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Bees that love tears: A review of Lisotrigona congregating at human and animal eyes (Hymenoptera: Apidae, Meliponini)

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Stingless bees (Apinae: Meliponini) exhibit astonishing and unusual behaviours, including tear-drinking or lachryphagy. In this review, we summarize lachryphagy in stingless bees, providing updated insights into their taxonomy, foraging patterns, ecology, hosts, evolutionary origins, and potential for pathogen transmission. In Northern Thailand, marked workers of the minute stingless bees Lisotrigona cacciae (Nurse) and L. furva Engel repeatedly return to human eyes, harvesting tears in short bouts that can last for hours or even over multiple days. Behavioural evidence suggests the presence of specialized tear collectors within these species. Single, experienced individuals can harvest tears gently, going unnoticed by the host, though large congregations can become bothersome. Lachryphagy occurs year-round and appears to be driven by high protein content in tears, in addition to salt and water. While Lisotrigona also visit flowers for nectar and pollen, tear collection may supplement or even replace pollen protein when floral resources are scarce or absent in their restricted habitats. Confirmed hosts include humans, zebu, dogs, cats, rabbits, chickens, and yellow tortoises. Lachryphagy has also been reported in other species of Lisotrigona in India. Interestingly, the similarly minute and widespread Tetragonula fuscobalteata (Cameron) is not lachryphagous but sucks sweat, as do other stingless bees, including Lisotrigona, though all visit flowers. This review also examines the potential for pathogen transmission via tear-drinking, particularly concerning viruses entering through the ocular surface, and discusses the evolutionary origins of lachryphagy in stingless bees.
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Journal of Meliology
Bee Biology, Ecology, Evolution, & Systematics
No. 121, pp. 1–19 30 September 2024
Copyright © H. Bӓnziger, M. D. Burge, S. Bӓnziger, & K. Klaithin
Creative Commons Aribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0).
ISSN 2325-4467
Bees that love tears: A review of Lisotrigona congregating at
human and animal eyes (Hymenoptera: Apidae, Meliponini)
Hans Bӓnziger1, Michael D. Burge2, Saengdao Bӓnziger 3, &
Kanokwan Klaithin1, 4
Abstract. Stingless bees (Apinae: Meliponini) exhibit astonishing and unusual behaviours, in-
cluding tear-drinking or lachryphagy. In this review, we summarize lachryphagy in stingless
bees, providing updated insights into their taxonomy, foraging paerns, ecology, hosts, evolu-
tionary origins, and potential for pathogen transmission. In Northern Thailand, marked work-
ers of the minute stingless bees Lisotrigona cacciae (Nurse) and L. furva Engel repeatedly return to
human eyes, harvesting tears in short bouts that can last for hours or even over multiple days.
Behavioural evidence suggests the presence of specialized tear collectors within these species.
Single, experienced individuals can harvest tears gently, going unnoticed by the host, though
large congregations can become bothersome. Lachryphagy occurs year-round and appears to be
driven by high protein content in tears, in addition to salt and water. While Lisotrigona also visit
owers for nectar and pollen, tear collection may supplement or even replace pollen protein
when oral resources are scarce or absent in their restricted habitats. Conrmed hosts include
humans, zebu, dogs, cats, rabbits, chickens, and yellow tortoises. Lachryphagy has also been re-
ported in other species of Lisotrigona in India. Interestingly, the similarly minute and widespread
Tetragonula fuscobalteata (Cameron) is not lachryphagous but sucks sweat, as do other stingless
bees, including Lisotrigona, though all visit owers. This review also examines the potential for
pathogen transmission via tear-drinking, particularly concerning viruses entering through the
ocular surface, and discusses the evolutionary origins of lachryphagy in stingless bees.
1 Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University,
Chiang Mai 50200, Thailand (hans.banziger@cmu.ac.th, kanokwan.kh@cmu.ac.th).
2 Department of Horticulture, Oregon State University, Corvallis, OR 97331, U.S.A (Michael.
Burge@oregonstate.edu).
3 Education Services and Student Quality Development, Faculty of Agriculture, Chiang Mai
University, Chiang Mai 50200, Thailand (sangdao.banziger@cmu.ac.th).
4 Department of Entomology, College of Agriculture and Natural Resources, National Chung
Hsing University, Taichung 40227, Taiwan (kanokwan.entomo@gmail.com).
doi: hps://doi.org/10.17161/jom.i117.22447
INTRODUCTION
Tears, present on the eyes of terrestrial vertebrates (except snakes and geckos),
is a saline liquid with proteins and minor amounts of lipids and other components,
Journal of Melittology2No. 121
with the main function to lubricate eye lid movements, wash o debris, protect against
pathogens, and prevent desiccation (Millodot, 2009). Many insects visit human and
animal eyes for their tears, especially ies of the families Chloropidae, Cryptochetidae,
Drosophilidae, and Muscidae (e.g., Greenberg, 1973; Sabrosky, 1987; Moon, 2002;
Otranto et al., 2006; Bänziger et al., 2009). The laer authors, besides mentioning that
172 specimens of 31 species of drosophilid ies sucked human tears in Thailand,
and that many moths (Lepidoptera) are nocturnal lachryphages, for the rst time
also documented stingless bees (Apidae: Meliponini) as avid tear drinkers: the tiny
Lisotrigona cacciae (Nurse), L. furva Engel (Fig. 1), and to a lesser degree Pariotrigona
klossi (Schwarz). Unpublished observations on some minute meliponines occasionally
pestering humans, including occasional ying to eyes, had already been locally
known, but were interpreted as accidental during more normal sucking of moisture
and salt from human skin. Araction to human sweat by minute meliponines had been
reported from afro- and neotropics (Michener, 1990a, b), but not from Asia (Michener,
2000). More recently in Thailand, pestiferous sweat suckers have not only been
found among minute species, including to a degree the mentioned lachryphagous
species, but also in medium-sized species such as Lepidotrigona terminata (Smith)
and Tetragonula sirindhornae (Michener & Boongird) (Bӓnziger et al., 2009). Tear- and
sweat-drinking species of Lisotrigona Moure have been recently observed also in
India (Thangjam et al., 2021). According to a very brief study in SW China by Li et
al. (2021) on Lisotrigona carpenteri Engel, now Ebaiotrigona carpenteri (Engel), it is not
clear whether it is essentially a sweat sucker, more or less accidentally approaching
the eye and imbibing tears that happened to be mixed with sweat in proximity of
human eyes or, a rather weak tear drinker. Similar observations were made by Tuan
Anh Truong (Engel et al., 2022) in N Vietnam. However, during a long-term study of
the nesting biology of E. carpenteri from March to December, Chinh et al. (2005) did not
mention any sweat- or tear-drinking behaviour by this species near at least 17 natural
nests at Cuc Phuong, Ninh Binh Prov., N Vietnam. Also the rst author in the present
contribution (H.B., unpubl. data), did not note lachryphagy in this species at the same
site in Vietnam, but observations were very brief (4 and 10 December, 2010). On the
other hand, persistent araction to, but no seling on, the upper parts of humans by L.
