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Antibacterial activity of honey from the Australian stingless bee Trigona carbonaria



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International Journal of Antimicrobial Agents 32 (2008) 89–98
Letters to the Editor
Antibacterial activity of honey from the Australian
stingless bee Trigona carbonaria
Honey produced by European honeybees (Apis mellif-
era) has been well studied for its antimicrobial properties,
and selected honeys display broad-spectrum antimicrobial
activity against a range of pathogens [1]. This activity
stems primarily from the production of hydrogen peroxide
by glucose oxidase, a bee-derived enzyme. Some honeys
also possess non-hydrogen peroxide-dependent antimicro-
bial activity that is linked to phytochemical factors derived
from the floral source and is particularly potent in honeys
from certain Leptospermum species such as manuka (Lep-
tospermum scoparium)[1,2]. However, few studies have
examined honey from stingless bees, a diverse group of the
highly eusocial bees. Trigona carbonaria is a stingless bee
of the east coast of Australia and is the country’s most com-
monly domesticated stingless bee species. The flavour and
aroma of Trigona honey is distinct from the honey of A.
mellifera and little is known about its antimicrobial prop-
erties. Therefore, the aim of this study was to investigate the
antibacterial activity of Australian T. carbonaria honey.
Twenty-two Trigona honey samples were collected from
separate hives in various locations around Brisbane (Queens-
land, Australia) between July and November 2006. One
sample (Sample 14) was collected from a hive of an unknown
species of Trigona; the remaining 21 samples were from hives
of T. carbonaria. Honey samples were assayed for antibac-
terial activity against Staphylococcus aureus ATCC 9144
using an agar well diffusion method described by Allen et al.
[2]. Briefly, 25% (w/v) solutions of honey were prepared in
sterile deionised water to test total activity (including hydro-
gen peroxide-dependent activity) and in 2800 U/mL catalase
solution to test non-peroxide activity. Solutions of 2–7%
(w/v) phenol were prepared in sterile deionised water and
zones of inhibition produced by these solutions were used to
generate a standard curve. A commercially available manuka
honey (Comvita, Te Puke, New Zealand) was included in
each plate as a positive control. All solutions were tested
in duplicate during each assay and each honey sample was
tested on at least five separate occasions over a period of up
to 30 weeks.
The antibacterial activities of the 22 samples of Trigona
honey are shown in Table 1. The initial total antibacte-
rial activity of the T. carbonaria honey samples was high
(mean 26.3% (w/v) phenol equivalent) compared with the
manuka honey control (mean total activity 18.0 ±0.9%
phenol equivalent; mean non-peroxide activity 17.5±1.0%
phenol equivalent) and other A. mellifera honeys (mean
13.4% (w/v) phenol equivalent) [2]. Previous studies on
the antibacterial activity of Meliponini honeys using various
methods have found a range of activities from non-inhibitory
[3] to effectively inhibiting both Gram-positive and Gram-
negative organisms [3–6].
The antibacterial activity of A. mellifera honey is sta-
ble over time [2], whereas the hydrogen peroxide-dependent
activity of 15 of the T. carbonaria honey samples (Samples
6, 7, 9–13 and 15–22) decreased by at least 4% (w/v) phenol
equivalent over the experimental period. This may be due to
the intrinsically higher water content of stingless bee honey;
however, the activity of seven samples (Samples 1–5, 8 and
14) was stable across all replicates. Little is known about
the biochemistry of T. carbonaria and it is likely that the
enzymes added during the conversion of nectar to honey are
different to those of A. mellifera. This may result in varying
stability of either the enzyme producing hydrogen peroxide
or the hydrogen peroxide itself. The non-peroxide activity
present in all 22 samples was largely stable throughout the
experimental period.
