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Journal of Food Composition and Analysis 73 (2018) 91–102

Contents lists available at ScienceDirect

Journal of Food Composition and Analysis


journal homepage: www.elsevier.com/locate/jfca

Review

Physicochemical properties of stingless bee honey from around the globe: A T


comprehensive review
Abid Nordina, Nur Qisya Afifah Veronica Sainika, Shiplu Roy Chowdhuryb, Aminuddin Bin Saimc,

Ruszymah Bt Hj Idrusa,
a
Department of Physiology, Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur,
Malaysia
b
Tissue Engineering Centre, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur, Malaysia
c
Ear, Nose & Throat Consultant Clinic, Ampang Puteri Specialist Hospital, Ampang, Selangor, 68000, Malaysia

A R T I C LE I N FO A B S T R A C T

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

3. Honey standards Moisture (g/100 g) max 20 max 30 max 35


Sum of Fructose and min 60 min 50 max 85
Honey contains approximately 200 distinct chemical compounds Glucose (g/100 g)
Sucrose (g/100 g) max 5 max 6 max 7.5
(Ramanauskiene et al., 2012). Each honey’s composition and properties
Maltose (g/100 g) Not applicable Not applicable max 9.5
are unique and are dependent to the floral and geographical origin of Free Acidity (meq/100 g) max 50 max 85 Not applicable
the nectar that the bee collected (Tomas-Barberan et al., 1992). Many Ash Content (g/100 g) max 0.5 max 0.5 max 1.0
techniques—such as pollen identification, gas chromatography spec- HMF Content (mg/kg) max 40 max 40 max 30
trometry, and identification of selected chemical parameters—have Diastase Activity (DN) min 8 min 3 Not applicable
pH Not applicable Not applicable 2.5 – 3.8
been employed to determine the floral and geographical origin of honey
Presence of plant Not applicable Not applicable Present
(Anklam et al., 1998). In 1990, an International Honey Commission phenolics
(IHC) was formed to revise the analytical method use to assess honey

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A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102

Table 2 Table 2 (continued)


