The cobblers stick to their lasts: Pollinators prefer native over alien plant species in a
multi-species experiment
Biological Invasions
Thomas Chrobock*,#, Pius Winiger, Markus Fischer and Mark van Kleunen
*Corresponding author; Institute of Plant Sciences, University of Bern, Altenbergrain 21, CH
– 3013 Bern, Switzerland, email: thomas.chrobock@ips.unibe.ch, telephone +41 (0)31 631
4938, telefax +41 (0)31 631 4942
Present address: Carl Zeiss Naturzentrum Amrum, Strunwai 31, D – 25946 Norddorf auf
#
Amrum, Germany
Online Resource
Online Resource Table 1 List of plant species used in our study with their breeding systems according to the BiolFlor database
(http://www2.ufz.de/biolflor/index.jsp), and the five pollinator groups that we observed most frequently on them. The pollinator groups are given
in order of descending frequency. On five plant species, we observed fewer than five pollinator groups. The codes for the breeding systems are
X (allogamous), XF (facultative allogamous), AFXF (mixed mating) and AF (facultative autogamous).
Family
Origin and
status#
Breeding
system
Achillea millefolium§
Asteraceae
Native
X
Leucanthemum vulgare¶
Asteraceae
Native
AFXF
Asteraceae
Non-invasive
-
Other bees, hoverflies, other dipterans, flies, honey bees
Osteospermum sp. ¶
Asteraceae
Non-invasive
-
Hoverflies, other bees, flies, honey bees, wasps
Helianthus annuus¶
Asteraceae
Invasive
X
Beetles, hoverflies, honey bees, other bees, other dipterans
Asteraceae
Invasive
X
Other bees, hoverflies, honey bees, beetles, other dipterans
Campanula rotundifolia
Campanulaceae
Native
X
Other bees, hoverflies, flies, honey bees, other dipterans
Platycodon grandiflorum
Campanulaceae
Non-invasive
-
Honey bees, other bees, flies, other dipterans, hoverflies
Lobelia erinus
Campanulaceae
Invasive
-
Other bees, hoverflies, honey bees, other dipterans, other pollinators
Dianthus armeria
Caryophyllaceae
Native
AF
Dianthus caryophyllus
Caryophyllaceae
Non-invasive
X
Malva moschata
Malvaceae
Native
XF
Alcea rosea
Malvaceae
Non-invasive
AFXF
Other dipterans
Hibiscus trionum
Malvaceae
Invasive
AFXF
Honey bees, other bees, flies
Impatiens noli-tangere
Balsaminaceae
Native
XF
Impatiens balfourii
Balsaminaceae
Non-invasive
-
Impatiens glandulifera
Balsaminaceae
Invasive
XF
Species
Achillea
filipendulina§
Rudbeckia
hirta§
Pollinator groups
Other bees, hoverflies, beetles, other dipterans, honey bees
Hoverflies, other bees, beetles, other dipterans, flies
Other bees, hoverflies, flies, beetles, honey bees
Honey bees, other bees, beetles, butterflies, hoverflies
Flies, bumble bees, wasps, other dipterans
Hoverflies
Honey bees, other pollinators, wasps, other dipterans, beetles
Other bees, honey bees, wasps, hoverflies
Online Resource Table 2 Numbers of plants of each study species that we used in each of the six study locations.
Urbanized habitat
Species
Semi-natural habitat
Botanical Garden
City Nursery
Muri
Rüderswil
Heimiswil Walliswil
Achillea millefolium
Leucanthemum
vulgare
Achillea filipendulina
4
4
2
4
4
4
4
4
4
4
4
4
4
4
2
4
4
4
Osteospermum sp.
4
4
4
4
4
4
Helianthus annuus
4
4
2
4
4
4
Rudbeckia hirta
Campanula
rotundifolia
Platycodon
grandiflorum
Lobelia erinus
4
4
4
4
4
4
5
4
-
-
3
2
5
4
-
-
3
2
5
4
-
-
3
2
Dianthus armeria
5
4
3
4
4
4
Dianthus caryophyllus
5
4
3
4
4
4
Malva moschata
2
-
2
-
-
-
Alcea rosea
2
-
2
-
-
-
Hibiscus trionum
2
-
2
-
-
-
Impatiens noli-tangere
2
-
2
-
-
-
Impatiens balfourii
2
-
2
-
-
-
Impatiens glandulifera
2
-
2
-
-
-
Online Resource Table 3 Results of the statistical analyses of pollinator visitation per plant of native and related alien plant species (belonging
to Asteraceae, Campanulaceae and Caryophyllaceae) in urbanized and semi-natural habitats in Switzerland. Subscript numbers denote error
term used for calculating quasi-F- and p-values.
d.f.
