Article

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

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Abstract

The use of "map-like" information from 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 naïve 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.

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... For instance, if anadromous and nonanadromous populations respond to magnetic displacements similarly, this might indicate that magnetic map cues are used as a general-purpose tool for establishing relative latitude (Bingman and Cheng 2005). In contrast, if the anadromous population displayed more robust responses to the magnetic displacements than the nonanadromous population, this may suggest that the magnetic map functions as a guidance mechanism to follow a population-specific marine migration route (Putman et al. 2020). ...
... Assuming such orientation biases are heritable, those salmon that choose favorable directions may be more likely to successfully complete their oceanic migration, return to spawn, and pass on that orientation bias to their offspring (Putman 2015). Such a process likely explains the ability of juveniles in other species to undertake complex marine migrations despite navigational naivety (Lohmann et al. 2001;Naisbett-Jones et al. 2017;Putman et al. 2020). ...
... 2C, 2E) (Bingman and Cheng 2005;Putman 2015) and for finer-scale information to follow along the migration route (Figs. 2D, 2E) (Putman et al. 2020). The finding that distinct populations of salmon may differentially orient to magnetic fields offers a potential way to investigate questions that have been major challenges to salmon management for decades (Neave 1964;Royce et al. 1968;Harden-Jones 1968). ...
Article
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Many animals undertaking long-distance migrations use Earth’s magnetic field as a “map” to assess their position for orientation. This phenomenon been particularly well-studied in salmonids using “magnetic displacement” experiments, in which animals are presented with magnetic field conditions that are characteristic of other geographic locations. However, whether use of magnetic map cues differs among populations of salmon has not been investigated. Here we show that nonanadromous and anadromous populations of Atlantic salmon (Salmo salar) raised under the same conditions within their native range differ in their response to magnetic displacements in the North Atlantic. The directions adopted by anadromous salmon juveniles to each of the magnetic displacements would support their migration from the eastern US to western Greenland, had the fish actually been at those locations. In contrast, nonanadromous salmon did not appear to respond to the magnetic displacements. The findings are consistent with the hypothesis that the innate magnetic map of anadromous salmon is adapted to guide their marine migration.
... The constant movement of most wildlife species in and out of varying artificial EMF can result in high exposures near communication structures, especially for flying species such as birds and insects. There is a substantial amount of scientific literature on the disrupting effects of RFR on wildlife (e.g., [190][191][192][193][194][195][196][197][198][199][200][201][202][203][204][205][206]). ...
... Many nonhuman species use Earth's geomagnetic fields for activities such as orientation and seasonal migration, food finding, mating, nest and den building [190]. For example, migratory bird species [191,192], honeybees [193], bats [194], fish [195][196][197], and numerous other species sense Earth's magnetic fields with specialized sensory receptors. Mechanisms likely involved in magneto-reception include magnetic induction of weak electric signals in specialized sensory receptors [198], magneto-mechanical interactions with the iron-based crystal magnetite [194], and/or free-radical interactions with cryptochrome photoreceptors [191,192]. ...
Article
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In the late-1990s, the FCC and ICNIRP adopted radiofrequency radiation (RFR) exposure limits to protect the public and workers from adverse effects of RFR. These limits were based on results from behavioral studies conducted in the 1980s involving 40–60-minute exposures in 5 monkeys and 8 rats, and then applying arbitrary safety factors to an apparent threshold specific absorption rate (SAR) of 4 W/kg. The limits were also based on two major assumptions: any biological effects were due to excessive tissue heating and no effects would occur below the putative threshold SAR, as well as twelve assumptions that were not specified by either the FCC or ICNIRP. In this paper, we show how the past 25 years of extensive research on RFR demonstrates that the assumptions underlying the FCC’s and ICNIRP’s exposure limits are invalid and continue to present a public health harm. Adverse effects observed at exposures below the assumed threshold SAR include non-thermal induction of reactive oxygen species, DNA damage, cardiomyopathy, carcinogenicity, sperm damage, and neurological effects, including electromagnetic hypersensitivity. Also, multiple human studies have found statistically significant associations between RFR exposure and increased brain and thyroid cancer risk. Yet, in 2020, and in light of the body of evidence reviewed in this article, the FCC and ICNIRP reaffirmed the same limits that were established in the 1990s. Consequently, these exposure limits, which are based on false suppositions, do not adequately protect workers, children, hypersensitive individuals, and the general population from short-term or long-term RFR exposures. Thus, urgently needed are health protective exposure limits for humans and the environment. These limits must be based on scientific evidence rather than on erroneous assumptions, especially given the increasing worldwide exposures of people and the environment to RFR, including novel forms of radiation from 5G telecommunications for which there are no adequate health effects studies.
... Several groups of animals that migrate when young are now known to have magnetic maps which help them navigate along migratory pathways and/or remain in appropriate geographic areas (e.g., Lohmann et al. 2001Lohmann et al. , 2012Putman et al. 2014cPutman et al. , 2020. In most such cases, magnetic fields that exist in particular geographic regions elicit directional changes at crucial locations and boundaries. ...
... The extent to which an animal relies on a magnetic map to guide its movement may depend in part on the nature of the environment and the degree to which alternative cues exist. Interestingly, at least two marine animals, loggerhead turtles and pink salmon, appear to rely at least partly on magnetic map information throughout their life cycle, from the first migration that the young undertake to the time when adults return to their natal area to reproduce Putman et al. 2014aPutman et al. , 2020Brothers and Lohmann 2015). An intriguing possibility is that magnetoreception is particularly well developed among marine animals, in part because so few other directional and positional cues are available in the open sea to animals that travel well below the surface. ...
Article
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In addition to providing animals with a source of directional or ‘compass’ information, Earth’s magnetic field also provides a potential source of positional or ‘map’ information that animals might exploit to assess location. In less than a generation, the idea that animals use Earth’s magnetic field as a kind of map has gone from a contentious hypothesis to a well-established tenet of animal navigation. Diverse animals ranging from lobsters to birds are now known to use magnetic positional information for a variety of purposes, including staying on track along migratory pathways, adjusting food intake at appropriate points in a migration, remaining within a suitable oceanic region, and navigating toward specific goals. Recent findings also indicate that sea turtles, salmon, and at least some birds imprint on the magnetic field of their natal area when young and use this information to facilitate return as adults, a process that may underlie long-distance natal homing (a.k.a. natal philopatry) in many species. Despite recent progress, much remains to be learned about the organization of magnetic maps, how they develop, and how animals use them in navigation.
... Magnetoreceptive species, such as the loggerhead sea turtle (Caretta caretta (Lohmann andLohmann 1994, 1996;Putman et al. 2011)), chinook salmon (Oncorhynchus tshawytscha (Putman et al. 2013(Putman et al. , 2014), pink salmon (O. gorbuscha (Putman et al. 2020)), Atlantic salmon (Salmo salar (Scanlan et al. 2018)), and European eel (Anguilla anguilla (Naisbett-Jones et al. 2017)), can use GMF intensity and inclination angle to form a bicoordinate magnetic map, use it to determine their current location, and make navigational course corrections toward their goal. Interestingly, juvenile sea turtles, salmon, and eels are known to imprint on the GMF signatures of their natal habitats (Lohmann 1991;Naisbett-Jones et al. 2017;Putman et al. 2011Putman et al. , 2014 and, as adults, use these magnetic data to successfully migrate back to these specific locations for reproduction. ...
... This study provides the first behavioral evidence that a stingray can detect and distinguish between the GMF cues used by other species to derive a sense of location. Magnetic pseudo-displacement experiments have shown that juvenile loggerhead sea turtles (Lohmann andLohmann 1994, 1996;Putman et al. 2011), European eels (Naisbett-Jones et al. 2017), Chinook (Putman et al. 2014), Atlantic (Scanlan et al. 2018), and pink salmon (Putman et al. 2020) use these cues to form a bicoordinate magnetic map and gain a sense of location. Recent evidence indicates that bonnethead sharks can use the GMF to derive a sense of location and orient toward a home range (Keller 2020); however, this ability has yet to be shown in any batoid (skate or ray). ...
Article
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Elasmobranch fishes (sharks, skates, and rays) are hypothesized to use environmental cues, such as the geomagnetic field (GMF), to navigate across the ocean. However, testing the sensory and navigation abilities of large highly migratory fishes in the field is challenging. This laboratory study tested whether the yellow stingray, Urobatis jamaicensis, could detect and distinguish between the GMF cues used by other magnetically sensitive species to actively determine their location. Stingrays were divided into two cohorts for initial behavioral conditioning: one was trained to associate a change in GMF intensity with an aversive stimulus, whereas the other was trained using a change in GMF inclination angle. Individuals from each cohort remained naïve to the GMF conditioning stimulus used to condition the other cohort. The combined group learned the initial association within a mean (± SE) of 184.0 ± 34.8 trials. Next, stingrays from each cohort were randomly exposed to their original GMF conditioning stimulus and the novel GMF stimulus. The original magnetic stimulus continued to be reinforced, whereas the novel stimulus was not. The group demonstrated a significantly different response to the original (reinforced) and novel (non-reinforced) stimuli, which indicates that stingrays could distinguish between the intensity and inclination angle of a magnetic field. This experiment is the first to show that a batoid (skate or ray) can detect and distinguish between changes in GMF intensity and inclination angle, and supports the idea that elasmobranchs might use GMF cues to form a magnetically based cognitive map and derive a sense of location.
... Laboratory studies conducting "magnetic displacement" studies revealed that salmon can rely on a magnetic map for their oceanic migration (e.g. Minkoff et al., 2020;Putman et al., 2020;Putman et al., 2014a,b) and that even non-anadromous populations of Atlantic salmon have such a mechanism, indicating that the trait may be ancestral and therefore common among various salmonids (Scanlan et al., 2018). Sensitivity to the Earth's magnetic field has also been investigated in the ocean. ...
