Long-term trends in the honeybee ‘whooping signal’ revealed by automated detection

<div><p>It is known that honeybees use vibrational communication pathways to transfer information. One honeybee signal that has been previously investigated is the short vibrational pulse named the ‘stop signal’, because its inhibitory effect is generally the most accepted interpretation. The present study demonstrates long term (over 9 months) automated <i>in-situ</i> non-invasive monitoring of a honeybee vibrational pulse with the same characteristics of what has previously been described as a stop signal using ultra-sensitive accelerometers embedded in the honeycomb located at the heart of honeybee colonies. We show that the signal is very common and highly repeatable, occurring mainly at night with a distinct decrease in instances towards midday, and that it can be elicited <i>en masse</i> from bees following the gentle shaking or knocking of their hive with distinct evidence of habituation. The results of our study suggest that this vibrational pulse is generated under many different circumstances, thereby unifying previous publication’s conflicting definitions, and we demonstrate that this pulse can be generated in response to a surprise stimulus. This work suggests that, using an artificial stimulus and monitoring the changes in the features of this signal could provide a sensitive tool to assess colony status.</p></div

Hourly Whooping signals occurrences with continuous rain.

<p>Central (top) and peripheral (bottom) accelerometers. Hourly rain is displayed in the central chart. Highlighted on all three plots is the 28^th October 2015.</p

Long-term evolution of the daily averaged spectrum of whooping signals.

<p>Data from Apr 18^th until Dec 25^th 2015 is shown, obtained after the subtraction of the background signal, which would otherwise produce a pronounced peak at 125Hz coming from the bees’ hum.</p

Distribution analysis for data coming from the central accelerometer.

<p><b>a</b>—Fundamental frequency distribution; <b>b</b>–The averaged spectrum of whooping signals with a specific amplitude displayed in descending order from highest (12 a.u.) to lowest (0 a.u.) amplitude Colour codes the measured amplitude in arbitrary units; <b>c</b>–Temporal histograms of whooping signals of a specific amplitude. Colour codes the likelihood of occurrences; <b>d</b>—Daily histogram of whooping signal fundamental frequencies.</p

Hourly number of whooping signals with weather.

<p>French dataset with corresponding: <b>a</b>—average outside temperature; <b>b</b>—cumulative rainfall, and <b>c</b>—average outside humidity. Red dots indicate the average number of whooping signals with black bars displaying ± 1 SE. The black curve on each graph shows the modal hourly whooping signals.</p

The time course and corresponding spectrogram of a typical honeybee whooping signal.

<p>The colour intensity of the spectrogram denotes the logarithmic amplitude of the measured acceleration with red being the highest acceleration and dark blue being the lowest.</p

Time course of the percentage of duplicated pulse detections on both channels.

<p>Dark blue is 0% duplications; yellow is 100% duplications. The modal daily accelerometer signal amplitude distribution is superimposed over the top, with a white line and acceleration given on the right hand side in mm/s².</p

Accelerometer configuration.

<p>A brood frame equipped with accelerometers in the centre and at the periphery, located in the centre of the hive. This photo was taken one year after installation, with accelerometers surrounded by honeycomb cells in near perfect condition. The photo shows the French set-up which is identical to the UK one.</p

Whooping signal hourly occurrences.

<p>Central (top) and peripheral (bottom) accelerometer logs of the French hive (2015 season). The colour codes the number of hourly occurrences from dark blue (≤1) to dark red (403 signals) on a logarithmic scale. White circles highlight the occurrences of the three swarms that occurred from this hive, with the first one being the primary swarm.</p

Outcome of training database following discrimination, from the 10 participants with the smallest error in prediction.

<p>Outcome of training database following discrimination, from the 10 participants with the smallest error in prediction.</p