water

Article
Impact of Changes of Land Use on Water Quality,
from Tropical Forest to Anthropogenic Occupation:
A Multivariate Approach
Alexis Joseph Rodríguez-Romero 1 , Axel Eduardo Rico-Sánchez 1 , Erick Mendoza-Martínez 1 ,
Andrea Gómez-Ruiz 1 , Jacinto Elías Sedeño-Díaz 2 and Eugenia López-López 1, *
1 Laboratorio de Evaluación de la Salud de los ecosistemas Acuáticos, Instituto Politécnico Nacional,
Prolongación de Carpio y Plan de Ayala 11340, 07738 Ciudad de Mexico, Mexico;
[email protected] (A.J.R.-R.); [email protected] (A.E.R.-S.);
[email protected] (E.M.-M.); [email protected] (A.G.-R.)
2 Coordinación Politécnica para la Sustentabilidad, Instituto Politécnico Nacional,
Instituto Politécnico Nacional, 07738 Ciudad de Mexico, Mexico; [email protected]
* Correspondence: [email protected] or [email protected]; Tel.: +52 57296000 (ext. 62328)




Received: 6 September 2018; Accepted: 23 October 2018; Published: 26 October 2018


Abstract: Worldwide, it is acknowledged that changes of land use influence water quality; however,
in tropical forests, the relationship between land use and water quality is still poorly understood.
This study assessed spatial and seasonal variations in water quality, and the relationship between
water quality and changes of land use in the Bobos-Nautla River, whose upper course runs across a
patch of a tropical cloud forest. Spatial and seasonal variations in water quality and land use were
assessed with multivariate tools. A cluster analysis, as well as a Principal Component Analysis
(PCA-3D), identified three groups of sites: (1) an upper portion, which showed the best water quality
and the broadest natural vegetation coverage; (2) a middle course, with high nitrogen and phosphorus
concentrations associated with extensive agricultural uses; and (3) a lower course, characterized
by the highest levels of total and fecal coliforms, as well as ammonia nitrogen, associated with the
highest percentage of urbanization and human settlements. Our findings demonstrate the impact of
changes of land use on water quality of rivers running through cloud forests in tropical zones, which
are currently endangered ecosystems.

Keywords: cloud forest; natural protected area; multivariate analysis; landscape; WQI; principal
component analysis in 3D

1. Introduction
It is recognized that climate change is a process that evolves slowly, reflecting a set of modifications
that are evident in the long term. However, changes of land use have short-term, frequently drastic
effects, leading to considerable impacts on environmental and hydrological processes (infiltration,
groundwater recharge, base flow, runoff, water quality) [1]. Understanding the relationship between
land use and freshwater quality is key for effective water management, both currently and in the
future [2,3].
The quality of freshwater reflects the combined effects of multiple natural processes and the
anthropogenic changes of land use [4,5]. Runoff from catchment areas into water bodies is the
main source of nutrients and pollutants [6]; consequently, the relationship between water quality
in lotic environments and changes of land use has raised a growing interest within the scientific
community, as landscape patterns regulate physical and biogeochemical processes in the basin [7].
Agriculture and urbanization are the main sources of nutrients and xenobiotics that degrade water

Water 2018, 10, 1518; doi:10.3390/w10111518 www.mdpi.com/journal/water

Water 2018, 10, 1518 2 of 16

quality in water bodies [8]. The conversion of native vegetation to agriculture and human settlements
has significantly increased the human well-being at the expense of the degradation of many ecosystem
services and biodiversity [9,10]. Particularly, the annual deforestation rate has increased dramatically
in tropical zones [11,12], and although the deforestation rate showed a 50% decrease in 2015
relative to 1990 worldwide, in Mexico the loss of forest areas still prevails [12]. According to the
Secretariat of Environment and Natural Resources (SEMARNAT), 29% of the original natural vegetation
coverage in the Mexican territory had been lost by 2011 [13], with mountain cloud forests among the
ecosystems most vulnerable to changes of land use [14]. In developing countries, the combination of a
vigorous population growth rate, industrialization, and expanding agricultural areas has exerted and
ever-increasing pressure on water [15] and forest resources, impacting ecological processes. In Mexico,
cloud forests are seriously threatened by deforestation and habitat fragmentation [16]. For this reason,
environmental policies and management plans for the conservation of water and forest resources
should be developed.
Cloud forests cover a mere 1% of the Mexican territory, ranking second among the ecosystems
with the highest species richness in Mesoamerica [17]. This forest is characterized by several arboreal
strata with a high abundance of ferns and epiphytes, as well as a high biodiversity associated with its
unique climatic conditions: high cloudiness, fog at the canopy level, and high relative humidity [18,19].
However, models on the effects of changes of land use on climate change have predicted an estimated
loss of up to 70% of cloud forest area by 2080 [20]. Changes of land use in ecosystems as vulnerable
as cloud forests affect biodiversity and ecosystem services, including the hydrological cycle [21].
The influence of changes of land use on water quality of rivers running through these forests is
currently poorly understood, particularly in areas with a mosaic of land uses along the river course.
Some research [22,23] has demonstrated that cloud forest vegetation can function as a natural filter
against pollutants dumped in watersheds; hence, vegetation cover, diversity, and structure are key
drivers of water quality. Although changes of land use associated with loss of water quality have
been reported for several countries in various works [22–24], the information on this issue in Mexico
is scarce. First-order streams with different land uses including cloud forest, grassland, and coffee
plantations, which were related to eight ions in water (Ca2+ , CO3 2− , NO3 − , Cl− , Na+ , Mg2+ , and K+ )
and total suspended solids, and to the structure of vegetation, were analyzed [25], indicating that the
ions studied increased in grassland and coffee plantations but were lower in forest cloud forest, and a
loss of vegetation diversity was detected.
In this sense, there is a large number of tools for the detection of the effects of climate change
and land uses on water quality [1,3]. Among them, modeling has proven to be a reliable tool for
predicting the long-term effects of climate change on water quality. Some models are based primarily
on spatial analysis using Geographic Information Systems (GIS) through satellite imagery and digital
elevation that incorporate various watershed attributes in addition to land use areas and water quality
parameters (slope, precipitation, air temperature, topography and soil parameters, river flow, elevation,
and anthropogenic factors influencing land use, among others) [1,3,26–28]; other models include
time series, linear models, multiple linear regression, and constrained least squares models [26,29].
Models are also used to explore the behavior of pollutant levels in stream water under different
scenarios. The current heavy deforestation and high rate of land use change in tropical forests cause
short-term effects in the water quality of rivers flowing across them; therefore, studies should be
conducted to identify the main factors affecting water quality in these areas.
Water quality is controlled by multiple factors, including the connectivity and interaction
of the river with the watershed. Multivariate statistical methods (cluster analysis, CA; principal
component analysis, PCA) are key methods to evaluate the correlations among the various water
quality parameters and land uses to identify the key drivers affecting water quality and influencing the
aquatic ecosystem. CA and PCA have been extensively used to characterize and evaluate freshwater
quality, revealing temporal and spatial variations caused by natural and anthropogenic factors [30–33].
CA is an unsupervised pattern-recognition technique that reveals the intrinsic structure or underlying
Water 2018, 10, 1518 3 of 16

