Geographical races of Apis cerana Fabricius in and their distribution. Review of recent Chinese publications and a preliminary statistical analysis Y.S. Peng, M.E. Nasr, S.J. Locke

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Y.S. Peng, M.E. Nasr, S.J. Locke. Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publications and a preliminary statistical analysis. Apidologie, Springer Verlag, 1989, 20 (1), pp.9-20. ￿hal-00890759￿

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Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publica- tions and a preliminary statistical analysis

Y.S. Peng, M.E. Nasr S.J. Locke

Department of Entomology, University of California, Davis, CA 95616, USA (received 1-11-1987, accepted 23-5-1988)

Summary — The authors have searched the Chinese literature for information on the geographical races of Apis cerana Fabricius and their distribution in China, compiled published data and subjec- ted a portion of the data to statistical analyses. Apis cerana in China can probably be grouped into 5 geographical races, including the , Eastern, Southern , Aba and Xizang () races; and possibly further into 7 biotypes, including the Palm Forest, and Mountain of Hainan, Guang- dong-, Hunnan, Yunnan plateau, Northern and Changbei Shan biotypes. The geographical distribution limit, and the discrepancy between the grouping of races and biotypes as well as the present results of stepwise discriminant analyses have been discussed.

Apis cerana Fabricius - geographical races - distribution

Résumé — Races géographiques d’Apis cerana Fabricius en Chine et leur répartition. Revue des publications chinoises récentes et analyse statistique préliminaire. Les auteurs ont traduit la littérature chinoise récente concernant les races géographiques d’Apis cerana Fabricius et leur répartition en Chine et soumis une partie de ces données à l’analyse statistique. Apis cerana peut être vraisemblablement divisée en 5 races géographiques : Hainan, Yunnan oriental et Yunnan du Sud, Aba et Xizang (Tibet) et 7 écotypes : forêt de palmes et montagne de Hainan, -Guangxi, Hunnan, plateau du Yunnan, nord et Changbei Shan. Néanmoins notre analyse discriminante par étapes portant sur la longueur du proboscis, la longueur de l’aile antérieure et l’index cubital des données compilées montre que seules les races du Yunnan oriental et dAba peuvent être différenciées avec un classement correct de 74,1 et 81,3% des échantillons. L’analyse statistique des mêmes caractères morphologiques n’a pas réussi à séparer les autres races géographiques. Les 5 écotypes du continent (c’est-à-dire tous les écotypes excepté les deux de l’île d’Hainan, dont l’échantillonnage était trop réduit) ont été classés correctement à 60,0, 37,1, 60,0, 50,0 et 50,0% respectivement à P = 0,05. Cet écart est dû au fait que seule une petite partie des données d’origine était disponible et a pu être utilisée pour l’analyse statistique. On discute la répartition géographique d’Apis cerana et ses relations avec la végétation et le climat des régions de Chine.

Apis cerana Fabricius - races géographiques — répartition

Zusammenfassung — Geographische Rassen von Apis cerena Fabricius in China und ihre Verbreitung. Die Autoren übersetzten die aktuelle chinesische Literatur über die geographischen Rassen von Apis cerana Fabricius und ihre Verbreitung in China und unterzogen einen Teil der Daten der statistischen Analyse. Apis cerana kann in China wahrscheinlich in 5 geographische Rassen (Hainan, Ost-Yunnan, Süd-Yunnan, Aba and Xizang (Tibet]) und 7 Biotypen (Palmwald und Bergland von Hainan, Guang- dong-Guangxi, Hunna, Yunnan-Plateau, Nördlicher und Changbei Shan Biotyp) eingeteilt werden. Jedoch erbrachte die schrittweise Diskriminanzanalyse von Rüssellänge, Länge des Vorderflügels und Cubital Index nur für die beiden Rassen Ost-Yunnan und Aba eine klare Trennung (mit 74.11 und 81.3°l korrekt klassifizierten Proben). Die statistischen Analysen der anderen Rassen ergaben bei Verwendung der gleichen morphologischen Merkmale keine Trennung. Die 5 Biotypen des Fest- landes (also alle außer den beiden Biotypen der Insel Hainan) wurden zu 60.0, 37.1, 60.0, 50.0 und 50.0% (bei P = 0.05) korrekt klassifiziert. Diese Diskrepanz beruht darauf, daß nur ein kleiner Teil der Originaldaten veröffentlicht wurde und zur statistischen Analyse verwendet werden konnte. Die Grenzen der geographischen Verbreitung von Apis cerana und ihre Beziehung zu Vegetation und Klima der Regionen Chinas wurden diskutiert.