Temaru et al. [6] identified non-peroxide activity in honey
samples from nine species of stingless bees from various
geographic regions and suggested that this was due to phy-
tochemical factors. Non-peroxide activity in A. mellifera
honeys is rare and is most commonly reported in hon-
eys derived from Leptospermum species. However, this is
unlikely to be the case for these Trigona honeys as the hives
were situated in suburban areas with a low abundance of
Leptospermum and in some cases the flowering period was
outside the 6-month foraging period prior to honey extrac-
tion. This, together with the fact that all the honey samples
possessed non-peroxide activity, indicates an entomological
rather than a phytochemical source of the activity. Cuticular
secretions from T. carbonaria have been reported to inhibit
bacterial growth [7] and may be linked to this activity in T.
carbonaria honey.
0924-8579/$ – see front matter © 2008 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.
90 Letters to the Editor / International Journal of Antimicrobial Agents 32 (2008) 89–98
Table 1
Antibacterial activity of Trigona honey expressed as mean % (w/v) phenol equivalent
Sample number Initial antibacterial activityaFinal antibacterial activityb
Sample age (weeks) Total activity Non-peroxide activity Sample age (weeks) Total activity Non-peroxide activity
1 10 19.0 ±1.13 18.4 ±0.07 40 23.1 ±0.21 21.7 ±0.21
2 10 28.5 ±0.78 17.3 ±1.63 40 27.8 ±0.28 19.6 ±0.14
3 10 27.5 ±0.07 18.0 ±1.91 40 26.0 ±0.35 21.0 ±0.99
4 10 25.3 ±1.56 19.4 ±1.41 40 26.8 ±0.07 21.6 ±0.07
5 6 17.5 ±0.92 13.6 ±0.92 28 16.3 ±0.14 14.9 ±0.57
6 6 25.6 ±0.28 12.6 ±0.21 28 17.4 ±0.71 14.0 ±0.49
7 6 28.9 ±0.64 14.9 ±0.07 28 20.4 ±0.64 18.1 ±0.35
8 3 26.4 ±0.07 23.7 ±0.14 24 24.3 ±0.42 21.5 ±0.00
9 10 23.8 ±0.00 16.4 ±0.14 30 18.2 ±1.56 17.8 ±0.42
10 7 23.7 ±0.57 15.1 ±1.06 28 18.5 ±0.28 16.7 ±0.07
11 3 25.0 ±0.57 13.2 ±0.14 25 22.0 ±0.07 14.6 ±0.49
12 6 27.0 ±0.57 16.2 ±0.57 28 21.4 ±0.35 18.1 ±0.35
13 6 25.6 ±1.84 13.7 ±0.42 28 19.4 ±0.14 16.2 ±0.28
14 6 20.4 ±0.07 16.1 ±0.57 28 19.5 ±0.85 18.3 ±0.49
15 9 27.5 ±0.57 13.4 ±0.64 23 14.2 ±0.00 12.3 ±0.00
16 9 29.6 ±0.28 11.5 ±0.35 23 11.5 ±0.07 11.1 ±0.21
17 9 28.6 ±0.14 13.3 ±0.42 23 17.1 ±2.33 13.4 ±0.57
18 7 27.6 ±0.49 16.5 ±0.28 20 19.3 ±0.71 16.5 ±0.64
19 7 27.4 ±0.64 17.3 ±0.14 20 18.4 ±0.00 18.0 ±0.49
20 7 30.8 ±0.71 14.7 ±0.14 20 16.1 ±2.12 13.9 ±0.14
21 7 31.5 ±1.13 13.8 ±0.35 20 25.2 ±0.57 13.9 ±0.49
22 7 32.1 ±0.78 13.4 ±0.28 20 16.1 ±0.42 14.7 ±0.21
aBased on initial four replicates.
bBased on final two replicates.
This is the first comprehensive study of the antimicrobial
activity of native Australian Trigona honey. All of the honey
samples possessed a high level of antibacterial activity and
a substantial proportion of this was stable in the presence
of catalase and over time. Non-peroxide activity is particu-
larly advantageous when using honey in clinical situations as
it is not destroyed by catalase present in serum. Whilst fur-
ther studies are required to establish the spectrum of activity
of Trigona honey against other pathogens, the stability and
potency of this activity in T. carbonaria honey indicates its
potential use as a therapeutic agent.