behavior of a data set without making a priori assumptions about the data, in order to sort the
components of a system into categories or clusters according to their similarity [34]. In the clustering
procedure, study sites (components) are sorted in such a way that similar components are clustered
into the same class sharing a particular set of properties [35]. Thus, cluster analysis allows interpreting
the data and identifying patterns [34]. For its part, PCA is a powerful tool for pattern recognition and
detection of correlations (or co-variances) among a set of variables or samples. It provides information
on the most significant parameters associated with spatial and temporal variations; it also describes
whole data sets by excluding the least significant parameters with minimum loss of the original
information [36]. It is extremely useful for the analysis of data involving a large number of variables.
It has been extensively used as an unbiased method that reveals associations between samples and
variables [37]. Furthermore, the potential capabilities of GIS combined with multivariate statistical
analyses for assessing water quality have been explored [38]. Thus, the combined use of GIS with CA
and PCA facilitates the interpretation of complex databases to gain a deeper insight on water quality
in watershed studies, being key in the development of appropriate strategies for effective management
of water resources [34]. Although several studies in temperate latitudes use CA/PCA to assess the
relationship between changes in land use and their impact on water quality, as is the case of [34], this is
the first study that uses both tools (CA/PCA) in combination with GIS to explore the effect of changes
of land use in a tropical cloud forest on water quality of a stream running through it in Mexico.
This study aims to investigate the temporal and spatial variations in water quality as related to
land uses along the Bobos River, Veracruz, a hydrological system that flows through an important
cloud forest area in the Gulf of Mexico slope. In order to analyze land uses and water quality indicators,
we used CA and PCA to detect patterns (clusters of study sites) and to identify the key parameters
(land uses and water quality indicators) associated with seasonal and spatial patterns.

2. Materials and Methods

2.1. Study Area

The Bobos River is located in the northeastern portion of the Gulf of Mexico slope, within the
Nautla River basin; a section of the main river channel flows across the natural protected area named
“Filobobos River and its Surroundings” (Río Filobobos y su Entorno; Figure 1). The basin is used for
multiple activities, including mining in the upper course, the production of banana, citrus, and coffee
in the middle course, and fisheries, humid-soil agriculture, induced pastures, and human settlements
in the lowlands. The region is also used for tourism activities such as rafting. The largest town,
Martínez de la Torre (>250,000 inhabitants), is located in the lowlands, a region that also includes less
densely populated towns (<250,000 inhabitants) such as Altotonga, Jalacingo, and Tlapacoyan [39].
Water 2018, 10, 1518 4 of 16
Water 2018, 10, x FOR PEER REVIEW 4 of 16

