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Native honeybees as flower visitors and pollinators in wild plant
communities in a biodiversity hotspot
DARA A. STANLEY ,
1,2,3,
SIMANGELE M. MSWELI ,
1
AND STEVEN D. JOHNSON
1
1
Centre for Functional Biodiversity, School of Life Sciences, University of KwaZulu-Natal, P Bag X01, Scottsville, Pietermaritzburg 3209,
South Africa
2
School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
3
Earth Institute, University College Dublin, Belfield,Dublin 4, Ireland
Citation: Stanley, D. A., S. Msweli, and S. D. Johnson. 2020. Native honeybees as flower visitors and pollinators in wild
plant communities in a biodiversity hotspot. Ecosphere 11(2):e02957. 10.1002/ecs2.2957
Abstract. Western honeybees (Apis mellifera L.), native to Europe and Africa, have been transported
worldwide and are now one of the most important global crop pollinator species. Although the relative
contribution of honeybees to global crop pollination is increasingly recognized, relatively little is known
about their importance as pollinators in wild plant communities. The only remaining wild and unmanaged
western honeybee populations are in Africa. We investigated the importance of honeybees as pollinators of
diverse wild plant communities in two protected areas within the Maputaland–Pondoland–Albany biodi-
versity hotspot in South Africa. Sites were far from any known areas of beekeeping, and so all honeybees
were most likely from wild colonies. Honeybees visited a large proportion of flowering plant species
within these two communities (40% and 35%) and also provided a substantial proportion of visits to the
plants they visited (40% and 32%, respectively). However, when pollinator importance indices (based on
abundance and the size and purity of pollen loads) were calculated for a small subset of plants, honeybees
were only important pollinators of 29% of the plants they visited. Our data provide a first step in determin-
ing the importance of honeybees as flower visitors and pollinators in wild plant communities and the
potential impacts of honeybee declines on these highly diverse grassland ecosystems. Our work suggests
that many plants in the grassland systems studied are visited by non-Apis flower visitors and therefore that
conservation efforts should also focus on these pollinator groups.
Key words: Apis mellifera; biodiversity hotspot; honey bee; pollination.
Received 8 July 2019; revised 13 September 2019; accepted 27 September 2019; final version received 30 October 2019.
Corresponding Editor: T'ai Roulston.
Copyright: ©2020 The Authors. This is an open access article under the terms of the Creative Commons Attribution
License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
E-mail: dara.stanley@ucd.ie
INTRODUCTION
Pollination is a vital ecosystem service, required
by 76% of global crops (Klein et al. 2007), and an
estimated 87.5% of all flowering plants (Ollerton
et al. 2011b). The most important crop pollinator
species globally is the western honeybee (Apis
mellifera L.), providing roughly 50% of global crop
pollination (Kleijn et al. 2015). Honeybees have
had a long history of associations with humans
(Roffet-Salque et al. 2015) and are the most
widely domesticated pollinator species globally.
A focus on honeybees as pollinators world-
wide has led to criticisms that their role in plant
pollination has been overplayed (Breeze et al.
2011, Ollerton et al. 2011a, Aebi et al. 2012). Wes-
tern honeybees are only one of approximately
20,000 bee species globally (Michener 2007), and
bees in turn are only a subset of the total pollina-
tor fauna which includes a diverse range of insect
taxa such as flies, beetles, butterflies, and moths,
as well as birds and small mammals. Although
critically important as pollinators due to their
domestication and large colony sizes, individual
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honeybees are known to be less successful polli-
nators at the individual scale than are many
other wild bee species (Willmer et al. 1994, 2017,
Vicens and Bosch 2000, Thomson and Goodell
2001, Monz
on et al. 2004), and many studies
have shown that honeybees are only part of a
suite of pollinators responsible for crop pollina-
tion with wild pollinators also playing an impor-
tant role (Garibaldi et al. 2011, 2013, Rader et al.
2015). In fact, the presence of wild pollinators
can actually alter the behavior of honeybees
resulting in an increase in their pollinating effi-
ciency (Greenleaf and Kremen 2006, Brittain
et al. 2013). Although we are beginning to under-
stand the role of honeybees in crop pollination,
surprisingly little is known about the importance
of honeybees as components of natural plant–
pollinator communities and their relative contri-
bution to wild plant reproduction (but see Hung
et al. 2018). Concerns over honeybee health with
issues such as colony collapse disorder, spread of
disease, Varroa destructor mites, hybridization
with other A. mellifera subspecies, and exposure
to pesticides (Van Engelsdorp et al. 2008, Mullin
et al. 2010, Furst et al. 2014) mean that informa-
tion on the ecological importance of these insects
is essential in the face of possible changes to their
abundance and range.
Apis mellifera is native to Africa and Europe,
but as a domesticated species has been trans-
ported worldwide (De la Rua et al. 2009). With
intensive breeding and management, the only
truly wild populations left in the native range of
this species are in Africa (De la Rua et al. 2009,
Jaffe et al. 2010) with populations maintaining
high genetic diversity (Wallberg et al. 2014). Afri-
can populations of A. mellifera are currently not
exposed to the same level of threats as the species
experiences elsewhere (Dietemann et al. 2009),
although these threats are on the increase (Pirk
et al. 2016). For example, the introduction of the
Varroa mite into the Cape (Allsopp 2004) and
other parts of Africa (Fazier et al. 2010, Pirk et al.