... Salmonids of the genus Oncorhynchus have also been common subjects of magnetoreception studies owing to their intrinsic natal homing [6]. Pink salmon (Oncorhynchus gorbuscha) have demonstrated magnetoreceptive abilities that are essential for them to migrate around the Pacific and back to their native rivers to spawn [7]. Although some studies indicate that salmonids may use magnetite-iron-containing crystals-to sense the Earth's magnetic field [8], this theory remains open for debate [9][10][11]. ...
Article
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Magnetoreceptive biology as a field remains relatively obscure; compared with the breadth of species believed to sense magnetic fields, it remains under-studied. Here, we present grounds for the expansion of magnetoreception studies among teleosts. We begin with the electromagnetic perceptive gene (EPG) from Kryptopterus vitreolus and expand to identify 72 teleosts with homologous proteins containing a conserved three-phenylalanine (3F) motif. Phylogenetic analysis provides insight as to how EPG may have evolved over time and indicates that certain clades may have experienced a loss of function driven by different fitness pressures. One potential factor is water type with freshwater fish significantly more likely to possess the functional motif version (FFF), and saltwater fish to have the non-functional variant (FXF). It was also revealed that when the 3F motif from the homologue of Brachyhypopomus gauderio (B.g.) is inserted into EPG—EPG(B.g.)—the response (as indicated by increased intracellular calcium) is faster. This indicates that EPG has the potential to be engineered to improve upon its response and increase its utility to be used as a controller for specific outcomes.
... Salmonids of the genus Oncorhynchus have also been common subjects of magnetoreception studies due to their intrinsic natal homing (6). Pink salmon (Oncorhynchus gorbuscha) have demonstrated magnetoreceptive abilities that are essential for them to migrate around the Pacific and back to their native rivers to spawn (7). Although some studies indicate that salmonids may use magnetite -iron containing crystals -to sense the Earth's magnetic field (8), this theory remains open for debate (9)(10)(11). ...
Preprint
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Magnetoreceptive biology as a field remains relatively obscure; compared to the breadth of species believed to sense magnetic fields, it remains under-studied. Here, we present grounds for the expansion of magnetoreception studies among Teleosts. We begin with the electromagnetic perceptive gene (EPG) from Kryptopterus vitreolus and expand to identify 72 Teleosts with homologous proteins containing a conserved three-phenylalanine (3F) motif. Phylogenetic analysis provides insight as to how EPG may have evolved over time, and indicates that certain clades may have experienced a loss of function driven by different fitness pressures. One potential factor is water type with freshwater fish significantly more likely to possess the functional motif version (FFF), and saltwater fish to have the non-functional variant (FXF). It was also revealed that when the 3F motif from the homolog of Brachyhypopomus gauderio (B.g.) is inserted into EPG – EPG(B.g.) – the response (as indicated by increased intracellular calcium) is faster. This indicates that EPG has the potential to be engineered to improve upon its response and increase its utility to be used as a controller for specific outcomes.
... The model could also be applied to studying the specific migratory patterns of various taxa, such as fish (Putman et al 2014b(Putman et al , 2020 and birds (Kishkinev et al 2015, Mouritsen et al 2016. Complex, multi-leg journeys could be facilitated in the model by chaining together a sequence of magnetic signature goals, where the agent switches to the next goal once it senses it has arrived at its current goal (Taylor et al 2021, McLaren et al 2023. ...
Article
Full-text available
Certain animal species use the Earth’s magnetic field (i.e. magnetoreception) alongside their other sensory modalities to navigate long distances that include continents and oceans. It is hypothesized that several animals use geomagnetic parameters, such as field intensity and inclination, to recognize specific locations or regions, potentially enabling migration without a pre-surveyed map. However, it is unknown how animals use geomagnetic information to generate guidance commands, or where in the world this type of strategy would maximize an animal’s fitness. While animal experiments have been invaluable in advancing this area, the phenomenon is difficult to study in vivo or in situ, especially on the global scale where the spatial layout of the geomagnetic field is not constant. Alongside empirical animal experiments, mathematical modeling and simulation are complementary tools that can be used to investigate animal navigation on a global scale, providing insights that can be informative across a number of species. In this study, we present a model in which a simulated animal (i.e. agent) navigates via an algorithm which determines travel heading based on local and goal magnetic signatures (here, combinations of geomagnetic intensity and inclination) in a realistic model of Earth’s magnetic field. By varying parameters of the navigation algorithm, different regions of the world can be made more or less reliable to navigate. We present a mathematical analysis of the system. Our results show that certain regions can be navigated effectively using this strategy when these parameters are properly tuned, while other regions may require more complex navigational strategies. In a real animal, parameters such as these could be tuned by evolution for successful navigation in the animal’s natural range. These results could also help with developing engineered navigation systems that are less reliant on satellite-based methods.
... A range of animals (migratory, non-migratory, terrestrial, aquatic) uses the earth's magnetic field to orient and navigate (Lohmann 2010). For instance, brown planthoppers (Nilaparvata lugens), spiny lobsters (Panulirus argus), pink salmon (Oncorhynchus gorbuscha) and yellow stingrays (Urobatis jamaicensis) all migrate using the earth's magnetic field (Boles and Lohmann 2003;Ernst and Lohmann 2016;Newton and Kajiura 2017;Putman et al. 2020;Zhang and Pan 2021). Sea turtles also have magnetoreception, which they use for navigation (Lohmann et al. 2012). ...
Article
Full-text available
Context Sea turtle hatchlings generally emerge at night from nests on sand beaches and immediately orient using visual cues, which are believed to entail the difference in brightness between the light seen in the seaward direction and that seen in the duneward direction. Aim The aim of this study was to understand how dune proximity affected hatchling orientations in two sea turtle species that share a nesting beach 15 km long and 25.3 ± 9.4 m (N = 215) from dune to waterline, with low to moderate artificial light nearby. Methods For hatchling loggerhead and green turtles, we measured accuracy and precision of orientation, tested differences in distance from nest to dune, and investigated the effect of dune proximity on hatchling orientation. Key results We found a significant decrease in hatchling orientation accuracy and precision in both species as the distance increased from nests to dune. Loggerhead and green turtles showed similar orientation ability when in the same proximity to the dune. Conclusions We conclude that dune features provide important cues for hatchling orientation on sea turtle nesting beaches. Implications Restoring and maintaining natural beach profiles, especially dune systems, is likely to increase the accuracy and precision of sea finding in hatchling sea turtles.
... In every waterbody except for the Laurentian Great Lakes (Kennedy et al., 2005), pink salmon return to coasts after about 12-14 months in the ocean to migrate into rivers and spawn. Like other salmonids, pink salmon have a magnetic map that they can use to orient from the ocean towards home rivers (Putman et al., 2020). Pink salmon have mainly entered Norwegian rivers from late June to mid-August, and Sandlund et al. (2019) and ...
Article
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While populations of other migratory salmonids suffer in the Anthropocene, pink salmon ( Oncorhynchus gorbusca Salmonidae) are thriving, and their distribution is expanding both within their natural range and in the Atlantic and Arctic following introduction of the species to the White Sea in the 1950s. Pink salmon are now rapidly spreading in Europe and even across the ocean to North America. Large numbers of pink salmon breed in Norwegian rivers and small numbers of individuals have been captured throughout the North Atlantic since 2017. Although little is known about the biology and ecology of the pink salmon in its novel distribution, the impacts of the species' introduction are potentially highly significant for native species and watershed productivity. Contrasts between pink salmon in the native and extended ranges will be key to navigating management strategies for Atlantic nations where the pink salmon is entrenching itself among the fish fauna, posing potential threats to native fish communities. One key conclusion of this paper is that the species' heritable traits are rapidly selected and drive local adaptation and evolution. Within the Atlantic region, this may facilitate further establishment and spread. The invasion of pink salmon in the Atlantic basin is ultimately a massive ecological experiment and one of the first examples of a major faunal change in the North Atlantic Ocean that is already undergoing rapid changes due to other anthropogenic stressors. New research is urgently needed to understand the role and potential future impacts of pink salmon in Atlantic ecosystems.
... To test for corrective behaviour, we conducted displacement experiments. Several studies were performed in which juvenile marine animals were displaced virtually by changing magnetic field conditions that simulated locations along their potential migration route [22][23][24][25][26][27] . In contrast, physical displacement of marine animals has been performed in the past only with adult animals, which could have already explored their spatial environment prior to displacement, similar to homing pigeons. ...
Article
Full-text available
Millions of minute, newly hatched coral reef fish larvae get carried into the open ocean by highly complex and variable currents. To survive, they must return to a suitable reef habitat within a species-specific time. Strikingly, previous studies have demonstrated that return to home reefs is much more frequent than would be expected by chance. It has been shown that magnetic and sun compass orientation can help cardinalfish maintain their innate swimming direction but do they also have a navigational map to cope with unexpected displacements? If displaced settling-stage cardinalfish Ostorhinchus doederleini use positional information during their pelagic dispersal, we would expect them to re-orient toward their home reef. However, after physical displacement by 180 km, the fish showed a swimming direction indistinguishable from original directions near the capture site. This suggests that the tested fish rely on innate or learned compass directions and show no evidence for map-based navigation.
... Diadrome fish, like salmonids, eels and sturgeons, use (among other environmental cues) the Earth's magnetic field to successfully migrate between spawning and feeding grounds [lit. 43]. As such, these species can sense small differences in magnetic field strengths, suggesting they could be affected by anthropogenic EMF. ...
Technical Report
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Technical report including a literature survey and modelling exercise of electromagnetic field levels of the Dutch Continental Shelf in relation to the Marine Strategy Framework Directive, descriptor 11 - Energy.
