Ecological Engineering 173 (2021) 106432

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Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Treatment of swine effluent mixed with domestic wastewater and

vegetation development in monoculture and polyculture horizontal
subsurface flow wetlands
Luis Carlos Sandoval Herazo a, Florentina Zurita b, *, Graciela Nani a, b, c, Oscar Andrés Del Ángel-
Coronel d, Fidel Alejandro Aguilar Aguilar e
a
Wetlands and Environmental Sustainability Laboratory, Division of Postgraduate Studies and Research, Tecnológico Nacional de México/Instituto Tecnológico Superior
de Misantla, Misantla, Veracruz 93821, Mexico
b
Environmental Quality Laboratory, Centro Universitario de la Ciénega, University of Guadalajara, Av. Universidad 1115, Ocotlán, Jalisco 4782, Mexico
c
Department of Engineering in Business Management, Tecnológico Nacional de México/Instituto Tecnológico Superior de Misantla, Misantla, Veracruz 93821, Mexico
d
Tecnológico Nacional de México-Instituto Tecnológico Superior de Huatusco, División de Ingeniería en Industrias Alimentarias, Programa de Maestría en Ingeniería, Av.
25 Poniente No. 100, Col. Reserva Territorial, 94100, Huatusco, Veracruz, Mexico
e
Universidad Tecnológica de Gutierrez Zamora. Prolongación Miguel Patiño s/n, Colonia Centro, CP 93556, Gutiérrez Zamora, Veracruz, Mexico.

A R T I C L E I N F O A B S T R A C T

Keywords: The aim of this study was to evaluate horizontal subsurface flow (HSSF) treatment wetlands (TW) for the
Total nitrogen treatment of swine effluents mixed with domestic wastewater, as well as to compare the efficiency of systems
Total phosphorus with monocultures and polycultures. Three species of plants were used in both monoculture and polyculture
Ornamental plants
experimental systems: a) Heliconia latispatha, b) Typha latifolia, c) Cyperus alternifolius, d) Heliconia latispatha +
Backyard livestock
Pig farming
Typha latifolia, e) Heliconia latispatha + Cyperus alternifolius and f) control (without plant). Each cell operated
with a hydraulic loading rate of 5.4 cm/d. The measured variables included environmental parameters (tem­
perature, relative humidity, light intensity, evapotranspiration, pH and dissolved oxygen –DO–), vegetative
growth (plant height, width and leaf length, stem thickness, leaf number and biomass production) and pollutant
measurements (chemical oxygen demand –COD–, total coliforms –TC–, total suspended solids –TSS–, volatile
suspended solids –VSS–, total nitrogen –TN– and total phosphorus –TP–). The results indicated that there were
significant differences (p ≤ 0.001) between the systems. In general, those systems with vegetation removed more
TP (from 44.3% to 63.4%) and TN (from 68.1% to 74.9%) than the system without vegetation (32.9% for TP and
55.6% for TN). In addition, the experimental configuration as mono or polyculture was a determinant factor in
the efficiency of the systems; the polyculture system with H. latispatha + T. latifolia was the most efficient in the
removal pollutants such as COD (68.9 ± 10.6%), TSS (55.6 ± 0.5%), VSS (57.8 ± 0.6%), TC (69.5 ± 6.1%) and
TN (74.9 ± 1.4). With regard to the evaluated species, H. latispatha showed the highest relative growth in both
monoculture and polyculture systems with this high nutrient-concentration wastewater. These results demon­
strate the HSSF TWs planted with monocultures and polycultures of plants in tropical climates represent an
option to reduce the pollutant load of wastewater resulting from the mixing of domestic wastewater and pig
farming wastewater.

1. Introduction
Given their low cost and relative simplicity of construction and
operation based on natural purification processes, the use of treatment
wetlands (TWs) for wastewater (WW) treatment is growing in the world
since they are used to treat different types of effluent for both domestic
and industrial origin (Rodríguez-Domínguez et al., 2020; Wang et al.,
2020). The treatment of agro-industrial effluents, specifically for WW
from the breeding and fattening of different types of livestock, is one of
the applications of TWs (Sultana et al., 2015; Wang et al., 2018).

* Corresponding author.
E-mail addresses: lcsandovalh@gmail.com (L.C.S. Herazo), fzurita@cuci.udg.mx (F. Zurita), genanir@itsm.edu.mx (G. Nani), oscardelangel.coronel@hotmail.com
(O.A. Del Ángel-Coronel), falexaguilar@gmail.com (F.A.A. Aguilar).

