Apis Florea Morphometrics
Apis Florea Morphometrics
Apis Florea Morphometrics
biogeography
H. Randall Hepburn, Sarah E. Radloff, Gard W. Otis, Stefan FUCHS, L.R.
VERMA, Tan Ken, T. Chaiyawong, G. Tahmasebi, R. Ebadi, Siriwat Wongsiri
aDepartment of Zoology and Entomology, Rhodes University, Grahamstown, 6140, South Africa
b Department of Statistics, Rhodes University, Grahamstown, 6140, South Africa
c Department of Environmental Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
d Institut für Bienenkunde (Polytechnische Gesellschaft) Fachbereich Biologie der J. W. Goethe-Universität
Frankfurt am Main, Karl-von-Frisch-Weg 2, 61440 Oberursel, Germany
e Department of Bio-Sciences, Himachal Pradesh University, Shimla 171005, HP, India
f Eastern Bee Research Institute of Yunnan Agricultural University, Kunming, China
g Department of Biology, Chulalongkorn University, Phayathai Road, Phathumwan, Bangkok 10330, Thailand
h Honeybee Department, Animal Science Research Institute, Karaj, Iran
Abstract – Multivariate morphometric analyses were performed on 2923 individual worker bees from 184
colonies representing 103 localities across the full distributional area of Apis florea Fabricius 1787 from
Vietnam and southeastern China to Iran and Oman (~7000 km). Morphologically A. florea is unequivocally
separable from A. andreniformis. Comparisons of geographically separated A. florea populations result in
morphoclusters that reflect sampling artifacts. These morphoclusters change clinally with latitude but
overlap when the full database is contained in the same principal component analysis. A cluster analysis
based on Euclidean distances suggests degrees of affinity between various geographic groupings of A.
florea. This species occupies a large area that includes rainforests, savannas, subtropical steppes, and
semideserts. The seasonality of reproductive swarming is temporally continuous allowing gene flow
throughout this panmictic species.
Takahashi et al., unpublished data), and differ- 1988, 1992; Engel, 1999). An improved range
ences in the timing of mating flights (Rinderer map showing the distribution of this wide-
et al., 1993). Several of these differences contrib- spread species is also included.
ute to complete reproductive isolation between
the two species (Koeniger and Koeniger, 1991,
2000, 2001; Dung et al., 1996). 2. MATERIALS AND METHODS
Considering infraspecific variation in A. flo-
rea, Maa (1953) taxonomically synonymized 2.1. Identification of A. florea
all previous subspecific taxa (Gerstäcker, and A. andreniformis
1863; Enderlein, 1906; von Buttel-Reepen,
1906; Cockerell, 1911; Dover, 1929). Since The morphometric database currently available
then no subspecies of A. florea have been pro- for A. andreniformis is still too fragmentary for
posed (Engel, 1999). inclusion here. This is unfortunate because some of
the historical confusion between A. florea and A.
Several univariate regional studies have
andreniformis stems from the fact that their classi-
appeared through the years but have not affected fication, is based on workers, which do not show
the taxonomy of this species. In the first multi- great morphological differentiation. Moreover, the
variate morphometric analysis of A. florea, descriptions and taxonomic keys of Maa (1953)
Ruttner (1988) had few samples from geograph- were based on limited numbers of specimens and
ically non-contiguous regions. Although the Maa’s purported differences between the two spe-
data were insufficient for a comprehensive anal- cies become blurred if all the workers of an entire
ysis, Ruttner (1988) demonstrated geographic colony are analyzed.
variability and obtained three morphoclusters The most reliable characters adequate for an
for A. florea. Recently Tahmasebi et al. (2002) indentification of A. florea and A. andreniformis are:
analyzed the A. florea of Iran and defined two the “thumb” of the bifurcated basitarsus of the
morphoclusters from a geographical contin- hindleg of drones of A. florea is much longer than
uum. Combining their data with that of Ruttner that of A. andreniformis (Ruttner, 1988); differences
in the structure of the endophallus (Lavrekhin, 1935;
(1988) and Mogga and Ruttner (1988), they also Wongsiri et al., 1990; Koeniger, 1991); in worker
reported three morphoclusters for all A. florea bees, the jugal-vannal ratio of the hindwing of A. flo-
but a lack of geographical contiguity applies to rea is greater (about 75) than that of A. andreniformis
this database as well. (about 65); and the cubital index of A. florea (about
New collections of A. florea from Myanmar, 3) is significantly less than in A. andreniformis
Nepal, Cambodia, Thailand, Vietnam, Iran, (about 6). Abdominal tergite 2 of A. andreniformis
Iraq, Afghanistan, Sri Lanka and Saudi Arabia is deeply punctate, that of A. florea not. The marginal
setae on the hind tibiae of A. florea are usually
have greatly augmented the database of A. flo- entirely white, those of A. andreniformis dark-brown
rea over a geographical continuum of about to blackish in sclerotized individuals. Permeating
7000 km. The additional, new samples fill gaps the older literature is the idea that abdominal tergites
to provide a population continuum over the full 1 and 2 of A. florea are reddish and other segments
range of the natural distribution of A. florea for at least partially reddish, while those of A. andreni-
the first time. Here we report the results of mul- formis are uniformly black. An inspection of several
tivariate morphometric analyses of A. florea hundred workers from each of several different col-
over its entire natural distribution and compare onies of each species quickly demonstrates the
these results with those obtained from the pre- extreme variation in pigmentation thus precluding
vious studies. Thus, the morphometric data- this as a useful distinguishing trait, a point recog-
nized rather long ago (Drory, 1888). Finally the
bases for A. florea from Iran, India, Thailand combs of the two species are very different (Rinderer
and Vietnam were analyzed separately and then et al., 1996). A full bibliography of the literature on
conjointly to assess the effects of interlocality A. florea is given in Hepburn and Hepburn (2005).
sampling distance on morphocluster forma-
tion, as was previously done for A. mellifera
(Radloff and Hepburn, 1998) and A. cerana 2.2. Geographical distribution
(Hepburn et al., 2001b). We also consider Because of long-standing confusion on whether
whether and how the morphometric data A. florea and A. andreniformis are distinct species
obtained might relate to past classification and because their distributions overlap widely in
schemes for A. florea (Maa, 1953; Ruttner, Southeast Asia (Otis, 1991), precise delineation of
Apis florea – classification, biogeography 361
the distributions of these two species based on all of Bandar Abbas, Iran from Tahmasebi et al. (2002)
the published literature (~ 792 publications on A. flo- against Obeursel; (3) data for North India from
rea and ~ 101 for A. andreniformis, Hepburn and Bhandari (1983) and Sharma (1983) against Pesha-
Hepburn, 2005) is somewhat difficult. The most war, Pakistan from Oberursel; and (4) data for
comprehensive and reliable distributional databases Chiang Mai, Thailand and Uminh, Vietnam from
for A. florea (as herein differentiated) are those of Oberursel was used to standardize the Grahamstown
Maa (1953), Ruttner (1988) and Otis (1997). database.
