Introduction

Epeoloides pilosulus (Cresson) (aka Macropis Cuckoo Bee - COSEWIC 2011) is one of the rarest bees in North America. The earliest records in Canada date from at least 1888 (Provancher 1888 and see Sheffield and Perron 2014) and, up to the most recent published accounts of this species in Canada (Sheffield et al. 2004, COSEWIC 2011), there have been only 12 specimens recorded from the country. In the last 60 years, only a handful of specimens have been collected in North America (Sheffield et al. 2004, Wagner and Ascher 2008), with the most recent collection event being a single specimen from Huyck Preserve in Albany County, New York State on July 8, 2014 (http://bugguide.net/node/view/954741) (see Gibbs et al. 2017).

Epeoloides pilosulus is a member of one of the most tenuous ecological existences seen in North American plant-pollinator relationships, being a cuckoo (=cleptoparasite) of and thus, dependent on Macropis bees (Melittidae) which in turn are uncommon oligoleges of oil-producing Lysimachia species (Primulaceae, Myrsinoideae) (Sheffield et al. 2004, Wagner and Ascher 2008, Alves-dos-Santos 2009) (Fig. 1).

Figure 1.  

Macropis nuda (Melittidae) on oil-producing flowers of Lysimachia terrestris (Linnaeus) (Primulaceae) near Middleton, Nova Scotia, Canada. Photo by C.S. Sheffield.

Epeoloides pilosulus is one of only two globally recognised species in the genus (Michener 2007), the other, E. coecutiens (Fabricius), which was studied in detail by Straka and Bogusch (2007b) is found in Europe (Popov 1958, Pekkarinen et al. 2003, Bogusch 2005, Michez and Patiny 2005, Dötterl and Schäffler 2006). Interestingly, these two species are presently considered members of the tribe Osiriini, a taxon otherwise restricted to the Neotropics (Michener 2007), though others have indicated that Epeoloides may have affiliations to other tribes in the Apidae (Straka and Bogusch 2007a, Cardinal et al. 2010). However, the known hosts of Epeoloides (i.e. Macropis bees) and their host plants (genus Lysimachia) have centres of diversity elsewhere (Michez and Patiny 2005, Michener 2007). In fact, both Macropis (Michez and Patiny 2005) and Lysimachia (Chen and Hu 1979, Zhang et al. 2006, Zhou et al. 2015) are most diverse in China; eight of the 16 Macropis species and 138 of the ca. 180 known plant species occurring there (Michez and Patiny 2005, Zhang et al. 2006), though Lysimachia also occurs in areas where neither genus of bee has been recorded (Marr and Bohm 1997). However, not all species of Lysimachia are oil-producing and, of the five recognised subgenera, only two contain species with oil-producing flowers that are co-occuring with Macropis bees (Michez and Patiny 2005). Michez and Patiny (2005) provide a detailed account of the biogeography of Macropis bees and Lysimachia hosts. Strangely, Epeoloides is seemingly absent from the centres of diversity of both Macropis bees and Lysimachia floral hosts (Michener 2007).

The purpose of this paper is to report on a recently collected specimen of E. pilosulus from Alberta, Canada which significantly increases the range of this species in western North America and additional specimens in the collections at the Royal Saskatchewan Museum and the University of Guelph. We also comment on its conservation status in Canada.

Materials and methods

Data resources

Taxon treatment

Epeoloides pilosulus (Cresson, 1878)

Nomenclature

Nomada pilosula Cresson 1878: 77 [♂]

Nomia compacta Provancher 1888: 337 [♂] [synonymy by Mitchell (1962)]

Epeolus pilosulus Provancher 1888: 426 [♀] [synonymy by Mitchell (1962)]

Viereckella obscura Swenk 1907: 299 [♀] [synonymy by C.D. Michener, as cited in Sheffield et al. (2004) and see Michener (2000)]

Viereckella ceanothina Cockerell, in Swenk 1907: 300 [♂] [synonymy of V. obscura by Swenk (1912)]

Epeoloides nearcticus Ducke 1909: 39 [♀] [synonymy by Bequaert (1920)]

