Cropscience
Cropscience
Affiliations:
1
Instituto de Investigaciones de Ciencias Agrarias de Rosario, CONICET, Facultad de
2
Instituto Multidisciplinario de Biología Vegetal, CONICET, Facultad de Ciencias
Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Av. Vélez Sarsfield 299,
Abstract
proximity to natural and semi-natural habitats (pastures, forest, tree lines, etc.). Managing
ecosystem services, such as insect pollination, is essential to increase crop yields. Although
insect pollination is linked to better yields in many crops, pollinators are usually not
considered as an input to be managed in crop production. In this study we evaluate for the
first time the influence of pollinators on the reproductive parameters of three canola stands
with exposed and non-exposed (covered with voile bags) flowers to insect visits were
This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1002/csc2.20450.
habitats. Observations of flower visitations by the insects were recorded during the flowering
period. The most frequent pollinator was Apis mellifera although twelve additional pollinator
morpho-species were registered. Seven of them were observed in canola flowers for the first
time. Pollinators increased the amount of pollen deposited on stigmas and all measured
reproductive parameters (fruit set, seeds per pod, seed mass). Seed production per
infructescence was increased with proximity to semi-natural habitats and with pollinators by
34% and 35% respectively. Therefore, the pollination ecosystem service is a relevant input
for canola production in central Argentina. It would be important to develop policies that
encourage diversified farming systems securing the protection of natural flora and pollinators.
INTRODUCTION
The Pampas, an extensive grassland, has been widely transformed into one of the largest
soybean or maize are the prevalent summer crops, and many fallow fields are frequent during
the cool-season (Molina, Poggio, & Ghersa, 2014). Some of the most frequent winter crops
are wheat and canola. Agricultural mechanization made considerable changes in the
Conde, & Poggio, 2011). Nowadays, semi-natural habitats are characterized by spontaneous
vegetation and represent a small portion of the agro-ecosystem but they are the locus of
essential ecosystem services such as pollination of crops. Loss and fragmentation of natural
and semi-natural habitats reduces the spatial and temporal stability of flower-visitors richness
and pollination services in crop fields (Garibaldi et al., 2011; Le Féon et al., 2016; Sáez,
important issue for those crops that interact with pollinators because they tend to have lower
Policy Platform on Biodiversity and Ecosystem Services [IPBES], 2016). In Europe, bee
diversity and the abundance of solitary bees were higher in canola stands adjacent to
grasslands and semi-natural habitats than in isolated crop stands (Carré et al., 2009;
Brassica napus L. is an important global crop with varieties that are benefited from
pollinators to increase their yields. Some studies highlight the role of Apis mellifera L. as a
canola pollinator (Bartomeus, Gagic, & Bommarco, 2015; Lindström, Klatt, Smith, &
Bommarco, 2018; Woodcock et al., 2016) but others social and solitary bees, dipterans and
butterflies have been reported as pollinators (Ali, Saeed, Sajjad, & Whittington, 2011;
Garratt, Bishop, et al., 2018; Perrot, Gaba, Roncoroni, Gautier, & Bretagnolle, 2018; Witter
et al., 2014). Most cross-pollination in canola occurs within a few meters of the source plant
(Funk, Wenzel, & Schwarz, 2006) although some longer-range events have been recorded
(i.e., 5 to 26 km away from pollinator sources at two Scottish sites(Ramsay, Thompson, &
Squire, 2003) and up to 3 km away at three different Australian sites (Rieger, Lamond,
Preston, Powles, & Roush, 2002). Although pollinators are not usually considered as an input
to be managed in canola crop production, insect pollination can increase its marketable yield
up to 47.5% (Bommarco, Marini, & Vaissière, 2012; Perrot et al., 2018). Canola reproductive
parameters and seed yield can be affected by pollinator diversity, visitation rates, or the
presence of honeybee hives (Bartomeus et al., 2014; Lindström et al., 2018; Perrot et al.,
According to FAO (2018), the cultivated area of canola in South America was 195,753 ha
with a production of 426,930 tons. year-1. Studies on pollinators visiting canola flowers in
Argentina and South America as a whole are scarce (Blochtein, Nunes-Silva, Halinski,
Lopes, & Witter, 2014; Durán et al., 2010; Mussury, Fernandes, & Scalon, 2003; Rosa,
range of factors (Marinozzi, 2016; Marinozzi, Villamil, & Gallez, 2017; Montaldo, Medan,
Roitman, D’Ambrogio, & Mantese, 1996). For example, Montaldo , Medan, Roitman,
D’Ambrogio, and Mantese (1996) evaluated the yield in small experimental plots and did not
find any effect of pollinators, although observations on flower visitors were not made.
