Research Article |
Corresponding author: Zachary M. Portman ( zportman@gmail.com ) Academic editor: Michael Ohl
© 2019 Zachary M. Portman, Michael C. Orr, Terry Griswold.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Portman ZM, Orr MC, Griswold T (2019) A review and updated classification of pollen gathering behavior in bees (Hymenoptera, Apoidea). Journal of Hymenoptera Research 71: 171-208. https://doi.org/10.3897/jhr.71.32671
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Pollen is the primary protein and nutrient source for bees and they employ many different behaviors to gather it. Numerous terms have been coined to describe pollen gathering behaviors, creating confusion as many are not clearly-defined or overlap with existing terms. There is a need for a clear yet flexible classification that enables accurate, succinct descriptions of pollen gathering behaviors to enable meaningful discussion and comparison. Here, we classify the different pollen gathering behaviors into two main classes: active and incidental pollen collection. Active pollen collection is subdivided into six behaviors: scraping with the extremities, buzzing, rubbing with the body and/or scopae, rubbing with the face, tapping, and rasping. In addition to the active and incidental pollen gathering behaviors, many bees have an intermediate step in which they temporarily accumulate pollen on a discrete patch of specialized hairs. Each behavior is described and illustrated with video examples. Many of these behaviors can be further broken down based on the variations found in different bee species. Different species or individual bees mix and match these pollen collecting behaviors depending on their behavioral plasticity and host plant morphology. Taken together, the different behaviors are combined to create complex behavioral repertoires built on a foundation of simple and basic steps. This classification sets the groundwork for further research on various topics, including behavioral plasticity in different species, comparisons between generalists and specialists, and the relative effectiveness of different pollen gathering behaviors.
Pollinators, pollen collection, foraging behavior, floral specialization, oligolecty, floral hosts, Anthophila
Bees visit flowers primarily for nectar and pollen, which they use as provisions for their young and to meet their own energetic and nutritional requirements (
Pollen-gathering behavior in bees has historically been divided into two main types: active and incidental (or passive) collection (
While pollen gathering behavior has previously been reviewed by others, these works tend to focus on such disparate fields as the phenological, chemical, and morphological adaptations of bees to flowers (
Pollen gathering videos were recorded by ZMP and MCO as well as gathered from other researchers or sources (e.g. youtube.com) and used with permission. To record behavior, we used a Sony A65 with a 90mm macro lens and a Pentax Optio WG-2. Scanning electron microscope images were taken with a Quanta FEG 650 Scanning Electron Microscope. Morphological terminology generally follows
We broadly surveyed the literature for descriptions of pollen gathering behavior. We combined keyword searches in google scholar with manual searching of older literature from the literature collection of the Pollinating Insect Research Unit. Selecting appropriate terminology proved difficult because every pollen gathering behavior has been referred to by multiple different terms. In general, three main considerations were taken into account in selecting the most appropriate terminology for the different pollen gathering behaviors: priority (first known instance of use), usage (prevalence of a term in the scientific and popular literature), and accuracy (how well a term describes a given behavior). Exceptions were made for usage and accuracy, particularly when terms had conflicting or multiple meanings, or when a particular usage is widely accepted.
We define pollen gathering behaviors as the movements that bees use to acquire, actively or incidentally, pollen from anthers or other pollen presenting structures. Pollen gathering is related to, but separate from, pollen transport, which refers to the carrying of accumulated pollen back to the nest in specialized transport structures (
In foraging from flowers, bees have three possible primary purposes on each trip: to acquire nectar (or oil), pollen, or both. We term pollen gathering active when pollen is the primary objective or when nectar (or oil) and pollen are co-objectives. Active pollen gathering is broken down into six pollen gathering behaviors as described below. We term pollen gathering incidental when nectar is the primary objective and pollen is passively accumulated on the body. The bee then “decides,” based on pollen and floral characteristics, and on need, to discard or keep the pollen. Bees may also incidentally collect pollen on non-target areas of the body while actively gathering pollen. Such pollen may or may not be gathered into the pollen transporting structures.