... The sun compass could be used collectively with other compass senses or be part of a cue cascade where one cue comes more into play if a higher ranked one is less available. Magnetic compass orientation would be plausible as this cue is omnipresent and has been demonstrated in a variety of fish species (Bottesch et al., 2016;Cresci et al., 2017;Putman et al., 2020). Whether herring can indeed use additional orientation mechanisms still needs to be determined. ...
Article
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Atlantic herring (Clupea harengus), an ecologically and economically important species in the Northern Hemisphere, shows pronounced seasonal migratory behaviour. To follow distinctive migration patterns over hundreds of kilometers between feeding, overwintering, and spawning grounds, they are probably guided by orientation mechanisms. We tested whether juvenile Western Baltic Spring-Spawning Herring use a sun compass for orientation just before they start leaving their hatching area. Fish were randomly divided into two groups, one of them clock-shifted 6 h backwards, to investigate if they shift their orientation direction accordingly. Individual fish were placed in a circular bowl and their orientation was tested multiple times with the sun as a sole visual orientational cue. Our results show for the first time that juvenile Atlantic herring use a time-compensated sun compass during their migration. Their swimming direction was impaired, but still present, even when the sky was very cloudy, indicating additional orientation capabilities.
... The orientation of pink salmon tested in the northern and southern magnetic fields differed significantly, indicating that they distinguished between the two magnetic fields and responded by swimming in different directions. Triangles represent the mean heading of individuals and the central arrow and gray shading shows the population-level mean direction and 95% CI, respectively (modified from Putman et al. 2020) et al. 2013). For salmon, geomagnetic imprinting might occur in parallel with olfactory imprinting (Lohmann et al. 2008b); thus, magnetic cues might bring fish back into the general area of a river mouth, close enough for chemical cues to guide fish to the final destination. ...
Article
Full-text available
As the largest and most diverse vertebrate group on the planet, fishes have evolved an impressive array of sensory abilities to overcome the challenges associated with navigating the aquatic realm. Among these, the ability to detect Earth’s magnetic field, or magnetoreception, is phylogenetically widespread and used by fish to guide movements over a wide range of spatial scales ranging from local movements to transoceanic migrations. A proliferation of recent studies, particularly in salmonids, has revealed that fish can exploit Earth’s magnetic field not only as a source of directional information for maintaining consistent headings, but also as a kind of map for determining location at sea and for returning to natal areas. Despite significant advances, much about magnetoreception in fishes remains enigmatic. How fish detect magnetic fields remains unknown and our understanding of the evolutionary origins of vertebrate magnetoreception would benefit greatly from studies that include a wider array of fish taxa. The rich diversity of life-history characteristics that fishes exhibit, the wide variety of environments they inhabit, and their suitability for manipulative studies, make fishes promising subjects for magnetoreception studies.
... This suggests that the largescale 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 (Putman et al. 2020). The initiation of the downstream migration of juveniles induces the expression of the brain-pituitary-thyroid (BPT) hormones, which then induce the upregulation of the NMDA receptor, inducing imprinting long-term potentiation (LTP), which enhances olfactory memory formation related to natal stream-specific odors. ...
Article
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Pacific salmon are recognized for their amazing abilities to memorize their natal river information during a short-distance downstream migration, carry out a long-distance feeding migration in the ocean for many years for growth, and make a precise long-distance spawning migration from oceanic feeding habitat to their natal river for reproduction. Two different sensory mechanisms, olfaction and magnetoreception, are involved in the imprinting and homing processes in Pacific salmon. It is considered that olfactory imprinting occurs from the spawning ground to the mouth of natal river, and olfactory homing occurs from the vicinity of the river mouth to the spawning ground of natal river (Ueda 2019, 2020); Geomagnetic imprinting is thought to occur as juveniles depart the mouth of natal river to oceanic nursery habitat, and geomagnetic homing occurs from the oceanic feeding habitat back to the mouth of natal river (Putman 2018, 2021) (Fig1). This report presents current findings on olfactory and geomagnetic imprinting and homing in Pacific salmon, and proposes international collaborative research project to test olfactory and geomagnetic imprinting and homing in Pacific salmon across the Pacific Ocean.
... Lohmann et al. 2004), but also fishes (salmon: e.g. Putman et al. 2020;Quinn 1980) and arthropods (lobster: Boles and Lohmann 2003;bogong moth: Dreyer et al. 2018; monarch butterfly: Guerra et al. 2014). However, the GMF may also be a useful cue for close-range orientation (Wyeth 2010). ...
Article
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At the beginning of their foraging careers, Cataglyphis desert ants calibrate their compass systems and learn the visual panorama surrounding the nest entrance. For that, they perform well-structured initial learning walks. During rotational body movements (pirouettes), naïve ants (novices) gaze back to the nest entrance to memorize their way back to the nest. To align their gaze directions, they rely on the geomagnetic field as a compass cue. In contrast, experienced ants (foragers) use celestial compass cues for path integration during food search. If the panorama at the nest entrance is changed, foragers perform re-learning walks prior to heading out on new foraging excursions. Here, we show that initial learning walks and re-learning walks are structurally different. During re-learning walks, foragers circle around the nest entrance before leaving the nest area to search for food. During pirouettes, they do not gaze back to the nest entrance. In addition, foragers do not use the magnetic field as a compass cue to align their gaze directions during re-learning walk pirouettes. Nevertheless, magnetic alterations during re-learning walks under manipulated panoramic conditions induce changes in nest-directed views indicating that foragers are still magnetosensitive in a cue conflict situation.
... Many aspects of the ocean environment conditions are spatial and temporally variable. However, some key aspects will have been relatively temporally and spatially stable over evolutionary time frames, of hundreds to thousands of generations, and provide a basis for adaptive evolution of migratory behaviour, facilitated by, for example, magnetoreception (Naisbett-Jones et al., 2020;Putman et al., 2020) to target optimal marine habitat areas for migration and feeding. Furthermore, where such habitats occur in multiple areas, the potential exists for different phylogeographic groups to have different migratory pathways and destinations. ...
Article
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The survival of Atlantic salmon (Salmo salar), an increasingly rare anadromous species, has declined dramatically during its marine phase, with disproportionate impacts on the poorly understood early post‐smolt period. Logistical constraints on collecting oceanic data to inform this issue pose a formidable obstacle. To advance understanding of post‐smolt distributional ecology in the North‐east Atlantic, a comprehensive analysis of existing information was undertaken. Data were synthesized from 385 marine cruises, 10,202 individual trawls, and 9,269 captured post‐smolts, spanning three decades and ~4.75 million km2 of ocean, with 3,423 individuals genetically assigned to regional phylogeographic origin. The findings confirm major migrational post‐smolt aggregations on the continental shelf‐edge off Ireland, Scotland and Norway, and an important marine foraging area in the Norwegian Sea. Genetic analysis shows that aggregational stock composition does not simply reflect distance to natal rivers, with northern phylogeographic stock groups significantly under‐represented in sampled high‐seas aggregations. It identifies a key foraging habitat for southern European post‐smolts located in international waters immediately west of the Vøring Plateau escarpment, potentially exposing them to a high by‐catch mortality from extra‐territorial pelagic fisheries. Evidence of the differential distribution of regional stocks points to fundamental differences in their migration behaviours and may lead to inter‐stock variation in responses to environmental change and marine survival. The study shows that understanding of post‐smolt marine ecology, as regards to stock‐specific variations in habitat utilization, biological performance and exposure to mortality factors, can be significantly advanced by data integration across studies and exploiting genetic approaches.
... In contrast, the utility of a magnetic map depends, at least to some degree, on distance. Magnetic maps have been shown to play an important role in long-distance movements (>75-100 km; e.g. by salmon, sea turtles, migratory birds and spiny lobsters; Chernetsov et al., 2017;Freake et al., 2006;Heyers et al., 2017;Kishkinev et al., 2015;Lohmann, 2007;Lohmann and Lohmann, 2006;Lohmann et al., 2007;Munro et al., 1997;Putman et al., 2020;Scanlan et al., 2018). Over distances of ∼10-50 km (at least in terrestrial environments), however, local irregularities in the MF caused by iron-containing minerals in the Earth's crust may make spatial variation in the MF an unreliable indicator of geographic position (Courtillotl et al., 1997;Lednor, 1982;Phillips, 1996;Vargas et al., 2006). ...
Article
Newts can use spatial variation in the magnetic field (MF) to derive geographic position, but it is unclear how they detect the ‘spatial signal’, which, over the distances that newts move in a day, is an order of magnitude lower than temporal variation in the MF. Previous work has shown that newts take map readings using their light-dependent magnetic compass to align a magnetite-based ‘map detector’ relative to the MF. In this study, time of day, location and light exposure (required by the magnetic compass) were varied to determine when newts obtain map information. Newts were displaced from breeding ponds without access to route-based cues to sites where they were held and/or tested under diffuse natural illumination. We found that: (1) newts held overnight at the testing site exhibited accurate homing orientation, but not if transported to the testing site on the day of testing; (2) newts held overnight under diffuse lighting at a ‘false testing site’ and then tested at a site located in a different direction from their home pond oriented in the home direction from the holding site, not from the site where they were tested; and (3) newts held overnight in total darkness (except for light exposure for specific periods) only exhibited homing orientation the following day if exposed to diffuse illumination during the preceding evening twilight in the ambient MF. These findings demonstrate that, to determine the home direction, newts require access to light and the ambient MF during evening twilight when temporal variation in the MF is minimal.
... In research into the biological effects of EMF, it has been known since the 1960s that many species are sensitive to low-level energy exposures. Numerous laboratory and field studies have noted heightened sensitivity and adverse effects in birds [15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32]; mammals (cows and bats [33][34][35][36][37][38]); insects [39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54] bacteria/protozoa [55][56][57][58][59][60][61]; amphibians [62][63][64][65][66][67]; fish and turtles [68][69][70][71][72][73][74][75][76][77][78][79][80][81][82]; and in trees and plants [83][84][85], among many others. ...
