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Keywords: Stingless bee honey has been reported to not meet the quality standards set for honey. In response, researchers
Food analysis from Venezuela and Malaysia have proposed unique quality standards for stingless bee honey. The aim of this
Food composition review is to compile the available data on the physicochemical properties of stingless bee honey already studied
Stingless bee from all over the world to propose a harmonized global quality standard for stingless bee. The literature review
Honey
resulted in the inclusion of 40 studies, assessing 522 honey samples, from 67 different species of stingless bee,
Meliponiculture
habituating 12 countries from all over the world. Taking into account the variety of bee species and the geo-
Physicochemical characteristics
Quality standards graphical origin for the collection of honey, enormous variability in terms of honey’s moisture content, free
Quality criteria acidity, pH, hydroxymethylfurfural content, ash content, electrical conductivity, sugar content, enzyme activity,
nitrogen content, soluble solids, minerals composition, phenolic compound, and color were observed. Stingless
bee honey possessed greater moisture content, higher acidity, lower sugar composition, and lower enzyme ac-
tivity in stingless bees compared to Apis mellifera bees. This review justifies the need for a more harmonized
standard of this food product, which will include stingless bee honey from around the globe.
1. Introduction globe. There are approximately 500 stingless bee species and 64 dif-
ferent genera have been identified (Michener, 2013). They are dis-
As the name suggests, the stingless bee species lacks a sting. They tributed in Latin America (Melipona, Tetragonisca, Scaptotrigona, and
belong to the same family as the sting bee, Hymenoptera, but differ at Plebeia), the mainland of Australia (Tetragonula), Africa (Meliponula),
the subfamily level. While the sting bee belongs to the Apis subfamily, and tropical parts of Asia (Lepidotrigona, Tetrigona, Homotrigona, Li-
the stingless bee belongs to the Meliponinae subfamily. Both bees sotrigona) (Biluca et al., 2016; Chuttong et al., 2016; Oddo et al., 2008;
produce honey and other bee by-products, such as pollen, bees wax, Souza et al., 2006). Hence, beekeeping practice with the stingless bee is
propolis and royal jelly (Rasmussen and Cameron, 2010). The most a better-known tradition in tropical countries such as Malaysia, Thai-
commonly-known honey in the world comes from the sting bee species land, Mexico, Venezuela, Brazil and Australia.
Apis mellifera. Unlike their counterpart, stingless bees store their honey In addition to their abundance in tropical climates, the relatively
in vertical pots made of cerumen (Abd Jalil et al., 2017; Vit et al., easy management of stingless bee farming has facilitated its popularity
2004). Cerumen, as it is exclusively known, is different to Apis mellifera among beekeepers. Because it does not sting, it is easier to extract the
propolis. Propolis is a natural resinous and waxy product that is pro- honey, pollen, and propolis compared with the extraction of sting bee
duced by mixing beeswax and resins collected from a variety of plant honey, which requires proper safety equipment and training (Abd Jalil
parts by Apis mellifera bees. In contrast, cerumen is a mixture that is et al., 2017). Furthermore, the stingless bees are not obnoxious in
similar to propolis but with the addition of the mandibular secretion of choosing the place to build their hive. As a result, it is easier to build an
the stingless bee during its construction (Simone-Finstrom and Spivak, artificial hive to manipulate the colony and increase the honey pro-
2010). duction compared to the honey bees, which are often lost and ismore
Stingless bees habituate the warm and humid forests around the vulnerable to diseases (Abd Jalil et al., 2017).
⁎
Corresponding author.
E-mail address: ruszymah@ppukm.ukm.edu.my (R.B.H. Idrus).
https://doi.org/10.1016/j.jfca.2018.06.002
Received 5 February 2018; Received in revised form 27 May 2018; Accepted 1 June 2018
Available online 01 June 2018
0889-1575/ © 2018 Elsevier Inc. All rights reserved.
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
According to the Codex Alimentarius (2001), honey is the natural quality. In 2001, the Codex Alimentarius was revised and the para-
sweet substance produced by honey bees from the nectar of plants or meters for honey quality were set (International Honey Commission,
from secretions of living parts of plants or excretions of plant sucking 2009).
insects on the living parts of plants, which the bees collect, transform by A good quality honey should have a moisture content that is not
combining with specific substances of their own, deposit, dehydrate, more than 20 g/100 g, and a sum of both fructose and glucose that is
store and leave in the honey comb to ripen and mature. However, this not less than 60 g/100 g, sucrose content that is not more than 5 g/
definition is specific to the honey produced by Apis mellifera bee and 100 g, free acidity of not more than 50 milliequivalents acid per 1 kg
may not apply to the stingless bee honey. Accordingly, quality stan- (meq/kg), ash content that is not more than 0.5 g/100 g, diastase ac-
dards have been laid out for Apis mellifera honey by the International tivity that is not less than 8 diastase number (DN), hydro-
Honey Commission (2009). Many have reported that stingless bee xymethylfurfural (HMF) content that is not more than 40 mg/kg, and
honey did not meet these quality standards, stressing the need for an electrical conductivity of not more than 0.8 mS/cm, and some other
exclusive standard of its own (Biluca et al., 2016; Chuttong et al., 2016; parameters with slight exception for certain types of honey as listed in
Oddo et al., 2008; Moniruzzaman et al., 2014; Vit et al., 1994; Gonnet the Codex Alimentarius.
et al., 1964). However, due to the insufficient knowledge of its com- However, the IHC standard for honey has been found to be un-
position, establishing quality standards for the stingless bee is difficult. favorable to the honey produced by stingless bees. A study done by
In Malaysia, efforts to establish Malaysian stingless bee honey Gonnet et al. in 1964 observed a higher moisture, invertase activity,
quality standards have been initiated since the first official re- and free acidity as well as a lower pH, and the lack of diastase in
introduction of the stingless bee farming economy by the Malaysian stingless bee honey. Several other studies have also supported the un-
Agricultural Research and Development Institute (MARDI) in 2012. suitability of the IHC honey standard to be used with stingless bee
This started when Moniruzzaman et al.’s study in 2014 revealed dif- honey (Biluca et al., 2016; Chuttong et al., 2016; Oddo et al., 2008;
ferences in some of the physicochemical properties of Malaysian Moniruzzaman et al., 2014; Vit et al., 1994). In response, a quality
honeys, including stingless bee, against the parameters set by the standard for medicinal use of Meliponinae (stingless bee) honey in
International Honey Commission. The journey has been fruitful and in Guatemala, Mexico, and Venezuela has been proposed by Vit et al.
