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Competition for pollinators and intracommunal spectral dissimilarity of flowers

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Competition for pollinators occurs when in a community of flowering plants several simultaneously flowering plant species depend on the same pollinator. Competition for pollinators increases interspecific pollen transfer rates, thereby reducing the number of viable offspring. In order to decrease interspecific pollen transfer, plant species can distinguish themselves from competitors by having a divergent phenotype. Floral colour is an important signalling cue to attract potential pollinators and thus a major aspect of the flower phenotype. In this study we analyse the amount of spectral dissimilarity of flowers among pollinator-competing plants in a Dutch nature reserve. We expected pollinator-competing plants to exhibit more spectral dissimilarity than non-competing plants. Using flower-visitation data of two years we determined the amount of competition for pollinators by different plant species. Plant species that were visited by the same pollinator were considered specialist and competing for that pollinator, whereas plant species visited by a broad array of pollinators were considered non-competing generalists. We used principal component analysis to quantify floral reflectance and we found evidence for enhanced spectral dissimilarity among plant species within specialist pollinator guilds (i.e. groups of plant species competing for the same pollinator). This is the first study that examines intracommunal dissimilarity in floral reflectance with a focus on the pollination system. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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RESEARCH PAPER
Competition for pollinators and intra-communal spectral
dissimilarity of flowers
C. J. van der Kooi
1,2
, I. Pen
3
, M. Staal
1
, D. G. Stavenga
2
& J. T. M. Elzenga
1
1 Plant Physiology, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
2 Computational Physics, Zernike Institute for Advanced Materials, University of Groningen, Groningen, The Netherlands
3 Theoretical Biology, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
Keywords
Biotic interactions; flower colouration; plant
pollinator signalling; principal components
analysis; reproductive character displacement.
Correspondence
J. T. M. Elzenga, Plant Physiology, Centre for
Ecological and Evolutionary Studies, University
of Groningen, Nijenborgh 7, NL-9747 AG
Groningen, The Netherlands.
E-mail: j.t.m.elzenga@rug.nl
Editor
A. Dafni
Received: 21 December 2014; Accepted: 3
March 2015
doi:10.1111/plb.12328
ABSTRACT
Competition for pollinators occurs when, in a community of flowering plants, several
simultaneously flowering plant species depend on the same pollinator. Competition
for pollinators increases interspecific pollen transfer rates, thereby reducing the num-
ber of viable offspring. In order to decrease interspecific pollen transfer, plant species
can distinguish themselves from competitors by having a divergent phenotype. Floral
colour is an important signalling cue to attract potential pollinators and thus a major
aspect of the flower phenotype. In this study, we analysed the amount of spectral dis-
similarity of flowers among pollinator-competing plants in a Dutch nature reserve.
We expected pollinator-competing plants to exhibit more spectral dissimilarity than
non-competing plants. Using flower visitation data of 2 years, we determined the
amount of competition for pollinators by different plant species. Plant species that
were visited by the same pollinator were considered specialist and competing for that
pollinator, whereas plant species visited by a broad array of pollinators were consid-
ered non-competing generalists. We used principal components analysis to quantify
floral reflectance, and found evidence for enhanced spectral dissimilarity among plant
species within specialist pollinator guilds (i.e. groups of plant species competing for
the same pollinator). This is the first study that examined intra-communal dissimilar-
ity in floral reflectance with a focus on the pollination system.
INTRODUCTION
Community structures are shaped by many types of biotic
interactions, e.g. plantherbivore, plantpathogen and plant
pollinator interactions (Gumbert et al. 1999; Sargent & Ackerly
2008; McEwen & Vamosi 2010). Plantpollinator interactions
are essential for outcrossing in many flowering plant species in
order to set seed. Simultaneously, flowering plant species that
strongly depend on the same shared pollinator are likely to
experience competition for that pollinator. Neighbouring plant
species that compete for pollinators will not only suffer from a
reduction in number of pollinator visits, but will also enhance
interspecific pollen transfer, which often reduces the amount of
viable offspring (reviewed in Ashman & Arceo-G
omez 2013).
Competition for pollinators might therefore influence the com-
munity assembly.
Flowering plants can avoid interspecific pollen transfer by
changing their flowering period, but if this period is relatively
fixed (e.g. by environmental factors, such as light, water and
nutrient availability; see Pleasants 1980), interspecific pollen
transfer can be prevented through phenotypic differentiation
from simultaneously flowering competitors (Heinrich 1975;
Caruso 2001). The latter process is often referred to as charac-
ter displacement (Wilson & Brown 1953; Heithaus 1974; Plea-
sants 1980; Armbruster et al. 1994; Muchhala & Potts 2007).
Character displacement is a change in appearance, effectively
leading to a greater distinction between plants that flower
simultaneously and share pollinators. In order to achieve char-
acter displacement, various floral features can be changed, e.g.
corolla length (Armbruster et al. 1994; Eaton et al. 2012), cor-
olla width (Caruso 2000), inflorescence height (Waddington
1979), nectar production (Eaton et al. 2012) and pollen place-
ment on the pollinator (Brown & Kodric-Brown 1979; Armbr-
uster et al. 1994; Muchhala & Potts 2007). In addition to these
morphological traits, floral colour is an important feature for
pollinator attraction (e.g. Kevan & Baker 1983; Barth 1991;
Schiestl & Johnson 2013; Shrestha et al. 2013; Renoult et al.
2014).
