Large Carpenter Bees as Agricultural Pollinators

Abstract

Large carpenter bees (genus Xylocopa) are wood-nesting generalist pollinators of broad geographical distribution that exhibit varying levels of sociality. Their foraging is characterized by a wide range of food plants, long season of activity, tolerance of high temperatures, and activity under low illumination levels. These traits make them attractive candidates for agricultural pollination in hot climates, particularly in greenhouses, and of night-blooming crops. Carpenter bees have demonstrated efficient pollination service in passionflower, blueberries, greenhouse tomatoes and greenhouse melons. Current challenges to the commercialization of these attempts lie in the difficulties of mass-rearing Xylocopa, and in the high levels of nectar robbing exhibited by the bees.

Full text

Hindawi Publishing Corporation
Psyche
Volume 2010, Article ID 927463, 7pages
doi:10.1155/2010/927463
Review Article
Large Carpenter Bees as Agricultural Pollinators
Tamar Keasar
Department of Science Education—Biology, University of Haifa, Oranim, Tivon 36006, Israel
Correspondence should be addressed to Tamar Keasar, tkeasar@research.haifa.ac.il
Received 12 September 2009; Accepted 9 January 2010
Academic Editor: Claus Rasmussen
Copyright © 2010 Tamar Keasar. This is an open access article distributed under the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Large carpenter bees (genus Xylocopa) are wood-nesting generalist pollinators of broad geographical distribution that exhibit
varying levels of sociality. Their foraging is characterized by a wide range of food plants, long season of activity, tolerance of high
temperatures, and activity under low illumination levels. These traits make them attractive candidates for agricultural pollination
in hot climates, particularly in greenhouses, and of night-blooming crops. Carpenter bees have demonstrated efficient pollination
service in passionflower, blueberries, greenhouse tomatoes and greenhouse melons. Current challenges to the commercialization
of these attempts lie in the difficulties of mass-rearing Xylocopa, and in the high levels of nectar robbing exhibited by the bees.
1.TheRoleofNon-ApisBeesin
Agricultural Pollination
Insect pollination of agricultural crops is a critical ecosystem
service. Fruit, vegetable or seed production from 87 of
the 115 leading global food crops depends upon animal
pollination [1]. The value of insect pollination for worldwide
agricultural production is estimated at C153 billion, which
represents 9.5% of the value of the world agricultural
production used for human food in 2005 [2]. The area
cultivated with pollinator-dependent crops has increased
disproportionately over the last decades, suggesting that the
need for pollination services will greatly increase in the near
future [3]. This contributes to the concern to beekeepers,
growers of insect-pollinated crops, and policy-makers over
recent widespread declines in honey bee populations (Colony
Collapse Disorder) [4–6].
Wild and domesticated non-Apis bees effectively comple-
ment honey bee pollination in many crops [7,8]. Examples
of management of non-Apis species for agricultural polli-
nation include the use of bumble bees, primarily for the
pollination of greenhouse tomatoes, the solitary bees Nomia
and Osmia for the pollination of orchard crops, Megachile for
alfalfa pollination, and social stingless bees to pollinate coffee
and other crops [9–12].
This paper focuses on the large cosmopolitan genus
Xylocopa as an additional provider of agricultural pollination
services. Aspects of these bees’ life-history, social organiza-
tion, and foraging ecology are discussed in the context of
their potential role as crop pollination agents.
2. The Biology and Life History of
Carpenter Bees
Large carpenter bees belong to the tribe Xylocopini within
the subfamily Xylocopinae (Hymenoptera: Apidae). They
are currently grouped into a single genus, Xylocopa [13].
The genus comprises at least three clades [14] and ca. 470
species [15]. Carpenter bees occur in tropical and subtropical
habitats around the world, and occasionally in temperate
areas [16]. Biogeographical analyses suggest that the genus
probably has an Oriental-Palaearctic origin, and that its
present world distribution results mainly from independent
dispersal events [14].
