Garden Plants Attractiveness To Bees

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Functional Ecology 2013 doi: 10.1111/1365-2435.

12178

Quantifying variation among garden plants in


attractiveness to bees and other flower-visiting insects
Mihail Garbuzov* and Francis L. W. Ratnieks
Laboratory of Apiculture & Social Insects, School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG,
UK

Summary
1. Pollinating insects are globally declining, with one of the main causes being the loss of flow-
ers. With the value of countryside reducing, urban areas, particularly gardens, are increasingly
recognized as of benefit to wildlife, including flower-visiting insects.
2. Many gardeners specifically select plant varieties attractive to wildlife. Given the wide public
interest, many lists of recommended varieties have been produced by both amateurs and
professional organizations, but appear not to be well grounded in empirical data. These lists,
however, are not without merit and are an obvious starting point. There is clearly a need to
put the process onto a firmer footing based more on data and less on opinion and general
experience.
3. We collected data over two summers by counting flower-visiting insects as they foraged on
32 popular summer-flowering garden plant varieties in a specially planted experimental garden,
with two smaller additional gardens set up in year two to check the generality of the results.
With many thousands of plant varieties available to gardeners in the United Kingdom, and
other countries or regions, it would have been an impossible task to make a comprehensive
survey resulting in a complete and authoritative list.
4. Our results are valuable and encouraging. Garden flowers attractive to the human eye vary
enormously, approximately 100-fold, in their attractiveness to insects. Insects, especially bees
and hover flies, can be attracted in large numbers with clear differences in the distribution of
types attracted by different varieties.
5. Our results clearly show that there is a great scope for making gardens and parks more bee-
and insect-friendly by plant selection. Horticulturally modified plant varieties created by plant
breeding, including hybrids, are not necessarily less attractive to insects and in some cases are
more attractive than their wild-type counterparts. Importantly, all the plants we compared
were considered highly attractive to humans, given that they are widely sold as ornamental
garden plants.
6. Helping insect pollinators in gardens does not involve extra cost or gardening effort, or loss
of aesthetic attractiveness. Furthermore, the methods of quantifying insect-friendliness of plant
varieties trialled in this study are relatively simple and can form the basis of further research,
including ‘citizen science’.

Key-words: bumblebees, butterflies, conservation, honeybees, hover flies, ornamental plants,


pollinators, urban ecology, wildlife friendly gardening

such as development and agricultural intensification, which


Introduction
lead to habitat loss and degradation (Goulson et al. 2005;
Global biodiversity is in decline (Barnosky et al. 2011). Biesmeijer et al. 2006; Potts et al. 2010). With the wildlife
Pollinating insects are no exception, with the main factor value of the countryside reducing, the value of urban areas
being loss of flowers, driven primarily by human activities, is increasingly being recognized (Frankie & Ehler 1978;
Cane 2005; Dearborn & Kark 2010; Sanderson & Huron
*Correspondence author. E-mail: [email protected] 2011). High species diversity has been recorded in urban