List of stingless bee species included in the review.
Bee species Source
Bee species Source
Tetragonisca angustula Puciarelli et al., 2014; Anacleto et al., 2009;
Cephalotrigona capitata Almeida and Marchini, 2004. Rodriguez et al., 2009; Almeida and Marchini, 2004;
Frieseomelitta aff varia Vit et al., 1994. Santiesteban-Hernandez et al., 2003; Denadai et al.,
Geniotrigona thoracica Tuksitha et al., 2018; Abu Bakar et al., 2017. 2002; Grajales et al., 2001; Rodrigues et al., 1998;
Heterotrigona Tuksitha et al., 2018. Vit et al., 1998.
erythrogastra Tetragonula fuscobalteata Chuttong et al., 2016.
Heterotrigona itama Tuksitha et al., 2018; Abu Bakar et al., 2017; Kek Tetragonula laeviceps Suntiparapop et al., 2012.
et al., 2017. Tetragonula laeviceps- Chuttong et al., 2016.
Homotrigona fimbriata Chuttong et al., 2016. pagdeni complex
Hypotrigona sp. Nweze et al., 2017. Tetragonula testaceitarsis Chuttong et al., 2016.
Lepidotrigona doipaensis Chuttong et al., 2016. Tetrigona apicalis Chuttong et al., 2016.
Lepidotrigona flavibasis Chuttong et al., 2016. Tetrigona melanoleuca Chuttong et al., 2016.
Lepidotrigona terminata Chuttong et al., 2016. Trigona angustula latreille Fuenmayor et al., 2012.
Lisotrigona furva Chuttong et al., 2016. Trigona fuscipennis Biluca et al., 2016.
Melipona asilvai Souza et al., 2004. Trigona sp. Issaro et al., 2013.
Melipona beecheii Alvarez-Suarez et al., 2018, Onyenso et al., 2011, Trigonalaeviceps Smith Issaro et al., 2013.
Santiesteban-Hernandez et al., 2003, Grajales et al., Trigonapagdenis Schwarz Issaro et al., 2013.
2001.
Melipona bicolor Biluca et al., 2016.
Melipona capixaba Lage et al., 2012.
Melipona compressipes Almeida-Muradian et al., 2007; Villas et al., 2004;
mellifera, the most commonly studied sting bee honey species, each of
Souza et al., 1998; Vit et al., 1994; Gonnet et al., the studies found focused on honey produced by different species of
1964. stingless bee. A total of 40 journal articles and conference proceedings
Melipona crinita Rodriguez et al., 2009. were identified, reporting physicochemical data of 522 honey samples.
Melipona eburnea Rodriguez et al., 2009.
A total of 67 different species of stingless bee from 20 different sub-
Melipona fasciculata Fernandes et al., 2018, Lemos et al., 2017.
Melipona favosa Vit et al., 1998, 1994. genera were investigated. The list of the different species is available in
Melipona flavolineata Lemos et al., 2017. Table 2.
Melipona grandis Rodriguez et al., 2009.
Melipona ilota Rodriguez et al., 2009.
Melipona lateralis Vit et al., 1998.
5. Geographical origin
kangarumensis
Melipona mandacaia Alves et al., 2005.
Melipona marginata Biluca et al., 2016. A significant portion of the articles that we obtained reported ana-
Melipona mondury Biluca et al., 2016; Lage et al., 2012. lysis on stingless bee honey that originated from the neotropical regions
Melipona paraensis Vit et al., 1998. of Central and South America (Alvárez-Suárez et al., 2018; Fernandes
Melipona quadrifasciata Biluca et al., 2016; Carvalho et al., 2009; Almeida
and Marchini, 2004.
et al., 2018; do Vale et al., 2017; Gomes et al., 2017; Lemos et al., 2018;
Melipona quadrifasciata Gonnet et al., 1964. Biluca et al., 2016; Jimenez et al., 2016; Sousa et al., 2016; Pucciarelli
anthidioides et al., 2014; Almeida-Muradian et al., 2013; Silva et al., 2013;
