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Comparative Nestmate Recognition in Asian Honey Bees, Apis Florea, Apis

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Comparative Nestmate Recognition in Asian Honey Bees, Apis Florea, Apis Apidologie 38 (2007) 411–418 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2007 www.apidologie.org DOI: 10.1051/apido:2007025 Original article Comparative nestmate recognition in Asian honey bees, Apis florea, Apis andreniformis, Apis dorsata,andApis cerana* Michael D. Breeda,b,Xiao-BaoDengb, Robert Buchwalda a EBIO CB 334, University of Colorado, Boulder, Department of Ecology and Evolutionary Biology, CO 80309-0334, USA b Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 66303, P.R. China Received 11 August 2006 – Revised 17 February 2007 – Accepted 19 February 2007 Abstract – In nestmate recognition bioassays, Apis florea, A andreniformis, A. dorsata and A. cerana do not exhibit aggressive responses. These negative results were obtained using three distinct techniques: pairings of bees between colonies, switching nest box locations (A. cerana only), and treatment with compounds known to serve as nestmate recognition pheromones in A. mellifera. This is in sharp contrast to previously observed responses in A. mellifera, which displays strong aggressive responses to conspecific non-nestmates in the same types of bioassays. A. cerana expresses nestmate recognition, but only under limited circum- stances – when robbing is precipitated by honey harvesting or the merger of colonies by a beekeeper. Our results suggest that robbing of stored food may be more characteristic of A. mellifera than other species in the genus Apis, and consequently A. mellifera displays a more strongly developed response to conspecific non-nestmates than other Apis species. nestmate recognition / Apis / defensive behavior 1. INTRODUCTION To our knowledge, only one previous study addresses nestmate recognition in a species of Nestmate recognition is a critical aspect of Apis other than A. mellifera (Sasagawa et al., colony defense in many social insects (Breed 2002; Oldroyd and Wongsiri, 2006). Most of et al., 2004a). Species such as the western our current knowledge of the comparative de- honey bee, Apis mellifera L., which are sub- fensive behavior of Apis species comes from jected to social parasitism, robbing of food, Seeley et al. (1982). One aspect of defense and robbing of brood, are typically capa- that they did not address was intraspecific nest- ble of discriminating nestmates from non- mate recognition; studies of species other than nestmates. Such discriminations, which are A. mellifera will give insight into the ecologi- generally characterized as nestmate recogni- cal and evolutionary malleability of nestmate tion, are expressed at the nest entrance with recognition. In this paper we report results a defensive response, such as biting, stinging, suggesting a lack of expression of nestmate or grappling (Breed, 1998b; Vander Meer and recognition in Asian species of Apis; publica- Morel, 1998; Lenoir et al., 2001a, b). Nestmate tion of such results is important in developing recognition is well known in all the major eu- an overall understanding of nest defense in so- social insect taxa (Vander Meer et al., 1998; cial insects (Gamboa et al., 1991). Starks, 2004). Many investigations have assumed that nestmate recognition is an extension of the Corresponding author: M. Breed, ability to make fine discriminations con- [email protected] cerning relatedness among nestmates (e.g. * Manuscript editor: Stan Schneider Greenberg, 1988; Bura and Gamboa, 1994, but Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2007025 412 M.D. Breed et al. see Dani et al., 2004). This may be true in Downs and Ratnieks, 2000; Guzman-Novoa primitively eusocial insects, such as the hal- et al., 2002) we hypothesized that other species ictid bees studied by Greenberg (1988). How- of Apis would display similar responses. We ever, in the highly eusocial insects nestmate tested nestmate recognition in A. cerana, A. recognition may be more related to the eco- florea, A. andreniformis and A. dorsata using logical circumstances and evolutionary history three different nestmate recognition bioassays of a species than to intracolonial discrimi- (Breed, 2003) in order to better understand in- nation of genetic groups. For example, Ar- terspecific differences in expression of nest- gentine ants (Linepithema humile) in Califor- mate recognition and defensive behavior. nia, whose colonies often comprise unrelated workers and queens, do not display nestmate recognition over a broad geographic range 2. METHODS (Tsutsui et al., 2003), nor do many polyg- ynous, polydomous ant species (e.g., Starks 2.1. General et al., 1998). The primitively eusocial bumble- bee, Bombus impatiens, also appears not to ex- Colonies were located in and near the hibit nestmate recognition (unpubl. data). Ad- Xishuangbanna Tropical Botanical Garden ditionally, resource abundance and associated (XTBG), Yunnan Province, People’s Republic foraging strategies may be important influ- of China, 21.41◦ N lat., 101.25◦ E long. XTBG ences on nestmate recognition. Increased com- is at 