Kim Aarestrup

Aquatic animal telemetry: A panoramic window into the underwater world

A brave new world with a wider view Researchers have long attempted to follow animals as they move through their environment. Until relatively recently, however, such efforts were limited to short distances and times in species large enough to carry large batteries and transmitters. New technologies have opened up new frontiers in animal tracking remote data collection. Hussey et al. review the unique directions such efforts have taken for marine systems, while Kays et al. review recent advances for terrestrial species. We have entered a new era of animal ecology, where animals act as both subjects and samplers of their environments. Science, this issue 10.1126/science.1255642, 10.1126/science.aaa2478 BACKGROUND Global aquatic environments are changing profoundly as a result of human actions; consequently, so too are the ways in which organisms are distributing themselves through space and time. Our ability to predict organism and community responses to these alterations will be dependent on knowledge of animal movements, interactions, and how the physiological and environmental processes underlying them shape species distributions. These patterns and processes ultimately structure aquatic ecosystems and provide the wealth of ecosystem services upon which humans depend. Until recently, the vast size, opacity, and dynamic nature of the aquatic realm have impeded our efforts to understand these ecosystems. With rapid technological advancement over the past several decades, a suite of electronic tracking devices (e.g., acoustic and satellite transmitters) that can remotely monitor animals in these challenging environments are now available. Aquatic telemetry technology is rapidly accelerating our ability to observe animal behavior and distribution and, as a consequence, is fundamentally altering our understanding of the structure and function of global aquatic ecosystems. These advances provide the toolbox to define how future global aquatic management practices must evolve. ADVANCES Aquatic telemetry has emerged through technological advances in miniaturization, battery engineering, and software and hardware development, allowing the monitoring of organisms whose habitats range from the poles to the tropics and the photic zone to the abyssal depths. This is enabling the characterization of the horizontal and vertical movements of individuals, populations, and entire communities over scales of meters to tens of thousands of kilometers and over time frames of hours to years and even over the entire lifetimes of individuals. Electronic tags can now be equipped with sensors that measure ambient physical parameters (depth, temperature, conductivity, fluorescence), providing simultaneous monitoring of animals’ environments. By linking telemetry with biologgers (e.g., jaw-motion sensors), it is possible to monitor individual feeding events. In addition, other devices on instrumented animals can communicate with one another, providing insights into predator-prey interactions and social behavior. Coupling telemetry with minute nonlethal biopsy allows understanding of how trophic dynamics, population connectivity, and gene-level basis for organismal health and condition relate to movement. These advances are revolutionizing the scope and scales of questions that can be addressed on the causes and consequences of animal distribution and movement. OUTLOOK Aquatic animal telemetry has advanced rapidly, yet new challenges present themselves in coordination of monitoring across large-spatial scales (ocean basins), data sharing, and data assimilation. The continued advancement of aquatic telemetry lies in establishing and maintaining accessible and cost-effective infrastructure and in promoting multidisciplinary tagging approaches to maximize cost benefits. A united global network and centralized database will provide the mechanism for global telemetry data and will promote a transparent environment for data sharing that will, in turn, increase global communication, scope for collaboration, intellectual advancement, and funding opportunities. An overarching global network will realize the potential of telemetry, which is essential for advancing scientific knowledge and effectively managing globally shared aquatic resources and their ecosystems in the face of mounting human pressures and environmental change. Aquatic telemetry in action. A southern rock lobster (Jasus edwardsii) (A) and a lemon shark (Negaprion brevirostris) (D) fitted with acoustic tags are detected and logged by moored receivers (D) or mobile receivers attached to opportunistic platforms or carried by large animals (C). A juvenile green turtle (Chelonia mydas) (B) fitted with a satellite tag is monitored in real time via orbiting satellites. A grey seal (Halichoerus grypus) “bioprobe” (C), fitted with intercommunicating acoustic and satellite transmitters, transmits and receives data on animal interactions and ocean conditions. The distribution and interactions of aquatic organisms across space and time structure our marine, freshwater, and estuarine ecosystems. Over the past decade, technological advances in telemetry have transformed our ability to observe aquatic animal behavior and movement. These advances are now providing unprecedented ecological insights by connecting animal movements with measures of their physiology and environment. These developments are revolutionizing the scope and scale of questions that can be asked about the causes and consequences of movement and are redefining how we view and manage individuals, populations, and entire ecosystems. The next advance in aquatic telemetry will be the development of a global collaborative effort to facilitate infrastructure and data sharing and management over scales not previously possible.