The criteria for regarding A. florea localities as
authentic are those of Otis (1997): (1) published 2.3.2. Measurements
locality data for A. florea for central India and points
west are unambiguous because of the absence of A. Twenty morphological characters were used in
andreniformis; (2) published locality data unambig- the analyses; 13 characters in the Ruttner/Oberursel
uously distinguishing A. florea from A. andreni- database, 20 characters in the Bhandari/Sharma
formis subsequent to the clear recognition of two (provided by Verma) and Grahamstown databases
biologically distinct species (e.g., Wu and Kuang, and 17 characters in the Chaiyawong database. The
1987); (3) data of Otis (1997); and (4) new distribu- original coded numbers assigned to these characters
tion records of the authors. Localities were obtained by Ruttner (1988) and Verma et al. (1989, 1994) are
with the appropriate geographical coordinates and given in rounded and square brackets, respectively,
plotted using GIS software (Fig. 1, Appendix). as follows: length of femur (5) [30]; length of tibia
The climatic data was derived from three princi- (6) [31]; metatarsus length (7) [32]; tergite 3, longi-
pal sources: a weatherbase website, http://www. tudinal (9) [42]; tergite 4, longitudinal (10) [45];
weatherbase.com, Müller (1982) and Troll and sternite 3, longitudinal (11) [49]; wax plate of ster-
Paffen (1980). Data on the seasonality of swarming/ nite 3, longitudinal (12) [48]; sternite 6, longitudinal
migration are from the following: China (Tan Ken, (15) [50]; forewing length (17) [5]; wing angle B4
pers. comm.); India (Aggarwal and Kapil, 1988; (22) [10]; wing angle D7 (23) [11]; wing angle G18
Deodikar et al., 1977; Millen, 1944; Mehta, 1948; (25) [13]; forewing-length of radial cell [1]; length
Ghatge, 1949; Soman and Chawda, 1996; Thakar of apical position of radial cell [4]; hind wing-length
and Tonapi, 1962; Muttoo, 1957; Sihag and Abrol, of basal portion of radial vein [20]; length of vannal
1986); Iran (Mossadegh, 1991; Tirgari, 1971); Oman lobe [29]; length of dark band of 4th tergite [44];
(Dutton and Free, 1979; Free, 1981); Thailand (antenna) length of antennal flagellum [54] and
(Akratanakul, 1977); Vietnam (Pham Hong Thai, total length of antenna [55]. The Iran database of
pers. comm.). Although used implicitly in past pub- Tahmasebi et al. (2002) had only 4 common charac-
lications, the terms macroscale, mesoscale and ters (tergites 3+4, longitudinal (9+10) [42+45];
microscale as used here equate to continental level, forewing length (17) [5]; LEG length (5+6+7) and
country/regional level and localized populations, wing angle G18 [13]) with the other four databases.
respectively. Cubital Index (CI) was common to the Oberursel,
Bhandari/Sharma and Tahmasebi databases but
absent from the Chaiyawong and Grahamstown
2.3. Morphometrics and statistics databases.
Figure 1. Distribution of Apis florea. Localities for which morphometric data are reported are indicated
by their country numbers shown in Table I. That the numbers for each country are not sequential derives
from the fact that these numbers correspond with the same locality numbers given in Appendix. All other
localities are represented by black circles. Not all localities could be shown because the scale used to
generate the map resulted in blurred areas because of high sample density. Full references available at
http://www.edpsciences.org/apido.
Apis florea – classification, biogeography 363
across mainland Asia along and below the Sharma and Sri Lanka from Oberursel (17 col-
southern flanks of the Himalayas, westwards to onies) using 10 common characters [(5), (6),
the Plateau of Iran and southerly into Oman (7), (9), (10), (17), CI, B4, D7 and G18] was
(Fig. 1). This constitutes some 70 degrees of performed. Three eigenvalues greater than one
longitude (40°–110° East) and nearly 30 degrees were isolated: PC 1, size related characters (5),
of latitude (6°–34° North). Variations in alti- (6), (7), (9), (10), (17) accounted for 57.1% of
tude range from sea level to about 2000 m. A. the variation; PC 2, angle of venation G18 (25)
florea has also been introduced in historical accounted for 15.8% of the variation; PC 3,
times in Saudi Arabia and Sudan, and occurred cubital index CI accounted for a further 12.2%
on Java, Indonesia, up until ~50 years ago. of the variation. The results of the PC plots
showed 2 distinct morphoclusters, a northern
3.2. Regional mesoscale analyses group of larger bees and a southern group of
smaller bees. A significant correlation between
altitude and the first principal component was
3.2.1. Thailand database found (r = 0.78, n = 16, P = 0.008).
A re-analysis of the raw data of Chaiyawong
(2001) for the A. florea of Thailand (localities 3.2.3. Iran database
8, 12, 14, 18, 20, 21, 23, 24, 27, 29–31, 34, 44–
46, 48, 54–57, 59–62 in Tab. I) was performed In this study combining the databases from
using 7 morphometric characters [(5), (6), (7), Tahmasebi et al. (2002) and Oberursel (58 col-
(9), (10), (17) and G18] common to the data- onies), the PC analysis using five common
bases from Oberursel, Chaiyawong and Gra- characters ((9+10), (17), CI, LEG and G18)
hamstown (62 colonies). Two principal com- revealed one morphocluster with two indistinct
ponents with eigenvalues greater than one were clusters of smaller eastern and larger western
isolated: PC 1, size-related characters (5), (6), bees. The two principal components with
(7), (9), (10) and (17) with component loadings eigenvalues greater than one accounted for
between 0.55 and 0.90 accounted for 57.7% of 72.5% of the variation: PC 1, size related char-
the variation; PC 2, angle of venation G18 (25) acters [(9+10), (17), LEG]; PC 2, angle of vena-
with component loading 0.82 accounted for tion [G18 (25)].
