Best practice recommendations for the use of fully implanted telemetry devices in pinnipeds

Electronic telemetry devices have enabled many novel and important data collection and experimental opportunities for difficult to observe species. Externally attached devices have limited retention and may affect thermoregulation, energetics, social and reproductive behavior, visibility, predation risk and entanglement. Internally placed, surgically implanted devices can mitigate some of these effects and may open additional experimental opportunities. However, improper implementation can significantly affect animals and data. From a review of recent studies using fully implanted tags and studying their effects, we present 15 specific best practice recommendations for the use of such tags in pinnipeds. Recommendations address issues including device size, coating and sterilization, implantation surgery and effect assessment, within the framework of the Three R’s: Reduction, Refinement, Replacement. While developed for pinnipeds, these recommendations could apply to other aquatic mammals and vertebrates and to partially implanted or even external tags.

[1]  Peter L. Boveng,et al.  Effects of time–depth recorders on maternal foraging and attendance behavior of Antarctic fur seals (Arctocephalus gazella) , 1995 .

[2]  Y. Handrich,et al.  Impact of Externally Attached Loggers on the Diving Behaviour of the King Penguin , 2000, Physiological and Biochemical Zoology.

[3]  G. Kollias,et al.  SURGICAL TECHNIQUE FOR INTRA-ABDOMINAL RADIOTRANSMITTER PLACEMENT IN NORTH AMERICAN RIVER OTTERS (LONTRA CANADENSIS) , 2009, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[4]  Steven J. Beaupre,et al.  Standards for Wildlife Research: Taxon-Specific Guidelines versus US Public Health Service Policy , 2012 .

[5]  D. Monson,et al.  FORAGING DEPTHS OF SEA OTTERS AND IMPLICATIONS TO COASTAL MARINE COMMUNITIES , 2004 .

[6]  Gene R. Ploskey,et al.  The Juvenile Salmon Acoustic Telemetry System: A New Tool , 2010 .

[7]  Buddy D Ratner,et al.  Engineering biomaterials to integrate and heal: The biocompatibility paradigm shifts , 2012, Biotechnology and bioengineering.

[8]  British Standard,et al.  Biological evaluation of medical devices , 2006 .

[9]  Donald F. Caccamise,et al.  An Aerodynamic Basis for Selecting Transmitter Loads in Birds , 1985 .

[10]  Charles J. Amlaner,et al.  A Practical Guide to Radio Tracking , 1980 .

[11]  M. Lacki,et al.  Use of methoxyfluorane to surgically implant transmitters in muskrats , 1989 .

[12]  Jason M. Jones,et al.  GUIDELINES TO THE USE OF WILD BIRDS IN RESEARCH , 2010 .

[13]  J. Harvey,et al.  Modified technique for the subcutaneous implantation of radio transmitters in harbour seals (Phoca vitulina richardii) under field conditions , 2015, Veterinary Record Case Reports.

[14]  Michael Balls,et al.  The Principles of Humane Experimental Technique: Timeless Insights and Unheeded Warnings , 2010 .

[15]  R. Einstein.  The use of telemetry to refine experimental technique , 2000 .

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

[17]  W. Melquist,et al.  Reproductive effects of intraperitoneal transmitter implants in river otters , 1986 .

[18]  L. Michael Romero,et al.  Stress and translocation: alterations in the stress physiology of translocated birds , 2009, Proceedings of the Royal Society B: Biological Sciences.

[19]  P. Flecknell,et al.  Chapter 5 – Management of Postoperative and Other Acute Pain , 2000 .

[20]  M. Horning,et al.  In cold blood: evidence of Pacific sleeper shark (Somniosus pacificus) predation on Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska , 2014 .

[21]  J. Kocik,et al.  Aquatic animal telemetry: A panoramic window into the underwater world , 2015, Science.

[22]  Penny Hawkins,et al.  Bio-logging and animal welfare: practical refinements , 2004 .

[23]  Daniel M. Weary,et al.  A review of the effects of different marking and tagging techniques on marine mammals , 2012, Wildlife Research.

[24]  T. F. Næsje,et al.  Long-term effects of different-sized surgically implanted acoustic transmitters on the sciaenid Arygyrosomus japonicus: breaking the 2% tag-to-body mass rule , 2011 .

[25]  D. Crocker,et al.  Effects of buoyancy on the diving behavior of northern elephant seals. , 1998, The Journal of experimental biology.

[26]  C. Shuert,et al.  The Effect of Novel Research Activities on Long-term Survival of Temporarily Captive Steller Sea Lions (Eumetopias jubatus) , 2015, PloS one.

[27]  G. Loupal,et al.  Common carp tissue reactions to surgically implanted radio tags with external antennas , 2007 .