https://doi.org/10.1016/j.ecoleng.2021.106432
Received 6 March 2021; Received in revised form 8 September 2021; Accepted 13 September 2021
Available online 27 September 2021
0925-8574/© 2021 Elsevier B.V. All rights reserved.
L.C.S. Herazo et al.
Recent works have demonstrated that TWs are quite effective for
secondary or tertiary treatment for swine effluents characterized by a
much higher pollutant load than that found in domestic wastewater
(Zhang et al., 2017; Xiang et al., 2020). On the other hand, TWs have
proven their functionality for the treatment of municipal wastewater
treatment in communities with low population density, such as rural
areas (Marín-Muñiz et al., 2020; Li et al., 2020). However, their use is
less common at a household level, even though they are an excellent
option for in situ WW treatment in households or dwellings without
connection to sewage systems (Tang and Huang, 2007; Lu et al., 2016;
Zamora et al., 2019).
In Mexico, another type of effluent that can be treated at a household
level by means of TWs are those from backyard livestock. Backyard
livestock is an activity that is practiced in a large part of the rural areas
of this region, since it is an economic activity that complements families’
diet, stimulates self-consumption and self-production (Bravo-Vasquez
et al., 2016). Backyard livestock consists of the breeding or fattening of
poultry, cattle, or pigs (Anampa et al., 2012; Bravo-Vasquez et al.,
2016). Only in Mexico, according to official data, in 2015, 23% of the
population lived in rural locations (with less than 2500 inhabitants)
(INEGI (Instituto Nacional de Estadística, Geografía e Informática),
2015). Unfortunately, the rural population has been characterized by
living in poverty and with low human development rates. This situation
encourages people to seek options that allow them to improve their
living conditions and among them, they have adapted in their homes the
production of different species of backyard livestock, mainly pigs, as a
complement to the basic family basket (Jiménez et al., 2019; Gutiérrez-
Triay et al., 2007). According to Mariaca Méndez (2012), only in the
rural areas of seven states in southeastern Mexico, there are about
2,200,000 family gardens that include backyard livestock.
The above represents a serious problem, since the WW produced
from backyard animal husbandry (especially pigs) are mixed with do­
mestic WW and are generally discharged untreated into local drainage
systems or are discharged into local rivers or nearby streams.
Swine effluents are characterized by having a high content of organic
matter (2000–30,000 mg/L de BOD5), N (800–2300 mg/L), and P
(50–230 mg/L), along with heavy metals (Xiang et al., 2020). Due to
their characteristics, TWs represent an important alternative to treat
these effluents. Through their implementation, they could contribute to
avoiding contamination of water bodies. Additionally, the treated WW
could be used to irrigate home gardens. Furthermore, plant species of
commercial interest may be produced in the same treatment systems. It
is well documented, that in horizontal subsurface flow (HSSF) treatment
wetlands (TWs) (which are one of the most economical versions of
treatment wetlands) it is possible to grow species that produce flowers of
commercial value (Zurita et al., 2006; Zurita et al., 2009; Sandoval et al.,
2019); while in vertical subsurface flow wetlands, maize, sunflower, and
soybean have been planted successfully (Garcia-Perez et al., 2017).
However, to the best of our knowledge, these systems have not yet been
applied to the treatment of wastewater from backyard animal husbandry
in Mexico.
Due to the extension of the practice of backyard livestock in devel­
oping countries, especially for pig farming, there is a need to generate
own criteria to treat this type of effluent with TWs. Therefore, the aim of
this study was to evaluate pilot-scale HSSF TWs for the treatment of
swine effluents mixed with domestic wastewater, as well as to compare
the efficiency of systems with monocultures (a single plant species in the
HSSF TW system) and polycultures (two plants species in the HSSF TW
system). The results of the research will allow proposing solutions to
address the pollution problem that is generated with backyard livestock
in rural areas in developing countries, particularly in Mexico.
2. Methodology
This study was carried out at the Tecnológico Nacional de Mexico
(TecNM), campus Misantla (in Misantla, Veracruz, Mexico) from
2
Ecological Engineering 173 (2021) 106432
October 2019 to June 2020. The weather in the area is classified as hot-
humid and it is located at an altitude of 400 m above sea level with an
average temperature of 22.7 ◦ C and a mean annual rainfall of 2036.4
mm.
2.1. System description
A 1500 L tank was used to mix domestic and swine wastewater in a 1:
1 (v/v) ratio with a 1 HP WEG EXCELL pump. The ratio 1:1 was used to
simulate a common situation in rural communities in this area of
Mexico. The volume of domestic wastewater generated by a family of 5
members is very similar to the volume of swine effluent generated by the
backyard livestock of 5 pigs. This information was obtained from pre­
vious studies of this research group (unpublished data).
Domestic sewage was taken from a sewer within the Misantla
campus, while pig sewage was pumped from a nearby home where 8
pigs were raised in the backyard. After mixing the two effluents, the tank
was given two hours for solids sedimentation, then the mixed waste­
water was pumped into a 1000-L tank to feed the pilot-scale treatment
wetlands.
Experimental units (which functioned as HSSF TWs), consisted of 12
cells, built of masonry (Fig. 1). Their dimensions were 1.4 m × 0.4 m ×
0.65 m, corresponding to the length, width, and depth, respectively. The
selection of this type of TW was due to the fact that it is one of the most
economical types of TWs compared to other types such as vertical sub­
surface flow treatment wetlands that are generally assisted by an electric
pump, which would make its implementation more difficult in low-
income rural communities in Mexico. The cells were filled from bot­
tom to top, as follows: the first 0.2 m, with red tezontle from 10 to 20 cm
in diameter (porosity of 0.63) this to promote anaerobic conditions and
the remaining 0.45 m, with red tezontle with a diameter of 1 to 4 mm,
with a porosity of 0.57. The water level was maintained at 0.60 m. The
material was obtained from a gravel bank nearby to the city of Misantla.
In total, 0.364 m3 of wastewater were treated daily in the entire system
(a volume of 0.0304 m3 per cell) with a hydraulic retention time of 6.5
days.
Three species of plants were used in the experiment and were ob­
tained in different ways. Heliconia latispatha (31.6 ± 5.7 cm of average
height) was obtained in its natural state in a nearby area to the experi­
mental site; Typha latifolia (64.5 ± 3.5 cm of average height) and Cyperus
alternifolius (30 ± 1.2 cm of average height) were extracted from the
banks of the Misantla River where they develop naturally near an
irregular discharge of sewage. The use of well-developed plants from the
beginning was due to the fact that one of our goals was to evaluate the
production of flowers and we had the limit of the backyard pig rearing
cycle which is six months. Additionally, according to our personal
experience, the adaptation of vegetation is faster when well-developed
plants are used.
The experimental units were configured as follows regarding the
vegetation (Fig. 1):
• Three duplicated cells, with monoculture (Heliconia latispatha, Typha
latifolia and Cyperus alternifolius). Four individuals of each species
were planted evenly distributed in the cells.
• Two duplicated cells, with plant polyculture in two combinations
(Heliconia latispatha + Typha latifolia and Heliconia latispatha +
Cyperus alternifolius). Two individuals of each species were planted.
• Two duplicated cells, without vegetation. These cells were used as
control units to determine the vegetation effects on the pollutant
removals.
One of the main objectives of this study was to evaluate the perfor­
mance of Heliconia latispatha in combination with other plants used in
the treatment of wastewater of porcine origin, such as Typha latifolia and
Cyperus alternifolius (Hunt et al., 2002; Soda et al., 2012; Huang et al.,
2017). Compared with the other species, H. lathispatha is a species of
L.C.S. Herazo et al. Ecological Engineering 173 (2021) 106432