© 2013 The Authors. © 2013 British Ecological Society


2 M. Garbuzov & F. L. W. Ratnieks

green spaces, such as parks and gardens (Helden & authoritative list. What our data do show, however, is
Leather 2004; Matteson, Ascher & Langellotto 2008; Owen valuable and encouraging. Garden flowers attractive to the
2010), with private gardens often being the largest and human eye vary enormously, approximately 100-fold, in
probably the most important component (Goddard, Dougill their attractiveness to insects. This shows that plant selec-
& Benton 2010). In the United Kingdom, 87% of house- tion can make a great difference in the value of gardens
holds are associated with a garden (Davies et al. 2009) and and parks to flower-visiting insects, and at no additional
gardening is a popular hobby (Taylor 2002). In addition, cost. Insects, and especially bees, can be attracted in large
many gardeners are supportive of wildlife, with most UK numbers with clear differences in the distribution of types
gardeners (74–78%) engaging in some form of ‘wildlife attracted by different garden plant varieties.
gardening’. That is, doing something to attract or encour-
age wildlife (Good 2000), including the 31% who select
plants attractive to wildlife or the 66% who feed birds in Materials and methods
their garden (Mew et al. 2003; DEFRA 2007).
Garden plants are often non-native, and this may reduce EXPERIMENTAL PLANT VARIETIES AND FLOWER BEDS
their usefulness to some wildlife. For example, many We studied 32 garden plant varieties that include 19 species and
herbivorous insects have a narrow range of suitable food hybrids, both native and exotic to Britain, with particular focus
plants (Novotny & Basset 2005; Dyer et al. 2007). How- on varieties of lavender (Lavandula spp.), as it is known to be
ever, this does not prevent them from being useful to attractive to bees (Pawelek et al. 2009; for full list see Table S1,
Supporting information). Varieties were selected based on the
flower-visiting insects seeking nectar and pollen, as these
following three criteria: they were (i) popular as garden plants in
are general resources. Nectar, for example, is mainly sugar their own right due to their attractive flowers or foliage (e.g.
and water (Nicolson & Thornburg 2007), and so it is Lamb’s ear, Stachys byzantina), (ii) widely and easily available for
edible whether from a native or a non-native plant. Many purchase and (iii) flowered mainly or exclusively in late summer,
garden plants have also been bred to alter their appear- July and August, as these are the months when honeybee foraging
distances in the same area are greatest (M.J. Couvillon, R.
ance, such as by the ‘doubling’ of petals, which may reduce
Sch€urch & F.L.W. Ratnieks, unpublished data), indicating chal-
floral rewards or their accessibility (Comba et al. 1999; lenging foraging conditions and, therefore, the period when gar-
Corbet et al. 2001). den flowers can be particularly beneficial to flower-visiting insects.
Given the public interest in helping wildlife, a large The main experimental flower bed was on the University of
number of recommended plant lists have been produced, Sussex campus (lat: 50865646, long: 0090771943) on chalky soil
of the South Downs. All 32 varieties were planted in 1 9 1 m
by both amateurs (e.g. Baines (2000); Lavelle & Lavelle
patches, two patches per variety, in two concentric circles (inner
(2007)) and professional organizations (e.g. Royal Horti- diameter 122 m, outer 192 m), with one variety per circle in a
cultural Society (2011); Xerces Society (2011)). However, random position (Fig. 1). There were gaps of c. 05 m (inner) and
these appear not to be well grounded in empirical data. 10 m (outer) between adjacent patches within the same circle and
For example, Thompson (2006) referred to one list of wild- 15 m between the circles. This arrangement was chosen to elimi-
nate any edge effects, which might have affected insect visitation.
life friendly plants produced by Natural England, a
Data were collected in both 2011 and 2012.
government-funded agency responsible for protection and Additionally, to ensure our results were not location specific, for
improvement of the natural environment, as ‘looks very example, due to local soil conditions or insect abundance, 13 of the
much as if it was put together late one Friday afternoon’. 32 varieties (Table S1) were planted at two additional locations in
In addition, lists of bee- and butterfly-friendly plants vary 2012. This subset was chosen to confirm certain notable trends seen
in the data at the end of the first season (2011). For example, Bora-
greatly even when they are for the same country, suggest-
go was mostly visited by honeybees, while Lavandula mostly by
ing that the underlying information is based mainly on bumblebees. L. 9 intermedia received more insect visits than
personal observations, experience, opinion and, perhaps, L. angustifolia, while sharp colour contrast (traditional blue/purple
uncritical recycling of earlier lists (M. Garbuzov & F.L.W. vs. white) had no effect on the number of visits. Open-flowered
Ratnieks, unpublished data). Dahlia varieties were more attractive than those with more modi-
fied flower forms. Origanum and Stachys seemed to have dispro-
Lists of bee- and butterfly-friendly plants are not with-
portionately large numbers of visits by ‘other’ wild bees, while
out merit and are an obvious starting point for determin- Erysimum was most attractive for butterflies and moths. One loca-
ing which plants are good for flower-visiting insects. tion was 45 km away at Plumpton College (lat: 50905665, long:
However, there is a need to put the process onto a firmer 0074753791) where the soil is also chalky, and the other 263 km
footing based more on data and less on opinion and gen- away in FR’s private garden in Magham Down (lat: 50880426,
long: 028488247), where the soil is sandy. Only one 1 9 1 m patch
eral experience. This study is an attempt to do this. We
per variety was planted, and the patches were arranged in a line
collected data over two summers in which flower-visiting with 30 cm gaps.
insects were counted as they foraged on 32 popular garden Perennials were bought in pots from nurseries and garden
plant varieties in a specially planted experimental garden. centres and planted in June 2011 (University of Sussex) and May-
In addition, two smaller gardens were set up in year two June 2012 (Plumpton College & Magham Down). Borage (Borago
officinalis), which is an annual, was sown in May each year to
to check the generality of the results. With many thou-
give peak flowering in July–August. Viper’s bugloss (Echium
sands of plant varieties available to gardeners in the Uni- vulgare) is a biennial, flowering in the second year of its life cycle.
ted Kingdom, it would have been an impossible task to However, we were able to induce flowering in the first year
make a comprehensive survey resulting in a complete and by keeping young seedlings in a greenhouse at 24:0 light/dark

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Garden plants for flower-visiting insects 3

32
On each day of data collection, the bloom intensity of patches
N 27
17 7
16
(a) was quantified by assigning a score 0 (absence of bloom), 1 (<⅓ of
22 23
maximum), 2 (⅓–⅔ of maximum) or 3 (full bloom, >⅔ of maxi-
26 9 12 22 21
2 30
4
mum; after Anderson & Hubricht 1940) and included as a
1
1 9 covariate in the analyses. In addition, as corolla length is known
14 28

