Annual Review of Entomology

Stingless Bee (Apidae: Apinae:

Meliponini) Ecology
David W. Roubik
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Smithsonian Tropical Research Institute, Balboa, Republic of Panamá; email: [email protected]

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Annu. Rev. Entomol. 2023. 68:231–56 Keywords

First published as a Review in Advance on
bee-keeping, honey, pollen, social bees, resin, tropics
October 5, 2022

The Annual Review of Entomology is online at Abstract

ento.annualreviews.org
Stingless bees form perennial colonies of honey-making insects. The >600
https://doi.org/10.1146/annurev-ento-120120-
species of stingless bees, mainly Neotropical, live throughout tropical
103938
latitudes. Foragers influence floral biology, plant reproduction, microbe dis-
This work is licensed under a Creative Commons
persal, and diverse ecosystem functions. As tropical forest residents since
Attribution 4.0 International License, which permits
unrestricted use, distribution, and reproduction in the upper Cretaceous, they have had a long evolutionary history without
any medium, provided the original author and competition from honey bees. Most stingless bees are smaller than any Apis
source are credited. See credit lines of images or
species and recruit nest mates to resources, while their defense strategies
other third-party material in this article for license
information. exclude stinging behavior but incorporate biting. Stingless bees have di-
versified ecologically; excel in nesting site selection and mutualisms with
plants, arthropods, and microbes; and display opportunism, including co-
opting plant defenses. As their biology becomes better known, applications
to human endeavors are imposing selective pressures from exploitation and
approaches to conservation that entail colony extraction from wildlands. Al-
though some meliponines can adjust to new conditions, their populations
shall require tropical diversity for survival and reproduction.

231
 There is a whole new world awaiting the person who determines what individuals actually do and what
intrapopulation variation there is in these characteristics. Such a study must, however, take great care
to distinguish between the environmental cues used and the selective pressures that led to a phenotype
that would respond to those cues.
—D. H. Janzen (68, p. 1)

1. INTRODUCTION
It has long been thought that Cretaceous meliponines were the first honey-bees, and they recruited
nest mates to flowers; their queens could not fly after fertilization, and neither the queen nor
worker caste had a stinger (see the sidebar titled Noteworthy Stingless Bee Attributes). All of
this may be true, but such assertions currently lack an evolutionary chronology. Like the tropical
plants that Janzen (68) ecologizes, much remains to be learned about stingless bee (SB) biology,
ecology, and evolution (174). My goal in this review is to synthesize the ecology and evolution of
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SBs. Readers interested in behavior or taxonomy are referred to References 51, 58, 94, 146, and
174, and those interested in pollination biology to References 136, 152, and 168.
Characterization of the more than 600 species of SBs across the tropics is not easy. How-
ever, their colonies are in many ways like trees in tropical forests, where ecological interactions
daily unfold. Placed within their communities, a queen may live for a year, a worker or male may
live for weeks or months, and a colony can last for decades (58, 138, 170). In Cretaceous times,
90 million years ago (mya) (51, 125), one might suppose that SBs sometimes used dinosaur tears,
recruiting nestmates to amino acids and nutrients as tiny Asian Meliponini do today (8, 9). The
Chicxulub asteroid impact curbed plant photosynthesis and flowering. It removed the dinosaurs,
but SB evolution continued apace. Some now forage on vertebrate sweat, motivated by a lack
of salt in their diet of honeydew from Hemiptera or by sodium scarcity (42, 44, 75, 137, 140)
(Figure 1h). There are also some unsavory habits of SBs in resource selection (Section 5.1). An
ancient origin of such traits is a distinct possibility.
Comparisons between SBs and honey bees (HBs) in terms of, e.g., microbial ecology (13,
74, 76, 78; JG Kueneman, E Bonadies, D Thomas, DW Roubik, and WT Wcislo, unpublished
manuscript), nestmate recruitment to resources (28, 58, 91, 117, 120, 123, 133, 149, 171, 172),
floral preferences (54, 57, 60, 72, 81, 116, 118, 122, 129, 133, 139, 142), or colony defense (58, 59,

NOTEWORTHY STINGLESS BEE ATTRIBUTES

1. Relatively small, stingless workers (2–15 mm)
2. Pantropical distribution, nesting predominantly in living trees, sometimes in subterranean cavities or
exposed on branches or cliffs; rarely in ant or termite nests
3. Small, medium, and large colonies (100–10,000+ individuals)
4. Infrequent, directed swarming with preparation of a new nest site by the female parent colony prior to
departure of the swarm—workers and a new (flight-capable) queen, who mates there
5. Queens are physogastric when gravid; cannot fly; and, like workers, lack a stinger
6. Males forage and are self-supporting
7. Stored honey and pollen are often highly acidic
8. Foragers recruit nestmates to resources, mediated by intra- and extranidal communication
9. In-nest mixing of self-secreted wax and saliva with collected resin create cerumen used to build containers
for food and broods in diverse architecture

232 Roubik
 a b c d

e
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f g h i

Figure 1
(a) Melipona fallax worker foraging building material from fruit of Coussapoa, forming the nest entrance with its seeds and waxy material,
thus allowing the hemiepiphyte plant to grow on the bee nest tree. (b) Tetragonula worker foraging resin from fruit of Corymbia,
dispersing seeds in flight and depositing resin and seeds around the nest entrance. (c) Hammerhead woodpecker (Dryocopus) predating
ants and nesting Plebeia (Nanoplebeia) sp. living with hemipteran Cryptostigma females in hollow internodes of living Cecropia, showing an
internal nest entrance ring made of resin and resin deposit, brood cells, and pollen storage pots. (d) Inside a nest of Plebeia (Nanoplebeia),
showing three workers taking honeydew from large female Cryptostigma sp. (Hemiptera: Coccidae), a worker removing wax strands
from a smaller female, females and crawlers in the nest, and brood cells. (e) Trigona fuscipennis worker chewing buds of Brownea to
remove nesting material. ( f ) Melipona fallax buzz-foraging Miconia and covered with its pollen. (g) Double nest entrance tube of
Tetragonisca angustula made of flexible cerumen. (h) Plebeia (Nanoplebeia) spp. foraging sweat on the author’s hand. (i) Plebeia (Nanoplebeia)
franki worker guarding its nest entrance tube made of firm resin-cerumen. Drawings courtesy of F. Gattesco from photos by the author
and inspired by the book by T. A. Heard (63).

173) reveal similarities and differences, explored below. Competition for resources is important
(37, 75, 121, 124, 130, 170). Molecular phylogenetic analysis (13, 86, 123, 125) indicates that SBs
coalesced from the same ancestral lineage as Apis, but SBs are twice the age of Apis and not direct
ancestors. In both SBs and HBs, stored food and brood attract natural enemies of all kinds (58,
131, 139) (Tables 1 and 2; see the sidebar titled Examples of Stingless Bee Natural Enemies).
There is evidence that, compared to HBs, SBs became better at biting or sheltering in place.
SBs are frequently opportunists and mutualists. In addition, the appearance of HBs as constant
competitors—within the last 400 years in the Americas and Australia due to human activity (93,
149) but since 40 mya in the Old World—helped to shape SB evolution. Intensified agriculture and
the exploitation of SBs for materials and pollination underscore that humans can also influence
SB ecology and evolution.