2016) is leading to concern over increased spread
of disease, while increased anthropogenic move-
ment of Cape honeybees A. mellifera capensis is
resulting in concern that hybridization with the
more widespread subspecies A. mellifera scutel-
lata will increase in the future. These factors, cou-
pled with increases in urbanization and
agricultural intensification which may decrease
habitat availability and quality, make it likely
that A. mellifera in Africa may be exposed to
more pressures in the future (Dietemann et al.
2009, Pirk et al. 2016).
South Africa, as well as being one of the only
regions of the world with a wild, native honey-
bee population, is also home to the Maputaland–
Pondoland–Albany biodiversity hotspot (CEPF
2010, Mucina and Rutherford 2011). This region
is so designated because of its huge diversity of
plant species, in particular in grassland habitats.
An increasing body of work on plant–pollinator
relationships in this region shows a diverse set of
associations between plants and their pollinators
(e.g., Shuttleworth and Johnson 2012, Johnson
and Raguso 2016). Although there has been
much work on pollination of single plant species,
studies at the community level are lacking in
South Africa in general (but see Carvalheiro et al.
2010, Pauw and Stanway 2015, Vrdoljak et al.
2016, Hansen et al. 2018) and little is known
about the role of wild honeybees in native plant
communities. For example, in a recent meta-anal-
ysis investigating the contribution of honeybees
to pollination of wild plants, only four out of
eighty studies were from continental Africa
(Hung et al. 2018). Therefore, obtaining more
detailed information on the functional roles of
honeybees in African wild grassland communi-
ties is crucial in light of potential threats to
honeybee populations and conservation of these
important habitats.
We investigated the importance of honeybees
as flower visitors in two diverse native grass-
lands within the Maputaland–Pondoland–
Albany biodiversity hotspot addressing the fol-
lowing questions:
1. What proportion of plants in these biodi-
verse grasslands receive visits from honey-
bees?
2. Are the plants visited by honeybees mostly
generalists (i.e., also receive visits from other
pollinator groups), and are any of these
plants of conservation concern?
3. Are honeybees among the most generalist
flower visitors, visiting a large number of
plant species in comparison with other polli-
nator groups?
4. Are honeybees the primary pollinators of
the majority of plants that they visit?
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STANLEY ET AL.
METHODS
We compiled data on honeybee visits in flow-
ering grassland plant communities in two high
diversity, protected areas within the Maputa-
land–Pondoland–Albany biodiversity hotspot in
South Africa; Mount Gilboa Nature Reserve
(29°190S, 30°170E; altitude ~1500 m; Fig. 1) and
Vernon Crookes Nature Reserve (30°160S,
30°370E; altitude ~450 m; Fig. 1). The Mt Gilboa
site is part of a large 36-km
2
nature reserve, mak-
ing it likely that any honeybees present are wild
and not domesticated. Sampling in Vernon
Crookes took place at least 500 m from the
reserve boundary; however, settlements outside
the boundary were low density and consist of
traditional communities who are not known to
engage in beekeeping, suggesting that most
honeybees in both sites were wild and not man-
aged.
Flower visitation data for both sites were
obtained from all known published and unpub-
lished sources. We compiled all known pub-
lished papers that investigated questions around
pollination ecology from each site published
between 2000 and 2015 (40 from Mt Gilboa, 22
from Vernon Crookes). We reviewed these
papers for information on the relative contribu-
tions of different flower visitor groups to plant
species visitation at the site level, which we were
able to extract from 18 papers for Mt Gilboa and
five papers from Vernon Crookes (Appendix S1).
Most papers covered pollination of single species
or species guilds, and information on the contri-
bution of different flower visitors to flower visi-
tation or pollen transport was extracted for each
plant species at the relevant site. The majority of
studies recorded the number of individual
insects visiting plant species; however, some
additionally recorded the number of individuals
found carrying pollen or evaluated the relative
pollen loads of different pollinator species. Based
on the type of data collected, we estimated the
proportion of contribution of each flower visitor
species visiting each plant species.
For both sites, we also included data collected
in two unpublished community studies. For Mt
Gilboa, data were included from an unpublished
network study (Johnson et al., unpublished data).
Transect sampling methods were used to collect
data on all flower visitors observed visiting all
plant species in the grassland areas at Mt Gilboa
on multiple occasions between 2000 and 2012.
For Vernon Crookes, we also included data
collected from a community-level network study
sampled using focal observations of flowering
plants (Stanley et al., unpublished data). Data were
collected over 17 d from January to April 2016,
and 11 d from January to April 2017, encompass-
ing the peak flowering period in this habitat. All
plants flowering in a plot of 160 950 m estab-
lished in an area of coastal grassland were
observed using focal observations of single spe-
cies on dry, calm days. Due to burning regimes
within the reserve, these plots were not in the
same position in both years but were adjacent
(~50 m apart) in a similar grassland habitat.