2017 the Malaysian Standards authority announced a new quality (2004). In this proposal, honey to be used for medicine should have a
standard for honey produced by stingless bees. moisture content that is not more than 30 g/100 g, sum of fructose and
Liberalization of food trade, growing consumer demand, develop- glucose that is not less than 50 g/100 g, sucrose content that is not more
ments in food science and technology, and improvements in transport than 6 g/100 g, free acidity that is not more than 85 meq/kg, ash con-
and communication, has all led to the expansion of the world economy. tent that is not more than 0.5 g/100 g, HMF content that is not more
Parallel to this, the international trade in fresh and processed food, than 40 mg/kg, and diastase activity that is not less than 3 DN (Vit
including stingless bee honey, is inevitable. Thus, a harmonized quality et al., 2004).
standard that applies to the stingless bee honey coming from different In 2017, the quality standards for Malaysian stingless bees was
countries is of paramount importance. published by the Department of Malaysian Standards to regulate the
The goal of this review is to provide a current overview of the re- sale and distribution of the stingless bee honey in Malaysia. According
ported physicochemical properties of stingless bee honey from coun- to the Malaysian Standard, a good quality stingless bee honey shall
tries all over the world.. We seek to utilize this review to facilitate the have moisture content that is not more than 35 g/100 g, sum of fructose
effort of setting a more harmonized international standard for honey and glucose that is not more than 85 g/100 g, sucrose content that is not
produced by the stingless bee species. more than 7.5 g/100 g, maltose content that is not more than 9.5 g/
100 g, ash content that is not more 1.0 g/100 g, HMF content that is not
2. Methods of review more than 30 mg/kg, pH within 2.5 and 3.8, and shall contain naturally
occurring plant phenolic (Malaysian Standards, 2017). Comparison
To ensure the inclusion of all of the available reports on the phy- between the three standards are presented in Table 1.
sicochemical properties of stingless bee honey, a literature search was
done by employing the Scopus (published between 1823 to May 2018)
4. Bee species
database with the combination of the following two sets of keywords
(1) stingless OR meliponini OR trigona OR stingless bee honey AND (2)
About 500 species of stingless bee are currently identified around
physic* OR chem* OR physicochemical*. Because physicochemical
the globe (Michener, 2013). The stingless bee belongs to the family
properties of honey are also very relevant to its therapeutic benefit, the
Hymenoptera and subfamily Meliponinae. They are further divided into
literature search was supplemented with search results from the
three tribes: Meliponini, Trigonini and Lestrimelitta (Michener, 2000).
Medline medical database (published between 1865 to May 2018),
The findings from the literature search is intriguing, unlike Apis
which was accessed via the Ebscohost search engine using similar
keywords. A manual search was also done using Google Scholar to
Table 1
further supplement the aforementioned search result. Snowball refer-
Quality standards for honey.
encing was also done from appropriate review articles obtained from
the search results. Parameter IHC Standards Vit et al. Malaysian
(2004) Standards
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A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
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A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Fig. 1. Map of the world indicating the geographical origin of stingless bee honey discussed in the review.
inclusion of all available data from all over the world, it is our intention 6.1. Moisture
to set this review as a guide for establishing international standards of
stingless bee honey. Fig. 1 presents the geographical origin of the honey Honey’s moisture content has been reported to be dependent on the
samples included in this review. environmental factors during harvesting and storage. Honey with a
high-water content translates to a greater fermentation potential, re-
sulting in more difficult preservation and storage (Babarinde et al.,
6. Honey’s physicochemical properties
2011). Stingless bee honey has been reported to contain greater water
content compared to Apis mellifera honey (Almeida-Muradian et al.,
The most studied stingless bee species is Tetragonula angustula,
2013; Souza et al., 2006; Vit et al., 1998). The higher water content in
which is known locally in Argentina as Yateí. A total of 88 honey
stingless bee honey may be related to the nature of their habitat; that is,
samples, as analysed by nine research teams were found (Pucciarelli
the humid tropical jungle. The moisture content reported in stingless
et al., 2014; Anacleto et al., 2009, Rodriguez-Malavera et al., 2009,
bee goes from as low as 13.26 g/100 g to as high as 45.8 g/100 g, with a
Almeida and Marchini, 2004, Santiesteban-Hernandez et al., 2003;
mean of 28.6 g/100 g and a standard deviation of 5.7 g/100 g (Table 3).
Denadai et al., 2002; Grajales et al., 2001; Rodrigues et al., 1998; Vit
The honey with the lowest moisture content comes from the species
et al., 1998). The Yateí habitat covers the tropical and subtropical re-
Trigona sp. from Thailand, while the honey with the highest moisture
gions of the American continent from Argentina to Panama and Mexico,
content comes from the species Partamona epiphytophila originated from
leading to its popularity among American researchers (Nogueira-Neto,
Peru (Issaro et al., 2013, Rodriguez et al., 2009).
1997). As expected, the physicochemical properties reported varies
The threshold set for good quality honey by the IHC in terms of
greatly due to the enormous variation in bee species and geographical
moisture is 20 g/100 g, which applies to Apis mellifera honey. However,
origin. Table 3,4 and 5 contains all of the compiled data that will be
out of the 498 honey samples with moisture data available, 97% of
discussed in this review.
them do not comply with this threshold. Specific to the stingless bee
Although the parameters chosen by each investigator varies slightly,
species, Vit et al. (2004), offered a slightly higher threshold of 30 g/
some common ground was apparent. It is noticeable that the honey’s
100 g. The Malaysian Standards have an even higher threshold at 35 g/
moisture is the most common parameter measured in stingless bee
100 g. Both of these standards do more justice to the honey of stingless
honey (498 samples). This is followed by free acidity (472 samples),
bee species. However, the presence of 74 samples of honey from Brazil,
sugar profile (447 samples), pH (430 samples), HMF (360 samples), ash
Peru and Thailand, that presented moisture content up to 47 g/100 g
content (341 samples), and electrical conductivity (304 samples). Less
may indicate that a more harmonized international standard is required
common parameters include enzyme activity (218 samples), nitrogen,
(Biluca et al., 2016; Chuttong et al., 2016; Rodriguez-Malavera et al.,
soluble solids (88 samples), color (71 samples), minerals (65 samples),
2009; Gonnet et al., 1964).
and phenolic compound (44 samples) (Alvarez-Suarez et al., 2018;
Fernandes et al., 2018; Tukshita et al., 2018; Abu Bakar et al., 2017; do
Vale et al., 2017; Gomes et al., 2017; Kek et al., 2017; Lemos et al., 6.2. Free acidity
2018; Nweze et al., 2017; Biluca et al., 2016; Chuttong et al., 2016;
Jimenez et al., 2016; Sousa et al., 2016; Pucciarelli et al., 2014; The free acidity of honey correlates to the presence of organic acids
Almeida-Muradian et al., 2013; Issaro et al., 2013; Silva et al., 2013; in honey. High acidity may indicate the fermentation of sugars into
Fuenmayor et al., 2012; Lage et al., 2012; Suntiparapop et al., 2012; organic acids (Sancho et al., 2013). In accordance to the known high
Onyenso et al., 2011; Anacleto et al., 2009; Carvalho et al., 2009; moisture content of stingless bee honey, free acidity values were also
Guerrini et al., 2009; Rodriguez-Malavera et al., 2009; Oddo et al., frequently reported to be higher in stingless bee honey compared to the
2008; Almeida-Muradian et al., 2007; Alves et al., 2005; Evangelista- Apis mellifera honey (Almeida-Muradian et al., 2013; Souza et al., 2006;
Rodrigues et al., 2005; Almeida and Marchini, 2004; Souza et al., 2004; Vit et al., 1998). Free acidity among the stingless bee honey has been
Villas-Boas and Malaspina, 2004; Santiesteban-Hernandez et al., 2003; reported to range from 5.9 meq/kg to 592 meq/kg. This brings about a
Denadai et al., 2002; Marchini et al., 1998; Rodrigues et al., 1998; mean of 73.59 meq/kg and standard deviation of 101.53 meq/kg
Souza and Bazlen, 1998; Vit et al., 1998, 1994; Gonnet et al., 1964). (Table 3). The lowest free acidity value was measured in Melipona
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A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Table 3
Common parameter for physicochemical data of stingless bee honey.
