Apidologie (2022) 53:10 Review article

© The Author(s), 2022

https://doi.org/10.1007/s13592-022-00919-4

Estimating bee abundance: can mark‑recapture methods

validate common sampling protocols?

Emma L. BRIGGS1,4, Christopher BARANSKI2, Olivia MÜNZER SCHAETZ2,

Gabriela GARRISON2, Jaime A. COLLAZO3, and Elsa YOUNGSTEADT1
1
 Department of Applied Ecology, North Carolina State University, NC, 27695 Raleigh, USA
2
 North Carolina Wildlife Resources Commission, 1751 Varsity Drive, NC, 27606 Raleigh, USA
3
 U.S. Geological Survey, North Carolina Cooperative Fish and Wildlife Research Unit, Department of Applied Ecology,
North Carolina State University, NC, 27695 Raleigh, USA
4
 Warnell School of Forestry and Natural Resources, University of Georgia, GA, 30602 Athens, USA

Received 28 October 2021 – Revised 10 January 2022 – Accepted 26 January 2022

Abstract – Wild bees can be essential pollinators in natural, agricultural, and urban systems, but populations
of some species have declined. Efforts to assess the status of wild bees are hindered by uncertainty in common
sampling methods, such as pan traps and aerial netting, which may or may not provide a valid index of abun-
dance across species and habitats. Mark-recapture methods are a common and effective means of estimating
population size, widely used in vertebrates but rarely applied to bees. Here we review existing mark-recapture
studies of wild bees and present a new case study comparing mark-recapture population estimates to pan trap
and net capture for four taxa in a wild bee community. Net, but not trap, capture was correlated with abundance
estimates across sites and taxa. Logistical limitations ensure that mark-recapture studies will not fully replace
other bee sampling methods, but they do provide a feasible way to monitor selected species and measure the
performance of other sampling methods.

apoidea / mark–recapture / abundance estimation / bee monitoring / pan traps

1. INTRODUCTION Williams et al. 2002). In recent years, evidence

Estimating abundance is a fundamental com-
ponent of population and conservation biology,
yet for some organisms of conservation concern,
abundance is essentially unknown (Henderson &
Southwood 2016; Noon et al. 2012). This knowl-
edge gap is concerning because many environ-
mental assessment studies, including those that
can prompt regulatory protections, require a clear
understanding of abundance trends (Nichols &
Williams 2006; Otis et al. 1978; Schwartz 2008;
Corresponding author: E. L.  BRIGGS,
emma.briggs@uga.edu
Manuscript Editor Klaus Hartfelder.
of declines in populations of bees and other pol-
linators has spurred strong interest in monitor-
ing bee abundance over time and among habitat
types (Packer & Darla-West 2021; Portman et al.
2020; Potts et al. 2010; Prendergast et al. 2020;
Westphal et al. 2008). In the USA, nine bee spe-
cies are now protected under the Endangered Spe-
cies Act of 1973, and repeated calls for large-scale
monitoring efforts led to the formation in 2020 of
the US National Native Bee Monitoring Research
Coordination Network (US Fish and Wildlife
Vol.:(0123456789)
Service 2021; Tepedino & Portman 2021; Woodard
et al. 2020). Monitoring bee populations has both
ecological and economic incentives, due to the
important role of bees as pollinators in natural,

13
10 Page 2 of 24 E. L. BRIGGS et al.
agricultural, and urban environments (Kearns
et al. 1998; Potts et al. 2016).
The most common sampling methods in eco-
logical or monitoring studies of bees include pan
traps, vane traps, trap nests, netting from flow-
ers, and observation (over specified time, tran-
sect, or area) (e.g., Packer & Darla-West 2021;
Prendergast et al. 2020). Each of these methods
provides a population index: they yield a count per
unit of sampling effort, rather than an estimate of
the number of individuals per unit area (McKelvey
& Pearson 2001). Differences in counts over
time, space, or species are nevertheless often
interpreted as proportional differences in abun-
dance or relative abundance of species (e.g.,
Moylett et al. 2020; Winfree et al. 2007). The
validity of this interpretation depends on a con-
sistent relationship between the index sample and
the size of the underlying populations. In other
words, capture probabilities must be consistent
across time, habitats, and species (McKelvey
& Pearson 2001; Slade & Blair 2000). Thus,
even if a sampling method provides a satisfac-
tory index for one species, differential capture
probabilities across species or habitats may yield
poor indices of community composition—that is,
the relative abundances of the species in a com-
munity (Conroy 1996). Multi-species studies in
other taxa, such as small mammals or terrestrial
arthropods, have concluded that indices such as
trap catch cannot represent the relative abundance
of species, due to different species-specific cap-
ture probabilities (e.g., Andersen 1995; Hopkins
& Kennedy 2004; Lang 2000).
The relationship between index samples and
underlying community composition has not been
examined in studies of bees. Few studies have
examined this relationship for individual bee spe-
cies (reviewed below), and none has done so at a
community scale. Instead, community-level work
typically compares two or more index methods to
each other, and these studies have found that each
method provides a different picture of the bee
community (Gibbs et al. 2017; Prendergast et al.
2020; Westphal et al. 2008; Wilson et al. 2008).
Moreover, circumstantial evidence suggests that
the efficiency of bee sampling methods such as
pan traps varies across habitats and taxa (Baum
13
& Wallen 2011; Cane et al. 2000; Portman et al.
2020; Prendergast & Hogendoorn 2021; Wilson
et al. 2008) Thus, capture probabilities clearly
differ among sampling methods and likely dif-
fer among habitats and taxa. Despite this con-
cern, there has been no attempt to quantify and
account for differing capture probabilities in any
bee community sampling method (Henderson &
Southwood 2016; Packer & Darla-West 2021).
Mark-recapture methods are a common and
often effective means to obtain estimates of ani-
mal abundance with explicit measures of pre-
cision (such as SE) (Henderson & Southwood
2016; Kéry & Royle 2016; Krebs 1999; Otis et al.
1978; Williams et al. 2002). While widely used
in studies of mammals, birds, and amphibians,
mark-recapture methods are rarely used to esti-
mate bee abundance (Henderson & Southwood
2016; Nichols et al. 1981; Portman et al. 2020).
Here, we review existing mark-recapture studies
of bees to assess the potential of mark-recapture
as a tool to estimate bee population sizes and
relative abundances. We conclude with a case
study in which we used mark-recapture methods
to assess whether aerial netting and pan trap-
ping yielded reliable indices of abundance and
relative abundance for sampled species in the
community.
2. SCOPE OF LITERATURE REVIEW
We searched Clarivate Analytics Web of Sci-
ence and Google Scholar databases in January
2021 to identify studies that used mark-recapture
methods to estimate bee abundance. We used
the following keyword combination for Web
of Science: [(“mark recapture” OR “capture
recapture” OR “mark release recapture” OR
batchmark) AND (apoidea OR bees OR bee)].
Google Scholar search phrases included “bee
mark recapture population estimate,” “bumble-
bee mark recapture,” and “capture recapture bee
population”. We found additional articles through
cited references in the primary studies.
We recovered 20 mark-recapture papers
that calculated population estimates of bee
species (Table I). We identified 37 additional
 Estimating bee abundance: can mark‑recapture methods validate common... Page 3 of 24 10

