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Native honeybees as flower visitors and pollinators in wild plant communities in a biodiversity hotspot

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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 biodiversity 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 determining 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.
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Native honeybees as ower 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, Beleld, Dublin 4, Ireland
3
Earth Institute, University College Dublin, Beleld,Dublin 4, Ireland
Citation: Stanley, D. A., S. Msweli, and S. D. Johnson. 2020. Native honeybees as ower 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 MaputalandPondolandAlbany 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 owering 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 rst step in determin-
ing the importance of honeybees as ower 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 ower 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; nal 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 owering 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 ies, beetles, butteries, and moths,
as well as birds and small mammals. Although
critically important as pollinators due to their
domestication and large colony sizes, individual
www.esajournals.org 1February 2020 Volume 11(2) Article e02957
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 ef-
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 intensication 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
PondolandAlbany 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 plantpollinator
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 ower visitors in two diverse native grass-
lands within the MaputalandPondoland
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
ower 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 ow-
ering grassland plant communities in two high
diversity, protected areas within the Maputa-
landPondolandAlbany 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 ower visitor groups to plant
species visitation at the site level, which we were
able to extract from 18 papers for Mt Gilboa and
ve papers from Vernon Crookes (Appendix S1).
Most papers covered pollination of single species
or species guilds, and information on the contri-
bution of different ower visitors to ower 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 ower 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 ower 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 owering
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 owering period in this habitat. All
plants owering 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 ow-
ers observed was recorded. Recorders stood 2
5 m away from the ower patches being
observed and caught any ower visitors interact-
ing with owers during a 15-min observation
period (unless identication was possible in the
eld; 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 identied to species level by rel-
evant experts (see Acknowledgments) or were
grouped to morphospecies if identication was
not possible. We aimed to carry out twelve focal
observations (three hours in total) for each plant
species owering in the study area across both
years; however, for some species that stopped
owering 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
owering 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 ower 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 identied 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 ower 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 plantpollinator interactions at the study sites within the
MaputalandPondolandAlbany 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 owers of Watsonia lepida. (c) Honeybee Apis mellifera on
Cyperus obtusiorus (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 yPhiloliche aethiopica on Watsonia lepida (Iridaceae) on Mount Gilboa. (h) Nymphalid butteryPrecis
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 ower visitor as the product of relative pol-
linator abundance, relative pollen load index, rel-
ative host plant delity, and pollination
efciency (for more information on the calcula-
tion of the index, see Johnson et al. 2009). Polli-
nation efciency was dened as the estimated
probability (based on morphological t 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 ve 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 ower visitors in the community
included beetles, birds, butteries, ies, moths,
wasps, solitary bees, and ants (Table 1). Of these
functional groups, solitary bees and ies 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 identications for
insects, a full comparison of the host range of all
ower visitors identied 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 ies, 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 ower 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 ower visitor
groups within the community (43 species)
Table 1. The number of plant species visited by each
ower 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
Buttery2116
Fly 45 16
Honeybee 34 18
Moth 4 3
Wasp 6 7
Notes: In total, there were 82 plant species with ower 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., sawies and bugs).Bold
values indicate honeybees (Apis mellifera)
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STANLEY ET AL.
followed by honeybees (18 species), butteries,
beetles, and ies (16 species each). Using data
from Stanley et al. (unpublished manuscript) that
identied ower 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 336% of the
visits to these species. However, when relative
pollinator abundance, pollen load, host plant
delity, and efciency 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
plantpollinator communities around the world
in terms of pollination networks (Schleuning
et al. 2012), there are almost no studies of whole
plantpollinator 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 owering plant
species in native grassland communities of the
MaputalandPondolandAlbany 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 ower 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
ower 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 ower 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 ower 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
delity 9pollination efciency)
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 laxiora 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 ve which may
reect 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, plantpollinator 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
plantpollinator 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 ower
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 MaputalandPondoland
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 ower visitor networks can provide
only limited insights into the ecological impor-
tance of honeybees. It is well known, for exam-
ple, that not all ower 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 ower 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 ower 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 identied a variety of native South
African species visited by honeybees. As sources
of nectar and pollen, these species are likely to be
www.esajournals.org 8February 2020 Volume 11(2) Article e02957
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 identication: 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 eldwork 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 nal 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 27:142143.
