Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields

Loggerhead sea turtles (Caretta caretta) derive both directional and positional information from the Earths magnetic field, but the mechanism underlying magnetic field detection in turtles has not been determined. One hypothesis is that crystals of biogenic, single-domain magnetite provide the physical basis of the magnetic sense. As a first step toward determining if magnetite is involved in sea turtle magnetoreception, hatchling loggerheads were exposed to pulsed magnetic fields (40 mT, 4 ms rise time) capable of altering the magnetic dipole moment of biogenic magnetite crystals. A control group of turtles was treated identically but not exposed to the pulsed fields. Both groups of turtles subsequently oriented toward a light source, implying that the pulsed fields did not disrupt the motivation to swim or the ability to maintain a consistent heading. However, when swimming in darkness under conditions in which turtles normally orient magnetically, control turtles oriented significantly toward the offshore migratory direction while those that were exposed to the magnetic pulses did not. These results are consistent with the hypothesis that at least part of the sea turtle magnetoreception system is based on magnetite. In principle, a magnetite-based magnetoreception system might be involved in detecting directional information, positional information, or both.     

Sea turtles, lobsters, and oceanic magnetic maps

Numerous marine animals can sense the Earth's magnetic field and use it as a cue in orientation and navigation. Two distinct types of information can potentially be extracted from the Earth's 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.     

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 Earth's magnetic field as a kind of bicoordinate magnetic map from which both longitudinal and latitudinal information can be extracted.     

Compass Orientation During Dispersal of Freshwater Hatchling Snapping Turtles (Chelydra serpentina) and Blanding's Turtles (Emydoidea blandingii)

Freshwater turtle hatchlings primarily use visual cues for orientation while dispersing from nests; however, hatchlings rapidly develop a relationship between a sun or geomagnetic compass and a dispersal target that allows them to maintain an established direction of movement when target habitats are not visible. We examined dispersal patterns of hatchling snapping turtles (Chelydra serpentina) and Blanding's turtles (Emydoidea blandingii) dispersing in large arenas in a mowed field and in dense corn. The dispersal of three categories of hatchlings were examined: (1) naïve individuals (no previous dispersal experience), (2) arena‐experienced (limited dispersal experience in arenas in natural habitat), and (3) natural‐experienced hatchling Blanding's turtles (captured after extensive experience dispersing W in natural habitats toward wetlands). Experienced hatchlings were assigned to treatments consisting of having a magnet or a non‐magnetic aluminum sham or nothing glued to their anterior carapace before release in the corn arena. Dispersal patterns of naïve hatchlings of both species were strongly directional in the field arena with visible target horizons and primarily random in the corn arena where typical target horizons were blocked. When released in corn, dispersal patterns were similar for arena‐experienced hatchlings with magnets or shams attached and differed from their prior dispersal headings in the field arena as naïve hatchlings. Natural‐experienced hatchling Blanding's turtles with and without magnets were able to accurately maintain their prior headings to the WNW while dispersing in the field or corn arenas (i.e., the presence of a magnet did not disrupt their ability to maintain their prior heading). Based on the assumption that no other type of compass exists in hatchlings, we conclude that they were not using a geomagnetic compass, but by default were using sun compass orientation to maintain dispersal headings in dense corn where no typical target habitats were visible.     

Warm water and cool nests are best. How global warming might influence hatchling green turtle swimming performance

For sea turtles nesting on beaches surrounded by coral reefs, the most important element of hatchling recruitment is escaping predation by fish as they swim across the fringing reef, and as a consequence hatchlings that minimize their exposure to fish predation by minimizing the time spent crossing the fringing reef have a greater chance of surviving the reef crossing. One way to decrease the time required to cross the fringing reef is to maximize swimming speed. We found that both water temperature and nest temperature influence swimming performance of hatchling green turtles, but in opposite directions. Warm water increases swimming ability, with hatchling turtles swimming in warm water having a faster stroke rate, while an increase in nest temperature decreases swimming ability with hatchlings from warm nests producing less thrust per stroke.     

