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Color-advertising strategies
of invasive plants through
the bee eye
Martin Dessart
1
†
,
João Marcelo Robazzi Bignelli Valente Aguiar
2
†
,
Eric Tabacchi
3
, Sylvie Guillerme
4
*
‡
and Martin Giurfa
5,6
*
‡
1
Institut de Recherche sur la Biologie de l'Insecte, Centre National de la Recherche Scientifique
(CNRS), University of Tours, Tours, France,
2
Programa de Po
´s-Graduac¸ão em Entomologia, Faculdade
de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São
Paulo, Brazil,
3
Centre de Recherche sur la Biodiversité et l'Environnement (CRBE), UMR 53000, Centre
National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Développement (IRD),
Institut National Polytechnique, Université Paul Sabatier, Toulouse, France,
4
Laboratoire Ge
´ographie
de l’Environnement (GEODE), Centre National de la Recherche Scientifique (CNRS), University
Toulouse Jean-Jaure
s, Toulouse, France,
5
Institut Universitaire de France, Paris, France,
6
Neuroscience Paris-Seine - Institut de Biologie Paris-Seine, Centre National de la Recherche
Scientifique (CNRS), Institut National de la Sante
´et de la Recherche Médicale (INSERM), Sorbonne
University, Paris, France
Invasive plants represent a significant global challenge as they compete with
native plants for limited resources such as space, nutrients and pollinators. Here,
we focused on four invasive species that are widely spread in the French
Pyrenees, Buddleja davidii,Reynoutria japonica,Spiraea japonica and Impatiens
glandulifera, and analyzed their visual advertisement signals with respect to those
displayed by their surrounding native species using a perceptual approach based
on the neural mechanisms of bee vision given that bees are regular pollinators of
these plants. We collected 543 spectral reflections from the 4 invasive species,
and 66 native species and estimated achromatic and chromatic similarities to the
bee eye. R. japonica, S. japonica and B. davidii were inconspicuous against the
foliage background and could be hardly discriminated in terms of color from their
surrounding native plants. These characteristics promote generalization,
potentially attracting pollinators foraging on similar native species. Two
morphs of I. glandulifera were both highly salient in chromatic and achromatic
terms and different from their surrounding native species. This distinctive identity
facilitates detection and learning in association with rich nectar. While visual
signals are not the only sensory cue accounting for invasive-plant success, our
study reveals new elements for understanding biological invasion processes from
the perspective of pollinator perceptual processes.
KEYWORDS
invasive plants, honey bee, vision, color detection, color discrimination
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Jair E. Garcia,
RMIT University, Australia
REVIEWED BY
Zong-Xin Ren,
Chinese Academy of Sciences (CAS), China
Junpeng Mu,
Mianyang Normal University, China
*CORRESPONDENCE
Sylvie Guillerme
sylvie.guillerme@univ-tlse2.fr
Martin Giurfa
martin.giurfa@sorbonne-universite.fr
†
These authors share first authorship
‡
These authors share senior authorship
RECEIVED 28 February 2024
ACCEPTED 30 April 2024
PUBLISHED 22 May 2024
CITATION
Dessart M, Aguiar JMRBV, Tabacchi E,
Guillerme S and Giurfa M (2024)
Color-advertising strategies of
invasive plants through the bee eye.
Front. Plant Sci. 15:1393204.
doi: 10.3389/fpls.2024.1393204
COPYRIGHT
©2024Dessart,Aguiar,Tabacchi,Guillerme
andGiurfa.Thisisanopen-accessarticle
distributed under the terms of the Creative
Commons Attribution License (CC BY). The
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
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accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Original Research
PUBLISHED 22 May 2024
DOI 10.3389/fpls.2024.1393204
1 Introduction
Invasive plant species represent a significant challenge in
globalization times as they compete with native plants and animals
for limited resources, modifying habitats and reducing biodiversity
(IUCN Council, 2000;Charles and Dukes, 2007;Hejda et al., 2009;
Pysek et al., 2012;Barney et al., 2013;Langmaier and Lapin, 2020).
Their success in certain biotopes indicates that some species rely on
highly competitive traits allowing themto conquer and thrive in newly
colonized ecosystems (Parker et al., 1999;Gioria and Osborne, 2014).
Invasive plant species compete with native species for space, nutrients
(Skurski et al., 2017) and pollinators (Traveset and Richardson, 2006;
Bjerknes et al., 2007;Kovacs-Hostyanszki et al., 2022). Several studies
have revealed the disruption of native plant-pollinator networks by
successful invasive plant species in detriment of native plant species,
highlighting thereby one of the key factors of their success (Ghazoul,
2004;Bjerknes et al., 2007;Bartomeus et al., 2008;Goodell and Parker,
2017;Stout and Tiedeken, 2017;Burns et al., 2019;Parra-Tabla and
Arceo-Gomez, 2021;Kovacs-Hostyanszki et al., 2022). Some invasive
plants may provide richer nectar, being therefore particularly
attractive for pollinators (Chittka and Schurkens, 2001), or more
conspicuous flowers that outcompete those of native plants (Traveset
and Richardson, 2006;Sooraj et al., 2019). They are also usually
generalists with respect to pollinators, a strategy that allows them
benefiting from the fertilization contribution of local pollinators
(Richardson et al., 2007;Parra-Tabla and Arceo-Gomez, 2021).
Abundant invasive plants can even dominate the plant-pollinator
network, to a point where the interaction between native plants and
their pollinators is modified (Albrecht et al., 2014).
Color is one of the main advertising cues displayed by flowers to
pollinators (Kevan, 1983;Weiss, 1991;Menzel and Shmida, 1993;
Chittka et al., 1999). Among the main pollinators of flowers, the
western honey bee (Apis mellifera L.) is the most frequent floral
visitor of crops worldwide (Hung et al., 2018;Khalifa et al., 2021).
Honey bees are also one of the insects best studied in terms of their
visual perception, from behavior to the neural underpinnings of
visual performances (Giurfa and Lehrer, 2001;Avarguès-Weber
et al., 2011;Avarguès-Weber et al., 2012;Mota et al., 2013;
Avarguès-Weber and Giurfa, 2014). Bees possess trichromatic
color vision based on three photoreceptors types with sensitivities
peaking at 344 nm in the short-wave (ultra violet) region of the
spectrum, 436 nm in the middle-wave (blue) region, and 544 nm in
the long-wave (green) region of the spectrum (L receptor),
respectively (Menzel and Blakers, 1976;Peitsch et al., 1992).
Photoreceptor signals are fed into color-opponent neurons
present in higher-order visual areas of the bee brain (Kien and
Menzel, 1977;Backhaus, 1991), giving origin to color sensations.
Color processing networks are therefore well-characterized in the
honey bee, which provided the basis for the conception of color
perceptual spaces that allow determining to what extent colors are
discriminable for a honey bee (Backhaus, 1991;Chittka, 1992). This
strategy has been used to assess flower color perception and
discrimination by bees in multiple studies e.g. (Kevan et al., 1996;
Reisenman and Giurfa, 2008;Arnold et al., 2009;Aguiar et al., 2020;
Shrestha et al., 2024).
However, few analyses have focused on the floral color of
invasive species and its role and contribution to their ecological
success from a pollinator vision perspective. Analyses performed on
an Indian community including 22 native and 8 invasive plant
species showed that invasive species with higher UV absorbance
tended to differ chromatically from native species, a strategy that
may increase their attractiveness and discriminability for
pollinators (Sooraj et al., 2019). Yet, the strategy adopted by
invasive plants may vary significantly according to the
characteristics of their ecological niche and those of the
surrounding native species.
The region of the Pyrenees, delimiting the border between
France and Spain, has been subjected to intensive invasion by
various plant species (Guillerme et al., 2020;Claudel et al., 2022).
