Many wild bee species are in global decline, yet much is still unknown about their diversity and contemporary distributions. National parks and forests offer unique areas of refuge important for the conservation of rare and declining species populations. Here we present the results of the first biodiversity survey of the bee fauna in the White Mountain National Forest (WMNF). More than a thousand specimens were collected from pan and sweep samples representing 137 species. Three species were recorded for the first time in New England and an additional seven species were documented for the first time in the state of New Hampshire. Four introduced species were also observed in the specimens collected. A checklist of the species found in the WMNF, as well as those found previously in Strafford County, NH, is included with new state records and introduced species noted as well as a map of collecting locations. Of particular interest was the relatively high abundance of Bombus terricola Kirby 1837 found in many of the higher elevation collection sites and the single specimen documented of Bombus fervidus (Fabricius 1798). Both of these bumble bee species are known to have declining populations in the northeast and are categorized as vulnerable on the International Union for Conservation of Nature’s Red List.

Bees are fundamental to a sustainable environment as they pollinate 90% of the world’s flowering plants, which are essential to most functioning terrestrial ecosystems (Ollerton et al. 2011). Despite their significance as pollinators, research shows that bee populations are declining globally (Bartomeus et al. 2013, Burkle et al. 2013, Garibaldi et al. 2013, Potts et al. 2010, Kerr et al. 2015). Historically there were about 3,600 bee species recorded in the United States (Ascher and Pickering 2016, Wilson and Carril 2016) across 111 genera (Droege et al. 2016). These species span six different families, although the family Melittidae, comprised of 33 species in the United States with only 8 in the northeast, is rarely collected (Wilson and Carril 2016).

Of particular concern in the Northeast is the severe decline of several historically widespread bumble bee species, Bombus affinis Cresson 1863, Bombus fervidus (Fabricius 1798), Bombus pensylvanicus (DeGeer 1773), and Bombus terricola Kirby 1837 (Colla and Packer 2008, Grixti et al. 2008, Cameron et al. 2011, Colla et al. 2012, Bartomeus et al. 2013). These four species were listed as Species of Greatest Conservation Need (SGCN) in 2015 as part of the New Hampshire Fish and Wildlife Service Wildlife Action Plan (Normandeau 2015). With population ranges reduced by 87% (Cameron et al. 2011), B.affinis, is also listed as Critically Endangered by the International Union for Conservation of Nature (IUCN, Hatfield et al. 2015a). Populations of B. fervidus have shown significant declines in Guelph, Canada (Colla and Packer 2008), Vermont (McFarland et al. 2015, Normandeau 2015), New York (Giles and Ascher 2006, Normandeau 2015), while B. pensylvanicus has lost 23% of its historical range and is absent in much of its former northern and eastern territory (Cameron et al. 2011). Both species are listed as a vulnerable on the IUCN Red List (Hatfield et al. 2015b). Populations of B. terricola have suffered severe declines with historical range reductions as high as 31% (Cameron et al. 2011) and are listed for conservation priority by the Xerces Society for Invertebrate Conservation (Evans et al. 2008, xerces.org) and also as vulnerable by the IUCN (Hatfield et al. 2015c).

New England has the potential to support some of the highest levels of wild bee biodiversity in the Northeast with many protected areas and unique ecological niches (Chandler and Peck 1992, Goldstein and Ascher 2016, Koh et al. 2016). As recent studies in Massachusetts (Goldstein and Ascher 2016), Connecticut (Wagner et al. 2014), Maine (Bushmann and Drummond 2015), and New Hampshire (Tucker and Rehan 2016) have begun to document New England’s wild bee biodiversity, many new state records, exotic introductions and species extirpations continue to be discovered in this relatively diverse and agriculturally important area. These prospective changes in New England biodiversity, along with the general global decline, emphasize the need for further surveys to monitor shifts in the wild bee community.

National parks and forests provide patches of protected habitat that can act as refuge to species in less than ideal environs sometimes leading to pockets of organisms rarely found elsewhere (Brown 1971, Dean 2000, Gillespie and Roderick 2002, Richards et al. 2011).The White Mountain National Forest (WMNF) contains 750,852 acres of protected land spanning three New Hampshire counties and over 100 miles of Appalachian Trail (USFS 2012) (Fig. 1). It is the largest alpine area in the eastern United States with its highest elevation at the peak of Mount Washington, which reaches 1,917 meters and classifies as tundra climate (Reiners and Lang 1979, Levesque and Burger 1982, Kimball and Weihrauch 2000, AMC 2016). The National Forest was first established in 1918, but has had few insect biodiversity assessments (McFarland 2003, Levesque and Burger 1982, McCall and Primack 1992, Chandler 1991) with little known about the wild bee fauna.

Fig. 1.

Top: WMNF relative to the northeast. New England is shaded in darker gray. The asterisk marks Durham, Strafford County, NH. Bottom: An enlargement of WMNF in light gray with black dots representing collecting locations (Table 1). The black triangle denotes the peak of Mount Washington. The dashed line shows the New Hampshire and Maine state boundary.

Fig. 1.

Top: WMNF relative to the northeast. New England is shaded in darker gray. The asterisk marks Durham, Strafford County, NH. Bottom: An enlargement of WMNF in light gray with black dots representing collecting locations (Table 1). The black triangle denotes the peak of Mount Washington. The dashed line shows the New Hampshire and Maine state boundary.

Here we document the first faunistic survey of wild bees in the WMNF. The objectives of this study were to, 1) provide a contemporary survey and species checklist of the wild bees currently inhabiting WMNF, 2) document any new or introduced species not historically recorded for the area, and 3) record any Bombus species found that are listed as SGCN by the NH Fish and Wildlife Action plan.

Methods

Location and Collection

Wild bee collection was conducted at 16 sites in northern New Hampshire over an approximate 331,520-acre area in the WMNF (geographic coordinates in Table 1; map Fig. 1). This sampling area covered a broad spectrum of elevations ranging from a low of 118 m to a high of 1,160m on Mount Washington (Table 1). Sampling was conducted over a 2-day period on 26 and 27 June 2015 and comprised an estimated 60 concerted man-hours. Bees were sampled using standard pan traps and sweep nets. About 300 pan traps (New Horizons Support Services, Inc., Upper Marlboro, MD; 3.5 oz.) of alternating color (yellow, blue, and white) were filled soapy water and set out for ∼8 h. The pan trap contents were poured through a sieve upon retrieval. Sweep netting was performed using collapsible aerial nets (Bioquip 7112CP; 30.5 cm in diameter, 12.7 cm aluminum handles) and sampled all possible flower blooms at collecting locations. Both pan trap and sweep netted specimens were labeled with collection information and placed in vials of 70% ethanol. Elevations of individual collection sites were estimated using the recorded GPS coordinates and freemaptool.com/elevation-finder.

Table 1.

WMNF collection site information. Numbers correspond to those found on the map in Figure 1

Map number Nearest Town Latitude Longitude Elevation (m) Bee Abundance Bee Diversity 
Milan 44.6 −71.2 334 18 16 
Berlin 44.5 −71.3 434 194 63 
Randolph 44.4 −71.3 892 68 28 
Gorham 44.4 −71.1 349 119 43 
Jefferson 44.4 −71.4 612 33 26 
Whitefield 44.4 −71.6 390 
Pinkham's Grant 44.3 −71.2 619 21 17 
Mount Washington Area 44.3 −71.3 1160 157 40 
Bretton Woods 44.3 −71.4 967 112 29 
10 Bartlett 44.1 −71.3 343 68 26 
11 Livermore 44.0 −71.4 419 13 
12 Hart's Location 44.1 −71.4 783 
13 Albany 44.0 −71.2 512 35 23 
14 Conway 44.0 −71.1 184 111 35 
15 Benton 44.0 −71.8 957 15 
16 Hanover 43.7 −72.3 118 36 17 
Total for all towns in survey    1010 137 
Durham 43.1 −71.0 26 2297 118 
Map number Nearest Town Latitude Longitude Elevation (m) Bee Abundance Bee Diversity 
Milan 44.6 −71.2 334 18 16 
Berlin 44.5 −71.3 434 194 63 
Randolph 44.4 −71.3 892 68 28 
Gorham 44.4 −71.1 349 119 43 
Jefferson 44.4 −71.4 612 33 26 
Whitefield 44.4 −71.6 390 
Pinkham's Grant 44.3 −71.2 619 21 17 
Mount Washington Area 44.3 −71.3 1160 157 40 
Bretton Woods 44.3 −71.4 967 112 29 
10 Bartlett 44.1 −71.3 343 68 26 
11 Livermore 44.0 −71.4 419 13 
12 Hart's Location 44.1 −71.4 783 
13 Albany 44.0 −71.2 512 35 23 
14 Conway 44.0 −71.1 184 111 35 
15 Benton 44.0 −71.8 957 15 
16 Hanover 43.7 −72.3 118 36 17 
Total for all towns in survey    1010 137 
Durham 43.1 −71.0 26 2297 118 

Total abundance and diversity counts for this survey are in bold italics. Collection information for comparison purposes from the Tucker and Rehan (2016) study in Strafford County, NH is marked with an asterisk.

