Abstract
A recent increase in the use of unmanned aerial vehicles (UAVs)—also known as remotely piloted aircraft (RPA)—in the Antarctic in private, commercial and scientific sectors suggests that operational guidelines are urgently needed. One of the factors inhibiting adoption of such guidelines is the lack of knowledge about the impact of UAVs on wildlife. During the austral summer field season of 2014/15, data were gathered on the behavioural reactions to UAVs of Gentoo (Pygoscelis papua) and Adélie penguins (Pygoscelis adeliae), both resident breeding species on Ardley Island, King George Island, South Shetland Islands. A series of overflights at different altitudes above the nesting penguins were conducted with a small octocopter UAV, and their behaviour was recorded by video. Penguin behaviour altered as a result of the UAV flights, and behavioural reactions were more pronounced when the UAV was flown at lower altitudes. In Adélie penguins, behavioural reactions caused by the UAV were evident at the highest tested altitude of 50 m, while in Gentoo penguins reactions were evident from 30 m downwards. For both species, the reactions increased markedly when the UAV was flown at low altitudes of 10–20 m. Gentoo penguins showed significant reactions when the UAV was launched at distances closer than 20 m. There was some evidence of habituation to the UAV at some altitudes for horizontal flights, but no evidence of habituation in vertical flights.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
ATCM (2014) Final Report of the Thirty-seventh Antarctic Treaty Consultative Meeting Vol 1. Secretariat of the Antarctic Treaty, Brasilia, Brazil
ATCM (2015) Final Report of the Thirty-eighth Antarctic Treaty Consultative Meeting Vol 1. Secretariat of the Antarctic Treaty, Sofia, Bulgaria
ATCM (2018) Final Report of the Forty-first Antarctic Treaty Consultative Meeting—preliminary version Vol 1. Secretariat of the Antarctic Treaty, Buenos Aires, Argentina
Bhardwaj A, Sam L, Martín-Torres FJ, Kumar R (2016) UAVs as remote sensing platform in glaciology: present applications and future prospects. Remote Sens Environ 175:196–204. https://doi.org/10.1016/j.rse.2015.12.029
Braun C, Mustafa O, Nordt A, Pfeiffer S, Peter H-U (2012) Environmental monitoring and management proposals for the Fildes region (King George Island, Antarctica). Polar Res 31:18206. https://doi.org/10.3402/polar.v31i0.18206
Brown P (2008) Fundamentals of audio and acoustics. In: Ballou G (ed) Handbook for sound engineers, 4th edn. Elsevier Focal Press, Amsterdam, pp 21–40
Carney KM, Sydeman WJ (1999) A review of human disturbance effects on nesting colonial waterbirds. Waterbirds 22(1):68–79
Cavoukian A (2012) Privacy and drones: unmanned aerial vehicles. Information and Privacy Commissioner of Ontario, Ontario
Chrétien L-P, Théau J, Ménard P (2016) Visible and thermal infrared remote sensing for the detection of white-tailed deer using an unmanned aerial system. Wildl Soc Bull 40:181–191. https://doi.org/10.1002/wsb.629
COMNAP (2016) Antarctic unmanned aerial systems (UAS) operator’s handbook. Prepared by the COMNAP UAS Working Group. https://www.comnap.aq/Groups/Air/SharedDocuments/2Handbookdraft431March2016.pdf. Accessed 25 May 2018
Ditmer MA, Vincent JB, Werden LK, Tanner JC, Laske TG, Iaizzo PA, Garshelis DL, Fieberg JR (2015) Bears show a physiological but limited behavioral response to unmanned aerial vehicles. Curr Biol 25:2278–2283. https://doi.org/10.1016/j.cub.2015.07.024
Dulava S, Bean WT, Richmond OMW (2015) Environmental reviews and case studies: applications of unmanned aircraft systems (UAS) for waterbird surveys. Environ Pract 17:201–210. https://doi.org/10.1017/S1466046615000186
Durban JW, Moore MJ, Chiang G, Hickmott LS, Bocconcelli A, Howes G, Bahamonde PA, Perryman WL, LeRoi DJ (2016) Photogrammetry of blue whales with an unmanned hexacopter. Mar Mamm Sci. https://doi.org/10.1111/mms.12328
Ellenberg U, Mattern T, Seddon PJ (2006) Physiological and reproductive consequences of human disturbance in Humboldt penguins: the need for species-specific visitor management. Biol Cons 133(1):95–106
Fraser WR, Patterson DL (1997) Human disturbance and long-term changes in Adelie penguin populations: a natural experiment at Palmer Station, Antarctic Peninsula. In: Battaglia B (ed) Antarctic communities, species, structure and survival. University Press, Cambridge, pp 445–452
Germany (2018) Environmental guidelines for operation of remotely piloted aircraft systems (RPAS) in Antarctica. ATCM XLI, Buenos Aires
Giese M, Riddle M (1999) Disturbance of emperor penguin Aptenodytes forsteri chicks by helicopters. Polar Biol 22:366–371
