The diversity and abundance of stingless bee (Hymenoptera: meliponini) in Peninsular Malaysia.
Malaysia is known as one of the world's twelve mega biodiversity countries . One of the indicators of the high biodiversity in Malaysia is the presence of 29 stingless bee species recorded [27,25] and of this number, 17 species are known to inhabit virgin forests . Since 2012, stingless bees have become popular to beekeepers for the collection of honey and as a pollinator species in agroecosystems. Four species of stingless bees, namely Heterotrigona itama, Geniotrigona thoracica, Tetragonilla atripes and Tetrigona peninsularis were studied as pollinator species for many important crops in Malaysia  and of these four, two species was successfully domesticated (H. itama and G. thoracica) in the agroecosystem for meliponiculture . The number of domesticated species is expected to increase yearly due to the decline of pollinators in agricultural areas.
Stingless bees are found to be a major pollinator of lowland dipterocarp species in Malaysia  and in semi-tropics forests . The pollination service provided by insect pollinators is worth [euro]50 billion in fruits and vegetables industries worldwide . In Malaysia, stingless bees are estimated to have a value of about 66 million per year  and since 2012, stingless bees have become a phenomenon due to the high nutrition and medicinal value in their honey and pollen  which contributed to its high market demand. However, the overuse of pesticides in agroecosystems, changes in land use, illegal logging and many other factors are associated with the decline of pollinator populations, especially bees .
In Malaysia's agricultural ecosystems, stingless bees are a common pollinator . However, there are no previous report proving stingless bees as a major pollinator and have the ability to enhance agricultural crop production in Malaysia. Interestingly, a study conducted by Azmi et al.  showed that stingless bees do not choose agriculture crops as their dominant food source.  also reported that the main food source of stingless bees in Taman Tropika Kenyir is the Dipterocarpacea family while Figueredo-Mecca et al.  strongly stated that stingless bees play a major role in the pollination of wild plants and it can be domesticated as a pollinator in agricultural ecosystems as a future pollinating agent.
To date, despite the high diversity of stingless bee species in Malaysia and their potential as the future pollinating agent in the country, there are only few studies conducted on the taxonomy and diversity of the Malaysian native stingless bees. As such, the main objectives of our study are to assess the diversity of stingless bees among the Malaysian states and to inventorize the present number of stingless bees species in Peninsular Malaysia.
MATERIALS AND METHODS
Samplings of stingless bees were conducted from June 2013 to June 2015 at selected recreational forest areas located adjacent or nearby to agriculture areas throughout Peninsular Malaysia (Table 1). Three sets of 300m sampling transects were established in each sampling site which ran approximately parallel to each other with 500m between them. Ten random baiting points were established along the transect. Salted fish with oil as a bait was used at the first transect, while honey with lemon and honey with salt were used at the second and third transects respectively. These baiting techniques were modified from techniques used by Momose et al. ; Salim et al.  and Siti Khairiyah et al. . All baiting points were checked and sampled for stingless bees using sweep nets for three consecutive days. The taxonomic keys used for the identification of stingless bee were based on several taxonomic key books, especially Smith . PAST software was used to analyze the Shannon Weiner index (H'), Simpson diversity index (D'), Evennes index (E') and Margalef richness index (R') of stingless bees. Data were also analyzed with One Way ANOVA and when the ANOVA result was significant, means were separated using Tukey's test at P<0.05. In addition, a two way cluster analysis was done using PC-ORD software (version 5) to find the treatment group based on sites and bait.
RESULTS AND DISCUSSION
A total of 1599 individuals comprising of 35 species of stingless bees were recorded in the Peninsular Malaysia. Five species were found to be the most dominant species recorded in this study. They are Heterotrigona itama (309 individuals) and this agrees with reports by Nagamitsu et al. ; Mohd Norowi et al.  and Salim et al. , followed by Geniotrigona thoracica, Tetragonula laeviceps, Lepidotrigona terminata and Tetrigona apicalis (Figure 1). Among these dominant species, H. itama and G. thoracica have been domesticated by the Malaysia Agriculture Research and Development Institute (MARDI) for the meliponiculture industry . Meanwhile, the minority species were Tetragonula melina, Tetragonulapagdeni, Tetragonula minor, Tetragonula pallidistigma and Lepidotrigona trochanterica.