An efficient way of character displacement is to increase flo-
ral colour contrast (i.e. to increase dissimilar spectral proper-
ties) between simultaneously flowering plant species (Levin
1985; Dyer & Chittka 2004; McEwen & Vamosi 2010; de Jager
et al. 2011; Muchhala et al. 2014). In community-wide studies,
reproductive character displacement by means of divergent
floral reflectance has been relatively little studied (but see
McEwen & Vamosi 2010; de Jager et al. 2011; Eaton et al.
2012; Muchhala et al. 2014). An elegant study on a subalpine
plant community from McEwen & Vamosi (2010) reported
significant spectral differences among co-flowering plant spe-
cies. Presumably this represents an example of character dis-
placement, but unfortunately actual flower visitations by
pollinators in this community were not recorded (as is often
Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands 1
Plant Biology ISSN 1435-8603
the case in studies on character displacement; see Waser
1983).
Plantpollinator interactions can be either specialised, i.e.
when a plant species is pollinated by a single pollinator species,
or generalised, i.e. when a species is serviced by a broad range
of pollinators (reviewed in Johnson & Steiner 2000; Ollerton
et al. 2007). Compared to generalists, specialist plants, which
depend strongly on a specific pollinator, are subjected to
increased selection pressure for strong floral signalling (Heit-
haus 1974). Consequently, spectral dissimilarity is expected to
be higher between specialists than between generalists (Waser
& Ollerton 2006).
In this study we determined the spectral dissimilarity of
flowers among specialists relative to generalists. We used
detailed insect visitation data collected in the Dutch nature
reserve Drentsche Aa (Hoffmann 2005). We grouped plant spe-
cies into either the generalist or a specialist guild based on the
width of the range of pollinator species that visits them. We
expected that in plant species that heavily depended on only a
few pollinator species, competition for pollination would be
stronger than between generalist species, and that therefore
flowers of specialist plant species would exhibit stronger spec-
tral differences. Using principal components analysis (PCA),
we found that the spectral dissimilarities of flowers within each
specialist guild were indeed higher than those within the gener-
alist guild. This is the first study that documents how character
displacement by means of spectral characteristics of flowers
might be related to the specialisation of plant species to pollin-
ators.
MATERIAL AND METHODS
Flower visitation observations
Flower and inflorescence visitation data were obtained from a
comprehensive database collected in 2000 and 2001 in the
Drentsche Aa (Hoffmann 2005). This nature reserve is charac-
terised by homogeneous, open grasslands that are separated by
rows of trees. The Drentsche Aa is rich in flowering plants,
including several rare plant species such as orchids (Grootjans
et al. 2002). Observations of insects on flowering plants were
done from May until October in 2000 and from May until
August in 2001, respectively. In total, the database comprises
observations of over 38,000 individual insects visiting more
than 1 million flowers of 88 different plant species (for details,
see Hoffmann 2005). We pooled insect visitation data per plant
species. To correct for rare flower morphs and species with
reproductive systems that do not rely on pollinators per se (i.e.
self-fertilisation or apomixis), we included only plant species
with a minimum of 20 individual insect visits (following Hoff-
mann 2005). In addition, we combined various Diptera species
to the genus level since pollination is often achieved by groups
of pollinator species (reviewed in Fenster et al. 2004). We
pooled only species with similar ecologies and avoided pooling
of species with different spectral sensitivities (following Vogt
1989).
To determine the importance of pollinators per plant species
rather than per individual plant, we calculated the relative visi-
tor numbers for all plant species. In the database, the vast
majority of insects visiting flowers were identified to the species
level, but for some visiting insects the species or genus could
not be determined (Hoffmann 2005). Therefore, to avoid a bias
in our analysis, we excluded plant species with more than 10%
unknown visitors. The observations on Bombus terrestris
include the less abundant B. lucorum because these bumblebee
species cannot be distinguished in the field (following Hoff-
mann 2005). Due to the large number of observations in the
database it was impossible to determine whether all flower visi-
tors in our study area are indeed pollinators. However, the
effects of e.g. occasional visitation or pollen theft by insects will
be negligible given the large number of visits recorded in the
database. Most importantly, all insect species or genera that we
considered as ‘specialist pollinators’ were documented else-
where to indeed be plant pollinators (Barth 1991; D’Arcy-Burt
& Blackshaw 1991; Goldblatt et al. 2005; Clement et al. 2007;
Ssymank et al. 2008; Garibaldi et al. 2013). We therefore con-
sidered all flower-visiting insects as pollinators.
Specialists and generalists
The degree of specialisation of a plant species to a pollinator
strongly depends on its habitat (reviewed in Richardson et al.
2000; Vazques & Aizen 2006). Preliminary analysis of the rela-
tive visitor numbers in our study area showed a distinct separa-
tion of generalists from specialists at ca. 40% visits (Figure S1).
This visit level has no fundamental justification but can be sub-
stantiated. A lower threshold yielded plant species that were
simultaneously ‘specialist’ for multiple insect guilds. For exam-
ple, some plant species were specialist for two insect guilds,
each guild accounting for 30% of the relative visitation num-
ber. Using the 40% criterion, the remaining visitations (maxi-
mum 60%) always consisted of many different, non-related
insect species. We thus considered plant species visited at least
40% by one insect genus as specialist for that genus (for further
details regarding this criterion, see the Discussion). Two polli-
nator guilds comprised only one plant species (of which one
was specialist for the honeybee Apis mellifera). We excluded
these guilds because it is impossible to compare plant species
within a guild with only one plant species. After applying our
criteria to the plant species in the Drentsche Aa dataset, 39
plant species remained, which were subsequently assigned to
either the generalist guild or to one of the six specialist guilds.