Bee species # Moisture (g/ Free Acidity pH HMF (mg/ Ash (g/ Electrical Conductivity Source
100 g) (mEq/kg) kg) 100 g) (ms/cm)
Cephalotrigona capitata 1 27 31.5 3.62 3.4 0.52 – Almeida and Marchini, 2004
Frieseomelitta aff varia 7 19.9 73 – 1.1 0.76 – Vit et al., 1994
Geniotrigona thoracica 1 28.17 – 3.36 – – – Abu Bakar et al., 2017
Heterotrigona itama 1 28.43 – 3.32 – 0.438 – Abu Bakar et al., 2017
3 – – – – 0.08 – Kek et al., 2017
Homotrigona fimbriata 1 41 528 3.3 46 1 2.6 Chuttong et al., 2016
Hypotrigona sp. 3 17.5 35.57 3.75 16.58 – 0.303 Nweze et al., 2017
Lepidotrigona doipaensis 2 31.5 197.5 3.5 2.3 0.512 1.193 Chuttong et al., 2016
Lepidotrigona flavibasis 4 28 168 3.7 8.5 0.51 1.3 Chuttong et al., 2016
Lepidotrigona terminata 1 30 194 3.5 – 0.245 0.78 Chuttong et al., 2016
Lisotrigona furva 2 28 53 3.6 0.215 0.183 0.345 Chuttong et al., 2016
Melipona asilvai 11 29.5 41.6 3.27 2.4 – – Souza et al., 2004
Melipona beecheii 8 28.62 41.52 3.2 9.23 0.46 0.58 Alvarez-Suarez et al., 2018
1 26.51 – 4.26 – – – Onyenso et al., 2011
1 24 28 4.5 64.8 – 0.55 Grajales et al., 2001
1 27 5.9 4.18 5.4 – 0.66 Santiesban-Hernandez et al.,
2003
Melipona bicolor 5 34.68 91.62 3.766 < 0.31 – 0.576 Biluca et al., 2016
Melipona capixaba 9 30.51 79.28 3.62 – – – Lage et al., 2012
Melipona compressipes 2 26.7 23.88 3.74 – – – Almeida-Muradian et al.,
2007
1 22.3 25.1 3.65 35.8 – – Gonnet et al., 1964
8 24.6 39 3.46 1.2 0.22 – Villas et al., 2004
1 25 45.8 4.06 30.5 – 8.77 Souza et al., 1998
5 23.4 48.4 – 1 0.3 – Vit et al., 1994
Melipona crinita 2 28.8 – – – – – Rodriguez et al., 2009
Melipona eburnea 1 23.8 – – – – – Rodriguez et al., 2009
Melipona fasciculata 20 25.45 29.05 4.35 – 0.32 – Fernandes et al., 2018
4 29.03 18.91 4.56 17.81 – – Lemos et al., 2017
Melipona favosa 14 25.2 62.9 – 1.2 0.29 – Vit et al., 1994
6 24.2 36.8 – 17.1 0.15 2.06 Vit et al., 1998
Melipona flavolineata 4 35.11 143.67 3.41 34.62 – – Lemos et al., 2017
Melipona grandis 5 27.5 – – – – – Rodriguez et al., 2009
Melipona ilota 1 28 – – – – – Rodriguez et al., 2009
Melipona lateralis kangarumensis 3 28.8 40.7 – 3.9 0.11 1.65 Vit et al., 1998
Melipona mandacaia 20 28.8 43.5 3.27 5.8 – 3.52 Alves et al., 2005
Melipona marginata 6 32.65 79.82 3.67 < 0.31 – 0.437 Biluca et al., 2016
Melipona mondury 11 61.51 4.19 – – – Lage et al., 2012
2 29.75 61.1 5.19 < 0.31 – 0.69 Biluca et al., 2016
Melipona paraensis 4 26.4 30.4 4.29 3.4 0.14 1.37 Vit et al., 1998
Melipona quadrifasciata 12 32.47 42.53 3.71 5.2 0.335 Biluca et al., 2016
1 25.2 6.25 6.64 1.27 0.393 0.596 Carvalho et al., 2009
1 30 28 3.74 1.45 0.146 0.217 Carvalho et al., 2009
1 34 16.5 4.52 1 0.54 – Almeida and Marchini, 2004
Melipona quadrifasciata 1 41.9 103.3 3.35 31.5 – – Gonnet et al., 1964
anthidioides
Melipona rufiventris 7 – 42 4.24 – – Lage et al., 2012
Melipona rufiventris mondury 1 27.7 38.2 4.21 < 0.31 – 0.25 Biluca et al., 2016
Melipona scutellaris 1 23.4 28.7 4.52 < 0.31 – 0.15 Biluca et al., 2016
2 28 40.38 3.55 1.77 0.181 0.268 Carvalho et al., 2009
1 25.3 28.3 4.66 18.9 0.17 – Evangelista et al., 2005
6 28.4 8.9 3.15 0.4 0.01 3.39 Marchini et al., 1998
Melipona scutellaris latrelle 12 25.5 42.75 3.83 – 0.165 0.524 Sousa et al., 2016
Melipona seminigra 2 30.4 26.54 3.78 – – – Almeida-Muradian et al.,
2007
8 26 79 3.53 0.8 0.15 – Villas et al., 2004
Melipona solani 1 25 85 4 78.5 – 0.62 Grajales et al., 2001
Melipona sp. 16 38.7 35.7 3.6 8.6 0.38 0.392 Do Vale et al., 2017
9 24.46 – 3.24 – 0.098 – Gomes et al., 2017
3 13.86 12.59 4.21 5.5 – 0.238 Nweze et al., 2017
Melipona subnitida 24 24.8 32.49 – 7.56 0.02 0.102 Almeida et al., 2013
Melipona subnitida ducke 12 26.4 42.65 3.95 – 0.198 0.514 Sousa et al., 2016
Melipona trinitatis 4 25.7 24.2 – 1.3 0.12 – Vit et al., 1994
Nannotrigona melanocera 1 33.4 – – – – – Rodriguez et al., 2009
Partamona epiphytophila 1 45.8 – – – – – Rodriguez et al., 2009
Partamona sp. 1 34.1 23.7 3.42 2.4 – 0.81 Santiesteban-Hernandez
et al., 2003
Pleibeia droryana 1 31 52 3.83 7.6 1.18 – Almeida and Marchini, 2004
Ptilotrigona lurida 1 35.2 – – – – – Rodriguez et al., 2009
Scaptotrigona bicuntata 2 23.95 48.95 4.48 < 0.31 0.63 Biluca et al., 2016
Scaptotrigona mexicana 12 23.94 – 3.75 12.61 0.499 0.285 Jimenez et al., 2016
4 24.7 76.7 4.05 42 – 0.76 Grajales et al., 2001
(continued on next page)
95
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Table 3 (continued)
Bee species # Moisture (g/ Free Acidity pH HMF (mg/ Ash (g/ Electrical Conductivity Source
100 g) (mEq/kg) kg) 100 g) (ms/cm)
beechei honey from Mexico (Santiesteban et al., 2003) and the highest parameter of honey freshness. HMF is usually absent in a freshly har-
free acidity value was obtained from Tetrigona melanoleuca honey from vested sample and it tends to increase over time. HMF is a breakdown
Thailand (Chuttong et al., 2016). Majority of stingless bee honey product of simple sugars, especially fructose. Several factors have been
samples with available free acidity data comply with the set standards reported to affect HMF content including heating, storage condition, pH
by the IHC which is free acidity of not more than 50 meq/kg. Never- of honey, and adulteration of honey with simple sugars from an ex-
theless, a significant portion of 40.4% out of the 472 stingless bee ternal source (Pasias et al., 2017). The available data on HMF revealed
