On the Use of Animal-Borne Instruments to Monitor the Ocean
Fabien Roquet and Lars Boehme
In addition to collecting information on the behavior of diving animals, miniaturized data loggers can now record physical and biogeochemical data to improve ocean-observing capabilities. Marine mammals in particular help gather oceanographic information on some of the harshest environments on the planet. Study species such as the elephant seals travel thousands of kilometers and continuously dive to great depths (up to 2,500 m). The past decade of animal tagging has demonstrated the feasibility and high value of this approach for ocean observation. At the core of this success has been collaboration between biologists and physical oceanographers, an example of a truly multidisciplinary approach that has yielded great results for both communities. The use of animal-borne instruments has been particularly successful in polar and coastal areas, and new opportunities are emerging as miniaturization and telemetry progress and new sensors and techniques are developed.
Sustained ocean observations are crucial for monitoring and understanding the marine environment and its variability within the Earth system. A range of ocean-observing systems have come a long way in balancing the sustained monitoring requirements with the need for research. The polar oceans are important marine environments that respond to environmental change and influence our planet, but are still undersampled. The harsh climate and remoteness of the polar regions, as well as the large-scale offshore pelagic environments, make them extremely difficult to observe. Achieving a comprehensive network of instruments delivering precise oceanographic measurements is a particular goal. For the last decade, diving marine animals equipped with sensors have been contributing to the observing systems and increasingly filling existing gaps, especially in the polar oceans.
Animals tagged with oceanographic sensors (Figure 1) have now become essential sources of temperature and salinity (TS) profiles, especially for high-latitude oceans (Charrassin et al., 2008; Boehme et al., 2010; Costa et al., 2010; Fedak, 2013; Roquet et al., 2014; Hussey et al., 2015). For example, data from elephant seals and Weddell seals represent 98% of the existing TS profiles within Southern Ocean pack ice. The instruments are non-invasive (attached to the animal’s fur and naturally falling off during the animal’s next molt) and they also record the animal’s behavior in the context of its environment. Since 2002, several hundreds diving marine animals, mainly Antarctic and Arctic seals, have been fitted with instruments delivering data to the ocean-observing system.
The international consortium MEOP (Marine mammals Exploring the Ocean Pole-to-pole, see Treasure et al., 2017, for a review), originally formed during the International Polar Year in 2008–2009, aims to coordinate animal tag deployments, and oceanographic data processing and data distribution globally. The data are made available to the global scientific community through http://www.meop.net (Figure 2). The value of the hydrographic data produced by MEOP within the existing Southern Ocean Observing System was demonstrated using seal-collected data. These data improved mixed-layer properties, circulation patterns, and sea-ice concentrations in model simulations (Roquet et al., 2013). The data collected within MEOP have already contributed to important oceanographic findings (e.g., Pellichero et al., 2016; Williams et al., 2016; Zhang et al. 2016) and insights into marine ecology through the availability of concurrent information about the animal’s behavior (e.g., Hindell et al., 2016).
A range of instruments are available that can be attached to marine animals, but only a few can deliver the data at the necessary quality to warrant inclusion in observing systems. One instrument meeting such specifications is the SPLASH tag manufactured by Wildlife Computers Inc. (USA). It generally incorporates a FastLoc GPS antenna for geolocation and an ARGOS antenna for telemetry, combined with pressure and temperature sensors with accuracies of ±5 dbar and 0.1°C, respectively. Owing to its small size, it can be used on most diving birds and marine mammal species, yielding thousands of profiles especially in various coastal and continental shelf areas.
