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Org. Agr.
https://doi.org/10.1007/s13165-017-0199-1
Nest refuse of leaf-cutting ants as a growing substrate
for organic farming systems
Rafaella Santana Santos &
Marcelo Braga Bueno Guerra &
Bianca Giuliano Ambrogi & Leandro Sousa-Souto
Received: 19 January 2017 / Accepted: 5 October 2017
# Springer Science+Business Media B.V. 2017
Abstract About one-third of organic agriculture production in Brazil is carried out by smallholders, who
seek to use low-cost organic fertilizers in their crops. In
this study, we evaluated the nest refuse of leaf-cutting
ants (NR) in the formulation of growing substrates for
lettuce (Lactuca sativa) and arugula (Eruca sativa)
seedlings. A completely randomized design with six
treatments and four repetitions was applied. The treatments were basis growing substrate (CONT), commercial substrate (TropstratoHT®—TROP), and four formulations using NR of two species of leaf-cutting ants
associated with 75 or 85% (volume fraction) of CONT.
Substrates were submitted to chemical analysis for determination of macro- and micronutrients while plant
vigor was evaluated considering plant height (PH), root
length (RL), stem diameter (SD), dry mass (DM), and
number of leaves (NL) at 15, 20, 25, and 30 days after
sowing. The data were submitted to a chemometric
evaluation by means of principal component analysis
(PCA). Treatments with 25% of NR resulted in lettuce
seedlings from 42 to 53% higher and with a twofold
increase of dry mass compared to the commercial substrate (TROP) (P < 0.05). For arugula, similar results
were found for PH and NL between TROP and the
substrate with 25% of NR and these results differed
significantly from the other treatments (P < 0.05).
PCA revealed the formation of five groups of treatments, with TROP and two treatments based on NR
presenting higher correlation with the nutrient content
and plant vigor (P < 0.01). This study is the first to
indicate the feasibility of nest refuse of leaf-cutting ants
in the composition of substrates for organic agriculture
in small-scale production.
R. S. Santos : B. G. Ambrogi : L. Sousa-Souto (*)
Programa de Pós-Graduação em Ecologia e Conservação,
Universidade Federal de Sergipe, São Cristovão, SE 49100-000,
Brazil
e-mail: [email protected]
Introduction
M. B. B. Guerra
School of Natural Sciences, Black Hills State University, 1200
University St., Spearfish, SD 57799, USA
M. B. B. Guerra
Centro de Energia Nuclear na Agricultura, Piracicaba, SP
13400-970, Brazil
Keywords Organic agriculture . Vegetables .
Formicidae . Atta opaciceps . Acromyrmex balzani .
Lettuce . Arugula
Organic farming is a system focused on a broad view of
agriculture, encompassing healthy relationships among
humans, animals, and plants, thus enabling food production in an environmentally sustainable way
(Nandwani and Nwosisi 2016; Usama and Siddiqui
2016). The organic farming system presents lower
yields than conventional agriculture, but environmental
benefits such as improved biodiversity, lower greenhouse gas emissions, and organic matter incorporation
Org. Agr.
to the soil may counterbalance economic differences
(Brito et al. 2012; Meng et al. 2017).
Brazil occupies 12th place in organic agricultural
land (including in-conversion areas) (Willer and
Lernoud 2016), with more than 1.5 million hectares
occupied and annual retail sales of approximately US$
1 billion (Santos et al. 2014). In this system, familyscale production accounts for about 30% of total agricultural products (Oliveira et al. 2008). Thus, it becomes
crucial to evaluate novel substrates that can provide
good plant performance with low costs of production,
mainly regarding organic crops.
In small-scale organic agriculture, the challenges start
from the choice of the substrate (growing media), which
must present some characteristics, such as low cost, easy
access, high content of nutrients, good texture and drainage, water retention, and the absence of pathogens
(Guilhoto et al. 2006). Moreover, substrates for production of organic seedlings should be free of synthetic
fertilizers; therefore, small producers generally use components from their own properties to prepare the substrate (Menezes Júnior et al. 2000; Olaria et al. 2016;
Nandwani and Nwosisi 2016). However, the selected
alternative components will not necessarily ensure good
seedling development (Oliveira et al. 2008; Medeiros
et al. 2010).