Curation and Preservation

Ethanol preserved specimens were washed under running tap water for 1 min, dried with a traveling bee dryer (a section of PVC pipe covered with a fine screen that a hair dryer blows through; modified from devices in Droege 2015), pinned and labeled with locality information. All specimens were identified to species, or species-group where appropriate, using standard taxonomic literature (Mitchell 1960; 1962, Michener et al. 1994, Gibbs 2011, Rehan and Sheffield 2011, Williams et al. 2014) and the identification guides available on DiscoverLife.org. To determine species previously documented in the state of New Hampshire specimens were compared to distribution records on DiscoverLife.org and records compiled from Bartomeus et al. (2013) and Tucker and Rehan (2016). Exotic species introductions were identified using the Very Handy Manual (Droege 2015). Voucher specimens are deposited in the University of New Hampshire Insect Collection (Durham, NH), USGS Native Bee Inventory and Monitoring Lab collection (Beltsville, MD), and the National Museum of Natural History (Washington, DC).

Results

Diversity and Abundance

A total of 1,010 bee specimens were collected from pan trap and sweep net sampling (Table 2). Of the specimens collected, 137 species were identified, in 18 genera, representing five bee families. Halictidae was by far the most abundant family represented with 472 specimens collected compared with 231 Apidae and 212 Andrenidae. It was also the most diverse with 52 species followed by 33 Andrenidae, 23 Apidae, 21 Megachilidae, and 6 Colletidae species. The most abundant genera were Lasioglossum (301 specimens), Andrena (202 specimens) and Bombus (182 specimens). Lasioglossum was also the most diverse genera with 37 species and Andrena close behind with 31 species. Although Halictidae was both the most abundant and diverse family, the two most abundant species found were Andrena wilkella (Kirby 1802) (Andrenidae, 81 specimens) and B.terricola (Apidae, 73 specimens). Both the highest abundance and diversity of bees in the WMNF were found at an elevation of 434m near Berlin, NH (Table 1). We also found 73 species (Fig. 2, Table 2) in the WMNF that were not found at lower elevations (26 m) the previous year (2014) in Strafford County, New Hampshire, during a comprehensive bee biodiversity survey (Tucker and Rehan 2016).

Fig. 2.

Venn diagram depicting the species of overlap (light gray) between wild bees surveyed in the WMNF (dark gray) and those documented by Tucker and Rehan (2016) in the same state at a much lower elevation in Strafford County, NH (medium gray).

Fig. 2.

Venn diagram depicting the species of overlap (light gray) between wild bees surveyed in the WMNF (dark gray) and those documented by Tucker and Rehan (2016) in the same state at a much lower elevation in Strafford County, NH (medium gray).

Table 2.

Species checklist of all the wild bee species recorded in the WMNF in June, 2015 and previously published records for Strafford County, NH in 2014 (Tucker and Rehan 2016)