[28]  Derek E. Lee,et al.  Survival probabilities and movements of harbor seals in central California , 2017 .

[29]  B. Owens.  Batteries for Implantable Biomedical Devices , 2012 .

[30]  M. Horning,et al.  Physiological and behavioral response to intra-abdominal transmitter implantation in Steller sea lions , 2007 .

[31]  Rory P. Wilson,et al.  Measuring devices on wild animals: what constitutes acceptable practice? , 2006 .

[32]  M. Horning,et al.  Juvenile Steller sea lion dive behavior following temporary captivity , 2008 .

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

[34]  D. Weary,et al.  Behavioural responses of juvenile Steller sea lions to abdominal surgery: Developing an assessment of post-operative pain , 2009 .

[35]  D. Monson,et al.  Long-term effects of the Exxon Valdez oil spill: sea otter foraging in the intertidal as a pathway of exposure to lingering oil , 2012 .

[36]  John M. Maniscalco.  The Effects of Birth Weight and Maternal Care on Survival of Juvenile Steller Sea Lions (Eumetopias jubatus) , 2014, PloS one.

[37]  Y. Naito,et al.  Summing the strokes: energy economy in northern elephant seals during large-scale foraging migrations , 2015, Movement ecology.

[38]  David C. Guynn,et al.  Pathological potential of intraperitoneal transmitter implants in beavers , 1987 .

[39]  R. Sikes,et al.  Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research , 2007 .

[40]  Rachel K. Berngartt,et al.  Efficacy of subcutaneous VHF implants and remote telemetry monitoring to assess survival rates in harbor seals , 2014 .

[41]  Martin Haulena,et al.  Intraperitoneal implantation of life-long telemetry transmitters in otariids , 2008, BMC veterinary research.

[42]  Daniel M Mulcahy,et al.  Surgical implantation of transmitters into fish. , 2003, ILAR journal.

[43]  C. J. Bridger,et al.  The Effects of Biotelemetry Transmitter Presence and Attachment Procedures on Fish Physiology and Behavior , 2003 .

[44]  Daniel M. Mulcahy,et al.  Legal, Ethical, and Procedural Bases for the Use of Aseptic Techniques to Implant Electronic Devices , 2013 .

[45]  Alan E. Burger,et al.  Foraging Behavior and Physiological Adaptation for Diving in Thick‐Billed Murres , 1992 .

[46]  Steven J. Cooke,et al.  Evidence to Challenge the ''2% Rule'' for Biotelemetry , 1999 .

[47]  Y. Ropert‐Coudert,et al.  Is abdominal implantation of devices a good alternative to external attachment? A comparative study in Adélie penguins , 2010, Journal of Ornithology.

[48]  S. Atkinson,et al.  Temporary Captivity as a Research Tool: Comprehensive Study of Wild Pinnipeds Under Controlled Conditions , 2006 .

[49]  C. Bradshaw,et al.  Blubber and buoyancy: monitoring the body condition of free-ranging seals using simple dive characteristics , 2003, Journal of Experimental Biology.

[50]  J. E. Mellish,et al.  The influence of time in captivity, food intake and acute trauma on blood analytes of juvenile Steller sea lions, Eumetopias jubatus , 2015, Conservation physiology.

[51]  R. Kays,et al.  Terrestrial animal tracking as an eye on life and planet , 2015, Science.

[52]  Udo Albus,et al.  Book Review: Guide for the Care and use of Laboratory Animals , 1998 .

[53]  Helen Bailey,et al.  Ontogeny in marine tagging and tracking science: technologies and data gaps , 2012 .

[54]  Akitada Nakamura,et al.  Simultaneus development of MHW guidelines for biological evaluation of medical devices and ISO 10993-Report of 10 years activity of the Standardization Committee of JSBM , 1999 .

[55]  S. Atkinson,et al.  Monitoring glucocorticoid response to rehabilitation and research procedures in California and Steller sea lions. , 2008, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[56]  John M. Maniscalco,et al.  High Natality Rates of Endangered Steller Sea Lions in Kenai Fjords, Alaska and Perceptions of Population Status in the Gulf of Alaska , 2010, PloS one.

[57]  K. Kovacs,et al.  Allometry of diving capacity in air-breathing vertebrates , 1997 .

[58]  C. Shuert,et al.  Physiological predictors of long-term survival in juvenile Steller sea lions (Eumetopias jubatus) , 2015, Conservation physiology.

[59]  D. Saavedra,et al.  REINTRODUCTION OF THE EURASIAN OTTER (LUTRA LUTRA) IN NORTHEASTERN SPAIN: TRAPPING, HANDLING, AND MEDICAL MANAGEMENT , 2009, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[60]  W. Russell,et al.  Ethical and Scientific Considerations Regarding Animal Testing and Research , 2011, PloS one.