cacciae and L. furva was observed in Cambodia and Laos, respectively (Lee et al., 2016),
and similarly by L. cacciae in Sri Lanka (Karunaratne et al., 2017), without any tear-
drinking cases. Nonetheless, on 13 December, 2008, one L. furva drank tears from the
eye of H.B. at Banteay Srei, near Angkor, Siem Reap, Cambodia (Bӓnziger & Bӓnziger,
2010). Interestingly, according to Engel et al. (2021), in the neotropics apparently there
are no meliponines exhibiting the typical lachryphagous behaviour as described for
Thailand, although minute species of Trigonisca Moure are vernacularly known as
‘eye-lickers’ in Latin America. Of course, whether a bee is successful in snatching tears
from a human also depends on his willingness to let meliponines have free access to
the eyes and, in the case of a researcher, on his patience to wait suciently long for
them to locate him as a source.
Unlike the vulture bees, such as the neotropical Trigona necrophaga Camargo &
Roubik, which, instead of pollen-eating are obligate necrophages (Roubik, 1982;
Camargo & Roubik, 1991), and occasionally carnivores (Mateus & Noll, 2004),
Lisotrigona also forage for pollen and nectar, probably their main foodstu when
available in the restricted habitat of the tiny bees, although data on this are still poor.
Lisotrigona furva was collected from Callistemon sp. (Myrtaceae) and Buddleia asiatica
Lour. (Buddlejaceae) (S. Boongird & C. Michener, in Engel, 2000), and from Tetrastigma
Bӓnziger et al.: Bees that love tears
2024 3
Figures 1–2. Tear-drinking and ower visiting Lisotrigona furva Engel. 1. A row of 18 worker bees
sipping tears from the eye of H. Bӓnziger in self-portrait. 2. Workers collecting pollen and nectar
from owers of lichi (Litchi chinensis Sonn.) (Sapindaceae). Scale bars 6 mm. Photos H. Bӓnziger.
baenzigeri C. L. Li and T. hookeri (Lawson) (Vitaceae) (Bänziger et al., 2009); L. cacciae
and L. furva were observed harvesting nectar and pollen from lichi (Litchi chinensis
Sonn.) (Fig. 2) and longan (Dimocarpus longan Lour.) (Sapindaceae), and carry pollen
from Leucaena leucocephala Lam., Senna siamea (Lmk.) Irwin & Barn (Leguminosae) (and
other owers the pollen of which, however, could not be identied) (Bӓnziger, 2018).
Herein, we review the lachryphagous behaviour of minute stingless bees,
providing updated information on their taxonomy, foraging behavior, ecology, hosts,
evolutionary origin, and potential for pathogen transmission.
Taxonomic Notes on Lachryphagous Species
In a genus-level revision of Lisotrigona Moure, Engel et al. (2022) transferred L.
carpenteri to the new genus Ebaiotrigona Engel & Nguyen on convincing morphological
Journal of Melittology4No. 121
evidence. Workers of E. carpenteri are easily distinguished from those of Lisotrigona
and Pariotrigona by the yellow face maculation (among other characters, including the
slightly larger size of E. carpenteri). This removal from Lisotrigona could also support
the behavioural dierence between species of the two genera, namely, that E. carpenteri
is not truly lachryphagous, or at most only rather weakly or accidentally so.
The very similar L. cacciae and L. furva from Thailand are best identied by
dierences in body size, as shown by Michener (2007), and conrmed with further
measurements by Bänziger & Bänziger (2010), viz. head width 1.05‒1.23 mm in L.
cacciae and 1.25‒1.41 in L. furva, without overlap. The body length is not a reliable
measurement because it is dependent on the crop fullness of the telescoping metasoma.
In India, besides the presence of L. cacciae, ve new species of Lisotrigona were
recently described, viz. L. mohandasi Jobirai & Narendran (Jobiraj & Narendran, 2004),
L. chandrai Viraktamath & Sajan Jose, L. revanai Viraktamath & Sajan Jose (Viraktamath
& Sajan Jose, 2017), L. darbhaensis Viraktamath, and L. kosumtaraensis Viraktamath
& Jagruti (Viraktamath et al., 2023). Whereas in the report by Thangjam et al. (2021)
there is no doubt that several specimens of Lisotrigona drank tears in three separate
cases in India, according to Viraktamath (pers. comm., 11 March, 2022), the identity of
such species remains unknown. Also, there is some controversy regarding the actual
number of good species of Lisotrigona in India (Rasmussen et al., 2017; Viraktamath et
al., 2021).
Regarding Pariotrigona klossi, Schwarz (1939) described it as a variety of P.
pendleburyi (Schwarz), then under Trigona, both from Peninsular Malaysia. But
Michener (2002 [2001]) found intergrading characters in specimens from Borneo,
Sumatra and Malaysia, and proposed P. klossi as a synonym of P. pendleburyi. This
was followed by Rasmussen (2008), Rasmussen et al. (2017), and Engel et al. (2018,
2022). However, in lachryphagous specimens found by H.B. in S Thailand, the main
characters consistently matched P. klossi, and Michener, whom H.B. had sent specimens
for verication, did not question H.B.’s identication. Unfortunately, Michener died
before we could redescribe P. klossi for validation. This is now in preparation, based
on additional material.
