Scientia Horticulturae 253 (2019) 341–348

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Seed weight predicts seedling emergence, and extremely acid soil and low T
availability of Phosphorus are associated with poor plant performances in
Lepidium meyenii Walpers (maca)
⁎
A. Lozano-Canalesa, M. Janampa-Santomea, Daniel Clarkb, Wilfredo L. Gonzálesa,
a
Laboratorio de Ecología Evolutiva, LID, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, Lima 31, Peru
b
Laboratorio de transformación de plantas, Unidad de genómica, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, Lima 31, Peru

A R T I C LE I N FO A B S T R A C T

Keywords: Lepidium meyenii Walpers (maca) is a Peruvian species cultivated in the high Andean region (ca. 4000 m.a.s.l.),
Maca highly praised for the nutritional properties of its hypocotyl. The benefits to human health and their relationship
Environmental stress with the hypocotyl have been well investigated. However, few studies have addressed the factors affecting field
Plant growth crop performance and the improvement of agronomic practices. Here we evaluate the effect of soil properties
Seed weight
(humidity, temperature, and fertility) and sowing method (ridge-furrow system and flat planting) on the bio-
Soil acidity
Phosphorus deficiency
logical performance of five seed accessions of maca in 6 experimental plots along an altitudinal gradient
(3554–4442 m.a.s.l.). Plots located at both the lowest and highest altitudes had lower plant survival, vegetative
growth, and hypocotyl size. Most of the differences among plots could be attributed to the acidity and the
concentration of available phosphorus in the soil. In addition, low soil temperature and humidity negatively
affected crop performance at different stages of plant development. The ridge-furrow system appeared to pro-
mote plant growth, although it did not favor plant survival under the unexpected climatic conditions experi-
enced. Finally, seed weight was found to be a good predictor of seedling emergence and plant survival.

1. Introduction
In high mountain ecosystems, agriculture is strongly affected by
environmental conditions. In particular, the high Andean region (Puna)
is characterized by infertile soils, freezing temperatures, long periods of
drought, and high UV radiation (Wilcox et al., 1988; Baied and
Wheeler, 1993); all of these cause severe stress on crop development
(Fonte et al., 2012).
Under this challenging environment, few species, such as the
Andean root and tuber crops, have evolved underground storage organs
as a strategy for survival (Flores et al., 2003). Among these species,
Lepidium meyenii Walpers [Brassicaceae], also known as maca, grows up
to an altitude of 4500 m.a.s.l., along with native grasses such as Festuca,
Poa, Stipa, Calamagrostis, Muhlenbergia, Bromus, and Agrostis species
(Wilcox, 1984), several varieties of bitter potatoes (Hermann and
Bernet, 2009), and species from other plant families such as Asteraceae,
Bromeliaceae, Cactaceae, as well as others (Kuentz et al., 2007). Maca is
cultivated for its edible hypocotyl, which has a nutritional value com-
parable to that of cereal grains such as maize, wheat, and rice (Quiros
and Aliaga, 1997). The hypocotyl is also appreciated for its multiple
pharmacological properties, including the improvement of sexual
function, vitality, and memory, as well as the control of anxiety (Wang
et al., 2007; Gonzales, 2012).
Different types of maca have been described according to the color
of its hypocotyl. Each color is suggested to have a distinct chemical
composition (Clément et al., 2010) and biological activity (Gonzales
et al., 2009; Gonzales, 2012), and thus a particular biological perfor-
mance. Because of these differences, consumer interest has shifted to
certain colors (e.g. red and black), leading some farmers to produce
seeds from specific colors. However, one of the main problems with
maca is the poor management of the botanical seed production as a
consequence of non-uniform practices among farmers (Quiros and
Aliaga, 1997), which not only affect seed quality but also introduce
considerable variation in plant performance.
Besides seed quality, environmental conditions impose serious
challenges to maca performance in the field. Poor soil quality and harsh
environmental conditions make the Puna region nearly infertile
(Romero, 2005). Soils are strongly acidic (pH < 4.5, Wilcox et al.,