Table I Summary of field methods for the 20 mark-recapture experiments that estimated population size

Reference Species Location Duration Intersample # of sites Study area Mark type Marking
period ­(m2) technique

Bischoff Andrena Germany 1 year  ~ 2 days 1 80 Individual Numbered

(2003) vaga date tag marker
pen
Danks Hylaeus UK 4 months 1 60,000 Site Paint
(1971) brevicornis
Goulson Bombus UK 6 weeks 14 2000 Genetic Tarsal
et al. lapidarius, sample
(2010) Bombus
pascuorum
Hennessy Eucera UK 3 months Variable 2 120–140 Individual Paint
et al. longicornis
(2020)
Hennessy Anthophora UK 3 months  ~ 2–3 days 1 250,000 Individual Paint
et al. retusa
(2021)
Iles et al. Bombus USA 2 months Variable 3 3000 Individual Numbered
(2019) bimaculatus, nest tag
Bombus
impatiens
Janzen Eulaema Costa 2 weeks 1 day 1 N/A Individual Hair removal
(1981) polychroma Rica date
Kroodsma Euglossa Costa 2 days  < 1 day 1 Individual Paint
(1975) imperialis Rica date
Larsson & Andrena Sweden 2 months  ~ 1 month 26 440– Date Paint
Franzén hattorfiana 181,000
(2007)
Larsson & Andrena Sweden 4 months 2–37 days 10 Date Paint
Franzén hattorfiana
(2008)
Matteson & Bombus USA 3 weeks 2–3 days 6 640–2188 Site Marker pen
Langellotto impatiens
(2009)
Michener Megachile USA 1 day 1 h 1 1045 Date Paint
(1953) brevis
Mola et al. Bombus USA 6 months 7–10 days 19 Genetic Tarsal
(2020a) bifarius, sample
Bombus
vosnesenskii
Mola et al. Bombus USA 9 months 4–30 days 11 Genetic Tarsal
(2020b) vosnesenskii sample
Steffan- Osmia Germany 5 days  ~ 5 days 5 10,842 Individual Numbered
Dewenter bicornis tag
& Schiele
(2004)
Stenström Bombus Sweden 4 month  ~ 2 days 1 1000 Individual Numbered
& alpinus, tag & paint
Bergman Bombus
(1998) hyperboreus

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10 Page 4 of 24 E. L. BRIGGS et al.

Table I (continued)

Reference Species Location Duration Intersample # of sites Study area Mark type Marking
period ­(m2) technique
Tepedino Eucera USA 2 month s 2–3 days 1 200 Date Enamel
(1981) pruinosa
Tosta et al. Euglossa Brazil 7 months  < 1 days 6 160,000– Date Leg segment
(2017) cordata, 2,000,000 removal
Euglossa
imperialis,
Euglossa
(9 spp.
pooled)
Wood et al. Bombus UK 20 days N/A 12 2,010,619 Genetic Tarsal
(2015) hortorum, sample
Bombus
terrestris
Yamamoto Xylocopa Brazil 17 days 1d 1 5000 Individual Numbered
et al. frontalis, tag
(2014) Xylocopa
(4 spp.
pooled)

mark-recapture papers that did not calculate pop-
ulation estimates, and these are listed in Text S1.
The geographic scope of the 20 reviewed stud-
ies was limited: 50% were completed in Europe,
30% in North America, 10% in South America,
and 10% in Central America (Table II). No stud-
ies were completed in Asia, Africa, or Australia.
3. TARGET SPECIES
If mark-recapture experiments are to be used
to validate other multi-species sampling meth-
ods, they must be feasible for a broad range
of bee diversity. To assess the breadth of prior
mark-recapture studies, we classified the target
species in each study according to their taxon-
omy (family), social organization (Text S2), nest-
ing substrate (Text S2), and body length (Text
S2). The reviewed studies sampled a total of 24
bee species, henceforth target species. Of the 24,
79% were in the family Apidae, 8% Andrenidae,
8% Megachilidae, and 4% Colletidae (Table II).
The families Halictidae, Melittidae, and Steno-
tritidae were not sampled. However, one study
that did not estimate population size collected
mark-recapture data for three halictid species—
indicating that population estimates should be
feasible for this bee family (Cecala & Wilson
Rankin 2020).
Target species represented a range of social
behaviors. Specifically, 38% of target species
were social, 13% broadly parasocial (semisocial
or communal), 42% solitary, 4% parasitic, and
4% had multiple social behaviors (Table II; Text
S2). The target species also exhibited diverse
nesting behavior, with 46% (mostly Bombus and
euglossine bees) nesting in pre-existing cavi-
ties, 21% in soil, 8% in wood, and only 4% in
stems (Table II; Text S2). Twenty-one percent
of the target species did not belong to a single
preferred nesting category or had unknown pref-
erences. To assess body size, we classified each
species as small (≤ 7 mm body length), medium
(7–12 mm), or large (≥ 13 mm) (Quistberg et al.
2016). Most target taxa (79%) were large, 13%
medium, 4% both large and medium (when
multiple species were pooled in a target genus),
and only 4% small-bodied (Table II; Text S2).
Often, researchers obtained separate abundance
estimates for male and female bees, owing to
differences in their phenology and behavior
(Table III).
Although mark-recapture methods have been
used to estimate population sizes in taxonomi-
cally and ecologically diverse bee species, the

13
 Estimating bee abundance: can mark-recapture methods validate common... Page 5 of 24 10

Table II Summary of target species in studies that generated bee population estimates using mark-recapture
methods

Speciesa Reference Location Family Socialityc Nesting Body

­substratec ­lengthb, c

Andrena Larsson & Sweden Andrenidae Solitary Soil L

hattorfiana Franzén
(2007, 2008)
Andrena vaga Bischoff (2003) Germany Andrenidae Solitary Soil L
Anthophora Hennessy et al. UK Apidae Solitary Soil L
retusa (2021)
Bombus Stenström & Sweden Apidae Social Cavity L
alpinus Bergman
(1998)
Bombus Mola et al. USA Apidae Social Cavity L
bifarius (2020a)
Bombus Iles et al. USA Apidae Social Cavity L
bimaculatus (2019)
Bombus Wood et al. UK Apidae Social Ground surface L
hortorum (2015)
Bombus Stenström & Sweden Apidae Parasitic Cavity L
hyperboreus Bergman
(1998)
Bombus Iles et al. USA Apidae Social Cavity L
impatiens (2019),
Matteson &
Langellotto
(2009)
Bombus Goulson et al. UK Apidae Social Cavity L
lapidarius (2010)
Bombus Goulson et al. UK Apidae Social Ground surface L
pascuorum (2010)
Bombus Wood et al. UK Apidae Social Cavity L
terrestris (2015)
Bombus Mola et al. USA Apidae Social Cavity L
vosnesenskii (2020a, b)
Eucera Hennessy et al. UK Apidae Solitary Soil L
longicornis (2020)
Eucera Tepedino USA Apidae Solitary Soil L
pruinosa (1981)
Euglossa Tosta et al. Brazil Apidae Parasocial Cavity M
cordata (2017)
Euglossa Kroodsma Costa Rica, Apidae Communal Cavity L
imperialis (1975), Tosta Brazil
et al. (2017)
Euglossa (9 Tosta et al. Brazil Apidae Parasocial, Cavity, M, L
spp. pooled)1 (2017) primitively unknown
eusocial,
semisocial,
solitary,
unknown

13
10 Page 6 of 24 E. L. BRIGGS et al.