13 10 29 11 to influence the type of flower-visitors and their ability to gather


3 21 nectar (e.g. Balfour, Garbuzov & Ratnieks 2013), it was estimated
31 3
5 26 in each variety by measuring 20 non-systematically selected flow-
8 16 7 25 ers (10 from each patch at bloom intensity 2 or 3) to the nearest
13 6 01 mm using digital callipers.
24 4
23 8
14 20 32 19

31 24 RECORDING INSECT FLOWER-VISITORS


29 12
25 11
27 19
30 18 17 15 2 In the main flower bed at the University of Sussex, insects visiting
10 5 the flowers were counted on 13 days from 14 July to 7 October
15 18
6 20 3m 2011 and 12 days from 29 June to 18 September 2012. Counts
28
were made only on days with favourable weather. That is, based
(b) on our experience, the combination of sunlight, temperature and
5: Dahlia wind was such as to allow all insect categories to be active. Counts
6: Dahlia ‘Bishop of Llandaff’ were made at approximately weekly intervals throughout the main
8: Dahlia
‘Bishop of Oxford’ flowering period of most plant varieties (Fig. S1). In addition,
‘Tahiti Sunrise’
insects were recorded on 6 days from 18 August to 18 September
2012 at Plumpton College and on 8 days from 9 August to 10
September 2012 at Magham Down.
24: Lavandula The number of insect flower-visitors on each patch was quanti-
26: Monarda ‘Sussex’
32: Stachys fied using ‘snapshot’ counts, in which the number of foraging
insects was determined near instantaneously (<10 s) by eye. This
21: Lavandula ‘Grosso’ ‘snapshot’ method was chosen over other possible methods, such
as counting the number of insects arriving at a patch in a defined
time interval, as it is quick to implement and therefore practical
for assessing many patches. In the main flower bed at the Univer-
29: Pelargonium sity of Sussex, one snapshot was taken from each patch at hourly
intervals between 9:30 and 16:30 BST, yielding eight snapshots per
patch per day. In the two additional flower beds, 10 snapshots per
Fig. 1. (a) Schematic layout of the experimental flower garden on patch were taken per day, typically during a c. 2-h period. As
the University of Sussex campus, showing the two concentric insects generally remained on the same patch for only a few min-
circles, each consisting of 32 1 9 1 m flower patches. Numbers utes during a foraging trip, the 60-min intervals between snapshots
correspond to the varieties, as listed in Table S1. (b) Photograph meant that the same insect was unlikely to have been counted
showing a section of the inner circle, taken in August 2011 when twice on the same patch visit. Thus, the data represent indepen-
most varieties were in full bloom. dent foraging choice decisions even though individual insects may
make multiple visits to the same patch. Even when multiple visits
by the same insect to the same patch do occur, this shows a real
photoperiod for 8 weeks before transplanting them to patches in preference rather than the mere persistence of the same insect at
the flower bed. The non-hardy anise hyssop (Agastache foenicu- the same patch during a single patch visit.
lum) and geranium (Pelargonium 9 hortorum) were dug out at the The insects counted in the snapshots were identified and
end of 2011 season, overwintered in a heated greenhouse and grouped to taxa as follows: (1) honeybees (A. mellifera L.), (2)
replanted in May 2012. The four Dahlia varieties, which are also two-banded white-tailed bumblebees (Bombus terrestris/lucorum
non-hardy, were grown from tubers in a greenhouse starting in group, after Fussell & Corbet (1992)), (3) three-banded white-
March each year and planted out 8 weeks later. Prior to planting, tailed bumblebees (Bombus hortorum group), (4) brown bumble-
all patches were fertilized with multipurpose organic fertilizer bees (Bombus pascuorum group), (5) other bumblebees, (6) other
(Fish, Blood & Bone, Sinclair) and controlled release fertilizer bees (non-Apis and non-Bombus), (7) hover flies (Diptera: Syrphi-
(Sincrocell 9, Sinclair). Table S1 gives the suppliers of each plant dae), (8) butterflies and moths (Lepidoptera) and (9) all other
variety. insects. Additionally, Lepidoptera (group 8) were identified to spe-
cies, other bees (groups 5, 6) and other insects (group 9) to species
or other taxonomic ranks, as appropriate. However, they were
PLANT AND PATCH CHARACTERISTICS grouped in analyses due to the low numbers of individual species
or subgroups in the data sets (Table 1, Fig. 2). The levels of iden-
In each patch, an appropriate number of plants were planted tification used were appropriate given the counting method, in
according to their size (Table S1) such that the patch was nearly which insects were identified as they foraged and were not
fully covered, but allowing for some further growth. Plants were collected. In practice, this meant that most insects (87–92% per
trimmed as necessary to ensure that they did not overgrow the data set) other than flies, Diptera, were identified to species or to
patch perimeter. In some cases, slow growth or plant death (only groups of species that could easily be separated in the field (e.g.
in E. vulgare at the University of Sussex) resulted in patches that the different bumblebee subgroups). These taxonomic groups also
were not covered completely. To allow for <100% plant cover, on reflect functional insect groups in relation to flower morphology.
each day of data collection, patches were photographed from For example, short- (honeybees) and long-tongued (bumblebees)
above to determine plant cover using ImageJ 1.45s software eusocial bees, solitary bees, very long-tongued Lepidoptera and
(National Institute of Health, USA). short-tongued hover flies.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
4 M. Garbuzov & F. L. W. Ratnieks

