High Frequency Sounds Produced by Cyprian Honeybees Apis Mellifera Cypria When Confronting Their Predator, the Oriental Hornet V

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High Frequency Sounds Produced by Cyprian Honeybees Apis Mellifera Cypria When Confronting Their Predator, the Oriental Hornet V High frequency sounds produced by Cyprian honeybees Apis mellifera cypria when confronting their predator, the Oriental hornet Vespa orientalis Alexandros Papachristoforou, Jérôme Sueur, Agnès Rortais, Sotirios Angelopoulos, Andreas Thrasyvoulou, Gérard Arnold To cite this version: Alexandros Papachristoforou, Jérôme Sueur, Agnès Rortais, Sotirios Angelopoulos, Andreas Thrasyvoulou, et al.. High frequency sounds produced by Cyprian honeybees Apis mellifera cypria when confronting their predator, the Oriental hornet Vespa orientalis. Apidologie, Springer Verlag, 2008, 39 (4), pp.468-474. hal-00891958 HAL Id: hal-00891958 https://hal.archives-ouvertes.fr/hal-00891958 Submitted on 1 Jan 2008 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 39 (2008) 468–474 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2008027 Original article High frequency sounds produced by Cyprian honeybees Apis mellifera cypria when confronting their predator, the Oriental hornet Vespa orientalis* Alexandros Papachristoforou1,JérômeSueur2, Agnès Rortais3, Sotirios Angelopoulos4, Andreas Thrasyvoulou1, Gérard Arnold3 1 Laboratory of Apiculture-Sericulture, School of Agriculture, Aristotle University of Thessaloniki, Greece 2 Muséum National d’Histoire Naturelle, Département Systématique et Évolution, USM 601 MNHN & UMR 5202 CNRS, BP 50, 45 rue Buffon, 75005 Paris, France 3 Laboratoire Évolution, Génomes, Spéciation, CNRS UPR 9034, Université Paris-Sud 11, Orsay, 91198 Gif-sur-Yvette, France 4 Laboratory of Engineering Geology, Faculty of Civil Engineering, Aristotle University of Thessaloniki, Greece Received 28 December 2007 – Revised 28 February 2008 – Accepted 18 March 2008 Abstract – Honeybees face several predators and their ability to express collective defence behaviour is one of their major life traits that promote colony survival. We discovered that, while confronting attacks by the Oriental hornet Vespa orientalis, Apis mellifera cypria honeybees engage in a distinct acoustic behaviour: they produce a characteristic hissing sound of unexpectedly high frequency. When recording and analysing these hissing sounds during an extended sample of artificial attacks by hornets, we found that honeybees can produce sounds covering a wide frequency spectrum with a dominant frequency around 6 kHz. Notably, these acoustic emissions are distinct from the background noise of neighbouring flying bees. These results provide a detailed description of the sounds generated by A. m. cypria when defending their nest against hornets, and they could be used for future research to better understand the biological function of the acoustic behaviour in honeybees’ colony defence. hissing sound / colony defence / Apis mellifera cypria / Vespa orientalis / prey-predator contest 1. INTRODUCTION velutina Lepeletier in France and its rapid dispersal (Villemant et al., 2006) may repre- Massive defence behaviour is a predom- sent a threat to bee colonies. Fine-tuning co- inant life trait of social bees. Honeybees evolving prey-predator relationships allow co- face several predators during their cycle. Hor- existence among sympatric species, but in the nets (Hymenoptera, Vespidae) are particularly case of recent invasion, such relationships may known to induce serious damages to apiaries not have the time to develop. However, given by killing many individual honeybees or even the relatively high number of Apis mellifera by destroying entire colonies and occupy- subspecies and their large geographic range ing the beehive, using its resources (honey, and habitat characteristics, a wide variety of pollen, brood and adult honeybees) to feed behavioural responses are expected among their brood (Morse, 1978; Ono et al., 1987, them (Ruttner, 1988), including defensive be- 1995; Abrol, 1994; Ken et al., 2005). The haviour. Collective anti-predator behaviour, recent invasion of the Asiatic hornet Vespa which promotes colony safety, may be char- acterized by specific displays such as the Corresponding author: A. Papachristoforou, so-called “curtain phenomenon”, the “heat- [email protected] balling” strategy and in some other cases the * Manuscript editor: Stan Schneider stinging behaviour (Breed et al., 2004). During Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2008027 A. m. cypria defence behaviour towards Vespa orientalis 469 such aggressive interactions, bees are also able made with a Sennheiser ME64 microphone (fre- to release alarm pheromones (i.e. isoamyl ac- quency response: ± 2.5 dB between 0.04 kHz and etate, 2-heptanone) and to produce typical 20 kHz) connected to a Marantz PMD 670 digital sounds, namely “hissing” or “shimmering”, recorder (16 bit/44.1 kHz sampling frequency). The which may serve as alarms to deter intruder microphone was set up at the beehive entrance, 5– attacks and recruit defending bees (Lindauer, 20 cm from the defending bees engaged in conflicts. 