The Shahnon-weiner species diversity index (H') indicated that Perak has the highest diversity with a H' of 2.64, while the lowest H' was recorded at 1.24 for Wilayah Persekutuan (WP). A similar trend was showed in the Margalef index (R') which showed significant difference between Perak and WP, but not in the Evenness Index (E'). For example, WP and Selangor had higher E' values than the other states, including Perak. This indicates that species evennes (E') plays a more important role than R'  in determing H' value (Table 2). The value of the Simpson diversity index (D') seems to follow the (H') value with Perak and WP having the highest and the lowest values respectively. It can be concluded that the overall abundance, evenness and richness of stingless bees decreases from the north to south of Peninsular Malaysia and also occurred in Australia . The 35 species recorded in this study was higher than previously recorded at 29 species by Schwarz .
Results on species accumulation curves were asymptotes and could be concluded that samples (1599) collected were sufficient (Fig. 2) and 35 species of stingless bees were discovered. Studies on the diversity of stingless bees in Peninsular Malaysia have never been published since 1939, where the researcher had found 29 species of stingless bees. The most recent study was done by Salim et al.  in six virgin jungle forests, namely Berembun Forest Reserve in Pahang, Gunung Angsi Forest Reserve in Negeri Sembilan, Gunung Tebu Forest Reserve in Terengganu, Kledang Saiong Forest Reserve in Perak, Semangkok Forest Reserve in Selangor and Ulu Gombak Forest Reserve also in Selangor which had recorded 17 species of stingless bees. However, the study did not cover all states in Peninsular Malaysia. In Sarawak, research on the diversity of stingless bees was carried out only by Schwarz  who found 32 species of stingless bees in Borneo.
Based on the two way cluster analysis result, it is clear that there are three groups of stingless bee species which have similarities of more than 70%. The first group contains 17 species of stingless bees, namely H. itama G. thoracica, Tetragonula geissleri, Lepidotrigona terminata, Tetragonilla fuscibasis, Tetragonilla atripes, Heterotrigona erythogastra, Lepidotrigona nitidiventris, Tetragonilla irridipenis, Tetragonilla collina, Tetragonilla fusco-balteata Tetrigona apicalis, Homotrigona alicae, Tetragonula laeviceps, Tetragonula pallidistigma, Tetragonula melina, and Tetragonula reepeni. This group can be labeled as the environment tolerance group since they are present in most locations. From our observation, most of them are able to nest in various places such as building cracks, pipe hoses, hollow trees and other places similarly decribed by Halcroft  on Australia species.
The second group comprises of 6 species of stingless bees, namely Lepidotrigona ventralis, Lophotrigona canifrons, Homotrigona fimbriata, Tetragonula gressiti, Hypotrigona scintillans, and Hypotrigona pendleburyi and have more than 50% similarity with each other. Compared to the species in group 1 where most of them are present in all locations, only T. gressiti and H. scintillans from this group are present in almost all locations. This indicates that the species in group 2 are more susceptible to habitat disturbance as stated by Boussathaanissa and Zihad  in their study on honey bees. There were 10 species having more than 50% similarity in group 3 (Fig. 3). In addition, Lepidotrigona trochanterica, Hypotrigona pendleburyi and Sundartigona moorei were not clustered into any groups. Roubik  reported that S. moorei is normally associated with ants nests. This special behavior does not occur in other species found in this study. This special characteristic could be the key to why this species was only found in one state (Pahang) in Peninsular Malaysia. Overall, the species in group 3 are more adaptable to habitat changes except in the Lata Kekabu Recreational Forest in Perak.