16.6% of the variation. The two principal com-
ponents accounted for a total of 74.4% of the 3.2.4. Iran, India and Sri Lanka
variation in the data. The principal components databases
results revealed one morphocluster with only 2
of the 10 colonies from Ko Samui and Ko In an analysis combining Bhandari/Sharma
Pha-ngan (3% of the total colonies) separated and Oberursel databases with that of Tahmasebi
from the principal morphocluster. Another et al. (2002) from Iran (61 colonies), the PC
principal components analysis using 17 char- results using 4 common characters [(9+10),
acters ((5), (6), (7), (9), (10), (11), (12), (15), (17), G18, LEG] showed 3 morphoclusters: a
(17), G18, [1], [4], [20], [29], [44], [54] and northwestern group of larger bees (Iran); a
[55]) common to Chaiyawong and Graham- northeastern group (eastern Iran and N. India)
stown (58 colonies) gave three principal com- and a southern group of smaller bees from S.
ponents with eigenvalues greater than one: PC India and Sri Lanka (Fig. 2). The northwestern
1, size related characters ((5), (6), (7), (9), (10), and southern groups are distinct. The first two
(11), (12), (15), (17), [20], [55]); PC 2, charac- principal components accounted for 94.2% of
ters [1], [4], [20], [29], [44], [54]; PC 3, angle the variation in the data: PC 1, size related char-
of venation G18 (25). The plots of PC 1, PC 2 acters [(9+10), (17), LEG; 70.5%]; PC 2, angle
and PC 3 scores again showed a single mor- of venation [G18 (25); 23.7%].
phocluster. The linear discriminant analysis results
classified 95.5% of colonies (n = 44) from Iran
3.2.2. India and Sri Lanka databases correctly into group 1 (larger bees) with a
posteriori probabilities P > 0.95 for 30 colonies,
A separate analysis of the combined data- 0.80 < P < 0.95 for 8 colonies, 0.75 < P < 0.80
bases for A. florea of India from Bhandari/ for 3 colonies, P = 0.56 for 1 colony, and
364 H.R. Hepburn et al.
INDIA
1. Jammu 32.45N 74.55E 327 1 B
3. Hamirpur 32.25N 75.20E 747 1 S
4. Nurpur 32.18N 75.53E 492 1 B
7. Gurdaspur 32.04N 75.28E 264 1 B
9. Hoshiarpu 31.30N 75.55E 316 1 S
10. Una 31.25N 76.15E 420 1 S
11. Karpurthala 224 1 B
21. Kalka 30.20N 76.45E 720 1 S
25. Sriganganagar 29.56N 73.53E 208 1 B
31. Hisar 29.07N 75.46E 212 1 B
111.Yarakapadi 12.18N 78.38E 1 O
IRAN
1. Ghasre-e-Shirin 34.30N 45.35E 343 1 T
2. Bishe-Moobed 33.18N 48.53E 1444 1 O
4. Mehran 33.07N 46.10E 136 1 T
5. Andimeshk 32.27N 48.21E 136 1 T
6. Dezfol 32.23N 48.28E 148 4 T
7. Lali 32.21N 49.06E 947 1 O
8. Deh Lowran 32.10N 48.46E 169 1 T
9. Shoshtar 32.03N 48.51E 67 1 O
10. Soush 32.00N 48.00E 90 1 T
11. Masjed Suleiman 31.59N 49.18E 337 1 O
12. Ghalieh-Khajeh 31.40N 49.41E 986 1 O
13. Ahwaz 31.17N 48.43E 33 3 O, T
14.Behbahan 30.34N 50.18E 317 3 O, T
16. Dogonbadan 30.21N 50.48E 724 1 T
17. Bidkhan 29.36N 56.30E 2726 1 T
18. Kazeroun 29.35N 51.40E 846 1 O
Apis florea – classification, biogeography 365
Table I. Continued.
MYANMAR
2. Mong La 22.07N 97.55E 811 7 G
3. Pyin-oo-lwin 22.05N 96.33E 1070 2 G
5. Mandalay 21.57N 96.04E 80 2 G
NEPAL
3. Tansen 27.52N 83.32E 1090 1 G
OMAN
8. Diqal 23.53N 56.54E 119 1 O
10. Qurm 23.36N 58.29E 14 1 O
11. Seeb 23.34N 58.15E 46 1 O
PAKISTAN
4. Peshawar 34.01N 71.40E 317 2 O
366 H.R. Hepburn et al.
Table I. Continued.
SAUDI ARABIA
3. Riyadh 24.39N 46.52E 6 1 O
SRI LANKA
7. Anuradhapura 8.18N 80.24E 8 5 O
16. Makandura 7.19N 79.58E 19 1 O
SUDAN
1. Al Khartum 15.35N 32.32E 377 2 O
THAILAND
2. Fang 20.05N 99.30E 471 1 O
8. Chiang Mai 18.48N 98.59E 310 4 O, G, C
12. Nong Khai 17.52N 102.44E 168 2 G, C
14. Uttaradit 17.37N 100.06E 246 1 C
16. Udon Thani 17.24N 102.47E 174 1 G
18. Sakhon Nahon 17.10N 104.08E 176 1 C
20. Tak 16.51N 99.08E 111 1 C
21. Phitsanulok 16.50N 100.15E 41 1 C
23. Khon Kaen 16.26N 102.49E 164 1 C
24. Roi Et 16.05N 103.38E 143 1 C
27. Ubon Ratchathani 15.13N 104.51E 12 1 C
29. Nakhon Ratchasima 15.00N 102.06E 177 2 C
30. Lopburi 14.49N 100.37E 6 7 G, C
31. Ang Thong 14.35N 100.25E 14 1 C
34. Suphan Buri 14.14N 100.07E 10 1 C
42. Bangkok 13.39N 100.31E 0 1 G
44. Samut Prakan 13.32N 100.35E 2 1 C
45. Ratchaburi 13.31N 99.47E 19 3 G, C
46. Samut Songkhram 13.25N 100.01E 5 3 G, C
47. Chon Buri 13.21N 100.58E 6 1 O
48. Phetburi 13.05N 99.58E 5 1 C
54. Chantaburi 12.36N 102.07E 6 2 O, C
55. Trat 12.16N 102.30E 12 1 C
56. Prachuap Khiri Khan 11.50N 100.01E 1 6 C
Apis florea – classification, biogeography 367
Table I. Continued.
