A fully implantable multi-channel biotelemetry system for measurement of blood flow and temperature: a first evaluation in the green sturgeon

The objective of this study was to evaluate a novel fully implantable radio-based blood flow biotelemetry system which allows simultaneously measurement of blood flow on two channels and temperature on one channel, in fish. These are the first recordings of blood flow from free-swimming fish, showing that the system is capable of recording blood flow in the ventral aorta (cardiac output) and celiacomesenteric artery (gastrointestinal blood flow) in green sturgeon Acipenser medirostris exposed to a series of different stimuli for up to 7 days after implantation. The results showed stable base line recordings and blood flow was used to calculated heart rate (fH) and stroke volume (Vs). It was possible to reproduce the same type of responses as has previously been reported during exposure to hypoxia, temperature, stress and feeding. The mass of our implant was less than 2% of the body mass which is well within the recommended sizes for surgically implanted telemetry transmitters and it fitted easily within the abdominal cavity of the sturgeon. A fully implantable system minimizes the risk of infection/expulsion and maximizes the likelihood that the studied fish will behave naturally and be treated normally by surrounding fish. The use of biotelemetry in basic comparative physiology and applied animal ecology could help scientists to collect information that has previously been challenging to obtain and to open the possibility for new types of physiological and ecophysiological studies.

[1]  J L Fuller,et al.  The Radio Inductograph--A Device for Recording Physiological Activity in Unrestrained Animals. , 1948, Science.

[2]  P. Williot,et al.  Circulatory and respiratory effects of an hypoxic stress in the Siberian sturgeon. , 1995, Respiration physiology.

[3]  D. Randall The Control of Respiration and Circulation in Fish During Exercise and Hypoxia , 1982 .

[4]  G. Claireaux,et al.  Post-prandial blood flow to the gastrointestinal tract is not compromised during hypoxia in the sea bass Dicentrarchus labrax. , 2002, The Journal of experimental biology.

[5]  Estimation of meal energy intake from heart rate records of pike, Esox lndus L. , 1991 .

[6]  Jian Huang,et al.  A semi-implantable multichannel telemetry system for continuous electrical, mechanical and hemodynamical recordings in animal cardiac research , 2007, Physiological measurement.

[7]  Boutilier,et al.  Cardiac output as a predictor of metabolic rate in cod gadus morhua , 1998, The Journal of experimental biology.

[8]  J. Cech,et al.  Artificial Spawning and Larval Rearing of Klamath River Green Sturgeon , 2001 .

[9]  J. Cech,et al.  Effects of temperature and carbon dioxide on green sturgeon blood–oxygen equilibria , 2006, Environmental Biology of Fishes.

[10]  Scott G. Hinch,et al.  Swim speeds and energy use of upriver-migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics , 1998 .

[11]  Julie M. Roessig,et al.  Effects of global climate change on marine and estuarine fishes and fisheries , 2004, Reviews in Fish Biology and Fisheries.

[12]  Cunada Effects of Swim Speed and Activity Pattern on Success of Adult , Sockeye Salmon Migration through an Area of Difficult Passage , 2000 .

[13]  D. Powers Fish as model systems. , 1989, Science.

[14]  Boutilier,et al.  Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating temperature conditions , 1995, The Journal of experimental biology.

[15]  I. Priede,et al.  Direct measurements of metabolism, activity and feeding behaviour of pike, Esox Zucius L., in the wild, by the use of heart rate telemetry , 1991 .

[16]  A. Farrell,et al.  Swimming patterns and behaviour of upriver-migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry in the Fraser River, British Columbia, Canada , 2002, Hydrobiologia.

[17]  D. Scruton,et al.  The effects of surgically-implanted dummy radio transmitters on the behaviour of wild Atlantic salmon smolts , 2002, Hydrobiologia.

[18]  T B Fryer,et al.  A multichannel implantable telemetry system for flow, pressure, and ECG measurements. , 1975, Journal of applied physiology.

[19]  James D. Meindl,et al.  Integrated circuits for a bidirectional implantable pulsed Doppler ultrasonic blood flowmeter , 1978 .

[20]  Jordi Altimiras,et al.  Non‐invasive recording of heart rate and ventilation rate in rainbow trout during rest and swimming. Fish go wireless! , 2000 .

[21]  Y Yonezawa,et al.  A miniaturized ultrasonic flowmeter and telemetry transmitter for chronic animal blood flow measurements. , 1989, Biomedical sciences instrumentation.

[22]  M. McCue,et al.  Specific dynamic action: a century of investigation. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[23]  D. Dixon,et al.  Assessment of cardiac output as a predictor of metabolic rate in rainbow trout , 2001 .

[24]  Stuart Egginton,et al.  Recording long-term heart rate in Paranotothenia angustata using an electronic datalogger , 2005 .

[25]  J. Reynolds,et al.  Climate Change and Distribution Shifts in Marine Fishes , 2005, Science.

[26]  J. Armstrong Heart rate as an indicator of activity, metabolic rate, food intake and digestion in pike, Esox lucius , 1986 .

[27]  D. Randall,et al.  Effects of environmental factors on exercise in fish , 1991 .

[28]  A. Farrell,et al.  Postprandial Intestinal Blood Flow, Metabolic Rates, and Exercise in Chinook Salmon (Oncorhynchus tshawytscha) , 2006, Physiological and Biochemical Zoology.

