how do pollinator visitation rate and seed set relate to speciesâ floral traits and community...
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PLANT-ANIMAL INTERACTIONS - ORIGINAL RESEARCH
How do pollinator visitation rate and seed set relate to species’floral traits and community context?
Amparo Lazaro • Anna Jakobsson •
Ørjan Totland
Received: 15 June 2012 / Accepted: 29 March 2013
� Springer-Verlag Berlin Heidelberg 2013
Abstract Differences among plant species in visitation
rate and seed set within a community may be explained
both by the species’ floral traits and the community con-
text. Additionally, the importance of species’ floral traits
vs. community context on visitation rate and seed set may
vary among communities. In communities where the pol-
linator-to-flower ratio is low, floral traits may be more
important than community context, as pollinators may have
the opportunity to be choosier when visiting plant species.
In this study we investigated whether species’ floral traits
(flower shape, size and number, and flowering duration)
and community context (conspecific and heterospecific
flower density, and pollinator abundance) could explain
among-species variation in visitation rate and seed set. For
this, we used data on 47 plant species from two Norwegian
plant communities differing in pollinator-to-flower ratio.
Differences among species in visitation rate and seed set
within a community could be explained by similar vari-
ables as those explaining visitation rate and seed set within
species. As expected, we found floral traits to be more
important than community context in the community with a
lower pollinator-to-flower ratio; whereas in the community
with a higher pollinator-to-flower ratio, community context
played a bigger role. Our study gives significant insights
into the relative importance of floral traits on species’
visitation rate and seed set, and contributes to our under-
standing of the role of the community context on the fitness
of plant species.
Keywords Conspecific flower density � Display traits �Heterospecific flower density � Inter-specific comparison �Pollinator abundance
Introduction
Plant species differ substantially in the number of polli-
nator visits they receive and in their seed set. Floral traits
are supposed to favour pollination both by attracting
pollinators and by maximizing pollinator efficiency (Fae-
gri and van der Pijl 1966). For this reason, differences
among species in floral traits may be partially responsible
for among-species differences in attractiveness and fitness.
In addition, the community context experienced by indi-
viduals, i.e. the abundance of pollinators and co-flowering
con- and heterospecific plants, is known to affect polli-
nation success (Rathcke 1983) and therefore, it may also
influence among-species differences in visitation rate and
seed set.
The floral traits of a species can be dissected into
components of floral design (e.g. flower shape, size and
number) and temporal characteristics (e.g. flowering
Communicated by Katherine Gross.
Electronic supplementary material The online version of thisarticle (doi:10.1007/s00442-013-2652-5) contains supplementarymaterial, which is available to authorized users.
A. Lazaro (&)
Department of Biodiversity and Conservation, Mediterranean
Institute for Advanced Studies (UIB-CSIC), C/Miquel
Marques 21, Esporles, Balearic Islands 07190, Spain
e-mail: [email protected]
A. Jakobsson
Department of Plant Ecology and Evolution, Uppsala University,
Norbyvagen 18d, 752 36 Uppsala, Sweden
Ø. Totland
Department of Ecology and Natural Resource Management,
Norwegian University of Life Sciences, P.O. Box 5003,
1432 As, Norway
123
Oecologia
DOI 10.1007/s00442-013-2652-5
duration). Intra-specific studies have shown that all of
these floral traits can influence visitation rate and fruit/
seed set. Flower shape can affect the frequency of visitors
(Gomez et al. 2009), and flower size is often positively
related to visitation rate (Bell 1985; Galen and Newport
1987; Eckhart 1991; Dudash et al. 2011) and seed pro-
duction (Galen and Newport 1987). Moreover, the total
number of visits to individuals usually increases with their
flower number, but in a decelerating manner (Robertson
and Macnair 1995; Ohashi and Yahara 2002; Mitchell
et al. 2004). Because of this, the visitation rate and seed
set per flower can be constant (Robertson and Macnair
1995; Goulson et al. 1998; Mitchell et al. 2004) or even
decrease with flower number (Klinkhamer and de Jong
1990; Grindeland et al. 2005). A negative relationship
between flowering duration and visitation rate is plausi-
ble, because long flower longevity and a long flowering
period are often related to a shortage of pollinator visits
and stochastic climatic conditions, respectively (Arroyo
et al. 1981; Blionis et al. 2001). Similar relationships
between floral traits and visitation rate and seed set to
those found within species could also be expected to
occur at the among-species level. However, if these
relationships exist they may be weaker, since plant spe-
cies also differ in other relevant characteristics that
influence visitation rate and seed set, such as reward
levels and the capability of self-fertilization. Lastly,
because morphologically specialized flowers tend to be
also ecologically specialized (Fenster et al. 2004), dif-
ferences among species in flower shape may influence
visitation frequencies (McCall and Primack 1992) and can
also modify the relationships between the variables
described above and visitation rate and seed set. To our
knowledge, only a couple of studies at the community
Table 1 The plant species (Mossberg and Stenberg 2007) of each community included in this study, their family, the observation time (Obs.time; hours) and the number of individuals sampled for seed set (Sam. ind.)
