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Not All Trees Sleep the Same—High Temporal Resolution Terrestrial Laser Scanning Shows Differences in Nocturnal Plant Movement

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Not All Trees Sleep the Same—High Temporal Resolution Terrestrial Laser Scanning Shows Differences in Nocturnal Plant Movement ORIGINAL RESEARCH published: 20 October 2017 doi: 10.3389/fpls.2017.01814 Not All Trees Sleep the Same—High Temporal Resolution Terrestrial Laser Scanning Shows Differences in Nocturnal Plant Movement András Zlinszky 1, 2*, Bence Molnár 3 and Anders S. Barfod 2 1 Balaton Limnological Institute, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany, Hungary, 2 Ecoinformatics and Biodiversity Section, Department of Bioscience, Aarhus University, Aarhus, Denmark, 3 Department of Photogrammetry and Geoinformatics, Budapest University of Technology and Economics, Budapest, Hungary Circadian leaf movements are widely known in plants, but nocturnal movement of tree branches were only recently discovered by using terrestrial laser scanning (TLS), a high resolution three-dimensional surveying technique. TLS uses a pulsed laser emitted in a regular scan pattern for rapid measurement of distances to the targets, thus producing three dimensional point cloud models of sub-centimeter resolution and accuracy in a few minutes. Here, we aim to gain an overview of the variability of circadian movement of small Edited by: Yann Guédon, trees across different taxonomic groups, growth forms and leaf anatomies. We surveyed Centre de Coopération Internationale a series of 18 full scans over a 12-h night period to measure nocturnal changes in shape en Recherche Agronomique pour le Développement (CIRAD), France simultaneously for an experimental setup of 22 plants representing different species. Reviewed by: Resulting point clouds were evaluated by comparing changes in height percentiles of Franck Hétroy-Wheeler, laser scanning points belonging to the canopy. Changes in crown shape were observed Université de Strasbourg, France for all studied trees, but clearly distinguishable sleep movements are apparently rare. Frédéric Boudon, Centre de Coopération Internationale Ambient light conditions were continuously dark between sunset (7:30 p.m.) and sunrise en Recherche Agronomique pour le (6:00 a.m.), but most changes in movement direction occurred during this period, thus Développement (CIRAD), France most of the recorded changes in crown shape were probably not controlled by ambient *Correspondence: András Zlinszky light. The highest movement amplitudes, for periodic circadian movement around 2 cm [email protected] were observed for Aesculus and Acer, compared to non-periodic continuous change in shape of 5 cm for Gleditschia and 2 cm for Fargesia. In several species we detected Specialty section: This article was submitted to 2–4 h cycles of minor crown movement of 0.5–1 cm, which is close to the limit of our Technical Advances in Plant Science, measurement accuracy. We present a conceptual framework for interpreting observed a section of the journal changes as a combination of circadian rhythm with a period close to 12 h, short-term Frontiers in Plant Science oscillation repeated every 2–4 h, aperiodic continuous movement in one direction and Received: 09 June 2017 Accepted: 05 October 2017 measurement noise which we assume to be random. Observed movement patterns Published: 20 October 2017 are interpreted within this framework, and connections with morphology and taxonomy Citation: are proposed. We confirm the existence of overnight “sleep” movement for some trees, Zlinszky A, Molnár B and Barfod AS but conclude that circadian movement is a variable phenomenon in plants, probably (2017) Not All Trees Sleep the Same—High Temporal Resolution controlled by a complex combination of anatomical, physiological, and morphological Terrestrial Laser Scanning Shows factors. Differences in Nocturnal Plant Movement. Front. Plant Sci. 8:1814. Keywords: circadian plant movement, laser scanning, tree canopy movement, 3-dimensional modeling, tree doi: 10.3389/fpls.2017.01814 physiology, turgor, chronobiology, circadian rhythm Frontiers in Plant Science | www.frontiersin.org 1 October 2017 | Volume 8 | Article 1814 Zlinszky et al. Not All Plants Sleep the Same INTRODUCTION Location and General Environment The experiment was carried out at a gardening shop at Circadian movement of leaves includes the process of nyctinasty, Balatonfüred, Western Hungary (N46◦56′16.91′′E17◦51′42.48′′), already known to the ancient Greeks (Bretzl, 1903) but first which has developed an open-air nursery for small-sized described by Darwin (Darwin and Darwin, 1880). The leaves container grown woody plants. The shrubs and young trees were of many shrubs and trees actively change position during the kept for at least half a year in the nursery, where they were night. In some fabaceous trees this phenomenon is particularly watered on a daily basis. All the plants included in this study striking. In a recent series of experiments by Puttonen et al. have thus been exposed to exactly the same weather and water (2016) terrestrial laser scanning (TLS) was applied to detect well- conditions for at