10 1111@een 12986

Ecological Entomology (2020), DOI: 10.1111/een.
12986
INVITED REVIEW
Nesting habitat of ground-nesting bees: a review

CÉ C I L E M . A N TO I N E and J E S S I C A R . K . F O R R E S T Department of Biology,
University of Ottawa, Ottawa, Ontario, Canada
Abstract. 1. About 3/4 of all wild bee species nest in the soil and spend much of their
life cycle underground. These insects require suitable environmental conditions for nest
construction and for the development and survival of their offspring. However, there
is little quantitative information on the nesting habitat requirements and preferences
of ground-nesting bees. Moreover, there are almost no data on the effects of nesting
conditions on these bees’ fitness.
2. Here, to better understand the factors that influence nest-site selection in
ground-nesting bees, we synthesise the literature on the nesting-habitat associations of
these important pollinators. We also review techniques that can be used to study the
nesting preferences of ground-nesting bees.
3. Our review reveals enormous variation among bee species in their associations
with such nesting-habitat attributes as soil texture, compaction, moisture, temperature,
ground surface features, and proximity to conspecifics or floral resources. However,
more studies–particularly experimental ones–are needed to segregate the influence
of each factor on bees’ choices of nesting location, since multiple factors are often
correlated. It is also unclear whether nesting-habitat associations vary geographically
or seasonally within species, or phylogenetically among ground-nesting bee species,
partly because we lack information on nesting habitat for many species.
4. We argue that studies using established habitat-selection methods are essential to
properly identify nesting-habitat preferences of ground-nesting species. Finally, more
research on nesting ecology is needed (especially in agroecosystems) to determine how
best to support this diverse group of bees and the vital ecosystem service they provide.
Key words. Ground-nesting bees, habitat requirements, Hymenoptera (Anthophila),
nesting behaviour, nest-site selection, soil characteristics.
Introduction nesting substrates. Yet many aspects of the nesting habitat

requirements of bees remain unknown, and this is particularly
Bees (Hymenoptera: Anthophila) are a diverse group of true for the ground-nesting species. Better understanding the
insects with more than 20,000 species described worldwide nesting characteristics of ground-nesting bees can help promote
(Michener, 2007). Although bees provide critical pollination their populations by allowing land-owners and managers to
services in both agricultural (Klein et al., 2007) and natural provide or maintain their preferred habitat.
ecosystems (Ollerton et al., 2011), they are threatened by a Many insects spend at least a portion of their lives underground
number of anthropogenic disturbances including habitat loss, (e.g. springtails; larvae or nymphs of root-feeding insects such as
reductions in floral resources, pesticide use, and spillover of cicadas, beetles, and flies; moth and beetle pupae) and may have
parasites and pathogens from managed bee species (Potts specific below-ground habitat requirements. A smaller number,
et al., 2016). While virtually all bees share a diet of floral including some earwigs, crickets, beetles, termites, wasps and
pollen and nectar, bee species exhibit differences in life-history bees, are true ground-nesters, in the sense that they excavate
traits and ecological characteristics, including their preferred and provide for their young in subterranean burrows (Gullan
& Cranston, 2010). Underground nesting is common among
Correspondence: Cécile M. Antoine, Department of Biology, Uni- bees: Cane and Neff (2011) reported that 64% of bee species
versity of Ottawa, 30 Marie Curie, Ottawa, Ontario K1N 6N5, Canada. construct nests beneath the soil surface; Harmon-Threatt (2020)
E-mail: cantoine@uottawa.ca calculates the number to be 83%. The below-ground-nesting
© 2020 The Royal Entomological Society 1

2 Cécile M. Antoine and Jessica R. K. Forrest
condition is believed to be ancestral in bees, as it is shared (Soucy, 2002; Richards et al., 2003). All eusocial species
with the crabronid wasps that are thought to be bees’ closest are characterised by overlapping generations and a permanent
relatives (Debevec et al., 2012; Sann et al., 2018). Females reproductive division of labour wherein a single female (the
of ground-nesting bees and wasps excavate tunnels leading to queen) produces worker offspring that build and defend the nest,
brood cells in which they lay eggs on top of a food reserve. forage for food, and care for the young. Highly eusocial bees,
Other bee species, and many wasps, do not dig underground such as honey bees (Apis spp.), are not ground-nesters and are
nests, and may be called cavity-nesters. This group includes not considered here; but many primitively eusocial and socially
species that excavate their own nests in wood, as well as those polymorphic bees belong to the family Halictidae, which is
(“renters”) that use pre-existing cavities–in wood, pithy stems, made up primarily of ground-nesters (Danforth et al., 2019).
stone walls or snail shells (reviewed by Cane et al., 2007; In these species, queens typically establish nests on their own
Danforth et al., 2019), or even below-ground, as in many bumble before producing workers. Solitary bees sometimes live in
bees (Bombus spp.; Apidae). Even though they sometimes nest communal nests sharing the same entrance but otherwise behave
in underground cavities, we do not consider bumble bees and independently as solitary females, producing offspring in their
honey bees to be ground-nesters for the purposes of this review: own brood cells (e.g. Andrena scotica Perkins, Andrenidae;
because they do not dig burrows, their criteria for nest-site Paxton et al., 1999). In temperate climates, queens of primitively
selection should differ from those of burrowing bees. Finally, eusocial species emerge from the ground at the beginning of
a minority of bee species are parasites of other ground-nesting the growing season and choose a nest location (which may be
bees (see Bee life history); however, we do not consider these the same nest in which they were reared, as in the halictid
species to be ground-nesters themselves. Lasioglossum versatum (Robertson), in which mated queens
Although the ground-nesting strategy is observed in every also overwinter in their natal nest; Michener, 1966). They then
bee family, in solitary and social species, and in every habitat initiate nest building, constructing and provisioning a few cells
in which bees occur, ground-nesting bees are proportionally until the first generation of workers takes over these tasks.
far less studied than cavity-nesters (Winfree, 2010). The latter Female workers continue digging galleries and creating new
can be observed using artificial nesting structures, but nests of brood chambers for another generation of workers, males, and
ground-nesters are typically difficult to locate, and there are few the next season’s queens (Packer et al., 2007).
easy methods for studying within-nest behaviour of these bees A minority of bee species are parasites (brood parasites and
(but see Leonard & Harmon-Threatt, 2019). Field and laboratory social parasites) that invade the nests of pollen-collecting bees;
studies of living ground-nesting bees are scarce relative to the many of these parasitic bees specialise on ground-nesting hosts
number of species in this group, and there is nesting information (Sick et al., 1994). Female brood parasites kill the host egg,
for only 26% of the 527 bee species that were studied in a recent or their larvae do so before eating the food resources in the
review (Harmon-Threatt, 2020). This leaves us with serious gaps brood cell. Social parasites usurp the nests of social bee species,
in our knowledge of the ecology and behaviour of these insects. causing the workers in the host nest to rear the larvae of
We begin with a brief overview of the biology of the parasite and sometimes killing the host queen (Danforth
ground-nesting bees. We then synthesise the existing infor- et al., 2019). Brood parasites, also known as cuckoo bees, spend
mation on the characteristics of ground-nesting bee nests and much of their time flying close to the ground, searching for host
the biotic and abiotic factors that influence where these bees nests. As they do not build their own nests but rather depend on
choose to nest. For some of these factors, there has been little their hosts, we do not consider these species as having nesting
research on ground-nesters, and we therefore refer to relevant preferences per se; however, these parasites could act as agents
studies on ground-nesting wasps and cavity-nesting bees. By of selection on host bee nest-site preferences (see Biotic factors).
identifying literature gaps and key research questions, and We also consider cuckoo bees as tools for locating nests of
also highlighting useful methodological tools, we hope to ground-nesting bees (see Methods).
encourage and direct new efforts to understand the ecology of
ground-nesting bees. Greater knowledge of bee nesting prefer-
ences is required if we are to determine which habitats and soil
Life cycle of ground-nesting bees
characteristics require protection or restoration to benefit bee
populations. Bees are holometabolous, and their life-stages vary in duration
depending on the species and its environment (e.g. temperature,
length of the flowering season). Some species or populations
Ground-nesting bee biology and life-history traits
are multivoltine, meaning they produce several generations per
Bee life history year (Michener, 2007; Danforth et al., 2019), while others have
just one, or take even more than a year to complete a generation
Bee life histories can be classified into three major types: (Forrest et al., 2019). For solitary ground-nesting bees, the activ-
solitary, social, and parasitic. More than 75% of described ity period starts with the emergence of adults from their under-
bee species are solitary, with females working alone to build ground nests followed by mating, and the active period may
their nest(s) and provide for their offspring (Michener, 2007). last only a few weeks. Among social species, the active season
However, there is a gradient of sociality, from solitary nesting to can last for months, as successive generations of adult work-
advanced eusociality, with the limits of each category not clearly ers are produced by the foundress. Females of all bee species
defined; furthermore, some species are socially polymorphic store sperm in their spermathecae, which allows them to spend
© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