Marking Experiments and Feeding Behaviour of the Bees
This was carried out in N Thailand, with wild populations of Lisotrigona in forest
sites to make sure that the behaviour was not potentially inuenced by articial
components (e.g., bees from meliponaries, degraded environment). Two sites were
visited at least once monthly, May 2013 to November 2014, another was visited daily,
31 May to 20 June, 2013; session time lasted 1.5–11 h depending on the bees’ harvesting
time (averaging more than 3 h), total session time 360 h (Bӓnziger, 2018). Bees were
marked (Fig. 3) while they avidly sucked tears, H.B. being both lachrymation source
and experimenter, by his applying a minuscule drop of waterproof paint to the
mesosoma back with a nely trimmed brush, viewed in a concave mirror. Generally,
during one day, only one or two bees were marked, the touching causing the bee to y
o. If she returned, the colour, shape and position of the mark, which diered in every
bee, were photographically recorded for correct recognition among large assemblages
over hours, and days. The marking, 34 L. cacciae and 23 L. furva, revealed that the
very same bees can visit human eyes up to 78 and 144 times in one day, respectively.
Depending on the bees’ position at the eye and competition with other bees, sucking
Bӓnziger et al.: Bees that love tears
2024 5
lasted 0.4‒6.2 min (average 2.2 min) in L. cacciae, 0.4‒5.3 min (average 1.6 min) in L.
furva. Intervals between consecutive visits were 1.5‒7.5 min (average 3.3 min) and
2.0‒8.0 min (average 3.8 min), respectively. In one day, the same bees may collect
tears for up to 10.5 h (includes round trip time), average 3 h 15 min in L. cacciae, 2
h 14 min in L. furva; ve workers of each returned on the following day for up to 78
and 44 harvesting bouts, respectively; one L. furva came on three consecutive and on
the seventh day. Tear drinking occurred throughout the year (rainy, dry hot, and dry
cold seasons), except during heavy rain and at temperatures below 22°C when no
workers left the colony to forage. Lachryphagy was observed even during light rain
and after a downpour. So water was not the principal component sought. The other
well-known component is salt (NaCl) but, generally not appreciated, there is a third
main component, viz. proteins, and they are on a par with that of salt, ca. 6.7 mg in 1
ml (Rauen, 1964), 200 times the proteins present in sweat.
Tear collecting is not a simple maer of imbibing moisture; it requires special
behavioural adaptations because the source is not dead maer or a ower, but can be
a highly mobile, sensitive and reactive vertebrate. Although single experienced tear
collectors can be so surreptitious and gentle to occasionally avoid detection by the
host, more often they tend to be avid and persistent to become pestiferous when in
large groups. The most critical time for lachryphagy is during the bees’ approach to the
eyes – not while sucking there. Humans normally ip them away when circling near
the face (in zig-zag ight in the horizontal plane, whereas the common lachryphagous
drosophilid ies tend to zig-zag vertically). The bees are likely to return and, if
they manage to avoid the ipping and are about to reach the eye, the eyelids may
automatically blink repulsing the bee. Animals, especially large herbivores, are less
sensitive but ip with their ears, chase them o by tail, paw, claws, or shake their head.
But in their persistence the bees tend to return time and again – like face ies do. The
host may walk away but, unless running, the bees tend to follow in pursuit. The most
experienced tear collectors will y in low and very gently land below near the cilia or
at the inner corner of the eye (e.g., Fig. 3) (no eyelashes there), less often at the outer
corner, and then advance to where their proboscis can reach the tears accumulating in
the menisci and trench between lid and eyeball. They evidently crawl by using only
the tarsal soft arolia pads but with the claws automatically in retracted position, as
described for honey bees when crawling on vertical smooth surfaces (Federle et al.,
2001). Once landed and feeding at the eye, often only a faint tickling is perceived, if at
all (H.B. occasionally had to check by mirror if a bee was still sipping or had already
departed). The bees’ proboscis is very ne and soft (about 1mm long, a third of the
bee’s body length, and only 0.025 mm wide distally) so essentially it is not perceived
on the conjunctiva and the eyeball, unlike the bees’ tarsi and claws of inexperienced
drinkers which may cause tickling to the host. When seled, the bees would not y o
if the host walks or even slowly runs away, but continue to feed until satiated.
Analysis of 117 photographs of Lisotrigona at human eyes revealed that none
of the 302 bees present carried pollen loads, whether small or large (Fig. 4), in their
corbiculae. From stereomicroscope checks of collection specimens from eyes, only a
few had pollen remnants, presumed result of the age polyethism from previous pollen
collecting, or from contacts with nest-inmates. Because, as detailed above, lachryphagy
is not a simple imbibing of liquids, but requires specic and unusual behavioural
adaptations, including additional features described below (e.g., the consecutive bouts
of tear drinking instead of switching to the much easier sucking of sweat), Bӓnziger
(2018) proposed that Lisotrigona might have specialized tear collectors – a new division
Journal of Melittology6No. 121
of labour in meliponines sensu Michener (1974), who used it in a broad sense, which in
Lisotrigona probably is a part-time division of labour.
Bee Scent Marking and Recruiting
Some Lisotrigona were also seen along the groove between the lids of closed eyes
of a drowsy or sleeping animal host, e.g., a dog. Presumably the bees can locate the
eye when they have scent marked it during a previous visit, or when aracted by the
odour of tear incrustations or tear seepings along where the lids meet. Scent marking is
indeed likely to occur: a fully satiated bee with turgid crop would not directly y away
but often remain a second or so while moving her head, antennae and forelegs, and
then causing a typical tickling sensation to the lid/cilia of H.B. as if forcibly grasping
them for an instant on take-o. Such head movements have been noted in neotropical
Trigona hyalinata (Lepeletier) for odour-marking by mandibular glands (Nieh et al.,
2003), and in Melipona seminigra Friese for tarsal ‘footprint’ marking (Hrncir et al., 2004).
Quite often H.B. felt a slight burning or itching sensation at the eyelid, continuing after
the bee had left, which indicate probable cases of scent marking.