least 6 months. To avoid the expected effect of defined circadian movement rhythm of the branches and the wind action we conducted the experiment in a greenhouse under trunk of the temperate tree Betula pendula. TLS (Dassot et al., construction, which had a glass roof, but no walls. During the 2011) allows for detailed measurement of the distance from full duration of the experiment weather conditions were stable sensor to a target object by measurement of the travel time of with no wind and no precipitation or condensation. The nearest short laser pulses emitted from a given position in a known streetlights were more than 1km away. During the overnight direction. Since the measurements are conducted during very experiment we made great effort to exclude all outdoor lights and short time (in the order of milliseconds), a high repetition rate is restrict the use of torch light to a minimum. A full moon allowed possible, which together with an equidistant scan pattern allows us to operate the scanner and read the instruments without an regular sampling of the target objects. The output of such a additional light source. measurement is a set of points with positioning coordinates and the amplitude of the reflected signal as an attribute. By employing Experiment Design and Studied Plants TLS, Puttonen et al. (2016) created detailed 3-dimensional The choice of plants was somewhat restricted to what was models of trees at hourly intervals during the night. Their results available to us at site. Nevertheless, we were able to include show that tree branches moved up to 8 cm downwards during in the experiment a broad range of growth forms (trees, the night and returned to their original position by daybreak. shrubs, bamboos, and palms), leaf phenologies (evergreen and By scanning two Betula trees nearly 2,000 km from each other, deciduous), leaf morphologies (entire, dissected, needle-shaped, they proved that this phenomenon is probably an attribute which and scaly), taxonomic groups, and ecoclimatic ranges (tropical, is unique to individual plant species. This seminal discovery subtropical, temperate). Although high priority was given to opened up many new questions. What is the adaptive advantage include tall and dense plants, the height was restricted by the of sleep movement (as Darwin called it and as we will also size of the containers. For most species we were unable to include call nocturnal changes in plant shape)? What are the processes more than one individual. governing sleep movements and how are these linked to ambient light, temperature, humidity, and soil water content? Are the Measurement Techniques movements driven by an internal circadian clock or induced Ambient Sensors and Instruments externally by photoperiodism? Are patterns of sleep movement Ambient air temperature and humidity were recorded by placing characteristic for certain taxonomic groups? six climate loggers on the trunks of six selected trees and Our aim is to gain an overview of the variability of plant near the LIDAR sensor (Easylog USBTM, Lascar ElectronicsR , circadian movement in seed plants. Our method measures UK), and temperature loggers (HOBO PendantTM) in the movement as the concerted displacement of branches and leaves. soil containers of the same trees. These were set to collect Under conditions monitored for light, humidity, temperature, data every 10 s. Wind speed was measured before each laser and (lack of) wind, we surveyed a wide taxonomic range of scanning measurement cycle using a simple hand-held ball trees and shrubs grown in containers. The experiment was set anemometer (Dwyer Instruments, Michigan City, IND, US). At up to compare sleep movement across taxonomic groups and the same time ambient light was recorded using a LabSphereTM different types of phenology and morphology. Advancing the integrating sphere mounted on a Li-CorTM data logger, within the methodology of nocturnal tree movement quantification was greenhouse frame as well as outside. outside the scope of this mainly qualitative study. Terrestrial Laser Scanning Instrument and Measurement Parameters MATERIALS AND METHODS Laser scanning can produce a high-density point cloud that allows for dynamic 3D modeling of complex shapes in few Measurement Setup minutes. For 3D data acquisition, a phase-based Terrestrial TM Timing Laser Scanner (TLS) was applied. FARO Focus S120 (FARO The study was carried out on 16–17 September 2016, close to the Technologies, Lake Mary, FL, US) operates a Class 3 laser autumn solstice when day and night are equally long. The first with 905 nm wavelength. Acquisition parameters were set to laser scanning was conducted at 6:30 p.m. and repeated every capture 7 × 109 points in 15min with highest quality. Based on 30min until 8:00 p.m. Hereafter, the scans were repeated every instruments data sheet (FARO, 2013), the distance measurement hour until 4:00 a.m. the next day. Finally a series of half-hourly has 0.95 mm accuracy on a solid, well-defined target while scans were conducted until 7:00a.m. angular deviation has ± 2 mm effect on accuracy at 25 m Frontiers in Plant Science | www.frontiersin.org 2 October 2017 | Volume 8 | Article 1814 Zlinszky et al.
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