Materials   Download as CSV 

Other materials:

1. scientificName:
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   ; kingdom:
   Animalia
   ; phylum:
   Arthropoda
   ; class:
   Insecta
   ; order:
   Hymenoptera
   ; family:
   Apidae
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   Macropis Cuckoo Bee
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   pilosulus
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    pilosulus
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    Macropis Cuckoo Bee
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    pilosulus
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    pilosulus
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Lectotype:

1. scientificName:
   Epeoloides pilosulus
   ; originalNameUsage:
   Epeolus pilosulus Provancher, 1888
   ; kingdom:
   Animalia
   ; phylum:
   Arthropoda
   ; class:
   Insecta
   ; order:
   Hymenoptera
   ; family:
   Apidae
   ; vernacularName:
   Macropis Cuckoo Bee
   ; genus:
   Epeoloides
   ; specificEpithet:
   pilosulus
   ; scientificNameAuthorship:
   (Cresson, 1878)
   ; continent:
   North America
   ; country:
   Canada
   ; stateProvince:
   Québec
   ; locality:
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   ; decimalLongitude:
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   L. Provancher
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   Insects
   ; ownerInstitutionCode:
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   ; basisOfRecord:
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Holotype:

1. scientificName:
   Epeoloides pilosulus
   ; originalNameUsage:
   Nomia compacta Provancher, 1888
   ; kingdom:
   Animalia
   ; phylum:
   Arthropoda
   ; class:
   Insecta
   ; order:
   Hymenoptera
   ; family:
   Apidae
   ; vernacularName:
   Macropis Cuckoo Bee
   ; genus:
   Epeoloides
   ; specificEpithet:
   pilosulus
   ; scientificNameAuthorship:
   (Cresson, 1878)
   ; continent:
   North America
   ; country:
   Canada
   ; stateProvince:
   Québec
   ; locality:
   Cap Rouge
   ; decimalLatitude:
   46.76
   ; decimalLongitude:
   -71.35
   ; individualCount:
   1
   ; sex:
   male
   ; lifeStage:
   adult
   ; catalogNumber:
   1670 [yellow label]
   ; recordedBy:
   L. Provancher
   ; identifiedBy:
   L. Provancher
   ; collectionCode:
   Insects
   ; ownerInstitutionCode:
   The Provancher Collection, Université Laval, Ste Foy, Québec
   ; basisOfRecord:
   PreservedSpecimen

Conservation

The species is assessed nationally as Endangered in Canada by COSEWIC (COSEWIC 2011), but has not been listed under the Canadian Species At Risk Act (SARA). The criteria COSEWIC uses to assess the status of species is adapted from the International Union for the Conservation of Nature (IUCN) Red-list categories (see COSEWIC 2012). Epeoloides pilosulus was assessed under the B criteria (i.e. meeting B2ab(iii) as the index of area of occupancy (4 km², calculated only for the last ten year period of assessment) was below the threshold of 500 km², the species had been found at only one location in the past 10 years, has always existed in fragmented populations and there is a continuing decline in suitable wetland habitat for the flowering plant species upon which the host cuckoo bee ultimately depends due to development, invasive species and reduction in wetland area) (COSEWIC 2011).

Each province and territory has separate legislation that protects species at risk in that jurisdiction. Though there are previous records of Epeoloides pilosulus from Nova Scotia, Quebec, Ontario, Manitoba and Saskatchewan, the species is only listed as a Species at Risk under the Nova Scotia Endangered Species Act (NSESA 2013). The species was assessed as Data Deficient by the Committee on the Status of Species at Risk in Ontario (COSSARO) (COSSARO 2010).

Non-legal conservation status ranks have also been completed using NatureServe methodology and definitons (Master et al. 2012). The global rank is G1 (critically imperilled - because of extreme rarity [often 5 or fewer occurrences] or because of some factor(s) such as very steep declines making it especially vulnerable to extirpation from the state/province). The national rank for (Canada) is N1 (critically inmperilled), with provincial ranks for Nova Scotia (S1), Quebec (SNR, unranked - conservation status not yet assessed), Ontario (S1), Manitoba (S1) and Saskatchwan (S1) (CESCC 2016, Atlantic Conservation Data Centre 2017).