At 75% habitat similarity, the two way cluster analysis had produced 4 groups. The first group consists of Johor and Selangor which represent two of the most industrialized states where there exists a lot of habitat disturbance. Pahang and Negeri Sembilan were clumped together, which is not surprising because two states are neighbours . While the third group consists of Perak and Malacca. Referring to the states' species, Perak has a higher diversity rate than Malacca. However, the intensity of sum species between states are not far enough. The last group consists of Perlis, Kelantan, Kedah and Terengganu. Habitat disturbance in these four states were not more than 20%. Most of the land area is green and there is less development and suitable for the stingless bees build their nest . Furthermore, these four states situated at three major mountain range which is extremely rich of diversity . Penang and WP were not grouped with other states as its land area is highly developed and most of the stingless bees' habitat disturbance occurs here (Fig. 3).
In Malaysia, studies on stingless bees' diversity and their abundance is important since there are changes of land use from forest areas to agricultural areas or development purposes. The methods for sampling of stingless bees must be expanded since from our data, using salted fish with oil and honey with salt provided the best results when sampling in forest areas, indicating that salt is the major ingredient in baiting components (Fig. 4). In our observation, we found that stingless bees always hover around us and take our sweat, indicating that salt are important for bees as also reported by Lau and Nieh . The sampling time may be an important factor in discovering stingless bees as they are active in the morning and inactive on rainy days .
Identifying the bees' taxonomy was a major constraint in studying the samples collected. We expect more new species to be recorded and named using the collected samples after detailed taxonomic study using more sample collections throughout Malaysia are conducted. As such, future studies should be done to assess every ecological variation in Peninsular Malaysia and its relation to the stingless bee population's abundance and diversity. Research on the food source of stingless bees has also not been fully carried out in Malaysia, as reported by Azmi et al.  and Ghazi . Also, some baseline data must be gathered for future studies purposes, for example in the breeding of stingless bees for conservation or pollination programs.
There is vast development of stingless bees apiary in Malaysia. Nevertheless, there is some effect on meliponiculture to biodiversity in Malaysia. Reaping of stingless bees colony from the forest area derived the ecosystem changes also alter the ecosystem services. As such, forest stingless bees species with resin tree as a main food source has been domesticated in the agriculture area; as a result the species will be collapse when there are no resources for their food and hives. That is the point of our data important to bee keepers, that some species must be remained in the forest.
In addition, our data found there are new common species which is T. laeviceps, L. terminata and T. apicalis. Study must be conducted to quantify their contribution to agricultural areas in Peninsular Malaysia. Before this, there are two species has been domesticated in meliponiculture in Malaysia by MARDI. In future, who knows, these species better than present domesticated species. Furthermore, one of the stingless bees species (T. laeviceps) found a lot in the urban areas and could be promoted as a one of main factor in urban farming.
This study has successfully updated and inventorized stingless bees of Peninsular Malaysia which has increased from 29 to 35 species. This shows that if conservation strategies could be implemented now, we are still on track to conserve the stingless bee population. This finding could also be used to educate decision makers and the general public about the importance and contribution of stingless bees in Malaysia.
The authors extend their appreciation for the financial support received from the Taman Tropika Kenyir project (KG0007410). The team will also like to thank Mr Jayprakash Pertabrai for his help in the identification process, Mr Zulidzham Mohd Sani and Mr Hamdan Sipon for technical support, and Mr Ganaraj Katharayan for guidance in the forest areas.
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(1,2) Mohd Fahimee Jaapar, (1) Madihah Halim, (2) Muhamad Radzali Mispan, (2) Rosliza Jajuli, (2) Mohd Masri Saranum, (2) Mohd Yusri Zainuddin, (3) Roziah Ghazi, (1) Idris Abd Ghani
(1) Mohd Fahimee Jaapar, Research Officer, (Centre of Insect Systematics, National University of Malaysia, Bangi/ Agrobiodiversity and Environment Research Centre, MARDI Headquarters, Serdang), Selangor, Malaysia. Madihah Halim, Researcher, Centre of Insect Systematics, National University of Malaysia, Bangi, Selangor, Malaysia.
(2) Muhamad Radzali Mispan, Research Officer, Agrobiodiversity and Environment Research Centre, MARDI Headquarters, Serdang, Selangor, Malaysia.