As implied by their name, carpenter bees dig their nests in
dead or decaying wood, except for the subgenus Proxylocopa
that nests in the soil [17]. The wood-nesting carpenter bees
construct two main types of nests: (i) unbranched (also
called linear), with tunnels extending in either one or both
directions from the nest entrance. Linear nests are usually
constructed in hollow or soft-centered plant material, such as
reeds; (ii) branched nests (>2 tunnels), usually constructed
in tree trunks or timber [18]. The type of nest constructed
usually varies with species, but some species show plasticity

2Psyche
in nest architecture, depending on the nesting substrate
available to them [19]. The nesting female lays one or a few
eggs along a tunnel during a brood cycle, provisions them,
and constructs partitions of masticated wood to separate
the offspring from one another. Maternal care in carpenter
bees also involves guarding of the immature offspring and
feeding of the newly matured ones by trophallaxis [20–22].
In some species, helper females participate in offspring care
rather than nesting independently, thus nesting can be social
(see below). Some species are univoltine, whereas others
produce more than one brood per year [19]. The activity
season of carpenter bees spans 8–12 months, depending on
species (e.g., [21,23–25]). Carpenter bees in temperate areas
hibernate during the cold season [19,26], but emerge to
forage on warm winter days [21,23].
The mating behavior of carpenter bees has been
described for 38 species belonging to 16 subgenera [27].
Variation in mating strategies among subgenera has been
recorded. In some subgenera, males search for females at
nesting sites, flowers, or landmarks (non-territoriality). In
others, they monopolize resources used by females, such
as flowers or nesting sites (resource-based territoriality).
Males may also monopolize areas lacking resources for
females (non-resource-based territories, or leks) [18,28]. A
phylogenetic analysis suggests that resource defense is the
ancestral state, and that this mating system is correlated with
low color dimorphism between males and females and a
small size of the mesosomal pheromonal gland [27].
Territorial males chase away intruding males [28,29],
which they identify by sight and by the odor emitted from
the intruders’ mandibular glands [30]. They also use a
pheromone secreted from their mandibular gland to mark
their territory [30]. When females enter the territories, males
follow and try to mount them [28,31]. Observations of
copulations in carpenter bees are extremely rare [28]and
were recorded only for a handful of species. In X. varipuncta,
matings take place in the non-resource territories [32], while
in X. sulcatipes and X. flavorufa, they occur at high elevation
during flight [21,31,33].
3. Social Organization
Sociality, involving non egg-laying guard bees and a domi-
nant egg-laying forager, has been described for ten species
of Xylocopa. In nests of the African species X. combusta,
first eclosing daughters remain in their natal nests and
perform guarding duties while their mothers produce a
second brood ([34]cf. [22]). Similarly, in nests of X.
pubescens sociality generally occurs after the emergence of
the young, where either the mother is the reproductive and
a daughter guards or vice versa [20,35]. Matrifilial nests of
X. virginica (comprised of a mother and her daughters) also
show reproductive skew, and guarding individuals become
reproductive in the following year. In these nests, the mother
performs all nest maintenance, foraging, cell preparation
and oviposition, whereas the younger inactive females only
perform guarding duties [36]. Nests of X. sulcatipes can
be matrifilial, composed of sisters, or involve the joining
of unrelated females [21,37]. Some X. sulcatipes nests are
initially quasisocial (no reproductive division of labor), but
after a brief period of reproductive competition involving
oophagy, a division of labor is usually established. Eventually
most nests contain one reproductive and a guard [38].
The helping role of female offspring has been suggested to
promote greater maternal investment in daughters than in
sons, leading to the female-biased sex ratio recorded in X.
sulcatipes [37]. In both X. pubescens and X. sulcatipes, the
reproductive females produce 100% of the offspring while
the guards produce none [39].
Nests of X. sonorina also exhibit high reproductive
skew, where the forager (mother) reproduces and feeds
nestmates via trophallaxis, and additional females (daughters
and/or joiners) share guarding duties [40]. For X. frontalis,
X. grisescens, and X. suspecta matrifilial, semisocial, and
communal nests have been recorded [41]. Genetic analysis
of X. aeratus and X. bombylans, which form multi-female
nests during part of the breeding season, indicated the
presence of multiple matrilines in approximately 50% of
nests. Socially nesting females were frequently sisters in one
of the populations studied, and were often unrelated in a
second population. The results also indicated that temporary
high reproductive skew occurred in multi-female nests, that
is, that different females were reproductive during different
parts of the season [22].
