The golden age of bio-logging: how animal-borne sensors are advancing the frontiers of ecology.

Great leaps forward in scientific understanding are often spurred by innovations in technology. The explosion of miniature sensors that are driving the boom in consumer electronics, such as smart phones, gaming platforms, and wearable fitness devices, are now becoming available to ecologists for remotely monitoring the activities of wild animals. While half a century ago researchers were attaching balloons to the backs of seals to measure their movement, today ecologists have access to an arsenal of sensors that can continuously measure most aspects of an animal's state (e.g., location, behavior, caloric expenditure, interactions with other animals) and external environment (e.g., temperature, salinity, depth). This technology is advancing our ability to study animal ecology by allowing researchers to (1) answer questions about the physiology, behavior, and ecology of wild animals in situ that would have previously been limited to tests on model organisms in highly controlled settings, (2) study cryptic or wide-ranging animals that have previously evaded investigation, and (3) develop and test entirely new theories. Here we explore how ecologists are using these tools to answer new questions about the physiological performance, energetics, foraging, migration, habitat selection, and sociality of wild animals, as well as collect data on the environments in which they live.

[1]  Mark S. Boyce,et al.  Evaluating Global Positioning System Telemetry Techniques for Estimating Cougar Predation Parameters , 2009 .

[2]  Torkel Gissel Nielsen,et al.  A whale of an opportunity: Examining the vertical structure of chlorophyll-a in high Arctic waters using instrumented marine predators , 2010 .

[3]  S. Sokolov,et al.  Tracking the Polar Front south of New Zealand using penguin dive data , 2006 .

[4]  Akinori Takahashi,et al.  Testing optimal foraging theory in a penguin–krill system , 2014, Proceedings of the Royal Society B: Biological Sciences.

[5]  Young-Hyang Park,et al.  Penguins as oceanographers unravel hidden mechanisms of marine productivity , 2002 .

[6]  Jan-Åke Nilsson,et al.  Patterns of Animal Migration , 2014 .

[7]  D. Zinner,et al.  Male tolerance and male–male bonds in a multilevel primate society , 2014, Proceedings of the National Academy of Sciences.

[8]  Melissa S. Bowlin,et al.  Mechanistic principles of locomotion performance in migrating animals , 2011 .

[9]  V. Yovovich,et al.  Scale Dependent Behavioral Responses to Human Development by a Large Predator, the Puma , 2013, PloS one.

[10]  Emmanuelle Autret,et al.  Animal‐borne sensors successfully capture the real‐time thermal properties of ocean basins , 2005 .

[11]  Daniel P. Costa,et al.  Upper ocean variability in west Antarctic Peninsula continental shelf waters as measured using instrumented seals , 2008 .

[12]  Mark Hebblewhite,et al.  A MULTI-SCALE TEST OF THE FORAGE MATURATION HYPOTHESIS IN A PARTIALLY MIGRATORY UNGULATE POPULATION , 2008 .

[13]  W. Getz,et al.  Trophic facilitation by introduced top predators: grey wolf subsidies to scavengers in Yellowstone National Park , 2003 .

[14]  Alan M. Wilson,et al.  Locomotion dynamics of hunting in wild cheetahs , 2013, Nature.

[15]  Terje Gobakken,et al.  Improving broad scale forage mapping and habitat selection analyses with airborne laser scanning: the case of moose , 2014 .

[16]  S. Cooke Biotelemetry and biologging in endangered species research and animal conservation: relevance to regional, national, and IUCN Red List threat assessments , 2008 .

[17]  Christian Rutz,et al.  New frontiers in biologging science , 2009, Biology Letters.

[18]  Young-Hyang Park,et al.  Fine resolution 3D temperature fields off Kerguelen from instrumented penguins , 2004 .

[19]  Horst Bornemann,et al.  All at sea with animal tracks; methodological and analytical solutions for the resolution of movement , 2007 .

[20]  Jeffrey D. Brawn,et al.  Meta‐analysis of transmitter effects on avian behaviour and ecology , 2010 .

[21]  Akinori Takahashi,et al.  Linking animal-borne video to accelerometers reveals prey capture variability , 2013, Proceedings of the National Academy of Sciences.

[22]  Tal Avgar,et al.  Towards an energetic landscape: broad-scale accelerometry in woodland caribou. , 2014, The Journal of animal ecology.

[23]  Pascal Monestiez,et al.  Can We Predict Foraging Success in a Marine Predator from Dive Patterns Only? Validation with Prey Capture Attempt Data , 2014, PloS one.

[24]  J. Andrew Royle,et al.  Spatially explicit models for inference about density in unmarked or partially marked populations , 2011, 1112.3250.

[25]  A. Hedenström,et al.  Migration and flight strategies in animals : new insights from tracking migratory journeys , 2014 .

[26]  Daniel P. Costa,et al.  Seals map bathymetry of the Antarctic continental shelf , 2010 .

[27]  Matthew Rutishauser,et al.  Movement, resting, and attack behaviors of wild pumas are revealed by tri-axial accelerometer measurements , 2015, Movement ecology.

[28]  Atle Mysterud,et al.  A Migratory Northern Ungulate in the Pursuit of Spring: Jumping or Surfing the Green Wave? , 2012, The American Naturalist.

[29]  W. Getz,et al.  The socioecology of elephants: analysis of the processes creating multitiered social structures , 2005, Animal Behaviour.

[30]  Mark A. Moline,et al.  Letting Penguins Lead: Dynamic Modeling of Penguin Locations Guides Autonomous Robotic Sampling , 2012 .

