African meliponine bees (Hymenoptera: Apidae) maintained in man-made hives as potential hosts for the small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae) Bridget O Bobadoye 1, 2 , Fombong T. Ayuka 1 , Nkoba Kiatoko 1 , Suresh Raina 1 , Peter Teal 3 , Baldwyn Torto Corresp. 1 1 International Centre of Insect Physiology and Ecology (icipe), P.O. Box 30772-00100, Nairobi, Kenya 2 Department of Entomology, College of Biological and Physical Sciences , P.O. Box 30197-00100, Chiromo Campus, University of Nairobi, Nairobi, Kenya 3 Center for Medical, Agricultural and Veterinary Entomology, 1600/1700 SW 23rd, Gainesville, FL 32606, USDA/ARS, Gainesville, Florida, United States Corresponding Author: Baldwyn Torto Email address: [email protected]Previous studies have shown that natural honeybee and bumble bee colonies are hosts of the small hive beetle (SHB) Aethina tumida, a pest of honeybee colonies in various regions of the world. Recent studies also reported the presence of SHBs in colonies of certain meliponine bee species. In this study, we investigated whether SHBs detect odors of African meliponine bees and their hive matrix components. We also compared the chemical profiles of the honeybee Apis mellifera scutellata and meliponine bee odors in order to identify common potential semiochemicals between the two bee species. We used dual-choice olfactometric assays to test the responses of adult male and female SHBs to intact colony odors from six meliponine bee species, namely Hypotrigona gribodoi, Meliponula ferruginea (black), M. ferruginea (reddish-brown), Plebeina hildbrandti, M. bocandei and M. lendiliana and their hive matrix components including pot honey, pot pollen, cerumen (involucrum) and propolis (batumen). We found that female SHBs responded more strongly to odors from intact colonies, pot honey and pollen from five out of the six species tested than male beetles. Chemical analysis identified several common components in colony odors emitted by both honeybees and a representative meliponine bee species, M. ferruginea (black). In particular, nine of these common components previously have been shown in honeybee volatiles to be semiochemicals for the SHB, suggesting that African meliponine bees can also serve as potential alternate hosts for the beetle. The implications of these results are discussed in the context of domesticating African meliponine bees in man-made hives for the pollination of crops. PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
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African meliponine bees (Hymenoptera: Apidae) maintained inman-made hives as potential hosts for the small hive beetle,Aethina tumida Murray (Coleoptera: Nitidulidae)Bridget O Bobadoye 1, 2 , Fombong T. Ayuka 1 , Nkoba Kiatoko 1 , Suresh Raina 1 , Peter Teal 3 , Baldwyn TortoCorresp. 1
1 International Centre of Insect Physiology and Ecology (icipe), P.O. Box 30772-00100, Nairobi, Kenya2 Department of Entomology, College of Biological and Physical Sciences , P.O. Box 30197-00100, Chiromo Campus, University of Nairobi, Nairobi, Kenya3 Center for Medical, Agricultural and Veterinary Entomology, 1600/1700 SW 23rd, Gainesville, FL 32606, USDA/ARS, Gainesville, Florida, United States
Previous studies have shown that natural honeybee and bumble bee colonies are hosts ofthe small hive beetle (SHB) Aethina tumida, a pest of honeybee colonies in various regionsof the world. Recent studies also reported the presence of SHBs in colonies of certainmeliponine bee species. In this study, we investigated whether SHBs detect odors ofAfrican meliponine bees and their hive matrix components. We also compared thechemical profiles of the honeybee Apis mellifera scutellata and meliponine bee odors inorder to identify common potential semiochemicals between the two bee species. We useddual-choice olfactometric assays to test the responses of adult male and female SHBs tointact colony odors from six meliponine bee species, namely Hypotrigona gribodoi,Meliponula ferruginea (black), M. ferruginea (reddish-brown), Plebeina hildbrandti, M.bocandei and M. lendiliana and their hive matrix components including pot honey, potpollen, cerumen (involucrum) and propolis (batumen). We found that female SHBsresponded more strongly to odors from intact colonies, pot honey and pollen from five outof the six species tested than male beetles. Chemical analysis identified several commoncomponents in colony odors emitted by both honeybees and a representative meliponinebee species, M. ferruginea (black). In particular, nine of these common componentspreviously have been shown in honeybee volatiles to be semiochemicals for the SHB,suggesting that African meliponine bees can also serve as potential alternate hosts for thebeetle. The implications of these results are discussed in the context of domesticatingAfrican meliponine bees in man-made hives for the pollination of crops.
PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
1 African meliponine bees (Hymenoptera: Apidae) maintained in man-made hives as 2 potential hosts for the small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae).
3 Bridget O. Bobadoye1, 2, Ayuka T. Fombong1, Nkoba Kiatoko1, Raina Suresh1, Peter E. A. Teal3, 4 Baldwyn Torto1*.
5 1International Centre of Insect Physiology and Ecology (icipe), P.O. Box 30772-00100 Nairobi, 6 Kenya;
7 2Department of Entomology, College of Biological and Physical Sciences, University of Nairobi 8 (UoN) , P.O. Box 30197-00100, Chiromo Campus, Nairobi, Kenya.
9 3USDA/ARS-Center for Medical, Agricultural and Veterinary Entomology, 1600/1700 SW23rd
10 Dr. Gainesville, FL 32606
11 † Peter Teal passed away on 11th February 2015.
PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
15 Abstract
16 Previous studies have shown that natural honeybee and bumble bee colonies are hosts of the 17 small hive beetle (SHB) Aethina tumida, a pest of honeybee colonies in various regions of the 18 world. Recent studies also reported the presence of SHBs in colonies of certain meliponine bee 19 species. In this study, we investigated whether SHBs detect odors of African meliponine bees 20 and their hive matrix components. We also compared the chemical profiles of the honeybee Apis 21 mellifera scutellata and meliponine bee odors in order to identify common potential 22 semiochemicals between the two bee species. We used dual-choice olfactometric assays to test 23 the responses of adult male and female SHBs to intact colony odors from six meliponine bee 24 species, namely Hypotrigona gribodoi, Meliponula ferruginea (black), M. ferruginea (reddish-25 brown), Plebeina hildbrandti, M. bocandei and M. lendiliana and their hive matrix components 26 including pot honey, pot pollen, cerumen (involucrum) and propolis (batumen). We found that 27 female SHBs responded more strongly to odors from intact colonies, pot honey and pollen from 28 five out of the six species tested than male beetles. Chemical analysis identified several common 29 components in colony odors emitted by both honeybees and a representative meliponine bee 30 species, M. ferruginea (black). In particular, nine of these common components previously have 31 been shown in honeybee volatiles to be semiochemicals for the SHB, suggesting that African 32 meliponine bees can also serve as potential alternate hosts for the beetle. The implications of 33 these results are discussed in the context of domesticating African meliponine bees in man-made 34 hives for the pollination of crops.
274 brown), M. bocandei, M. lendiliana, Plebeina hildbrandti and Hypotrigona gribodoi, and found
275 that both sexes of the beetle responded differently to the odors released from intact colonies of
276 these meliponine bee species as well as their matrix components, including pot honey, pot
277 pollen, cerumen and propolis. Previous work on stingless bees have mainly focused on
278 pheromones within and between species (Jarau et al., 2003; Strangler et al., 2009;Cruz-Lopez et
279 al., 2001; Engels et al.,1986; Johnson et al., 1983, 1985; Smith and Roubik,1983). Our findings
280 provide the first behavioral evidence of SHB attraction to stingless bee species.