Several ecological and life-history variables were sug-
gested to promote social nesting in carpenter bees. Social
living was found to correlate with late season [42]andolder
age [35]inX. pubescens, possibly because matrifilial nesting
only occurs when mothers produce their second brood. Nest
structure was proposed as an additional factor that affects
social organization: in some species, females in branched
nests build and provision separate tunnels at the same time,
which can result in a communal social organization. In
other species, females construct one tunnel for the first
brood generation and only construct a new tunnel after the
first brood has reached maturity. This can then result in
eusocial nesting, where the daughters of the first generation
assist their mother in building and provisioning subsequent
tunnels [19]. Finally, a period of reproductive inactivity of
mature offspring was proposed as a transition step toward
social living. Such a period occurs in some solitary species
(such as X. frontalis and X. grisescens), where newly emerged
adult females remain in their natal nest for 20–30 days.
During this time, they are provisioned by their mother or
by their oldest sister, if the mother is absent. In some species,
this association becomes permanent in a fraction of the nests
(e.g., in X. suspecta [25]), which then become social.
Improved defense against parasites and predators has
been suggested to favor the evolution of social nesting in bees
(e.g., [43]). Carpenter bee nests are attacked by several types
of natural enemies, including parasitoid wasps and flies,
predatory wasps, ants, termites, and insectivorous birds [21,
44]. However, in X. pubescens, the frequency of parasitism did
not differ between social and solitary nests [45]. Thus the role
of guards in reducing nest parasitism is not supported so far.
The most extensive work on the consequences of sociality
has been carried out for X. pubescens. In this species, the

Psyche 3
frequency of social nesting increases as the reproductive
season progresses. It has been suggested that this increase
has evolutionarily been imposed on females by shortage in
nesting sites [20]. Social nesters spend more time foraging
outside their nests as compared with solitary individuals,
perhaps because the presence of the guard in the nest
reduces the risk of prolonged foraging [46]. Social nesters
also suffer fewer nest takeovers by intruders than solitary
nesters, providing a possible benefit for social nesting when
competition for nests is high. The guards, in turn, may
benefit from increased indirect fitness (if related to the
reproductive), and increase their chances of eventually taking
over the nest [46]. Thus, social organization can affect the
fitness of X. pubescens females. Social and solitary nesters
that foraged within a greenhouse differed in their food-plant
preferences. Social females directed more of their foraging
to a pollen source (Portulaca oleracea) than solitary nesters,
possibly because of their higher brood production rates [47].
4. Foraging Ecology
4.1. Abiotic Requirements for Foraging. Carpenter bees toler-
ate high ambient temperatures during foraging, and most
species are inactive at low temperatures. For example, the
lower activity temperature thresholds are 23◦CforX. capitata
[48], 21◦CforX. sulcatipes, and 18◦CforX. pubescens [21].
Flower visit rates in X. olivieri are highest at a combination
of high (25–35◦C) temperatures and low (1–100 Lux) illu-
mination levels [17]. X. arizonensis individuals that foraged
on Agave schottii together with honey bees and bumble
bees were active mainly during the late morning hours,
whilehoneybeesandbumblebeesweremorecrepuscular.
Thesepatternsweresuggestedtoreflectlowcompetitive
ability, together with high thermal tolerance, in the carpenter
bees [49]. X. varipuncta maintains flight activity within
an ambient temperature range of 12–40◦C[50]. This heat
tolerance suggests good heat regulation ability in carpenter
bees, possibly controlled by a thermoregulatory center in the
prothorax [51].
The activity period of some species, for example, X.
sulcatipes, X.cearensis, and X. ordinaria, spans most of
the daylight hours [21,52,53]. In other species (such as
X. pubescens, X. tabaniformis,andX. olivieri), activity is
crepuscular [17,21,54,55]. A few species are nocturnal:
X. tenuiscapa forages on its pollen host on moonless nights
[56], and X. tranquebarica [57] has been observed foraging
on moonlit nights.