Responses of hatchling sea turtles to rotational displacements

After emerging from underground nests, sea turtle hatchlings migrate through the surf zone and out to the open ocean. During this migration, both waves and water currents can disrupt hatchling orientation by unpredictably rotating the turtles away from their migratory headings. In addition, waves cause turtles to roll and pitch, temporarily impeding forward swimming by forcing the hatchlings into steeply inclined positions. To maintain seaward orientation and remain upright in the water column, hatchlings must continuously compensate for such displacements. As a first step toward determining how this is achieved, we studied the responses of loggerhead (Caretta caretta L.) sea turtle hatchlings to rotational displacements involving yaw, roll, and pitch. Hatchlings responded to rotations in the horizontal plane (yaw) by extending the rear flipper on the side opposite the direction of rotation. Thus, the flipper presumably acts as a rudder to help turn the turtle back toward its original heading. Turtles responded to rotations in the roll plane with stereotypic movements of the front flippers that act to right the hatchlings with respect to gravity. Finally, hatchlings responded to rotations in the pitch plane with movements of the hind flippers that appear likely to curtail or counteract the pitching motion. Thus, the results of these experiments imply that young sea turtles emerge from their nests possessing a suite of stereotypic behavioral responses that function to counteract rotational displacements, enable the animals to maintain equilibrium, and facilitate efficient movement toward the open sea.     

Magnetic orientation and navigation in marine turtles, lobsters, and molluscs: concepts and conundrums

The Earth's magnetic field provides a pervasive source of directionalinformation used by phylogenetically diverse marine animals.Behavioral experiments with sea turtles, spiny lobsters, andsea slugs have revealed that all have a magnetic compass sense,despite vast differences in the environment each inhabits andthe spatial scale over which each moves. For two of these animals,the Earth's field also serves as a source of positional information.Hatchling loggerhead sea turtles from Florida responded to themagnetic fields found in three widely separated regions of theAtlantic Ocean by swimming in directions that would, in eachcase, facilitate movement along the migratory route. Thus, foryoung loggerheads, regional magnetic fields function as navigationalmarkers and elicit changes in swimming direction at crucialgeographic boundaries. Older turtles, as well as spiny lobsters,apparently acquire a "magnetic map" that enables them to usemagnetic topography to determine their position relative tospecific goals. Relatively little is known about the neuralmechanisms that underlie magnetic orientation and navigation.A promising model system is the marine mollusc Tritonia diomedea,which possesses both a magnetic compass and a relatively simplenervous system. Six neurons in the brain of T. diomedea havebeen identified that respond to changes in magnetic fields.At least some of these appear to be ciliary motor neurons thatgenerate or modulate the final behavioral output of the orientationcircuitry. These findings represent an encouraging step towarda holistic understanding of the cells and circuitry that underliemagnetic orientation behavior in one model organism.     

Navigation by green turtles: which strategy do displaced adults use to find Ascension Island?

Sea turtles are known to perform long-distance, oceanic migrations between disparate feeding areas and breeding sites, some of them located on isolated oceanic islands. These migrations demonstrate impressive navigational abilities, but the sensory mechanisms used are still largely unknown. Green turtles breeding at Ascension Island perform long oceanic migrations (>2200 km) between foraging areas along the Brazilian coast and the isolated island. By performing displacement experiments of female green turtles tracked by satellite telemetry in the waters around Ascension Island we investigated which strategies most probably are used by the turtles in locating the island. In the present paper we analysed the search trajectories in relation to alternative navigation strategies including the use of global geomagnetic cues, ocean currents, celestial cues and wind. The results suggest that the turtles did not use chemical information transported with ocean currents. Neither did the results indicate that the turtles use true bi-coordinate geomagnetic navigation nor did they use indirect navigation with respect to any of the available magnetic gradients (total field intensity, horizontal field intensity, vertical field intensity, inclination and declination) or celestial cues. The female green turtles successfully locating Ascension Island seemed to use a combination of searching followed by beaconing, since they searched for sensory contact with the island until they reached positions NW and N of the Island and from there presumably used cues transported by wind to locate the island during the final stages of the search.     

The role of geomagnetic cues in green turtle open sea navigation

Background

Laboratory and field experiments have provided evidence that sea turtles use geomagnetic cues to navigate in the open sea. For instance, green turtles (Chelonia mydas) displaced 100 km away from their nesting site were impaired in returning home when carrying a strong magnet glued on the head. However, the actual role of geomagnetic cues remains unclear, since magnetically treated green turtles can perform large scale (>2000 km) post-nesting migrations no differently from controls.

