Magnetic map in nonanadromous Atlantic salmon.

Long-distance migrants, including Pacific salmon (Oncorhynchus spp), can use geomagnetic information to navigate. We tested the hypothesis that a "magnetic map" (i.e., an ability to extract positional information from Earth's magnetic field) also exists in a population of salmon that do not undertake oceanic migrations. This study examined juvenile Atlantic salmon (Salmo salar) originally from a nonanadromous population in Maine transferred ∼60 years ago to a lake in central Oregon. We exposed juveniles to magnetic displacements representative of locations at the latitudinal boundaries of the Pacific salmon oceanic range in the North Pacific and at the periphery of their ancestral oceanic range in the North Atlantic. Orientation differed among the magnetic treatments, indicating that Atlantic salmon detect map information from the geomagnetic field. Despite no recent history of ocean migration, these fish displayed adaptive orientation responses similar to those observed in native Pacific salmonids. These findings indicate that use of map information from the geomagnetic field is a shared ancestral character in the family Salmonidae and is not restricted to populations with anadromous life histories. Lastly, given that Atlantic salmon are transported throughout the world for capture fisheries and aquaculture, such a robust navigational system is of some concern. Escaped individuals may have greater potential to successfully navigate, and thus invade, introduced habitats than previously suspected.

Managing fisheries in a world with more sea turtles.

For decades, fisheries have been managed to limit the accidental capture of vulnerable species and many of these populations are now rebounding. While encouraging from a conservation perspective, as populations of protected species increase so will bycatch, triggering management actions that limit fishing. Here, we show that despite extensive regulations to limit sea turtle bycatch in a coastal gillnet fishery on the eastern United States, the catch per trip of Kemp's ridley has increased by more than 300% and green turtles by more than 650% (2001-2016). These bycatch rates closely track regional indices of turtle abundance, which are a function of increased reproductive output at distant nesting sites and the oceanic dispersal of juveniles to near shore habitats. The regulations imposed to help protect turtles have decreased fishing effort and harvest by more than 50%. Given uncertainty in the population status of sea turtles, however, simply removing protections is unwarranted. Stock-assessment models for sea turtles must be developed to determine what level of mortality can be sustained while balancing continued turtle population growth and fishing opportunity. Implementation of management targets should involve federal and state managers partnering with specific fisheries to develop bycatch reduction plans that are proportional to their impact on turtles.

Asymmetrical gene flow in five co-distributed syngnathids explained by ocean currents and rafting propensity.

Ocean circulation driving macro-algal rafting is believed to serve as an important mode of dispersal for many marine organisms, leading to predictions on population-level genetic connectivity and the directionality of effective dispersal. Here, we use genome-wide single nucleotide polymorphism data to investigate whether gene flow directionality in two seahorses (Hippocampus) and three pipefishes (Syngnathus) follows the predominant ocean circulation patterns in the Gulf of Mexico and northwestern Atlantic. In addition, we explore whether gene flow magnitudes are predicted by traits related to active dispersal ability and habitat preference. We inferred demographic histories of these co-distributed syngnathid species, and coalescent model-based estimates indicate that gene flow directionality is in agreement with ocean circulation data that predicts eastward and northward macro-algal transport. However, the magnitude to which ocean currents influence this pattern appears strongly dependent on the species-specific traits related to rafting propensity and habitat preferences. Higher levels of gene flow and stronger directionality are observed in Hippocampus erectus, Syngnathus floridae and Syngnathus louisianae, which closely associated with the pelagic macro-algae Sargassum spp., compared to Hippocampus zosterae and the Syngnathus scovelli/Syngnathus fuscus sister-species pair, which prefer near shore habitats and are weakly associated with pelagic Sargassum. This study highlights how the combination of population genomic inference together with ocean circulation data can help explain patterns of population structure and diversity in marine ecosystems.

A sense of place: pink salmon use a magnetic map for orientation.