Family Species Species authority New record WMNF abundance WMNF relative abundance Tucker and Rehan abundance Tucker and Rehan relative abundance 
Andrenidae        
 Andrena accepta Viereck 1916 yes 0.1% – – 
 Andrena alleghaniensis Viereck 1907  0.3% 0.04% 
 Andrena asteris Robertson 1891  – – 0.26% 
 Andrena bisalicis Viereck 1908  – – 0.04% 
 Andrena braccata Viereck 1907  – – 0.13% 
 Andrena brevipalpis Cockerell 1930  0.2% – – 
 Andrena canadensis Dalla Torre 1896  0.1% – – 
 Andrena carlini Cockerell 1901  – – 13 0.57% 
 Andrena carolina Viereck 1909  0.1% 0.04% 
 Andrena ceanothi Viereck 1917  0.2% – – 
 Andrena commoda Smith 1879  12 1.2% 0.13% 
 Andrena confederata Viereck 1917  0.2% 0.04% 
 Andrena crataegi Robertson 1893  21 2.1% 0.09% 
 Andrena cressonii Robertson 1891  0.5% 0.35% 
 Andrena distans Provancher 1888  – – 0.17% 
 Andrena dunningi Cockerell 1898  – – 0.17% 
 Andrena erigeniae Robertson 1891  – – 0.26% 
 Andrena erythronii Robertson 1891  – – 0.04% 
 Andrena forbesii Robertson 1891  0.2% – – 
 Andrena fragilis Smith 1853  – – 0.04% 
 Andrena frigida Smith 1853  – – 0.04% 
 Andrena geranii Robertson 1891  – – 0.04% 
 Andrena heraclei Robertson 1897 yes 0.1% – – 
 Andrena hilaris Smith 1853  – – 0.04% 
 Andrena hippotes Robertson 1895  0.2% – – 
 Andrena hirticincta Provancher 1888  – – 0.13% 
 Andrena ignota LaBerge 1967  – – 0.04% 
 Andrena imitatrix Cresson 1872  0.3% 0.04% 
 Andrena kalmiae Atwood 1934  0.1% – – 
 Andrena krigiana Robertson 1901  0.1% 0.04% 
 Andrena mandibularis Robertson 1892  0.1% – – 
 Andrena mariae Robertson 1891  0.1% – – 
 Andrena milwaukeensis Graenicher 1903  17 1.7% – – 
 Andrena miranda Smith 1879  0.4% – – 
 Andrena miserabilis Cresson 1872  0.2% 10 0.44% 
 Andrena nasonii Robertson 1895  – – 0.04% 
 Andrena nigra Smith 1853 yes 0.1% – – 
 Andrena nigrihirta (Ashmead 1890)  0.5% – – 
 Andrena nivalis Smith 1853  0.8% 0.26% 
 Andrena perplexa Smith 1853  – – 0.22% 
 Andrena regularis Malloch 1917  0.1% 0.04% 
 Andrena robertsonii Dalla Torre 1896  0.2% 0.04% 
 Andrena rudbeckiae Robertson 1891  – – 0.04% 
 Andrena rufosignata Cockerell 1902  0.3% – – 
 Andrena sigmundi Cockerell 1902  – – 0.09% 
 Andrena simplex Smith 1853  – – 0.04% 
 Andrena spiraeana Robertson 1895  0.3% – – 
 Andrena thaspii Graenicher 1903  11 1.1% – – 
 Andrena vicina Smith 1853  – – 0.09% 
 Andrena w-scripta Viereck 1904  0.4% – – 
 Andrena wilkella* (Kirby 1802)  81 8.0% 13 0.57% 
 Andrena ziziae Robertson 1891  0.1% – – 
 Calliopsis andreniformis Smith 1853  0.7% 25 1.09% 
 Calliopsis nebraskensis Crawford 1902  – – 0.09% 
 Protandrena bancrofti Dunning 1897  – – 0.04% 
Apidae        
 Anthophora terminalis Cresson 1869  - – 0.13% 
 Bombus bimaculatus Cresson 1863  0.8% 48 2.09% 
 Bombus borealis Kirby 1837  0.2% – – 
 Bombus fervidus (F. 1798)  0.1% 0.04% 
 Bombus griseocollis (DeGeer 1773)  0.2% 0.17% 
 Bombus impatiens Cresson 1863  0.5% 423 18.42% 
 Bombus perplexus Cresson 1863  0.9% 0.04% 
 Bombus sandersoni Franklin 1913  16 1.6% – – 
 Bombus ternarius Say 1837  33 3.3% – – 
 Bombus terricola Kirby 1837  73 7.2% – – 
 Bombus vagans Smith 1854  33 3.3% 43 1.87% 
 Ceratina calcarata Robertson 1900  0.4% 33 1.44% 
 Ceratina dupla Say 1837  18 1.8% 16 0.70% 
 Ceratina mikmaqi Rehan and Sheffield 2011  0.7% 13 0.57% 
 Ceratina strenua Smith 1879  0.1% – – 
 Melissodes druriella (Kirby 1802)  – – 0.17% 
 Melissodes subillata LaBerge 1961  – – 0.22% 
 Melissodes trinodis Robertson 1901  – – 0.04% 
 Nomada articulata Smith 1854  0.4% 0.13% 
 Nomada australis Mitchell 1962  0.1% – – 
 Nomada bella Cresson 1863  – – 0.04% 
 Nomada bidentate species-group   0.3% – – 
 Nomada depressa Cresson 1863  0.1% – – 
 Nomada florilega Lovell and Cockerell 1905  – – 0.04% 
 Nomada gracilis Cresson 1863  0.1% – – 
 Nomada lehighensis Cockerell 1903  0.1% – – 
 Nomada lepida Cresson 1863  – – 0.09% 
 Nomada maculata Cresson 1863  – – 0.09% 
 Nomada pygmaea Cresson 1863  0.3% – – 
 Nomada sayi Robertson 1893  0.1% – – 
 Nomada valida Smith 1854  0.4% – – 
 Peponapis pruinosa (Say 1837)  – – 0.13% 
 Xylocopa virginica (L. 1771)  – – 25 1.09% 
Colletidae        
 Colletes inaequalis Say 1837  - – 0.04% 
 Hylaeus affinis (Smith 1853)  - – 0.35% 
 Hylaeus affinis/modestus (Smith 1853)/(Cockerell 1896)  0.7% – – 
 Hylaeus annulatus (L. 1758)  0.3% 0.04% 
 Hylaeus basalis (Smith 1853)  0.2% – – 
 Hylaeus mesillae (Cockerell 1896)  0.2% 0.04% 
 Hylaeus modestus Say 1837  0.9% 0.13% 
 H. nelumbonis (Robertson 1890) yes 0.2% – – 
Halictidae        
 Agapostemon sericeus (Forster 1771)  0.8% – – 
 Agapostemon texanus Cresson 1872  0.2% 15 0.65% 
 Agapostemon virescens (F. 1775)  54 5.3% 410 17.85% 
 Augochlora pura (Say 1837)  0.4% 0.09% 
 Augochlora aurata (Smith 1853)  48 4.8% 161 7.01% 
 Augochloropsis metallica (F. 1793)  – – 0.17% 
 Halictus confusus Smith 1853  13 1.3% 27 1.18% 
 Halictus ligatus Say 1837  25 2.5% 309 13.45% 
 Halictus rubicundus (Christ 1791)  0.7% 26 1.13% 
 Halictus tectus* Radoszkowski 1876  – – 0.04% 
 Lasioglossum abanci (Crawford 1932)  – – 0.04% 
 Lasioglossum achilleae (Mitchell 1960 – – 0.04% 
 Lasioglossum acuminatum McGinley 1986  0.2% – – 
 Lasioglossum admirandum (Sandhouse 1924)  0.2% 21 0.91% 
 Lasioglossum albipenne (Robertson 1890)  – – 10 0.44% 
 Lasioglossum atwoodi Gibbs 2010  – – 0.04% 
 Lasioglossum birkmanni (Crawford 1906)  0.1% – – 
 Lasioglossum boreale Svensson, Ebmer and Sakagami 1977  0.1% – – 
 Lasioglossum bruneri (Crawford 1902)  – – 0.09% 
 Lasioglossum cinctipes (Provancher 1888)  0.1% 0.13% 
 Lasioglossum coeruleus (Robertson 1893)  – – 0.04% 
 Lasioglossum coriaceum (Smith 1853)  29 2.9% 65 2.83% 
 Lassioglossum creberrimum (Smith 1853) yes 0.2% – – 
 Lassioglossum cressonii (Robertson 1890)  52 5.1% 67 2.92% 
 Lasioglossum ephialtum Gibbs 2010  0.8% – – 
 Lasioglossum fuscipenne (Smith 1853)  0.2% 11 0.48% 
 Lassioglossum hemimelas (Cockerell 1901) yes 0.1% – – 
 Lasioglossum heterognathum (Mitchell 1960 – – 0.04% 
 Lasioglossum hitchensi Gibbs 2012  0.1% 0.09% 
 Lasioglossum imitatum (Smith 1853)  16 1.6% 0.04% 
 Lasioglossum inconditum (Cockerell 1916)  0.2% – – 
 Lasioglossum laevissimum (Smith 1853)  0.2% 17 0.74% 
 Lasioglossum leucocomum (Lovell 1908)  10 1.0% 0.09% 
 Lassioglossum leucozonium* (Schrank 1781)  10 1.0% 0.22% 