Fig. 1. Configuration of the pilot-scale HSSF TW with monoculture and polyculture of two species.

greater aesthetic value for the community and is easily available in the unit (gdw/m2).
surroundings where the study was carried out. BA = Average biomass from the aerial part (expressed as gdw/plant).
BR = Average biomass from the root part (expressed as gdw/plant).
2.2. Parameters and pollutant measurements NP = Number of plants counted into the experimental unit
(expressed as plant).
2.2.1. Environmental and control parameters 0.56 = Surface area of each cell (expressed as m2).
Ambient temperature, relative humidity was monitored three times
per day (between 9:00 a.m. to 10:00 a.m., 1:00 p.m. to 2:00 p.m. and 2.2.3. Pollutant measurement
6:00 p.m. to 7:00 p.m. respectively) with a JsmanTM digital hydrometer Once the system was presumably stabilized (2 months after the start-
thermometer, model HTC-1. Light intensity was measured with a Ster­ up), the pollutant concentrations in the influent and effluents of the cells
enTM lux meter model HER-410 between 12:00 to 13:00 h. In addition, were measured each week for 6 months (from 01/01/2020 to 25/06/
evapotranspiration was measured by quantifying inlet and outlet flow 2020). The study lasted 6 months, since it is the maximum cycle for
rates of the cells to calculate real pollutant concentrations in the backyard pig farming in rural communities in the region. The waste­
effluents. water quality parameters are shown in Table 1; samples were processed
Water temperature and pH were measured with a Hanna multi- immediately after sampling in the wastewater laboratory of the TecNM,
parameter portable meter model HI98121 and dissolved oxygen (DO) Campus Misantla.
was measured with a Milwaukee meter, model MW600, in the water at
both the inlet and outlet of each cell. 2.2.4. Experimental design and statistical analysis
The data were subjected to a two-way ANOVA using Minitab® v.16
2.2.2. Plant development (Minitab Inc., State College, Pennsylvania) and Tukey’s mean compar­
To investigate the vegetation development, the following plant ison test was carried out at p ≤ 0.05. A completely randomized design
measurements were taken in each cell three times (when planted, in the was used. Each cell was considered as the experimental unit; there were
third month, and sixth month of the study): plant height, width and leaf a total of 12 experimental units divided into six treatments with repli­
length (with a metric tape), stem thickness (with an UltraTech®) digital cations. Five treatments with plants were arranged in monoculture (1, 2
caliper) and leaf number (visually counted). Additionally, biomass and 3) and polyculture (4 and 5) systems: 1) Heliconia latispatha, 2)
production per square meter was quantified at the end of the experi­ Cyperus alternifolius, 3) Typha latifolia, 4) H. latispatha + Typha latifolia,
ment. For this, two individuals of each species were randomly chosen 5) H. latispatha + C. alternifolius; and one treatment as a control (without
from each monoculture and polyculture cell and were separated in aerial plant). Additionally, the Pearson correlation coefficient was calculated
and underground parts. Each part was washed with tap water and dried
with paper towels, then the fresh weight of each plant was obtained. Table 1
After that, the plants were dried in the open air for 8 days and finally Measured pollutants and methods used.
dried at a temperature of 105 ◦ C in an electric stove, for at least 3 h, until
Parameter Method Reference
reaching a constant weight. The results were expressed as dry weight of
biomass, both for the aerial and underground parts. The plant biomass COD (mg/L) Dichromate American Public Health
Association (APHA) (2005)
was calculated from the sum of the averages of dry weight for the aerial
Total coliforms MPN - NMX-AA-042- Galván and Lucio (2017).
and radical parts of the two chosen plants and the result was multiplied (NMP/100 mL) SCFI-2015
by plant density (number of plants) in each cell to obtain the total TSS (mg/L) Gravimetric American Public Health
biomass per surface unit (m2), as shown in the following equation. Association (APHA) (2005)
VSS (mg/L) Gravimetric American Public Health
NP x (BA + BR) Association (APHA) (2005)
BT = (1) TP (mg/L) Adenosine phosphate American Public Health
0.56
monohydrate Association (APHA) (2005)
where TN (mg/L) Chromotropic Acid American Public Health
Association (APHA) (2005)
BT = Total biomass –expressed as grams of dry weight per surface