Flowering patches of single species were chosen
at random on each visit, and the number of flow-
ers observed was recorded. Recorders stood 2–
5 m away from the flower patches being
observed and caught any flower visitors interact-
ing with flowers during a 15-min observation
period (unless identification was possible in the
field; Fig. 1). Flower visitors were caught in
either a net or a vial as was most appropriate for
the individual, and every effort was made to
minimize disturbance during this process. Speci-
mens were later identified to species level by rel-
evant experts (see Acknowledgments) or were
grouped to morphospecies if identification was
not possible. We aimed to carry out twelve focal
observations (three hours in total) for each plant
species flowering in the study area across both
years; however, for some species that stopped
flowering within the sampling period, we were
unable to gather the full three hours of observa-
tion. We therefore only included species in fur-
ther analyses that had more than one hour of
observations to ensure a minimum sampling
effort throughout. Approximately 15 species
flowering in the community were omitted from
further analyses as they were not observed for
the full length of time, or because no insects were
observed to visit them. In addition, we recorded
additional flower visits to plant species observed
in an ad hoc way outside focal observation times
when walking around the site, and these interac-
tions were added to the focal observation dataset
to increase sample sizes. In 2017, not all sunbird
species were identified to species level, and so
sunbirds were grouped for further analyses.
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STANLEY ET AL.
To compare frequency of different visitors
sampled using a variety of methods from both
published and unpublished work, we calculated
the proportion of visits of each flower visitor spe-
cies to each plant species for both communities
(Appendix S2: Tables S1, S2). For any plant spe-
cies that occurred in more than one study, we
pooled the available data and calculated overall
proportional contributions of different pollinator
groups.
At Mt Gilboa, we compiled visitation data for
82 plant species from 23 families (Appendix S2:
Table S2). Of these, the Asteraceae were most
widely represented (21 species) followed by the
a)
b)
c) d)
e)
f)
g)
h)
Fig. 1. Vegetation and representative examples of plant–pollinator interactions at the study sites within the
Maputaland–Pondoland–Albany biodiversity hotspot. (a) Grassland vegetation with scattered bush clumps at
Vernon Crookes Nature Reserve. (b) Grassland vegetation on the summit of Mount Gilboa with Protea caffra
shrubs in the foreground and a mass display of pink flowers of Watsonia lepida. (c) Honeybee Apis mellifera on
Cyperus obtusiflorus (Cyperaceae) at Vernon Crookes. (d) Megachilid bee Megachile cincta on Eriosema distinctum
(Fabaceae) at Mount Gilboa. (e) Pompilid wasp Hemipepsis hilaris on Eucomis autumnalis (Hyacinthaceae) at Ver-
non Crookes. (f) Cetoniine beetle Atrichelaphinis tigrina on Crassula vaginata (Crassulaceae) at Vernon Crookes. (g)
Tabanid flyPhiloliche aethiopica on Watsonia lepida (Iridaceae) on Mount Gilboa. (h) Nymphalid butterflyPrecis
octavia sesamus on Pentanisia prunelloides (Rubiaceae) at Vernon Crookes. Photographs by SDJ and DS.
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STANLEY ET AL.
Iridaceae and Orchidaceae (nine species each).
The majority of plants were listed as Least Con-
cern (64 species) on the South African Red List of
Plants (SANBI 2015), with two Rare, two Vulner-
able, one Declining, one Near Threatened, and 12
without a designation due to lack of taxonomic
resolution.
At Vernon Crookes, we compiled data for 52
plant species from 28 families (Appendix S2:
Table S2). The Asteraceae and Fabaceae were the
most widely represented plant families (eight
and nine species, respectively), followed by
Lamiaceae and Rubiaceae (four and three species
each). The majority of plants were again listed as
Least Concern, with one species Near Threat-
ened, one Not Evaluated, and two naturalized
exotics.
To assess pollinator importance, we used pub-
lished data from Johnson et al. (2009) on 21 spe-
cies in the Mt Gilboa community where
pollinator observations of each species were com-
bined with analyses of pollen loads carried. A
pollinator importance index was calculated for
each flower visitor as the product of relative pol-
linator abundance, relative pollen load index, rel-
ative host plant fidelity, and pollination
efficiency (for more information on the calcula-
tion of the index, see Johnson et al. 2009). Polli-
nation efficiency was defined as the estimated
probability (based on morphological fit and
observed behavior) that foraging activity of a
given visitor results in contact with the anthers
and stigma (Lindsey 1984).
RESULTS
Mt Gilboa community
Of the 82 plant species in our compiled data-
set, 34 (40%) were visited by A. mellifera (Table 1;
Appendix S2: Table S1). These species repre-
sented 18 plant families. On average, A. mellifera
provided 40% of visits to these plant species
(Fig. 2a), and only six species (7%; from five fam-
ilies) were recorded to be visited exclusively by
A. mellifera, namely Ornithogalum virens,Cyanotis
speciosa,Euryops laxus,Gerbera ambigua,Indigofera
foliosa, and Rubus ludwigii. All plants visited by
honeybees were listed as Least Concern on the
South African Red list (SANBI 2015), except for
Eucomis comosa (declining) to which honeybees
provided just 0.3% of visits.
Other flower visitors in the community
included beetles, birds, butterflies, flies, moths,
wasps, solitary bees, and ants (Table 1). Of these
functional groups, solitary bees and flies visited
the most species within the community (54 and
45 species, respectively), followed by honeybees
(34 species) and beetles (27 species). As data
were compiled from different studies, some of
which used morphospecies identifications for
insects, a full comparison of the host range of all
flower visitors identified to species level was not
possible. However, A. mellifera visited the high-
est number of plant species recorded for any pol-
linator species, followed by a Lasioglossum bee
species, Calliphoridae flies, and the cetoniine
beetle Atrichelaphinis tigrina.