2. COLONY LIFE AND COMMUNITY ORGANIZATION

SB colonies cannot move. Populations are viscous, and forests contain many SB nests per hectare
(26, 50, 58, 66, 70, 139). When a colony does reproduce, it is via a single drone or a singly mated
www.annualreviews.org • Understanding the Stingless Bees 233
 Table 1 Arthropod natural enemies of stingless bees
Order Genus and species Family Region and prey or host
Hymenoptera Bembix flava Bembicidae Australia; male Tetragonula
Hymenoptera Bembix tuberculiventris Bembicidae Australia; Tetragonula, Austroplebeia
Hymenoptera Oecophylla smaragdina Formicidae Asia; stingless bees
Hymenoptera Eciton spp. Formicidae Neotropics; Melipona, etc.
Hemiptera Apiomerus Reduviidae Neotropics; Melipona, etc.
Hymenoptera Neivamyrmex Formicidae Neotropics; Plebeia, etc.
Hymenoptera Syntretus trigonaphagus Braconidae Australia; Tetragonula
Diptera Melaloncha Phoridae Neotropics; Cephalotrigona, Scaptotrigona, etc.
Diptera Pseudohypocera kerteszi Phoridae Neotropics; many host genera
Diptera Dohrniphora trigonae Phoridae Australia; Tetragonula
Diptera Ceriana ornata Syrphidae Australia; Tetragonula, Austroplebeia
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Diptera Hermetia illucens Stratiomyidae Neotropics, invasive; general

Coleoptera Aethina tumida Nitidulidae Africa, invasive; Dactylurina, Meliponula, general
Acari Pyemotes tritici Pyemotidae Neotropics; Frieseomelitta, Tetragoniscaa
Coleoptera Haptoncus luteolus Nitidulidae Asia; stingless bees
Coleoptera Procoryphaeus wallacei Histeridae Asia; stingless bees
Coleoptera Cleidostethus meliponae Cucujidae Africa; stingless bees
Hymenoptera Lestrimelitta (20+ spp.) Apidae Neotropics; Scaptotrigona, Melipona, Plebeia, others
Hymenoptera Liotrigona (Cleptotrigona) cubiceps Apidae Africa; stingless bees

a
Management issue.
Data taken from References 58, 63, and 133 and the author’s personal observations.

queen. When two such individuals succeed, Darwinian fitness is equal to 1; the little field data
available indicate that colonies may require two decades to replace themselves (57, 67). Most im-
portant, workers always prepare a preswarming nest site (17, 117, 138, 170), a behavior dubbed
directed swarming in this review. Although not assured success, the queen and daughter colonies
are thereby given food, shelter, and a direct route to security from the mother nest. The new queen
mates with one male near that new nest. After its formation, a daughter colony may take resources
from the mother colony (170, 174), but documentation of the process is meager. Males of multi-
ple colonies (21) compete for mating opportunities near nests, resulting from queen mortality or
colony foundation. The males seem better suited to locating mating sites than females, although
females share similar flight capability (65, 103, 154). The presumptive benefit of farther or more
male flights is to minimize risks undergone by exposed virgin queens. Males can forage and shel-
ter far from natal nests and also enter other nests (58). In concert, single mating and directed
swarming promote local selection and adaptation by SB colonies.
Nuanced dynamics within colonies reduce inbreeding and maintain genetic diversity. A flight-
less gravid queen has mated only once and cannot disperse, and she or her offspring may be rejected
or replaced (170); males are sometimes the offspring of workers (164, 170). Furthermore, males
and workers can be the offspring of a mated queen from another nest (164). A newly fertilized
queen, prior to becoming gravid and unable to fly, may be accepted by a queenless colony—as has
been observed among Neotropical Melipona in meliponaries, the SB equivalent to an apiary.
Strict nesting site and dispersal limitations are exemplified in the widespread Neotropical
species Trigona fulviventris, which has been researched in large study plots of dry forest in Costa
Rica and moist forest in Panama (66, 142). Colonies nest underground at the bases of large trees
within immense egg-shaped nodules of resin (142). Colonies were found to be overdispersed

234 Roubik
 Table 2 Supraspecific stingless bee groups (genus or subgenus) and associated microbes, studied using laboratory
cultures or RNA amplicon techniques
Stingless bee Microbe(s) Reference(s)
Neotropical
Asperplebeiaa NA NA
Cephalotrigonaa,b NA NA
Duckeolaa,b NA NA
Friesellaa,b NA NA
Frieseomelittaa,b,c Bifidobacterium 33, 92; JG Kueneman, E Bonadies, D Thomas, DW Roubik, and
Lactobacillus WT Wcislo, unpublished manuscript
Starmarella
Geotrigonaa,b,c NA NA
Lestrimelittaa,b NA NA
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Meliponaa,b,c
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Acute paralysis virus 10, 13, 17, 23, 33, 90–92, 96, 109; JG Kueneman, E Bonadies,
Deformed wing virus D Thomas, DW Roubik, and WT Wcislo, unpublished
Bacillus manuscript
Bifidobacterium
Crithidia
Lactobacillus
Melissococcus
Micromonospora
Paenibacillus
Snodgrassella
Streptomyces
Aspergillis
Candida
Curvularia
Monascus
Monila
Nigrospora
Penicillium
Starmarella
Talaromyces
Trichoderma
Meliwilleaa,b NA NA
Nannotrigonaa,b,c Acute paralysis virus 17, 33; JG Kueneman, E Bonadies, D Thomas, DW Roubik, and
Deformed wing virus WT Wcislo, unpublished manuscript
Black queen cell virus
Lactobacillus
Nogueirapisa,b NA NA
Oxytrigonaa,b,c Bifidobacterium 92; JG Kueneman, E Bonadies, D Thomas, DW Roubik, and WT
Lactobacillus Wcislo, unpublished manuscript
Paratrigonaa,b,c Kodamaea 33, 165
Metschnikowia
Paratrigonoidesa,b NA NA
(Continued)

www.annualreviews.org • Understanding the Stingless Bees 235

 Table 2 (Continued)
Stingless bee Microbe(s) Reference(s)
Partamonaa,b,c Bifidobacterium 23, 76, 92; JG Kueneman, E Bonadies, D Thomas, DW Roubik,
Gilliamella and WT Wcislo, unpublished manuscript
Lactobacillus
Snodgrassella
Plebeiaa,b,c Bifidobacterium 13, 33, 92, 165; JG Kueneman, E Bonadies, D Thomas, DW
Lactobacillus Roubik, and WT Wcislo, unpublished manuscript
Candida
Metschnikowia
Plectoplebeiaa NA NA
Ptilotrigonaa,b,c Candida 13, 33, 92
Scaptotrigonaa,b,c Bacillus 13, 33, 92, 96, 109, 165; JG Kueneman, E Bonadies, D Thomas,
Bifidobacterium DW Roubik, and WT Wcislo, unpublished manuscript
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Lactobacillus
Candida
Kodamaea
Metschnikowia
Monascus
Zygosaccharomyces
Scaurab NA NA
Schwarzulab NA NA
Tetragonaa,b,c Acute paralysis virus 17, 33, 76, 92, 165; JG Kueneman, E Bonadies, D Thomas, DW
Deformed wing virus Roubik, and WT Wcislo, unpublished manuscript
Black queen cell virus
Bifidobacterium
Gilliamella
Lactobacillus
Kodamaea
Tetragoniscaa,b,c Acute paralysis virus 13, 17, 23, 33, 90–92, 165; JG Kueneman, E Bonadies, D Thomas,
Deformed wing virus DW Roubik, and WT Wcislo, unpublished manuscript
Black queen cell virus
Snodgrassella
Streptomyces
Aspergillis
Candida
Curvularia
Fusarium
Metschnikowia
Monila
Mucor
Nigrospora
Starmarella
Trichoderma
Trichotrigonaa,b Lactobacillus JG Kueneman, E Bonadies, D Thomas, DW Roubik, and WT
Wcislo, unpublished manuscript
(Continued)