VIETNAM
1. Sonla 21.19N 103.54E 662 4 G
3. Chieng Khua 20.51N 104.28E 1171 1 G
4. Moc Chau 20.15N 104.37E 1050 1 G
5. Kon Tum 14.22N 107.57E 513 1 G
6. Pleiku 14.07N 108.04E 792 1 G
11. Dalat 11.56N 108.25E 1475 1 G
18. Cho Gao 10.20N 106.28E 0 6 G
19. Pho Quoc Island 10.19N 104.00E 115 2 G
20. Can Tho 10.03N 105.46E 2 1 G
21. Uminh 9.20N 104.54E 4 O, G
* The numbering used in this table is based on the full list of all localities for which A. florea has been reported
in the literature and is available at http://www.edpsciences.org/apido.
Figure 2. Factor scores (PC) of colony samples of A. florea from 1 = Iran, 2 = N. India, 3 = S. India and
Sri Lanka.
368 H.R. Hepburn et al.
misclassified two colonies into cluster 2; Including the Iran data from Tahmasebi (139
90.0% of the colonies (n = 10) from N. India colonies) and using 4 common characters
into cluster 2 with a posteriori probabilities P [(9+10), (17), G18, LEG], the PC results
0.98 for 6 colonies, 0.84 < P < 0.98 for showed the same two clusters. Including
3 colonies and misclassified one colony into Oberursel’s Sri Lanka database (145 colonies)
cluster 1; 100% of the colonies (n = 7) from S. and using 4 common characters [(9+10), (17),
India and Sri Lanka into cluster 3 (smaller bees) G18, LEG], the PC results showed the same
with a posteriori probabilities P = 1.0 for two clusters with a slight isolation of smaller
5 colonies and 0.97 < P < 1.0 for 2 colonies. To bees from S. India and Sri Lanka along the
test the equality of the group means for the PC 1 axis.
characters used in the discriminant function,
Wilks’ lambda approximated by the F statistic 3.3. Multivariate analysis of total
was determined. A significant difference morphometric database
between the means of the three groups was
established (Λ = 0.155, F = 21.2, (8, 110) d.f., Principal components analyses were carried
P < 0.0001). out on the total morphometric databases of
Oberursel, Grahamstown, Bhandari/Sharma and
3.2.5. Vietnam database Tahmasebi (184 colonies). Using seven mor-
phometric characters of worker honeybees
In an analysis of the A. florea of Vietnam, shared in common among the databases [(5),
the databases of Vietnam from Grahamstown (6), (7), (9), (10), (17), G18] reduced the
and Oberursel were combined (22 colonies). number of colonies in the analysis to 130. Two
The PC analysis using 9 common characters principal components with eigenvalues greater
[(5), (6), (7), (9), (10), (17), B4, D7, G18] iso- than one were isolated: PC 1, size-related char-
lated two principal components with eigenval- acters (5), (6), (7), (9) and (10) with component
ues greater than one: PC 1, size related charac- loadings between 0.85 and 0.90 accounted for
ters (5), (6), (7), (9), (10), (17) accounted for 58.9% of the variation; PC 2, angle of venation
50.8% of the variation; PC 2, angles of venation (25) and size (17) with component loadings
D7 and G18 accounted for 20.7% of the varia- 0.87 and 0.57 respectively, accounted for
tion. The PC plot revealed a single morphoclus- 16.6% of the variation. The two principal com-
ter with two indistinct groups: a northern group ponents accounted for a total of 75.5% of the
of larger bees (latitude > 20°) and a southern variation in the data. The PC plot using the first
group of smaller bees (latitude < 10° from Pho and second PC scores revealed one mor-
Quoc Island and Cho Gao). phocluster with an isolation of larger bees from
Iran in the far right of the morphocluster along
the PC 1 axis and a group of smaller bees from
3.2.6. Iran, India, Thailand and Vietnam
S. India and Sri Lanka in the lower left quad-
databases
rant. The colonies from Cambodia, India,
Finally, an analysis was made of the samples Myanmar, Nepal, Thailand and Vietnam clus-
from Iran, India, Thailand and Vietnam. Com- tered together along the PC 1 axis. Colonies
bining the databases of these countries from from Mong La (N. Myanmar), Larkarna
Bhandari/Sharma, Oberursel and Graham- (Pakistan) and Seeb (Oman) were closer to the
stown (99 colonies), the PC analysis using 7 Iran cluster, whilst the colony from Qurm
common characters [(5), (6), (7), (9), (10), (17), (Oman) was isolated with the smaller bees from
G18] revealed two morphoclusters: a group of S. India and Sri Lanka.
larger bees from Iran and another group of bees Using these 7 characters in the analysis
from India, Thailand and Vietnam along the PC excluded the Iranian data from Tahmasebi et al.
1 axis and a slight clustering of the colonies (2002). The analysis was, therefore, repeated
from N. India along the PC 2 axis. The first two using 4 characters common to all databases
principal components accounted for 73.7% of [(9+10), (17), G18, LEG]. This increased the
the variation in the data: PC 1, size related char- number of colonies in the analysis to 170 (G18
acters [(5), (6), (7), (9), (10), (17); 56.2%]; values were missing in 14 samples) and gave
PC 2, angle of venation [G18 (25); 17.5%]. very similar results (Fig. 3). PC 1, size-related
Apis florea – classification, biogeography 369
Figure 3. Factor scores (PC) of colony samples of A. florea from 1 = Iran, 2 = Oman, 3 = Pakistan, 4 = N.
India, 5 = S. India and Sri Lanka, 6 = Nepal, 7 = Myanmar, 8 = Thailand, 9 = Cambodia, 10 = Vietnam.
characters [(9+10), (17) and LEG] with com- single linkage (nearest neighbour) procedure
ponent loadings between 0.88 and 0.92 was carried out on colony mean character val-
accounted for 61.4% of the variation; PC 2, ues [(5), (6), (7), (9), (10), (17), G18 (25)] com-
angle of venation G18 (25) with component bined for countries (Quinn and Keough, 2002).
loading 0.98 accounted for 26.4% of the vari- The results showed a dendrogram of three main
ation. The two principal components accounted clusters (Fig. 4). Phenetically, cluster 1 first
for a total of 87.8% of the variation in the data. linked colonies from Myanmar and Thailand,
The morphocluster of larger bees from Iran and then Cambodia and finally N. Vietnam; cluster
the morphocluster of smaller bees from S. India 2 first linked colonies from Oman, N. India and
and Sri Lanka are distinct. The discriminant Nepal followed by those from S. India; cluster
analysis results classified 97.9% of colonies 3 linked colonies from Iran and Pakistan; col-
(n = 47) from Iran correctly into group 1 (larger onies from S. Vietnam were linked to clusters
bees) and misclassified one colony into cluster 2 and 3.