Table II (continued)

Speciesa Reference Location Family Socialityc Nesting Body

­substratec ­lengthb, c

Eulaema Janzen (1981) Costa Rica Apidae Parasocial Cavity L

polychroma
Hylaeus Danks (1971) UK Colletidae Solitary Stem S
brevicornis
Megachile Michener USA Megachilidae Solitary Stem, cavity M
brevis (1953)
Osmia bicornis Steffan-Dewenter Germany Megachilidae Solitary Stem, cavity M
& Schiele
(2004)
Xylocopa Yamamoto Brazil Apidae Solitary Wood L
frontalis et al. (2014)
Xylocopa (4 Yamamoto Brazil Apidae Solitary Wood L
spp. pooled) et al. (2014)
a
 Target species whose traits have been inferred from closely related species (Text S2)
b
 S small (≤ 7 mm), M medium (7–12 mm), L large (≥ 13 mm)
c
 Sources for sociality, nesting, and size are provided in Table SI

applicability of this approach remains under-
explored in certain groups. Small-bodied bees
in general, and halictids in particular, are under-
represented in mark-recapture studies, given their
abundance and diversity in samples obtained by
trapping or netting (Portman et al. 2020; Roulston
et al. 2007). Moreover, several endangered bees
are small-bodied species in the genus Hylaeus
(USFWS 2016); conservation efforts could directly
benefit from non-destructive population estimates
generated from mark-recapture experiments. There
is clearly a need to develop and test mark-recapture
methods suitable for small-bodied species.
4. MARKING TECHNIQUES
AND ASSUMPTIONS
Researchers marked bees with a variety of per-
manent and impermanent methods. Impermanent
methods included marking the dorsal thorax of
each bee with colored marker pens, paints, enam-
els, or numbered plastic tags (Table I). Despite
the potential for impermanent marks to fall off
or fade, they can last for at least several weeks.
For instance, euglossine bees marked with paint
or plastic tags have been recovered 7–8 weeks
after their initial capture (Ackerman & Montalvo
1985; Pokorny et al. 2015). Permanent marking
methods included abdominal hair shaving and
removal of a tarsal segment (Janzen 1981; Tosta
et al. 2017). Although hair-shaved bees have been
recovered up to 6 weeks after marking (Janzen
1981), even permanent marks could eventually
be obscured by bodily wear or injury.
No matter the permanence of the marking
method, physical marks can be applied individu-
ally or in batches. With individual marking, every
captured bee receives a unique identifier such as a
numbered tag, a distinctive combination of paint
dots, or a unique hair shaving pattern. With batch
marking, multiple individuals receive the same
marking pattern, which represents only their col-
lective location or time of capture. Batch marking
has been performed with impermanent colored
paints, enamels, and leg segment removal.
Finally, genetic mark-recapture methods do not
require that insects be physically marked and
instead identify individuals or siblings by geno-
typing, often using a nonlethally sampled leg seg-
ment. Although genetic mark-recapture can, in
principle, be used for any species (Pennell et al.
2013), in studies of bees, it has been used exclu-
sively for bumble bees with the goal of estimating
the total number of colonies (not individual bees)
present at a study site (Goulson et al. 2010; Mola
et al. 2020a, b; Wood et al. 2015).

13
 Table III Results summary for the 20 mark-recapture experiments that estimated population size

Reference Species Sexa # ­capturesb Mean % MR ­modelc Mean N̂i Mean CV of N ̂ i Mean N̂ Mean CV of
recaptures (range)b (range)b,d (range)b,d,e (range)b,f N
̂ (range)5

Bischoff (2003) Andrena vaga M 90–293 32 (19–48) JS 66 (17–235) 45 (19–89) 140 (59–250)
F 71–959 41 (24–56) JS 226 (28–1445) 32 (10–99) 893 (140–2080)
Danks (1971) Hylaeus F 34 9 LP 204 41
brevicornis
Goulson et al. Bombus lapidarius N 2–81 36 (0–72) TIR 80 (15–416)
(2010) Bombus N 49–79 40 (13–77) TIR 90 (17–313)
pascuorum
Hennessy et al. Eucera longicornis M 25–121 24 (13–28) POPAN 31 (1–216) 51 (12–116) 116 (38–280) 31 (13–64)
(2020) F 23–263 28 (16–32) POPAN 61 (5–47) 34 (15–71) 205 (25–440) 17 (10–23)
Hennessy et al. Anthophora retusa M 50–160 24 (22–27) POPAN 14 (1–33) 32 (16–75) 107 (47–167) 6 (4–9)
(2021) F 42–57 6 (0–12) POPAN 6 (1–18) 54 (16–100) 44 10
Iles et al. (2019) Bombus N 11–40 73 (72–75) CAPTURE 6 (3–10)
bimaculatus,
Bombus impatiens
Janzen (1981) Eulaema M 407 8 (6–11) LP 981 (710– 38 (28–42)
polychroma 1388)
Kroodsma Euglossa M 396 6 LP 2187 18
(1975) imperialis
Larsson & Andrena F 565 (across Craig 43 (1–250)
Franzén (2007) hattorfiana 26 sites)
Larsson & Andrena F 6–434 33 (14–62) MP 141 (9–637)
Franzén (2008) hattorfiana
Estimating bee abundance: can mark-recapture methods validate common...

Matteson & Bombus impatiens F 27–67 45 (30–68) SE 88 (46–164)

Langellotto
(2009)
Michener (1953) Megachile brevis M 55 35 LP 66
Mola et al. Bombus bifarius N 161–240 11 (8–14) TIR 991 (975–
(2020a) 1007)
Bombus vosnesenskii N 332 42 TIR 413
Page 7 of 24 10

13
 Table III (continued) 10
Reference Species Sexa # ­capturesb Mean % MR ­modelc Mean N̂i Mean CV of N ̂ i Mean N̂ Mean CV of
recaptures (range)b (range)b,d (range)b,d,e (range)b,f N
̂ (range)5

Mola et al. Bombus N 17–199 12 (0–24) TIR 666 (228–

vosnesenskii
Page 8 of 24

(2020b) 1600)
Steffan-Dewenter Osmia bicornis F 21–404 23 (4–45) LP 251 (90–420)
& Schiele
(2004)
Bombus alpinus,

13
Stenström & F 210 25 SE 350
Bergman Bombus
(1998) hyperboreus
Tepedino (1981) Eucera pruinosa M MP 61 (35–110)
F MP 58 (17–106)
Tosta et al. Euglossa cordata M 12–36 15 (14–17) JS 66 (22–110) 50 (43–56)
(2017) Euglossa M 42 10 JS 611 27
imperialis
Euglossa (9 spp.) M 31–71 9 (6–12) JS 483 (111–1385) 37 (28–56)
Wood et al. Bombus hortorum N TIR 92–1780
(2015) Bombus terrestris N TIR 185 (65–412)
E. L. BRIGGS et al.