⁎
Corresponding author.
E-mail addresses: alejandra.lozano.c@upch.pe (A. Lozano-Canales), maria.janampa@upch.pe (M. Janampa-Santome), daniel.clark@upch.pe (D. Clark),
wilfredo.gonzales@upch.pe (W.L. Gonzáles).

https://doi.org/10.1016/j.scienta.2019.04.059
Received 15 February 2018; Received in revised form 19 April 2019; Accepted 23 April 2019
Available online 28 April 2019
0304-4238/ © 2019 Elsevier B.V. All rights reserved.
A. Lozano-Canales, et al.
Fig. 1. Geographical location of the experimental plots. “Meseta del Bombón”: CL (4442 m.a.s.l. - 10°53.778′ S 76°02.294′ W), NP (4187 m.a.s.l. - 10°52.482′ S
76°05.007′ W), OL (4173 m.a.s.l. - 11°08.889′ S 76°04.919′ W), OP (4104 m.a.s.l. - 11°08.598′ S 76°04.712′ W). “Valle del Mantaro”: AA (3820 m.a.s.l. - 12°10.297′ S
75°22.427′ W), MM (3554 m.a.s.l. - 11°46.288′ S 75°25.743′ W).
1988), which may affect the early developmental stages of the plant
(Shoemaker and Carlson, 1990; Yan et al., 1992). Also, they have a slow
nutrient cycling, which may limit agriculture (Rolando et al., 2017);
low availability of phosphorus, due to high reactivity in the soil matrix,
and reduced nitrogen availability, associated with a slow decomposi-
tion of organic matter (Fonte et al., 2012; Holford, 1997; Sarmiento and
Bottner, 2002). As for climatic variables, the daily temperature varia-
tion is higher than the seasonal temperature variation, with recurrent
nocturnal frosts (Wilcox et al., 1988). These increase the risk of crop
failure, as low temperatures may affect several physiological processes
and delay or stop the early developmental stages of the plant (Jacobsen
et al., 2003). Precipitation shows a strong seasonal variation: the rainy
season takes place between October and March and is followed by a
long period of drought (Winterhalder and Thomas, 1978; Wilcox et al.,
1988). However, rainfall is irregular in the Puna, often leading to re-
duced yields for crops managed under rainfed conditions, as in the case
of maca (Fonte et al., 2012). Some environmental conditions, including
irregular frequency of rainfall, frosts, and soil nutrient deficiency, are
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Scientia Horticulturae 253 (2019) 341–348
expected to become intensified over the next years as a result of climate
change and of unsustainable and intensive agricultural practices
(Thibeault et al., 2010; Rolando et al., 2017; Lobell and Gourdji, 2012).
Despite the increasing demand for maca in the market, the crop
yield is usually far from optimal, mainly due to frosts and unstable
rainfall regimes. Research carried out to understand the effects of en-
vironmental conditions on plant performance is scarce, and only a few
local technical studies have proposed agronomic measures to improve
crop yield. Moreover, because of the interest in producing seeds from
particular hypocotyl colors, selection of good quality seeds becomes
critical to ensure better plant performances. However, criteria to
identify good quality seeds have not been established so far, thus urging
the need to investigate whether seed attributes such as the source
(hypocotyl) color and/or seed weight significantly influence plant
performance. The aim of this study was to evaluate the influence of soil
properties (humidity, temperature, and fertility), seed traits and sowing
methods on the biological performance of maca.
A. Lozano-Canales, et al.
2. Materials and methods
2.1. Botanical description
Maca is an herbaceous biennial plant of the Brassicaceae family. The
vegetative stage, which was the subject of this study, is characterized by
decumbent stems with little branching, and large and fleshy leaves
arranged in rosettes over the soil surface. An underground storage
organ, formed by the taproot and the lower part of the hypocotyl, is
developed during this stage (Quiros and Aliaga, 1997). This organ is
commonly known as hypocotyl and displays a variety of colors from
purple to cream and yellow (León, 1964).
2.2. Seed source
Seeds harvested in 2015 were provided by maca producers from the
Junín region (Perú). Accessions differed in hypocotyl color [red (R),
black (B) and yellow (Y)], and source [Junín (J) and Chupaca (C)]. The
5 accessions used are hereinafter referred to as: RJ, BJ, YJ, BC, and YC.
The seeds were cleaned, weighed, and stored in vials at 4 °C until
sowing. The mean weight (performed in triplicate) of 1000 seeds per
accession was: 0.7253 g for RJ; 0.6787 g for BJ, 0.8817 g for YJ; 0.4560
g for BC and 0.8057 g for YC.
2.3. Field experiment
2.3.1. Land characteristics and conditioning of the plots
Six plots were located between 3550 and 4450 m.a.s.l in 5 districts
within 2 maca producing areas from the Pasco and the Junín regions
“Meseta del Bombón” and “Valle del Mantaro”. Four plots were estab-
lished around Lake Junín (Meseta del Bombón) in the districts of
Óndores (referred to as OP and OL, province of Junín), Carhuamayo
(CL, province of Junín), and Ninacaca (NP, province of Pasco). The
other two plots were located in “Valle del Mantaro”, in the districts of
Yanacancha (AA, province of Chupaca) and Masma (MM, province of
Jauja) (see Fig. 1).
According to the farmers, the lands used in the experiment were
“virgin” (without previous agricultural use). A few months before
sowing, clods were broken up to aerate the soil and improve nutrient
content by favoring the decomposition of the removed weeds (a tech-
nique called “roturado” and commonly used by farmers). Neither water