Article
Ambient levels of electromagnetic fields (EMF) have risen sharply in the last 80 years, creating a novel energetic exposure that previously did not exist. Most recent decades have seen exponential increases in nearly all environments, including rural/remote areas and lower atmospheric regions. Because of unique physiologies, some species of flora and fauna are sensitive to exogenous EMF in ways that may surpass human reactivity. There is limited, but comprehensive, baseline data in the U.S. from the 1980s against which to compare significant new surveys from different countries. This now provides broader and more precise data on potential transient and chronic exposures to wildlife and habitats. Biological effects have been seen broadly across all taxa and frequencies at vanishingly low intensities comparable to today’s ambient exposures. Broad wildlife effects have been seen on orientation and migration, food finding, reproduction, mating, nest and den building, territorial maintenance and defense, and longevity and survivorship. Cyto- and geno-toxic effects have been observed. The above issues are explored in three consecutive parts: Part 1 questions today’s ambient EMF capabilities to adversely affect wildlife, with more urgency regarding 5G technologies. Part 2 explores natural and man-made fields, animal magnetoreception mechanisms, and pertinent studies to all wildlife kingdoms. Part 3 examines current exposure standards, applicable laws, and future directions. It is time to recognize ambient EMF as a novel form of pollution and develop rules at regulatory agencies that designate air as ‘habitat’ so EMF can be regulated like other pollutants. Wildlife loss is often unseen and undocumented until tipping points are reached. Long-term chronic low-level EMF exposure standards, which do not now exist, should be set accordingly for wildlife, and environmental laws should be strictly enforced.
... Species like loggerhead sea turtles (Caretta caretta), European eel (Anguilla anguilla), and pink salmon (O. gorbuscha) will adopt headings that, had the animals been at the geographic location of the magnetic field, would guide them along their typical migratory route (Lohmann, Putman, & Lohmann, 2012;Naisbett-Jones, Putman, Stephenson, Ladak, & Young, 2017;Putman, Williams, Gallagher, & Dittman, 2020). The findings from these studies show that (a) specific components of the magnetic field are perceptible to animals, (b) demonstrate that this information is used for orientation, and (c) provide ecological context for the sensory ability (Putman, Ueda, & Noakes, 2019). ...
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The number of subsea cables in the marine environment is likely to grow substantially in the near future. Arrays of energy‐generating windmills or wave power generators are planned for installation in the coastal waters of many countries worldwide. The electricity generated by these and other marine energy sources will be transported to shore through cables with the current and voltage creating electromagnetic fields (EMFs). Furthermore, there are also plans for the installation of undersea cables to interconnect countries and islands for the purpose of sharing power and communications. These also will generate EMFs in the marine environment. While shielding can negate the presence of direct electric fields, induced electric and magnetic fields readily penetrate into the water column. Cables carrying electric current produce anomalies in the earth's main field, which could have the potential for disrupting the migrations of fishes and diverse marine animals that rely on magnetic cues for orientation or navigation. Studies designed to test how these anthropogenic magnetic fields disrupt magnetic orientation have only recently started to be conducted. Given the cultural, economic, and conservation value of many of the species potentially at risk, such work should be immediately prioritized.
... [26][27][28][29] Along with studies on true navigation using geomagnetic cues, the method has been used successfully to reveal the innate signpost mechanisms used by hatchling sea turtles, eels, and salmonids. 26,27,[30][31][32][33] The results of virtual magnetic displacement experiments with reed warblers suggest that they can respond to such treatments as if they had been physically displaced to the respective magnetically simulated unfamiliar locations, despite the fact that they are physically located at the site of their capture, which suggests true navigation ability. 28,29,[34][35][36] However, in these previous studies, reed warblers were presented with inclination, declination, and intensity values they could have experienced during their year-round movements, even if not in the specific combinations used in the experiments ( Figure S1) 28,29,35 and so do not necessarily support the use of a map extrapolated to unfamiliar values of the magnetic field. ...
Article
Displacement experiments have demonstrated that experienced migratory birds translocated thousands of kilometers away from their migratory corridor can orient toward and ultimately reach their intended destinations. This implies that they are capable of ‘‘true navigation,’’ commonly defined as the ability to return to a known destination after displacement to an unknown location without relying on familiar surroundings, cues that emanate from the destination, or information collected during the outward journey. In birds, true navigation appears to require previous migratory experience (but see Kishkinev et al. and Piersma et al.). It is generally assumed that, to correct for displacements outside the familiar area, birds initially gather information within their year-round distribution range, learn predictable spatial gradients of environmental cues within it, and extrapolate from those to unfamiliar magnitudes—the gradient hypothesis. However, the nature of the cues and evidence for actual extrapolation remain elusive. Geomagnetic cues (inclination, declination, and total intensity) provide predictable spatial gradients across large parts of the globe and could serve for navigation. We tested the orientation of long-distance migrants, Eurasian reed warblers, exposing them to geomagnetic cues of unfamiliar magnitude encountered beyond their natural distribution range. The birds demonstrated re-orientation toward their migratory corridor as if they were translocated to the corresponding location but only when all naturally occurring magnetic cues were presented, not when declination was changed alone. This result represents direct evidence for migratory birds’ ability to navigate using geomagnetic cues extrapolated beyond their previous experience.
... This study, drawing on data taken over the past 80 years, provides information on the ecological implications of magnetic navigation not possible using other approaches. What's more, the underlying assumptions and predictions of this work can be directly tested with techniques like magnetic displacement experiments (in which magnetic fields are precisely manipulated around the entire body of the animal and with the aim of inducing predictable, oriented movement that differs between two or more magnetic fields) [2,18]. The present findings with seabirds [6] combined with recent physical displacement experiments in common cuckoos (Cuculus canorus) [19] suggest that the navigational strategies and tools used by birds might be more similar to those of marine migrants than previously appreciated. ...
Article
Shifts in the return locations of juvenile seabirds migrating from the Irish Sea to Argentina can be accurately predicted by changes in Earth’s magnetic field, suggesting that these birds rely on a geomagnetic map for navigation.
... Swimming behavior in small-bodied marine animals appears to be relatively consistent through time and function to move animals toward regions of the ocean that are typically favorable (Putman et al., 2012aPutman, 2015Putman, , 2018Naisbett-Jones et al., 2017). Thus, ocean dynamics are likely to be the primary source of variability in the movements in these animals and, indeed, can account for much of the spatial and temporal variability in the distributions of many species (Putman and Naro-Maciel, 2013;Baltazar-Soares et al., 2014;Hays, 2017;Putman et al., 2020). While it is likely that the relative seasonal, annual, and site differences detected in our model are representative of actual conditions, the magnitude of these differences might differ substantially (e.g., dispersal distance from Rancho Nuevo would likely always exceed dispersal distances from Padre Island, but by how much will depend upon aspects of swimming behavior that we do not have information to parameterize) (Putman et al., 2012a,b). ...
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Environmental variability can be an important factor in the population dynamics of many species. In marine systems, for instance, whether environmental conditions facilitate or impede the movements of juvenile animals to nursery habitat can have a large influence on subsequent population abundance. Both subtle differences in the position of oceanographic features (such as meandering currents) and major disturbances (such as hurricanes) can greatly alter dispersal outcomes. Here, we use an ocean circulation model to explore seasonal and annual variation in the dispersal of post-hatchling Kemp’s ridley sea turtles (Lepidochelys kempii). We simulated the transport of 24 cohorts of young-of-the-year Kemp’s ridley sea turtles dispersing from the three primary nesting areas in the western Gulf of Mexico to describe variability in transport during the main hatching season and across years. We examined whether differences in transport distance among Kemp’s ridley cohorts could be explained by hurricane events. We found that years with high numbers of hurricanes corresponded to shorter dispersal distances and less variance within the first 6 months. Our findings suggest that differences in dispersal among sites and the impact of hurricane frequency and intensity could influence the survivorship and somatic growth rates of turtles from different nesting sites and hatching cohorts, either improving survival by encouraging retention in optimal pelagic habitat or decreasing survival by pushing hatchlings into dangerous shallow habitats. Considering such factors in future population assessments may aid in predicting how the potential for increasing tropical storms, a phenomenon linked to climate change, could affect Kemp’s ridley and other populations of sea turtles in the Atlantic Ocean.
... In the present study, salmon subjected to a pulse did not differ in orientation from control fish when tested in the local magnetic field, but did differ significantly when tested in the magnetic field of a location near the southern periphery of their range (Fig. 4C,D). Interestingly, salmon are known to possess both a magnetic 'compass' that enables them to use Earth's magnetic field as a directional cue (Quinn, 1980) and a magnetic 'map' that allows them, in effect, to assess their position within an ocean basin (Putman et al., 2014a(Putman et al., , 2020Putman, 2015;Scanlan et al., 2018). In principle, the mechanism underlying the compass, the map or both might have been affected by the magnetic pulse. ...
Article
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.
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Empirical evidence suggests that marine animals perceive and orient to local distortions in the earth’s natural magnetic field. Magnetic fields (MFs) generated by electrified underwater cables may produce similar local distortions in the earth’s main field. Concern exists that these distortions may impact migration movements of MF-sensitive animals. The Trans Bay Cable (TBC) is a ± 200-kV, 400-megawatt, 85-km high-voltage direct current transmission line buried through San Francisco Bay (37° 56′ 8.81″ N, 122° 27′ 0.19″ W). Detections of adult green sturgeon implanted with acoustic transmitters were used from six cross-bay receiver arrays from 2006 to 2015 to investigate how inbound and outbound migration movements through lower portions of their route to/from upstream breeding grounds are related to the TBC’s energization status (off/on) and other local environmental variables. Here, we assess how these variables impacted transit success, misdirection from the migration route, transit times, and migration path locations within stretches between the Bay’s mouth and the start of the Sacramento River. Overall, there was varied evidence for any effect on migration behavior associated with cable status (off/on). A higher percentage of inbound fish successfully transited after the cable was energized, but this effect was nonsignificant in models including temperature. Outbound fish took longer to transit after cable energization. Inbound and outbound migration path locations were not significantly influenced by cable energization, but results suggest a potential subtle relationship between energization and both inbound and outbound paths. Overall, additional migration-based studies are needed to investigate the impact of anthropogenic cables on marine species.