3
L.C.S. Herazo et al.
using the same software for all variables. Mass removal efficiencies were
calculated for each pollutant.
3. Results and discussions
3.1. Description of environmental conditions and plant development
The study was performed under a tropical climate which was re­
flected in the values of the environmental parameters measured along
the six months of experimentation (Table 2). Such conditions were
adequate for the development of the plants used in the study. For
example, Heliconia latispatha grows best in a range of temperature of
18 ◦ C to 34 ◦ C, as well as in conditions of relative humidity greater than
50%; also, for this species, the high light conditions measured in this
study were adequate for its correct development (Jerez, 2007; Landero-
Torres et al., 2014). Concerning to Cyperus alternifolius, this species
spreads rapidly in high-temperature conditions (in environmental con­
ditions below 10 ◦ C its growth is paralyzed and its survival is difficult);
climates with high relative humidity (70 to 100%) (Ohga and Royse,
2004; Charris and Caselles-Osorio, 2016) and the light intensity condi­
tions of tropical climates are suitable for its development (Whittaker,
1972). Regarding Thypha latifolia, it is the most known wetland species
for its ability to grow in almost all climates. However, in warmer cli­
mates (such as tropical climates) its growth may be greater. It can sur­
vive temperatures up to 30 ◦ C in conditions of high or low relative
humidity (Li et al., 2004).
The value of evapotranspiration was calculated from the average
inflow volume per day (0.0304 ± 0.0015 m3/d) along the study and the
average outflow volume per day (0.0252 ± 0.0021 m3/d) during the dry
season. The value found in this study is similar to that found in tropical
climates in other reports (Yang et al., 2020). Additionally, it was very
interesting to note that similar to other studies in tropical climates, such
as that carried out in Colombia (Gutiérrez-Mosquera and Peña-Varón,
2011), the evapotranspiration rate did not show a significant difference
between planted and non-planted systems (p > 0.05). This suggests that
the water losses were mainly due to other physical factors rather than
the presence of plants, like solar radiation (Stewart et al., 1999; Watts
et al., 1999).
3.2. Vegetative growth
The different measurements of the plants taken throughout the
experimentation are shown in Fig. 2a-F. Fig. 2a shows that T. latifolia
was the species with the highest average plant height, reaching
maximum values of 2.6 m (monoculture) and 3.65 m (polyculture) in
height. These values are within the range reported for this species, from
1 to 4 m in height (Grace and Harrison, 1986; Vymazal, 2013). In
addition, Fig. 2(b and c) shows that this species exhibited the highest
average stem diameter (13 and 19 cm) and number of leaves (12 and 13)
in both monoculture and polyculture systems. Therefore, these results
are in line with the fact that T. latifolia has a faster growth rate compared
to other species and its use is recommended in wetland systems where
rapid vegetation cover is required (Butterworth et al., 2016). However,
when the vegetative growth data are transformed to the relative growth
rate (the number of times that the measurement parameter was
Table 2
Environmental parameters measured throughout the study.
Parameter Mean ± range
Ambient Temperature 28 ± 4
Humidity (%) 66 ± 12
Light Intensity (lux) 54,100 ± 14,300
Evapotranspiration (mm/d)* 9.3 ± 5.6
*
This value corresponds to dry periods, during rain periods values
could not be measured due to high precipitation; n = 69.
4
Ecological Engineering 173 (2021) 106432
increased throughout the six months of the study) (Table 3), the species
that showed the highest relative growth was H. latispatha in mono­
culture. This species registered a longitudinal growth of the stem 4 times
greater than the length observed when it was transplanted; that is, an
increase of 400% in height.
Accordingly, H. latispatha also recorded the second and fourth
highest rates of increase in stem length in polyculture wetland systems,
when planted in combination with T. latifolia and C. alternifolius, in
which its increase was 3.65 and 2.51 times, respectively, with respect to
the initial height of the stem. The maximum values of plant height
reached by H. latispatha ranged between 123 and 163 cm height. These
values are characteristic of this species, and they even exceeded the
values reported for some H. latispatha genotypes such as cultivars
‘Golden Torch’, ‘Distans’, ‘Kenya Red’ and ‘Tropics’ with average re­
ported plant heights of 61.98, 138.72, 88.74, 140.76 cm, respectively
(Kannan et al., 2019). Regarding the leaf width, H. latispatha was also
the species that not only registered the highest values, but was also the
species that showed the highest growth rates in leaf width at the end of
the study both in monoculture and polyculture (Fig. 2d and Table 3).
These results highlight the ability of this species to adapt to the mixture
of domestic and swine wastewaters. This enhanced its relative growth
even above species typically reported in natural wetlands such as
T. latifolia and C. alternifolius (Kipasika et al., 2016). In addition, even
though it has been reported that T. latifolia can displace other species in
polyculture systems (Escutia-Lara et al., 2010) for its rapid growth, the
results of the present work show that H. latispatha showed a better ca­
pacity to adapt to this type of wastewater than T. latifolia. In mono­
culture systems, the increase in plant density was higher for
C. alternifolius followed by H. latispatha and then by T. latifolia. However,
the general growth and plant density were higher for H. latispatha when
planted as polyculture (Table 3). This same pattern was observed in the
amount of total biomass produced by H. latispatha, being the species that
registered the highest dry weight per unit area (Table 4). With respect to
C. alternifolius, it was the species that was most affected when planted in
polyculture systems, exhibiting the lowest rate of increase (50%) in
plant density. In contrast, when planted as a monoculture, this species
showed the highest increase in plant density with an average number of
196.4 plants⋅m− 2 at the end of the study.
The number of flowers produced by the three species were impres­
sively high in the monoculture systems (Fig. 2f and Table 3). However,
when planted in polyculture systems, the three species showed a clear
reduction, but this reduction was less for H. latispatha. Therefore, the
greater capacity of H. latispatha to compete and dominate the other
wetland species when planted as a polyculture was confirmed.
Finally, regarding the amount of biomass produced in the different
systems, the results agreed with the previous ones. The highest total
biomass weight was produced by H. latipatha in both monoculture and
polyculture systems (Table 4), probably as a result of a better assimi­
lation of nutrients. In addition, it is important to highlight the differ­
ences when analyzing the distribution of biomass in aerial and
underground parts, since such differences are related to the way nutri­
ents are metabolized in the plant, specifically inorganic nitrogen. Ni­
trogen, both in the form of nitrate and ammonia, is taken up by the roots
of the plant and can be used in the same organ or transported to be used
in the aerial part of the plant (Bidwell, 1993). Some insights on this
matter are exposed by Gómez et al. (2012), who applied several ratios of
nitrate/ammonium to Heliconia psittacorum plants under hydroponic
conditions. They found that H. psittacorum responds to different nitrate/
ammonium ratios, for instance, the number of leaves per plant, foliar
area, stem diameter and root length were higher –but not statistically
different– at 85/15% NO3− /NH4+ ratio. At this same ratio of NO3− /
NH4+, they observed a higher accumulation of N, P, K, Ca, Mg, Fe and
Mn in the roots. Conversely, accumulation of N, P, K, Mg, Zn, Mn and B
in pseudostems was higher in plants treated with 68/32% NO3− /NH4+
ratio. Therefore, it is possible to hypothesize that the highest dry weight
of the roots for the three plant species may correspond to a more active
L.C.S. Herazo et al. Ecological Engineering 173 (2021) 106432

