A View of the Ocean from Pacific Predators
Barbara A. Block1, Daniel P. Costa2, Steven J. Bograd3
1Hopkins Marine Station, Department of Biology, Stanford University, Pacific Grove, California, USA
2Long Marine Laboratory, Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California, USA
3Environmental Research Division, National Oceanic and Atmospheric Administration, Southwest Fisheries Science Center, Pacific Grove, California, USA
15.1. Large Pelagic Species in the Marine Ecosystems of the North Pacific
In the oceanic realm, species diversity, population structure, migrations, and gene flow in marine pelagic species are poorly understood. Large marine animals such as whales, pinnipeds, seabirds, turtles, sharks, and tunas have behaviors and life-history strategies that involve high dispersal movements and vagile populations. Most of these animals lack obvious geographic barriers in the marine environment. Obtaining baseline information about seasonal movement patterns, regional habitat use, and location of foraging and breeding grounds has remained elusive. The population status and general oceanic movements of many species and guilds were virtually unknown in the eastern Pacific basin when Tagging of Pacific Predators (TOPP) was initiated as a field program of the Census of Marine Life. Additionally, potential effects of global climate change on species diversity, biomass, and community structure in pelagic environments remain largely unexplored and difficult to assess or predict. These are alarming facts, given that many species face an unprecedented level of exploitation from both directed fisheries and bycatch, and ecosystem management is dependent upon a scientific understanding of habitat use.
The lack of knowledge about large marine species is primarily due to the challenges inherent in studying marine animals. The sheer size of the Pacific Ocean makes it challenging to use traditional techniques such as ship surveys. In an effort to rectify this lack of knowledge the Census initiated two Pacific tagging efforts, TOPP (see www.topp.org), and the Pacific Ocean Shelf Tracking Project (POST) (www.postcoml.org; see Chapter 14). These programs proposed to use electronic tracking technology to study the movements of marine organisms in the North Pacific. In the case of TOPP, biotelemetry or biologging (use of electronic tags carried by the animal to measure its biology) became the major ecological tool of choice for advancing knowledge of multi-species habitat use. We proposed combining electronic tag technology data with oceanographic data acquired through remote sensing and, when possible, with foraging ecology and genetics. We hypothesized that the primary physical forces that influence temporal distribution patterns were temperature and primary production. We expected that by studying multiple species within an ecosystem such as the California Current, we could reveal common locations for feeding, migration highways, potential reproduction regions, and hot spots. The principal factors acting on population dynamics might be revealed, and these would include seasonal variations in thermal regimes and the formation of prey-aggregating physical features, which were assumed to cause variation in food supply, physiological performance, and predation pressures. Understanding behavior of organisms relative to the physical and biological forces they experience was considered prerequisite to a study of multi-species community structure of large pelagic species in the North Pacific Ocean.
15.2. Tagging of Pacific Predators, 2000–2008
These individuals represent the members of the various organismal working groups of TOPP. Their work and perseverance in field tagging efforts and dedication to the TOPP program made this ten-year effort possible. [more]
15.2.1. Planning and Initiation of TOPP
TOPP scientists proposed a decade-long tagging campaign to elucidate the distribution, movements, behavior, and ecological niche of apex marine predators within the oceanic ecosystems of the North Pacific Ocean. To examine whether it was possible to observe and monitor multiple species in coastal and open-ocean habitats in the North Pacific, a series of planning workshops was initiated. Ninety participants from the USA, Canada, Mexico, France, and Japan met in Monterey, California, USA, for four days in November 2000 to discuss the experimental tagging approaches, selection of organisms, and together developed the foundation deployments of the TOPP program. This workshop led to a formal TOPP plan to use biologging techniques in concert with oceanographic data, feeding studies, and molecular techniques to examine 23 top predators of the North Pacific Ocean (Block et al. 2003). After the initial TOPP workshop, ten working groups were formed and met separately to plan the details of the program and experiments, and coordinate the ocean-scale tagging efforts (Box 15.1). The working groups were concentrated around seven organismal teams (tunas, sharks, squid, pinnipeds, seabirds, cetaceans, and turtles), as well as oceanography, tag development, data management, and education and outreach. As with any project of this size and complexity the work reported here could not have been done without the participation and dedication of many individuals to the TOPP program (Box 15.1).
The workshop participants recommended a staged implementation of the TOPP program, beginning with species selection. An emphasis was placed initially on the use of current technologies that had a track record of proven deployment success in large-scale experiments (for example archival/TDR tags), on species that would most likely yield quick data returns (elephant seals, Pacific bluefin tuna). Initiation of pilot studies to explore new and potentially challenging species (for example squid and swordfish), and to test large-scale deployments or new technologies and attachment strategies were also initiated (for example spot tags on shark dorsal fins, archival tags on shearwaters). After the successful completion of this testing and development phase (2003–2005), a second round of field efforts focused on increasing the scale of the tag deployments throughout the program (2006–2009). Large-scale deployments (approximately 3,000 tags) of existing and new technologies across multiple taxa in a synoptic seasonal pattern occurred. Central to the TOPP plan was selection of approximately two dozen key target species that had distributions within the eastern and central North Pacific Ocean and were tractable for tagging and population studies. The implementation plan built on the known tagging success of key species during the early years, to inform the selection of TOPP target species. The tag data would be combined with in situ and remotely sensed oceanographic observations to build a decade-long survey of key species in the North Pacific Ocean. As data began to be collected, TOPP scientists focused on the improvement of electronic tagging technology, implementation of simultaneous large-scale tagging, development of a data acquisition system capable of handling multiple tagging platforms, and integration and visualization of multiple data streams and initiation of four-dimensional display.
Workshop deliberations and early tagging experiments generated a list of key animals that became the research subjects of TOPP (Box 15.2, p. 308). This included a diverse group of species with interesting ecological linkages. One key concept that emerged early in the program was the focus on tagging of guilds of closely related species. The TOPP species guilds include sharks of the family Lamnidae (white, mako, and salmon), fish of the Thunnus guild (yellowfin, bluefin, and albacore), albatrosses (black footed and Laysan), pinnipeds (elephant seals, California sea lions, and northern fur seals), rorqual whales (blue, fin, and humpback whales), and sea turtles (loggerheads and leatherbacks). The guild concept turned out to be among the most successful ideas in TOPP for exploration of the oceanic environment harnessing the evolutionary power for related species. By using this classic comparative approach, we were able to examine how organisms of similar phylogeny have diverged in their niche use and foraging ecology and the physiological mechanisms used (Feder 1987; Costa & Sinervo 2004). Additionally, we found that tagging techniques could easily be passed on to multiple species, improving the trophic connections and comparative methodologies (Block 2005). Several additional species that shared similar habitats complemented the original guild species. These species included blue and thresher sharks that overlapped with the lamnid guild, molas that were common in the tuna guild ecosystem, and shearwaters that overlapped with the albatross guild. The guild approach simplified the logistics of the tagging efforts. More than one species within a guild is often found in the same region at the same time of year, making it possible to maximize the success of the tagging effort by using a single platform to tag multiple species. Details of the types of tag used, and how tag technology progressed during TOPP, are given below.
TOPP species. The species in this list were chosen by the organismal working groups as having those biological and ecological attributes meeting the goals of the TOPP program.
Leatherback turtle, Dermochelys coriacea
Loggerhead turtle, Caretta caretta
Black-footed albatross, Phoebastria nigripes
Laysan albatross, Phoebastria immutabilis
Elephant seal, Mirounga angustirostris
California sea lion, Zalophus californianus
Northern fur seal, Callorhinus ursinus
Blue whale, Balaenoptera musculus
Fin whale, Balaenoptera physalus
Humpback whale, Megaptera novaeangliae
Sperm whale, Physeter macrocephalus
Sooty shearwater, Puffinus griseus
Pink shearwater, Puffinus creatopus
Fish, shark, and squid
Bluefin tuna, Thunnus thynnus orientalis
Salmon shark, Lamna ditropis
Yellowfin tuna, Thunnus albacares
Blue shark, Prionace glauca
Albacore tuna, Thunnus alalunga
Common thresher shark, Alopias vulpinus
Humboldt or giant squid, Dosidicus gigas
Mako shark, Isurus oxyrinchus
Ocean sunfish, Mola mola
15.2.2. Developing Tag Technologies for Marine Biologging
Biologging technology allows researchers to take measurements from free-swimming marine animals as they move undisturbed through their environment. Importantly, it permits researchers to observe animals beyond the natural reach of humans, and provides extensive data on both the animals' behavior and their physical environment. Biologging can be used for observational studies of animal behavior, controlled experimental studies (translocation experiments), oceanographic observations of the in situ environment surrounding the animal, and ecological research such as foraging dynamics.