Table 1. Breakdown of main insect groups that were grouped together in the analyses

University of University of Plumpton College Magham Down


Common name Sussex 2011 (%) Sussex 2012 (%) 2012 (%) 2012 (%)

Other Bombus groups


Black-bodied red tails 12 20 – 45
Banded red tails 84 78 100 7
Unidentified 4 2 – 48
Other bees
Anthidium manicatum Wool-carder bee Not identified 95 100 100
Unidentified Not identified 5 – –
Lepidoptera
Butterflies
Aglais urticae Small tortoiseshell 3 10 – 38
Aphantopus hyperantus Ringlet – 1 – –
Gonepteryx rhamni Brimstone – 1 – –
Inachis io Peacock – 1 – –
Lycaena phlaeas Small copper – 1 – –
Maniola jurtina Meadow brown 22 62 71 52
Ochlodes sylvanus Large skipper 2 – –
Pieris brassicae Large white 3 1 – 5
Pieris rapae Small white 34 4 29 –
Polygonia c-album Comma 3 – – –
Polyommatus coridon Chalkhill blue 2 – – –
Polyommatus icarus Common blue – 9 – –
Pyronia tithonus Gatekeeper – 1 – –
Thymelicus sylvestris Small skipper 2 4 – –
Vanessa atalanta Red admiral 3 1 – –
Vanessa cardui Painted lady 2 – – –
Moths
Autographa gamma Silver Y – 1 – 5
Macroglossum stellatarum Hummingbird hawk-moth 22 – – –
Pyrausta aurata Mint moth – 2 – –
Zygaena spp. Burnet moths – 1 – –
Other insects
Coleoptera Beetles 20 95 11 4
Diptera True flies 63 90 89 92
Vespula spp. Yellowjacket wasps 17 05 – 4

Bombus subgroups follow Fussell & Corbet (1992). For the relative abundance of groups see Figs 2 and S2.

The significance of terms was determined using F-tests on a full


STATISTICAL ANALYSES
model, which is appropriate, because the main aim was to ana-
The number of insects per snapshot was divided by plant area lyse the significance of terms, rather than to use the models pre-
cover to form the response variable in the analyses. This is justi- dictively (Whittingham et al. 2006). Post hoc pairwise
fiable, because the number of insects per snapshot is linearly comparisons of plant varieties were performed using Tukey’s
related to the area (M. Garbuzov, A. Madsen & F.L.W. Rat- HSD test [function glht, package multcomp (Hothorn, Bretz &
nieks, unpublished data). All statistical analyses were performed Westfall 2008)].
in R v.3.0.0 (R Development Core Team 2013). Prior to analy- Consistency among data sets was tested using Spearman’s rank
ses, the data were explored as advised by Zuur, Ieno & Elphick correlation test. This is more appropriate than a parametric corre-
(2010). General linear models [GLMs; function gls, package nlme lation test, because consistency in rank is both more conservative
(Pinheiro et al. 2012)] were used to examine the relationships and more relevant to the underlying aim of the study than consis-
between the response variable, plant variety, bloom intensity and tency in the absolute numbers of insects attracted, which may vary
mean corolla length as main fixed effects. No interactions were among years and locations. All other relationships (in the attrac-
modelled, as they were not part of the a priori hypotheses to be tiveness of plant varieties among different insect flower-visitor
investigated. The data set was ‘collapsed’ by averaging out across groups) were tested using Pearson’s correlation test (function
the two patches of each plant variety, and also within each day, cor.test for all correlation tests).
by taking daily means. Further, to account for temporal autocor-
relation within the data recorded at approximately weekly inter-
vals across the season, the AR-1 correlation structure was added Results
to the models (Zuur et al. 2009). One model was fitted for each
insect group in both the 2011 and 2012 University of Sussex data
ATTRACTIVENESS OF PLANT VARIETIES TO INSECT
sets. The significance of P-values was judged against the Bonfer-
roni-corrected a-level (005 divided by the number of models per FLOWER-VISITORS
data set). As plant variety and mean corolla tube length were
highly correlated (i.e. each variety had a different mean length),
The relative abundance of insect groups at the University
only one of these variables was included in a model at a time. of Sussex is shown in Fig. 2. Across the 2 years, over

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Garden plants for flower-visiting insects 5

(a) 2011 CONSISTENCY AMONG YEARS AND LOCATIONS

7% 1% 1% The relative abundance of insect groups and plant variety


3%
26% attractiveness at Plumpton College and Magham Down in
3%
2012 (Fig. S2) were similar to those recorded at the Uni-
versity of Sussex in both years. In addition, the mean num-
ber of insects per snapshot per m2 recorded on different
18%
varieties at the University of Sussex correlated highly
between 2011 and 2012 (Spearman’s correlation:
rs = 0754, S = 134362, P < 0001, Fig. 4a). The numbers
1%
of insects per variety recorded at the University of Sussex
in 2012 were also significantly related to those recorded at
40% both Plumpton College (rs = 0650, S = 12735, P = 0016,
Fig. 4b) and Magham Down (rs = 0791, S = 7600,
(b) 2012 P = 0002, Fig. 4b) flower beds. This suggests that the
3% 3%
results are general, rather than being year or location
10%
specific.