Scaled log10(Number of flower units)6
Scaled flower unit diameter1
Family1
Origin1
Non-native status1
Species6
Habitat type2
Location5
Family × Habitat type3
Origin × Habitat type3
Non-native status × Habitat type3
Species × Habitat type6
Family × Location4
Origin × Location4
Non-native status × Location4
Species × Location6
Observation session6
Residuals
1
1
2
1
1
5
1
4
2
1
1
6
6
4
4
20
62
105
Number of pollinator
individuals
Number of pollinator
morpho-species
Number of taxonomic
pollinator groups
Mean
quasi-F
deviance†
30.463
11.124**#
21.018
0.795#
37.400
1.415
260.259
9.846*
24.838
0.940
26.434
9.653***
112.195
10.733*
10.453
3.527*
2.983
1.187
0.29
0.116
0.336
0.134
2.512
0.917
7.701
2.110
5.527
1.515
6.279
1.721
3.649
1.333
2.964
1.082
2.739
Mean
quasi-F
deviance†
14.092
12.169**#
14.608
1.721#
12.990
1.530
56.648
6.674*
3.739
0.441
8.488
7.330***
32.816
20.238*
1.622
1.385
1.697
1.385
1.056
0.726
1.191
0.819
1.454
1.256
2.760
2.382
1.844
1.591
1.923
2.659
1.159
1.001
1.171
1.011
1.158
Mean
deviance†
6.898
13.285
5.597
19.441
0.389
5.582
20.316
1.629
1.207
2.133
0.596
1.023
1.298
0.700
1.197
1.078
0.702
0.907
quasi-F
7.602*#
2.380#
1.003
3.483
0.070
6.152***
12.472*
2.321
1.180
2.085
0.583
1.127
1.204
0.649
1.111
1.188
0.774
Error terms: 1: Species; 2: Location; 3: Species × Habitat type; 4: Species × Location; 5: Observation session; 6: Residuals. #: covariables had a positive
effect on response variables. †: The proportion of variation explained by each factor can be estimated using the change in deviance (i.e. the mean deviance
multiplied by the d.f.) relative to the total deviance; d.f.: degrees of freedom, ***p<0.001, **0.001<p<0.01, *0.01<p<0.05
Online Resource Figure 1 Log10 (time a pollinator spent on a plant) observed within 30
minutes in urbanized and semi-natural habitats in Switzerland. Missing error bars indicate
species with pollinator visitation in only one of the observation periods in the respective
habitat type, shown are means ±1SE
Native
Urbanized habitat
Semi-natural habitat
Asteraceae
2.5
Campanulaceae
Introduced non-invasive
Introduced invasive
Caryophyllaceae
Malvaceae
Balsaminaceae
1.5
1
0.5
Impatiens glandulifera
Impatiens balfourii
Impatiens noli-tangere
Hibiscus trionum
Alcea rosea
Malva moschata
Dianthus caryophyllus
Dianthus armeria
Lobelia erinus
Platycodon grandiflorum
Campanula rotundifolia
Rudbeckia hirta
Helianthus annuus
Osteospermum sp.
Achillea filipendulina
Leucanthemum vulgare
0
Achillea millefolium
log10(Time a pollinator
spent on a plant)
2
Online Resource Table 4 Results of the statistical analysis of the time a pollinator spent on
native and related alien plant species (Asteraceae, Campanulaceae, Caryophyllaceae) in
urbanized and semi-natural habitats in Switzerland, per plant. Subscript numbers denote
error term used for calculating F- and p-values. Species without flower visitors were
excluded from these analyses.
log10(Time a pollinator spent on a plant)
Scaled(log10(Number of flower units))6
Scaled flower unit diameter1
Family1
Origin1
Non-native status1
Species6
Habitat type2
Location5
Family × Habitat type3
Origin × Habitat type3
Non-native status × Habitat type3
Species × Habitat type6
Family × Location4
Origin × Location4
Non-native status × Location4
Species × Location6
Observation session6
Residuals
d.f.