The components most commonly used for substrate formulation are earthworm humus (Gomes
et al. 2008), shredded bark of pinus (Martins
et al. 2013), coconut fiber (Carrijo et al. 2002;
Oliveira et al. 2009), and cattle and pig manures
(Fawzy et al. 2016; Zhang et al. 2016). However,
it is crucial to find novel substrates given the
seasonality and low availability of most of the
abovementioned components in different regions
of Brazil. In this regard, it is relevant to conduct
studies on the performance evaluation of suitable
materials to be used as substrates, especially target
components obtained by environmental services of
fauna and flora, e.g., earthworm humus (Gomes
et al. 2008) and the nest refuse (NR) from the
Neotropical leaf-cutting ants (Hymenoptera:
Formicidae, genera Atta and Acromyrmex) (Guerra
et al. 2007; Sousa-Souto et al. 2012). The NR is
composed by a homogeneous, soft substrate with
organic flakes (0.5 to 1 mm of size) with degraded
plant material (flowers, leaves, seeds) previously
carried into the nest and processed by the workers
for maintenance of the fungus garden (Moutinho
et al. 2003; Sousa-Souto et al. 2008a). After being
consumed by workers and larvae, this substrate is
discarded with dead ants and exhausted parts of
the fungus in order to avoid risks of nest contamination (Bot et al. 2001).
Nest refuse of arboreal ants has already been tested as
growing media of epiphytes in natural conditions
(Longino 1986), but so far there are no studies on its
viability in organic farming systems, in spite of their
high concentration of nutrients (Guerra et al. 2007). This
substrate may represent an alternative source of essential
elements for the production of seedlings, becoming as
important as the most common sources obtained from
animal and plants (Cerda et al. 2012).
The NR is extremely rich in several nutrients, increasing phosphorus content in the soil up to 400 times,
when compared to soil samples without the direct influence of ant colonies (Moutinho et al. 2003; Sousa-Souto
et al. 2007). The high nutrient availability often increases the plant diversity and productivity of the ecosystem (Farji-Brener and Werenkraut 2014). Thus, the
NR from leaf-cutting ant nests may represent an organic
source with high potential to compose alternative substrates (Cerda et al. 2012).
The aim of this study was to evaluate the feasibility
of NR from the leaf-cutting ant species Atta opaciceps
and Acromyrmex balzani as components in the formulation of alternative substrates in the production of seedlings of vegetables.
Materials and methods
Experimental design
To test the feasibility of NR obtained from two species
of leaf-cutting ants in the production of seedlings, we
performed a greenhouse experiment (11° 00′ 54″ S, 37°
12′ 21″ W) with temperature range of 25–30 °C, 65–
78% RH, without supplemental lighting. The vegetables
grown were lettuce (Lactuca sativa, cruly large rapids —
TBR) and arugula (Eruca sativa, giant large leaf).
The experiment was conducted using six treatments
(substrates) with four replicates for each treatment, distributed in four randomized blocks. The treatments
consisted of the following soilless growing media
(considering volume fraction of all components): (a)
CONT — control substrate, comprised by the mixture
of bark of Pinus sp. + coconut fiber + vermiculite in the
Org. Agr.
3:3:1 ratio; (b) AT15 — substrate composed of nest
refuse of A. opaciceps (15%) + CONT (85%); (c)
AT25 — substrate with nest refuse of A. opaciceps
(25%) + CONT (75%); (d) AC15 — substrate with nest
refuse of A. balzani (15%) + CONT (85%); (e) AC25 —
substrate with nest refuse of A. balzani (25%) + CONT
(75%); and (f) TROP — commercial substrate
TropstratoHT® (100%). The main objective of using
the NR from two ant species was to evaluate possible
different chemical and physical attributes in the foraged
plant material, since A. balzani cuts exclusively herbaceous plants (mainly Poacea), while A. opaciceps selects
arboreal species as a food resource (Sousa-Souto et al.
2012).
The nest refuse of A. balzani was collected in the
field in September 2015, next to disposal piles of 15
colonies, while the nest refuse from A. opaciceps was
obtained from five colonies (each one with approximately two liters of fungus and 1500 worker ants)
maintained in the laboratory since its emergence in
2009 (for details about the colonies, see Sousa-Souto
et al. 2008b).
Before seeding, all components of the substrates used
in this experiment were oven-dried at 60 °C, during 48 h
with the purpose of eliminating possible pathogens and/
or alien seeds. For the preparation of the substrates, the
components were sieved using a nested sieve (20 cm
diameter and 2-mm mesh screen) and mixed manually
according to the treatments. For growing the seedlings,
polystyrene trays with 128 cells and volume of 40 cm3
each were used.