Aizen, M. A., and P. Feinsinger. 1994. Habitat fragmen-
tation, native insect pollinators, and feral honey-
bees in Argentine Chaco Serrano. Ecological Appli-
cations 4:378392.
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 24:8794.
Baldock, K. C. R., J. Memmott, J. C. Ruiz-Guajardo, D.
Roze, and G. N. Stone. 2011. Daily temporal struc-
ture in African savanna ower visitation networks
and consequences for network sampling. Ecology
92:687698.
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. Scientic Reports 7:8389.
Ballantyne, G., K. C. R. Baldock, and P. G. Willmer.
2015. Constructing more informative plantpolli-
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 313:351354.
Bond, W. J. 2016. Ancient grasslands at risk. Science
351:120122.
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 170:151156.
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 142:137143.
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 47:810820.
CEPF. 2010. Ecosystem prole: 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
40:263284.
Dietemann, V., C. W. W. Pirk, and R. Crewe. 2009. Is
there a need for conservation of honeybees in
Africa? Apidologie 40:285295.
Fazier, M., E. Muli, T. Conklin, D. Schmehl, B. Torto, J.
Frazier, J. Tumlinson, J. D. Evans, and S. Raina.
2010. A scientic note on Varroa destructor found in
East Africa; threat or opportunity? Apidologie
41:463465.
Fenster, C. B., W. S. Armbruster, P. Wilson, M. R.
Dudash, and J. D. Thomson. 2004. Pollination syn-
dromes and oral specialization. Annual Review
of Ecology Evolution and Systematics 35:375403.
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 506:364366.
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 339:16081611.
Goulson, D., E. Nicholls, C. Bot
ıas, and E. L. Rotheray.
2015. Bee declines driven by combined stress from
parasites, pesticides, and lack of owers. Science
347:1255957.
Greenleaf, S. S., and C. Kremen. 2006. Wild bees
enhance honey beespollination of hybrid sun-
ower. Proceedings of the National Academy of
Sciences of the United States of America
103:1389013895.
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 ower visitation networks. Diversity
and Distributions 24:5868.
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 91:16931703.
Hargreaves, A. L., S. D. Johnson, and E. Nol. 2004. Do
oral syndromes predict specialization in plant
pollination systems? An experimental test in an
ornithophilousAfrican Protea. Oecologia
140:295301.
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 13:191205.
Jaffe, R., et al. 2010. Estimating the density of honey-
bee colonies across their natural range to ll the
gap in pollinator decline censuses. Conservation
Biology 24:583593.
Johnson, S. D., L. F. Harris, and S
ß. Proches
ß. 2009. Polli-
nation and breeding systems of selected wildow-
ers in a southern African grassland community.
South African Journal of Botany 75:630645.
Johnson, S. D., and R. A. Raguso. 2016. The long-tongued
hawkmoth pollinator niche for native and invasive
plants in Africa. Annals of Botany 117:2536.
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 ower
visitors and as structuring mechanism of ecological
networks. Functional Ecology 27:329341.
Kaiser-Bunbury, C. N., T. Valentin, J. Mougal, D. Mata-
tiken, and J. Ghazoul. 2011. The tolerance of island
plantpollinator networks to alien plants. Journal
of Ecology 99:202213.
Kleijn, D., et al. 2015. Delivery of crop pollination ser-
vices is an insufcient 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 274:303313.
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 71:375387.
Macdonald, I. A. W. 1989. Man's role in changing the
face of southern Africa. Pages 5178 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 271:26052611.
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 Comicepear.
Apidologie 35:575585.
Motten, A. F. 1986. Pollination ecology of the spring
wildower community of a temperate deciduous
forest. Ecological Monographs 56:2142.
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 8:181192.