Mean squares
F
1
1
2
1
1
5
1
4
2
1
1
6
6
4
4
19
62
77
0.012
1.200
0.559
2.038
0.293
0.904
0.497
0.507
0.291
0.398
0.009
0.103
0.215
0.363
0.167
0.244
0.327
0.254
0.049#
1.328#
0.618
2.255
0.325
3.556*
0.979
1.552
2.815
3.857
0.091
0.406
0.880
1.489
0.683
0.959
1.286
Error terms: 1: Species; 2: Location; 3: Species × Habitat type; 4: Species × Location; 5: Observation
session; 6: Residuals. #: covariables had a positive effect on response variable. d.f.: degrees of
freedom, *0.01<p<0.05
Online Resource Table 5 Results of the statistical analyses of pollinator visitation per plant of native and related introduced plant
species (without Caryophyllaceae) in urbanized and semi-natural habitats in Switzerland. Subscript numbers denote error term
used for calculating quasi-F- and p-values.
Number of pollinator
individuals
d.f.
Scaled log10(Number of flower units)6
Scaled flower diameter1
Family1
Origin1
Non-native status1
Species6
Habitat type2
Location5
Family × Habitat type3
Origin × Habitat type3
Non-native status × Habitat type3
Species × Habitat type6
Family × Location4
Origin × Location4
Non-native status × Location4
Species × Location6
Observation session6
Residuals
1
1
3
1
1
8
1
4
1
1
1
5
4
4
4
20
48
95
Mean
deviance†
quasi-F
80.368
1.325
32.581
216.662
5.781
22.213
110.209
6.237
0.678
0.008
0.620
3.102
9.367
7.886
5.151
4.044
2.955
33.796***
0.060
1.467
9.754*
0.260
9.341***
17.669*
2.111
0.219
0.003
0.200
1.304
2.317
1.950
1.274
1.700*
1.242
2.378
Number of pollinator
morpho-species
Number of taxonomic
pollinator groups
Mean
quasi-F
deviance†
27.140 25.375***
5.634
0.790
15.174
2.128
45.581 6.392*
0.004
0.001
7.130 6.666***
28.975 20.167*
1.437
1.274
3.023
3.340
1.814
2.004
3.645
4.027
0.905
0.846
1.916
1.730
2.367
2.138
1.389
1.254
1.107
1.035
1.127
1.054
1.070
Mean
quasi-F
deviance†
14.616 17.700***
6.625
1.346
8.190
1.664
13.886
2.821
0.427
0.087
4.923 5.961***
21.005 20.329*
1.033
1.475
0.447
2.323
3.943 20.494**
2.754 14.314
0.192
0.233
1.154
1.047
1.299
1.177
0.740
0.671
1.103
1.336
0.700
0.848
0.826
Error terms: 1: Species; 2: Location; 3: Species × Habitat type; 4: Species × Location; 5: Observation session; 6: Residuals. #: covariables had a positive
effect on response variables. †: The proportion of variation explained by each factor can be estimated using the change in deviance (i.e. the mean deviance
multiplied by the d.f.) relative to the total deviance; d.f.: degrees of freedom, ***p<0.001, **0.001<p<0.01, *0.01<p<05.
Online Resource Table 6 Results of the statistical analysis of the time a pollinator spent on
native and related introduced plant species (without Caryophyllaceae) in urbanized and
semi-natural habitats in Switzerland, per plant. Subscript numbers denote error term used for
calculating F- and p-values. Species without flower visitors were excluded from these
analyses.
log10(Time a pollinator spent on a plant)
Scaled(log10(Number of flower units))6
Scaled flower diameter1
Family1
Origin1
Non-native status1
Species6
Habitat type2
Location5
Family × Habitat type3
Origin × Habitat type3
Non-native status × Habitat type3
Species × Habitat type6
Family × Location4
Origin × Location4
Non-native status × Location4
Species × Location6
Observation session6
Residuals
d.f.