236 Roubik
 Table 2 (Continued)
Stingless bee Microbe(s) Reference(s)
Trigonab,c Bacillus 13, 23, 33, 76, 91, 92, 96, 105, 109; JG Kueneman, E Bonadies, D
Bifidobacterium Thomas, DW Roubik, and WT Wcislo, unpublished manuscript
Gilliamella
Lactobacillus
Snodgrassella
Curvularia
Rhizopus
Starmarella
Trigoniscab NA NA
Aphaneuraa NA NA
Leurotrigonaa,b NA NA
Melikerriaa,b,c NA NA
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Michmeliaa,b,c NA NA
Mourellaa,b NA NA
Necrotrigonaa,c NA NA
Parapartamonaa,b NA NA
Schwarzianaa,b NA NA
Schwarzulab NA NA
Afrotropical
Axestotrigonaa,c Bifidobacterium 160
Lactobacillus
Dactylurinaa,c Bifidobacterium 160
Lactobacillus
Hypotrigonaa,c Bifidobacterium 160
Lactobacillus
Liotrigonaa,c Bifidobacterium 160
Lactobacillus
Meliplebeiaa,c Bifidobacterium 160
Lactobacillus
Meliponulaa,c Bifidobacterium 160
Lactobacillus
Plebeinaa,c Bifidobacterium 160
Lactobacillus
Plebiellaa NA NA
Apotrigonaa NA NA
Cleptotrigonaa NA NA
Paleo-Australian
Austroplebeiaa,c Acinetobacter 33, 96, 159
Lactobacillus
Geniotrigonaa,c NA NA
Heterotrigonaa,c Lactobacillus 33
Fructobacillus
Homotrigonaa,c NA NA
(Continued)

www.annualreviews.org • Understanding the Stingless Bees 237

 Table 2 (Continued)
Stingless bee Microbe(s) Reference(s)
Lepidotrigonaa,c Carnimonas 96, 154, 159
Escherichia-Shigella
Pseudomonas
Psychrobacter
Snodgrassella
Lisotrigonaa NA NA
Papuatrigonaa NA NA
Pariotrigonaa NA NA
Tetragonulaa,c Acinetobacter 33, 49, 91, 92, 96, 154, 159
Carnimonas
Escherichia-Shigella
Lactobacillus
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Lysinibacillus
Nosema (protozoan)
Pseudomonas
Psychrobacter
Snodgrassella
Streptomyces
Rhizopus
Wallacetrigonaa,c NA NA
Borneotrigonaa,c NA NA
Lophotrigonaa,c NA NA
Platytrigonaa,c NA NA
Sahulotrigonaa,c NA NA
Sundatrigonaa,c NA NA
Tetragonillaa,c Rhizopus 47
Tetrigonaa,c NA NA

a
Genus or subgenus name following Reference 51.
b
Genus name following Reference 20.
c
Species for which at least one study has been conducted.
Abbreviation: NA, not applicable.

(uniformly distributed) in dry forest, but in moist forest, they occurred in a straight line fol-
lowing a LiDAR-detected dry stream bed. One observed colony killed another, as sometimes
occurs between kleptoparasitic Lestrimelitta that compete for victim SB colonies (59, 139, 142).
Because 230,000 trees and 40 of the same size and species that hosted the eight T. fulviventris were

EXAMPLES OF STINGLESS BEE NATURAL ENEMIES

Many predators [such as birds (see also Figure 1c) and dragonflies, e.g., Anax] take stingless bees in flight. There
are persistent predators at nest entrances, including salticid spiders and lizards such as Tropiduras hispidus in the
Neotropics and Hemidactylus mubouia worldwide. Studies of bee defenses against these predators have seldom been
made; bee-keepers protect their hives by placing an inverted funnel collar around hive entrances. Various toads,
especially the cane toad, Rhinella, stand and consume bees at nest or hive entrances. While many invertebrates
are minor predators, the social insects and vertebrates eat far more bees or nest contents. Bears, anteaters, apes,
armadillos, civets, procyonids, pangolins, aardvarks, humans, and mustelids are among the macropredators.

238 Roubik
 scattered in the 75 ha Panama study plot, there was no tree species preference, but instead a consis-
tent topographical choice. No investigation has been made of subsoil conditions for nesting SBs,
but pre-existing cavities were essential for the populations in this study. SB nesting preferences,
resource requirements (50, 66, 70; see Section 5), and colony competition must be better known to
understand the factors that shape colony number or size per unit area, survival and reproduction,
and many other subjects.

3. DISTRIBUTION AND ABUNDANCE

The origin of SBs and the entire corbiculate (hindleg pollen-basket) clade of bumble bees, orchid
bees, SBs, and HBs was Neotropical (86); SB diversity evolved in the Neotropics over at least
80 million years (125). Deep ocean already separated Africa from South America throughout this
time, and multiple dispersal modes must have been used by SBs (58, 125). However, fewer species
live in Old World forests. There are approximately 10–20 species in all of Australia or in any single
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African or Asian tropical locale (58, 91, 138, 146).

SB richness is far greater in the Neotropics than in other regions (174). In contrast, all HBs are
Asian save one—the African lineage Apis mellifera (94, 146). Although these observations led to the
hypothesis that SB diversity is related to resource competition with HBs (133), thereby making
SB or HB geographic dominance inversely related, additional hypotheses apply.
Honey storage potentially evolved among tropical bees to reduce competition (68) and to make
it possible to hoard food (or nesting materials) to be used during scarcity. SB colonies store both
pollen and honey that can last the colony a few months (136; see Sections 4 and 5). These stores
can also allow marine dispersal of colonies via rafting. Terrestrial nesting (139) likely prevented
arrival of minute Pariotrigona or Lisotrigona in Australia from Southeast Asia (8, 9), for example,
because nests underground or among rocks cannot float. In contrast, tiny bees that had multiple
nests in floating trees or vegetation mats may well have dispersed populations while avoiding
inbreeding. Small size has been repeatedly documented in fossilized taxa (51, 58). SB diasporas
were thus often made up of tiny Meliponini a few millimeters in length. Tiny meliponines inhabit
almost all tropical forests, whereas large species are quite restricted (see below).

3.1. Comprehending Stingless Bee Global Patterns

The usual latitudinal gradient encountered with insects is higher diversity and richness in the
tropics. In contrast, bee communities and richness often show the reverse trend, largely under-
stood to be the result of perennial bees colonies—the SBs and HBs. Competitive interactions
hypothetically led to the reverse latitudinal gradient in bee species. Some middle latitudes have
more bee species per habitat than any equatorial forest, but only in the Old World do they contain
the perennial colonies of Apis. The omnipresence of bee colonies in the tropics may severely limit
bee diversity due to niche pre-emption (134, 135). A continental gradient in eusocial bee diversity
(93) also appears to be linked to competition for food and nesting resources.
Bee colonies, whether those of HBs or SBs, apparently limit general bee species richness, all
other things being equal. Yet there are additional explanations for this phenomenon (107). One
is biogeographical, considering isolation by barriers; a second is botanically driven; and a third
includes the time since colonization or divergence, as well as extinction rates. The appearance of
HBs in any part of the world would lower SB diversity and success. However, habitat disturbance
often corresponds with HB distribution by humans, and therefore the roles of different selective
factors, including interspecific competition, are often difficult to assess. There are at least 80 formal
supraspecific names applied to SBs (51), as suggested by recent inquiries. Attendant biogeographic
studies should soon follow and be used to test hypotheses.