Ollerton, J., R. Winfree, and S. Tarrant. 2011b. How
many owering plants are pollinated by animals?
Oikos 120:321326.
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
27:141142.
Pannell, J. R., et al. 2015. The scope of Baker's law.
New Phytologist 208:656667.
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 42:652661.
Pirk, C. W. W., U. Strauss, A. A. Yusuf, F. Demares,
and H. Human. 2016. Honeybee health in Africa-a
review. Apidologie 47:276300.
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 25:345353.
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:: 146151.
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 22:19251931.
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 168:278299.
Thomson, J. D., and K. Goodell. 2001. Pollen removal
and deposition by honeybee and bumblebee visi-
tors to apple and almond owers. Journal of
Applied Ecology 38:10321044.
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 efcacy of
Osmia cornuta and Apis mellifera (Hymenoptera :
Megachilidae, Apidae) on red Deliciousapple.
Environmental Entomology 29:235240.
Vrdoljak, S. M., M. J. Samways, and J. P. Simaika. 2016.
Pollinator conservation at the local scale: Flower
density, diversity and community structure
increase ower visiting insect activity to mixed o-
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 inuence of oral traits on
specialization and modularity of plantpollinator
networks in a biodiversity hotspot in the Peruvian
Andes. Annals of Botany 118: 415429.
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 ower colour. Arthropod-
Plant Interactions 6:114.
Wester, P., and S. D. Johnson. 2017. Importance of
birds versus insects as pollinators of the African
shrub Syncolostemon densiorus (Lamiaceae). Botan-
ical Journal of the Linnean Society 185:225239.
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 owers. Ecologi-
cal Entomology 19:271284.
Willmer, P. G., H. Cunnold, and G. Ballantyne. 2017.
Insights from measuring pollen deposition: quanti-
fying the pre-eminence of bees as ower visitors
and effective pollinators. Arthropod-Plant Interac-
tions 11:411425.
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... Smaller bee species readily visit older pollen-depleted flowers in search of this pollen and may as a result be more effective pollinators than honeybees. In a community-level study conducted at the MG site, Stanley et al. (2020) found that honeybees were among the most common floral visitors in the community but were important pollinators of only a small fraction of the plant species studied (Stanley et al., 2020). ...
... Smaller bee species readily visit older pollen-depleted flowers in search of this pollen and may as a result be more effective pollinators than honeybees. In a community-level study conducted at the MG site, Stanley et al. (2020) found that honeybees were among the most common floral visitors in the community but were important pollinators of only a small fraction of the plant species studied (Stanley et al., 2020). ...
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Pollination is a crucial ecological process with far-reaching impacts on natural and agricultural systems. Approximately 85% of flowering plants depend on animal pollinators for successful reproduction. Over 75% of global food crops rely on pollinators, making them indispensable for sustaining human populations. Wind, water, insects, birds, bats, mammals, amphibians, and mollusks accomplish the pollination process. The design features of flowers and pollinators in angiosperms make the pollination process functionally effective and efficient. In this paper, we analyze the design aspects of the honeybee-enabled flower pollination process using the axiomatic design methodology. We tabulate functional requirements (FRs) of flower and honeybee components and map them onto nature-chosen design parameters (DPs). We apply the “independence axiom” of the axiomatic design methodology to identify couplings and to evaluate if the features of a flower and a honeybee form a good design (i.e., uncoupled design) or an underperforming design (i.e., coupled design). We also apply the axiomatic design methodology’s “information axiom” to assess the pollination process’s robustness and reliability. Through this exploration, we observed that the pollination process is not only a good design but also a robust design. This approach to assessing whether nature’s processes are good or bad designs can be valuable for biomimicry studies. This approach can also inform design considerations for bio-inspired innovations such as microrobots.