An early challenge for TOPP was to solve the many technological issues associated with the tag platforms before launching the major deployment phase. For the first three years of TOPP deployments (2001–2004), the priority was to develop efficient deployment strategies of proven technologies, while simultaneously investing in and testing new tags. TOPP worked with four manufacturers of commercial tags and advised significant engineering decisions, which over the course of a decade led to advancements in all major tag types used. Testing included a development phase with new ARGOS transmitters, Fastloc GPS, novel sensors with oceanographic capabilities, increased memory, miniaturization, new track filtering, and data compression algorithms (Teo et al. 2004a, 2009; Kuhn & Costa 2006; Tremblay et al. 2006, 2007, 2009; Biuw et al. 2007; Bailey et al. 2008; Kuhn et al. 2009; Costa et al. 2010a; Simmons et al. 2009).
Stable and prototype electronic tags were both available in 2000. They ranged from ARGOS tags to data storage tags (archival) that could be attached or implanted surgically, and pop-up satellite archival tags designed to track large-scale movements and behavior of animals for which the use of real-time ARGOS satellite tags was not possible. The pop-up satellite tags jettisoned from the animal on a pre-programmed date and transmitted data about depth, ambient temperature, pressure, and light to ARGOS satellites (Block et al. 1998). Each generation of the tags had technological issues that included the accuracy of sensors, the resilience of tag components, pressure housing problems, and algorithm limitations. In the first phase of TOPP we tested many of the tags on free-ranging animals to ensure that they would be sufficiently robust for the larger-scale deployments in the second phase.
Tag attachment strategies were another early challenge. Strategies were shared among organismal working groups, and the increased communication with multiple taxa specialists helped to facilitate the exchange of ideas and techniques. In addition, the increased memory capacity of the new tags, and the scale of the TOPP deployments, resulted in the need for investment in a novel data management system, improved analytical and visualization tools, and methods to synthesize a vast array of disparate data streams (Teo et al. 2004b; Tremblay et al. 2006, 2007, 2009; Bailey et al. 2008). Simply put, TOPP is the first large-scale tagging program to implement automation of the ARGOS and geolocation tag management, metadata delivery, and integration of online data display in near-real-time with oceanographic data information. A public display in a browser format (las.pfeg.noaa.gov/TOPP) was developed for the TOPP team members and education and outreach.
Four broad classes of electronic tags were tested, refined and/or developed, and deployed as part of the TOPP program.
18.104.22.168. Archival Tags
Archival tags log high-resolution time-series data from sensors that measure pressure, water temperature, body temperature, salinity, and light level (Biuw et al. 2007; Simmons et al. 2009; Teo et al. 2009; Costa et al. 2010b). Archival tags are either implanted in the animal (fish), glued to the hair or feathers (birds and mammals), or attached to a leg band (birds). The major limitation of this tag type is that it must be recovered to obtain the data. In fish this tag can only be used on highly exploited species (tunas) where an enhanced reward is offered to recover the tag after capture. Archival tags are also used with species that have a high probability of returning to the colony where they were initially tagged (that is, sea lion, elephant seal, albatross, and shearwater). Archival tags have provided tracks covering up to 1,000 days in northern bluefin tuna (Block et al. 2001; Block 2005) and 1,160 days in yellowfin tuna (Schaefer et al. 2007). These tags were a mainstay of the TOPP program, with over approximately 1,600 light, temperature, depth (LTD) (Lotek) 2310 tags deployed, primarily on bluefin (Kitagawa et al. 2007; Boustany et al. 2010), yellowfin (Schaefer et al. 2007, 2009) and albacore tunas. This archival tag (D-series) has a pressure accuracy of ±1% of the full-scale reading (up to 2,000 m). The LTD temperature ranged from –5 to 40 °C, with an accuracy of 0.05 °C. The temperature response is less than 2 seconds, so that as an animal dives, it provides a temperature profile with depth (Simmons et al. 2009). In the TOPP program, archival tags were used primarily on tunas that were juveniles (3–20 kg) and adolescents (up to 55 kg). The smallest animal tagged was the sooty shearwater (Shaffer et al. 2006), weighing approximately 800 g. For this, we used the smallest archival tag the Lotek LTD 2410 that weighs only 5.5 g and is 11 mm in diameter and 35 mm long.
Archival tags often carry sensitive optical detectors that can measure variations in light level quite accurately. The Lotek 2310 tag used by TOPP has a polystyrene light stalk that extends externally from an animal after it has been surgically implanted. The wall of the stalk contains a fluorescent dye that is sensitive to narrow band blue light (470 nm) passing through the side wall of this optical fiber. When excited, it radiates light in the green wavelengths and focuses the light down the base of the fiber where it is detected by a photodiode. The photodiode is used to convert the flow of photons into a flow of electrons that is measured with an electrometer with about 9 decades of range, allowing detection of sunrise and sunset while a tuna is cruising at depths. On board or post-processing algorithms allow construction of light-level curves and the calculation of local apparent noon to determine longitude. Estimates of time of sunrise and sunset are used to determine day length and latitude using threshold techniques (Hill & Braun 2001; Ekstrom 2004). These locations can be improved by using archival tag observed measurements of sea surface temperature, and TOPP research with double tag datasets provided a robust improvement for these algorithms (Teo et al. 2004a). Archival tags have also been used to estimate in situ chlorophyll concentrations (Teo et al. 2009).
22.214.171.124. ARGOS Satellite Tags
Satellite tags provide at-sea locations and have the advantage that the data can be recovered in real time and remotely without the need to recover the tag. The satellites are operated by CLS-ARGOS (Toulouse, France, or Landover, Maryland, USA) and the data are acquired from this service over the Internet. Because the antenna on the satellite transmitter must be out of the water to communicate with an orbiting ARGOS satellite, the technology has mainly been used on air-breathing vertebrates that surface regularly (McConnell et al. 1992a, 1992b; Le Boeuf et al. 2000; Polovina et al. 2000; Weimerskirch et al. 2000; Shaffer & Costa 2006). A significant innovation of the TOPP program was the realization that satellite tags could be effectively deployed on sharks (Weng et al. 2005; Jorgensen et al. 2010). For large fish, sharks, or other animals that remain continuously submerged, the ability to transmit to ARGOS at the surface is not possible. For these organisms, a pop-up satellite archival tag (PSAT) was developed (Block et al. 1998, 2001; Lutcavage et al. 1999; Boustany et al. 2002). Pop-up satellite archival tags combine data-storage tags with satellite transmitters. These tags are externally attached and are programmed to release or pop off at a preprogrammed time. The pop-up satellite devices communicate with the ARGOS satellites that serve both to uplink data and calculate an end-point location. Importantly, the tags are fisheries-independent in that they do not require recapture of the fish for data acquisition. The Mk10Pat model, the most used in TOPP, has a pressure sensor with resolution of about 0.5 dBar. The temperature accuracy improved as an external thermistor was tested and used to improve acquisition of oceanographic quality data (temperature accuracy is ±0.1°C with 0.05 °C accuracy from about –5 to 40 °C) (Simmons et al. 2009). The temperature response is less than a second over a 70% step in this range. Further advances in the form of data compression have made it possible to get significantly more data through the limitations of the ARGOS system, including detailed oceanographic and behavioral information (Fedak et al. 2001). ARGOS satellite tags are larger than archival tags, with the smallest unit weighing 30 g.
126.96.36.199. GPS Tags
With funds from the National Oceanographic Partnership Program (NOPP), TOPP supported the development of a GPS tag for use on marine species (Decker & Reed 2009; Costa et al. 2010b). The advantage of GPS tags is twofold. First, GPS tags provide an increase in the precision of animal movement data to within 10 m compared with the 1–10 km possible with ARGOS satellite tags. Second, GPS tags provide a higher time resolution, with positions acquired every few minutes compared with a maximum of about eight to ten positions a day with ARGOS. However, standard navigational GPS units do not work with diving species, as they require many seconds or even minutes of exposure to GPS satellites to calculate positions and the onboard processing consumes considerable power. At the beginning of the TOPP project, two conceptual solutions to this problem were identified and resources invested in the development and testing of the Fastloc system developed by Wildtrack Telemetry Systems (Leeds, UK). The Fastloc uses a novel intermediate solution that couples brief satellite reception with limited onboard processing to reduce the memory required to store or transmit the location. This system captures the GPS satellite signals and identifies the observed satellites, calculates their pseudo-ranges without the ephemeris or satellite almanac, and produces a location estimate that can be transmitted by ARGOS. Final locations are post-processed from the pseudo-ranges after the data are received using archived GPS constellation orbitography data accessed through the Internet. Although this technology provides a major advance in our ability to monitor the movements and habitat use of marine animals (Fig. 15.1), TOPP researchers have also used these tags to validate the error associated with ARGOS satellite locations (Costa et al. 2010a).