Apis cerana Fabricius - geographische Rassenverbreitung

Introduction nesia) (Ruttner, 1975). In China, the mor- phological and behavioral variations of cerana have been the of The Oriental bee, Apis cerana Apis subject Fabricius 1793 is found in southern and many systematic studies (Kellogg, 1930, eastern Asia, from and to 1936, 1938, 1968; Wang, 1937; Xie, 1944; et China and and southeast to the Maa, 1953; Zhang, 1958; Huang al., Moluccas (Ruttner, 1971, 1985; Michener, 1963; Yang, 1964; Liu, 1965; Zhang, 1974). Its southern form is often called 1966; as cited in Yang, 1982a). Beginning Apis indica (Michener, 1974; Ruttner, in 1975, China launched a national survey of the races of cerana and their dis- 1975). Apis cerana is a close relative of Apis tribution the and the common or European , throughout country (Yang Xu, All the results of this survey Apis mellifera. They were originally allo- 1982). have been in the Chinese patric species, but man has been respon- published api- cultural literature. as the result sible for bringing these 2 species together However, throughout Asia. of the language barrier, this invaluable information is unfortunately largely un- The of cerana that is subspecies Apis known outside of China. Therefore, for the distributed widely in various geographic purpose of bridging this information gap, regions and climatic zones in China is we have searched the literature, compiled often referred to in the Chinese literature known published data concerning Apis as Apis cerana cerana. It is this typical cerana, and presented this information of bee that was subspecies honey here as a series of review articles on the domesticated the Chinese 3,000 by years and distribution of races of before the introduction of the biology Apis European cerana in China. honey bee at the turn of the twentieth century (see reviews by Chou, 1980; Kong, 1982). As in the European honey bee, Apis Materials and Methods cerana has evolved into several distinct races. the races from the north Generally, Beginning in 1975, more than one thousand (, Himalaya, China) are larger locations throughout China were surveyed for than those from the south (Ceylon, Indo- races of Apis cerana. Samples collected from 222 locations were used in the survey analysis Results by Yang (1984a, b; see also Fig. 2). Three to 20 morphological and behavioral characteristics of worker bees, as well as economic charact- The distribution limit of Apis cerana eristics of colonies were assessed in these cerana covers a wide of studies. The characteristics used in the Chine- Apis range geo- and climatic in China. As se studies are listed in Table I. A list of pub- graphical ranges lished references including sampling locations, shown in the distribution maps (Fig. 1), sample sizes, and morphometric and other besides the desert Xinjiang and the Nei- parameters used in these studies are also sum- mengu marized in Table II. (Inner Mongolia) prairie, Apis cerana is found throughout Hainan Island Unfortunately, most of these publications did and the mainland, from the coastal plains not the set of data, nor did provide complete to the at over they describe the statistical methods used for Qingzhan Gaoyuan plateau analysis. Since proboscis length, fore-wing 4 000 m in altitude. The distribution limit length, and cubital index are the 3 most com- (Yang, 1984a) begins from the southern monly used morphological characteristics in Xiaosinganling Shanmo mountain range these publications, we compiled the data of in the northeast, and goes down along the these 3 characteristics from the original publi- Yenshan Shanmo and the Great Wall to cations and subjected them to statistical anal- of and Wuchu A discriminant Yenchi, Haiyuan Ningxia, ysis. stepwise analysis (Hand, Shan mountain in It then 1981; Dixon, 1985) was then performed to province. stretches further west to cover the assess the prediction of membership in the tes- ted groups of Apis cerana. Wushao Ling mountain range, over the Chiliang Shan to Xining, turning south to high meadow and regions accord- the northern ranges of the A’nyemaqen ing to Yang’s data (1984a). We also not- Shan, and the upper river valleys of Dadu iced that the 380 mm annual precipitation Hei river in . The distribution limit line, or the western limit of nonoasis agri- continues southwest, passing the Yalong culture line, closely approximates the dis- Jiang river, the Jingsha Jiang, the Nu tributional limits of Apis cerana as well as Jiang (Salween river), and to the middle the climatic regions of China (Hou, 1983). of the Yarlung Zangbo Jiang (the upper The population density of Apis cerana cerana is also Brahmaputra river). Apis in China varies from region to region. It is distributed