4.2. Water Balance. Carpenter bees often ingest excess water
during nectar foraging. Analysis of nectar consumed by X.
capitata showed that it is very concentrated. Nevertheless,
their hemolymph is only moderately concentrated, and their
urine is very dilute. This suggests that ions, rather than water,
may be limiting for carpenter bees [58]. This hypothesis
is supported by the observation that bees often excrete
water before and during flight, and that they often engage
in water evaporation from ingested nectar [59]. A similar
excess of water ingestion, which leads to copious excretion
and evaporation of water, was described for X. pubescens
foraging on the nectar of Callotropis. On the other hand,
physiological water requirements are finely balanced with the
water contents of Callotropis nectar in the sympatric species
X. sulcatipes, possibly due to extended coevolution with this
plant [59].
4.3. Nectar Robbing. Nectar-foraging carpenter bees often
perforate the corollas of long-tubed flowers, and thereby
reach the nectaries without contact with the anthers. Such
“illegitimate pollination” or “nectar theft” has been reported
for X. virginica and X. micans foraging on blueberries. Nectar
robbing in blueberries may reach 100% of the visits [60]and
significantly reduces fruit set and seed number as compared
with plants visited by honey bees ([61], but see [62]). Nectar
robbing by carpenter bees has also been observed in the wild
plants Petrocoptis grandiflora [63], Fouquieria splendens [64],
Glechoma longituba [65], and Duranta erecta [66]. Corolla
tube perforation contributed to the reproductive success
of the plants in P. g r a n di fl ora and F. splend e ns, indicating
that the nectar robbers were dusted with pollen during
foraging, and functioned as pollinators. In G. longituba and
D. erecta, on the other hand, nectar robbing by carpenter
bees reduced seed set, as compared with plants visited by
legitimate pollinators [63–66].
4.4. Food Sources. Carpenter bees in natural habitats are
generalist nectar and pollen foragers. For example, foraging
X. cearensis were recorded from 43 plant species in Bahia,
Brazil [52], while X. latipes and X. pubescens foraged on 30
species in India [67]; In Israel, X. pubescens and X. sulcatipes
used 61 species as forage plants [21]; X. darwini in the Pacific
is known to visit the flowers of 79 plant species [29]; 28 plant
species provide nectar and pollen for X. ordinaria in Brazil
[53].
Carpenter bees can also be trained to collect sucrose
solution from feeders in experimental settings. In laboratory
experiments, X. micans were able to discriminate between
sucrose solutions that differed in mean volume (1 versus 3
microliter) and concentration (10% versus 30%). They were
indifferent to variability in both nectar volume and nectar
sugar concentrations. This risk indifference was recorded if
the bees were fed or starved [68].
5. Crop Plants That Are Pollinated by
Carpenter Bees
Carpenter bees pollinate passionflower (Passiflora spp.)in
their native habitats [69] and in commercial agricultural
settings [70–73]. They provide better pollination service
than honey bees for this crop [71]. Xylocopa subgenus
Lestis has been successfully reared in greenhouses for tomato
pollination in Australia. Their foraging activity led to an
increase in tomato weight by 10% relative to a combination
of wind and insect pollination. The efficiency of carpenter
bees in pollinating tomatoes is increased by their ability to
buzz the anthers [9]. In a pilot study in Israel, the fruit
set of greenhouse-grown honeydew melons was three times

4Psyche
higher when pollinated by X. pubescens compared to honey
bee pollination [74]. Social and solitary nesters had similar
efficiency in pollinating this crop: they did not differ in the
daily activity patterns and flower visitation rates. Pollination
by both types of nesters led to similar fruit sets, fruit mass,
and fruit seed number [47].
Carpenter bees are important pollinators of cotton in
Pakistan, India, and Egypt [33]. X. varipuncta is compared
favorably with honey bees (Apis mellifera) as pollinators of
male-sterile cotton in field cages in the USA [75]. However,
X. pubescens in Israel did not provide satisfactory pollination
of cotton for hybrid seed production (D. Weil, personal
communication). Finally, the night-flowering cactus Cereus
repandus (syn. C. peruvianus) is pollinated by X. pubescens in
Israel [76].