Mean squares
F
1
1
3
1
1
8
1
4
1
1
1
5
4
4
4
17
48
68
0.668
0.735
1.432
1.708
0.726
0.702
0.287
0.593
0.543
0.212
0.037
0.115
0.277
0.144
0.083
0.283
0.313
0.256
2.604
1.047
2.040
2.432
1.034
2.737*
0.484
1.899
4.721
1.843
0.318
0.448
0.978
0.510
0.294
1.104
1.219
Error terms: 1: Species; 2: Location; 3: Species × Habitat type; 4: Species × Location; 5: Observation
session; 6: Residuals. #: covariables had a positive effect on response variable. d.f.: degrees of
freedom, *0.01<p<0.05
Online Resource Test for differences in pollinator-community composition
To test whether the composition of the pollinator community differed among native, invasive
alien and non-invasive alien species, and between urbanized and semi-natural habitat types,
we used non-metric multidimensional scaling (NMDS) and permutational multivariate
analysis of variance (PERMANOVA), as implemented in the vegan package (Oksanen et al.
2011) of the statistical software R (R Development Core Team 2009). For both the NMDS
analysis (Vegan function metaMDS) and the PERMANOVA (Vegan function adonis), we first
calculated a Gower dissimilarity matrix based on a matrix containing the number of visits by
each group of pollinators (honeybees, bumblebees, other bees, hover flies, flies, wasps,
other dipterans, butterflies, beetles, and other pollinators) to each of the 252 individuals
plants in our study. For the NMDS analysis, we set the number of axes equal to three, as
increasing the number of axes did not greatly reduce the stress value, and we set the
maximum number of random starts equal to 50. The final stress value was 0.142. To assess
whether the NMDS values differed consistently among the three groups of species and
between the two habitat types, we used linear models. For the PERMANOVA, the P-values
were based on 999 permutations. Because the three groups of species and the two habitat
types were repeated for each of the plant families, data permutations were done within
families. In this analysis, it was not possible to include interactions of family with the other
factors.
Visual inspection of the NMDS plots (Appendix Figure 1) reveals that there was more
spread in the NMDS values among species when the observations were done in urbanized
(open symbols) instead of semi-natural habitats (closed symbols). Similarly, at least in the
plot of NMDS2 vs NMDS3, the alien species (triangles) showed more spread in NMDS
values than the native species (circles). Although the analyses of the NMDS values revealed
significant effects of the number of flower unites on NMDS values, variation among species
and variation among locations, these analyses did not reveal significant differences among
the native, invasive alien and non-invasive alien species, and also not between the urbanized
and semi-natural habitat types (Appendix Table 6).
The PERMANOVA, however, revealed significant differences in pollinator-group composition
between native and alien species, irrespective of whether the latter are invasive or noninvasive, and between the urbanized and semi-natural habitat types (Appendix Table 7).
Inspection of the NMDS plots (Appendix Figure 1) suggest that these differences in
pollinator-community composition mainly reflect higher frequencies of other bees, hover flies,
flies and beetles on native than on alien species, and in semi-natural than in urbanized
habitats.
References
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL,
Solymos P, Stevens MHH, Wagner H (2011) Vegan: Community Ecology Package. R
package version 2.0-0. http://CRAN.R-project.org/package=vegan
R Development Core Team (2009) R: A language and environment for statistical computing.
R Foundation for Statistical Computing, Vienna, Austria.
Online Resource Figure 2 The three non-metric multidimensional scaling (NMDS) axes
derived from a Gower-dissimilarity matrix of differences in composition of the pollinator
groups visiting the plants in our study. The NMDS analysis was based on a pollinatorvisitation matrix including all 252 individual plants in our study. However, for clarity we only
present average NMDS values per status group (circles: native species, upward triangles:
invasive alien species, downward triangles: non-invasive alien species) for each of the five
plant families (black: Asteraceae, blue: Campanulaceae, green: Malvaceae, pink:
Caryophyllaceae, red: Balsaminaceae) separately for the two habitat types (open symbols:
urbanized habitats, closed symbols: semi-natural habitats). We also plotted the positions of
the different pollinator groups in the plots.