Community Species Family Obs.
time
Sam.
ind.
Community Species Family Obs.
time
Sam.
ind.
Ryghsetra Anthyllis vulneraria Fabaceae 6.3 26 Finse Astragalus alpinus Fabaceae 21.3 26
Centaurea jacea Asteraceae 11.3 36 Bartsia alpina Scrophulariaceae 20.7 44
Centaurea scabiosa Asteraceae 3.0 31 Campanula rotundifolia Campanulaceae 3.7 36
Fragaria vesca Rosaceae 9.0 28 Cerastium alpinum Caryophyllaceae 11.3 33
Galium boreale Rubiaceae 5.0 23 Dryas octopetala Rosaceae 9.0 34
Galium mollugo Rubiaceae 20.0 55 Erigeron uniflorus Asteraceae 15.3 50
Geranium sylvaticum Geraniaceae 7.0 15 Euphrasia frigida Scrophulariaceae 6.0 86
Geum rivale Rosaceae 5.7 15 Gentiana nivalis Gentianaceae 4.3 41
Hieracium sec. hieracium Asteraceae 1.0 15 Gentianella campestris var. suecica Gentianaceae 1.3 23
Knautia arvensis Dipsacaceae 3.0 15 Geranium sylvaticum Geraniaceae 10.3 23
Lathyrus linifolius Fabaceae 3.0 15 Leontodon autumnalis Asteraceae 22.3 34
Leucanthemum vulgare Asteraceae 17.0 66 Parnassia palustris Celastraceae 19.7 80
Linum catharticum Linaceae 9.0 71 Pinguicula vulgaris Lentibulariaceae 4.0 20
Lotus corniculatus Fabaceae 8.0 17 Potentilla crantzii Rosaceae 15.0 40
Pilosella lactucella Asteraceae 6.3 34 Pyrola minor Ericaceae 3.0 16
Pilosella officinarum Asteraceae 10.3 27 Ranunculus acris Ranunculaceae 18.7 29
Pilosella pubescens Asteraceae 6.3 41 Saussurea alpina Asteraceae 5.3 44
Polygala vulgaris Polygalaceae 12.0 48 Silene acaulis Caryophyllaceae 20.3 49
Potentilla erecta Rosaceae 24.7 51 Tofieldia pusilla Liliaceae 8.0 32
Potentilla thuringiaca Rosaceae 7.3 24 Veronica alpina Plantaginaceae 7.0 53
Primula veris Primulaceae 5.7 51 Viscaria alpina Caryophyllaceae 0.7 15
Prunella vulgaris Lamiaceae 2.3 15
Ranunculus acris Ranunculaceae 7.7 15
Trifolium medium Fabaceae 5.3 16
Trifolium pratense Fabaceae 10.7 17
Vicia cracca Fabaceae 4.3 15
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level have related species’ floral traits to visitation rates
(McCall and Primack 1992; Hegland and Totland 2005);
and these studies have not examined the relationship
between species’ floral traits and seed set.
In addition to species’ floral traits, the community
context, i.e. the plants and pollinators occurring simulta-
neously in the community, may also influence visitation
rate and seed set through competitive or facilitative inter-
actions (Rathcke 1983). The local plant density of a species
is often positively related to its visitation rate (Klinkhamer
and de Jong 1990; Feinsinger et al. 1991; Kunin 1993;
Makino et al. 2007) and seed set (Feinsinger et al. 1991;
Jennersten and Nilsson 1993; Kunin 1993), because poll-
inators preferentially visit high-density patches (Stephens
and Krebs 1986; Goulson 2003; Hersch and Roy 2007)
and/or because there is an increased likelihood of receiving
outcross and compatible pollen at high conspecific density
(Jennersten and Nilsson 1993; Karron et al. 1995). The
abundance of other blooming species can have either
positive or negative effects on pollinator visitation rate and
seed set of a species (Schemske 1981; Rathcke 1983;
Feinsinger et al. 1991; Moeller 2004). Moreover, the
abundance of adequate pollinators during the flowering
period of a species may be positively related to its visita-
tion rate and seed set (Kudo 1993; Kwak and Bergman
1996; Price et al. 2005).
The distinction between the effect of species’ floral
traits and the community context is relevant in ecology
and evolution, because while species’ floral traits are
supposed to have evolved to favour pollination, the con-
text in which they exist is fortuitous. However, to date
little is known about the relative importance of commu-
nity context and species’ floral traits on visitation rate and
seed set. Moreover, the effects of floral traits and local
community context on visitation rate often vary among
plant populations (Eckhart 1991; Lazaro and Totland
2010) and insect taxa (Thompson 2001; Lazaro et al.