Active pollen gathering behaviors can be broken up into six types, listed loosely in order of prevalence:
Scraping with the extremities: use of the legs or mouthparts to remove pollen directly from anthers, or, less commonly, to glean pollen from flowers.
Buzzing: use of the flight muscles to vibrate a flower to assist with pollen release.
Rubbing with the body and/or scopa(e): the gathering of pollen through direct and more or less continuous contact with the anthers by the main trunk of the body (thorax, abdomen) and/or the scopal hairs.
Tapping: picking up pollen from anthers by a rapid up and down motion of the abdominal venter.
Rubbing with the face: continuous and more or less direct contact with the anthers by the face.
Rasping: rubbing of the thoracic dorsum against anthers, causing the anthers to vibrate and release the pollen.
Incidental pollen gathering (not broken down into types): the use of pollen that has accumulated on the body either through nectar gathering or on non-target areas as a result of a primary pollen gathering behavior. A major component of incidental behavior is the degree of movement by the bee, which influences the amount of pollen that adheres to the bee through contact.
Scraping with the extremities refers to the use of the legs and/or mouthparts (including biting with the mandibles) to gather pollen with a repetitive unidirectional motion (Figure
Scraping pollen directly from the anthers or other pollen-presenting structures with the basitarsal brushes of the forelegs is the most common pollen gathering method used by bees (
One term that refers to scraping with the forelegs – “scrabbling” – is particularly problematic because it has apparently adopted two different meanings. In the original, and most well-accepted usage, it refers to scraping with the forelegs and mandibles (
The mouthparts are also frequently used to gather or loosen pollen. The mandibles are most often used to bite anthers to loosen the pollen in tandem with scraping with the forelegs (
The midlegs are generally used to assist the forelegs in scraping pollen (
Scraping movements are also made with the hind legs, particularly on keel-shaped flowers. In these cases, the hind legs appear to be used because the front and middle legs are occupied in obtaining purchase and spreading the wing petals to expose the anthers. Various Andrena (Andrenidae), Anthophora (Apidae), Apis, Bombus, and megachilids use these behaviors on keel-shaped flowers such as Collinsia (Plantaginaceae) and Lupinus (Fabaceae) (
In bees that gather pollen primarily by rubbing with the body and/or scopae (discussed in a later section), the hind legs are often used in an accessory fashion to gather a clump of anthers and draw them to the body, as well as to help scrape pollen from the gathered anthers. This gathering and scraping behavior is seen in Megachilidae such as Osmia cornuta (Latreille) (
Bees that scrape with the extremities often possess morphological features that improve their efficiency. Many examples of hooked hairs on the forelegs and especially the foretarsi are associated with specialization on flowers with narrow corollas (
Similar to the forelegs, the mouthparts (primarily the stipes, galea, and labial and maxillary palpi) can be modified, often with hooked hairs, to extract pollen from flowers with narrow corollas. The presence and use of modified hairs on the mouthparts have been reviewed by
Buzzing, commonly referred to by the suboptimal terms “buzz pollination” and “floral sonication,” is the use of the thoracic flight muscles to generate audible vibrations that aide in accessing and collecting pollen from a flower (Figure
Here, we focus primarily on terminology because the extent and occurrence of buzzing behavior has been reviewed by others (see
Terminology used to refer to buzzing in the literature. This list is not comprehensive; instead, it focuses on the first usage of terms and major works on buzzing.