Biological analyses (plant vigor)
The performance of the seedlings (hereinafter named
vigor) under each treatment was evaluated in four periods, at 15, 20, 25, and 30 days after the sowing (Trani
et al. 2004). In each trial, two plants/block (n = 8) were
previously chosen and the following parameters were
assessed: plant height (PH), number of leaves (NL), root
length (RL), stem diameter (SD), and dry mass (DM)
(Smiderle et al. 2001; Wallace et al. 2012). In each
evaluation, the seedlings were removed from the cells
and washed with tap water. For PH, RL, and SD measurements, a caliper rule with 0.01 mm precision was
used. For determination of DM, the seedlings were
oven-dried at 60 °C for 48 h and subsequently weighed
in an analytical balance.
Chemical analysis
The mass fractions of macro- and micronutrients (P, K,
Ca, Mg, S, Fe, Cu, Mn, Zn, and B) were determined in
all substrates (Hansen et al. 2013). Samples were dried
in an oven at 60 °C until constant weight and cryogenically ground for 20 min. Certified reference materials
(CRMs) from NIST (apple, peach, and tomato leaves)
were used to check the trueness of the method. Samples
and CRMs were digested with the following procedure:
150 mg of dried and ground material were weighed in
triplicate in TFM® digestions vessels and 3 mL of 30%
mm−1 H2O2 and 6 mL of 20% v v−1 HNO3 were added.
The vessels were placed in the digestion system
(Ultrawave, Milestone, Sorisole, Italy) and the following heating program was applied: (i) pressurization with
nitrogen at 40 bar, (ii) heating ramp up to 240 °C during
20 min, (iii) 20 min at 240 °C, and (iv) cooling for
15 min. After reaching the room temperature, the obtained digests were transferred to 15-mL volumetric
flasks and the final volume was made up with deionized
water. The liquid solutions were analyzed by ICP OES
using a dual-view spectrometer (iCAP 6500,
ThermoScientific, Waltham, MA, USA). A PEEK Mira
Mist® nebulizer and a cyclonic spray chamber were
employed. The following operating conditions were
used: 27 MHz of radiofrequency generator; 1.2 kW of
radiofrequency power; and the following argon flow
rates: 12, 0.5, and 0.6 L min−1 for the plasma, auxiliary,
and nebulizer, respectively. A sample flow rate of
1.5 mL min−1 and measurement time of 20 s were used.
The following emission lines were monitored in axial
viewing mode: Fe II 261.187 nm, Cu I 327.396 nm, Mn
II 257.610 nm, Zn I 213.856 nm, and B I 249.772 nm
and in the radial viewing mode: P I 214.914 nm, K I
766.490 nm, Ca II 184.006 nm, Mg II 280.270 nm, and
S I 180.731 nm.
For pH measurement, the following procedure was
applied: 10 g of dried material of each substrate was
weighed into previously decontaminated polypropylene
centrifuge tubes, with further addition of 25 mL of
deionized water and shaking with a glass rod for
2 min. The samples were allowed to stand for 1 h and
the potentiometric pH measurement was performed.
Statistical analysis
Chemical differences among substrates were tested
using one-way ANOVA, followed by Tukey HSD tests.
Org. Agr.
The classification of substrates in relation to their nutrient contents and vigor of the plants was obtained
through principal component analysis (PCA). Data were
auto-scaled, for giving the same importance to all variables. The values generated in the first principal component (PC 1) were used as the response variable and
submitted to one-way ANOVA, followed by Tukey
HSD test to detect differences between treatments. Additionally, for each variable (response), a linear regression analysis was performed, taking the values of PC 1
as explanatory variable.
Differences in morphological characteristics of the
seedlings (PH, NL, RL, SD, DM), among the evaluated
substrates, were compared using linear models with
mixed effects (LMEs). In these models, the morphological characteristics analyzed were used as fixed factor,
while the temporal series (day of sampling) and the
blocks were used as random factors (Crawley 2013).
Models that showed significant differences were submitted to a posteriori contrast (RT4Bio package in R
software) for identification of treatments that resulted in
these differences (P < 0.05). Statistical analyses were
made using the software R (R Development Core Team
2017).
Results
Chemical characteristics of treatments
The six treatments (substrates) presented clear differences in nutrient contents (Table 1). For macronutrients,
for example, the commercial substrate (TROP) shows a
better result when compared with treatment from AT25
substrate based on the levels of P, Ca, and S (47, 39, and
36% higher, respectively), but presented ca. 66% lower
K and Mg contents than the AT25 sample (Table 1).
