Scientific Papers

Classification of African ground pangolin behaviour based on accelerometer readouts: validation of bio-logging methods | Animal Biotelemetry


  • Shepard ELC, Wilson RP, Quintana F, Laich AG, Liebsch N, Albareda DA, et al. Identification of animal movement patterns using tri-axial accelerometry. Endanger Species Res. 2008;10:47–60.

    Article 

    Google Scholar
     

  • Snell-Rood EC. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav. 2013;85(5):1004–11.

    Article 

    Google Scholar
     

  • Moiron M, Laskowski KL, Niemelä PT. Individual differences in behaviour explain variation in survival: a meta-analysis. Ecol Lett. 2020;23(2):399–408.

    Article 
    PubMed 

    Google Scholar
     

  • Sumpter DJT, Broomhead DS. Relating individual behaviour to population dynamics. Proc R Soc Lond B. 2001;268(1470):925–32.

    Article 
    CAS 

    Google Scholar
     

  • Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA, et al. Building the bridge between animal movement and population dynamics. Philos Trans R Soc B. 2010;365(1550):2289–301.

    Article 

    Google Scholar
     

  • Wilson MW, Ridlon AD, Gaynor KM, Gaines SD, Stier AC, Halpern BS. Ecological impacts of human-induced animal behaviour change. Ecol Lett. 2020;23(10):1522–36.

    Article 
    PubMed 

    Google Scholar
     

  • Buchholz R. Behavioural biology: an effective and relevant conservation tool. Trends Ecol Evol. 2007;22(8):401–7.

    Article 
    PubMed 

    Google Scholar
     

  • Roever CL, Beyer HL, Chase MJ, van Aarde RJ. The pitfalls of ignoring behaviour when quantifying habitat selection. Divers Distrib. 2014;20(3):322–33.

    Article 

    Google Scholar
     

  • Matthews SG, Miller AL, Clapp J, Plötz T, Kyriazakis I. Early detection of health and welfare compromises through automated detection of behavioural changes in pigs. Vet J. 2016;217:43–51.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. Observing the unwatchable through acceleration logging of animal behavior. Anim Biotelem. 2013;1(1):1–16.

    Article 

    Google Scholar
     

  • Hughey LF, Hein AM, Strandburg-Peshkin A, Jensen FH. Challenges and solutions for studying collective animal behaviour in the wild. Philos Trans R Soc B. 2018;373(1746):20170005.

    Article 

    Google Scholar
     

  • Lush L, Ellwood S, Markham A, Ward AI, Wheeler P. Use of tri-axial accelerometers to assess terrestrial mammal behaviour in the wild. J Zool. 2016;298(4):257–65.

    Article 

    Google Scholar
     

  • Hays GC. New insights: animal-borne cameras and accelerometers reveal the secret lives of cryptic species. J Anim Ecol. 2015;84(3):587–9.

    Article 
    PubMed 

    Google Scholar
     

  • Desbiez ALJ, Kluyber D, Massocato GF, Attias N. Methods for the characterization of activity patterns in elusive species: the giant armadillo in the Brazilian Pantanal. J Zool. 2021;315(4):301–12.

    Article 

    Google Scholar
     

  • Canine NG. Unrecognized anti-predator behaviour can bias observational data. Anim Behav. 1990;39(1):195–7.

    Article 

    Google Scholar
     

  • Wade MR, Zalucki MP, Franzmann BA. Influence of observer presence on pacific damsel bug behavior: who is watching whom? J Insect Behav. 2005;18(5):651–67.

    Article 

    Google Scholar
     

  • Wilmers CC, Nickel B, Bryce CM, Smith JA, Wheat RE, Yovovich V. The golden age of bio-logging: how animal-borne sensors are advancing the frontiers of ecology. Ecology. 2015;96(7):1741–53.

    Article 
    PubMed 

    Google Scholar
     

  • O’Connell AF, Nichols JD, Karanth KU. Camera traps in animal ecology: methods and analyses, vol. 271. Berlin: Springer; 2011.

    Book 

    Google Scholar
     

  • Pettorelli N, Laurance WF, O’Brien TG, Wegmann M, Nagendra H, Turner W. Satellite remote sensing for applied ecologists: opportunities and challenges. J Appl Ecol. 2014;51(4):839–48.

    Article 

    Google Scholar
     

  • Infantes E, Carroll D, Silva WTAF, Härkönen T, Edwards SV, Harding KC. An automated work-flow for pinniped surveys: a new tool for monitoring population dynamics. Front Ecol Evol. 2022;10:905309. https://doi.org/10.3389/fevo.2022.905309.

  • Carroll D, Infantes E, Pagan EV, Harding KC. Approaching a population‐level assessment of body size in pinnipeds using drones, an early warning of environmental degradation. Remote Sens Ecol Conserv. 2024.

