Cuckoo bees: Epeoloides pilosula (Cresson 1878)
(Hymenoptera: [Apoidea:] Apidae: Apinae: Osirini)
Profile prepared by John S. Ascher, American Museum of Natural History, updated by Sarina Jepsen, The Xerces Society
This distinctive cleptoparasite of Macropis oil bees was once widely distributed in the northern and eastern United States and southern Canada. A lack of records from the latter half of the 20th century led to speculation that this species was extinct until two male Epeoloides pilosula were collected in 2002 in Nova Scotia, northeast of its historical range. Epeoloides is entirely dependant on nesting aggregations of its host bees, multiple species of Macropis, which in turn are strict specialists of Lysimachia (yellow loosestrife), from which they obtain pollen and oil. Conservation of Epeoloides pilosula will require study and conservation of Macropis and Lysimachia species.
Epeoloides pilosula (Cresson) is a moderate-sized cleptoparasitic bee with a smooth, black, shining integument, short but densely plumose, erect pubescence, and a convex (emphorine-like) vertex. This distinctive bee differs from other similar bees in the following ways:
- the integument of Epeoloides is entirely black without the red and/or yellow markings of many nomadine cleptoparasites;
- Epeoloides lacks the striking bands and patches of appressed, very short hair (superficially resembling integumental maculations) typical of Epeolini (Nomadinae);
- Epeoloides possesses apical tergal bands of erect, densely plumose, white hair;
- the second of the three submarginal cells is much smaller than the first or third; and
- the marginal cell is separated from the wing margin and its apex is gradually bent away from the wing margin (the marginal cell touches the wing margin and has an apex that is on the wing margin or more abruptly truncate in most other similar bees).
Epeoloides females can readily be recognized as cleptoparasites as they lack specialized pollen-collecting hairs (i.e. scopae), and the abdomen is pointed posteriorly. Unlike most nomadine females, Epeoloides females lack a well-defined pseudopygidial area. Male Epeoloides have large eyes, which are strongly convergent above. Mitchell (1962) and Sheffield et al. (2004) illustrated various structures, and the latter also provided a habitus drawing. Epeoloides pilosula is the only member of the tribe Osirini in America north of Mexico and the only New World Epeoloides and can therefore be easily identified using keys in Mitchell (1962), Michener, McGinley, and Danforth (1994), and Michener (2000) based on the presence of tribal characters for Osirini and generic characters for Epeoloides (see also Roig- Alsina, 1989). A distinctive osirine character is the apex of the marginal cell gradually bending away from the wing margin, as described above.
Epeoloides pilosula (Cresson, 1878; described in the genus Nomada) is the only species of the cleptoparasitic tribe Osirini (Apidae: Apinae) present in the United States and Canada and one of only two species of genus Epeoloides worldwide (Michener, 2000). The other Epeoloides species, the type species Epeoloides coecutiens (Fabricius, 1775; described in the genus Apis) from Europe, is also an obligate cleptoparasite of Macropis. Although a separate genus, Viereckella, was described for North American Epeoloides, the Nearctic and Palearctic Epeoloides species are closely related and therefore regarded as congeners. The genus Epeoloides comprises a Holarctic clade sister to the Neotropical osirine clade Osirinus + Protosiris + Osiris (Roig-Alsina, 1989). Within the latter clade, the derived genera Osiris and Protosiris occur north to northwestern Mexico (Sonora and Sinaloa; specimens in the Essig Museum of Entomology). Parepeolus sensu Michener (2000; including subgenus Ecclitodes) from temperate South America was resolved by Roig-Alsina (1989) as the basal lineage of Osirini. Thus, Roig- Alsina’s (1989) phylogenetic studies place Epeoloides within Osirini, contradicting prior placement of Epeoloides in its own tribe, Epeoloidini, in subfamily Nomadinae. All Osirini are known or suspected to be cleptoparasites of oil-collecting bees, so this behavior can be considered a synapomorphy of the tribe. The following nominal species were treated by Mitchell (1962) and subsequent authors as synonyms of Epeoloides pilosula (Cresson): Nomia compacta Provancher, 1888; Viereckella ceanothina Cockerell, 1907; Epeoloides nearcticus Ducke, 1909. Viereckella obscura Swenk, 1907, was treated as a valid species by Hurd (1979) but is probably an additional synonym (Michener, 2000; Sheffield et al., 2004).