the eastern coastal throughout estimated that approximately 70% of col- the island of , the regions including onies are found in the provinces south of southwestern part of Xishuangbanna the Chang Jiang (Yangtze river). In the Daizu Zizizhou, and further south to Hai- northern regions, it mainly occurs along nan Island (Yang, 1984a). the Huang He (Yellow river), Glin Ling, When the distribution limit of Apis Dayi Shanmo, Taihang Shanmo, Dabie cerana drawn by Yang (1984a) is com- Shan and Changbai Shan. pared to the maps of the vegetational There are 2,000,000 regions of China (Hou, 1983), it appears approximately colonies of Apis cerana in that the distribution of Apis cerana parall- managed China. of them are in els with certain vegetational regions Sixty percent kept traditional , and the rest are man- (Fig. 1 ). Apis cerana is found primarily in in standard, movable frame hives. the temperate broad-leaved aged The average honey ranges between forests, the subtropical evergreen broad- yield 15—20 leaved forests, the tropical seasonal rain kg annually (Yang, 1984b). forests and the southern portion of the The distribution and population density temperate steppe regions. It is not found of Apis cerana in China have been signifi- in temperate desert regions or in the cold- cantly reduced since the introduction of Apis mellifera. In the northern and north- General characteristics eastern regions, Apis mellifera has basi- The ranges of body length are . cally replaced Apis cerana. Such displa- 10—13 mm for the worker bees, 10—16 cement is also found in the western, mm for the queen bees; and 12—14 mm central and eastern regions, particularly for the drones. Generally, races of Apis along transportation routes. Compared to cerana found in the subtropical and tropi- their historical distributions and population cal regions, such as Guangdong, Guangxi, and the southern areas of Yun- densities in these regions, many races of nan provinces are smaller compared to cerana will be on their to Apis clearly way those in the northern temperate zones extinction if no protective measures are and the mountainous regions in the west taken in the near future (Yang, 1984b). (Yang, 1984b). The scape of a ’s index measures 2.32—6.00 in the worker is yellow. The scutellum can be yellow, bee and measures 1.17—3.36 mm in the brown or black. The color of the abdomi- ; the length of terga III and IV nal terga III and IV varies, with most races measures 3.85—4.47 mm in the worker of Apis cerana having varying degrees of bee; the distance between the anterior yellow spots or bands. Except for the apodemes of tergum IV measures 3.81— bees in the western mountainous regions 4.58 mm in the worker bee; and the 1 st above 2 000 m in elevation and those in wax mirrow measures 2.00-2.10 mm in regions north of 42° North latitude, the length and 1.2—1.25 mm in width (Yang, bees are black. Interesting enough, Yang 1984a). (1984a, b) indicated that the pattern of yellow bands and the proportion of yellow Geographical races, distribution, and to black on the body varies according to characters climatic and seasonal factors as well as In the conclusion of the survey, Yang geographic location, although no data (1984b) has grouped Apis cerana in were given in his publications. For China into 5 geographical races and 7 in cerana around the Bei- example, Apis The races 60% of III and IV biotypes. geographical sugges- jing (Peking) area, terga ted by him include the Hainan, Eastern, are in the summer. Since their yellow legs Southern Yunna, Aba and Xizang (Tibet) and abdomen are also yellow, this makes races. The 7 biotypes are the Palm these bees in the summer. appear yellow Forest, and the Mountain of Hainan; But in and at the end of fall, early spring Guangdong-Guangxi; Hunan; Yunnan; as a result of a reduction in yellow bands, Northern and Changbei Shan biotypes. bees in the same black. colony appear Their morphological characteristics and The ratio of bands to black areas yellow other characters used also varies individuals by Yang (1984b) significantly among are summarized in Table 111. within the same colony. Such seasonal change in abdominal tergal color is more The stepwise discriminant analysis of obvious in bees from mountainous our compiled data, including the proboscis regions than bees found in subtropical length, fore-wing length and cubital index and tropical regions. Bees in the latter of bee samples collected from 54 and 166 regions have the yellow bands year round locations in the Eastern and Aba regions (Yang, 1984a). respectively, showed that there was a Queen bees have 2 basic body color significant discrimination (P < 0.05) bet- types. One type is black with distinct ween these 2 geographical