irrigation, pesticides nor fertilization were used in the plots during
plant growth.
2.3.2. Experimental design
The experiment was conducted from December 2015 through July
2016. Each plot (total area: 6 m x 12 m) was divided into 4 adjacent
blocks (6 m x 3 m) alternating 2 sowing methods: ridge-furrow method
(RF) and flat planting method (FP). For the ridge-furrow method, fur-
rows were excavated (without filling them with water) and the soil
removed was used to form raised sowing beds (ridges); in the flat
planting method (FP), the soil was leveled out. Each block had five 6-m
long rows, with a single accession sown per row. Forty sowing spots
separated by 15 cm were established along each row, with three seeds
planted per spot (N = 120 seeds). The night before sowing, the seeds
were treated for 1 h with gibberellic acid (400 mg/L) to promote ger-
mination and ensure the survival of at least 1 seed per sowing spot.
Some farmers increase their production with this germination promoter
(commercially known as “gibberellin”). Seeds were sown on December
18, 2015, in “Meseta del Bombón”, and on January 2, 2016, in “Valle
del Mantaro”. The time gap was due to a delay in the rainy season
caused by El Niño/Southern Oscillation (ENSO). Plant performance and
soil properties were assessed monthly, whenever possible. Harvest took
place in June and July 2016, according to the growth and maturity of
the plants at each plot.
In order to explore whether seed weight was positively associated
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Scientia Horticulturae 253 (2019) 341–348
with successful plant establishment, an additional experimental plot
was observed from October 2016 to July 2017 (Carhuamayo, 4172
m.a.s.l.). Regular climatic conditions were registered in the working
area during this experiment. Sixteen seed accessions from hypocotyls of
different colors and producers were evaluated. Seven accessions had 3
replicated blocks as part of an independent research project, whereas
each of the remaining had only one block. A total of 30 blocks (5 m x 2
m each) were installed in a plot of 43 m x 12 m. Seed accessions were
randomly sown in the blocks and plant survival was evaluated at each
block after 70 days. The mean percentage of seedling emergence by
seed accession is reported.
2.4. Measurements
2.4.1. Soil characterization
Three random soil samples were collected from each plot at 15–20
cm depth, roughly every two months, to determine moisture content
and fertility parameters. Moisture content was estimated in all samples
by the gravimetric method. As for the fertility parameters, the 3 sam-
ples of a plot were mixed to carry out the following analyses: pH (1:1),
available phosphorus (P) (Olsen method), available potassium (K)
(Ammonium Acetate Method), organic matter content (OM%; Walkley
and Black method), electrical conductivity (EC (1:1)), and exchange-
able acidity (Al+3+H+; Yuan method). Soil temperature was registered
every 30 min on a daily basis with a digital sensor (HOBO Pendant®
Temperature/Light 8 K Data Logger, Part#UA-002-08) placed at 4 cm
depth.
2.4.2. Plant performance
All measurements were made at the vegetative stage of maca. As
part of this study we report: plant survival at harvest (165–190 days
after sowing at “Valle del Mantaro” and 220 days after sowing at
“Meseta del Bombón”, approximately), vegetative growth, and phy-
siological performance (Optimal Quantum Yield [Fv/Fm], measured
with a Fluorimeter - OS-30 P, Opti-Sciences, USA) at the middle of the
experiment (approximately 130 days after sowing), when the hypocotyl
was already formed and the rosette was fully developed. For the latter
two variables, at least 15 plants per accession per row were randomly
evaluated. Harvest took place in June-July according to the growth and
maturity of the plants at each plot. Plants were harvested distinguishing
them by seed accessions and sowing methods. The hypocotyl fresh
weight (FW) at harvest was considered sufficient to estimate crop yield
because it showed a strong correlation with its dry weight (Pearson
correlation, r = 0.98, p < 0.05, N = 300 samples). Each variable was
analyzed against plots, accessions and sowing methods.
2.5. Data analysis
All variables related to plant performance were analyzed using a
main effects ANOVA design with three factors (plot, seed accession, and
sowing method) followed by a Fisher LSD post hoc test. No interactions
were included in our model due to poor or null plant survival with some
treatment combinations (e.g. plot x seed accession, plot x sowing
method). Soil moisture content was analyzed with a two-way factorial
ANOVA (factors: date and plot); only dates for which data was available
from all 6 experimental plots were included in the analyses. Because the
soil fertility parameters were statistically correlated, we conducted a
principal component analysis (PCA). The first two components (PC1
and PC2) accounted for more than 71% of the total variance. We used a
multivariate analysis of variance (MANOVA) to determine whether the
plot had a significant effect on both principal component scores. Since
that was indeed the case (Table 2), individual principal components
were analyzed using a one-way ANOVA followed by a Fisher LSD post
hoc test. To determine if seed weight is a good predictor of plant sur-
vival, a quadratic univariate regression model was fitted with data from
the experimental plot established in October 2016.
A. Lozano-Canales, et al. Scientia Horticulturae 253 (2019) 341–348

