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Arthropod-Plant Interactions

, Volume 11, Issue 3, pp 257–261 | Cite as

Specialist bees collect Asteraceae pollen by distinctive abdominal drumming (Osmia) or tapping (Melissodes, Svastra)

  • James H. Cane
Original Paper

Abstract

Four species of western US Osmia (3 Cephalosmia) that are Asteraceae specialists (mesoleges) were observed using a stereotypical means of collecting pollen—abdominal drumming—to gather pollen from 21 flowering species representing nine tribes of Asteraceae. Abdominal drumming is a rapid dorso-ventral motion of the female’s abdomen (467 pats/min) used to directly collect and place pollen in the bee’s ventral scopa. A co-occurring generalist, O. lignaria, never drummed Asteraceae flowers for pollen, but instead used its legs to harvest pollen. Observed drumming by several other osmiines is noted. A different pollen-harvesting behavior, abdominal tapping, is described for two eucerine bees (Melissodes agilis and Svastra obliqua), both oligolectic for the Asteraceae. The behavior also involves a dorso-ventral motion, but they tap their distal abdominal venter against disk flowers at a slower tempo (304 taps/min). These females’ distal sternites have distinctly dense and long hair brushes for acquiring pollen by this behavior. Brief accounts of similar abdominal pollen gathering behaviors by other megachilids are summarized.

Keywords

Bees Apiformes Megachilidae Foraging Grooming 

Introduction

The world’s 16,000+ known species of non-parasitic bees collect and transport pollen as well as nectar (and sometimes oils) to feed their progeny (Michener 2007). Given the great diversity of sizes and morphologies of flowers in general, and anthers and pollen in particular, it is no surprise that bees employ a variety of behaviors, structures, and hair morphologies to collect, groom, transfer, and transport pollen back to their nests (Jander 1976; Thorp 2000). New and distinctive combinations of morphologies and behaviors for pollen collection, particularly by oligolectic (pollen specialist) bees, continue to be found and reported (e.g., Müller 2008).

Research by the late Dr. Charles Michener contributed substantial new insights into bee behavior, most notably the evolution of sociality. Over the decades, he also published studies of bees’ nesting and foraging behaviors and their attendant morphologies. In one unassuming paper (Michener 1962), he was the first to report floral sonication (so-called buzz pollination) by bees, compiled from his field notes taken in five tropical countries. Obviously, sonication of poricidal anthers by bees was available for others to see and hear, but it was Dr. Michener who appreciated the significance of this distinctive pollen-harvesting behavior. His report opened up an entire field of productive inquiry, stimulating several hundred published studies with contributions from every continent. In the spirit of honoring Dr. Michener’s interest in characterizing new pollen-foraging behaviors of bees, the following study characterizes two stereotypical foraging behaviors—abdominal drumming and tapping—described here for several pollen specialists among Osmia, Melissodes, and Svastra bees.

Bees that forage at flowers of the Asteraceae contend with secondary pollen presentation (Yeo 1993). The small flowers (florets) composing a capitulum (flowerhead) have tubular corollas within which the anthers are joined in a cylinder. Pollen is presented in one of two ways (Fig. 48 in Yeo 1993). It is commonly transferred from the inserted anthers to a stylar brush (i.e., pollen presenter or “Pseudo-Staubblatt”) borne by the pair of styles as they elongate beyond the staminal tube (e.g., Centaurea). Alternatively, pollen is presented by a piston mechanism (e.g., Senecio), whereby pollen is pushed out of the cylinder on the tips of the styles (“Nudelspritze”). Either mechanism presents pollen where bees can pick it up actively and/or passively on ventral surfaces as they walk about the capitulum surface probing for nectar.

Materials and methods

Bees’ visitation and handling behaviors were sought at diverse species of Asteraceae. Females of all three bee genera were seen collecting pollen from wild hosts around the region and at several cultivated species grown in our laboratory’s research garden. In addition, annual Asteraceae representing other tribes were presented to female Osmia nesting in the greenhouse. These were started from seed in the winter greenhouse, advancing their typical summer bloom to coincide with the natural springtime emergence of three Osmia species. Two of these (Osmia californica Cresson and O. montana Cresson) collect pollen from multiple tribes of the Asteraceae (Rust 1974), and so are mesolectic (Cane and Sipes 2007). For comparison, the third species (O. lignaria Say) is a floral generalist (polylege) (Rust 1974). All were wintered at our laboratory. Because only nesting females collect pollen, relatively few females were placed in a large greenhouse cage along with a few males, abundant supplemental bloom, and drilled wooden nesting blocks. Oligolectic species of Melissodes and Svastra bees were only observed at Asteraceae growing in our common garden, not the greenhouse, as their subterranean nests are immovable.