Term used | Genus or Species | Floral Host | Citation |
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“einer gewaltsamen Vibration des Insektenkörpers und zugleich der ganzen Blüte” [a violent vibration of the insect body and at the same time the whole flower] | Bombus (Apidae) | Senna (Fabaceae) |
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“die Bienen … versetzen die Blüte in starke Vibration, so dass der Pollen aus den Antheren herausgeschüttelt” [the bees… cause the flower to vibrate strongly, causing the pollen to be shaken out of the anthers] | Augchlora (Halictidae), Oxaea (Andrenidae), Ptiloglossa (Colletidae), Xylocopa (Apidae) | Senna, Physalis (Solanaceae), Solanum (Solanaceae) |
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“the worker seizes the anthers with her mandibles and first two pairs of legs, and shakes them, emitting an impatient buzz, as if angry because the stamens do not give up their pollen at once” | Anthophora (Apidae), Bombus | Rosa (Rosaceae), Rubus (Rosaceae) |
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“vigorous whirrings” and “whirring method” | Bombus, Megachile (Megachilidae) | Melampyrum (Orobanchaceae) |
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“while…collecting pollen…she makes the continuous sound that has been compared with that of a honey-bee caught in a spider’s web” | Amegilla (Apidae) | Not specified |
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“vibrar las anteras” [“vibrates the anthers”] | Bombus, Xylocopa | Not specified |
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“vibrating the flowers with rapid leg movements accompanied by a high pitched hum” | Not specified | Solanum [as Lycopersicon] (Solanaceae) |
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“buzz,” “buzzing,” “buzzing behavior,” and “vibrate” | Various Andrenidae, Apidae, and Halictidae | Cassia (Fabaceae), Solanum |
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“buzzing,” “buzzing behavior,” and “buzzing technique” | Various Apidae, Colletidae, and Halictidae | Cassia |
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“vibrate the anthers” | Various Apidae, Andrenidae, and Colletidae | Solanum |
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“vibratory pollen collection” and “wing vibration” | Bombus, various Halictidae | Dodecatheon (Primulaceae) |
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“buzz,” “buzzing,” and “buzzing behavior” | Agapostemon (Halictidae) | Chamaecrista (Fabaceae), Solanum |
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“buzzed the anthers” and “vibrate the anthers” | Caupolicana (Colletidae), Ptiloglossa | Datura (Solanaceae), Solanum |
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“vibrate their wings” | Bombus terricola Kirby | Solanum, Spiraea (Rosaceae) |
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“buzz (vibratile) pollination,” “buzzing,” and “buzzing technique” | Centris (Apidae), Melipona (Apidae) | Senna [as Cassia] |
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“vibratory behavior” and “vibrated anthers” | Various Apidae and Halictidae | Chamaecrista [as Cassia] |
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“vibration of the thorax” | Anthophora, Augochlorella (Halictidae), Bombus, Psaenythia (Andrenidae), Xylocopa | Solanum |
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“buzz,” “buzzing,” and “vibrated the anthers while emitting a buzzing sound” | Bombus | Rosa, Solanum, Vaccinium (Ericaceae) |
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“buzz,” “buzz pollination,” “buzzing,” “buzzing behavior,” and “vibratile pollination” | Anthophora, Bombus, Colletes, Xylocopa. Also, Volucella (Syrphidae) | Solanum |
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“buzz,” “’buzz’ pollination,” “buzzing,” “shivering,” “vibratile pollination,” and “vibrational pollination” | Not specified | Solanum |
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“wing vibration” and “wing vibration method” | Bombus | Echeandia (Asparagaceae) |
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“buzz pollination,” “buzzing,” “buzzing behavior,” and “vibratory behavior,” | Not specified | Not specified |
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“buzzing” and “vibratile behavior” | Not specified | Not specified |