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Virtual magnetic displacements are used to examine the magnetoreceptive ability of animals by changing the local magnetic field to emulate one that exists elsewhere. This technique can be used to test whether animals use a magnetic map. The viability of a magnetic map is dependant upon which magnetic parameters an animal’s coordinate system is composed of, and how sensitive they are to those parameters. Previous research has not considered the degree to which sensitivity can change an animal’s impression of where a virtual magnetic displacement is located. We re-assessed all published studies that use virtual magnetic displacements assuming the highest likely level of sensitivity to magnetic parameters in animals. The vast majority are susceptible to the existence of alternate possible virtual locations. In some cases, this can cause results to become ambiguous. We present a tool for visualising all possible virtual magnetic displacement alternative locations (ViMDAL) and propose changes to how further research on animal magnetoreception is conducted and reported.
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There is enough evidence to indicate we may be damaging non-human species at ecosystem and biosphere levels across all taxa from rising background levels of anthropogenic non-ionizing electromagnetic fields (EMF) from 0 Hz to 300 GHz. The focus of this Perspective paper is on the unique physiology of non-human species, their extraordinary sensitivity to both natural and anthropogenic EMF, and the likelihood that artificial EMF in the static, extremely low frequency (ELF) and radiofrequency (RF) ranges of the non-ionizing electromagnetic spectrum are capable at very low intensities of adversely affecting both fauna and flora in all species studied. Any existing exposure standards are for humans only; wildlife is unprotected, including within the safety margins of existing guidelines, which are inappropriate for trans-species sensitivities and different non-human physiology. Mechanistic, genotoxic, and potential ecosystem effects are discussed.
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The magnetic field of the Earth provides animals with various kinds of information. Its use as a compass was discovered in the mid-1960s in birds, when it was first met with considerable skepticism, because it initially proved difficult to obtain evidence for magnetic sensitivity by conditioning experiments. Meanwhile, a magnetic compass was found to be widespread. It has now been demonstrated in members of all vertebrate classes, in mollusks and several arthropod species, in crustaceans as well as in insects. The use of the geomagnetic field as a ‘map’ for determining position, although already considered in the nineteenth century, was demonstrated by magnetically simulating displacements only after 2000, namely when animals, tested in the magnetic field of a distant site, responded as if they were physically displaced to that site and compensated for the displacement. Another use of the magnetic field is that as a ‘sign post’ or trigger: specific magnetic conditions elicit spontaneous responses that are helpful when animals reach the regions where these magnetic characteristics occur. Altogether, the geomagnetic field is a widely used valuable source of navigational information for mobile animals.
Article
Ambient levels of nonionizing electromagnetic fields (EMF) have risen sharply in the last five decades to become a ubiquitous, continuous, biologically active environmental pollutant, even in rural and remote areas. Many species of flora and fauna, because of unique physiologies and habitats, are sensitive to exogenous EMF in ways that surpass human reactivity. This can lead to complex endogenous reactions that are highly variable, largely unseen, and a possible contributing factor in species extinctions, sometimes localized. Non-human magnetoreception mechanisms are explored. Numerous studies across all frequencies and taxa indicate that current low-level anthropogenic EMF can have myriad adverse and synergistic effects, including on orientation and migration, food finding, reproduction, mating, nest and den building, territorial maintenance and defense, and on vitality, longevity and survivorship itself. Effects have been observed in mammals such as bats, cervids, cetaceans, and pinnipeds among others, and on birds, insects, amphibians, reptiles, microbes and many species of flora. Cyto- and geno-toxic effects have long been observed in laboratory research on animal models that can be extrapolated to wildlife. Unusual multi-system mechanisms can come into play with non-human species — including in aquatic environments — that rely on the Earth’s natural geomagnetic fields for critical life-sustaining information. Part 2 of this 3-part series includes four online supplement tables of effects seen in animals from both ELF and RFR at vanishingly low intensities. Taken as a whole, this indicates enough information to raise concerns about ambient exposures to nonionizing radiation at ecosystem levels. Wildlife loss is often unseen and undocumented until tipping points are reached. It is time to recognize ambient EMF as a novel form of pollution and develop rules at regulatory agencies that designate air as ‘habitat’ so EMF can be regulated like other pollutants. Long-term chronic low-level EMF exposure standards, which do not now exist, should be set accordingly for wildlife, and environmental laws should be strictly enforced — a subject explored in Part 3.
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Diverse taxa use Earth’s magnetic field in conjunction with other sensory modalities to accomplish navigation tasks ranging from local homing to long-distance migration across continents and ocean basins. However, despite extensive research, the mechanisms that underlie animal magnetoreception are not clearly understood, and how animals use Earth’s magnetic field to navigate is an active area of investigation. Concurrently, Earth’s magnetic field offers a signal that engineered systems can leverage for navigation in environments where man-made systems such as GPS are unavailable or unreliable. Using a proxy for Earth’s magnetic field, and inspired by migratory animal behavior, this work implements a behavioral strategy that uses combinations of magnetic field inclination and intensity as rare or unique signatures that mark specific locations. Specifically, to increase the realism of previous work, in this study, a simulated agent uses a magnetic signatures based strategy to migrate in magnetic environments where lines of constant inclination and intensity are not necessarily orthogonal. The results further support existing notions that some animals may use combinations of magnetic properties as navigational markers, and provide insights into features and constraints that could enable navigational success or failure in either a biological or engineered system.
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Diverse marine animals migrate across vast expanses of seemingly featureless ocean before returning as adults to reproduce in the area where they originated. How animals accomplish such feats of natal homing is an enduring mystery. Growing evidence suggests, however, that sea turtles and salmon imprint on the magnetic field of their home area when young and then use this information to return as adults. Both turtles and salmon have the sensory abilities needed to detect the unique 'magnetic signature' of a coastal area. Analyses have revealed that, for both groups of animals, subtle changes in the geomagnetic field of the home region are correlated with changes in natal homing behavior. In turtles, a relationship between population genetic structure and the magnetic fields that exist at nesting beaches has also been detected, consistent with the hypothesis that turtles recognize their natal areas on the basis of magnetic cues. Salmon likely use a biphasic navigational strategy in which magnetic cues guide fish through the open sea and into the proximity of the home river where chemical cues allow completion of the spawning migration. Similarly, turtles may also exploit local cues to help pinpoint nesting areas once they have arrived in the vicinity. Throughout most of the natal homing migration, however, magnetic navigation appears to be the primary mode of long-distance guidance in both sea turtles and salmon.
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Recently, virtual magnetic displacement experiments have shown that magnetic cues are indeed important for determining position in migratory birds; but which sensory system(s) do they use to detect the magnetic map cues? Here, we show that Eurasian reed warblers need trigeminal input to detect that they have been virtually magnetically displaced. Birds with bilaterally ablated ophthalmic branches of the trigeminal nerves were not able to re-orient towards their conspecific breeding grounds after a virtual magnetic displacement, exactly like they were not able to compensate for a real physical displacement. In contrast, sham-operated reed warblers re-oriented after the virtual displacement, like intact controls did in the past. Our results show that trigeminally mediated sensory information is necessary for the correct function of the reed warblers' magnetic positioning system.
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European eels (Anguilla anguilla) migrate between the southwestern Sargasso Sea and the European and Mediterranean coasts. In a recent paper in Current Biology, Naisbett-Jones et al. [1] claim to “provide the first evidence that they [eels] derive positional information from the Earth's magnetic field” and that this information guides their migration. The evidence reported by Naisbett-Jones et al. [1] in support of this conclusion was derived from eels collected in the Severn River (UK), approximately 50 km upstream of the estuary (i.e. not “in the Severn Estuary” as stated by the authors). Eels collected this far into rivers are benthic and fully adapted to freshwater; that is, they are late-stage glass eels (∼ 2 years old), not the pelagic leptocephalus (larval) life stage that actually undertakes the trans-Atlantic migration. The entire interpretive framework for the Naisbett-Jones et al. [1] study rests on the assumption that the behaviour of these late-stage freshwater glass eels, and their responses to magnetic fields, can be used as a proxy for the responses of eel leptocephali. The authors present no evidence in support of this key assumption. Durif et al. take issue with a recent Current Biology study on eel migration.
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Migration allows animals to track the environmental conditions that maximize growth, survival, and reproduction [1–3]. Improved understanding of the mechanisms underlying migrations allows for improved management of species and ecosystems [1–4]. For centuries, the catadromous European eel (Anguilla anguilla) has provided one of Europe’s most important fisheries and has sparked considerable scientific inquiry, most recently owing to the dramatic collapse of juvenile recruitment [5]. Larval eels are transported by ocean currents associated with the Gulf Stream System from Sargasso Sea breeding grounds to coastal and freshwater habitats from North Africa to Scandinavia [6, 7]. After a decade or more, maturing adults migrate back to the Sargasso Sea, spawn, and die [8]. However, the migratory mechanisms that bring juvenile eels to Europe and return adults to the Sargasso Sea remain equivocal [9, 10]. Here, we used a ‘‘magnetic displacement’’ experiment [11, 12] to show that the orientation of juvenile eels varies in response to subtle differences in magnetic field intensity and inclination angle along their marine migration route. Simulations using an ocean circulation model revealed that even weakly swimming in the experimentally observed directions at the locations corresponding to the magnetic displacements would increase entrainment of juvenile eels into the Gulf Stream System. These findings provide new insight into the migration ecology and recruitment dynamics of eels and suggest that an adaptive magnetic map, tuned to large-scale features of ocean circulation, facilitates the vast oceanic migrations of the Anguilla genus [7, 13, 14].