Table 1
Descriptive statistics of chemical variables in six experimental plots. Means sharing a letter are not significantly different (p < 0.05, Fisher LSD post-hoc test). Plots:
MM (Masma), AA (Achipampa), OP and OL (plots in Óndores), CL (plot in Carhuamayo) and NP (plot in Ninacaca).
Plot pH P ppm K ppm MO (%) EC (es) Al+3 + H+ (meq/100)

OP 6.54 ± 0.08 a 27.08 ± 3.18 a 155.83 ± 20.06 c 9.24 ± 0.50 b 0.61 ± 0.11 b 0.00 ± 0.00 d
OL 4.83 ± 0.08 b 18.60 ± 2.42 b 179.33 ± 25.20 bc 12.22 ± 0.63 a 0.52 ± 0.13 b 0.68 ± 0.12 bc
NP 4.92 ± 0.07 b 24.84 ± 4.76 ab 219.40 ± 26.87 b 10.01 ± 1.01 b 1.27 ± 0.24 a 0.26 ± 0.06 cd
AA 4.55 ± 0.05 c 5.76 ± 0.50 c 333.80 ± 1.83 a 9.54 ± 0.44 b 1.48 ± 0.27 a 0.40 ± 0.05 cd
CL 4.37 ± 0.09 c 7.60 ± 2.67 c 151.00 ± 22.62 c 9.10 ± 0.62 b 0.38 ± 0.05 b 2.62 ± 0.40 a
MM 4.53 ± 0.08 c 8.43 ± 1.43 c 147.50 ± 19.96 c 1.51 ± 0.25 c 0.16 ± 0.04 b 1.00 ± 0.21 b