honey samples presented in this review still do not comply to the a highest value of HMF at 78.5 mg/kg in Melipona solani from Mexico
standard. The threshold set for Scaptotrigona species by Vit et al. (Grajales et al., 2001). HMF content has been set to be not more than
(2004), is more lenient at 85 meq/kg, resulting in the inclusion of 88% 40 mg/kg in a good quality Apis mellifera honey. The same value was
percent of the total sample into the standard compliant group. also suggested by Vit et al. for the stingless bee species. In the Malaysian
Standard, the threshold was reduced to be lower than 30 mg/kg.18
samples from Brazil, Mexico, and Thailand are found to be non-com-
6.3. pH
pliant with the Malaysian Standards threshold (Lemos et al., 2018;
Chuttong et al., 2016; Grajales et al., 2001; Gonnet et al., 1964),.
Honey is acidic in nature, with a pH ranging from 3.2 to 4.5
Stingless bee honeys are often subjected to accusation of adulteration
(Solayman et al., 2016). Honey pH has been useful in the determination
due to their high HMF content. In reality, their naturally higher
its geographical origin (Acquarone et al., 2007). Overall, the pH of
moisture content directly influences their HMF content. However,
stingless bee honey ranges from 3.15 to 6.64. The mean for pH was 3.85
stingless bee honey has been reported to be more resistant to HMF
with a standard deviation of 0.53 (Table 1). The lowest pH value, 3.15,
formation than Apis mellifera honey when subjected to thermal treat-
was detected from the honey of Melipona scutellaris from Brazil
ment (Biluca et al., 2014). Consequently, a revision of the HMF stan-
(Marchini et al., 1998). The highest pH value was detected from honey
dard set for stingless bee is of paramount importance.
of Melipona quadrifasciata from Brazil (Carvalho et al., 2009). There is
no standard in terms of pH for honey set by the IHC or Vit et al (2004).
However, the Malaysian Standard has set an acceptable pH range of 2.5
6.5. Ash content
to 3.8 for stingless bee honey. Considering the range set by Malaysian
Standard, 176 out of the 430 samples (40.9%) with pH data available
The ash content of honey correlates to its mineral content and is
were not compliant. A harmonized international standard may offer a
influenced by the composition of source plant nectar. The original
more lenient pH range but a lot of validation needs to be done on the
nectar-bearing plant absorbs minerals from the soil, which eventually
currently available data.
end up in the nectar (Felsner et al., 2004). This gives an insight into the
quality of honey in terms of inorganic contaminants, such as pesticides
6.4. Hydroxymethylfurfural content (Moniruzzaman et al., 2014). The ash content of stingless bee honey
ranges from as low as 0.01 g/100 g to as high as 3.1 g/100 g honey
Hydroxymethylfurfural (HMF) content is widely recognised as a (Table 3). The mean value was 0.40 g/100 g, with a standard deviation
96
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Table 4
Sugar profile of stingless bee.
Bee species # Total Reducing Sugar Fructose (g/ Glucose (g/ Maltose (g/ Sucrose (g/ Source
(g/100 g) 100 g) 100 g) 100 g) 100 g)
97
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Table 4 (continued)
Bee species # Total Reducing Sugar Fructose (g/ Glucose (g/ Maltose (g/ Sucrose (g/ Source
(g/100 g) 100 g) 100 g) 100 g) 100 g)
0.48 g/100 g. The lowest ash content was observed in Melipona scu- the review are compliant to the standard set.
tellaris honey from Brazil and the highest ash content was observed in Apart from the reducing sugars, other sugars, such as sucrose and
Tetrigona melanoleuca from Thailand (Chuttong et al., 2016; Marchini maltose, were also reported in honey. Their presence is often reported
et al., 1998). Both the IHC and Vit et al. set the ash content threshold at in lower content compared to fructose and glucose, or sometimes were
not more than 0.5 g/100 g for a good quality honey from both Apis not detected at all (Solayman et al., 2016; Sousa et al., 2016). In terms
mellifera and Meliponinae species. Almost all of the samples (94%) of sucrose, their detection in stingless bee honey goes from 0.025 g/
comply with the standards. The Malaysian Standards have set an even 100 g to 32.33 g/100 g, with a mean of 3.6 g/100 g and standard de-
higher threshold at 1.0 g/100 g resulting in a better inclusion of 99%. viation of 5.8 g/100 g (Table 4).
Only one sample from Brazil and two samples from Thailand did not According to the standards set by the IHC, a good quality honey
comply with the Malaysian Standards (Chuttong et al., 2016; Almeida should have a sucrose content that is not more than 5 g/100 g. Vit et al.
and Marchini, 2004). The Tetrigona melanoleuca honey from Thailand has increased the threshold for sucrose a little higher at 6 g/100 g to
reported the highest ash content of 3.1 g/100 g, which was probably accommodate the slightly higher sucrose content reported in stingless
influenced by the composition of the original nectar-producing plant bee honey. For Malaysian Standards, the maximum threshold of 7.5 g/
(Chuttong et al., 2016). 100 g sucrose was set to regulate honey adulteration. In terms of su-
crose, only Tetragonula laeviceps from Thailand and Heterotrigona itama
6.6. Electrical conductivity from Malaysia did not comply with the standard set by all three groups
(Kek et al., 2017; Suntiparapop et al., 2012).