Nesting habitat of ground-nesting bees 3
the rest of their life after mating building their nest, provision-
ing brood cells and laying eggs. Eggs hatch within a few days
(up to 6 days for Andrena vicina Smith, Andrenidae; Miliczky &
Osgood, 1995). The progeny then enter the larval stage, during
which they consume the food reserves provided by their mother
or their sisters (in social species). In temperate regions, many
solitary bee species overwinter in the prepupal stage, sometimes
within cocoons, before completing metamorphosis in the spring.
Other species complete metamorphosis before overwintering as
adults, again sometimes within their cocoons. Regardless of
their developmental stage, solitary ground-nesting bees, as well
as the foundresses of some social species, spend the winter in
a dormant state within the larval brood cell; thus, the mother’s
choice of nesting site determines her offspring’s overwintering
location. Immature bees can spend several months (sometimes
more than a year; Torchio, 1975; Danforth, 1999) of their lives
below-ground, where they are susceptible to environmental haz-
ards such as wildfires (reviewed by Cane and Neff 2011) and
flooding (Roubik & Michener, 1980; Fellendorf et al., 2004),
before emerging as adults that are active for only a few weeks.
Female ground-nesting bees do not care for their offspring
after provisioning and sealing brood cells. Consequently, the
main way they can maximise the success of their brood is
by providing high-quality food and a high-quality location
for larval development and survival. The latter may include a
nest site protected from adverse weather conditions, excessive
humidity, and other incidental risks such as predators and
parasites (Roulston & Goodell, 2011). On the other hand, the
more time a female spends searching for the ideal location Fig. 1. Variety of nest architecture seen in ground-nesting bees: (a)
and creating a nest, the less time she will have to provision One-celled nest with a plug as described by Roubik and Michener (1980)
and lay eggs in it or to construct additional nests. In other for Epicharis zonata. (b) Turret forming the nest entrance, and brood
words, energy and time invested in nest-site selection and nest cells piled in a chamber-like structure, as observed in halictid bees
such as Augochlorella striata, following Packer et al. (1989). (c) Nest
construction come with potential fitness costs–just as energy
composed of a main vertical gallery with lateral tunnels and brood cells
and time invested in long foraging bouts can trade off against directly connected to the main tunnels, with loops surrounding a few
lifetime offspring production (Zurbuchen et al., 2010a). This cells as observed in Halictus ligatus by Packer & Knerer (1986a) and
means that nest-site selection may play a key role in female bee described in other Halictidae by Eickwort & Sakagami (1979). (d) Nest
fitness (Brockmann, 1979). entrance forming a tumulus and leading to some brood cells connected
to the main tunnel by a short lateral tunnel, inspired by Mathewson
(1968) for Peponapis pruinosa and other examples from Sakagami
Nest construction & Michener (1962). Image created by Cécile Antoine and Philippe
Tremblay. [Colour figure can be viewed at wileyonlinelibrary.com].
Nest architecture varies widely among ground-nesting bee
species (Fig. 1). Typically, nests are composed of a main vertical
gallery with lateral tunnels leading to ovoid brood cells, with Ground-nesting female bees initiate nest excavation using
one offspring per cell. Depending on the species, lateral tunnels their mandibles and/or their forelegs and push out the soil
vary in length and in the angle at which they connect to using their hind legs and abdominal movements (Martins &
the vertical shaft. Most halictid bees have no lateral tunnels Antonini, 1994). Unlike cavity-nesting bees, ground-nesters
at all, their brood cells being directly connected to the main have specialised pygidial (on the 6th segment of the female
gallery (Sakagami & Michener, 1962). Nests can also contain abdomen) and basitibial plates. These plates allow the bee
chamber-like structures–larger than single brood cells–in which to dig, pack soil, and move easily within the nest (Danforth
several cells are clustered together (Packer et al., 1989). Others et al., 2019). Male ground-nesting bees do not participate in
contain loops that reconnect tunnels to the main gallery or nest construction, although males of some Perdita (Andrenidae)
sometimes dead ends (Rozen Jr., 1970; Wcislo et al., 1993; species may dig temporary shallow burrows in which to spend
Wuellner & Jang, 1996). The nests of most ground-nesting bee the night or periods of bad weather. Males occasionally enter a
species have not yet been described, but based on a worldwide female’s nest before nightfall, as in Perdita maculigera Cock-
review of 449 species by Cane and Neff (2011), cell depth can erell (Michener & Ordway, 1963), P. floridensis Timberlake
range from 1 to 530 cm, with an average minimum cell depth of (Norden et al., 2003) and Macrotera texana Cresson (as P. tex-
17 cm beneath the soil surface. ana; Neff & Danforth, 1991).