2; 88.8% of the colonies (n = 116) from N.
India, Oman, Pakistan, Cambodia, Myanmar,
Thailand, Vietnam into cluster 2 and misclassified 4. DISCUSSION
five colonies into cluster 1 and eight colonies
into cluster 3; 100% of the colonies (n = 7) from
S. India and Sri Lanka into cluster 3 (smaller 4.1. Biogeography
bees). The climatic zones of A. florea change from
To test the equality of the group means for tropical rainforest in the east to savanna at a line
the characters used in the discriminant between Karachi, New Delhi and Simla in the
function, Wilks’ lambda approximated by the west. Further westwards, there is a transition
F statistic was determined. A significant from tropical to subtropical steppe and semi-
difference between the means of the three desert. There is a seasonal rainfall gradient
groups was established (Λ = 0.201, F = 50.5, across the range of A. florea from the eastern
(8, 328) d.f., P < 0.0001).The colony means tropical to the western subtropical and semi-
and standard deviations of nine morphometric desert climates of the west (Tab. III). There is
characters [(5), (6), (7), (9), (10), (17), G18 also a gradient of mean daily temperature
(25), (9+10), LEG] averaged for countries are extremes that increases from the eastern tropi-
shown in Table II. A cluster analysis using the cal zone to the western subtropical zones. In
370
Table II. Means (m) and standard deviations (sd) of nine morphometric characters (measurements in mm, angles in degrees) of A. florea and n = number
of colonies.
Cambodia N. India S. India / Iran Myanmar Nepal Oman Pakistan Thailand Vietnam
Character n=6 n=10 Sri Lanka n=7 n=18 n=11 n=1 n=3 n=3 n=62 n=22
m±sd m±sd m±sd m±sd m±sd m±sd m±sd m±sd m±sd m±sd
(5) 1.72±0.02 1.74±0.04 1.67±0.04 1.83±0.03 1.76±0.04 1.74±0.00 1.74±0.06 1.75±0.05 1.74±0.03 1.78±0.02
(6) 2.24±0.03 2.19±0.06 2.09±0.06 2.30±0.03 2.27±0.03 2.29±0.00 2.17±0.08 2.18±0.07 2.22±0.04 2.29±0.03
(7) 1.38±0.02 1.35±0.01 1.29±0.02 1.41±0.03 1.39±0.03 1.39±0.00 1.35±0.04 1.35±0.02 1.35±0.03 1.37±0.01
(9) 1.45±0.03 1.40±0.07 1.32±0.04 1.51±0.04 1.44±0.03 1.47±0.00 1.39±0.05 1.40±0.04 1.41±0.04 1.43±0.02
(10) 1.40±0.02 1.37±0.07 1.27±0.05 1.47±0.04 1.38±0.03 1.40±0.00 1.34±0.04 1.37±0.03 1.36±0.03 1.37±0.02
H.R. Hepburn et al.
(17) 6.13±0.05 6.58±0.08 6.14±0.09 6.85±0.13 6.44±0.24 6.33±0.00 6.52±0.18 6.61±0.03 6.17±0.11 6.23±0.06
G18 102.13±1.10 106.20±1.99 106.14±2.89 104.66±1.59 102.71±1.53 105.59±0.00 105.85±0.68 105.10±1.85 102.81±2.16 103.96±1.85
(9+10) 2.85±0.04 2.78±0.12 2.59±0.09 2.96±0.10 2.82±0.06 2.87±0.00 2.73±0.09 2.78±0.07 2.77±0.07 2.80±0.04
LEG 5.34±0.06 5.26±0.11 5.05±0.10 5.54±0.09 5.42±0.11 5.42±0.00 5.26±0.18 5.28±0.14 5.32±0.09 5.44±0.06
Apis florea – classification, biogeography 371
Table III. Selected climatic data representative of the different regions in which A. florea naturally occurs.
Rainy months are defined as those in excess of 100 mm/month. Mean daily monthly temperatures suitable
for flight are taken at 15 °C. Periods of reproductive swarming and migration are included*.
LOCALITY RAINS DRY TEMP SWARM MIGRATE
MTHS AMT MTHS AMT MTHS MTHS MTHS
China
Kunming 5–10 980 11–4 115 4–10 4–5, 9–10 3, 8
Guiyang 5–10 960 11–4 250 4–10 4–5, 9–10 3, 8
Nanning 5–10 1040 11–4 280 3–12 4–5, 9–10 3, 8
Vietnam
Buon Me Thout 5–10 1560 11–4 230 1–12 7–8
Hai Phong 5–10 1470 11–4 250 1–12 3–4
Thailand
Chiang Mai 5–10 1100 11–4 120 1–12 1–3, 8–10
Bangkok 5–10 1220 11–4 220 1–12 2–4, 8–10
Surat Thani 4–12 1700 1–3 110 1–12 4–6, 8–10
India
South: Bangalore 5–10 730 11–4 140 1–12 3–4, 10–12
Central: Nagpur 6–9 1090 10–5 170 1–12
Northeast: Calcutta 5–10 1455 11–4 145 1–12
Northwest: New Delhi 7–9 470 10–6 170 2–11
Northnorth: Simla 6–9 1190 10–5 380 5–9 3–4, 9–10
Iran
Northeast: Qandahar 12–3 140 4–11 25 4–10
Southeast: Chah Bahar 12–2 90 3–11 15 1–12
Northwest: Esfahan 10–3 70 4–9 10 3–10
Southwest: Bandar 12–2 130 3–11 20 1–12 4–5, 7
Abbas
Oman
Ash-Shariqah 12–3 75 4–10 25 1–12 2–4, 9–10
* Parts of Iran and Oman appear anomalous; however, rainfall never exceeds 100 mm per month in some areas.
views on this point (Sharma, 1983). We Tahmasebi et al. (2002) reported an analysis
obtained a strong significant positive correla- of A. florea from 26 localities in southern Iran
tion between altitude and the principal compo- extending some 2000 km along an east/west
nents variables reflecting size within the sam- transect between 25° to 35° N latitude (locali-
ple from India. This pattern might benefit from ties 1, 4–6, 8, 10, 13, 14, 16–17, 20–21, 24–25,
additional attention. 27–34, 36–37, and 40–41 in Tab. I). In a
Apis florea – classification, biogeography 373
principal components analysis of 12 morpho- lack of infraspecific taxa in the two dwarf hon-
metric characters they obtained two mor- eybee (Micrapis) species may reflect a limited
phoclusters in Iran, a western group of larger dispersal ability, as evidenced by their absence
bees at higher latitudes (29°–34°) and a lower on most offshore island groups (Otis, 1997).