Yamamoto et al. Xylocopa frontalis M, F 40–142 33 (28–39) JS 252 (43–448) 83 (64–103)

(2014) Xylocopa (4 spp.) M, F 105–310 16 (7–25) JS 496 (118–1032)
a
  M  male, F  female, N  nest
b
 Values are ranges of estimates across sites, dates, or site-date combinations. Missing values were not reported or could not be readily computed from reported data
c
 JS  Jolly-Seber, LP  Lincoln-Petersen, TIR  Two Innate Rates, POPAN  POPAN (Jolly-Seber), MP  Manly-Parr, SE  Schumacher-Eschmeyer
d ̂
  N i refers to daily population estimates generated from the minimum number of sampling periods
e
 CV is the coefficient of variation, that is, the SE of the population estimate as a percentage of the estimate itself
f ̂
  N refers to gross population estimates, that is, the cumulative number of individuals that existed in the population across multiple sampling periods
 Estimating bee abundance: can mark-recapture methods validate common...
All studies assumed that marks were not lost
over time, and all but one study assumed that
marking did not affect a bee’s survival or behav-
ior. However, it is important to explicitly test these
assumptions because paints and markers often con-
tain toxic materials, and some permanent mark-
ing methods may create wounds that can become
infected (Henderson & Southwood 2016). In addi-
tion, colorful marks could cause bees to be more
vulnerable to predation or alter their thermoregu-
latory ability. Nevertheless, few studies examined
the validity of these assumptions, either directly
(e.g., laboratory or field studies) or indirectly (e.g.,
goodness-of-fit tests). In laboratory studies, cel-
lulose paint markings and thoracic scratch marks
were not lost over time and did not affect bee lon-
gevity, although the authors provided few details
about their methods (Danks 1971; Pokorny et al.
2015). No bee study explicitly tested mark longev-
ity in the field, but this could be done with double-
marking, which allows researchers to detect mark
loss (Henderson & Southwood 2016; Henry &
Jarne 2007; Seber & Felton 1981).
A double-marking system could also be used
to jointly test the effects of marking on bee sur-
vival and behavior (Henderson & Southwood
2016; Seber & Felton 1981). With this approach,
two marking techniques are used individually
and concurrently. For example, bees could be
marked with either egg albumin protein pow-
der that is undetectable to the naked eye, tradi-
tional paint marks, or both. If bees have similar
recapture rates regardless of mark type, then the
type of marks applied likely have no impact on
the survival or behavior of the bees. Bischoff
(2003) took another approach, using a χ2 test
to determine whether capture rates of Andrena
vaga individuals differed among unmarked,
once-marked, or multiple-marked bees. Capture
probability declined only after eleven markings,
suggesting that the impact of marking on bee
behavior was likely small.
Small-bodied bees appear to be underrepre-
sented in the mark-recapture literature, perhaps
because of challenges inherent in marking very
small animals. However, several novel marking
techniques could be useful in future work on
small-sized species. Microdots are small polymer
Page 9 of 24 10
discs (0.5-mm diameter) that can display up to
26 characters of information. Whitehead &
Peakall (2012) successfully used microdots in a
mark-recapture study of a 9-mm-long parasitoid
wasp species. Similarly, protein powder marks
have been developed for other mark-recapture
studies and may also be useful for batch marking
in abundance studies. Advances by Boyle et al.
(2018a, b), and Jones et al. (2006) have shown
that protein powders can be applied directly to
adult bees or to cocoons, that they persist through
repeated exposures to simulated rain, and can
be sampled nonlethally from recaptured bees.
The recovered proteins are then identified in an
ELISA assay, which requires a relatively modest
investment in equipment. Protein marking is now
a reasonable option for mark-recapture studies
targeting potentially vulnerable wild bee species.
5. MARK‑RECAPTURE MODELS
Mark-recapture models can be divided into
two broad categories—closed and open. Within
these categories, the 20 studies used seven mod-
eling approaches and methods (Table III), gen-
erating population estimates using a wide range
of sample sizes (number of captures, n = 3 to
959; mode = 23) (Fig. 1). Sixty-one percent of
the sample sizes were ≤ 50 and 73% were ≤ 100.
All the mark-recapture models described below,
except for genetic mark-recapture models, can
be used with batch marked bees. Details of these
models can be found in Craig (1953), Henderson
& Southwood (2016), Krebs (1999), and Matter
& Roland (2004).
5.1. Closed population models
Closed mark-recapture models assume that
there are no births, deaths, immigrations, or emi-
grations during the period of study (Henderson &
Southwood 2016). The closed models that have
been used in bees include the Craig (Craig 1953),
Lincoln-Petersen (Lincoln 1930), Schumacher-
Eschmeyer (Schumacher & Eschmeyer 1943),
and K-sample capture-recapture models (Otis
et al. 1978; Williams et al. 2002). These models
share three main assumptions: (1) the population
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10 Page 10 of 24 E. L. BRIGGS et al.
Figure  1.  Total number of capture events in mark-recapture studies that computed a population estimate. Figure
excludes four studies that used genetic mark-recapture methods and one study that did not report sample sizes.
is closed throughout the study period, (2) bees do
not lose their marks over time, and (3) all marks
are correctly noted at each sampling occasion
(Henderson & Southwood 2016; Krebs 1999;
Matter & Roland 2004; Nichols et  al. 1981).
The Craig, Lincoln-Petersen, and Schumacher-
Eschmeyer methods assume a constant and equal
capture probability for all individuals, and lack
goodness-of-fit (GOF) tests that would suggest
whether assumptions were met (Henderson &
Southwood 2016; Krebs 1999).
K-sample capture-recapture models, which
we employed in the case study below, relax this
assumption and incorporate GOF tests (Otis
et al. 1978). This method uses a family of closed
population models where each member of the
family holds different assumptions about the
potential sources of variation in capture prob-
ability (Nichols et al. 1981). Commonly used
models include ­M0 (which assumes a constant
capture probability), M­ t (time varying capture
probability), ­Mb (behavioral response to cap-
ture impacts capture probability), and M ­ h (het-
erogeneity in capture probability among indi-
viduals for unknown reasons) (Otis et al. 1978).
Mixed models that combine assumptions are
also frequently used. By systematically testing
each member of the family of closed popula-
tion models, the model that best fits the data is
identified (Henderson & Southwood 2016). This
approach improves upon older closed population
models, but functions best when at least four or
13
five sampling periods are completed (Henderson
& Southwood 2016; Krebs 1999).
Four studies used genetic mark-recapture
techniques to compute the population size of
social bee species (Table III). These studies also
assumed a closed population yet required no phys-
ical marking (Miller et al. 2005). All four genetic
mark-recapture studies used the two innate rates
model (TIRM), which allows individuals to be
captured multiple times per sampling session and
does not assume equal capture probability among
all individuals (Pennell et al. 2013).
5.2. Open population models
Open mark-recapture models assume that
populations do change during the study period.
In our review, two types of open mark-recapture
models were used to estimate population size: the
Manly-Parr and Jolly-Seber methods (Jolly 1965;
Manly & Parr 1968; Seber 1965). The Manly-
Parr method requires multiple sampling events
and allows mortality to vary with age (Manly
& Parr 1968). While this method does require
sampling a relatively high proportion of the total
population (> 25% for populations with less than
250 individuals and > 10% for larger populations)
and can produce larger standard errors than other
open population models, it is particularly suited
to populations where mortality may be related to
age (Henderson & Southwood 2016).
 Estimating bee abundance: can mark-recapture methods validate common...
The Jolly-Seber method was the most com-
monly used population model in the reviewed
studies (Table III). This method includes mul-
tiple versions such as the POPAN, Link-Barker,
Burnham JS, Pradel-recruitment, and Pradel-λ
models (Henderson & Southwood 2016). The
Jolly-Seber method requires multiple sampling
periods and has six main assumptions: (1) all
individuals have an equal probability of capture,
(2) every marked animal has the same probabil-
ity of survival, (3) marks are not lost, (4) marks
are not overlooked at capture, (5) all captured
individuals have the same probability of being
returned to the population, and (6) sampling
time is negligible in relation to intervals between
samples (Krebs 1999; Nichols et al. 1981). Addi-
tionally, the Jolly-Seber method assumes that all
individuals are captured from one freely mixed
population that is located within a single area
and that all losses through emigration or death
are permanent (Jolly 1965; Nichols et al. 1981).
Population estimates generated from the Jolly-
Seber method are usually reliable if more than 9%
of the total population is sampled and the sur-
vival rate from one sampling period to the next
is not less than 0.5 (Bishop & Sheppard 1973).
While the Jolly-Seber method is a useful mark-
recapture model, it may be less accurate when
the mortality of the study organism is related to
age (Henderson & Southwood 2016). Some bee
species do have increased mortality with age,
indicating that the Jolly-Seber method may be
inappropriate (e.g., Goldblatt & Fell 1987) and
should instead be used when the duration of the
study is very short compared to the adult lifespan,
and when mortality is primarily due to predation
or environmental stressors. However, researchers
are now developing Jolly-Seber models with age-
dependent processes, but these novel approaches
have so far relied on individual marking and have
not been conducted in bees (e.g., Hostetter et al.
2021).
To determine whether age-dependent mor-
tality is a concern, researchers can evaluate the
