- Email: [email protected]
Animal Navigation: Salmon Track Magnetic Variation
Current Biology Vol 23 No 4 R144
Dispatches
Animal Navigation: Salmon Track Magnetic Variation How animals navigate long distances to specific targets remains enigmatic. For Pacific salmon, new evidence suggests fish imprint on the magnetic coordinates of their home river and use this information to guide their return from distant open-ocean feeding areas. Graeme C. Hays* The ability of some animals to conduct long-distance migrations, sometimes spanning many 1000s of kilometres, is one of the wonders of the natural world. Well-known migrators span a range of taxa, including fish, insects, reptiles, birds and mammals. For example, it is well known that, after foraging in the open ocean, salmon can return to the river system they hatched from [1]; likewise, sea turtles return from sometimes very distant foraging grounds to breed as adults in the areas where they hatched [2]; while some birds conduct seasonal migrations of many 100s or 1000s of km, often between summer foraging areas and more equatorial overwintering areas, and can return to specific sites to breed year upon year [3]. As well as the physiological and morphological adaptations that allow for such long distance movements, a notable component of these journeys is the navigational ability that allows animals to return to specific target sites. There has been long-standing interest in trying to unfathom the navigational cues animals use to find their targets. For example, more than a decade after publishing the Origin of Species, Charles Darwin remained intrigued by animal navigation and as part of a Letter to Nature in 1873 he marvelled at the ability of green turtles to find their way back to their isolated breeding ground of Ascension Island in the middle of the Atlantic: ‘‘. how can we account, for instance, for the turtles which formerly congregated in multitudes, only at one season of the year, on the shores of the Isle of Ascension, finding their way to that speck of land in the midst of the great Atlantic Ocean?’’ [4]. A paper in this issue of Current Biology [5] sheds new light on how animals navigate during long-distance migration. Unravelling how animals complete their long-distance migrations remains challenging to this day and there is
a broad dichotomy in the approaches that have been employed to address this question. On the one hand, progress has been made with laboratory studies where the environment animals perceive is manipulated and the resulting behaviour of captive animals is recorded. Using this type of approach it has been shown that young green (Chelonia mydas) and loggerhead sea turtles (Caretta caretta) are able to perceive components of the Earth’s magnetic field (magnetic inclination and intensity) that may provide them with some map information in the open ocean [6,7]. On the other hand, in field studies either environmental cues animals experience while travelling have been manipulated or animal movements have been recorded in relation to natural spatial and temporal variability in environmental cues. For example, magnets have been attached to migrating adult turtles during their pan-oceanic migrations. In some cases [8], the movements of turtles have been impacted, highlighting the importance of magnetic information for navigation in free-swimming adult turtles. However in other cases [9], the movements of migrating adult turtles have been largely unimpaired, which implies that even when animals are able to perceive the Earth’s magnetic field, this perception may not necessarily be vital to complete long journeys. In other words, several types of navigation information may be used, with some level of redundancy, so that if one system is unavailable animals can use alternative mechanisms to find their way. This is akin to using your satellite navigation system when driving to a distant destination, but having a map to hand just in case the system fails. Set against this backdrop, Putman et al. [5] have brought a clever, fresh approach to this long-standing question of which navigational cues are used during long-distance migration. Their study focuses on the cues that
Pacific sockeye salmon (Oncorhynchus nerka) use when they return from the open ocean to the rivers they hatched from. It is well known that salmon are accomplished migrants: after spending their early years in river systems, they travel to the open ocean, sometimes travelling thousands of kilometres from their home river where they hatched. Having reached sexual maturity, they return to spawn in the stream that they hatched from. This fact is well known from tagging individuals and logging their return from the open ocean. Furthermore, it has been known for several decades that the smell of the water is key to salmon detecting their home river [1,10]. For example, experiments in the 1950s showed that salmon that were rendered unable to smell could not distinguish their home stream [1]. Furthermore, when odours were artificially added to some rivers, and then the odours were subsequently moved from one