6. Domestication and Mass Rearing of
Carpenter Bees for Agricultural Pollination
A major obstacle to the commercial use of native pollinators
in agriculture is the need to mass-rear them, rather than col-
lect them from nature. Devising efficient and cost-effective
mass-rearing protocols for X. pubescens is a necessary step
in this direction. Attempts to mass-rear carpenter bees
have focused on the construction of nest boxes that are
placed in natural habitats to enhance nesting success. Skaife
[77] constructed observation nests of bamboo tubes and
transferred hibernating X. caffra into them. Most of the
females remained in these nests after they exited hibernation.
Oliviera and Freitas [78] designed and tested nest boxes
for X. frontalis, based on the general design of Langstroth
honey bee hives. Each of nine wooden frames in these
boxes was modified to serve as an independent Xylocopa
nest. Colonization rates of these boxes ranged from 19% to
52%, and the proportion of males in the emerging brood
was 0.38. Efforts to develop protocols for captive mating
and rearing of carpenter bees have so far met with limited
success (unpublished results). The endocrine and molecular
pathways that underlie reproduction in carpenter bees are
yet unknown. Elucidation of these pathways will help
identify the bottlenecks in the bees’ reproduction, which may
include overwintering of adults, mating, sperm storage and
choice, nest construction and/or brood care. Information on
the potential reproductive pitfalls, and their physiological
mechanisms, is expected to facilitate the development of
effective captive breeding methods for Xylocopa.
7. Conclusions and Future Prospects
Carpenter bees possess several advantages as potential crop
pollinators compared to other non-Apis bees. Many solitary
bees have a short activity season and/or are specialist
foragers, and therefore do not provide a broad alternative
to honey bee pollination. Carpenter bees, on the other
hand, have long activity seasons and feed on a wide range
of plant species. In addition, they are capable of buzz-
pollination. This makes them potentially more versatile as
agricultural pollinators. Hibernation occurs in the adult
stage, and females start foraging whenever temperatures
reach high enough values. This means that it is relatively easy
to manipulate the onset of foraging in greenhouses. Another
important advantage is that the genus has a worldwide
distribution. This implies that local species of Xylocopa can
potentially be used over wide areas, reducing the need to
import exotic pollinators. The possibility to lure these bees
into suitable artificial nesting material allows provisioning
of nesting material that can be easily used in agricultural
settings and moved to places where pollination services are
needed [79].
In spite of higher per-capita pollination efficiency in
some crops, carpenter bees are clearly inferior to honey bees
in terms of pollinator work force, as they do not form large
nests. Therefore they are expected to contribute most to crop
pollination when honey bees are ineffective. For example, the
high termoregulatory ability of carpenter bees enables them
to forage at higher ambient temperatures than honey bees.
This makes them attractive candidates as pollinators in hot
areas and in hot microclimates, such as in glass houses. The
crepuscular and nocturnal activity of some species may also
allow them to pollinate night-flowering crops, which are not
visited by honey bees.
Several problems remain in the management of carpenter
bees for crop pollination, which call for further research.
Most important is the need to develop an efficient captive
breeding program for carpenter bees, which would include
controlled selection of genotypes, mating, and nest founding.
Such protocols have already been developed for other non-
Apis pollinators, such as Osmia lignaria [80]andOsmia
cornuta [81]. They include guidelines for nest construction
and placement, overwintering and transportation of the bees.
A complementary challenge is to enhance reproduction of
wild Xylocopa populations, through provisioning of nesting
material to their natural habitat. The availability of nesting
resources was shown to correlate with the community struc-
ture of wild bees [82]. Moreover, experimental enhancement
of nest site availability has led to dramatic increases in wild
populations of Osmia rufa [83]. These findings suggest that
Xylocopa populations, and the pollination services they pro-
vide, may also benefit from nest site enhancement in agro-
ecosystems. Additional information about the pathogens and
parasites of the genus is needed as well [84]. A combination
of ecological, physiological, and molecular genetic studies is
likely to provide these essential data.
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