The electrical conductivity of the honey is directly related to its For maltose, the value goes from 0.6 g/100 g to 53 g/100 g with a
concentration of mineral, salts, organic acids and proteins (Solayman mean of 29.98 g/100 g and standard deviation of 20.11 g/100 g in
and other 2016). This parameter compliments the other parameters stingless bee (Table 4). Only the Malaysian Standards set a threshold for
used in the determination of honey floral origin (Acquarone et al., maltose, a maximum of 9.5 g/100 g. Only two groups measured maltose
2007). In stingless bees, electrical conductivity ranges from 0.102 ms/ in honey; that is, those from Thailand and Australia (Chuttong et al.,
cm to 8.770 ms/cm (Table 3). The lowest electrical conductivity value 2016; Oddo et al., 2008). Out of all the maltose data, only maltose
was observed in the Melipona subnitida honey collected from Brazil content from Lisotrigona furva species from Thailand complied to the
(Almeida-Muradian et al., 2013). In contrast, the highest electrical Malaysian Standards (Chuttong et al., 2016).
conductivity value was observed in Melipona compressipes honey col-
lected also from Brazil. The electrical conductivity brings about a mean 6.8. Enzyme activity
of 1.160 ms/cm with standard deviation of 1.6 ms/cm, which shows
that there is a huge variability between the samples. The IHC re- Two key enzymes have been selected for the validation of honey
commended that electrical conductivity should not be more than quality: diastase and invertase. Diastase is the common name for the
0.8 ms/cm. However, it is not mentioned in either Vit et al. (2004) enzyme alpha-amylase. It is naturally present in honey and the activity
proposal or the Malaysia Standard, suggesting the unsuitability of this tends to reduce over time. Hence, diastase activity is usually used as an
parameter for a stingless bee honey standard. indicator of honey’s freshness (Pasias et al., 2017). There are 217 honey
samples which have diastase activity data. The value goes from 0.15 DN
6.7. Sugar content to 32.28 DN, with the mean of 7.08 DN and standard deviation of 8.01
DN (Table 5). The lowest diastase activity was reported with Tetrigona
Carbohydrates in the form of sugars are the major constituents of melanoleuca honey from Thailand and the highest diastase activity was
honey (Sato and Miyata, 2000). The reducing sugars fructose and glu- reported with Tetragonisca angustula honey from Brazil. The set stan-
cose were frequently reported to make up the majority portion of sugar dard for diastase activity by IHC is no less than 8 DN. The lack of
in honey (Solayman et al., 2016). In stingless bee honey, the sum of diastase in stingless bee honey has been reported previously (Vit and
reducing sugars goes from 12.5 g/100 g to 75.7 g/100 g, with the mean Pulcini 1996; Gonnet et al., 1964). Accordingly, the standards set for
of 57.79 g/100 g and standard deviation of 16.23 g/100 g (Table 4). The stingless bee by Vit et al. reduced the threshold for diastase to 3 DN.
lowest reducing sugars content was detected in the honey of Tetrigona There is no standard set in terms of bee enzyme by the Malaysian
apicalis from Thailand while the highest reducing sugars content was Standards.
detected in the honey of Melipona compressipes from Venezuela The sucrose-hydrolytic enzyme, invertase has a key role in trans-
(Chuttong et al., 2016; Vit et al., 1994). forming the sucrose of nectar into the glucose and fructose in honey (Vit
According to the standards set by the IHC, a good quality honey and Pucini, 1996). In terms of invertase, only two studies—Oddo
should have the sum of both fructose and glucose that is not less than (2008) and Vit (1998)—measured this parameter. The enzyme is also
60 g/100 g. Stingless bees have been reported to contain lower sugar not included in all of the honey quality standards, probably because
content compared to Apis mellifera honey. In response, Vit et al. has invertase is more susceptible to heat damage than is diastase. This leads
lowered the threshold for stingless bee at 50 g/100 g. For Malaysian to a shorter half-life, rendering it difficult to be utilized as a quality
Standards, a maximum threshold was set to regulate honey adultera- parameter (Oddo et al., 1999).
tion. In Malaysia, a marketed honey should not have a sum of fructose
and glucose that is more than 85 g/100 g. Considering IHC standards, 6.9. Nitrogen
40.7% of the honey samples with the sum of fructose and glucose
content data did not comply with the standards. Vit et al. (2004) pro- The nitrogen measurement represents the brute protein content in
posal does more justice to stingless bee honey because it includes 96% honey. This protein can include the enzymes that are crucial in the
of the honey samples. With Malaysian Standards, all honey samples in formation of the honey (Anklam, 1998). The nitrogen content is
98
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Table 5
Less common parameter for physicochemical data of stingless bee honey.
Bee species # Diastase (DN) Invertase (IU) Nitrogen (mg/100 g) Soluble Solids (Brix) Color (pFund) Source
99
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
316.92 Brix. In stingless bee, the soluble solid values have a mean of Table 7
70.39 Brix and a standard deviation of 3.83 Brix (Table 5). The lowest Phenolic compounds detected in stingless bee honey.
value of soluble solids was detected in the honey of Melipona bicolor and Phenolic compound Melipona seminigra Melipona beecheii
the highest value of soluble solids was detected in the honey of Melipona
scutellaris (Biluca et al., 2016). Both stingless bee species originated Coumaric acid Yes Yes
Luteolin Yes Yes
from Brazil. This parameter is not regarded in any of the quality stan-
Gallic acid Yes No
dards for honey. 3,4 Dihydroxybenzoic acid Yes No
4-Hydroxybenzoic acid Yes No
Vanillic acid Yes No
6.11. Minerals
Salicylic acid Yes No
Syringic acid Yes No
In Apis mellifera honey, the mineral content of the honey is fre- Cinnamic acid Yes No
quently reported to relate the nutritional benefit of honey (Solayman Catechol Yes No
trans,trans Abscisic Yes No
et al., 2016). In stingless bee honey, mineral content was evaluated in
cis, trans Absicic Yes No
65 samples. A total of 14 minerals had been studied by 6 research Taxifolin Yes No
groups, potassium (K), sodium (Na), calcium (Ca), magnesium (Mg), Naringenin Yes No
manganese (Mn), phosphorus (P), iron (Fe), copper (Cu), zinc (Zn), Dihydrocaffeic acid No Yes
barium (Ba), cadmium (Cd), lead (Pb), arsenic (As), and mercury (Hg) C-pentosyl-C-hexosyl-apigenin No Yes
Quercetin deoxyhexosyl hexoside No Yes
(Abu Bakar et al., 2017; Kek et al., 2017; Lemos et al., 2018; Biluca
Apigenin trihexoside No Yes
et al., 2016; Fuenmayor et al., 2012, Onyenso et al., 2011). Four major Kaempferol deoxyhexosyl hexoside No Yes
minerals were detected in stingless bee honey, which are K, Na, Ca, and Isorhamnetin deoxyhexosyl hexoside No Yes
Mg. The most abundant minerals in stingless bee honey was found to be Quercetin No Yes
K, ranging from 45.9 mg/100 g to 1357.76 mg/100 g. This is followed Isorhamnetin No Yes
Bis-methylated quercetin No Yes
by Na, ranging from 0.78 mg/100 g to 589.7 mg/100 g. Next is Ca, Apigenin No Yes
ranging from 3.85 mg/100 g to 199.6 mg/100 g, and finally Mg, ran- Kaempferol No Yes
ging from 1.15 mg/100 g to 73.76 mg/100 g. Table 6 illustrated the Methyl luteolin No Yes
minerals content in stingless bee honey. No specific standards have Methyl quercetin No Yes
been set in terms of the mineral content of stingless bee honey.