Figure 1. Geographic location of the Bobos river basin and study sites. Red dots mark study sites. PI
Figure 1. Geographic location of the Bobos river basin and study sites. Red dots mark study
= Pimiento, HU = Huapala, JL = Jalacingo, TM = Tomata, EN = Encanto, TZ = Tezcapa, MA = Manantial,
sites. PI = Pimiento, HU = Huapala, JL = Jalacingo, TM = Tomata, EN = Encanto, TZ = Tezcapa,
PI = Puente Filo, PA = Palmillas, RG = Rojo Gómez, MZ = Martínez de la Torre, and PL = Paso Largo.
MA = Manantial, PI = Puente Filo, PA = Palmillas, RG = Rojo Gómez, MZ = Martínez de la Torre, and
PL = Paso Largo.
2.2. Field Work
2.2. Field
ThisWork
study involved 12 study sites located along the Bobos and Nautla rivers. In the upper
course, the
This studysitesinvolved
selected were Pimiento
12 study sites (PI) and along
located Huapalathe(HU).
BobosAlong the Alseseca
and Nautla rivers.river tributary,
In the upper
the sites selected were Jalacingo (JL), Tomata (TM), and Encanto (EN), located
course, the sites selected were Pimiento (PI) and Huapala (HU). Along the Alseseca river tributary, close to Tlapacoyan
and
the within
sites the natural
selected protected (JL),
were Jalacingo area.Tomata
Last, the(TM),
sites and
Tezcapa (TZ),(EN),
Encanto Manantial
located(MA), Puente
close Filo (FI),
to Tlapacoyan
Palmillas (PA), Rojo Gómez (RG), Martí nez de la Torre (MZ), and Paso Largo
and within the natural protected area. Last, the sites Tezcapa (TZ), Manantial (MA), Puente Filo (PL) are located along
(FI),
Palmillas (PA), Rojo Gómez (RG), Martínez de la Torre (MZ), and Paso Largo (PL) are located alongthe
the mainstream of Bobos-Nautla rivers, with RG, MZ, and PL being close to the largest town in the
region (Martinez de la Torre). The study involved six monitoring events that
mainstream of Bobos-Nautla rivers, with RG, MZ, and PL being close to the largest town in the regionencompassed the dry,
wet, and de
(Martinez cold seasons,The
la Torre). thestudy
latterinvolved
influenced six by northerlyevents
monitoring windsthat
(cold fronts): August
encompassed (rainy)
the dry, wet,and
and
December (cold) 2013, February (cold), June, and September (rainy) 2014, and
cold seasons, the latter influenced by northerly winds (cold fronts): August (rainy) and December September (rainy) 2015.
In addition,
(cold) the altitudinal
2013, February profile
(cold), June, andofSeptember
each stream in the
(rainy) basin
2014, andwas delineated,
September locating
(rainy) 2015. study sites
In addition,
according to altitude and distance traveled, in kilometers, from the highest to the
the altitudinal profile of each stream in the basin was delineated, locating study sites according to lowest study site; a
topographic map was included.
altitude and distance traveled, in kilometers, from the highest to the lowest study site; a topographic
The following variables were recorded at each site and study season: dissolved oxygen (mg/L),
map was included.
water temperature (°C), conductivity (μs/cm), turbidity (NTU), and pH (using a Quanta® probe,
The following variables were recorded at each site and study season: dissolved oxygen (mg/L),
Hydrolab, Austin, TX, USA). In addition, water samples (100 mL and 500 mL) were collected from
water temperature (◦ C), conductivity (µs/cm), turbidity (NTU), and pH (using a Quanta® probe,
each site for microbiological and chemical testing in the laboratory.
Hydrolab, Austin, TX, USA). In addition, water samples (100 mL and 500 mL) were collected from
each site for microbiological and chemical testing in the laboratory.
2.3. Water Quality
2.3. Water
WaterQuality
samples were tested for nitrates (mg/L), nitrites (mg/L), ammonia nitrogen (mg/L), total
nitrogen (mg/L), orthophosphates (mg/L), total phosphorus (mg/L), color (Pt–Co U), and hardness,
Water samples were tested for nitrates (mg/L), nitrites (mg/L), ammonia nitrogen (mg/L), total
using the spectrophotometric techniques of the Hach® DR 3900 instrument (Hach, Loveland, CO,
nitrogen (mg/L), orthophosphates (mg/L), total phosphorus (mg/L), color (Pt–Co U), and hardness,
USA); on the other hand, chlorides (mg/L), BOD5 (mg/L), alkalinity (mg/L CaCO3), and total and fecal
using the spectrophotometric techniques of the Hach® DR 3900 instrument (Hach, Loveland, CO, USA);
coliforms (MPN/100 mL) were determined using American Public Health Association (APHA)
on the other hand, chlorides (mg/L), BOD5 (mg/L), alkalinity (mg/L CaCO3 ), and total and fecal
techniques [40]. The water quality index (WQI) was calculated from the multiplicative weighted
coliforms (MPN/100 mL) were determined using American Public Health Association (APHA)
index proposed by Dinius [41], ranging from 0 to 100, where zero corresponds to extremely poor
Water 2018, 10, 1518 5 of 16

techniques [40]. The water quality index (WQI) was calculated from the multiplicative weighted
index proposed by Dinius [41], ranging from 0 to 100, where zero corresponds to extremely poor
water quality and 100 to excellent water quality, considering five different potential uses of water
(public water supply, fish and shellfish, agricultural, industrial, and recreational uses). The WQI
considers the percentage of oxygen saturation (%DO), BOD5 , NO3 concentration, water hardness,
conductivity, color, total and fecal coliforms, alkalinity, chlorides, pH, and atmospheric and water
temperature, using the following equation:
n
∏ Ii i
w
WQI =
i =1

where WQI = Water Quality Index (0 to 100); Ii = subindex of the ith parameter (0 to 100);
Wi = weighting value of the parameter (0 to 1); n = number of parameters.

2.4. Land Uses

For the characterization of study sites based on land uses, an interactive map was developed
based on the geographic layers of land use at 1:250,000 scale provided by INEGI (National Institute of
Statistical and Geography), using the QGIS software (Las Palmas version) (Open Source Geospatial
Foundation, Chicago, IL, USA). For each study site, “buffers” (i.e., zones influenced by land use) were
set measuring 2 km in length upstream of the monitoring site by 500 m at both sides (2 km × 500 m).
Additionally, land use was assessed watershed upstream from each study site. In this case, we
calculated the percentage of each land use by means of the Simulador de Flujos de Agua de Cuencas
Hidrográficas (SIATL) (3.2) [42]; these were subsequently grouped into major land-use categories.

2.5. Statistical Analysis

A dissimilarity analysis was conducted between study sites through Euclidean distances, with
the dendrogram drawn according to the Ward’s hierarchical clustering method using averages of
physicochemical parameters for each study site to identify sections along the river and to define
clusters for comparison.
Homoscedasticity testing was performed with cluster data; afterwards, analysis of variance
(ANOVA) (α = 0.95) and multiple comparison tests between clusters were performed using the
Student–Newman–Keuls method.
The physicochemical characterization of study sites and their relationship with land uses
were performed through a principal component analysis with three dimensions (PCA-3D) using
the Spearman’s correlation coefficient. To this end, a matrix was built with study sites as rows
and environmental parameters and land uses as columns. This analysis considered averages of
physicochemical parameters for sampling seasons and percentage of each land use. The data set was
√
standardized using the formula X = log (x + 1); for percentages, the formula was 2π × arcsin p, where
p is the relative value of each individual land use. All statistical analyses were run using the software
XLStat-2015 (Addinsoft, Paris, France).