Vernon Crookes community
Of the 52 plant species in the dataset, eighteen
plant species (35%) from 11 families were visited
by A. mellifera (Table 1; Appendix S2: Table S1),
which on average provided 32% of visits
(Fig. 2b). All plants visited were of Least Con-
cern, and only one species (Agapanthus sp.) was
visited exclusively by honeybees.
Other flower visitors at Vernon Crookes
belonged to similar taxonomic groups to those at
Gilboa (Table 1). Solitary bees visited the largest
number of plant species of any flower visitor
groups within the community (43 species)
Table 1. The number of plant species visited by each
flower visitor group in each community
Pollinator group
Total number of plant species
visited by each pollinator
group
Mt Gilboa Vernon Crookes
Ants 1 5
Bees (excluding honeybees) 54 43
Beetles 27 16
Bird 7 3
Butterfly2116
Fly 45 16
Honeybee 34 18
Moth 4 3
Wasp 6 7
Notes: In total, there were 82 plant species with flower vis-
itors observed on Mt Gilboa, and 52 plant species observed at
Vernon Crookes. Insect groups which visited two or
fewer plants are not included (e.g., sawflies and bugs).Bold
values indicate honeybees (Apis mellifera)
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STANLEY ET AL.
followed by honeybees (18 species), butterflies,
beetles, and flies (16 species each). Using data
from Stanley et al. (unpublished manuscript) that
identified flower visitors to species level, we
were able to determine that A. mellifera visited
the highest number of plant species of any indi-
vidual pollinator species (18 species), along with
two Allodape bee species that visited 18 and 11
plant species, respectively (Fig. 3).
Pollinator importance
Of the 21 plant species for which we had polli-
nator importance data, eight (38%) were visited
by honeybees. Honeybees provided 3–36% of the
visits to these species. However, when relative
pollinator abundance, pollen load, host plant
fidelity, and efficiency were taken into account in
a pollinator importance index (Johnson et al.
2009), honeybees were important pollinators of
just two (29%) of the seven species where polli-
nator importance measures could be calculated
(Table 2).
DISCUSSION
Although there has been much work on wild
plant–pollinator communities around the world
in terms of pollination networks (Schleuning
et al. 2012), there are almost no studies of whole
plant–pollinator communities in Africa where
honeybees are native and remain wild (but see
Baldock et al. 2011, Pauw and Stanway 2015,
Willmer et al. 2017). Our work shows that
honeybees visit a substantial portion (Gilboa
40%, Vernon Crookes 35%) of flowering plant
species in native grassland communities of the
Maputaland–Pondoland–Albany biodiversity
hotspot. However, relatively few of these plants
were exclusively visited by honeybees, and none
that were visited were of conservation concern.
The proportion of plant species visited by honey-
bees outside South Africa, in areas where they
have been introduced or managed, seems vari-
able, but is concordant overall with the values
we obtained in South Africa. For example, the
percentage of plant species visited by honeybees
was 35% across eight sites in the Peruvian Andes
(Watts et al. 2016); 84% in sites both invaded by
alien plant species and uninvaded in Seychelles
(Kaiser-Bunbury et al. 2011); 64% in a meadow
in Germany (Junker et al. 2013); 46% in a decidu-
ous forest in United States (Motten 1986); 2% in
montane forest in Australia (Inouye and Pyke
Fig. 2. The mean (SE) proportion of visits provided by flower visitor groups to the plants they visit at (a)
Mt. Gilboa and (b) Vernon Crookes. Honeybees are represented in dark gray.
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STANLEY ET AL.
1988); and 35% and 87% in Azores and Mauri-
tius, respectively (Olesen et al. 2002). In an anal-
ysis of 80 networks globally, A. mellifera was
recorded to visit about half of all plant taxa and
was detected in a similar proportion of networks
from both its native and introduced range (Hung
et al. 2018). That honeybees tend to visit a similar
proportion of plant species in communities
where they are native, and in communities where
they are introduced, is consistent with the
opportunistic behavior of these social insects and
their ability to exploit a wide range of novel
flower types.
Honeybees in South Africa are not yet exposed
to similar threats to those facing honeybees and
other pollinators elsewhere (Dietemann et al.
2009), but some threats are emerging (Pirk et al.
2016). For example, Varroa mites have only
recently arrived in South Africa (Allsopp 2004)
which could mean an impact on honeybee
Fig. 3. The number of plants visited by each flower visitor species (ranked from most to least generalist) in the
Vernon Crookes community. The black bar and arrow show the honeybee (Apis mellifera) which visited 18 plant
species, making it (along with Allodape rufogastra, Apidae) one of the most generalist flower visitor species in the
community. These data are from the Stanley et al. (unpublished) study only as insects were recorded to species
level.
