Honey Bee Dancing at Belwin

Researchers conducted flower surveys and collected flowers within Belwin's reconstructed prairies to aid their study.

Excerpted from the article published February 12, 2020. Read the complete paper online at https://doi.org/10.1371/journal.pone.0228169

Many insect populations around the world have faced rapid declines in recent decades due to human-induced landscape changes, including massive increases in the area of land devoted to monocrop agriculture [1,2,3,4]. Declines in bee populations in particular have raised alarm because of the essential pollination services that bees provide [5,6], contributing to the global economy and improving human nutrition by making diverse fruits and vegetables cheaper to grow [5]. The most widely managed crop pollinator species, Apis mellifera L., the European honey bee, contributes an estimated $14 billion yearly in pollination services in the United States alone [7]. In recent years, beekeepers have seen increased honey bee colony mortality in several regions, including the United States [8,9].

While exposure to pathogens, parasites, and pesticides undoubtedly contribute to high colony mortality, poor nutrition likely plays a key role [6,9,10,11,12,13,14]. Like all bee species, honey bees require both pollen, their primary source of proteins and lipids, and nectar, their primary source of carbohydrates [15,16,17]. In temperate regions, colonies may need to collect an estimated 25 kg of pollen [17,18] and potentially over 300 kg of nectar [19] to function during the summer and survive the cold winters. In addition to quantity, diet quality is also very important. Diverse pollen sources help honey bees combat pathogens and parasites [20,21,22,23] and increase their ability to detoxify pesticides [24]. Colonies living in the temperate zone must respond to frequent changes in the species of blooming flowers from spring to fall [25,26] and may experience periods of dearth where temperatures remain high but few rewarding flowers bloom [27,28].

Researcher Morgan K. Carr holds a sugar-water feeder and marks honey bees in order to get them to go back to the observation hives and waggle dance for known distances. “That gave us calibration data, or relationship between distance and waggle run duration in their dances, that we used when mapping waggle dances for flowers,” she says.

Many groups around the world are interested in helping maintain healthy bee populations by planting flowers for bees [29,30,31]. Simultaneously, many organizations are more broadly interested in restoring native habitats that had been converted to agriculture or other human uses [32]. Before European colonization, the Upper Midwest of the United States mainly consisted of prairie lands, defined as temperate grasslands with a moderate rainfall and deep-rooted perennial forbs [33,34]. Today less than 2% of the original prairies remain [34], and there is great interest in restoring native prairie habitats [35]. Unfortunately, governments and organizations interested in helping bees often have limited information about how different land management schemes [36] or seed mixes [29] will affect bee foraging success. Prairie restoration projects are very likely to benefit native bee species, especially bees that specialize on prairie flowers [37,38,39]. It is less clear to what extent non-native honey bees will be attracted to and use patches of flowers in reconstructed prairies.

Honey bees’ unique life cycle and foraging strategy may affect their use of flowering resources in prairies. Honey bees are generalist foragers that have a very wide foraging range, with most foraging trips occurring within 4 km of the nest [40,41,42,43] but some trips as far as 14 km away [44,45]. Honey bee colonies contain thousands of foragers that can communicate with each other about the locations of the most rewarding patches of flowers using a signal called a waggle dance, a behavior unique to bees in the genus Apis [26,44]. This signal involves repeated figure-eight runs in which the dancer waggles her abdomen back and forth during the straight middle portion of the figure-eight, called the waggle run. The waggle run provides dance follower bees with a vector containing both the direction of the flower patch relative to the azimuth of the sun and the distance to the patch [44]. Foragers will only dance to advertise the locations of flower patches that they perceive as profitable (having a favorable ratio of nutrients gained to energy expended) [46]. These characteristics of honey bee foraging behavior may lead colonies to focus on the densest patches of flowers and ignore sparser flowers within non-rewarding grasses, as is common in reconstructed prairie habitats. However, the density and size of flower patches in prairies change across the season as different species of flowers bloom. Even if honey bee foragers only perceive flowers in prairies as profitable resources during part of the foraging season, access to prairies may boost colony health by supplying nectar or pollen when there is a dearth of non-prairie food sources [47].

The honey bee waggle dance provides us with a window into how honey bee foragers perceive the resources that they encounter in the landscape around their hives [36]. At the level of the colony, the proportion of dances advertising flower patches in a given habitat serves as a measure of the decision-making process that allocates foragers among habitat types based on their relative profitability [36]. At the level of the individual, if a forager brings back food from a particular species of flowers and dances to advertise the site that she visited, it indicates that she perceived those flowers as sufficiently profitable to recruit nestmates. It is currently feasible to determine which flower taxon was advertised in a dance from the pollen that the dancer carried but not from nectar carried by dancers [48,49]. In addition, characteristics of dances advertising nectar sources can give more nuanced information about the perceived profitability of the resource. The total number of waggle runs that a nectar dancer performs in a dance is correlated with her assessment of the profitability of the resource advertised [46]. This relationship has been demonstrated multiple times with artificial sugar-water feeders [50,51,52], but so far has not been demonstrated with pollen or pollen substitutes ([53] but see [54]). Multiple studies have also shown that colonies tend to advertise sites at greater distances in order to find profitable nectar sources during dearth periods [27,40,42,55].

Therefore, we took advantage of the information in honey bee waggle dances to answer two main questions about how honey bee colonies perceive flowers in prairie habitats: first, is there any part of the season in which the foraging force of a honey bee colony will devote a large proportion of its recruitment efforts (waggle dances) to pollen or nectar sources within prairies? To better understand seasonal changes in the proportion of dances advertising prairies, we asked two additional questions: 1) During times of year when a large proportion of nectar dances advertise sources within prairies, do dances for prairie sites include more waggle runs and thus indicate a higher perceived profitability than dances for sites outside of prairies, and 2) Is there a seasonal change in the average distance of advertised nectar sources? For our second main question, we asked whether honey bee foragers will advertise patches of native prairie flowers as high-quality pollen sources, and, if so, which taxa will they advertise? To answer these questions, we placed honey bee colonies in glass-walled observation hives with access to two large, reconstructed prairies. The glass-walled hives allowed us to record the dances performed by members of these colonies throughout the summer and early fall. From these recordings we decoded the direction and distance information within the dances, mapped them as probability density distributions using a Bayesian modeling approach [56], and determined what percentage of the dances advertised sites within prairies during different parts of the season. At sites with a seasonal change in the proportion of dances for food sources in prairies, we also quantified waggle runs per dance to determine if the bees perceived the prairie flowers as more profitable compared to flowers outside of prairies. We also explored whether there were seasonal changes in the average distance of advertised nectar sources. Finally, to both map and identify the taxa that the foragers considered to be profitable pollen sources, we captured a subset of dancing bees who were carrying pollen loads and identified the pollen source using microscopy and DNA barcoding.

Continue reading: https://doi.org/10.1371/journal.pone.0228169_


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