281 In general, females of the SHB responded more strongly to the different odors than males. These
282 results suggest a number of reasons to account for these differences. Firstly, there could be sex
283 variation in the sensitivity of the SHB to detect and process meliponine bee odors both at the
284 peripheral and central nervous systems to successfully carry out biological processes such as
285 feeding and reproduction. For instance, it would be advantageous for females to be more
286 responsive to a wide range of stingless bee colony volatiles than males because an intact colony
287 rich or limited with food resources such as pollen and honey would be essential for feeding by
288 females to reach sexual maturity early and for pheromone production to attract the opposite sex
289 for mating and egg development in mated females (Mustafa et al., 2015). On the other hand,
290 since males were more responsive to only the colony odors of M. ferruginea (black) suggests that
291 they may appear to be more selective in their nutritional needs than females. Secondly, whole
292 colony matrix component quantity and concentration such as the number of stingless bees and
PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
293 caste developmental stages, amounts of honey, pollen, cerumen and propolis present in a colony
294 at the time of assays, would all contribute to the quality of the odor signal detected and
295 behavioral response elicited in both sexes of the beetle. Our data appears to match these
296 suggestions as shown by the strong responses of females to the different odor sources especially
297 pollen odors compared to males across the six meliponine bee species studied. They are also in
298 agreement with a previous study, which showed that female SHBs showed a stronger dose-
299 dependent response than males in wind tunnel assays to odors of fresh pollen obtained from
300 honeybee colonies (Suazo et al., 2003). However, further studies are required to investigate these
301 suggestions.
302 Interestingly, despite the strong responses to colony, pollen and honey odors, both sexes of the
303 beetle responded rather weakly or even avoided odors of cerumen from certain meliponine
304 species. Notably, odors that were emitted by cerumen obtained from the stingless bee species
305 Meliponula ferruginea (black) and Plebeina hildbrandti were avoided by both sexes of the
306 beetle, suggesting that they may contain repellents. Cerumen is a mixture of pure plant resins and
307 bee secretions molded into protective sheaths in the brood and food chambers in most
308 meliponine bees (Greco et al., 2009). It is known to possess anti-bacterial, anti-fungal and anti-
309 predatory properties (Patricio et al., 2002; Lehmberg et al., 2008). Consistent with our
310 observations for SHB responses to other matrix components, there were also notable sex
311 variation responses to cerumen odors emitted, in particular by M. ferruginea (reddish-brown), M.
312 bocandei and M. lendiliana. The basis for these differences is unknown, but it appears that it
313 may be associated with the quality and quantity of the odor emitted by the whole hive matrix
314 component. These results suggest that more detailed research is needed to investigate the pattern
315 of responses of the SHB to colony and matrix component odors at different seasons.
316 A comparison of the odor profiles revealed a high and complex chemical diversity including
317 esters, ketones, aldehydes, terpenes, benzenoids and hydrocarbons emitted by the intact colonies
318 of honeybee and the stingless bee species M. ferruginea. Most of the compounds identified in the
319 volatiles emitted by the two different colonies have previously been reported as components of
320 floral volatiles (Knudsen et al., 1993; Torto et al., 2005, 2007b, 2007c; Strangler et al., 2009).
321 However, the level of qualitative similarity between the odor profiles was low (~20%). These
322 results suggest that the nectar and pollen sources may be different for the two different bee
PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
323 species in accordance with the fact that these two bee species show preference to certain plants
324 as pollen and nectar sources (Vit et al., 2013). Although this study did not investigate the
325 volatiles emitted by the other five stingless bee species, we hypothesize that a similar chemical
326 diversity may be present in their odor profiles. Additional studies are needed to test this
327 hypothesis. Notably, a few of the compounds identified including isopentyl acetate, 2-heptanone,
328 octanal, hexyl acetate, nonanal, 2-nonanone, methyl benzoate and decanal are semiochemicals
329 for the SHB (Torto et al., 2005). Of these semiochemicals, the honeybee alarm pheromones
330 isopentyl acetate and 2-heptanone, and the aldehydes octanal and nonanal, are also constituents
331 of the volatiles of M. ferruginea (black). Also, the compounds 2-heptanol, 2-heptanone, octanal,
332 hexanoic acid, nonanal, 2-nonanol, 2-nonanone, octanoic acid, decanal and decanoic acid to
333 name a few have been reported as components of the cephalic volatile bouquet of Scaptotrigona
334 postica queens (Engels et al.,1986) , with 2-heptanol as an alarm pheromone component of the
335 stingless bees M. fasciata, M. interrupta triplaridis, and Trigona sylvestriana (Engels et al.,
336 1986; Johnson et al., 1985; Smith and Roubik,1983).