Table 2. The proportion of visits to each plant species by Apis mellifera in the pollinator importance study, the
numbers of A. mellifera observed, the number of A. mellifera individuals sampled for pollen, and the index of
pollinator importance of A. mellifera to that species (abundance 9pollen load index 9host plant
fidelity 9pollination efficiency)
Plant species
Proportion of
visits
No. of individuals
observed
No. of individuals sampled for
pollen
Pollinator importance
index
Dierama
dracomontanum
0.11 2 1 0
Eriosema distinctum 0.36 47 2 0
Eucomis comosa 0.03 1 1 4.07
Kniphophia laxiflora 0.01 1 1 0
Moraea inclinata 0.18 5 3 28.61
Pentanisia
prunelloides
0.04 4 1 0
Watsonia lepida 0.01 1 1 0
Note: Data from Johnson et al. (2009).
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STANLEY ET AL.
populations in the near future. From our data,
we can hypothesize what might happen if
honeybees were to become reduced in numbers,
or even extinct, in our study sites. In Vernon
Crookes, honeybees provided an average of 32%
of visits to plants they visited and only one plant
species was exclusively visited by honeybees;
therefore, removal of honeybees from the system
may not have drastic consequences for plant
reproduction. On the other hand, on Mt Gilboa
honeybees provided a higher proportion of visits
(40%) to plant species they visited, and six spe-
cies were visited exclusively by A. mellifera
(although the maximum number of individuals
observed on these species was five which may
reflect low sampling intensity, and more samples
may have yielded more pollinators of these spe-
cies). Therefore, changes in honeybee abundance
in this system may have more direct conse-
quences for any plant species reliant on honey-
bees for reproduction. Using a modeling
approach, plant–pollinator communities have
been shown to be reasonably resilient to extinc-
tion of single pollinator species, including highly
linked ones. For example, Memmott et al. (2004)
simulated the impacts of species removal on
plant–pollinator network structure. They found
that removal of the most linked species (such as
honeybees in our system) caused a decline in
plant species no less than linear because of
redundancy within the network, although their
study assumed that all plants in the community
were obligate outcrossers, which is unlikely to be
realistic (Pannell et al. 2015), and that all flower
visitors are pollinators which may also not be the
case (Ballantyne et al. 2015). In addition to
changes in honeybee abundances, alterations to
existing ecosystems may cause differences in
honeybee visitation. For example, honeybee
visits were found to increase with increasing
levels of fragmentation, while visitation by
wild bees decreased (Aizen and Feinsinger 1994).
If grasslands in the Maputaland–Pondoland–
Albany hotspot were to become more frag-
mented than they are currently, the importance
of honeybees in these systems may increase. This
may not be due to fragmentation per se, but
rather the association between habitat fragmen-
tation and general anthropogenic activities
including an increase in the number of managed
hives.
Studies of flower visitor networks can provide
only limited insights into the ecological impor-
tance of honeybees. It is well known, for exam-
ple, that not all flower visitors are equal in terms
of their per-visit effectiveness as pollinators (Fen-
ster et al. 2004, Ballantyne et al. 2015). The effects
of honeybee extinctions, or reductions in num-
bers, on plant pollination are all dependent on
the effectiveness of honeybees as pollinators
rather than being a product of their simple
numerical abundance as flower visitors. Interest-
ingly, data from pollinator importance work
show that although honeybees may visit many
plant species, they may not be effective pollina-
tors of all of them (Willmer et al. 2017, Hung
et al. 2018). We show for a subset of 21 species
on Mt Gilboa that although A. mellifera visits
eight species, it is only an important pollinator of
two of these. Variation in the importance of
honeybees as pollinators is also apparent from
more in-depth studies of single-species interac-
tions in a South African context, from honeybees
and Lipotriches sp (Halictidae) being equally
abundant and similarly effective pollinators of
two Wahlenbergia species (Welsford and Johnson
2012), to honeybees being abundant but making
a negligible contribution to pollination of some
Aloe,Protea, and Syncolostemon species (Harg-
reaves et al. 2004, 2010, Botes et al. 2009, Wester
and Johnson 2017). On a larger scale, Willmer
et al. (2017) have also found that honeybees are
less effective than both bumblebees and solitary
bees in a variety of sites across different coun-
tries, and when investigating 34 studies of polli-
nator effectiveness, A. mellifera did not differ
from the average flower visitor in terms of single
visit effectiveness, but was less effective than the
most effective visitors (Hung et al. 2018)
Although honeybees may not be effective pol-
linators for all of the species they visit, our data
do provide an indication of the diversity of plant
species that honeybees use as a resource. Decli-
nes in available forage resources are often sug-
gested to be one of the main threats to bees (Potts
et al. 2010, Goulson et al. 2015), with parallel
declines in species richness of bees and insect-
pollinated plants recorded in both Britain and
the Netherlands (Biesmeijer et al. 2006). Our
work has identified a variety of native South
African species visited by honeybees. As sources
of nectar and pollen, these species are likely to be
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STANLEY ET AL.
important for sustaining wild honeybee popula-
tions. They may also be useful as part of directed
actions to support honeybees, such as native gar-
den plantings or conservation farming.