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Ocean currents or temperature may substantially influence migration behavior in many marine species. However, high-resolution data on animal movement in the marine environment are scarce; therefore, analysts and managers must typically rely on unvalidated assumptions regarding movement, behavior, and habitat use. We used a spatially explicit, individual-based model of early marine migration with two stocks of yearling Chinook salmon to quantify the influence of external forces on estimates of swim speed, consumption, and growth. Model results suggest that salmon behaviorally compensate for changes in the strength and direction of ocean currents. These compensations can result in salmon swimming several times farther than their net movement (straight-line distance) would indicate. However, the magnitude of discrepancy between compensated and straight-line distances varied between oceanographic models. Nevertheless, estimates of relative swim speed among fish groups were less sensitive to the choice of model than estimates of absolute individual swim speed. By comparing groups of fish, this tool can be applied to management questions, such as how experiences and behavior may differ between groups of hatchery fish released early vs. later in the season. By taking into account the experiences and behavior of individual fish, as well as the influence of physical ocean processes, our approach helps illuminate the “black box” of juvenile salmon behavior in the early marine phase of the life cycle.
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It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.
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Displacement studies have shown that long-distance, night-migrating songbirds are able to perform true navigation from their first spring migration onwards . True navigation requires both a map and a compass. Whereas birds are known to have sun, star, and magnetic compasses, the nature of the map cues used has remained highly controversial. There is quite strong experimental evidence for the involvement of olfactory map cues in pigeon and seabird homing. In contrast, the evidence for the use of magnetic map cues has remained weak and very little is known about the map cues used by long-distance migratory songbirds. In earlier experiments, we have shown that Eurasian reed warblers physically displaced 1,000 km eastward from Rybachy to Zvenigorod re-orient towards their breeding destinations by changing their orientation in Emlen funnels from the NE to the NW. We have also previously shown that this re-orientation cannot be explained by a ‘jetlag effect’. We have now used this model system to show that Eurasian reed warblers use geomagnetic map cues to determine their position.
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The 12th revision of the International Geomagnetic Reference Field (IGRF) was issued in December 2014 by the International Association of Geomagnetism and Aeronomy (IAGA) Division V Working Group V-MOD (http://www.ngdc.noaa.gov/IAGA/vmod/igrf.html). This revision comprises new spherical harmonic main field models for epochs 2010.0 (DGRF-2010) and 2015.0 (IGRF-2015) and predictive linear secular variation for the interval 2015.0-2020.0 (SV-2010-2015). The models were derived from weighted averages of candidate models submitted by ten international teams. Teams were led by the British Geological Survey (UK), DTU Space (Denmark), ISTerre (France), IZMIRAN (Russia), NOAA/NGDC (USA), GFZ Potsdam (Germany), NASA/GSFC (USA), IPGP (France), LPG Nantes (France), and ETH Zurich (Switzerland). Each candidate model was carefully evaluated and compared to all other models and a mean model using well-defined statistical criteria in the spectral domain and maps in the physical space. These analyses were made to pinpoint both troublesome coefficients and the geographical regions where the candidate models most significantly differ. Some models showed clear deviation from other candidate models. However, a majority of the task force members appointed by IAGA thought that the differences were not sufficient to exclude models that were well documented and based on different techniques. The task force thus voted for and applied an iterative robust estimation scheme in space. In this paper, we report on the evaluations of the candidate models and provide details of the algorithm that was used to derive the IGRF-12 product.
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Migration in animals has evolved as an adaptation to environmental variability across space and through time. The availability of reliable sensory cues and guidance mechanisms used in navigating among disparate locations is an essential component of this behavior. An "inherited magnetic map" is navigational solution that has evolved in some marine animals that, without prior experience or guidance from older conspecifics, migrate to oceanic foraging grounds. Laboratory experiments demonstrate that navigationally naive salmon encountering magnetic fields characteristic of certain regions along their migratory route will bias their swimming in a particular direction. Simulations of this behavior within realistic models of oceanic circulation suggest that such behavior is highly adaptive, making the migratory route more predictable and facilitating movement into favorable oceanic regions. Such behavior is possible due to the spatial gradients of components of the geomagnetic field (e.g., the inclination angle of field lines and the total field intensity) that provide a bicoordinate grid across much of the Earth's surface. However, this environmental feature is not static, but experiences gradual and unpredictable changes that can be substantial over successive generations. Thus, drift of the geomagnetic field, in addition to variable oceanic conditions, could play a major role in shaping the distribution of marine taxa that are dependent upon such mechanisms for migratory guidance. Several possibilities are discussed for how animals might mitigate the effects of geomagnetic drift, such as calibrating their inherited magnetic map relative to the field in which they develop. Further exploration of the dynamics of the geomagnetic field in context of animal navigation is a promising avenue for understanding the how animals deal with an ever-changing environment.
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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. © 2015. Published by The Company of Biologists Ltd.
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Loggerhead sea turtle hatchlings (Caretta caretta) use regional magnetic fields as open-ocean navigational markers during trans-oceanic migrations. Little is known, however, about the ontogeny of this behaviour. As a first step towards investigating whether the magnetic environment in which hatchlings develop affects subsequent magnetic orientation behaviour, eggs deposited by nesting female loggerheads were permitted to develop in situ either in the natural ambient magnetic field or in a magnetic field distorted by magnets placed around the nest. In orientation experiments, hatchlings that developed in the normal ambient field oriented approximately south when exposed to a field that exists near the northern coast of Portugal, a direction consistent with their migratory route in the northeastern Atlantic. By contrast, hatchlings that developed in a distorted magnetic field had orientation indistinguishable from random when tested in the same north Portugal field. No differences existed between the two groups in orientation assays involving responses to orbital movements of waves or sea-finding, neither of which involves magnetic field perception. These findings, to our knowledge, demonstrate for the first time that the magnetic environment present during early development can influence the magnetic orientation behaviour of a neonatal migratory animal.
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Animals navigate using a variety of sensory cues, but how each is weighted during different phases of movement (e.g. dispersal, foraging, homing) is controversial. Here, we examine the geomagnetic and olfactory imprinting hypotheses of natal homing with datasets that recorded variation in the migratory routes of sockeye (Oncorhynchus nerka) and pink (Oncorhynchus gorbuscha) salmon returning from the Pacific Ocean to the Fraser River, British Columbia. Drift of the magnetic field (i.e. geomagnetic imprinting) uniquely accounted for 23.2% and 44.0% of the variation in migration routes for sockeye and pink salmon, respectively. Ocean circulation (i.e. olfactory imprinting) predicted 6.1% and 0.1% of the variation in sockeye and pink migration routes, respectively. Sea surface temperature (a variable influencing salmon distribution but not navigation, directly) accounted for 13.0% of the variation in sockeye migration but was unrelated to pink migration. These findings suggest that geomagnetic navigation plays an important role in long-distance homing in salmon and that consideration of navigation mechanisms can aid in the management of migratory fishes by better predicting movement patterns. Finally, given the diversity of animals that use the Earth's magnetic field for navigation, geomagnetic drift may provide a unifying explanation for spatio-temporal variation in the movement patterns of many species.
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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.
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WHETHER migratory animals can determine their global position by detecting features of the Earth's magnetic field has long been debated1-4. To do this an animal must perceive (at least) two distinct magnetic parameters, each of which must vary in a different direction across the Earth's surface3,5. There has been no evidence that any animal can perceive two such magnetic features, and whether 'magnetic maps' exist at all has remained controversial2-6. Several populations of sea turtles7-9 undergo transoceanic migrations before returning to nest on or near the same beaches where they themselves hatched. Along the migratory routes, all or most locations have unique combinations of magnetic field intensity and field line inclination. It has been demonstrated that hatchling loggerhead turtles can distinguish between different magnetic inclination angles10. Here we report that turtles can also distinguish between different field intensities found along their migratory route. Thus sea turtles possess the minimal sensory abilities necessary to approximate global position using a bicoordinate magnetic map.
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Loggerhead sea turtle hatchlings emerge from nests on either the east or west coast of the South Florida peninsula and then migrate offshore in opposite directions. Under laboratory conditions, magnetic cues induce east coast hatchlings to swim in directions that promote their transport by oceanic surface currents, such as the North Atlantic gyre. However, the surface currents used by west coast hatchlings are unknown. We examined the responses of west (Sarasota) hatchlings to magnetic cues in the Gulf of Mexico, the Florida Straits, and the Gulf Stream to determine their (1) likely migratory routes (2) orientation where currents lead into the Atlantic Ocean, and (3) orientation adjacent to Florida’s east coast. The results suggest that migration inside Gulf waters may be circuitous, that the turtles respond appropriately to enter Atlantic waters, and that orientation along Florida’s east coast probably promotes transport by the Gulf Stream into the North Atlantic gyre.
Article
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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.
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Young loggerhead sea turtles (Caretta caretta) from the east coast of Florida, USA, undertake a transoceanic migration around the North Atlantic Gyre, the circular current system that flows around the Sargasso Sea. Previous experiments indicated that loggerhead hatchlings, when exposed to magnetic fields replicating those that exist at five widely separated locations along the migratory pathway, responded by swimming in directions that would, in each case, help turtles remain in the gyre and advance along the migratory route. In this study, hatchlings were exposed to several additional magnetic fields that exist along or outside of the gyre's northern boundary. Hatchlings responded to fields that exist within the gyre currents by swimming in directions consistent with their migratory route at each location, whereas turtles exposed to a field that exists north of the gyre had an orientation that was statistically indistinguishable from random. These results are consistent with the hypothesis that loggerhead turtles entering the sea for the first time possess a navigational system in which a series of regional magnetic fields sequentially trigger orientation responses that help steer turtles along the migratory route. By contrast, hatchlings may fail to respond to fields that exist in locations beyond the turtles' normal geographic range.