 Lasioglossum lineatulum (Crawford 1906)  – – 0.22% 
 Lasioglossum macoupinense (Robertson 1895)  0.2% – – 
 Lasioglossum nigroviride (Graenicher 1911)  10 1.0% – – 
 Lasioglossum nr. tenax (Sandhouse 1924)  0.5% – – 
 Lasioglossum nymphaerum (Cockerell 1916)  0.5% 0.22% 
 Lasioglossum oblongum (Lovell 1905)  0.6% – – 
 Lasioglossum oenotherae (Stevens 1920)  0.6% – – 
 Lasioglossum paradmirandium (Knerer and Atwood 1966)  0.5% 0.17% 
 Lasioglossum pectorale (Smith 1853)  17 1.7% 0.26% 
 Lasioglossum pilosum (Smith 1853)  37 3.7% 89 3.87% 
 Lasioglossum planatum (Lovell 1905)  0.4% – – 
 Lasioglossum quebecense (Crawford 1907)  – – 0.09% 
 Lassioglossum sagax (Sandhouse 1924) yes 11 1.1% – – 
 Lassioglossum seillean Gibbs and Packer 2013 yes 0.1% – – 
 Lasioglossum smilacinae (Robertson 1897)  0.1% – – 
 Lasioglossum sp.   0.8% 0.26% 
 Lasioglossum subversans (Mitchell 1960 0.5% – – 
 Lasioglossum subviridatum (Cockerell 1938)  0.1% – – 
 Lasioglossum taylorae Gibbs 2010  0.2% – – 
 Lasioglossum tegulare (Robertson 1890)  17 1.7% 69 3.00% 
 Lasioglossum truncatum (Robertson 1901)  – – 0.04% 
 Lasioglossum versans (Lovell 1905)  0.9% 0.13% 
 Lasioglossum versatum (Robertson 1902)  0.5% 84 3.66% 
 Lasioglossum viridatum (Lovell 1905)  0.2% – – 
 Lasioglossum zonulum* (Smith 1848)  – – 0.04% 
 Sphecodes antennariae Robertson 1891  – – 0.04% 
 Sphecodes clematidis Robertson 1897  – – 0.09% 
 Sphecodes coronus Mitchell 1956 yes 0.2% – – 
 Sphecodes cressonii (Robertson 1903)  0.1% – – 
 Sphecodes johnsonii Lovell 1909  – – 0.09% 
 Sphecodes levis Lovell and Cockerell 1907  0.2% 0.04% 
 Sphecodes minor Robertson 1898  0.1% – – 
 Sphecodes prosphorus Lovell and Cockerell 1907  0.1% – – 
 Sphecodes sp. –  0.1% 0.04% 
 Sphecodes species_A –  0.1% – – 
 Sphecodes species_D –  0.1% – – 
Megachilidae        
 Anthidium manicatum* (L. 1758)  0.1% 0.04% 
 Anthidium oblongatum* (Illiger 1806)  0.3% 0.35% 
 Coelioxys porterae Cockerell 1900  0.1% – – 
 Coelioxys sayi Robertson 1897  0.1% – – 
 Coelioxys sodalis Cresson 1878  0.3% – – 
 Heriades carinata Cresson 1864  0.1% 0.09% 
 Hoplitis producta (Cresson 1864)  13 1.3% – – 
 Hoplitis simplex (Cresson 1864) yes 0.1% – – 
 Hoplitis spoliata (Provancher 1888)  0.1% 0.04% 
 Hoplitis truncata (Cresson 1878)  0.2% – – 
 Megachile centuncularis (L. 1758)  – – 0.09% 
 Megachile gemula Cresson 1878  0.8% – – 
 Megachile inermis Provancher 1888  – – 0.17% 
 Megachile latimanus Say 1823  0.2% – – 
 Megachile melanophaea Smith 1853  12 1.2% – – 
 Megachile relativa Cresson 1878  0.6% 0.04% 
 Osmia albiventris Cresson 1864  0.1% – – 
 Osmia atriventris Cresson 1864  0.3% 0.13% 
 Osmia bucephala Cresson 1864  0.2% – – 
 Osmia collinsiae Robertson 1905  0.1% – – 
 Osmia cornifrons* (Radoszkowski 1887)  – – 0.04% 
 Osmia proxima Cresson 1864  0.5% – – 
 Osmia georgica Cresson 1878  – – 0.04% 
 Osmia inermis (Zetterstedt 1838)  – – 0.39% 
 Osmia inspergens Lovell and Cockerell 1907  – – 0.26% 
 Osmia pumila Cresson 1864  0.2% – – 
 Osmia tersula Cockerell 1912  0.1% – – 
 Osmia taurus* Smith 1873  – – 0.04% 
Melittidae        
 Melllita eickworti Snelling and Stage 1995  – – 0.04% 
Family Species Species authority New record WMNF abundance WMNF relative abundance Tucker and Rehan abundance Tucker and Rehan relative abundance 
Andrenidae        
 Andrena accepta Viereck 1916 yes 0.1% – – 
 Andrena alleghaniensis Viereck 1907  0.3% 0.04% 
 Andrena asteris Robertson 1891  – – 0.26% 
 Andrena bisalicis Viereck 1908  – – 0.04% 
 Andrena braccata Viereck 1907  – – 0.13% 
 Andrena brevipalpis Cockerell 1930  0.2% – – 
 Andrena canadensis Dalla Torre 1896  0.1% – – 
 Andrena carlini Cockerell 1901  – – 13 0.57% 
 Andrena carolina Viereck 1909  0.1% 0.04% 
 Andrena ceanothi Viereck 1917  0.2% – – 
 Andrena commoda Smith 1879  12 1.2% 0.13% 
 Andrena confederata Viereck 1917  0.2% 0.04% 
 Andrena crataegi Robertson 1893  21 2.1% 0.09% 
 Andrena cressonii Robertson 1891  0.5% 0.35% 
 Andrena distans Provancher 1888  – – 0.17% 
 Andrena dunningi Cockerell 1898  – – 0.17% 
 Andrena erigeniae Robertson 1891  – – 0.26% 
 Andrena erythronii Robertson 1891  – – 0.04% 
 Andrena forbesii Robertson 1891  0.2% – – 
 Andrena fragilis Smith 1853  – – 0.04% 
 Andrena frigida Smith 1853  – – 0.04% 
 Andrena geranii Robertson 1891  – – 0.04% 
 Andrena heraclei Robertson 1897 yes 0.1% – – 
 Andrena hilaris Smith 1853  – – 0.04% 
 Andrena hippotes Robertson 1895  0.2% – – 
 Andrena hirticincta Provancher 1888  – – 0.13% 
 Andrena ignota LaBerge 1967  – – 0.04% 
 Andrena imitatrix Cresson 1872  0.3% 0.04% 
 Andrena kalmiae Atwood 1934  0.1% – – 
 Andrena krigiana Robertson 1901  0.1% 0.04% 
 Andrena mandibularis Robertson 1892  0.1% – – 
 Andrena mariae Robertson 1891  0.1% – – 
 Andrena milwaukeensis Graenicher 1903  17 1.7% – – 
 Andrena miranda Smith 1879  0.4% – – 
 Andrena miserabilis Cresson 1872  0.2% 10 0.44% 
 Andrena nasonii Robertson 1895  – – 0.04% 
 Andrena nigra Smith 1853 yes 0.1% – – 
 Andrena nigrihirta (Ashmead 1890)  0.5% – – 
 Andrena nivalis Smith 1853  0.8% 0.26% 
 Andrena perplexa Smith 1853  – – 0.22% 
 Andrena regularis Malloch 1917  0.1% 0.04% 
 Andrena robertsonii Dalla Torre 1896  0.2% 0.04% 
 Andrena rudbeckiae Robertson 1891  – – 0.04% 
 Andrena rufosignata Cockerell 1902  0.3% – – 
 Andrena sigmundi Cockerell 1902  – – 0.09% 
 Andrena simplex Smith 1853  – – 0.04% 
 Andrena spiraeana Robertson 1895  0.3% – – 
 Andrena thaspii Graenicher 1903  11 1.1% – – 
 Andrena vicina Smith 1853  – – 0.09% 
 Andrena w-scripta Viereck 1904  0.4% – – 
 Andrena wilkella* (Kirby 1802)  81 8.0% 13 0.57% 
 Andrena ziziae Robertson 1891  0.1% – – 
 Calliopsis andreniformis Smith 1853  0.7% 25 1.09% 
 Calliopsis nebraskensis Crawford 1902  – – 0.09% 
 Protandrena bancrofti Dunning 1897  – – 0.04% 
Apidae        
 Anthophora terminalis Cresson 1869  - – 0.13% 
 Bombus bimaculatus Cresson 1863  0.8% 48 2.09% 
 Bombus borealis Kirby 1837  0.2% – – 
 Bombus fervidus (F. 1798)  0.1% 0.04% 
 Bombus griseocollis (DeGeer 1773)  0.2% 0.17% 
 Bombus impatiens Cresson 1863  0.5% 423 18.42% 
 Bombus perplexus Cresson 1863  0.9% 0.04% 
 Bombus sandersoni Franklin 1913  16 1.6% – – 
 Bombus ternarius Say 1837  33 3.3% – – 
 Bombus terricola Kirby 1837  73 7.2% – – 
 Bombus vagans Smith 1854  33 3.3% 43 1.87% 