The four recent records from Alberta in 2010, Ontario in 1978 (both reported here) and Nova Scotia in 2002 (Sheffield et al. 2004) are the only specimens of this species collected in Canada since 1960.

Analysis

Since the time of the COSEWIC assessment of this species for Canada (COSEWIC 2011), the new records from Alberta (Elk Island National Park) (Fig. 2) and southern Ontario increases the Extent of Occurrence (EOO) in Canada from ca. 0.91 million km² (204,490 km² was reported by COSEWIC 2011) to ca. 1.5 million km² and the Area of Occupancy (AO, based on 2 x 2 = 4 km² grids) from 24 km² to 160 km² (Fig. 3). As this species is dependent on and confined within the range of its host bees (Macropis) (Fig. 4; EOO of 1.9 million km² in Canada) which in turn are dependent on oil-producing species of Lysmiachia, the range of suitable native host plants in Canada represents the possible range extent of the cuckoo bee, which is almost 5 million km² (Fig. 5); likely it is even greater considering that at least some species of Lysimachia occur in the Northwest Territories and Yukon (Porsild and Cody 1980, Cody 2000). However, E. pilosulus has not previously been recorded this far west in North America (Ascher and Pickering 2018); the genus was not even included in the key to bee genera of north-western North America (Stephen et al. 1969).

Figure 2.  

The Macropis Cuckoo Bee, Epeoloides pilosulus (Cresson) (Apidae). Female, lateral view. Specimen from Alberta. Photo by R. Oram, Royal Saskatchewan Museum.

Figure 3.  

The known Extent of Occurrence (EOO) of Epeoloides pilosulus (Cresson) (Apidae) within Canada's extent of jurisdiction (yellow area) and based on minimum convex polygon (within blue lines).

Figure 4.  

The known Extent of Occurrence (EOO) of Macropis bees, M. nuda (Provancher), M. ciliata Patton (Melittidae) within Canada's extent of jurisdiction (yellow area) and based on minimum convex polygon (within blue lines). Data from the Canadian National Collection of Insects, Arachnids and Nematodes (CNC), the Royal Saskatchewan Museum (RSKM) and other sources (Suppl. material 1).

Figure 5.  

Extent of Occurrance (EOO) of native oil-producing Lysimachia species (Primulaceae) in Canada. Figure produced using records obtained from GBIF for species listed in Table 1 (see GBIF 2018, and Suppl. material 2).

Discussion

The newly recorded Canadian specimen of E. pilosulus greatly increases the recorded EOO of this species in Canada (Fig. 3) and for North America, being the furthest into the northwest that this species has been observed. Recently, but not suprisingly due to the presence of the host plant(s), the main Macropis host in Canada, M. nuda (Provancher), was photographed in south-central British Columbia (see Kline 2017), though specimens have been known from that province since 1914 (Fig. 4), suggesting that E. pilosulus may also be present in that province. The genus Lysimachia however is more widespread than either bee species in this triumvariate, with two species, L. thyrsiflora and L. ciliata occuring well into the north of Canada and Alaska (Table 1). Porsild and Cody (1980) recorded L. thyrsiflora from the Northwest Territories, but this species is a non-oil producer, so is likely not being used by Macropis bees as a source of oil. The other northernly distributed species, L. ciliata is an oil-producer (Fig. 6) and is used by Macropis bees in southern parts of the plants range, though neither this genus nor the cuckoo bee have been recorded that far north, suggesting that the bees, but not the plant, are dependants within these plant-pollinator (+ cuckoo) relationships. However, there are also six non-native Lysimachia species in North America, four of which are oil-producers (Table 1) and most of these are grown ornamentally (Fig. 7).

Table 1.

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Species of Lysmiachia in North America, showing their native status, oil production and notes on distribution. Compiled from data in Cody (2000), Coffey and Jones (1980), Estes et al. (2015), Porsild and Cody (1980), Ray (1956), USDA (2017).

