Catherine M. F. Lohmann

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.

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.

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.

A Light-Independent Magnetic Compass in the Leatherback Sea Turtle

Diverse animals can orient to the earths magnetic field (1-6), but the mechanism or mechanisms undrlying magnetic field detection have not been determined. Behavioral (7-9) amd neurophysiological (10-12) results suggest that the transduction process underlying magnetic compass orientation in vertebrates is light-dependent, a finding consistent with theoretical models proposing that magnetoreception involves a modulation of the response of retinal photoreceptors to light (13, 14). We report, however, that leatherback sea turtle (Dermochelys coriacea) hatchlings orient to the geomagnetic field in complete darkness. Thus, light-dependence is not a universal feature of vertebrate magnetic compasses.

Sea turtles, lobsters, and oceanic magnetic maps

Numerous marine animals can sense the Earths magnetic field and use it as a cue in orientation and navigation. Two distinct types of information can potentially be extracted from the Earths field. Directional or compass information enables animals to maintain a consistent heading in a particular direction such as north or south. In contrast, positional or map information can be used by animals to assess geographic location and, in some cases, to navigate to specific target areas. Marine animals exploit magnetic positional information in at least two different ways. For hatchling loggerhead sea turtles, regional magnetic fields function as open-sea navigational markers, eliciting changes in swimming direction at crucial points in the migratory route. Older sea turtles, as well as spiny lobsters, use magnetic information in a more complex way, exploiting it as a component of a classical navigational map, which permits an assessment of position relative to specific geographic destinations. These “magnetic maps” have not yet been fully characterized. They may be organized in several fundamentally different ways, some of which bear little resemblance to human maps, and they may also be used in conjunction with unconventional navigational strategies. Unraveling the nature of magnetic maps and exploring how they are used represents one of the most exciting frontiers of behavioral and sensory biology.

Migratory guidance mechanisms in marine turtles

Hatchling sea turtles emerge from underground nests, scramble to the ocean, and migrate to the open sea. Loggerhead Caretta caretta hatchlings from eastern Florida, U.S.A., appear to use three different sets of orientation cues sequentially as they migrate offshore. On the beach, hatchlings crawl seaward by orienting toward the low, bright oceanic horizon. In the ocean, turtles initially orient offshore by swimming into waves, which can be detected as wave surge motion or orbital movements. As a hatchling crawls across the beach, swims offshore, or both, it apparently transfers the initial seaward heading to a magnetic compass. This transfer of directional information may allow turtles to maintain offshore courses in deep water where waves no longer move reliably toward land. Sea turtles may use the earths magnetic field not only as a cue for compass orientation but also as a source of positional information. Results have demonstrated that loggerheads can detect inclination angle and field intensity, two geomagnetic features that vary predictably across the earths surface. Hatchlings responded to magnetic features found along their migratory route by swimming in directions that would presumably favor retention within the North Atlantic gyre, an oceanic region favorable for growth and development. How adult turtles navigate to their natal regions to nest is not known. We speculate, however, that adults may exploit geomagnetic features in one of several different ways to guide themselves into the vicinity of a nesting area.

Multi-Modal Homing in Sea Turtles: Modeling Dual Use of Geomagnetic and Chemical Cues in Island-Finding

Sea turtles are capable of navigating across large expanses of ocean to arrive at remote islands for nesting, but how they do so has remained enigmatic. An interesting example involves green turtles (Chelonia mydas) that nest on Ascension Island, a tiny land mass located approximately 2000 km from the turtles’ foraging grounds along the coast of Brazil. Sensory cues that turtles are known to detect, and which might hypothetically be used to help locate Ascension Island, include the geomagnetic field, airborne odorants, and waterborne odorants. One possibility is that turtles use magnetic cues to arrive in the vicinity of the island, then use chemical cues to pinpoint its location. As a first step toward investigating this hypothesis, we used oceanic, atmospheric, and geomagnetic models to assess whether magnetic and chemical cues might plausibly be used by turtles to locate Ascension Island. Results suggest that waterborne and airborne odorants alone are insufficient to guide turtles from Brazil to Ascension, but might permit localization of the island once turtles arrive in its vicinity. By contrast, magnetic cues might lead turtles into the vicinity of the island, but would not typically permit its localization because the field shifts gradually over time. Simulations reveal, however, that the sequential use of magnetic and chemical cues can potentially provide a robust navigational strategy for locating Ascension Island. Specifically, one strategy that appears viable is following a magnetic isoline into the vicinity of Ascension Island until an odor plume emanating from the island is encountered, after which turtles might either: (1) initiate a search strategy; or (2) follow the plume to its island source. These findings are consistent with the hypothesis that sea turtles, and perhaps other marine animals, use a multi-modal navigational strategy for locating remote islands.