337 Previous studies had shown that stingless bee colonies that were infested by the SHB were
338 predominantly from the Trigona and Dactylurina genera (Halcroft et al., 2011; Neumann et al.,
339 2004). Thus, our results clearly show that, like previously shown in the host location of
340 honeybees by SHBs (Suazo et al., 2003; Torto et al., 2005; 2007a), olfaction also plays a major
341 role in the host location process of the beetle in locating stingless bee colonies. As such, we
342 suggest that the domestication of stingless bee species in fabricated man-made hives for
343 pollination services would require use of well-constructed hives, free of crevices and cracks,
344 which are known to facilitate easy entry by the SHB into man-made honeybee hives (Elzen et al.,
345 1999). We also suggest that, and an efficient maintenance schedule for these man-made hives
346 may be required to prevent infestations and expansion of the potential host range and dispersal
347 into new landscapes by the SHB.
348 In summary, we have shown that the olfactory responses of SHBs to stingless bee volatiles can
349 vary based on the species of the bee and its matrix components. We have also shown that sex of
350 the SHB can also determine its responses to these different odor sources, and that the volatile
351 profiles of both honeybees and stingless bees can be very complex and diverse, but a small
352 proportion of it is identical. Thus, our results suggest that the SHB has the potential to expand its
PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2310v1 | CC BY 4.0 Open Access | rec: 22 Jul 2016, publ: 22 Jul 2016
353 host range to include various species of meliponine bees, requiring that our quest to domesticate
354 stingless bees’ species in man-made hives for future pollination of crops warrants further study.
355
356
357 Acknowledgements:
358 The authors wish to acknowledge African Women in Agricultural Research and Development
359 (AWARD) for providing an advanced science internship, the International Centre for Insect
360 Physiology and Ecology – icipe (Behavioral and Chemical Ecology Unit (BCEU) for providing
361 valuable material and technical support for this project for access and use of its meliponary in
362 Kakamega, Kenya for the study. This project was partly funded by the United States Department
363 of Agriculture – Agricultural Research Service Project No. SCA-586615-7-119F and icipe
364 CORE funds.
365
366
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480 Torto B, Suazo A, Alborn H, Tumlinson JH, Teal PEA. 2005. Response of the small hive beetle 481 (Aethina tumida) to a blend of chemicals identified from honeybee (Apis mellifera) 482 volatiles. Apidologie 36: 523-532.483 Wilson EO. 1971. The Insect Societies. Harvard University Press, Cambridge, Massachusetts. 484485
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512 FIGURE CAPTIONS:
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516 Figure 1: Olfactometer setup.
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524 Figure 2: Male and female SHBs responses to individual and whole hive components.
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526 Fig 3: A representative chromatogram of chemical components of whole hive odors in 527 Meliponine (Meliponula ferruginea (black) and Honeybees (Apis mellifera scutellata).528
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537538 Fig 4: A representative diagram of unique and common chemical components of whole hive 539 odors in Meliponine bees (Meliponula ferruginea) and Honeybees (Apis mellifera scutellata)540541542543544545546547548
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552 TABLES:
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554 Table 1: A summary of the ANOVA of Aethina tumida responses to odors of four hive 555 components from six Afro tropical stingless bee species