188.8.131.52. Conductivity, Temperature, and Depth Tags
A fundamental component of the TOPP program was a desire to further the development of using animals to collect oceanographic data. This served two functions: the first was to acquire physical oceanographic data that were not otherwise available, and the second was to collect physical environmental data at a scale and resolution that matched the animal's behavior. As with the GPS tag, funds from the NOPP program allowed TOPP to support the development and testing of a reliable and commercially available conductivity, temperature, and depth (CTD) tag for animals, in collaboration with the Sea Mammal Research Unit at St. Andrew's University, UK (SMRU; www.smru.st-andrews.ac.uk). A conductivity–temperature–depth satellite relay data logger (CTD-SRDL) incorporates a Valeport CTD sensor with pressure accuracy ±5 dBar, temperature resolution of ±0.001 °C, with an accuracy of 0.01 °C and an inductive coil for measuring conductivity with resolution of ±0.003 mS cm –1. The tag is optimized to collect oceanographic data at the descent and ascent speeds exhibited by seals (approximately 1 m s –1). In addition to collecting data on an animal's location and diving behavior, it collects CTD profiles (Fig. 15.2). The tag looks for the deepest dive for a 1- or 2-hour interval. Every time a deeper dive is detected for that interval, the tag begins rapidly sampling (2 Hz) temperature, conductivity, and depth from the bottom of the dive to the surface. These high-resolution data are then summarized into a set of 20 depth points with corresponding temperatures and conductivities. These 20 depth points include 10 predefined depths and 10 inflection points chosen by a “broken stick” selection algorithm (Fedak et al. 2002). These data are then held in a buffer for transmission by ARGOS. Given the limitations of the ARGOS system, all records cannot be transmitted; therefore a pseudo-random method is used to transmit an unbiased sample of stored records. If the SRDLs are recovered, all data collected for transmission, whether or not it was successfully relayed, can be recovered. The use of these tags has led to insights into both the animal's behavior relative to its environment (Biuw et al. 2007) as well as the physical oceanography (Boehme et al. 2008a, 2008b; Charrassin et al. 2008; Nicholls et al. 2008; Costa et al. 2010b).
15.2.3. Top Predator Distributions and the Discovery of Basin-Scale Migrations
One of the principal results of the TOPP program was a new understanding of the distribution and migration patterns of a suite of apex marine predators. Over the course of the TOPP program, 4,306 animals, representing 23 species (Box 15.2), were equipped with a variety of sophisticated tags carrying high-resolution sensors (Figs. 15.1A and B). The predators recorded data on their position, the ocean environment, habitat use, and behaviors while traveling remarkable distances underwater. The dataset yielded many surprises and demonstrated for the first time seasonal patterns and fidelity to the eastern Pacific for many species tagged in TOPP and unlimited boundaries when roaming over vast reaches of the Pacific Ocean for others (Figs. 15.3, 15.4, and 15.5). For example, white sharks show a coastal to offshore migration from California nearshore waters to offshore waters of Hawaii and back, resulting in homing behavior (Boustany et al. 2002; Weng et al. 2007a; Jorgensen et al. 2010). Salmon sharks move from the Arctic to the sub-tropical reaches of the North Pacific Ocean and back to the foraging grounds in Prince William Sound (Weng et al. 2005), whereas bluefin tuna and loggerhead turtles range across the North Pacific, breeding in the western Pacific but migrating as juveniles and adolescents to the eastern Pacific to take advantage of the highly productive California Current (Peckham et al. 2007; Boustany et al. 2009). Leatherback turtles tagged on their nesting beaches in Indonesia cross the Pacific basin to feed off central California, whereas sooty shearwaters use the entire Pacific Ocean from the Antarctic to the Bering Sea (Shaffer et al. 2006). These trans-oceanic journeys require remarkable animal navigation, energetics, and philopatry. The TOPP species that best illustrate these trans-oceanic migrations are the Pacific bluefin tuna, the sooty shearwater, and the leatherback turtle.
|Figure 15.4 The migrations of sooty shearwaters. From Shaffer et al. 2006.
184.108.40.206. Pacific Bluefin Tuna
Pacific bluefin tuna are one of three species of bluefin tuna that inhabit subtropical to subpolar seas throughout the world's oceans. Among Thunnus, Pacific bluefin tuna have the largest individual home range, being found throughout the North Pacific Ocean and ranging into the western South Pacific (Collette & Nauen 1983). Pacific bluefin tuna remain in the western Pacific after being spawned (near the Sea of Japan) but a proportion of the juveniles make extensive migrations into the eastern Pacific late in the first or second year (Bayliff 1994; Inagake et al. 2001). It has been hypothesized that the trans-Pacific migrations from west to east are linked to local sardine abundances off Japan (Polovina 1996). TOPP researchers deployed over 600 archival tags on juvenile Pacific bluefin in the eastern Pacific. Recovery rates ranged from 50% to 75%, indicative of high mortality on these juveniles. The bluefin tagged displayed a cyclical pattern of movements on a seasonal scale that ranged annually from the southern tip of Baja California to the coast of Oregon (Boustany et al. 2010). This seasonal signal was apparent and provided the first clear signal that the California Current has a seasonality that many TOPP species (bluefin, yellowfin, and albacore tunas, blue whales, lamnid sharks, and shearwaters) were following. Approximately 5% of the recovered tagged bluefin tuna migrated back into the western Pacific using the North Pacific Transition Zone (Fig. 15.3). Large adult Pacific bluefin tuna were also tagged in the south Pacific off New Zealand during TOPP (Fig. 15.1). The emerging story is of a Pacific bluefin that travels across the entire North Pacific Ocean as a juvenile and adolescent, and that is capable of post-spawning migrations from the North Pacific to the South Pacific. Taken together, the electronic tag data on adolescents and adults demonstrate this tuna species encompasses one of the largest home ranges on the planet.
220.127.116.11. Sooty Shearwaters
Equally impressive was the TOPP observation with archival tags that sooty shearwaters that breed off the Southern Islands of New Zealand cross the equator to feed in diverse regions of the North Pacific Ocean, from Japan to Alaska and California (Shaffer et al. 2006, 2009). We were able to document this trans-equatorial migration using newly developed miniature archival tags that log data for estimating position, dive depth, and ambient temperature. The Pacific Ocean migration cycle had a figure-eight pattern (Fig. 15.4) while traveling, on average, 64,037 ± 9,779 km round trip over 198 ± 17 days. This is the longest migration of any individual animal ever tracked. Shearwaters foraged in one of three discrete regions off Japan, Alaska, or California before returning to New Zealand through a relatively narrow corridor in the central Pacific Ocean. These migrations allow shearwaters to take advantage of prey resources in both the Northern and Southern hemispheres during the most productive periods; in other words, they exist in an “endless summer.”
18.104.22.168. Leatherback Turtles
Two distinct populations of leatherback turtles were tagged during TOPP: one that breeds on the Indonesian islands of the western Pacific and another that breeds on the beaches of Costa Rica. A portion of the tagged western Pacific leatherbacks undergo remarkable trans-Pacific migrations, arriving off the coast of California in late summer to forage on dense aggregations of jellyfish. The eastern Pacific population, in contrast, undergoes a cross-equatorial migration that takes them into the oligotrophic waters of the eastern subtropical South Pacific (Shillinger et al. 2008). Nearly all of the tagged eastern Pacific leatherbacks made this journey, traversing a relatively narrow migration corridor through the highly dynamic equatorial Pacific. The apparently different migration and foraging strategies of these two populations of Pacific leatherbacks was another surprise result of TOPP.