latitude group of smaller bees to the east (< 29° This apparent inability of A. florea to disperse
latitude). In our study the PC analysis revealed from peripheral populations, coupled with syn-
one morphocluster with two indistinct clusters chronous reproductive seasons across its distri-
of smaller eastern and larger western bees. bution, have apparently limited regional differ-
In studies of variation in mitochondrial entiation of these species into recognizable
DNA, Smith (1991) established that A. florea subspecies/races.
were homogeneous in Thailand and also in The comparisons of A. florea from India/Sri
southern India but had diverged between the Lanka (3.2.2 above) or Iran, India, Thailand
two countries. The homogeneity of mtDNA in and Vietnam (3.2.6 above) both yielded two
A. florea from Thailand was subsequently con- morphoclusters. Similarly, the analyses of
firmed (Nanork et al., 2001). Smith also Ruttner (1988) and Tahmasebi et al. (2002)
observed that different mtDNA clusters occur yielded three morphoclusters and precisely the
in A. cerana from N. and S. India, paralleling same result is shown in Figures 2 and 3. As pre-
the differences observed in A. florea. More viously noted, the effects of sample size and
recently, Takahashi et al. (unpublished data) interlocality distance have major implications
proposed three distinct mtDNA lineages for A. for morphocluster group formation (Radloff
florea from eastern Asia: (1) China/Myanmar; and Hepburn, 1998). Here, the distributional
(2) Southeast Asia: Thailand, Vietnam, Cam- variation in morphometric characters is clinal:
bodia, and part of China; (3) India. While there northwestern bees are larger than southeastern
are no inconsistencies among these three stud- ones. In the final analysis, A. florea is a single
ies, available information is insufficient to species comprised of three discernible morpho-
apply to the whole area of A. florea distribution. clusters. The northwestern-most bees comprise
Similarly, available data on enzyme polymor- a morphocluster (1) that is statistically quite
phism in A. florea (Li et al., 1986; Sheppard and distinct from that to the southeast (3); but, they
Berlocher, 1989; Gan et al., 1991) are likewise are not isolated, they are joined by large areas
geographically limited precluding extrapola- of intermediate forms (2) resulting in a contin-
tion to the whole A. florea population. The uous cline in morphometric traits within this
available genetic data are too regional in nature panmictic species.
to be informative for the species as a whole.
portant sur 2923 ouvrières prélevées dans 184 colo- nachbarten Gruppierungen auf. Im Resultat ergibt
nies réparties dans 103 lieux dispersés dans toute la sich aus der Analyse, dass A. florea einen einzigen
zone de répartition d’A. florea (Fig. 1). Morphokluster ohne deutliche Untergruppierungen
Il ressort en premier lieu qu’A. florea se différencie aufweist, dieser ist allerdings klinal entlang der
sans équivoque d’A. andreniformis par la morpho- geographischen Länge und Meereshöhe struktu-
logie. La comparaison des populations séparées riert. Innerhalb der Einschränkungen des Datenma-
géographiquement fournit tout d’abord des groupes terials und der Analyse reicht die gegebene Varia-
morphologiques (morphoclusters) (Fig. 2). Mais tionsbreite nicht aus, um infraspezifische Taxa zu
ceux-ci reflètent des artéfacts liés à l’échantillon- identifizieren. Die Spezies hat ein sehr ausgedehn-
nage et disparaissent dès que l’ensemble des don- tes Verbreitungsgebiet, geographisch umfasst die-
nées est inclus dans une même analyse en compo- ses Gebiete mit tropischen Regenfällen über Savan-
santes principales. Malgré cela une analyse de nengebiete bis zur subtropischen Steppe. Allerdings
groupement (cluster analysis) sur la base des distan- ist die Saisonalität des reproduktiven Schwärmens
ces euclidiennes montre des affinités entre groupe- derart, dass sich über die gesamte Population ein
ments géographiquement voisins. Il en résulte que zeitlicher Zusammenhang ergibt (Tab. III).
l’A. florea présente un seul groupe morphologique
sans sous-regroupements nets. Les caractères mor- Apis florea / Morphometrie / Verbreitung /
phométriques varient selon un gradient géographi- Biogeographie / Schwarm / Wanderung
que, ou cline, en fonction de la latitude et l’altitude.
La variation n’est pas suffisante au sein des données
et de l’analyse pour identifier des taxons infraspéci-
fiques. L’espèce a une aire de répartition très éten- REFERENCES
due, depuis les forêts pluviales jusqu’aux steppes
subtropicales en passant par les zones de savanes. Aggarwal K., Kapil R.P. (1988) Seasonal population
L’essaimage reproductif a lieu de façon continue dynamics of Tropilaelaps clareae (Acari:
dans le temps permettant un flux de gènes au sein de Laelapidae) in Apis dorsata colonies, in:
cette espèce panmictique. Channabasavanna G.P., Viraktamath C.A. (Eds.),
Progress in Acarology, Oxford and IBH
Publishing Company, New Delhi, India, pp. 283–
Apis florea / morphométrie / répartition 286.
géographique / biogéographie / essaimage /
migration Akratanakul P. (1977) The natural history of the
dwarf honey bee, Apis florea F. in Thailand,
Thesis, Cornell University, Ithaca, New York,
pp. 1–91.
Zusammenfassung – Multivariate morphome- Bhandari V.C. (1983) Biometrical studies on Apis
trische Analyse von Apis florea. In den letzten 2 florea F. and Apis dorsata F. of north-western
Jahrhunderten wurden verschiedene Unterarten und India, Thesis, Himachal Pradesh University,
Varietäten von Apis florea Fabricius 1787 beschrie- Simla, India, pp. 1–92.
ben, diese wurden später von Maa (1953) wieder
zusammengefasst. Seither wurde einige Untersu- Chaiyawong T. (2001) Morphometric study of Apis
florea in Thailand, MSc. Thesis, Chulalongkorn
chungen über mittlelgrosse Areale durchgeführt, University, Bangkok, Thailand, 108 p.
die die Klassifikation allerdings nicht beeinflussten.
In der vorliegenden Untersuchung wurden die Chen Y. (1993) Apiculture in China, Agricultural
Daten aus mehreren Datenbanken (Oberursel, Gra- Scitech Publishing House of China, Beijing,
hamstown) und Untersuchungen Bhandari (1983), pp. 1–178.