3. Results

3.1. Clustering of Study Sites According to Their Physicochemical Properties

The dendrogram of the dissimilarity analysis of study sites (Figure 2) revealed three clusters.
The first (C1) grouped together sites PI, HU, MA, TZ, and FI and was defined as the upper course.
C2 clustered sites RG and PA (the middle course of the Bobos River) and sites JL, TM, and EN (from the
Alseseca River tributary); finally, a third cluster (C3) included sites PL and MTZ (the lower course).
Water 2018, 10, 1518 6 of 16
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C2
C2

C3
C3

C1
C1

Dendrogram of
Figure 2. Dendrogram
Figure of dissimilarity
dissimilarity of
of Euclidean
Euclidean distances
distances between
between study
study sites
sites based
based on
on average
average
Figure 2. Dendrogram of dissimilarity of Euclidean distances between study sites based on average
physicochemical values of all study periods.
physicochemical values of all study periods.
3.2. Longitudinal Profile of the River
3.2. Longitudinal
3.2. Longitudinal Profile
Profile of
of the
the River
River
The longitudinal profile of the river, including topographic relief and slope of each river section,
The longitudinal
The longitudinal profile
profile of
of the
the river,
river, including topographic
topographic relief
relief and
and slope
slope of
of each
each river section,
section,
as defined by the dissimilarity analysis,including
led to the identification of a marked changeriver
in gradient
as defined
as defined by
by the
the dissimilarity
dissimilarity analysis,
analysis, led to
to the
the identification
identification of
of aa marked
marked change in in gradient
gradient
(Figure 3A,B); as expected, C1 showed theled steepest slope (4.76%), C2 attained anchange
intermediate slope
(Figure
(Figure 3A,B); as expected, C1 showed the steepest slope (4.76%), C2 attained an intermediate slope
(3.18%),3A,B);
and C3ashad
expected, C1 showed
the lowest the steepest slope (4.76%), C2 attained an intermediate slope
slope (0.44%).
(3.18%), and
(3.18%), and C3
C3 had
had the
the lowest
lowest slope
slope (0.44%).
(0.44%).

Figure 3. Altitudinal profile and

Altitudinal profile and topographicrelief
relief ofthe
the Bobos-NautlaRiver.
River. (A) Altitudinal profile
Figure 3.
Figure Altitudinal and topographic
topographic reliefofof theBobos-Nautla
Bobos-Nautla River.(A)(A)Altitudinal
Altitudinalprofile of
profile
of streams
streams in in the
the Bobos-Nautla
Bobos-Nautla Riverbasin.
River basin.The
Therelative
relativeslope
slope(%)
(%)for
foreach
each section
section is shown in brackets
brackets
of streams in the Bobos-Nautla River basin. The relative slope (%) for each section is shown in brackets
according
according toto the
to the clustering
the clustering from
clustering from the
from the dissimilarity
thedissimilarity analysis.
dissimilarity analysis. (B)
analysis. (B) Topographic
(B)Topographic relief
Topographic relief of
relief of the
of the Bobos-Nautla
theBobos-Nautla
Bobos-Nautla
according
River
River watershed.
watershed.
River watershed.
Water 2018, 10, 1518 7 of 16
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3.3. WQI
3.3. WQI
Mean WQI values for each site ranged from 70.58 ± 0.95 in Martinez de la Torre (MZ) to
Mean WQI values for each site ranged from 70.58 ± 0.95 in Martinez de la Torre (MZ) to 80.04 ±
2.53 ±
80.04 for2.53 for Jalacingo
Jalacingo (JL) (Figure
(JL) (Figure 4). However,
4). However, differences
differences between
between study
study sites
sites werenot
were notstatistically
statistically
significant
significant(p(p>>0.05).
0.05).
The
Themean
meanWQI WQIattained
attained the
the highest
highest value
value inin the
the upper
upper course (78.05 ±
course (78.05 0.97), which
± 0.97), which was was
significantly different from the lower course (72.38 ± 1.48; p < 0.05). Furthermore,
significantly different from the lower course (72.38 ± 1.48; p < 0.05). Furthermore, in accordance with in accordance
with
the the
waterwater quality
quality categories
categories of [41],
of [41], WQIWQI values
values forfor
thethe upper
upper coursecan
course canbebeclassified
classifiedasasfollows:
follows:
“Acceptable for all water sports; “Acceptable for fish and shellfish”; “Minor
“Acceptable for all water sports; “Acceptable for fish and shellfish”; “Minor purification for cropspurification for crops
requiring high-quality water”; “Treatment needed for public water supply.” By
requiring high-quality water”; “Treatment needed for public water supply.” By contrast, WQI values contrast, WQI values
ininthe
thelower
lowercourse
coursecorrespond
correspondto tothe
thefollowing
followingcategories:
categories: “Becoming polluted to
“Becoming polluted to practice
practice any
anywater
water
sports”; “Marginal quality for sensitive fish and shellfish”; “No treatment needed
sports”; “Marginal quality for sensitive fish and shellfish”; “No treatment needed for most crops and for most crops and
industries”,
industries”,“Treatment
“Treatmentrequired
requiredfor forpublic
publicwater
watersupply.”
supply.”
OnOnthetheother
otherhand,
hand,averages
averagesby byseason
season(Figure
(Figure 4)4) yielded
yielded the lowest values in in the
the rainy
rainy seasons
seasons
ofofAugust 2013 and June 2014 (71.30 ± 0.77 and 73.82 ± 1.04, respectively), which
August 2013 and June 2014 (71.30 ± 0.77 and 73.82 ± 1.04, respectively), which were significantly were significantly
different
different(p(p<<0.05)
0.05)versus
versusDecember
December2013 2013 and
and February
February 2014, when the highest highest values
values were
wererecorded
recorded
(79.36±±0.97
(79.36 0.97and 84.42±± 0.93,
and84.42 0.93, respectively). According to
respectively). According to WQI
WQI values,
values, the
the seasonal
seasonal patterns
patterns show
show
differences only in the case of public water supply, which fell into the category
differences only in the case of public water supply, which fell into the category “Minor purification “Minor purification
required”
required”ininthethedry
dryseason,
season,butbutinto
intothe
thecategory
categoryofof“Necessary
“NecessaryTreatment
Treatment for Public
for Public Water
Water Supply”
Supply” in
the
in rainy season.
the rainy TheThe
season. global WQI
global for the
WQI whole
for the study
whole areaarea
study ranges from
ranges mildly
from polluted
mildly for for
polluted human
humanuse
touse to excellent
excellent qualityquality for industrial,
for industrial, recreational,
recreational, and fishing
and fishing uses.uses.

