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The Electronic Bee Spy: Eavesdropping on Honeybee Communication Via Electrostatic Field Recordings

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The Electronic Bee Spy: Eavesdropping on Honeybee Communication Via Electrostatic Field Recordings ORIGINAL RESEARCH published: 28 April 2021 doi: 10.3389/fnbeh.2021.647224 The Electronic Bee Spy: Eavesdropping on Honeybee Communication via Electrostatic Field Recordings Benjamin H. Paffhausen 1†, Julian Petrasch 2†, Uwe Greggers 1, Aron Duer 1, Zhengwei Wang 3, Simon Menzel 1, Peter Stieber 3, Karén Haink 1, Morgan Geldenhuys 4, Jana Cˇavojská 2, Timo A. Stein 5, Sophia Wutke 1, Anja Voigt 1, Josephine Coburn 1 and Randolf Menzel 1* 1Department Biology, Neurobiology, Freie Universität Berlin, Berlin, Germany, 2Department Information Science, Freie Universität Berlin, Berlin, Germany, 3CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, China, 4Independent Researcher, HAPE Imkerei GmbH, Neulußheim, Germany, 5Complex and Distributed IT Systems, Technische Universtät Berlin, Berlin, Germany, 6Department of Physics, University of Oslo, Oslo, Norway Edited by: As a canary in a coalmine warns of dwindling breathable air, the honeybee can indicate Ralf Heinrich, the health of an ecosystem. Honeybees are the most important pollinators of fruit-bearing University of Göttingen, Germany flowers, and share similar ecological niches with many other pollinators; therefore, the Reviewed by: Qiang Huang, health of a honeybee colony can reflect the conditions of a whole ecosystem. The Jiangxi Agricultural University, China health of a colony may be mirrored in social signals that bees exchange during their Roger Schürch, Virginia Tech, United States sophisticated body movements such as the waggle dance. To observe these changes, *Correspondence: we developed an automatic system that records and quantifies social signals under Randolf Menzel normal beekeeping conditions. Here, we describe the system and report representative [email protected] cases of normal social behavior in honeybees. Our approach utilizes the fact that †These authors share first authorship honeybee bodies are electrically charged by friction during flight and inside the colony, Specialty section: and thus they emanate characteristic electrostatic fields when they move their bodies. This article was submitted to Individual and Social Behaviors, These signals, together with physical measurements inside and outside the colony a section of the journal (temperature, humidity, weight of the hive, and activity at the hive entrance) will allow Frontiers in Behavioral Neuroscience quantification of normal and detrimental conditions of the whole colony. The information Received: 29 December 2020 provided instructs how to setup the recording device, how to install it in a normal bee Accepted: 06 April 2021 colony, and how to interpret its data. Published: 28 April 2021 Keywords: honey bee (Apis mellifera L.), social, electrostatic field, behavior, datalogger Citation: Paffhausen BH, Petrasch J, Greggers U, Duer A, Wang Z, Menzel S, Stieber P, Haink K, INTRODUCTION Geldenhuys M, Cˇ avojská J, Stein TA, Wutke S, Voigt A, Coburn J and A honeybee colony is a well-organized unit of social life that is composed of highly interacting Menzel R (2021) The Electronic Bee groups of single organisms with different duties, age-dependent behavioral routines, and Spy: Eavesdropping on Honeybee experience. Many of the messages communicated between these organisms are accessible by Communication via Electrostatic Field Recordings. electric-field measurements. These are electrostatic signals that workers produce due to their body Front. Behav. Neurosci. 15:647224. movements, e.g., their dances, shivering to control temperature, fanning behavior to regulate hive doi: 10.3389/fnbeh.2021.647224 humidity and CO2, ‘‘stop’’ and ‘‘whooping’’ signals, and overall motor activities characteristic of Frontiers in Behavioral Neuroscience| www.frontiersin.org 1 April 2021 | Volume 15 | Article 647224 Paffhausen et al. Eavesdropping on Honeybee Communication arousal states, preparation for play flights of young bees, allow unsupervised long-term monitoring of health conditions and preparation for swarming. Dances are particularly rich in in honeybee colonies. information because they encode specific meaning in a symbolic form (von Frisch, 1967). Rhythmic movements of bee bodies, in MATERIALS AND METHODS whole or in part (e.g., the abdomen and the wings), are technically easily observable because they produce characteristic patterns of Hive electrostatic fields (ESF; Greggers et al., 2013). This is because The bee hive contained 11 regular comb frames (Zander system, the wax-covered body surface of bees charge up electrostatically Holtermann, Germany) and one frame for the measuring devices due to friction between body parts, between