1956; Schneider and Kloft, 1971; Fuchs and To simulate attacks, hornets were collected in the Koeniger, 1974; Ohtani and Kamada, 1980; apiaries and were anaesthetized by CO2 for 5 sec- Seeley et al., 1982; Kastberger and Sharma, onds and then tied at the petiole to a stick with a 2000; Sen-Sarma et al., 2002). These signals 10 cm nylon wire to a stick. When hornets fully recovered, they were brought to the beehive flight show a 0.3–0.7 kHz fundamental frequency board and exposed to colonies guards. with harmonic bands extending up to 5 kHz. Sounds emitted during visual and physical con- In the endemic honeybee of Cyprus A. m. ff tacts with hornets were analysed using Avisoft cypria, a specific and e ective defensive (Specht, 2004) and Seewave (Sueur et al., in press). behaviour against its main native predator, the Hisses were detected by computing sliding short- Oriental hornet V. orientalis has been demon- term Fourier transforms (Hamming window du- strated (Morse, 1978). This behaviour consists ration = 0.023 s, 87.5% of overlap). Hiss dura- of coordinated, collective defence behaviour tion was measured with a 0.001 s precision, and against the attacking hornet that involves frequency properties were described by comput- shimmering and balling. During conflict and, ing Fourier transform in the middle of the sound especially, during balling, Cyprian honeybees (frequency precision = 11 Hz). The resulting fre- can induce the death of the predator through quency spectrum allowed measuring the funda- asphyxiation (Papachristoforou et al., 2007) mental frequency f0 (i.e. the lowest frequency and produce a very distinct hissing sound band) and the dominant frequency (i.e. the fre- (Butler, 1954). Yet, no systematic acoustic quency band with the highest energy). Because the documentation deriving from a large sample of fundamental frequency was difficult to detect, it recordings of this acoustic behaviour has ever was indirectly estimated by measuring two succes- been attempted. In particular, no comparison sive harmonic peaks fn and fn+1 and computing − = + − = has been conducted to estimate its variability fn+1 fn (n 1) f0 nf0 f0. The fundamental and to test for potential acoustic differences frequency of the background sound due to flying bees was estimated on spectrum computed imme- within and between colonies. To better under- diately before or after the hiss. stand the interactions between honeybees and Mean, standard deviation and inter-quartile- one of their main predator and thus to help esti- range (IQR) were calculated for each variable mating the risks for apiculture, but also for bio- (hiss duration, hiss dominant frequency, hiss and diversity since such predators may have an im- buzz fundamental frequency) and the normality portant impact on ecosystems (Abrol, 1994), Shapiro-Wilk test was run before conducting para- we studied in detail the high-frequency sounds metric or non-parametric tests (one-way ANOVAs produced by A. m. cypria when attacked by V. and Kruskal-Wallis tests, respectively). To assess orientalis. potential differences between colonies, the ratio CVw/CVb was calculated for each parameter, where CVw is the within-colony variation and CVb is the 2. MATERIALS AND METHODS between-colony variation (Sokal and Rohlf, 1995). All statistics were run using R (R Development The sounds produced by A. m. cypria were Core Team, 2004). recorded in nine colonies in Cyprus (Amiantos- N34◦53’, E32◦56’; Alassa-N34◦46’, E32◦57’). These sounds included both defence hisses pro- 3. RESULTS duced by guards and buzzes due to flying activity of workers. Experiments were conducted between the During conflict with hornets, honeybees ex- end of September and beginning of October 2006, hibited intense collective defence by engulfing which is the period of the most extensive flying ac- and trapping the intruder in balls of 50–120 de- tivity and predation for hornets. Recordings were fending guards. Before the beginning or during 470 A. Papachristoforou et al. Figure 1. Two successive hisses produced during hornet attacks:
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