Introduction
As one of the most valuable pollinators, bumble bees are vitally
important to productivity for both natural and agricultural systems
(Hegland & Totland, 2008; Garratt et al., 2014). They are distributed
world-wide in temperate climates (Williams & Osborne, 2009). An
increasing number of papers have suggested that high priority should be
given to their conservation due to the serious risk of declines (Goulson
et al., 2008a, 2015; Williams et al., 2009; Roulston & Goodell, 2011).
A main cause for bumble bee decline is the decrease of floral resources
(Roulston & Goodell, 2011; Goulson et al., 2015; Thomson, 2016); there
is strong evidence that floral resources significantly influence
abundance of bumble bees (reviewed in Roulston & Goodell, 2011 and
Goulson et al., 2015) and that responses to floral resources can be
species-specific (Ogilvie et al., 2017). However, the interspecific
interactions of bee species in response to changing floral resources
still need to be explored, as they are fundamental for understanding the
patterns and mechanisms of bee decline in this changing world (Thomson,
2016).
It was suggested that two or more bumble bee species coexisting in a
plant community may have to obey rules for partitioning the limited
floral resources through competitive interactions (Inouye, 1978;
Heinrich, 1976; Ranta & Lundberg, 1980), and niche differentiation in
bumble bee proboscis length and flower use could be be an effective way
of partitioning resources (Heinrich, 1976; Inouye, 1980; Pyke, 1982).
Matching of proboscis length and flower depth was identified as a key
component for the resource partitioning among bumble bee species
(Inouye, 1977; Ranta et al., 1981; Pyke, 1982). Therefore, differences
in proboscis length may influence niche relations and community
structure for bumble bee species (Ranta & Vepsalainen, 1981; Pyke,
1982; Pyke et al., 2012). On this basis, a classic hypothesis was
postulated that coexistence would be difficult for bumble bee species
with similar proboscis length in a community (Inouye, 1977, 1978, 1980;
Pyke, 1982; Ishii et al., 2008). However, studies also indicated that
the structure of bumble bees may also depend on the community’s temporal
and spatial factors rather than niche differentiation in proboscis
length and flower use (Ranta & Lundberg, 1980; Ranta & Vepsalainen,
1981; Pyke et al., 2012; Miller-Struttmann & Galen, 2014). However,
studies revealed that multiple bumble bee species with similar proboscis
length can coexist in a community with few differences in their
abundance (Ranta, 1982, 1984; Ranta & Tiainen, 1982; Williams, 1989;
Goulson & Darvill, 2004). This indicated that the interspecific
interactions within a community of bumble bees are more complex than
previously thought.
The intensity of interspecific competition among bumble bee species was
thought to be highly environment-dependent (Ranta & Lundberg, 1980).
For example, Ranta et al. (1981) showed that the niche overlaps of the
bumble bees were smaller in a northern (unstable environment) than in
the southern community (more stable environment) in
Fennoscandinavia.
Moreover, the foraging strategy of bumble bees displayed a high level of
plasticity in response to changes in landscape factors and floral
resource diversity (Jha & Kremen, 2013). However, whether and how
interspecific competition influences the foraging strategy of bumble
bees in a scenario of changing floral resources remains unclear, but is
fundamental for understanding the coexistence of multiple bumble bee
species. Thus it may be important to incorporate a phenological
component to study of their resource use, as abundance of bees in the
annual colonies changes markedly during the course of the summer.
Nutritional requirement was proved to be a key force in shaping foraging
strategy and floral preference for bumble bees (Vaudo et al., 2016),
which is not surprising given the impact of diet on their colony health
(Roger et al., 2017). Different bumble bee species may vary in
nutritional requirements, which would force them to prefer different
plant species for comprehensive nutrition intake (Pyke, 1982; Goulson et
al., 2005; Hanley et al., 2008; Moerman et al., 2016; Woodard, 2017).
Given that pollen and nectar of flowering plants provide different
nutrients for pollinators (reviewed in Baker & Baker, 1983; Roulston &
Cane, 2000), bumble bees may differ in preference for pollen or nectar,
and thus preferentially forage on different plants since some plants do
not provide nectar (Konzmann & Lunau, 2014). For the bumble bees that
forage preferentially for pollen rather than nectar, niche
differentiation in proboscis length and flower use may not be important
in partitioning of floral resources, although such mechanisms are not
well studied. Detecting the influence of intensity of interspecific
competition for floral resources on foraging strategy of mainly
pollen-seeking bumble bees should provide a good perspective to
understand their community structure.
In this study, we hypothesized that the intensity of interspecific
competition may influence foraging strategy of bumble bees. On one hand,
the niche differentiation in proboscis length and flower use might not
be stationary, but depend on the degree of competition. Alternatively,
the foraging preference for pollen or nectar might also be plastic when
coexisting species reduce the available floral resources. To understand
better the factors influencing community structure and the coexistence
of bumble bees with similar proboscis lengths, it is necessary to
consider study sites where the level of spatiotemporal variability is
minimal, or sites are sufficiently isolated that immigration should not
be significant (Pyke et al., 2012). To test the hypothesis, we conducted
field investigations on a relatively
isolated alpine meadow in the
eastern Himalayan of Yunnan Province, China, a world top biodiversity
hotspot. Three Bombus species, namely, B. friseanus,B. lepidus and B. festivus were the most abundant species,
and their proboscis lengths (workers and males) vary from about 6 to 10
mm. Specifically, the main objectives of the study are: (i). what is the
pattern of partitioning of floral resources by the three bumble bees?
(ii). whether and how the niche differentiation in proboscis length and
flower use is influenced by intensity of interspecific competition for
the three bumble bees; and (iii). whether and how the intensity of
interspecific competition influences foraging preference between pollen
and nectar for the three bumble bees.