Despite this, TROP treatment presented the highest
values in six of the 11 chemical variables analyzed.
The AT15 treatment, however, presented the lowest
Fe, B, and Zn levels. On the other hand, the treatment
AT25 presented higher values of K and B as well as
intermediate values of P, Ca, Mg, S, Cu, and Zn. Considering all NR-based compounds, AT25 presented the
most similar chemical characteristics to the commercial
substrate (TROP). The growing media AC15 and AC25
presented similar chemical characteristics for most of
the evaluated parameters. The control substrate has at
least one order of magnitude lower P, Ca, and S levels
than the commercial substrate; however, it was enriched
in Mg and Fe (Table 1).
Biological analyses (plant vigor)
In general, the vigor of plants treated with the nest
refuse-based substrates exhibited significant differences
when compared with the control treatment and even to
the commercial substrate, for several periods of evaluation (LME, P < 0.001, Table 2).
For lettuce, seedlings cultivated with NR substrates
(mainly AT25, AC25, and AT15) resulted in plants with
high performance (higher values of PH, DM, SD, and
NL), throughout the experiment, when compared with
commercial or control substrates (Table 2).
For instance, plants grown on AT25 substrate presented better performance regarding PH (53%), stem
diameter (10%), and dry mass (twofold), after 30 days
of sowing. However, the root lengths were not statistically different between plants cultivated in the evaluated
substrates (F = 35.45, P < 0.05). The heights of the
seedlings were 30% higher among the group cultivated
on AC15 and AC25 than for those grown on TROP, as
evaluated after the 15th, 20th, and 25th day of experiment. Conversely, the plants from the control substrate
presented the worst performance parameters evaluated
herein (Table 2).
The obtained responses for the parameters related to
the plant vigor differed between plant species and growing media. However, similar results were observed in
the plants cultivated on the growing substrates AT25,
AC25, and TROP for the following characteristics: plant
height (after 20, 25, and 30 days), root length (AC25
after 15 days), stem diameter (AT25 after 20 and
25 days), number of leaves (mainly after 25 days), and
dry mass (AT15, AT25, and AC25 after 15 days). Notwithstanding, the commercial substrate systematically
promoted the best plant performance indicators during
the four evaluated periods.
PCA analysis
The principal component analysis related to the evaluation of the variables of plant vigor and the contents of
nutrients obtained in each treatment resulted in the formation of five distinct groups, for both lettuce and
arugula plants (Fig. 1). The resulting ordination indicated that the TROP treatment was strongly correlated to
higher values of PC1, while the AT15 and AT25
Trop — 100% of commercial substrate (TropstratoHT®)
AT15 — substrate composed by nest refuse of A. opaciceps (15%) + CONT (85%)
AT25 — substrate composed by nest refuse of A. opaciceps (25%) + CONT (75%)
AC15 — substrate composed by nest refuse of A. balzani (15%) + CONT (85%)
AC25 — substrate composed by nest refuse of A. balzani (25%) + CONT (75%)
CONT — control substrate, comprised by the mixture of bark of Pinus sp. + coconut fiber + vermiculite in the 3:3:1 ratio
1
2
3
4
5
6
11,608 ± 815a
0.3 ± 0.02e
1.14 ± 0.09f
3.91 ± 0.29d
0.14 ± 0.01e
5.1 ± 0.12b
CONT6
Values are means ± standard error. Means with different letters within the same column are significantly different (a posteriori contrast, P = 0.05)
34.9 ± 0.98a
27.7 ± 2.14c
94.4 ± 0.26b
25.48 ± 1.55b
30.6 ± 0.47b
36.0 ± 1.59a
5.8 ± 0.51c
87.7 ± 1.55c
23.58 ± 0.55c
9422 ± 262b
0.7 ± 0.01d
5.9 ± 0.12a
AC255
0.28 ± 0.05d
2.65 ± 0.05e
4.11 ± 0.05c
29.4 ± 0.31b
9.4 ± 0.52b
26.2 ± 0.43c
75.9 ± 1.02d
87.2 ± 1.19c
22.40 ± 0.25c
29.79 ± 0.34a
9365 ± 91b
0.8 ± 0.01d
8.2 ± 0.35b
8460 ± 86c
1.9 ± 0.01b
28.5 ± 0.29b
3.39 ± 0.06e
4.61 ± 0.05c
10.73 ± 0.10a
5.2 ± 0.17b
AC154
1.09 ± 0.09b
5.4 ± 0.23b
AT253
0.34 ± 0.02d
8.31 ± 0.09b
27.9 ± 0.29b
9.1 ± 0.46b
21.4 ± 0.61d
26.6 ± 0.32c
179.4 ± 1.26a
65.2 ± 1.43e
22.49 ± 0.43c
18.63 ± 0.28d
17.0 ± 0.18a
5.3 ± 0.31c
8111 ± 136c
7707 ± 162d
2.6 ± 0.02a
0.9 ± 0.02c
11.1 ± 0.09d
25.5 ± 0.53c
3.72 ± 0.10d
11.6 ± 0.06a
3.52 ± 0.04d
6.01 ± 0.15b
5.3 ± 0.17b
AT152
1.61 ± 0.02a
6.0 ± 0.23a
TROP1
0.52 ± 0.11c
Zn
Mn
B
Cu
Fe
S
Mg
Ca
K
P
pH
Substrate
Table 1 Chemical characteristics of six treatments (substrates) used in this study. Macronutrients: P, K, Ca, Mg, and S (g kg−1). Micronutrients: Fe, Cu, B, Mn, Zn (mg kg−1)
Org. Agr.
