Introduction
Bees are important pollinators of a variety of crops and wildflowers,
with their ecosystem services being valued at \euro153 billion
(Gallai, Salles, Settele, & Vaissière, 2009). Honey bees have been
introduced for crop pollination around the globe, and when present,
contribute to approximately 19% of all crop plant visits in a region
(Hung, Kingston, Albrecht, Holway, & Kohn, 2018). Wild bees are also
known to contribute to increases in fruit production for
pollinator-dependent crops (Garibaldi et al., 2013), and similar
environmental factors contribute to both honey bee and wild bee health
and conservation (Evans, Smart, Cariveau, & Spivak, 2018). The
taxonomic identity and relative abundance of floral resources collected
by bee species can vary through time (Baum, Rubink, Coulson, & Bryant,
2004; Wood, Kaplan, & Szendrei, 2018). In addition, foraging strategies
that facilitate the collection of resources, such as nectar and pollen,
are variable among bee species (Rollin et al., 2013; Saleh & Chittka,
2007; Visscher & Seeley, 1982). To facilitate pollinator conservation,
it is imperative to understand how foraging strategy influences patterns
of resource collection.
Polylectic bees with an extended foraging season, such as honey bees and
bumble bees, must navigate variable spatial and temporal resource
availability challenges (Goulson, 1999). Pollen provides the primary
source of macronutrients such as protein, lipids, sterols, and minerals,
which are important for the growth and development of bee larvae and
colonies (Avni, Hendriksma, Dag, Uni, & Shafir, 2014; Di Pasquale et
al., 2013; Moerman, Vanderplanck, Fournier, Jacquemart, & Michez, 2017;
Roulston & Cane, 2002). However, not all plant pollen is equivalent in
the relative amount of nutrients or their ratios (Roulston, Cane, &
Buchmann, 2000; Ruedenauer, Spaethe, Kooi, & Leonhardt, 2019).
Generalist bees, therefore, have to collect pollen from a variety of
plant taxa to maintain a nutritional balance that ensures appropriate
growth and development (Filipiak et al., 2017), and to mitigate other
stressors such as infection from parasites (Di Pasquale et al. 2013).
Collecting pollen from a variety of plant taxa can be a challenge in
high intensity agricultural landscapes, and low diversity in collected
pollen can reduce colony growth rate (Hass et al., 2019). The foraging
strategy of bees, such as the presence of dance communication for honey
bees and the trapline foraging of bumble bees, may help bees navigate
such challenges and ensure the collection of an adequate diversity of
pollen resources in their diet.
Both honey bees and bumble bees are generalist central place foragers
that must locate, collect, and return to the nest with a diverse array
of resources to provision the colony. A major foraging strategy employed
by honey bees is dance communication, whereby scouts and successful
foragers transmit information regarding the distance and direction to
profitable resource patches (Seeley, Camazine, & Sneyd, 1991; Visscher
& Seeley, 1982; Von Frisch, 1967). This strategy facilitates large
scale recruitment to profitable resources, such as blooms of monoculture
crops (Rollin et al., 2013). In contrast, bumble bee individuals develop
and follow trapline foraging routes among known resource patches,
‘majoring,’ while simultaneously monitoring for changes in resource
availability through ‘minor’ routes (Bernd, 1979; Ohashi & Thomson
2009; Pasquaretta, Jeanson, Andalo, Chittka, & Lihoreau, 2017;
Woodgate, Makinson, Lim, Reynolds, & Chittka, 2017). Trapline foraging
by bumble bees is considered an optimal foraging strategy whereby
individual bees learn, over successive foraging bouts the location of
profitable resource patches and develop efficient routes that minimize
distances traveled (Lihoreau et al., 2012; Woodgate et al., 2017). Based
on these distinct foraging strategies, we expect honey bees to forage at
monofloral resource patches, while individual bumble bees will disperse
more evenly among all available resources, as has previously been
observed in other agricultural systems (Rollin et al., 2013). We thus
predict that bumble bees will be less flower constant relative to honey
bees on individual foraging trips, where flower constancy is defined as
the proportion of foraging bees that collect a single pollen morphotype
during individual foraging bouts.
The frequency of flower constancy by individual bees can affect the
richness and diversity of pollen collected at the colony level, along
with the distribution of foragers among available resource patches. As
bumble bees individually learn the location of rewarding flowers, and we
expect individuals to collect from a greater number of plant types in
single foraging bouts, we predict a greater richness of pollen collected
by bumble bee colonies compared to honey bees. Furthermore, there is
evidence indicating that bumble bees show preference for pollen
resources, and that these preferences are sustained within and among
colonies in a shared landscape (Saifuddin & Jha, 2014). Such
preferences could lead to increased evenness among the collected
resources, and hence to greater pollen diversity. In contrast, we expect
most honey bee foragers to be recruited to resources based on their
abundance in the landscape (Rollin et al., 2013; Visscher & Seeley,
1982), as opposed to demonstrating preferences, where a plant type would
be visited more often than predicted based on its abundance. If we
assume unequal abundance of plant types in the environment, we expect a
lower evenness among collected resources, and together with lower
species richness, lower pollen diversity for pollen collected by honey
bees compared to bumble bees.
In the current study, we examined the pollen foraging behavior of honey
bees (Apis mellifera ) and bumble bees (Bombus impatiens )
in a shared landscape. We collected pollen from returning foragers of
each bee species over five time periods at each of three sites in a
suburban-agricultural landscape. We quantified the frequency of flower
constant foragers, and the richness and diversity of pollen collected by
colonies. In addition, we examined bees’ preferences by comparing pollen
collected to resources available. We tested the following predictions
derived from the known foraging strategies for these two bee species: i)
bumble bees are less flower constant relative to honey bees during a
foraging trip; ii) bumble bee colonies collect a greater richness of
pollen types relative to honey bees, along with greater pollen diversity
and iii) honey bees forage randomly while bumble bees exhibit
preferences for some plant types. Results are discussed in terms of
differences in bee foraging strategies and how understanding such
differences may be used to improve pollinator habitat and facilitate
increased productivity in pollinator-dependent crops.