Melipona rufiventris Lage et al., 2012. Fuenmayor et al., 2012; Lage et al., 2012; Anacleto et al., 2009;
Melipona rufiventris Biluca et al., 2016.
Carvalho et al., 2009; Guerrini et al., 2009; Rodriguez-Malavera et al.,
mondury
Melipona scutellaris Biluca et al., 2016; Carvalho et al., 2009; 2009; Almeida-Muradian et al., 2007; Vit et al., 1998). This might be
Evangelista-Rodrigues et al., 2005; Marchini et al., due to the more abundant occurrence of stingless bees in the region.
1998. There is also ample information regarding the history of the cultivation
Melipona scutellaris Sousa et al., 2016. of stingless bee honey by the Mayan civilization, which may correlate to
latrelle
Melipona seminigra Almeida-Muradian et al., 2007; Villas-Boas and
the Central and South American scientist’s motivation to study them
Malaspina 2005. (Weaver and Weaver, 2015). Countries from the regions include Ar-
Melipona seminigra Silva et al., 2013. gentina (Puciarreli et al., 2014), Brazil (Fernandes et al., 2018; do Vale
merrillae et al., 2017; Gomes et al., 2017; Lemos et al., 2018; Biluca et al., 2016;
Melipona solani Grajales et al., 2001.
Sousa et al., 2016; Almeida-Muradian et al., 2013; Silva et al., 2013;
Melipona sp. Do Vale et al., 2017; Gomes et al., 2017; Nweze
et al., 2017. Lage et al., 2012; Anacleto et al., 2009; Carvalho et al., 2009; Almeida-
Melipona subnitida Almeida-Muradian 2013. Muradian et al., 2007; Alves et al., 2005; Evangelista-Rodrigues et al.,
Melipona subnitida ducke Sousa et al., 2016. 2005; Almeida and Marchini, 2004; Souza et al., 2004; Villas-Boas and
Melipona trinitatis Vit et al., 1994. Malaspina, 2004; Denadai et al., 2002; Marchini et al., 1998; Rodrigues
Nannotrigona melanocera Rodriguez et al., 2009.
Partamona epiphytophila Rodriguez et al., 2009.
et al., 1998; Souza and Bazlen, 1998; Gonnet et al., 1964), Cuba (Al-
Partamona sp. Santiesteban-Hernandez et al., 2003. varez-Suarez et al., 2018), Colombia (Fuenmayor 2012), Ecuador
Pleibeia droryana Almeida and Marchini, 2004. (Guerrini et al., 2009), Mexico (Jimenez et al., 2016; Santiesteban-
Ptilotrigona lurida Rodriguez et al., 2009. Hernandez et al., 2003; Grajales et al., 2001), Peru (Rodriguez-
Scaptotrigona bicuntata Biluca et al., 2016.
Malavera et al., 2009), and Venezuela (Vit et al., 1998, 1994). Each
Scaptotrigona mexicana Jimenez et al., 2016.
Scaptotrigona pachysoma Santiesteban-Hernandez et al., 2003. honey sample was collected from differing provinces in each country,
Scaptotrigona polystica Rodriguez et al., 2009. resulting in a more widespread sampling of the honey’s geographical
Scaptotrigona postica Gonnet et al., 1964. origin.
Scaptotrigona sp. Lemos et al., 2017. Apart from the American countries, the data discussed in this review
Scaura latitarsis Rodriguez et al., 2009.
Tetragona carbonaria Onyenso et al., 2011, Oddo et al., 2008.
also come from Thailand (Chuttong et al., 2016; Issaro et al., 2013;
Tetragona clavipes Biluca et al., 2016. Suntiparapop 2012), Malaysia (Tukshita et al., 2018, Abu Bakar et al.,
Tetragonilla collina Chuttong et al., 2016. 2017; Kek et al., 2017), Nigeria (Onyenso et al., 2011, Nweze et al.,
2017), and Australia (Oddo et al., 2008). In all four countries, the re-
introduction of Meliponiculture is rather new, despite years of un-
documented traditional Meliponiculture locally. Nevertheless, with the