The observation that there tended to be an exponential increase in arrivals following
the rst tear collector, indicates that Lisotrigona employ some form of recruiting. No trail-
laying was observed. Possibly, an experienced collector piloted a recruit by sight and/
or by an aerial scent plume released by the guide. Occasionally, H.B. noted that when
a Lisotrigona was squeezed between his ngers, a strong odour was perceived; such a
volatile might be used as a guiding plume. This type of recruiting had been proposed
by Lindauer & Kerr (1958) for neotropical meliponines. The information exchange and
recruiting behavior in Lisotrigona supports the use of the term ‘congregating’ rather
than ‘aggregating’ when describing lachryphagous Lisotrigona. The former suggests
a directional approach towards a known assembling site, whereas the laer denotes
arrivals from any direction, casually aracted by a local resource.
Tear Proteins as Nutrition
The repetitive ingestion of full-crop loads of tears in successive sucking bouts is
possible only if the preceding load is either regurgitated or anally excreted. In the laer
case, tears would have to go through the digestive system and, since the proteins are
dissolved, we know of no mechanism how Lisotrigona could extract and separate the
proteins from the tears to be selectively discarded by excretion, if proteins were indeed
unwanted ballast. They would inevitably be digested and assimilated, making them a
nutritional resource rather than waste.
More likely is regurgitation where there are two possibilities, viz. trophallaxis to
receiver bees, or disgorging into containers (pollen and/or honey pots, and/or brood
cells). Bӓnziger (2018) thought that trophallaxis would be the more probable procedure
because the tear collectors can readily return to harvest more tears. In the nest, tears
might be used to dilute highly concentrated honey for the brood. Or nurse bees may
process the tears to produce brood food. In all these cases the tears’ dissolved proteins
end up, volens nolens, enriching the nourishment.
Although pollen is far richer in proteins and lipids (Winston, 1987), tears are
superior in having dissolved, readily digestible proteins, not enclosed in indigestible
Bӓnziger et al.: Bees that love tears
2024 7
exine walls as in pollen. Also, 20‒25% of the protein in human tears is lysozyme (e.g.,
Millodot, 2009), an enzyme with bactericidal properties, which could help against
spoilage of tears in pots, until itself consumed as nutrition. The basic main tear
composition of proteins, salt and water is also present in other mammals, birds and
reptiles though the concentration of total proteins is highest in humans and lowest
in reptiles (Raposo et al., 2020; Oriá et al., 2020). Moreover, tears are energetically less
costly in harvesting. Namely, no hovering for pollen transfer to corbiculae is required,
crop lling is in a seled position, taking just 1‒6 min, and crop transporting allows
a larger load than corbiculae (Michener, 1974), hence fewer return trips are necessary
than for pollen. Additionally, pollen production by a ower is not continuous and soon
exhausted, whereas tears are not only secreted continuously (30–120 µl/h in humans;
Millodot, 2009), hence produced virtually in unlimited amounts for tiny Lisotrigona
but, unlike seasonal owering, are produced year-round.
Finally, under certain circumstances tears could be a crucial alternative to pollen
protein because small bees typically have narrower ying ranges than larger species
(e.g., Araújo et al., 2004). The much larger honey bee has a harvesting range of over 100
km2 (Seeley, 1985), but L. furva’s is only a small fraction of that. Since a small area is
more prone to scarce or temporary lack of owering than a large one due to its lower
biodiversity, tears could compensate or replace pollen protein.
The Signicance of Salt in Tears
No doubt the tears’ salt (NaCl) plays a role. In a review of publications on animals
searching for salt, Bӓnziger (2021) listed seven mammal and three bird families with
species visiting salt licks, and various insects imbibing sweat, tears or visiting salt-
containing puddles, including seven families of lachryphagous moths (Lepidoptera).
Interestingly, many of these zoophilous moths are unable to digest proteins in the adult
stage, including, unexpectedly, the vampire moths (8 species of Calyptra Ochsenheimer,
Erebidae) which sequester salt as the main substance from blood. In Thailand, the
following non-lachryphagous stingless bees are known to sele on human skin to
imbibe sweat: Tetragonula fuscobalteata (Cameron) (Fig. 5), T. hirashimai (Sakagami), T.
pagdeni (Schwarz), T. pagdeniformis (Sakagami), T. sirindhornae (Michener & Boongird),
T. testaceitarsis (Cameron), Lepidotrigona doipaensis (Schwarz), L. avibasis (Cockerell), L.
satun Aasopa & Bӓnziger, and L. terminata (Smith) (Bӓnziger et al., 2009; H.B., unpubl.
data). At present it is not known whether they search for salt, water, or more probably
either of them depending on circumstantial requirements. However, considering the
above-mentioned wide-spread want for salt, generally this is the main resource sought.
Similarly, those Lisotrigona that imbibe perspiration are probably after the salt but,
signicantly, all marked tear collectors consistently harvested only tears, in dry and
humid weather. Hence, despite the importance of salt across the mentioned animal
world, these harvesters prefer tears, although sweat is available over a much wider
body area, and does not require special eye-landing dexterity. Since tears are 200-times
richer in proteins than sweat, this component is a likely reason for their predilection.
Presumably salt is not required in such large amounts as harvested by long-term tear-
sucking Lisotrigona but the surplus can be easily excreted via the Malpighian tubes
(Wigglesworth, 1973).
Journal of Melittology8No. 121
The Signicance of Water in Tears
The tears’ water is likely important in honey dilution and moisture replenishment
during dry hot periods. March to early May tend to have the highest temperature
and lowest humidity at the study sites (T: min-max 26‒35.7 oC, averages 27‒33 oC;
RH: min-max 25‒67%, averages 35‒54%). Dozens of the mentioned sweat sucking
meliponines may crawl at the same time all over one’s skin to avidly lick perspiration,
often in mixed-species assemblages (e.g., Fig. 5) and annoying persistence. Under
such conditions, water appears to be the more important resource, presumably
Figures 3–5. Tear and sweat-drinking stingless bees. 3. Seven workers of Lisotrigona cacciae
(Nurse) imbibing tears from the eye of H. Bӓnziger in self-portrait. The orange-marked bee
(arrow) is on the 21st of her 74 visits of her second day of lachryphagy. 4. Pinned specimen of L.
furva Engel with large corbicular pollen loads. 5. Tetragonula fuscobalteata (Cameron) (left) and
L. furva (right) sucking sweat on wrist of H. Bӓnziger. Note slightly larger T. fuscobalteata with
whitish bands on mesosoma (lacking in L. furva), and yellowish-brown metasoma (blackish in L.
furva). Scale bar 2 mm, except 3 mm in Fig. 3. Photos H. Bӓnziger.