The area is also rich and reputed for the diversity of local flora
(Saule, 2002) and the presence of numerous bee pollinating species
so that it provides an attractive and relevant scenario to study the
color strategies used by invasive plant species. Understanding the
role of floral coloration through the bee eye is a powerful proxy for
understanding the success of invasive plants’reproduction. We thus
focused on four dominant invasive plant species that can be found
in the French Pyrenees, the butterflybush(Buddleja davidii,
Scrophulariaceae), the Japanese Knotweed (Reynoutria japonica,
Polygonaceae), the Japanese Spirea (Spiraea japonica, Rosaceae)
and the Himalaya Balsam (Impatiens glandulifera, Balsaminaceae),
which are frequently visited by honey bees (Ellis and Ellis-Adam,
1993;Najberek et al., 2023). We studied how their color displays are
perceived by bee pollinators in comparison to those of surrounding
native species. To this end, we used perceptual neural modelling of
honey bee vision, which allowed us to analyze the color advertising
strategies of invasive species as seen by the bee eye. While an
integrative analysis of invasive-plant success should include
measures of plant visitation by pollinators and of plant fitness,
our goal here was to rely on a neuroscience approach to provide
evidence on pollinator perception that could serve as guide for
future works by scholars working in ecology, plant science and
other related disciplines.
Our results show that the color advertising strategies of the four
species considered are heterogeneous as some of them display
colors that are similar to those of surrounding native species,
potentially promoting generalization, while others display highly
prominent color and achromatic cues different from those of the
surrounding native species to facilitate color detection and learning
by pollinators.
2 Materials and methods
2.1 Study area and invasive plant species
We investigated two sites located at the foothills of the Central
Pyrenees Mountains (SW France, Figure 1): the Pique Valley (42°45’
N, 0°37’E, 1200 m mean altitude) (Figure 1A) and the Oussouet
Valley (43°5’N, 0°5’E, 800 m mean altitude) (Figure 1B). Both have
very similar landscapes including agro-pastoral and forested units
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hosting high levels of plant and animal biodiversity (Rhone, 2015),
including abundant invasive species (Tabacchi et al., 2010;Guillerme
et al., 2020;Jantzi et al., 2021). The climate of the sampled sites
corresponds to mountain-oceanic temperate conditions (Mean
temperature: 4,0 –16,5°C; Monthly accumulated precipitation:
27,8mm –174,2mm).
The dominant invasive species found in the study areas were the
butterfly bush (Buddleja davidii Franch.; Figure 1C), the Japanese
Knotweed (Reynoutria japonica Houtt.; Figure 1D), the Japanese
Spirea (Spiraea japonica L.;Figure 1E) and the Himalaya Balsam
(Impatiens glandulifera Royle; Figure 1F), which provided the basis
for our study. The latter included three different morphs, which
appeared violet (Figure 1G), white (Figure 1H) and pink (Figure 1I)
to the human eye.
We conducted our surveys at four distinct dates - 20
th
and 22
nd
of July 2020, 23
rd
and 28
th
of September 2020 - which corresponded
to the average maximum development of the vegetation.
For each sampling session, we chose 12 representative
permanent vegetation patches centered on a particular hotspot of
a specific invasive plants among the four species targeted. Each
patch corresponded to one invasive species; in total, we established
2 patches for B. davidii, 3 patches for R. japonica, 1 patch for S.
japonica and 2 patches for each morph of I. glandulifera (6 patches
for I glandulifera). Each patch corresponded to a particular site in
order to integrate spatial variability. Data were pooled as an analysis
per patch would require a higher number of replicates, which was
not easily accessible. At the regional scale, these sampling units were
selected based on an aerial photograph survey. The location of each
patch was confirmed by local preliminary field surveys. Within each
identified patch, we delineated four concentric zones (Figure 1J).
The ‘core zone’was densely and almost exclusively occupied by one
of the invasive species chosen for our study. The ‘inner edge zone’
was delineated as an inner ring within the core zone (~1,5 m wide
strip) using the average quasi-absence (< 5% cover) of the invader as
criterion. The ‘outer edge zone’was defined as an external ring
surrounding the core zone (~1,5 m wide strip) in which the invader
was totally absent. Finally, the more eccentric ‘surrounding zone’
was defined as a broader area included within a 20m width strip
beyond the outer edge zone. By definition the more external zone
corresponds to areas where the invader was absent. This is a
consequence of the patchy pattern induced by the competition/
colonization processes, but probably also by the effect of
management (mowing) in the outer zone.
2.2 Reflectance measurements and analysis
A minimum of three fresh flowers of each species were
systematically collected at each patch along the four zones in order
to measure their spectral reflectance. Reflectance measurements in
the bee visible range (300 –650 nm) (Menzel and Blakers, 1976) were
performed in situ and with a resolution of 1 nm using a UV-VIS
Ocean Optics USB400 spectrometer (Dunedin, Florida, USA) and a
pulsed Xenon Lamp PX-2 light source. A white standard (barium
FIGURE 1
Study areas, invasive species studied and sampling strategy. (A) Relief map of the Pique Valley (42°45’N, 0°37’E, 1200 m mean altitude), one of the
areas chosen for our study. (B) Relief map of the Oussouet Valley (43°5’N, 0°5’E, 800 m mean altitude), the other area chosen for our study.
(C) The invasive butterfly bush (Buddleja davidii Franch). (D) The invasive Japanese Knotweed (Reynoutria japonica Houtt). (E) The invasive Japanese
Spirea (Spiraea japonica L.). (F) The invasive Himalaya Balsam (Impatiens glandulifera Royle). The latter included three different morphs, which
appeared violet (G), white (H) and pink (I) to the human eye. (J) Sampling strategy of permanent vegetation patches centred on a particular hotspot
of a specific invasive plants. Within each patch, four concentric zones were established. The ‘core zone’was densely invaded by one of the invasive
species chosen for our study. The ‘inner edge zone’was delineated as an inner ring within the core zone (~1,5 m wide strip) using the average quasi-
absence (< 5% cover) of the invader as criterion. The ‘outer edge zone’was defined as an external ring surrounding the core zone (~1,5 m wide strip)
in which the invader was totally absent. Finally, the more eccentric ‘surrounding zone’was defined as a broader area included within a 20m width
strip beyond the outer edge zone. For each plant species, we estimated visually the relative cover within each zone.
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sulphate) was used to calibrate the spectrophotometer before each
session of measurements. The reflectance spectra of 70 plant species
were included in our analyses (see Supplementary Table S2).
Reflectance spectra were obtained from 50 native species (n = 333
spectra; 1 spectrum corresponding to 1 flower part) and from the 4
invasive species mentioned above (n = 102 spectra), all collected in
the field, in the areas defined for our sampling. The FRED database
(Arnold et al., 2010) allowed us to include 16 additional native species
(n = 34 spectra) to complement our measurements (Supplementary
Table S2). These species were present in the field and were counted
for abundancy measurements but were inaccessible for reflectance
measurements. The same database was used to include
complementary measurements for 32 native species (n = 74
spectra) that were also sampled in the field (see Supplementary
Table S2 for details). Overall, our analyses included 543 spectra
(435 from the field and 108 from the FRED data), from 70 plant
species, including the 4 invasive species, which were the focus of our
study, and 66 native species (18 exclusively from the field, 16
exclusively from the FRED data base, and 32 both from the field
and the FRED data base). For all species, both spectral curves and
relative abundance measurements were available and used for our
analyses. We also measured the spectral reflectance from leaves of 15
species (n = 25 spectra) to characterize the green foliage background
(see Supplementary Table S2).
2.3 Color perception models
We used the pavo package (Maia et al., 2013) to normalize
reflectance spectra in the wavelength range comprised between 300-
650 nm. Curves were smoothed to remove noise. Flower reflectance
curves were averaged within each species. All statistical analyses
were conducted using R software version 4.0.4 (https://www.r-
project.org/).