Methodology/Principal Findings

In the present homing experiment, 24 green turtles were displaced 200 km away from their nesting site on an oceanic island, and tracked, for the first time in this type of experiment, with Global Positioning System (GPS), which is able to provide much more frequent and accurate locations than previously used tracking methods. Eight turtles were magnetically treated for 24–48 h on the nesting beach prior to displacement, and another eight turtles had a magnet glued on the head at the release site. The last eight turtles were used as controls. Detailed analyses of water masses-related (i.e., current-corrected) homing paths showed that magnetically treated turtles were able to navigate toward their nesting site as efficiently as controls, but those carrying magnets were significantly impaired once they arrived within 50 km of home.

Conclusions/Significance

While green turtles do not seem to need geomagnetic cues to navigate far from the goal, these cues become necessary when turtles get closer to home. As the very last part of the homing trip (within a few kilometers of home) likely depends on non-magnetic cues, our results suggest that magnetic cues play a key role in sea turtle navigation at an intermediate scale by bridging the gap between large and small scale navigational processes, which both appear to depend on non-magnetic cues.     

The magnetic map of hatchling loggerhead sea turtles

Young loggerhead sea turtles (Caretta caretta) from eastern Florida, U.S.A., undertake a transoceanic migration in which they gradually circle the North Atlantic Ocean before returning to the North American coast. Hatchlings in the open sea are guided at least partly by a 'magnetic map' in which regional magnetic fields function as navigational markers and elicit changes in swimming direction at crucial locations along the migratory route. The magnetic map exists in turtles that have never migrated and thus appears to be inherited. Turtles derive both longitudinal and latitudinal information from the Earth's field, most likely by exploiting unique combinations of field inclination and intensity that occur in different geographic areas. Similar mechanisms may function in the migrations of diverse animals.     

Does maternal oviposition site influence offspring dispersal to suitable habitat?

Orientation and dispersal to suitable habitat affects fitness in many animals, but the factors that govern these behaviors are poorly understood. In many turtle species, hatchlings must orient and disperse to suitable aquatic habitat immediately after emergence from subterranean nests. Thus, the location of nest sites relative to aquatic habitats ideally should be associated with the direction of hatchling dispersal. At our study site, painted turtles (Chrysemys picta) nest to the west (on an island) and east (on the mainland) of a wetland, which determines the direction that hatchlings must travel to reach suitable aquatic habitat. To determine if hatchling orientation is intrinsically influenced by the location where their mothers nest, we employed a two-part cross-fostering experiment in the field, whereby half the eggs laid in mainland nests were swapped with half the eggs laid in island nests. Moreover, because C. picta hatchlings overwinter inside their nests, we performed a second cross-fostering experiment to fully decouple the effects of (1) the maternally chosen nest location, (2) the embryonic developmental location, and (3) the overwinter location. We released hatchlings into a circular arena in the field and found that turtles generally dispersed in a westerly direction, regardless of the maternally chosen nest location and independent of the locations of embryonic development and overwintering. Although this westerly direction was towards suitable aquatic habitat, we could not distinguish whether naïve hatchling turtles (i) use environmental cues/stimuli to orient their movement, or (ii) have an intrinsic bias to orient west in the absence of stimuli. Nevertheless, these findings suggest that the orientation behavior of naïve hatchling turtles during terrestrial dispersal is not dependent upon the location of maternally-chosen nest sites.     

Swimming behaviour and dispersal patterns of headstarted loggerhead turtles Caretta caretta

Swimming behaviour and dispersal patterns were studied in headstarted loggerhead turtles Caretta caretta which were released at three different sites on the Caribbean island of Curaçao (Netherlands Antilles) and at one site on the neighbouring island of Klein Curaçao, after 1–2.5 yrs of captivity. Turtles were tagged and followed up to a distance of 6125 m offshore, using a boat with a Global Positioning Unit. The released turtles reverted to typical hatchling behaviour and showed an offshore migration almost perpendicular to the coastline. No significant differences were found in directional swimming among the four sites. The turtles swam almost continuously about 30 cm under the water surface; their mean overall swimming speed was higher than in adult wild loggerheads suggesting a 'frenzy'-like swimming stage. The turtles exhibited diving behaviour, and the dive frequency and duration was comparable to that of similar-sized (wild) turtles. The present study demonstrates that upon release the headstarted loggerheads behave naturally and show dispersal patterns similar to wild hatchling turtles. The fact that the released turtles were still able to show offshore directional swimming suggests that the headstarting did not affect their short-term orientation abilities.     