15.2.4. Identification of Biological Hot Spots, Niche Separation, Homing, And Fidelity
In addition to identifying trans-oceanic migration routes, another fundamental result of the TOPP program was the identification of critical foraging habitat, migration corridors, and regions of high occupancy: that is, biological hot spots. The identification and characterization of biological hot spots is a new focus in marine ecological research, with important implications for understanding ecosystem functions, prioritizing habitat for marine zoning, and managing targeted fisheries populations (Worm et al. 2003; Sydeman et al. 2006). Although it is well known that top predators, including large predatory fishes, cetaceans, pinnipeds, sea turtles, marine birds, and human fishers, congregate at locations of enhanced prey (Olson et al. 1994; Polovina et al. 2000), little is known about why particular regions or physical features are hot spots, how the animals locate and use these features, and what trophic interactions occur within the hot spots. The inaccessibility of open ocean hot spots has precluded systematic field studies that could elucidate the physical characteristics and ecological function of biological hot spots. The TOPP dataset has provided a unique view of North Pacific top predator hot spots, allowing us to address several compelling questions. What conditions occur within hot spots to make these areas of confluence for a diverse set of species? What are the physical characteristics and spatial-temporal persistence of the hot spots? What are the behavioral responses of different species when they enter a hot spot? What trophic interactions occur within hot spots? How can a better understanding of critical habitat result in enhanced conservation and management of these species?
Efforts at studying biological hot spots have relied on two complementary approaches. From a “bottom-up” perspective, standard oceanographic sampling (particularly remote sensing) can be used to describe ocean features of relevance to apex pelagic predators. This approach has several advantages: (1) it can provide global, near-real-time views of the ocean surface; (2) it can identify regions of enhanced biological activity (from ocean color); (3) it can identify features that are persistent or recurrent in space and time, which may be appealing areas for migratory animals; and (4) it can describe the dominant scales of ocean variability, from which hot spots can be classified (that is, based on their spatial-temporal scale, their degree of persistence or recurrence, their forcing mechanisms, and their potential biological impacts) (Palacios et al. 2006).
A more direct “top-down” approach is to let the animals identify and describe hot spots through large-scale tagging studies such as TOPP (Costa 1993; Block et al. 2001, 2003; Block 2005; Costa et al. 2010b). This approach allows (1) a direct detection and observation of the preferred habitats of the animals; (2) a matching of behavioral cues to local oceanographic conditions; (3) a differentiation of behavioral responses in relation to ocean features, allowing a classification of hot spots by their ecological function (for example, aggregation, migration, foraging, diving, and breeding); and (4) a differentiation between species-specific hot spots and hot spots that are biologically diverse and more universally occupied. Understanding the oceanographic, ecological, and physiological factors that are important in attracting apex marine predators to these hot spots, and determining how and why they remain retentive to these species, is a continuing research aim of TOPP and will likely be one of its primary legacies.
Two oceanographic regions that have emerged as key top predator hot spots in the North Pacific Ocean are the California Current and the North Pacific Transition Zone, which are described in detail below.
The California Current ecosystem (CCS) has emerged as a major hot spot for more than a dozen exploited, protected, threatened, or endangered predators that range throughout the eastern Pacific, including leatherback and loggerhead turtles, sooty shearwaters, Laysan and black-footed albatrosses, blue and humpback whales, sea lions, northern fur seals, elephant seals, bluefin, yellowfin and albacore tunas, white, makos, salmon, blue, and thresher sharks. The CCS is a highly productive eastern boundary current system, driven by seasonal coastal upwelling, which maintains numerous economically important marine fisheries. This region is characterized by strong cross-shore gradients in physical and biological fields, is strongly modulated by seasonal wind forcing and Ekman dynamics, and has a complex and energetic current structure (Hickey 1998; Palacios et al. 2006). These dynamics contribute to the aggregation of prey and, hence, top predators. Within the California Current, several areas have emerged as critical multi-species hot spots. These include areas we have designated as the California Marine Sanctuaries Hot Spot (CMHS), the Southern California Bight Hot Spot (SCBHS), and the Baja California Hot Spot (BCHS).
TOPP data have shown that the North Pacific Transition Zone (NPTZ) is equivalent to a major top predator highway across the North Pacific Ocean. Bluefin and albacore tunas, albatrosses, shearwaters, elephant seals, fur seals, and turtles all occur with great frequency in this region. The NPTZ is a complex region encompassing an abrupt north to south transition from subarctic to subtropical water masses, has an abundance of energetic mesoscale features (fronts and eddies), and is dominated by biological patchiness (Roden 1991). Interactions between eddies and the mean flow create transient jets and submesoscale vortices, resulting in up- and downwelling patches a few kilometers across that contribute to this biological patchiness (Woods 1988; Roden 1991). This large basin-scale frontal feature serves as a primary foraging area and migratory corridor for most of the TOPP predators that undergo trans-oceanic movements.
The CCS and NPTZ hot spots support several important ecological functions for North Pacific top predators. TOPP data has also revealed distinct niche separation among TOPP guilds that use these regions (Figs. 15.1, 15.3, and 15.7). At the initiation of the Census we knew that there were differences in the thermal tolerances of marine predators. As a result of the TOPP program, we now know that the physiological tolerance of marine predators, their energetics, and physiological constraints on the cardiac system (Weng et al. 2005) determine the home range of many of the TOPP species. For example, endothermy enables birds, mammals, salmon sharks, and bluefin tuna to range over vast regions of the North Pacific Ocean, including the colder temperate and subarctic oceans. In contrast, species such as yellowfin tuna, mako, and blue sharks are more constrained in their thermal tolerances to the warm temperate to subtropical waters of the North Pacific Ocean. The clear separation in habitat between members of fish or shark guilds occurs primarily by thermal preferences, with sister taxa (for example yellowfin and bluefin) occupying warm to cold environs on a latitudinal scale. Secondly, diet has emerged as a major factor in niche separation. For example, adult white sharks show a marine mammal preference and hence are localized for a portion of the year near pinniped colonies close to shore, whereas mako sharks primarily eat fish and are more frequently associated with the continental shelf and slope areas (Pyle et al. 1996; Anderson et al. 2008; Goldman & Musick 2008; Jorgensen et al. 2010). Advances in electronic tagging in TOPP, combined with genetic research, have made it possible to discern the importance of philopatry for population structure of pelagic marine predators once thought to be panmictic (Jorgensen et al. 2010). These results are illustrated below for several of the TOPP guilds.
|Figure 15.7 Map of individual SSSM-derived tracks for 92 tags on blue whales, Balaenoptera musculus, deployed between 1994 and 2007 that transmitted for more than seven days, color coded by deployment location. In each panel the four tag deployment locations are shown as white circles, the annual climatological position of the CRD as a white contour, and the bathymetry as shades of blue. Map projection: sinusoidal (equal area). From Bailey et al. ( 2010).
TOPP has recorded more than 92,000 days of archival tag data for Pacific, yellowfin, and albacore tunas occupying the California Current (Schaefer et al. 2007, 2008; Boustany et al. 2010). Pacific bluefin are spawned in the waters off Japan and recruit to the eastern Pacific late in year one or as two-year-olds. TOPP tagging was conducted in the eastern Pacific on individuals from 2 to 5 years of age, and most fish remained in the eastern Pacific for several years (Kitagawa et al. 2007; Boustany et al. 2010). The principal pan-tuna hot spot was the SCBHS, which has ample bathymetric forcing and seasonal upwelling that may attract the prey these species feed upon. Furthermore, the region is within the thermal preferences of all three species for a large part of the year. Tunas show latitudinal movement patterns that were correlated with peaks in coastal upwelling-induced primary productivity (Boustany et al. 2009). Habitat use distributions derived from kernel density analyses of daily geolocations indicate that all three CCS hot spot regions are occupied by one or all three Thunnus species in a predictable seasonal pattern. Each species showed distinct thermal preferences that lead to spatial and temporal separation of the species. Bluefin and albacore showed distinct geographic areas of niche overlap, but diel distinctions in their vertical movements. Pacific bluefin fed in the mixed layer, consistent with a forage preference for sardines and anchovy, whereas albacore tended to occupy the deep scattering layer. Interannual variation in the locality of the productivity peaks can be linked to movement patterns of the tunas (Boustany et al. 2010).
Perhaps no marine predators have been more challenging to study than the large predacious sharks of the lamnid guild. This includes closely related species such as the white, mako, and salmon shark. The lamnids, along with blue and thresher sharks, have been heavily studied in TOPP (Weng et al. 2005, 2007b, 2008), with more than 50,000 days of tracking data obtained. Among the lamnid sharks there is a remarkable niche diversification, with salmon sharks occupying the most expansive regions ranging from northern cold-temperate to subpolar habitats and occupying year round temperatures below 6 °C. They frequent Prince William Sound, the Alaskan Gyre, the North Pacific Subtropical Gyre, and the CCS. White sharks move from the CCS to the oligotrophic regions of the central Pacific and back. Mako sharks use the CCS throughout the North American continental shelf, overlapping with the blue and thresher sharks. TOPP data have shown that the three lamnid sharks have very little overlap in niche use. In fact, there appears to be diversification of habitat use for most of the year, with each shark group being specialized for foraging on specific prey items. Adult white sharks use marine mammals, salmon sharks eat pollock and herring, and makos and blues appear to specialize on sardines and squid (Pyle et al. 1996; Anderson et al. 2008; Goldman and Musick 2008; Lopez et al. 2009). The tagging has provided an oceanic view of the habitat selection and niche use of closely related groups of sharks. Again, the SCBHS emerges as an important foraging region and nursery ground for blue, mako, thresher, and juvenile white sharks.