To test differences in flower colour according to pollinator vision,
floral reflectance data were transformed into color loci within the
color hexagon, a perceptual space allowing the evaluation of flower
colors as seen by honey bees, which are dominant pollinators in the
regions of interest (Chittka, 1992). For calculations, we used the
standard illuminant function D65, the average function obtained
from green leaves sampled as the background and the spectral
sensitivity curves of the three photoreceptor types of the honey bee
Apis mellifera (Peitsch et al., 1992). We created the coldspace object
by passing the vismodel object and selected the hexagon to plot our
models. To calculate color distances, we passed the coldspace object
and obtained unweighted Euclidean distances. All the data and code
used are available in: https://github.com/martindessart/
Invasive_plants_through_bee-eye_Pyrenees.
2.4 Data clustering and PCA analysis
In order to evaluate the color similarity of invasive and native
flower species to the honey bee eye, we first calculated indices to
determine the optimized number of clusters of flower loci within the
hexagon space. These clusters were used to describe our dataset into
predefined groups that have similar properties.
We first used the NbClust package from R software (Charrad
et al., 2014), which provides 30 indices and allows choosing the best
clustering size for our data set. We verified this choice using the
function fviz_nbclust associated with the silhouette method from
the FactoExtra package (Kassambara and Mundt, 2020). We ran a
PCA analysis based on the coordinates of the flower loci in the
hexagon space using k-means clustering. This method of vector
quantization partitioned our data into k groups that minimized the
sum of squares from points to the assigned cluster center (see
Supplementary Material). All statistical analyses were conducted
using R software version 4.0.4 (https://www.r-project.org/).
2.5 Question 1: do invasive floral species
have more salient visual cues to the
bee eye?
For each flower species, we calculated the chromatic contrast,
the achromatic contrast and the spectral purity. The chromatic
contrast refers to the perceptual difference between the color of the
flower and that of the background. Given that the color hexagon is a
bidimensional space that includes only the dimensions of hue and
saturation (i.e. no brightness dimension), the chromatic contrast
can be quantified as the distance between the locus of a flower
species in that space and that of the background. The latter occupies
the center of the space (0, 0 coordinates) as it acts as the adaptation
background against which colors are evaluated (Chittka, 1992).
Chromatic contrast involves true color vision and allows close-up
detection of color targets with larger visual angles, i.e. typically
larger than 15° (Giurfa et al., 1996b;Giurfa et al., 1997). Chromatic
differences between color loci are quantified in terms of the
Euclidian distance between two color loci (see below); in the
hexagon this distance is given in hexagon units HU (Chittka, 1992).
The achromatic contrast refers to the relative number of
absorbed quanta by the L-receptor type (longwave or ‘green’
photoreceptor type) upon stimulation with the flower color with
respect to the background. This receptor-specific contrast provides
an achromatic channel allowing long-distance detection of visual
targets (i.e. targets with a reduced visual angle, typically smaller
than 15°) (Giurfa et al., 1997;Giurfa and Vorobyev, 1998).
Finally, the spectral purity represents the saturation of a given
color, a variable that may affect floral preference in bees (Lunau,
1990;Lunau, 1992;Lunau et al., 2006;Rohde et al., 2013). It is
quantified by dividing the distance between the loci of the floral
color and the background (chromatic contrast, see above) by the
distance between the corresponding monochromatic light with the
same dominant wavelength as the color target and the background
(Lunau et al., 1996).
Two steps were designed for the analysis of flower salience. First,
group-level salience was assessed by comparing invasive and native
flowers in terms of three variables defined above (i.e., chromatic
contrast, achromatic contrast and spectral purity) using a one-
sample Kruskal-Wallis H test with group as the fixed factor. To
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analyze the salience of one invasive species with respect to groups of
native species, a one-sample Wilcoxon signed-rank test was used
setting the invasive-species value of the variable considered as
reference for the comparison. This analysis was also performed
segregating groups and invasive species according to the sample
areas (core, inner and outer edges and surrounding).
2.6 Question 2: are invasive flowers
species discriminable from native species
to the bee eye?
We followed the procedure from Maia and White (2018) to
determine if colors were discriminable from each other. The
method considers the statistical distribution, the within-group
variation and the discriminability of groups based on honey bee
visual abilities. A distance-based PERMANOVA using the
Euclidian distances between species in the hexagon was applied to
two groups of interest (e.g., groups determined by the clustering
analysis) to determine if they were significantly distinct. A bootstrap
procedure was then applied to simulate new samples, in order to
obtain a distribution of the mean distance between each sample and
the group geometric mean, and thus a 95% confidence interval for
each color comparison. We finally compared the values obtained for
each invasive species to the bees’color discrimination threshold of
0.1 hexagon units (HU), which has been reported for bees trained
under absolute conditioning (a single color rewarded) (Dyer and
Chittka, 2004). This kind of training corresponds to the ecological
scenario of a flower-constant pollinator visiting a single species
during its foraging bouts. If a color distance was lower than this
threshold, we concluded that the samples compared were
perceptually similar and thus indistinguishable in chromatic
terms by honey bees (Maia and White, 2018).
3 Results
3.1 Spectral reflectance curves and flower
colors in perceptual color spaces
We measured the spectral reflectance of the four invasive
species considered in our study, Reynoutria japonica, which was
whitish to the human eye, Buddleja davidii, which was violet-
pinkish to the human eye, Spiraea japonica L., which was pink to
the human eye (Figure 2A), and Impatiens glandulifera, which
presented three different colored morphs that appeared violet, white
and pink to the human eye (inset of Figure 2A). In addition, we
measured the average reflectance of green leaves present in the
sampling areas (Figure 2A) in order to use it as the background for
representing flower colors in perceptual color spaces. Our
measurements allowed us to represent the loci of the invasive
species, together with those of all flower species included in our
study, in the perceptual spaces of the color hexagon (Figure 2B) and
the color opponent coding space (Figure 2C)defined for the honey
bee. Subsequent analyses on flower color loci were restricted to the
color hexagon given the higher generality of this perceptual space
for pollinators other than honey bees (Backhaus, 1991;
Chittka, 1992).
ABC
FIGURE 2
(A) Spectral reflectance curves of the four invasive floral species studied. Normalized average reflectance (%) of Buddleja davidii,Reynoutria japonica,
Spiraea japonica and Impatiens glandulifera. Royle in the visible range of the honey bee Apis mellifera (from 300 to 650 nm). The average
reflectance of green leaves used as background for further perceptual analyses of floral colors is also shown. The inset shows the normalized
average reflectance (%) of the three morphs of I. glandulifera,IgP (pink), IgV (violet) and IgW (white). (B) Color loci of the flower species analyzed in
the color hexagon. The colour hexagon is a generalized color opponent space with metrics applicable to numerous species of Hymenoptera. The
average reflectance of green leaves was used as background and corresponds to the center of the hexagon. Photoreceptor excitations E(UV), E(B), E
(G) are plotted at angles of 120°. The hexagon is divided in six segments corresponding to six categories, which refer to the ways in which the bees’
receptors are stimulated by given pure broad-band spectral stimuli, or with uv-green, mixed spectral stimuli: u (ultraviolet), ub (ultraviolet-blue), b
(blue), bg (blue-green), g (green) and ug (ultraviolet-green). The loci within the space correspond to the 66 native species (black dots) and the 4
invasive species, one of which had three different morphs (white diamonds), i.e. 72 color loci represented. The closed line surrounding the floral
color loci defines the boundaries of color perception at adaptation light. The loci along the spectral line are marked in 10 nm steps, and the mixtures
of 300 and 550 nm (ultraviolet-green) in 10% steps. (C) Color loci of the flower species included in our analyses in the color opponent coding (COC)
space. The COC space is a color opponent space in which floral color loci of invasive species, native species of Group1 and native species of Group
2 are plotted as a function of the responses of two types of colour opponent coding cells, A and B. The origin of the graph represents the green
leaves used as background. The loci within the space correspond to the 66 native species (black dots) and the 4 invasive species, one of which had
three different morphs (white diamonds), i.e. 72 color loci represented. The closed line surrounding the floral color loci defines the boundaries of
color perception at adaptation light. The loci along the spectral line are marked in 10 nm steps, and the mixtures of 300 and 550 nm (ultraviolet-
green) in 10% steps.