2009). Therefore, it is conceivable that the relative
importance of species’ floral traits versus community
context on visitation rate and seed set also vary among
communities, depending on the abundance of their poll-
inators. In communities where the pollinator-to-flower
ratio is low, competition theory predicts a low competi-
tion among pollinators for floral resources (Alley 1982);
and pollinators may be choosier when deciding which
plant species to visit (Schmitt 1983). In such communities
we expect floral traits to be more important than com-
munity context. Conversely, in communities with high
pollinator-to-flower ratio (i.e. where pollinators may
compete for floral resources), pollinator competence may
alter initial flower preferences (e.g. Chittka and Thomson
2001), and pollinators would not have the opportunity to
be choosy (Schmitt 1983). As a result, pollinator choices
of plant species may be more influenced by the commu-
nity context.
In this study, we investigated the relative importance of
species’ floral traits and community context on visitation
rate and seed set, using data from two communities in
southern Norway: one semi-natural species-rich meadow
with a high abundance and diversity of pollinators, and one
alpine community where pollinators are at a lower abun-
dance. Our specific objectives were: (1) to investigate how
pollinator visitation rate and seed set relate to species’
floral traits (flower shape, size and number, and flowering
duration) and community context (conspecific and hetero-
specific flower density, and pollinator abundance) in the
two study communities; and (2) to determine whether the
importance of species’ floral traits vs. community context
differed between the two study communities; we expected
less importance of the community context in the commu-
nity where pollinators are scarce.
Materials and methods
Study areas and species
We conducted our study in two plant communities of
southern Norway. The first community is a species-rich
semi-natural meadow at Ryghsetra (59�4400300N,
10�0204800E), Buskerud county, at 300 m altitude. Here, the
blooming season starts in early-mid May and terminates in
mid-late August, and around 55 species are in flower dur-
ing this period. The flower visitor assemblage of this
community consisted of 72.7 % bumblebees, 11 % mus-
coid flies, 5.5 % solitary bees, 4.7 % hover flies, 2.4 %
ants, 1.6 % butterflies, 0.9 % honeybees, 0.5 % beetles,
0.5 % beeflies, and 0.04 % wasps in the study year. The
average (across all the species) number of pollinator visits
recorded per hour was 64.7, and the pollinator visits to
flowers ratio was 0.17.
The second community is a southwest exposed slope on
Sandalsnuten, at Finse (*60�N, 7�E), in southwest alpine
Norway, at 1,450 m altitude. Here, the blooming season
starts in late June and terminates in late August, and ca. 25
species are in flower during this period. The flower visitor
assemblage of this community consisted of 85.8 % mus-
coid flies, 7.9 % butterflies, 3.6 % bumblebees and 2.5 %
hover flies in the study year. The average number of pol-
linator visits recorded per hour was 47.9, and the pollinator
visits to flowers ratio was 0.09. Thus, at Finse there is
substantially more flowers relative to flower visits, com-
pared to Ryghsetra.
We included in this study the 47 plant species (26 from
Ryghsetra and 21 from Finse) for whichwe obtained ade-
quate sample sizes to conduct the analyses (Table 1).
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Pollinator observations and flower densities
We observed insect visitation to plant species from 13 May
to 19 July 2006 at Ryghsetra, and from 3 July to 5 August
2006 at Finse. These periods cover the whole flowering
period of most plant species in these communities. At the
beginning of the field season, we placed 30 permanent
2 9 2-m plots in both communities. The inner 1 9 1-m
square of these plots was marked and observations were
conducted within it. Due to the particular characteristics of
the study sites, and in order to get the best representation of
each community, we placed the plots at random at Finse,
and systematically at Ryghsetra. Twenty additional non-
permanent plots were located at Ryghsetra during June
(flowering peak of the community). The location of these
additional plots was randomly changed after each obser-
vation period. This was necessary in order to collect
enough information on the visits to all the species bloom-
ing during the flowering peak of the community. These
differences in sampling strategy likely had no influence on
our results, since we focus on among-species comparisons
within communities.
Observations were conducted every day with weather
conditions allowing pollinator activity, between 0900 and
1800 hours, using 20-min observation periods. The order
of observation of plots was random, but we never
observed the same plot more than once per day. During
each observation period we noted the number of flower
visitors to flowers or inflorescences (depending on the
species) of all flowering species in the plots. A visit was
defined to have occurred when the visitor’s body made
contact with the reproductive organs (stigma or anther) of
the flower. Flower visitors that contacted reproductive
organs of plants were regarded as pollinators, although
some of these visitors may be ineffective pollinators. In
total, we conducted 118 and 134 observation periods at
Ryghsetra and Finse, respectively (see Table 1 for total
number of observation hours for each study plant
species).
After each observation period, we counted the number
of open flower units of each species occurring both in the
2 9 2-m plots and in the 1 9 1-m inner squares. The
number of flower units counted in the 1 9 1-m inner
squares was used to calculate flower visitation rates,
whereas the number of flower units counted in the 2 9 2-m
plots was used to calculate floral abundances (see below).