The remaining 39 plants had relatively long flowering periods,
and based on the insect observations, we found that the overlap
of the flowering time for plants within the same guild was at
least 1 month.
Flower species and reflectance measurements
Flower samples were either collected locally from meadows
around Groningen, the Netherlands, or grown from seed
(obtained from Cruydt-Hoeck, Nijeberkoop, the Netherlands).
Reflectance spectra of the flowers were measured with a bifur-
cated fibre-optic probe (Avantes FCR-7UV200; Avantes, Eer-
beek, the Netherlands) using an AvaSpec 2048-2 CCD detector
array spectrometer. The light source was a halogen-deuterium
lamp (AvaLight-D(H)-S); a white diffuse tile (WS-2; Avantes)
was used as a reference. We measured several reflectance spec-
tra from the dominant coloured petal areas (following McEwen
& Vamosi 2010). In these areas, the shape of the spectra
was virtually constant and only the amplitude varied slightly.
We obtained reflectance spectra of additional flowering plant
Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands2
Competition and spectral dissimilarlity of flowers van der Kooi, Pen, Staal, Stavenga & Elzenga
species from the online floral database www.reflectance.co.uk
(Arnold et al. 2010).
To correct for brightness, we subtracted, for each species, the
mean percentage reflectance, and thus specifically compared
spectral quality differences (Cuthill et al. 1999; McEwen & Va-
mosi 2010). We analysed the wavelength range from 300 to
600 nm (which includes the ultraviolet light wavelength range
and excludes the red wavelength range) as insects that are sen-
sitive in the red part of the spectrum (e.g. beetles and butter-
flies; Briscoe & Chittka 2001) only very rarely visited our plant
species (Table S1).
Ideally, floral reflectance is analysed by incorporating polli-
nator spectral sensitivity (Peitsch et al. 1992; Lunau et al. 2011;
Dyer et al. 2012; Shrestha et al. 2013; Burd et al. 2014). How-
ever, for many important flower-visiting insects in our study
area (notably Diptera), we currently have insufficient reliable
information to model colour vision for these species (Lunau
2014). We therefore strictly aim to describe the spectral proper-
ties of co-occurring plants, rather than floral colour as per-
ceived by pollinators.
Statistical analyses
Statistical analyses were conducted using R Statistical Software
(R Core Team 2012). We calculated the spectral differences
using two complementary methods. The spectral differences
were calculated based on the raw spectra and by transforming
the spectra using PCA. PCA allowed us to easily visualise the
spectral differences, whereas calculations based on the raw
spectra provided more statistical power. The PCA was per-
formed using the 39 standardised reflectance spectra with bins
of 1 nm. The principal components 1 (PC1) and 2 (PC2)
together largely explained the variance (see below), in accor-
dance with similar studies (e.g. Cuthill et al. 1999; Grill & Rush
2000; Renoult et al. 2013; Sun et al. 2014). To visualise the dif-
ferences in spectra between guilds, we constructed a PCA scat-
terplot comprising all plant species using the PC1 and PC2
values of each plant species as x- and y-coordinates, respec-
tively. To quantify the spectral contrast, we calculated the
Euclidean pair-wise distances between the plant species within
each guild, resulting in a mean pair-wise distance (MPD) value
per guild. To account for the total variance, and not only the
92% explained by PC1 and PC2, the MPDs were calculated
using all 39 principal components. The MPD was also deter-
mined directly from the raw spectra. For all flowers within a
guild we calculated the absolute difference between the
reflectance values for each nanometre, and then we averaged
the obtained values over the examined wavelength range
(300600 nm). The guild’s MPD was then calculated by averag-
ing the obtained spectral differences.
The MPDs derived from both the PCA and the raw spectra
were used in two different randomisation tests. We calculated
the difference between the average MPD of the specialist guilds
and the MPD of the generalist guild, denoted by DMPD. Based
on our hypothesis, we expected DMPD to be positive (i.e. more
spectral dissimilarity exists between the flowers that belong to a
group of specialist plants and the flowers of generalist plants)
and therefore we performed a one-tailed test. To test its signifi-
cance, we generated 1,000,000 ‘random’ plant communities by
randomly assigning the 39 plant species to one of the six spe-
cialist guilds or the generalist guild, keeping the sample size for
each guild identical to that in the original plant community
(see Table 1). For each of the random communities we then
calculated and stored DMPD, thus generating a null distribu-
tion of DMPD values. Finally, we tested if the observed spectral
dissimilarity was larger than that expected by chance, by
inspecting the quantile of the observed DMPD value in the null
distribution (V
azques & Aizen 2006).
RESULTS
Specialists and generalists
Throughout our study period, 39 simultaneously flowering
plant species (from 14 angiosperm families) were frequently
visited by insects (Table S1). We excluded 49 plant species that
did not occur frequently and were thus only rarely visited by
insects, or because they were visited mostly by unidentified
insect species (Table S2). A total of 17 frequently occurring
plant species were visited by many different insects, and we
subsequently considered these plant species as generalist
(Table 1; Figure S1). Despite its apomictic mode of reproduc-
tion, Taraxacum officinale was included in the generalist guild
because it affects the community’s colour composition due to
its frequent occurrence and high number of pollinator visita-
tions in our study area (Table S1). A total of 22 frequently
occurring plant species were, at least 40%, visited by one polli-
nator, and we accordingly assigned these plant species to one
of the six specialist pollinator guilds (Table 1; Figure S1). The
degree of specialisation of specialist plant species to an insect
Table 1. Assignment of generalist and specialist plant species to different pollinator guilds and the degree of specialisation (in parentheses).