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3.2 Data clustering and PCA analysis
Unsupervised hierarchical clustering was performed on our
flower data set to group species by color. First, we assessed the
clustering tendency by calculating the Hopkins statistic using the
get_clust_tendency function from the FactoExtra R package
(Kassambara and Mundt, 2020). The closer the Hopkins statistic is
to 1, the more the data are clustered (Jove et al., 2020). In our case, the
value of 0.726 indicated that the dataset contained suitable information
for clustering. We then performed two independent analyses to
validate the correct number of clusters using the NbClust package
and the FactoExtra package. The data clustering analysis separated two
distinct groups according to their color loci (Figure 3A).
The first group (hereafter Group 1) included 52 species (48 native
species and the 4 invasive species), which were located in the bee UV-
blue and blue regions of the hexagon (human blue –purple)
(Figure 2B). The second group (hereafter Group 2) included 18
native species, which were located in the bee ultraviolet-green and
green regions of the hexagon (Figure 2B). Invasive flower species were
located per definition in the core zone as sampling patches were
centered on a particular hotspot of an invasive plant species
(Figure 3B). They could also bee found in the inner edge zone.
Group-1 native species were mostly found close to patch core zones,
i.e. in the inner and the outer edge zones. Group-2 native species were
less frequent and usually located in the outer edge and the
surrounding zones of the designed plots in the field (Figure 3B).
3.3 Question 1: do invasive floral species
have more salient visual cues to the
bee eye?
We calculated the average chromatic contrast, achromatic
contrast and spectral purity for the four invasive species and for
the native species of Group 1 and Group 2 (Figures 4A–C; see
Supplementary Table S3 for complete set of values).
Chromatic contrast calculations based on the visual system of
honey bees yielded values ranging from 0.05 to 0.40 hexagon units
(HU) (Figure 4A; Group 1: 0.15 ± 0.05; Group 2: 0.18 ± 0.08; Invasive
Species: 0.18 ± 0.08; mean ± SD), which did not differ significantly
between groups (Kruskal Wallis Test: c
2
= 1.69, df: 2 p = 0.43). The
calculation of achromatic contrast yielded values ranging from 0.57
to 1.21 (Figure 4B; Group 1: 0.68 ± 0.12; Group 2: 0.65 ± 0.03;
Invasive Species: 0.76 ± 0.23; mean ± SD), which did also not differ
between groups (c
2
= 0.86, df:2, p = 0.65). Finally, spectral purity
values, which ranged from 0.11 to 0.73 HU (Figure 4C; Group 1: 0.37
± 0.11; Group 2: 0.36 ± 0.15; Invasive Species: 0.40 ± 0.15; mean ±
SD; see Supplementary Table S3), did also not differ between groups
(c
2
= 1.78, df = 2; p = 0.41). These results indicate that when taken
together the four invasive species did not differ in chromatic and
achromatic salience to bee eye. Yet, as the four invasive species
differed in their visual display, averaging their values for a between-
category analysis may hide significant trends at a single-species level.
We thus performed separate comparisons between each invasive
species and the two groups of native species defined in our
cluster analysis.
While no clear differentiation trend was observable for B.
davidii, R. japonica and S. japonica in terms of chromatic
contrast, spectral purity and achromatic contrast, highly
significant differences were found between the I. glandulifera
morphs and Group 1 and 2 of native species (Table 1). While the
violet (Ig V) and the pink (Ig P) morphs presented significantly
higher chromatic and achromatic contrasts, as well as a higher
spectral purity than native species in Groups 1 and 2 (p < 0.0001 for
10 of the 12 comparisons, and p < 0.03 for the remaining two
comparison; see Table 1), the white morph (Ig W) had significantly
lower values for the three variables considered than native species in
Groups 1 and 2 (p < 0.0001 for all 6 comparisons; see Table 1). This
AB
FIGURE 3
(A) Clustering analysis of the floral data set used in this study. Unsupervised hierarchical clustering performed on our flower data set allowed to
distinguish two groups according to their color loci in the hexagon. The two axes indicate in parentheses the % of the data variance accounted for
by our analysis. Group 1 (violet dots) included 52 species: 48 native species and the 4 invasive species Bd (Buddleja davidii), Sj (Spiraea japonica), Rj
(Reynoutria japonica) and the three morphs of Ig (Impatiens glandulifera) IgV, IgW and IgP, all located in the bee ultraviolet-blue and blue regions of
the hexagon. Invasive species are shown by red dots. Group 2 (yellow dots) included 18 native species located in the ultraviolet-green and green
regions of the hexagon. (B) Relative frequency of the invasive species and the two groups of native species in each sampled zone. Per definition,
invasive species were mostly located in the core zone, as sampling areas were centered on a particular hotspot of an invasive plant species. They
could also be located in the inner edge zone among the four species targeted. Group 1 species were mostly found in the inner edge and in the
outer edge zone. Group 2 species were less frequent and usually located in the outer edge and the surrounding zones. Boxplots show the median
(horizontal line) and interquartile ranges. Bars indicate +/- interquartile ranges. Dark squares indicate mean value for the zone considered.
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analysis thus shows that three of the invasive species, B. davidii, R.
japonica and S. japonica, which clustered with native species of
Group 1 (Figure 3), did not differ particularly from their
surrounding native species while I. glandulifera morphs, which
were outside that cluster (Figure 3), adopted a different displaying
strategy to the bees’eyes: the violet and the pink morphs appeared
more salient and thus better detectable to pollinators than native
species, while the white morph was less salient than the
native species.
In order to refine this analysis, we repeated the previous analysis
of chromatic and achromatic contrasts and spectral purity but this
time segregating the data according to the sampling zones defined
in Figure 1J.Figures 5A–Cand Table 2 show the three variables
evaluated (chromatic contrast, achromatic contrast and spectral
purity, respectively) for Groups 1 and 2 of native species and for the
invasive species as a function of the sampling zone. Some significant
differences were found for the three variables when invasive species
were compared to Group 2 of native species (see Table 2, right), in
particular in the case of the achromatic contrast. Yet, the interesting
comparisons are those between invasive species and Group 1 of
native plants as relative-abundance analyses (see Figure 3) showed
that Group 1 species tended to be more present around invasive
species in the central sampling areas (core, inner and outer edge)
than Group 2 species. Figure 5 and Table 2 show that while R.
japonica did neither differ from its surrounding native species in
chromatic contrast nor in achromatic contrast nor in spectral
purity, the other invasive species showed either partial (for one or
two variables) or total (for all three variables) significant differences
with native species of Group 1. B. davidii, for instance, had a higher
achromatic contrast than native species of Group, 1 which favors
long-distance detection (Giurfa et al., 1997), while S. japonica was
more salient in terms of chromatic variables such as chromatic
contrast and spectral purity. I. glandulifera morphs presented
consistent significant differences in all three variables when
compared to surrounding native species of Group 1. The violet
andthepinkmorphs(IgVandIgP)hadsignificantly higher
achromatic and chromatic contrasts and spectral purity than
surrounding native species, which provides advantages in terms
of farther visual detection and higher chromatic salience which may
favour better associative learning by pollinators. Interestingly the
opposite trend was found for the white morph (IgW), which had
significantly lower values for all three variables.