570 M elevation, on the Luosuo tribu- petition for resources and intercolonial inter- tary of the Mekong River near the border of actions could influence selection for stronger the PRC, Laos and Myanmar. This evergreen nestmate recognition. Reeve (1989) made an seasonal tropical forest habitat (1560 mm an- important theoretical contribution, pointing nual precipitation) has a long hot dry season, out that thresholds for expressing behavioral mid-March to May, and a cool dry season from responses to non-nestmates may be dependent November to February; the balance of the year on ecological conditions. is characterized by frequent rains. A. florea, Comparative studies of nestmate recogni- A. dorsata and A. andreniformis are seasonal tion also may give insight into the diversity migrants in this habitat, moving to higher ele- of chemical cues used in nestmate recogni- vations during the rainy season. These exper- tion. Nestmate recognition cue chemistry is iments were conducted from October 2004 to well known for some social insects. In Cam- July 2005. ponotus fellah ants, the predominant nestmate For the first set of experiments, in Octo- recognition signals are alkenes, which are dis- ber 2004, six A. cerana colonies, located in tributed among colony members via the post- the XTBG and maintained by a beekeeper in pharyngeal organ (Lenoir et al., 2001b). How- moveable frame hives, were used. The A. cer- ever, in Argentine ants, Linepithema humile, ana colonies were roughly equal in size, each environmentally-derived cues are strongly im- in a box approximately the size of standard plicated (Liang and Silverman, 2000). Nest- Langstroth hive. We also used three A. florea mate recognition signals in Polistes wasps are colonies, located on a farm several hundred methyl-branched alkanes (Dani et al., 2001). meters higher in elevation than the XTBG, 20– In the western honeybee, Apis mellifera, fatty 30 meters apart from each other. The three A. acids play an important role, as do alkenes florea colonies were roughly equal in size as (Breed, 1998a). Differences in nestmate recog- well, as judged by the mass of bees on the nition among Apis species could correlate with nest. Additionally, two A. dorsata colonies, differences in cue chemistry, sensitivity, or di- 30 kilometers separated, were used in these ex- versity, or could be affected by differences periments. One was located near XTBG, and among species in response thresholds (Reeve, one 330 meters higher in elevation; both were 1989). typically-sized colonies for this area. The sea- Given the strong nestmate recognition re- son when our study was conducted is appar- sponse of A. mellifera (Moore et al., 1987; ently unfavorable at the elevation of the XTBG Nestmate recognition in the genus Apis 413 for A. dorsata and A. florea.However,the nestmate in a higher percentage of replicates A. cerana colonies at that elevation were ac- (Breed et al., 2004b). This result confirms the tively foraging for both pollen and nectar, and activity of the 18 carbon acids as recognition showed no signs of the cessation of foraging pheromones. These same acids function sim- that is characteristic of dearth conditions. ilarly, and bees respond in the same type of bioassays, in a stingless bee, Trigona fulviven- tris (Buchwald and Breed, 2005). Unpublished 2.2. Bioassay 1. Intra- and intercolonial results (Lyon, Breed and Buchwald) show that aggression flax oil has the same effect as the pure fatty acids in Apis mellifera. Aggression bioasssays, following methods used with A. mellifera (Breed, 2004a; Downs and Ratnieks, 2000) and the general principles described by Breed (2003) were conducted 2.4. Bioassay 3. Colony transpositions in within and between colonies of each of the Apis cerana three species. In these bioassays, bees were captured and paired in 5 mL glass vials. The A third bioassay approach was used in A. interactions between the bees were observed cerana, with the object of providing a more for 5 min; in each pairing the observer was natural context for the expression of nestmate blind with respect to whether the bees were recognition. In this bioassay foragers from nestmates or non-nestmates. In A. cerana, bees pairs of colonies were marked with enamel for the bioassays were collected from near paint, each colony receiving a different color. the nest entrance. Although guards are not as We marked the bees from 1500 h to 1700 h one easily identified in A. cerana as in A. mel- day, and then at 2000 h that evening (after sun- lifera (Moore et al., 1987), most of the bees set) the colony locations were transposed. The used in the experiments were seen shimmer- next day experienced foragers return to their ing (see Results) and could therefore be con- colony’s previous location, where they en- sidered guards. Identifying guards in A. flo- counter workers from the other colony. We did rea and A. dorsata,wasmoredifficult. A. flo- four such switches, using six colonies. Colony rea and A. dorsata workers for bioassays were entrances were observed for 1.0 hour begin- removed from the outer layer of bees blan- ning at 0700 h and the number of foragers keting the comb.
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