Sharma (1983), Tahmasebi et al. (2002) und Cockerell T.D.A. (1911) Descriptions and records of
Chaiyawong (2001) zusammengeführt und durch bees XXXV, Ann. Mag. Nat. Hist. Series London
neue Daten ergänzt. Hierdurch konnte eine multiva- 8, 310–319.
riate Analyse über 2923 Arbeiterinnen aus 184 Völ- Deodikar G.B., Ghatge A.L., Phadke R.P., Mahindre
kern von 103 über das gesamte Verbreitungsgebiet D.B., Kshirsagar K.K., Muvel K.S., Thakar C.V.
von A. florea verteilten Fundorten durchgeführt (1977) Nesting behaviour of Indian honeybees.
werden (Abb. 1). III. Nesting behaviour of Apis dorsata Fab.,
Zunächst zeigte sich, dass A. florea morphologisch Indian Bee J. 39, 1–12.
eindeutig von A. andreniformis abgegrenzt werden Dover C. (1929) Wasps and bees in the Raffles
kann. Der Vergleich von durch größere geographi- Museum, Singapore, Bull. Raffles’ Museum
sche Distanzen getrennten Datensätzen ergaben Singapore 2, 43–70.
zunächst Morphokluster (Abb. 2). Diese sind Drory E. (1888) From my notebook: notes on bees
allerdings auf die Begrenztheit der Sammlung from a trip around the world, Bienenvater 20, 20–
zurückzuführen und verschwinden, sobald die 30 (in German).
gesamte Datenmenge in die Hauptkomponentena- Dung P.X., Thai P.H., Trung L.Q. (1996) Some
nalyse eingeschlossen wird. Dessen ungeachtet comparative characteristics between Apis florea
zeigt eine Klusteranalyse auf Basis der euklidischen and Apis andreniformis in Minh Hai Province,
Distanzen Affinitäten zwischen geographisch be- Proc. 3rd Asian Apic. Assoc. Hanoi, p. 62.
Apis florea – classification, biogeography 375
Dutton R.W., Free J.B. (1979) The present status of Li S., Meng Y.P., Chang J.T., Li J.H., He S.Y., Kuang
beekeeping in Oman, Bee World 60, 176–185. B.Y. (1986) A comparative study of esterase
Enderlein G. (1906) New honeybees and contribution isozymes in 6 species of Apis and 9 genera of
to the distribution of the genus Apis, Stett. Apoidea, J. Apic. Res. 25, 129–133.
Entomol. Ztg. 67, 331–334 (in German). Maa T. (1953) An enquiry into the systematics of the
Engel M.S. (1999) The taxonomy of recent and fossil tribus Apidini or honey bees (Hymenoptera),
honey bees (Hymenoptera: Apidae; Apis), J. Treubia 21, 525–640.
Hymenoptera Res. 8, 165–196. Mehta V.K. (1948) Apis florea, Indian Bee J. 10, 79–81.
Fabricius J.C. (1787) Mantissa Insectorum, Hafniae, Millen T.W. (1944) Apis florea, Indian Bee J. 6, 106–
Proft. Vol. 1, p. 348 (cited from Maa, 1953). 108.
Free J.B. (1981) Biology and behaviour of the Mogga J., Ruttner F. (1988) Apis florea in Africa:
honeybee, Apis florea, and possibilities for source of the founder population, Bee World 69,
beekeeping, Bee World 62, 46–59. 100–103.
Gan Y.Y., Otis G.W., Mardan M.B., Tan S.G. (1991) Mossadegh M.S. (1991) Geographical distribution,
Allozyme diversity in Asian Apis, in: Smith D.R. levels of infestation and population density of the
(Ed.), Diversity in the Genus Apis, Westview mite Euvarroa sinhai Delfinado and Baker
Press, Boulder, Co., pp. 117–130. (Acarina: Mesostigmata) in Apis florea F.
Gerstäcker C.E.A. (1863) On the geographical colonies in Iran, Apidologie 22, 127–134.
distribution of honeybees, Ann. Mag. Nat. Hist. Müller M.J. (1982) Selected Climatic Data for a
London 11, 270–283; 333–347. Global Set of Standard Stations for Vegetation
Ghatge A. (1949) Some research work on Apis florea, Sciences, Junk, The Hague.
Indian Bee J. 11, 5–6; 9. Muttoo R.N. (1957) Some so called “peculiarities”
Hepburn H.R. (2004) Absconding, migration and of behaviour of Indian honeybees as compared
swarming in honeybees: an ecological and evolu- to the European bees, Indian Bee J. 19, 62–64.
tionary perspective, Proc. IUSSI Conference on Nanork P., Deowanish S., Wongsiri S. (2001)
Social Insects, St. Petersburg (in press). Mitochondrial DNA variability of dwarf honey
Hepburn H.R., Hepburn C. (2005) Bibliography of bee [Apis florea Fabricius (1787)] in Thailand by
Apis florea, Apidologie, 36, 377–378 (available using PCR-RFLP technique, Proc. 7th Int. Conf.
at http://www.edpsciences.org/apido). Apic. Trop. Climates, Chiang Mai, pp. 341–345.
Hepburn H.R., Smith D.R., Radloff S.E., Otis G.W. Narayanan E.S., Sharma P.L., Phadke K.G. (1960)
(2001a) Infraspecific categories of Apis cerana: Studies on biometry of the Indian bees II. Tongue
morphometric, allozymal and mtDNA diversity, length, wing hooks, worker-brood-cell size and
Apidologie 32, 3–23. thickness of comb of Apis florea F. at Pusa
Hepburn H.R., Radloff S.E., Verma S., Verma L.R. (Bihar), Indian Bee J. 22, 81–88.
(2001b) Morphometric analysis of Apis cerana Nunamaker R.A., Wilson W.T., Ahmad R. (1984)
populations in the southern Himalayan region, Malate dehydrogenase and non-specific esterase
Apidologie 32, 435–447. isoenzymes of Apis florea, A. dorsata, and A.
Johnson R.A., Wichern D.W. (1998) Applied cerana as detected by isoelectric focusing, J.
Multivariate Statistical Analysis, 4th ed., Prentice Kansas Entomol. Soc. 57, 591–595.