Goebel ME, Perryman WL, Hinke JT, Krause DJ, Hann NA, Gardner S, LeRoi DJ (2015) A small unmanned aerial system for estimating abundance and size of Antarctic predators. Polar Biol 38:619–630. https://doi.org/10.1007/s00300-014-1625-4
Grenzdörffer G (2013) UAS-based automatic bird count of a common gull colony. Int Arch Photogramm Remote Sens Spat Inf Sci. https://doi.org/10.5194/isprsarchives-XL-1-W2-169-2013
Hänninen L, Pastell M (2009) CowLog: open source software for coding behaviors from digital video. Behav Res Methods 41(2):472–476
Hanson L, Holmquist-Johnson CL, Cowardin ML (2014) Evaluation of the Raven sUAS to detect and monitor greater sage-grouse leks within the Middle Park population. Open file report. Reston. https://doi.org/10.3133/ofr20141205
Harris CM (2005) Aircraft operations near concentrations of birds in Antarctica: the development of practical guidelines. Biol Cons 125:309–322. https://doi.org/10.1016/j.biocon.2005.04.002
Hockey PAR, Hallinan J (1981) Effect of human disturbance on the breeding behavior of Jackass Penguins Spheniscus demersus. S Afr J Wildl Res 11:59–62
Israel M (2011) A UAV-based roe deer fawn detection system. Int Arch Photogramm Remote Sens 38:1–5
Jouventin P (1982) Visual and vocal signals in penguins, their evolution and adaptive characters. Adv Ethol 24:148
Korczak-Abshire M, Kidawa A, Zmarz A, Storvold R, Karlsen SR, Rodzewicz M, Chwedorzewska K, Znój A (2016) Preliminary study on nesting Adélie penguins disturbance by unmanned aerial vehicles. CCAMLR Sci 23:1–16
Koski WR, Allen T, Ireland D, Buck G, Smith PR, Macrander AM, Halick MA, Rushing C, Sliwa DJ, McDonald TL (2009) Evaluation of an unmanned airborne system for monitoring marine mammals. Aquat Mamm 35:347
Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Package ‘lmerTest’ R package version 2
Liu C-C, Chen Y-H, Wen H-L (2015) Supporting the annual international black-faced spoonbill census with a low-cost unmanned aerial vehicle. Ecol Inform 30:170–178. https://doi.org/10.1016/j.ecoinf.2015.10.008
Lucieer A, Robinson S, Turner D, Harwin S, Kelcey J (2012) Using a micro-UAV for ultra-high resolution multi-sensor observations of Antarctic moss beds. Int Arch Photogramm Remote Sens Spat Inf Sci. https://doi.org/10.5194/isprsarchives-XXXIX-B1-429-2012
McEvoy JF, Hall GP, McDonald PG (2016) Evaluation of unmanned aerial vehicle shape, flight path and camera type for waterfowl surveys: disturbance effects and species recognition. PeerJ 4:e1831. https://doi.org/10.7717/peerj.1831
McGill PR, Reisenbichler KR, Etchemendy SA, Dawe TC, Hobson BW (2011) Aerial surveys and tagging of free-drifting icebergs using an unmanned aerial vehicle (UAV). Deep Sea Res Part II 58:1318–1326. https://doi.org/10.1016/j.dsr2.2010.11.007
Mulero-Pázmány M, Jenni-Eiermann S, Strebel N, Sattler T, Negro JJ, Tablado Z (2017) Unmanned aircraft systems as a new source of disturbance for wildlife: a systematic review. PLoS ONE 12(6):e0178448
Müller-Schwarze D, Müller-Schwarze C (1977) Pinguine. Die Neue Brehm-Bücherei, Wittenberg Lutherstadt
Mustafa O, Esefeld J, Hertel F, Krietsch J, Peter H-U, Pfeifer C, Rümmler M-C, Staeding A, et al. (2014) Mapping of Pygoscelis penguins by using an UAV in the vicinity of southwestern King George Island. Paper presented at the XXXIII SCAR open science conference Auckland, New Zealand
Mustafa O, Esefeld J, Grämer H, Maercker J, Peter H-U, Rümmler M-C, Senf M, Pfeifer C (2017) Monitoring penguin colonies in the Antarctic using remote sensing data. On behalf of the German Environment Agency. Dessau-Roßlau. https://www.umweltbundesamt.de/publikationen/monitoring-penguin-colonies-in-the-antarctic-using
Peasgood S, Valentin M (2015) Drones: a rising market. An industry to lift your returns. Sophic capital
Pomeroy P, O’Connor L, Davies P (2015) Assessing use of and reaction to unmanned aerial systems in gray and harbor seals during breeding and molt in the UK. J Unmanned Veh Syst 3:102–113. https://doi.org/10.1139/juvs-2015-0013
R Development Core Team (2008) R: A language and environment for statistical computing R foundation for statistical computing
Ratcliffe N, Guihen D, Robst J, Crofts S, Stanworth A, Enderlein P (2015) A protocol for the aerial survey of penguin colonies using UAVs. J Unmanned Veh Syst 3:95–101. https://doi.org/10.1139/juvs-2015-0006
RStudio Team (2016). RStudio: integrated development for R. RStudio, Inc., Boston. http://www.rstudio.com/
Rümmler M-C, Mustafa O, Maercker J, Peter H-U, Esefeld J (2016) Measuring the influence of unmanned aerial vehicles on Adélie penguins. Pol Biol 39:1329–1334. https://doi.org/10.1007/s00300-015-1838-1