3. Results

3.1. Soil characterization

3.1.1. Chemical composition

Soils of all plots were acid (pH range from 6.5 to 4.3), non-saline
(EC < 2 dS/m; Richards, 1954), and showed no available potassium
deficiency (K > 131 ppm; Mallarino et al., 2003). Plots from MM and
CL had the highest concentration of exchangeable acidity Al+3+H+
(> 1.00 meq/100) and, along with AA, the lowest levels of available
phosphorous (P < 5–10 ppm). In addition, MM had the lowest organic
matter content (< 2%) compared to the remaining plots (> 9%)
(Table 1).

3.1.2. Moisture content

Both date and plot had significant effects on soil moisture content. Fig. 2. Soil moisture content at the plots throughout the experiment. Data
From day 80 after sowing onward, soil moisture tended to decrease, presented are mean values + 1 S.E. Plots: MM (Masma), AA (Achipampa), OP
except for sudden increases due to sporadic rainfalls, as observed in OP and OL (plots in Óndores), CL (plot in Carhuamayo) and NP (plot in Ninacaca).
(Fig. 2). The soil from plots AA and MM, located near “Valle del
Mantaro”, reached the lowest moisture contents at the end of the ex-
periment through different paths: while AA underwent a pronounced
moisture content reduction, MM showed the lowest values during the
entire period examined (less than 9%; Fig. 2).

3.1.3. Temperature
Soil temperature decreased over time in all plots. The mean and
minimum daily temperatures were higher at AA and MM in the first
three months after sowing (0–90 days), whereas the lowest values were
registered at CL and NP. The plots located at the highest (CL) and the
lowest (MM) altitudes, which showed the poorest plant development,
were also those where the lowest (CL) and the highest (MM) soil tem-
peratures were registered during the entire experiment (Fig. 3).

3.2. Plant performance

3.2.1. Plant survival

The three factors considered for the analyses - plot, seed accession,
and sowing method - had a significant effect on plant survival. Plots
located at intermediate altitudes (plots in Óndores, OP and OL) showed
the highest plant survival (˜18% and ˜15%, respectively). While the post Fig. 3. Soil temperature (mean, maximum, minimum) at the plots throughout
hoc test did not find significant differences among the remaining plots, the experiment. Plots: MM (Masma), AA (Achipampa), OP and OL (plots in
Óndores), CL (plot in Carhuamayo) and NP (plot in Ninacaca).
Table 2
Results of MANOVA and one-way ANOVAs performed to test the plot effect on
the first two principal components. Significant effects are highlighted in bold.
the lowest plant survival (˜2%) was observed in those plots located at
either the highest (Carhuamayo, CL) or the lowest (Masma, MM) alti-
Wilks' λ F DF p tude (Fig. 4A). The accessions associated with black hypocotyls had low
MANOVA survival percentages (BJ: ˜7%; BC: ˜5%) as compared to the remaining
Plot 0.030 22.991 10. 48 < 0.0001 accessions (Fig. 4B). As for the sowing methods (Fig. 4C), more plants
Univariate ANOVAs survived with flat planting method (˜10%) than using the ridge-furrow
PC1 method (˜6%). Results from the experimental plot established in Oc-
Plot 31.977 5. 25 < 0.0001
tober 2016 revealed a positive association between seed weight and the
PC2
Plot 16.865 5. 25 < 0.0001 mean percentage of seedling emergence (quadratic regression model,