[61]  Rory P. Wilson,et al.  SWIMMING ENERGETICS AND PERFORMANCE OF INSTRUMENTED ADELIE PENGUINS (PYGOSCELIS ADELIAE) , 1991 .

[62]  Kathleen M. Carter,et al.  An Evaluation of the Maximum Tag Burden for Implantation of Acoustic Transmitters in Juvenile Chinook Salmon , 2010 .

[63]  M. Horning,et al.  Spatially explicit detection of predation on individual pinnipeds from implanted post-mortem satellite data transmitters , 2009 .

[64]  Trevor McIntyre,et al.  Trends in tagging of marine mammals: a review of marine mammal biologging studies , 2014 .

[65]  Paul M. Thompson,et al.  Guidelines for the treatment of marine mammals in field research , 2009 .

[66]  M. Horning,et al.  Predation on an Upper Trophic Marine Predator, the Steller Sea Lion: Evaluating High Juvenile Mortality in a Density Dependent Conceptual Framework , 2012, PloS one.

[67]  E. Ågren,et al.  SURGICAL IMPLANTATION OF RADIOTELEMETRY TRANSMITTERS IN EUROPEAN BADGERS (MELES MELES) , 2009, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[68]  H. Reynolds,et al.  Field Surgical Techniques for Implanting Temperature-Sensitive Radio Transmitters in Grizzly Bears , 1981 .

[69]  E. Fuglei,et al.  SURGICAL IMPLANTATION OF RADIO TRANSMITTERS IN ARCTIC FOXES (ALOPEX LAGOPUS) ON SVALBARD, NORWAY , 2009, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[70]  R. Harcourt,et al.  MOLECULAR DETECTION OF ANTIBIOTIC-RESISTANCE DETERMINANTS IN ESCHERICHIA COLI ISOLATED FROM THE ENDANGERED AUSTRALIAN SEA LION (NEOPHOCA CINEREA) , 2015, Journal of wildlife diseases.

[71]  C. Woodley,et al.  Influence of Incision Location on Transmitter Loss, Healing, Survival, Growth, and Suture Retention of Juvenile Chinook Salmon , 2011 .

[72]  Patrick J. Butler,et al.  Trial Implantation of Heart Rate Data Loggers in Pinnipeds , 2009 .

[73]  R.D. Hill,et al.  Designing an archival Satellite transmitter for life-long deployments on oceanic vertebrates: the life history transmitter , 2005, IEEE Journal of Oceanic Engineering.

[74]  M. Horning,et al.  Intraperitoneal implantation of life-long telemetry transmitters in three rehabilitated harbor seal pups , 2017, BMC Veterinary Research.

[75]  Charles J. Amlaner,et al.  A Handbook on Biotelemetry and Radio Tracking , 1980 .

[76]  John M. Maniscalco,et al.  Population Trend and Elasticities of Vital Rates for Steller Sea Lions (Eumetopias jubatus) in the Eastern Gulf of Alaska: A New Life-History Table Analysis , 2015, PloS one.

[77]  J. Harvey,et al.  IMPLANTATION OF SUBCUTANEOUS RADIO TRANSMITTERS IN THE HARBOR SEAL (PHOCA VITULINA) , 2005 .

[78]  P. Flecknell,et al.  Chapter 1 – Animal Pain – An Introduction , 2000 .

[79]  J. R. Macmillan,et al.  Guidelines for use of fishes in research , 2014 .

[80]  R. Clarke,et al.  The theory and practice of catching, holding, moving and releasing animals , 2012 .

[81]  D. Weary,et al.  The effects of two analgesic regimes on behavior after abdominal surgery in Steller sea lions. , 2011, The Veterinary Journal.

[82]  E. Hammond,et al.  A Novel Method for Capturing and Implanting Radiotransmitters in Nutria , 2006 .

[83]  A. Shoieb,et al.  Peritoneal Sarcomatosis Associated with Telemetry Implants in Sprague Dawley CD Rats , 2012, Toxicologic pathology.

[84]  Dan Li,et al.  Biocompatible polymer materials : Role of protein-surface interactions , 2008 .

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

[86]  Ruth M. Casper.  Guidelines for the instrumentation of wild birds and mammals , 2009, Animal Behaviour.

[87]  Bernie J. McConnell,et al.  Bio-logging science: Logging and relaying physical and biological data using animal-attached tags , 2007 .

[88]  Penny Hawkins,et al.  Refinements in telemetry procedures: Seventh report of BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement, Part A , 2003, Laboratory animals.

[89]  A. Hall,et al.  Salmonella infection in grey seals (Halichoerus grypus), a marine mammal sentinel species: pathogenicity and molecular typing of Salmonella strains compared with human and livestock isolates. , 2016, Environmental microbiology.