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“high frequency wing vibrations” and “vibrating” | Bombus | Pedicularis (Orobanchaceae) |
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“buzz pollination,” “buzzing,” “floral vibration,” “vibratile pollination,” and “vibratile technique” | Euglossa (Apidae), Paratetrapedia (Apidae) | Mouriri (Melastomataceae) |
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“buzz,” “buzz pollination,” “buzzing behavior,” “buzzing, “vibratile pollen harvesting,” “vibratile manipulation,” “vibrational pollination,” “vibrating,” and “floral vibration” | Various Apidae, Andrenidae, Colletidae, Halictidae, Melittidae | Various plant families |
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“thoracic vibration” and “vibrate” | Lasioglossum (Halictidae) | Hibbertia (Dilleniaceae) |
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“buzzing technique” | Stenotritidae | Not specified |
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“buzz-pollination” and “floral sonication” | Bombus | “poricidally dehiscent, nectar-free flowers” |
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“buzz,” “buzz pollination,” “buzz or vibratile pollen foraging” “buzzing,” “buzzing behavior,” “floral buzzing,” and “floral sonication” | Bombus, Melitta americana (Smith) (Melittidae) | Vaccinium |
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“buzz,” “buzz pollination,” “buzzing,” “buzzing behavior,” “floral buzzing,” “floral vibration,” “vibratile methods,” “vibratile pollen-collecting behavior,” “vibratile pollen harvesting,” “vibratile foraging behavior,” “vibrating,” “vibratory pollen-collecting behavior,” “vibratory manner,” and “vibratory pollen harvesting” | Bombus, Eucera [as Xenoglossa] (Apidae), Megachile, Xylocopa | Asteraceae, Cucurbitaceae, Papaveraceae, Rosaceae, Scrophulariaceae |
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“buzz,” “buzz pollination,” “buzzing,” and “vibratory pollen collection” | Bombus | Actinidia (Actidiniaceae), Borago (Boraginaceae), Polygonatum (Asparagaceae), Symphtum (Boraginaceae) |
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“buzz,” “buzzing,” and “sonicate” | Bombus, Habropoda (Apidae) | Vaccinium |
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“thoracic vibration,” “vibratile behavior,” and “vibratile pollen-harvesting” | Megachile | Chamaecrista |
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“buzz,” “buzz-harvesting,” “buzz-milking,” “buzz pollination,” “buzzing,” and “sonicate” | Protandrena mexicanorum (Cockerell) (Andrenidae) | Solanum |
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“buzz,” “buzzing,” “floral sonication,” “sonicate,” and “vibratile buzzes” | Bombus, Ptiloglossa | Solanum |
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“buzzing,” “buzz-collection” | Various | Various |
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“buzzing” | Not specified | Not specified |
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“floral sonication” and “sonicate” | Not specified | Not specified |
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“buzz,” “buzz pollination,” “buzzing,” “buzzing behavior,” “sonication,” “sonication behavior,” “vibratile or buzz pollination,” and “vibrating” | Various Andrenidae, Apidae, Colletidae, Halictidae, Megachilidae, Melittidae, and Stenotritidae | Various floral hosts |
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Members of all bee families have been documented using buzzing behavior, though it is uncommon or rare in Andrenidae, Melittidae, and Megachilidae (
Rubbing with the body and/or scopae refers to the use of direct, more or less continuous contact between the anthers and the scopae and/or venter of the main body segments (thorax or abdomen). The defining character of rubbing with the body and/or scopae is the curling of the abdomen, which generally moves in an up and down motion, or less often, a back-and-forth or telescoping motion (Figure
Rubbing with the body and/or scopae. A Andrena sp. (Andrenidae) rubbing with the abdomen and scopae on Camissonia (Onagraceae) B Ptilothrix bombiformis (Cresson) (Apidae) rubbing with the abdomen and scopae on Hibiscus (Malvaceae) C, D Melissodes sp. (Apidae) rubbing with the abdomen on Helianthus (Asteraceae) E, F Andrena helianthi Robertson rubbing with the abdomen on Helianthus G, H Macropis sp. (Melittidae) rubbing with the venter of the thorax and abdomen on Lysimachia (Primulaceae).