  • Whitford M, Klimley AP. An overview of behavioral, physiological, and environmental sensors used in animal biotelemetry and biologging studies. Anim Biotelem. 2019;7(1):26.

    Article 

    Google Scholar
     

  • Nathan R, Spiegel O, Fortmann-Roe S, Harel R, Wikelski M, Getz WM. Using tri-axial acceleration data to identify behavioral modes of free-ranging animals: general concepts and tools illustrated for griffon vultures. J Exp Biol. 2012;215(6):986–96.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leos-Barajas V, Photopoulou T, Langrock R, Patterson TA, Watanabe YY, Murgatroyd M, et al. Analysis of animal accelerometer data using hidden Markov models. Methods Ecol Evol. 2017;8(2):161–73.

    Article 

    Google Scholar
     

  • Williams HJ, Taylor LA, Benhamou S, Bijleveld AI, Clay TA, de Grissac S, et al. Optimizing the use of biologgers for movement ecology research. J Anim Ecol. 2020;89(1):186–206.

    Article 
    PubMed 

    Google Scholar
     

  • Collins PM, Green JA, Warwick-Evans V, Dodd S, Shaw PJA, Arnould JPY, et al. Interpreting behaviors from accelerometry: a method combining simplicity and objectivity. Ecol Evol. 2015;5(20):4642–54.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Soulsbury CD, Gray HE, Smith LM, Braithwaite V, Cotter SC, Elwood RW, et al. The welfare and ethics of research involving wild animals: a primer. Methods Ecol Evol. 2020;11(10):1164–81.

    Article 

    Google Scholar
     

  • Hounslow JL, Brewster LR, Lear KO, Guttridge TL, Daly R, Whitney NM, et al. Assessing the effects of sampling frequency on behavioural classification of accelerometer data. J Exp Mar Biol Ecol. 2019;512:22–30.

    Article 

    Google Scholar
     

  • Yan RC, Wilson RP. Subjectivity in bio-logging science: do logged data mislead? Mem Natl Inst Polar Res Spec Issue. 2004;58:23–33.


    Google Scholar
     

  • Kölzsch A, Neefjes M, Barkway J, Müskens GJDM, Van Langevelde F, De Boer WF, et al. Neckband or backpack? Differences in tag design and their effects on GPS/accelerometer tracking results in large waterbirds. Anim Biotelem. 2016;4(1):13.

    Article 

    Google Scholar
     

  • Garde B, Wilson RP, Fell A, Cole N, Tatayah V, Holton MD, et al. Ecological inference using data from accelerometers needs careful protocols. Methods Ecol Evol. 2022;13(4):813–25.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • IUCN. The IUCN red list of threatened species. 2023. Version 2023-1.

  • Heinrich S, Wittmann TA, Prowse TAA, Ross JV, Delean S, Shepherd CR, et al. Where did all the pangolins go? International CITES trade in pangolin species. Glob Ecol Conserv. 2016;8:241–53.


    Google Scholar
     

  • Ingram DJ, Coad L, Abernethy KA, Maisels F, Stokes EJ, Bobo KS, et al. Assessing Africa-Wide Pangolin exploitation by scaling local data. Conserv Lett. 2018;11(2):1–9.

    Article 

    Google Scholar
     

  • Ingram DJ, Cronin DT, Challender DWS, Venditti DM, Gonder MK. Characterising trafficking and trade of pangolins in the Gulf of Guinea. Glob Ecol Conserv. 2019;17:e00576.


    Google Scholar
     

  • Wright, N., Jimerson, J. The rescue, rehabilitation and release of pangolins in Pangolins: Science, Society and Conservation. Challender, D. W. S., Nash, H. C., Waterman, C., Nyhus, P. J, editors. Academic Press; 2020. p. 495–504.

  • Nash H, Lee PB, Low MR. Rescue, rehabilitation and release of Sunda pangolins in Singapore. In: Global reintroduction perspectives: 2018 case studies from around the globe. Soorae, P. S, editor. IUCN/SSC Reintroduction Specialist Group, Gland, Switzerland and Environment Agency. Abu Dhabi, UAE; 2018. p. 221-225.

  • Carroll D, Harvey-Carroll J, Trivella CM, Connelly E. Non-fatal removal of ground pangolin (Smutsia temminckii Smuts, 1832) tracking devices by predators. Afr J Ecol. 2023;62:e13225.

  • Pavese S, Centeno C, Von Fersen L, Eguizábal GV, Donet L, Asencio CJ, et al. Video validation of tri-axial accelerometer for monitoring zoo-housed Tamandua tetradactyla activity patterns in response to changes in husbandry conditions. Animals. 2022;12(19):2516.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Auge AC, Blouin-Demers G, Murray DL. Developing a classification system to assign activity states to two species of freshwater turtles. PLoS ONE. 2022;17(11):e0277491.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clark BL. Northern gannet Morus bassanus foraging ecology: a multidimensional approach. Exeter: University of Exeter; 2019.