Solitary female bees typically construct and provision brood Simpson, 1992; Wcislo et al., 1993). The function of these tur-
cells one at a time, although some exceptions exist (Danforth rets is unclear, but they may prevent soil particles or water from
et al., 2019). Most species construct multiple cells per nest, falling into the open entrance; they could help females locate
and cell size is correlated with bee body size (Kamm, 1974). their nest or recognise it among others in an aggregation; or
There may be a single cell per lateral tunnel, or cells may be they could keep parasites and predators, such as ants, from enter-
clustered together, either arranged linearly as in some Colletes ing the nest. However, some species scatter the loose soil, per-
species (Michener, 2007; Almeida, 2008) or surrounded by a haps to make the nest less conspicuous, and others plug the nest
cavity as in some Halictidae (Sakagami & Michener, 1962; Eick- entrance with the excavated soil after nest completion (Martins
wort & Sakagami, 1979). When excavating the cell, the digging et al., 1996; Wuellner & Jang, 1996). Some bees also plug the
bee usually uses her pygidial plate to smooth the walls and nest entrance temporarily after a provisioning trip (while inside),
apply a shiny waterproof film. Even though not all bees line presumably to avoid predator invasion (Wuellner & Jang, 1996).
their brood cells (e.g. some Perdita spp. construct unlined brood These different behaviours may be species-specific or may be
cells; Danforth, 1989), most ground-nesting bees use glandular adaptations to local environmental conditions.
secretions that they brush on the cell walls (Batra, 1964; Dan-
forth, 1991). This lining is a secretion product of the Dufour’s
gland, located at the base of the sting in female bees, and it forms Nest-site selection: Which characteristics matter?
a transparent, waxy coating around the brood cell (Cane, 1981).
Although soil may seem an unlimited resource, female bees
Bees of the family Colletidae, which includes ground-nesting
likely select specific soil features that limit their nesting habi-
species, produce a unique cellophane-like membrane, also from
tat to a subset of the species’ range. Here, we discuss envi-
Dufour’s gland secretions, which is insoluble by many solvents
ronmental variables that may influence nest-site selection and
(Almeida, 2008). Regardless of its specific chemical make-up,
provide examples (see Table 1 and Supplementary Table S1).
the brood-cell lining probably helps protect the brood from
Differences among species in environmental tolerances, preda-
microbial infestation and from water infiltration. After ovipo-
tion pressures, and/or host-plant associations may explain why
sition, the mother bee plugs the cell and begins to create a new
there is such interspecific variation in preferred environmental
one. Some species, though, such as Perdita maculigera (Mich-
conditions for nesting.
ener & Ordway, 1963), Fidelia villosa Brauns (Megachilidae;
Rozen Jr., 1970), and Diadasina distincta (Holmberg) (Apidae;
Martins & Antonini, 1994), create one-celled nests; individu- Abiotic factors
als must therefore dig multiple independent nests. Michener &
Ordway (1963) suggested that this behaviour might occur only Soil texture. Soil texture is thought to be a key factor influenc-
in species whose nests are easily excavated (shallow or in soft ing where ground-nesting insects choose to nest. A soil’s texture
substrates), requiring minimal investment of time and energy is defined by its particle size distribution–that is, the relative
per nest; but the one- or two-celled nests of some Ptilothrix amounts of sand, silt, and clay (in order of decreasing parti-
species are constructed in hard-packed soil (Rust, 1980; Mar- cle size). Particle size distribution affects soil hardness, which
tins et al., 1996). It therefore seems likely that construction of likely influences bee nesting-site preferences (see next section).
single-celled nests is a strategy to minimise chances of acciden- Sand particles in particular are abrasive and could cause wear
tal nest destruction or parasite invasion killing all of an individ- to the mandibles and wings. Nevertheless, most ground-nesting
ual’s progeny. bee nests have been described as occurring in sandy or sandy
Brood-inspection behaviour has been observed in some social loam soils, and it has therefore been inferred that they prefer
ground-nesting bees (e.g. Lasioglossum versatum; Batra, 1968), these soil textures (Cane, 1991).
in which females open the completed brood cell to check on the An important early investigation of the textural prefer-
egg or larva. If the outcome of the inspection is satisfactory, ences of ground-nesting Hymenoptera was conducted by
they immediately reseal the cell. If not, they fill the cell with Brockmann (1979), who studied the digger wasp Sphex ich-
soil and plug it as if burying the larva, perhaps an adaptation to neumoneus (L.). She observed that wasps initiated nests in
prevent movement of pathogens or parasites to other brood cells. soils with high sand content (50–88%) and smaller amounts
Lasioglossum versatum also closes brood cells from which adult of silt and clay; they did not nest in nearby areas with finer
bees have emerged, perhaps because they contain faecal matter. soil texture (i.e. less sand). She concluded that wasps were
Excess soil can be used to reinforce the nest’s structure, but it generally choosing the sandiest soil available, which would
is usually brought to the surface, creating a “tumulus” (mound provide better drainage, while still containing enough clay
of soil) marking the entrance of freshly dug nests (Sakagami & to support their large (1 cm diameter) burrows. Soil texture
Michener, 1962). Multiple bee species build turrets, or “chim- analysis in aggregations of Halictus rubicundus (Christ) (Hal-
neys”, at their nest entrances. Typically, turrets rise vertically ictidae) revealed a sand fraction between 35 and 100%, with
from the nest entrance, although they are sometimes curved a combined silt–clay fraction of less than 5%, the rest being
or horizontal, as in Anthophora sp. (Batra & Norden, 1996), gravel (Potts & Willmer, 1997). This study found no association
Diadasina distincta (Martins & Antonini, 1994) and Halic- between sand or silt–clay fractions and nest density, but more
tus confusus Smith (Sakagami & Michener, 1962). The turrets nests were found in more gravelly soils. In a broad survey
have consolidated and cemented inner walls, constructed from across the U.S.A., Cane (1991) measured sand percentages of
soil mixed with glandular secretions (Ordway, 1984; Neff & 34–94% at the nest locations of 32 species of ground-nesting

Table 1. A non-exhaustive list of studies that have investigated the soil variables associated with ground-nesting (GN) bee nests, in reverse chronological order.
Soil predictors
Study Species Response variable(s) Compaction* Ground cover† Texture Temp. Slope Other: Method(s) Region
Maher et al., 2019 Andrena cineraria × × Shade Descriptive Ireland

Andrena fulva Citizen science United Kingdom
Halictus rubicundus
Colletes hederae
Olliff-Yang & Mesler, 2018 Habropoda miserabilis Phenology × Moisture Correlational California, USA
Pane & Community of GN bees Nest presence × Moisture Correlational Illinois, USA
Harmon-Threatt, 2017 (18 species) Emergence traps
Fortel et al., 2016 Community of GN bees Abundance × Manipulative France
(37 species) Diversity Artificial habitat
Richness
Sardiñas et al., 2016 Community of GN bees (10 Abundance × × × × Irregularities‡ Correlational California, USA
species) Nest presence Emergence traps
Halictus sp. Richness
Lasioglossum sp.
López-Uribe et al., 2015 Colletes inaequalis Nest presence × × × Correlational New York, USA
Spatial modelling
Cane, 2015 Halictus rubicundus Nest number × Stones (pebbles) Manipulative Utah, USA
Sardiñas & Kremen, 2014 Community of GN bees (54 Abundance × × × Irregularities Correlational California, USA
species) Emergence traps
Vinchesi et al., 2013 Nomia melanderi Phenology × Manipulative Washington, USA
Xie et al. 2013 Andrena camellia Nest number × × × × Moisture Correlational China
Polidori et al., 2010 Lasioglossum malachurum × × × × Stones Descriptive Italy
pH
Grundel et al., 2010 All bees (170 species) Abundance × × Organic matter Correlational Indiana, USA
Richness Shade
Community
composition

Kim et al., 2006 Halictus tripartitus Nest number × × Correlational California, USA
Halictus ligatus Emergence traps
Lasioglossum (Dialictus)
6 species of GN bees
Potts et al. 2003, 2005 All bees (116 species in 1999 Abundance × × × Irregularities Correlational Israel
and 170 over 1999–2000) Richness
Wuellner, 1999 Dieunomia triangulifera Nest number × × × Sun exposure Correlational Kansas, USA
Moisture
Irregularities
Potts & Willmer, 1997 Halictus rubicundus Nest number × × × × Moisture Correlational United Kingdom
Stones
Cane, 1991 32 species of GN bees × × Moisture Descriptive USA
Note: Only studies that present quantitative data on soil variables (excluding soil disturbances such as tillage and fire) are included; see Supplementary Table S1 for a more comprehensive list. In ‘Methods’, ‘manipulative’ studies
are those that experimentally modified one or more soil variables. Observational studies are listed as ‘correlative’ when the authors tested for an association between the response variable and one or more soil variables; ‘descriptive’
studies simply documented the values of one or more soil variables near nests (and therefore do not involve a response variable). We also note under ‘Methods’ any distinctive techniques that were used in the study (see Methods).
Temp. = temperature; Abundance = abundance of adult GN bees; Richness = species richness of GN bees.
∗ Also called soil hardness.
† Includes categories such as vegetation cover, bare ground, litter, etc.
Nesting habitat of ground-nesting bees
‡ For example, cracks in the soil and small cavities.