White sharks are a cosmopolitan species that occur circumglobally. In TOPP we combined satellite tagging, passive acoustic monitoring, and genetics to reveal how eastern Pacific white sharks adhere to a highly predictable migratory cycle (Fig. 15.5) (Jorgensen et al. 2010). Pop-up satellite tagging revealed how individual sharks return to the same network of coastal hot spots following distant oceanic migrations, and comprise a population genetically distinct from previously identified phylogenetic clades. The homing behavior has been hypothesized to have led to the separation of the (TOPP-tagged) northeastern Pacific population after an introduction from Australia/New Zealand migrants during the late Pleistocene. Mitochondrial DNA collected from samples obtained during tagging provided independent evidence for a demographically independent management unit not previously recognized. This fidelity to discrete and predictable migration pathways and locations offers clear population assessment, monitoring, and management options vital for ensuring the white sharks' protection.
Satellite tags directly attached to the dorsal fin of salmon sharks have provided long-term datasets (as long as four consecutive years) on the movements and environmental preferences of female salmon sharks in the eastern Pacific (Weng et al. 2005, 2007b). This research has shown that there are repeated annual patterns of migration in the eastern North Pacific of the population being tagged in Alaska, and incredible fidelity to Prince William Sound (the location of deployments). Salmon sharks are believed to use the southern extent of their range as nursery areas; in particular, regions around the NPTZ (Nakano & Nagasawa 1996) and potentially even the CCS (Goldman & Musick 2006) are believed to be parturition areas, suggesting that movements to and within these hot spots may be related to reproductive activities.
Albatrosses and shearwaters are highly migratory species, traveling widely across entire ocean basins and passing through many territorial regions. The highly productive CCS is a major destination for seabirds traveling from as far away as New Zealand (Shaffer et al. 2006). Previous research has shown that black-footed albatrosses travel from breeding colonies in the Northwest Hawaiian Islands (NWHI) to the west coast of North America to forage within the CCS during breeding (Hyrenbach et al. 2002). This was verified with a greater time-series and tracking effort during the TOPP program (Kappes et al. 2010) (Figs. 15.4 and 15.6). However, visits to the CCS are typically on the order of days because adults must return to feed their chicks. We have now tracked adult albatrosses during the post-breeding exodus and their subsequent return to breeding, a period lasting about 160 days. Using archival data loggers, our data show that black-footed albatrosses from NWHI spend several months within the CCS, whereas Laysan albatrosses from the same colony use the habitat of the NPTZ (Shaffer et al. 2009; Kappes et al. 2010). The oceanographic conditions that black-footed albatrosses experience within the CCS, warmer water temperatures, higher productivity, and lower sea surface height were quite different than those experienced by Laysan albatrosses (Kappes et al. 2010), reflecting a difference in preferred foraging habitat.
Blue and humpback whales showed consistent use of the CCS, moving from as far south as the Costa Rica Dome in the eastern tropical Pacific to regions off Oregon and Washington (Fig. 15.7). The occurrence of area restricted search behavior throughout the migration cycle, including the Eastern Tropical Pacific, provides evidence that these animals forage year-round (Bailey et al. 2010). The extent of their northward migration from Baja California to Washington during summer/fall varied significantly interannually, likely in response to environmental changes affecting their prey. Most blue whales traveled within 100–200 km of the California coast, although individuals ranged offshore up to 2,000 km. In contrast, humpback whales remained closer to the coast. The blue whales moved at higher speeds and also appeared to be more transient, with movements up and down the coast, than the humpbacks. One whale that was tracked for more than 16 months repeated much of the previous year's pattern during the fall and winter, with multiple offshore routes during the southward migration. Humpback migration routes extended from California and Oregon to southern breeding areas, including one whale with an extended stay in the Banderas Bay region of Mexico and another venturing farther south off Nicaragua. These tracks provide the first evidence for the actual route, rate of speed, and timing of the southbound migration for California humpback whales to their breeding areas. Although sample sizes are still limited compared with other TOPP species, there are general patterns emerging about the behavior and habitat use of large whales. In general, blue whales move farther from shore into deeper water than the humpback whales, probably reflecting the differences in diet between the two species. Blue whales feed on euphausids, whereas the humpback whales have a more generalized diet, which includes small schooling fish found predominately nearshore (Fiedler et al. 1998; Clapham 2009; Sears & Perrin 2009). The long track durations obtained from electronic tagging have provided essential new information about the critical habitats of eastern Pacific whale populations.
22.214.171.124. California Sea Lions
Just as TOPP has shown that animals move across large ocean basins, TOPP data have also revealed that animal distributions can be significantly affected by climate fluctuations. California sea lions feed throughout the highly productive CCS, with male sea lions moving from the breeding grounds of the Southern California Islands to winter foraging grounds along the coasts of California, Oregon, and Washington. In contrast, female California sea lions remain mostly in and around the Southern California Bight, as they are limited by the need to return to their dependent pups on the breeding islands. However, we have documented changes in the foraging patterns of California sea lions in response to anomalous warming in the CCS. During what could be considered a normal winter of 2003–04, adult male sea lions remained close to the California coast and the durations of their foraging excursions averaged 12 hours, feeding almost exclusively over the continental shelf during trips lasting only 0.8 days. This pattern markedly contrasts with that of the 2004–05 season, where male sea lions traveled 300–500 km offshore for durations of 2.5 days on average, though longer trips also occurred (Weise et al. 2006). During spring and summer of 2005, the seasonal upwelling pattern was greatly delayed, resulting in the most spatially extensive and persistent sea surface temperature and primary productivity anomalies in the CCS since the 1997–98 El Niño. Although there was no seasonal variation in the proportion of time male sea lions spent surface swimming during 2003–04, there was a monthly increase during 2004–05 that corresponded to the increasing SST anomaly. Anomalous conditions in 2005 led to large disruptions in the trophic structure of the fish community off California during 2005. These geographic shifts in prey distribution were reflected in the diet of sea lions in central California. Sardine and rockfish were more abundant in the diet during 2005 compared with 2004, whereas market squid and anchovy declined. This redistribution of prey probably forced sea lions to search farther from shore and spend more time swimming at sea in 2005.
126.96.36.199. Elephant Seals
Female northern elephant seals forage across the highly productive regions of the NPTZ. However, the use of the NPTZ is seasonal, with the greatest number of females foraging there during their longest at-sea migration over the summer months and the fewest in the winter/spring, when the females are on shore pupping or conducting shorter foraging trips (Fig. 15.8). The TOPP program was able to extend our knowledge of the foraging patterns of elephant seals and track animals from colonies that represent the southern (San Benitos Islands, Baja, Mexico) and northern (Año Nuevo California) limits of their range. These two colonies span the entire known breeding range of northern elephant seals, a distance of 1,200 km. Tracking seals over their extant range has provided a more complete understanding of the foraging ecology of this species throughout the North Pacific Ocean. Interestingly, females from the southernmost regions travel further to reach the same regions of the NPTZ used by females transiting from the northern colonies. Data from repeat trips suggest that female elephant seals rely on the persistence of the NPTZ as a key foraging ground, as they return to the same region year after year. Although these repeat visits have been seen in females over a two- to three-year period, the most impressive repeat track was from a female first tagged in 1995 when she was six years old and then tagged again 11 years later. What is remarkable about this record is the two tracks are almost identical.
|Figure 15.8 Kernel density plots showing the seasonal changes in the use of the North Pacific Ocean by female northern elephant seals. The numbers above each panel reflect the number of individual tracks used to create the image.
15.2.5. Conservation Applications
Many TOPP species are harvested by human fishers whereas others are caught indirectly as a byproduct of fishing activities (loggerhead and leatherback turtles, shearwaters, and albatross). Tracking data show that TOPP species (tuna and sharks) do not recognize political boundaries and travel through the exclusive economic zones of many countries, making it clear that these species require multinational protection. For example, Laysan albatrosses tagged at Guadalupe are found within the CCS and within at least three different exclusive economic zones. Pacific bluefin tuna that were spawned in the western Pacific were found to be so overexploited in the eastern Pacific that approximately 65% of the tags were recovered over the course of TOPP archival tagging, and few individuals lived long enough to make trans-Pacific migrations back to the spawning grounds near Japan. Similarly, over 50% of TOPP yellowfin tags were recovered, indicative of high purse seine effort in the Baja California region.