Lysimachia Species	Subgenus	Native	Oil	Distribution
L. asperulifolia Poir.	Lysimachia	yes	yes	Southeast USA
L. barystachys Bunge	Palladia	no	no	Southeast USA
L. ciliata L.	Seleucia	yes	yes	CAN, USA [incl. AK]
L. clethroides Duby	Palladia	no	no	Eastern CAN and USA
L. × commixta Fernald [terrestris × thyrsiflora]	Lysimachia	yes	yes	Eastern CAN and USA
L. fraseri Duby	Lysimachia	yes	yes	Southeast USA
L. graminea (Greene) Hand.-Maz.	Seleucia	yes	yes	Southeast USA
L. hybrida Michx.	Seleucia	yes	yes	CAN, USA
L. japonica Thunb.	Lysimachia	no	yes	Southeast USA
L. lanceolata Walter	Seleucia	yes	yes	Eastern CAN and USA
L. lewisii Estes, Shaw & Mausert-Mooney	Seleucia	yes	yes	Southeast USA
L. loomisii Torr.	Lysimachia	yes	yes	Southeast USA
L. nummularia L.	Nummularia	no	yes	CAN, USA
L. × producta (A. Gray) Fernald (pro sp.) [quadrifolia × terrestris]	Lysimachia	yes	yes	Eastern CAN and USA
L. punctata L.	Lysimachia	no	yes	CAN, USA
L. quadriflora Sims	Seleucia	yes	yes	Central CAN and USA
L. × radfordii H.E. Ahles [loomisii × quadrifolia]	Lysimachia	yes	yes	Southeast USA
L. radicans Hook.	Seleucia	yes	yes	Southern USA
L. terrestris (L.) Britton, Sterns & Poggenb.	Lysimachia	yes	yes	CAN, USA [not AK, YT, NT]
L. thyrsiflora L.	Naumburgia	yes	no	CAN, USA [including AK, YT, NT]
L. tonsa (Alph. Wood) Alph. Wood ex Pax & R. Knuth	Seleucia	yes	yes	Southeast USA
L. vulgaris L.	Lysimachia	no	yes	CAN, USA

a

b

Figure 6.

Lysimachia ciliata L. (Primulaceae), a native oil-producing species.

a: Growing at river's edge, Speed River, Guelph Ontario. Photo by C. Sheffield.  
b: Flowers up close. The central reddish areas are oil-producing glands.  

Figure 7.  

A non-native oil producing species, Lysimachia punctata L. (Primulaceae), growing as an ornamental in Guelph, Ontario. Photo by C. Sheffield.

Assessing the conservation status of cuckoo bees is challenging, particularly because these species are dependent on the presence of their host(s), are typically present in low abundance due to their specialised life histories and, therefore, are not as commonly collected as non-parasitic bees (Sheffield et al. 2013b). Additionally, the host(s) of very few cuckoo bees are known (Michener 2007, Sheffield et al. 2013b), so the threats to host(s) may be unknown. Most of the recently collected specimens of E. pilosulus have been captured through passive methods of sampling; specimens collected in 2002 in Nova Scotia (Sheffield et al. 2004) and 2005-2006 in Connecticut (Wagner and Ascher 2008, Wagner et al. 2014) were from pan traps. While these traps are easily set, choosing the appropriate habitat can be challenging because little is known about the microhabitat characteristics of the cuckoo bee in North America, though somewhat known for the host (see Rozen and Jacobson 1980, Cane et al. 1983). Macropis bees are relatively widespread but uncommon, though potential host plants are also widely distributed (Fig. 5). Presence and abundance of Lysimachia are not strong indicators of the host bee’s presence (COSEWIC 2011) and both are not uniformly distributed throughout the landscape. Therefore, it is also assumed these factors also limit the population of E. pilosulus.