www.annualreviews.org • Understanding the Stingless Bees 239

 3.2. Explaining the Richest Highly Eusocial Bee Communities
The skewness of SB species distribution, with 80% of the world’s species being Neotropical (5,
140), makes biogeography central to understanding SBs. Importantly, no HB is native to the New
World. The recent discovery that a western Amazon field station has almost as many SB species as
found in the entire Old World (140) underscores the diversity divide. Australia has two SB genera,
whereas there are nine in Asia, eight in Africa, and 26 in the Neotropics (51, 58) (Table 2). Isola-
tion, mountain ranges, and large arid areas have helped to create relatively depauperate SB faunas
while likely leading to the prevalence of other solitary or seasonal bees (93, 133). Considering SB
fauna by country area, Costa Rica is richest with nearly 70 species in 55,000 km2 , while India and
Australia have the lowest richness (146). Approximately 400 species occupy South America (110,
140), while another 100 occur from Mexico to Panama (18, 20, 167, 168). These subcontinents
share few species. The Old World contains approximately 120 SB species, 30 of them African. In
the most diverse SB community studied, that of the Yasuní Biosphere Reserve, Ecuador, 40% of
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the recorded 100 SB species are still unnamed, and 25% are small or tiny (140, 141).
Drought, deserts, winter, or prolonged dry seasons often thwart development of rich biotic
communities. In contrast, high floral diversity and lack of an extensive dry season best explain
the high insect biotic diversity in Amazonian and other tropical forests (12, 45, 140). SBs follow
this trend but are unique, as seen in their likely response to HB competition. In Yasuní, the lack
of a dry season and an unrivaled 3,000 native tree species, 600 vines and lianas, and 1,000 herbs
afford SBs many resource options. Evidence from 30 forest fragments in Costa Rica (15) and
in tropical Australia also suggest that plant diversity increases SB species richness (46, 71, 163);
moreover, forest degradation in equatorial Africa decreases SB species richness (73). In Yasuní,
the fact that the forest grows on low rolling hills allows light environments to vary. As known by
Kayapó tribal SB experts in central Amazonia, along with thousands of human generations in the
tropics, regenerating forest patches and varied light environments correlate with SB diversity (18,
72, 116, 140), particularly when surrounded by an older forest.

3.3. Explaining Bee Size Distributions

There is no robust analysis of bee diversity, and a distributional listing (93, 107) fails to evalu-
ate competition from perennial colonies. The richness and abundance of flower species broadly
correlate with tropical SB diversity (12), but this trend excludes extinction data. Size seems to
affect the evolution of highly eusocial bees, since the largest SB and HB workers have similar
masses (58, 134, 149, 157). Furthermore, small Apis species have similar masses to medium-sized
SBs, but most SBs are smaller than small HBs. This must reduce competition. Large SB species—
most Neotropical Melipona, some Trigona, Duckeola, Ptilotrigona, Cephalotrigona, and some African
Meliponula—evolved in environments with no HBs or with only one Apis species present. Asian
SBs are dominated by Tetragonula of varied size, but only four Asian SBs reach even medium size
(6–8 mm), similar to a small Asian Apis or small Melipona. SB and HB foraging niches and frequency
of flower visitation most likely are determined by forager size, regardless of phytochemistry, but
many research avenues are needed to assess generalization or specialization in foraging niche (see
Section 5).

4. DEFENSE STRATEGIES AND SOLUTIONS

4.1. Guards and Nest Construction
SBs can no longer sting, but they have other modes of defense (58, 139). Workers are chemically
labeled, which permits nest mate recognition and further classification by other bees (102). Why

240 Roubik
 SBs lost one of their primary lines of defense is unknown, but the tiny meliponines like contempo-
rary Plebeia, Trigonisca, Hypotrigona, Liotrigona, Lisotrigona, and Pariotrigona (Table 2) were likely
too small to manage effective stinging. Their defense strategies have thus diversified.
SBs of all sizes carefully select preformed cavities. The colonies shelter in solid constructs
including underground, in hardwood trees or lianas, or in an exposed nest on rock or wood. Nest
walls are reinforced with hard resin, bee fecal pollen exines (143), mud-clay, or pebble barriers.
Sticky resin provides glue for the colony constructs; vertebrate feces or resin deposits in the nest
are rigorously applied to invaders by Melipona and Trigona, which carry resin or mixed materials
on their hindlegs; however, these behaviors are seldom studied (58, 139, 150, 173).
Workers of species that always make exposed or vulnerable nests predictably bite intruders,
but so do roughly half of all species regardless of nest type (see the sidebar titled Examples of
Stingless Bee Natural Enemies); biting is rarely combined with spitting formic acid (Neotropical
Oxytrigona), but much more commonly involves applying resin and release of alarm pheromones
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and acrid odors (58, 133, 148, 173). Soldier workers are slightly larger than others. They may repel
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raiding obligate kleptobiotic colonies, such as those of Lestrimelitta (over 20 spp.; see 18) in the
Neotropics, Liotrigona (Cleptotrigona) cubiceps in Africa, and possibly Trichotrigona in the Amazon;
they remain best studied in a Neotropical species (58, 59). Nest raiding within species seems rare.
Obligate kleptoparasites must reproduce by usurping a host nest, but Neotropical Tetragonsica
angustula may turn a raid by a robber into nest usurpation by the victim (139). Information on
intraspecific nest robbing or aggression that leads to colony death is fragmentary at best, and
obtaining more information would shed light on soldier subcaste evolution and kleptobiosis.

4.2. Nest Component Complexity

Colonies procure living symbionts while harvesting food, resins, latex, gum, or mud, which also
may carry secondary plant metabolites or other chemicals that are repellent or antimicrobial (115,
150; see Section 5). Resin flavonoids function as antimicrobials within the nest, while terpenoids
repel ants at nest entrances (58, 173), but these functions are only the beginning.
Meliponines certainly have co-opted phytochemical adaptations against ants and vertebrates.
Seeds that are protected from vertebrate herbivores sometimes result in plants that have fruit with
resins or waxes used by SBs. This presumably led to pollination mutualisms (see below). Resins are
applied at the SB nest entrance and renewed after disturbances by large animals (see the sidebar
titled Examples of Stingless Bee Natural Enemies) or attack by salticid spiders, lizards, ants, and
others (Table 1); entrance borders are often sticky (58, 139, 173) (Figure 1).
As SBs use resin and gum to fashion nests, they also mix salivary gland secretions with self-
made wax and foraged resin to make cerumen (58, 89). SB cerumen is produced in nests (see
the sidebar titled Noteworthy Stingless Bee Attributes; Figure 1) as worker mandibles combine
secreted wax and collected resins, stored in large single or in multiple deposits. Cerumen differs
in composition and texture from Apis wax and propolis (58, 115, 139, 150). SBs and HBs entomb
invaders with resin; HBs target wax moths (Galleria) (149). In contrast, SBs mostly entomb large
beetles, and sticky resin, often with irritant chemicals, is carried by defending workers to deposit
on vertebrates. Is resin in cerumen an effective deterrent of wax moths, which never invade SB
nests?
SB cerumen functions as the major nest material and generally provides a malleable, recyclable
substance. It is recycled from brood cells after the pupal cocoon is formed and is likely recycled
throughout SB nests (33, 58, 111, 139, 150, 175). Circulation among nest elements has not been
studied. Marked individual bees (marked with RFID tags; see 103, 173) and labeled cerumen, wax,
or resin would ideally sort through the labyrinth of intranest material cycling of clay-like cerumen
and collected substances.

www.annualreviews.org • Understanding the Stingless Bees 241

 Cerumen may be a precise mix of wax and resin and is sometimes sticky (like resins) due to
the contribution of hemipteran wax (139). Within the large Neotropical genus Plebeia (18), only
Plebeia droryana removes the wax of Ceroplastes scale insects feeding on Myrcia (Myrtaceae) and is
not a mutualist but an opportunist (112); SBs also often forage sap (44, 133). In contrast, Cecropia
bees (Nanoplebeia) opportunistically create melittophytes by co-opting ant plants and coevolved
mutualism with Cryptostigma (Coccidae) as obligate nest inhabitants (77, 141). Those mutual-
ists within nests provide wax and honeydew, and bees who form this mutualism store no honey
(141) (Figure 1). Unrelated Amazonian Schwarzula also use honeydew and wax from symbiotic
Cryptostigma but make copious honey and harvest wax using specialized morphology (20, 141).