The CTD Satellite Relay Data Logger (CTD-SRDL) built at the Sea Mammal Research Unit (SMRU, University of St Andrews, UK) is currently the only existing tag that includes a miniaturized CTD unit (Figure 3). CTD-SRDLs record temperature and conductivity during the ascent part of an animal’s dive (Boehme et al., 2009; Roquet et al., 2011). These CTD profiles are then telemetered in a compressed form (between 10 and 25 depth levels per profile depending on the configuration) using radio telemetry (ARGOS, GSM, UHF). More detailed descriptions of the instruments can be found in Fedak et al. (2002), Cronin and McConnell (2008), Boehme et al. (2009) and Photopoulou et al. (2015). CTD-SRDLs are calibrated by the manufacturer, and the delayed-mode data quality is estimated to be ±0.03°C in temperature and ±0.05 psu or better in salinity (Roquet et al., 2011).
Most loggers also archive data at the maximum sampling frequency in an internal memory. The complete data set can then be downloaded if the instrument can be retrieved in the field. Recovery is often not possible due to the nature of tagging animals in remote places, but has been done in some areas. For example, instruments deployed on elephant seals on the Kerguelen Islands (Southern Ocean), Marion Island (Southern Ocean), and at Año Nuevo (California, USA) were often recovered, providing data sets with exceptional spatio-temporal resolution—typically 60+ TS profiles per day for two to four month periods—in critical areas of the ocean.
Manufacturers are integrating sensor capabilities beyond measuring basic physical ocean variables. Instruments can now include sensors to measure light levels, fluorescence, or oxygen (e.g., Guinet et al., 2013; Bailleul et al., 2015). This step is important and will lead to a better understanding of the link between physical and biogeochemical processes. A recent pilot study showed that accelerometers on tags can be used to monitor wave conditions when animals are near the surface (Cazau et al., 2017b), while other logger types that record the underwater acoustic signal could be used to estimate the surface wind speed with an accuracy of 2 m s–1 (Cazau et al., 2017a). This opens the possibility of using bio-logged animals as weather buoys of opportunity.
Integration into the Global Ocean Observing System
Animal-borne instruments provide several thousand oceanographic profiles per year, closing gaps in our understanding of the climate system and complementing other observing platforms such as Argo floats. They also deliver data from shallow and highly dynamic coastal areas in which other autonomous platforms have difficulty operating. The concurrent behavioral information also makes the data useful, for example, for understanding the foraging behavior and ecological vulnerability of the tagged species, which in turn can improve our understanding of ocean health. The successful and useful integration of data from animal-borne instruments into ocean-observing systems depends on three key requirements: sufficient quality, data standardization, and robust data delivery.
While animal-borne instruments have been recording oceanographic variables for a long time, accuracies needed for tracking oceanographic changes were only achieved recently. The CTD-SRDL was the first to provide calibrated sensors with oceanographic applications in mind, but other instruments are emerging that are able to provide, for example, temperature measurements with an accuracy of better than 0.1°C. Manufacturers are now aiming to integrate sensors that can deliver data that are better by one order of magnitude. Improved calibration methods and delayed-mode quality procedures appear as crucial as the quality of sensor technology in achieving the best data accuracy.
Timely data delivery is important for ocean-observing systems. Data from animal-borne instruments are often provided to the observing systems after considerable quality control. Many of the quality-control processes have been adapted from proven systems supporting, for example, the Argo float community. Data can also be transmitted in near-real time using the ARGOS or GSM networks. Such data, especially from remote locations or from the sea-ice zones, are particularly important to the real-time services supported by the observing systems. Large efforts are ongoing to provide a unified real-time data flow for such operational applications.
Regional communities and initiatives are coming together to promote integration of this multidisciplinary tool into the observing system, including the US Animal Telemetry Network (ATN, Block et al., 2016), the EuroGOOS Animal-Borne Instrument (ABI) Task Team in Europe, the Australian Integrated Marine Observing System (IMOS), and the Canadian Ocean Tracking Network (OTN). Better coordination with other marine observing capabilities is supported within the framework provided by the Observations Coordination Group of the Joint WMO-IOC Technical Commission for Oceanography and Marine Meteorology (JCOMM-OCG). Ultimately, the objective is to have the animal tagging approach become an integral component of the Global Ocean Observing System, making a sustained contribution to climate and marine life monitoring.