TOPP data have been used by several national and international bodies. For example, TOPP data have been used in listing black-footed albatrosses as an endangered species by the US Fish and Wildlife Service and have been incorporated into BirdLife International and the US Fish and Wildlife Service for deliberations within the international Agreement for the Conservation of Albatrosses and Petrels. The discovery of a persistent and predictable migration corridor for eastern Pacific leatherback turtles (Shillinger et al. 2008) also led to an International Union for Conservation of Nature resolution to conserve this endangered species in the open seas. Another example of a successful conservation application in TOPP was the creation of a marine protected area off the coast of Baja California to protect loggerhead turtles (Fig. 15.9) (Peckham et al. 2007). The satellite and acoustic tagging of white sharks, combined with a new Bayesian model to provide population estimates, have provided a baseline for future studies focused on monitoring and assessing the white shark population (Jorgensen et al. 2010; T. Chapple, unpublished observations). Over the course of the program, the TOPP team has shown that monitoring population trends and designing new tools for the protection of pelagic predators is possible. These efforts can be used as templates for future work or expanded to include multiple species.
15.3. Limitations to Knowledge of Marine Top Predators
The structure and function of open ocean pelagic ecosystems, including the roles played by top predators, is challenging to understand. Obtaining reliable data on the physiology, behavior, population structure, and ecology of a diverse suite of apex marine predators has been limited by a lack of appropriate observational tools and methods. The mechanisms linking physical forcing, primary and secondary production, prey abundance and distribution to top predator movements are still being elucidated. Furthermore, the influence of climate variations, and potential impacts of climate change, on top predator distributions remain largely unknown. In TOPP, the acquisition of synoptic positional data from apex predators simultaneously with environmental data has provided a unique opportunity to synthesize how distinct ecological guilds of top predators use common habitats, as well as a framework for comparative studies between species groups.
Removal of top predators by intense overexploitation by high-seas fisheries is threatening epipelagic ecosystems (Myers & Worm 2003; Sibert et al. 2006) and poses serious, but as yet unquantified, threats to the stability of marine ecosystems (Jackson et al. 2001). The removal of top predators from ecosystems due to the impact of commercial fisheries has been shown to have a cascading effect throughout the food web, resulting in a shift in species composition (Springer et al. 2003; Frank et al. 2005; Pauly et al. 2005). The role of biodiversity in maintaining the structure and integrity of pelagic ecosystems has been challenging to study because of the difficulties associated with monitoring species over such large spatial scales. The resilience of ecosystems in the face of climate variability as well as the top-down elimination of oceanic predators has been difficult to quantify. The uncertainty associated with the inability to appropriately study and visualize the response of pelagic ecosystems to climate effects or human perturbations is hampering our ability to describe the nature of pelagic predator populations.
Knowledge of how predators use the oceanic ecosystem lags far behind terrestrial ecology, partly because of the challenge of following large, highly migratory animals at sea. Limits to our knowledge are due largely to technological limitations, such as our ability to increase battery life, miniaturize electronics, develop inexpensive silicone-based technologies, increase the rate of data transmission to satellites, apply GPS technologies to marine animals, reduce the error associated with geolocations, and develop methods to infer behavior of marine animals from tagging data. TOPP is providing fundamental information that is addressing these unknowns.
15.4. The Future of Marine Biologging
As humans place enormous pressure on marine ecosystems through overexploitation and climate change, the challenges of understanding critical ecosystem processes and learning how to monitor, model, and manage these ecosystems will be of increasing importance. TOPP has provided proof that direct observation of large marine ecosystems is possible. Linking the biotic and abiotic processes is technologically within our reach. The challenge is building the infrastructure and commitment to continue what has been started during the past decade.
Biologging offers new tools for fisheries managers to obtain critical information on exploited and unexploited populations required to better understand ecosystem function. In most cases before TOPP, scientists and managers lacked important distribution, abundance, and ecological information for modeling populations in the North Pacific Ocean. For managing protected areas and building spatially explicit models, appropriate distribution and abundance data on a scale never before obtained is now available for many top predator groups. These data can now support population assessments that are critical for management decisions. By establishing technologies that can be used reliably, remotely, and in combination with satellite data, we can provide inputs of ecological and physiological data that will improve predictive models. By making innovative efforts, TOPP has provided a road map for comprehensive new approaches to animal observation and for improving our understanding of habitat use. This information, in turn, will lay a foundation for improved ecosystem-based management.
Although conventional survey methods provide the potential to fully characterize the biota of a particular ocean region that is accessible (by vessel, submersible, divers, and so forth), the region outside the search area will always remain unknown and in many cases unknowable. Electronic tags report on an animal's whereabouts and the characteristics of its environment wherever the animal may go, completely independently of our ability to reach these areas with conventional survey platforms such as ships. Electronic tags also allow us to identify biodiversity hot spots, areas where the greatest abundance and diversity of tagged animals are aggregated, as well as to understand the oceanic processes responsible for the formation of these biological hot spots. Before TOPP, few studies provided information on top predator distribution and biodiversity on an oceanic scale.
What we as yet cannot do is predict how the ecosystems of the North Pacific Ocean are changing in the long term. We have just begun to understand the foraging responses of a select group of species, and we lack a true understanding of the connectivity and ecological interactions among the full suite of apex marine predators. Until we deploy biologging technologies continuously and on the oceanic scale, it will be difficult to get a more complete picture of how ocean ecosystems work. TOPP has, however, provided the baseline of a decade of study of top predators in the North Pacific from which future monitoring programs can compare or contrast results.
The maintenance of biodiversity on Earth depends upon our capacity to understand and manage it in our lifetime. TOPP scientists have demonstrated that biologging is a powerful tool for observing and monitoring how animals use the blue ocean ecosystems. In less than a decade, TOPP has shown a remarkable capacity to generate ocean-scale spatial and temporal movement data that have far-reaching impacts for stewardship and management activities in our oceans. The science of biologging is still evolving and incorporation of tagging data into population assessment models is only just beginning.
TOPP has provided a decade-long view of the distribution and movements of 23 top predators in the North Pacific Ocean. The repeatable observation of philopatry in TOPP animals such as white sharks, leatherbacks, elephant seals, and bluefin tuna is indicative of a large-scale biogeographic patterning of the North Pacific. Although some long-lived species remain reproductively active in the western Pacific, their inclination and success when foraging in the eastern Pacific provides the basis for epic trans-oceanic migrations. This biogeographic pattern is only now emerging, and shows the California Current system to be a retentive habitat for some species and an attractive habitat for others. Following up these tracking studies with genetic (Jorgensen et al. 2010) and genomic studies may reveal important information on how the species of the eastern Pacific have come to colonize these highly variable ocean ecosystems, and may reveal critical information on how these species can adapt to the stresses of this unique and highly variable environment.
TOPP has also shown that newly developed sensor capabilities in animal tags are a remarkable new addition to in situ ocean observing networks. The high mobility of marine predators, coupled with the remarkable technical advances made in biologging, has enabled the collection of a variety of high-resolution oceanographic data that are important for improving four-dimensional ocean observations. In TOPP, more than 200,000 tagging days and 2,000,000 profiles were collected by our “animal oceanographers”. This dataset has high quality ocean data that are now being assimilated into an animal ocean portal that will serve OBIS data (see Chapter 17) to National Aeronautics and Space Administration (NASA) and National Oceanic and Atmospheric Administration (NOAA) portals. Biologging provides the only means to measure in situ ocean conditions concomitant with, and at the scale of, the behavioral response of the animals. Most importantly, TOPP has built the capacity for, and demonstrated the efficacy of, an ocean-scale biologging program that is essential for monitoring and sustaining the health of our ocean ecosystems.