 Ceratina calcarata Robertson 1900  0.4% 33 1.44% 
 Ceratina dupla Say 1837  18 1.8% 16 0.70% 
 Ceratina mikmaqi Rehan and Sheffield 2011  0.7% 13 0.57% 
 Ceratina strenua Smith 1879  0.1% – – 
 Melissodes druriella (Kirby 1802)  – – 0.17% 
 Melissodes subillata LaBerge 1961  – – 0.22% 
 Melissodes trinodis Robertson 1901  – – 0.04% 
 Nomada articulata Smith 1854  0.4% 0.13% 
 Nomada australis Mitchell 1962  0.1% – – 
 Nomada bella Cresson 1863  – – 0.04% 
 Nomada bidentate species-group   0.3% – – 
 Nomada depressa Cresson 1863  0.1% – – 
 Nomada florilega Lovell and Cockerell 1905  – – 0.04% 
 Nomada gracilis Cresson 1863  0.1% – – 
 Nomada lehighensis Cockerell 1903  0.1% – – 
 Nomada lepida Cresson 1863  – – 0.09% 
 Nomada maculata Cresson 1863  – – 0.09% 
 Nomada pygmaea Cresson 1863  0.3% – – 
 Nomada sayi Robertson 1893  0.1% – – 
 Nomada valida Smith 1854  0.4% – – 
 Peponapis pruinosa (Say 1837)  – – 0.13% 
 Xylocopa virginica (L. 1771)  – – 25 1.09% 
Colletidae        
 Colletes inaequalis Say 1837  - – 0.04% 
 Hylaeus affinis (Smith 1853)  - – 0.35% 
 Hylaeus affinis/modestus (Smith 1853)/(Cockerell 1896)  0.7% – – 
 Hylaeus annulatus (L. 1758)  0.3% 0.04% 
 Hylaeus basalis (Smith 1853)  0.2% – – 
 Hylaeus mesillae (Cockerell 1896)  0.2% 0.04% 
 Hylaeus modestus Say 1837  0.9% 0.13% 
 H. nelumbonis (Robertson 1890) yes 0.2% – – 
Halictidae        
 Agapostemon sericeus (Forster 1771)  0.8% – – 
 Agapostemon texanus Cresson 1872  0.2% 15 0.65% 
 Agapostemon virescens (F. 1775)  54 5.3% 410 17.85% 
 Augochlora pura (Say 1837)  0.4% 0.09% 
 Augochlora aurata (Smith 1853)  48 4.8% 161 7.01% 
 Augochloropsis metallica (F. 1793)  – – 0.17% 
 Halictus confusus Smith 1853  13 1.3% 27 1.18% 
 Halictus ligatus Say 1837  25 2.5% 309 13.45% 
 Halictus rubicundus (Christ 1791)  0.7% 26 1.13% 
 Halictus tectus* Radoszkowski 1876  – – 0.04% 
 Lasioglossum abanci (Crawford 1932)  – – 0.04% 
 Lasioglossum achilleae (Mitchell 1960 – – 0.04% 
 Lasioglossum acuminatum McGinley 1986  0.2% – – 
 Lasioglossum admirandum (Sandhouse 1924)  0.2% 21 0.91% 
 Lasioglossum albipenne (Robertson 1890)  – – 10 0.44% 
 Lasioglossum atwoodi Gibbs 2010  – – 0.04% 
 Lasioglossum birkmanni (Crawford 1906)  0.1% – – 
 Lasioglossum boreale Svensson, Ebmer and Sakagami 1977  0.1% – – 
 Lasioglossum bruneri (Crawford 1902)  – – 0.09% 
 Lasioglossum cinctipes (Provancher 1888)  0.1% 0.13% 
 Lasioglossum coeruleus (Robertson 1893)  – – 0.04% 
 Lasioglossum coriaceum (Smith 1853)  29 2.9% 65 2.83% 
 Lassioglossum creberrimum (Smith 1853) yes 0.2% – – 
 Lassioglossum cressonii (Robertson 1890)  52 5.1% 67 2.92% 
 Lasioglossum ephialtum Gibbs 2010  0.8% – – 
 Lasioglossum fuscipenne (Smith 1853)  0.2% 11 0.48% 
 Lassioglossum hemimelas (Cockerell 1901) yes 0.1% – – 
 Lasioglossum heterognathum (Mitchell 1960 – – 0.04% 
 Lasioglossum hitchensi Gibbs 2012  0.1% 0.09% 
 Lasioglossum imitatum (Smith 1853)  16 1.6% 0.04% 
 Lasioglossum inconditum (Cockerell 1916)  0.2% – – 
 Lasioglossum laevissimum (Smith 1853)  0.2% 17 0.74% 
 Lasioglossum leucocomum (Lovell 1908)  10 1.0% 0.09% 
 Lassioglossum leucozonium* (Schrank 1781)  10 1.0% 0.22% 
 Lasioglossum lineatulum (Crawford 1906)  – – 0.22% 
 Lasioglossum macoupinense (Robertson 1895)  0.2% – – 
 Lasioglossum nigroviride (Graenicher 1911)  10 1.0% – – 
 Lasioglossum nr. tenax (Sandhouse 1924)  0.5% – – 
 Lasioglossum nymphaerum (Cockerell 1916)  0.5% 0.22% 
 Lasioglossum oblongum (Lovell 1905)  0.6% – – 
 Lasioglossum oenotherae (Stevens 1920)  0.6% – – 
 Lasioglossum paradmirandium (Knerer and Atwood 1966)  0.5% 0.17% 
 Lasioglossum pectorale (Smith 1853)  17 1.7% 0.26% 
 Lasioglossum pilosum (Smith 1853)  37 3.7% 89 3.87% 
 Lasioglossum planatum (Lovell 1905)  0.4% – – 
 Lasioglossum quebecense (Crawford 1907)  – – 0.09% 
 Lassioglossum sagax (Sandhouse 1924) yes 11 1.1% – – 
 Lassioglossum seillean Gibbs and Packer 2013 yes 0.1% – – 
 Lasioglossum smilacinae (Robertson 1897)  0.1% – – 
 Lasioglossum sp.   0.8% 0.26% 
 Lasioglossum subversans (Mitchell 1960 0.5% – – 
 Lasioglossum subviridatum (Cockerell 1938)  0.1% – – 
 Lasioglossum taylorae Gibbs 2010  0.2% – – 
 Lasioglossum tegulare (Robertson 1890)  17 1.7% 69 3.00% 
 Lasioglossum truncatum (Robertson 1901)  – – 0.04% 
 Lasioglossum versans (Lovell 1905)  0.9% 0.13% 
 Lasioglossum versatum (Robertson 1902)  0.5% 84 3.66% 
 Lasioglossum viridatum (Lovell 1905)  0.2% – – 
 Lasioglossum zonulum* (Smith 1848)  – – 0.04% 
 Sphecodes antennariae Robertson 1891  – – 0.04% 
 Sphecodes clematidis Robertson 1897  – – 0.09% 
 Sphecodes coronus Mitchell 1956 yes 0.2% – – 
 Sphecodes cressonii (Robertson 1903)  0.1% – – 
 Sphecodes johnsonii Lovell 1909  – – 0.09% 
 Sphecodes levis Lovell and Cockerell 1907  0.2% 0.04% 
 Sphecodes minor Robertson 1898  0.1% – – 
 Sphecodes prosphorus Lovell and Cockerell 1907  0.1% – – 
 Sphecodes sp. –  0.1% 0.04% 
 Sphecodes species_A –  0.1% – – 
 Sphecodes species_D –  0.1% – – 
Megachilidae        
 Anthidium manicatum* (L. 1758)  0.1% 0.04% 
 Anthidium oblongatum* (Illiger 1806)  0.3% 0.35% 
 Coelioxys porterae Cockerell 1900  0.1% – – 
 Coelioxys sayi Robertson 1897  0.1% – – 
 Coelioxys sodalis Cresson 1878  0.3% – – 
 Heriades carinata Cresson 1864  0.1% 0.09% 
 Hoplitis producta (Cresson 1864)  13 1.3% – – 
 Hoplitis simplex (Cresson 1864) yes 0.1% – – 
 Hoplitis spoliata (Provancher 1888)  0.1% 0.04% 
 Hoplitis truncata (Cresson 1878)  0.2% – – 
 Megachile centuncularis (L. 1758)  – – 0.09% 
 Megachile gemula Cresson 1878  0.8% – – 
 Megachile inermis Provancher 1888  – – 0.17% 
 Megachile latimanus Say 1823  0.2% – – 
 Megachile melanophaea Smith 1853  12 1.2% – – 
 Megachile relativa Cresson 1878  0.6% 0.04% 
 Osmia albiventris Cresson 1864  0.1% – – 
 Osmia atriventris Cresson 1864  0.3% 0.13% 
 Osmia bucephala Cresson 1864  0.2% – – 
 Osmia collinsiae Robertson 1905  0.1% – – 
 Osmia cornifrons* (Radoszkowski 1887)  – – 0.04% 
 Osmia proxima Cresson 1864  0.5% – – 
 Osmia georgica Cresson 1878  – – 0.04% 
 Osmia inermis (Zetterstedt 1838)  – – 0.39% 
 Osmia inspergens Lovell and Cockerell 1907  – – 0.26% 
 Osmia pumila Cresson 1864  0.2% – – 
 Osmia tersula Cockerell 1912  0.1% – – 
 Osmia taurus* Smith 1873  – – 0.04% 
Melittidae        
 Melllita eickworti Snelling and Stage 1995  – – 0.04% 