river to another, returning salmon could be fooled into returning to the wrong river [10]. So, salmon use their sense of smell to find their home river. Problem solved? Or is there more to learn? As mentioned above for sea turtles, there may be several navigational cues used in long-distance travel. The same seems to apply to Pacific salmon. Putman et al. [5] looked at a 56 year time series of the routes that salmon used to return to a particular home river. On the Pacific coast of Washington, Vancouver Island lies off-shore of the Fraser River, a major salmon river. Returning salmon have to either swim north or south around Vancouver Island to get to the Fraser River. Putman et al. [5] showed that the proportion of fish travelling via the northerly and southerly routes varied hugely from one year to another. For example, in some years >90% of salmon travelled via the northerly route, while in other years the figure was <10%. At first glance, this looks like a perplexing result. But, the authors took the clever step of looking at long-term changes in the Earth’s magnetic field in this area. It is well known that the Earth’s magnetic field is not static but moves constantly. The magnetic north pole, for example,
Dispatch R145
Pacific Ocean 200 km Current Biology
Figure 1. Movement of the Earth’s magnetic field influences salmon homing. By recording the movements of animals in relation to potential navigation cues, evidence for and against the use of certain cues can be gained. For 56 years the return direction of sockeye salmon to the Fraser River has been recorded. In some years most salmon returned via the south of Vancouver Island while in other years most salmon returned via the northern route. This inter-annual variation in return path is linked to movement of the inclination and intensity of the Earth’s magnetic field, suggesting that salmon use the magnetic field to navigate. Circle: mouth of Fraser River; triangle: Vancouver Island. Red arrows indicate inferred return directions of salmon. Salmon illustration courtesy of the estate of Harry Heine.
moves by 50–60 km each year. Likewise other parameters of the Earth’s magnetic field, such as its intensity and inclination, constantly move, a phenomenon known as ‘secular variation’ [11]. So over time, a magnetic map based on the Earth’s magnetic inclination and intensity will shift and, consequently, any animals following this map should change their routes of travel accordingly. Putman et al. [5] showed that the proportion of salmon returning to the Fraser River via the northerly or southerly routes could be explained by this inter-annual movement of the magnetic map. So, salmon seem to be using the Earth’s magnetic field to navigate as they cross the open ocean towards their home river and then switch to using smell to find their specific home stream (Figure 1). These results parallel the conclusion for long-distance migration in sea turtles where it is thought that magnetic information may be one of the cues used in ocean crossings before a switch to more localised cues, including the smell of land, as they approach their target [12]. Thus, it appears that in diverse migrants, such as turtles and salmon, the geomagnetic map is rather crude, allowing animals to return to roughly the correct area, with fine-scale target
finding facilitated by other cues, such as smell [13]. So, what important questions remain unresolved? If the movement of the Earth’s magnetic field impacts the routes that migrating animals follow, then this may be a surmountable problem when animals migrate fairly regularly, as over only a few years the movement of the magnetic map may be relatively small. However, other animals may only complete their return journey to specific sites many decades after they completed the outward leg. For example, turtles may only return to breeding sites for the first time after more than 20 years [14]. Likewise freshwater eels, such as the Atlantic eel (Anguilla anguilla), may take decades to mature in river systems before they return to distant ocean sites to breed [15]. Over these long time-scales, movement of the Earth’s magnetic field may be considerable: possibly many 100s of km. In such circumstances how animals find specific targets, rather than ending up 100s of km away, remains enigmatic. While Charles Darwin would no doubt be pleased to learn of all the recent discoveries into the navigational cues used by long-distance migrants, he surely would still be intrigued by the unresolved questions. References 1. Wisby, W.J., and Hasler, A.D. (1954). Effect of occlusion on migrating silver salmon (Oncorhynchus kisutch). J. Fish. Res. Bd. Can. 11, 472–478. 2. Bowen, B.W., Meylan, A.B., and Avise, J.C. (1989). An odyssey of the green sea turtle – Ascension Island revisited. Proc. Natl. Acad. Sci USA 86, 573–576. 3. Klaassen, R.H.G., Hake, M., Strandberg, R., and Alerstam, T. (2011). Geographical and temporal flexibility in the response to crosswinds by migrating raptors. Proc. R. Soc. B 278, 1339–1346. 4. Darwin, C. (1873). Perception in the lower animals. Nature 7, 360.