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This chapter presents an analysis of the impact of neonicotinoids on the bee population. Neonicotinoids are widely used pesticides that are toxic to bees and thus pose a threat to pollinators and bee-dependent ecosystems. The importance and use of neonicotinoids were discussed and the importance of studying their impact on bees was explained. Then, the characteristics of pesticides of this group and their various applications in agriculture and other sectors of the economy are presented. The results of scientific research confirming the toxicity of neonicotinoids to bees were presented. The methods by which these chemicals affect bee organisms and influence their behaviour, health and functioning of bees working in colonies are discussed. The adverse effects of neonicotinoids have been identified at the scale of individual beekeepers and their honeybee colonies. The consequences of neonicotinoid use on bee population dynamics and the role of these pesticides in bee decline and colony breakdown were analysed. The effect of neonicotinoids on biological diversity and ecosystems is an additional factor to consider. The effects of the application of this group of pesticides on other pollinating insects and harmless organisms, as well as the impact on bee-dependent ecosystems, are discussed. The chapter also contains an analysis of the existing legal regulations regarding the use of neonicotinoids and the related controversies. Actions taken to protect bees and alternative approaches to the protection of plants and pollinators were indicated. A summary and conclusions close the chapter, presenting the key results and findings. They point to the need for further research and action to protect bees from the effects of neonicotinoids, which are important for maintaining healthy ecosystems and ensuring the necessary role of pollinators in maintaining biodiversity.
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Pollination services are crucial for maintaining ecological stability and ensuring food security for humans. Managed honey bees, which are economically valuable and are experiencing population growth due to the increasing demand for their products, play a significant role in pollination. To produce high-quality honey, beekeepers often choose natural high meadows, characterized by high plant species richness, for their apiaries. This practice, in turn, may contribute to the pollination of native plants, as managed honey bees are likely to forage on diverse floral resources within these meadows In this study, we investigated the nutritional position of managed bees in the pollination of native plants in Iran using the melissopalynology method to determine the extent of their contribution to the pollination of native plants. Ninety-four honey samples were collected from beekeepers located in the natural pastures of two biodiversity hotspots in Iran (Zagros and Alborz). Then, plant pollens were extracted from the honey and photographed by scanning electron microscopy. In the next step, plant species were identified, and their abundance was calculated. The results showed that managed bees visited 54 plant genera, seven of which were non-native plants. Additionally, more plant species and the highest abundance of pollen were observed at altitudes ranging from 1000 to 3000 m. Therefore, beekeepers set up their hives in this altitude range to obtain high-quality honey. In general, in this study, the results of melissopalynological analysis, involving the identification of plant genera and pollen counts, revealed that managed honey bees likely contributed less than 3% to the pollination of native plant species in Iran.
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Insects, the most abundant creatures on earth, both in terms of number and diversity are often taken for granted by the masses due to either negligence or the annoyance that a few species create. Insects are an imperative part of the majority of the food webs that exist across the globe and also play a significant role in the functioning of the ecosystem. Moreover, insects regulate environmental sustainability in many ways such as by pollinating plants, cycling up nutrients, maintaining the structure and fertility of solum, decomposing various organic matter, etc. However, this harmony is now disturbed due to the worldwide increase in anthropogenic activities in the last few decades, leading to significant biodiversity losses in insects. Global pollution, climate change, and habitat demolition are some of the major causes of insect decline. Thus, to maintain the ecological balance and for our survival also, new and efficient efforts on the conservation of insects and their diversity are needed immediately.
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The structure of pollination networks is described for two oceanic islands, the Azorean Flores and the Mauritian Ile aux Aigrettes. At each island site, all interactions between endemic, non-endemic native and introduced plants and pollinators were mapped. Linkage level, i.e. number of species interactions per species, was significantly higher for endemic species than for non-endemic native and introduced species. Linkage levels of the two latter categories were similar. Nine types of interaction may be recognized among endemic, non-endemic native and introduced plants and pollinators. Similar types had similar frequencies in the two networks. Specifically, we looked for the presence of 'invader complexes' of mutualists, defined as groups of introduced species interacting more with each other than expected by chance and thus facilitating each other's establishment. On both islands, observed frequencies of interactions between native (endemic and non-endemic) and introduced pollinators and plants differed from random. Introduced pollinators and plants interacted less than expected by chance. Thus, the data did not support the exist- ence of invader complexes. Instead, our study suggested that endemic super-generalist species, i.e. pollinators or plant species with a very wide pollination niche, include new invaders in their set of food plants or pollinators and thereby improve establishment success of the invaders. Reviewing other studies, super generalists seem to be a widespread island phenomenon, i.e. island pollination networks include one or a few species with a very high generalization level compared to co-occurring species. Low density of island species may lead to low interspecific competition, high abundance and ultimately wide niches and super generalization.