5
bees, with maximum sand content observed near nests of On the other hand, burrows in softer soils may be more prone
the genera Hesperapis (Melittidae) and Colletes (Colletidae). to collapse or excavation by vertebrate predators. The greater
Larger bees tended to nest in more clay-rich soils (Cane, 1991). structural integrity of burrows built in more compact soil may be
In another study, Colletes inaequalis Say were found to nest particularly important for bees that nest in aggregations. As the
in soils with a mean sand content of 64% and never less than distance between neighbouring nests decreases, the advantage of
30% (López-Uribe et al., 2015). Another colletid, Caupolicana easy excavation may be outweighed by the disadvantage of pos-
yarrowi (Cresson), has been observed nesting in 45–55% sand sible nest collapse. Potts and Willmer (1997) reasoned that this
(Rozen et al., 2019). Unfortunately, none of the latter three phenomenon must account for the greater densities of H. rubi-
studies compared soil texture between nesting sites and nearby cundus nests at sites with greater soil compaction. In contrast,
areas without nests, making it difficult to be sure that the Polidori et al. (2010) observed no association between aggre-
characteristics of the nesting locations reflect bees’ preferences. gation size and soil hardness in Lasioglossum malachurum,
Although they do not demonstrate that ground-nesting bees although it should be noted that all five aggregations they studied
prefer sand, the studies above do show that these bees’ nests were in hard-packed soils. Several gregarious species, including
are often associated with sandy soils. However, there is also Macrotera opuntiae (Cockerell), Colletes kincaidii Cockerell,
plenty of variation, with Lasioglossum malachurum (Kirby) and Anthophora pueblo Orr, have even been reported to exca-
nests recorded in soils containing only 10–41% sand (Polidori vate nests in sandstone despite the presumed energetic costs and
et al., 2010), and several Anthophora species (A. abrupta Say, mandible wear (Bennett & Breed, 1985; Torchio et al., 1988; Orr
A. bomboides Kirby and A. walshii Cresson) nesting in soil et al., 2016). As with other soil characteristics, soil-compaction
with 20–30% clay content (Cane, 1991). Anthophora abrupta preferences seem to be species-specific. For example, consider
can even nest in bags of clay (Graham et al., 2015) and clay three common halictid taxa studied by Kim et al. (2006): Halic-
walls (Norden, 1984). Alkali bees (Nomia melanderi Cockerell), tus tripartitus Cockerell nested in hard soils, whereas H. ligatus
which are sometimes managed for alfalfa pollination, are known Say was found in highest densities at medium soil hardness, and
for nesting in clay soils with a pH > 8 and a high moisture level there was no association between soil hardness and nest density
(Cane, 2003, 2008; Vinchesi et al., 2013). Fortel et al. (2016) in Lasioglossum (Dialictus) sp.
found no influence of soil texture on species richness or
abundance of ground-nesting bees in experimental plots set up
for this purpose; however, this result could mask interspecific Soil moisture. With their broad geographical distribution,
differences, since species likely differ in their soil-texture bees have been found nesting in situations that vary enormously
preferences (Leonard & Harmon-Threatt, 2019). Seemingly in soil moisture. Cane (1991) measured in situ water content
contradictory results could also be due to the use of different in 32 bee species’ nests across the U.S.A. and found that
methods for soil textural analysis, from sieving and weighing soil moisture ranged from 2.7 to 37.8%. Other studies have
different soil fractions, to particle size analysis either with a reported nests in wetter soil (Packer & Knerer, 1986a), with
hydrometer (Bouyoucos method) or a pipette (U.S. Department Potts & Willmer (1997) reporting a mean soil moisture of
of Agriculture, Bureau of Plant Industry, Soils, 1951). 80%. Still others have documented nests that are temporarily
submerged (Roubik & Michener, 1980; Visscher et al., 1994;
Norden et al., 2003) or even permanently waterlogged (Pietsch
Soil compaction. Soil compaction, or hardness, is a mea- et al., 2016). The ability to nest in flooded sites may help bees
sure of compressive strength at the soil surface that can be avoid competition for nest sites, or the cover of water may help
taken using a penetrometer. Soils can be classified as soft protect nests from attack by parasites or predators.
(<1.5 kgf cm−2 = <147 kPa), medium (1.6–3.0 kgf cm−2 ) or A common feature of the nests of ground-nesting bees is a
hard (>3.1 kgf cm−2 ) (Kim et al., 2006). More compact soils waterproof brood-cell lining secreted by the Dufour’s gland of
have fewer pores and higher density, making them more diffi- the mother bee (May, 1972; Cane, 1981; Visscher et al., 1994).
cult to excavate and impeding water percolation. Compaction This waterproof lining may function to retain soil moisture
is often the result of the passage of animals, vehicles, or within the cell, but its primary function is probably to exclude
machines such as the compressive rollers used in agricultural excess water (May, 1972; Roubik & Michener, 1980). Even
environments. when submerged in water for up to 24 hours, brood cells
In theory, soil compaction should be an important factor of Diadasina distincta and Ptilothrix plumata Smith experi-
affecting nest-site selection, as nest excavation appears to repre- enced no water infiltration (Martins & Antonini, 1994; Martins
sent a major investment of time and energy for a ground-nesting et al., 1996), showing that the cells are completely waterproofed
bee. All else being equal, females should prefer softer substrates and can withstand heavy rains or flooding.
to limit these costs. Indeed, although Potts and Willmer (1997) There are costs and benefits to nesting in damp soils. Soil
observed Halictus rubicundus nesting in soils ranging in moisture is crucial for larval development because larvae take
hardness from 0.6 to 5.5 kgf cm−2 , they found greater nest up water as a component of weight gain (May, 1972), particu-
densities in softer soils at the site they studied in most detail. larly during the later larval stages. This water is likely to come
The bees avoided nesting in hard-packed substrate, as did the from moisture within the brood cell, as relative humidity inside
digger wasp Sphex ichneumoneus (Brockmann, 1979). Sardiñas the nest can approach 100% (Potts & Willmer, 1997). How-
& Kremen (2014) also found fewer ground-nesting bees in ever, moisture can also cause mould to develop inside the cells,
emergence traps placed over harder soils. degrading the food supply and jeopardising offspring survival,

as observed in Diadasia opuntiae Cockerell (Ordway, 1984). (Larsson, 1991), timing of adult emergence, rates of larval devel-
Nesting populations of alkali bees (Nomia melanderi), which opment (Forrest, 2017), and number of generations produced
prefer soils with high moisture content, are sometimes main- per year (Forrest et al., 2019). Temperature at the nest entrance
tained by sub-irrigation and application of NaCl (in part to pre- can influence when a bee can begin foraging in the morning,
vent loss of soil moisture) to the nesting beds (Cane, 2008). while below-ground temperatures may affect whether larvae can
However, Stephen (1965) showed that high soil moisture in arti- complete development before the end of the growing season.
ficial N. melanderi beds led to the development of fungi that Although adult bees are partially endothermic and can elevate
killed overwintering bees. Flooding of the nesting area during their body temperature using thoracic flight muscles (Stone &
diapause can also delay emergence, as shown in male Calliopsis Willmer, 1989), female ground-nesters cannot control the tem-
pugionis Cockerell (Visscher et al., 1994). Even more dramati- perature within the nest, nor can bee larvae thermoregulate. In
cally, Andrena vaga Panzer offspring died during a prolonged addition, the metabolic costs of raising body temperature to the
inundation, leading to a local population decline (Fellendorf level required for activity are greater when ambient temperatures
et al., 2004). are lower (Willmer & Stone, 2004). As such, we expect temper-
Other adaptations to avoid excess water include the excavation ature to strongly influence nest-site quality for ground-nesting
of a cavity around the cell cluster to increase the rate of soil bees.
water evaporation around the brood cells, as in the halictids Female ground-nesting bees spend the night in their nests
Halictus ligatus and Augochlorella striata (Provancher) (Packer and forage when ambient temperature is warm, but below
& Knerer, 1986a; Packer et al., 1989). In swampy habitats, their maximum thermal tolerance (Westrich, 1996). Despite
Epicharis zonata Smith (Apidae) build a double cell plug inside their thermoregulatory abilities, bees rely on warm air and/or
the nest (Roubik & Michener, 1980), presumably for the same solar radiation to warm up. For example, Stone (1994) found
purpose. Most species of Perdita do not have a brood-cell that Anthophora plumipes (Pallas) females with warmer nest
lining, but Norden et al. (2003) reported that Perdita floridensis entrance tunnels began foraging more than 3 h earlier in the day
prepupae secrete a water-repellent coating on their cuticle that than conspecifics nesting in cooler microhabitats. Anthophora
presumably protects them from drowning and sand abrasion. abrupta females appear to use the turrets protruding from their
While bees in moist habitats often exhibit traits that appear nest entrances to warm up on cool mornings, because these heat
to minimize water infiltration and damage, ground-nesting bees up more quickly in the sun than do the nest interiors; individuals
in drier habitats may preferentially select sites with higher whose nests lacked turrets required up to an hour longer to
soil moisture. For example, female Dieunomia triangulifera begin foraging (Norden, 1984). While flight is particularly
(Vachal) in the U.S. Great Plains only began nest construction temperature-dependent, even nest construction can be slowed
when soil was moist enough for excavation (Wuellner, 1999), by cool temperatures. Weissel et al. (2006) showed that cooler
postponing nest establishment in drier years until rains softened below-ground temperatures (at 20 and 40 cm) were associated
the soil (Minckley et al., 1994). Some species, especially with slower nest founding and construction in the eusocial
Anthophora spp., bring water from outside the nest (sometimes bee Lasioglossum malachurum. Because of the limited season
mixed with nectar) to moisten the soil while digging, as in available to most bees for building and provisioning their nests,
Anthophora abrupta and A. villosula (Pallas) (as A. pilipes; getting an earlier start may translate into more total reproductive
Batra & Norden, 1996). This behaviour might be related to output.
nest architecture: anthophorine bees sometimes nest in soil In addition to affecting adult activity, temperature also influ-
that is rich in clay and may need added moisture to construct ences bee development. Warmer temperatures during each larval
the turrets that often mark their nest entrances. Similarly, the stage can increase developmental rate and survival (Jeanne &
desert bee Caupolicana yarrowi uses regurgitated nectar to Morgan, 1992; Whitfield & Richards, 1992), at least as long
soften the soil and smooth the interior surface of nest cells and as they remain below species- and stage-specific critical ther-
walls–a behaviour that is probably an adaptation to the dry and mal maxima. For example, prepupal development of Nomia
hard-packed soil (Rozen et al., 2019). melanderi is fastest at 29 ∘ C and inhibited below 17 ∘ C and
Allowing for variation in local environment and above 35 ∘ C (Stephen, 1965; Vinchesi et al., 2013). Conse-
species-specific moisture preferences, most ground-nesting quently, temperature can also affect voltinism (the number of
bee species are probably searching for a soil patch that is well generations in a year). In the cavity-nesting bee Osmia iridis
drained but not too dry (Potts & Willmer, 1997). However, Cockerell and Titus, temperatures experienced early in larval
whether female bees select nest locations based on soil moisture development influence whether a bee adopts a 1- or a 2-year life
or on soil texture (see above) is often unclear, because soil cycle (Forrest et al., 2019). Variation in voltinism also occurs
texture is a major determinant of water content: clay soils among ground-nesting species (e.g. Diadasia rinconis Cockerell
retain water, while sandy soils do not. Thus, distinguishing the and D. afflicta (Cresson) are both partially bivoltine), but it is
influence of these two variables on bee nest-site selection may so far unclear whether temperature controls this variation (Neff
require manipulative experimentation. et al., 1982; Neff & Simpson, 1992). In multivoltine species
such as Lasioglossum malachurum, warmer below-ground tem-
peratures decrease the duration of the intervals between genera-
Temperature. As with all ectotherms, temperature influences tions, which correspond to periods of larval development. When
many aspects of the lives of bees, including activity rates (Bor- below-ground temperature is 2 ∘ C warmer, more colonies pro-
rell & Medeiros, 2004; Woods et al., 2005), mating behaviour duce three broods instead of two (although the effect is small,

