Canadian Journal of Arthropod Identification

Cleptoparasitic Bees of the Genus Epeolus Latreille (Hymenoptera: Apidae) in Canada

CJAI 30 -- March 30, 2017

Thomas M. Onuferko

| Abstract | Introduction | Methods | Taxonomy & Biology | Checklist | Keys to species | Acknowledgments | References | PDF | Cite |


Specimens of Epeolus species are similar to those of Triepeolus in general appearance, and males can be particularly difficult to distinguish. In Epeolus, the male pygidial plate is generally wider basally, with the lateral margins convergent toward the apex (e.g. as in Epeolus ainsliei Crawford [Figure 1a] and E. olympiellus Cockerell [Figure 1b]). In Triepeolus, the pygidial plate is generally comparatively narrow (e.g. as in Triepeolus pectoralis (Robertson) [Figure 1c] and T. lunatus (Say) [Figure 1d]), and its lateral margins are typically somewhat concave or sinuate. Female Epeolus have a very distinct sixth sternum, which is often partly visible in pinned specimens even without dissection (Figure 2a) as two convergent spatulate lateral processes bearing setae modified into pointed denticles; the processes are joined by a large lobe-like disc, which is usually not visible unless excised (Figure 2b). By contrast, S6 in female Triepeolus has a pair of narrow, elongate, forceps-like processes with coarse spine-like setae, separated by a disc reduced to a narrow transverse bar (Figure 2c, 2d). The apices of these processes and their long spine-like setae are often visible without dissection in pinned specimens. These morphological differences between females of Epeolus and Triepeolus are presumably related to host specialization (Rightmyer 2004) and the mechanism whereby the female oviposits into the cell wall of its host’s nest or between the caps separating brood cells (Roig-Alsina 1991). The spinose setae of Triepeolus seem to be for digging holes in the soil walls of host cells (Torchio 1986) and/or may have a tactile function (Rightmyer 2004). In Epeolus, tooth-like setae on the lateral processes and the rigid attachment of these processes to the disc of the sternum indicate a saw-like function necessary for breaking through the tough polyester lining that separates brood cells and coats the cell walls of its host nest (Torchio and Burdick 1988). In at least one species of Epeolus, this process is aided by a glandular secretion that dissolves the polyester lining of the host nest on contact, and later resolidifies to close the gap (Torchio and Burdick 1988). Females of the two genera may be further distinguished by the pseudopygidial area – the medioapical region of T5 that generally changes slope (and may be elevated) from the rest of the tergum, and whose disc is flat or somewhat depressed and usually covered in shiny short hairs that are often uniform in length (Michener 2007). In Epeolus, the shape of this area is either campanulate (Figure 3a) or lunate (Figure 3b, 3c, 3d, 3e), whereas in Triepeolus it is more variable, and may be ovate or round (Figure 2c), quadrate, triangular, a shape intermediate between triangular and quadrate, or a shape more complex in outline. With one notable exception, the pseudopygidial area of Triepeolus is always relatively longer than in Epeolus (Rightmyer 2008); in the unusual Mesoamerican T. epeolurus Rightmyer, the transverse band of metallic setae on the pseudopygidial area (Figure 3f) is remarkably similar to that of some species of Epeolus, but is concave rather than arched in dorsal view. Another unusual feature of T. epeolurus is that the pseudopygidial setae reflect silver, whereas in most Triepeolus they reflect a golden colour (Rightmyer 2004).

Epeolus is represented by 102 valid species worldwide (Integrated Taxonomic Information System on-line database, [Retrieved 11.ii.2016]. Based on my own knowledge in combination with records available on Discover Life (Ascher and Pickering 2016), 45 species were until the date of this publication recognized as occurring in North America excluding Mexico and the West Indies. The first species described as being a North American Epeolus, E. mercatus Fabricius, cannot be confidently assigned to Epeolus or Triepeolus, as the original description is vague and the type material apparently has been lost (Rightmyer 2008). Therefore, the numbers above do not include Epeolus mercatus Fabricius. Nonetheless, it would be surprising if this species did not represent another described species in one of these two genera. Brumley (1965) described an additional seven species (all from the American Southwest), but as he did not publish his work his names cannot be formally recognized. Apparently, one of these species, occurring in Arizona and Texas, USA, had already been described by Smith (1879) from Oaxaca, Mexico (Rightmyer 2008). None of the seven “new” species, however, are known to range into Canada. Despite the diversity of Epeolus in North America, with more known species than any other continent, the genus is poorly understood.

Several North American species of Epeolus were originally described as belonging to Phileremus Latreille and Triepeolus. Phileremus (Ammobates Latreille subgenus Ammobates Latreille s. str. in Michener 2007) included cleptoparasitic bee species in which the fore wing has two rather than three submarginal cells. This character is variable even within species (and sometimes specimens) of Epeolus, and Phileremus contained species from a large number of genera (mostly Nomadinae), including Ammobates, Ammobatoides Radoszkowski, Biastes Panzer, Epeolus, Dioxys Lepeletier and Serville, Holcopasites Ashmead, Melanempis Saussure, Neolarra Ashmead, Neopasites Ashmead, and Pasites Jurine (Ascher and Pickering 2016).