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The western honey bee (Apis mellifera) is the most frequent floral visitor of crops worldwide, but quantitative knowledge of its role as a pollinator outside of managed habitats is largely lacking. Here we use a global dataset of 80 published plant-pollinator interaction networks as well as pollinator effectiveness measures from 34 plant species to assess the importance of A. mellifera in natural habitats. Apis mellifera is the most frequent floral visitor in natural habitats worldwide, averaging 13% of floral visits across all networks (range 0-85%), with 5% of plant species recorded as being exclusively visited by A. mellifera For 33% of the networks and 49% of plant species, however, A. mellifera visitation was never observed, illustrating that many flowering plant taxa and assemblages remain dependent on non-A. mellifera visitors for pollination. Apis mellifera visitation was higher in warmer, less variable climates and on mainland rather than island sites, but did not differ between its native and introduced ranges. With respect to single-visit pollination effectiveness, A. mellifera did not differ from the average non-A. mellifera floral visitor, though it was generally less effective than the most effective non-A. mellifera visitor. Our results argue for a deeper understanding of how A. mellifera, and potential future changes in its range and abundance, shape the ecology, evolution, and conservation of plants, pollinators, and their interactions in natural habitats.
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Aim Habitat fragmentation and alien species are among the leading causes of biodiversity loss. In an attempt to reduce the impact of forestry on natural systems, networks of natural corridors and patches of natural habitat are often maintained within the afforested matrix, yet these can be subject to degradation by invasion of non‐native species. Both habitat fragmentation and alien invasive species disrupt the complex interaction networks typical of native communities. This study examines whether an invasive plant and/or the fragmented nature of the forestry landscape influences natural flower visitation networks ( FVN s), flower–visitor abundance and richness or flower/visitor species composition. Location The species rich and diverse grasslands in the KwaZulu‐Natal Midlands, South Africa is under threat from transformation, particularly by commercial forestry plantations, restricting much of the remaining untransformed grasslands into remnant grassland patches ( RGP s). Remaining patches are under additional threat from the invasive Rubus cuneifolius Pursh (bramble). Sites were established in RGP s and in a nearby protected area ( PA ), with and without brambles present for both areas. Results Flower abundance and flower area of native plant species were greater within RGP than in PA , but only in the absence of R. cuneifolius . Flower–visitor assemblages differed between invaded and uninvaded sites and also differed between PA and RGP sites. Both areas lost specialist flower–visitor species in the presence of brambles. Network modularity was greatly reduced by the presence of bramble, indicating a reduction in complexity and organization. The structure of FVN s was otherwise unaffected by presence of bramble or being located in RGP s or the PA . Main conclusions The RPG s contribute to regional biodiversity conservation through additional compositional diversity and intact FVN s. Rubus cuneifolius reduces ecological complexity of both RGP s and PA s, however, and its removal must be prioritized to conserve FVN s.
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Accurate predictions of pollination service delivery require a comprehensive understanding of the interactions between plants and flower visitors. To improve measurements of pollinator performance underlying such predictions, we surveyed visitation frequency, pollinator effectiveness (pollen deposition ability) and pollinator importance (the product of visitation frequency and effectiveness) of flower visitors in a diverse Mediterranean flower meadow. With these data we constructed the largest pollinator importance network to date and compared it with the corresponding visitation network to estimate the specialisation of the community with greater precision. Visitation frequencies at the community level were positively correlated with the amount of pollen deposited during individual visits, though rarely correlated at lower taxonomic resolution. Bees had the highest levels of pollinator effectiveness, with Apis, Andrena, Lasioglossum and Osmiini bees being the most effective visitors to a number of plant species. Bomblyiid flies were the most effective non-bee flower visitors. Predictions of community specialisation (H2′) were higher in the pollinator importance network than the visitation network, mirroring previous studies. Our results increase confidence in existing measures of pollinator redundancy at the community level using visitation data, while also providing detailed information on interaction quality at the plant species level.