Genus or Species | Behavior Description | Floral Host | Citation |
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Family Andrenidae | |||
Protoxaea gloriosa (Fox) | Holding the anthers against the abdominal venter and hind legs and shaking them while rotating the body | Kallstroemia (Zygophyllaceae) |
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Andrena erigeniae Robertson | “pollen was … rubbed from the anthers onto the bee’s body and legs” | Claytonia (Montiaceae) |
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Andrena sp. | Rubbing with abdominal and hind leg scopae | Camissonia (Onagraceae) | Figure |
Family Apidae | |||
Eucera (Tetralonia) fulvescens (Giraud) [as Tetralonia dufouri [sic]] | “tummy-tapping” | Asteraceae |
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Eucerini spp. | “tummy-tapping” | Asteraceae |
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Melitoma spp. | “scraping [anthers] with the hind legs” | Ipomoea (Convolvulaceae) |
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Ptilothrix bombiformis (Cresson) | “pollen was worked into the scopae” | Hibiscus (Malvaceae) |
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Ptilothrix fructifera (Holmberg) | “brush the anthers [between the midlegs, hindlegs, and abdomen]” | Opuntia (Cactaceae) |
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Svastra obliqua (Say) | “tummy-tapping … with the distal portion of the abdominal venter” | Asteraceae |
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S. obliqua and Melissodes agilis Cresson | “rhythmically tapping … with the distal venter of their slightly decurved abdomen” | Asteraceae |
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Family Colletidae | |||
Perditomorpha brunerii Ashmead | “pollen grains were also scraped directly from the anthers with the scopal setae on the abdominal sterna” | Malvaceae |
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Tetraglossula bigamica (Strand) | “rubbing the abdomen against the anthers” | Ludwigia (Onagraceae) |
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Family Halictidae | |||
Dieunomia triangulifera (Vachal) | “waggling the abdomen vigorously from side to side” | Helianthus (Asteraceae) |
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D. triangulifera | “tapping the heads of the disc flowers with the ventral surface of the metasoma” | Helianthus |
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Nomiinae spp. | “tummy-tapping” | Asteraceae |
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Systropha planidens Giraud | “they rapidly moved their abdomen up and down” | Convolvulus |
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Family Megachilidae | |||
Hoplitis anthocopoides (Schenck) | “she vibrates [the abdomen] back and forth rapidly against the anthers while her hind legs also move back and forth against the anthers and scopa” | Echium (Boraginaceae) |
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H. anthocopoides, H. producta (Cresson), Megachile relativa Cresson, Osmia caerulescens (L.) [as O. coerulescens (L.)] | “rapidly contracts and expands her abdomen, accordion fashion, over the anthers” | Echium |
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O. lignaria Say, Megachile spp. | “filaments are held between the hind legs and … raked against the scopal hairs” | Collinsia (Plantaginaceae) |
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Hoplitis simplex (Cresson) | “scrapes pollen directly from the anthers into her abdominal scopa using her hind legs while tapping the anthers with her abdomen” | Nemophila (Boraginaceae) |
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Ochreriades fasciatus (Friese) | “repeatedly tap their metasomal scopa directly against the anthers” | Ballota (Lamiaceae) |
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Family Melittidae | |||
Hesperapis regularis (Cresson) | “scraping [with the scopae]” | Clarkia |
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H. regularis | “rapid lateral oscillations of the abdomen” | Clarkia |
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Macropis nuda (Provancher) | “patting motions of the metasoma” | Lysimachia (Primulaceae) |
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M. fulvipes (Fabricius) | “females pressed the ventral side of the abdomen (by bending) against the anthers” | Lysimachia |
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Gathering pollen directly with the abdomen and/or scopae has been known since at least the late 1800’s though it was not described in detail (
Most bees that gather pollen via rubbing take up the pollen directly with the abdominal scopa (e.g. Megachilidae) or by a combination of the hind leg scopae and abdomen (e.g. Ptilothrix and Andrena sp. – Figure
Finally, various mentions in the literature suggest that rubbing behavior has been observed in additional species but precise enough descriptions for confirmation are lacking, and many of these could refer to tapping (see next section). This includes suggestions of rubbing by Osmia lignaria, O. indeprensa Sandhouse, and O. kincaidii Cockerell (“the anthers are drawn to the scopal hairs by the hind legs,”
Tapping refers to the act of picking up pollen through a rapid up and down motion of the abdominal venter directly against the anthers (Figure
Tapping behavior in the literature. All bee species are in Megachilidae.