Hall, Upper Saddle River, New Jersey. Otis G.W. (1991) A review of the diversity of species
Koeniger G. (1991) Diversity in Apis mating systems, within Apis, in: Smith D.R. (Ed.), Diversity in the
in: Smith D.R. (Ed.), Diversity in the Genus Apis, Genus Apis, Westview Press, Boulder, Colorado,
Westview Press, Boulder, Co., pp. 199–212. pp. 29–49.
Koeniger N., Koeniger G. (1991) An evolutionary Otis G.W. (1997) Distributions of recently recognized
approach to mating behaviour and drone copula- species of honey bees (Hymenoptera: Apidae;
tory organs in Apis, Apidologie 22, 581–590. Apis) in Asia, J. Kansas Entomol. Soc. 69
Koeniger N., Koeniger G. (2000) Reproductive (Suppl.), 311–333.
isolation among species of the genus Apis, Quinn G.P., Keough M.J. (2002) Experimental
Apidologie 31, 313–339. Design and Data Analysis for Biologists,
Koeniger N., Koeniger G. (2001) Behavioural mating Cambridge University Press, Cambridge.
barriers among sympatric species of the genus, Radloff S.E., Hepburn H.R. (1998) The matter of
Apis, Proc. 7th Int. Conf. Apic. Trop. Climates, sampling distance and confidence levels in the
Chiang Mai, pp. 80–85. subspecific classification of honeybees, Apis
Kuang B.Y., Li Y.C. (1985) The genus Apis in China, mellifera L., Apidologie 29, 491–501.
Chinese Beekeeping 76, 7–9 (in Chinese). Radloff S.E., Hepburn H.R. (2000) Population
Lavrekhin F.A. (1935) Contribution to the study of structure and morphometric variance in the Apis
variation of the honey bee. 2. A comparative mellifera scutellata group of honeybees in Africa,
biometric characteristic of the sexual appendages Genet. Mol. Biol. 23, 305–316.
of the drones belonging to different forms Rao P.V. (1998) Statistical Research Methods in Life
of the genus Apis, Zool. Zh. 14, 655–663 Sciences, Brooks/Cole Publishing Company,
(in Russian). Pacific Grove, CA.
376 H.R. Hepburn et al.
Rinderer T.E., Oldroyd B.P., Wongsiri S., Sylvester Tahmasebi G., Ebadi R., Tajabadi N., Akhoundi M.,
H.A., De Guzman L.I., Potichot S., Sheppard Faraji S. (2002) The effects of geographical and
W.S., Buchmann S.L. (1993) Time of drone flight climatic conditions on the morphological
in four honey bee species in south-eastern variation and seperation of Iranian small
Thailand, J. Apic. Res. 32, 27–33. honeybee (Apis florea F.) populations, J. Sci.
Rinderer T.E., Oldroyd B.P., Wongsiri S., Sylvester Technol. Agric. Nat. Res., Iran 6, 169–176.
H.A., De Guzman L.I., Stelzer J.A., Riggio R.M. Thakar C.V., Tonapi K.V. (1962) Nesting behaviour
(1995) A morphological comparison of the dwarf of Indian honeybees. II. Nesting habits and comb
honey bees of south-eastern Thailand and cell differentiation in Apis florea Fab., Indian Bee
Palawan, Philippines, Apidologie 26, 387–394. J. 24, 27–31.
Rinderer T.E., Wongsiri S., Kuang B.Y., Liu J.S., Tirgari S. (1971) On the biology and manipulation of
Oldroyd B.P., Sylvester H.A., De Guzman L.I. Apis (Micrapis) florea F. in Iran, Proc. 23rd Int.
(1996) Comparative nest architecture of the dwarf Beek. Congr., pp. 330–332.
honey bees, J. Apic. Res. 35, 19–26.
Ruttner F. (1975) A metatarsal clasping structure in Troll C., Paffen K.H. (1980) Jahreszeitenclimate der
the Apis drone, Entomol. Ger. 2, 22–29. Erde, Berlin.
Ruttner F. (1988) Biogeography and Taxonomy of Verma L.R., Kafle G.P., Sharma A., Mattu V.K.
Honeybees, Springer-Verlag, Berlin, Germany, (1989) Biometry of Apis cerana of Nepal
pp. 1–284. Himalayas, in: Proc. 4th Int. Conf. Apic. Trop.
Climates, pp. 458–465.
Ruttner F. (1992) Naturgeschichte der Honigbienen,
Ehrenwirth, Munchen, Germany. Verma L.R., Mattu V.K., Daly H.V. (1994)
Multivariate morphometrics of the Indian
Sharma P.C. (1983) Morphometric studies on Apis
florea F. and Apis dorsata F. of Himachal Pradesh honeybee in the northwest Himalayan region,
and Punjab, Thesis, Himachal Pradesh Apidologie 25, 203–223.
University, India, pp. 1–83. von Buttel-Reepen H. (1906) Contributions to the
Sheppard W.S., Berlocher S.H. (1989) Allozyme systematics, biology as well as the historical and
variation and differentiation among four Apis geographical distribution of honeybees (Apis
species, Apidologie 20, 419–431. mellifica L.) their variability and other Apis
species, Mitt. Zool. Museum Berlin 3, 117–201
Sihag R.C., Abrol D.P. (1986) Correlation and path- (in German).
coefficient analysis of environmental factors
influencing flight activity of Apis florea F., J. Wongsiri S., Limbipichai K., Tangkanasing P.,
Apic. Res. 25, 202–208. Mardan M., Rinderer T., Sylvester H.A.,
Smith D.R. (1991) Mitochondrial DNA and Honey Koeniger G., Otis G.W. (1990) Evidence of
Bee Biogeography, in: Smith D.R. (Ed.), reproductive isolation confirms that Apis
Divserity in the Genus Apis, Westview Press, andreniformis (Smith, 1858) is a separate species
Boulder, Co., pp. 131–176. from sympatric Apis florea (Fabricius, 1787),
Apidologie 21, 47–52.
Smith F. (1858) Catalogue of the hymenopterous
insects collected at Sarawak, Borneo, Proc. Linn. Wu Y.R., Kuang B. (1986) A study of the genus
Soc. London 2, 42–130. Micrapis (Apidae), Zool. Res. 7, 99–102 (in
Soman A.G., Chawda S.S. (1996) A contribution to Chinese).
the biology and behaviour of the dwarf bee, Apis Wu Y.R., Kuang B. (1987) Two species of small
florea F. and its economic importance in Kutch, honeybee – a study of the genus Micrapis, Bee
Gujarat, India, Indian Bee J. 58, 81–88. World 68, 153–155.