastern Horqin sandy land, northern China.
Appl. Soil Ecol. 61 (0):34–39. https://doi.org/10.1016/j.apsoil.2012.04.003.
Yusong, D., Shuwen, D., Dong, X., Chongfa, C., 2017. Soil erodibility and physicochemical
properties of alluvial fan of collapsing gullies in South China. Pedosphere https://
doi.org/10.1016/S1002-0160(15)60105-9.
Zhu, G.-y., Deng, L., Zhang, X.-b., Shangguan, Z.-p., 2016. Effects of grazing exclusion on
plant community and soil physicochemical properties in a desert steppe on the Loess
Plateau, China. Ecol. Eng. 90:372–381. https://doi.org/10.1016/j.ecoleng.2016.02.001.