Epeoloides pilosula has not been reared from Macropis (Melittidae: Melittina e: Macropidini) nests but is generally accepted to be an obligate cleptoparasite of Macropis species based on the well known association between E. coecutiens and Macropis hosts in Europe (Pekkarinen, 2003; Bogusch, 2003, 2005) and extensive circumstantial evidence such as frequent historical co-occurrence of Macropis and Epeoloides in and near patches of Lysimachia spp. (yellow or fringed loosestrife; Primulaceae). Epeoloides pilosula can be inferred to parasitize multiple Macropis species (as does E. coecutiens in Europe; see Bogusch, 2005), and its host range quite possibly includes all four North American species. Macropis nuda (Provancher) is almost certainly a host of Epeoloides pilosula, as this is the only Macropis species known from much of the Canadian range of Epeoloides (see Sheffield et al., 2004). Other species of Macropis are likely additional hosts of Epeoloides in the USA, as Epeoloides is recorded south to Georgia where Macropis ciliata Patton and M. steironematis Robertson occur but not M. nuda. Epeoloides pilosula has also been collected together with Macropis patellata Patton at Plummer’s Island, Maryland, and elsewhere. The known flight season of E. pilosula is from June to July (Mitchell, 1962), corresponding with peak nesting activity of Macropis and peak bloom of its host plant, Lysimachia. Epeoloides pilosula visits a variety of plants for nectar (Mitchell, 1962, listed four floral records), but ultimately depends upon populations of Lysimachia, since the Macropis hosts of Epeoloides are strict Lysimachia specialists. Macropis females gather both pollen and floral oils from Lysimachia species such as L. terrestris and L. ciliata.
Epeoloides pilosula is known historically from much of eastern and central North America south to Georgia and northwest to Montana and Saskatchewan, including the vicinity of major cities such as New York City (e.g., Flatbush in Brooklyn, Kings County, New York, in 1894 and 1896; Palisades, New Jersey in 1918 and 1920), Washington, D.C. (Plummers Island, Maryland, 1905-1917), and Boston (Needham: 1921-1927). Mitchell (1962) and Hurd (1979) recorded Epeoloides pilosula from the following states and provinces (dates listed in parentheses are the most recent specimens from each area examined [new information]): Massachusetts (Needham: 1921-1927), Connecticut (South Meriden: 1911), Wisconsin (Dane County: 1910), Michigan (Paw Paw Lake: 1906), Ohio, New York (Springlake, Cayuga Co.: 1918, Tuxedo: 1928, Yaphank: 1930, Yonkers: 1935), Virginia, North Carolina, Georgia, North Dakota (Fargo: 1913), Nebraska, and Quebec. Sheffield et al. (2004) published additional Canadian records from Ontario (One Sided [=Oneside] Lake: 1960), Manitoba (Aweme: 1916), and Saskatchewan (Wallwort: 1942, Wood Mountain: 1955). Additional records are from Montana (International Peace Garden, Turtle Mountain: 1958), Illinois (Savannah: 1917), New Jersey (Plainfield: 1927), Pennsylvania, Maryland, West Virginia, and Virginia (new information). Note that of these collections all post-1935 records are from southern Canada from western Ontario to Saskatchewan, and from nearby Montana. According to Michener (2000), The American species, Epeoloides pilosula (Cresson) seems not to have been collected since 1942; it is possibly extinct, although its presumed host, Macropis, remains widespread but localized to patches of its required flower, Lysimachia (Primulaceae). Subsequently, Sheffield et al. (2004) reported their rediscovery of Epeoloides in Nova Scotia, and published Canadian records from the 1950s and one from 1960 (cited above).