survivorship of their target species over time.
For example, to determine if the Jolly-Seber or
Manly-Parr method was appropriate for a mark-
recapture study of the butterfly Maniola jurtina,
Page 11 of 24 10
Brakefield (1982) modeled survivorship curves
for the butterfly by first releasing a cohort of
freshly emerged marked individuals and tracking
their recaptures over time. The butterflies initially
exhibited a period of constant survival, followed
by a period of senescence. Similar approaches
could be used in studies of bees to identify time
periods during which the Jolly-Seber model is
appropriate. Although none of the bee mark-
recapture studies that used the Jolly-Seber
method plotted survivorship curves for their tar-
get species, some experiments were completed
over a very short time period of time, as little as
8 days (Table I) (Tosta et al. 2017; Yamamoto
et al. 2014). However, other studies that lasted
weeks or months may be subject to more substan-
tial impacts, and future work would benefit from
explicit tests of age-dependent survival.
5.3. Fit and precision
Few studies reported whether their data met
mark-recapture model assumptions. Even when
GOF tests or model selection were employed,
the results of fit tests were not reported (Bischoff
2003; Goulson et al. 2010; Hennessy et al. 2020,
2021). In the absence of GOF tests, or direct field
tests of model assumptions, the validity of the
resulting population estimates is unknown, and
these oversights must be explicitly addressed in
future studies.
Assuming that model assumptions were met,
the precision of the resulting estimates is of
interest. If an intense sampling effort produces
imprecise estimates, the cost of the estimate may
exceed its usefulness. The coefficient of varia-
tion (CV) is a common measure of precision,
computed as the standard error of the estimated
population size divided by the estimate itself,
often presented as a percentage. Smaller values
indicate greater precision. The CV depends on
sample size, population parameters such as cap-
ture and survival probabilities, and the specific
model employed. As a rule of thumb, Pollock
et al. (1990) suggested that a CV of 20% should
be a reasonable target when planning a mark-
recapture study. Not all reviewed studies reported
13
10 Page 12 of 24 E. L. BRIGGS et al.
the CV or information required to compute it.
Among those that did, the average CV across
estimates was often larger than 20%, but nearly
every study—excluding those of male orchid
bees (Eulaema, Euglossa)—yielded at least
some estimates with high precision (Table III).
Although bee population estimates will often
be noisy, the range of detection probabilities
(0.06–0.93) and CVs (Table  III) they report
broadly overlap those in similar studies in other
taxa (e.g., Bailey et al. 2004; Haddad et al. 2008;
Nichols et al. 1981) suggesting that informative
population estimates are possible and can be up-
weighted in downstream analyses or decisions
(e.g., Bolam et al. 2019).
5.4. Future directions in modeling bee
population size
Developments in modeling approaches have
made it possible to handle and account for key
assumptions (e.g., population closure), incorpo-
rate sources of variation (e.g., heterogeneity), and
use additional information (e.g., locational data)
to derive more ecologically meaningful popula-
tion parameters (Borchers & Fewster 2016; Kéry
& Royle 2016; Williams et al. 2002). For exam-
ple, Pollock (1982) described the robust design
to compute population size. This method uses a
nested sampling structure, composed of a series
of closely spaced mark-recapture samples, which
are separated by longer time intervals. K-sample
closed population capture-recapture models
such as those described by Otis et al. (1978) are
applied to the groups of closely spaced samples.
During the longer time intervals, the population
is assumed to be open (Henderson & Southwood
2016; Pollock 1982). By combining these tech-
niques, the robust design can reduce bias caused
by unequal catchability and provide estimates
for population parameters (such as birth rate and
population size) in the first primary sampling
period that cannot be generated with open popu-
lation models alone (Henderson & Southwood
2016; Pollock 1982).
Another area of major advances in model
development that might be applicable to bee
13
research are spatial mark-recapture models
(Borchers & Fewster 2016). Bee research-
ers have yet to apply these types of models
because mark-recapture studies typically cap-
ture bees at a single resource (flowers or nests)
that is clumped in the landscape. Estimates of
the population at a given resource patch are
likely unique to that patch and do not represent
landscape-scale densities. However, if appro-
priate and feasible, spatial mark-recapture
models are a powerful research tool because
they yield explicit estimates of population
density, not just population size (N) within an
area of interest (Sollmann et al. 2012). Spatial
mark-recapture models account for heteroge-
neity in capture probability arising from the
interaction between animal activity centers and
sampled locations (Borchers & Fewster 2016;
Chandler & Royle 2013). Generally, spatial
recaptures imply that the identity of the bee
be known to obtain locational (spatial) data.
Marking bees can be challenging, particularly
for smaller-sized bees. In such cases, Chandler
and Royle (2013) and Augustine et al. (2018)
have developed methodological approaches to
deal with unmarked or partially marked popu-
lations (e.g., batch marking). Data require-
ments consist of spatially referenced counts
made on one or multiple occasions at closely
spaced sample units such that individuals in
the population are encountered at multiple
locations (Chandler & Royle 2013). However,
spatial mark-recapture models still assume that
movements and resource use are independent
among individuals; thus, if the assumption of
independence is not met in social bee studies,
estimates of population abundance might be
biased with inflated variance (overdispersion).
Finally, in social bee species, there is a
distinction between reproductive population
(number of colonies) and total population
(number of workers). Depending on the study
goals, either parameter may be of interest.
Both genetic and non-genetic mark-recapture
methods can provide these estimates. Colony-
level models have been applied only to Bom‑
bus and not to other social or parasocial spe-
cies, such as many halictids and euglossines.
 Estimating bee abundance: can mark-recapture methods validate common...
In these taxa, where the morphological distinc-
tion between castes is subtle or absent, genetic
mark-recapture holds promise for providing
estimates of the reproductive population size.
Even when a total worker population size is
desired, genetic mark-recapture may help
overcome difficulties with physically mark-
ing small insects.
6. USING MARK‑RECAPTURE
POPULATION ESTIMATES
TO VALIDATE INDEX SAMPLES
Given that mark-recapture methodology is
established in bee studies and has produced
reasonably precise estimates, it may be a viable
method to evaluate the biases of index sampling
methods. Only four studies, however, compared
mark-recapture population estimates to index
sampling methods, including nest counts, sur-
vey walks, and pan traps (Table IV). All stud-
ies made this comparison within individual
species, not among members of a community.
Three studies compared population estimates of
the number of bees counted during survey walks,
with mixed results. In the solitary bee species
Andrena hattorfiana, survey counts and popula-
tion estimates were highly correlated (r = 0.99,
p < 0.001) (Larsson & Franzén 2008). However,
in the solitary Eucera pruinosa, Tepedino (1981)
concluded that counts during survey walks over-
estimated population size early in the season,
when few flowers were open and the same bees
were counted repeatedly as they moved from
flower to flower. The third study addressed two
social species (Bombus hortorum and Bombus
terrestris) and compared the numbers of bum-
ble bees observed on transect walks, the number
caught in pan traps, and the number of colonies
estimated using genetic mark-recapture. These
three metrics were uncorrelated, but it is per-
haps not surprising that forager number and nest
number were unrelated since nest size can vary
(Wood et al. 2015).
Finally, one 2-month study of Andrena vaga
compared repeated nest counts to the estimated
Page 13 of 24 10
number of females in the population. Both met-
rics fluctuated through the season, but were
not correlated (Bischoff 2003). Many females
detected early in the season likely failed to
nest, whereas some females built more than
one nest, such that population size and nest
counts represented different aspects of the spe-
cies’ demography. Thus, two of the four studies
compared population estimates to index samples
that represented entirely different demographic
rates (colony number vs. worker number; total
females vs. nests) and thus tell us little about the
validity of those index samples. Mark-recapture
methods are clearly underutilized as a means to
understand the performance of other common
methods such as aerial netting and pan trap
sampling.
7. CASE STUDY
Although mark-recapture methods in stud-
ies of bees have been employed since the
1950s, they have rarely been used to inform
community-level work. Five of the reviewed
studies attempted to compute population esti-
mates for multiple closely related target spe-
cies, but none obtained estimates for more than
two species in a single study (Table III). To
assess the feasibility of multi-species mark-
recapture in bee studies and to compare these
population estimates to other sampling meth-
ods, we conducted a mark-recapture study in
2020 at three study sites in the Butner-Falls of
Neuse Game Lands. Sites were near Raleigh,
NC, USA (“site A,” 36.0278, − 78.6715,
“site B,” 36.0040, − 78.6813, and “site C,”
36.0276, − 78.6661). Sites A and C were
about 0.5  km apart, while site B was 3  km
away. Each study site was located in a clearing
within a pine forest that had undergone pre-
scribed fire in the past three years; vegetation
included grasses, forbs, shrubs, and tree sap-
lings (Fig. 2). We selected these sites due to
their association with an ongoing study by the
North Carolina Wildlife Resources Commis-
sion (NCWRC).
13
10 Page 14 of 24 E. L. BRIGGS et al.