Oceanic Spawning Migration of the European Eel (Anguilla anguilla)

Satellite tracking technology has allowed scientists to map part of the migration route of the European eel. European eels (Anguilla anguilla) undertake a ~5000-kilometer (km) spawning migration from Europe to the Sargasso Sea. The larvae are transported back to European waters by the Gulf Stream and North Atlantic Drift. However, details of the spawning migration remain unknown because tracking eels in the Atlantic Ocean has, so far, eluded study. Recent advances in satellite tracking enable investigation of migratory behavior of large ocean-dwelling animals. However, sizes of available tags have precluded tracking smaller animals like European eels. Here, we present information about the swimming direction, depth, and migratory behavior of European eels during spawning migration, based on a miniaturized pop-up satellite archival transmitter. Although the tagging experiment fell short of revealing the full migration to the Sargasso Sea, the data covered the first 1300 km and provided unique insights.

All roads lead to home: panmixia of European eel in the Sargasso Sea

European eels (Anguilla anguilla) spawn in the remote Sargasso Sea in partial sympatry with American eels (Anguilla rostrata), and juveniles are transported more than 5000 km back to the European and North African coasts. The two species have been regarded as classic textbook examples of panmixia, each comprising a single, randomly mating population. However, several recent studies based on continental samples have found subtle, but significant, genetic differentiation, interpreted as geographical or temporal heterogeneity between samples. Moreover, European and American eels can hybridize, but hybrids have been observed almost exclusively in Iceland, suggesting hybridization in a specific region of the Sargasso Sea and subsequent nonrandom dispersal of larvae. Here, we report the first molecular population genetics study based on analysis of 21 microsatellite loci in larvae of both Atlantic eel species sampled directly in the spawning area, supplemented by analysis of European glass eel samples. Despite a clear East-West gradient in the overlapping distribution of the two species in the Sargasso Sea, we only observed a single putative hybrid, providing evidence against the hypothesis of a wide marine hybrid zone. Analyses of genetic differentiation, isolation by distance, isolation by time and assignment tests provided strong evidence for panmixia in both the Sargasso Sea and across all continental samples of European eel after accounting for the presence of sibs among newly hatched larvae. European eel has declined catastrophically, and our findings call for management of the species as a single unit, necessitating coordinated international conservation efforts.

Survival of radio-tagged Atlantic salmon (Salmo salar L.) and trout (Salmo trutta L.) smolts passing a reservoir during seaward migration

High mortality-rates of seaward migrating salmonid smolts when passing reservoirs and lakes have earlier been found in the Danish River Gudena watershed. To reveal the causes of mortality of migrating smolts in Lake Tange, a 12 km long, shallow reservoir, 50 salmon smolts and 24 trout smolts were tagged with internal miniature radio-transmitters, and released in the river just upstream the reservoir on May 1, 1996. The salmon smolts were hatchery-reared, while the trout smolts were wild fish, caught in a smolt trap. The tagged smolts were tracked daily for 3 weeks, and when possible the cause of death was determined. During the 3-week period, 90% of the tagged smolts died. The main cause of death for both trout and salmon was predation from fish and birds. The most important predator was pike (Esox lucius L.), being responsible for 56% of the observed mortality. Avian predators were assumed to be responsible for 31% of the observed mortality. No trout smolts left the reservoir, but 5 salmon-smolts got out through the turbines. Others did traverse the reservoir, but were unable to enter the river downstream, and were later eaten. The present results suggest that mortalities for migrating smolts through Lake Tange are of such a magnitude, that stocking of juveniles in the river upstream is futile, and further, that the establishment of a natural population of salmon or sea-trout in river Gudena, upstream Tange, is unrealistic under present conditions.

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.

Oceanic fronts in the Sargasso Sea control the early life and drift of Atlantic eels

Anguillid freshwater eels show remarkable life histories. In the Atlantic, the European eel (Anguilla anguilla) and American eel (Anguilla rostrata) undertake extensive migrations to spawn in the oceanic Sargasso Sea, and subsequently the offspring drift to foraging areas in Europe and North America, first as leaf-like leptocephali larvae that later metamorphose into glass eels. Since recruitment of European and American glass eels has declined drastically during past decades, there is a strong demand for further understanding of the early, oceanic phase of their life cycle. Consequently, during a field expedition to the eel spawning sites in the Sargasso Sea, we carried out a wide range of dedicated bio-physical studies across areas of eel larval distribution. Our findings suggest a key role of oceanic frontal processes, retaining eel larvae within a zone of enhanced feeding conditions and steering their drift. The majority of the more westerly distributed American eel larvae are likely to follow a westerly/northerly drift route entrained in the Antilles/Florida Currents. European eel larvae are generally believed to initially follow the same route, but their more easterly distribution close to the eastward flowing Subtropical Counter Current indicates that these larvae could follow a shorter, eastward route towards the Azores and Europe. The findings emphasize the significance of oceanic physical–biological linkages in the life-cycle completion of Atlantic eels.