Manuka honey was kindly supplied by Comvita, Te Puke,
New Zealand.
Funding: Rural Industries Research and Development
Corporation Honeybee Committee grant number US-128A.
J.I. is supported by an Australian Postgraduate Award and
a Rural Industries Research and Development Corporation
top-up scholarship.
Competing interests: None declared.
Ethical approval: Not required.
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[2] Allen KL, Molan PC, Reid GM. A survey of the antibacterial activity of
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[3] DeMera JH, Angert ER. Comparison of the antimicrobial activity of
honey produced by Tetragonisca angustula (Meliponinae) and Apis mel-
lifera from different phytogeographic regions of Costa Rica. Apidologie
(Celle) 2004;35:411–17.
[4] Garedew A, Schmolz E, Lamprecht I. Microcalorimetric investigation
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and comparison of some parameters with those obtained with standard
methods. Thermochim Acta 2004;415:99–106.
[5] Miorin PL, Levy Jr NC, Custodio AR, Bretz WA, Marcucci MC.
Antibacterial activity of honey and propolis from Apis mellifera and
Tetragonisca angustula against Staphylococcus aureus.J Appl Microbiol
[6] Temaru E, Shimura S, Amano K, Karasawa T. Antibacterial activity of
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Julie Irish
Dee A. Carter
Shona E. Blair
School of Molecular and Microbial Biosciences,
Building G08, University of Sydney,
New South Wales 2006, Australia
Tim A. Heard
CSIRO Entomology, 120 Meiers Road, Indooroopilly,
Queensland 4068, Australia
Corresponding author. Tel.: +61 2 9351 6041;
fax: +61 2 9351 4571.
E-mail address:
(J. Irish)
doi: 10.1016/j.ijantimicag.2008.02.012
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The purpose of the present study was to investigate and compare the demonstrated variation in antimicrobial activity of honey produced by introduced A. mellifera and the stingless bee, Tetragonisca angustula, commonly kept in hives in Costa Rica. There was no difference in activity of honey produced by Apis mellifera and T. angustula against the 5 microbes tested. Honey from different phytogeographic regions exhibited differential antimicrobial activity and susceptibility of yeasts to honey of either species was greater than that of bacteria.
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The antibacterial activity against Staphylococcus aureus of honey and propolis produced by Apis mellifera and Tetragonisca angustula was evaluated. Secondary aims included the study of the chemical composition of propolis and honey samples and its relationship with antibacterial activity against S. aureus. The antibacterial activity of honey and propolis was determined by the method of macrodilution. The minimum inhibitory concentration (MICs) of A. mellifera honey ranged from 126.23 to 185.70 mg ml(-1) and of T. angustula from 142.87 to 214.33 mg ml(-1). For propolis, the MIC ranged from 0.36 to 3.65 mg ml(-1) (A. mellifera) and from 0.44 to 2.01 mg ml(-1) (T. angustula). Honey and propolis were evaluated by high-performance liquid chromatography. Some typical compounds of Brazilian propolis were also identified in honey samples. Principal component analysis revealed that the chemical composition of honey and propolis samples was distinct based on the geographical location of the samples. Propolis samples had higher antibacterial activity against S. aureus when compared with honey. However, both propolis and honey samples had antibacterial against S. aureus. These antimicrobial properties would warrant further studies on the clinical applications of propolis and honey against S. aureus.
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Evidence for the antiquity and importance of microbial pathogens as selective agents is found in the proliferation of antimicrobial defences throughout the animal kingdom. Social insects, typified by crowding and often by low genetic variation, have high probabilities of disease transmission and eusocial Hymenoptera may be particularly vulnerable because of haplodiploidy. Mechanisms they employ to reduce the risk of disease include antimicrobial secretions which are particularly important primary barriers to infection. However, until now, whether or not there is selection for stronger antimicrobial secretions when the risk of disease increases because of sociality has not been tested. Here, we present evidence that the production of progressively stronger antimicrobial compounds was critical to the evolution of sociality in bees. We found that increases in group size and genetic relatedness were strongly correlated with increasing antimicrobial strength. The antimicrobials of even the most primitive semi-social species were an order of magnitude stronger that those of solitary species, suggesting a point of no return, beyond which disease control was essential. Our results suggest that selection by microbial pathogens was critical to the evolution of sociality and required the production of strong, front-line antimicrobial defences.
