Abstract
Regular light–dark cycles greatly affect organisms, and events like eclipses induce distinctive physiological and behavioural shifts. While well documented in animals, plant behaviour during eclipses remains largely unexplored. Here, we monitored multiple spruce trees to assess their individual and collective bioelectrical responses to a solar eclipse. Trees anticipated the eclipse, synchronizing their bioelectrical behaviour hours in advance. Older trees displayed greater anticipatory behaviour with early time-asymmetry and entropy increases. These results reveal a relationship between trees, shaped by individual age and physiology as well as collective history. This highlights the significance of synchrony in plants, offering new insights into coordinated behaviours in nature.
Introduction
Sunlight and its periodicity drive global weather patterns, seasons and climate and make life possible on our planet. Daily and seasonal cycles of natural light organize biological systems by synchronizing their internal clock with the geophysical cycles of the Earth.
At a time marked by growing human-induced changes to natural cycles, unusual astronomical events such as eclipses effectively function as natural experiments, providing valuable insights into how living organisms respond to sudden and infrequent changes in their environment. Even with their infrequent and momentary occurrence, eclipses and their impact on organismal behaviour have been observed for millennia and are now well documented. In humans, for example, solar eclipses have played a transformative role inspiring awe and arousing social cohesion and prosocial tendencies, even capable of ending wars . Heightened tendencies of individuals to form collectives by huddling, gathering and synchronizing group movements during solar eclipses are also seen across several terrestrial and aquatic animal groups . These coordinated behaviours during eclipses suggest a potential role in enhancing survival chances for individuals and their groups. While these events may not pose an immediate threat to survival, they elicit adaptive responses that reflect broader strategies for coping with sudden and unpredictable environmental changes. Such behaviours likely evolved as mechanisms to reduce individual vulnerability by enhancing group vigilance and coordination in uncertain situations . These responses can increase the resilience of both individuals and groups to environmental perturbations. If solar eclipses play such a vital role in shaping individuals and their groups to ensure collective survival across species, it is remarkable that very little is known about how plants respond to these astronomical events and such knowledge is limited to responses at the individual level , overlooking that group behaviour is also observed in plants.
In this study, we leverage our newly developed remote measurement system to simultaneously monitor multiple trees in a forest. This allows us to directly test whether and to what extent individual trees respond to a solar eclipse together, functioning as a larger living collective. We investigated the electrical signals (electrome) of spruce trees (Picea abies) to characterize their bioelectrical activity during a partial solar eclipse that occurred in a forest located in the Dolomites mountain region, northeastern Italy.
Figure 1. Experimental set-up to simultaneously monitor the electrome of multiple trees during solar eclipse. (A) The location of the experimental site at the Costa Bocche forest near Paneveggio in the Dolomites area, Italy. (B) Diagram of the Saros 124 event, the solar eclipse that occurred on 25 October 2022. Green continuous lines trace the Sun’s shadow at ground level; the dashed line corresponds to a coverage of 50% of the Sun’s disc and the pink line to the Sun’s path. Eclipse predictions by Fred Espenak, NASA’s GSFC. (C) In situ installation of 10 xylematic electrodes (labelled with Greek letters) on a spruce tree. Stainless steel threaded rods of 6 mm diameter were spaced 50 cm apart along the trunk and in contact with the core of the tree. Each electrode was then connected to the CyberTree devices via low-impedance audio cables. (D) Horizontal view of the phloematic configuration with electrodes in contact with the superficial layer of the tree and radially arranged in two arrays: (i) one array was located at 1 m above ground with electrodes at a radial distance of 60° from each other; and (ii) the other array was located at 3 m above ground with electrodes at a radial distance of 90° from each other. Cardinal and ordinal directions are indicated.
The word electrome refers to the collection of electrical activities generated by living cells or tissues in an organism, encompassing all bioelectrical signals, such as action potentials, ion channel activities and electrical potentials across membranes. It is analogous to terms like ‘genome’ or ‘proteome’, but specifically focuses on the electrical properties and phenomena within biological systems. A biological signal like those within the electrome is an active, functional electrical or biochemical process that originates within an organism and is used for communication or coordination within the organism’s body. Biological signals are a subset of the electrome ensemble. Electrome dynamics enable plants to coordinate various physiological functions for rapid response to environmental changes. These dynamics exhibit non-random behaviour, long-range temporal correlations and persistence , suggesting a potential role in long-distance signalling. The studies by Saraiva et al. and Souza et al., which focused on electrical signalling in individual plants under conditions like osmotic stimuli and temperature variations, provide foundational insights into the plant electrome dynamics. These insights suggest that trees may coordinate physiological responses to environmental changes, including unique disturbances like those caused by a solar eclipse. This supports our hypothesis that by monitoring electrome changes during the eclipse, we can identify distinct stages of a coordinated behavioural response. In a previous study within this forest, we established methods for measuring, analysing and sorting electrome dynamics of spruce trees at different stages (healthy young, healthy old, logs) and found correlations with solar (and lunar) cycles, while other studies related the electrome of pine trees to meteorological and geomagnetic parameters. Building on this knowledge, we hypothesize that by monitoring electrome changes during the eclipse, we can identify the distinct stages of a behavioural response to a specific event, like a solar eclipse.
Read the full article at Royal Society Open Science.