Genus or Species | Behavior Description | Floral Host (all Asteraceae) | Citation |
Heriades spp. | “l’abdomen qui tapote de haut en bas sur les étamines” [the abdomen taps up and down on the stamens] | Asteraceae |
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Osmia montana Cresson | “a rapid thumping movement of the abdomen” | Helianthus |
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O. californica Cresson and O. montana | “very rapidly tapping the abdominal scopa against the composite disk anthers” | Asteraceae |
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O. californica | “tamp their abdomens” | Balsamorhiza, Helianthella, Helianthus |
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Megachile melanopyga Costa and M. octosignata Nylander | “rapid up and down movements [of the abdomen]” | Centaurea |
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O. californica | “patting the flowers with their abdominal venters” | Balsamorhiza |
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Heriades truncorum (L.) | “moving the abdomen rapidly up and down” | Asteraceae |
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O. californica and O. montana | “rapidly drumming or patting their abdomens up and down against the pollen-bearing floral styles” | Balsamorhiza |
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O. californica, O. coloradensis Cresson, O. montana, O. subaustralis Cockerell, Heriades cressoni Michener (as H. cressonii) | “drumming” | Various Asteraceae |
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Heriades crenulatus Nylander, Lithurgus chrysurus Fonscolombe, Pseudoanthidium literatum (Panzer), Trachusa dumerlei (Warncke) | “the rapid movement of their abdomen up and down” | Centaurea |
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Wainia eremoplana (Mavromoustakis) | “rapid up and down movements of the metasoma” | Asteraceae |
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Osmia sp. | Tapping with the abdominal scopa | Asteraceae | Figure |
Historically, “rubbing” and “tapping” with the abdomen have often been lumped together (e.g.
In this behavior, the face (anterior head) is used to gather pollen through direct, continuous rubbing contact with the anthers (Figure
Additional and recent examples of bees with modified facial pilosity that gather pollen from nototribic flowers include Lasioglossum tropidonotum McGinley (
Rasping is defined as rubbing anthers with the thoracic dorsum by moving the entire body in and out of the flower, causing vibrations which release pollen (Figure
Genus or species | Behavior Description | Floral Host | Citation |
Pseudomasaris vespoides (Cresson) (Vespidae) | “[the anthers] rub against the thoracic surface” | Penstemon (Plantaginaceae) |
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Hymenoptera spp. | “the anthers have teeth that rasp against the back and wings of the pollinator” | Penstemon |
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Osmia spp. | “the deliberate rubbing of their backs against the anthers” | Penstemon |
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O. brevis Cresson | “rasping” | Penstemon |
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When pollen accumulates on a bees body as a by-product of another behavior without any obvious deliberate pollen gathering movements related to that area, it is termed incidental (Suppl. material
Incidental pollen collection is always a secondary behavior that occurs when a bee performs a primary behavior such as nectar collecting, oil collecting, or another pollen collecting behavior. Incidental pollen gathering is further characterized by the accumulation of pollen on generalized body hairs rather than specifically on a specialized brush or patch of hairs. This is particularly relevant when incidental buildup occurs during other primary behaviors such as rubbing or tapping, where pollen is incidentally accumulated on non-target areas. The amount of pollen actually picked up depends on the degree of contact with the anthers and the hairiness of the bee (
A major component of incidental pollen gathering is the degree of movement exhibited by the bee, since the act of moving over or through anthers invariably results in the incidental accumulation of pollen. The degree of movement represents a continuum, encompassing bees that move simply to reach the next anther or nectary and bees that seem to purposefully move as a means to rapidly accumulate additional pollen on their bodies. For example, on open flowers such as Cornus (Cornaceae), Daucus (Apiaceae), and Spiraea (Rosaceae), Bombus wade rapidly over flowers with their mid and hind legs and abdomen appressed in a way that maximizes the incidental collection of pollen, although the primary active mode of pollen gathering is still scraping with the forelegs (