5. Putman, N.F., Lohmann, K.J., Putman, E.M., Quinn, T.P., Klimley, A.P., and Noakes, D.L.G. (2013). Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon. Curr. Biol. 23, 312–316. 6. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A., and Swing, T. (2004). Geomagnetic map used in sea-turtle navigation. Nature 428, 909–910. 7. Putman, N.F., Endres, C.S., Lohmann, C.M.F., and Lohmann, K.J. (2011). Longitude perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21, 463–466. 8. Luschi, P., Benhamou, S., Girard, C., Ciccione, S., Roos, D., Sudre, J., and Benvenuti, S. (2007). Marine turtles use geomagnetic cues during open-sea homing. Curr. Biol. 17, 126–133. 9. Papi, F., Luschi, P., A˚kesson, S., Capogrossi, S., and Hays, G.C. (2000). Open-sea migration of magnetically disturbed sea turtles. J. Exp. Biol. 203, 3435–3443. 10. Scholz, A.T., Horrall, R.M., Cooper, J.C., and Hasler, A.D. (1976). Imprinting to chemical cues: the basis for home stream selection in Salmon. Science 192, 1247–1249. 11. Lohmann, K.J., Luschi, P., and Hays, G.C. (2008). Goal navigation and island-finding in sea turtles. J. Exp. Mar. Biol. Ecol. 356, 83–95. 12. Hays, G.C., A˚kesson, S., Broderick, A.C., Glen, F., Godley, B.J., Papi, F., and Luschi, P. (2003). Island-finding ability of marine turtles. P. Roy. Soc. Lond. B 270(suppl), S5–S7. 13. Luschi, P., Akesson, S., Broderick, A.C., Glen, F., Godley, B.J., Papi, F., and Hays, G.C. (2001). Testing the navigational abilities of ocean migrants: displacement experiments on green sea turtles (Chelonia mydas). Beh. Ecol. Sociobiol. 50, 528–534. 14. Scott, R., Marsh, R., and Hays, G.C. (2012). Life in the really slow lane: loggerhead sea turtles mature late relative to other reptiles. Funct. Ecol. 26, 227–235. http://dx.doi.org/10.1111/ j.1365-2435.2011.01915.x. 15. Aarestrup, K., Okland, F., Hansen, M.M., Righton, D., Gargan, P., Castonguay, M., Bernatchez, L., Howey, P., Sparholt, H., Pedersen, M.I., et al. (2009). Oceanic spawning migration of the European Eel (Anguilla anguilla). Science 325, 1660.
Department of Biosciences, College of Science, Swansea University SA2 8PP, UK. Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Warrnambool, Victoria 3280, Australia. *E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2013.01.025
Cytokinesis: Centralspindlin Moonlights as a Membrane Anchor The hardest working complex in animal cell division has a new gig. This extraordinary machine, the centralspindlin complex, works overtime, contributing to nearly every step in cytokinesis. It has now been shown to stabilize an association between the plasma membrane and the midbody microtubules prior to abscission. Michael Glotzer Centralspindlin is a stable heterotetramer consisting of a dimer of
the kinesin MKLP1 and a dimer of the accessory protein Cyk4 (also known as MgcRacGAP) [1] (Figure 1A). The MKLP1 subunit of centralspindlin is
Dispatches
Animal Navigation: Salmon Track Magnetic Variation How animals navigate long distances to specific targets remains enigmatic. For Pacific salmon, new evidence suggests fish imprint on the magnetic coordinates of their home river and use this information to guide their return from distant open-ocean feeding areas. Graeme C. Hays* The ability of some animals to conduct long-distance migrations, sometimes spanning many 1000s of kilometres, is one of the wonders of the natural world. Well-known migrators span a range of taxa, including fish, insects, reptiles, birds and mammals. For example, it is well known that, after foraging in the open ocean, salmon can return to the river system they hatched from [1]; likewise, sea turtles return from sometimes very distant foraging grounds to breed as adults in the areas where they hatched [2]; while some birds conduct seasonal migrations of many 100s or 1000s of km, often between summer foraging areas and more equatorial overwintering areas, and can return to specific sites to breed year upon year [3]. As well as the physiological and morphological adaptations that allow for such long distance movements, a notable component of these journeys is the navigational ability that allows animals to return to specific target sites. There has been long-standing interest in trying to unfathom the navigational cues animals use to find their targets. For example, more than a decade after publishing the Origin of Species, Charles Darwin remained intrigued by animal navigation and as part of a Letter to Nature in 1873 he marvelled at the ability of green turtles to find their way back to their isolated breeding ground of Ascension Island in the middle of the Atlantic: ‘‘. how can we account, for instance, for the turtles which formerly congregated in multitudes, only at one season of the year, on the shores of the Isle of Ascension, finding their way to that speck of land in the midst of the great Atlantic Ocean?’’ [4]. A paper in this issue of Current Biology [5] sheds new light on how animals navigate during long-distance migration. Unravelling how animals complete their long-distance migrations remains challenging to this day and there is