    Google Scholar
     

  • Clark B, Irigoin-Lovera C, Gonzales-DelCarpio D, Diaz-Santibañez I, Votier S, Zavalaga C. Interactions between anchovy fisheries and Peruvian boobies revealed by bird-borne cameras and movement loggers. Mar Ecol Prog Ser. 2022;701:145–57.

    Article 

    Google Scholar
     

  • Reisinger RR, Corney S, Raymond B, Lombard AT, Bester MN, Crawford RJM, et al. Habitat model forecasts suggest potential redistribution of marine predators in the southern Indian Ocean. Divers Distrib. 2022;28(1):142–59.

    Article 

    Google Scholar
     

  • Reisinger RR, Raymond B, Hindell MA, Bester MN, Crawford RJM, Davies D, et al. Habitat modelling of tracking data from multiple marine predators identifies important areas in the Southern Indian Ocean. Divers Distrib. 2018;24(4):535–50.

    Article 

    Google Scholar
     

  • Kuhn M. A Short Introduction to the caret package. R Found Stat Comput. 2015;1:1–10.


    Google Scholar
     

  • Wright MN, Ziegler A. ranger: a fast implementation of random forests for high dimensional data in C++ and R. J Stat Softw. 2017;77:1–17.

    Article 

    Google Scholar
     

  • Friard O, Gamba M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol. 2016;7(11):1325–30.

    Article 

    Google Scholar
     

  • R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2024.

  • Zeileis A, Grothendieck G. zoo: S3 infrastructure for regular and irregular time series. J Stat Softw. 2005;14(6):1–27.

    Article 

    Google Scholar
     

  • Grolemund G, Wickham H. Dates and times made easy with lubridate. J Stat Softw. 2011;40(3):1–25.

    Article 

    Google Scholar
     

  • Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer; 2016.

    Book 

    Google Scholar
     

  • Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, et al. Welcome to the tidyverse. J Open Source Softw. 2019;4(43):1686.

    Article 

    Google Scholar
     

  • Wickham H, François R, Henry L, Müller K, Vaughan D. dplyr: a grammar of data manipulation. R package version 1.1.4. 2023.

  • Barrett T, Dowle M, Srinivasan A, Gorecki J, Chirico M, Hocking T. data.table: Extension of ‘data.frame’. R package version 1.15.0. 2024.

  • Kuhn, M. Building Predictive Models in R Using the caret Package. Journal of Statistical Software, 2008;28(5), 1–26.

  • Jeantet L, Dell’Amico F, Forin-Wiart MA, Coutant M, Bonola M, Etienne D, et al. Combined use of two supervised learning algorithms to model sea turtle behaviours from tri-axial acceleration data. J Exp Biol. 2018;221(10): jeb177378.

  • Kirchner TM, Devineau O, Chimienti M, Thompson DP, Crouse J, Evans AL, et al. Predicting moose behaviors from tri-axial accelerometer data using a supervised classification algorithm. Anim Biotelem. 2023;11(1):32.

    Article 

    Google Scholar
     

  • Tatler J, Cassey P, Prowse TAA. High accuracy at low frequency: detailed behavioural classification from accelerometer data. J Exp Biol. 2018;221 (23): jeb184085.

  • Price E, Langford J, Fawcett TW, Wilson AJ, Croft DP. Classifying the posture and activity of ewes and lambs using accelerometers and machine learning on a commercial flock. Appl Anim Behav Sci. 2022;251:105630.

    Article 

    Google Scholar
     

  • Rautiainen H, Alam M, Blackwell PG, Skarin A. Identification of reindeer fine-scale foraging behaviour using tri-axial accelerometer data. Mov Ecol. 2022;10(1):40.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Walton E, Casey C, Mitsch J, Vázquez-Diosdado JA, Yan J, Dottorini T, et al. Evaluation of sampling frequency, window size and sensor position for classification of sheep behaviour. R Soc Open Sci. 2018;5(2):171442.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Broell F, Noda T, Wright S, Domenici P, Steffensen JF, Auclair JP, et al. Accelerometer tags: detecting and identifying activities in fish and the effect of sampling frequency. J Exp Biol. 2013;216(Pt 7):1255–64.

    PubMed 

    Google Scholar
     

  • Yu H, Muijres FT, te Lindert JS, Hedenström A, Henningsson P. Accelerometer sampling requirements for animal behaviour classification and estimation of energy expenditure. Anim Biotelem. 2023;11(1):28.