Table 6
Mineral content of stingless bee honey.
Bee Species K (mg/100 g) Na (mg/ Ca (mg/ Mg (mg/ Mn (mg/ P (mg/ Fe (mg/ Cu (mg/ Zn (mg/ Ba (mg/ Reference
100 g) 100 g) 100 g) 100 g) 100 g) 100 g) 100 g) 100 g) 100 g)
100
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
6.13. Color Alvárez-Suárez, J.M., Giampieri, F., Brenciani, A., Mazzoni, L., Gasparrini, M., Gonzalez-
Paramas, A.M., Santos-Buelga, C., Morroni, G., Simoni, S., Forbes-Hernandez, T.Y.,
Afrin, S., Givanetti, E., Battino, M., 2018. Apis mellifera vs Melipona beecheii cuban
Honey’s color can vary from straw yellow to almost black. This polifloral honeys: a comparison base on their physicochemical parameters, chemical
property is dependent to the mineral content, pollen and phenolic composition and biology properties. LWT Food Sci. Technol. 87, 272–279.
content of the honey (Solayman et al., 2016). Honey’s color varies Alves, R.M.O., Carvalho, C.A.L., Souza, B.A., Sodré, G.S., Marchini, L.C., 2005.
Características físico-químicas de amostras de mel de Melipona mandacaia Smith
greatly according to its geographical origin (Bertoncelj et al., 2007). (Hymenoptera: Apidae). Ciênc Tecnol Aliment 25, 644–650.
The method of production and agricultural practices also can influence Anacleto, D.A., Souza, B.A., Marchini, L.C., 2009. Composition of the honey of samples
the color of honey (Almeida-Muradian and other 2013). In stingless originated from Jatai bees (Tetragonisca angustula latreille, 1811). Cienc Technol
Aliment 29 (3), 535–541.
bees, the honey color ranges from 26 Pfund to 150 Pfund when mea- Anklam, E., 1998. A review of the analytical methods to determine the geographical and
sured using a photometer (Table 5). The data has a mean of 92.9 Pfund botanical origin of honey. Food Chem. 63 (4), 549–562.
and a standard deviation of 38.92 Pfund. The highest intensity of color Babarinde, G.O., Babarinde, S.A., Adegbola, D.O., Ajayeoba, S.I., 2011. Effects of har-
vesting methods on physicochemical and microbial qualities of honey. J. Food Sci.
was detected in Tetragonisca angustula honey from Brazil and the lowest
Technol. 48 (5), 628–634.
intensity of color was detected in Melipona ilota from Peru. There is no Bertoncelj, J., Dobersek, U., Jamnik, M., Golob, T., 2007. Evaluation of the phenolic
standard set for honey in terms of color. content, antioxidant activity and colour of Slovenian honey. Food Chem. 105,
822–828.
Biluca, F.C., Braghini, F., Gonzaga, L.V., Costa, A.C.O., Fett, R., 2016. Physicochemical
7. Strength and limitation profiles, minerals, and bioactive compounds of stingless bee honey (Meliponinae). J.
Food Comp. Anal. 50, 61–69.
A literature search using predefined keywords in two separate da- Carvalho, C.A.L., Sodre, G.S., Fonseca, A.A.O., Alves, R.M.O., Souza, B.A., Clarton, L.,
2009. Physicochemical characteristics and sensory profile of honey samples from
tabases has allowed us to obtain all of the available reports on the stingless bees (Apidae: Meliponinae) submitted to a dehumidification process. A
stingless bee honey composition. However, the search strategy might Acad. Bras Cienc 81 (1), 143–149.
miss some studies that did not use standard keywords during indexing. Chuttong, B., Chanbang, Y., Sringarm, K., Burgett, M., 2016. Physicochemical profiles of
stingless bee (Apidae: Meliponini) honey from South East Asia (Thailand). Food
The search might also miss studies that look into the composition of Chem. 192, 149–155.
stingless bee honey as a secondary outcome. The compiled literature Codex Alimentarius Commission, 2001. Alinorm 41/10: revised standard for honey.
revealed a variation of stingless bee honey species, making interpreta- Alinorm 1, 19–26.
Denadai, J.M., Ramos-Filho, M.M., Costa, D.C., 2002. Caracterização físico-química de
tion of the results difficult. However, this review might be a guide to mel de abelhas Jataí (Tetragonisca angustula) do município de Campo Grande - MS.
start the standardization of studies done on stingless bee honey around Obtenção de parâmetros para análise de rotina. Anais XIV Cong. Bras. de
the globe. Apicultura. 80.
do Vale, M.A.D., Fábio Augusto Gomes, F.A., dos Santos, B.R.C., Ferreira, J.B., 2017.
Honey quality of Melipona sp. bees in Acre, Brazil. Acta Agron 67 (2), 201–207.
8. Conclusion Evangelista-Rodrígues, A., Silva, E.M., Beserra, E.M., Rodrígues, M.L., 2005. Análise
físicoquímica dos méis das abelhas Apis mellifera e Melipona scutellaris produzidos
This review has revealed significant difference in terms of stingless em duas regiões no Estado de Paraíba. Ciênc Rural 35, 1166–1171.
Felsner, M.L., Cano, C.B., Bruns, R.E., Watanabe, H.M., Almeida-Muradian, L.B., Matos,
bee species of interest that was selected by researchers from different J.R., 2004. Characterization of monofloral honeys by ash contents through a hier-
part of the globe. In general, the current data on stingless bee supported archical design. J. Food Comp. Anal. 17, 737–747.
previously reported greater moisture content, higher acidity, lower Fernandes, R.T., Rosa, I.G., Conti-Silva, A.C., 2018. Microbiological and physical-che-
mical characteristics of honeys from the bee Melipona fasciculata produced in two
sugar composition, and lower enzyme activity in stingless bees com- regions of Brazil. Ciênc Rural 48 (5), e20180025.
pared to Apis mellifera bees. The current data reiterates the need for an Fuenmayor, C.A., Zuluaga-Dominguez, C.M., Diaz-Moreno, A.C., Quicazan, M.C., 2012.
exclusive standard of quality for stingless bee and validates the pre- Miel de angelita: Nutritional composition and physicochemical properties of
Tetragonisca angustula honey. Intercencia 37, 142–147.
viously available standards from Latin America and Malaysia. A har- Gomes, V.V., Dourado, G.S., Costa, S.C., Lima, A.K.O., Silva, D.S., Bandeira, A.M.,
monized international standard is proposed to better accommodate Vasconcelos, A.A., Taube, P.S., 2017. Evaluation of the quality of honey commer-
stingless bee honey from all over the world. cialized in Western Pará. Braz. Rev. Virtual Quim 9 (2), 815–826.