The flower units were normally flowers, except in the case
of species with pseudanthia (e.g. Asteraceae, Knautia
arvensis), for which the flower unit was the inflorescence
[Hegland and Totland 2005; see Table S1, Electronic
Supplementary Material (ESM) for flower units used for
each species].
Visitation rate
For each species, we calculated a visitation rate per flower
unit in each 20-min observation period by dividing the
number of observed pollinator visits by the number of
observed open flower units. The values per observation
period were averaged to obtain species’ means (hereafter
‘visitation rate’).
Seed set
We haphazardly selected and marked from one to three
individuals per plant species in each plot where they
occurred, counted their total number of flowers and
inflorescences, and marked one flower unit (Table S1,
ESM) on each individual. For plant species with low
abundance (B30 individuals) in the permanent plots, we
haphazardly selected 15 additional individuals outside the
plots to increase sample size for the study of seed set.
When fruits were ripe we counted the total number of fruit
units and collected the fruit units of the marked flower
units. Fruit units were fruits or infructescences depending
on the species (see Table S1, ESM, for fruit units for each
species). The number of undeveloped seeds, aborted seeds
and fully developed seeds of these fruit units were counted
in the lab. We calculated fruit set as the proportion of
female flower units that developed fruit units. In order to
use a standardized measure of fecundity that was compa-
rable among plant species and that included both the
production of fruits and seed set per fruit, we estimated
total seed set at the plant level. This total seed set (here-
after ‘seed set’) was calculated by dividing the total
number of developed seeds produced by the plant (fruit
set 9 average number of developed seeds per fruit
unit 9 flower units) by the total number of ovules pro-
duced by the plant (average number of ovules per flower
unit 9 number of flower units). We were unable to count
the number of undeveloped seeds in Primula veris, so in
order to estimate the total number of ovules produced by a
plant, we multiplied its number of flowers by 50, which is
the average number of ovules in this species (Wissman
2006). The values per individual plant were averaged to
obtain species’ means.
Species’ floral traits
All the floral traits of the species included in this study were
calculated at the flower level, except for the species with
pseudanthia (i.e. inflorescences with a flower-like struc-
ture), for which the pseudanthium was used instead. For
each plant species we used the same flower units as those
used for the estimation of visitation rates and abundances
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(Table S1, ESM). For the description of floral traits we used
the term ‘flower’ to refer to flowers or pseudanthia.
Flower shape
To describe flower shape in a simple manner that allows
statistical analyses, we categorised species into ‘unspe-
cialized’ and ‘specialized’ flowers, following the termi-
nology by Larson and Barrett (2000). Unspecialized
flowers could potentially be visited by a wide range of
pollinator groups, and included open flowers (e.g. Poten-
tilla erecta) and small clusters of flowers in open inflo-
rescences (e.g. Asteraceae). Specialized flowers were those
that exerted a difficulty of handling, and consequently
could only be accessed by a subset of the pollinator fauna.
Among the specialized flowers we included closed flowers
(e.g. Fabaceae), semi-closed flowers (e.g. Scrophularia-
ceae) and pendular flowers (e.g. Geum rivale). Table S1
(ESM) shows the categories of flower shape used for the
study species.
Flower size
We measured tube length and width of flowers on all
species except those with pseudanthia (e.g. Asteraceae,
Knautia arvensis), for which we measured width and
length of inflorescences. Measurements (to the nearest
millimetre) were conducted in the field on 30 randomly
selected individuals per species (one flower/pseudanthia
per individual), using a digital calliper. In order to obtain a
value for flower size that integrated all these measure-
ments, we calculated the area of the flower, following
Hegland and Totland (2005). Thus, for visual displays with
circular outline (e.g. Leucanthemum vulgare) we used the
formula pr2, where r = radius; and for visual displays with
a length dimension (e.g. Lathyrus linifolius) we used the
formula of a cylinder (without a base) 2prl ? pr2, where
l = length. We used these areas for visual displays of
different shape to take into account how insects approach
the flowers (either from the upper part of them, or from
different heights and angles). Table S1 (ESM) shows the
flower size calculated for each study species.
Flower number
We calculated flower number for each species as the
average number of flowers per individual.
Flowering duration
We estimated flowering duration as the number of days
each species flowered, from the first to the last day we
observed open flowers of the species.
Community context
Conspecific flower density
We estimated conspecific flower density as the average
number of flower units of each species per square metre
(only the 2 9 2-m permanent plots were included in this
calculation). Although conspecific flower density is a
population variable, we included it as a community context
variable, since with our variable classification, we intended
to discriminate between the traits of individuals within
species and the variables related to the context of
individuals.
Heterospecific flower density
We calculated heterospecific flower density in each com-
munity during the flowering period of each study species.
For this, we averaged the number of open heterospecific
flower units (i.e. all except the focal species) recorded per
plot in the whole community while the focal species
flowered.