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Using our accumulated datasets from Kenyan savanna, Mediterranean garigue, UK gardens and heathland, involving 76 plants from 30 families, we present detailed data to quantify the superiority of bees as pollinators of most flowering plants when compared with other flower visitors. Bees provided the majority of visits to study species at all sites, and 33 of the 76 plants received more than 90% of their visits from bees. Furthermore, pollen deposition onto stigmas from single-visit events (SVD, a measure of pollination effectiveness) was significantly higher for bees than non-bees at all the four sites where a major proportion of the flora was sampled. Solitary bees, and also bumblebees in temperate habitats, were the best potential pollinators for most plants in this respect, and significantly out-performed honeybees. Only a few plants were well served by bombyliid flies, and fewer again by larger hoverflies, butterflies, or solitary wasps. Bees also achieved better matches of their visit timing to peak pollen availability (measured indirectly as peak SVD), and made much shorter visits to flowers than did non-bees, permitting a substantially greater visit frequency. Additionally, they deposited significantly lower levels of potentially deleterious heterospecific pollen on stigmas in heathland and Mediterranean garigue, though not in the UK garden with densely clustered high-diversity flowering, or in the Kenyan savanna site with particularly dispersed flowering patches and some specialist non-bee flowers. Our data provide a novel and quantified characterisation of the specific advantages of bees as flower visitors, and underline the need to conserve diverse bee communities.
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Based on the ready availability of nectar and pollen, and on the large numbers and great diversity of insect visitors, species in the Apiaceae have been labeled promiscuous. The distinction between floral visitors and effective pollinators, however, is extremely important and is rarely discerned. Floral visitation was documented for plants of nine populations in a comparative study of three species of the closely related apioid genera, Thaspium Nutt. and Zizia Koch. A pollinator importance index was calculated for each floral visitor using visitor abundance, pollen load composition and foraging behavior as its basic components. Results showed that, despite a high diversity of insect visitors, generally 1–4 species accounted for a minimum of about 74% of the pollinations in all populations. This specialization in pollination appears in part to be the result of an oligolectic relationship between Andrena ziziae (Hymenoptera; Andrenidae) and plants of the taxa studied, but solitary bees of Andrenidae, Colletidae and Halictidae in general were efficient and important pollinators. This study emphasizes that visitation records, when considered alone, effectively disguise specialization in the pollination system.
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Flowers visited by a broad assemblage of animals may nevertheless be considered to have a specialized pollination system if pollen deposition is effected mainly by a subset of these visitors. The importance of a particular animal group for pollination derives mainly from the relative rate of floral visitation and per-visit effectiveness for pollen deposition. We assessed the relative importance of birds and insects for pollination of the African shrub Syncolostemon densiflorus (Lamiaceae). Flower visitors were observed to evaluate their visitation rates. Virgin flowers were exposed to single visits by nine animal visitor groups to evaluate their effectiveness at depositing pollen on stigmas. We selectively excluded birds and larger insects from flowers to assess the contribution of smaller visitors to pollen deposition and seed set. Sunbirds and insects visited flowers at a similar frequency, but on a per-visit basis, sunbirds deposited more pollen on stigmas than did any of the insect groups, including honeybees, long-proboscid flies, butterflies and day-flying hawkmoths. Selective exclusion of birds and larger insects resulted in a large decline in pollen deposition on stigmas and seed production. These results show that S. densiflorus is pollinated mainly by sunbirds, despite its attraction of a broad assemblage of insect flower visitors. These findings highlight the importance of per-visit pollination effectiveness and selective exclusion for understanding the ecological importance of different flower visitors.