We thank the TOPP team for inspiring our Pacific-wide effort and for their dedication to long hours at sea deploying instruments. The work would not have been possible without a dedicated data management team throughout the past decade. We are indebted to A. Swithenbank, J. Ganong, M. Castleton, L. deWitt, D. Foley, and R. Weber, who all helped create the outputs and web browser for TOPP. We thank Dr. Randy Kochevar and Don Kohrs of Stanford University for their dedication and outreach for this program. The postdoctoral scholars and students of TOPP have dedicated energy, thought, and enthusiasm to the program. We thank our Steering Committee and the primary funders of this research: Sloan, Packard, Moore, and Monterey Bay Aquarium Foundations, the Office of Naval Research (ONR) and the National Oceanic and Atmospheric Administration. All work was done in accordance with the IACUC requirements of Stanford University and University of California.
|Anderson, S.D., Becker, B.H. & Allen, S.G. (2008) Observations and prey of white sharks, Carcharodon carcharias, at point reyes national seashore: 1982–2004. California Fish and Game 94, 33–43.|
|Bailey, H., Mate, B.R., Palacios, D.M., et al. (2010) Behavioural estimation of blue whale movements in the Northeast Pacific from state space model analysis of satellite tracks. Endangered Species Research 10, 93–106.|
|Bailey, H.R., Shillinger, G.L., Palacios, D.M., et al. (2008) Identifying and comparing phases of movement by leatherback turtles using state-space models. Journal of Experimental Marine Biology and Ecology 356, 128–135.|
|Bayliff, W.H. (1994) A review of the biology and fisheries for northern bluefin tuna, Thunnus thynnus, in the Pacific Ocean. FAO (Food and Agriculture Organization of the United Nations) Fisheries Technical Paper 336, part 2, pp. 244–295.|
|Biuw, M., Boehme, L., Guinet, C., et al. (2007) Variations in behavior and condition of a Southern Ocean top predator in relation to in situ oceanographic conditions. Proceedings of the National Academy of Sciences of the USA 104, 13705–13710.|
|Block, B.A. (2005) Physiological ecology in the 21st century: advancements in biologging science. Integrative and Comparative Biology 45, 305–320.|
|Block, B.A., Costa, D.P., Boehlert, G.W. & Kochevar, R.E. (2003) Revealing pelagic habitat use: the tagging of Pacific pelagics program. Oceanologica Acta 25, 255–266.|
|Block, B.A., Dewar, H., Blackwell, S.B., et al. (2001) Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 293, 1310–1314.|
|Block, B.A., Dewar, H., Farwell, C. & Prince, E.D. (1998) A new satellite technology for tracking the movements of Atlantic bluefin tuna. Proceedings of the National Academy of Sciences of the USA 95, 9384–9389.|
|Boehme, L., Meredith, M.P., Thorpe, S.E., et al. (2008a) Antarctic Circumpolar Current frontal system in the South Atlantic: monitoring using merged Argo and animal-borne sensor data. Journal of Geophysics Research 113, C08009, doi:10.1029/2007JC004647.|
|Boehme, L., Thorpe, S.E., Biuw, M., et al. (2008b) Monitoring Drake Passage with elephant seals: frontal structures and snapshots of transport. Limnology and Oceanography 53, 2350–2360.|
|Boustany, A., Matteson, R., Castleton, M.R., et al. (2010) Movements of Pacific bluefin tuna (Thunnus orientalis) in the Eastern North Pacific revealed with archival tags. Progress in Oceanography (in press).|
|Boustany, A.M., Davis, S.F., Pyle, P., et al. (2002) Satellite tagging: Expanded niche for white sharks. Nature 415, 35–36.|
|Charrassin, J.-B., Hindell, M., Rintoul, S.R., et al. (2008) Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals. Proceedings of the National Academy of Sciences of the USA 105, 11634–11639.|
|Clapham, P.J. (2009) Humpback whale, Megaptera novaeangliae. In: Encyclopedia of Marine Mammals (eds. W.F. Perrin, B. Würsig, and J.G.M. Thewissen), pp. 582–585. New York: Elsevier-Academic.|
|Collette, B.B. & Nauen, C.E. (1983) Scombrids of The World. FAO Species Catalog 125.|
|Costa, D.P. (1993). The secret life of marine mammals: novel tools for studying their behavior and biology at sea. Oceanography 6, 120–128.|
|Costa, D.P., Robinson, P.E., Arnould, J.P.Y., et al. (2010a) Accuracy of ARGOS locations of marine mammals at sea estimated using Fastloc GPS. PloS ONE 5, e8677. doi:10.1371/journal.pone.0008677.|
|Costa, D.P., Huckstadt L.A., Crocker, D.E., et al. (2010b) Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds. Integrative and Comparative Biology doi:10.1093/icb/icq054.|
|Costa, D.P. & Sinervo B. (2004) Field physiology: physiological insights from animals in nature. Annual Review of Physiology 66, 209–238.|
|Decker, C.J. & Reed, C. (2009) The National Oceanographic Partnership Program: a decade of impacts on oceanography. Oceanography 22, 208–227.|
|Ekstrom, P.A. (2004) An advance in geolocation by light. Memoirs of the National Institute of Polar Research 58, 210–226|
|Fedak, M., Lovell, P., McConnell, B. & Hunter, C. (2002) Overcoming the constraints of long range radio telemetry from animals: getting more useful data from smaller packages. Integrated Comparative Biology 42, 3–10.|
|Fedak, M.A., Lovell, P. & Grant, S.M. (2001) Two approaches to compressing and interpreting time–depth information as collected by time–depth recorders and satellite-linked data recorders. Marine Mammal Science 17, 94–110.|
|Feder, M.E. (1987) The analysis of physiological diversity: the prospects for pattern documentation and general questions in physiological ecology. In: New Directions in Physiological Ecology (eds. M.E. Feder, A.F. Bennett, W. Burggren, & R.B. Huey). pp. 38–75. Cambridge, UK: Cambridge University Press.|
|Fiedler, P.C., Reilly, S.B., Hewitt, R.P., et al. (1998) Blue whale habitat and prey in the California Channel Islands. Deep-Sea Research II 45, 1781–1801.|
|Frank, K.T., Petrie, B., Choi, J.S. & Leggett, W.C. (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621–1623.|
|Goldman, K.J. & Musick, J.A. (2006) Growth and maturity of salmon sharks (Lamna ditropis) in the eastern and western North Pacific, and comments on back-calculation methods. Fishery Bulletin 104, 278–292.|
|Goldman, K.J. & Musick, J.A. (2008) The biology and ecology of the salmon shark, Lamna ditropis. Fish and Aquatic Resources Series 13, 95–104.|
|Hickey, B.M. (1998) Coastal oceanography of western North America from the tip of Baja California to Vancouver Island. In: The Sea, The Global Coastal Ocean, Regional Studies and Syntheses (eds. A.R. Robinson & K.H. Brink), pp. 345–393. New York: Wiley.|
|Hill, R.D. & Braun, M.J. (2001) Geolocation by light level – the next step: latitude. In: Electronic Tagging and Tracking in Marine Fisheries (eds. J.R. Sibert & J. Nielsen), pp. 315–330. The Netherlands: Kluwer.|
|Hyrenbach, K.D., Fernandez, P. & Anderson, D.J. (2002) Oceanographic habitats of two sympatric North Pacific albatrosses during the breeding season. Marine Ecology Progress Series 233, 283–301.|
|Inagake, D.H., Yamada, K., Segawa, M., et al. (2001) Migration of young bluefin tuna, Thunnus orientalis Temminck et Schlegel, through archival tagging experiments and its relation with oceanographic conditions in the western North Pacific. Bulletin of the National Research Institute of Far Seas Fisheries 38, 53–81.|
|Jackson, J.B., Kirby, M.X., Berger, K.A., et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637.|
|Jorgensen, S.J., Reeb, C.A. Chapple, T., et al. (2010) Philopatry and migration of Pacific white sharks. Proceedings of the Royal Society of London B 277, 679–688.|
|Kappes, M.A., Shaffer, S.A., Tremblay, Y., et al. (2010) Hawaiian albatrosses track interannual variability of marine habitats in the North Pacific. Progress in Oceanography doi:10.1016/j.pocean.2010.04.012.|
|Kitagawa, T., Boustany, A.M., Farwell, C.J., et al. (2007) Horizontal and vertical movements of juvenile bluefin tuna (Thunnus orientalis) in relation to seasons and oceanographic conditions in the eastern Pacific Ocean. Fisheries Oceanography 16, 409–421.|
|Kuhn, C.E. & Costa, D.P. (2006) Identifying and quantifying prey consumption using stomach temperature change in pinnipeds. Journal of Experimental Biology 209, 4524–4532.|