Figure 4. Mean values of water quality index (WQI) by study site, season, and river portion. a 6= b
Figure 4. Mean values of water quality index (WQI) by study site, season, and river portion. a ≠ b (p
(p < 0.05).
< 0.05).
Water 2018, 10, 1518 8 of 16
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3.4.
3.4.Land
LandUses
Uses
Nine
Ninedifferent
differentland
landuses
useswere
wereidentified
identifiedininthe
theassessment
assessmentofofland landuse
usewatershed
watershedupstream
upstreamfrom from
each study site (tropical mountain cloud forest, TMCF; coniferous forest, CF;
each study site (tropical mountain cloud forest, TMCF; coniferous forest, CF; high evergreen forest, high evergreen forest,
HEF;
HEF;humid
humidsoil soilagriculture,
agriculture,HSA; HSA;rainfed
rainfedagriculture,
agriculture,RA;RA;induced
inducedpasture,
pasture,IP;
IP;cultivated
cultivatedpasture,
pasture,
CP;
CP;human
humansettlements,
settlements,HS; HS;urban
urbanzones,
zones,UZ)UZ)(Figure
(Figure5).5).Land-use
Land-usepercentages
percentagesobtained
obtainedfromfromthis
this
assessment
assessment (Figure 5A) show that the tree types of forests (TMCF, CF, and HEF) are representedallin
(Figure 5A) show that the tree types of forests (TMCF, CF, and HEF) are represented in
study sites,sites,
all study ranging fromfrom
ranging 24 to2438% in C3
to 38% inand C2, and
C3 and fromfrom
C2, and 41 to4165% in CI.
to 65% in Agriculture
CI. Agricultureusesuses(RA,(RA,
IP,
CP, and HSA) ranged from 62 to 76% in C3 (particularly HSA) and from 35
IP, CP, and HSA) ranged from 62 to 76% in C3 (particularly HSA) and from 35 to 58% in both C2 andto 58% in both C2 and C1.
InC1.
allIn
clusters, HS and
all clusters, HSUZ andshowed
UZ showed values belowbelow
values 1%. On1%.theOnother hand,hand,
the other the assessment
the assessmentof landof use
land
including the buffer
use including zone (2
the buffer km(2×km
zone 500×m) 500(Figures 5B and
m) (Figures 5B6) showed
and two types
6) showed of forest
two types (TMCF
of forest and
(TMCF
HEF); in C1,in
and HEF); theC1,percentages rangedranged
the percentages from 23 to 100%,
from although
23 to 100%, forestsforests
although were not represented
were in threein
not represented
study
three sites
study ofsites
this of
cluster (TZ, MA,
this cluster (TZ,andMA, FI);
andHEF
FI);was
HEFobserved
was observedin only inone
onlyC2 siteC2
one (PA:
site8%)
(PA:but was
8%) but
completely
was completely absentabsent
in C3. HS andHS
in C3. UZandranged
UZ from
ranged25 from
to 42% 25intoC3;
42% in in
C2,C3;
UZinvaried from
C2, UZ 5 to 20%
varied fromonly
5 to
in20%
study
onlysites PA and
in study RG;PA
sites C1and
shows RG;no C1influence
shows noofinfluence
this land ofuse.
this land use.

A) B)
100% 100%

90% 90%

80% 80%

70% 70%

60% 60%

50% 50%

40% 40%

30% 30%

20% 20%

10% 10%

0% 0%
PI HU TZ MA FI JL TM EN PA RG MZ PL PI HU TZ MA FI JL TM EN PA RG MZ PL
Tropical montane cloud forest (TMCF) Coniferous forest (CF) Rainfed agriculture (RA) Cultivated pasture (CP)

High evergreen forest (HEF) Induced pasture (IP) Humid soil agriculture (HSA)

Human settlements (HS) Urban zone (UZ)

Figure5.5.Percentage
Figure Percentageofofland
landuse
useinineach
eachstudy
studysite.
site.(A)
(A)Percentage
Percentageofofland
landuse
usefor
forwatershed
watershedupstream
upstream
from
fromeach
eachstudy
studysite.
site.(B)
(B)Percentage
Percentageofofland
landuse
usefor
forthe
theupstream 500mm××22km
upstream500 kmbuffer
bufferzone.
zone.
Water 2018, 10, 1518 9 of 16
Water 2018, 10, x FOR PEER REVIEW 9 of 16

6%

WQI = 75.65 ± 2.08 WQI = 70.58 ± 1.35

33% 32%

12% 62%
67% 1%

WQI = 75.52 ± 1.66 14%

23%
55%
19%

21% WQI = 72.98 ± 2.06

76%
WQI = 73.84 ± 3.32
79%
MZ
43%

41%
57%
WQI = 79.11 ± 2.50
WQI = 75.20 ± 2.27 59%
4%

6%

WQI = 80.04 ± 2.77

27%
WQI = 78.08 ± 2.84
96%
67%
Vegetation and Land Uses 29%

Tropical montane cloud forest (TMCF)

71% WQI = 77.66 ± 1.97
Rainfed agriculture (RA)
Cultivated pasture (CP) 8%

High evergreen forest (HEF)

Induced pasture (IP) WQI = 78.87 ± 2.11
92%
Humid soil agriculture (HSA)
Human settlements (HS)
Urban zone (UZ)
WQI = 76.42 ± 1.60
100%

Figure 6.
Figure 6. Percentage
Percentage of
of land
land uses
uses from
from buffer
buffer and
and mean
mean WQI
WQI of study sites
of study sites along
along the
the Bobos
Bobos River.
River.
Tributaries and streams are shown in colors as in Figure
Tributaries and streams are shown in colors as in Figure 1.1.