Taken together, these results indicate that the four invasive
species considered in our study use different visual advertising
strategies when compared to their surrounding native species
(Group 1): in general terms, they tended to be more salient to the
bee eye either in one, two or in the three visual variables considered,
which may facilitate their visual detection from farther distances
and their learning based on chromatic cues associated with nectar
reward. Only the white morph of I. glandulifera seems to be in
disadvantage with respect to native species, thus raising the
question of the mechanisms used by this morph to compensate
via other (non-visual) advertising mechanisms for this deficit.
Similar trends were found for the comparisons between invasive
species and native species of Group 2, although these were
less consistent.
3.4 Question 2: are invasive flowers
species discriminable from native species
to the bee eye?
Invasive species had higher achromatic and chromatic contrasts
as well as higher spectral purity, which facilitate visual detection and
learning by bee pollinators; yet, to what extent bees perceive them as
chromatically similar to surrounding native species (i.e. Group 1)
needs to be addressed separately. We thus determined the color
similarity between invasive and native species, which can be
estimated based on the distance between color loci in the color
hexagon. We used the threshold value of 0.1 hexagon units (HU)
reported for colour discrimination of bees trained under absolute
conditioning (Dyer and Chittka, 2004) and determined if the color
distance between the invasive species considered in our work and
Groups 1 and 2 of native species was above or below this threshold.
AB C
FIGURE 4
(A) Chromatic contrast (hexagon Units, HU) of Group1, Group 2 and the invasive species analyzed in our study. No significant differences between
groups were found for this parameter. (B) Achromatic contrast (L-receptor contrast with respect to the background) of Group1, Group 2 and the
invasive species analyzed in our study. No significant differences between groups were found for this parameter. (C) Spectral purity (hexagon Units,
HU) of Group1, Group 2 and the invasive species analyzed in our study. No significant differences between groups were found for this parameter.
Boxplots show the median values (thick line) and interquartile ranges; dots indicate values recorded for each species; black squares indicate mean
values of each group. Number in parentheses indicate sample sizes. NS, not significant.
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TABLE 1 Chromatic contrast, achromatic contrast and spectral purity of single invasive species compared to values of Group 1 and Group 2 of native species.
Comparisons with Group 1 Comparisons with Group 2
Chromatic contrast Achromatic contrast Spectral purity Chromatic contrast Achromatic contrast Spectral purity
V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p
Ig V 054< 0.0001 054< 0.0001 054< 0.0001 318< 0.0001 018< 0.0001 318< 0.0001
Ig P 83 54 < 0.0001 117 54 < 0.0001 244 54 < 0.0001 36 18 0.03 018< 0.0001 35 18 0.03
Ig W 1423 54 < 0.0001 1420 54 < 0.0001 1423 54 < 0.0001 171 18 < 0.0001 170 18 < 0.0001 171 18 < 0.0001
Bd 698 54 0.88 479 54 0.04 727 54 0.92 113 18 0.25 20 18 < 0.01 51 18 0.14
Rj 930 54 0.06 867 54 0.18 829 54 0.32 130 18 0.05 100 18 0.55 66 18 0.42
Sj 446 54 0.02 836 54 0.29 365 54 < 0.01 83 18 0.93 98 18 0.61 36 18 0.03
To analyze the salience of a single invasive species with respect to Groups 1 and 2 of native species, a one-sample Wilcoxon signed-rank test was used setting the invasive-species value of the variable considered as reference for the comparison. V statistic values, sample sizes
(n) of the Group and p values are provided for each comparison performed; df: 1 for all comparisons. Ig V, violet morph of Impatiens glandulifera; Ig P, pink morph of Impatiens glandulifera; Ig W, violet morph of Impatiens glandulifera; Bd, Buddleja davidii; Rj, Reynoutria
japonica; Sj, Spiraea japonica. Values in red indicate significant P values.
TABLE 2 Chromatic contrast (A), achromatic contrast (B) and spectral purity (C) of single invasive species compared to values of Group 1 and Group 2 of native species according to the sample zone (Core, Inner
Edge, Outer Edge and Surrounding).
A)
Chromatic Contrast
Comparisons with Group 1 Comparisons with Group 2
Core Inner Edge Outer Edge Surrounding Core Inner Edge Outer Edge Surrounding
V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p
Ig V 033< 0.0001 054< 0.0001 082< 0.0001 086< 0.0001 6 6 0,2 10 14 < 0.01 15 30 < 0.0001 21 38 < 0.0001
Ig P 16 33 < 0.0001 63 54 < 0.0001 135 82 < 0.0001 121 86 < 0.0001 18 6 0,55 57 14 0,89 155 30 0,07 229 38 0,02
Ig
W595 33 < 0.0001 1540 54 < 0.0001 3482 82 < 0.0001 3819 86 < 0.0001 28 6 0,02 120 14 < 0.001 496 30 < 0.0001 780 38 < 0.0001
Bd 232 33 0,27 746 54 0,84 1622 82 0,58 1825 86 0,71 23 6 0,15 93 14 0,06 395 30 < 0.01 582 38 < 0.01
Rj 332 33 0,56 971 54 0,09 2090 82 0,12 2340 86 0,07 26 6 0,05 100 14 0,02 431 30 < 0.001 647 38 < 0.001
Sj 152 33 0,01 496 54 0,02 1093 82 < 0.01 1147 86 < 0.01 21 6 0,27 81 14 0,24 317 30 0,18 444 38 0,45
(Continued)
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TABLE 2 Continued
B)
Achromatic Contrast
Comparisons with Group 1 Comparisons with Group 2
Core Inner Edge Outer Edge Surrounding Core Inner Edge Outer Edge Surrounding
V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p
Ig V 033< 0.0001 054< 0.0001 082< 0.0001 086< 0.0001 060,02 014< 0.001 030< 0.0001 038< 0.0001
Ig P 15 33 < 0.0001 88 54 < 0.0001 138 82 < 0.0001 135 86 < 0.0001 060,02 014< 0.001 030< 0.0001 038< 0.0001
Ig
W584 33 < 0.0001 1523 54 < 0.0001 3463 82 < 0.0001 3809 86 < 0.0001 27 6 0,03 119 14
<
0.001 495 30 < 0.0001 779 38 < 0.0001
Bd 142 33 < 0.01 466 54 0,01 933 82 < 0.001 1047 86 < 0.001 360,08 36 14 0,18 103 30 < 0.01 162 38 < 0.01
Rj 268 33 0,62 851 54 0,5 1845 82 0,65 2098 86 0,44 18 6 0,55 98 14 0,03 377 30 0,01 622 38 < 0.01
Sj 266 33 0,6 833 54 0,6 1793 82 0,82 2034 86 0,61 18 6 0,55 98 14 0,03 376 30 0,01 621 38 < 0.01
C)
Spectral Purity
Comparisons with Group 1 Comparisons with Group 2
Core Inner Edge Outer Edge Surrounding Core Inner Edge Outer Edge Surrounding
V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p V statistic n p
Ig V 033< 0.0001 054< 0.0001 082< 0.0001 086< 0.0001 6 6 0,2 10 14 < 0.01 15 30 < 0.0001 21 38 < 0.0001
Ig P 109 33 < 0.01 310 54 < 0.001 750 82 < 0.0001 711 86 < 0.0001 18 6 0,55 54 14 0,75 145 30 0,04 219 38 0,02
Ig
W595 33 < 0.0001 1540 54 < 0.0001 3482 82 < 0.0001 3819 86 < 0.0001 28 6 0,02 120 14 < 0.001 496 30 < 0.0001 780 38 < 0.0001
Bd 260 33 0,53 793 54 0,85 1740 82 0,99 1918 86 0,99 19 6 0,45 66 14 0,75 228 30 0,7 310 38 0,27
Rj 323 33 0,67 894 54 0,3 1939 82 0,37 2132 86 0,36 21 6 0,27 81 14 0,24 286 30 0,46 391 38 0,99
Sj 144 33 < 0.01 440 54 < 0.01 1024 82 < 0.01 1063 86 < 0.001 18 6 0,55 57 14 0,89 155 30 0,07 229 38 0,02
A one-sample Wilcoxon signed-rank test was used to compare Group 1 and Group 2 values to invasive-species values considered as reference for the comparison. V statistic values, sample sizes (n) of the Group and p values are provided for each comparison performed; df: 1 for all
comparisons. Ig V, violet morph of Impatiens glandulifera; Ig P, pink morph of Impatiens glandulifera; Ig W, violet morph of Impatiens glandulifera; Bd, Buddleja davidii; Rj, Reynoutria japonica; Sj, Spiraea japonica. Values in red indicate significant P values.