In the past decade, interest in bee conservation has grown and sampling for bees has increased substantially, though much of this has been project specific and new records have been identified as part of larger studies (Sheffield et al. 2013a, Wagner et al. 2014), as opposed to efforts specifically targeting this species throughout its range (COSEWIC 2011). However comprehensive sampling for bees continues to be challenging and some cuckoo bee species can be rare within certain landscapes, have a limited flight period synchronised with the host(s) and/or may have population fluctuations, making their detection difficult (Sheffield et al. 2013b). However, for E. pilosulus and other cuckoos of oil bees (Alves-dos-Santos 2009), it may be possible to develop specific sampling methods to accurately assess the bee’s presence in the landscape based on chemical ecology. For example, European species of Macropis and E. coecutiens (and likely its North American counter) find the flowers and nests of its Macropis hosts, respectively by the scent of floral oils (Dötterl and Schäffler 2006, Dotterl 2008), so developing a chemical lure for E. pilosulus in North American as a tool for conservation monitoring may be possible.

Acknowledgements

References

Alves-dos-Santos I (2009)
Cleptoparasite bees, with emphasis on the oilbees hosts
.
Acta Biológica Colombiana
14
(
2
):
107
‑
114
. URL: http://ref.scielo.org/nfk9rs
Ascher J, Pickering J (2018)
Discover Life bee species guide and world checklist
. http://www.discoverlife.org/mp/20q?guide=Apoidea_species&flags=HAS:. Accessed on: 2018-3-08.
Atlantic Conservation Data Centre (2017)
Species Ranks
. http://www.accdc.com/en/ranks.html. Accessed on: 2017-12-06.
Bequaert J (1920)
Hymenoptera collected near Boston, Mass., with description of a variety of Bombus affinis
.
Psyche
27
(
1
):
6
‑
12
. https://doi.org/10.1155/1920/45767
Bogusch P (2005)
Biology of the cleptoparasitic bee Epeoloides coecutiens (Hymenoptera: Apidae: Osirini)
.
Journal of the Kansas Entomological Society
78
(
1
):
1
‑
12
. https://doi.org/10.2317/0310.16.1
Cane JH, Eickwort GC, Wesley FR, Spielholz J (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
(
2
):
257
‑
264
. https://doi.org/10.2307/2425267
Cardinal S, Straka J, Danforth BN (2010)
Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism
.
Proceedings of the National Academy of Sciences
107
(
37
):
16207
‑
16211
. https://doi.org/10.1073/pnas.1006299107
CESCC (2016)
Wild Species 2015: The General Status of Species in Canada
.
Canadian Endangered Species Conservation Council, National General Status Working Group
,
128
pp. URL: https://www.wildspecies.ca/reports
Chen FH, Hu CM (1979)
Taxonomic and phytogeographic studies on Chinese species of Lysimachia
.
Acta Phytotaxonomica Sinica
17
:
21
‑
53
.
Cody WJ (2000)
Flora of the Yukon Territory
.
Second Edition
.
NRC Research Press
,
Ottawa
,
669
pp. [ISBN
978-0-660-18110-3
]
Coffey VJ, Jones SB (1980)
Biosystematics of Lysimachia section Seleucia (Primulaceae)
.
Brittonia
32
(
3
):
309
. https://doi.org/10.2307/2806721
COSEWIC (2011)
COSEWIC Assessment and Status Report on the Macropis Cuckoo Bee Epeoloides pilosulus in Canada
.
Committee of the Status of Endangered Wildlife in Canada
,
Ottawa
. URL: http://www.registrelep-sararegistry.gc.ca/document/default_e.cfm?documentID=2297
COSEWIC (2012)
COSEWIC Assessment Process, Categories and Guidelines