3.5.
3.5. Multivariate
Multivariate Analysis
Analysis
The
The principal component analysis
principal component analysis(PCA-3D)
(PCA-3D)accounted
accountedfor for69.51%
69.51%ofofthe thecumulative
cumulative variance
variance of
of the data set in the first three axes (F1: 35.56%, F2: 20.91%, and F3: 13.03%);
the data set in the first three axes (F1: 35.56%, F2: 20.91%, and F3: 13.03%); factor loadings are shown factor loadings are
shown
in Tablein Table
1. The1.first
The component
first component (F1) (F1) showed
showed thethe importance
importance of ofthethealtitudinal
altitudinalgradient
gradient andand the
the
variables associated with changes along the river course: altitude and WQI
variables associated with changes along the river course: altitude and WQI are inversely proportional are inversely proportional
to
to turbidity,
turbidity,temperature,
temperature,nitrogen
nitrogen(NH(NH33 andand TN),
TN), coliforms
coliforms (total
(total and
and fecal),
fecal), total
total suspended
suspended solids,
solids,
alkalinity,
alkalinity, chloride,
chloride, color,
color, and
and land
land uses
uses HS HS and
andUZ; UZ;F2 F2isisrelated
relatedto tonutrient
nutrientenrichment
enrichment(NO (NO33 and
and
O–PO ) and mineralization (conductivity, SO , and hardness; land uses related
O–PO44) and mineralization (conductivity, SO44, and hardness; land uses related to F2 were cultivated to F2 were cultivated
and
and induced
induced pastures,
pastures, allall of
of which
which were
were directly
directly proportional
proportional to to F2); finally, F3
F2); finally, F3 isis related
related toto DO, BOD,
DO, BOD,
and rainfed agriculture, which are directly proportional to F3 (Table 1). The
and rainfed agriculture, which are directly proportional to F3 (Table 1). The 3-D plot (Figure 7) shows3-D plot (Figure 7) shows
clusters
clusters of
of study
study sites:
sites: Cluster
Cluster II comprises
comprises sitessites PI,
PI, HU,
HU, TZ,
TZ, MA,
MA, and
and FI, FI, characterized
characterized by by the
the highest
highest
conductivity,
conductivity,alkalinity,
alkalinity,hardness,
hardness,dissolved
dissolvedoxygen,
oxygen,and andsulfates.
sulfates.These
Thesesites sitesalso
also reached
reachedthe the highest
highest
WQI values of the six periods studied; in addition, these showed the highest
WQI values of the six periods studied; in addition, these showed the highest percentages of natural percentages of natural
vegetation
vegetation (tropical
(tropical mountain
mountain cloudcloud forest
forest and
and high
high evergreen
evergreen forest),
forest), as as well
well as as rainfed
rainfed agriculture
agriculture
from
from TZTZ toto FL,
FL, along
along with
with clearing
clearing of
of natural
natural vegetation.
vegetation. Cluster
Cluster IIII includes
includes sites sites located
located along
along the
the
Alseseca river tributary (JL, TM, and EN) and sites in the middle course (RG
Alseseca river tributary (JL, TM, and EN) and sites in the middle course (RG and PA), characterized and PA), characterized by
the highest
by the levels
highest of nitrates,
levels nitrites,
of nitrates, orthophosphates,
nitrites, orthophosphates, total total
phosphorus,
phosphorus, chlorides, BOD5BOD
chlorides, , and5,fecal
and
coliforms. These sites were closely related to rainfed agriculture, as well as
fecal coliforms. These sites were closely related to rainfed agriculture, as well as to induced and to induced and cultivated
pastures.
cultivatedFinally,
pastures.Cluster III includes
Finally, Cluster sites located in
III includes the located
sites lower course
in the(MZ lowerandcourse
PL), associated
(MZ and with PL),
the highest percentage
associated of humanpercentage
with the highest settlementsof andhuman
urban zones, humidand
settlements soil agriculture,
urban zones, andhumid
the highestsoil
values of total nitrogen, ammonia nitrogen, pH, total coliforms, turbidity, suspended
agriculture, and the highest values of total nitrogen, ammonia nitrogen, pH, total coliforms, turbidity, solids, and color
(Table 2). solids, and color (Table 2).
suspended
Water 2018, 10, 1518 10 of 16

Table 1. Factor loadings and variance (%) for components F1, F2, and F3. Figures in bold are significant
(p < 0.05 for each component).

Parameter F1 (35.56%) F2 (20.91%) F3 (13.03%)

DO −0.0871 −0.0171 0.8850
pH 0.3879 0.3074 0.6906
COND 0.0979 0.7551 −0.3434
TURB 0.8437 −0.1793 0.1031
T (◦ C) 0.7824 0.1094 −0.4135
NO3 −0.7053 −0.5861 −0.0335
NO2 −0.1607 −0.6586 0.5103
NH3 0.9559 0.1313 0.0420
TN 0.8492 0.1585 0.1872
O–PO4 −0.0362 −0.6673 −0.0824
TP 0.5200 −0.5171 −0.0259
SO4 −0.1264 0.6642 −0.3709
BDO5 −0.2876 −0.0906 0.7283
TC 0.8242 −0.2818 0.0543
FC 0.7499 −0.5891 −0.2426
TSS 0.9432 −0.1323 0.0726
HARD −0.3486 0.8449 −0.0211
ALC −0.1793 0.8110 −0.2087
Cl− 0.3173 −0.2528 −0.2921
ALT −0.8523 −0.1603 0.1463
CLR 0.8230 −0.0156 0.1958
TMCF −0.4623 0.4379 0.6355
HEF −0.1492 0.2514 −0.1479
IP −0.1868 −0.7041 0.2858
CP −0.0485 −0.7128 −0.4024
RA −0.4603 −0.4009 −0.6416
HSA 0.7789 0.2416 0.1623
UZ 0.8628 0.2615 0.0455
HS 0.8325 0.2567 0.0858
WQI −0.5758 0.2582 0.0610
Water 2018, 10, x FOR PEER REVIEW 11 of 16

Figure 7. Principal component analysis for study sites, physicochemical variables, WQI, and land uses.
Figure 7. Principal component analysis for study sites, physicochemical variables, WQI, and land
(A) Environmental and land-use variables; (B) clusters of study sites.
uses. (A) Environmental and land-use variables; (B) clusters of study sites.