Pollinator abundance
We calculated pollinator abundance for each study species
by using the average number of pollinator visits recorded
per observation period in the whole community during the
flowering period of the study species.
Statistical analyses
To study the relative importance of species’ floral traits and
community context for pollinator visitation rate and seed
set, we used generalized linear models separately for each
community and response variable. In these analyses the
plant species were the sample units and visitation rate and
seed set the response variables. Due to the nature of the
data, we used: (1) gamma distributions and inverse link
functions for the analyses of visitation rate (visitation rate
?1; in order to avoid zeros in the response variable); and
(2) binomial distributions and logit link functions for the
analyses of seed set. We used all the variables described in
Species’ floral traits and Community context as predictors.
We included visitation rate as an additional predictor in the
models of seed set to account for the potential direct effect
of visitation rate on seed set (Jennersten 1988; Pauw 2007),
that is independent on its effect through floral traits or
community context. We also included sampling effort (i.e.
the number of hours we observed plots containing each
species) as an additional predictor variable in the analyses
of visitation rate. We conducted the analyses of visitation
rate with and without the plant species observed \3 h
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(Table 1), but since the results did not change (results not
shown), we present here the results using all the study
species. Prior to analyses, we ran variation inflation factor
(VIF) analyses to identify collinear predictor variables that
should be removed from further analyses (Zuur et al.
2009). VIF values were smaller than 3 for all variables, so
none of the predictors needed to be removed (Zuur et al.
2009). We used automatic selection of best models
(package glmulti, R 12.2) using corrected Akaike infor-
mation criterion to select the best models (Calcagno and de
Mazancourt 2010). All analyses were conducted in R 12.2
(R Development Core Team 2008). Means are accompa-
nied by their SE throughout the text.
Results
Visitation rate
At Ryghsetra, several variables describing species’ floral
traits significantly explained variation among species in
visitation rate (Table 2). Visitation rate was higher for
species with unspecialized flowers compared to species
with specialized flowers (1.34 ± 0.15 vs. 0.13 ± 0.01
visits/20 min, respectively), and decreased with flower
number (Table 2; Fig. 1a). Visitation rate was also
related to flowering duration, but this relationship dif-
fered between species with unspecialized and specialized
flowers (Table 2): while visitation rate was negatively
related to flowering duration in species with unspecial-
ized flowers, there was no relationship between flowering
duration and visitation rate for species with specialized
flowers (Fig. 1b). In addition, visitation rate was signif-
icantly related to two variables describing the community
context: pollinator abundance and heterospecific flower
density (Table 2). Visitation rate increased with pollina-
tor abundance in the community consistently for both
specialized and unspecialized flowers (Table 2; Fig. 1c);
however, the relationship between visitation rate and
heterospecific flower density depended on flower shape.
Visitation rate decreased with heterospecific flower
density in species with unspecialized flowers, whereas
visitation rate of species with specialized flowers was
not related to heterospecific flower density (Table 2;
Fig. 1d).
At Finse, visitation rate was also higher for species with
unspecialized flowers compared to species with specialized
flowers (0.57 ± 0.04 vs. 0.15 ± 0.03 visits/20 min,
respectively; Table 2), and increased with flower size
(Table 2; Fig. 2). None of the variables describing the
community context significantly explained variation
among species in visitation rate in this community
(P [[ 0.05).
Seed set
At Ryghsetra, several variables describing species’ floral
traits significantly explained variation among species in
their seed set. Seed set was higher for species with
unspecialized flowers compared to species with specialized
flowers (0.46 ± 0.01 vs. 0.25 ± 0.02 seeds/ovules,
respectively; Table 3) and decreased with flower number
(Table 3; Fig. 3a). Flowering duration was also related to
seed set; however, the direction of the relationship between
flowering duration and seed set was different for species
with specialized and unspecialized flowers (Table 3;
Fig. 3b). While there was a positive relationship between
flowering duration and seed set in species with unspecial-
ized flowers, there was a negative relationship between
these two variables in species with specialized flowers
(Fig. 3b). In addition, variables describing the community
context also significantly explained variation among spe-
cies in their seed set. Thus, seed set increased with polli-
nator abundance (Fig. 3c), conspecific flower density
(Fig. 3d) and heterospecific flower density (Fig. 3e). The
relationship between seed set and heterospecific flower
density was, however, stronger in species with specialized
than unspecialized flowers (Table 3; Fig. 3e).
At Finse, seed set was higher in species with specialized
than unspecialized flowers (0.64 ± 0.04 vs. 0.58 ± 0.03
seeds/ovules, respectively; Table 3). Seed set decreased
with flower number (Fig. 4a), and flowering duration
(Fig. 4b), whereas it increased with flower size (Fig. 4c).
None of the variables describing the community context
significantly explained variation among species in seed set
at Finse (P � 0.05).
