Kenneth J. Lohmann

The Biology of Sea Turtles

Physiology as Integrated Systems Amanda Southwood Williard Vision Kerstin A. Fritsches and Eric J. Warrant Natal Homing and Imprinting in Sea Turtles Kenneth J. Lohmann, Catherine M.F. Lohmann, J. Roger Brothers, and Nathan F. Putman The Skeleton: An In Vivo View of Structure Jeanette Wyneken Age and Age Estimation in Sea Turtles Larisa Avens and Melissa L. Snover Molecular Genetics of Sea Turtles Michael P. Jensen, Nancy N. FitzSimmons, and Peter H. Dutton Oceanic Habits and Habitats: Dermochelys coriacea Vincent S. Saba Oceanic Habits and Habitats: Caretta caretta Katherine L. Mansfield and Nathan F. Putman Feeding Biology: Advances from Field-Based Observations, Physiological Studies, and Molecular Techniques T. Todd Jones and Jeffrey A. Seminoff Predators, Prey, and the Ecological Roles of Sea Turtles Michael R. Heithaus Exposure to and Effects of Persistent Organic Pollutants Jennifer M. Keller Fisheries Bycatch of Marine Turtles: Lessons Learned from Decades of Research and Conservation Rebecca Lewison, Bryan Wallace, Joana Alfaro-Shigueto, Jeff Mangel, Sara Maxwell, and Elliott Hazen Climate Change and Marine Turtles Mark Hamann, Mariana M.P.B. Fuentes, Natalie C. Ban, and Veronique J.L. Mocellin Free-Ranging Sea Turtle Health Mark Flint Sea Turtle Epibiosis Michael G. Frick and Joseph B. Pfaller Parasites of Marine Turtles Ellis C. Greiner Index

The physics and neurobiology of magnetoreception

Diverse animals can detect magnetic fields but little is known about how they do so. Three main hypotheses of magnetic field perception have been proposed. Electrosensitive marine fish might detect the Earths field through electromagnetic induction, but direct evidence that induction underlies magnetoreception in such fish has not been obtained. Studies in other animals have provided evidence that is consistent with two other mechanisms: biogenic magnetite and chemical reactions that are modulated by weak magnetic fields. Despite recent advances, however, magnetoreceptors have not been identified with certainty in any animal, and the mode of transduction for the magnetic sense remains unknown.

True navigation and magnetic maps in spiny lobsters

Animals are capable of true navigation if, after displacement to a location where they have never been, they can determine their position relative to a goal without relying on familiar surroundings, cues that emanate from the destination, or information collected during the outward journey. So far, only a few animals, all vertebrates, have been shown to possess true navigation. Those few invertebrates that have been carefully studied return to target areas using path integration, landmark recognition, compass orientation and other mechanisms that cannot compensate for displacements into unfamiliar territory. Here we report, however, that the spiny lobster Panulirus argus oriented reliably towards a capture site when displaced 12–37 km to unfamiliar locations, even when deprived of all known orientation cues en route. Little is known about how lobsters and other animals determine position during true navigation. To test the hypothesis that lobsters derive positional information from the Earths magnetic field, lobsters were exposed to fields replicating those that exist at specific locations in their environment. Lobsters tested in a field north of the capture site oriented themselves southwards, whereas those tested in a field south of the capture site oriented themselves northwards. These results imply that true navigation in spiny lobsters, and perhaps in other animals, is based on a magnetic map sense.

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 Earths 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.

Magnetoreception in animals

Determining how animals orient themselves using Earth’s magnetic field can be even more difficult than finding a needle in a haystack. It is like finding a needle in a stack of needles.

The neurobiology of magnetoreception in vertebrate animals

Diverse vertebrate animals can sense the earths magnetic field, but little is known about the physiological mechanisms that underlie this sensory ability. Three major hypotheses of magnetic-field detection have been proposed. Electrosensitive marine fish might sense the geomagnetic field through electromagnetic induction, although definitive evidence that such fish actually do so has not yet been obtained. Studies with other vertebrates have provided evidence consistent with two different mechanisms: biogenic magnetite and chemical reactions that are modulated by magnetic fields. Despite recent progress, however, primary magnetoreceptors have not yet been identified unambiguously in any animal.