    Article 

    Google Scholar
     

  • Graf PM, Wilson RP, Qasem L, Hackländer K, Rosell F. The use of acceleration to code for animal behaviours; a case study in free-ranging Eurasian beavers castor fiber. PLoS ONE. 2015;10(8):e0136751.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dentinger JE, Börger L, Holton MD, Jafari-Marandi R, Norman DA, Smith BK, et al. A probabilistic framework for behavioral identification from animal-borne accelerometers. Ecol Model. 2022;464:109818.

    Article 

    Google Scholar
     

  • Pietersen DW, McKechnie AE, Jansen R. Home range, habitat selection and activity patterns of an arid-zone population of Temminck’s ground pangolins, Smutsia temminckii. Afr Zool. 2014;49(2):265–76.


    Google Scholar
     

  • Richer R, Coulson I, Heath M. Foraging behaviour and ecology of the Cape pangolin (Manis temminckii) in north-western Zimbabwe. Afr J Ecol. 1997;35(4):361–9.

    Article 

    Google Scholar
     

  • Gaubert P, Wilson D, Mittermeier R. Family manidae. In: Handbook of the Mammals of the World, vol.2. Wilson DE, Mittermeier RA, editors. Lynx Edicions; 2011. p. 82–103.


    Google Scholar
     

  • Swart J. Smutsia temminckii Ground pangolin. In: Mammals of Africa, vol. V, carnivores, pangolins, equids, rhinoceroses. Kingdon J, Hoffmann M, editors.  London: Bloomsbury Publishing; 2013. p. 400–405.

  • Panaino W, Parrini F, Kamerman PR, Hetem RS, Meyer LCR, Smith D, et al. Temminck’s pangolins relax the precision of body temperature regulation when resources are scarce in a semi-arid environment. Conserv Physiol. 2023;11(1):coad068.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Champagnon J, Elmberg J, Guillemain M, Gauthier-Clerc M, Lebreton JD. Conspecifics can be aliens too: a review of effects of restocking practices in vertebrates. J Nat Conserv. 2012;20(4):231–41.

    Article 

    Google Scholar
     

  • Harrington LA, Moehrenschlager A, Gelling M, Atkinson RPD, Hughes J, Macdonald DW. Conflicting and complementary ethics of animal welfare considerations in reintroductions. Conserv Biol. 2013;27(3):486–500.

    Article 
    PubMed 

    Google Scholar
     

  • Molony SE, Dowding CV, Baker PJ, Cuthill IC, Harris S. The effect of translocation and temporary captivity on wildlife rehabilitation success: an experimental study using European hedgehogs (Erinaceus europaeus). Biol Conserv. 2006;130(4):530–7.

    Article 

    Google Scholar
     

  • Ewen JG, Armstrong DP, Parker KA, Seddon PJ, editors. Reintroduction biology: integrating science and management. 1st ed. Hoboken: Wiley; 2012.


    Google Scholar
     

  • Mihoub J, Le Gouar P, Sarrazin F. Breeding habitat selection behaviors in heterogeneous environments: implications for modeling reintroduction. Oikos. 2009;118(5):663–74.

    Article 

    Google Scholar
     

  • Scillitani L, Darmon G, Monaco A, Cocca G, Sturaro E, Rossi L, et al. Habitat selection in translocated gregarious ungulate species: an interplay between sociality and ecological requirements. J Wildl Manag. 2013;77(4):761–9.

    Article 

    Google Scholar
     

  • Richardson KM, Ewen JG. Habitat selection in a reintroduced population: social effects differ between natal and post-release dispersal. Anim Conserv. 2016;19(5):413–21.

    Article 

    Google Scholar
     

  • Picardi S, Coates P, Kolar J, O’Neil S, Mathews S, Dahlgren D. Behavioural state-dependent habitat selection and implications for animal translocations. J Appl Ecol. 2022;59(2):624–35.

    Article 

    Google Scholar
     

  • Silva WT, Harding KC, Marques GM, Bäcklin BM, Sonne C, Dietz R, et al. Life cycle bioenergetics of the gray seal (Halichoerus grypus) in the Baltic Sea: population response to environmental stress. Environ Int. 2020;145:106145.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Heighton SP, Gaubert P. A timely systematic review on pangolin research, commercialization, and popularization to identify knowledge gaps and produce conservation guidelines. Biol Conserv. 2021;256:109042.

    Article 

    Google Scholar
     

  • Zanvo S, Djagoun CAMS, Gaubert P, Azihou AF, Jézéquel C, Djossa B, et al. Modeling population extirpation rates of white-bellied and giant pangolins in Benin using validated local ecological knowledge. Conserv Sci Pract. 2023;5(8):e12986.

    Article 

    Google Scholar
     

  • Carroll D, Ahola MP, Carlsson AM, Sköld M, Harding KC. 120-years of ecological monitoring data shows that the risk of overhunting is increased by environmental degradation for an isolated marine mammal population: the Baltic grey seal. J Anim Ecol. 2024;93:525–39.

    Article 
    PubMed 

    Google Scholar
     



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