4.3. Protection Mutualisms

Protection modes likely evolved sequentially and diversified as opportunism or mutualism evolved
from established nest architecture, construction behavior, and materials chemistry. The nest must
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be chemically disinfected by the bees and their collected materials (33, 79) and protected from
other natural enemies (see the sidebar titled Examples of Stingless Bee Natural Enemies). Al-
though SB brood develop in closed cells used only once, they also have associates (59, 114). The
adult SBs defecate in their nest. Their colony trash, except that deposited in latrines leading from
nest cavities, is ejected by worker bees (58, 139). Mutualisms may evolve when brood are accom-
panied by microbes or mites and detritus or excreta attract nematodes, collembolans, or beetles
that surround the brood areas (30, 58). Whether all such invertebrates contact bee immatures
is unknown but appears unlikely. Mutualism in nesting associations, either concerning nesting
site plants (where SBs attack defoliators of spiny species, like Rutaceae and Arecaceae) or among
arthropods, is far less common (139, 175).

4.3.1. Arthropod associates. Arthropod associates are too many and varied to adequately char-
acterize, but certain groups are better researched. Opportunism is unlikely in mite and blind
beetle associates. Mites in healthy colonies feed on detritus and other mites, fungi, and nema-
todes (30). Three meliponine genera in Brazil nest with 3 orders, 14 genera, and 18 species of
Acari that overlap little. Common taxa include Hypoaspis alfabetica, Melissotydeus bipunctata, Procto-
tydaeus quadrifasciatae, Lorryia meliponarum, and Tyrophagus putrescentiae. Laelapidae may specialize
on SBs, and Tydeidae may specialize on SB colony fungi. It seems likely that mites make a living
on colony trash but are not indispensable. However, mite population dynamics in bee nests are
unknown, and immigration to bee nests of such mutualists has barely been studied. Phoretic bee-
tles (Leiodidae) travel on Melipona and Cephalotrigona workers (139). These beetles have evolved
notched mandibles for transport upon bee hairs fringing the corbiculae and can achieve inter-
colony transfer at mud collecting sites. Scotocryptus, blind and flightless leiodid beetles, live only
with meliponine colonies and consume detritus, slime molds, and pollen (139).
Nesting associations sometimes give more benefit to one participant than the other. Two
Melipona with dissimilar defensive behavior, Melipona fallax and Melipona panamica, sometimes
coinhabit a single nest (133, 145). Another infrequent but widespread SB adaptation is nesting
within nests of defensive and well-protected ants or termites or near wasp nests (58, 133, 136,
141). Most conesting bees defend little, but conesting Trigona or Partamona are violently aggres-
sive. A few SBs (some Plebeia, Partamona, Tetragonula) nest in aggregations and collectively attack
intruders (139). A chemical or food basis has yet to be worked out: Is this opportunism or mutual-
ism? When they are unaggressive and provide no food or materials, associated SBs do not benefit
ants or termites. Some ants are significant colony predators (Table 1). The ant-deterrent mate-
rials added to bee nests could have permitted the evolution of protective mutualism by thwarting
host retaliation. Over the course of evolution, SBs may gain protection, as the balance in benefits

242 Roubik
 is modified to feed or protect ants or termites, but we still do not know if this is the case. In the
Melipona, foragers of M. panamica give nectar to defending Melipona fallax workers as they enter a
nest (133).

4.3.2. Microbe associates in colony ecology. Theoretically, host bee ecology should be re-
lated to bacterial strain (species) and potentially give evidence for host-switching, coevolution,
or independent introduction of microbes (74, 165; JG Kueneman, E Bonadies, D Thomas, DW
Roubik, and WT Wcislo, unpublished manuscript). The acidity of SB honey and pollen helps con-
trol fermentation that occurs because moisture content is high. It also, at pH4, favors acidophilic
bacteria (2, 33, 88, 154, 158).
What do acidophilic bacteria and other microbiota do? SBs use microbial symbionts to detox-
ify plant resources, process sugars, and displace harmful bacteria (33, 55, 171, 175). Yeasts, molds,
fungi, and bacteria are common within adult bees in portions of the alimentary tract or in labial
and hypopharyngeal glands (48), in the nest (resin, building material), in the processed pollen
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provisions eaten by larvae and newly emerged adults, and in stored honey or stored nectar (un-
ripe honey). Trehalulose in SB honey might derive from behaviors and biochemistry that convert
disaccharides (54, 114); the sugar also occurs in hemipteran honeydew, resulting from symbiotic
bacteria (16), and likely constitutes a source of trehalulose for SBs.
The developing larva voids its gut microbes, but adults receive new ones. Microbiota come from
bees in the same nest (via vertical transmission); from nest materials (also via vertical transmission);
or from transmission hubs outside the nest, primarily at flowers (horizontal transmission) (52, 88,
89). During feeding or foraging, spores (5 µm in size) are removed by the proventriculus in the
gut portion that receives honey stomach contents (149). Live bacteria pass through the barrier to
process food in the stomach; most live in the illium and hindgut.
Data on microbes (33, 41, 56, 78, 88, 105, 153; JG Kueneman, E Bonadies, D Thomas,
DW Roubik, and WT Wcislo, unpublished manuscript) imply that they form symbioses with
Meliponini, often at the species level; however, in Apinae, whether microbes are harmful, ben-
eficial, or neutral is often unknown (39, 40, 74; JG Kueneman, E Bonadies, D Thomas, DW
Roubik, and WT Wcislo, unpublished manuscript). Microbe and host SB associations are in-
dicated in Table 2. Fungi or a particular mold or yeast may provide nutrition in lieu of honey
for the Neotropical Ptilotrigona studied by Camargo & Pedro (19). Mutualisms with fungi are
widespread in SBs. New species of Penicillium were found with Melipona scutellaris in Brazil (10).
For Neotropical SBs, Starmerella may be the most important fungal mutualist (33, 40, 57, 58,
165, 167, 168). A remarkable discovery of a symbiotic mutualism of Scaptotrigona with filamentous
fungi for nutrition and gene regulation in steroid production (33, 109) lacks confirmed generality
among Meliponini.
Preswarming honey stores and newly collected pollen for all SB-directed swarms suggest
inoculation with microbes (33, 168), but no detailed study of these phenomena exists. Yet mi-
crobes may be lost or exchanged. Gilliamella apicola metabolizes toxic sugars (176) and lives
with some Neotropical Meliponini but not with other Neotropical, Asian, and African SBs
(23, 33, 74, 78, 159, 160). Lactobacillus malfermentans inhabits Southeast Asian SB honey (131)
(Table 2). Neotropical Melipona sometimes lack Snodgrassella and Gilliamella (23, 73, 74, 160; JG
Kueneman, E Bonadies, D Thomas, DW Roubik, and WT Wcislo, unpublished manuscript), pos-
sibly as an artifact of moving colonies (62; JG Kueneman, E Bonadies, D Thomas, DW Roubik,
and WT Wcislo, unpublished manuscript). They may be replaced by Starmerella (57).
In Africa, colonies from Kakamega forest were moved to savanna near Nairobi, where Liotrig-
ona, Plebeina, Axestotrigona, Hypotrigona, and Meliponula displayed 60% total reads (nucleic acid
sequences) in phylum Firmicutes: Lactobacillus, Acetilactobacillus, and Bombilactobacillus (Table 2).