Article
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For animals that migrate long distances, the magnetic field of the earth provides not only a possible cue for compass orientation, but a potential source of world-wide positional information. At each location on the globe, the geomagnetic field lines intersect the earth’s surface at a specific angle of inclination. Because inclination angles vary with latitude, an animal able to distinguish between different field inclinations might, in principle, determine its approximate latitude. Such an ability, however, has never been demonstrated in any animal. We studied the magnetic orientation behavior of hatchling loggerhead sea turtles (Caretta caretta L.) exposed to earth-strength magnetic fields of different inclinations. Hatchlings exposed to the natural field of their natal beach swam eastward, as they normally do during their offshore migration. In contrast, those subjected to an inclination angle found on the northern boundary of the North Atlantic gyre (their presumed migratory path) swam south-southwest. Hatchlings exposed to an inclination angle found near the southern boundary of the gyre swam in a northeasterly direction, and those exposed to inclination angles they do not normally encounter, or to a field inclination found well within the northern and southern extremes of the gyre, were not significantly oriented. These results demonstrate that sea turtles can distinguish between different magnetic inclination angles and perhaps derive from them an approximation of latitude. Most sea turtles nest on coastlines that are aligned approximately north–south, so that each region of nesting beach has a unique inclination angle associated with it. We therefore hypothesize that the ability to recognize specific inclination angles may largely explain how adult sea turtles can identify their natal beaches after years at sea.
Article
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Young loggerhead sea turtles (Caretta caretta) from eastern Florida undertake a transoceanic migration in which they gradually circle the north Atlantic Ocean before returning to the North American coast. Here we report that hatchling loggerheads, when exposed to magnetic fields replicating those found in three widely separated oceanic regions, responded by swimming in directions that would, in each case, help keep turtles within the currents of the North Atlantic gyre and facilitate movement along the migratory pathway. These results imply that young loggerheads have a guidance system in which regional magnetic fields function as navigational markers and elicit changes in swimming direction at crucial geographic boundaries.
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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 Earth's 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.
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Migratory animals capable of navigating to a specific destination, and of compensating for an artificial displacement into unfamiliar territory, are thought to have a compass for maintaining their direction of travel and a map sense that enables them to know their location relative to their destination. Compasses are based on environmental cues such as the stars, the Sun, skylight polarization and magnetism, but little is known about the sensory mechanism responsible for the map sense. Here we show that the green sea-turtle (Chelonia mydas) has a map that is at least partly based on geomagnetic cues.
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Diverse animals detect the Earth's magnetic field and use it as a cue in orientation and navigation. Most research on magnetoreception has focused on the directional or ;compass' information that can be extracted from the Earth's field. Because the field varies predictably across the surface of the globe, however, it also provides a potential source of positional or 'map' information, which some animals use to steer themselves along migratory pathways or to navigate toward specific target areas. The use of magnetic positional information has been demonstrated in several diverse animals including sea turtles, spiny lobsters, newts and birds, suggesting that such systems are phylogenetically widespread and can function over a wide range of spatial scales. 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.
Article
Significance Diverse species that undertake long-distance migrations use geomagnetic “map” information to orient. Whether this is true for nonmigratory populations within these species or those migrating over considerably shorter distances is less studied. We show nonanadromous Atlantic salmon ( Salmo salar ) can extract map information from the geomagnetic field. Despite having no recent history of ocean migration and being translocated from Maine to Oregon approximately 60 years ago, juveniles exposed to magnetic fields characteristic of the North Pacific displayed adaptive orientation responses similar to those of anadromous Pacific salmonids. This navigational ability generates some concern since Atlantic salmon are transported throughout the world for aquaculture. Escaped individuals might have greater potential to successfully navigate, and thus invade, novel habitats than previously suspected.
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There is great diversity in the animal species that migrate, the biomechanics that propel their locomotion and the ecosystems through which they transit. This diversity, however, is unified by a common condition: the relative suitability of places changes in predictable and cyclical ways. Owing to the periodicity of environmental change (e.g., seasons) and animal life-cycles (e.g., growth and maturation) locations become favorable, lose favorability and become favorable again at somewhat regular intervals. Migratory animals have adapted to these predictable fluctuations by moving among locations, sometimes over extraordinary distances (Figure 1).
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For centuries, humans have been fascinated by how migratory animals find their way over thousands of kilometres. Here, I review the mechanisms used in animal orientation and navigation with a particular focus on long-distance migrants and magnetoreception. I contend that any long-distance navigational task consists of three phases and that no single cue or mechanism will enable animals to navigate with pinpoint accuracy over thousands of kilometres. Multiscale and multisensory cue integration in the brain is needed. I conclude by raising twenty important mechanistic questions related to long-distance animal navigation that should be solved over the next twenty years.
Article
Our recent study [1] in Current Biology used a magnetic displacement experiment and simulations in an ocean circulation model to provide evidence that young European eels possess a ‘magnetic map’ that can aid their marine migration. Our results support two major conclusions: first, young eels distinguish among magnetic fields corresponding to locations across their marine range; second, for the fields that elicited significantly non-random orientation, swimming in the experimentally observed direction from the corresponding locations would increase entrainment in the Gulf Stream system. In their critique, Durif et al. [2] seem to conflate the separate and potentially independent ‘map step’ and ‘compass step’ of animal navigation. In the map step, an animal derives positional information to select a direction, whereas in the compass step the animal maintains that heading 3 ; 4. Our experiment was designed such that differences in eel orientation among treatments would indicate an ability to use the magnetic field as a map; the compass cue(s) used by eels was not investigated.
Article
The longitude problem (determining east-west position) is a classical problem in human sea navigation. Prior to the use of GPS satellites, extraordinarily accurate clocks measuring the difference between local time and a fixed reference (e.g., GMT) [1] were needed to determine longitude. Birds do not appear to possess a time-difference clock sense [2]. Nevertheless, experienced night-migratory songbirds can correct for east-west displacements to unknown locations [3-9]. Consequently, migratory birds must solve the longitude problem in a different way, but how they do so has remained a scientific mystery [10]. We suggest that experienced adult Eurasian reed warblers (Acrocephalus scirpaceus) can use magnetic declination to solve the longitude problem at least under some circumstances under clear skies. Experienced migrants tested during autumn migration in Rybachy, Russia, were exposed to an 8.5° change in declination while all other cues remained unchanged. This corresponds to a virtual magnetic displacement to Scotland if and only if magnetic declination is a part of their map. The adult migrants responded by changing their heading by 151° from WSW to ESE, consistent with compensation for the virtual magnetic displacement. Juvenile migrants that had not yet established a navigational map also oriented WSW at the capture site but became randomly oriented when the magnetic declination was shifted 8.5°. In combination with latitudinal cues, which birds are known to detect and use [10-12], magnetic declination could provide the mostly east-west component for a true bi-coordinate navigation system under clear skies for experienced migratory birds in some areas of the globe.
Book
Not since F. R. Harden Jones published his masterwork on fish migration in 1968 has a book so thoroughly demystified the subject. With stunning clarity, David Hallock Secor's Migration Ecology of Fishes finally penetrates the clandestine nature of marine fish migration. Secor explains how the four decades of research since Jones's classic have employed digital-age technologies-including electronic miniaturization, computing, microchemistry, ocean observing systems, and telecommunications-that render overt the previously hidden migration behaviors of fish. Emerging from the millions of observed, telemetered, simulated, and chemically traced movement paths is an appreciation of the individual fish. Members of the same populations may stay put, explore, delay, accelerate, evacuate, and change course as they conditionally respond to their marine existence. But rather than a morass of individual behaviors, Secor shows us that populations are collectively organized through partial migration, which causes groups of individuals to embark on very different migration pathways despite being members of the same population. Case studies throughout the book emphasize how migration ecology confounds current fisheries management. Yet, as Secor explains, conservation frameworks that explicitly consider the influence of migration on yield, stability, and resilience outcomes have the potential to transform fisheries management. A synthetic treatment of all marine fish taxa (teleosts and elasmobranchs), this book employs explanatory frameworks from avian and systems ecology while arguing that migrations are emergent phenomena, structured through schooling, phenotypic plasticity, and other collective agencies. The book provides overviews of the following concepts:. The comparative movement ecology of fishes and birds. The alignment of mating systems with larval dispersal. Schooling and migration as adaptations to marine food webs. Natal homing. Connectivity in populations and metapopulations. The contribution of migration ecology to population resilience.
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New 'virtual displacement' experiments demonstrate that migrating reed warblers know the magnetic coordinates of their destination, and can set a novel course to their goal with only magnetic-field parameters as a guide.
Article
Before migrating from their home streams to the ocean, young Pacific salmon already know the magnetic parameters of their feeding grounds, allowing them to steer into a favorable habitat. What kind of 'map' representation underlies this remarkable ability?
Article
Migratory marine animals exploit resources in different oceanic regions at different life stages, but how they navigate to specific oceanic areas is poorly understood [1-3]. A particular challenge is explaining how juvenile animals with no prior migratory experience are able to locate specific oceanic feeding habitats that are hundreds or thousands of kilometers from their natal sites [1-7]. Although adults reproducing in the vicinity of favorable ocean currents can facilitate transport of their offspring to these habitats [7-9], variation in ocean circulation makes passive transport unreliable, and young animals probably take an active role in controlling their migratory trajectories [10-13]. Here we experimentally demonstrate that juvenile Chinook salmon (Oncorhynchus tshawytscha) respond to magnetic fields like those at the latitudinal extremes of their ocean range by orienting in directions that would, in each case, lead toward their marine feeding grounds. We further show that fish use the combination of magnetic intensity and inclination angle to assess their geographic location. The "magnetic map" of salmon appears to be inherited, as the fish had no prior migratory experience. These results, paired with findings in sea turtles [12-21], imply that magnetic maps are phylogenetically widespread and likely explain the extraordinary navigational abilities evident in many long-distance underwater migrants.