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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)

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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)

Scaptotrigona pachysoma 1 26.9 6.6 3.94 1.1 – 0.49 Santiesteban-Hernandez


et al., 2003
Scaptotrigona polystica 1 33 – – – – – Rodriguez et al., 2009
Scaptotrigona postica 1 26.5 83.7 3.4 18.9 – – Gonnet et al., 1964
Scaptotrigona sp. 3 30.22 60.98 3.89 24.71 – – Lemos et al., 2017
Scaura latitarsis 1 20.8 – – – – – Rodriguez et al., 2009
Tetragona carbonaria 8 26.5 128.9 4 1.2 0.48 1.64 Oddo et al., 2008
Tetragona clavipes 1 25.2 91.2 4.28 < 0.31 – 1.01 Biluca et al., 2016
Tetragonilla collina 1 28 25 3.9 5.9 0.245 0.435 Chuttong et al., 2016
Tetragonisca angustula 28 24 79 3.72 – – – Puciarelli et al., 2014
20 24.37 45.23 4.1 9.39 0.39 0.134 Anacleto et al., 2009
1 28.9 – – – – – Rodriguez et al., 2009
3 23.2 48.3 – 9.8 0.38 7.32 Vit et al., 1998
5 26 – – 5 – – Rodrigues et al., 1998
1 25.5 26 3.69 8.1 0.32 – Almeida and Marchini, 2004
1 26.7 7.7 3.88 4.3 – 0.78 Santiesteban-Hernandez
et al., 2003
25 23.7 109 3.8 – 0.45 – Denadai et al., 2002
4 23.2 57.5 4.35 39.1 – 1.1 Grajales et al., 2001
Tetragonula fuscobalteata 2 26 96.5 3.7 22 0.67 1.35 Chuttong et al., 2016
Tetragonula laeviceps 19 26.98 81.37 3.62 1.07 0.27 0.62 Suntiparapop et al., 2012
Tetragonula laeviceps-pagdeni 10 28 76 3.6 5.4 0.22 0.587 Chuttong et al., 2016
complex
Tetragonula testaceitarsis 2 30.5 70.5 3.6 2.95 0.205 0.59 Chuttong et al., 2016
Tetrigona apicalis 2 42 495 3.2 0.26 1.4 2.6 Chuttong et al., 2016
Tetrigona melanoleuca 1 43 592 3.4 28 3.1 2.8 Chuttong et al., 2016
Trigona angustula latreille 44 24.3 39.2 4.2 1.3 0.205 0.658 Fuenmayor et al., 2012
Trigona fuscipennis 1 34.4 46.7 3.44 < 0.31 – 0.31 Biluca et al., 2016
Trigona sp. 1 13.26 78.14 3.35 3.18 0.2 0.57 Issaro et al., 2013
Trigonalaeviceps Smith 1 15.73 50.83 3.44 3.32 0.14 0.57 Issaro et al., 2013
Trigonapagdenis Schwarz 1 14.66 20 4.01 3.97 0.22 0.45 Issaro et al., 2013
Average 27.68 73.59 3.85 12.12 0.404 1.160
Standard Deviation 5.8 101.53 0.53 16.22 0.49 1.60