|Kuhn, C.E., Crocker, D.E., Tremblay, Y. & Costa, D.P. (2009) Time to eat: measurements of feeding behaviour in a large marine predator, the northern elephant seal Mirounga angustirostris. Journal of Animal Ecology 78, 513–523.|
|Le Boeuf, B.J., Crocker, D.E., Costa, D.P., et al. (2000) Foraging ecology of northern elephant seals. Ecological Monographs 70, 353–382.|
|Lopez, S., Melendez, R. & Barria, P. (2009) Feeding of the shortfin mako shark Isurus oxyrinchus Rafinesque, 1810 (Lamniformes: Lamnidae) in the Southeastern Pacific. Revista de Biologia Marina y Oceanografia 44, 439–451.|
|Lutcavage, M.E., Brill, R.W., Skomal, G.B., et al. (1999) Results of pop-up satellite tagging of spawning size class fish in the Gulf of Maine: do North Atlantic bluefin tuna spawn in the mid-Atlantic? Canadian Journal of Fisheries and Aquatic Sciences 56: 173–177.|
|McConnell, B.J., Chambers, C. & Fedak, M.A. (1992a) Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean. Antarctic Science 4, 393–398.|
|McConnell, B.J., Chambers, C., Nicholas, K.S. & Fedak, M.A. (1992b) Satellite tracking of grey seals (Halichoerus grypus). Journal of Zoology 226, 271–282.|
|Myers, R.A. & Worm, B. (2003) Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283.|
|Nakano, H. & Nagasawa, K. (1996) Distribution of pelagic elasmobranchs caught by salmon research gillnets in the North Pacific. Fisheries Science 62, 860–865.|
|Nicholls, K.W., Boehme, L., Biuw, M. & Fedak, M.A. (2008) Wintertime ocean conditions over the southern Weddell Sea continental shelf, Antarctica. Geophysical Research Letters 35, L21605.|
|Olson, D.B., Hitchcock, G.L., Mariano, A.J., et al. (1994) Life on the edge: marine life and fronts. Oceanography 7, 52–60.|
|Palacios, D.M., Bograd, S.J., Foley, D.G. & Schwing, F.B. (2006) Oceanographic characteristics of biological hot spots in the North Pacific: a remote sensing perspective. Deep Sea Research II 53, 250–269.|
|Pauly, D., Watson, R. & Alder, J. (2005) Global trends in world fisheries: impacts on marine ecosystems and food security. Philosophical Transactions of the Royal Society of London B 360, 5–12.|
|Peckham, S.H., Diaz, D.M., Walli, A., Ruiz, G., Crowder, L.B., et al. (2007) Small-scale fisheries bycatch jeopardizes endangered pacific loggerhead turtles. PLoS ONE 2(10), e1041. doi:10.1371/journal.pone.0001041.|
|Polovina, J.J. (1996) Decadal variation in the trans-Pacific migration of northern bluefin tuna (Thunnus thynnus) coherent with climate-induced change in prey abundance. Fisheries Oceanography 5, 114–119.|
|Polovina, J.J., Kobayashi, D.R., Parker, D.M., et al. (2000) Turtles on the edge: Movement of loggerhead turtles (Caretta caretta) along oceanic fronts, spanning longline fishing grounds in the central North Pacific, 1997–1998. Fisheries Oceanography 9, 71–82.|
|Pyle, P., Anderson, S.D. & Ainley, D.G. (1996) Trends in white shark predation at the South Farallon Islands, 1968–1993. In: Great White Sharks (eds. A. Klimley & D. Ainley), pp. 375–379. Elsevier.|
|Roden, G.I. (1991) Subarctic–Subtropical Transition Zone of the North Pacific Large-Scale Aspects and Mesoscale Structure. In: Biology, Oceanography, and Fisheries of the North Pacific Transition Zone and Subarctic Frontal Zone (ed. J. A. Wetherall), pp. 1–38. NOAA Technical Report NMFS, US Department of Commerce.|
|Schaefer, K.M., Fuller, D.W. & Block, B.A. (2007) Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data. Marine Biology 152, 503–525.|
|Schaefer, K.M., Fuller, D.W. & Block, B.A. (2008) Comparative vertical movements and habitat utilization of bigeye (Thunnus obesus), yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas in the equatorial eastern Pacific Ocean. In: Tagging and Tracking of Marine Animals with Electronic Devices (ed. J.L. Nielsen et al.), pp. 121–144 (Reviews: Methods and Technologies in Fish Biology and Fisheries 9). Springer Science+Business Media B.V.|
|Schaefer, K.M., Fuller, D.W. & Block, B.A. (2009) Tagging and tracking of marine animals with electronic devices. In: Reviews: Methods and Technologies in Fish Biology and Fisheries (eds. S.J. Fragoso, et al.), pp. 121–144 9. Dordrecht and London: Springer eBooks.|
|Sears, R. & Perrin, W.F. (2009) Blue whale, Balaenoptera musculus. In: Encyclopedia of Marine Mammals (eds. W.F. Perrin, B. Würsig, & J.G.M. Thewissen), pp. 120–124. New York: Elsevier-Academic.|
|Shaffer, S.A. & Costa, D.P. (2006) A database for the study of marine mammal behavior: gap analysis, data standardization, and future directions. Oceanic Engineering 31, 82–86.|
|Shaffer, S.A., Tremblay, Y., Weimerskirch, H., et al. (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proceedings of the National Academy of Sciences of the USA 103, 12799–12802.|
|Shaffer, S.A., Weimerskirch, H., Scott, D., et al. (2009) Spatiotemporal habitat use by breeding sooty shearwaters Puffinus griseus. Marine Ecology Progress Series 391, 209–220.|
|Shillinger, G.L., Palacios, D.M., Bailey, H. et al. (2008) Persistent leatherback turtle migrations present opportunities for conservation. PLoS Biology 6, e171.|
|Sibert, J., Hampton, J., Kleiber, P. & Maunder, M. (2006) Biomass, size, and trophic status of top predators in the Pacific Ocean. Science 314, 1773–1776.|
|Simmons, S.E., Tremblay, Y. & Costa, D.P. (2009) Pinnipeds as ocean-temperature samplers: calibrations, validations, and data quality. Limnology and Oceanography: Methods 7, 648–656.|
|Springer, A.M., Estes, J.A., van Vliet, G.B., et al. (2003) Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? Proceedings of the National Academy of Science of the USA 100, 12223–12228.|
|Sydeman, W.J., Brodeur, R.D., Grimes, C.B., et al. (2006) Marine habitat “hotspots” and their use by migratory species and top predators in the North Pacific Ocean: introduction. Deep Sea Research II 53, 247–249.|
|Teo, S.L.H., Boustany, A., Blackwell, S., et al. (2004a) Validation of geolocation estimates based on light level and sea surface temperature from electronic tags. Marine Ecology Progress Series 283, 81–98.|
|Teo, S.L.H., Boustany, A., Blackwell, S.B., et al. (2004b) Validation of geolocation estimates based on light level and sea surface temperature from electronic tags. Marine Ecology Progress Series 283, 81–98.|
|Teo, S.L.H., Kudela, R.M., Rais, A., et al. (2009) Estimating chlorophyll profiles from electronic tags deployed on pelagic animals. Aquatic Biology 5, 195–207.|
|Tremblay, Y.A. Roberts, A.J. & Costa, D.P. (2007) Fractal landscape method: an alternative approach to measuring area-restricted searching behavior. Journal of Experimental Biology 210, 935–945.|
|Tremblay, Y., Robinson, P.W. & Costa, D.P. (2009) A parsimonious approach to modeling animal movement data. PLoS ONE 4(3), doi: 10.1371/journal.pone.0004711.|
|Tremblay, Y., Shaffer, S.A., Fowler, S.L., et al. (2006) Interpolation of animal tracking data in a fluid environment. Journal of Experimental Biology 209, 128–140.|
|Weimerskirch, H., Guionnet, T., Martin, J., et al. (2000) Fast and fuel efficient? Optimal use of wind by flying albatrosses. Proceedings of the Royal Society of London B 267, 1869–1874.|
|Weise, M.J., Costa, D.P. & Kudela, R.M. (2006) Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004. Geophysic Research Letters 33, L22S10.|
|Weng, K.C., Boustany, A.M. Pyle, P., et al. (2007a) Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Marine Biology 152, 877–894.|
|Weng, K.C., Castilho, P.C., Morrissette, J.M., et al. (2005) Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science 310, 104–106.|
|Weng, K.C., O'Sullivan, J.B., Lowe, C.G., et al. (2007b) Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific. Marine Ecology Progress Series 338, 211–224.|
|Weng, K.C., Foley, D.G., Ganong, J.E., et al. (2008) Migration of an upper trophic level predator, the salmon shark, Lamna ditropis, between distant ecoregions. Marine Ecological Progress Series 372: 253–264.|
|Woods, J.D. (1988) Scale upwelling and primary production. NATO ASI series. Series C, Mathematical and physical sciences 239, 7–38.|
|Worm, B., Lotze, H.K. & Myers, R.A. (2003) Predator diversity hotspots in the blue ocean. Proceedings of the National Academy of Sciences of the USA 100, 9884–9888.|