32%
5% COMPARISON OF LAVENDER VARIETIES

4% Closer examination of lavender varieties showed that (i)


not all varieties were equally attractive (GLM:
F12,13 = 975, P < 0001) and (ii) L. 9 intermedia as a
14% group (mean  SE = 291  031 insects snapshot 1 m 2)
were more attractive than both the L. angustifolia
4% group (mean  SE = 088  009 insects snapshot 1 m 2)
25%
and L. stoechas (mean  SE = 066  054 insects snap-
Honeybees 2-banded bumblebees shot 1 m 2; F1,20 = 3486, P < 0001; Fig. 5a). However,
3-banded bumblebees Brown bumblebees the number of insects attracted was not affected by either
Other bumblebees Other bees total bloom duration (F1,20 = 352, P = 0075; Fig. 5b) or
Hover flies Butterflies & moths corolla tube length (F1,20 = 00004, P = 0985).
Other insects Honeybees and bumblebees together comprised the
majority (mean 90%, range 73–97%) of flower-visitors on
Fig. 2. Relative abundance of insects in nine main groups
recorded in the 2 years at the University of Sussex in 2011 (a) and Lavandula varieties. The number of honeybees, as a propor-
2012 (b). More detailed taxonomic breakdowns of other bumble- tion of honeybees and bumblebees together, varied consid-
bees, other bees, butterflies & moths, and other insects are given erably among varieties (range 11–55%). However, this was
in Table 1. not consistent between 2011 and 2012 (r = 0290,
P = 0337) and did not correlate with corolla tube length in
2011 (r = 0199, P = 0515), 2012 (r = 0202, P = 0508)
84% of insects recorded were bees, comprising 47–62% or the mean of 2011 and 2012 (r = 0094, P = 0759).
Bombus spp., 26–32% A. mellifera and 3–5% other bee
species. Hover flies were 7–10%, butterflies and moths
CORRELATIONS OF PLANT VARIETY PREFERENCE
1–3% and other insects 1–3%. Further taxonomic break-
AMONG INSECT GROUPS
downs of these groups are given in Table 1. The mean
number of insects per snapshot per m2 was significantly There was no significant correlation between the number of
affected by plant variety in most main insect groups honeybees and bumblebees per snapshot per m2 among the
(Table S2). Bloom intensity (covariate) was also signifi- 32 varieties (r = 0257, P = 0155; Fig. 6a), suggesting that
cant in most models (Table S2). The length of flower their preferences do not, generally, coincide. However,
corolla tube was a significant predictor in only a few visitation by short-tongued bumblebees (B. terrestris/
models (Table S2). However, the slope estimates of rela- lucorum group) correlated significantly with visitation by
tionships were close to zero (001–004), making these long-tongued bumblebees (B. hortorum and B. pascuorum
relationships of little importance. The results of post hoc groups; r = 0565, P < 0001; Fig. 6b). We then looked at
Tukey’s HSD tests comparing plant varieties are shown correlations in preference between both honeybees and
in Fig. 3. Due to the very large numbers of pairwise bumblebees vs. other bee species, hover flies and butterflies
comparisons, the test had low power to differentiate and moths and found only one of these correlations to
between varieties. Nevertheless, it was sufficient to reveal be significant (bumblebees vs. butterflies & moths (r =
the broad picture. 0665s, P < 0001); Fig. 7c). All other correlations were

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
6 M. Garbuzov & F. L. W. Ratnieks

Honeybees 2-banded bumblebees 3-banded bumblebees


Brown bumblebees Other bumblebees Other bees
Hover flies Butterflies & moths Other insects
a (a) 2011
b b b b b b b b b b
Daily mean insects per snapshot per m 2

8 c c c
d d d d
7 e e e e e e e
6 f f
g g g
5 h h h h h h
4 i i i
j j j j j j j j
3 k k k k
2 l l l l l l l l l l l
m m m m m m m m m m m m m m m
1
0

a a a a a (b) 2012
b b b b b b
Daily mean insects per snapshot per m 2

8
c c c c c c c c c
7 d d d d
e e
6
f f f f f f f f f f f f f f f f f f f f f f
5 g g g g g g g g g g g g g g g g g g g g g g
h h h h h
4
3
2
1
0

Fig. 3. Daily mean numbers of insects per snapshot per 1 9 1 m patch recorded on 32 garden plant varieties at the University of Sussex
in 2011 (a) and 2012 (b), Letters above bars represent significant differences based on Tukey’s HSD test, where varieties sharing a common
letter are not significantly different from each other at a = 005. Full plant names are given in Table S1.