Long-distance navigation in sea turtles

Adult sea turtles of several species migrate across vast expanses of ocean to arrive at specific nesting areas and feeding sites. Two hypotheses have been proposed to account for this remarkable navigation. The first is that chemical cues emanating from target areas guide turtles to their destinations. The second is that turtles can approximate their position relative to target regions using features of the earths magnetic field. Because animals often rely on multiple cues while migrating, the two hypotheses are not mutually exclusive. Satellite tracking experiments have revealed that migrating turtles often swim directly to distant goals, even when traveling perpendicularly to water currents. Because animals usually change course frequently while seeking the source of a chemical plume, the consistency of headings casts doubt on the hypothesis that turtles follow such plumes over great distances. Chemical cues may nevertheless play a role in enabling turtles to recognize a target area in the final stages...

Longitude Perception and Bicoordinate Magnetic Maps in Sea Turtles

Long-distance animal migrants often navigate in ways that imply an awareness of both latitude and longitude. Although several species are known to use magnetic cues as a surrogate for latitude, it is not known how any animal perceives longitude. Magnetic parameters appear to be unpromising as longitudinal markers because they typically vary more in a north-south rather than an east-west direction. Here we report, however, that hatchling loggerhead sea turtles (Caretta caretta) from Florida, USA, when exposed to magnetic fields that exist at two locations with the same latitude but on opposite sides of the Atlantic Ocean, responded by swimming in different directions that would, in each case, help them advance along their circular migratory route. The results demonstrate for the first time that longitude can be encoded into the magnetic positioning system of a migratory animal. Because turtles also assess north-south position magnetically, the findings imply that loggerheads have a navigational system that exploits the Earths magnetic field as a kind of bicoordinate magnetic map from which both longitudinal and latitudinal information can be extracted.

Evidence for Geomagnetic Imprinting as a Homing Mechanism in Pacific Salmon

In the final phase of their spawning migration, Pacific salmon use chemical cues to identify their home river, but how they navigate from the open ocean to the correct coastal area has remained enigmatic. To test the hypothesis that salmon imprint on the magnetic field that exists where they first enter the sea and later seek the same field upon return, we analyzed a 56-year fisheries data set on Fraser River sockeye salmon, which must detour around Vancouver Island to approach the river through either a northern or southern passageway. We found that the proportion of salmon using each route was predicted by geomagnetic field drift: the more the field at a passage entrance diverged from the field at the river mouth, the fewer fish used the passage. We also found that more fish used the northern passage in years with warmer sea surface temperature (presumably because fish were constrained to more northern latitudes). Field drift accounted for 16% of the variation in migratory route used, temperature 22%, and the interaction between these variables 28%. These results provide the first empirical evidence of geomagnetic imprinting in any species and imply that forecasting salmon movements is possible using geomagnetic models.

The sensory ecology of ocean navigation

SUMMARY How animals guide themselves across vast expanses of open ocean, sometimes to specific geographic areas, has remained an enduring mystery of behavioral biology. In this review we briefly contrast underwater oceanic navigation with terrestrial navigation and summarize the advantages and constraints of different approaches used to analyze animal navigation in the sea. In addition, we highlight studies and techniques that have begun to unravel the sensory cues that underlie navigation in sea turtles, salmon and other ocean migrants. Environmental signals of importance include geomagnetic, chemical and hydrodynamic cues, perhaps supplemented in some cases by celestial cues or other sources of information that remain to be discovered. An interesting similarity between sea turtles and salmon is that both have been hypothesized to complete long-distance reproductive migrations using navigational systems composed of two different suites of mechanisms that function sequentially over different spatial scales. The basic organization of navigation in these two groups of animals may be functionally similar, and perhaps also representative of other long-distance ocean navigators.