treatments were associated with higher PC2 values. The
other treatments (AC15, AC25, and CONT) were associated with lower values of PC1 and PC2 (Fig. 1).
For lettuce, the first two principal components explained 79% of the variance of the data, the first principal component explaining 52% of variation, with high
influence of phosphorus (r2 = 0.97, P < 0.001), sulfur
(r 2 = 0.96, P < 0.001), and calcium (r 2 = 0.94,
P < 0.001). Negative significant correlation was found
for Mg and Fe (r2 = − 0.87 and r2 = − 0.75, respectively). The variables PH, NL, DS, and DM also showed a
significant correlation with the first principal component
(r2 > 0.55).
In a similar way, for arugula, PC1 and PC2 explained
71% of total variance (PC1 explained 54%), with high
influence of calcium (r2 = 0.95, P < 0.001), phosphorus
(r2 = 0.93, P < 0.001), and sulfur (r2 = 0.94, P < 0.001).
Negative significant correlation was found for Mg and
Fe (r2 = − 0.92 and r2 = − 0.70, respectively). The
variables PH, RL, NL, DS, and DM also showed a
significant correlation with the first principal component
(r2 > 0.70).
Discussion
In this study, we found promising results regarding the
use of substrates composed by nest refuse of leaf-cutting
ants for the production of seedlings of vegetables. In
general, substrates based on NR had high nutrient contents and resulted in plants with similar or superior
performances to the commercial formulation, especially
after 30 days of sowing. The present data are in accordance with previous studies that also used substrates
made with organic materials and compared their performances with TropstratoHT® in the production of lettuce
seedlings (Oliveira et al. 2017).
Contrary to what was expected, NR-based treatments
did not have the highest nutrient levels, excepted for K,
B, and Zn and the only exception was AT25 that presented similar or even higher nutrient contents than
TROP. In spite of this, it is possible that the nutrient
contents, associated to the physical characteristics of the
substrates, have contributed to the high number of
emerged leaves, stem diameter, and dry mass of the
seedlings found in this study. This trend was previously
found by Castoldi et al. (2014) who verified that alternative substrates produced larger lettuce seedlings with
10 days less in the life cycle. Previous studies have also
4.10 ± 0.37a
2.71 ± 0.23b
AC255
CONT6
4.09 ± 0.44a
2.98 ± 0.24a
3.98 ± 0.35a
3.16 ± 0.46a
3.68 ± 0.43a
AT25
AC15
AC25
CONT
3.12 ± 0.20b
0.75 ± 0.04b
0.91 ± 0.07a
0.79 ± 0.08b
0.82 ± 0.06b
0.58 ± 0.04b
AT25
AC15
AC25
4.83 ± 0.21a
4.43 ± 0.17b
4.16 ± 0.12b
3.25 ± 0.25c
AT25
AC15
AC25
CONT
TROP
4.46 ± 1.05b
3.83 ± 0.22c
AT15
Dry mass (mg)
4.12 ± 0.22b