344
A. Lozano-Canales, et al. Scientia Horticulturae 253 (2019) 341–348

Fig. 4. Variables related to plant performance according to: plots, seed accessions and sowing methods. Data presented are mean values ± 1S.E. Means sharing a
letter above bar are not significantly different (p < 0.05, Fisher LSD post-hoc test). Plots: MM (Masma), AA (Achipampa), OP and OL (plots in Óndores), CL (plot in
Carhuamayo) and NP (plot in Ninacaca). Seed accessions: RJ, YJ and BJ (red, yellow and black accessions from Junín), YC and BC (yellow and black accessions from
Chupaca). Sowing method: RF (ridge-furrow method) and FP (flat planting method) (For interpretation of the references to colour in this figure legend, the reader is
referred to the web version of this article).

345
A. Lozano-Canales, et al.
Fig. 5. Quadratic regression model between seed weight and mean percentage
of seedling emergence in the experimental plot implemented during October
2016. Seed accessions are represented by each dot (N = 16).
R2 = 60%, Fig. 5); therefore, accessions with higher seed weight had a
greater percentage of seedling emergence than those with lighter seeds.
The data allowed us to identify an optimal maca seed weight with re-
gard to seedling emergence, which ranges from 0.6 to 0.7 g per 1000
seeds.
3.2.2. Vegetative growth
Both the number of leaves and the rosette diameter were sig-
nificantly affected by the plots. Larger rosette diameters (˜13-18 cm;
Fig. 4A) and a higher number of leaves (˜14-17; Fig. 4A) were observed
in plants from OL, followed by OP and NP. As in the case of plant
survival, plants from plots located at the highest and the lowest alti-
tudes showed common features. CL and MM plants had smaller rosettes
(˜4-6 cm; Fig. 4A), and MM plants had the smallest number of leaves
(˜4), closely followed by CL plants (˜7; Fig. 4A). Seed accession only had
a significant effect on rosette diameter, which was smaller in BJ, YC,
and BC (˜13 cm) than in the remaining accessions (˜14-15 cm; Fig. 4B).
Sowing methods affected only the number of leaves: plants from the
ridge-furrow method possessed a higher number of leaves (˜14) than
those from flat planting method (˜12; Fig. 4C).
3.2.3. Physiological performance
Physiological performance, estimated as the Optimal Quantum
Yield (Fv/Fm), was significantly different among plots and slightly
different among seed accessions. No significant differences could be
detected between sowing methods. Sub-optimal Fv/Fm ratios were
observed only in the plot at the lowest altitude (MM: ˜0.55), indicating
that those plants did experience physiological stress (Fig. 4A). The Fv/
Fm ratios of plants grown from different seed accessions were statisti-
cally different but fell within the optimal range (Fig. 4B).
3.2.4. Crop yield
Crop yield, reflected by the hypocotyl FW, was significantly dif-
ferent among plots. The heaviest hypocotyls were harvested at OL (˜29
g), followed by OP (˜15 g) and CP (˜12 g), whereas much lower hy-
pocotyl FW values were found at CL (˜4 g), AA (˜2 g) and MM (˜0.2 g)
(Fig. 4A). Neither seed accessions nor sowing methods affected yield
significantly.
3.3. Fertility parameters and their relation with plant performance
According to PCA, two components accounted for more than 71% of
the total variance. While pH, available P, and Al+3+H+ contributed to
PC1, available K and EC contributed to PC2 (Fig. 6A) The PC1 graph
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Scientia Horticulturae 253 (2019) 341–348
established a correspondence with plant survival and yield. Thus, the
combination of soil pH, available P, and Al+3+H+, distinguished plots
with greater plant performance (OL, OP, and NP) from plots with low
(AA) and very low (CL and MM) plant performance (Fig. 6B). The best
performance was achieved in soils with a pH higher than 4.8, and with
higher levels of available P (P > 18 ppm) (Table 1). On the other hand,
lower pH and available P, as well as higher Al+3+H+, characterized
plots with poor plant performance, such as CL and MM. PC2 also dis-
tinguished plots; however, the graph did not establish a correspondence
with plant performance.
4. Discussion
In this study, we evaluated the influence of soil, seed traits, and
sowing method on maca growth and performance in the field. While
defining interactions between the environment and plant development