Most bees appear to use incidental pollen collection to supplement their primary pollen gathering behaviors. For example, many groom off the incidentally accumulated pollen between flower visits and pack it into their pollen transport structures. However, some species appear to collect the majority of their pollen incidentally. For example, Megachile fortis Cresson gathers pollen by accumulating it on the body while foraging for nectar (
In addition to the seven main pollen gathering behaviors, temporarily accumulating pollen on a specialized patch of hairs represents an important intermediate step in the pollen gathering behavior of many bee species (Suppl. material
Specialized hairs on the venter of the thorax of A Perdita turgiceps Timberlake (Andrenidae) with specialized hairs on the fore-coxae (left) and ventral mesepisternum (right) and B Protandrena maculata Timberlake (Andrenidae) with specialized hairs on the ventral mesepisternum (left) and hind-coxae (far right). Specimens are positioned belly-up, with the head to the left. Scale bars: 200 micrometers.
Panurgine (Andrenidae) bees documented to temporarily accumulating pollen.
Genus or species | Floral host | Citation |
Anthemurgus passiflorae (Robertson) | Passiflora (Passifloraceae) |
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Calliopsis subalpina Cockerell | Sphaeralcea (Malvaceae) | Suppl. material |
Macrotera mortuaria (Timberlake) | Arctomecon (Papaveraceae) | Suppl. material |
M. opuntiae (Cockerell) | Opuntia (Cactaceae) |
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M. texana Cresson | Opuntia |
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Panurginus polytrichus Cockerell | Polylectic |
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Perdita floridensis Timberlake | Ilex (Aquifoliaceae) |
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P. gerhardi Viereck | Monarda (Lamiaceae) |
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P. halictoides Smith | Physalis (Solanaceae) |
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P. minima Cockrell | Euphorbia (Euphorbiaceae) | Suppl. material |
P. multiflorae Parker | Mentzelia (Loasaceae) | Suppl. material |
P. octomaculata (Say) | Solidago (Asteraceae) |
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P. sphaeralceae Cockerell | Sphaeralcea | Suppl. material |
P. spp. | Prosopis (Fabaceae) |
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Rhophitulus anomalus (Moure and Lucas de Oliveira) [as Cephalurgus anomalus] | Malvaceae |
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Temporarily accumulating pollen in a specialized hair patch is well-documented in Panurginae (Table
In addition to panurgines, other bee groups temporarily accumulate pollen but the behavior is not as well-documented. Trigona (Apidae) also load the specialized hair patch on the thoracic venter with the forelegs, but appear to transfer pollen to the corbiculae while hovering (
Finally, temporarily accumulating pollen in genal hair baskets has been observed in some bee groups, but it is not clear whether these baskets are loaded by directly scraping against pollen or are loaded with the forelegs. This is seen in Perdita subgenus Heteroperdita, specialists on Tiquilia (Boraginaceae) (
The pollen gathering behaviors of bees are not rigid, stereotyped actions performed in isolation. Instead, bees combine different behaviors, mixing and matching them depending on their behavioral repertoires and the morphology of their host plants. The use of different behaviors on flowers with different morphologies has been well-demonstrated in Apis and Bombus, which will switch between collecting pollen either actively via scraping or incidentally depending on the floral host (
In addition to using different behaviors on the same or different hosts, many bees perform multiple pollen gathering behaviors simultaneously. For example, Andrena helianthi on Helianthus (Figure
While some bees display flexibility in pollen gathering behavior, others have more limited behavioral suites. One might expect generalist bees to have a broader suite of pollen gathering behaviors than specialist bees. Social bees in particular are expected to be more versatile in their pollen gathering behavior compared to solitary bees because their colonies are active for longer periods and must therefore utilize a broad array of successively blooming plants (
The repertoire of pollen gathering behavior of bee species may influence their floral host choices. For example, some specialists have limited ability to collect pollen from alternative hosts even though their larvae can develop on alternative pollen sources (