TROP
Number of leaves
CONT
1.06 ± 0.07a
0.70 ± 0.06b
7.42 ± 0.66b
4.25 ± 0.31b
5.85 ± 0.22a
4.87 ± 0.29b
5.75 ± 0.16a
5.16 ± 0.12b
4.87 ± 0.29b
1.08 ± 0.09a
1.30 ± 0.09a
1.10 ± 0.06a
0.65 ± 0.11b
AT15
1.21 ± 0.07a
5.06 ± 0.44a
TROP
Stem diameter (mm)
4.48 ± 0.28a
1.20 ± 0.07b
2.45 ± 0.11b
3.07 ± 0.49a
AT15
4.28 ± 0.42a
3.16 ± 0.32b
5.18 ± 0.19a
4.8 1 ± 0.45a
5.50 ± 0.35a
3.87 ± 0.19b
3.75 ± 0.14b
20d
Lettuce
TROP
Root length (cm)
4.31 ± 0.33a
AC154
AT25
4.96 ± 0.27a
3.21 ± 0.29b
3
3.22 ± 0.45b
AT152
15d
TROP1
Plant height (cm)
Substrate
8.70 ± 1.66b
4.67 ± 0.24c
6.00 ± 0.26b
5.62 ± 0.26c
6.87 ± 0.29a
7.00 ± 0.32a
5.32 ± 0.30c
0.80 ± 0.02c
1.08 ± 0.10b
1.30 ± 0.10b
1.46 ± 0.05a
1.30 ± 0.04b
1.20 ± 0.06b
4.34 ± 0.22b
4.58 ± 0.20a
5.07 ± 0.19a
4.10 ± 0.28b
3.25 ± 0.33b
3.66 ± 0.52b
3.77 ± 0.30c
5.34 ± 0.35b
5.44 ± 0.45b
7.00 ± 0.40a
4.45 ± 0.25c
4.28 ± 0.35c
25d
12.70 ± 1.28b
4.71 ± 0.15c
6.00 ± 0.32b
5.75 ± 0.25b
7.00 ± 0.26a
7.00 ± 0.26a
5.42 ± 0.17b
1.05 ± 0.07c
1.44 ± 0.05b
1.31 ± 0.05b
1.65 ± 0.06a
1.34 ± 0.04b
1.50 ± 0.06b
4.64 ± 0.42a
4.77 ± 0.26b
5.56 ± 0.39b
5.05 ± 0.31a
4.47 ± 0.26a
5.62 ± 0.24a
4.95 ± 0.48c
7.00 ± 0.38a
5.77 ± 0.45b
7.51 ± 0.42a
5.47 ± 0.26b
4.91 ± 0.34c
30d
5.77 ± 1.01a
2.00 ± 0.05b
2.50 ± 0.19a
2.12 ± 0.12b
2.56 ± 0.17a
2.62 ± 0.18a
2.75 ± 0.16a
0.53 ± 0.06b
0.55 ± 0.08b
0.51 ± 0.02b
0.62 ± 0.04b
0.63 ± 0.07b
0.73 ± 0.06a
3.02 ± 0.36b
4.33 ± 0.43a
3.90 ± 0.33b
3.90 ± 0.34b
2.65 ± 0.35b
4.03 ± 0.47a
2.03 ± 0.16b
3.21 ± 0.16a
3.05 ± 0.30a
3.26 ± 0.33a
2.76 ± 0.17a
3.71 ± 0.30a
15d
11.85 ± 2.07a
2.12 ± 0.12c
2.75 ± 0.16b
2.65 ± 0.32b
3.00 ± 0.05b
2.87 ± 0.22b
3.25 ± 0.16a
0.53 ± 0.04b
0.66 ± 0.06b
0.64 ± 0.05b
0.82 ± 0.04a
0.70 ± 0.04b
0.87 ± 0.07a
3.51 ± 0.61b
4.66 ± 0.37b
4.81 ± 0.36b
4.81 ± 0.36b
3.98 ± 0.59b
4.88 ± 0.31a
2.49 ± 0.21c
3.38 ± 0.14a
3.15 ± 0.19b
3.28 ± 0.28a
3.18 ± 0.22b
4.60 ± 0.37a
20d
Arugula
16.7 ± 3.39a
2.5 ± 0.16b
3.6 ± 0.26a
3.1 ± 0.22a
3.5 ± 0.16a
3.4 ± 0.17a
3.9 ± 0.22a
0.53 ± 0.03b
0.89 ± 0.06a
0.69 ± 0.07b
0.95 ± 0.07a
0.82 ± 0.04a
1.03 ± 0.09a
3.7 ± 0.51c
5.1 ± 0.24b
4.9 ± 0.37b
4.8 ± 0.37b
4.7 ± 0.32b
6.1 ± 0.83a
2.73 ± 0.16c
3.08 ± 0.38a
3.79 ± 0.35b
4.23 ± 0.20a
3.51 ± 0.12b
5.10 ± 0.65a
25d
32.8 ± 8.13a
2.5 ± 0.16c
4.0 ± 0.19b
3.6 ± 0.14b
4.9 ± 0.22a
4.4 ± 0.17a
4.5 ± 0.32a
0.72 ± 0.03c
1.04 ± 0.09b
0.95 ± 0.09b
1.19 ± 0.07b
1.01 ± 0.08b
1.34 ± 0.12a
5.2 ± 0.40b
5.4 ± 0.55b
5.4 ± 0.44b
5.2 ± 0.44b
5.0 ± 0.47b
6.6 ± 0.50a
2.88 ± 0.12c
3.75 ± 1.06a
3.81 ± 0.32b
5.49 ± 0.37a
4.40 ± 0.31b
6.08 ± 0.66a
30d
Table 2 Average values of plant vigor for lettuce (Lactuca sativa) and Arugula (Eruca sativa) seedlings grown on different substrates, at 15, 20, 25, and 30 days after sowing
Org. Agr.