Loss or reduction of Macropis nest aggregations is likely the most general threat to Epeoloides. Macropis species depend upon Lysimachia species for pollen and floral oils, so Macropis populations are vulnerable to loss or reduction of Lysimachia populations. Although Lysimachia flowers can still be found at many sites, most populations located recently in New York are small, and Macropis has been found only at relatively natural sites, not in association with Lysimachia growing along roadside ditches. However, in Nova Scotia Macropis nuda has been collected on Lysimachia growing in small patches along roadsides and in larger “weedy” patches growing in recently cleared areas (Sheffield, in litt., 2005), and in the Czech Republic five of nine study sites for Epeoloides coecutiens were anthropogenous (Bogusch, 2005). Certain Lysimachia species are endangered at least in parts of their range (e.g., Lysimachia radicans (Creeping Loosestrife) is listed as endangered in Illinois). The status of associated specialist bees is unknown. Lysimachia patches are vulnerable to loss and degradation of appropriate habitat, which includes swamps, and stream, pond, and lake margins. Specific threats include clearing of native vegetation along lake margins, especially vacation home frontage, and drainage resulting in drying and loss of Lysimachia populations through succession. Another threat is usurpation of Lysimachia habitat by invasive weeds such as Phragmites and Lythrum (purple loosetrife, Lythraceae; not closely related to yellow loosestrife despite their homonymous names) as has been observed in the case of Lythrum at Six Mile Creek in Ithaca, New York (new information). Pollution may contribute to replacement of native Lysimachia by invasive competitors. Many streamside sites have undoubtedly been lost due to channelization. Due to their occurrence in and near wetlands, Macropis and Epeoloides may also be more vulnerable than other bees to insecticides applied to control mosquitoes. Applications of broad-spectrum DDT and other organophosphates in the 1940s and 1950s may correspond to the period of decline for Epeoloides. Near eradication of the beaver across much of North America after European settlement must have drastically decreased available wetland margin habitat for Lysimachia, likely resulting in decreased in populations of Macropis and Epeoloides. The drastic decline of Epeoloides in North America is evidently due to a cause specific to this continent, as the European Epeoloides coecutiens remains locally numerous in central Europe and has apparently extended its range north in recent times to Finland and the Baltics (Pekkarinen et al., 2003) although localized populations in certain areas have been recognized as potentially vulnerable (Westrich, 1989; Falk, 1991).
Epeoloides is dependent for its survival upon nest aggregations of its Macropis hosts, often located in south- facing sandy banks near wet Lysimachia habitat (see Bogusch, 2005). Macropis nests sites are restricted in occurrence and perennial (e.g., the nest site of Macropis nuda at Huyck Preserve, Rensslaerville, New York, studied by Rozen and Jacobson, 1980, was still active in 2004). Therefore, it would be helpful to locate these to ensure their protection and to facilitate multi- year surveys for Epeoloides. Control of invasive plants such as Lythrum would undoubtedly benefit Lysimachia at many sites. Surveys of the past and present distribution and conservation status of Lysimachia are needed. Maintenance of native vegetation along pond, lake, and stream margins is essential.
An obvious priority for research is to locate a viable population of Epeoloides pilosula in association with a Macropis nest site. This would allow for life history studies and initiation of land use practices designed to maintain and enhance populations of Lysimachia, Macropis, and Epeoloides. Surveys for Lysimachia and Macropis in Nova Scotia, and in the northern Great Plains and adjacent areas (e.g., southcentral Canada from western Ontario to Saskatchewan, Montana) would be particularly worthwhile as these are the only areas where Epeoloides is known to have persisted subsequent to 1935. Data on the occurrence of Macropis species and Lysimachia hosts across North America would be valuable even if Epeoloides is not found, as certain Macropis species (e.g., M. patellata, M. ciliata, M. steironematis) and certain Lysimachia species are local, perhaps declining, and worthy of consideration as species of special concern. Additional life history and population studies of the relatively numerous European Epeoloides species would be useful pending discovery of viable populations of the Nearctic species.