The use of 'map-like' information from the Earth's magnetic field for orientation has been shown in diverse taxa, but questions remain regarding the function of such maps. We used a 'magnetic displacement' experiment to demonstrate that juvenile pink salmon (Oncorhynchus gorbuscha) use magnetic cues to orient. The experiment was designed to simultaneously explore whether their magnetic map is used to direct fish (i) homeward, (ii) toward the center of their broad oceanic range or (iii) along their oceanic migratory route. The headings adopted by these navigationally naive fish coincided remarkably well with the direction of the juveniles' migration inferred from historical tagging and catch data. This suggests that the large-scale movements of pink salmon across the North Pacific may be driven largely by their innate use of geomagnetic map cues. Key aspects of the oceanic ecology of pink salmon and other marine migrants might therefore be predicted from magnetic displacement experiments.

Magnetoreception in fishes: the effect of magnetic pulses on orientation of juvenile Pacific salmon.

A variety of animals sense Earth's magnetic field and use it to guide movements over a wide range of spatial scales. Little is known, however, about the mechanisms that underlie magnetic field detection. Among teleost fish, growing evidence suggests that crystals of the mineral magnetite provide the physical basis of the magnetic sense. In this study, juvenile Chinook salmon (Oncorhynchus tshawytscha) were exposed to a brief but strong magnetic pulse capable of altering the magnetic dipole moment of biogenic magnetite. Orientation behaviour of pulsed fish and untreated control fish was then compared in a magnetic coil system under two conditions: (1) the local magnetic field and (2) a magnetic field that exists near the southern boundary of the natural oceanic range of Chinook salmon. In the local field, no significant difference existed between the orientation of the control and pulsed groups. By contrast, orientation of the two groups was significantly different in the magnetic field from the distant site. These results demonstrate that a magnetic pulse can alter the magnetic orientation behaviour of a fish and are consistent with the hypothesis that salmon have magnetite-based magnetoreception.

Geomagnetic field influences upward movement of young Chinook salmon emerging from nests.

Organisms use a variety of environmental cues to orient their movements in three-dimensional space. Here, we show that the upward movement of young Chinook salmon (Oncorhynchus tshawytscha) emerging from gravel nests is influenced by the geomagnetic field. Fish in the ambient geomagnetic field travelled farther upwards through substrate than did fish tested in a field with the vertical component inverted. This suggests that the magnetic field is one of several factors that influences emergence from the gravel, possibly by serving as an orientation cue that helps fish determine which way is up. Moreover, our work indicates that the Oncorhynchus species are sensitive to the magnetic field throughout their life cycles, and that it guides their movements across a range of spatial scales and habitats.

First satellite tracks of South Atlantic sea turtle 'lost years': seasonal variation in trans-equatorial movement.

In the South Atlantic Ocean, few data exist regarding the dispersal of young oceanic sea turtles. We characterized the movements of laboratory-reared yearling loggerhead turtles from Brazilian rookeries using novel telemetry techniques, testing for differences in dispersal during different periods of the sea turtle hatching season that correspond to seasonal changes in ocean currents. Oceanographic drifters deployed alongside satellite-tagged turtles allowed us to explore the mechanisms of dispersal (passive drift or active swimming). Early in the hatching season turtles transited south with strong southward currents. Late in the hatching season, when currents flowed in the opposite direction, turtles uniformly moved northwards across the Equator. However, the movement of individuals differed from what was predicted by surface currents alone. Swimming velocity inferred from track data and an ocean circulation model strongly suggest that turtles' swimming plays a role in maintaining their position within frontal zones seaward of the continental shelf. The long nesting season of adults and behaviour of post-hatchlings exposes young turtles to seasonally varying ocean conditions that lead some individuals further into the South Atlantic and others into the Northern Hemisphere. Such migratory route diversity may ultimately buffer the population against environmental changes or anthropologic threats, fostering population resiliency.

Earth-strength magnetic field affects the rheotactic threshold of zebrafish swimming in shoals.