Net ground speed of downstream migrating radio-tagged Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.) smolts in relation to environmental factors

The downstream migration of Atlantic salmon (Salmo salarL.) and sea trout smolt (S. trutta L.) was investigated using radio telemetry in the spring of 1999 and 2000. Forty wild sea trout smolts, 20 F1 sea trout smolts, 20 hatchery salmon smolts and 20 salmon smolts from river stockings were radio tagged and released in the Danish River Lilleaa. The downstream migration of the different groups of fish was monitored by manual tracking and by three automatic listening stations. The downstream migration of radio tagged smolts of both species occurred concurrently with their untagged counterparts. The diel migration pattern of the radio tagged smolts was predominantly nocturnal in both species. Wild sea trout smolt migrated significantly faster than both the F1 trout and the introduced salmon. There was no correlation between net ground speed, gill Na+,K+-ATPase activity or fish length in any of the different groups. The migration speed of wild sea trout smolts was positively correlated with water discharge in both years. In F1 sea trout smolts, migration speed was positively correlated with temperature in 1999. The migration speed of salmon smolts did not correlate to any of the investigated parameters.

Shark Predation on Migrating Adult American Eels (Anguilla rostrata) in the Gulf of St. Lawrence

In an attempt to document the migratory pathways and the environmental conditions encountered by American eels during their oceanic migration to the Sargasso Sea, we tagged eight silver eels with miniature satellite pop-up tags during their migration from the St. Lawrence River in Québec, Canada. Surprisingly, of the seven tags that successfully transmitted archived data, six were ingested by warm-gutted predators, as observed by a sudden increase in water temperature. Gut temperatures were in the range of 20 to 25°C—too cold for marine mammals but within the range of endothermic fish. In order to identify the eel predators, we compared their vertical migratory behavior with those of satellite-tagged porbeagle shark and bluefin tuna, the only endothermic fishes occurring non-marginally in the Gulf of St. Lawrence. We accurately distinguished between tuna and shark by using the behavioral criteria generated by comparing the diving behavior of these two species with those of our unknown predators. Depth profile characteristics of most eel predators more closely resembled those of sharks than those of tuna. During the first days following tagging, all eels remained in surface waters and did not exhibit diel vertical migrations. Three eels were eaten at this time. Two eels exhibited inverse diel vertical migrations (at surface during the day) during several days prior to predation. Four eels were eaten during daytime, whereas the two night-predation events occurred at full moon. Although tagging itself may contribute to increasing the eels susceptibility to predation, we discuss evidence suggesting that predation of silver-stage American eels by porbeagle sharks may represent a significant source of mortality inside the Gulf of St. Lawrence and raises the possibility that eels may represent a reliable, predictable food resource for porbeagle sharks.

Partition of aerobic and anaerobic swimming costs related to gait transitions in a labriform swimmer

SUMMARY Members of the family Embiotocidae exhibit a distinct gait transition from exclusively pectoral fin oscillation to combined pectoral and caudal fin propulsion with increasing swimming speed. The pectoral–caudal gait transition occurs at a threshold speed termed Up–c. The objective of this study was to partition aerobic and anaerobic swimming costs at speeds below and above the Up–c in the striped surfperch Embiotoca lateralis using swimming respirometry and video analysis to test the hypothesis that the gait transition marks the switch from aerobic to anaerobic power output. Exercise oxygen consumption rate was measured at 1.4, 1.9 and 2.3 L s–1. The presence and magnitude of excess post-exercise oxygen consumption (EPOC) were evaluated after each swimming speed. The data demonstrated that 1.4 L s–1 was below the Up–c, whereas 1.9 and 2.3 L s–1 were above the Up–c. These last two swimming speeds included caudal fin propulsion in a mostly steady and unsteady (burst-assisted) mode, respectively. There was no evidence of EPOC after swimming at 1.4 and 1.9 L s–1, indicating that the pectoral–caudal gait transition was not a threshold for anaerobic metabolism. At 2.3 L s–1, E. lateralis switched to an unsteady burst and flap gait. This swimming speed resulted in EPOC, suggesting that anaerobic metabolism constituted 25% of the total costs. Burst activity correlated positively with the magnitude of the EPOC. Collectively, these data indicate that steady axial propulsion does not lead to EPOC whereas transition to burst-assisted swimming above Up–c is associated with anaerobic metabolism in this labriform swimmer.

Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): recovery in normoxia and hypoxia

Under certain conditions, a number of fish species may perform brief excursions into severe hypoxia and return to water with a higher oxygen content. The term severe hypoxia describes oxygen condit...