6.0 ± 0.49c
AT25 — substrate composed by nest refuse of A. opaciceps (25%) + CONT (75%)
AC15 — substrate composed by nest refuse of A. balzani (15%) + CONT (85%)
AC25 — substrate composed by nest refuse of A. balzani (25%) + CONT (75%)
4
5
CONT— control substrate, comprised by the mixture of bark of Pinus sp. + coconut fiber + vermiculite in the 3:3:1 ratio
AT15 — substrate composed by nest refuse of A. opaciceps (15%) + CONT (85%)
3
6
Trop — commercial substrate (TropstratoHT®)
2
Values are means ± standard error. Means with different letters within the same column are significantly different (a posteriori contrast, P = 0.05)
1
4.2 ± 0.54d
3.65 ± 0.38c
3.51 ± 0.31b
11.41 ± 2.73b
2.86 ± 0.52b
CONT
3.70 ± 0.41c
5.58 ± 1.23b
5.88 ± 0.67b
9.5 ± 2.90b
15.0 ± 1.75b
10.3 ± 1.62b
7.18 ± 0.85b
6.35 ± 1.29a
30.20 ± 3.62a
15.36 ± 2.10a
19.6 ± 1.79b
AC25
10.73 ± 0.59a
6.8 ± 1.53c
5.61 ± 0.63b
3.07 ± 0.51b
15.91 ± 2.48b
6.47 ± 0.89a
AC15
8.37 ± 1.43b
6.27 ± 0.88b
AT25
14.53 ± 1.57a
8.8 ± 0.55b
9.7 ± 1.54b
7.52 ± 0.83b
6.66 ± 0.82b
5.75 ± 0.92a
5.32 ± 0.78a
30.18 ± 3.79a
14.77 ± 0.92b
6.20 ± 0.37b
4.36 ± 0.39b
AT15
10.00 ± 1.85b
20.12 ± 2.11a
Arugula
Lettuce
Substrate
Table 2 (continued)
10.28 ± 1.28a
16.0 ± 2.56b
Org. Agr.
shown that organic substrates based on manure from
sheep and goats resulted in plants with better vigor
(number of leaves and dry mass) than plants grown with
TropstratoHT® (Pereira et al. 2012; Souza et al. 2014).
Higher number of leaves and dry mass were also found
for one alternative substrate based on 50% earthworm
humus (obtained from Eiseinia foetida and cattle manure) compared to two brands of commercial substrate
(Menezes Júnior et al. 2000).
The chemical composition among substrates with
25% of NR and TropstratoHT® was similar and this
may have contributed to the similarities in plant vigor
(for lettuce) observed in those treatments, mainly at
30 days after germination. Thus, the ideal proportion
of NR to be recommended for this plant species in
organic substrates would be 25%. The results for arugula, however, indicate that there are specific nutritional
requirements of each plant species (Sánchez-Monedero
et al. 2004) and thus further studies are needed to adjust
the proportion of the compounds used in the substrates.
It is important to stress that in a previous experiment
(unpublished data), a substrate with 50% of NR did not
promote germination (all seedlings died before 30 days),
probably due to the excess of some nutrients (Grattan
and Grieve 1998).