Rheotaxis, the unconditioned orienting response to water currents, is a main component of fish behavior. Rheotaxis is achieved using multiple sensory systems, including visual and tactile cues. Rheotactic orientation in open or low-visibility waters might also benefit from the stable frame of reference provided by the geomagnetic field, but this possibility has not been explored before. Zebrafish (Danio rerio) form shoals living in freshwater systems with low visibility, show a robust positive rheotaxis, and respond to geomagnetic fields. Here, we investigated whether a static magnetic field in the Earth-strength range influenced the rheotactic threshold of zebrafish in a swimming tunnel. The direction of the horizontal component of the magnetic field relative to water flow influenced the rheotactic threshold of fish as part of a shoal, but not of fish tested alone. Results obtained after disabling the lateral line of shoaling individuals with Co2+ suggest that this organ system is involved in the observed magneto-rheotactic response. These findings constitute preliminary evidence that magnetic fields influence rheotaxis and suggest new avenues for further research.

Passive drift or active swimming in marine organisms?

Predictions of organismal movements in a fluid require knowing the fluid's velocity and potential contributions of the organism's behaviour (e.g. swimming or flying). While theoretical aspects of this work are reasonably well-developed, field-based validation is challenging. A much-needed study recently published by Briscoe and colleagues in Proceedings of the Royal Society B compared movements and distribution of satellite-tracked juvenile sea turtles to virtual particles released in a data-assimilating hindcast ocean circulation model. Substantial differences observed between turtles and particles were considered evidence for an important role of active swimming by turtles. However, the experimental design implicitly assumed that transport predictions were insensitive to (i) start location, (ii) tracking duration, (iii) depth, and (iv) physical processes not depicted in the model. Here, we show that the magnitude of variation in physical parameters between turtles and virtual particles can profoundly alter transport predictions, potentially sufficient to explain the reported differences without evoking swimming behaviour. We present a more robust method to derive the environmental contributions to individual movements, but caution that resolving the ocean velocities experienced by individual organisms remains a problem for assessing the role of behaviour in organismal movements and population distributions.

Magnetic navigation behavior and the oceanic ecology of young loggerhead sea turtles.

During long-distance migrations, animals navigate using a variety of sensory cues, mechanisms and strategies. Although guidance mechanisms are usually studied under controlled laboratory conditions, such methods seldom allow for navigation behavior to be examined in an environmental context. Similarly, although realistic environmental models are often used to investigate the ecological implications of animal movement, explicit consideration of navigation mechanisms in such models is rare. Here, we used an interdisciplinary approach in which we first conducted lab-based experiments to determine how hatchling loggerhead sea turtles (Caretta caretta) respond to magnetic fields that exist at five widely separated locations along their migratory route, and then studied the consequences of the observed behavior by simulating it within an ocean circulation model. Magnetic fields associated with two geographic regions that pose risks to young turtles (due to cold wintertime temperatures or potential displacement from the migratory route) elicited oriented swimming, whereas fields from three locations where surface currents and temperature pose no such risk did not. Additionally, at locations with fields that elicited oriented swimming, simulations indicate that the observed behavior greatly increases the likelihood of turtles advancing along the migratory pathway. Our findings suggest that the magnetic navigation behavior of sea turtles is intimately tied to their oceanic ecology and is shaped by a complex interplay between ocean circulation and geomagnetic dynamics.

Deepwater Horizon oil spill impacts on sea turtles could span the Atlantic.

We investigated the extent that the 2010 Deepwater Horizon oil spill potentially affected oceanic-stage sea turtles from populations across the Atlantic. Within an ocean-circulation model, particles were backtracked from the Gulf of Mexico spill site to determine the probability of young turtles arriving in this area from major nesting beaches. The abundance of turtles in the vicinity of the oil spill was derived by forward-tracking particles from focal beaches and integrating population size, oceanic-stage duration and stage-specific survival rates. Simulations indicated that 321 401 (66 199-397 864) green (Chelonia mydas), loggerhead (Caretta caretta) and Kemp's ridley (Lepidochelys kempii) turtles were likely within the spill site. These predictions compared favourably with estimates from in-water observations recently made available to the public (though our initial predictions for Kemp's ridley were substantially lower than in-water estimates, better agreement was obtained with modifications to mimic behaviour of young Kemp's ridley turtles in the northern Gulf). Simulations predicted 75.2% (71.9-76.3%) of turtles came from Mexico, 14.8% (11-18%) from Costa Rica, 5.9% (4.8-7.9%) from countries in northern South America, 3.4% (2.4-3.5%) from the United States and 1.6% (0.6-2.0%) from West African countries. Thus, the spill's impacts may extend far beyond the current focus on the northern Gulf of Mexico.