I synonymize 14 previously proposed names under those of four valid species. Epeolus americanus and E. minimus are similar to some species that are not treated here because they occur south of Canada only. They include a cryptic species revealed by DNA barcoding (BOLD:ACZ2142) within the “americanus group”, whose subtle morphological differences and collection date and locality record within Los Angeles County, California are shared with the holotype of E. asperatus Cockerell, which I have seen and examined. Also similar is the holotype of E. melectimimus Cockerell and Sandhouse. Epeolus barberiellus Cockerell is another species similar to E. americanus, with unique physical attributes and known to occur only in New Mexico and Texas. A species very similar to E. minimus is E. banksi (Cockerell), with unique physical attributes, and apparently restricted to parts of the mid-Atlantic and southeastern States. DNA barcode data are not yet available, but morphology suggests that specimens identified as E. banksi are clearly distinct from E. minimus. The names E. americanus and E. minimus antedate those of the abovementioned similar or cryptic species, and for the reasons stated herein I am confident that the new synonymies proposed are correct for the taxa in question, and do not apply to any other species.



All Epeolus species for which host use has been assessed are cleptoparasites of Colletes Latreille, the type genus of the family Colletidae (Michener 2007). The reproductive biology and immature stages of Epeolus were first described for E. pusillus Cresson in association with Colletes ciliatoides Stephen (Torchio 1965) and C. compactus compactus Cresson (Rozen and Favreau 1968). Both host species construct a single cell at the end of a lateral tunnel that branches from the meandering, mostly vertical main tunnel. Rozen and Favreau (1968) noted female E. pusillus flying swiftly 15–20 cm above the ground, slowing down over what presumably to them seemed to be nest entrances – one female flew quickly toward a burrow from which a host Colletes had previously been collected, descended, and re-emerged within a minute. When Rozen and Favreau (1968) excavated the brood cell, they found that it had an Epeolus egg attached, positioned between the inner and outer envelopes of the cell lining.

There is some indication that female Epeolus repeatedly visit and inspect the nest or nests of their host species of Colletes, likely to confirm the suitability of the nest site and ensure that they are present at the right time for oviposition. For instance, Graenicher (1906) reported that upon discovering a C. eulophi Robertson nest (about midday), a female E. minimus (Robertson) began crawling over the ground with quivering wings. The female approached the nest from various angles without entering. The female Epeolus then perched motionless on a small plant, or twig at times, about 20 cm above the nest entrance while the female Colletes returned with provisions. The female Epeolus preened herself at that time, and again after the host female left before the Epeolus herself entered the nest for about one minute. The female then emerged and examined the surrounding area. The process of examining the nest entrance, perching, entering the nest, and examining the surrounding area was repeated within a particular day and on different days (confirmed by marking of the female Epeolus specimen). To be successful, the female Epeolus must avoid detection by the host. In Central Europe, Bogusch (2003) twice observed a female C. similis Schenck successfully defending a nest from a female E. variegatus (L.).

Like other Nomadinae, Epeolus females enter unsealed cells while the host is foraging during the nest provisioning stage. Whereas Colletes eggs were found to be attached to the inner polyester lining of the cell, the egg of E. pusillus was laid between the inner and outer polyester linings of the double-layered nest lining of its host (Rozen and Favreau 1968). Where the egg is laid depends on the host and type of nest constructed. Torchio and Burdick (1988) documented two strategies used by E. compactus Cresson. Its host species, C. kincaidii Cockerell, may reuse abandoned nests. In this case, E. compactus inserts its eggs between the inner lining of the burrow and residual lining (assuming it is intact) from previous nest use, because there is sufficient space and presumably also to protect the egg from getting wet. Interestingly, rates of cleptoparasitism were higher for reused nests. Torchio and Burdick (1988) found overall rates of nest parasitism of C. kincaidii by E. compactus to be as high as nearly 18%. If the nest was newly founded by the female Colletes host (and only a single polyester layer separates the cell from bare ground), E. compactus instead attaches its eggs to the caps of completed cells separating the brood cells (Torchio and Burdick 1988). Although the egg is exposed within the already completed cell, the larva hatches into the cell that was incomplete when the parent Epeolus oviposited. In some instances, multiple eggs may be deposited through a cell cap, but it is not known if these belong to the same or multiple female Epeolus. Oviposition through the cellophane-like cell lining of another colletid genus (Scrapter Lepeletier and Serville) has similarly been documented in the nomadine cleptoparasitic genus Sphecodopsis Bischoff (Rozen and Michener 1968 – as Pseudodichroa). Rozen (1968) suggested that Sphecodopsis females puncture the lining and poke a hole in the sand outside the cell (where the egg is to be embedded) using the heavily sclerotized, median process of S6.

Rozen and Favreau (1968) observed that when the larva of E. pusillus hatched, it immediately found and killed the host egg. Similarly, Torchio and Burdick (1988) found that the larva of E. compactus killed the host egg or larva using its long, sickle-shaped mandibles, and combated the other Epeolus larvae in superparasitized host cells until a single survivor remained. In the case of E. pusillus, the rate of larval development was found to be much faster than that of the host (C. compactus compactus in this case), and by the time the cleptoparasite larva went into diapause, neighbouring representatives of its host species had consumed less than half of their provisions (Rozen and Favreau 1968).