It was expected that substrates with a higher proportion of NR would have the highest nutrient values but
the nutrient contents found in AC15 samples were similar with the values found in AC25. However, since the
samples of A. balzani (AC treatments) were collected in
the field, this variability of chemical composition is
plausible, as the nutrient content in the nest refuse of
colonies may vary depending on the type of vegetation
harvested (Sousa-Souto et al. 2007). In addition, the
formation of three different groups in the PCA with the
treatments based on NR (AT25, AT15, and one of AC15
and AC25) indicates two possibilities: first, the plant
source of the nest refuse may affect the nutrient releasing rates of the final product. In other words, as
A. balzani cuts preferentially herbs (Poaceae) while Atta
opaciceps harvests mainly tree leaves (Kooij et al.
2014), the organic composition of the corresponding
NR can alter the availability of nutrients to the seedlings.
Thus, the quality of the substrate from ant colonies may
be improved if the nests are located close to high fertility
soils or if ants harvest nitrogen-accumulating plant species (Sousa-Souto et al. 2012). Second, since that the
mineralization rates of these materials occur by different
pathways, the nutrients are mineralized faster in field
Org. Agr.
Fig. 1 Principal component analysis (PCA) of lettuce (left) and arugula (right), for nutrients and plant vigor variables, determined among six
treatments (growing substrates)
than in laboratory conditions (Sousa-Souto et al. 2012).
Thus, based on the reported results, in order to obtain a
substrate of better quality, we recommend that the collection of NR in external piles of the colonies be performed soon after its disposal by the ants (Herz et al.
2007).
Taking into account the number of emerged leaves
and height of the lettuce seedlings, the treatments AC25,
AT15, and AT25 presented values above to the recommended threshold level for transplantation (Kampf
2000). The root length was not influenced by the substrates used herein, which is an unexpected result given
the sensitiveness of this plant tissue to alterations in the
chemical and physical aspects of substrates where the
vegetal has been grown (Trani et al. 2007). On the other
hand, for lettuce, the stem diameter and dry mass were
higher in the treatments AT25 and AC25 in relation to
the seedlings from commercial substrate. These parameters are two important indicators of quality of the
seedling development before field transplantation
(Campos and Uchida 2002) and are commonly associated with those requirements of high quality substrates
(Souza et al. 2013; Cunha et al. 2014). For example,
higher dry mass can be correlated to an increase in the
availability of nutrients by the substrate, mainly in relation to P, which exerts a strong influence on the growth
of the aerial part of the plants (Gourley et al. 1994).
Thus, growing substrates based on NR emerge as a
novel alternative in the organic farming system, and
the results found in this study highlight the importance
of testing organic materials that promote the
development of seedlings with high performance and
low costs (Cunha et al. 2014).
Considering a small-scale production of vegetables,
only a small amount of NR is required. For example, in
the present study, approximately 450 g of NR was used,
which was enough to produce 150 seedlings. Due to the
high density of colonies of A. balzani, in the northeastern region of Brazil, reaching more than 900 colonies
per hectare (Sousa-Souto et al. 2013), producers can
collect the NR discarded in the field by this species
directly from the nest entrances. Alternatively, the collection of nest refuse can also be made by direct excavation of nests in the farm.
Conclusion
This is the first study to investigate the effect of nest
refuse of leaf-cutting ants for growing plants in greenhouse conditions, and the results proved a promising
alternative for organic, family-based farming, due to the
ease of collection and low production costs. For lettuce,
in all the parameters evaluated, the substrates with 25%
of NR showed similar or higher performance compared
to the commercial substrate (TropstratoHT®). For arugula, substrates with 25% of NR content can be a
starting point but additional studies should be conducted
to determine the optimum NR volume ratio for attaining
better plant development. In summary, the results obtained in this study indicate that the effect of NR-based
substrates may vary depending on the cultivated plant
Org. Agr.
species, and careful optimization regarding the NR volume ratio is required for ensuring a better plant
development.
Acknowledgements The authors thank Dr. Brianna Mount for
the language improvement. The authors also thank James Cardozo
and Dr. Maria de Fátima Souza for the support in the acquisition of
material used as raw substrates for this study. We are grateful to the
staff of the laboratory of Entomology of UFS for the support in the
experiments, Aparecida de Fátima Patreze and Prof. Francisco
José Krug from CENA/USP for helping us in the chemical analyses of the substrates, Capes/CNPq for the scholarship, and National Science Foundation (NSF MRI Award 1429544) and
FAPESP (2012/16203-5) for the financial support.
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