Bailleul, F., J. Vacquie-Garcia, and C. Guinet. 2015. Dissolved oxygen sensor in animal-borne instruments: An innovation for monitoring the health of oceans and investigating the functioning of marine ecosystems. PLoS ONE 10:e0132681, https://doi.org/10.1371/journal.pone.0132681.
Block, B.A., C.M. Holbrook, S.E. Simmons, K.N. Holland, J.S. Ault, D.P. Costa, B.R. Mate, A.C. Seitz, M.D. Arendt, J.C. Payne, and others. 2016. Toward a national animal telemetry network for aquatic observations in the United States. Animal Biotelemetry 4:6, https://doi.org/10.1186/s40317-015-0092-1.
Boehme, L., K. Kovacs, C. Lydersen, O.A. Nøst, M. Biuw, J.-B. Charrassin, F. Roquet, C. Guinet, M. Meredith, K. Nicholls, and others. 2010. Biologging in the global ocean observing system. In: Proceedings of Ocean Obs 09: Sustained Ocean Observations and Information for Society. J. Hall, D.E. Harrison, and D. Stammer, eds, Venice, Italy, European Space Agency, ESA Publication, WPP-306, Vol. 2, https://doi.org/10.5270/OceanObs09.cwp.06.
Boehme, L., P. Lovell, M. Biuw, F. Roquet, J. Nicholson, S. Thorpe, M.P. Meredith, and M. Fedak. 2009. Technical note: Animal-borne CTD-Satellite Relay Data Loggers for real-time oceanographic data collection. Ocean Science 5:685–695, https://doi.org/10.5194/os-5-685-2009.
Cazau, D., J. Bonnel, J. Jouma’a, Y. le Bras, and C. Guinet. 2017a. Measuring the marine soundscape of the Indian Ocean with southern elephant seals used as acoustic gliders of opportunity. Journal of Atmospheric and Oceanic Technology 34:207–223, https://doi.org/10.1175/JTECH-D-16-0124.1.
Cazau, D., C. Pradalier, J. Bonnel, and C. Guinet. 2017b. Do southern elephant seals behave like weather buoys? Oceanography 30(2):140–149, https://doi.org/10.5670/oceanog.2017.236.
Charrassin, J.-B., M. Hindell, S.R. Rintoul, F. Roquet, S. Sokolov, M. Biuw, D. Costa, L. Boehme, P. Lovell, R. Coleman, and others. 2008. Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals. Proceedings of the National Academy of Sciences of the United States of America 105:11,634–11,639, https://doi.org/10.1073/pnas.0800790105.
Costa, D.P., L.A. Huckstadt, D.E. Crocker, B.I. McDonald, M.E. Goebel, and M.A. Fedak. 2010. Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds. Integrative and Comparative Biology 50:1,018–1,030, https://doi.org/10.1093/icb/icq054.
Cronin, M.A., and B.J. McConnell. 2008. SMS seal: A new technique to measure haul-out behaviour in marine vertebrates. Journal of Experimental Marine Biology and Ecology 362:43–48, https://doi.org/10.1016/j.jembe.2008.05.010.
Fedak, M.A. 2013. The impact of animal platforms on polar ocean observation. Deep Sea Research Part II 88–89:7–13, https://doi.org/10.1016/j.dsr2.2012.07.007.
Fedak, M.A., P. Lovell, B.J. McConnell, and C. Hunter. 2002. Overcoming the constraints of long range radio telemetry from animals: Getting more useful data from smaller packages. Integrative and Comparative Biology 42(1):3–10, https://doi.org/10.1093/icb/42.1.3.
Guinet, C., X. Xing, E. Walker, P. Monestiez, S. Marchand, B. Picard, T. Jaud, M. Authier, C. Cotte, A.C. Dragon, and others. 2013. Calibration procedures and first dataset of Southern Ocean chlorophyll a profiles collected by elephant seals equipped with a newly developed CTD-fluorescence tags. Earth System Science Data 5:15–29, https://doi.org/10.5194/essd-5-15-2013.