Floral handling behaviors by pollen-collecting females were observed directly, as well as during playbacks of digital video recordings taken using slow-motion macrovideography (Exilim ZR710 camera, Casio Computer Co., Japan). Speed was 240 frames/s, slowing action by 7.8×. Playback speed was checked by filming a running stopwatch. Drumming and tapping tempos were timed during playback. Numbers are reported as mean ± standard error. Plants and bees were identified as needed using published keys and comparison with museum specimens. Representative bee vouchers are deposited with the USDA-ARS bee collection at PIRU. Exserted heights of floral styles were measured with calipers. For simplicity and clarity, I will refer to plant species in the text by just their genus name if only one species is included in Table 1. Morphologically, the third major body division of a bee is by definition a part of the abdomen more accurately called the “metasoma,” a term only familiar to melittologists (Michener 2007).
Table 1

Pollen-collecting behaviors of four species of Osmia bees visiting species in diverse tribes of Asteraceae

Asteraceae tribe

Taxon

Osmia species

polylege

mesolege

lignaria a

californica a

montana a

colora densis b

Anthemideae

Tanacetum densum

   

Drum

Ursinia anethoides

Leg stroke

Drum

Drum

 

Astereae

Brachycome iberidifolia

Leg stroke

   

Cardueae

Centaurea cyanus, montana

 

Drum

Drum

 

Cirsium foliosum

   

Drum

Calenduleae

Calendula officinalis (2 var)

Leg stroke

Drum

Drum

 

Osteospermum grandiflorum

Leg stroke

Drum

Drum

 

Cichorieae

Crepis occidentalis

   

Drum

Taraxacum officinale

  

Leg stroke

 

Coreopsideae

Coreopsis basalis

 

Drum

Drum

 

Cynareae

Xeranthemum annuum

Leg stroke

Drum

Drum

 

Eupatorieae

Ageratum houstonianum

Leg stroke

   

Gnaphalieae

Helichrysum roseum

Leg Stroke

   

Helenieae

Chaenactis douglasii

 

Drum

Drum

 

Helenium amarum

Leg stroke

Drum

Drum

 

Heliantheae

Balsamorhiza sagitatta, macrophylla

 

Drum

Drum

 
 

Gaillardia pulchella

 

Drum

Drum

 
 

Helianthella uniflora

   

Drum

 

Helianthus annuus

 

Drum

Drum

 
 

Tithonia rotundifolia

 

Drum

Drum

 
 

Viguiera multiflora

 

Drum

Drum

 
 

Wyethia amplexicaulis

 

Drum

Drum

 

Senecioneae

Senecio triangularis c

    

aSubgenus Cephalosmia

bSubgenus Helicosmia

cDrummed by O. subaustralis

Results and discussion

Abdominal drumming for pollen

Four species of Osmia were seen drumming flowers of 21 species representing nine tribes of the Asteraceae (Table 1). Drumming, as defined here, is a rapid, vigorous dorso-ventral motion of the abdomen, typically against disk flowers of the Asteraceae (movie at Online Resource 1). While drumming, the bee slowly walks about the capitulum, usually probing for nectar simultaneously. Multiple females were seen drumming each floral host. Drumming directly places pollen in the scopal hair brushes that megachilid bees use to transport pollen back to their nests (Fig. 1). The behavior (as “patting”) had been briefly noted before for O. californica and O. montana (Cripps and Rust 1989; Cane 2005). A summer-flying Osmia, O. coloradensis, was encountered drumming additional wild Asteraceae species (Table 1). One uncommon species, O. subaustralis, was only encountered at Senecio triangularis, whose disk flowers it also drummed for pollen.
Fig. 1

Female O. californica bee collecting pollen from disk flowers of H. annuus. Notice the pollen load in the scopa under her abdomen, and the pairs of curled floral styles that secondarily present the pollen