Gonnet, M., Lavie, P., Nogueira-Neto, P., 1964. Étude de quelques characteristiques des
miels récoltés para certains méliponines brésiliens. Compt. Rend. Acad. Sci. Paris
Acknowledgments 258, 3107–3109.
Grajales, C.J., Rincón, R.M., Vandame, R., Santiesteban, N.A., Guzmán, D., 2001.
Características físicas, químicas y efecto microbiológico de mieles de Meliponinos y
This work was supported by Universiti Kebangsaan Malaysia
Apis mellifera de la región Soconusco, Chiapas. II Seminario Mexicano sobre Abejas
(UKM). We would like to acknowledge the UKM library for access to the sin Aguijón, Mérida, Mexico, pp. 61–66.
scientific databases. UKM also provided financial support in the form Guerrini, A., Bruni, R., Maietti, S., Poli, F., Rossi, D., Paganetto, G., Muzzoli, M.,
scholarship (Zamalah UKM) for Abid Nordin to pursue his PhD degree. Scalvenzi, L., Sacchetti, G., 2009. Ecuadorian stingless bee (Meliponinae) honey: a
chemical and functional profile of an ancient health product. Food Chem. 114,
We would also like to acknowledge AMRUS Medik Sdn. Bhd. for fi- 1413–1420.
nancial support in the form of research grant (FF-2017-20). International Honey Commission, 2009. Harmonised Methods of the International Honey
Commission. 63 pp. Swiss Bee Research Centre, Bern: FAM, Liebefeld.
Issaro, N., Weerakul, T., Machana, S., Ornnim, P., Phanudulkitti, C., Srijan, T.,
References Laiwattanaphaisal, J., Pattarapanich, C., 2013. Stingless bee honey II: qualitative and
quantitative studies on honey produced by three stingless bee species collected from a
Abd Jalil, M.A., Kasmuri, A.R., Haid, H., 2017. Stingless bee honey, the natural wound mangosteen garden in Chantaburi province, Thailand. Thai J. Pharm. Sci. 38 Suppl.
healer: a review. Skin. Pharmacol. Physiol. 30, 66–75. Jimenez, M., Beristain, C.I., Azuara, E., Mendoza, M.R., Pascual, L.A., 2016.
Abu Bakar, M., Sanusi, S., Abu Bakar, F., Cong, O., Mian, Z., 2017. Physicochemical and Physicochemical and antioxidant properties of honey from Scaptotrigona mexicana
antioxidant potential of raw unprocessed honey from Malaysian stingless bees. Pak. J. bee. J. Apic. Res. http://dx.doi.org/10.1080/00218839.2016.1205294.
Nutr. 16 (11), 888–894. Kek, S., Chin, N., Yusof, Y., Tan, S., Chua, L., 2017. Classification of entomological origin
Acquarone, C., Buera, P., Elizalde, B., 2007. Pattern of pH and electrical conductivity of honey based on its physicochemical and antioxidant properties. In J. Food Prop. 20
upon honey dilution as a complementary tool for discriminating geographical origin (sup3), S2723–S2738.
of honeys. Food Chem. 101, 695–703. Lage, L.G.A., Coelho, L.L., Resende, H.C., Tavares, M.G., Campos, L.A.O., Fernandes-
Almeida, D., Marchini, L.C., 2004. Physicochemical and pollinic composition of honey Salomao, T.M., 2012. Honey physicochemical properties of three species of the
samples of stingless bees (Hymenoptera: Apidae: Meliponini) from the Cerrado of brazilian Melipona. A Acad. Bras Cienc 84 (3), 605–608.
Pirassununga campus, University of São Paulo, in Pirassununga, State of São Paulo, Lemos, M., Venturieri, G., Dantas Filho, H., Dantas, K., 2018. Evaluation of the physi-
Brazil. Proc. 8th Int. Conf. on Tropical Bees and VI Encontro sobre Abelhas. pp. 585. cochemical parameters and inorganic constituents of honeys from the amazon region.
Almeida-Muradian, L.B., Matsuda, A.H., Bastos, D.H.M., 2007. Physicochemical para- J. Api Res. 57 (1), 135–144.
meters of Amazon Melipona honey. Quim Nova 30 (3), 707–708. Malaysian Standards, 2017. Kelulut (Stingless Bee) Honey – Specification. Department of
Almeida-Muradian, L.B., Stramm, K.M., Horita, A., Barth, O.M., Freitas, A.S., Estevinho, Standards Malaysia. MS, pp. 2683.
L.M., 2013. Comparative study of the physicochemical and palynological character- Marchini, L.C., Carvalho, C.A.L., Alves, R.M.O., Teixeira, G.M., Rubia, V.R., 1998.
istics of honey from Melipona subnitida and Apis Mellifera. Int. Food Sci. Technol. Características físico-químicas de amostras de méis da abelha Uruçu (Melipona scu-
48, 1698–1706. tellaris). XII Congresso Brasileiro de Apicultura 201.
101
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102
Michener, C.D., 2000. The Bees of the World. The Johns Hopkins University Press, 468–469.
Baltimore, Maryland, USA, pp. 913. Silva, I.A.A., Silva, T.M.S., Camara, C.A., Queiroz, N., Magnani, M., Novais, J.S.,
Michener, C.D., 2013. The meliponini. In: Vit, P., Pedro, S.R.M., Roubik, D.W. (Eds.), Pot- Soledade, L.E.B., Oliveira Lima, E., Souza, A.L., Souza, A.G., 2013. Phenolic profile,
Honey: A Legacy of Stingless Bees. Springer, New York, pp. 3–17. antioxidant activity and palynological analysis of stingless bee honey from
Moniruzzaman, M., Chowdhury, M.A.Z., Abdur Rahman, M., Sulaiman, S.A., Siew, H.G., Amazonas, Northern Brazil. Food Chem. 141, 3552–3558.
2014. Determination of mineral, trace element, and pesticide levels in honey samples Simone-Finstrom, M., Spivak, M., 2010. Propolis and bee health: the natural history and
originating from different regions of Malaysia compared to manuka honey. Biomed. significance of resin use by honey bees. Apidologie 41, 295–311.
Res. Int. http://dx.doi.org/10.1155/2014/359890. Article ID 359890, 10 pages. Solayman, M., Islam, M.A., Paul, S., Ali, Y., Khalil, M.I., Alam, N., Gan, S.H., 2016.
