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Research on Higher Trophic Levels Daniel P. Costa,* Yann Tremblay,† Sean Hayes‡ Our understanding of the mechanisms responsible for biophysical coupling in marine ecosystems has developed significantly over the last two decades, but is limited to the mechanisms that relate physical oceano- graphic processes to primary production and primary consumers (zoo- plankton). In contrast, our knowledge of the linkages between biology and physics of higher trophic levels remains quite descriptive at best. This is unfortunate because higher trophic level species are increasingly under threat of extinction along with a loss in marine biodiversity. This is occur- ring as we are becoming aware of the importance of upper trophic levels in structuring marine communities due to both their role as predators (Estes et al. 1998; Myers and Worm 2003) and as they transport nutrients across and within the water column (Smetacek and Cloern 2008). As the first Census of Marine Life (CoML, ends in 2010 we will have gained significant insights and developed new tools to study a wide variety of marine habitats, from the coastal margin to the deep sea. However, these studies were separated in space and time. Imagine what could be accomplished if this research was applied in an integrated manner, providing a seamless transition from the benthos through the water column to the intertidal. With measurements of the movement patterns of top predators coupled with the abundance of * University of California, Santa Cruz †  Institut pour la Recherche et le Développement, France ‡  Fisheries Ecology Division, Southwest Fisheries Science Center 124

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Daniel P. Costa et al. 125 zooplankton. Such an integrated effort would need to be focused on a number of regions where existing infrastructure is in place or locations that are representative of critical marine habitats. Such an integrated effort would provide not just a onetime snapshot of the biodiversity of a marine habitat, but would provide a dynamic view into the processes that maintain biodiversity and a better understanding of how it can be protected. A critically important aspect of this is that we will be able to monitor how life in the ocean is changing in response to climate change. Such information will be critical to policy makers to provide them with the information necessary to mitigate such impacts. Models will be an important component of such an effort, as much of the data collected will be descriptive. While NPZ models have proven quite informative for lower trophic levels, they do not scale up to higher trophic levels. Individual Based Models (IBMs) can represent the move- ments of a single marine animal and can create an energy budget that incorporates the costs of movement and acquiring prey. Such a model would be spatially explicit, and influenced by environmental and other relevant factors affecting animal behavior. A suite of these IBMs can be released into a model to represent a population of a given species. The movement patterns relative to oceanographic features and prey availabil- ity can then be modeled along with information on species interactions. The development of such models would require a mechanistic under- standing of the habitat utilization patterns of higher trophic levels. Elec- tronic tags can be used to help elucidate the habitat utilization patterns of marine organisms and provide data that are appropriate for incorporation into IBMs. Integration of oceanographic data with marine animal distribu- tion and behavior can be used to build models that describe the interre- lationships of marine animal movements to their physical and ecological habitat. Such a modeling approach would provide an “experimental test bed” to examine the processes that determine animal distributions, local abundance and movement patterns. Under the auspices of the CoML, a variety of technologies have been developed, among them is the use of electronic tagging that has been deployed on a large scale in an integrated manner to track the move- ments and behavior of large marine vertebrates, in the Tagging of Pacific Pelagics (TOPP) program ( and in the Pacific Ocean Shelf (POST) tracking project program ( The primary methods for tracking marine organisms include: GPS, ARGOS satellite, acoustic and archival data storage tags (Figures 1 and 2). Over the last decade the capability of electronic tags has increased considerably. However, there are a number of technological advances that need further development, including novel ways of powering the tags, increased sensor capabilities (including oceanographic sensors and animal behavior and/or physiol-

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126 OCEANOGRAPHY IN 2025 FIGURE 1  Southern elephant seal with a Sea Mammal Research Unit CTD tag attached to its head. These tags transmit information on the animal’s surface track (Figure 2A), dive behavior (Figure 2B) and temperature and salinity profiles (Figure 2C). ogy), better attachment methods, miniaturization of tags, and alternative methods of data recovery. While new higher capacity batteries may be developed, an alternative would be to develop other methods of obtain- ing power. For example, these animals move through the water and some undergo considerable changes in pressure. Conceptually, this seems very straightforward, but the development of reliable power harvesting sys- tems has not begun. Other sensors that could be added to the tags include FIGURE 2  Tracks of southern elephant seals showing the range of data that can be derived. A) surface track only, B) surface track with underwater behavior, and C) track with CT profile along route of the animal.