Article
In a series of papers, Lohmann and Lohmann (1991, 1994a, 1994b, 1996) provide evidence for remarkable sensitivity of sea-turtles to the earth's magnetic field and suggest that it is used by these animals to determine global position and to navigate. In this paper, we emphasize that a consequence of these observations taken together is that sea-turtles should be able to accurately detect the full (vector) magnetic-field, and perhaps spatial gradients. In order to interpret these observations, we propose a simple model in which the turtle is considered as a small permanent magnet, on which the geomagnetic field exerts a torque. This torque varies as a function of turtle azimuth and field parameters which depend mainly on latitude. Although this simple model accounts for some of the observational evidence, discrepancies might be due to a number of other factors, such as speed of magnetic field changes during experiments or lack of field homogeneity. Also, the earth's field has varied significantly over the last few centuries and some of the magnetic features observed today and suggested by the Lohmanns for use in sea-turtle navigation were very different or even not present two or three centuries ago. This would place constraints on the rate at which genetically inherited magnetic behavioural preferences can change with time. Alternately, it may imply that the experimental results need to be re-evaluated and complemented.
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Homing pigeons are able to return to their lofts after displacement to unfamiliar sites hundreds of kilometres away. A map sense enables them to determine their location, and a hierarchy of compass senses orient their flight. Recent experiments implicate magnetic and olfactory cues as the basis of the mysterious map sense.
Article
The optimal dimensions of thin coil systems of three and four square coils for producing uniform magnetic fields are calculated. We find that for three square coils, of side d and separation s between the outer coils, the most uniform field distribution occurs with s/d=0.821 116 and with I′/I=0.512 797. I′/I is the ratio of the currents in the center coil to that of the outer coils. With four square coils, the best uniformity is obtained when a/d=0.128 106 and b/d=0.505 492, where a is the distance from the center to the inner coils and b is the distance from the center to the outer coils. The ratio of the current in the inner pair of coils to that in the outer pair must be I′/I=0.423 514. We compare the uniformity of the field produced by these coil systems with each other and with Rubens’ five‐coil system, both on and off axis. It is shown that the optimal four‐coil design is superior to the three‐ and five‐coil systems. The sensitivity of the uniformity to the precision of construction is discussed. Dimensions of regions around the center of the coil systems, uniform to 1 part in 106 to 1 part in 102, are given.
Article
The question of whether animals navigate using ‘map’ information derived from one or more spatial gradients in the Earth's magnetic field has been debated for half a century. Although there is evidence that certain animals possess the sensory abilities necessary to perceive at least two magnetic components that vary spatially, there previously has been no direct test of the use of magnetic map information by experienced adult migrants. Magnetic information could provide information about an animal's geographic position along a single axis (‘unicoordinate map’) or could be part of a position-fixing system that provides positional information along two nonparallel axes (‘bicoordinate map’) with the second axis being derived from either magnetic or nonmagnetic cues. Here we report that adult eastern red-spotted newts,Notophthalmus viridescens , displaced approximately 45 km NNE of their home ponds oriented in the home direction when exposed either to the ambient magnetic field of the testing site, or to a 2° increase in magnetic inclination (normally found further from the home ponds in the same general direction as the testing site). When exposed to a 2° decrease in inclination resulting in a value that would normally be found on the other side of the home ponds from the testing site, however, newts reversed their direction of orientation. The same changes in magnetic inclination had no effect on shoreward magnetic compass orientation, which does not rely on map information. These findings provide support for two critical predictions of the magnetic map hypothesis, and suggest that information about geographic position along at least one axis relative to home may be derived from the magnetic field.
Article
This volume is divided into four parts. Part one consists of an introduction to migration and methods for its study. The second part examines proximate factors in migration: migration, winds and currents; physiology of migration; biomechanical and bioenergetic constraints on migration; and orientation and navigation. Part three examines migratory life histories and their evolution: seasonal migrations; migration to special habitats; migration under ephemeral conditions; behavioural variability in migration; polymorphisms and polyphenisms; and evolutionary genetics of migration. The final part discusses applications and implications in terms of pest management and conservation. -S.R.Harris
Article
Little is known of the physiological mechanisms underlying the effects of climate change on animals, yet it is clear that some species appear more resilient than others. As pink salmon (Oncorhynchus gorbuscha) in British Columbia, Canada, have flourished in the current era of climate warming in contrast to other Pacific salmonids in the same watershed, this study investigated whether the continuing success of pink salmon may be linked with exceptional cardiorespiratory adaptations and thermal tolerance of adult fish during their spawning migration. Sex-specific differences existed in minimum and maximum oxygen consumption rates (M(O2,min) and M(O2,max), respectively) across the temperature range of 8 to 28°C, reflected in a higher aerobic scope (M(O2,max)-M(O2,min)) for males. Nevertheless, the aerobic scope of both sexes was optimal at 21°C (T(opt)) and was elevated across the entire temperature range in comparison with other Pacific salmonids. As T(opt) for aerobic scope of this pink salmon population is higher than in other Pacific salmonids, and historic river temperature data reveal that this population rarely encounters temperatures exceeding T(opt), these findings offer a physiological explanation for the continuing success of this species throughout the current climate-warming period. Despite this, declining cardiac output was evident above 17°C, and maximum attainable swimming speed was impaired above ∼23°C, suggesting negative implications under prolonged thermal exposure. While forecasted summer river temperatures over the next century are likely to negatively impact all Pacific salmonids, we suggest that the cardiorespiratory capacity of pink salmon may confer a selective advantage over other species.
Article
Diverse ocean migrants, including some sea turtles, elephant seals, and salmon, begin life in particular reproductive areas along coastlines, disperse across vast expanses of sea, and then return as adults to their natal areas to reproduce 1, 2 and 3. Little is known about how such marine animals guide themselves to the correct coastal region from hundreds or thousands of kilometers away and after absences ranging in duration from a few months to a decade or more. One hypothesis is that animals imprint on the magnetic field of their home area and use this information to return [1]. The Earth's field varies predictably across the globe, so different geographic areas are marked by distinctive magnetic fields that might, in principle, provide unique magnetic signatures for natal areas [4]. A potentially serious complication for this hypothesis is that the Earth's field changes gradually over time 1 and 4, causing the magnetic signatures that define natal areas to slowly drift. This secular variation could make natal homing via magnetic imprinting impossible if the magnetic signatures moved too far from the natal area 1, 5 and 6. To investigate whether magnetic imprinting is compatible with secular variation, we sought a species with a life history that poses challenges for the hypothesis, reasoning that if magnetic imprinting is consistent with natal homing under unfavorable circumstances, then it would also be plausible in most other cases. We chose the Kemp's ridley sea turtle (Lepidochelys kempii), an endangered species that ranges widely over the Gulf of Mexico, northern Caribbean, and the eastern U.S. coast, but returns to nest along a single, limited region of coastline in northern Mexico [7]. This species requires approximately 10–15 years to reach sexual maturity [7] and is thus absent from its natal area for much longer than animals such as salmon and elephant seals 2 and 3. Given this long absence, the Kemp's ridley appears to be particularly susceptible to effects of secular variation if it relies on magnetic imprinting. The modeling results we report here show that the magnetic imprinting hypothesis can account for how the Kemp's ridley turtle returns to its natal region even after absences of a decade or more.
Article
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.
Article
The amazing abilities of Pacific salmon to migrate long distances from the ocean to their natal streams for spawning have been investigated intensively since 1950's, but there are still many mysteries because of difficulties to follow their whole life cycle and to wait their sole reproductive timing for several years. In my laboratory, we have tried to clarify physiological mechanisms of homing migration in Pacific salmon, using four anadromous Pacific salmon (pink, Oncorhynchus gorbuscha; chum, Oncorhynchus keta; sockeye, Oncorhynchus nerka; masu, Oncorhynchus masou) in the north Pacific Ocean as well as two lacustrine salmon (sockeye and masu) in Lake Toya and Lake Shikotsu, Hokkaido, Japan, where the lakes serve as a model "ocean". Three different approaches from behavioral to molecular biological researches have been conducted using these model fish. First, the homing behaviors of adult chum salmon from the Bering Sea to Hokkaido as well as lacustrine sockeye and masu salmon in Lake Toya were examined by means of physiological biotelemetry techniques, and revealed that salmon can navigate in open water using different sensory systems. Second, the hormone profiles in the brain-pituitary-gonadal (BPG) axis were investigated in chum salmon and lacustrine sockeye salmon during their homing migration by means of hormone specific time-resolved fluoroimmunoassay (TR-FIA) systems, and clarified that salmon gonadotropin-releasing hormone (sGnRH) plays leading roles on homing migration. Third, the olfactory functions of salmon were studied by means of electrophysiological, behavioral, and molecular biological techniques, and made clear that olfactory discriminating ability of natal stream odors. These results have discussed with the evolutional aspects of four Pacific salmon, sexual differences in homing profiles, and the possibility of dissolved free amino acids (DFAA) as natal stream odors for salmon.
Article
Spatial variation in the inclination of the geomagnetic field has been implicated in the map component of homing by eastern red-spotted newts Notophthalmus viridescens. Here we show that when newts are exposed to small changes in magnetic inclination, the most dramatic effects on homing orientation occur at values close to the 'home value', as predicted by the magnetic map hypothesis (Phillips 1996). Newts reverse the direction of homing orientation over a range of inclination of 0.5 degrees spanning the home value, providing further evidence that magnetic inclination or one of its components (i.e., vertical or horizontal intensity) is used to derive map information.
Article
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.