Honey has been used as a medicine since ancient times in many cultures and is still used in ‘folk medicine’. The use of honey as a therapeutic substance has been rediscovered by the medical profession in more recent times, and it is gaining acceptance as an antibacterial agent for the treatment of ulcers and bed sores, and other infections resulting from burns and wounds. In many of the cases in the cited reports, honey was used on infections not responding to standard effective in rapidly clearing up infection and promoting healing. Honey has also been found to be effective in treating bacterial gastoentertis in infants. This is the published version of an article published in the journal: Bee World. Used with permission.
To assess the variation in antibacterial activity of honey a survey was carried out on 345 samples of unpasteurized honey obtained from commercial apiarists throughout New Zealand. Most of the honeys were considered to be monofloral, from 26 different floral sources. The honeys were tested against Staphylococcus aureus in an agar well diffusion assay, with reference to phenol as a standard. Antibacterial activity was found to range from the equivalent of less than 2% (w/v) phenol to 58% (w/v) phenol, with a median of 13.6 and a standard deviation of 12.5. Neither the age of the honey samples nor whether they had been processed by the apiarist was associated with lower activity. However, the difference between floral sources in the antibacterial activity was very highly significant. Kanuka (Kunzea ericoides (A. Rich.) J. Thompson. Family: Myrtaceae), manuka (Leptospermum scoparium J. R. et G. Forst. Family: Myrtaceae), ling heather (Calluna vulgaris (L.) Hull. Family: Ericaceae) and kamahi (Weinmannia racemosa Linn. f. Family: Cunoniaceae) were shown to be sources likely to give honey with high antibacterial activity. When antibacterial activity was assayed with catalase added to remove hydrogen peroxide, most of the honeys showed no detectable antibacterial activity. Only manuka and vipers bugloss (Echium vulgare L. Family: Boraginaceae) honeys showed this type of activity in a significant proportion of the samples. The high antibacterial activity of manuka honey was in many cases due entirely to this non-peroxide component.
The aim of the study was to examine antibacterial activity of the honey of stingless honeybees (Meliponinae). An agar well diffusion assay demonstrated that many honey samples of stingless honeybees inhibited the growth of test strains of Staphylococcus aureus, Enterococcus faecalis, Escherichia coli and Pseudomonas aeruginosa; moreover, they exhibited non-peroxide antibacterial activity against those strains. This is the first time that non-peroxide antimicrobial activity of honey from a number of species of stingless honeybees has been demonstrated. These antibacterial activities appear to be powerful, even when compared to those of"manuka honey" from Apinae honeybees.
A survey of the antibacterial activity of some New Zealand honeys
  • Allen Kl Molan
  • Pc
  • Reid
  • Gm
Allen KL, Molan PC, Reid GM. A survey of the antibacterial activity of some New Zealand honeys. J Pharm Pharmacol 1991;43:817–22.
Australia Tim A. Heard CSIRO Entomology, 120 Meiers Road
  • Julie Irish
  • A Dee
  • Carter
  • E Shona
Julie Irish * Dee A. Carter Shona E. Blair School of Molecular and Microbial Biosciences, Building G08, University of Sydney, New South Wales 2006, Australia Tim A. Heard CSIRO Entomology, 120 Meiers Road, Indooroopilly, Queensland 4068, Australia * Corresponding author. Tel.: +61 2 9351 6041; fax: +61 2 9351 4571. E-mail address: (J. Irish) doi: 10.1016/j.ijantimicag.2008.02.012