guild plant species
generalists Achillea millefolia;Aegopodium podagraria;Angelica sylvestris;Chamerion angustifolium;Cirsium arvense;Cirsium palustre;
Epilobium hirsutum;Eupatorium cannabinum;Glechoma hederacea;Jasione montana;Lamium album;Lychnis flos-cuculi;Lycopus
europaeus;Lythrum salicaria;Mentha aquatica;Rorippa amphibia;Taraxacum officinale
Bibio Heracleum sphondylium (47); Hieracium pilosella (45)
Musca Filipendula ulmaria (47); Hieracium aurantiacum (59)
Eristalis Nasturtium officinale (47); Sonchus arvensis (62); Succisa pratensis (69); Valeriana officinalis (46)
Rhingia campestris Ajuga reptans (86); Phyteuma spicatum (60); Silene dioica (59)
Bombus pascuorum Galeopsis tetrahit (52); Linaria vulgaris (43); Lotus corniculatus (59); Stachys palustris (50); Symphytum officinale (62); Trifolium
pratense (55); Trifolium repens (51); Vicia cracca (93); Vicia sativa (82)
Bombus terrestris Lupinus polyphyllus (86); Rhinanthus angustifolius (68)
Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands 3
van der Kooi, Pen, Staal, Stavenga & Elzenga Competition and spectral dissimilarlity of flowers
guild ranged from 43% (moderately specialised) to 93%
(highly specialised).
Floral reflectance analysis
Flowers that appear white to the human eye are always low in
ultraviolet reflectance (Kevan et al. 1996), but spectra with
peaks in the medium or long wavelength range can co-occur
with high reflectance in the ultraviolet wavelength range
(depending on the nature of the pigment; Grotewold 2006; Lee
2007; van der Kooi et al. 2014, 2015). The PCA of flowers in
our study area yielded two principal components, PC1 and
PC2, which accounted for 92.4% of the total variation in the
reflectance spectra (53.7% and 38.7%, respectively). The two
principal components strongly depended on the different
wavelength ranges of the reflectance spectra (Fig. 2a). Flowers
with reflectance peaks in the ultraviolet or short wavelength
range yielded a high PC1 score, and had low, medium or high
PC2 scores. Flowers with high reflectance in the medium and
long wavelength range yielded low PC1 scores and high and
low PC2 scores, respectively. A plot of PC2 versus PC1 thus
formed a reflectance scatterplot, with different floral reflectance
spectra clustering in different sections of the scatterplot
(Fig. 2b).
To quantify the spectral differences, we calculated the MPD
between plant species belonging to the same pollinator guild.
We calculated the MPD using both the PCA-transformed spec-
tra and the raw spectra (see Figure S2). This yielded very simi-
lar results. The MPDs within all six specialist guilds were larger
than MPDs within the generalist guild (Fig. 3a), which is sig-
nificant according to a binomial test (P=0.017). Furthermore,
the average MPD between the specialist guilds and the general-
ist guild was 7.1, which yielded a P-value of 0.050 according to
our randomisation test (Fig. 3b). Similarly, the results based on
the raw spectra were significant, with a P-value of 0.052.
DISCUSSION
The present investigation of the spectral properties of co-flow-
ering plants within pollinator guilds lends support to the
hypothesis that flower communities are, at least in part, struc-
tured by plantpollinator interactions. The results obtained for
lowland flowers are in fair agreement with earlier findings in a
subalpine community (McEwen & Vamosi 2010) and also with
a recent study on hummingbird-pollinated Solanaceae (Much-
hala et al. 2014).
We could distinguish several pollinator guilds in our study
area. Some plants were pollinated by various insect species,
others mainly by insects of one of six specialist pollinator
guilds (Table 1). Three of six specialist guilds are defined to the
insect genus level, meaning that within these specialist guilds,
plant species were visited by different species from that genus.
Nevertheless, a plant species visited by various insect species of
one insect genus with similar ecologies is more specialist than a
plant species visited by only a few insect species from distinct
lineages with different ecologies (G
omez & Zamora 2006). The
pollinator guilds observed in our study can thus be regarded as
functional pollinator groups.
Fig. 1. Flower reflectance spectra of four exemplar plant species: Lythrum
salicaria (1), Jasione montana (2), Heracleum sphondylium (3) and Sonchus
arvensis (4).
(a)
(b)
Fig. 2. (a) Coefficients of the first two principal components of the PCA per-
formed on the spectra of the species listed in Table 1. PC1 represents the rel-
ative amount of short to long wavelength reflectance. PC2 represents the
relative amount of medium wavelength reflectance to both short (<400 nm)
and long (>500 nm) wavelength reflectance. (b) Flower reflectance scatter-
plot based on the PC1 and PC2 values of our 39 plant species. Similarly as
perceived by the human eye, different floral reflectance spectra cluster in
different sectors of the scatterplot, as indicated by ellipses. The positions of
the four exemplar plant species with different spectra (see Fig. 1) are indi-
cated with numbers (14).
Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands4
Competition and spectral dissimilarlity of flowers van der Kooi, Pen, Staal, Stavenga & Elzenga
The generalist flowers in our study are visited by a large
array of insect species (Table S1). These generalists are not
restricted to a specific region in the reflectance scatterplot,
indicating that the generalist guild comprises plant species
with different spectral properties (Fig. 2b). Spectral dissimilar-
ity among generalists seems to contradict our hypothesis that
generalist plants are more similar in spectral reflectance than
specialists. However, the MPD value of the generalists is smal-
ler than in any of the specialist groups (Fig. 3), meaning that
within the generalist guild the spectral properties are more
similar than among specialists. Furthermore, the derived spec-
tral dissimilarities are larger than expected for a random
assembly. The same spectral dissimilarities were obtained
based on distance between the raw spectra, and thus the trans-
formation of spectra into principal components did not sig-
nificantly alter our results. Interestingly, for generalists,
spectral dissimilarity might not be a prerequisite for survival
in the community in fact, the opposite might be true
because similar reflectance spectra might increase visitation
from generalist pollinators (e.g. Schiestl & Johnson 2013).
Furthermore, generalist plants may have converged in floral
colouration, yet can be specialist in e.g. floral morphology
(Eaton et al. 2012; Low et al. 2015).
The number of potential pollinators in a community is
reduced if the morphology of the plant requires a specific mor-
phological fit to the pollinator (Cresswell 1998; Schemske &
Bradshaw 1999; G
omez & Zamora 2006; Mur
ua & Esp
ındola
2015). In other words, a ‘complex’ morphology might render a
plant specialist. Complex morphologies are often associated
with specific angiosperm families, e.g. in Fabaceae and Lamia-
ceae, where anthers and stigmas are not as easily accessible as
in members of the Apiaceae and Asteraceae. In addition, occur-
rence of floral pigments, and hence floral reflectance, might be
conserved within families (Levin 1985; Grotewold 2006). Floral
reflectance and morphology might thus potentially be linked
through ancestry. However, generalist plant species are located
throughout the reflectance scatterplot, and both the generalist
and specialist guilds include multiple plant families, indicating
that phylogenetic constraints do not exist (Fig. 2b). This is cor-
roborated by many studies that report phylogenetic effects on
floral reflectance are negligible in large communities (e.g.
Schemske & Bradshaw 1999; Sargent & Otto 2006; McEwen &
Vamosi 2010; Eaton et al. 2012; Muchhala et al. 2014).
We note that a theoretical framework for the effects of
plantpollinator relations on plant community composition is
not fully developed. A theoretical framework might provide a
more solid basis for the criteria by which plant species can be
grouped into generalist and specialist guilds. In the present
study, the grouping of plant species proved to be rather
straightforward, since plants were either visited by numerous
different insect species or predominantly by a single group
together with a limited number of other species. However, the
chosen minimal percentage of at least 40% visits covered by the
principal pollinator is somewhat arbitrary and has no funda-
mental justification.
We conclude that spectral dissimilarity is most likely a prere-
quisite for pollinator-competing plants. When flowers of dif-
ferent species within a community have dissimilar reflectance
spectra, pollinators are less likely to switch between species
(Dyer & Chittka 2004), and thereby interspecific pollen transfer
is reduced. Even though our results are not highly significant,
pollinators are documented as capable of detecting small spec-
tral differences (e.g. Papiorek et al. 2013; Renoult et al. 2013).
Clearly, for specialists, spectral dissimilarity is an efficient sig-
nalling cue, as it can be perceived by insects from far longer
distances than is the case with morphological traits such as cor-
olla length (Schemske 1976). Interestingly, a study performed
on a South African flower community showed that flowers
with similar spectral properties carry a fitness cost, yet co-flow-
ering plant species had rather similar spectral characteristics
(de Jager et al. 2011). The latter might be explained by a high
prevalence of a particular type of pollinator or by the species
composition in that specific community, as it largely consisted
of plant species that belong to the same genus. This might indi-
cate that the specific set of conditions present in the Drentsche
Aa nature reserve (e.g. plant and pollinator species composi-
tion) create a level of competition for pollinators in which
character displacement can be observed.
The dissimilarity in spectral properties between co-flowering
plants in specialised pollinator guilds that we encountered
in our study area might also occur in other communities.
(a)
(b)
Fig. 3. Observed mean pair-wise distance (MPD) between the PCA-trans-
formed floral reflectance spectra within each pollinator guild. (a) All plant
species within specialist guilds have more spectral contrast than generalist
plants. The MPDs between plant species within each guild were calculated
using the Euclidean distance based on the 39 principal components describ-
ing the spectral properties of the flowers. (b) Distribution of specialistgener-
alist spectral differences, calculated over the 1,000,000 communities with
randomly assigned guilds. The observed spectral contrast (vertical line) is
higher than the spectral contrast expected by chance.
Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands 5
van der Kooi, Pen, Staal, Stavenga & Elzenga Competition and spectral dissimilarlity of flowers
Comparisons with other habitats are particularly relevant, as
plant reproductive strategies often differ between habitats (Lin-
hart & Feinsinger 1980; Waser & Ollerton 2006). In addition,
since both plant and insect diversity often depend on the envi-
ronment, the selective pressures on floral traits, such as spectral
reflectance, might be different between environments (Gum-
bert et al. 1999; L
azaro et al. 2015). Future studies on plant
pollinator interactions will help explain the differences in plant
reproductive strategies between populations.
ACKNOWLEDGEMENTS
The authors thank Frank Hoffman for kindly providing the
Drentsche Aa dataset and Adrian G. Dyer, Aidan Vey and three
referees for their suggestions for improvements. We also thank
Ger Telkamp, Hein Leertouwer and Jacob Hogendorf for assis-
tance in acquiring samples of the plant species and their practi-
cal support.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
Figure S1. Relative pollinator visitation of plants used in this
study.