non-significant [honeybees vs. other bees (r = 0169, the 32 plant varieties at the University of Sussex in the
P = 0354), honeybees vs. hover flies (r = 0251, P = 0165), total number of insects attracted. This clearly shows that
honeybees vs. butterflies & moths (r = 0157, P = 0390), there is great scope for making gardens and parks more
bumblebees vs. other bees (r = 0077, P = 0675), bumble- bee- and insect-friendly by judicious plant selection.
bees vs. hover flies (r = 0266, P = 0141)] (Fig. 7a–c). The Importantly, this need not involve extra cost or gardening
significant correlations (Figs 6b and 7c) remained signifi- effort, or, indeed, a loss of aesthetic attractiveness, given
cant after Bonferroni correction (a = 005/8). that all the plants we compared were considered to be
highly attractive, and were easily available at comparable
and low prices. Our results can be considered as a contri-
Discussion
bution to the lists of recommended garden plants.
The results showed very large, approximately 100-fold However, this should be done with caution, as we only
(c. 300-fold in 2011, c. 80-fold in 2012), variation among compared 32 varieties, which is a very small proportion of

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Garden plants for flower-visiting insects 7

(a) attractiveness, it cannot be a major factor, because the rel-


m2 at the University of Sussex flower bed in
8
Mean number of insects per snapshot per P < 0·001
rs = 0·754 ative abundances of different taxa were broadly very simi-
lar among years and locations (Fig. 2). The majority of
6
insects, at least 84% in each data set, were bees, of
which approximately one-third were honeybees, two-thirds
2011

4
were bumblebees plus a small percentage of other bee gen-
era. Hover flies were always the next most abundant taxon
(7–10%). Butterflies and moths (1–3%) and all other
2 insects (1–3%) were always a small percentage. Overall,
our results suggest that garden plants can easily help bees,
which showed up in large numbers, by providing forage.
0
This agrees with Goulson et al. (2010), who found evi-
Mean number of insects per snapshot per m2 at

6 (b) dence of positive influence of urban gardens on bumblebee


● Plumpton College
P = 0·016 nest density and survival on a landscape scale. Bumblebees
rs = 0·650
○ Magham Down
[maximum foraging range c. 15 km, (Osborne et al. 2008)]
two extra gardens in 2012

4
P = 0·002 and especially honeybees [maximum foraging range c.
rs = 0·791 10 km, (Beekman & Ratnieks 2000)] can forage at long
distances from their nest and thus are able to exploit gar-
den resources. By contrast, butterflies and moths, being
2 relatively scarce garden flower-visitors, can perhaps not be
as easily helped by garden flowers, despite not being cen-
tral place foragers. There is also little evidence that the
0
abundance of adult resources, apart from shelter, has any
0 2 4 6 8 impact on population size or trends in European butterflies
Mean number of insects per snapshot per m2 at (Thomas, Simcox & Hovestadt 2011).
the University of Sussex flower bed in 2012
The absence of a positive correlation between the attrac-
Fig. 4. Correlations between the number of insects per snapshot tiveness of plant varieties to honeybees and bumblebees
recorded on different plant varieties at the University of Sussex (Fig. 6a) suggests that their foraging preferences do not,
flower bed in 2012 with that in (a) 2011, and (b) the additional generally, coincide. Furthermore, the absence of a negative
flower beds at Plumpton College (●) and Magham Down (○) in correlation seems to suggest that these bees do not appear
2012.
to be in competition with each other. However, N.J.
Balfour, S. Gandy & F.L.W. Ratnieks (unpublished data)
the thousands of varieties available (Cubey & Merrick showed competition on L. 9 intermedia ‘Grosso’ experi-
2011) with similar habit (small shrubs and herbaceous mentally. In particular, honeybee numbers increased c. 30
plants suitable for a mixed border). fold on patches from which bumblebees were excluded
Attractiveness of plant varieties correlated strongly (Fig. 6a). It is likely, therefore, that the lack of correlation
between 2011 and 2012 at the University of Sussex between honeybees and bumblebees reflects both the effects
(Fig. 4a). It also correlated between the University of of preferences and competition. As these two types of bees
Sussex and the two additional flower beds at Plumpton were the most abundant flower-visitors, each probably has
College and Magham Down (Fig. 4b). This shows that the capacity to affect the other via consumptive competi-
our results apply generally to a wider area and are not tion (N.J. Balfour, S. Gandy & F.L.W. Ratnieks unpub-
unduly year- or location-specific. Some variation among lished data). In the case of L. 9 intermedia ‘Grosso’, the
locations may be due to local conditions (e.g. microclimate mean corolla tube length of 72 mm was experimentally
or soil type) or differences in the flower-visiting insect com- shown to disadvantage honeybees (mean tongue length
munities present. However, most insect species or groups 66 mm) vs. bumblebees (mean tongue length 78 mm) by
we recorded are common, so would be present in almost causing longer flower-handling times (Balfour, Garbuzov
any area, but not necessarily in the same proportions. Sim- & Ratnieks 2013).
ilarly, some variation between the 2 years could be driven Plant variety attractiveness was similar between the
by annual fluctuations in insect populations. Additionally, short-tongued (B. terrestris/lucorum group) and the long-
in our study, the variation observed between years could tongued (B. hortorum and B. pascuorum groups) bumble-
be due to the different stages of establishment of perennial bees, perhaps, reflecting preferences common to Bombus in
plant varieties. In 2011, the plants had been put into the general (Fig. 6b) or the fact that tongue length variation
patches soon after being delivered from suppliers, who among bumblebees had little effect in our gardens, despite
grew them in pots, while in 2012, most varieties had had reported effects being noted in the literature (Goulson
an extra year in the ground to establish. et al. 2005; Goulson, Lye & Darvill 2008). Nepeta 9
Although variation in relative abundance of insects faassenii ‘Six Hills Giant’ stood out from this correlation,
may explain a small proportion of variation in plant being very attractive to long-tongued bumble bees [length