Bӓnziger et al.: Bees that love tears
2024 9
also for Lisotrigona which come in greater numbers, whether sweat-drinking or
tear-harvesting. Despite the abundance and accessibility of sweat, all marked tear-
collecting Lisotrigona kept undeterred their regular bouts in drinking, leaving and
returning to the eyes, throughout their hour-long tear harvesting. The persistent focus
of Lisotrigona on collecting tears, rather than switching to sweat for salt or moisture,
strongly suggest a division of labour within the species. One would expect the marked
Lisotrigona to switch to sweat if it were not for their specic role in harvesting tears,
further emphasizing their specialized task.
Lisotrigona were never seen at water basins placed at the study sites, nor observed to
drink water from natural pool sides or at wet sand at streams where other meliponines,
honey bees, and other hymenopterans gathered. Possibly, guation from plants or
atmospheric water condensation early in the morning may be sucient sources for
these tiny bees. Dew formation in the tree canopy and on ground vegetation is often
very profuse in N Thailand due to marked overnight cooling between December and
March (Bӓnziger, 2021: p 183).
While water could have a cooling function to prevent overheating of the nest
by evaporation of collected water, as found in honey bees (Lindauer, 1954), this
ability is thought to be lacking in meliponines (Roubik, 2006). However, neotropical
Melipona colimana Ayala, and Scaptotrigona depilis (Moure), have recently been found to
regurgitate water and fan their wings to cool down (Macías-Macías et al., 2011; Vollet-
Neto et al., 2015). It is not excluded that Lisotrigona may be able to use tears for cooling,
but in the forest habitat temperatures were mostly below 33 °C during the hoest
months and reached a maximum of 35.7 °C only once. This is below the maximum
brood chamber temperature of 36.2 °C recorded in neotropical Trigona spinipes (F.)
(Zucchi & Sakagami, 1972) and is well below 38.5°C and 40°C when 0% and 50%
mortality, respectively, occurred in S. postica (Latreille) (Macieira & Proni, 2004). For
comparison, optimal brood temperatures for honey bees range between 34 and 36 °C
(Seeley, 1985). Given these relative low temperatures, cooling via tear collection would
likely not be necessary for Lisotrigona.
Hosts
Apart from humans, L. cacciae imbibed tears from cat, dog, chicken (Fig. 6), and the
elongated tortoise [or yellow tortoise, Indotestudo elongata (Blyh)] (Fig. 7), but seling
aempts on rabbit [Oryctolagus cuniculus (Linnaeus)] were repulsed by eye blinking.
Lisotrigona furva also imbibed tears from rabbit and zebu (Bos indicus Linnaeus)
(Bänziger et al., 2009; Bänziger & Bänziger, 2010), with photographic documentation
of lachryphagy of all except from cat and zebu. In Packer (2023), there is a photograph
by K. Kulkarni of a group of Lisotrigona sp. at the eyes of a changeable hawk-eagle
[Nisaetus cirrhatus (Gmelin)] in the wild in Madhya Pradesh, India, and H.B. has noted
in a documentary lm where incidentally tiny meliponines were aacking the eye of
a harpy eagle [Harpia harpyja (Linnaeus)] in South America, and in another where a
minute meliponine was molesting a goliath frog [Conraua goliath (Boulenger)] on its
eye in Cameroon, W Africa. The laer case would be the rst where an amphibian
eye was visited by a stingless bee, but there is need of further observations to conrm
that it was not an anecdotal, abnormal case. Interestingly, contrary to what one would
intuitively expect in birds as sensitive animals, the chicken was the least reactive against
the bees sucking from its eyes. Also, the nictitating membrane of the eye did not aect
the bees, they just continued sucking, at most briey retracting their proboscis.
Journal of Melittology10 No. 121
It is important to point out that all these animals (not considering the non-
reconrmed case of the frog) lack sweat, showing that perspiration plays no role in
aracting Lisotrigona, and that lachryphagy is not an accidental feeding upon sweat.
Rather, that Lisotrigona have developed specialized capabilities to locate and recognize
variously shaped eyes of dierent vertebrates, probably both by vision and olfaction,
to harvest their lachrymation. In humans, though, perspiration could play a role in
aracting tear collectors from a distance.
A problem of bees sucking tears compared with visiting owers is that animals
can be highly mobile. Hence, while the bees avidly imbibe tears, the host may move
beyond the homing range of Lisotrigona which could risk being unable to nd her way
back. Because of this, there was motivation to assess a bee’s returning range while
on lachryphagous duty. This required novel experimental methods, dierent from
conventional ones. One method was to obtain the distance covered by a gently running
host (H.B.) while a marked L. furva sucked his tears, from the starting point where she
had landed on the waiting host to where she ew o once satiated. The distance run
by the host was considered her returning capability, if the same marked bee later came
back to the host at the original starting point (where she had been eye visiting for
some time already) for another tear-drinking bout. This was repeated with the same
marked bee on the host running in the opposite direction. This was required because
the nest’s exact position was not known, but must have been somewhere between
the two direction ends. The most conservative assumption was a position halfway
between the opposite extremes (205 m and 650 m), i.e., 425 m – the distance could not
have been less than this. However, on subsequent surveys (Bӓnziger, unpubl. data) the
nest was found 30 m distance from the waiting place, on a limestone rock face 2.2 m
above ground, a ssure with a tiny tubelet entrance of 4.5x6 mm. Hence the maximum
returning distance must have been up to at least 680 m. The results are preliminary,
the data too limited (9 L. furva examined) for statistical analysis. The distance is very
high for such a minute bee, possibly an adaptation to feeding from mobile vertebrates.