Figure S2. Raw reflectance spectra for the plants within each
pollinator guild.
Table S1. Total insect visitation counts (obtained from
Hoffmann 2005) of the 39 plant species investigated in this
study.
Table S2. Overview of plant species that were excluded from
the analysis and the reason for exclusion.
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Plant Biology ©2015 German Botanical Society and The Royal Botanical Society of the Netherlands 7
van der Kooi, Pen, Staal, Stavenga & Elzenga Competition and spectral dissimilarlity of flowers
... Cleistogamy is a dimorphic flowering system that implies the production of both permanently closed small flowers (cleistogamous, CL), which are obligately selfed, and open, insect-pollinated flowers (chasmogamous, CH), potentially capable of outcrossing (Uphof 1938;Maheshwari 1962;Lord 1981;Culley & Klooster 2007;Stojanova et al. 2020). Cleistogamy is widespread across angiosperms, present in at least 50 families, evolving multiple times in their evolutionary history, suggesting this system may confer advantages to the fitness of individuals (Culley & Klooster 2007). ...
... Thus, cleistogamy expression in C. broussonetii would be mainly prompted by abiotic factors such as degraded microenvironmental conditions, as documented elsewhere for other CL species (e.g. Uphof 1938;Stojanova et al. 2020;Furukawa et al. 2020;Sternberger et al. 2020). However, despite the lack of influence of the pollination environment in the expression of cleistogamy in our study sites, we did observe differences in the relative reproductive success between CH and CL flowers in burned sites, where CH flowers set more seeds than CL flowers in both low and high fire frequency conditions. ...
... In contrast, seed set was similar between CH and CL flowers in unburned sites, which may indicate that the pollinator effect on CH flowers in these more diverse communities may have been diluted among the higher number of CH flowers offered by C. broussonetii and also by the increased flower offer by other species, thereby increasing interspecific competition for pollinators (e.g. van der Kooi et al. 2016). These aspects of increased floral offer and competition in unburned sites may have also been responsible for the lower seed mass of CH flowers. ...
Article
Full-text available
Increased fire frequency usually erodes microenvironmental conditions causing a drastic limitation of edaphic resources. Thus, the production of permanently closed-small flowers (cleistogamous, CL) should increase in sites with high fire frequency as it implies a less-expensive reproductive-assurance strategy. However, because open, insect-pollinated flowers (chasmogamous, CH) have the potential capability to outcross via pollinators, CH progeny produced at any site should outperform selfed CL progeny. We evaluate the effect of fire frequency on the relative production of CL/CH flowers and fruits, and their seed-set, along with several progeny performance parameters in Cologania broussonetii (Fabaceae), a resprouting herb with dimorphic cleistogamy native to the Chaco Serrano. Fire frequency increased cleistogamy expression, reaching extreme levels in high fire frequency sites. Seed-set was similarly high for both CH and CL flowers in the unburned condition, while in burned sites the few developed CH flowers set more seeds than CL flowers. However, progeny performance was similar between CH and CL progeny at each and across all fire frequency conditions. Cleistogamy expression in C. broussonetii is maximized in abiotically degraded frequently burned habitats, although the selfed CL progeny is as successful as potentially outcrossed CH one. Fire frequency may decreased floral size and abundance selecting autogamous reproduction, which restricts not only the genetic potential of plant populations but also the resources offered to pollinators. At the community level, increased cleistogamy expression may potentially have negative implications for non-cleistogamous, more outcrossing species surviving in frequently burned environments.
... It has been hypothesized that co-occurring species with overlapping flowering tend to be more divergent in floral colour than might be expected by chance as a way to ensure floral constancy and avoid competition for pollinators (Botes et al., 2008;Caruso, 2000;Chittka et al., 1999;Dyer & Chittka, 2004;Spaethe et al., 2001;van der Kooi et al., 2016). The few studies addressing this issue have provided some evidence in this sense (McEwen & Vamosi, 2010;Shrestha et al., 2014). ...
... Chromatic contrast was the most important colour parameter associated with nectar concentration, this association accounting for 7.3% of reward variability. Chromatic contrast has previously been proven to play a significant role at the plant community level and it has been suggested that plant species may maximize chromatic contrast as a way to distinguish themselves from their co-flowering neighbours (McEwen & Vamosi, 2010;van der Kooi et al., 2016). Given the importance of chromatic contrast for visual detection by bees (Dyer et al., 2007), in bee-pollinated species with overlapping flowering periods, an association between chromatic contrast and reward could be a way to promote flower constancy and to prevent heterospecific pollen deposition. ...
Article
The high variability observed in floral traits has been interpreted as resulting from the adaptation of plants to pollinators, as the latter present innate preferences for specific floral traits and impose selection over them. However, some pollinators such as bees can learn to associate floral signals with rewards, thus increasing floral constancy on more rewarding flowers. The integration of all these rewards and cues is markedly important at community level, where co-flowering species compete for pollinators. In order to verify the honesty of the above-mentioned signals, we examined the association between floral visual signals (size, colour, symmetry and floral display) and rewards (pollen and nectar) for 98 species in a Mediterranean community. The associations between floral traits were analysed considering the phylogenetic relationship between the different species. Flower colour, size, pollen volume or amount of sucrose exhibited no phylogenetic signal, which suggests an adaptive evolution in response to different conditions in the pollinator community. Flower size was seen to constitute the most honest signal for pollinators, as this was significantly associated with quantities of pollen and nectar. In contrast, nectar concentration was observed to be positively associated with chromatic contrast. We detected no relationship between flower shape and rewards, on the one hand, nor between flower display and rewards, on the other. Our study unequivocally demonstrates the correlation between rewards and the visual signals perceived by bees, the most effective pollinators in the Mediterranean Basin. In the community studied, bees employed flower size at longer distances and chromatic contrast at shorter distances to predict rewards. The limited number of studies existing in this sense indicates that this kind of association appears to be community specific. A free Plain Language Summary can be found within the Supporting Information of this article.