In the greenhouse, abdominal drumming by O. californica and O. montana at potted sunflower (H. annuus) cultivars could be seen (Fig. 1), characterized and videotaped in more detail (movie at Online Resource 1). Their rhythmic drumming was very rapid (467 ± 18 pats/min, n = 20 recorded bouts, species pooled). They drummed disk flowers ninefold faster than they probed them for nectar (56 ± 6 probes/min) (movie at Online Resource 1). Their pace of probing flowers for nectar is more akin to that reported for Megachiloides fortis (Megachilidae) working wild sunflowers (120 florets/min) (Neff and Simpson 1990). Foraging O. lignaria never drummed any Asteraceae flowers, but rather stroked the exserted styles with their legs to collect pollen (Table 1). Some greenhouse offerings representing other tribes were not visited by the specialist Osmia (e.g., Gazania, Gerbera, Ageratum).

Abdominal drumming has been noted for some additional megachilid taxa. The European oligolege O. (Hoplosmia) spinulosa was seen collecting pollen from diverse species of Asteraceae using a “seesawing” motion of the abdomen (pg. 302 in Müller 1994). At Pulicaria (Asteraceae), Pseudoanthidium eximium (Anthidiini: Megachilidae) was seen “rapidly seesawing” to collect pollen (Müller 1996). At one Utah site, a much smaller megachild bee, Heriades cressonii, was found regularly drumming the small flowers of Erigeron divergens (Astereae). However, drumming is far from universal among megachilid bees, despite abdominal scopae being ubiquitous among the non-parasitic forms. For example, Neff and Simpson (1990) observed Megachile fortis passively acquiring sunflower pollen while nectaring, then using their legs to periodically groom and wipe accumulated bodily pollen into their ventral scopae. The taxonomic limits and range of contexts for abdominal drumming across the Megachilidae await formal investigation.

At a few Asteraceae hosts, mesolectic Osmia collected pollen differently. Instead of drumming flowers of Taraxacum, 13 of 14 O. montana females used their hind legs to pull the ligulate flowers’ styles under their abdomens to wipe off the presented pollen. Cripps and Rust (1989) mentioned this same pollen-collecting behavior for the bee O. lignaria. At Centaurea montana, which has especially tall, widely spaced styles, O. montana females also pulled floral styles under their abdomens (1–3 at a time), but then drummed their tips to remove pollen (movie at Online Resource 2). Müller (1996) mentioned that three species of oligolectic anthidiine bee species collected pollen of other Centaurea by this same method. These alternative behaviors are associated with two qualities of the floral styles, height and suppleness. The height of the style tip above the surface on which the bee can walk is maximal for C. montana (30 mm). Styles are far shorter for other exemplar species that Osmia drummed (e.g., C. cyanus and Helianthus—5 mm, Coreopsis—3 mm). Thistles (Cardueae) are long-styled too (Torres 2000), but their styles form a dense brush on which the bee can walk, enabling drumming (Table 1). Styles of Taraxacum are closely spaced amid a thicket of ligules. These styles are not particularly tall (Torres 2000), but they seem exceedingly supple, perhaps favoring wiping over drumming. Which floral traits actually trigger drumming remains a mystery.

Abdominal tapping for pollen

Females of two oligolectic eucerine bees, M. agilis and S. obliqua (Apidae), were regularly seen collecting pollen in a similar way from Helianthus annuus (movie at Online Resources 3), Echinacea angustifolia (movie at Online Resource 4), and Ratibita columnifera (all tribe Astereae). While walking forward, foragers collected pollen by rhythmically tapping the disk flowers with the distal venter of their slightly decurved abdomen. The dorso-ventral motion is akin to drumming by the four Osmia species, but noticeably slower, their tempo averaging 304 ± 18 taps/min (16 videotaped bouts of both species’ females). This behavior was briefly mentioned as “tummy-tapping” by Simpson and Neff (1987). Abdominal tapping accumulates pollen into dense brushes of long, erect, unbranched hairs on metasomal sternites 3–5 of these two species (Fig. 2). From there, females then transfer pollen to the hairy scopae on their hind legs for transport back to the nest (movie at Online Resource 3). Compared with some other sunflower bees, these two specialist bees are unsurpassed pollinators, as measured in terms of either seeds set per second foraging on the capitulum (S. obliqua) (Neff and Simpson 1990) or seed-set per capitulum visit (M. agilis) (Parker 1981). Abdominal tapping and drumming seem certain to regularly transfer pollen to stigmatic surfaces, likely explaining why female M. agilis are fourfold more effective than males in pollinating sunflower (Parker 1981).
Fig. 2