Nogeuira-Neto, P., 1997. Carateristicas diversas, distribuicao geografica e aclimatacao. Physicochemical properties, minerals, trace elements, and heavy metals in honey of
In: Nogueira-Neto, P. (Ed.), Vida e criacao de abelhas indigenas sem ferrao. Sao different origins: a comprehensive review. Compr. Rev. Food Sci. Food Saf. 15,
Paulo, Noguerapis, pp. 33–38. 219–233.
Nweze, J.A., Okafor, J.I., Nweze, E.I., Nweze, J.E., 2017. Evaluation of physicochemical Sousa, J.M.B., Souza, E.L., Marques, G., Toledo Benassi, M., Gullon, B., Pintado, M.M.,
and antioxidant properties of two stingless bee honeys: a comparison with Apis Magnani, M., 2016. Sugar profile, physicochemical and sensory aspects of monofloral
mellifera honey from Nsukka. Niger. BMC Res. Notes 10, 566. honeys produced by different stingless bee species in Brazilian semi-arid region. Food
Oddo, L.P., Piazza, M.G., Pulcini, P., 1999. Invertase activity in honey. Apidologie 30, Sci. Technol. 65, 645–651.
57–65. Souza, D.C., Bazlen, K., 1998. Análises preliminares de características físico-químicas de
Oddo, L.P., Heard, T.A., Rodriguez-Malaver, A., Perez, R.A., Fernandez-Muino, M., méis de tiúba (melipona compressipes). Anais XII Cong. Bras. de Apicultura.
Sancho, M.T., Sesta, G., Lusco, L., Vit, P., 2008. Composition and antioxidant activity 267–268.
of trigona carbonaria honey from Australia. J. Med. Food 11 (4), 789–794. Souza, B.A., Carvalho, C.A.L., Sodre, G.S., Marchini, L.C., 2004. Caracteristicasfisico-
Onyenso, A.L., Akachuku, C.O., 2011. Physico-chemical properties of honeys produced by quimicas de amostrasde mel de Melipona asilvai (Hymenoptera: Apidae). Cienc Rural
two stingless bee species—Trigonacarbonaria and Melipona Beecheii in South- 34, 1623–1624.
Eastern Nigeria. J. Agric. For. Soc. Sci. 9 (1), 19–26. Souza, B., Roubik, D., Barth, O., Heard, T., Enriquez, E., Carvalho, C., Villas-Boas, J.,
Pasias, I.N., Kiriakou, I.K., Proestos, C., 2017. HMF and diastase activity in honeys: a fully Marchini, L., Locatelli, J., Persano-Oddo, L., Almeida-Muradian, L., Bogdanov, S., Vit,
validated approach and a chemometric analysis for identification of honey freshness P., 2006. Composition of stingless bee honey: setting quality standards. Interciencia
and adulteration. Food Chem. 229, 425–431. 31, 867–875.
Puciarelli, A.B., Schapovaloff, M.E., Kummritz, S., Senuk, I.A., Brumovsky, L.A., Suntiparapop, K., Prapaipong, P., Chantawannakul, P., 2012. Chemical and biological
Dallagnol, A.M., 2014. Microbiological and physicochemical analysis of yatei properties of honey from Thai stingless bee (Tetragonula leaviceps). J. Apic. Res. 51
(Tetragonisca angustula) honey for assessing quality standards and commercializa- (1), 45–52.
tion. Rev. Argent Microbiol. 46 (4), 325–332. Tomas-Barberan, F.A., Ferreres, F., Garcia-Viguera, C., Tomas-Lorente, F., 1992.
Ramanauskiene, K., Stelmakiene, A., Briedis, V., Ivanauskas, L., Jakštas, V., 2012. The Flavonoids in honey of different geographical origin. Lebensmittel Untersuchung und
quantitative analysis of biologically active compounds in Lithuanian honey. Food Forschung 196, 38–44.
Chem. 132, 1544–1548. Tuksitha, L., Chen, Y., Chen, Y., Wong, K., Peng, C., 2018. Antioxidant and antibacterial
Rasmussen, C., Cameron, S.A., 2010. Global stingless bee phylogeny supports ancient capacity of stingless bee honey from Borneo (Sarawak). J Asia Pac. Entomol 21 (2),
divergence, vicariance, and long distance dispersal. Biol. J. Linn. Soc. 99, 206–232. 563–570.
Rodrigues, A.C.L., Marchini, L.C., Carvalho, C.A.L., 1998. Análises de mel de Apis mel- Villas-Bôas, J.K., Malaspina, O., 2005. Parâmetros físico-químicos propostos para o
lifera L. 1758 e Tetragonisca angustula (Latreille, 1811) coletado em Piracicaba-SP. controle de qualidade do mel de abelhas sem ferrão no Brasil. Mensagem Doce 82,
Rev. Agric. 73, 255–262. 6–16.
Rodríguez-Malavera, A.J., Rasmussen, C., Gutiérrez, M.G., Gild, F., Nieves, B., Vit, P., Vit, P., Pucini, P., 1996. Diastase and invertase activities in Meliponini and Trigonini
2009. Properties of honey from ten species of Peruvian stingless bees. NPC 4 (9), honeys from Venezuela. J. Apic. Res. 35 (2), 57–62.
1221–1226. Vit, P., Bogdanov, S., Kilchenmann, V., 1994. Composition of Venezuelan honeys from
Sancho, M.T., Mato, I., Huidobro, J.F., Fernández-Muiño, M.A., Pascual-Maté, A., 2013. stingless bee (Apidae: Meliponinae) and Apis mellifera L. Apidologie 25, 278–288.
Nonaromatic organic acids of honeys. In: Vit, P., Pedro, S.R.M., Roubik, D.W. (Eds.), Vit, P., Persano Oddo, L., Marano, M.L., Salas de Mejías, E., 1998. Venezuelan stingless
Pot-Honey: A Legacy of Stingless Bees. Springer, New York, pp. 447–458. bee honeys characterized by multivariate analysis of physicochemical properties.
Santiesteban-Hernández, A., Cuadriello, J.A., Loper, G., 2003. Comparación de Apidologie 29, 377–389.
parámetros físico-químicos de mieles de abejas sin aguijón y Apis mellifera de la Vit, P., Medina, M., Enriquez, M.E., 2004. Quality standards for medicinal uses of
región del Sonocusco, Chiapas, México. III Seminario Mesoamericano sobre Abejas Meliponinae honey in Guatemala, Mexico and Venezuela. Bee World. 85 (11), 2–5.
sin Aguijón. Tapachula, Mexico, pp. 60–61. Weaver, N., Weaver, E.C., 2015. Beekeeping with the stingless Bee Meupona Beecheii, by
Sato, T., Miyata, G., 2000. The nutraceutical benefit, part 3: honey. Nutrition 16, the Yucatecan Maya. Bee World 62 (1), 7–19.
102