... Achillea millefolium L. is an ancient herbaceous medicinal plant belonging to the Asteraceae family, commonly known as Yarrow, thousand-leaf, pepper and thousandseal. Van Der Kooi et al. (2015). Achillea millefolium is 0.2-1 m in height and has a spreading rhizomatous growth shape, growing one to multiple stems. ...
... A flat-toped capitulum cluster produces the inflorescence and many insects frequent the inflorescences with a generalized pollination scheme. Van Der Kooi et al. (2015). Yarrow is widely used due to its many pharmacological properties, such as antiinflammatory drugs, in folk medicine (Goldberg et al., 1969), antispasmodic (Falk et al., 1975), antiseptic (Candan et al., 2003), diaphoretic, anti-swelling, and antihypertensive (Sweetman et al., 2002), diuretic and antidiarrheal (Honda et al., 1996) and emmenagogue (Schulz et al., 2001). ...
Article
Full-text available
Achillea millefolium is a major medicinal and aromatic herb and has antioxidant, antimicrobial, antispasmodic and antitumor effects in its essential oil. This research was conducted at Floriculture Farm and in the Laboratories of Horticulture Departments, Faculty of Agriculture at Moshtohor, Benha Univ., during 2018/2019 and 2019/2020 seasons to study the effect of foliar spraying at 2000 mg/l with various potassium sources i.e., potassium chloride, potassium citrate, potassium humate, potassium nitrate, potassium silicate, potassium sulphate, monopotassium phosphate and di-potassium hydrogen phosphate on vegetative growth, flowering, essential oil productivity and some chemical constituents of yarrow (Achillea millefolium L.) plants. Results showed that various potassium sources scored highly significant effects on vegetative growth and flowering of A. millefolium L. plant, particularly potassium nitrate followed potassium humate. Moreover, the richest leaf N% was resulted by potassium nitrate, whereas, spraying A. millefolium L. plants with monopotassium phosphate treatment induced the highest values of the percentage of P (%) and total chlorophylls content (%) as well as the maximum K (%), while total carbohydrate content was given by potassium sulphate. In addition, spraying yarrow plant with potassium citrate treatment induced the maximum values of essential oil parameters. Furthermore, the constituents of volatile oil of A. millefolium L. showed 13 components have been recognized. The major components were α-bisabolol oxide B, limonene, carvacrol and chamazulene. Consequently, spraying A. millefolium L. plants with potassium nitrate or potassium humate is recommended, to boost growth, flowering and some chemical constituents, whereas potassium citrate and potassium silicate treatment induced the richest values of essential oils production.
... The natural vegetation commonly contributes to pollination in some crop areas because the natural areas maintain quantity and diversity of resources, which can maintain pollinators able to visit crops during blooms(Cunningham & Le Feuvre, 2013;Latini et al., 2020;Saturni et al., 2016). In natural environments, plants may compete for pollinators simultaneously during flowering, which stimulates the selection of divergent flower phenotypes (van derKooi et al., 2015). ...
Article
Although West Indian Cherry (WIC) trees have abundant flowering, specimens of this species have low fructification rates, potentially associated with the dependence of these plants on pollinators for cross-pollination and fruit production. We quantified fructification rates and assessed the market value of pollination services by conducting an experiment with six treatments, including manual and open pollination, pollinator exclusion treatment, and open pollination with blue and yellow attractants. The investigation occurred at two sampling periods (November–December 2015 and January–February 2016) in a commercial orchard of WIC in Brazil. Despite the six different treatments in the two sampling periods, the fructification rate only differed in open pollination treatments with colour attractants, increasing the fructification rate between 160% (for blue-coloured attractants) and 240% (for yellow-coloured attractants). Considering that yield is directly affected by the increase in the fructification rate, the yield might be enhanced by up to 70 ton/ha by the coloured attractants. Economically speaking, this result means an approximate 130% increase in the earnings for farmers and maybe transferable to other crops contributing to food production and recognizing the importance of biodiversity and associated ecosystem services. link to free access: https://onlinelibrary.wiley.com/share/author/AUMMHDTMMDXW7USFP954?target=10.1111/jen.12964
... Finally, studies of pollinator-mediated interactions have almost exclusively relied on estimates of flower visitation to infer positive versus negative interactions among plant species (e.g. Ghazoul 2006;Sieber et al. 2011;Ye et al. 2014;van der Kooi et al. 2016) despite that flower visitation alone can be a poor proxy of overall pollination success (e.g. King et al. 2013). ...