races (Fig. 2). black abdominal bands and yellow areas By using these 3 morphological character- shaded grey. The other color type is red- istics, the stepwise analysis procedure dish brown, with bright yellow bands and can classify the Eastern and the Aba narrow black bands. The drones are races with 74.1 and 81.3% correct classifi- generally black or dark grey and are cation respectively. Therefore, our current covered with white hairs (Yang, 1984a). analysis also supports Yang’s (1984) conclusion that the Eastern and the Aba Other morphological characters men- tioned in Yang’s reports (1984a, b) are : races can be separated. However, our the proboscis of the worker bee measures statistical analysis of other geographical 4.60—5.60 mm; the right fore-wing mea- races using the same morphological cha- sures 7.70—9.00 mm in the worker bee; racteristics failed to discriminate among the fore-wing width measures 2.81— the races.This discrepancy is mainly due 3.21 mm in the worker bee; the cubital to the fact that only a small portion of the original data was published and available; tributed from the northern temperate zone hence we used only a small data set in to the southern subtropical and tropical our statistical analysis. Yang (1984b; areas with overlapping geographical Table III) used more characteristics and a regions (Fig. 1 It is well adapted to the larger data set in his study, although no areas characterized by cold winters; hot, statistical analyses were mentioned in his rainy summers; early spring and late fall reports. sources. This race is commonly found in the and Yang (1984b) showed that among all 5 Northeast, North, South, Southeast climatic with geographical races the Hainan race has regions (Fig. 1) the smallest body size. Its legs, scutellum vegetational regions including temperate deciduous broad-leaved and abdomen are yellow. Terga III and IV forests, subtropi- cal broad-leaved are dark brown in the winter and are yel- evergreen forests, tropi- cal seasonal rain forests and some tem- low during other seasons. The coastal This race palm forest biotype appears to be smaller perate steppe regions (Fig. 1). than the central mountain biotype. The is known for its resistance to parasitic latter also is darker in body color. The and predaceous wasps, and is the main race used in China for Hainan race has a strong and . absconding tendency, particularly in July The Southern Yunnan race occurs in and August. It is a race adapted to the Yunnan south of 24.30°N; mainly at the tropical rain forest; hence, it cannot river valleys of Xishuangbanna, and survive in the northern Bejing area if Dehung Daizu Zizhizhou (Fig. 1 The moved there. It is a good collector, morphological characteristics of the Sou- but stores very little honey. thern Yunnan race indicate that it is Apis Enderlein (1906) considered the speci- cerana indica (Yang, 1984b). It has a men of Apis cerana collected from Hai- strong absconding tendency. nan Island to be Apis indica javana. The Aba race is distributed along river However, according to present data, the valleys of the Yalung Jiang and Dadu He Apis cerana race in Hainan has a longer including Aba Zangzu Zizhizhou and proboscis, wider sternum III, more strong- Garze Zangzu Zizhizhou in western ly arched sternum II, and a much larger Sichuan; southern Gansu including Gan- colony size as compared to Apis indica nan Zangzu Zizhizhou, Linxia Huizu javana. Therefore, Yang (1984b) consid- Zizhizhou, Tianshui, Wudu Xian; Minhe, ered the Apis cerana race on the Hainan Ledu, Hualong, Xunhua, Guide, and Island to be distinctively different from Gandu xian of Qinghai; and plateaus of Apis indica javana. Daxue Shan, Glionglai Shan, Min Shan The Eastern race, Apis cerana cerana, and Qilian Shan at 2 000 m elevation is predominant in China, being widely dis- (Yang, 1984b; Fig. 1 It is the largest race of Apis cerana in China. It is a black bee They are the Guangdong-Guangxi, without any seasonal change in body Hunan, Yunnan, Northern, and Changbei color (Table 111). It has a black abdomen Shan biotypes. However, they cannot be and legs; the yellow band on tergum IV easily distinguished based upon their remains very narrow, and it has a dark morphological characteristics (Yang, brown to black scutellum. This bee can 1984b). Our current discriminant analysis build up strong colonies, does not swarm shows that on the basis of proboscis much, and can utilize large nectar length, fore-wing length and cubital index, sources. Therefore, Yang (1984b) indic- the 5 biotypes are classified correctly at ated that it is a race with economic poten- 60.0, 37.1, 60.0, 50.0 and 50.0%, respect- tial. ively. The discrimination function is signifi- cant at P = 0.05. the