Bogusch, P. 2003. Hosts, foraging behavior and distribution of six species of cleptoparasitic bees of the subfamily Anthophorinae (Hymenoptera: Apidae). Acta Societatis Zoologicae Bohemicae 67:65-70.
Bogusch, P. 2005. Biology of the cleptoparasitic bee Epeoloides coecutiens (Hymenoptera: Apidae: Osirini). Journal of the Kansas Entomological Society 78:1-12.
Cane, J. H., G. C. Eickwort, F. R. Wesley, and J. Spielholz. 1983. Foraging, grooming, and mate-seeking behaviors of Macropis nuda (Hymenoptera, Melittidae) and use of Lysimachia ciliata (Primulaceae) oils in larval provisions and cell linings. American Midland Naturalist 110: 257-264.
Celary, W. 2004. A comparative study on the biology of Macropis fulvipes (Fabricius, 1804) and Macropis europaea Warncke, 1973 (Hymenoptera: Apoidea: Melittidae). Folia Biologica (Cracow) 52: 81-85.
Falk, 1991. A review of the scarce and threatened bees, wasps and ants of Great Britain. Peterborough, UK: Joint Nature Conservation Committee, Nature Conservancy Council. 344 pp.
Hurd Jr., P. D. 1979. Superfamily Apoidea, pp. 1741-2209 in K. V. Krombein, P. D. Hurd, Jr., D. R. Smith, and B. D. Burks, eds., Catalog of Hymenoptera in America north of Mexico , Vol. 2. Washington, D.C.: Smithsonian Institution Press.
Malyshev, S. I. 1929. The nesting habits of Macropis Pz. Eos 5: 97-109.
Michener, C.D. 2000. The Bees of the World. Baltimore, MD: Johns Hopkins University Press.
Michener, C.D., R. J. McGinley, and B. N. Danforth. 1994. The Bee Genera of North and Central America. Washington, D.C.: Smithsonian Institution Press.
Mitchell, T. B. 1962. Bees of the eastern United States. Volume II. North Carolina Agricultural Experiment Station Technical Bulletin No. 152. 557 pp.
Pekkarinen, A., O. Berg, I. Calabuig, L.-?. Janzon, and J. Luig. 2003. Distribution and co-existence of the Macropis species and their cleptoparasite Epeoloides coecutiens (Fabr.) in NW Europe (Hymenoptera: Apoidea, Melittidae and Apidae). Entomologica Fennica 14: 53-59.
Roig-Alsina, A. 1989. The tribe Osirini, its scope, classification, and revisions of the genera Parepeolus and Osirinus. University of Kansas Science Bulletin 54: 1-23.
Rozen, J. G., Jr., and N. R. Jacobson. 1980. Biology and immature stages of Macropis nuda, including comparisons to related bees. American Museum Novitates no. 2702: 1- 11.
Sheffield, C. S., S. M. Rigby, R. F. Smith, and P. G. Kevan. 2004. The rare cleptoparasitic bee Epeoloides pilosula (Hymenoptera: Apoidea: Apidae) discovered in Nova Scotia, Canada, with distributional notes. Journal of the Kansas Entomological Society 77: 161-164.
Westrich, P. 1989. Die Wildbienen Baden-Wurttembergs: Allgemeiner Teil, pp. 1-431; Spezieller Teil: Die Gattungen Und Arten, pp. 437-972. Stuttgart, Germany: Eugene Ulmer.
Cory S. Sheffield reviewed the manuscript, made several useful additions and corrections, and provided unpublished data about Macropis habitat in Nova Scotia.
Leif Richardson contributed information about two more recent Connecticut records of this species.
Ascher, J. S. 2005. Species Profile: Epeoloides pilosula. In Shepherd, M. D., D. M. Vaughan, and S. H. Black (Eds). Red List of Pollinator Insects of North America. Portland, OR: The Xerces Society for Invertebrate Conservation.