Article
Full-text available
Pollinator-mediated competition and facilitation are two important mechanisms mediating co-flowering community assembly. Experimental studies, however, have mostly focused on evaluating outcomes for a single interacting partner at a single location. Studies that evaluate spatial variation in the bidirectional effects between co-flowering species are necessary if we aim to advance our understanding of the processes that mediate species coexistence in diverse co-flowering communities. Here, we examine geographic variation (i.e., at landscape level) in bidirectional pollinator-mediated effects between co-flowering Mimulus guttatus and Delphinium uliginosum. We evaluated effects on pollen transfer dynamics (conspecific and heterospecific pollen deposition) and plant reproductive success. We found evidence of asymmetrical effects (one species is disrupted and the other one is facilitated) but the effects were highly dependent on geographical location. Furthermore, effects on pollen transfer dynamics did not always translate to effects on overall plant reproductive success (i.e., pollen tube growth) highlighting the importance of evaluating effects at multiple stages of the pollination process. Overall, our results provide evidence of a spatial mosaic of pollinator-mediated interactions between co-flowering species and suggest that community assembly processes could result from competition and facilitation acting simultaneously. Our study highlights the importance of experimental studies that evaluate the prevalence of competitive and facilitative interactions in the field, and that expand across a wide geographical context, in order to more fully understand the mechanisms that shape plant communities in nature.
... Several studies used null models based on random assembly to evaluate the pattern of FCA, and revealed that FCA was non-random in most plant communities and highly shaped by the plant-pollinator interaction (de Jager et al., 2011;Muchhala et al., 2014;Makino and Yokoyama, 2015;Ohashi et al., 2015;Kemp et al., 2019), although evidence of random assembly also exists for the continental island of Australia (Shrestha et al., 2019b). Competition for pollinator visitations was the major selection force to shape the FCA of plant communities in high latitudes and high altitudes, which often caused floral color over-dispersion (Muchhala et al., 2014;van der Kooi et al., 2016;Bergamo et al., 2018), but there is also some evidence of clustering at high altitudes (Bergamo et al., 2018). As both number and abundance of pollinators are thought to generally decrease with increasing altitudes (Warren et al., 1988;Bingham and Orthner, 1998), but see Shrestha et al. (2014) for a different effect in the Himalayan mountains, it is plausible this may affect FCA. ...
Article
Full-text available
Pollinators with different vision are a key driver of flower coloration. Islands provide important insights into evolutionary processes, and previous work suggests islands may have restricted flower colors. Due to both species richness with high endemism in tropical-subtropical environments, and potentially changing pollinator distributions with altitude, we evaluated flower color diversity across the mountainous island of Taiwan in a comparative framework to understand the cause of color diversity. We sampled flower color signaling on the tropical-subtropical island of Taiwan considering altitudes from sea level to 3300 m to inform how over-dispersion, random processes or clustering may influence flower signaling. We employed a model of bee color space to plot loci from 727 species to enable direct comparisons to data sets from continental studies representing Northern and Southern Hemispheres, and also a continental mountain region. We observed that flower color diversity was similar to flowers that exist in mainland continental studies, and also showed evidence that flowers predominantly had evolved color signals that closely matched bee color preferences. At high altitudes floras tend to be phylogenetically clustered rather than over-dispersed, and their floral colors exhibited weak phylogenetic signal which is consistent with character displacement that facilitated the coexistence of related species. Overall flower color signaling on a tropical-subtropical island is mainly influenced by color preferences of key bee pollinators, a pattern consistent with continental studies.
... Then, following Kantsa et al. (2017), we described the dominant color of the corolla using color saturation (r) or "spectral purity", a measure of how much gray or white is mixed with pure color, and tonality (angle θ; 0 -360°). Because variation in the amplitude of the reflectance for each species was small, we randomly selected one reflectance curve for the construction of the bee color vision model (van der Kooi et al. 2016). We omitted floral symmetry (radial vs. bilateral) from our analyses, even though it can contribute to ...
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1. The ecological dynamics of co-flowering communities are largely mediated by pollinators. However, current understanding of pollinator-mediated interactions primarily relies on how co-flowering plants influence attraction of shared pollinators, and much less is known about plan-plant interactions that occur via heterospecific pollen (HP) transfer. Invaded communities in particular can be highly affected by the transfer of alien pollen, but the strength, drivers, and fitness consequences of these interactions at a community scale are not well understood. 2. Here we analyze HP transfer networks in nine coastal communities in the Yucatan Mexico that vary in the relative abundance of invasive flowers to evaluate how HP donation and receipt varies between native and alien plants. We further evaluate whether HP donation and receipt are mediated by floral traits (e.g. display, flower size) or pollinator visitation rate. Finally, we evaluated whether post-pollination success (proportion of pollen tubes produced) was affected by alien HP receipt and whether the effect varied between native and alien recipients. 3. HP transfer networks exhibit relatively high connectance (ca. 15%), suggesting high HP transfer within the studied communities. Significant network nestedness further suggests the existence of species that predominantly act as HP donors or recipients in the community. Species-level analyses showed that natives receive 80% more HP compared to alien species, and that alien plants donate 40% more HP than natives. HP receipt and donation were mediated by different floral traits and such effects were independent of plant origin (native or alien). The proportion of alien HP received significantly affected conspecific pollen tube success in natives, but not that of alien species. 4. Synthesis. Our results suggest that HP transfer in invaded communities is widespread, and that native and alien species play different roles within HP transfer networks, which are mediated by a different suite of floral traits. Alien species, in particular, play a central role as HP donors and are more tolerant to HP receipt than natives-a finding that points to two overlooked mechanisms facilitating alien plant invasion and success within native co-flowering communities.
... Studies conducted in recent years have shown that flowering also has a significant negative effect on signals obtained from vegetation canopies (Behrens et al. 2006;Fang et al. 2016;Ge et al. 2006;Kooi et al. 2016;Landmann et al. 2015;Mirik et al. 2013). Presence of flowers increases reflectance measurements especially in the green and red regions, causing the models established to come up with predictions to produce misleading results. ...
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