Conversely, other studies presented data on flower insect visitors (Marinozzi, 2016;
Therefore, this study aimed to evaluate -for the first time in the region- the influence of
semi-natural habitats providing pollinators and the influence of them on canola reproductive
and thus the closer the crop is to the semi-natural habitats, the higher are productive
parameters. In particular, our predictions are: (1) the flowers of inflorescences exposed to
pollinators will show both: greater amount of pollen deposited on stigmas and reproductive
parameters (fruit set, seeds per pod, seed mass, and seed production per infructescence) than
the covered flowers; (2) the amount of pollen on stigmas and the reproductive parameters
(fruit set, seeds per pod, seed mass, and seed production per infructescence) in plants with
inflorescences exposed to insect pollination will be decreased as the distance of the crop-
Study area
The study was carried out in three stands cultivated with B. napus, one located in Zavalla
(stand A: 33 ° 01'00 "S 60 ° 53'00" O, Santa Fe, Argentina, sowed with the spring-type
Advanta Hybrid: Hyola 76, with a density of 6.5 Kg of seeds.ha-1) and the other two in
Bustinza (stands B and C: 32 ° 44'00 "S 61 ° 18'26" O, Santa Fe, Argentina, sowed with
A: an area of 1 ha, located at 500 m from the Villarino park (a forest of ca. 100 ha), 500 m
from a grove (4.31 ha, with Eucalyptus sp., Broussonetia papyrifera L. and Ligustrum
lucidum W.T. Aiton) and 500 m from a permanent closure (3 ha since 1983) of pasture and
shrubby vegetation. This plot was surrounded by a pasture of Medicago sativa L. and fallow
field. Stand B: an area of 5 ha, next to an abandoned forest dominated mainly by implanted
Eucalyptus sp. and spontaneous Broussonetia papyrifera (1.20 ha). Stand C: an area of 50 ha,
surrounded by an agricultural matrix except for a curtain of trees placed on the East side
(mainly individuals of Melia azedarach L. and Ligustrum lucidum). All stands were located 6
km from each other, so they were considered independent due to the maximum distance that
potential pollinators can forage (Mendizabal, 2005). Insecticides were not applied during
crop flowering.
Pollinators
Ciencias Agrarias [FCA], 2016) so we recorded insect visits from 12 p.m. to 2 p.m.: the hours
of highest temperature (average 13.7ºC) and pollinators activity (Mussury et al., 2003).
Observations were performed throughout the flowering period (from the beginning of canola
flowering with about 20% of open flowers, to the end of the flowering) using an imaginary
square of 0.25 m2 (50x50 cm square). This area can cover 2, 3, or 4 plants, according to their
size. All flowers were observed in each square for five minutes. The frequency of pollinator
Insects were collected and photographed (see Supplemental Figure S1). The identification
was carried out with the help of Specialists of Zoology Department College of Agricultural
To assess the effect of the distance to the semi-natural habitats (pastures, forest, tree lines,
etc.) on the pollination of canola, four transects per site (100 m length each and spaced 25m
between them) were determined from the stand edge into the agricultural matrix. Each
transect consisted of sampling stations starting from the edge of the crop and placed 10 m
apart each other. Sampling stations were grouped into those proximal (<50 m) or distant (>50
m) from semi-natural habitats, because the different sizes and locations of semi-natural
habitats of the different stands. For example in the stand A (1 ha), semi-natural habitats
surrounded the plot. So, all sampling stations were considered in the proximity to semi-
natural habitats (n =40). For stand B (5 ha) and C (50 ha), those stations placed within a 50 m
radius from the trees were considered in the proximity to semi-natural habitats (n =67) and
those located >50 m radius as distant stations (n =69). Because canola is not a widespread
crop, we prefer to have 3 stands with similar regional conditions; even if there are no plants
Two comparable lateral inflorescences (with similar size, phenological stage and, number
of buds) located above the canopy per sampling station were chosen and two treatments were
applied: one inflorescence with flowers exposed to insect visits during the entire flowering
period (the inflorescence was tagged just before the start of the flowering period), and
another inflorescence with flowers covered (the flowers of the inflorescence were isolated
from pollinators covering them with voile bags (15x30 cm) during flowering). We assumed
that the effect of voile bags on seed production was insignificant because the covered
inflorescence is a small portion of the whole plant and the photoassimilates in canola are
distributed mostly by the main plant stem (Iriarte, Valetti, & Apella, 2008).
Flowers were collected at the end of the anthesis, one per treated inflorescence and fixed
with FAA (formaldehyde, alcohol, acetic). Seventy-eight flowers (n=39 per treatment) were
selected and dissected, and each gynoecium was hydrolyzed in NA (OH) 8N. The squash
technique was applied ensuring that the stigma had a maximum final size within the visual
field with 4X magnification. Each stigma was photographed. On each image of the total
stigmatic surface, a square-grid was applied. The deposited pollen grains were counted in two
of the grid-squares and were used as an estimator of the response variable (amount of pollen
deposited on stigmas).