[31]  S. Gehrt,et al.  New Radiocollars for the Detection of Proximity among Individuals , 2006 .

[32]  Gabriel Hugh Elkaim,et al.  Instantaneous energetics of puma kills reveal advantage of felid sneak attacks , 2014, Science.

[33]  B. Manly,et al.  Resource selection by animals: statistical design and analysis for field studies. , 1994 .

[34]  Francis Daunt,et al.  A new method to quantify prey acquisition in diving seabirds using wing stroke frequency , 2008, Journal of Experimental Biology.

[35]  Phillip Cassey,et al.  Implantation reduces the negative effects of bio-logging devices on birds , 2013, Journal of Experimental Biology.

[36]  Yuzhi Cai,et al.  Wild state secrets: ultra‐sensitive measurement of micro‐movement can reveal internal processes in animals , 2014 .

[37]  Daniel P. Costa,et al.  New Insights into Pelagic Migrations: Implications for Ecology and Conservation , 2012 .

[38]  Daniel P. Costa,et al.  Three-dimensional resting behaviour of northern elephant seals: drifting like a falling leaf , 2010, Biology Letters.

[39]  Wolfgang Heidrich,et al.  Accelerometer-informed GPS telemetry : Reducing the trade-off between resolution and longevity , 2012 .

[40]  Emily L. C. Shepard,et al.  Energy Beyond Food: Foraging Theory Informs Time Spent in Thermals by a Large Soaring Bird , 2011, PloS one.

[41]  Gerald L. Kooyman,et al.  Genesis and evolution of bio-logging devices: 1963-2002 , 2004 .

[42]  David M. Scantlebury,et al.  Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism , 2014, Science.

[43]  S. Creel,et al.  Female elk contacts are neither frequency nor density dependent. , 2013, Ecology.

[44]  Bernie J. McConnell,et al.  Salinity and temperature structure of a freezing Arctic fjord—monitored by white whales (Delphinapterus leucas) , 2002 .

[45]  Sascha K. Hooker,et al.  Salinity sensors on seals: use of marine predators to carry CTD data loggers , 2003 .

[46]  M. James,et al.  Behavioral and metabolic contributions to thermoregulation in freely swimming leatherback turtles at high latitudes , 2014, Journal of Experimental Biology.

[47]  Barry Sinervo,et al.  Field physiology: physiological insights from animals in nature. , 2004, Annual review of physiology.

[48]  Panayotis Dimopoulos,et al.  Microhabitat selection by sea turtles in a dynamic thermal marine environment. , 2009, The Journal of animal ecology.

[49]  A P Farrell,et al.  Calibrating acoustic acceleration transmitters for estimating energy use by wild adult Pacific salmon. , 2013, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[50]  Sergio A. Lambertucci,et al.  Energy Landscapes Shape Animal Movement Ecology , 2013, The American Naturalist.

[51]  S. Gehrt,et al.  Frequency and duration of contacts between free-ranging raccoons: uncovering a hidden social system , 2011 .

[52]  Patrick J Butler,et al.  Biotelemetry: a mechanistic approach to ecology. , 2004, Trends in ecology & evolution.

[53]  Andrew W. Trites,et al.  Northern fur seals augment ship-derived ocean temperatures with higher temporal and spatial resolution data in the eastern Bering Sea , 2013 .

[54]  P. Ponganis,et al.  Bio-logging of physiological parameters in higher marine vertebrates , 2007 .

[55]  Kristen M. Hart,et al.  Satellite telemetry of marine megavertebrates: the coming of age of an experimental science , 2009 .

[56]  D. Costa,et al.  Estimating chlorophyll profiles from electronic tags deployed on pelagic animals , 2009 .

[57]  P. E. Kopp,et al.  Superspreading and the effect of individual variation on disease emergence , 2005, Nature.

[58]  John M. Fryxell,et al.  Why are Migratory Ungulates So Abundant? , 1988, The American Naturalist.

[59]  Kevin S. White,et al.  Benefits of migration in relation to nutritional condition and predation risk in a partially migratory moose population. , 2014, Ecology.

[60]  Gerald L. Kooyman,et al.  Techniques used in measuring diving capacities of Weddell Seals , 1965, Polar Record.

[61]  Charles R. Anderson,et al.  Landscape and anthropogenic features influence the use of auditory vigilance by mule deer , 2015 .

[62]  C. Holbrook,et al.  Tracking animals in freshwater with electronic tags: past, present and future , 2013, Animal Biotelemetry.

[63]  R. Kays,et al.  Animal behavior, cost-based corridor models, and real corridors , 2013, Landscape Ecology.

[64]  K. Fraser,et al.  Repeat Tracking of Individual Songbirds Reveals Consistent Migration Timing but Flexibility in Route , 2012, PloS one.

[65]  Michael A. Fedak,et al.  The impact of animal platforms on polar ocean observation , 2013 .

[66]  M. A. Fedak,et al.  Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals , 2008, Proceedings of the National Academy of Sciences.

[67]  Birgitte I. McDonald,et al.  Approaches to studying climatic change and its role on the habitat selection of antarctic pinnipeds. , 2010, Integrative and comparative biology.

[68]  P. Falkowski,et al.  Photosynthetic rates derived from satellite‐based chlorophyll concentration , 1997 .

[69]  Felix Liechti,et al.  First evidence of a 200-day non-stop flight in a bird , 2013, Nature Communications.