Are there enough acceptable hosts for Lisotrigona to harvest signicant amounts of
tear proteins? As suitable potential hosts (i.e., cat-size and larger), Bӓnziger & Bӓnziger
(2010) mentioned that in Thailand there are, conservatively, some 45 medium- to large-
sized terrestrial mammal species (Lekagul & McNeely, 1977; Francis, 2001; Parr, 2003),
21 phasianid-sized bird species (Lekagul & Cronin, 1974), and 24 turtle- to crocodile-
sized reptilian species (Das, 2010). Several of the hosts are common domestic animals,
and Lisotrigona occasionally nest in house poles or garden trees. Further, animals
are not necessarily on the move all the time but can be site-bound for as long as a
plant in ower when rearing their nestlings for weeks. Ruminants lay down chewing
for hours. Whereas most modern urban people are unlikely to allow tear snatching,
people engaged in hard rural work are less sensitive, and tropical forest natives are
so accustomed to mosquito and other scourges that they will tolerate Lisotrigona as a
minor nuisance.
Interestingly, in diversity of host spectrum, spanning three vertebrate classes,
Lisotrigona beat their moth (Lepidoptera) homologues whose lachryphagy is,
essentially, restricted to mammals as the only class. This dearth is not due to lack
of data, because tear-drinking moths are comparatively well-researched, discovered
already a century ago (e.g., de Joannis, 1911; Büiker & Whellan, 1966; Bӓnziger &
Büiker, 1969; Bӓnziger, 1988, 1995) and counting more than 100 species in seven
families (Bӓnziger, 2021: p 67, 191). An important dierence to Lisotrigona is that
being nocturnal reduces visual detection by their hosts and, due to drowsiness, the
Bӓnziger et al.: Bees that love tears
2024 11
hosts’ alertness and tactile sensitivity. This allows far larger sizes in these moths (up
to 84 mm wingspan in notodontid Tarsolepis remicauda Butler), and more aggressive
behaviour. Some species can cause pain to eyes due, not to their proboscis, which
apically is relatively soft but, as photographically documented, mainly by clawing of
the eyelid (Figs. 8, 9). In drepanid Chaeopsestis ludovicae Le Cerf, wingspan 45 mm, the
foretarsi alone of 4.4 mm length is much longer than the entire body length of L. furva
(2.7‒3.3 mm; in Fig. 8 the foretarsi may appear shorter but this is due to their inclined
position).
Figures 6–9. Tear-drinking stingless bees and moths. 6. Lisotrigona furva Engel drinking tears
from the eye of a chicken. 7. Lisotrigona furva imbibing owed-down tears from the eye of an
elongated tortoise [Indotestudo elongata (Blyh)]. 8, 9. Drepanid moth Chaeopsestis ludovicae Le Cerf
imbing tears from the eye of H. Bӓnziger in self-portrait. Note the moth’s foretarsi clawing the
eyelid (arrows in photo 8, lines in drawing 9). Modied from H. Bӓnziger (1992). Scale bars 6
mm. Photos H. Bӓnziger.
Journal of Melittology12 No. 121
Medical and Veterinary Signicance
The feeding from such a wide host spectrum in three vertebrate classes, some
as domestic animals in close vicinity to humans, can have medical and veterinary
implications. Previously, stingless bees most likely to pose a health danger were
necrophagous and lth visiting species in Peru (Baumgartner & Roubik, 1989), but
these bees were considered of only minimal danger as vectors of pathogens because
their species richness and abundance was highest in asynanthropic areas (lacking
human selements), and they did not sele on humans to feed. Lisotrigona are both
synanthropic and asynanthropic. Not only can they sele on humans in numbers, but
tend to do so repeatedly and, signicantly, at a very exposed site for pathogen entrance
(see below), viz. the ocular surface with the conjunctiva of the lids. Transmission could
occur via contact of the bees’ foretarsi and proboscis applied to the lid’s conjunctiva,
the proboscis also reaching into the trough between the conjunctiva and eye ball and,
occasionally, brief direct contact with the eye ball. The antennae also touch from time
to time the ocular surfaces. Importantly, L. furva and L. cacciae exhibited readiness to
use multiple hosts, viz. zebu-man and man-dog, respectively (Bӓnziger et al., 2009: p
141).
Potentially, Lisotrigona could pose a danger similar to eye gnats (Chloropidae),
suspected vectors of the bacterium Haemophilus inuenzae biogroup aegyptius (Hae),
which causes conjunctivitis in human and, in virulent forms, Brazilian Purpuric
Fever, which is highly lethal to young children (e.g., Paganelli & Sabrosky, 1993).
More recently, Miner et al. (2016) found the Zika virus to cause eye inammation and
shedding of the virus in mice tears.
Of particular signicance is ophthalmologist Coroneo (2021) who reviewed the
evidence that ocular and periocular tissue in human may be uniquely placed as an
entry portal for viral invasion and primary site of virus replication. Also, he drew
aention that Dr. Li Wenliang, the whistle-blower who warned about the outbreak of
COVID-19 in late 2019 and subsequently died from it, was an ophthalmologist who
probably got infected by SARS-CoV-2 via the eyes in Wuhan, China. In retrospect,
although H.B. (2018) assessed the risk of pathogen transmission by lachryphagous
Lisotrigona as remote, his decision to be sole experimenter during his eld study, was,
after all, appropriate.
Possible Origin and Evolution of Lachryphagy in Stingless Bees
It has been proposed that tear collecting in stingless bees may have originated in
connection with humans (Bӓnziger, 2018) because, unique among vertebrates (except
amphibians and hippopotamuses) in producing signicant amounts of perspiration,
they are visited by sweat-sucking meliponines, at times in large and diverse
assemblages. Among these, the minute-sized species were preadapted to develop tear
collectors, thanks to their reduced visibility, weaker mechanical impact, and gentler
feeding act, such that some of the tiniest species have evolved behaviours to snatch
lachrymation without much disturbance. Moreover, a feature may have facilitated
bee-human contact: meliponine nests in limestone hollows entered through ssures
in rock faces (Bӓnziger & Bӓnziger, 2010; Bӓnziger et al. 2011). The many types of
meliponine nests are otherwise well-known (e.g., Wille & Michener, 1973; Camargo
& Pedro, 2003; Rasmussen & Camargo, 2008; Roubik, 2006) overwhelmingly from
the neotropics, but some also from Thailand (Inson, 2006; Khamyotchai, 2014), not so
Bӓnziger et al.: Bees that love tears
2024 13
nests in limestone ssures. But in some natural habitats of W and N Thailand, H.B.