www.annualreviews.org • Understanding the Stingless Bees 243

 The overall similarity was striking and seems too high. Losses due to colony transport were pos-
sible; new acquisitions likely came from the environment (62). Studies in Brazil using four SB
genera (34) in quite disturbed habitat found 141 operational taxonomic units for bacterial genera,
and Escherichia (Melipona quadrifasciata, Trigona spinipes), Sphingomonas, Xanthomonas (Tetragonisca
angustula), endophyte Gluconobacter, and plant phylosphere surface resident Pseudomonas (with
Frieseomelitta spp.) were dominant. Microbial surveys within nests of Tetragonisca, Frieseomelitta,
Trigona, and Melipona (common genera in South America) present nest microecoregions that rep-
resent phyloplanes—plant surface microbes (34). Pesticides may also circulate in the environment
and be taken from plant surfaces into bee nests (60), and all of the above factors have continuous
interplay within nests and among SB foragers.
The SB gut biome does not assemble at random and is most similar among bees within
phylogenetic units. The four corbiculate apine clades show microbiome similarity that can vary
by region, by season, and after hive or colony relocation (23, 62, 74, 91, 158, 159, 160; JG
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Kueneman, E Bonadies, D Thomas, DW Roubik, and WT Wcislo, unpublished manuscript).

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Major groups of bacteria are shared among corbiculate bees and others ( JG Kueneman, E
Bonadies, D Thomas, DW Roubik, and WT Wcislo, unpublished manuscript). Many meliponine
genera are unstudied (Table 2), and there are few comparative SB data from forests. Three
sympatric SB species, Austoplebeia and two Tetragonula in Northeast Queensland forest, shared
Lactobacillus that were host-specific, yet closely similar to Halictidae-associated bee bacteria (81).

4.4. Pathogens of Colonies

Studies of virus and phage interactions with SB are ongoing (33). Diseases and pathogens of SBs
have been known only since 2015 (3, 17, 33, 35, 40, 43, 52, 60, 61, 91, 118). Transfer of Nosema
disease from A. mellifera to SBs via flowers was recently demonstrated (Table 2). The virome of
M. quadrifasciata in southern Brazil (17) contained Dicistroviradae, Paroviradae, and Circoviridae
among mostly unhealthy colonies that were exploited by the viruses.

5. FORAGE AND POLLINATION ECOLOGY

Incoming forage ad infinitum multiplies SB associates—among them flowering plant nectar,
pollen, and resin, and also dispersing spores with which Meliponini are associated, even as food
(33, 49, 106). SBs visit but do not necessarily pollinate many thousands of tropical flowers (58, 121,
130, 133, 140, 144). Although we cannot say whether the original SB had the kinds of commu-
nication and forager recruitment seen today (8, 47, 58, 98, 99, 102, 113, 117, 122, 127, 133, 138),
such behavior, which allows masses of SBs to dominate tropical trees and other blooms, permeates
tropical ecology worldwide.

5.1. Natural Products in Meliponine Biology

Resins may amplify defenses already provided by low pH, H2 O2 , and osmolarity in all insect honey
(13). They prevent microbial damage of stored food and are heavily foraged by SBs (115, 133).
At their source, they deter herbivores, both vertebrate and invertebrate, and antipollinators—
nectarivores and pollenivores (mostly bees and ants) (126, 133). In addition, unsavory materials,
including urine, feces, and carrion, are sometimes foraged (34, 58, 83, 133). Central American
Trigona necrophaga was the first obligate necrophage bee discovered (132). Certain meliponines,
mostly those that also forage feces (Neotropical Oxytrigona, Trigona, Partamona, and Melipona),
and primarily obligate necrophages (a few Trigona) visit cadavers or moribund animals, including
dying wasp larvae and worms, for food, salts, and nutrients (53, 85, 101).

244 Roubik
 5.1.1. Phytochemical overviews. The diversity of secondary compounds in SB forage involves
many plant compounds that have been discussed in recent overviews (79, 82, 96, 115, 129, 150,
154, 162). Surveys of temperate-zone plants and a few tropical genera (Citrus, Persea, Solanum)
reveal that flavonoids and alkaloids are common in nectar and pollen, as are terpenoids and acids
(105, 108). Such chemical compounds, however, vary within a plant species. There are flavones
and terpenes, as well as phenolic compounds, in pure pollen (6, 108, 129). Examinations of antiox-
idant flavonoid contents in the honey of a common SB in the Neotropics, Tetragonisca angustula,
suggest that chemicals are potentially exchanged between honey and cerumen in SB nests (2, 111,
168), as has also been found in one African meliponine (114). Exchange between constantly cy-
cled nest material and incoming forage would tend to stabilize the many roles, yet to be proven
or adequately studied, of phytochemicals in SB colony and nest ecology.

5.1.2. New paradigms. In Quassia amara (Simaroubaceae), the flower-perforating Trigona ful-
viventris makes a ring of floral tissue around its holes in flowers, which may deter ant secondary
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nectar robbers via the plant tissue–derived repellent quasin (133). Secondary metabolites in pollen
(6, 108) may deter ants, which avoid this protein source. Bees have more protein and carbohydrate
resources than was previously thought (156). Have SBs experienced strong selection pressures
from the actions of ants at plants, and has this led to the use of microbes or enzymes that detoxify
nectar or pollen?
Highly eusocial bee harvest of secondary plant metabolites—from buds (171), wounded trees,
floral or fruit resins or waxes, and even seeds—appears to be universal. SBs gather mucilage, wax,
and resin that protect fruit or seeds from vertebrate herbivores. Such forage from fruit or flowers
is documented in Dalechampia (Euphorbiaceae), Clusia (Clusiaceae), Coussapoa (Urticaceae), and
Corymbia (Myrtaceae) in tropical America and Australia (4; 5; 14; 80; 115; 136, p. 29; 150; 173)
(Figure 1). Certain Tetragonula in Australia and many Melipona in Neotropical forests have become
seed dispersers (80, 133, 173) (Figure 1). In this case, as in many forms of mutualism between SBs
and associates, opportunism apparently evolved into a mutualism. Natural selection has produced
nest material–based pollination mutualisms with bees, but no one has determined whether the
dipterocarp resins of Southeast Asian forests have been selected to support SBs as pollinators.