. http://www.cosewic.gc.ca/94D0444D-369C-49ED-A586-EC00C3FEF69B/Assessment_process_and_criteria_e.pdf. Accessed on: 2017-12-06.
COSSARO (2010)
COSSARO Candidate Species at Risk Evaluation Form for Macropis Cuckoo Bee (Epeoloides pilosula)
.
Committee on the Status of Species at Risk in Ontario (COSSARO)
,
Peterborough
,
5
pp. URL: http://www.ontla.on.ca/library/repository/mon/26004/317237.pdf
Cresson ET (1878)
Descriptions of new North American Hymenoptera in the collection of the American Entomological Society
.
Transactions of the American Entomological Society
7
:
61
‑
136
. https://doi.org/10.2307/25076368
Dotterl S (2008)
Antennal responses of an oligolectic bee and its cleptoparasite to plant volatiles
.
Plant Signaling & Behavior
3
(
5
):
296
‑
297
. https://doi.org/10.4161/psb.3.5.5271
Dötterl S, Schäffler I (2006)
Flower scent of floral oil-producing Lysimachia punctata as attractant for the oil-bee Macropis fulvipes
.
Journal of Chemical Ecology
33
(
2
):
441
‑
445
. https://doi.org/10.1007/s10886-006-9237-2
Ducke A (1909)
Contributions à la connaissance des Hyménoptères des deux Amériques
.
Revue d’Entomologie
27
:
28
‑
55
.
Estes D, Shaw J, Mausert-Mooney C (2015)
Lysimachia lewisii (Primulaceae): a new species from Tennessee and Alabama
.
Phytoneuron
17
:
1
‑
15
.
GBIF (2018)
GBIF Occurrence Download
. https://doi.org/10.15468/dl.4mglnz. Accessed on: 2018-3-31.
Gibbs J, Ascher JS, Rightmyer MG, Isaacs R (2017)
The bees of Michigan (Hymenoptera: Apoidea: Anthophila), with notes on distribution, taxonomy, pollination, and natural history
.
Zootaxa
4352
(
1
):
1
‑
160
. https://doi.org/10.11646/zootaxa.4352.1.1
Kline B (2017)
New bee family discovered in Kootenays
. http://www.castlegarnews.com/news/new-bee-family-discovered-in-kootenays. Accessed on: 2017-9-04.
Marr KL, Bohm BA (1997)
A taxonomic revision of the endemic Hawaiian Lysimachia (Primulaceae) including three new species
.
Pacific Science
51
(
3
):
254
‑
287
.
Master L, Faber-Langendoen D, Bittman R, Hammerson GA, Heidel B, Ramsay L, Snow K, Teucher A, Tomaino A (2012)
NatureServe Conservation Status Assessments: Factors for Evaluating Species and Ecosystem Risk
.
NatureServe
,
Arlington
,
64
pp. URL: http://www.natureserve.org/sites/default/files/publications/files/natureserveconservationstatusfactors_apr12_1.pdf
Michener CD (2000)
The Bees of the World
.
The Johns Hopkins University Press
,
Baltimore
,
913
pp. [ISBN
0-8018-6133-0
]
Michener CD (2007)
The Bees of the World. Second Edition
.
The Johns Hopkins University Press
,
Baltimore
,
953
pp. [ISBN
13: 978-0-8018-8573-0
]
Michez D, Patiny S (2005)
World revision of the oil-collecting bee genus Macropis Panzer, 1809 (Hymenoptera: Apoidea: Melittidae) with a description of a new species from Laos
.
Annales de la Société entomologique de France (N.S.)
41
(
1
):
15
‑
28
. https://doi.org/10.1080/00379271.2005.10697439
Mitchell TB (1962)
Bees of the eastern United States. Volume II
.
North Carolina Agricultural Experiment Station Technical Bulletin
152
:
1
‑
557
.
NSESA (2013)
Species at Risk Overview. NS Endangered Species Act: Legally Listed Species
. https://novascotia.ca/natr/wildlife/biodiversity/species-list.asp. Accessed on: 2018-3-09.
Pekkarinen A, Berg O, Calabuig I, Janzon LA, Luig J (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
(
1
):
53
‑
59
.
Popov VB (1958)
Peculiar features of correlated evolution of two genera of bees—Macropis and Epeoloides (Hymenoptera, Apoidea)—and a plant genus Lysimachia (Primulaceae)