Tropical grasslands are under huge threat from
afforestation and general encroachment of
woody vegetation (Bond 2016). The subtropical
grasslands of KwaZulu-Natal are no exception
and are mainly threatened with commercial
plantation forestry (Macdonald 1989). It is there-
fore crucial to understand the ecology of these
systems, including the relative importance of dif-
ferent pollinator groups. We have shown that
honeybees visit a large proportion of plant spe-
cies in grassland communities and thus likely
depend on these for pollen and nectar. However,
from the plant perspective the overall impor-
tance of honeybees as pollinators seems to be rel-
atively low. This could be taken to imply that the
consequences of declines in natural honeybee
populations may not be as catastrophic for natu-
ral ecosystems as is often implied in the popular
press, but we caution that the present study
incorporates pollinator importance values for a
limited subset of plants in just two natural com-
munities. A next step to this work will be to eval-
uate the effectiveness of honeybees as pollinators
of a much larger sample set of plant species in
these and in other communities. Although a
huge undertaking that has so far as only been
carried out fully in low diversity systems (Ballan-
tyne et al. 2015), with some additional work on
partial communities in high diversity systems
(Ballantyne et al. 2017), this would provide much
needed in-depth data on the ecological impor-
tance of honeybees in wild plant communities in
biodiverse regions.
ACKNOWLEDGMENTS
We would like to thank the following people for
help with species identification: Connal Eardley (bees),
Denis Brothers (wasps), and Isabel Johnson (plants).
Nombuso Gongo, Keeveshnee Govender, Kerushka
Pillay, Marco Balducci, Karl Sweeney, and Daniel Buck-
ley all helped with fieldwork in Vernon Crookes. This
work was funded under the South African National
Research Foundation (NRF) Research Chair funding
program (grant 46372) awarded to SDJ. DAS and SDJ
conceived and designed the study; DAS and SM col-
lected data from Vernon Crookes, and SDJ provided
data from Mt Gilboa; DS analyzed the data and drafted
the manuscript; and all authors provided comments on
the manuscript and gave final approval for publica-
tion. We would like to dedicate this paper to the mem-
ory of our colleague and friend Keeveshnee Govender.
LITERATURE CITED
Aebi, A., B. E. Vaissiere, D. Van Engelsdorp, K. S. Dela-
plane, D. W. Roubik, and P. Neumann. 2012. Back
to the future: Apis versus non-Apis pollination-a
response to Ollerton et al. Trends in Ecology &
Evolution 27:142–143.
Aizen, M. A., and P. Feinsinger. 1994. Habitat fragmen-
tation, native insect pollinators, and feral honey-
bees in Argentine Chaco Serrano. Ecological Appli-
cations 4:378–392.
Allsopp, M. 2004. Cape honeybee (Apis mellifera capen-
sis Eshscholtz) and Varroa mite (Varroa destructor
Anderson & Trueman) threats to honeybees and
beekeeping in Africa. International Journal of Trop-
ical Insect Science 24:87–94.
Baldock, K. C. R., J. Memmott, J. C. Ruiz-Guajardo, D.
Roze, and G. N. Stone. 2011. Daily temporal struc-
ture in African savanna flower visitation networks
and consequences for network sampling. Ecology
92:687–698.
Ballantyne, G., K. C. R. Baldock, L. Rendell, and P. G.
Willmer. 2017. Pollinator importance networks
illustrate the crucial value of bees in a highly spe-
ciose plant community. Scientific Reports 7:8389.
Ballantyne, G., K. C. R. Baldock, and P. G. Willmer.
2015. Constructing more informative plant–polli-
nator networks: visitation and pollen deposition
networks in a heathland plant community. Pro-
ceedings of the Royal Society of London B: Biologi-
cal Sciences 282:1814.
Biesmeijer, J. C., et al. 2006. Parallel declines in pollina-
tors and insect-pollinated plants in Britain and the
Netherlands. Science 313:351–354.
Bond, W. J. 2016. Ancient grasslands at risk. Science
351:120–122.
Botes, C., S. D. Johnson, and R. M Cowling. 2009. The
Birds and the Bees: using selective exclusion to
identify effective pollinators of African tree aloes.
International Journal of Plant Sciences 170:151–156.
Breeze, T. D., A. P. Bailey, K. G. Balcombe, and S. G.
Potts. 2011. Pollination services in the UK: How
important are honeybees? Agriculture, Ecosystems
& Environment 142:137–143.
Brittain, C., N. Williams, C. Kremen, and A.-M. Klein.
2013. Synergistic effects of non-Apis bees and
honey bees for pollination services. Proceedings of
the Royal Society B: Biological Sciences 280:20122767.
Carvalheiro, L. G., C. L. Seymour, R. Veldtman, and S.
W. Nicolson. 2010. Pollination services decline with
❖www.esajournals.org 9February 2020 ❖Volume 11(2) ❖Article e02957
STANLEY ET AL.
distance from natural habitat even in biodiversity-
rich areas. Journal of Applied Ecology 47:810–820.
CEPF. 2010. Ecosystem profile: Maputaland-Pon-
doland-Albany Biodiversity Hotspot. Critical
Ecosystem Partnership Fund, Conservation Inter-
national Southern African Hotspots Programme
South African National Biodiversity Institute.
De la Rua, P., R. Jaffe, R. Dall'Olio, I. Munoz, and J.
Serrano. 2009. Biodiversity, conservation and cur-
rent threats to European honeybees. Apidologie
40:263–284.
Dietemann, V., C. W. W. Pirk, and R. Crewe. 2009. Is
there a need for conservation of honeybees in
Africa? Apidologie 40:285–295.
Fazier, M., E. Muli, T. Conklin, D. Schmehl, B. Torto, J.
Frazier, J. Tumlinson, J. D. Evans, and S. Raina.