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

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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)

Frieseomelitta aff varia 7 61 – – – 4.8 Vit et al., 1994


Geniotrigona thoracica 1 29.64 12.01 17.63 35.3 – Tukshita et al., 2018.
1 71.52 – – – – Abu Bakar et al., 2017
Heterotrigona itama 1 40.5 19.5 21 33.7 – Tukshita et al., 2018.
1 70.74 – – – – Abu Bakar et al., 2017
3 24.99 15.77 9.22 – 32.33 Kek et al., 2017
Heterotrigona erythrogastra 1 27.2 12.3 14.9 45.2 – Tukshita et al., 2018.
Homotrigona fimbriata 1 22 7.4 15 – – Chuttong et al., 2016
Hypotrigona sp. 3 60.49 – – – 1.83 Nweze et al., 2017
Lepidotrigona doipaensis 2 38.5 12 11.9 – – Chuttong et al., 2016
Lepidotrigona flavibasis 4 68 16 13 39 – Chuttong et al., 2016
Lepidotrigona terminata 1 66 8.1 4.9 53 – Chuttong et al., 2016
Lisotrigona furva 2 62.5 33.5 26.5 0.6 – Chuttong et al., 2016
Melipona asilvai 11 68.9 – – – 4.7 Souza et al., 2004
Melipona beecheii 1 69.21 – – – 1.6 Onyenso et al., 2011
1 68 – – – 1.6 Santiesban-Hernandez et al.,
2003
Melipona bicolor 5 60.14 32.84 27.22 – < 0.074 Biluca et al., 2016
Melipona compressipes 2 31.38 29.02 – 0.15 Almeida-Muradian et al., 2007
8 65.3 – – – 3.5 Villas et al., 2004
5 75.7 – – – 1.6 Vit et al., 1994
Melipona fasciculata 20 51.35 – – – Fernandes et al., 2018
4 70.57 – – – 2.17 Lemos et al., 2017
Melipona favosa 14 72.1 – – – 1.5 Vit et al., 1994
6 70.3 – – – 2 Vit et al., 1998
Melipona flavolineata 4 59.31 – – – 5.52 Lemos et al., 2017
Melipona lateralis kangarumensis 3 64.8 – – – 1.1 Vit et al., 1998
Melipona mandacaia 20 74.8 – – – 2.9 Alves et al., 2005
Melipona marginata 8 64.49 36.25 28.24 – < 0.074 Biluca et al., 2016
Melipona paraensis 4 60.8 – – – 1.2 Vit et al., 1998
Melipona quadrifasciata 12 61.77 34.71 27.42 – Biluca et al., 2016
2 60.24 – – – 1.3 Carvalho et al., 2009
Melipona rufiventris mondury 1 65.6 35.6 30.1 – < 0.074 Biluca et al., 2016
Melipona scutellaris 1 62.7 – – – < 0.074 Biluca et al., 2016
2 55.45 – – – 2.14 Carvalho et al., 2009
Melipona scutellaris latrelle 12 67.38 54.3 42.43 – 2.4 Sousa et al., 2016
Melipona seminigra 2 – 31.84 29.6 – 0.18 Almeida-Muradian et al., 2007
8 65.4 – – – 3 Villas et al., 2004
Melipona sp. 16 49.4 – – – 3.8 Do Vale et al., 2017
9 59.21 – – – Gomes et al., 2017
3 75.64 – – – 5.06 Nweze et al., 2017
Melipona subnitida 24 – 29.21 21.76 – 4.86 Almeida et al., 2013
Melipona subnitida ducke 12 67.63 54.38 42.73 – 1.85 Sousa et al., 2016
Melipona trinitatis 4 73.7 – – – 1.5 Vit et al., 1994
Partamona sp. 1 62.5 – – – 1.1 Santiesteban-Hernandez et al.,
2003
Scaptotrigona bicuntata 2 62.95 35.65 27.2 – < 0.074 Biluca et al., 2016
Scaptotrigona mexicana 12 56.48 – – – Jimenez et al., 2016
Scaptotrigona pachysoma 1 70.1 – – – 2 Santiesteban-Hernandez et al.,
2003
Scaptotrigona sp. 3 62.34 – – – 4.83 Lemos et al., 2017
Tetragona carbonaria 8 – 17.5 24.5 20.3 1.8 Oddo et al., 2008
Tetragona clavipes 1 48.6 40.2 8.21 – < 0.074 Biluca et al., 2016
Tetragonilla collina 1 52 26 26 – – Chuttong et al., 2016
Tetragonisca angustula 28 – 24 19 – – Puciarelli et al., 2014
20 55.46 – – – 0.95 Anacleto et al., 2009
3 65.9 – – – 2.1 Vit et al., 1998
5 58.7 – – – Rodrigues et al., 1998
1 70 – – – 2.4 Santiesteban-Hernandez et al.,
2003
25 58 – – – 2.4 Denadai et al., 2002
Tetragonula fuscobalteata 2 32.5 21 31.5 – Chuttong et al., 2016
Tetragonula laeviceps 19 47.87 27.08 20.8 – 19.15 Suntiparapop et al., 2012
Tetragonula laeviceps-pagdeni 10 29 17 12 37 0.025 Chuttong et al., 2016
complex
Tetragonula testaceitarsis 2 41 22 19 – – Chuttong et al., 2016
Tetrigona apicalis 2 12.5 6.75 5.9 – – Chuttong et al., 2016
Tetrigona melanoleuca 1 15 6 8.9 – – Chuttong et al., 2016
Trigona angustula latreille 44 – 23.5 30.1 – – Fuenmayor et al., 2012
Trigona fuscipennis 1 56.6 36.22 20.4 – < 0.074 Biluca et al., 2016
Trigona sp. 1 29.34 – – – – Issaro et al., 2013
Trigonalaeviceps Smith 1 27.37 – – – – Issaro et al., 2013
Trigonapagdenis Schwarz 1 41.64 – – – – Issaro et al., 2013
(continued on next page)