Rearing in a distorted magnetic field disrupts the 'map sense' of juvenile steelhead trout.

We used simulated magnetic displacements to test orientation preferences of juvenile steelhead trout (Oncorhynchus mykiss) exposed to magnetic fields existing at the northernmost and southernmost boundaries of their oceanic range. Fish reared in natural magnetic conditions distinguished between these two fields by orienting in opposite directions, with headings that would lead fish towards marine foraging grounds. However, fish reared in a spatially distorted magnetic field failed to distinguish between the experimental fields and were randomly oriented. The non-uniform field in which fish were reared is probably typical of fields that many hatchery fish encounter due to magnetic distortions associated with the infrastructure of aquaculture. Given that the reduced navigational abilities we observed could negatively influence marine survival, homing ability and hatchery efficiency, we recommend further study on the implications of rearing salmonids in unnatural magnetic fields.

Finding the 'lost years' in green turtles: insights from ocean circulation models and genetic analysis.

Organismal movement is an essential component of ecological processes and connectivity among ecosystems. However, estimating connectivity and identifying corridors of movement are challenging in oceanic organisms such as young turtles that disperse into the open sea and remain largely unobserved during a period known as 'the lost years'. Using predictions of transport within an ocean circulation model and data from published genetic analysis, we present to our knowledge, the first basin-scale hypothesis of distribution and connectivity among major rookeries and foraging grounds (FGs) of green turtles (Chelonia mydas) during their 'lost years'. Simulations indicate that transatlantic dispersal is likely to be common and that recurrent connectivity between the southwestern Indian Ocean and the South Atlantic is possible. The predicted distribution of pelagic juvenile turtles suggests that many 'lost years hotspots' are presently unstudied and located outside protected areas. These models, therefore, provide new information on possible dispersal pathways that link nesting beaches with FGs. These pathways may be of exceptional conservation concern owing to their importance for sea turtles during a critical developmental period.

Predicting the distribution of oceanic-stage Kemp's ridley sea turtles.

The inaccessibility of open ocean habitat and the cryptic nature of small animals are fundamental problems when assessing the distribution of oceanic-stage sea turtles and other marine animals sharing similar life-history traits. Most methods that estimate patterns of abundance cannot be applied in situations that are extremely data limited. Here, we use a movement ecology framework to generate the first predicted distributions for the oceanic stage of the Kemp's ridley sea turtle (Lepidochelys kempii). Our simulations of particle dispersal within ocean circulation models reveal substantial annual variation in distribution and survival among simulated cohorts. Such techniques can help prioritize areas for conservation, and supply inputs for more realistic demographic models attempting to characterize population trends.

Modeling juvenile sea turtle bycatch risk in commercial and recreational fisheries.

Understanding the drivers of fisheries bycatch is essential for limiting its impacts on vulnerable species. Here we present a model to estimate the relative magnitude of sea turtle bycatch in major coastal fisheries across the southeastern US based on spatiotemporal variation in fishing effort and the simulated distributions of juvenile Kemp's ridley (Lepidochelys kempii) and green (Chelonia mydas) sea turtles recruiting from oceanic to nearshore habitats. Over the period modeled (1996-2017), bycatch in recreational fisheries was estimated to be greater than the sum of bycatch that occurred in commercial fisheries that have historically been considered high risks to turtles (e.g., those using trawls, gillnets, and bottom longlines). Prioritizing engagement with recreational anglers to reduce bycatch could be especially beneficial to sea turtle populations. Applying lessons learned from efforts to protect turtles in commercial fisheries may help meet the challenges that arise from the large, diffuse recreational fishing sector.