Infructescences of each treatment were manually harvested (n = 104 and 100 exposed to
insect visits and covered infructescences, respectively). The harvested material was left at
room temperature and when it reached constant weight (15 days), the response variables were
measured.
The total number of fruits per infructescence was counted. For quantifying the number of
seeds per pod and measure the seed mass, six fruits within the inflorescence were randomly
sampled (base, middle and, apex) taking into account that the whole flowering period lasted
one month. A total of 50 seeds per inflorescence were weighted to obtain the mean mass per
seed. Seed production per infructescence (SP) was calculated as follows: fruit set x seed per
pod x seed mass. Differences in SP regard to pollination mode (self- vs self + entomophilous)
Data analyses
Data were analyzed using mixed models. Fixed effects were "pollination treatment"(with
two levels: exposed and covered) and "distance to semi-natural habitats” (with two levels,
proximal or distant). The random effect was “stand” (with three levels: A, B, and C) (see
Supplementary Material S1). All statistical analyses were performed using R Project (R Core
Team, 2016) through Linear Mixed Models (MLMs) and Generalized Linear Mixed Models
(GLMMs) using the lmer and glmer functions, respectively, with the statistical package lme4
(Bates, Mächler, Bolker, & Walker, 2015). The most parsimonious model was chosen by the
RESULTS
Pollinators
648 visits of insect pollinators were recorded during a total of 820 minutes of observation.
Insects were classified into three orders (Hymenoptera, Diptera, and Lepidoptera), seven
families, and twelve species and morpho- species. Apis mellifera was the most frequent
pollinator species and the frequency of its visits was 93.06% of the total visits. The second
place was occupied by Allograpta exotica (1.54%) and Toxomerus sp (1.54%). The frequency
of the other pollinators varied from 0.77% (Eristalis sp. and Bibionidae sp.) to 0.15 %
Pollination treatment
between pollination treatments, and was greater in the inflorescences exposed to insects
(Table 2; Figure 1(a)). Fruit set, seeds per pod, and seed mass showed higher values for
insect-pollinated flowers in comparison with covered flowers (Table 2; Figure 1(b, c, d)).
The amount of pollen deposited on stigmas, seeds per pod, and seed mass did not show
(Figure 1(a, c, d), Table 2). Fruit set and SP were higher in plants growing in the proximity to
semi-natural habitats compared to distant plants (Figure 1(b, e), Table 2). Summarizing,
proximity to semi-natural habitats compared to distant ones. Finally, we present the detailed
results showing variations for the different response variables for each canola variety used in
the study as supplementary material (see Supplemental Text S1 and Supplemental Figure S2).
DISCUSSION
Pollinators
Apis mellifera showed a higher frequency of visits to canola flowers compared to the
ones reported in different regions of the world (e.g., Brazil: Mussury et al., 2003; Rosa et al.,
2010; Witter et al., 2014; Europe: Bartomeus et al., 2014; Hoyle, Hayter, and Cresswell,
2007; Lindström, Klatt, Smith, and Bommarco, 2018). This can be explained because
beekeepers are present in the study region (Iriondo with 24 apiaries and 1,103 hives; and
dependent crops in South America (Sáez, Sabatino, & Aizen, 2012). Canola is one of the
most important food sources for bees during the winter in the study region, where semi-
natural areas in the landscape are scarce and when most stands are sowed with wheat or are
fallow fields during the cold season (Le Féon et al., 2016).
of insect captures but fewer days of observations during the crop flowering, have used
indirect methodologies to record pollinators (e.g., pan traps, sweep nets) (Bartomeus et al.,
2014; Evans, Smart, Cariveau, & Spivak, 2018; Zou et al., 2017). Instead, we only recorded
insects visiting the flowers, even though being more accurate, our records may be
underestimating the insect visits of very low frequencies and could be overlooking some
other pollinators. However, with minimum temperatures close to 0 °C, the activity of
nocturnal and twilight insects was unlikely (Martín, Castiel, & Sandoval, 2015).
Pollination treatment
The number of pollen grains on stigmas of canola flowers exposed to pollinators was
about twice higher than those from covered flowers. Hayter and Cresswell (2006) found a
positive correlation between the abundance of pollinators and pollen deposited on the stigmas
contrary, previous studies did not find significant differences in the pollen deposited on
stigmas between covered and exposed flowers to canola pollinators (Montaldo et al., 1996).
These different trends could be explained because of variations in the grain counting
methodologies and the crop varieties used in the experiments. In the present study, the mean
ovules per flower. Therefore, the differences found in reproductive parameters would not be
attributable to pollen limitation in quantity but to its quality. Low pollen quality usually has
negative effects on both seed set and fruit set (Aizen & Harder, 2007; Lee, 1988).