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
8 M. Garbuzov & F. L. W. Ratnieks

d
5 (a)
Mean number of insects per snapshot per m2

Honeybees
cd
2-banded bumblebees
4 3-banded bumblebees abc abcd abc bcd
Brown bumblebees
Other bumblebees
3 Other bees
Hover flies
Butterflies & moths
Other insects
2
a ab ab a ab a a
1

0
Arctic Folgate Hidcote Imperial Melissa Rosea Edelweiss Gros Grosso Hidcote Old Sussex Anouk
Snow Gem Lilac Bleu Giant English

100
(b) Fig. 5. (a) Numbers of insects per snapshot
Bloom duration in 2012 (days)

80 per m2 on 13 Lavandula varieties. Bar


heights are grand means of two data sets
60 (University of Sussex 2011 & 2012)  SE.
Letters above bars denote results of post
40 hoc Tukey’s HSD pairwise comparison
tests. (b) Total bloom duration of each
20 variety in 2012, c. 15 months after planting

0
Arctic Folgate Hidcote Imperial Melissa Rosea Edelweiss Gros Grosso Hidcote Old Sussex
*
Anouk
out when plants were well established, thus
showing natural phenology. * L. stoechas
Snow Gem Lilac Bleu Giant English ‘Anouk’ was in poor condition and did not
Lavandula angustifolia Lavandula × intermedia Lavandula reach full bloom in 2012. Photographs
stoechas courtesy Dr. Simon Charlesworth.

85–125 mm (Goulson et al. 2005)], but relatively choices based on nectar and pollen rewards in bees (Seeley
unattractive to short-tongued species (length 75–76 mm), 1995; Goulson & Osborne 2010) and hover flies (Haslett
possibly due to its relatively long corolla tube 1989) and nectar rewards in other insects (Kim, Gilet &
(119  02 mm). However, other plant species with simi- Bush 2011). Our data showed no effect of corolla tube
larly long corolla tubes were attractive to short-tongued length (Table S2). However, in specific cases, corolla tube
species due to large corolla width (e.g. E. vulgare), which length may be important. In the case of lamb’s ear (Sta-
allowed short-tongued insects to place their whole head or chys byzantina), its attractiveness to wool-carder bees (An-
body far into the flower, reducing or eliminating the need thidium manicatum) is probably due to the abundant leaf
for a long tongue. In general, attractiveness did not corre- trichomes (pubescence) and possibly trichome secretions,
late between honeybees and bumblebees on the one hand, which are collected by females as nest lining material
and other bees, hover flies and butterflies + moths on the (M€ uller, Topfl & Amiet 1996; Payne, Schildroth & Starks
other, with the exception of the positive correlation 2011). In addition, lamb’s ear flowers are also visited by
between bumblebees vs. butterflies + moths (Fig. 7). How- wool carders. Some plants may be more attractive than
ever, certain plants stood out as particularly good for others by virtue of their longer flowering period. For
other, non-Apis and non-Bombus, bees (Origanum vulgare, example, N. 9 faassenii ‘Six Hills Giant’ and Erysimum li-
E. vulgare, S. byzantina, Achillea millefolium), hover flies nifolium ‘Bowles Mauve’, which are sterile hybrids unable
(O. vulgare, A. foeniculum, E. vulgare) and butterflies & to set seed, had flowering periods extending far beyond
moths (A. foeniculum, Erysimum linifolium). Interestingly, our c. 3-month observation periods. Indeed, E. linifolium
three of the four species particularly attractive to other flowers for approximately 9 months per year in Sussex.
bees are also native to Britain, suggesting that native The attractiveness of such varieties is, therefore, underesti-
plants may be more important for non-Apis and mated in our data.
non-Bombus bees. Closer examination of lavenders showed that hybrid
The factors potentially responsible for variation in L. 9 intermedia varieties were more attractive than both
attractiveness among plant varieties are diverse (e.g. size, L. angustifolia varieties and L. stoechas (Fig. 5). This
shape, colour or scent, reviewed by Pellmyr (2002)). How- difference was not explained by either bloom duration or
ever, as the insects counted were flower-visiting foragers, corolla tube length. In addition, flower colour, which ran-
this variation is presumably largely a result of foraging ged from light (e.g. white ‘Arctic Snow’, ‘Edelweiss’, rose