explaining less than 2% of the variance) (Weissel et al., 2006). In other regions (e.g. hot deserts), female ground-nesting
While we normally expect faster development and shorter gener- bees could adopt the opposite strategy to avoid overheating
ations to translate into higher rates of population increase, high the young and might therefore dig deeper burrows or select
temperatures can also be associated with smaller adult body size poleward-facing slopes to find cooler underground environ-
and higher rates of mortality in ectotherms, such that the fit- ments. Bees might assess surface temperature directly to deter-
ness consequences of nesting in warm microenvironments can mine where to nest, or they might use other cues, such as aspect
be complex (Kingsolver & Huey, 2008; Forrest, 2017). or solar irradiation, that correlate with nest temperatures (see
Temperatures near the soil surface vary over the course of Soil surface features). In practice, it may be difficult to dis-
a day (Xu et al., 2002), and they can also vary by several tinguish preferences for temperature per se from preferences
degrees over small (<50 m) spatial scales owing to variation for other factors that are correlated with temperature; however,
in shading, vegetative cover, surface reflectance (albedo), and given the potentially major fitness consequences of nest temper-
topography (Redding et al., 2003; Mikola et al., 2018; Davis atures, it seems likely that temperature would be an important
et al., 2019). For example, in some termite and ant species, ultimate driver of nest-site selection, even if it is not the proxi-
nest temperatures can be influenced by nest orientation, which mate driver.
affects the amount of solar radiation reaching the nest entrance
and therefore the amount of solar heat absorbed by the nest
(reviewed by Jones & Oldroyd, 2006). Ground-nesting bees Soil surface features. Other variables, such as cracks in the
may respond to this variation in soil-surface temperature and soil, stones, slope, and vegetation cover, have been reported to
choose to nest in locations that experience higher or lower daily influence where bees nest, with specific associations depending
maxima, or that experience desirable temperatures at particular on the study and the species. The North American bee Calliop-
times of day, such as the early morning. Indeed, Sakagami sis pugionis sometimes nests within cracks in dry flood-plains
& Hayashida (1961) demonstrated that nests of Lasioglossum (Visscher & Danforth, 1993), as does the Australian bee Leio-
duplex (Dalla Torre) (as Halictus duplex) in the Hokkaido proctus muelleri Houston and Maynard (Colletidae; Houston &
University Botanical Garden, Japan, were preferentially located Maynard, 2012). Potts and Willmer (1997) observed a strong
in areas that received morning sunlight–even if these locations preference for stones among Halictus rubicundus, with 57% of
were similar to less favoured locations in terms of total duration the bees at one study site initiating a nest near or under stones.
of insolation. Other halictid bees (Augochlorella striata, Lasioglossum (Evy-
Below-ground temperatures are generally correlated with, but laeus) cinctipes (Provancher) and L. comagenense (Knerer and
much less variable than, surface temperatures, with the strength Atwood)) also locate their nest entrances near surface stones
of the correlation decreasing with increasing depth (West, 1952; (Packer et al., 1989). Halictus ligatus nests often occur near
Xu et al., 1997; Rajver et al., 2006). Heat penetration into the rocks and pebbles (Packer & Knerer, 1986b), and indeed a pref-
soil (i.e. the thermal diffusivity of the soil) increases with soil erence was demonstrated experimentally by Cane (2015), who
water content and decreases with increasing soil bulk density added pebbles in a nesting area of this species: females con-
(Marshall et al., 1996), such that below-ground temperatures sistently preferred to nest near stream pebbles instead of bare
in drier, more compacted soils are less correlated with surface ground. However, Sardiñas & Kremen (2014) found that cav-
temperature than those in moister but better-aerated soils. ities and cracks in the soil predicted nest occurrence for one
Regardless, because temperatures below a certain depth (on the species of Lasioglossum (Dialictus) but not for all Lasioglos-
order of 20 cm) are not predictable from surface temperatures sum species, so this preference might again be species-specific
(see Rajver et al., 2006), below-ground temperature is unlikely or context-dependent.
to influence the choice of nesting location for bees that construct It is often assumed that female bees prefer open bare ground
brood cells much below this depth. However, for bees that to vegetative cover to initiate nests, as has been shown for
nest closer to the surface, near-surface temperatures should be Dieunomia triangulifera (Wuellner, 1999), because bee nests are
good indicators of the temperatures that would be experienced often found in sparsely vegetated areas. However, this might
by brood and may be used in site selection for this reason. reflect the difficulty of finding nests among vegetation rather
Indeed, Potts and Willmer (1997) found that the areas with the than bee preferences. Some species, such as H. ligatus (Packer
highest densities of Halictus rubicundus nests in their Scottish & Knerer, 1986a), have actually been observed nesting under
study sites were significantly warmer at 5 cm belowground (the vegetation. Lasioglossum rohweri (Ellis) nested in aggregations
mean depth of the brood cells of this species), compared to in sparsely vegetated areas, but not in bare ground, in dense
the ambient air temperature, than nearby areas without nests. vegetation, or under dead plant material (Breed, 1975).
Temperatures at 5 cm depth were strongly correlated with soil There could be multiple reasons for choosing to nest in cracks
surface temperatures, meaning that females’ assessments of or near stones, pebbles, or vegetation. First, these features
surface temperatures could inform them about the likely thermal could act as visual cues, helping the bee to locate her nest
quality of nests constructed at different locations. when returning from a foraging trip (but see Wuellner, 1999).
Overall, we expect bees that construct shallow below-ground Indeed, ground-nesting bees learn and evaluate distance to visual
nests in temperate regions to choose sites with maximum sun- landmarks to locate their nests (Brünnert et al., 1994). Second,
light exposure, facing towards the equator or eastward if the pebbles and stones help regulate underground temperature by
ground is on a slope, to maximize heat at the nest entrance in heating the soil and the nest entrance located next to it, as stones
the morning and in the brood cells during larval development. can absorb solar radiation and retain heat (Packer et al., 1989;