usually represents a great challenge due to the large number of factors
involved, a clear effect of soil properties on plant performance could be
observed in this case. Plots with extremely acid soils (pH < 4.6 and
occasionally high Al+3+H+ concentration) and low levels of available
phosphorus (P) showed a markedly diminished plant survival, vegeta-
tive growth, and yield.
According to Quiros et al. (1996), maca performs better in neutral
soils (pH 6.6) than in acid soils (pH 5.3). In our study, a neutral pH was
only found in the OP plot, whereas OL and CP presented strongly acidic
pH, and AA, CL, and MM, extremely acidic pH. These results imply that
maca might not be reaching its full potential in most of the cultivated
areas in the Puna. In organic acid soils such as those found in this high
Andean region, an elevated concentration of H+, likely liberated from
humic substances (Kidd and Proctor, 2001; Blume et al., 2016), might
play an important role in acid soil stress and has been reported to have
a significant impact on germination (Deska et al., 2011) and root cell
structure and function in Arabidopsis (Koyama et al., 2001), barley
(Song et al., 2011), and common bean (Rangel et al., 2005). Acid soil
stress might also cause nutritional disorders by interfering with P, Ca,
and Mg uptake (Poschenrieder et al., 1995).
Plots with deficient P concentration also showed diminished plant
performance (plant survival, growth, and yield). We think that phos-
phorus might be a limiting nutrient for the development of the maca
crop system, affecting both vegetative and root growth. In accordance
with our view, other studies (Fonte et al., 2012; Vanek and Drinkwater,
2013) have mentioned that phosphorus limits soil fertility in most
Andean environments. In our study, the scenario could have been ag-
gravated by soil acidity, which may have not only affected plant growth
directly but also indirectly by decreasing the bioavailability of nutrients
(Pessarakli, 1999; Poschenrieder et al., 1995; Foy, 1992). Phosphorus is
an essential macronutrient involved in energy generation, nucleic acid
and membrane lipid synthesis, photosynthesis, and other plant meta-
bolic processes (Vance et al., 2003). However, the identification of the
physiological processes affected by the deficiency of this nutrient was
beyond the scope of our study, and therefore awaits future investiga-
tions.
Low levels of soil moisture and either high or low temperature in-
tensified the stress in specific plots. The delay and shortening of the
rainy season caused by “El Niño” 2015–2016 affected more severely the
two plots located near the producing area of “Valle del Mantaro”.
Throughout the experiment, MM had a soil moisture content of less
than 9%, which has been proposed to be the minimum required for seed
germination and seedling emergence and growth (Forcella et al., 2000).
Plot AA experienced an abrupt decay in soil moisture content in the last
2 months of the experiment, reaching very low levels (˜6%). As hypo-
cotyl maturation demands high amounts of water (Cortes, 2000), this
event and thus hypocotyl weight may have been negatively affected.
The combination of water stress and high temperatures is likely to
have caused damage to photosystem II in plants from the lowest alti-
tude plot (MM), as inferred by their low Optimal Quantum Yield values
A. Lozano-Canales, et al.
(Hassan, 2006). In addition, the low temperatures recorded in CL may
have delayed germination and seedling emergence, as has been re-
ported for other species such as Brassica campestris (Kondra et al., 1983)
and Brassica napus (Nykiforuk and Johnson-Flanagan, 1997). This
delay, in turn, might reduce seedling vigor (Singh and Dhaliwal, 1972),
thus contributing to poor plant performances.
Plant performance was also influenced by seed accession.
Accessions associated with black hypocotyls tended to exhibit low
survival percentages and a diminished vegetative growth, thus sug-
gesting a seed source (hypocotyl color) effect. These accessions also had
the seeds with lowest weights (see materials and methods), alter-
natively suggesting an effect of seed weight rather than seed source.
The results from the additional experimental plot established in 2016
with a larger number of accessions clearly showed that accessions with
lighter seeds had lower seedling emergences (Fig. 5), favoring the hy-