Table IV Summary of studies comparing estimates of local bee populations using mark-recapture models and
non-mark-recapture approaches
Source Species Index method Correlationa pb

Bischoff (2003) Andrena vaga Nest counts R = 0.243 0.413

Larsson & Franzén (2008) Andrena hattorfiana Survey walks R = 0.99  < 0.001
Tepedino (1981) Eucera pruinosa Survey walks R =  − 0.29c 0.58c
Wood et al. (2015) Bombus hortorum Survey walks ρ = 0.11 0.73
Pan traps ρ = 0.06 0.85
Bombus terrestris Survey walks ρ = 0.26 0.42
Pan traps ρ = 0.16 0.63
This study Multiple taxa Aerial netting R = 0.71 0.03
Pan traps R = 0.33 0.39
a
 Correlation coefficient, if reported or estimable from reported data
b
 p-value of correlation coefficient; bold values are significant at α = 0.05
c
 Our analysis using digitized plots in the original reference

7.1. Methods On pan trap and net sampling days, 30 pan

The study was divided into five two-week
sampling periods from July 6 to Sept. 11, 2020.
During each period, we dedicated 3  days to
mark-recapture activity, followed by 1 day of
sampling with pan traps and aerial netting. On
mark-recapture days, we captured bees using
insect nets. All bees were netted within 50 m of a
permanent pan trap transect. Sampling occurred
during clear weather conditions from 10:00 am
to 4:00 pm. Four bee taxa were captured: eastern
carpenter bees (Xylocopa virginica), leafcutting
bees (Megachile spp.), two-spotted longhorn
bees (Melissodes bimaculatus), and green sweat
bees (Augochlorella spp., Augochlora pura, &
Augochloropsis spp.). Each site received 30
person-minutes of active search time in the
morning (10:00 am–1:00 pm) and 30 person-
minutes in the afternoon (1:00 pm–4:00 pm).
We visited the sites in a different order each
sampling period. After capture, we transferred
bees into a “bee squeezer” (Kearns & Thomson
2001), where we marked them on the dorsal tho-
rax with a dot of color using Posca extra fine-
point paint pens (Uni Mitsubishi Pencil, Tokyo,
Japan; Fig. 2). A different paint color was used
on each sampling day. Bees recaptured on days
two and three of the survey were marked with an
additional spot of paint and released.
traps were placed approximately 30 cm off the
ground along a fixed 10 m × 45 m transect. The
transect consisted of 10 pan trap triplets (blue,
yellow, white) arrayed in 10 parallel rows. All
pan traps were spaced 5  m apart within and
between rows. Traps were deployed for about
10 h per day during daylight hours. While traps
were deployed, we sampled by aerial netting
within 50  m of the transect. Each study site
received 30  min of active search time in the
morning (~ 10:00 am–1:00 pm) and 30 min in
the afternoon (~ 1:00 pm–5:00 pm). The lag time
between the mark-recapture and pan trap and net
sampling ranged from 1 to 7 days, with a mean
of 3.6 days across all five sampling periods. This
variation was unavoidable since different enti-
ties performed these methods and did so within
weather constraints.
We estimated population sizes using program
CAPTURE for closed population K-sample
models featured in program MARK (Otis et al.
1978, White & Burnham 1999). Population clo-
sure was reasonable for our study because each
3-day mark-recapture sample was completed
within a 5-day period, which is short relative to
the adult activity period of the focal bee taxa. We
attempted to generate population estimates for
every unique combination of target taxa, study
site, and survey week; however, some estimates