New records are the first documentation of a species for the state of New Hampshire. Species with asterisk are introduced species.

New Records and Introduced Species

Three species were discovered for the first time in New England from this survey (Andrena nigra, Provancher 1895; Lasioglossum hemimelas, Cockerell 1901; Lasioglossum seillean, Gibbs and Packer 2013). Seven species were documented for the first time in New Hampshire (Andrena accepta, Viereck 1916; Andrena heraclei, Robertson 1897; Hoplitis simplex, Cresson 1864; Hylaeus nelumbonis, Robertson 1890; Lasioglossum creberrimum, Smith 1853; Lasioglossum sagax, Sandhouse 1924; Sphecodes coronus, Mitchell 1956; Table 2). Four introduced species (indicated by an asterisk in Table 2) were found in the WMNF (A. wilkella, Anthidium manicatum, (L.) 1758; Anthidium oblongatum, Illiger 1806; Lasioglossum leucozonium, Schrank 1781). All of these species have previously been recorded in the state of New Hampshire and, except for L. leucozonium, are relatively common species well established throughout the Northeast (Droege 2015).

The composition of the bee species recorded in the WMNF was also different than what has previously been recorded in other parts of New England. Of the 137 species recorded in the WMNF survey, 72 species were unique to the higher elevation area, while 54 of the 118 species previously documented in Stafford County (elevation 26 m; Tucker and Rehan 2016) were not found in WMNF and only 64 species were found in both areas (Fig. 2, Table 2).

Species of Concern

We found a relatively large population (73 specimens) of the New Hampshire species of concern B. terricola in the WMNF. Sampled sites near Bretton Woods, elevation 967 m, had the highest number of specimens recorded (20) with survey locations near Conway (elev. 184 m, 17 specimens) and Berlin (elev. 434 m) also containing many (12) specimens of B. terricola. One specimen of B. fervidus was discovered in Hanover (elev. 118 m). We did not find any specimens of the other two species of concern: B. affinis or B. pensylvanicus.

Discussion

Abundance and Diversity

In the intensive 60 man-hour collecting period we found 137 wild bee species in the WMNF, which is a remarkable amount of diversity compared with much longer studies. In a 1-year period 124 bee species were found in St. Catharines, Ontario (Richards et al. 2011) and 118 in Strafford County, New Hampshire (Tucker and Rehan 2016). Over a 2-year period only 54 species were found in Illinois (Burkle et al. 2013) and 64 species in Pennsylvania (Russo et al. 2013), with higher diversity found in Connecticut with 163 species (Wagner et al. 2016) and Massachusetts with 182 species (Goldstein and Ascher 2016). In three years, 133 bee species were recorded in Maine (Bushmann and Drummond 2015), yet only 54 species were documented during a 4-year survey and 104 species in a 6-year survey in New York (Matteson et al. 2008, Russo et al. 2015) with an even longer 10-year study in Ontario only finding 150 species (Onuferko et al. 2015).

Despite these concerted collecting efforts and variable duration of these studies, many species that are known to be in the area are still missed as historical state records estimate 400 species in Ontario (MacKay and Knerer 1979, Grixti and Packer 2006, Sheffield et al. 2011), about 325 in New Hampshire (Discoverlife.org), 296 in Illinois (Marlin and LaBerge 2001), 371 species historically in Pennsylvania (Donovall and vanEngelsdorp 2010), at least 355 species in Connecticut (discoverlife.org), 377 documented in Massachusetts (Goldstein and Ascher 2016), 329 in Maine (discoverlife.org), and 447 species historically in New York (Ascher et al. 2014).

Obtaining accurate documentation of a region’s diverse bee fauna is not an easy task (Russo et al. 2015). Documentation of bee community diversity is exasperated by its inclusion of many rare and few abundant species that often exhibit significant annual variation and cryptic morphologies (Olesen and Jordano 2002, Wilson et al. 2008, Grundel et al. 2011, Russo et al. 2011). Both short term intensive surveys spanning many locations as well as long term studies conducted in the same location are required for representative species monitoring and documentation.

Where we found A. wilkella (an introduced species) and B. terricola (a species of concern) to be the dominant presence (Fig. 2, Table 2), other studies have found Bombus impatiens (Cresson 1863) to be dominant (Matteson et al. 2008, Russo et al. 2011, Tucker and Rehan 2016) as well as Augochlorella aurata (Smith 1853) (Wagner et al. 2014, Goldstein and Ascher 2016) and Lasioglossum cressonii (Robertson 1890) (Bushmann and Drummond 2015). The high abundance of A. wilkella found in the WMNF is, however, concordant with recent bee surveys, which also found this species to be widely distributed and abundant in Massachusetts (Goldstein and Ascher 2016). For a complete species list of the WMNF or New Hampshire in general, long-term surveys are needed as highlighted by the difference in species composition (Fig. 2) found in this study compared with that of Tucker and Rehan (2016). Although some differences in species composition may be attributed to different habitat or elevations between collection sites, much is likely due to the short-term nature of both studies (2 days and 1 year; Minckley et al. 1999; Grixti and Packer 2006) as many species found in just one of the two habitats are only represented by a few specimens (Table 2).

New Records and Introduced Species

Other species of note that were collected in the WMNF were three singleton specimens: one andrenid and two halictids. A.nigra is primarily a western species with few records east of the Rocky Mountains (DiscoverLife.org). L.hemimelas typically ranges throughout the Midwest, while the specimen of L.seillean represents the southern most record of this northern species that is reported to be restricted to high altitudes (Gibbs et al. 2013). L. seillean has been recorded as far south as Michigan, but is typically found from the Northwest Territories to Newfoundland and south to New Brunswick (DiscoverLife.org, Gibbs et al. 2013). It is possible that these specimens may predict future range expansions for these species; however, more data would certainly be needed to support this conjecture. The other seven species representing new state records were somewhat expected as they have previously been found in the northern New England region, but not previously documented in New Hampshire.

Species of Concern

There was a relatively high abundance of B. terricola (40% of collected Bombus) found in the WMNF. A low abundance of this species (1% of collected Bombus records) was recently found in Maine (Bushmann and Drummond 2015), but this species is not reported in any of the other bee faunal studies in New England (Wagner et al. 2014, Goldstein and Ascher 2016, Tucker and Rehan 2016). This high abundance of B. terricola does however corroborate some findings suggesting populations may still be enduring, but relegated to areas of higher elevation (Colla et al. 2012, Hatfield et al. 2015c). The seeming relegation of B. terricola populations to higher elevation refugial habitats may lead to evolutionary consequences detrimental to the species long-term persistence (Cameron et al. 2011). Bees tend to be particularly vulnerable to genetic threats, reducing community fitness and species potential viability, especially in small population sizes (Zayed 2009). If populations of B. terricola become isolated in these high elevation refugia, reduced gene flow between populations could contribute to further species decline (Cameron et al. 2011).

A single specimen of B. fervidus was collected during this survey. Only a single specimen of this species was found in the recent Massachusetts survey (Goldstein and Ascher 2016), with two specimens (0.2% of total Bombus) found in Maine in 2010 (Bushmann and Drummond 2015). An additional 14 specimens were found in Connecticut between 2005 and 2006, but this still only made up 4% of all the Bombus collected during that study (Wagner et al. 2014). We did not find any specimens of the two other bumble bee species of concern, B. affinis and B. pensylvanicus. What was historically a common species throughout eastern North America (Millrion 1971, Hatfield et al 2015a), B. affinis, is now believed to be on the brink of extinction and is closely related to B. terricola (Cameron et al. 2007). Based on data from the University of New Hampshire Insect Collection (UNHC) the last time B. affinis was documented in New Hampshire was 1993 when one specimen was discovered in Durham. There was however a single specimen sighted in Maine and one in Connecticut in 2015 (BumbleBeeWatch.org). It is even longer since B.pensylvanicus has been recorded in New Hampshire, although it was seldom documented historically in the state, with only six records (out of 1,246 total Bombus records, >0.1%) between 1899 and 1965 (UNHC). The last record of B. pensylvanicus in the state of New Hampshire was in Durham in 1965 (UNHC) and since then appears to be locally extirpated.