Discussion
We have shown here that differences among species in
visitation rate and seed set within a community can be
explained by similar variables to those explaining visitation
rate and seed set within species. In our study, species’ floral
traits (flower shape, size and number, and flowering dura-
tion), significantly explained variation in visitation rates and
seed set among species in both communities. However, as
expected, the variables describing the community context
(conspecific and heterospecific flower density and pollina-
tor abundance) were significantly related to visitation rate
and seed set only at Ryghsetra, the community where the
pollinator-to-flower ratio was higher. Although the vari-
ables that explained variation in visitation rate also
explained variation in seed set, the best models for seed set
were more complex and included more variables. This
indicates that the relationship between visitation and seed
production is not straightforward (as shown also by the lack
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123
of significance of the variable visitation rate in the models
of seed set). Such decoupling between visitation rate and
seed set is not surprising, and can occur if species can
compensate for pollen limitation through self-fertilization
(Karoly 1992; Kalisz et al. 2004), if they differ in the
number of pollinator visits needed to fertilize the ovules
(Molano-Flores et al. 1999), or when resource acquisition
limits seed production or maturation (e.g. Totland 2001).
Moreover, an absence of a direct link between visitation and
seed production can be due to inter-specific pollen transfer
(Galen and Gregory 1989; Caruso and Alfaro 2000; Ja-
kobsson et al. 2007), and/or pollinator behaviour that dif-
ferentially affect the quantity and quality of flower visits
(e.g. de Jong et al. 1993; Klinkhamer and de Jong 1993).
Table 2 Best models explaining inter-specific variation in visitation rate at Ryghsetra and Finse, using gamma distributions and inverse link
functions, and corrected Akaike information criterion (AICc) for model selection
Community Variable Estimate SE t P-value
Ryghsetra Intercept 1.04 0.17 5.95 \0.0001
Shape (unspecialized) -0.87 0.20 -4.29 0.0004
Flower number 0.004 0.0008 4.67 0.0002
Pollinator abundance -0.008 0.001 -5.65 \0.0001
Flowering duration -0.003 0.004 -0.57 0.57
Heterospecific flower density -0.003 0.005 -0.53 0.61
Shape (unspecialized) 9 flowering duration 0.01 0.005 2.08 0.052
Shape (unspecialized) 9 heterospecific flower density 0.01 0.006 2.54 0.021
Finse Intercept 1.13 0.13 8.96 \0.0001
Shape (unspecialized) -0.30 0.11 -2.85 0.01
Flower size -0.001 0.0003 -3.53 0.002
Note that the sign of the parameter estimates is opposite to the direction of the relationship between variables due to the use of an inverse link
function
Fig. 1 Relationships between
visitation rate at Ryghsetra and
a flower number, b flowering
duration, c pollinator abundance
and d heterospecific flower
density. Lines represent the
estimates of the best model and
the circles represent the partial
residuals of the model. When
there is a significant interaction,
the relationship is shown for
species with unspecialized
(empty circles, dotted lines) and
specialized flowers (filledcircles, solid lines)
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123
Species’ floral traits
In both communities, species with unspecialized flowers
had higher visitation rates than those with specialized
flowers; this is in line with the findings of McCall and
Primack (1992) who showed higher visitation rates to open
flowers compared to tubular flowers. As expected, flower
shape also modified the relationships between other pre-
dictor variables and visitation rate and seed set.
At Finse, we found that both visitation rate and seed set
increased with flower size. Several studies at the within-
species level have found flower size to positively affect
visitation (Bell 1985; Galen and Newport 1987; Eckhart
1991; Dudash et al. 2011) and seed production (Galen and
Newport 1987), and this effect has mainly been attributed
to a higher attractiveness of larger flowers. However,
higher seed production in larger flowers could also reflect
resource acquisition rather than increased pollination suc-
cess (Harder and Johnson 2009). To our knowledge, our
study is the first to report relationships between flower size
and visitation rate and seed set at the among-species level.
However, we only found these relationships in the alpine
community, Finse. The greater importance of flower size in
the alpine community can be due to a stronger plant species
selectivity by insects there (Schmitt 1983) and/or a larger
similarity among plant species in other floral traits [most
often unspecialized (Table 2) and with single or few
flowers]. Future studies may shed light on whether the
difference among species in flower size is an important
determinant of visitation rate and seed set in other alpine
communities.