Fig. 2. Plant growth during the six-month study, planted in HSSF TW as monoculture and polyculture: a) Plant height, b) Number of leaves, c) Stem diameter, d) Leaf
width, e) Plant density and f) Number of flowers.

Table 3
Vegetative growth percentage increase rate for 6 months after vegetable species transplantation in HSSF TW fed with domestic and swine wastewater.
Variable* Monoculture system Polyculture system

H. latispatha & T. latifolia H. latispatha & C. alternifolius

Heliconia latispatha Cyperus alternifolius Typha latifolia H. latispatha T. latifolia H. latispatha C. alternifolius

Plant width 4 2.5 2.88 2.51 0.51 3.65 2.13

Leaf width 1.86 0.69 0.4 0.66 0.81 3.75 0.71
Number of leaves 0 1 1 1 0.44 0.33 0.14
Stem thickness 0.91 0.16 2.02 1.24 1 1.14 0.64
Number of flowers 63 110 24 16 0 26 4
Plant density 7 26.5 6.75 6 1 11.5 0.5
*
Percentage increase rate (%) = value x 100.

nitrogen metabolism in these organs. The root system represented the

Table 4 highest proportion of the total biomass dry weight for the three species
Root and total aerial biomass produced in plants (grams in dry weight per m− 2).
in both monoculture and polyculture systems (from 61.8% to 80.6%). It
Cultivation Plant Biomass* Biomass* Total* has been observed for different species of Heliconia that an extensive
system aerial root biomass
growth of the root system or rhizomes occur in response to soils with
Monoculture Heliconia 1857.1 3000.1 4857.1 water retention capacity or with temporary flood conditions. In this
latispatha way, the increase in the production of active cellulose (in the rhizomes)
Typha latifolia 1079.4 3183.1 4262.5
Cyperus 687.5 2848.2 3535.7
allow them to provide water and nutrients necessary to support the large
alternifolius amount of leaf area (Rundel et al., 1998; Guimarães Simão and Scatena,
Polyculture (1) Heliconia 812.5 1312.5 2125.0 2001).
latispatha
Typha latifolia 104.4 308.1 412.5
Polyculture (2) Heliconia 1450.9 2343.7 3794.6
3.3. Water temperature, dissolved oxygen, and pH
latispatha
Cyperus 18.7 77.6 96.4
alternifolius Table 5 shows the control parameters for this study. Water temper­
ature is an important parameter as it affects the speed of the different
reactions that take place in treatment wetlands as well as the solubility
of oxygen. The results ranged between 17.1 ± 0.9 and 23.6 ± 1.8 ◦ C,