5.1.3. Analytical approaches. Common among natural product SB investigations are chemical
profiling with no assays, or pharmacological tests lacking chemical profiles. This makes claims of
medicinal value unconvincing (90, 115, 150). Samples taken from a resin deposit in the nest, a nest
entrance, or interior cerumen pots or brood cells differ, but often, source material is not identified
or functionally classified. Although species are identified infrequently, studies in the Neotropics
and Southeast Asia show that the same bees sometimes have distinctive material chemistry in
different places, while different bee species may have similar chemistry in one habitat. Plant resin
origins, when identified, are often exotic species or of farmland (79, 82, 83, 96, 115).
Satisfactory bioactivity analysis requires chemical study of taxonomically known bee–plant
combinations followed by pharmacological testing using sample fractions and, ultimately, pure
compounds (115, 141, 151). In order of frequency of occurrence, antioxidant effects, antifungal
and antibacterial effects, free-radical scavenging, anti-inflammatory effects, antiviral effects, anti-
cancer cell growth, and inhibition of bone loss compounds have been demonstrated for materials
derived from SBs. Many more medically relevant materials are known for SBs than for Apis. Pio-
neering analysis of diterpenes has progressed to mangostins (from cultivated mangosteen Garcinia,
Clusiaceae) (4), which inhibit human melanoma growth, and xanthine oxidase, which has poten-
tial antigout activity, both of which are found in Southeast Asian Lepidotrigona, Tetragonula pagdeni,
and a bee taxonomically near Tetragonula biroi (96). Mohammad et al. (96) summarize world data
and works in progress.

www.annualreviews.org • Understanding the Stingless Bees 245

 Gum, latex, and sticky plant polysaccharides contain galactose, arabinose, rhamnose, uronic
acids, galactoronic acid, protein, Ca, and Mg as major structural constituents, as well as glucose,
xylose, mannose, protein, and fat as minor constituents (95). It is likely that SBs use them as food
or building materials, but studies are needed to confirm this.

5.2. Pollen Surveys

SB nests and foragers provide pollen grains, which can be counted and identified under micro-
scopes. Such pollen identification supplements field observations, which are often difficult to
conduct in tall forest and canopy settings. Substitution of molecular databases for identified ref-
erence pollen slides (163, 168) has been slow due to the sheer size of the tropical flora. Both kinds
of databases are incomplete.

5.2.1. Melittopalynology and melissopalynology. Many tropical trees (20–30%) flower in-
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frequently or are unisexual; thus, bee resource use and pollination ecology present complex
challenges to ecologists (144, 167, 168). Paradoxically, flowers heavily foraged by SBs and HBs
are often nectarless. That is, pollen in the flowers is the only pollinator reward; there is never
any nectar. Although pollen from a nectarless species will never indicate a carbohydrate source,
honey may contain abundant pollen of nectarless flowers, which is dusted on the bees’ bodies and
is mixed in foraged nectar within bee nests. Honey is often misclassified as monofloral, in tra-
ditional melissopalynology, based on abundant pollen of nectarless species in tropical honey (11,
144). Pollen studies also count grains to quantify utilization or consumption by bee larvae (1, 11,
32) or tally pollen or foraged corbicular pellets (135, 143, 144). If pollen species are similar in size,
then comparable methods can be used to quantify them. The difference in size between the pollen
of Miconia and Piper (10 µm) versus the pollen of palms, cucurbits, and euphorbs (50–100 µm),
for instance, makes grain counts difficult to interpret unless literally monofloral foraged pollen
pellets are measured or weighed. The melittopalynology of bees and their proteinaceous food—
pollen—is more straightforward than the melissopalynology—the important honey sources. The
latter is more difficult to garner from pollen data.
Diet breadth in studies conducted over longer periods of time (32, 84, 85, 128, 143, 145, 166,
167, 168) reveals diversity together with specialization. Scaptotrigona fulvicutis, the largest bee
in its genus, utilizes 98 plant species in central Amazonia (85). This is comparable to the num-
ber of pollen species from Melipona panamica at 9°N in Panama (145). To obtain comprehensive
pollen resource data, two studies examine accumulated bee pollen feces. Cephalotrigona deposits
feces in a block at the nest floor, called loloc in Yucatecan Mayan, and studies of a 20-year-old
Trigona corvina colony dissected a scutellum nest shell of pollen feces (143, 145). Cephalotrigona
colonies were relatively specialized on palms (Iriartea), Pterocarpus and Machaerium (legumes), an
unidentified Asteraceae, and Arrabidaea and Brosimum (Bignoniaceae and Moraceae). The Trigona
heavily used Cecropia, Pseudobombax, Machaerium, Spondias, and particularly Chamaesyce (Euphor-
biaceae) and palms (Elaeis, Attalea). In-depth studies of Melipona beecheii nest pollen across central
Yucatan, Mexico revealed a large amount of pollen from the so-called living fenceposts Gliri-
cidia and Bursera (167, 168). Remarkably, another study in Northeast Brazil within similar forest
and farm landscapes found comparable pollen representation of the same top-five plant fami-
lies (those most frequently recorded among taxa) for Melipona scutellaris (122, 168) as those seen
in Yucatan for M. beecheii. Additional work with honey in Brazilian Amazon floodplain forest
discovered that Melipona interrupta and Melipona seminigra honey had Miconia (Melastomataceae)
and Tapirira (Anacardiaceae) in greatest abundance. The first is nectarless; the second is unisexual
and contains powerful antimicrobials (128, 147, 161).

246 Roubik
 The sources of native tropical honey, as well as bee fitness and food, remain somewhat elusive
but appear to depend on both successional and mature plant assemblages. Brazilian pollen studies,
which were largely performed to inform honey source management (36), list an impressive 50 SB
species from 16 genera; these studies highlight Australian Eucalyptus, which indicates Anthro-
pocene habitat, and also find many nectarless plants. Studies heavily favor the large Melipona and
highly adaptable (nesting in buildings, cities, countryside, and wildlands) Scaptotrigona and Tetra-
gonisca angustula, which are widely kept (1, 7, 11, 29, 32, 38, 58, 64, 84, 85, 104, 105, 122, 128, 144,
145, 167, 168). A few studies have been conducted in natural forests. If comprehensive informa-
tion were available for plant species, and ground truth was established with observation at flowers,
then relative floral resource importance for SBs could be clarified in reasonably well-documented
floral landscapes and wildlands.
SBs forage extrafloral nectar that attracts ants, which discourage herbivory (11, 36, 97). Such
nectar contains honeydew elements such as fungal hyphae, frequently found in the honey of SB
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species, excluding Melipona (in 18 of 28 samples), and sometimes in the honey of Apis (11, 13). A
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large SB survey found that 12 botanical families provided the dominant pollen types (>45%) (11);
however, as in many tropical pollen surveys, genera or families but not species were identifiable.
When a botanical survey establishes how many species are in a genus and their flowering phe-
nology, studies of bee pollen harvest can yield better ecological insights. Knowledge from a small
sample does not allow one to rank plant importance to bees, and acetolyzed (cleaned and cleared)
pollen is needed for identification at most generic and species levels (143, 144, 168).

5.2.2. Bee-cycling of carbon and energy. Bee pollen, nectar, and resin can be quantified by
registering forager traffic. Mechanical counts are preferable, but the data at hand came from direct
observation. Combining detailed pollen-load and body weight studies (120); forest surveys of bee
colony activity in Panama and the Amazon at 9°N and 10°S, respectively (28, 142); and nest surveys
in Borneo at 5°N (50) indicate that 20–200 kg of pollen and resin are taken annually by SBs residing
in a hectare of forest. Viewed as a carbon sink, SBs of 1–10 colonies × ha−1 observed in tropical
forests (26, 50, 66, 70, 136) recycle large amounts of carbon and energy. In the reference studies,
approximately 50–70% of nonpollen or resin forage was nectar, which varied during wet versus
dry seasons.