13
 Estimating bee abundance: can mark-recapture methods validate common... Page 15 of 24 10

Figure 2.  Images of the typical vegetation at each site in the case study (a), a top and side view of a bee squeezer (b,
c), and a marked eastern carpenter bee (Xylocopa virginica) (d).

could not be generated due to low capture or
recapture rates. We determined if models met
model assumptions (GOF) using chi-square
tests. We generated observed/expected frequen-
cies from the most generalized model (global)
in the model set using the program MARK (i.e.,
output/specific model output/residuals). We
summed the chi-square values and computed
a probability whose degrees of freedom were
equal to the number of encounter histories minus
one. If expected values were small (i.e., < 2), we
pooled encounter histories to minimize spurious
chi-square results.
For index samples to provide a reliable indi-
cator of community composition, each spe-
cies must have similar detection probabilities
in the index sample, such that index captures
and population estimates fit a single linear
relationship for all species in the community.
To test this relationship for our focal taxa, we
conducted linear regression analyses in which
mark-recapture estimates were the predictor,
and net and trap capture were the responses,
with one data point per site-species combi-
nation. Specifically, for each site-species
combination, we summed pan trap and aerial
netting captures across sampling periods, and
we took a weighted average of all the mark-
recapture estimates across sampling periods
(weighted by the reciprocal of the width of
the 95% confidence interval, after log trans-
formation). Because mark-recapture was per-
formed on different days than netting and pan
trapping, this pooled dataset prevented daily
weather or other transient conditions from
obscuring overall relationships between the
samples and population estimates at the study
sites.

13
10 Page 16 of 24 E. L. BRIGGS et al.

7.2. Results and discussion reported in prior studies of individual taxa

Of sixty possible site-species-date combi-
nations, we generated 22 population estimates
(Table V, Fig. 3). The CAPTURE model ­M0,
which assumes a constant capture probability,
was the most common model fit to the data.
Twenty estimates were obtained from models
that met assumptions (chi-square GOF, P > 0.05).
Observed/expected values were insufficient to
run GOF tests on the two remaining models.
The precision of estimates was similar to that
(Table III), with CVs ranging from 0.12 to 0.90.
Capture probabilities ranged from 0.04 to
0.52 across all sites and target taxa. Across sites,
the average capture probability (mean ± SE)
of green sweat bees was 0.21 ± 0.07, leafcut-
ting bees 0.27 ± 0.06, two-spotted longhorn
bees 0.36 ± 0.05, and eastern carpenter bees
0.23 ± 0.07. Across sites and dates, the standard
sampling methods yielded a sample of 77 bees
of the focal taxa by aerial netting and 42 in pan
traps. Species-level identifications of captured

Figure 3.  Pan trap, aerial netting, and mark-recapture results for all study sites, dates, and target taxa. Numbers of
bees are log-transformed to improve their distribution. Error bars on the mark-recapture results represent the 95%
confidence interval of the population estimate from program MARK.

13
 Estimating bee abundance: can mark-recapture methods validate common... Page 17 of 24 10

Figure  4.  Across sites and species, pan trap capture (a) was independent of population estimates, while net cap-
ture (b) increased with population. For reference, species are represented by different symbols, but species was not
included in the statistical analysis (GSB, green sweat bee; Meg, Megachile; Mel, Melissodes bimaculatus; Xyl, Xylo‑
copa virginica).

green sweat bees and leafcutting bees are provided
in Tables SIII-SVI. Eastern carpenter bees and
leafcutting bees were rarely or never captured in
pan traps, while other target taxa such as long-
horn bees and green sweat bees were more com-
monly sampled (Fig. 3).
The linear regressions of index samples on
population estimates included nine data points
each because the original 22 mark-recapture
estimates correspond to nine site-species com-
binations  (Fig.  4). Population estimates were
correlated with aerial netting captures (R2 = 0.51,
r = 0.71, p = 0.03) but not pan trap captures
(R2 = 0.11, p = 0.39). The correlation between net
capture and population size approaches r = 0.8, a
guideline suggested by Slade and Blair (2000) to
determine when an index sampling method pro-
vides a good indicator of population size.
Collector bias is a common concern with
aerial netting, but in this case, netting per-
formed well relative to mark-recapture estimates
even though these methods were conducted by

13
 10

Table V Summary of mark-recapture results for study sites and target taxa that produced population estimates in the case study

Target taxa Site Week Total # Total # % ­recaptureda Population Standard error CV CAPTURE Capture probability Total % of
marked recaptured ­estimateb model population
Page 18 of 24

­captureda

Green sweat bees A 2 36 14 39% 30 4.4 0.15 M0 0.40 120%

C 1* 8 1 13% 17 12.1 0.71 M0 0.16 47%

13
2 18 1 6% 97 85.7 0.88 M0 0.06 19%
3 31 3 10% 98 47.8 0.49 M0 0.11 32%
5* 4 1 25% 4 1.5 0.38 Mh 0.33 100%
Megachile spp. A 1 34 15 44% 27 3.6 0.13 M0 0.43 126%
2* 6 1 17% 9 5.4 0.60 M0 0.23 67%
B 1 20 1 5% 121 108.4 0.90 M0 0.05 17%
2* 6 2 33% 5 1.9 0.39 M0 0.38 120%
3 75 7 9% 254 83.0 0.33 M0 0.10 30%
4 89 12 13% 206 48.1 0.23 M0 0.14 43%
5 75 9 12% 189 52.0 0.28 Mt 0.07, 0.18, 0.17 40%
C 1 22 12 55% 14 1.7 0.12 M0 0.52 157%
E. L. BRIGGS et al.

2* 4 1 25% 3 1.3 0.42 M0 0.42 133%

Melissodes bimaculatus A 1* 5 2 40% 4 1.1 0.27 Mh 0.42 125%
B 3 12 3 25% 13 3.0 0.23 Mh 0.30 92%
Xylocopa virginica B 1 59 5 8% 201 75.4 0.37 Mt 0.12, 0.04, 0.13 29%
2 42 10 24% 41 6.6 0.16 Mbh 0.44, 0.44, 0.44 102%
3* 8 1 13% 17 12.1 0.71 M0 0.16 47%
5 19 1 5% 35 5.8 0.17 Mh 0.18 54%
C 1 19 1 5% 109 96.8 0.89 M0 0.06 17%
2 17 8 47% 13 2.3 0.18 M0 0.44 131%