Potts & Willmer, 1997; Cane, 2015). Stones, pebbles, and However, we know of no evidence so far that natural enemies
vegetation can also help soil to retain moisture, which can be have influenced bee preferences for specific below-ground soil
advantageous in dry environments (see Soil moisture), and they features such as texture or moisture.
could also help maintain nest structural integrity. In particular,
dead vegetation or leaf litter may prevent desiccation of the
soil surface and help regulate soil temperature. Finally, these Presence of conspecifics. Many ground-nesting bees choose
features could serve to conceal nest entrances from predators and to nest near conspecifics, for reasons that are not always clear.
parasites (Potts & Willmer, 1997; Wuellner, 1999). Conversely, Gregarious behaviour occurs among solitary, communal and
Wuellner (1999) suggested that D. triangulifera might select social ground-nesters and leads to the aggregation of conspecific
unvegetated areas for their nests because parasitic conopid flies nests in the same area. In these aggregations, nest density can
use the tips of plant leaves or stems as perches from which vary from a dozen to more than 300/m2 in Halictus rubicundus
to observe their bee hosts. Alternatively, bare ground may be (Potts & Willmer, 1997) to 1650/m2 in some aggregations of
preferred because roots impede nest excavation, and might Calliopsis pugionis (Visscher & Danforth, 1993). Aggregations
destroy completed cells or because vegetation makes it difficult can persist for many bee generations (Neff, 2003) and as
for bees to find their nest entrances (Wuellner, 1999). long as 50 years (Cane, 2008). Large nesting aggregations
Finally, slope is another factor that is likely important in can be conspicuous; but even so, nesting in an aggregation
may be a form of defence against parasites (reviewed by
nest-site selection. Many ground-nesting bees nest in embank-
Rosenheim, 1990). The presence of large numbers of active
ments close to rivers or roads, which can be steep or even
bees entering or exiting their nests can prevent parasites from
vertical. For example, Anthophora abrupta has been reported
approaching undetected, and the activity may even distract or
nesting in a clay wall (Norden, 1984) and Neocorynura fumipen-
frighten some prospective predators. In rare cases, members of
nis Friese (Halictidae) in the vertical banks of a ditch (Michener
an aggregation may collectively attack intruders (Thorp, 1969).
et al., 1966). Maher et al. (2019) compared the slope–as well as
On the other hand, areas of high nest density can also attract
vegetation and shade–of 236 nesting sites belonging to four dif-
parasites and therefore suffer disproportionately from parasite
ferent species and recorded by citizen scientists, and many nests
attack (e.g. Polidori et al., 2005). In these cases, any adaptive
of Colletes hederae Schmidt and Westrich (a greater proportion
value of nesting in aggregations seems unrelated to defence.
than in the other three species) were located on sloping ground.
Regardless of their adaptive value, aggregations can form
However, there was no evidence that these bees preferred slop-
through three possible processes (reviewed by Cane, 1997):
ing substrates, and their nests were found equally often on flat
First, bees may nest in aggregations simply because conspecifics
ground. Slopes could be favoured in some cases because they
have similar preferences and many individuals therefore (inde-
facilitate water drainage, and, when the area is exposed to the
pendently) select the same place. Second, aggregations may
sun and south-facing, because they enable nests to be warmer
arise because of natal philopatry (i.e. bees returning to nest at
(see Temperature). However, it is difficult to conclude from
the site from which they emerged) combined with population
observations alone whether ground-nesting bees are selecting
growth (Crozier et al., 1987; Yanega, 1990); or, third, because
nest sites based on slope, solar radiation, or temperature, all of
bees are attracted by the presence of conspecifics. In the latter
which can be confounded. To segregate the influence of each of
two mechanisms, bees are choosing to nest at a location that
these factors, experimental studies are required.
has been deemed (or even proven) suitable by others, presum-
ably because copying the choices of other individuals is less
risky, or requires less investment of time or energy, than iden-
Biotic factors tifying a suitable site independently. There is in fact abundant
evidence, discussed in detail by Michener (1974), that bees are
Natural enemies. Biotic factors could have a strong influence
attracted by conspecifics. The specific cues responsible for this
on where bees nest, potentially acting both as proximate indica-
attraction are generally unknown, although odour or visual sig-
tors of nest-site suitability and as ultimate drivers of habitat pref- nals are suspected (e.g. Roubik & Michener, 1980). One of the
erences. In particular, natural enemies (pathogens, parasites and few experimental tests (Wuellner, 1999) found no evidence that
predators) are thought to have played a major role in shaping the the ground-nesting bee Dieunomia triangulifera was attracted to
nesting habits of bees (Wcislo & Cane, 1996). Numerous natural conspecific tumuli (here created “by hand” from soil taken from
enemies attack bees at their nests, including parasitic wasps and actual nest tumuli).
cleptoparasitic bees; bombyliid flies; clerid and meloid beetles;
ants; and even insectivorous mammals (Danforth et al., 2019;
Minckley & Danforth, 2019). Bee brood cells and larvae can Floral and nesting resources. As central-place foragers, bees
also suffer infection by fungal and other microbial pathogens require food and nesting resources within flying range of their
(Gerdin & Cane, 1983; Antonini et al., 2003). All of these can nests (Westrich, 1996). Pollen and nectar are the primary food
impose significant mortality on ground-nesting bees (Gerdin & resources for ground-nesting bees, although some species also
Cane, 1983; Wcislo, 1996; Minckley & Danforth, 2019), and, collect floral oils and resins (Michener, 2007), while nesting
as such, have likely been major agents of selection on nesting resources can include abiotic elements (water, mud), resin (used
behaviour (e.g. Batra & Bohart, 1969). As noted above, para- as a cell-lining in Trachusa spp.; Cane, 1981, 1996) or leaves
sites or predators may be responsible for the tendency of some (Requier & Leonhardt, 2020). Female bees must complete sev-
bees to nest in cryptic locations (e.g. Potts & Willmer, 1997). eral foraging bouts to provision a single brood cell, and the