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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)

Average 55.79 25.16 21.49 33.01 3.65


Standard Deviation 16.23 12.78 9.72 16.11 5.8

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

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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

Frieseomelitta aff varia 7 7.8 – 134.12 – – Vit et al., 1994


Lepidotrigona doipaensis 2 1.6 – – – – Chuttong et al., 2016
Lepidotrigona flavibasis 4 3.1 – – – – Chuttong et al., 2016
Lepidotrigona terminata 1 0.29 – – – – Chuttong et al., 2016
Melipona beecheii 8 1.3 – – – – Alvarez-Suarez et al., 2018
Melipona bicolor 5 <3 – – 64.56 – Biluca et al., 2016
Melipona capixaba 9 – – – 68.23 – Lage et al., 2012
Melipona compressipes 8 7.9 – 448 – – Villas et al., 2004
5 1.1 – 489.4 – – Vit et al., 1994
Melipona crinita 2 – – 370 – 88 Rodriguez et al., 2009
Melipona eburnea 1 – – 650 – 103 Rodriguez et al., 2009
Melipona favosa 14 0.9 – 406.6 – – Vit et al., 1994
6 2.9 90.1 708.7 – – Vit et al., 1998
Melipona grandis 5 – – 350 – 38 Rodriguez et al., 2009
Melipona ilota 1 – – 300 – 26 Rodriguez et al., 2009
Melipona lateralis kangarumensis 3 2.8 58.9 234.2 – – Vit et al., 1998
Melipona marginata 1 <3 – – 66.32 – Biluca et al., 2016
Melipona mondury 11 – – – 68.09 – Lage et al., 2012
1 13.5 – – 69.35 – Biluca et al., 2016
Melipona paraensis 4 2.9 19.8 143.4 – – Vit et al., 1998
Melipona quadrifasciata 12 <3 – – 66.43 – Biluca et al., 2016
1 1.77 – – – – Carvalho et al., 2009
Melipona rufiventris 7 – – 74.12 – Lage et al., 2012
Melipona rufiventris mondury 1 <3 – – 71.7 – Biluca et al., 2016
Melipona scutellaris 1 <3 – – 75.8 – Biluca et al., 2016
1 2.16 – – – – Carvalho et al., 2009
1 3.01 – – – – Carvalho et al., 2009
6 – 816 – – Marchini et al., 1998
Melipona scutellaris latrelle 12 – 375 73.15 74.83 Sousa et al., 2016
8 5 – 560 – Villas et al., 2004
Melipona sp. 16 15.63 – – Do Vale et al., 2017
Melipona subnitida 24 – – 280 – 70 Almeida et al., 2013
Melipona subnitida ducke 12 – – 350 72.55 60.23 Sousa et al., 2016
Melipona trinitatis 4 1 – 478.2 – Vit et al., 1994
Nannotrigona melanocera 1 – – 146 – 150 Rodriguez et al., 2009
Partamona epiphytophila 1 – – 126 – 78 Rodriguez et al., 2009
Ptilotrigona lurida 1 – – 288 – 120 Rodriguez et al., 2009
Scaptotrigona bicuntata 2 4.34 – – 75.1 Biluca et al., 2016
Scaptotrigona mexicana 12 – – – 72.57 Jimenez et al., 2016
Scaptotrigona polystica 1 – 115 – 128 Rodriguez et al., 2009
Scaptotrigona postica 1 – 24.6 – – Gonnet et al., 1964
Scaura latitarsis 1 – 113 – 130 Rodriguez et al., 2009
Tetragona carbonaria 8 0.4 5.7 – – 84.6 Oddo et al., 2008
Tetragona clavipes 1 19.1 – – 73.4 – Biluca et al., 2016
Tetragonilla collina 1 0.34 – – – – Chuttong et al., 2016
Tetragonisca angustula 20 32.28 – 370 – – Anacleto et al., 2009
1 – – 107 – 150 Rodriguez et al., 2009
3 23 50.1 142.27 – – Vit et al., 1998
5 17.9 – – Rodrigues et al., 1998
25 – – 144 – – Denadai et al., 2002
1 4.7 – – – – Chuttong et al., 2016
Tetragonula laeviceps-pagdeni complex 10 0.63 – – – – Chuttong et al., 2016
Tetragonula testaceitarsis 2 0.22 – – – – Chuttong et al., 2016
Tetrigona apicalis 1 4.9 – – – – Chuttong et al., 2016
Tetrigona melanoleuca 1 0.15 – – – – Chuttong et al., 2016
Trigona angustula latreille 44 16.7 – – – – Fuenmayor et al., 2012
Trigona fuscipennis 1 <3 – – 64.5 – Biluca et al., 2016
Trigona sp. 1 16.67 – 173.8 – – Issaro et al., 2013
Trigonalaeviceps Smith 1 13.64 – 178.7 – – Issaro et al., 2013
Trigonapagdenis Schwarz 1 11.11 – 136.4 – – Issaro et al., 2013
Average 7.08 41.5 314.96 70.39 92.90
Standard Deviation 8.01 30.9 194.77 3.83 38.92

typically reduced or absent in adulterated, overheated or excessively 6.10. Soluble solids


stored honey (Almeida-Muradian et al., 2013). In stingless bees, ni-
trogen content reported ranges from 107 mg/100 g to 816 mg/100 g The soluble solids in honey include sugars, organic acids, and mi-
with the mean of 323 mg/100 g and standard deviation of 184 mg/ nerals. The value of this parameter reveals the relationship between the
100 g (Table 5). The lowest nitrogen content reported in Tetragonisca water and sugar content (Biluca et al., 2016). In general, the soluble
angustula honey from Peru and the highest nitrogen content was ob- solids value in stingless bee honey is lower than Apis mellifera honey
served in Melipona scutellaris honey from Brazil. No standard has been due to the higher water content and lower sugar content. This is ap-
set regarding the nitrogen content of honey. parent because the value ranges from 64.5 Brix to 75.8 Brix in stingless
bee compared to Apis mellifera honey that ranges from 78.77 Brix to