Flower number was negatively related to visitation rate
and seed set in both communities. At the within-species
level, several studies have shown that the total number of
visits to a plant increases with its flower number (Eckhart
1991; Makino et al. 2007), but in a decelerating manner
(Robertson and Macnair 1995; Ohashi and Yahara 2002;
Mitchell et al. 2004). One reason for such a pattern may be
that insects attempt to avoid revisiting previously visited,
and thus less rewarding, flowers (Dreisig 1995). As a
consequence, visitation rate and seed set per flower may be
independent of (Robertson and Macnair 1995; Goulson
et al. 1998; Mitchell et al. 2004), or even decrease with,
flower number (Klinkhamer and de Jong 1990; Grindeland
et al. 2005). This may explain the negative relationship
between flower number and visitation rate and seed set that
we found at the inter-specific level at Ryghsetra. At Finse,
seed set was also negatively related to flower number, but
Fig. 2 Relationship between visitation and flower size at Finse. The
line represents the estimates of the best model and the circlesrepresent the partial residuals of the model
Table 3 Best models explaining inter-specific variation in seed set at Ryghsetra and Finse, using binomial distributions and logit link functions,
and AICc for model selection
Community Variable Estimate SE t P-value
Ryghsetra Intercept -0.71 0.18 -3.90 \0.0001
Shape (unspecialized) -1.28 0.37 -3.45 0.0006
Flower number -0.01 0.005 -20.59 \0.0001
Conspecific flower density 0.18 0.01 15.94 \0.0001
Pollinator abundance 0.03 0.01 5.31 \0.0001
Flowering duration -0.05 0.01 -5.74 \0.0001
Heterospecific flower density 0.05 0.01 7.28 \0.0001
Shape (unspecialized) 9 flowering duration 0.07 0.01 6.94 \0.0001
Shape (unspecialized) 9 heterospecific flower density -0.04 0.01 -4.16 \0.0001
Finse Intercept 1.60 0.07 24.38 \0.0001
Shape (unspecialized) -0.28 0.06 -4.53 \0.0001
Flower number -0.02 0.003 -9.63 \0.0001
Flowering duration -0.06 0.005 -12.93 \0.0001
Flower size 0.01 0.0003 17.91 \0.0001
Oecologia
123
visitation rate was not. Although flower number can be
correlated with seed set due to resource rather than polli-
nation limitation (Harder and Johnson 2009), this possi-
bility seems quite unlikely in this case, because the
relationship found is negative, whereas a higher number of
flowers should indicate more resources in the plant to set
the seeds. Instead, reduced seed set in species with larger
flower numbers at Finse may more likely be due to a
negative effect of increased geitonogamy (Brys and Jac-
quemyn 2010).
The results for flowering duration were complex. At
Ryghsetra, flowering duration was negatively related to
visitation rate, whereas it was positively related to seed set
in species with unspecialized flowers. These results agreed
with our expectations: while total visitation (across the
whole flowering period) and seed set may increase with
flowering duration (Dieringer 1991), visitation rate per
flower might decrease with flowering duration, since spe-
cies with low flower visitation rates may compensate with
long flowering periods or longer flower duration (Arroyo
et al. 1981; Blionis et al. 2001). For specialized species at
Ryghsetra, however, seed set decreased with flowering
duration; and the same occurred with both specialized and
unspecialized species at Finse. These unexpected rela-
tionships could appear if the species that bloom longer do it
partially during ‘inappropriate’ periods. Thus, it could be
Fig. 3 Relationships between
seed set at Ryghsetra and
a flower number, b flowering
duration, c pollinator
abundance, d conspecific flower
density and e heterospecific
flower density. Lines represent
the estimates of the best model
and the circles represent the
partial residuals of the model.
When there is a significant
interaction, the relationship is
shown for species with
unspecialized (empty circles,
dotted lines) and specialized
flowers (filled circles, solidlines)
Oecologia
123
that part of the flowering period of long-flowering spe-
cialized species at Ryghsetra does not overlap with the
phenological timing of their specific pollinators. In the case
of Finse, an early flowering period is known to increase the
probability of completing seed production before the onset
of winter (Totland 1993). Perhaps in this community the
longest flowering species begin setting part of their fruits
too late, when abiotic conditions are not adequate for fruit
and seed maturation. Future studies may confirm whether
this negative relationship is maintained over the years and/
or similar patterns are found in specialized flowers and in
other alpine communities.
Community context
Among-species variation in visitation rate and seed set was
related to the community context variables (conspecific and
heterospecific flower density and pollinator abundance)
only at Ryghsetra, the community with a higher pollinator-
to-flower ratio. We hypothesized that the community con-
text would have a stronger influence on visitation rate and
seed set in communities with a higher pollinator-to-flower
ratio compared to those with a lower pollinator-to-flower-
ratio. Pollinator foraging is determined by energetic
requirements (Stephens and Krebs 1986; Goulson 2003),
and when the pollinator-to-flower ratio is low there may be
low competition among pollinators for flowers (Alley
1982). Pollinators could then be choosier (Schmitt 1983)
and visit those flowers they prefer based on innate prefer-
ences and/or acquired experience (e.g. Chittka and Thom-
son 2001). On the contrary, when the pollinator-to-flower
ratio is high, competition among pollinators may modify the
reward levels and exploitation costs of otherwise preferred
plant species, and pollinators would not have the opportu-
nity to be so choosy (Schmitt 1983). As a result, insect
choices of plant species during foraging might be more
influenced by the scenario imposed by the plant-pollinator
community. Our results, showing a larger influence of
context variables on visitation rate and seed set at Ryghs-
etra, but not Finse, supported our hypothesis. However, our
correlative approach conducted in two communities has
important limitations. First, our failure to detect relation-
ships between the community context and seed set in the
alpine community could also be caused by strong resource
limitation that cancels out these relationships. However, we
find this possibility quite unlikely because significant rela-
tionships between floral traits and seed set are found at
Finse, and because flower density (included among the
community context variables) is one of the factors that can
strongly influence resource acquisition and therefore, seed
set. Second, the lack of replication of sites with high and
low pollinator-to-flower ratios does not allow us to form
strong conclusions about the importance of community
context for plant fitness in communities differing in polli-
nator-to-flower ratio. Although complex studies at the
community level are difficult to replicate in many localities,
the analysis of more communities is desirable to test whe-
ther the results presented here can be generalised.