The dependence of canola yields on pollinators varies from 0 to 50%, depending on the
crop variety (Garratt, Brown, Hartfield, Hart, & Potts, 2018). We did not measure yield
(weight of seeds per ha), but we demonstrated the increase in many reproductive parameters
that might result in a higher yield. For example, the fruit set has been considered the most
important indicator to estimate yields in B. napus (Durán et al., 2010). When comparing the
number of fruits per plant produced between covered and exposed plants, the values ranged
from no significant differences (Garratt, Bishop, et al., 2018) to high increases (Adegas &
Nogueira Couto, 1992; Durán et al., 2010; Lerin & Rivault, 1982; Zou et al., 2017). In our
study, a concomitant rise between seed production and mean seed mass was observed and
agrees with previous reports (Ali et al., 2011; Bommarco et al., 2012; Witter et al., 2014; Zou
et al., 2017); although some other studies report a trade-off between total seed production per
plant and mean seed mass (Hayter & Cresswell, 2006; Lerin & Rivault, 1982; Steffan-
dewenter, 2003). Nevertheless, seed mass is a complex trait that can be strongly influenced
by genetic and environmental factors (Jauker & Wolters, 2008). Our results suggest that the
local pollinator community can improve all reproductive parameters of canola in the two
The amount of pollen deposited on stigmas did not differ significantly between exposed
flowers distant or in the proximity to semi-natural habitats. Our records of visits were high
enough to let us propose that all exposed flowers did not have pollen limitation. In European
reproductive parameters with pollinators, they did not find effects of distances to semi-natural
habitats (within a range of 20 to 200 m) (Perrot et al., 2018; Woodcock et al., 2016). In
contrast, we showed the negative effects of distance for canola reproductive parameters,
particularly a significant decrease in fruit set of those plants located distances over 50 m from
the semi-natural habitats. These different trends for distance effects may involve many
factors; among them, European beekeepers have a higher annual loss in their hives compared
to Argentina (Maggi et al., 2016; IPBES, 2016), feral honey bees are more common in South
America (Freitas et al., 2009) and also because there are beekeepers in the study region (see
above).
would be important to establish policies that encourage the protection of natural flora near
stands like edges of crops and support diversified farming systems, like the incorporation of
previous crops that attract insects to keep nectar offer all year (Carvalheiro, Seymour,
Nicolson, & Veldtman, 2012). For crop pollination, the policy goal could be to secure a
that pollinators can move across them (Dicks et al., 2016). Some countries where
monocultures prevail are promoting new initiatives to protect pollinators and promote
CONCLUSIONS
exotica Wiedemann and Toxomerus sp. are mentioned for the first time in this study.
Besides, this is the first report for Diptera of the families Bibioinidae and Sarcophagidae
braziliensis Moore, and Colias lesbia Fabricius. Two B. napus varieties studied in
pollinators and to the proximity from semi-natural habitats. Pollinators increased fruit set,
seeds per pod, seed mass, and seed production per infructescence, and crop proximity to
scarce and small semi-natural habitats was enough to increase fruit set and seed
input for canola production even in landscapes of central Argentina with low natural
biodiversity.
ACKNOWLEDGMENTS
We are grateful to Tom Breeze for his help in English grammar and discussion. We thank
two anonymous reviewers for their helpful comments on the manuscript; C. Fernández and
G. Montero for her collaboration in the identification of species and P. Torres for her
contributions with the statistical analysis; and CONICET, SECyT (UNC), FONCyT, and
support.
Author contributions
Mariana Mazzei
Jose Vesprini
Leonardo Galetto
SUPPLEMENTAL MATERIAL
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Insect pollination
Frequency of
Order Family Genus Species Morpho-species visits (%)
Apis
Apis mellifera Apis mellifera 93.06
Apidae Xylocopa - Xylocopa sp. 0.15
SS SS
Model Treatment Distance
Amount of pollen deposited on stigmas, LMER with family Gaussian
1 treatment+ distance+(1|stand)
2 treatment+(1|stand) <0.001 -
Fruit set, GLMER with Poisson family
1 treatment+ distance+(1|stand) <0.001 <0.05
2 treatment+(1|stand)
Seed per pod, LMER with Gaussian family
1 treatment+ distance+(1|stand)
2 treatment+(1|stand) <0.001 -
Seed mass, LMER with Gaussian family
1 treatment+ distance+(1|stand)
2 treatment+(1|stand) <0.001 -
Seed production per infructescence, GLMER with Gamma family
1 treatment+ distance +(1|stand) <0.05 <0.001
2 treatment+(1|stand)
Table 2. Selection of models. Models tested and selected (in bold) for each of the variables
analyzed. The last two columns refer to the statistical significance (SS) of the fixed factors