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Garden plants for flower-visiting insects 9

- HB ‘Rosea’) to more typical shades of blue, did not appear to


3·5 ‘Grosso’ control (a) be an important factor (Fig. 5). We note that L. 9 inter-
r = 0·026
3 P = 0·155 media varieties tended to be larger plants with taller inflo-
rescences than L. angustifolia or L. stoechas. However, the
Number of bumblebees
per snapshot per m2

2·5 definitive explanation causing the difference in attractive-


2
ness remains unknown and would be a valuable subject for
‘Grosso’
further research.
1·5 Within the Dahlia genus, the two open-flowered varie-
1
ties (Bishop of Llandaff and Bishop of Oxford) were
consistently more attractive compared with the two vari-
0·5 -BB eties with highly modified flower forms (pompon ‘Franz
0
Kafka’, semi-cactus ‘Tahiti Sunrise’). This was likely due
Number of honeybees to the limited accessibility of disc florets, which provide
per snapshot per m2
nectar and pollen, due to the unusual shapes of the ray
2
(b) florets resulting from plant breeding. Additionally, the
Number of long-tongued bumblebees

r = 0·565 increased size and number of ray florets may be accom-


P < 0·001
1·5 Nepeta panied by a reduction in the number of disc florets, as
per snapshot per m2

compared to the open-flowered varieties. These results


are supported by data from a survey of garden plants in
1 a public garden in the nearby town of Lewes, where
‘open’ flowered varieties attracted significantly more
insects than ‘closed’ flowered varieties (M. Garbuzov,
0·5
E.E.W. Samuelson & F.L.W. Ratnieks, unpublished
data).
0 Among other notable results is the pattern seen on
0 0·5 1 1·5 2 2·5 3 3·5 B. officinalis, where the vast majority of its visitors were
Number of short-tongued bumblebees
per snapshot per m2 honeybees (mean 813% per data set). The highest propor-
tions of butterflies and moths were recorded on E. linifoli-
Fig. 6. (a) The absence of correlation between the attractiveness um (mean 111% per data set). Pelargonium 9 hortorum
of plant varieties to honeybees and bumblebees. Coloured dots ‘Cramden Red’ was consistently the least attractive variety
refer to three experimental treatments: honeybee exclusion (-HB,
in each data set, with only 0027 mean insects per snapshot
open square), bumblebee exclusion (-BB, open triangle) and con-
trol (open circle) on Lavandula 9 intermedia ‘Grosso’ (N.J. Bal- per m2 recorded. The four native species and the four wild-
four, S. Gandy & F.L.W. Ratnieks, unpublished data). ‘Grosso’ type varieties (Table S1) were not consistently more or less
control (open circle) attracted a higher number of bumblebees attractive than exotic or horticulturally modified varieties,
than ‘Grosso’ in our data (closed circle) due to the data being showing that nativeness per se is not an important factor,
gathered on 4 days during the flowering peak in the former case,
and that horticultural modification need not reduce flower
and over c. 3 months in the latter case. (b) Significant correlation
between the attractiveness of plant varieties to short-tongued attractiveness to insect flower-visitors. Indeed, the case of
bumblebees (Bombus terrestris/lucorum group) and long-tongued lavender shows that the breeding of hybrid varieties can
bumblebees (B. hortorum and B. pascuorum groups). Black dots make plants more attractive to insects. In addition, varie-
are means of two data sets (University of Sussex 2011 & 2012). ties with very long bloom durations, such as E. linifolium

Origanum Agastache
1·2 (a) 1·6 (b) Origanum 0·25 (c)
Number of butterflies & moths

1·4
1
Number of other bees

Number of hover flies


per snapshot per m 2

per snapshot per m2

0·2
1·2
per snapshot per m2

Agastache
0·8 Erysimum
1 0·15
Stachys Echium
0·6 0·8
Echium 0·1
0·6
0·4
Achillea 0·4 0·05
0·2
0·2
0 0 0
0 1 2 3 4 0 1 2 3 4 0 1 2 3 4
Number of honeybees (●) or bumble- Number of honeybees (●) or bumble- Number of honeybees (●) or bumble-
bees (○) per snapshot per m2 bees (○) per snapshot per m2 bees (○) per snapshot per m2

Fig. 7. Correlations between the attractiveness of plant varieties to honeybees (●) & bumblebees (○) vs. other bees (a), hover flies (b), and
butterflies & moths (c). The only significant correlation found was between bumblebees and butterflies & moths (r = 0665, P < 0001).

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
10 M. Garbuzov & F. L. W. Ratnieks

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© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

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