5
L.C.S. Herazo et al.
Table 5
Control parameters in the HSSF TW (Mean ± Standard deviation, n = 46).
Parameter Influent Monoculture system
Heliconia latispatha Cyperus alternifolius
Temperature (◦ C) 23.6 ± 1.8 18.3 ± 0.9 18.7 ± 1.5
DO (mg/L) 1.4 ± 0.8 2.6 ± 0.9 2.7 ± 0.4
pH 6.7 ± 0.2 7.6 ± 0.1 7.8 ± 0.2
falling in the range reported as adequate for the removal of contami­
nants in this type of systems (Akratos and Tsihrintzis, 2007). Dissolved
oxygen concentration was increased significantly in the effluents.
However, it is likely that this increase was due to the exposure of the
effluent containers to atmospheric air. It is well known that in HSSF TW,
the internal conditions are mostly anaerobic given the constant satura­
tion of the system; microorganisms for the degradation of organic matter
and nitrification rapidly consume oxygen (Lin et al., 2020). The values
of pH in the influent were between 6.7 and 7.9 and increased signifi­
cantly on an average of 1.2 in the effluent of the systems. Such behavior
is similar to those found by Jia et al. (2017) in HSSF TW fed with swine
wastewater operating in similar conditions of this study.
3.4. Removal of organic matter, suspended solids and coliforms
3.4.1. Organic matter
Organic matter was measured as COD and the concentrations in the
influent were in the range of 969 ± 226 mg/L and 1663 ± 302 mg/L in
the dry season and between 98.5 ± 14 and 985 ± 119 mg/L in the rainy
season (from days 136 to 184) (Fig. 3a). With these concentrations,
organic loading rates were calculated for the dry and rainy seasons, as
well as for the entire period of experimentation (Table 6). The concen­
trations of COD found in this study were expected for a mixture of do­
mestic and swine WW. In previous studies, it was found that the average
concentrations of organic matter measured as biochemical oxygen de­
mand were 115.9 ± 23.1 mg/L (Sandoval-Herazo et al., 2018) and
111.8 ± 1.85 mg/L (Sandoval et al., 2019) for the same domestic
wastewater; these values of BOD5 correspond to a maximum concen­
tration of COD of around 400 mg/L (considering a BOD5/COD ratio of
only 0.29) In contrast, values of COD in the range of 3478 to 16,888 mg/
L have been reported in Mexico, for swine effluents from small farms of
up to 2500 pigs (Garzón-Zúñiga and Buelna, 2014a).
Despite the high concentrations of COD in the influent (average of
966.1 ± 460 mg/L), a highly significant reduction (p ≤ 0.001) of COD in
all the effluents was observed (ranging from 288.4 ± 138 to 417.4 ± 186
mg/L) (Fig. 3a). In the same way, highly significant differences (p ≤
0.001) were observed for the average removal efficiencies between
treatments, showing a tendency to higher efficiency in the polyculture
system (68.9 ± 10.6% planted with H. latispatha + T. latifolia; the lower
efficiency was found in the monoculture of H. latispatha (53.9 ± 11.2%).
Additionally, it is interesting to note that the unvegetated system was as
effective as the vegetated systems. These results indicate and support the
findings of other authors who argue that the sedimentation process is a
determining mechanism for the removal of COD in TWs for swine ef­
fluents (Akratos and Tsihrintzis, 2007; Headley and Tanner, 2012) in
addition to biodegradation. However, these results are probably mainly
due to the relatively short period of evaluation and could change after a
longer period of operation with the development of a variety of well-
established microbial communities that could enhance the biodegrada­
tion process in planted systems. On the other hand, these results are
higher than the 30–50% mentioned by Vidal et al. (2018) reported for
free water surface wetlands when treated swine effluents. However, our
results are lower in around 7.2 to 15.2% than the average efficiency of
76% reported by La Mora-Orozco et al. (2018) when treating digested
swine effluent with a COD concentration of 400–1200 mg/L in a HSSF
TW planted with Thypa sp., and Scirpus sp. These higher removals
compared to our study could be explained by the fact that during
Ecological Engineering 173 (2021) 106432
Polyculture system
Typha latifolia H. latispatha & C. alternifolius H. latispatha & T. latifolia Control
18.5 ± 0.4 17.1 ± 0.9 19.1 ± 0.6 18.6 ± 2.3
2.1 ± 0.7 2.8 ± 0.5 2.6 ± 0.2 2.0 ± 0.6
7.7 ± 0.1 7.9 ± 0.2 7.6 ± 0.2 7.4 ± 0.3
anaerobic digestion, recalcitrant organic matter is transformed into
more easily biodegradable products that, consequently, are more easily
removed in TW.
3.4.2. Total suspended solids
TSS concentrations during the study are shown in Fig. 3c, in both
influent and effluents of the systems. Average removals were found to
vary from 40.4% to 55.6% in the different systems, with highly signif­
icant differences between them (p ≤ 0.001). The most efficient systems
for TSS removal were those planted with H. latispatha (54.9 ± 0.3%) and
with H. latispatha + T. latifolia (55.6 ± 0.5%); while the least efficient
was the one planted with C. alternifolius (40.4 ± 0.2%), even less than
the control treatment. As expected, this behavior of the treatments was
practically repeated with the VSS (Fig. 3e-f), since the largest fraction of
the TSS is organic in nature. These results corroborate that the main
mechanism of removal of suspended solids, as well as COD, was sedi­
mentation. In this sense, and due to the high concentration of TSS in the
influent, the prior removal of TSS through a primary treatment is highly
recommended to avoid the clogging of the TWs in the mid-term in real-
scale systems. Although no signs of obstruction were observed during
the 6-month study. On the other hand, the contribution of plants to
sedimentation process and solids retention in their roots is ratified as
well as the importance of adequate selection of. It is interesting to note
that the species with the lowest efficiency (C. alternifolius) was the one
that recorded the highest plant density (Table 3) and the lowest root
biomass quantity (but not much different from the other two species).
This probably indicates that not only the quantity of roots is determinant
for the removal of TSS, but the way in which the root system develops.
Other authors when treating swine effluents (Escalante-Estrada et al.,
2019) have already reported the influence of plants on VSS removal. On
the other hand, similar to our results, González et al. (2009) found TSS
removefficiencies in HSSF TW fed with swine wastewater ranging from
35% to 78%. These authors argue that in tropical climates TSS removal
is influenced by three important factors: 1) the season of the year –dry or
rainy-; 2) the great variation in the composition of swine waste; and 3)
the presence/absence of vegetation in the wetlands. Regarding the last
factor, the authors concluded that the differences found between sys­
tems with and without plants (or between different species) were not
clear and that high concentrations of pollutants could probably mask the
contribution of the plants (Fimbristylis spadicea, Typha latifolia, Eleocharis
interstincta, A. berteroniana and Cladium jamaicensis) in the removal of
pollutants. Probably, in this study it was possible to identify the influ­
ence of plants due to the lower concentrations of TSS.
3.4.3. Total coliforms
TC concentrations and removal efficiencies in the systems are shown
in Fig. 3g and h, respectively. In general, the removals were low and
ranged from 52 to 69%. These values are much lower than the 92%
found by Zurita and Carreón-Álvarez (2015) in HSSF TWs planted with
Canna hibrids for the treatment of domestic wastewater. One explanation
for these low results is the fact that TCs are capable of growing in
polluted and even in non-polluted waters (Zurita and Carreón-Álvarez,
2015). TCs easily reproduce in swine wastewater given the high pres­
ence of organic matter and nutrients (La Mora-Orozco et al., 2018). In
this specific case, although the concentrations of organic matter and
nutrients are lower than those present in pig wastewater (Garzón-Zúñiga
and Buelna, 2014b), they are higher than those found in domestic
6
L.C.S. Herazo et al. Ecological Engineering 173 (2021) 106432