Conclusions

Protected areas such as national parks and forests can provide safe havens for vulnerable and endangered species of concern. This survey found the WMNF to be an excellent example of a terrestrial refuge for wild bees with its broad diversity of species being more speciose than other areas in the Northeast including relatively nearby habitats in the same state. Despite our thorough sampling of the WMNF, it is likely there are many more species residing and taking refuge in the WMNF as most ecosystems have a high species composition turnover and we sampled during a single two-day collection period. In addition to the high species diversity, the WMNF also appears to be a sanctuary for a considerable abundance of B. terricola, a species of particular concern in North America. The presence of B. terricola, as well as B. fervidus and numerous new state records including several species far outside their historical geographic range, underscores the importance of protected land areas in invertebrate conservation and the need for further bee biodiversity studies throughout New England.

Acknowledgments

We thank Sam Droege, Joan Milam and Michael Viet for assistance with bee collection and identification. We also thank Don Chandler and all the participants of the NH Bee Bioblitz for their assistance with fieldwork and specimen processing. We thank the National Forest Service and NH Fish and Wildlife for permitting this event as well as the Appalachian Mountain Club for providing accommodations. Partial funding was provided by the New Hampshire Agricultural Experiment Station. This work was supported by the USDA National Institute of Food and Agriculture Hatch Project 1004515.

References Cited

(AMC) Appalachian Mountain Club.
2016
. Hiking Mount Washington. (http://www.outdoors.org/recreation/tripplanner/plan/hiking-mt-washington.cfm).
Ascher
J. S.
Pickering
J.
.
2016
. Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). (http://www.discoverlife.org/mp/20q?guide=Apoidea_species).
Ascher
J. S.
Kornbluth
S.
Geolet
R. G.
.
2014
.
Bees (Hymenoptera: Apoidea: Anthophila) of Gardiners Island, Suffolk County, New York
.
Northeast. Nat
 .
21
:
47
71
.
Bartomeus
I.
Ascher
J. S.
Gibbs
J.
Danforth
B. N.
Wagner
D. L.
Hedtke
S. M.
Winfree
R.
.
2013
.
Historical Changes in northeastern US bee pollinators related to shared ecological traits
.
Proc. Natl. Acad. Sci. U.S.A
 .
110
:
4656
4660
.
Brown
J. H.
1971
.
Mammals on mountaintops: nonequilibrium insular biogeography
.
Am. Nat
 .
105
:
467
478
.
Burkle
L. A.
Marlin
J. C.
Knight
T. M.
.
2013
.
Plant-pollinator interactions over 120 years: Loss of species, co-occurrence and function
.
Science
 .
339
:
1611
1615
.
Bushmann
S. L.
Drummond
F. A.
.
2015
.
Abundance and diversity of wild bees (Hymenoptera: Apoidea) found in lowbush blueberry growing regions of downeast Maine
.
Environ. Entomol
 .
44
:
975
989
.
Cameron
S. A.
Hines
H. M.
Williams
P. H.
.
2007
.
A comprehensive phylogeny of the bumble bees (Bombus)
.
Biol. J. Linn. Soc
 .
91
:
161
188
.
Cameron
S. A.
Lozier
J. D.
Strange
J. P.
Koch
J. B.
Cordes
N.
Solter
L. F.
Griswold
T. L.
Robinson
G. L.
.
2011
.
Patterns of widespread decline in North American bumble bees
.
Proc. Natl. Acad. Sci. U.S.A
 .
108
:
662
667
.
Chandler
D. S.
1991
.
Comparison of some slime-mold and fungus feeding beetles (Coleoptera: Eucinetoidea, Cucujoidea) in an old-growth and 40-year-old forest in New Hampshire
.
Coleopt. Bull
 .
45
:
239
256
.
Chandler
D. S.
Peck
S. B.
.
1992
.
Diversity and seasonality of Leiodid Beetles (Coleoptera: Leiodidae) in an old-growth and a 40-year-old forest in New Hampshire
.
Environ. Entomol
 .
21
:
1283
1293
.
Colla
S. R.
Packer
L.
.
2008
.
Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson
.
Biodivers. Conserv
 .
17
:
1379
1391
.
Colla
S. R.
Gadallah
F.
Richardson
L.
Wagner
D.
Gall
L.
.
2012
.
Assessing declines of North American bumble bees (Bombus spp.) using museum specimens
.
Biodivers. Conserv
 .
21
:
3585
3595
.
Dean
C.
2000
.
Island insect trove could spur revival of mainland populations
.
New York Times
 
149
: 51,509.
Donovall
L. R.
vanEngelsdorp
D.
.
2010
.
A checklist of the bees (Hymenoptera: Apoidea) of Pennsylvania
.
J. Kans. Entomol. Soc
 .
83
:
7
24a
.
Droege
S.
2015
.
The very handy manual: how to catch and identify bees and manage a collection
 .
USGS Native Bee Inventory and Monitoring Lab
,
Beltsville, USA
.
Droege
S.
Jean
R.
Orr
M.
.
2016
. Discover Life bee genera of eastern North America. Draft. Discover Life. (http://www.discoverlife.org/mp/20q?guide=Bee_genera).
Evans
E.
Thorp
R.
Jepsen
S.
Black
S. H.
.
2008
. Status review of three formerly common species of bumble bee in the subgenus Bombus. Xerces Society. (http://www.xerces.org/wp-content/uploads/2009/03/xerces_2008_bombus_status_review.pdf).
Garibaldi
L. A.
Steffan-Dewenter
I.
Winfree
R.
Aizen
M. A.
Bommarco
R.
Cunningham
S. A.
Kremen
C.
Carvalheiro
L. G.
Harder
L. D.
Afik
O.
, et al.  .
2013
.
Wild pollinators enhance fruit set of crops regardless of honey bee abundance
.
Science
 .
339
:
1608
1611
.
Gibbs
J.
2011
.
Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini)
.
Zootaxa
 .
3073
:
1
216
.
Gibbs
J.
Packer
L.
Dumesh
S.
Danforth
B. N.
.
2013
.
Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae)
.
Zootaxa
 .
3672
:
001
117
.
Giles
V.
Ascher
J. S.
.
2006
.
Bees of the Black Rock Forest Preserve, New York (Hymenoptera: Apoidea)
.
J. Hymenoptera Res
 .
15
:
208
231
.
Gillespie
R. G.
Roderick
G. K.
.
2002
.
Arthropods on islands: Colonization, speciation, and conservation
.
Annu. Rev. Entomol
 .
47
:
595
632
.
Goldstein
P. Z.
Ascher
J. S.
.
2016
.
Taxonomic and behavioral composition of an island fauna: a survey of bees (Hymenopter: Apoidea: Anthophila) on Martha’s Vineyard, Massachusetts
.
Proc. Entomol. Soc. Wash
 .
118
:
37
92
.
Grixti
J. C.
Wong
L. T.
Cameron
S. A.
Favret
C.
.
2008
.
Decline of bumble bees (Bombus) in the American Midwest
.
Biol. Conserv
 .
142
:
75
84
.
Grixti
J. C.
Packer
L.
.
2006
.
Changes in the bee fauna (Hymenoptera: Apoidea) of an old field site in southern Ontario, revisited after 34 years
.
Can. Entomol
 .
138
:
147
164
.
Grundel
R.
Frohnapple
K. J.
Jean
R. P.
Pavlovic
N. B.
.
2011
.
Effectiveness of bowl trapping and netting for inventory of a bee community
.
Environ. Entomol
 .
40
:
374
380
.
Hatfield
R.
Jepsen
S.
Thorp
R.
Richardson
L.
Colla
S.
Foltz
J. S.
Evans
E.
.
2015a
. Bombus affinis. The IUCN Red List of Threatened Species 2015: e.T44937399A46440196. (http://dx.doi.org/10.2305/IUCN.UK.2015-2.RLTS.T44937399A46440196.en).
Hatfield
R.
Jepsen
S.
Thorp
R.
Richardson
L.
Colla
S.
Foltz
J. S.
.
2015b
. Bombus fervidus. The IUCN Red List of Threatened Species 2015: e.T21215132A21215225. (http://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T21215132A21215225.en).
Hatfield
R.
Jepsen
S.
Thorp
R.
Richardson
L.
Colla
S.
.
2015c
. B. terricola. The IUCN Red List of Threatened Species 2015: e.T44937505A46440206. (http://dx.doi.org/10.2305/IUCN.UK.2015-2.RLTS.T44937505A46440206.en).
Kerr
J. T.
Pindar
A.
Galpern
P.
Packer
L.
Potts
S. G.
Roberts
S. M.
Rasmont
P.
Schweiger
O.
Colla
S. R.
Richardson
L. L.
, et al.  .
2015
.
Climate change impacts on bumblebees converge across continents
.
Science
 