flight distance within which those bouts are conducted is con- nesters. Assembling a list of species within a community per-
strained by environmental factors (e.g. landscape configura- mits studies of bee responses to their environment (includ-
tion) and by the bee’s physiological capabilities. Flight dis- ing disturbances) based on their functional traits, of which
tances are generally correlated with body size in bees (Gathmann nesting location is one (Williams et al., 2010). For example,
et al., 1994; Gathmann & Tscharntke, 2002), with larger bees several studies have examined the effects of different anthro-
able to fly disproportionately further than smaller ones (Green- pogenic and environmental factors (agricultural management
leaf et al., 2007). Small bees (smaller than 1 cm long) typically (Martins et al., 2018), agricultural intensification (Williams
do not forage beyond 100–300 m from their nest (Zurbuchen et al., 2010; Renauld et al., 2016; Carrié et al., 2018), fire
et al., 2010b). Ground-nesting bees, many of which are small (Burkle et al., 2019; Galbraith et al., 2019), habitat management
(as little as 2 mm long in some Perdita Andrenidae), therefore (Buckles & Harmon-Threatt, 2019), etc.) on ground-nesting bee
need adequate soil substrate close to floral resources, and, all abundance and diversity.
else being equal, should prefer to nest near flowers. Furthermore, To sample a broad array of bee species, the use of multi-
many solitary bees are dietary specialists that collect pollen only ple techniques is recommended (Sardiñas & Kremen, 2014).
from certain plant taxa; these bees require appropriate nesting Active sampling methods consist of visual observation followed
habitat within flight distance of their specific floral host-plants. by active pursuit of the bee, and collection with a net or aspi-
It is certainly the case that dietary specialists (oligoleges) nest rator (“pooter”). Passive trapping involves installing pan traps
near their host plants: squash bee (Peponapis pruinosa (Say), (Kearns & Inouye, 1993), pitfall traps, window traps (Gullan
Apidae) nests occur in squash (Cucurbita spp.) fields (Julier & Cranston, 2010), vane traps or malaise traps (Darling &
& Roulston, 2009; Skidmore et al., 2019); Nomia melanderi Packer, 1988) in a site and returning later to collect the cap-
nest near alfalfa (Medicago sativa (Linnaeus)) (Cane, 1997, tured insects. Unfortunately, these techniques are not specific
2008; Vinchesi et al., 2013); and Dieunomia triangulifera to ground-nesting bees, and because they capture bees mov-
nest near sunflowers (Helianthus annuus (Linnaeus)) (Minckley ing towards or between food patches, mates, or nesting sites,
et al., 1994). Oddly, however, it is not known whether bees it is impossible to know if the nests of the captured bees are
actually use the presence or abundance of host-plant flowers nearby. However, given the limited foraging ranges of most
or foliage when choosing where to nest: they may simply ground-nesting bees, most sampled bees’ nests are presumably
be found alongside their host-plants because of philopatry, or within a few hundred metres of the sampling location (see Floral
because they share substrate preferences with their host-plants. and nesting resources).
Experiments (such as those of Wuellner, 1999, and Julier & At a smaller scale, assemblages of ground-nesting bees can be
Roulston, 2009, or those suggested by Cane, 1997) are still sampled in a more targeted fashion using tent-like emergence
needed to determine which factors are used by ground-nesting traps. These structures have an open bottom and an aperture
bees as proximate cues for where to nest, as opposed to those at the top leading to an insect killing jar, and they can be
that are simply correlated with nest presence. placed haphazardly on the ground to opportunistically collect
any bees emerging from a previous year’s nest, or, if placed
overnight, to capture nesting females as they exit their nests in
Methods for studying the nesting habitat the morning. Emergence traps are useful to examine the effects
of ground-nesting bees of substrate characteristics on the abundance and richness of
ground-nesting bees (e.g. Sardiñas & Kremen, 2014). However,
A variety of techniques can be used to study the nesting
their efficiency is questionable, compared to other trapping
behaviour and habitat of ground-nesting bees, depending on
methods (Cope et al., 2019), because they cover only a small
the researcher’s objectives. Documenting habitat associations
area of the ground, and the tents are expensive; furthermore,
and responses to environmental perturbations can be done by
their effectiveness in catching actively nesting bees decreases
sampling entire communities of bees (see At the community
after 48 h of deployment (Pane & Harmon-Threatt, 2017). Still,
level), while studying nest construction or within-nest behaviour
they have the advantage of allowing the researcher to link the
requires more targeted methods (see At the nest level). Accu-
occurrence of bee nests with habitat characteristics measured at
rately characterising nest-site selection also requires locating
individual nests–either in the field or in enclosed arenas. Finding a very local scale.
nests is one of the main challenges in studying ground-nesting One way to collect extensive ecological data, including on
bees. Here, we review the existing methods, both experimental ground-nesting bees, is by working with citizen scientists
and observational, used to study the habitat of ground-nesters, (Deguines et al., 2016), who can potentially sample on a broad
and we highlight some techniques that we hope will be used spatial and temporal scale at low cost. When observers are
more broadly in future. trained to identify local pollinator taxa (or groups of similar
taxa), the quality of the resulting data can be similar to that
of professionals (Kremen et al., 2011). Maher et al. (2019)
At the community level used citizen science to investigate the nesting requirements of
four European species of gregarious ground-nesters: Andrena
One method to survey ground-nesting bees is to observe cineraria (Linnaeus), A. fulva (Müller), Halictus rubicundus and
or sample the whole bee community. By identifying bees to Colletes hederae. To validate records, pictures were submitted
the genus or even family level, it is often possible to sort to an online platform and checked by scientists. The researchers
them by nesting type, distinguishing above- from below-ground were able to gather data on several variables, including number

of nests in the aggregation, extent of shading, and type of ground be useful. A small tube or inverted transparent cup can be placed
cover from 236 verified nests (out of 394 submitted records). over the nest entrance when the mother bee is inside (at night or
This example shows how citizen scientists can help overcome between foraging trips) (Wcislo, 1993; Neff & Simpson, 1997);
the logistical difficulty of finding ground-nesting bee nests; how- one can then wait for the bee to emerge, at which point she
ever, these four species were targeted because of their gre- can be measured, identified, individually marked (e.g. Andrena
gariousness and ease of identification. Less gregarious species vaga, Anthophora plumipes; Straka et al., 2014), or collected
would be more challenging (Maher et al., 2019). (Linsley et al., 1952; Michener et al., 1955). Alternatively, the
nest location can be marked and an emergence trap placed over
it the following year to collect emerging progeny (or parasites),
At the nest level
thereby quantifying the reproductive output from that nest.
Relative to cavity-nesters, ground-nesters are challenging to Although ground-nesting bees can be found in many different
study at their nests. Cavity-nesting bees occur naturally in natural environments, most are unwilling to nest in captivity.
wood cavities and hollow plant stems, and there is a sim- One exception is the squash bee, Peponapis pruinosa, which
ple method to monitor them using human-made infrastructure has consequently been used as a model species in many studies
such as nest boxes, also called “bee hotels” or “trap nests” (Julier & Roulston, 2009; Ullmann et al., 2016; Willis Chan
(reviewed by MacIvor 2017). These have been useful for study- et al., 2019). These bees tolerate a broad range of soil condi-
ing nest provisioning and reproductive output in above-ground tions, as long as they have access to their host plant, Cucurbita
cavity-nesting bees (Steffan-Dewenter & Schiele, 2008; For- spp. (Cucurbitaceae), and have, therefore, been reared in cages
rest & Chisholm, 2017; Schenk et al., 2018). Analogous arti- or greenhouses to investigate the effects of agricultural practices
ficial nesting structures have not been successfully developed on ground-nesting bees. A few species of ground-nesting bees
for ground-nesting bees; however, Fortel et al. (2016) had some have even been reared in the laboratory (reviewed in Leonard
success in attracting bees to nest in experimental plots of soil and Harmon-Threatt 2019), using observation chambers with
(1 m2 × 0.5 m deep). These authors obtained 232 individuals of glass windows to investigate their behaviour and nest archi-
37 ground-nesting bee species across their 16 urban study sites tecture (Michener et al., 1955). These nest boxes, similar to
(representing a total area of 36 m2 of substrate from which bees the ones commonly used to study ants, kept below-ground or
were collected) over a 2-year period (Fortel et al., 2016). This moved above-ground, have been used to observe Lasioglos-
method has not yet been widely deployed, but these results sug- sum zephyrum (Smith) (Batra, 1964, 1968; Michener &
gest that it could be an effective technique for assessing bee soil Brothers, 1971), Nomia melanderi (Batra, 1970), Macrotera
preferences and even, perhaps, for enhancing bee habitat. portalis (Timberlake) (Danforth, 1991) and Anthophora sp.
As noted previously, locating nests of ground-nesting bees in (Batra & Norden, 1996), among others (see Leonard and
more natural settings can be a substantial challenge, especially Harmon-Threatt 2019). However, this method works mainly
for species that do not form aggregations. One way to locate with social and communal bees (mostly halictids), and even
those nests could be by following nest-searching cleptoparasites with these, attempts are sometimes unsuccessful (Michener
(e.g. Nomada spp., Apidae), which often fly slowly and close et al., 1955). More research is needed on rearing other species,
to the ground and are therefore more conspicuous and readily as these could eventually be integrated in agricultural prac-
tracked than their hosts. By following parasites and noting how tices, with populations sustained in nesting beds (as has been
long they spend in an underground hole (cell parasitism takes done with Nomia melanderi; Cane, 2008) for crop pollination
more than 120 s), one could determine the location of the host purposes.
species’ nest (e.g. Sick et al., 1994). López-Uribe et al. (2015)
overcame the difficulty of finding nests by building a predictive Future directions
spatial model to detect suitable nesting habitat for Colletes
inaequalis based on ecological variables thought to be important Until the early 1990s, most studies of ground-nesting bees
for this species. The authors were able to identify 13 new were field observations describing nest architecture, imma-
aggregations thanks to this technique. More such models should ture stages, and parasites, as well as taxonomic notes (see
be developed to assess habitat suitability for ground-nesting Supplementary Table S1). These papers helped build a body
bees; however, this can only be achieved with species for which of knowledge on the nest structures and life histories of
the important habitat variables are already known. ground-nesters. Rearing projects yielded more knowledge of
Once nests have been identified, various techniques can within-nest behaviour and daily activity patterns. Since then,
be used to study the nest interior or other aspects of the studies have included more species, looking at the entire com-
species’ life history. Nest excavation techniques were first munity of ground-nesting bees in the context of nesting habitat
described in the 1930s by S.I. Malyshev (in Russian) and characteristics (Potts et al., 2005; Sardiñas & Kremen, 2014).
were published in English by Linsley et al. (1952). Excavation But only a handful of papers (e.g. Potts & Willmer, 1997) have
techniques have been improved and used since then to study nest actually focused on soil characteristics near nests in order to
architecture and reproductive output of many ground-nesting assess nesting preferences, and they have produced conflicting
bees. Unfortunately, this procedure is both destructive and results (e.g. soil hardness in Kim et al., 2006). As noted by
extremely meticulous, given the challenge of tracking tunnels Harmon-Threatt (2020), it is difficult to generalise about abiotic
in the midst of falling debris (Marinho et al., 2018). If internal preferences across ground-nesting bee species. Furthermore,
nest architecture is not the focus, targeted emergence traps can we still have no information on the nesting biology–including

