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Cropscience

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Mariana Mazzei
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© © All Rights Reserved
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Semi-natural habitats and their proximity to the crop enhances canola (Brassica napus) pollination

and reproductive parameters in Argentina

Mazzei, Mariana Paola1*, Vesprini, José Luis1, Galetto, Leonardo2

Affiliations:

1
Instituto de Investigaciones de Ciencias Agrarias de Rosario, CONICET, Facultad de

Ciencias Agrarias de Rosario, Universidad Nacional de Rosario, Campo Experimental

Villarino, Provincia de Santa Fe, Zavalla S2125ZAA, Argentina.

2
Instituto Multidisciplinario de Biología Vegetal, CONICET, Facultad de Ciencias

Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Av. Vélez Sarsfield 299,

Provincia de Córdoba, Córdoba X5000JJC, Argentina.

“Received ___________. *Mazzei, Mariana Paola ([email protected]).”

Abbreviations: SP, seed production per infructescence.

Abstract

The diversity and abundance of pollinators are increased in cultivated areas in

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

placed at different distances from semi-natural habitats in central Argentina. Inflorescences

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.

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compared in plants growing in the proximity (<50 m) and distant (>50 m) from semi-natural

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

agricultural regions of the world (~5Mha) (Leguizamón, 2014). Currently, herbicide-tolerant

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

landscape, affecting mainly non-crop habitats such as semi-natural grasslands (Cerezo,

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,

Sabatino, & Aizen, 2014). Consequently, biodiversity conservation in agro-ecosystems is an

important issue for those crops that interact with pollinators because they tend to have lower

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2
yields in the absence of pollinators (Garibaldi et al., 2013; The Intergovernmental Science-

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;

Holzschuh, Dormann, Tscharntke, & Steffan-Dewenter, 2011).

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.,

2018; Zou et al., 2017).

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,

This article is protected by copyright. All rights reserved.


3
Blochtein, Ferreira, & Witter, 2010; Witter et al., 2014) and most only consider a limited

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;

Marinozzi et al., 2017) but did not report yield components.

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

parameters. We hypothesize that insect pollination improves canola reproductive parameters

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-

plants is increased from the semi-natural habitats.

MATERIALS AND METHODS

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

This article is protected by copyright. All rights reserved.


4
spring-type variety of Nuseed: Bioaureo 2486, with a density of 4.5 kg of seeds.ha-1). Stand

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

Minimum temperatures during the sampling period were close to 0 °C (Facultad de

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

visits was calculated as: abundance of a morpho-species /total pollinator abundance*100.

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

Sciences Rosario National University.

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5
Distance to semi-natural habitats and pollination treatment

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

away from semi-natural habitats in one of them (stand A).

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).

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6
Impacts on the pollination process

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).

Impacts on reproductive parameters

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)

were calculated as SP of exposed inflorescences - SP of covered inflorescences) / SP of

exposed inflorescences x 100. Differences in SP for the proximity to semi-natural habitats

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were calculated as SP of proximal inflorescences - SP of distant inflorescences / SP of

proximal inflorescences x 100.

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

likelihood ratio test with the ANOVA function.

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 %

(Xylocopa sp .and Anthomyiidae sp.) (Table 1).

Pollination treatment

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The amount of pollen deposited on stigmas showed significant differences (p <0.001)

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)).

Also, insect pollination increased SP by 35% in exposed inflorescences compared to covered

(Table 2; Figure 1(e)).

Distance to semi-natural habitats

The amount of pollen deposited on stigmas, seeds per pod, and seed mass did not show

significant differences between flowers in the proximity or distant to semi-natural habitats

(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,

pollinators associated with semi-natural habitats increased SP by 34% in plants in the

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

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9
Rosario with 12 apiaries and 932 hives) (Ministerio de Producción y Trabajo, 2019) and feral

honeybees usually dominate pollinator assemblages associated with many pollinator-

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).

Regarding the methodology, other investigations, which included larger daily-periods

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

indicating that pollen deposition is a reliable indicator of pollinator abundance. On the

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

This article is protected by copyright. All rights reserved.


10
pollen deposited per stigmas in both experimental treatments greatly exceeded the number of

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

varieties evaluated in the present study (Supplemental Figure S2).

Distance to semi-natural habitats

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

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11
studies, the richness of Apoidea interacting with canola was invariable to the heterogeneity of

landscapes (Bommarco et al., 2012). Although some authors reported an increase in

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).

Agro-ecosystems need to incorporate pollinators as an input for some crops

conceptualizing semi-natural habitats as important as other usual issues for agriculture. It

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

minimum level of appropriate habitat distributed throughout productive landscapes at scales

that pollinators can move across them (Dicks et al., 2016). Some countries where

monocultures prevail are promoting new initiatives to protect pollinators and promote

agroecology (Garibaldi et al., 2019).

CONCLUSIONS

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12
Although Apis mellifera (exotic pollinator) was the most frequent pollinator, Allograpta

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

visiting canola flowers, as well as three Lepidoptera: Vanessa carye Hübner, V.

braziliensis Moore, and Colias lesbia Fabricius. Two B. napus varieties studied in

Argentina positively responded in pollen deposited and reproductive parameters to

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

production per infructescence. Therefore, the pollination ecosystem service is a relevant

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

PDTS (Proyecto de desarrollo Tecnológico y Social) CONICET-SYNGENTA for financial

support.

Author contributions

Mariana Mazzei

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13
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing-

original draft, Writing-review & editing.

Jose Vesprini

Conceptualization, Data curation, Investigation, Methodology, Resources, Supervision,

Writing-review & editing.

Leonardo Galetto

Conceptualization, Formal analysis, Funding acquisition, Methodology, Project

administration, Resources, Supervision, Writing-review & editing.

SUPPLEMENTAL MATERIAL

Pollinator photos (Supplemental Figure S1), and Reproductive parameters differences

between stands (Supplemental Text S1, Figure S2).

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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

Hymenoptera Vespidae Brachygastra - Brachygastra sp. 0.46


Allograpta Allograpta
Allograpta exotica exotica 1.54

Toxomerus - Toxomerus sp. 1.54


Syrphidae Eristalis - Eristalis sp. 0.77
Sarcophagidae
Anthomyiidae - - sp. 0.15

Bibionidae - - Bibionidae sp. 0.77


Diptera Unidentified - - Unidentified 0.46
Vanessa
Vanessa carye Vanessa carye 0.46
Vanessa Vanessa
Nymphalidae Vanessa braziliensis braziliensis 0.62
Colias
Lepidoptera Pieridae Colias lesbia1 Colias lesbia1 -

Table 1. Observed pollinators and frequency of visits (%).

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1
Species observed outside the sampling sites.

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

analyzed for the selected model (p-value<0.001, p-value<0.05).

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Figure. 1 Box-plots of response variables for two treatments (covered and exposed inflorescences to
pollinators) and two distances (proximal and distant to semi-natural habitats). (a) amount of pollen
deposited on stigmas, exposed flowers to pollinators presented a higher significant number of pollen
grains (see Table 2); (b) fruit set (number of pods per infructescence), exposed flowers to pollinators
and plants growing in proximity to semi-natural habitats presented a higher significant fruit set (see
Table 2); (c) seeds per pod, exposed flowers presented significant higher seeds per pod (see Table 2);
(d) seed mass (g mean mass per seed), seed mass was significantly higher in flowers exposed to
pollinators (see Table 2); (e) SP: seed production per infructescence (fruit set x seeds per pod x seed
mass), seed production per infructescence was significantly higher in flowers exposed to pollinators and
in plants growing in proximity to
semi-natural habitats (see Table 2).

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