Table 2. Mean values (± Standard Error (SE)) of components related to N and P, WQI, and
predominant land uses (%) for each study site.

O–PO4 Predominant
Site NO3 (mg/L) NO2 (mg/L) NH3 (mg/L) TN (mg/L) TP (mg/L) WQI
Water 2018, 10, 1518 11 of 16

Table 2. Mean values (± Standard Error (SE)) of components related to N and P, WQI, and predominant
land uses (%) for each study site.

O–PO4 Predominant
Site NO3 (mg/L) NO2 (mg/L) NH3 (mg/L) TN (mg/L) TP (mg/L) WQI
(mg/L) Land Use
PI 1.17 (±1.007) 0.007 (±0.004) 0.19 (±0.09) 7.94 (±3.43) 0.47 (±0.13) 0.76 (±0.4) 76.42 ± 1.60 TMCF (100%)
HU 1.02 (±0.1) 0.007 (±0.002) 0.18 (±0.04) 6.63 (±2.18) 0.31 (±0.31) 0.59 (±0.1) 78.87 ± 2.11 TMCF (92%)
TZ 0.97 (±0.09) 0.007 (±0.001) 0.21 (±0.02) 8.16 (±2.17) 0.34 (±0.07) 0.65 (±0.12) 76.66 ± 1.97 RA (77.6%)
MA 1.34 (±0.13) 0.006 (±0.001) 0.19 (±0.01) 7.45 (±2) 0.48 (±0.08) 0.72 (±0.07) 78.08 ± 2.48 RA (96%)
FI 0.96 (±0.09) 0.005 (±0.001) 0.25 (±0.06) 8.56 (±1.56) 0.51 (±0.1) 0.89 (±0.13) 79.11 ± 2.50 RA (79.11%)
JL 1.46 (±0.22) 0.013 (±0.003) 0.21 (±0.03) 7.65 (±2.02) 0.56 (±0.07) 0.8 (±0.12) 80.04 ± 2.77 RA (67%)
TM 1.27 (±0.3) 0.011 (±0.004) 0.26 (±0.1) 8.05 (±3.42) 0.53 (±0.17) 0.93 (±0.4) 75.20 ± 2.27 RA (59%)
EN 1.21 (±0.25) 0.008 (±0.002) 0.3 (±0.12) 9.31 (±1.95) 0.66 (±0.05) 1.23 (±0.3) 73.84 ± 3.32 CP (79%)
PA 1.07 (±0.15) 0.008 (±0.002) 0.27 (±0.08) 9.34 (±2.43) 0.45 (±0.07) 0.8 (±0.15) 75.52 ± 1.62 RA, HS (59%, 14%)
RG 1.03 (±0.16) 0.007 (±0.002) 0.27 (±0.05) 9.89 (±2.8) 0.4 (±0.1) 0.74 (±0.08) 75.65 ± 2.08 RA (67%)
HSA, HS, UZ
MZ 0.53 (±0.39) 0.005 (±0.005) 0.48 (±0.45) 10.15 (±9.69) 0.25 (±0.03) 0.79 (±0.20) 70.58 ± 1.35
(62%, 32%, 6%)
HSA, HS, UZ
PL 1.12 (±0.1) 0.008 (±0.002) 0.35 (±0.14) 9.96 (±2.9) 0.64 (±0.16) 1.08 (±0.33) 72.98 ±2.06
(76%, 23%, 1%)

4. Discussion
The water quality index proposed by Dinius [41] has been used by several authors to indicate the
effect of anthropogenic impacts and used as an easy-to-interpret tool for assessing water quality [43].
The results obtained in this work demonstrate a marked temporal variation, with the dry cold season
(February 2014) showing the highest water quality; however, as regards spatial variation, this index is
insensitive to variations between sites, seemingly unsuitable for identifying sections with different
characteristics along the river. Some authors [44] stress that this analysis should be conducted in
parallel with an assessment of the changes of land use, since study sites with different land uses yielded
very similar scores. The above derives from the fact that the WQI does not include water-quality
parameters that are affected by changes of land use, such as nutrients (orthophosphates, ammonia,
nitrites, and nitrates) [44–46]. However, the combined analysis of the 23 physicochemical variables
and all land uses considered in this study and using multivariate methods (CA and PCA) allowed for
the identification of the relationship between changes of land use and physicochemical water quality,
and revealed spatial variation patterns.
The CA identified three regions along the course of the river, which share local issues requiring
particular attention or management. For instance, C1 (upper course) shows effects of the changes of
land use (HP, CP, and RA) according to the PCA, although it showed the highest coverage of TMCF
vegetation. These changes of land use were most evident in sites TZ, MA, and FL, characterized
by nutrient enrichment. C1 sites, despite their location in the best preserved area, should be closely
monitored and deforestation should be regulated. Furthermore, the steep slope along the river course
in this zone promotes self-purification. Nilsson et al. [47] indicate that the upper course of any stream
is key for the conservation of water quality in the rest of the basin, as it plays a key role in maintaining
the buffering system and diluting pollutants downstream.
For its part, the PCA evidenced that C2 is closely related to agricultural practices (RA, CP,
and IP account for the higher nutrient levels in sites TM, JL, RG, and PA), contributing to high
nitrogen (NO2 and NO3 ) and phosphorus (O–PO4 ) inputs. This has been highlighted by various
authors [47–50], who point out that increased nutrient levels in water bodies are directly related to
the use of agrochemicals, with higher concentrations during the rainy season as a result of leaching
and runoff. This fact evidences the need to implement best management practices to prevent excess
nutrient discharges into the river.
Last, C3 (MTZ and PL) was associated with human settlements (UZ, HS, and HSA) and showed
wastewater indicators (fecal and total coliforms, ammonium, total N, and chlorides). Due to the low
gradient in this section of the river, its self-cleaning capacity decreases sharply, as reported by [51]
for the lower course of the Potrero de los Funes river, Argentina. The zone of the river associated
with C3 requires the establishment of wastewater treatment facilities before discharge into the river.
In all cases, the studies relating land-use changes at different spatio-temporal scales show that forest
Water 2018, 10, 1518 12 of 16