Abdominal venter of S. obliqua, showing the thick brushes of long hairs on metasomal segments 3–5

Most other Melissodes and all Svastra seem to be oligolectic for a tribe of two of the Asteraceae (Hurd et al. 1980), and so probably use abdominal tapping to collect pollen as well. Likely exceptions include M. tristis (Hurd et al. 1980) and M. dagosa, many individuals of which have floral labels from the Fabaceae, not the Asteraceae, in the PIRU collections. The brushes on their metasomal sterna are much less developed than those described here (Fig. 2), with some hairs either branched (M. dagosa) or wavy-tipped (M. tristis). Six oligolectic European species of another eucerine genus, Tetraloniella, collect pollen from styles of Inula (Asteraceae) by an alternative motion; they rapidly telescope their metasomal segments in and out (Müller 2008).

Dorso-ventral abdominal patting has been reported for several oligolectic bees working other kinds of flowers. Westrich (1989) briefly described two megachilids abdominally “dabbing” composite flowers of Inula (Osmia) and Tanacetum (Heriades), as well as a Chelostoma species “dabbing” Ranunculus (buttercup) anthers. Another megachilid, Hoplitis (Formicapis) robusta, collected pollen by “seesawing” their abdomens against anthers of Potentilla flowers (Rosaceae) (Müller and Mauss 2016). Females of the narrowly oligolectic oil-bee, Macropis nuda (Melittidae), were seen rapidly patting their abdomens against the staminal columns of their host, Lysimachia ciliata (Primulaceae), while using their forelegs to mop floral oils (Cane et al. 1983). Another Helianthus oligolege, Dieunomia triangulifera (Halictidae), was reported to pat disk flowers for pollen (Minckley et al. 1994). As with the two eucerines, these bees then transfer the collected pollen to hind leg scopae for transport back to the nest.

Clearly, individual bees can have multiple methods for obtaining pollen from different flowers, and in turn, a given flowering species can attract multiple bee species employing different methods for pollen acquisition (Table 1). Thus, O. montana drums flowers of multiple species of Heliantheae, but then wipes anthers of Taraxacum. Congeneric O. lignaria never drums Asteraceae flowers. At H. annuus, two mesolectic Osmia drum, two oligolectic eucerines tap, and most other visitors do not actively use their abdomens to collect pollen. The relative trade-offs and efficacies of these different pollen-collecting strategies, and the stimuli that trigger them, offer opportunities for future comparative study.

Documentation using today’s convenient digital videography would confirm whether these (and other) bee species employ what I describe as “abdominal tapping” or the more rapid drumming behavior, or whether other distinctive, stereotypical pollen-foraging behaviors are being used by oligolectic bees at their floral hosts. Mere written descriptions without videographic documentation can be difficult to align with these specific behaviors, especially those published in other languages.

Notes

Acknowledgements

I thank Byron Love for assistance in the greenhouse and the field, particularly with plant propagation, plus several observations of drumming. Andreas Müller was an invaluable guide to the European literature, and with John Neff, provided insightful reviews. These behaviors were discussed with Zach Portman, who is reviewing pollen-handling behaviors of bees. Marianne Harris kindly helped nurture greenhouse seedlings. I am forever grateful to Charles Michener, who set my path and opened doors in the field of melittology while serving as a gentle yet inspirational role model to generations of young bee biologists like me.

Supplementary material

Movie 1

Movie clip of paint-marked O. montana drumming flowers of H. annuus. Recorded in the greenhouse in real time (MP4 1358 kb)

Movie 2

Movie clip of O. montana working flowers of C. montana for pollen. Recorded outdoors in slow motion (1/8 speed) (MP4 10237 kb)

Movie 3

Movie 3. Movie clip of M. agilis tapping disk flowers of H. annuus for pollen. Recorded outdoors in real time (MP4 3280 kb)

Movie 4

Movie 4. Movie clip of S. obliqua tapping disk flowers of E. angustifolia for pollen. Recorded outdoors in slow motion (1/8 speed) (MP4 5641 kb)

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Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2016

Authors and Affiliations

  1. 1.USDA-ARS Pollinating Insect Research Unit (PIRU)Utah State UniversityLoganUSA

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