.
Entomological Review
37
:
499
‑
519
. [In
Russian
].
Porsild AE, Cody WJ (1980)
Vascular Plants of Continental Northwest Territories, Canada
.
National Museum of Natural Sciences
,
Ottawa
,
667
pp. [ISBN
0-660-00119-5
]
Provancher L (1888)
Additions et corrections au Volume II de la Faune Entomologique du Canada. Traitant des Hyménoptères
.
C. Darveau
,
Québec
,
475
pp. [In
French
].
Ray JD (1956)
The genus Lysimachia in the new world
.
Illinois Biology Monographs
24
:
1
‑
160
.
Rozen JG, Jacobson NR (1980)
Biology and immature stages of Macropis nuda, including comparisons to related bees (Apoidea, Melittidae)
.
American Museum Novitates
2702
:
1
‑
11
.
Sheffield CS, Rigby SM, Smith RF, Kevan PG (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
(
3
):
161
‑
164
. https://doi.org/10.2317/0310.23.1
Sheffield CS, Kevan PG, Pindar A, Packer L (2013a)
Bee (Hymenoptera: Apoidea) diversity within apple orchards and old fields in the Annapolis Valley, Nova Scotia, Canada
.
The Canadian Entomologist
145
:
94
‑
114
. https://doi.org/10.4039/tce.2012.89
Sheffield CS, Pindar A, Packer L, Kevan PG (2013b)
The potential of cleptoparasitic bees as indicator taxa for assessing bee communities
.
Apidologie
44
(
5
):
501
‑
510
. https://doi.org/10.1007/s13592-013-0200-2
Sheffield CS, Perron J (2014)
Annotated catalogue of the bees described by Léon Provancher (Hymenoptera: Apoidea)
.
The Canadian Entomologist
146
(
02
):
117
‑
169
. https://doi.org/10.4039/tce.2013.64
Stephen WP, Bohart GE, Torchio PF (1969)
The Biology and External Morphology of Bees with a Synopsis of the Genera of Northwestern America
.
Agricultural Experiment Station, Oregon State University
,
Corvallis
,
140
pp.
Straka J, Bogusch P (2007a)
Phylogeny of the bees of the family Apidae based on larval characters with focus on the origin of cleptoparasitism (Hymenoptera: Apiformes)
.
Systematic Entomology
32
(
4
):
700
‑
711
. https://doi.org/10.1111/j.1365-3113.2007.00394.x
Straka J, Bogusch P (2007b)
Description of immature stages of cleptoparasitic bees Epeoloides coecutiens and Leiopodus trochantericus (Hymenoptera: Apidae: Osirini, Protepeolini) with remarks to their unusual biology
.
Entomologica Fennica
18
:
242
‑
254
.
Swenk MH (1907)
The bees of Nebraska. III
.
Entomological News
18
:
293
‑
300
.
Swenk MH (1912)
Studies of North American bees I. Family Nomadidae
.
University Studies of the University of Nebraska
12
(
1
):
1
‑
113
.
USDA (2017)
The PLANTS Database
. http://plants.usda.gov. Accessed on: 2017-3-14.
Wagner DL, Ascher JS (2008)
Rediscovery of Epeoloides pilosula (Cresson) (Hymenoptera: Apidae) in New England
.
Journal of the Kansas Entomological Society
81
(
2
):
81
‑
83
. https://doi.org/10.2317/jkes-703.19.1
Wagner DL, Ascher JS, Bricker NK (2014)
A transmission right-of-way as habitat for wild bees (Hymenoptera: Apoidea: Anthophila) in Connecticut
.
Annals of the Entomological Society of America
107
(
6
):
1110
‑
1120
. https://doi.org/10.1603/AN14001
Zhang M, Shui Y, Chen W, Wei Z (2006)
Lysimachia gesnerioides (Myrsinaceae), a new species from China and Vietnam
.
Annales Botanici Fennici
43
:
317
‑
319
.
Zhou J, Yu X, Deng Y, Yan H, Lin Z (2015)
Lysimachia huangsangensis (Primulaceae), a new species from Hunan, China
.
PLOS ONE
10
(
7
):
e0132713
. https://doi.org/10.1371/journal.pone.0132713

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