a
 Percentages have been rounded to the nearest whole number
b
 Populations were not estimable for some mark-recapture periods due to low capture rates or lack of recaptures
*
 Asterisks indicate that sample sizes were not sufficient to run a GOF test; all other model runs met model assumptions
 Estimating bee abundance: can mark-recapture methods validate common...
different individuals. Moreover, during netting
for the mark-recapture study, we detected no dif-
ference in the capture probability among taxa.
Taken together, these relationships suggest that,
across sites and species, aerial netting captured
bees in proportion to their underlying abundance
and provided a reasonable index of community
composition, whereas pan traps did not. While
pan traps can be useful in bee diversity surveys
(Prendergast et al. 2020; Westphal et al. 2008),
our results validate concerns that they should not
be used as a quantitative index of population size
or relative abundance of species. However, the
pan trap samples collected during this study were
small. Many authors have noted that the appar-
ent efficiency of pan traps varies among years
and habitats (Baum & Wallen 2011; Cane et al.
2000; Wilson et al. 2008), and further research
is needed to identify conditions under which pan
traps can and cannot provide a reliable index of
bee abundance and composition.
8. CONCLUSIONS AND FUTURE
DIRECTIONS
Our literature review and case study demon-
strate that mark-recapture methods are feasible
in taxonomically and ecologically diverse bees
and can produce reasonably precise population
estimates (Table III; Table V). Although labor-
intensive to generate, mark-recapture population
estimates could inform other sampling methods
or conservation actions and are currently under-
utilized in the ongoing global discussion of bee
sampling and monitoring methods. Despite their
potential, mark-recapture methods in studies of
bees do have several limitations and challenges, as
well as exciting future directions, which we sum-
marize below as a guide to planning future studies.
8.1. Challenges and future directions
Challenge: Small body sizes  Because small-bodied
bees are frequently captured in some index sam-
pling methods, such as pan traps (Roulston et al.
2007), future comparative work needs to tackle
Page 19 of 24 10
population estimates in these small-bodied
groups. Our case study, as well as the work of
Cecala & Wilson Rankin (2020), suggests that
marking is feasible in these groups. Newer methods
—including the use of microdots, protein pow-
ders, or genetic mark-recapture—may also
improve the feasibility and precision of popula-
tion estimates in small species.
Challenge: Species identification  For many
bees, identification of species is nearly impos-
sible without microscopic examination. Mark-
recapture studies, which rely on field identifica-
tion, are often limited in their ability to identify
bees beyond genus or morphospecies. This limi-
tation may hinder conservation studies focused
on individual species that are difficult to iden-
tify in the field. Genetic mark-recapture meth-
ods have the potential to overcome this hurdle
since nonlethal genetic samples could be taken
from all individuals encountered, and their spe-
cies identity confirmed by barcoding in the lab
(Magnacca & Brown 2012). Even without this
advance, mark-recapture experiments have use-
ful applications for easily identifiable bee spe-
cies and for validating the detection rates of other
sampling methods at the genus level.
Future direction: Community‑level studies Since
bees are often sampled as a community, where
the relative abundance of different species is of
interest, there is a need for continued work vali-
dating the assumption of equal detection prob-
abilities that underlies community sampling
methods. Our case study was limited in scope due
to pandemic restrictions, but nevertheless dem-
onstrates that community-level mark-recapture
is a feasible goal: With two people working for
15 days in the field, we obtained 22 population
estimates for four taxa. To our knowledge, this
is the first example of a mark-recapture study in
which separate population estimates were gener-
ated for multiple, unrelated bee species. A full-
scale project could use similar approaches to
test the performance of index sampling methods
across habitats, taxa, and seasons.
13
10 Page 20 of 24 E. L. BRIGGS et al.
Future direction: Mark‑recapture models Valid-
ity of mark-recapture estimates depends on meet-
ing model assumptions, and future work on bees
will benefit from explicit tests of assumptions in
the field, and GOF tests at the analysis stage. We
note that our GOF tests included model sets that
contained models ­M0, ­Mb, and ­Mt, but ­Mh was
included on only two occasions. Our inability to
fit ­Mh suggests that larger capture/recapture sam-
ples were required to fit the model (Link 2004).
There is also a need to quantify the rate of mark
loss in the field, the effects of marking on bee
survival and behavior in the field, and, for open
population models, to assess the age-dependent
mortality of study species. We outlined several
approaches to these knowledge gaps, which
should be a priority in future mark-recapture
work on bees.
Among established models, the CAPTURE
models for closed populations, as well as Jolly-
Seber and Manly-Parr models for open popula-
tions, are sound choices for many bee studies;
older models that lack GOF tests will rarely be
as useful. However, bee research has not yet
used the full range of mark-recapture models
that may be appropriate to these taxa. Although
a few bumble bee studies have begun to take a
landscape-scale approach in their analyses of
abundance and movement (Mola et al. 2020a, b),
there is a need to develop and implement spatial
mark-recapture models for bees. Similarly, the
so-called robust design that incorporates both
open and closed population models may be par-
ticularly relevant for bee studies, where popula-
tions may function as closed over short periods
of a few days but are open over typical intersam-
ple periods of weeks to months.
8.2. Conclusion
In non-bee taxa, such as mammals and terres-
trial invertebrates, the need to validate popula-
tion indices has been recognized and addressed
at least since the 1970s (McKelvey & Pearson
2001; Topping & Sunderland 1992). Despite a
rapidly growing global interest in assessing and
13
monitoring bee populations, and strong circum-
stantial evidence of bias in current sampling
methods (Packer & Darla-West 2021; Portman
et al. 2020; Prendergast & Hogendoorn 2021;
but see Saunders et al. 2021), bee research has
yet to fully tackle this issue. Numerous studies
have compared different index sampling meth-
ods to one another and found that they differ,
but the biases of each method are impossible to
quantify without comparison to estimates of the
underlying populations that account for detec-
tion probabilities. The resulting uncertainty hin-
ders attempts to demonstrate how bee abundance
and community composition shift as a result of
environmental change. Although limitations of
mark-recapture methods in studies of bees (labor
intensiveness, limited species identification)
mean that they will never fully replace other
sampling methods, they do provide a feasible
way to monitor selected species and to measure
the performance of other sampling methods.
SUPPLEMENTARY INFORMATION
The online version contains supplementary material
available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 13592-0​ 22-0​ 0919-4.
ACKNOWLEDGEMENTS 
Henry Ritterpusch assisted with data collection in the
field.
AUTHOR CONTRIBUTION 
E.B. and E.Y. conducted the literature review. E.B., E.Y.,
and G.G. designed the field study. C.B., O.M.S., and G.G.
selected field sites. E.B., C.B., and O.M.S. collected field
data. E.B., J.C., and E.Y. analyzed data. E.B. drafted and
revised the manuscript, and all authors reviewed and
approved the final manuscript.
FUNDING 
This work was supported in part by the USDA National
Institute of Food and Agriculture, Hatch project 1018689
to E.Y. and by North Carolina State University.
DATA AVAILABILITY 
The field datasets generated and analyzed during the cur-
rent study are available in the DRYAD repository.
 Estimating bee abundance: can mark-recapture methods validate common...
CODE AVAILABILITY  Baum KA, Wallen KE (2011) Potential bias in pan trap-
Not applicable.
DECLARATIONS  Andrenidae) studied using mark-recapture and nest
Ethics approval  Not applicable.
Consent to participate  Not applicable.
Consent for publication  Not applicable.
Competing interests  The authors declare no competing
interests.
Disclaimer  Any use of trade, firm, or product names is for
descriptive purposes only and does not imply endorsement
by the U.S. Government.
Open access  This article is licensed under a Creative
Commons Attribution 4.0 International license, which
permits use, sharing, adaptation, distribution and repro-
duction in any medium or format, as long as you give
appropriate credit to the original author(s) and the source,
provide a link to the creative commons licence, and indi-
cate if changes were made. The images or other third party
material in this article are included in the article’s Crea-
tive Commons licence, unless indicated otherwise in a
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the article’s Creative Commons licence and your intended
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permitted use, you will need to obtain permission directly
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visit http://​creat​iveco​mmons.​Org/​licen​ses/​by/4.​0/.
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