6. BEE-KEEPING ECOLOGY
Stingless bee-keeping (2, 24, 25, 27, 38, 58, 65, 69, 100, 116, 119, 166), indoor and field crop
pollination, illegal trade, and disease spread are now studied closely (3, 17, 22, 31, 29, 35, 40, 43, 52,
60, 87, 152). Harvested by humans from wild bee nests, different kinds of cerumen are historically
prized for the fletching of arrows, metal lost-wax foundry, and boat patching (113, 150, 155).
Floral resin from Dalechampia and Clusia foraged by SBs hardens slowly (5; 14; 133, p. 29) and
makes cerumen more pliable. Taffy-like or tar-like SB resins and other SB-produced substances
are widely applicable. Harvest of SB products, particularly resins and honey, is switching from
extraction in wildlands to cultivation and husbandry, and thus may foster sustainability.
The relative ease of SB colony management has galvanized research, but SBs seem less ro-
bust to manipulation than HBs. In the coming years, meliponines may be found to resemble
A. mellifera in studies of disease spillover, toxins, parasite and microbe transfer at floral hubs, inter-
breeding, competition with native species, pillaging, or negative pollination impact (e.g., 52, 126).
New management and technology may address some problems in advance, and lessons from honey
bee biology provide a potential scenario (89, 118). Commercial success has led to administrative
and legal guidelines to obtaining or selling SBs. Nonetheless, among six Brazilian biomes, trans-
fers frequently occur over hundreds or thousands of kilometers, covering 10.8–27.6° in latitude

www.annualreviews.org • Understanding the Stingless Bees 247

 (43). The possibility that exotic SB colonies may colonize or substantially alter biota is a concern
(22). Some SBs may form new mutualisms or adapt to climate (62), but ecological predictions are
somewhat tentative (67). Natural enemy hubs at flowers are mostly unresearched.
Industrial production of SB colonies creates unanticipated results. Scaptotrigona in commer-
cial hives threaten traditional Apis bee-keeping by pillaging and have caused reprisals (172). In
Brazil, artificially produced queens for new Scaptotrigona colonies demand management. They are
not, like HBs in the United States, shunted between regions. Whether they will become dispos-
able pollination units, like commercial Bombus spp. in mid-latitudes, is difficult to predict. Many
colonies are extracted from trees and kept by inexperienced bee-keepers, then die and are replaced.
Husbandry, education, and innovations are needed.

7. CONCLUSIONS
The longer a bee lineage lives within tropical diversity, the more likely it is that it accumulates
Annu. Rev. Entomol. 2023.68:231-256. Downloaded from www.annualreviews.org
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significant interactions. A review of SBs in 1983 (175) mentions 20 biological traits, many revisited
in this review. Research since 1983 has overturned some views held then, including that a stinger
remnant in Melipona indicates antiquity. Melipona arose in the Miocene (123). I previously sug-
gested that vulture bees give a carrion slurry to receiver bees (132, 133). However, we now know
that these bees directly deposit forage in cerumen pots, where microbes convert it into glucose
and amino acids (18, 53, 55, 87, 101). Seeds gathered by Melipona from fruit were once thought
to be from Vismia but are instead from Coussapoa in a matrix of wax, not resin (133); behavior-
inducing chemicals are from labial glands, not mandibular glands (58, 148); and there is no fossil
Nogueirapis (51). It has been confirmed that Lestrimelitta, Cleptotrigona, and obligate necrophage
Trigona never visit flowers (58). In all cases, an HB analogy fails to guide investigation. Study of
comparative ecology, sometimes by contrasting SBs with Apis, now profits more by considering
SBs alone.

FUTURE ISSUES
1. Do obligate necrophage foragers also provision brood with glandular secretions?
2. Why do Amazonian Ptilotrigona store no honey?
3. Does any kind of stingless bee-keeping help sustain natural communities or populations?
4. Why are there kleptobiotic Meliponini in tropical America and Africa but not Asia, and
why do obligate necrophages occur only in the Neotropics?
5. Why has the microbiome of meliponines shifted so often, and which microbes are truly
essential?

DISCLOSURE STATEMENT
The author is not aware of any affiliations, memberships, funding or financial holdings that might
be perceived as affecting the objectivity of this review.

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Contents
Volume 68, 2023

Complex and Beautiful: Unraveling the Intricate Communication

Systems Among Plants and Insects
James H. Tumlinson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Chemical Ecology of Floral Resources in Conservation Biological Control
Stefano Colazza, Ezio Peri, and Antonino Cusumano p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p13
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Management of Insect Pests with Bt Crops in the United States

Aaron J. Gassmann and Dominic D. Reisig p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p31
Iron Homeostasis in Insects
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Phoresy and Mites: More Than Just a Free Ride
Owen D. Seeman and David Evans Walter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p69
Postcopulatory Behavior of Tephritid Flies
Diana Pérez-Staples and Solana Abraham p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
The Biology and Ecology of Parasitoid Wasps of Predatory Arthropods
Minghui Fei, Rieta Gols, and Jeffrey A. Harvey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 109
Dehydration Dynamics in Terrestrial Arthropods: From Water Sensing to
Trophic Interactions
Joshua B. Benoit, Kevin E. McCluney, Matthew J. DeGennaro,
and Julian A.T. Dow p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 129
Biology and Management of the Spotted Lanternfly, Lycorma delicatula
(Hemiptera: Fulgoridae), in the United States
Julie M. Urban and Heather Leach p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 151
Historical and Contemporary Control Options Against Bed Bugs,
Cimex spp.
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Functional Diversity of Vibrational Signaling Systems in Insects
Meta Virant-Doberlet, Nataša Stritih-Peljhan, Alenka Žunič-Kosi,
and Jernej Polajnar p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 191
Forest Insect Biosecurity: Processes, Patterns, Predictions, Pitfalls
Helen F. Nahrung, Andrew M. Liebhold, Eckehard G. Brockerhoff,
and Davide Rassati p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 211

viii
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Stingless Bee (Apidae: Apinae: Meliponini) Ecology

David W. Roubik p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231
Diapause in Univoltine and Semivoltine Life Cycles
Hideharu Numata and Yoshinori Shintani p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 257
Early Monitoring of Forest Wood-Boring Pests with Remote Sensing
Youqing Luo, Huaguo Huang, and Alain Roques p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 277
Spodoptera frugiperda: Ecology, Evolution, and Management Options
of an Invasive Species
Wee Tek Tay, Robert L. Meagher Jr., Cecilia Czepak, and Astrid T. Groot p p p p p p p p p p p p p p 299
Molecular Mechanisms of Winter Survival
Nicholas M. Teets, Katie E. Marshall, and Julie A. Reynolds p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 319
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Arthropod and Pathogen Damage on Fossil and Modern Plants:

Exploring the Origins and Evolution of Herbivory on Land
Conrad C. Labandeira and Torsten Wappler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 341
The Resilience of Plant–Pollinator Networks
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The Mechanisms of Silkworm Resistance to the Baculovirus
and Antiviral Breeding
Zhaoyang Hu, Feifei Zhu, and Keping Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 381
Diversity, Form, and Postembryonic Development of Paleozoic Insects
Jakub Prokop, André Nel, and Michael S. Engel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 401
Molecular Mechanisms Underlying Host Plant Specificity in Aphids
Po-Yuan Shih, Akiko Sugio, and Jean-Christophe Simon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 431
Adaptive Plasticity of Insect Eggs in Response to Environmental
Challenges
Monika Hilker, Hassan Salem, and Nina E. Fatouros p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 451

Errata

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