clearing or replacement of natural vegetation coverage within a basin leads to the deterioration of
water quality [48,49,52].
The combination of two multivariate tools was useful in this study. The cluster analysis produced
groups based on similarities and differences; for its part, the PCA allowed identifying the variables,
producing a new set of variables (principal components) that are consistent with the clusters derived
from CA. In this study, the PCA confirmed its validity as a method for monitoring changes in water
systems and the key drivers associated with them.
In contrast with the assessment of the effect of land use in the watershed upstream from each
study site, the interpretation of the effects of land use on water quality from the analysis of buffer
zones involves scale and interpretation implications according to the research hypothesis established a
priori. It has been pointed out [53,54] that the significant effects on water quality result from changes
of land use in the areas closest to the study sites, since it is in these areas that the watershed is being
washed off of materials, which enter river water and cause immediate effects. Our findings reveal
that, when the influence of land uses is explored according to the watershed upstream from each
study site, C2 and C3 include percentages of forests (TMCF, HEF, and CF) with an altitudinal range
lacking an evident relationship with the river course; thus, these may not directly affect water quality.
For their part, AH and ZU display a minor relative influence, since both represent a small and constant
percentage across all study sites (<1%), particularly in C3, which is the area where human settlements
are located in the proximity of the river; consequently, wastewater indicators are evident. On the
other hand, our results show that changes at a local scale (buffer land uses) significantly affect water
quality, as stressed by [7]. In this respect, our results show that study sites located in the upper course
(PI and HU), with extensive coverage of natural vegetation (92% and 100%, respectively), show good
water quality, as nutrient concentrations were low, while C2 and C3 showed the highest impact by
agricultural practices and human settlements.
Gove et al. [55] found a greater influence of upstream vs. lateral inputs as the length of the
catchment area increases. The fact that these increases reach a point of diminishing returns indicates
that processing within the river eventually dampens the memory of upstream events relative to more
recent longitudinal and lateral inputs. Therefore, if the total cumulative upstream land use governs
water quality at any point in the basin, water quality measurements would exhibit little variations
downstream. In this study, when watershed upstream from each study site are considered, land
uses that are distant from the river course become evident, offsetting the effect of land uses adjacent
to the river. On the other hand, the use of a 2 km × 500 m buffer zone use reveals a shift of land
uses with an immediate effect on the water body. The cluster analysis showed three different groups
based on similar water quality characteristics, which are consistent with Figure 5B. In this sense, and
considering the objectives of this study, the use of information derived from small-scale buffers seems
more appropriate, since these actually provide information on the effects of land uses adjacent to the
river course.
The analysis of results discussed in this work proposes a baseline assessment methodology
for intertropical latitudes, as environmental monitoring data are scarce in many Latin American
countries [25], and Mexico has poor records of historical changes of either land use or water quality.
Based on the above, developing countries in tropical zones should start to identify the direct
effects of different land uses using approaches similar to the one described herein, in order to
investigate cause–effect responses. According to [55], the incorporation of the effect of the watershed
upstream of each study site could be masking/neutralizing the effects of land uses adjacent to the
river course. Working with small-scale buffers (e.g., 2 km × 500 m) and building a monitoring
network produce baseline data on the effects of land uses in different basins, and produce useful
parameters for incorporation into various modeling tools such as SWAT. In turn, this facilitates
building models on potential changes of land use and the expected hydrological changes, which
should be taken into account by policy makers focused on sustainable water resource management
and climate change, as suggested in [56]. In turn, these tools predict the effects of changes of land
Water 2018, 10, 1518 13 of 16

uses; examples include [3], wherein future changes in water quality within a watershed dominated by
agriculture are anticipated, [57], wherein various hydrological land-use scenarios in the upper portion
of the Mississippi river are modeled to 2091 and the impact of land uses on hydrologic processes is
determined, and [1], wherein different scenarios of the effects of climate change on water quality are
assessed. In this sense, our results can be used as a small-scale quantitative component for use in
future predictions about changes of land use and land cover, as defined in [58], and in the development
of management plans and public policies for conservation.

5. Conclusions
The loss of tropical cloud forest is mainly due to the change of land cover to anthropogenic
land uses. Our results revealed that streams located in this basin are highly vulnerable to changes of
land use. These changes alter the proper functioning of the tropical cloud forest and the ecosystem
services, including water quality. Hence, conservation measures targeting cloud forests and high
evergreen forests, along with reforestation programs in the rest of the basin, should be implemented;
wastewater treatment plants should also be established in the lower course of the river—the section
most affected by direct pollution issues and where the river self-purification capacity is not as efficient
as in the upper course. Our results evidence that the natural protected area in the river urgently
requires the implementation of reforestation programs to improve the condition of the local ecosystems
(streams and forest).

Author Contributions: E.L.-L. and J.E.S.-D. participated in the conceptualization and design stages, performed
the methodology, and obtained funding resources; A.J.R.-R. and E.M.-M. carried out data collection and analysis;
A.E.R.-S. and A.G.-R. also participated in the investigation. All authors contributed to the manuscript.
Funding: This research was funded by CONACyT (National Council for Science and Technology), grant number
[PY-FOINS-CONACyT-1931], and by the SIP Secretariat for Research and Postgraduate Studies at Instituto
Politécnico Nacional, grant number (SIP 20170908).
Acknowledgments: María Elena Sánchez-Salazar translated the manuscript into English and contributed to the
edition of the final manuscript.
Conflicts of Interest: The authors declare no conflict of interest. The sponsors had no role in study design, data
collection, analyses, or interpretation; drafting the manuscript, or the decision to publish the results.

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