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The global analysis (i.e. taking all invasive species together) showed
no significative differences of variance homogeneity within the three
groups (one-way ANOVA: F2,78 = 2.21, p = 0.11). The between-
group comparison showed significant differences of color distance
between Groups 1 and 2 (PERMANOVA: F2,78 = 86.6, p < 0.01)
and between the Invasive group and Group 2 (PERMANOVA:
F2,78 = 13.8, p < 0.01). Thus, both Group 1 and 2 and Group 2 and
the Invasive group appeared clearly distinct to bees. No significant
difference was found between the Invasive group and Group 1
(PERMANOVA: F2,78 = 0.04, p = 0.14), thus suggesting that taken
together, invasive species tended to be chromatically similar to plant
species in Group 1 and different from plant species in Group 2.
As invasive species differ in their color display strategies, we
refined the analysis of color similarity by comparing the color
distance (HU units) between each invasive species/morph and
Groups1and2ofnativespecies.Figure 6 confirms that honey
bees should be able to discriminate all four invasive species from
the native species of Group 2 as the color distances separating
them are well above threshold. However, the situation changes
when the comparison is between invasive species and Group 1 of
native species, which are precisely those surrounding principally
the invasive species considered. Indeed, B. davidii,R. japonica and
S. japonica are likely to be chromatically undistinguishable from
the average color of Group 1 species as their mean color distance,
lower and upper limits of the 95% confidence interval were 0.06,
0.03, 0.08 (B. davidii), 0.04, 0.02, 0.06 (R. japonica) and 0.05, 0.03,
0.07 (S. japonica). The white morph of I. glandulifera exhibited a
similar trend although its values were at the threshold of
discrimination (0,12, 0.10, 0.14) so that it is unclear whether it
can be distinguished from Group 1 species in color terms. On the
contrary, the highly salient violet and pink morphs of I.
glandulifera are clearly distinguishable from Group 1 species in
color terms (Ig V: 0.31, 0.29, 0.34; Ig P: 0.20, 0.18, 0.23), thus
showing that the color-display strategies adopted by the four
invasive species are not homogeneous. While the colors of three
of them (B. davidii,R. japonica and S. japonica)favoured
generalization with respect to surrounding native species, the
highly salient I. glandulifera pink and violet morphs presented
differentiable color displays.
4 Discussion
4.1 Visual signals of flowers as seen
through the bee eye
Communication between plants and pollinators is essential for
an effective pollination process (Proctor and Yeo, 1972;Barth, 1985).
Throughout evolution, flowering plants have developed floral
features aimed at pollinators to advertize feeding resources such as
pollen and nectar. In exchange, flower-constant pollinators such as
bees transport pollen grains to other flowers of the same species, thus
enabling flower fertilization. In this partnership, visual signals play a
fundamental role to guide pollinators to flowers from the distance
(Kevan, 1978;Chittka and Menzel, 1992). Behavioral and
physiological studies on honey bee vision, an insect with a model
status for the analysis of perceptual phenomena (Giurfa and Menzel,
1997), have revealed that besides the fundamental role of color (i.e.
dominant wavelength) displayed by flowers for advertisement, other
parameter such as the achromatic contrast (the contrast of the visual
target against the background evaluated through the L-receptor
channel) and the spectral purity (the amount of a single
wavelength component within a target reflection) are also used for
visual orientation at different ranges. The achromatic contrast
provided by a visual target enables farthest detection, i.e. when the
targets subtend small visual angles between 5 and ca. 15° (Giurfa
et al., 1996b;Giurfa et al., 1997) so that highest achromatic contrasts
provide more visibility at the distance. At closer distances, i.e. at
larger visual angles subtended by the targets, color (wavelength)
information determines the choice of bees based on innate
preferences in the first flights (Giurfa et al., 1995) and then on
experience through the association of color and food reward
(Menzel, 1985). In addition, spectral purity, which is the equivalent
of color saturation, also guides the bees at even closer ranges, during
the close-up recognition process. In this situation bees tend to follow
the increasing gradient of spectral purity from the petal periphery to
A
B
C
FIGURE 5
(A) Chromatic contrast (hexagon Units, HU), (B) Achromatic contrast
(L-receptor contrast with respect to the background) and (C)
Spectral purity (hexagon Units, HU) of Group1 (G.1), Group 2 (G.2)
and the invasive species (Inv.) analyzed according to the sampling
zones, core, inner and outer edges and surrounding zone. Bd,
Buddleja davidii; Sj, Spiraea japonica; Rj, Reynoutria japonica; Ig,
Impatiens glandulifera; IgV, IgW and IgP, violet, white and pink
morphs of Ig. Number in parentheses indicate sample sizes.
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the center of the corolla and the enhanced spectral purity of nectar
guides (Lunau, 1990;Lunau, 1992;Rohde et al., 2013), thus providing
a direct orientation to the hidden location of reward within a flower.
Thus, given the importance of these visual signals for flower
detection and recognition by pollinators, it is relevant to study to
what extent the success of invasive plants relies on them in the
competition with native species for pollinators using insect vision as
an interpretational framework. In this study, we analyzed the color
signals of four successful invasive species in the French Pyrenees
and compared them with those of surrounding native species. Our
analyses were performed from the perspective of honey bee vision
in order to understand the strategies deployed by invasive plants to
compete for pollinators and ensure a higher reproductive success.
Clearly, honey bees are not the only pollinators of these plants, but
they are among the major ones, and other frequent visitors such as
bumble bees have a very similar set of color photoreceptors and a
similar color vision (Peitsch et al., 1992).
Importantly, in this analysis we focused on chromatic and
achromatic cues knowing that flower recognition may rely on
further visual cues such as shape or symmetry (Lehrer et al.,
1995;Giurfa et al., 1996a;Dafni and Kevan, 1997) and on non-
visual cues such as scent (Dobson and Bergstrom, 2000;Friberg
et al., 2014)orflower texture (Kevan and Lane, 1985), among
others. Yet, in the case of bees, scent and spatial details contained in
shape, as well as texture, operate in shorter, close-up ranges when
compared with color cues, i.e. when the approach decision has been
already made, as shown by studies by Karl von Frisch (1967). Thus,
while these cues may divert a bee from inspecting an erroneous
target once it has been chosen, the primary decision of approaching
and choosing such a target is driven by cues such as the achromatic
contrast and the chromatic contrast of a floral target, which were
analyzed in our study.