Fig. 3. Concentration and percentage of elimination of COD (a, b), TSS (c, d), VSS (e, f) and TC (g, h) in the different monoculture and polyculture HSSF TW.

wastewater in the study area (Sandoval et al., 2019). On the other hand,
highly significant differences (p ≤ 0.001) were found among treatments
for TC reduction. Similar to what was found for TSS, the least effective
system was the one planted with C. alternifolius, followed by the control
treatment. The other systems showed similar efficiencies, although those
with polyculture of H. latispatha + T. latifolia and with monoculture of
H. latispatha showed a tendency towards higher values. With respect to
the system without vegetation, in general, a greater variability in the
results was found, with a lower average value compared to some of the
systems with vegetation. This coincides with Kipasika et al. (2016), who

7
L.C.S. Herazo et al. Ecological Engineering 173 (2021) 106432

Table 6 in the area, evaluated in previous studies (99.3 ± 25.78 mg/L) (Nakase
Average values (± SD) of organic loading rates (g of COD/m2.d). et al., 2019); although it is lower than the values recorded for swine
Treatments Rainy season Dry season Both seasons effluents (around 2034 mg/L) in Mexican farms (Garzón-Zúñiga and
Buelna, 2014a). On the other hand, as expected, highly significant dif­
Influent 38.71 ± 33.99 126.15 ± 25.25 99.54 ± 49.27
Heliconia latispatha 18.62 ± 16.16 53.67 ± 6.42 43.01 ± 19.23 ferences were found between treatments (p ≤ 0.001). The systems with
Cyperus alternifolius 15.15 ± 14.24 50.84 ± 11.54 39.98 ± 20.64 vegetation were more effective compared to the control treatment. The
Typha latifolia 14.58 ± 13.64 48.91 ± 12.69 38.46 ± 20.49 most efficient systems were those planted with Typha latifolia, both in
H. latispatha + C. alternifolius 13.19 ± 12.74 49.06 ± 11.45 38.15 ± 20.39 monoculture and polyculture, followed by the system with H. latispatha
H. latispatha + T. latifolia 11.47 ± 10.76 37.69 ± 6.57 29.71 ± 14.56
Control 15.20 ± 13.71 44.83 ± 6.01 35.81 ± 16.41
+ C. alternifolius and finally the systems with monocultures of
H. latispatha and Cyperus alternifolius. These results indicate that poly­
culture systems tended to be better for TN removal for this type of
found that wetland systems planted with macrophytes such as effluent. The TN removal percentages found in this study varied between
C. alternifolius, C. papyrus, P. mauritianus, and T. latifolia -in mono­ 68.1 and 74.9% in the systems with vegetation and were higher on
culture- positively influenced the removal of pathogenic bacteria from average between 12.5 and 19.3% with respect to the control treatment.
wastewater. Other authors agree that the presence of vegetation con­ These percentages are high in comparison to those found in TWs for the
tributes to the reduction of pathogens due to the release of antibiotics in treatment of domestic wastewater (Torres et al., 2017) and are even
the root zone and that the type of species is determinant (Zurita and higher if it is considered that the concentration of TN in the effluent was
Carreón-Álvarez, 2015; Marín-Muñiz et al., 2020; Du et al., 2020). higher than that in a typical domestic wastewater. Among the TN
removal mechanisms, the uptake of NH4+ by plants is probably found,
since it is the inorganic form of nitrogen preferred by most macrophytes
3.5. Removal of nitrogen and phosphorus
(Del Toro Farías and Zurita Martínez, 2020) and the vigorous develop­
ment of the vegetation was evident as discussed above. In tropical
3.5.1. Total Nitrogen
conditions such as those prevailing in the region where the study was
The concentrations and removal of TN in the different systems are
conducted, it is typical to observe the development of thicker stems,
shown in Fig. 4a-b. TN in wastewater is mainly composed of organic
larger leaves, and the production of a greater number of offsprings in the
nitrogen, ammonium, and nitrate. In the case of swine effluents, re­
vegetation (Casierra-Martínez et al., 2017). Nitrogen is assimilated
ported in Mexico, more than 85% of the nitrogen is in the form of
within the plant forming amino acids, proteins, organic compounds
ammonium (Garzón-Zúñiga and Buelna, 2014a). Similar to the other
(Yadav et al., 2017) and participates directly in the formation of chlo­
parameters, TN concentrations in the influent were very different during
rophyll, so there is a positive correlation between the content of chlo­
the dry and rainy seasons (which began from the day 136), recording
rophyll and nitrogen in the leaves; that is, N stimulates vegetative
average values of 219.4 ± 13 mg/L and 63.2 ± 6.2 mg/L, respectively;
growth. Another probable route of elimination of N was the trans­
while throughout the study, the average concentration was 171.9 ±
formation of NH4+ to NO3− by the action of ammonium-oxidizing
74.3 mg/L. This value is substantially high for the municipal wastewater

Fig. 4. Concentration and percentage removal of TN (a, b) and TP (c, d) in the different monoculture and polyculture HSSF TW.