[29]  Craig A. Harms,et al.  Surgery in Fish Research: Common Procedures and Postoperative Care , 2005, Lab Animal.

[30]  J Jossinet,et al.  Detailed description of an implantable directional Doppler flowmeter. , 1976, Biotelemetry.

[31]  R D Rader,et al.  An implantable blood pressure and flow transmitter. , 1973, IEEE transactions on bio-medical engineering.

[32]  A. Farrell,et al.  Cardiorespiratory responses of white sturgeon to environmental hypercapnia. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[33]  Tom G. Pottinger,et al.  Current issues in fish welfare , 2006 .

[34]  J.J. Cupal,et al.  A system to acquire and record physiological and behavioral data remotely from nonhuman primates , 1991, IEEE Transactions on Biomedical Engineering.

[35]  A. J. Smith,et al.  Guidelines for health and welfare monitoring of fish used in research , 2006, Laboratory animals.

[36]  I. Priede,et al.  An acoustic telemetry system for monitoring the heart rate of pike, Esox lucius L., and other fish in their natural environment. , 1989, The Journal of experimental biology.

[37]  Fred S. Conte,et al.  Stress and the welfare of cultured fish , 2004 .

[38]  C. Daxboeck,et al.  Cardiovascular changes in the rainbow trout (Salmo gairdneri Richardson) during exercise , 1982 .

[39]  R. L. Citters,et al.  Blood Velocity telemetered from Untethered Animals , 1964, Nature.

[40]  Imants G. Priede,et al.  Heart rate as a measure of metabolic rate in teleost fishes; Salmo gairdneri, Salmo trutta and Gadus morhua , 1977 .

[41]  A. Farrell,et al.  Tribute to P. L. Lutz: a message from the heart – why hypoxic bradycardia in fishes? , 2007, Journal of Experimental Biology.

[42]  E. Baras,et al.  Surgical implantation of telemetry transmitters in fish: how much have we learned? , 2002 .

[43]  R. A. Miller,et al.  The Cost of Chronic Stress: Impacts of a Nonhabituating Stress Response on Metabolic Variables and Swimming Performance in Sturgeon , 2005, Physiological and Biochemical Zoology.

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

[45]  A. Farrell,et al.  INTESTINAL BLOOD FLOW IN SWIMMING CHINOOK SALMON ONCORHYNCHUS TSHAWYTSCHA AND THE EFFECTS OF HAEMATOCRIT ON BLOOD FLOW DISTRIBUTION , 1993 .

[46]  Paul J. Ashley Fish welfare: Current issues in aquaculture , 2007 .

[47]  S. Hinch,et al.  Energy expenditures during reproduction by sockeye salmon (Oncorhynchus nerka) , 2003 .

[48]  A. Farrell Effects of temperature on cardiovascular performance , 1997 .

[49]  J. Cech,et al.  Time of day and water temperature modify the physiological stress response in green sturgeon, Acipenser medirostris. , 2003, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[50]  U. Schulz Effects of surgically implanted dummy transmitters on the South American catfish Jundiá (Rhamdia quelen). , 2003, Brazilian journal of biology = Revista brasleira de biologia.

[51]  R. Fritsche,et al.  Effects of exercise, hypoxia and feeding on the gastrointestinal blood flow in the Atlantic cod Gadus morhua. , 1991, The Journal of experimental biology.

[52]  A. Farrell,et al.  Regulation of cardiac output and gut blood flow in the sea raven,Hemitripterus americanus , 1989, Fish Physiology and Biochemistry.

[53]  W. Wildgoose BSAVA manual of ornamental fish , 2001 .

[54]  J. Kieffer,et al.  Hematology and stress physiology of juvenile diploid and triploid shortnose sturgeon (Acipenser brevirostrum) , 2005, Fish Physiology and Biochemistry.

[55]  D. Fontenot,et al.  Wound management in teleost fish: biology of the healing process, evaluation, and treatment. , 2004, The veterinary clinics of North America. Exotic animal practice.

[56]  T. Nakayama,et al.  Radio telemetry directional ultrasonic blood flowmeter for use with unrestrained animals , 1992, Medical and Biological Engineering and Computing.

[57]  J. Lagardère,et al.  Fish telemetry in aquaculture: review and perspectives , 1995, Aquaculture International.

[58]  Scott G. Hinch,et al.  Swimming patterns and behaviour of upriver-migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry in the Fraser River, British Columbia, Canada , 2002 .

[59]  I. Boyd,et al.  Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods , 2004 .

[60]  M. Lucas Heart rate as an indicator of metabolic rate and activity in adult Atlantic salmon, Salmo salar , 1994 .

[61]  S. R. Winters Diagnosis by Wireless , 1921 .

[62]  G S Kassab,et al.  A novel, fully implantable, multichannel biotelemetry system for measurement of blood flow, pressure, ECG, and temperature. , 2007, Journal of applied physiology.

[63]  L. Hansen,et al.  Potential impacts of global climate change on freshwater fisheries , 2007, Reviews in Fish Biology and Fisheries.

[64]  J W Knutti,et al.  Totally implantable directional Doppler flowmeters. , 1979, Biotelemetry and patient monitoring.

[65]  A. Farrell,et al.  The limitations of heart rate as a predictor of metabolic rate in fish , 1996 .