0.2
0.2
Hover flies
NMDS 3
Other bees
Honey bees
Beetles
Wasps
Beetles
Wasps
Flies
0.0
Other pollinators
0.1
Bumble bees
0.1
NMDS 2
Butterflies
Other bees
0.0
Flies
Hover flies
Butterflies
Other dipterans
-0.1
-0.1
Other dipterans
Other pollinators
-0.2
-0.2
-0.1
0.1
0.2
0.2
Butterflies
0.1
Wasps
NMDS 3
Beetles
Other bees
Flies
0.0
Hover flies
Other dipterans
-0.1
Honey bees
-0.2
-0.2
-0.1
0.0
NMDS 2
-0.2
-0.1
0.0
NMDS 1
NMDS 1
Other pollinators
Honey bees
-0.2
0.0
0.1
0.2
0.1
0.2
Online Resource Table 7 Results of the statistical analyses of NMDS (non-metric
multidimensional scaling) values of individual plants of related native and alien plant species
in urbanized and semi-natural habitats in Switzerland. Subscript numbers denote error term
used for calculating F- and p-values.
NMDS1
NMDS2
NMDS3
Scaled log10(Number of flower units)6
d.f.
MS
F
1
0.09239 11.11**
MS
F
0.00319 0.47
MS
F
0.05103 9.01**
Scaled flower unit diameter1
1
0.06704 2.71
0.05258 3.59
0.05059 5.81**
Family1
4
0.038
1.54
0.01234 0.84
0.00342 0.39
Origin1
1
0.00135 0.05
0.00882 0.60
0.00009 0.01
Non-native status1
1
0.0072
0.00105 0.07
0.00052 0.06
Species6
9
0.02475 2.98**
0.01468 2.14*
0.00871 1.54
Habitat type2
1
0.03467 1.19
0.00003 0.00
0.02498 3.01
Location5
4
0.02918 2.62*
0.03255 3.28*
0.00829 1.22
Family × Habitat type3
2
0.0032
0.00012 0.01
0.00767 0.88
Origin × Habitat type3
1
0.00018 0.045
0.00120 0.10
0.00104 0.12
Non-native status × Habitat type3
1
0.01389 3.51
0.00081 0.07
0.01840 2.11
Species × Habitat type6
6
0.00396 0.48
0.01182 1.73
0.00872 1.54
Family × Location4
8
0.01121 0.96
0.00781 0.64
0.00842 0.68
Origin × Location4
4
0.00471 0.40
0.00652 0.54
0.00451 0.37
Non-native status × Location4
4
0.00418 0.36
0.00526 0.43
0.01118 0.91
Species × Location6
24
0.01165 1.40
0.01216 1.78*
0.01234 2.18**
Observation session6
66
0.01115 1.34
0.00992 1.45*
0.00679 1.20
Residuals
113 0.00831
0.00684
0.00566
0.29
0.81
Error terms: 1: Species; 2: Location; 3: Species × Habitat type; 4: Species × Location; 5: Observation
session; 6: Residuals. d.f.: degrees of freedom, **0.001<p<0.01, *0.01<p<0.05
Online Resource Table 8 Results of a PERMANOVA (permutational multivariate analysis of
variance) on the matrix of plant individuals and pollinator groups to test for differences in
composition of the pollinator-group community on native, invasive alien and non-invasive
alien species in urbanized and semi-natural habitats. Interactions of family with other factors
could not be included in the model. P-values are based on 999 permutations.
R2
p-value
0.00691 1.69
0.00512
0.260
1
0.00060 0.15
0.00045
0.950
Family
4
0.01835 4.48
0.05446
0.001***
Origin
1
0.02815 6.88
0.02088
0.001***
Non-native status
1
0.00704 1.72
0.00522
0.211
Species
9
0.01052 2.57
0.07023
0.001***
Habitat type
1
0.02951 7.21
0.02189
0.001***
Location
4
0.00753 1.84
0.02233
0.022*
Observation session
82
0.00532 1.30
0.32342
0.002**
Origin × Habitat type
1
0.00902 2.20
0.00669
0.056
Non-native status × Habitat type
1
0.00352 0.86
0.00261
0.546
Species × Habitat type
5
0.00623 1.52
0.02311
0.065
Origin × Location
4
0.01096 2.68
0.03251
0.002**
Non-native status × Location
4
0.00451 1.10
0.01340
0.431
Species × Location
19
0.00387 0.94
0.05450
0.543
Residuals
113
0.00409
0.34319
d.f.
MS
Scaled log10(Number of flower units)
1
Scaled flower unit diameter
***p<0.001, **0.001<p<0.01, *0.01<p<0.05
F