8
L.C.S. Herazo et al.
bacteria in the rhizosphere; which was then denitrified by heterotrophic
bacteria in the anoxic/anaerobic zones of the systems (Yadav et al.,
2017; Arteaga-Cortez et al., 2019). This may have been favored by the
environmental conditions shown in Table 2 that stimulate microbial
processes in TWs and are characteristic of tropical climates (Rodríguez-
Domínguez et al., 2020). In addition, denitrification was carried out
efficiently due to the high C/N ratio in the influent (5.6). According to
different authors, a low C/N ratio is the main factor that limit such
process and consequently, TN removal, which was not the case in this
study (Del Toro et al., 2019; Del Toro Farías and Zurita Martínez, 2020).
3.5.2. Phosphorus
The behavior of TP concentrations during the study are shown in
Fig. 4c. For this parameter, highly significant statistical differences (p ≤
0.001) were found between treatments. TP concentrations in the efflu­
ents varied between 39.8 and 21.7 mg/L. Similar to what was observed
with respect to TN, all systems with vegetation were more effective than
the system without vegetation. The system with the highest removal
percentage was the monoculture system with H. latispatha (63.4 ±
0.43%) followed by the system planted with H. laptispatha + T. latifolia
(58.5 ± 0.03%) and then the monoculture system with T. latifolia (55.4
± 0.18%). Again, the least effective system was the monoculture system
with C. alternifolius (44.3 ± 0.55%). In general, the systems with vege­
tation removed 11.4 to 30.5% more TP than the system without vege­
tation (Fig. 4d). According to the results, the species that most
contributed to the removal of TP was H. latispatha, since the systems
planted with this species both in monoculture and in polyculture (with
T. latifolia) registered the highest removal percentages. In general, high
levels of phosphorus positively affect plant growth and increase biomass
accumulation, since phosphorus plays an important role in various
metabolic processes. Phosphorus is a constituent of nucleic acids,
phospholipids of cell membranes and coenzymes that activate the pro­
duction of amino acids used in synthesis of proteins, DNA, RNA and ATP
(Chrysargyris et al., 2016). This is congruent with the plant development
(Table 3) and biomass production (Table 4) observed in the systems in
this study. It is probable that the greater intensity of light and temper­
ature (Table 2), in the tropical conditions where the study was carried
out, could have favored the vegetation development, promoting
removal processes through the plants, as indicated by Wu et al. (2013).
In addition, the high presence of iron dioxide in tezontle (Zurita et al.,
2006) potentially reacts with phosphates. Furthermore, it is likely that
part of the phosphorus was also removed with the suspended matter,
through sedimentation and retention processes, in addition to physico­
chemical processes such as interaction with the filter media. On the
other hand, our results were lower than the 82% obtained by Anh et al.
(2020) in HSSF TW with different combination of filter material (gravel-
sand-limestone and gravel-limestone-rice husk) and planted with
Phragmites australis and Cyperus altenifolius. The explanation of these
higher removals in comparison to our study was the precipitation of P
resulting from the high content of Ca in limestone, as well as the P-
sorption on the sand.
4. Conclusions
The results of this study demonstrate that HSSF TWs, planted with
monocultures and polycultures of plants in tropical climates represent
an option to reduce the pollutant load of wastewater resulting from the
mixing of domestic wastewater and pig raising, which is a widespread
activity in rural areas of developing countries such as Mexico. However,
despite the efficiencies found for the removal of organic matter, sus­
pended solids, TC, nitrogen, and phosphorus, it is evident that a single
treatment stage is not sufficient, so future studies should focus on the
inclusion of another type of TW as part of a treatment train to achieve a
more complete decontamination of this type of effluent that could
comply with Mexican standards for effluents that are discharged into
surface water bodies. This treatment train must include a sedimentation
9
Ecological Engineering 173 (2021) 106432
process for the reduction of TSS, due to its high concentration, to avoid
the clogging of the TWs in the mid-term. Also, it is necessary analyze
other mechanisms of N removal. On the other hand, it was found that a
determining factor in the efficiency of the systems was the species of
macrophyte and its configuration as a monoculture or polyculture. The
most effective system was that with polycultures of H. latispatha + T.
latifolia plants for the removal of organic matter (measured as COD),
TSS, VSS, TC and TN, and the second most efficient in the removal of TP.
In contrast, the system with the worst performance was the monoculture
with C. alternifolius. Therefore, the efficiency is related to the develop­
ment of each species and its capacity for adaptation and growth in the
presence of high concentrations of organic matter and nutrients. For this
type of effluent, the best adapted species were H. latispatha and T. lat­
ifolia. However, H. latispatha was the species that showed the highest
relative growth in both monoculture and polyculture; it was also the
dominant species and negatively affected the growth of T. latifolia and
C. alternifolius in polyculture. This species was mainly determinant for
phosphorus removal, which may be related to its predominance in the
highest flower production, as well as the greater accumulation of total
biomass.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This study was funded by the Tecnológico Nacional de México in the
Call 2019 “Support for Scientific and Technological Research”. Project
“Treatment of wastewater produced by pig micro-enterprises in Vera­
cruz, Mexico through artificial wetlands (Code 503.19-P).
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