4.2 The color similarity strategy: the case
of B. davidii, R. japonica and S. japonica
The invasive species B. davidii, R. japonica and S. japonica
shared a common chromatic identity with most native plant species,
which exhibited blue and blue-purple flowers to the human eye
(UV-blue, blue and blue-green to the bee eye; Group 1). These three
invasive species clustered with Group 1 of native species (Figure 3),
thus highlighting commonalities in terms of color properties. They
were clearly different from other native species, which appeared
yellow to the human eye (blue-green and green to the bee eye;
Group 2). Interestingly, perceptual similarity correlated with
adjacency. Group 1 species, which were similar to B. davidii, R.
japonica and S. japonica, were more common in central sampling
zones that constituted the immediate surrounding of an invasive
species spot. On the contrary, Group 2 species, which differed from
the three invasive species, were more frequent at the outermost
zones of the sampling areas. Thus, the three invasive species shared
similarcolorswiththenativespeciesthatconstitutedtheir
immediate surroundings and differed chromatically from distant
native species. This suggests that invasive plants may profit from the
established communication between pollinators and native plants to
succeed in the invaded area, as reported for the invasive Acacia
saligna in South Africa (Gibson et al., 2012). By adopting similar
colors as their surrounding native plants, B. davidii, R. japonica and
S. japonica may benefit from color generalization and thus attract
pollinators from the distance. This hypothesis was further
confirmed by the analysis of chromatic and achromatic contrasts,
and spectral purity. These variables tended to be similar to those of
native species (Table 1), thus indicating that the three invasive
species were not perceptually salient among their surrounding
native competitors. The analysis of color similarity, which
provides a direct assessment of the bees’capacity to discriminate
between different color stimuli, showed that B. davidii, R. japonica
and S. japonica were below the discrimination threshold when
compared to the mean locus of Group 1 species (Figure 6). This
results thus confirms that the color of these three invasive species
could be confused or generalized with respect to that of the native
species immediately surrounding them, a strategy that may increase
their visitation rate and fertilization but also those of surrounding
native species as the clustering of flowers with the same colors in the
same area could attract more pollinators, a phenomenon termed
‘the magnet effect’(Moeller, 2004;Peter and Johnson, 2008;
Cuadra-Valdes et al., 2021).
Although the magnet effect can be advantageous for both the
invasive and the native species depending on their fertility success,
it could lead to more heterospecific (interspecific) pollen deposition,
which could represent a waste of pollen grains (Morales and
Traveset, 2008). This scenario could be detrimental for less
frequent species as they could lose more pollen via the deposit on
FIGURE 6
Color similarity (color distance in hexagon units, HU) between the
invasive species and Group 1 and Group 2 of native species. The
dashed line at 0.1 HU indicates the color discrimination threshold
reported for bees trained under absolute conditioning (Dyer and
Chittka, 2004), which corresponds to the ecological scenario of a
color-constant foraging bee. All invasive species differed in color
from the native species of Group 2. Three invasive species, Buddleia
davidii,Reynoutria japonica and Spiraea japonica, were
undistinguishable from the surrounding species of Group 1 in terms
of color. The white morph of Impatiens glandulifera was separated
from native species of Group 1 by a distance that was at the
threshold of discrimination. The two other morphs of I. glandulifera
(pink and violet) were clearly distinguishable from native species of
Group 1.
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the wrong flowers. Thus, less abundant native species could suffer
fromthepresenceofinvasivespeciesinthearea,giventhe
abundance of the latter in the Pyrenees region.
4.3 The color salience strategy: the case of
the pink and violet morphs of
I. glandulifera
One of the invasive species, Impatiens glandulifera, presented
floral color polymorphism, with white, pink and violet morphs,
which appeared uv-blue/blue to the bee eye (Figure 2). The pink and
the violet morphs did not cluster with the native species of Group 1
and even less with the native species of Group 2 (Figure 3). They
thus differed significantly from all native species in their visual
properties. For instance, they had significantly higher achromatic
contrasts against the background when compared to surrounding
native species of Group 1 (Table 2), which means that they were
more detectable from the distance, at smaller visual angles, in terms
of this achromatic variable, even before bees could perceive the
color of the targets they were aiming at (Giurfa et al., 1996b;Giurfa
et al., 1997). They also had significantly higher chromatic contrast
and spectral purity than surrounding native species of Group 1
(Table 1), which means that their colors were more salient against
the green background and their higher spectral purity rendered
them more attractive for pollinators (Lunau, 1990;Rohde et al.,
2013). Besides, their colors were dissimilar from those of native
species of Group 1 and 2 (Figure 6), thus bestowing a unique, highly
detectable and salient identity.
These characteristics may confer these I. glandulifera morphs
with exceptional advantages in the context of bee pollination
activities, which are governed by associative learning. In fact,
flower constancy, the essential characteristic of bee foraging
(Grant, 1950;Waser, 1986;Chittka et al., 1999) relies on the bees’
capacity to learn and memorize flower features such as the ones
evaluated in our work based on their association with food reward
(nectar or pollen) (Giurfa, 2007). Analyses of foraging activities
using a Pavlovian learning framework have led to successful and
valuable prediction of bee foraging activities (Greggers and Menzel,
1993;Montague et al., 1995). From these perspective, a basic tenet
of Pavlovian associative learning refers to the salience of the stimuli
to be learned and to the intensity of the reward delivered during
learning trials (Rescorla and Wagner, 1972): salient stimuli increase
the learning rate, leading to a faster reaching of a learning plateau.
Similarly, better rewards facilitate learning. Thus, the pink and the
violet morphs of I. glandulifera could eventually outcompete their
surrounding native flowers via highly attractive and salient visual
cues, which could be better learned than those of their native
competitors, ensuring thereby efficient flower constancy.
Additionally, I. glandulifera flowers have a particularly rich
nectar, which is more rewarding than that of any known native
plant in central Europe (Chittka and Schurkens, 2001), thus
fulfilling the reward-intensity criterion required for improved
associative learning.
In addition to nectar, pollen may also act as a reinforcing
resource for bee pollinators (Muth et al., 2016). Quantitative
information for pollen abundance and quality is not available to
the best of our knowledge for the invasive species considered in our
work. Yet, invasive pollen transport by Hymenoptera (honey bees
and bumblebees) in field plots in which I. glandulifera coexisted
with native species was significantly high as bees were found to
carry more pollen from I. glandulifera than from native species
(Lopezaraiza-Mikel et al., 2007). Thus, this invasive species may
reinforce pollinator visits not only via particularly rich nectar but
also via pollen.
Based on these features, the pink and violet morphs of I.
glandulifera are, in principle, well equipped to tempt bee
pollinators away from native flowers, potentially reducing thereby
the fitness of native flora. Indeed, studies on the effects of both
proximity and abundance of I. glandulifera on the reproductive
success of native plant species showed that abundance of the
invasive species led both honey bees and bumble bees to visit
more often the invasive species to the detriment of the native
ones (Cawoy et al., 2012). These arguments should, nevertheless be
considered with caution in the absence of fitness studies focusing on
the native and the invasive plants in the study community and
because visual signals are not the only ones predicting the
reproductive success of insect-pollinated plants.
4.4 The case of the white morph of
I. glandulifera
The white morph of I. glandulifera represents an interesting
case in visual terms as it is neither well detectable against the
background (Table 2) nor well distinguishable from its surrounding
native plants as the color distance separating them is at the
threshold of discrimination (Figure 6). The flowers of this morph
presented significantly lower achromatic contrast and chromatic
contrast against the background and lower spectral purity
(Figure 5). Its flowers appear white to human eyes but not to bees
as they do not reflect evenly along all the visible spectrum of bees, as
shown in the inset of Figure 2A (Kevan et al., 1996); given the lack
of reflection in the UV range, the flowers of this morph appear blue-
green to bees. Less is known about these white morphs in terms of
their natural pollinators. Also, reports on their relative abundance
in different regions are scarce; however, when color morphs of I.
glandulifera were quantified, white morphs co-occurred with the
other morphs, yet being clearly less abundant (Valentine, 1971).