animals inside of the (Figure 1A). The four vertical walls of the hive box were made crowded hive, and between the air and body during flight. We of two layers of wood glued together with a metal mesh between used these signals to characterize and quantify the information them to act as a Faraday cage. The mesh layers were connected to flow inside the hive. Here we describe how we measured the the ground. The floor consisted of a metal mesh for ventilation relevant signals under undisturbed bee keeping conditions, how and access of bees to the combs. In order to close the Faraday we related these electrostatic signals to body movements of single cage, a roof made of tin was also connected to the mesh layers and bees, and how we shall use these signals to identify biologically ground. The system was designed such that normal beekeeping meaningful states of the colony. was combined with electric-noise shielding. The back of the hive ESF data collected from whole colonies are relevant in box was elongated to house the electronics and a car battery as many respects. Honeybees are the most efficient pollinators power supply. of economically and environmentally highly relevant plants (Klein et al., 2007; Potts et al., 2016). Dance activities tightly Sensors mirror foraging activities across an area of some 5 km radius A plastic tube extending from the side-wall of the hive contained around a hive (von Frisch, 1967). Since a dance codes the a GPS module (UBX-G7020, u-blox, China, not shown), which outbound component of a flight to the pollinated flowers or was used to synchronize time and spatial date information other food sources, available information potentially allows from satellites. The hive weight was monitored with three load spatial tracking of pollination activities (Steffan-Dewenter and cells (LC; 50 kg, AUTODA, China) connected to load cell Kuhn, 2003; Seeley, 2011; Couvillon et al., 2014). These efforts, amplifiers (Avia Semiconductor, HX711 ADC, China). A sensor however, provided rather limited information because of the for external temperature and humidity (HTU21D-F breakout experimental challenges to decode the large number of dances board, Adafruit, NY, USA) was located below the extension of necessary for ecological studies. ESF measurements allow for the hive (Figure 1A, TS/HS sensor outside). A second sensor for a quantification of colony-related pollination activity and its internal temperature and humidity was located in the measuring dynamics over time and space. The health of honeybee colonies, frame (Figure 1B, TS/HS sensor inside). The entrance consisted and thus their pollination efficiency depends on multiple of a plastic tube (diameter: 50 mm, length: 10 cm) with a landing components including season, environmental conditions, bee platform (Figure 1A, insert). The inside of the tube was equipped keeping activities, infections by parasites (viruses, bacteria, fungi, with two metal rings (width: 1 cm) that were connected to a mites), and exposure of/to insecticides (Chauzat et al., 2010; capacity sensor (FDC1004, Texas Instruments, TX, USA). A brass Moritz et al., 2010; Morawetz et al., 2019). The latter conditions tube (diameter: 1 cm) was placed in the middle of the plastic are particularly relevant in modern agricultures since many tube and served as a reference potential by being connected insecticides (e.g., neonicotinoids) act directly on the nervous to ground. These capacity sensors at the entrance served as an system of honeybees (Eiri and Nieh, 2012; Casida and Durkin, activity measure of bees entering and leaving the hive. Changes 2013), and have been found to compromise not only foraging of capacitance depended on the numbers and frequencies of bees activity and navigation, but also dance communication (Van der traveling through the tube since the dielectric constant of the Sluijs et al., 2015; Tison et al., 2020). Other insect pollinators bee body (mainly water) is approximately 80 times higher than (butterflies, beetles, flies, solitary bee) are also affected by that of air. The high dynamic range of the sensor allowed nearly insecticides, and thus monitoring the effect of insecticides on single-bee resolution, and measurements from an absence of bees honeybee communication may provide information beyond to full bee beard and above. honeybee pollination activities (Pisa et al., 2015). In this The ESF measurements sensors were placed in a sense, ESF measurements in honeybee colonies offer access to box—referred to as measuring comb—(Figure 1C) made of biologically and environmentally relevant data about the health 4 mm thick Plexiglas sheets which occupied a third of a standard condition of ecosystems. Zander frame with a thickness identical to regular combs. The Our approach aims to implement a robust ESF measuring sensors pointed towards the neighboring comb
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