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Daniel P. Costa et al. 127 such important oceanographic measure as O2, pH, CO2, and chlorophyll, as well as important measures of animal behavior as 3-axis acceleration, feeding and heart rate and possibly active sonar to measure prey fields in front of the animal. Finally, novel methods of data recovery would greatly enhance the range of species that these tags could be deployed on. Currently, archival tags have to be recovered to obtain the data. This is done when the animal returns to a rookery (seals and birds), the tag is released and floats to the surface where it transmits a subset of the infor- mation (pop up tags), or the data are transmitted via ARGOS when the animals come to the surface (air-breathing vertebrates and some sharks). A major advance would be achieved if the data obtained by electronic tags could be telemetered underwater via an acoustic modem. The data could be collected when the animal swims past an acoustic receiver such as being proposed by the Ocean Tracking Network program (OTN; www. As these tools evolved, they reached a sophistication and reliability where the data collected were equivalent to the industry standards for oceanographic sampling tools. For example, elephant seals can sample the water column 60 times a day reaching depths of 1000 m under their own power across broad expanses of the ocean that are difficult to reach by ships or other conventional means (Figure 3) (Boehlert et al. 2001). The research subjects became research tools and can provide oceanographic data for a fraction of the costs and can provide coverage in regions where conventional methods do not work such as polar regions (Charrassin et al. FIGURE 3  Left: tracks of 12 southern elephant seals instrumented with ARGOS linked CTD tags. Right Top: a close up showing the actual profiles data collected; Right Middle: a close up of the temperature profiles that can be interpolated from those casts; Right Bottom: a close up of the conductivity profiles that can be inter- polated from those casts.

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128 OCEANOGRAPHY IN 2025 2008; Costa et al. 2008). At the same time technologies have been improv- ing to study the movements of smaller fish species at sea. Instrument size currently limits satellite telemetry to the largest fish species such as sharks and tunas. Archival tag technology has become sufficiently miniaturized so that juvenile fish less than 100 g can be tagged without significant increases to their mortality. However, for juvenile salmon which reliably return to a river of origin where they can be predictably captured, marine sur- vival rates are only 2-5%, making the cost of deploying archival tags prohibitive. As a result, acoustic technologies have moved to the fore- front of marine fisheries movement research. In the North Pacific alone thousands of fish from over a dozen species are now being tagged with small, relatively inexpensive acoustic transmitters, and their movements are being monitored by a growing network of acoustic arrays led by the OTN and POST. These networks are providing new insights into the movements of fish past fixed listening arrays in the ocean without the need for tag recovery. Unfortunately, these data have two limitations over the archival and satellite tag technologies. The first is a lack of oceano- graphic habitat sensors to collect data in the environment where the fish is found and second is array deployment limited to the continental shelf. These limitations could be overcome by deploying “business card tags” (BCTs) on larger marine animals such as elephant seals. BCTs are capable of alternating between transferring and receiving data from other BCTs and regular acoustic pinger tags when they come within range. As more tags are deployed there would be a high probability of regular encounters between a BCT tagged elephant seal and other acoustically tagged spe- cies. While one might consider the ocean to be vast, marine organisms are likely to converge on the same oceanographic features, dramatically increasing the probability of encounters. An added advantage is that larger marine organisms could not only carry the larger BCT tag, but could carry additional sensors that would provide information on the physical environment (e.g., CTD). References Boehlert, G.W., D.P. Costa, D.E. Crocker, P. Green, T. O’Brien, S. Levitus, and B.J. Le Boeuf. 2001. Autonomous Pinniped Environmental Samplers: Using Instrumented Animals as Oceanographic Data Collectors. Journal of Atmospheric and Oceanic Technology. 18: 1882-1893. Charrassin, J.-B., M. Hindell, S.R. Rintoul, F. Roquet, S. Sokolov, M. Biuw, D. Costa, L. Boehme, P. Lovell, R. Coleman, R. Timmermann, A. Meijers, M. Meredith, Y.-H. Park, F. Bailleul, M. Goebel, Y. Tremblay, C.-A. Bost, C.R. McMahon, I.C. Field, M.A. Fedak, and C. Guinet. 2008. Southern Ocean Frontal Structure and Sea-ice Formation Rates Revealed by Elephant Seals. PNAS. 105: 11634-11639.

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Daniel P. Costa et al. 129 Costa, D.P., J.M. Klinck, E.E. Hofmann, M.S. Dinniman, and J.M. Burns. 2008. Upper Ocean Variability in West Antarctic Peninsula Continental Shelf Waters as Measured Using Instrumented Seals. Deep Sea Research Part II: Topical Studies in Oceanography. 55: 323- 337. Estes, J.A., M.T. Tinker, T.M. Williams, and D.F. Doak. 1998. Killer Whale Predation on Sea Otters Linking Oceanic and Nearshore Ecosystems. Science. 282: 473-476. Myers, R.A. and B. Worm. 2003. Rapid Worldwide Depletion of Predatory Fish Communi- ties. Nature. 423: 280-283. Smetacek, V. and J.E. Cloern. 2008. Oceans—On Phytoplankton Trends. Science. 319: 1346- 1348.