scatter The Xizang (Tibetan) race occurs in Furthermore, Xizang at the elevation of 2 000—4 000 plot of the canonical variables shows that the can m, along the river valleys of the Yarlung- only Guangdong-Guangxi biotype zangbu Jiang, the Zayu Qu, the Xiloumu be well separated from the rest of the bio- He, Kamen, and the Subansiri He, Cona, types. The scattered plot further indicates Medog and Zayu xian (Fig. 1 The body that the Yunnan plateau biotype contains the Shan and Hunan color appears to be greyish yellow or Northern, Changbei greyish black. Abdominal sternum III has biotypes. Apparently, more data are need- yellow spots, whereas tergum IV is black, ed, specifically for the last four biotypes, in order to understand their to and the posterior area of abdominal seg- relationship ments IV to VI are covered with distinct each other. white hairs. Abdominal tergum V is slen- The Guangdong-Guangxi biotype’s dis- der. This bee also has a strong tendency tribution is mainly along the coastal plains for swarming, and colonies have a low and hills of Guangdong, Guangxi, Zhe- honey yield. Maa (1944) placed the bee jiang, and Fujian provinces. The bees are collected from southern Tibet in the sub- yellow with a small body size; they swarm species Apis indica skorikovi Maa. Yang and abscond frequently; and they are (1984b) was in agreement with Maa’s resistant to parasitic mites (Peng et al., conclusion. 1987a, b) and predaceous wasps. The colony size usually is small. Biotypes, distribution and characters The Hunan biotype is reported to be Yang (1984b) further classified the Hainan bigger than the Guangdong-Guangxi bio- race into two biotypes; the coastal palm type (Yang, 1984b), having larger colony forest and the mountain biotypes. The size compared to the latter biotype. The coastal palm forest biotype appears to be yellow and black bands of the body smaller than the central mountain biotype. change to black in the winter. Its distrib- The latter is also darker in body color. Due ution lies in Jiangxi, Anhuei, Hunan, Guiz- to insufficient data in publications, we hou, Hubei, Sichun provinces, and the made no attempt to use stepwise discrimi- northern regions of Zhejiang and Guang- nant analysis to separate these two bio- dong provinces. types. The major characteristics of the Yun- There are as many as 5 biotypes within nan plateau biotype are a long proboscis the Eastern race, separated according to measuring up to 5.30 mm, as well as a their ecological and geographical differ- large colony size which can contain as ences as suggested by Yang (1984b). many as 10 combs. They are well adap- ted to the Yunnan Gaoyuan plateau and or India (Mattu and Verma, 1983 and the mountains of western Guizhou. 1984). Therefore, it is not known how The Northern biotype is found in closely related races of Apis cerana in Shanxi, Shaanxi, Hebei, and Shandong China are to those of Japan, Sri Lanka, or provinces. It is well adapted to the cold India, except in the case of the geographi- climate of the north China plain, with cal race of southern Yunnan, which very is cerana as 180—240 frost-free days, and an annual likely Apis indica, suggested mean temperature of 4—8°C. Similar to by Yang (1984b). the Yunnan plateau biotype, it also has a The same rationale can also be used large colony size occupying up to 10 to some extent in our analysis of data on combs, but, it has a shorter proboscis Apis cerana taken from Chinese publica- length, and can defend robbing from other tions after the survey of 1975. We could colonies well. only apply the data on the proboscis The fifth biotype which inhabits the length, fore-wing length and cubital index northeastern region is the Changbei Shan in our current stepwise discriminant analy- sis. Because we used 3 type. It occurs mainly in the mountains of only morphologi- Changbei Shan in Jilin province, and cal measurements in our analysis, it is not Xiaoxiang Lin of Heilungjiang Province. It surprising to note a discrepancy between our and the conclusion of is adapted to the severe winter climates analysis Yang Further statistical that of the northeastern region with an annual (1984b). analyses include more characters will mean temperature of 2-60, and morphometric 100—180 frost-free days (Fig. 1) (also definitely enhance the accuracy of the dis- criminant as indicated referred to the maps in Hou, 1983). This analysis, by DuPraw and Ruttner et al. bee has a large body size; black terga III (1965) (1978), and it to the and IV; and a mostly dark brown scutel- may help separate geogra- races and further than in lum. It usually nests in tree trunks and phical biotypes our current builds a large colony, sometimes with analysis. combs up to one meter long.