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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.

honey samples. However, only two phenolic compounds, coumaric acid


6.12. Phenolic compound and luteolin, were shared by both samples. Table 7 illustrate the phe-
nolic compound detected in stingless bee honey. Detection of coumaric
According to the Malaysian Standards, the presence of plant phe- acid in both honey samples qualify them to be of good quality following
nolic is an indicator of a good quality stingless bee honey. Benzoic acid, Malaysian standards (Malaysian Standards, 2017). However, detection
phenylpropanoic acid, 4-hydroxybenzoic acid, 4-hydroxyphenylacetic of 4-hydroxybenzoic acid and vanilic acid in Melipona seminigra sug-
acid, vanilic acid, protocatechuic acid, and p-coumaric acid are among gested a superior quality according to the Malaysian Standards (Silva
the suggested indicators of a good quality honey (Malaysian Standards, et al., 2013). Hence, a more harmonized standard in terms of phenolic
2017). Two studies reported the presence of individual phenolic com- compound of the stingless bee is also of a paramount importance.
pound in their stingless bee honey sample (Alvarez-Suarez et al., 2018,
Silva et al., 2013). Both studies detected the presence of 14 different
phenolic compounds in their Melipona seminigra and Melipona beecheii

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)

Geniotrigona thoracica 352.53 – 84.12 51.61 – – – – 3.61 – Abu Bakar et al.,


2017
Heterotrigona itama 539.46 – 135.78 31.61 – – – – 4.72 – Abu Bakar et al.,
2017
732.2 589.7 191.9 33.81 – 0.21 6.57 1.766 2.16 – Kek et al., 2017
Melipona beecheii – 11.96 26.51 – – 1.03 – – – – Onyenso et al.,
2011
Melipona bicolor 126.12 4.75 14.79 5.96 0.70 – – – – – Biluca et al., 2016
Melipona fasciculata 448.80 555.07 44.42 12.37 0.17 – – 0.02 – 0.68 Lemos et al., 2017
Melipona flavolineata 127.52 235.28 58.41 28.73 5.51 25.61 – 0.15 – 0.15 Lemos et al., 2017
Melipona marginata 109.06 6.942 11.052 4.17 0.37 – – – – – Biluca et al., 2016
Melipona mondury 194.5 9.335 21.03 9.785 1.12 – – – – Biluca et al., 2016
Melipona quadrifasciata 87.33 4.96 8.03 3.56 0.61 – – – – – Biluca et al., 2016
Melipona rufiventris 45.9 2.25 5.78 2.32 < 0.91 – – – – – Biluca et al., 2016
mondury
Melipona scutellaris < 10.55 0.78 8.24 2.11 < 0.91 – – – – – Biluca et al., 2016
Scaptotrigona bicuntata 168 6.31 10.32 4.45 0.26 – – – – – Biluca et al., 2016
Scaptotrigona sp. 1357.76 212.62 124.82 73.76 1.69 23.69 – 0.53 – 0.12 Lemos et al., 2017
Tetragona clavipes 278 9.04 15.9 7.71 < 0.91 – – – – – Biluca et al., 2016
Trigona angustula 576.6 155.0 199.6 56.0 – – 5.8 0.9 19.6 – Fuenmayor et al.,
latreille 2012
Trigona carbonaria – 12.67 25.43 – – 0.76 – – – – Onyenso et al.,
2011
Trigona fuscipennis 49.2 2.66 3.85 1.15 < 0.91 – – – – – Biluca et al., 2016

100
A. Nordin et al. Journal of Food Composition and Analysis 73 (2018) 91–102

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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.,
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chemical and functional profile of an ancient health product. Food Chem. 114,
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nancial support in the form of research grant (FF-2017-20). International Honey Commission, 2009. Harmonised Methods of the International Honey
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