Fuel use and corticosterone dynamics in hatchling green sea turtles (Chelonia mydas) during natal dispersal

During their natal dispersal hatchling sea turtles depart their nest, beach and inshore areas quickly to move into offshore developmental habitat using their finite energy stores. Patterns of fuel use and endocrine responses that could facilitate hatchling sea turtle dispersal activity are poorly understood. This study, examined aspects of intermediary metabolism by measuring plasma fuel use and an endocrine response of hatchling green turtles (Chelonia mydas) during terrestrial and aquatic activity coinciding with natal dispersal. Specifically, we measured plasma concentrations of glucose, non-esterised free fatty acids and protein to gauge the contributions of carbohydrate, lipid and protein metabolism for fuelling natal dispersal. In addition, we measured plasma levels of the steroid hormone corticosterone (CORT) a hormone implicated in regulating a number of metabolic events associated with migration and energy use in vertebrates. During terrestrial activity, hatchlings ascended through the sand from their nests and exhibited significant increases in plasma CORT and lactate indicating intense periods of anaerobic activity. During swimming, all plasma metabolites, with the exception of plasma protein, peaked between 1 and 4 h post-beginning swimming activity. Plasma CORT peaked at between 3 and 5 h of swimming activity. These plasma concentrations are consistent with intensive activity inducing catabolism of carbohydrate, lipid and protein stores to support prolonged activity. These results are similar to other vertebrates and suggest a relatively uniform cascade of physiological processes during such arduous migratory events.     

The role of skylight polarization in the orientation of a day-migrating bird species

To assess the role of skylight polarization in the orientation system of a day-migrating bird, Yellow-faced Honeyeaters (Lichenostomus chrysops, Meliphagidae) were tested in funnel cages for their directional preferences. In control tests in the natural local geomagnetic field under the clear natural sky, they preferred their normal migratory course. Manipulations of the e-vector by depolarizing the skylight or rotating the axis of polarization failed to affect the orientation as long as the natural geomagnetic field was present. When deprived of magnetic information, the birds continued in their normal migratory direction as long as they had access to information from the natural sky, or when either the sun or polarized light was available. However, when sun was hidden by clouds, depolarizers caused disorientation. — These findings indicate that polarized skylight can be used for orientation when no other known cues are available. However in the hierarchy of cues of this species, the polarization pattern clearly ranks lower than information from the geomagnetic field.     

Magnetic maps in animals: a theory comes of age?

The magnetic map hypothesis proposes that animals can use spatial gradients in the Earth's magnetic field to help determine geographic location. This ability would permit true navigation--reaching a goal from an entirely unfamiliar site with no goal-emanating cues to assist. It is a highly contentious hypothesis since the geomagnetic field fluctuates in time and spatial gradients may be disturbed by geological anomalies. Nevertheless, a substantial body of evidence offers support for the hypothesis. Much of the evidence has been indirect in nature, such as the identification of avian magnetoreceptor mechanisms with functional properties that are consistent with those of a putative map detector or the patterns of orientation of animals exposed to temporal and/or spatial geomagnetic anomalies. However; the most important advances have been made in conducting direct tests of the magnetic map hypothesis by exposing experienced migrants to specific geomagnetic values representing simulated displacements. Appropriate shifts in the direction of orientation, which compensate for the simulated displacements, have been observed in newts, birds, sea turtles, and lobsters, and provide the strongest evidence to date for magnetic map navigation. Careful experimental design and interpretation of orientation data will be essential in the future to determine which components of the magnetic field are used to derive geographic position.     

Marine turtles use geomagnetic cues during open-sea homing

Marine turtles are renowned long-distance navigators, able to reach remote targets in the oceanic environment; yet the sensory cues and navigational mechanisms they employ remain unclear [1, 3]. Recent arena experiments indicated an involvement of magnetic cues in juvenile turtles' homing ability after simulated displacements [4, 5], but the actual role of geomagnetic information in guiding turtles navigating in their natural environment has remained beyond the reach of experimental investigations. In the present experiment, twenty satellite-tracked green turtles (Chelonia mydas) were transported to four open-sea release sites 100-120 km from their nesting beach on Mayotte island in the Mozambique Channel; 13 of them had magnets attached to their head either during the outward journey or during the homing trip. All but one turtle safely returned to Mayotte to complete their egg-laying cycle, albeit with indirect routes, and showed a general inability to take into account the deflecting action of ocean currents as estimated through remote-sensing oceanographic measurements [7]. Magnetically treated turtles displayed a significant lengthening of their homing paths with respect to controls, either when treated during transportation or when treated during homing. These findings represent the first field evidence for the involvement of geomagnetic cues in sea-turtle navigation.     