2010. A scientific note on Varroa destructor found in
East Africa; threat or opportunity? Apidologie
41:463–465.
Fenster, C. B., W. S. Armbruster, P. Wilson, M. R.
Dudash, and J. D. Thomson. 2004. Pollination syn-
dromes and floral specialization. Annual Review
of Ecology Evolution and Systematics 35:375–403.
Furst, M. A., D. P. McMahon, J. L. Osborne, R. J. Pax-
ton, and M. J. F. Brown. 2014. Disease associations
between honeybees and bumblebees as a threat to
wild pollinators. Nature 506:364–366.
Garibaldi, L. A., et al. 2011. Stability of pollination ser-
vices decreases with isolation from natural areas
despite honey bee visits. Ecology Letters 14:1062–
1072.
Garibaldi, L. A., et al. 2013. Wild pollinators enhance
fruit set of crops regardless of honey bee abun-
dance. Science 339:1608–1611.
Goulson, D., E. Nicholls, C. Bot
ıas, and E. L. Rotheray.
2015. Bee declines driven by combined stress from
parasites, pesticides, and lack of flowers. Science
347:1255957.
Greenleaf, S. S., and C. Kremen. 2006. Wild bees
enhance honey bees’pollination of hybrid sun-
flower. Proceedings of the National Academy of
Sciences of the United States of America
103:13890–13895.
Hansen, S., F. Roets, C. L. Seymour, E. Th
ebault, F. J. F.
Veen, and J. S. Pryke. 2018. Alien plants have
greater impact than habitat fragmentation on
native insect flower visitation networks. Diversity
and Distributions 24:58–68.
Hargreaves, A. L., L. D. Harder, and S. D. Johnson.
2010. Native pollen thieves reduce the reproduc-
tive success of a hermaphroditic plant, Aloe macu-
lata. Ecology 91:1693–1703.
Hargreaves, A. L., S. D. Johnson, and E. Nol. 2004. Do
floral syndromes predict specialization in plant
pollination systems? An experimental test in an
“ornithophilous”African Protea. Oecologia
140:295–301.
Hung, K. L. J., J. M. Kingston, M. Albrecht, D. A. Hol-
way, and J. R. Kohn. 2018. The worldwide impor-
tance of honey bees as pollinators in natural
habitats. Proceedings of the Royal Society B-Biolog-
ical Sciences 285:8.
Inouye, D. W., and G. H. Pyke. 1988. Pollination biol-
ogy in the Snowy Mountains of Australia: compar-
isons with montane Colorado, USA. Australian
Journal of Ecology 13:191–205.
Jaffe, R., et al. 2010. Estimating the density of honey-
bee colonies across their natural range to fill the
gap in pollinator decline censuses. Conservation
Biology 24:583–593.
Johnson, S. D., L. F. Harris, and S
ß. Proches
ß. 2009. Polli-
nation and breeding systems of selected wildflow-
ers in a southern African grassland community.
South African Journal of Botany 75:630–645.
Johnson, S. D., and R. A. Raguso. 2016. The long-tongued
hawkmoth pollinator niche for native and invasive
plants in Africa. Annals of Botany 117:25–36.
Junker,R.R.,N.Bl
€
uthgen,T.Brehm,J.Binkenstein,J.Paulus,
H. Martin Schaefer, and M. Stang. 2013. Specialization
on traits as basis for the niche-breadth of flower
visitors and as structuring mechanism of ecological
networks. Functional Ecology 27:329–341.
Kaiser-Bunbury, C. N., T. Valentin, J. Mougal, D. Mata-
tiken, and J. Ghazoul. 2011. The tolerance of island
plant–pollinator networks to alien plants. Journal
of Ecology 99:202–213.
Kleijn, D., et al. 2015. Delivery of crop pollination ser-
vices is an insufficient argument for wild pollinator
conservation. Nature Communications 6:7414.
Klein,A.M.,B.E.Vaissiere,J.H.Cane,I.Steffan-Dewen-
ter, S. A. Cunningham, C. Kremen, and T. Tscharn-
tke. 2007. Importance of pollinators in changing
landscapes for world crops. Proceedings of the
Royal Society B-Biological Sciences 274:303–313.
Lindsey, A. H. 1984. Reproductive biology of Api-
aceae. I. Floral visitors to Thaspium and Zizia and
their importance in pollination. American Journal
of Botany 71:375–387.
Macdonald, I. A. W. 1989. Man's role in changing the
face of southern Africa. Pages 51–78 in B. J. Hunt-
ley, editor. Biotic diversity in southern Africa: con-
cepts and conservation. Oxford University Press,
Cape Town, South Africa.
Memmott, J., N. M. Waser, and M. V. Price. 2004. Toler-
ance of pollination networks to species extinctions.
Proceedings of the Royal Society B-Biological
Sciences 271:2605–2611.
Michener, C. D. 2007. The bees of the world. John
Hopkins University Press, Baltimore, Maryland,
USA.
❖www.esajournals.org 10 February 2020 ❖Volume 11(2) ❖Article e02957
STANLEY ET AL.
Monz
on, V. H., J. Bosch, and J. Retana. 2004. Foraging
behavior and pollinating effectiveness of Osmia cor-
nuta (Hymenoptera: Megachilidae) and Apis mellif-
era (Hymenoptera: Apidae) on “Comice”pear.