Simulating transoceanic migrations of young loggerhead sea turtles: merging magnetic navigation behavior with an ocean circulation model.

Young loggerhead sea turtles (Caretta caretta) from eastern Florida, USA, undertake a transoceanic migration in which they gradually circle the Sargasso Sea before returning to the North American coast. Loggerheads possess a 'magnetic map' in which regional magnetic fields elicit changes in swimming direction along the migratory pathway. In some geographic areas, however, ocean currents move more rapidly than young turtles can swim. Thus, the degree to which turtles can control their migratory movements has remained unclear. In this study, the movements of young turtles were simulated within a high-resolution ocean circulation model using several different behavioral scenarios, including one in which turtles drifted passively and others in which turtles swam briefly in accordance with experimentally derived data on magnetic navigation. Results revealed that small amounts of oriented swimming in response to regional magnetic fields profoundly affected migratory routes and endpoints. Turtles that engaged in directed swimming for as little as 1-3 h per day were 43-187% more likely than passive drifters to reach the Azores, a productive foraging area frequented by Florida loggerheads. They were also more likely to remain within warm-water currents favorable for growth and survival, avoid areas on the perimeter of the migratory route where predation risk and thermal conditions pose threats, and successfully return to the open-sea migratory route if carried into coastal areas. These findings imply that even weakly swimming marine animals may be able to exert strong effects on their migratory trajectories and open-sea distributions through simple navigation responses and minimal swimming.

Geomagnetic imprinting: A unifying hypothesis of long-distance natal homing in salmon and sea turtles.

Several marine animals, including salmon and sea turtles, disperse across vast expanses of ocean before returning as adults to their natal areas to reproduce. How animals accomplish such feats of natal homing has remained an enduring mystery. Salmon are known to use chemical cues to identify their home rivers at the end of spawning migrations. Such cues, however, do not extend far enough into the ocean to guide migratory movements that begin in open-sea locations hundreds or thousands of kilometers away. Similarly, how sea turtles reach their nesting areas from distant sites is unknown. However, both salmon and sea turtles detect the magnetic field of the Earth and use it as a directional cue. In addition, sea turtles derive positional information from two magnetic elements (inclination angle and intensity) that vary predictably across the globe and endow different geographic areas with unique magnetic signatures. Here we propose that salmon and sea turtles imprint on the magnetic field of their natal areas and later use this information to direct natal homing. This novel hypothesis provides the first plausible explanation for how marine animals can navigate to natal areas from distant oceanic locations. The hypothesis appears to be compatible with present and recent rates of field change (secular variation); one implication, however, is that unusually rapid changes in the Earth's field, as occasionally occur during geomagnetic polarity reversals, may affect ecological processes by disrupting natal homing, resulting in widespread colonization events and changes in population structure.

Animal navigation: What is truth?

'True navigation' indicates that animals can move toward a destination without using familiar landmarks. Migratory birds apparently achieve this by extrapolating their position from geomagnetic cues. What this ability implies about the function and representation of animals' large-scale maps remains uncertain.

Map-like use of Earth's magnetic field in sharks.

Migration is common in marine animals,1-5 and use of the map-like information of Earth's magnetic field appears to play an important role.2,6-9 While sharks are iconic migrants10-12 and well known for their sensitivity to electromagnetic fields,13-20 whether this ability is used for navigation is unresolved.14,17,21,22 We conducted magnetic displacement experiments on wild-caught bonnetheads (Sphyrna tiburo) and show that magnetic map cues can elicit homeward orientation. We further show that use of a magnetic map to derive positional information may help explain aspects of the genetic structure of bonnethead populations in the northwest Atlantic.23-26 These results offer a compelling explanation for the puzzle of how migratory routes and population structure are maintained in marine environments, where few physical barriers limit movements of vagile species. VIDEO ABSTRACT.