the soil preferences–of many species. It remains impossible to to combat insect pests. A few papers have investigated the
draw conclusions about geographic or seasonal patterns (e.g. do effect of tillage (Ullmann et al., 2016; Skidmore et al., 2019),
ground-nesting bees that are active in cooler conditions–due to irrigation (Julier & Roulston, 2009) and pesticides (Willis Chan
an early flight season, or because they occupy high altitudes or et al., 2019) on ground-nesting bees, but more research is
latitudes–have stronger preferences for nesting in warm micro- needed on different species of ground-nesters, other than squash
habitats?). bees, and their reproductive output. We still know little about
As nest-site characteristics for ground-nesting bees have the effects of agrochemicals on survival of ground-nesting
received little quantitative study, there might be important fac- bees, whether at the underground larval stages or as adults,
tors influencing nest quality and nest-site selection that have but recent studies have begun to show impacts of pesticides
never been identified. What about the effect of below-ground on bees through exposure to contaminated soil (Anderson &
oxygen levels on larval survival? Or the effects of soil pH (as Harmon-Threatt, 2019; Willis Chan et al., 2019). There are
described for Eucera nigrilabris Lepeletier [Apidae] by Shebl also many unanswered questions related to the impacts on bee
et al., 2016), organic matter, and chemistry (including salin- populations of agricultural machinery in settings that could
ity and the presence of pollutants)? Similarly, few studies have be attractive nesting habitat for ground-nesters, but that could
investigated the influence of natural enemies on nest-site selec- act as ecological traps if nests are subsequently destroyed.
tion. For example, do certain soils create conditions more vul- Similarly, we know little about the consequences of cover
nerable to pathogen infection within the brood cell, or does the crops, mulch, plastic cover or straw on the soil surface for the
presence of predators or parasites influence where bees choose reproductive success of ground-nesting bees. Knowing more
to nest? about nesting requirements would allow farmers to supply
To identify and isolate the habitat characteristics that influ- patches of undisturbed habitat suitable for ground-nesting bees,
ence nest-site selection in ground-nesting bees, an experimen- along with the necessary floral resources. One practice to
tal or rigorous comparative approach is required. For example, create nesting resources is the development of patches of bare
comparing the attributes of nesting sites that are selected ground (Severns, 2004; Gregory & Wright, 2005) or sandy areas
by females, with those investigated but not used–as in the (Wesserling & Tscharntke, 1995). Such techniques are used by
study by Brockmann (1979) on the digger wasp Sphex ichneu- gardeners but could be developed at a broader scale in urban and
moneus–provides stronger evidence of preference than merely agricultural environments if shown to be effective.
quantifying the attributes of sites with nests. Well-developed Finally, studies are needed to quantify the importance for
methods to detect habitat selection (by comparing factors at the ground-nesting bee populations of soil habitat relative to other
nest site and at unused sites nearby) have been reviewed for factors such as floral resources or natural enemies (Roulston
birds by Jones (2001) and for all animals by Montgomery & & Goodell, 2011). To be sure, nesting sites and food are
Roloff (2017). While these methods were developed for verte- non-substitutable resources, but it is unclear how often each of
brates, they are equally applicable to bees–yet have scarcely these limits bee populations in nature (or in human-modified
been employed. Once nesting-site preferences have been doc- habitats). Better understanding the variables that have a major
umented, they can be incorporated in predictive models (as in influence on ground-nesting bees will help decision-makers, as
López-Uribe et al., 2015), to create maps of suitable nesting well as interested members of the public, to provide habitat and
habitat and to predict likely occurrences of the focal species. In conserve targeted species.
all such studies, it is crucial to consider the scale at which the
study organisms perceive their environment and within which
Acknowledgements
they can select habitat (Johnson, 1980). Studies that rigorously
document the factors involved in nest-site selection would allow We thank members of the Forrest lab and two anonymous
researchers to propose, and then test, adaptive hypotheses for the reviewers for constructive comments on earlier versions of the
observed preferences. manuscript. We have no conflicts of interest to report. Funding
More experimental research is needed to test which soil was provided by an Early Researcher Award to JF from the
factors (texture, compaction, moisture, etc.) are selected by Ontario Ministry of Research, Innovation and Science.
ground-nesting bees when choosing their nest location, and why.
For example, to test the preference for texture, one could give
female bees a choice among different soil textures–while hold- Data availability statement
ing all other factors constant–and document their preferences. In
addition to documenting the mother’s choice, measuring compo- Data sharing is not applicable to this article as no new data were
nents of offspring fitness would be required to assess the perfor- created or analyzed in this study.
mance of bee larvae under different conditions (i.e. the quality
of the nest location), which may not correspond exactly with the
mother’s preference. There is a huge gap in the literature regard- Supporting Information
ing the fitness of ground-nesting bees in relation to the various
Additional supporting information may be found online in the
soil characteristics we have reviewed.
Supporting Information section at the end of the article.
Such research would be especially valuable in agricultural
systems, where farming practices can involve mixing the soil to a Supplementary Table S1 A non-exhaustive list of primary
depth of up to 40 cm during tillage, and the use of agrochemicals research articles that have investigated the habitat associated

with ground-nesting (GN) bees. Bee species names are given as interspecific trait variation of native bees and flowering plants across
reported in the original paper. Variables are listed as predictor (P) burned and unburned landscapes. Frontiers in Ecology and Evolution,
or response (R) where appropriate. Under ‘Approach’, ‘manip- 7, 252.
ulative’ studies are those that experimentally modified one or Cane, J.H. (1981) Dufour’s gland secretion in the cell linings of bees
(Hymenoptera: Apoidea). Journal of Chemical Ecology, 7, 403–410.
more variables; ‘method’ studies focused on one method for
Cane, J.H. (1991) Soils of ground-nesting bees (Hymenoptera:
studying GN bees; ‘correlative’ studies are observational studies
Apoidea): texture, moisture, cell depth and climate. Journal of the
where the authors tested for an association between the response Kansas Entomological Society, 64, 406–413.
variable and one or more predictors; and ‘descriptive’ studies Cane, J.H. (1996) Nesting resins obtained from Larrea pollen host
generally documented the nesting biology of ground-nesting by an oligolectic bee, Trachusa larreae (Cockerell) (Hymenoptera:
bee species (nesting behaviour, pollen provisions, developmen- Megachilidae). Journal of the Kansas Entomological Society, 69,
tal stages, etc.). Studies are listed in reverse chronological order 99–102.
of publication. Cane, J.H. (1997) Ground-nesting bees: the neglected pollinator
resource for agriculture. Acta Horticulturae, 437, 309–324.
Cane, J.H. (2003) Annual displacement of soil in nest tumuli of
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Ecological Entomology (2020), DOI: 10.1111/een.

Nesting habitat of ground-nesting bees: a review

Introduction nesting substrates. Yet many aspects of the nesting habitat

© 2020 The Royal Entomological Society 1

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

Maher et al., 2019 Andrena cineraria × × Shade Descriptive Ireland

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

‡ For example, cracks in the soil and small cavities.

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

© 2020 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/een.12986

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