Apidologie 35:575–585.
Motten, A. F. 1986. Pollination ecology of the spring
wildflower community of a temperate deciduous
forest. Ecological Monographs 56:21–42.
Mucina, L., and M. C. Rutherford. 2011. The vegeta-
tion of South Africa, Lesotho and Swaziland. Stre-
litzia 19. South African Biodiversity Institute,
Pretoria, South Africa.
Mullin, C. A., M. Frazier, J. L. Frazier, S. Ashcraft, R.
Simonds, D. vanEngelsdorp, and J. S. Pettis. 2010.
High levels of miticides and agrochemicals in
North American apiaries: implications for honey
bee health. PLOS ONE 5:e9754.
Olesen, J. M., L. I. Eskildsen, and S. Venkatasamy.
2002. Invasion of pollination networks on oceanic
islands: importance of invader complexes and
endemic super generalists. Diversity and Distribu-
tions 8:181–192.
Ollerton, J., R. Winfree, and S. Tarrant. 2011b. How
many flowering plants are pollinated by animals?
Oikos 120:321–326.
Ollerton, J., et al. 2011a. Overplaying the role of honey
bees as pollinators: a comment on Aebi and Neu-
mann (2011). Trends in Ecology & Evolution
27:141–142.
Pannell, J. R., et al. 2015. The scope of Baker's law.
New Phytologist 208:656–667.
Pauw, A., and R. Stanway. 2015. Unrivalled specializa-
tion in a pollination network from South Africa
reveals that specialization increases with latitude
only in the Southern Hemisphere. Journal of Bio-
geography 42:652–661.
Pirk, C. W. W., U. Strauss, A. A. Yusuf, F. Demares,
and H. Human. 2016. Honeybee health in Africa-a
review. Apidologie 47:276–300.
Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann,
O. Schweiger, and W. E. Kunin. 2010. Global polli-
nator declines: trends, impacts and drivers. Trends
in Ecology & Evolution 25:345–353.
Rader, R., et al. 2015. Non-bee insects are important
contributors to global crop pollination. Proceed-
ings of the National Academy of Sciences of the
United States of America 113:: 146–151.
Roffet-Salque, M., et al. 2015. Widespread exploitation
of the honeybee by early Neolithic farmers. Nature
527:226.
SANBI. 2015. Red list of South African plants 2015.1.
South African National Biodiversity Institute, Pre-
toria, South Africa.
Schleuning, M., et al. 2012. Specialization of mutualis-
tic interaction networks decreases toward tropical
latitudes. Current Biology 22:1925–1931.
Shuttleworth, A., and S. D. Johnson. 2012. The
Hemipepsis wasp-pollination system in South
Africa: a comparative analysis of trait convergence
in a highly specialized plant guild. Botanical Jour-
nal of the Linnean Society 168:278–299.
Thomson, J. D., and K. Goodell. 2001. Pollen removal
and deposition by honeybee and bumblebee visi-
tors to apple and almond flowers. Journal of
Applied Ecology 38:1032–1044.
Van Engelsdorp, D., J. Hayes, R. M. Underwood, and
J. Pettis. 2008. A survey of honey bee colony losses
in the US, Fall 2007 to Spring 2008. PLOS ONE 3:
e4071.
Vicens, N., and J. Bosch. 2000. Pollinating efficacy of
Osmia cornuta and Apis mellifera (Hymenoptera :
Megachilidae, Apidae) on ‘red Delicious’apple.
Environmental Entomology 29:235–240.
Vrdoljak, S. M., M. J. Samways, and J. P. Simaika. 2016.
Pollinator conservation at the local scale: Flower
density, diversity and community structure
increase flower visiting insect activity to mixed flo-
ral stands. Journal of Insect Conservation 20:711–
721.
Wallberg, A., et al. 2014. A worldwide survey of gen-
ome sequence variation provides insight into the
evolutionary history of the honeybee Apis mellifera.
Nature Genetics 46:1081.
Watts, S., C. F. Dormann, A. M. Mart
ın Gonz
alez, and
J. Ollerton. 2016. The influence of floral traits on
specialization and modularity of plant–pollinator
networks in a biodiversity hotspot in the Peruvian
Andes. Annals of Botany 118: 415–429.
Welsford, M. R., and S. D. Johnson. 2012. Solitary and
social bees as pollinators of Wahlenbergia (Campan-
ulaceae): single-visit effectiveness, overnight shel-
tering and responses to flower colour. Arthropod-
Plant Interactions 6:1–14.
Wester, P., and S. D. Johnson. 2017. Importance of
birds versus insects as pollinators of the African
shrub Syncolostemon densiflorus (Lamiaceae). Botan-
ical Journal of the Linnean Society 185:225–239.
Willmer, P. G., A. A. M. Bataw, and J. P. Hughes. 1994.
The superiority of bumblebee to honeybees as pol-
linators - insect visits to raspberry flowers. Ecologi-
cal Entomology 19:271–284.
Willmer, P. G., H. Cunnold, and G. Ballantyne. 2017.
Insights from measuring pollen deposition: quanti-
fying the pre-eminence of bees as flower visitors
and effective pollinators. Arthropod-Plant Interac-
tions 11:411–425.
❖www.esajournals.org 11 February 2020 ❖Volume 11(2) ❖Article e02957
STANLEY ET AL.
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