Fig. 4 Relationships between seed set at Finse and a flower number,
b flowering duration and c flower size. The lines represent the
estimates of the best model and the circles represent the partial
residuals of the model
Oecologia
123
Seed set, but not visitation rate, increased with con-
specific flower density. Other studies have found seed set to
be positively related to conspecific density, through an
increase in the number of visits (Klinkhamer and de Jong
1990; Kunin 1993; Field et al. 2005; Makino et al. 2007)
and/or their quality (i.e. higher number of conspecific and
outcross pollen grains deposited on the stigmas; Jennersten
and Nilsson 1993; Kunin 1993; Bosch and Waser 1999;
Field et al. 2005) with density. Since we did not find any
relationship between conspecific density and visitation rate,
the relationship between conspecific density and seed set
may more likely be due to an increase in the amount of
available conspecific outcross pollen (Jennersten and
Nilsson 1993; Karron et al. 1995) in more abundant species
in this community.
Visitation rate and seed set were also related to the other
two variables describing the community context (hetero-
specific flower density and pollinator abundance) at Ry-
ghsetra. Visitation rate and seed set consistently increased
with pollinator abundance in species with both specialised
and generalised flowers. This was expected because the
higher the abundance of pollinators in the community at the
time a species flowers, the higher the chance a flower of
this species has of being visited and the higher the chance
of this species to set seeds. Lastly, heterospecific flower
density was negatively related to visitation rate in unspe-
cialized flowers, indicating inter-specific competition for
pollinator attraction when the density of co-flowering
species is high (Rathcke 1983). The species with special-
ized flowers were not affected by the heterospecific flower
density, perhaps because they have more loyal specific
pollinators (McCall and Primack 1992; Fenster et al. 2004).
Contrary to this, there was a positive relationship between
heterospecific flower density and seed set for species with
both specialized and unspecialized flowers. It is possible
that even though competition with other co-flowering
species decreased visitation rates, pollinators become
choosier when the resource is abundant (Schmitt 1983;
Lazaro et al. 2009, 2010), segregating their niches and
therefore increasing the quality of each visit (i.e. increasing
the amount of conspecific pollen deposited on the stigmas).
Future work will be needed to explore this idea.
Conclusion
In this study we have shown that the relationships between
floral traits and community context and visitation rate and
seed set, which are commonly found within species, also
exist among species. Moreover, in the community with the
lowest pollinator-to-flower ratio, species’ floral traits had
more influence on visitation rate and seed set than the
community context. We hypothesized a lower effect of
community context on plant fitness when the pollinator-to-
flower ratio is low, because when there is weak competition
between pollinators for flowers, insects might be choosier
as regards the plant species they visit (Schmitt 1983).
However, while our results support this hypothesis, the
inclusion of more communities in the analyses would be
needed to properly test it. The inter-specific relationships
between species’ traits and community context and the
fitness of species are still far from understood and their
study deserves further exploration. Experimental manipu-
lations would help to assess cause-effect relationships that
our correlative data do not allow us to ascertain. Also,
inclusion in the analyses of other species traits such as
capability of self-pollination and flower rewards, and
examination of the interactions that may exist between
predictor variables on visitation rate and seed set (Stanton
et al. 1991; Ohashi and Yahara 2002; Grindeland et al.
2005; Biernaskie and Gegear 2007), would help to improve
future studies on this subject.
Acknowledgments We thank Paul Aakerøy, Amparo Castillo,
Astrid Haavik, Manuel Hidalgo, Kristian Kyed, Rebekka Lundgren,
Kirsten Marthinsen, Anton Perez, Martın Piazzon, Anna Karina
Schmidt, Mari Steinert, Siril Stenerud, Jorum Vallestad, Hartvig
Velund, Silje Wang, Torstein Wilmot, and Magnus Øye for their
invaluable help in the field and the lab. We are also very grateful to
Asier R. Larrinaga and Martin Piazzon for their statistical advice and
to Amanda M. Dorsett for language editing. This study was supported
by the project 170532/V40 financed by the Norwegian Research
Council. During the writing of this manuscript A. L. was supported
by a Juan de la Cierva contract (Spanish Ministry of Economy and
Competitiveness). The sampling complies with the current laws of the
country (Norway) where it was performed.
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