(2) Rosliza Jajuli, Deputy Director, Agrobiodiversity and Environment Research Centre, MARDI Headquarters, Serdang, Selangor, Malaysia.
(2) Mohd Masri Saranum, Research Officer, Agrobiodiversity and Environment Research Centre, MARDI Headquarters, Serdang Selangor, Malaysia.
(2) Mohd Yusri Zainuddin, Research Officer, Agrobiodiversity and Environment Research Centre, MARDI Headquarters, Serdang, Selangor.
(3) Roziah Ghazi, Researcher, Institute Agropolis, Sultan Zainal Abidin University, Besut, Terengganu, Malaysia.
(1) Idris Abd Ghani, Professor, Centre of Insect Systematics, National University of Malaysia, Selangor, Malaysia.
Address For Correspondence:
Idris A. B, Department of Environment and Natural Resources Sciences, Faculty of Science and Technology, National University of Malaysia 43600 Bangi, Selangor, Malaysia.
Tel: +60389215973, Fax: +60389253357, E-mail: firstname.lastname@example.org
Received 12 July 2016; Accepted 18 September 2016; Available online 22 September 2016
Table 1: Sampling sites employed for the sampling of stingless bees throughout Peninsular Malaysia conducted from June 2013 to June 2015 Sampling sites Coordinate Perlis (Perlis State 6[degrees]38'42.4"N 100[degrees]12'12.2"E Park) Kedah (Titi Hayun 5[degrees]47'39.8"N 100[degrees]24'06.2"E recreational forest) Perak (Lata Kekabu 5[degrees]02'39.9"N 100[degrees]56'57.9"E Recreational forest) Penang (Kampung Tengah 5[degrees]26'54.9"N 100[degrees]12'12.8"E Teluk Bahang) Selangor (Gunung Nuang 3[degrees]13'02.5"N 101[degrees]52'56.8"E Recreational forest) Wilayah Persekutuan 3[degrees]09'01.4"N 101[degrees]42'05.7"E (Bukit Nanas recreational forest) Negri Sembilan (Gunung 2[degrees]32'36.9"N 102[degrees]10'09.0"E Datuk Recreational Forest) Melaka (Sungai Udang 2[degrees]18'00.3"N 102[degrees]07'52.1"E Recreational forest) Johor (Gunung Ledang 2[degrees]20'29.1"N 102[degrees]37'02.6"E Recreational Forest) Pahang (Kampung Pagi, 4[degrees]27'00.7"N 102[degrees]28'56.3"E National Park) Terengganu (Pulau 5[degrees]09'51.5"N 102[degrees]44'41.8"E Tekak, Tasik Kenyir) Kelantan (Jelawang) 5[degrees]20'21.9"N 101[degrees]58'28.3"E Table 2: Ecological indices of stingless bees in Peninsular Malaysia Ecological indices Shahnon- weiner Simpson diversity Evennes Margalef diversity State index index index index (H') (E') (R') (D') Perak 2.64 (a) 0.64 5.20 0.89 Kedah 2.56 (a) 0.66 5.12 0.89 Terengganu 2.46 (a) 0.71 4.19 0.88 Selangor 2.37 (a) (b) 0.78 3.90 0.88 Pahang 2.34 (a) (b) 0.67 3.63 0.86 Kelantan 2.30 (a) (b) 0.69 3.58 0.87 Negeri 2.24 (a) (b) 0.71 3.41 0.86 Sembilan Perlis 2.10 (a) (b) 0.75 3.03 0.85 Malacca 2.01 (a) (b) 0.66 2.73 0.82 Johore 1.75 (b) (c) 0.67 2.30 0.76 Penang 1.74 (b) (c) 0.66 2.25 0.75 Wilayah 1.24 (c) 0.73 1.51 0.63 Persekutuan Letters (a) and (b) indicate whether there are significant differences in terms of species diversity between the different species (Tukey's Test)
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|Author:||Jaapar, Mohd Fahimee; Halim, Madihah; Mispan, Muhamad Radzali; Jajuli, Rosliza; Saranum, Mohd Masri;|
|Publication:||Advances in Environmental Biology|
|Date:||Sep 1, 2016|
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