Acknowledgments

Discussion The authors wish to thank Drs. Richard M. Bohart and Phillip S. Ward for their critical review of the manuscript and many valuable In analyzing the data, we found it is very suggestions. difficult to compare the published data of Yang and his colleagues to the earlier works of Carlisle (1955), Kellogg (1930, 1936, 1938 and 1968), and Maa (1953), References largely due to discrepancies in sampling methods, different morphometric systems Carlisle E. (1955) Biometrical investigations of some and other races of bees. used various authors, as well as European honey by Bee World 36, 41-45 incomplete data given in the publications. Chou 1. (1980) A History of Chinese entomolo- The same reason is also true when com- gy. Entomotaxonomia, pp. 2133 data on cerana collected in paring Apis Dixon W.J. (1985) BMDP Statistical Software. China to those collected in Japan (Saka- University of California Press, Berkeley, Califor- gami, 1959), Sri Lanka (Fernando, 1959) nia, pp. 737 DuPraw E.J. (1965) Non-Linnaean Peng Y.S., Fang Y, Xu S.Y, Ge L.S. & Nasi and the systematics of honey bees. Syst. Zool. M.E. (1987) The response of the foster Asian 14, 1-24 honey bee (Apis cerana Fabr.) colonies to the Enderlein G. (1906) Neue Honigbienen und brood of European honey bee (Apis mellifera BeitrAge zur Kenntnis der Verbreitung der Gat- Linn.) infested with parasitic , tung Apis. Stett Entomol. Ztg. 67, 331-334 jacobsoni Oudemans. J. lnvertebr. PathoL 49, 259-264 Fernando E.F.W. (1959) Some biometrical fea- tures of Apis cerana F. from Sri Lanka. Indian Ruttner F. (1975) Races of Bees. In : The Hive Bee J. 41, 5-8 and the Honey Bee. Dadant & Sons, Hamilton, Hand D.J. Discrimination and Classifi- Illinois, pp. 19-38 (1981) . cation. John Wiley & Sons, New York, pp. 2188 Ruttner F., Tassencourt L. & Louveaux J. 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(1982) Studies on the morphologi- cal characteristics of the Chinese bee in Zhang S.F. (1982) A preliminary report of the honey various areas of Guizhou In : Selec- survey of the Chinese honey bee in Sichuan. province. In : Selected References on the Chinese ted References on the Chinese Honey Bee. Honey Bee. Gansu Provincial Apicultural Res- Gansu Provincial Apicultural Research Institute, earch Institute, Tianshui, 179-189 (in Chinese) Tianshui, 213-227 (in Chinese)