Magnetic field perception in the rainbow trout Oncorynchus mykiss: magnetite mediated, light dependent or both?

In the present study, we demonstrate the role of the trigeminal system in the perception process of different magnetic field parameters by heartbeat conditioning, i.e. a significantly longer interval between two consecutive heartbeats after magnetic stimulus onset in the salmonid fish Oncorhynchus mykiss. The electrocardiogram was recorded with subcutaneous silver wire electrodes in freely swimming fish. Inactivation of the ophthalmic branch of the trigeminal nerve by local anaesthesia revealed its role in the perception of intensity/inclination of the magnetic field by abolishing the conditioned response (CR). In contrast, experiments with 90° direction shifts clearly showed the normal conditioning effect during trigeminal inactivation. In experiments under red light and in darkness, CR occurred in case of both the intensity/inclination stimulation and 90° direction shifts, respectively. With regard to the data obtained, we propose the trigeminal system to perceive the intensity/inclination of the magnetic field in rainbow trouts and suggest the existence of another light-independent sensory structure that enables fish to detect the magnetic field direction.     

High thermal variance in naturally incubated turtle nests produces faster offspring

The effects of climate change on populations are complex and difficult to predict, and can result in mismatches between interdependent organisms or between organisms and their environment. Reptiles with temperature-dependent sex determination may be able to compensate for potential skews in offspring sex ratio caused by climate change by selecting cooler (i.e., shadier) nest sites. Although changing nest location may prevent sex ratio skews, it may also affect thermally sensitive performance traits in offspring. I tested righting, sprinting, and swimming performance in hatchling painted turtles (Chrysemys picta), produced by female turtles from five populations across the species’ geographic range, nesting in a common-garden environment. I found that speed of hatchling performance was faster in hatchlings whose mothers originated from warmer climates, and that nests with higher mean daily variation in incubation temperature produced faster hatchlings. These results suggest that the increased temperatures predicted by climate change models could result in hatchling turtles that are faster at sprinting and swimming; however, it is not yet known how these performance measures translate into fitness.     

Swimming performance of hatchling green turtles is affected by incubation temperature

In an experiment repeated for two separate years, incubation temperature was found to affect the body size and swimming performance of hatchling green turtles (Chelonia mydas). In the first year, hatchlings from eggs incubated at 26°C were larger in size than hatchlings from 28 and 30°C, whilst in the second year hatchlings from 25.5°C were similar in size to hatchings from 30°C. Clutch of origin influenced the size of hatchlings at all incubation temperatures even when differences in egg size were taken into account. In laboratory measurements of swimming performance, in seawater at 28°C, hatchlings from eggs incubated at 25.5 and 26°C had a lower stroke rate frequency and lower force output than hatchlings from 28 and 30°C. These differences appeared to be caused by the muscles of hatchlings from cooler temperatures fatiguing at a faster rate. Clutch of origin did not influence swimming performance. This finding that hatchling males incubated at lower temperature had reduced swimming ability may affect their survival whilst running the gauntlet of predators in shallow near-shore waters, prior to reaching the relative safety of the open sea.     

Light effects on the multicellular magnetotactic prokaryote ‘<Emphasis Type="Italic">Candidatus</Emphasis> Magnetoglobus multicellularis’ are cancelled by radiofrequency fields: the involvement of radical pair mechanisms

‘Candidatus Magnetoglobus multicellularis’ is the most studied multicellular magnetotactic prokaryote. It presents a light-dependent photokinesis: green light decreases the translation velocity whereas red light increases it, in comparison to blue and white light. The present article shows that radio-frequency electromagnetic fields cancel the light effect on photokinesis. The frequency to cancel the light effect corresponds to the Zeeman resonance frequency (DC magnetic field of 4 Oe and radio-frequency of 11.5 MHz), indicating the involvement of a radical pair mechanism. An analysis of the orientation angle relative to the magnetic field direction shows that radio-frequency electromagnetic fields disturb the swimming orientation when the microorganisms are illuminated with red light. The analysis also shows that at low magnetic fields (1.6 Oe) the swimming orientation angles are well scattered around the magnetic field direction, showing that magnetotaxis is not efficiently in the swimming orientation to the geomagnetic field. The results do not support cryptochrome as being the responsible chromophore for the radical pair mechanism and perhaps two different chromophores are necessary to explain the radio-frequency effects.