Hindell, M.A., C.R. McMahon, M.N. Bester, L. Boehme, D. Costa, M.A. Fedak, C. Guinet, L. Herraiz-Borreguero, R.G. Harcourt, L. Huckstadt, and others. 2016. Circumpolar habitat use in the southern elephant seal: implications for foraging success and population trajectories. Ecosphere 7, https://doi.org/10.1002/ecs2.1213.
Hussey, N.E., S.T. Kessel, K. Aarestrup, S.J. Cooke, P.D. Cowley, A.T. Fisk, R.G. Harcourt, K.N. Holland, S.J. Iverson, J.F. Kocik, and others. 2015. Aquatic animal telemetry: A panoramic window into the underwater world. Science 348:1255642, https://doi.org/10.1126/science.1255642.
Pellichero, V., J.B. Sallée, S. Schmidtko, F. Roquet, and J.-B. Charrassin. 2016. The ocean mixed-layer under Southern Ocean sea-ice: Seasonal cycle and forcing. Journal of Geophysical Research 122:1,608–1,633, https://doi.org/10.1002/2016JC011970.
Photopoulou, T., M.A. Fedak, J. Matthiopoulos, B. McConnell, and P. Lovell. 2015. The generalized data management and collection protocol for Conductivity-Temperature-Depth Satellite Relay Data Loggers. Animal Biotelemetry 3:21, https://doi.org/10.1186/s40317-015-0053-8.
Roquet, F., J.-B. Charrassin, S. Marchand, L. Boehme, M. Fedak, G. Reverdin, and C. Guinet. 2011. Delayed-mode calibration of hydrographic data obtained from animal-borne Satellite Relay Data Loggers. Journal of Atmospheric and Oceanic Technology 28:787–801, https://doi.org/10.1175/2010JTECHO801.1.
Roquet, F., G. Williams, M.A. Hindell, R. Harcourt, C. McMahon, C. Guinet, J.-B. Charrassin, G. Reverdin, L. Boehme, P. Lovell, and M. Fedak. 2014. A Southern Indian Ocean database of hydrographic profiles obtained with instrumented elephant seals. Nature Scientific Data 1:140028, https://doi.org/10.1038/sdata.2014.28.
Roquet, F., C. Wunsch, G. Forget, P. Heimbach, C. Guinet, G. Reverdin, J.-B. Charrassin, F. Bailleul, D.P. Costa, L.A. Huckstadt, and others. 2013. Estimates of the Southern Ocean general crculation improved by animal-borne instruments. Geophysical Research Letters 40:1–5, https://doi.org/10.1002/2013GL058304.
Treasure, A., F. Roquet, I.J. Ansorge, M.N. Bester, L. Boehme, H. Bornemann, J.-B. Charrassin, D. Chevallier, D. Costa, M.A. Fedak, and others. 2017. Marine Mammals Exploring the Oceans Pole to Pole: A review of the MEOP consortium. Oceanography 30(2):132–138, https://doi.org/10.5670/oceanog.2017.234.
Williams, G.D., L. Herraiz-Borreguero, F. Roquet, T. Tamura, K.I. Ohshima, Y. Fukamachi, A.D. Fraser, L. Gao, H. Chen, C.R. McMahon, and others. 2016. The suppression of Antarctic bottom water formation by melting ice shelves in Prydz Bay. Nature Communications 7:12577, https://doi.org/10.1038/ncomms12577.
Zhang, X., A.F. Thompson, M.M. Flexas, F. Roquet, and H. Bornemann. 2016. Circulation and meltwater distribution in the Bellingshausen Sea: From shelf break to coast. Geophysical Research Letters 43:6,402–6,409, https://doi.org/10.1002/2016GL068998.
Fabien Roquet, Department of Meteorology (MISU), Stockholm University, Stockholm, Sweden, email@example.com
Lars Boehme, Scottish Oceans Institute, University of St Andrews, UK, firstname.lastname@example.org