Given their visual characteristics, it is tempting to suggest that white
flowers of I. glandulifera rely on other, non-visual cues (e.g. scent),
to attract pollinators. The lower chromatic distance to surrounding
flowers (Figure 6) may promote approaches to the white flowers by
pollinators foraging on surrounding native species, which would
give them the opportunity to sense these cues and associate them
with the rich nectar present in the white flowers. As our analyses
revolved around honey bee vision, it could be possible that the main
recipients of the white-morph signals are not bees but other animals
Dessart et al. 10.3389/fpls.2024.1393204
Frontiers in Plant Science frontiersin.org12
endowed with a different visual system. The nature of non-visual
advertisement in the white morph of I. glandulifera remains to be
determined and constitutes a fascinating topic for future research.
5 Conclusions
Plant invasion relies not only on the competition for space,
nutrients and sunlight with native species but also on the
competition for local pollinators to enhance reproductive success
and spread. Thus, a fundamental component for understanding the
success of invasive plants is to evaluate their characteristics from the
perspective of the sensory and cognitive abilities of pollinators,
which are the main addressees of their signals. We adopted this
perspective to analyze the case of four successful invasive plants in
the French Pyrenees and evaluated their color signals using the
extensive knowledge gathered on honey bee vision. By recording the
spectral signals of these species as well as those of native species in
the same areas in which the invasive plants are located, we could
estimate the achromatic and chromatic salience of the invasive
species and their color similarity to surrounding native species. In
this way, we were able to distinguish the color advertising strategies
employed by the invasive species and evaluate their contribution to
their invasive success.
We showed that the four invasive species differ in their color
advertising strategy. Three species (R. japonica, S. japonica and B.
davidii) were generally inconspicuous against the background in
achromatic and chromatic terms and could be hardly discriminated
in terms of color from their immedialy surrounding native plants.
These characteristics may promote generalization and potentially
attract visits from a flower constant pollinator foraging on a similar
native species. The remaining species, I. glandulifera, presented three
morphs with different characteristics. The pink and the violet morph
were highly salient in chromatic and achromatic terms against the
background and were very different from their surrounding native
species. These features provide a distinctive identity, which may
facilitate their detection and learning in association with the rich
nectar they provide, thus potentially endowing the plants with
significant advantages in the competition for pollinators. The white
morph, on the contrary, did not present salient visual features, thus
raising the double question of the sensory channels it may use to
advertise its presence and of the natural addressees of its signals.
Our study focused on honey bees as a main pollinator of the
four invasive floral species considered in our work in the Pyrenees
landscape. Yet, in the same environment, many other insect species
visit the invasive species analyzed, thus raising the question of the
generality of our findings with respect to the perceptual capacities of
these alternative pollinators. Answering this question is difficult as
for some insect species that visit these invasive flower species,
photoreceptor types may not have been characterized by means
of electrophysiological recordings, thus precluding perceptual
modeling analyses and building of color spaces for which this
information is mandatory. In the case of other hymenopterans
such as bumble bees, which are also regular visitors of the four
invasive species considered, the spectral sensitivity curves of their
three photoreceptor types show high similarity with that of honey
bees (Peitsch et al., 1992). Modeling analyses on the optimality of
spectral sensitivity curves in Hymenoptera showed that the optimal
color receptors in terms of their capacity to finely code flower colors
invariably display peak sensitivities at wavelengths of 330, 430 and
530 nm (Chittka and Menzel, 1992). These values correspond to
those of l
max
found both in honey bees and bumble bees as well as
in many other hymenopterans for which photoreceptor sensitivities
have been characterized by means of electrophysiological methods.
Thus, the conclusions reported in our work may not differ
substantially in the case of bumble bees and other trichromatic
hymenopterans with similar photoreceptor sensitivities.
While the unveiling of the visual strategies used by invasive
plant species enlightens some crucial aspects of their success, it is,
however, obvious that such success does not rely exclusively on
visual cues but depends on multiple sensory dimensions,
physiological adaptations and reproductive specificities, among
others. It is thus important to stress that other cues [e.g., odors
(Suchet et al., 2011), taste (Bestea et al., 2021)] may be as relevant as
the visual cues analyzed in our study for the process of flower
attraction and recognition and that their analysis should be based
on the perceptual dimensions of the addressees. Overall, by
adopting the perspective of the signal receiver, studies on
biological invasion processes may uncover unknown aspects of
the biology of invasive plants and contribute to the development
of conservation strategies for native plants.
Data availability statement
The datasets presented in this study can be found in online
repositories. The names of the repository/repositories and accession
number(s) can be found below: https://github.com/martindessart/
Invasive_plants_through_bee-eye_Pyrenees.
Author contributions
MD: Formal analysis, Methodology, Writing –review & editing.
JA: Formal analysis, Methodology, Writing –review & editing. ET:
Conceptualization, Methodology, Writing –review & editing. SG:
Conceptualization, Funding acquisition, Supervision, Writing –
review & editing. MG: Conceptualization, Funding acquisition,
Supervision, Writing –original draft.
Funding
The author(s) declare that financial support was received for the
research, authorship, and/or publication of this article.
Acknowledgments
Funding was provided by the “Région Occitanie - Appel à
projets Recherche et Société(s) 2019”and by the Maison des
Dessart et al. 10.3389/fpls.2024.1393204
Frontiers in Plant Science frontiersin.org13
Sciences de l'Homme et de la Société de Toulouse (MSH-T) APEX
2020. This work is endorsed by the CNRS/INEE Zone Atelier
Pyrénées Garonne (ZA PYGAR). The Zones Ateliers network
(RZA) is recognized by ALLENVI as an ESFRI eLTER (European
Long-Term Ecological Research) “Integrated European Long-Term
Ecosystem, Critical Zone & Socio-Ecological System Research
Infrastructure”. We also thank the CNRS, the University Jean
Jaures Toulouse II and the University Paul Sabatier Toulouse III
for support. M. Giurfa thanks in addition the Institut Universitaire
de France for continuous support.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
The author(s) declared that they were an editorial board
member of Frontiers, at the time of submission. This had no
impact on the peer review process and the final decision.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fpls.2024.1393204/
full#supplementary-material
SUPPLEMENTARY TABLE 1
Relative abundance of invasive flowers. Patches labelled from A to L represent
the 12 sampling sites. ‘Core’,‘inner edge’,‘outer edge’and ‘surrounding’refer to
areas of each patch for sampling (see Figure 1J, main text). Numbers indicate the
percentage of relative abundance measured in the field. See main text for details.
SUPPLEMENTARY TABLE 2
Flower and leave reflectance spectra included in our analyses. Reflectance
spectra were obtained from 50 native species (n = 333 spectra; 1 spectrum
corresponding to 1 flower part) and from the 4 invasive species mentioned
above (n = 102 spectra), all collected in the field (left column, “measured in the
field”). The FRED database (http://www.reflectance.co.uk/) allowed us to
include 16 additional native species (n = 34 spectra) to complement our
measurements (middle column, “measured in the field”). These species were
present in the field and were counted for abundancy measurements but were
inaccessible for reflectance measurements. The same database was used to
include complementary measurements for 32 native species (n = 74 spectra)
that were also sampled in the field. Overall, our analyses included 543 spectra
(435 from thefield and 108 from the FRED data) from70 plant species, including
the 4 invasive species (bottom of left column), which were the focus of our
study, and 66 native species (18 exclusively from the field, highlighted in green,
16 exclusively from the FRED data base, highlighted in yellow) and 32 both from
the field and the FREDdata base; not highlighted). The spectralreflectance from
leaves of 15 species (n = 25 spectra) was also measured to characterize the
green foliage background (right column, “leave reflectance spectra”).
SUPPLEMENTARY TABLE 3
Chromatic contrast, achromatic contrast and spectral purity dataset. ‘Group’
refers to the three categories used for analyses: ‘Invasive’, which indicates an
invasive species, ‘Group 1’and ‘Group 2’, which refer to the two groups of
invasive plants defined through clustering analysis (see Figure 3, main text).
The three morphs of I. glandulifera (P = pink, V = violet and W = white) are
indicated in separate lines.
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