Schuster KC (2010) Impact of human and other disturbance on behaviour and heart rate of incubating Adélie penguins (Pygoscelis adeliae). Dissertation, Philips-Universität Marburg
Thomson RB (1977) Effects of human disturbance on an Adélie penguin rookery and measures of control. In: Llano GA (ed) Adaptations within Antarctic ecosystems. Smithsonian Institution, Washington, pp 1177–1180
Van Zinderen Bakker EM, Winterbottom JM, Dyer RA (1971) A behaviour analysis of the Gentoo penguin. In: Marion and Prince Edward Islands. Report on the south african biological and geological expedition/1965–1966. Balkema, Cape Town, p 251–272
Vas E et al (2015) Approaching birds with drones: first experiments and ethical guidelines. Biol Lett 11(2):20140754
Vermeulen C, Lejeune P, Lisein J, Sawadogo P, Bouché P (2013) Unmanned aerial survey of elephants. PLoS ONE 8:e54700. https://doi.org/10.1371/journal.pone.0054700
Weimerskirch H, Prudor A, Schull Q (2018) Flights of drones over sub-Antarctic seabirds show species-and status-specific behavioural and physiological responses. Pol Biol 41(2):259–266
Wilson RP, Coria NR, Spairani HJ, Adelung D, Culik B (1989) Human-induced behaviour in Adélie penguins Pygoscelis adeliae. Pol Biol 10:77–80
Acknowledgements
We would like to thank the personnel of the Bellingshausen Station for accommodation and support during our expedition. Logistic support was kindly provided by Alejo Contreras and Aerovias DAP on-site and by Alfred-Wegener-Institute, in general. We also would like to thank Dr. Markus Bernhardt-Römermann for valuable advices on statistical analysis and Colin Harris for extensive language editing.
Funding
The study was funded by the Federal Ministry for the Environment, Nature Conservation, Building and Nuclear Safety (UFOPLAN 3713 12 101).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The study was commissioned by the German Environment Agency, Dessau-Rosslau. All applicable international, national and/or institutional guidelines for the care and use of animals were followed. Permissions to enter ASPA No. 150 were given by the responsible authority.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
300_2018_2385_MOESM1_ESM.tif
Example of a flight scenario. Shown is a horizontal overflight (GPS-tracked flight path, red) on an elevation model of Ardley Island with the breeding groups of the colony (orange), the observed breeding group G1 (light blue), the analysed part of the breeding group (focal group/individuals, dark blue) and the position of the recording camera. Supplementary material 1 (TIFF 1003 kb)
300_2018_2385_MOESM2_ESM.tif
Boxplots of the disturbance index of individuals as defined in Table 2 for Gentoo (left) and Adélie (right) penguins (Pygoscelis papua/P. adeliae) during overflights in horizontal (bottom) and vertical (top) flight modes. The area shaded grey indicates undisturbed behaviour. The data is jittered with a factor of 0.1 to improve visibility of the boxplot features. An increase in observed disturbed behaviours with lowering flight altitudes can be seen for all four scenarios. Supplementary material 2 (TIFF 183 kb)
300_2018_2385_MOESM3_ESM.tif
Boxplots of the disturbance index of Gentoo penguins (Pygoscelis papua) during the take-off experiments. The data is jittered with a factor of 0.1 to improve visibility of the boxplot features. A gradual increase in disturbance can be seen from distances of 20 m to the closest distance at 5 m. At distances farther than 30 m no further decrease is evident. Supplementary material 3 (TIFF 132 kb)
300_2018_2385_MOESM4_ESM.tif
Boxplots of habituation to fly-overs above Adélie and Gentoo penguins (Pygoscelis adeliae/P. papua). For each altitude separately, the proportion of individuals showing disturbed behaviour of each of the three flights per day is shown. Altitudes with statistically significant habituation effects are marked with asterisk. Supplementary material 4 (TIFF 607 kb)
300_2018_2385_MOESM5_ESM.tif
Boxplots of influence of seasonality on the reaction of Adélie and Gentoo penguins (Pygoscelis adeliae/P. papua) to horizontal and vertical overflights. The proportion of individuals showing disturbed behaviour is given for each observation day. Supplementary material 5 (TIFF 161 kb)
Rights and permissions
About this article
Cite this article
Rümmler, MC., Mustafa, O., Maercker, J. et al. Sensitivity of Adélie and Gentoo penguins to various flight activities of a micro UAV. Polar Biol 41, 2481–2493 (2018). https://doi.org/10.1007/s00300-018-2385-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-018-2385-3