349
:
177
180
.
Kimball
K. D.
Weihrauch
D. M.
.
2000
. Wilderness science in a time of change conference. Alpine vegetation communities and the alpine-treeline ecotone boundary in New England as biomonitors for climate change, pp. 93-101. In Wilderness science in a time of change conference, Wilderness as a place for scientific inquiry, 23– 27 May 1999, Missoula, MT. Proceedings RMRS-P-15-VOL-3. U.S.Department of Agriculture, Forest Service, Rocky Mountain Research Station Ogden, UT.
Koh
I.
Lonsdorf
E. V.
Williams
N. M.
Brittain
C.
Isaacs
R.
Gibbs
J.
Ricketts
T. H.
.
2016
.
Modeling the status, trends, and impacts of wild bee abundance in the United States
.
Proc. Natl. Acad. Sci. U.S.A
 .
113
:
140
145
.
Levesque
C. M.
Burger
J. F.
.
1982
.
Insects (Diptera, Hymenoptera) associated with Minuartia groenlandica (Caryophyllaceae) on Mount Washington, New Hampshire, U.S.A., and their possible role as pollinators. Arct
.
Antarct. Alp. Res
 .
14
:
117
124
.
MacKay
P. A.
Knerer
G.
.
1979
.
Seasonal occurrence and abundance in a community of wild bees from an old field habitat in southern Ontario
.
Can. Entomol
 .
11
:
367
376
.
Matteson
K. C.
Ascher
J. S.
Langellotto
G. A.
.
2008
.
Bee richness and abundance in New York City urban gardens
.
Ann. Entomol. Soc. Am
 .
101
:
140
150
.
Marlin
J. C.
LaBerge
W. E.
.
2001
.
The native bee fauna of Carlinville, Illinois, revisited after 75 years: a case for persistence
.
Conserv. Ecol
 .
5
:
9.
McCall
C.
Primack
R. B.
.
1992
.
Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities
.
Am. J. Bot
 .
79
:
434
442
.
McFarland
K. P.
2003
. Conservation Assessment of two endemic butterflies (White Mountain Arctic, Oeneis melissa semidea, and White Mountain Fritillary, Boloria titania montinus) in the Presidential Range alpine zone White Mountains, New Hampshire. USDA, Forest Service.
McFarland
K. P.
Richardson
L.
Zahendra
S.
.
2015
. Vermont Bumble Bee Atlas. Vermont Center for Ecostudies – Vermont Atlas of Life. (http://val.vtecostudies.org).
Michener
C. D.
McGinley
R. J.
Danforth
B. N.
.
1994
.
The bee genera of North and Central America
 .
Smithsonian Institution Press
,
Washington, D. C
.
Milliron
H. E.
1971
.
A monograph of the western hemisphere bumblebees (Hymenoptera: Apidae; Bombinae)
.
Mem. Entomol. Soc. Can
 .
103
:
1
80
.
Minckley
R. L.
Cane
J. H.
Kervin
L.
Roulston
T. H.
.
1999
.
Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource
.
Biol. J. Linn. Soc
 .
67
:
119
147
.
Mitchell
T. B.
1960
. Bees of the eastern United States, vol. 1. Technical Bulletin no. 141, North Carolina Agricultural Experiment Station. Raleigh, North Carolina.
Mitchell
T. B.
1962
. Bees of the eastern United States, vol. 2. Technical Bulletin no. 152, North Carolina Agricultural Experiment Station. Raleigh, North Carolina.
Normandeau
G.
2015
. New Hampshire wildlife action plan, other insects: Tiger Beetles and Bees, Appendix A – Species Profiles. New Hampshire Fish and Game Department. (http://www.wildlife.state.nh.us/wildlife/documents/wap/appendixa-insects.pdf).
Ollerton
J.
Winfree
R.
Tarrant
S.
.
2011
.
How many flowering plants are pollinated by animals?
.
Oikos
 
120
:
321
326
.
Olesen
J. M.
Jordano
P.
.
2002
.
Geographic patterns in plant–pollinator mutualistic networks
.
Ecology
 
83
:
2416
2424
.
Onuferko
T. M.
Kutby
R.
Richards
M. H.
.
2015
.
A list of bee species (Hymenopter: Apoidea) recorded from three municipalities in the Niagara Region of Ontario, including a new record of Lasioglossum fuunculum Gibbs (Halictidae) in Canada
.
J. Entomol. Soc. Ont
 .
146
:
3
22
.
Potts
S. G.
Biesmeijer
J. C.
Kremen
C.
Neumann
P.
Schweiger
O.
Kunin
W. E.
.
2010
.
Global pollinator declines: trends, impacts and drivers
.
Trends Ecol. E
 .
25
:
345
353
.
Rehan
S. M.
Sheffield
C. S.
.
2011
.
Morphological and molecular delineation of a new species in the Ceratina dupla species-group (Hymenoptera: Apidae) of eastern North America
.
Zootaxa
 
2873
:
35
50
.
Reiners
W. A.
Lang
G. E.
.
1979
.
Vegetational patterns and processes in the balsam fir zone, White Mountains, New Hampshire
.
Ecology
 
60
:
403
417
.
Richards
M. H.
Rutgers-Kelly
A.
Gibbs
J.
Vickruck
J. L.
Rehan
S. M.
Sheffield
C. S.
.
2011
.
Bee diversity in naturalizing patches of Carolinian grasslands in southern Ontario, Canada
.
Can. Entomol
 .
143
:
279
299
.
Russo
L.
DeBarros
N.
Yang
S.
Shea
K.
Mortensen
D.
.
2013
.
Supporting crop pollinators with floral resources: network-based phenological matching
.
Ecol. E
 .
3
:
3125
3140
.
Russo
L.
Park
M.
Gibbs
J.
Danforth
B.
.
2015
.
The challenge of accurately documenting bee species richness in agroecosystems: bee diversity in eastern apple orchards
.
Ecol. E
 .
5
:
3531
3540
.
Sheffield
C. S.
Dumesh
S.
Cheryomina
M.
.
2011
.
Hylaeus punctatus (Hymenoptera: Colletidae), a bee species new to Canada, with notes on other non-native species
.
J. Entomol. Soc. Ont
 .
142
:
29
43
.
Tucker
E. M.
Rehan
S. M.
.
2016
.
Wild bee pollination networks in northern New England
.
J. Insect Conserv
 .
1
13
.
(USFS) U.S. Forest Service.
2012
. Land areas of the national forest system. USDA, Forest Service. (http://www.fs.fed.us/land/staff/lar/).
Wagner
D. L.
Ascher
J.
Bricker
N. K.
.
2014
.
A transmission right-of-way as habitat for wild bees (Hymenoptera: Apoidea: Anthophila) in Connecticut
.
Ann. Entomol. Soc. Am
 .
107
:
1110
1120
.
Williams
P. H.
Thorp
R. W.
Richardson
L. L.
Colla
S. R.
.
2014
.
Bumble bees of North America: An identification guide
 .
Princeton University Press
,
New Jersey
.
Wilson
J. S.
Griswold
T.
Messinger
O. J.
.
2008
.
Sampling bee communities (Hymenoptera: Apiformes) in a desert landscape: are pan traps sufficient?
J. Kans. Entomol. Soc
 .
81
:
288
300
.
Wilson
J. S.
Carril
O. M.
.
2016
.
The Bees in Your Backyard: A Guide to North America’s bees
 .
Princeton University Press
,
New Jersey, USA
.
Zayed
A.
2009
.
Bee genetics and conservation
.
Apidologie
 .
40
:
237
262
.

Author notes

Subject Editor: Phyllis Weintraub
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com