has found more stingless bee nests in limestone faces than in tree trunks at least
12 meliponine species, from the smallest to the largest. Early humans frequented or
lived in limestone caves for generations already 105‒106 years ago when, thanks to this
close vicinity, lachryphagy may have originated in Lisotrigona or her ancestors. An
alternative to this two step (rst sweat, then tears) hypothesis might be an earlier, 30‒70
million years ago (mya), direct araction to eyes of birds or mammals as a source of
moisture during geologically periods of drier climate. Whether due to periodical water
or salt constraints, in the course of time tear-drinking could have evolved into a year-
round feeding habit, thanks to the tears’ reliable content of ready-to-digest dissolved
proteins as nutrition. Roubik (2023) expanded on this and conjectured a yet earlier
possible lachryphagy when meliponines might have recruited nestmates to dinosaur
eyes in late Cretaceous times (90 mya). Stingless bees have been detected in amber
dating back 95‒70 mya (Michener & Grimaldi, 1988) and were therefore contemporary
with the late dinosaurs. Perhaps, because in those early times owering plants were
still uncommon – notwithstanding the then already presence of gymnosperms which
produce pollen, though theirs is mostly wind-dispersed – primitive meliponines’ diet
may have consisted substantially of animal-derived proteins, including tears. Yet,
all three proposals could be correct. Lachryphagy may have been developed, lost
and redeveloped more than once by Lisotrigona and her ancestors, not necessarily
phylogenetically related, during the 90 mya years since the appearance of stingless bees.
For comparison, cleptoparasitism originated at least four times in Apidae (Cardinal et
al., 2010). Interestingly, whereas minuteness appears to be a sine qua non condition for
developing lachryphagy, not all minute meliponines exhibit tear-drinking habits. The
smallest exponent of the widespread and species-rich genus Tetragonula Moure is the
tiny T. fuscobalteata, head width 1.39‒1.46 mm (Sakagami, 1978), hence only slightly
larger than L. furva. It is one of six species of Tetragonula frequently found to suck
sweat from H.B. (Fig. 5), but never his tears, nor are we aware of any report of an eye
visitation from anywhere, although it is common and wide-spread, from mainland
SE Asia to Sumatra, Borneo, the Philippines, and Sulawesi (Schwarz, 1939; Sakagami,
1978; Rasmussen, 2008; Lee et al., 2016). This is interpreted as a further indication
that lachryphagy is not a simple uptake of uid, but a result of special behavioural
adaptations developed only by a select group of stingless bees for harvesting tears
under the very eyes of their victims.
Future Studies
Our study focused on wild Lisotrigona populations in forest habitat to avoid potential
non-typical behaviours (e.g., meliponinary bees, degraded environment). Results
suggest that tear drinking in Lisotrigona is neither accidental nor for individual bees’
needs, but for colony requirements, by specialized tear collectors with an indication
of a part-time division of labour. However, new questions arose and, since now
lachryphagy is no more in doubt, future investigations should include experiments
with bees inside and in close connection with nests/hives, with possible invasive
techniques and use of articial tears to avoid pathogen transmission.
Main questions are: Do Lisotrigona regurgitate their tear harvest to receiver bees
as proposed above, rather than into honey or pollen pots, or brood cells? Are tear
proteins eaten and assimilated by Lisotrigona’s brood? Do Lisotrigona disgorge tears
onto nest surfaces and fan with their wings to cool the nest during very hot, life-
Journal of Melittology14 No. 121
threatening temperatures, but not during the ‘normal’ forest temperatures we found?
Do only some of the workers exhibit lachryphagy, or can it occur in all workers, and
is it exhibited at a late age? When seled on human skin, do Lisotrigona imbibe sweat
to cover their individual needs, or do they repeatedly return for additional harvesting
for colony requirements, and if so, where do they regurgitate it: to adult nest inmates,
into pots, brood cells, or nest surfaces?
ACKNOWLEDGEMENTS
We are indebted to Laurence Packer for valuable comments; to Robert W. Sites for
his evaluation of H.B.’s 2018 article; to Charles D. Michener and Somnuk Boongird
for their initial help in meliponine taxonomy; to Korrawat Aasopa and Chun-I Chiu
for valuable suggestions; to Orapan Kankonsue and Tossapol Moonmanee for nding
dicult references; and to three peer reviewers for comments on the manuscript.
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The Journal of Meliology is an international, open access journal that seeks to rapidly
disseminate the results of research conducted on bees (Apoidea: Anthophila) in their
broadest sense. Our mission is to promote the understanding and conservation of wild and
managed bees and to facilitate communication and collaboration among researchers and the
public worldwide. The Journal covers all aspects of bee research including but not limited to:
anatomy, behavioral ecology, biodiversity, biogeography, chemical ecology, comparative
morphology, conservation, cultural aspects, cytogenetics, ecology, ethnobiology, history,
identication (keys), invasion ecology, management, meliopalynology, molecular
ecology, neurobiology, occurrence data, paleontology, parasitism, phenology, phylogeny,
physiology, pollination biology, sociobiology, systematics, and taxonomy.
The Journal of Meliology was established at the University of Kansas through the
eorts of Michael S. Engel, Victor H. Gonzalez, Ismael A. Hinojosa-Díaz, and Charles D.