pothesis that seed weight, rather than the ecotype, affects plant per-
formance. This interpretation is in accordance with previous findings
that seed weight affects seedling fitness (Ambika et al., 2014; Finch-
Savage and Bassel, 2015), as heavier seeds might have greater food
reserves to cope better with environmental stresses (Geritz, 1995;
Leishman et al., 2000). According to these results, seed weight could be
used as a quality predictor of maca performance referred to seedling
emergence and plant survival.
With regard to sowing methods, we found higher plant survival
percentages when using flat planting, although plants grown in the
ridge-furrow methods had more leaves. Several studies support the
notion that ridge-furrow systems allow gaining heat and creating a
microenvironment with higher temperatures than flat planting, thus
favoring seedling establishment in cold environments (Hatfield et al.,
1998). However, under unexpected climate changes that involve in-
creased temperatures and reduced precipitation such as ENSO condi-
tions, this sowing method may become unfavorable because of the
higher evaporation promoted in the ridge that affects seed germination,
seedling establishment, and ultimately plant survival.
Although our results might help improving crop management of
Lepidium meyenii, some limitations in our study should be pointed out.
First, the experimental unit was smaller and the seed density lower
(about 10%) than those regularly used for commercial production by
farmers. Secondly, because no contingency fund was available in case of
unpredicted climatic variations (ENSO 2015–2016), it was not possible
to carry out a full experiment replication in a different season. Only the
effect of seed weight on seedling establishment could be evaluated
during October 2016–July 2017. In addition, the lack of pest control in
the experimental plots may have contributed to the poor yield observed
at lower altitudes. Nonetheless, our findings improve the understanding
of the performance of this species under adverse climatic scenarios such
as ENSO, which have already caused food insecurity in several cropland
areas worldwide (Heino et al., 2018) and might be more frequent in the
347
Scientia Horticulturae 253 (2019) 341–348
Fig. 6. (A) Ordination of the experimental plots
according to the soil chemical properties by
principal components analysis (PCA). (B)
Comparison of the principal components of the
soil chemical properties (PC1 and PC2) of the
six experimental plots. Data presented are
mean values + 1 S.E. Means sharing a letter
above bar are not significantly different
(p < 0.05, Fisher LSD post-hoc test). Plots: MM
(Masma), AA (Achipampa), OP and OL (plots in
Óndores), CL (plot in Carhuamayo) and NP
(plot in Ninacaca).
future (Cai et al., 2015).
5. Conclusions
The cultivation of maca is a high-potential income source for
farmers of the Central Peruvian Andes. Therefore, information on the
factors that may limit its production and the practices that can be im-
plemented to overcome those limitations are of great importance. In
this study, poor plant performances were mainly associated with ex-
tremely acid soil and low availability of Phosphorus. These findings
deserve further investigation and should be taken into account in future
programs for soil management. In addition, our results strongly suggest
that seed weight, rather than seed source (hypocotyl color), is a robust
determinant of seedling emergence and plant survival, and therefore
might be considered as a good indicator of seed quality.
Funding
This research was supported by a grant from the Fondo Nacional de
Desarrollo Científico, Tecnológico y de Innovación Tecnológica (FON-
DECYT-PERU) (190-2015-FONDECYT-DE), which provided research
support for Alejandra Lozano.
Acknowledgements
We thank Jonhny Vílchez for field assistance, as well as Moisés
Alderete, Arturo Cárdenas, and Efraín Zúñiga for providing the seed
accessions of maca. We are also grateful to Angélica Pérez, Ovaldo
Rojas, Fluber Mamani, and the “Asociación de Productores
Agropecuarios Orgánicos de Carhuamayo” for logistical support and for
generously sharing their knowledge on this crop. Cristina Guerra helped
with the style editing of the manuscript. Finally, we are indebted to
several colleagues who helped us with data collection and material
processing.
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