In contrast, some other specialist bees readily gather pollen from alternative hosts, particularly in times of pollen shortage (
Evidence suggests that there is a relationship between pollen gathering behavior and host plant preference. For example, rasping and rubbing with the face are associated with nototribic flowers (
Although some behaviors are associated with particular host plants or floral types, the diversity of pollen gathering behaviors on a given host plant make clear that there is not necessarily a “right way” to gather pollen from a particular host plant. For example, on Helianthus, honey bees gather pollen incidentally while nectaring, generalist Lasioglossum gather pollen by scraping with the forelegs, Osmia californica gather pollen by tapping with the scopae, and Melissodes gather pollen by rubbing with the abdomen and scopae. These behavioral differences could potentially be explained by a number of reasons. For example, specialist behaviors such as tapping could be more efficient at particular hosts but less efficient at gathering from alternative hosts (
Pollen gathering behavior in bees is a complex process that involves the mixing and matching of different behaviors depending on the behavioral repertoire of a given bee species and the floral morphology of host plants. Despite this complexity, pollen gathering can be broken down into two broad categories, “active” and “incidental,” with active pollen gathering further divided into six subtypes. In addition, there is an intriguing intermediate step found in disparate groups that involves temporary accumulation of pollen on a discrete patch of specialized hairs. It is our hope that this updated classification of pollen gathering behavior will enable effective communication and comparison of future research, particularly given the rise of low cost, high definition video recording devices.
Despite the abundance of behavioral observations, the breadth and flexibility of pollen gathering behaviors remain poorly understood. Learning more about the behavior of specific species can help shed light on the evolution of pollen gathering, particularly how behaviors such as rubbing with the abdomen and/or scopa(e), tapping, and rasping evolved and whether they are consistently associated with specific hosts or floral morphologies. Further, it is not clear why some specialist bees have broad behavioral flexibility, while others appear to have much more rigid repertoires. Similarly, it’s not clear why some generalists have a smaller breadth of behaviors, particularly the apparent inability of Apis and Trigona to buzz flowers. Examining the tradeoffs between behavioral breadth and pollen gathering efficiency, as well as the genetic and physiological bases of these behavioral limitations, could shed light on these questions. Towards this end, a comprehensive dataset of the pollen-gathering behaviors of different bee species is needed.
One of the biggest unanswered questions is whether specialized behaviors are more effective at gathering pollen, either by increasing the efficiency of pollen uptake or by allowing bees to perform more than one behavior simultaneously, such as gathering pollen and nectar simultaneously (
We thank the many people who engaged in discussions or pointed to further resources: Skyler Burrows, Jim Cane, Brian Rozick, Avery Russell, and Irmgard Schäffler. Special thanks to Vince Tepedino for reviewing early drafts of the manuscript. Robert Klips and sigma1920HD graciously contributed videos from YouTube. We thank Jack Neff and Claus Rasmussen, whose comments and suggestions helped improve and clarify this manuscript. Harold Ikerd and Skyler burrows assisted with the identification of Andrena helianthi and A. chlorogaster. This work was funded in part by the National Science Foundation Graduate Research Fellowship under grant number DGE-1147384 to ZMP. We acknowledge the support from the Microscopy Core Facility at Utah State University for the SEM work.
Scraping with the extremities
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Buzzing
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Rubbing with the body and/or scopae
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Tapping
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Rubbing with the face
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Rasping
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Incidental pollen gathering
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Temporary accumulation of pollen by panurgine bees
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Temporary accumulation of pollen by melittid bees
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