Michener in 2013 and each article is published as its own number, with issues appearing
online as soon as they are ready. Papers are composed using Microsoft Word® and Adobe
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A Journal of Bee Biology, Ecology, Evolution, & Systematics
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Chulalongkorn University, Thailand
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University of Kansas
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University of Kansas
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Article
Full-text available
Wild Lisotrigona cacciae (Nurse) and L. furva Engel were studied in their natural forest habitat at three sites in northern Thailand, May 2013-November 2014. The author, both experimenter and tear source, marked the minute bees while they drank from his eyes viewed in a mirror. All marked workers, 34 L. cacciae and 23 L. furva, came repeatedly to engorge, 34 and 27 times on average, respectively. The maximum number of times the same L. cacciae and L. furva came was 78 and 144 visits in one day, respectively; the maximum over two days was 145 visits by one L. cacciae; the maximum number of visiting days by the same bee was four over seven days by one L. furva which made 65 visits totally. The same forager may collect tears for more than 10 h in a day, on average for 3 h 15 min and 2 h 14 min for L. cacciae and L. furva, respectively. Engorging from the inner eye corner averaged 3.1 and 2.2 min, respectively, but only 1.3 and 0.9 min when settled on the lower eye lid/ciliae. The interval between consecutive visits averaged 3.3 min and 3.8 min, respectively. Lachryphagy occurred during all months of the year, with 91-320 foragers a day during the hot season and 6-280 foragers during the rainy season; tear collecting resumed after a downpour. During the cold season eye visitation was reduced to 3-64 foragers, but none left her nest when the temperature was below 22°C. Flying ranges were greater than in comparable non-lachryphagous meliponines. It is proposed that Lisotrigona colonies have workers that are, besides nectar and pollen foragers, specialized tear collectors. Tears are 200 times richer in proteins than sweat, a secretion well-known to be imbibed by many meliponines. Digestion of proteins dissolved in tears is not hampered by an exine wall as in pollen, and they have bactericidal properties. These data corroborate the inference that Lisotrigona, which also visit other mammals, birds and reptiles, harvest lachrymation mainly for its content of proteins rather than only for salt and water.
Article
Full-text available
Zika virus (ZIKV) is an emerging flavivirus that causes congenital abnormalities and Guillain-Barré syndrome. ZIKV infection also results in severe eye disease characterized by optic neuritis, chorioretinal atrophy, and blindness in newborns and conjunctivitis and uveitis in adults. We evaluated ZIKV infection of the eye by using recently developed mouse models of pathogenesis. ZIKV-inoculated mice developed conjunctivitis, panuveitis, and infection of the cornea, iris, optic nerve, and ganglion and bipolar cells in the retina. This phenotype was independent of the entry receptors Axl or Mertk, given that Axl−/−, Mertk−/−, and Axl−/−Mertk−/− double knockout mice sustained levels of infection similar to those of control animals. We also detected abundant viral RNA in tears, suggesting that virus might be secreted from lacrimal glands or shed from the cornea. This model provides a foundation for studying ZIKV-induced ocular disease, defining mechanisms of viral persistence, and developing therapeutic approaches for viral infections of the eye.
Article
Oculo-centric factors may provide a key to understanding invasion success by SARS-CoV-2, a highly contagious, potentially lethal, virus with ocular tropism. Respiratory infection transmission via the eye and lacrimal-nasal pathway elucidated during the 1918 influenza pandemic, remains to be explored in this crisis. The eye and its adnexae represent a large surface area directly exposed to airborne viral particles and hand contact. The virus may bind to corneal and conjunctival angiotensin converting enzyme 2 (ACE2) receptors and potentially to the lipophilic periocular skin and superficial tear film with downstream carriage into the nasopharynx and subsequent access to the lungs and gut. Adenoviruses and influenza viruses share this ocular tropism and despite differing ocular and systemic manifestations and disease patterns, common lessons, particularly in management, emerge. Slit lamp usage places ophthalmologists at particular risk of exposure to high viral loads (and poor prognosis) and as for adenoviral epidemics, this may be a setting for disease transmission. Local, rather than systemic treatments blocking virus binding in this pathway (advocated for adenovirus) are worth considering. This pathway is accessible with eye drops or aerosols containing drugs which appear efficacious via systemic administration. A combination such as hydroxychloroquine, azithromycin and zinc, all of which have previously been used topically in the eye and which work at least in part by blocking ACE2 receptors, may offer a safe, cost-effective and resource-sparing intervention.
Book
I Development in the Egg.- References.- II The Integument.- Properties of the cuticle.- Formation and shedding of the cuticle.- References.- III Growth.- Moulting.- Metamorphosis.- Determination of characters during post-embryonic development.- Regeneration.- Diapause.- References.- IV Muscular System and Locomotion.- Anatomy and histology.- Physiological properties of insect muscles.- Locomotion.- References.- V Nervous and Endocrine Systems.- Nervous system.- Visceral nervous system.- Endocrine system.- References.- VI Sense Organs: Vision.- Compound eye.- Simple eyes.- References.- VII Sense Organs: Mechanical and Chemical Senses.- Mechanical senses.- Hearing.- Chemical senses.- Temperature and humidity.- References.- VIII Behaviour.- Kinesis and related phenomena.- Orientation.- Co-ordinated behaviour.- References.- IX Respiration.- Tracheal system.- Development of the tracheal system.- Transport of oxygen to the tracheal endings.- Elimination of carbon dioxide.- Respiration of aquatic insects.- Respiration of endoparasitic insects.- Respiratory function of the blood.- Regulation of respiratory movements.- References.- X The Circulatory System and Associated Tissues.- Circulatory system.- Haemolymph.- Haemocytes.- Pericardial cells and so-called 'nephrocytes'.- Fat body.- Oenocytes.- Light-producing organs.- References.- XI Digestion and Nutrition.- Fore-gut.- Peritrophic membrane.- Mid-gut.- Hind-gut.- Secretions of the alimentary canal.- Digestion of some skeletal and other substances of plants and animals.- The role of lower organisms in digestion.- Nutrition.- References.- XII Excretion.- Urine.- Intermediary nitrogen metabolism.- Malpighian tubes.- Histophysiology of the Malpighian tubes.- Accessory functions of Malpighian tubes.- Malpighian tubes during moulting and metamorphosis.- Cephalic excretory organs and intestinal excretion.- Storage excretion.- References.- XIII Metabolism.- Chemical transformations.- Some chemical products of insects.- Pigment metabolism.- Respiratory metabolism.- References.- XIV Water and Temperature.- Water relations.- Temperature relations.- References.- XV Reproductive System.- Female reproductive system.- Male reproductive system.- Mating, impregnation and fertilization.- Some factors controlling fertility and fecundity.- Special modes of reproduction.- Sex determination.- Transmission of symbiotic micro-organisms.- References.- Index of Authors.- General Index.