a broad dichotomy in the approaches that have been employed to address this question. On the one hand, progress has been made with laboratory studies where the environment animals perceive is manipulated and the resulting behaviour of captive animals is recorded. Using this type of approach it has been shown that young green (Chelonia mydas) and loggerhead sea turtles (Caretta caretta) are able to perceive components of the Earth’s magnetic field (magnetic inclination and intensity) that may provide them with some map information in the open ocean [6,7]. On the other hand, in field studies either environmental cues animals experience while travelling have been manipulated or animal movements have been recorded in relation to natural spatial and temporal variability in environmental cues. For example, magnets have been attached to migrating adult turtles during their pan-oceanic migrations. In some cases [8], the movements of turtles have been impacted, highlighting the importance of magnetic information for navigation in free-swimming adult turtles. However in other cases [9], the movements of migrating adult turtles have been largely unimpaired, which implies that even when animals are able to perceive the Earth’s magnetic field, this perception may not necessarily be vital to complete long journeys. In other words, several types of navigation information may be used, with some level of redundancy, so that if one system is unavailable animals can use alternative mechanisms to find their way. This is akin to using your satellite navigation system when driving to a distant destination, but having a map to hand just in case the system fails. Set against this backdrop, Putman et al. [5] have brought a clever, fresh approach to this long-standing question of which navigational cues are used during long-distance migration. Their study focuses on the cues that
Pacific sockeye salmon (Oncorhynchus nerka) use when they return from the open ocean to the rivers they hatched from. It is well known that salmon are accomplished migrants: after spending their early years in river systems, they travel to the open ocean, sometimes travelling thousands of kilometres from their home river where they hatched. Having reached sexual maturity, they return to spawn in the stream that they hatched from. This fact is well known from tagging individuals and logging their return from the open ocean. Furthermore, it has been known for several decades that the smell of the water is key to salmon detecting their home river [1,10]. For example, experiments in the 1950s showed that salmon that were rendered unable to smell could not distinguish their home stream [1]. Furthermore, when odours were artificially added to some rivers, and then the odours were subsequently moved from one river to another, returning salmon could be fooled into returning to the wrong river [10]. So, salmon use their sense of smell to find their home river. Problem solved? Or is there more to learn? As mentioned above for sea turtles, there may be several navigational cues used in long-distance travel. The same seems to apply to Pacific salmon. Putman et al. [5] looked at a 56 year time series of the routes that salmon used to return to a particular home river. On the Pacific coast of Washington, Vancouver Island lies off-shore of the Fraser River, a major salmon river. Returning salmon have to either swim north or south around Vancouver Island to get to the Fraser River. Putman et al. [5] showed that the proportion of fish travelling via the northerly and southerly routes varied hugely from one year to another. For example, in some years >90% of salmon travelled via the northerly route, while in other years the figure was <10%. At first glance, this looks like a perplexing result. But, the authors took the clever step of looking at long-term changes in the Earth’s magnetic field in this area. It is well known that the Earth’s magnetic field is not static but moves constantly. The magnetic north pole, for example,
Dispatch R145
Pacific Ocean 200 km Current Biology
Figure 1. Movement of the Earth’s magnetic field influences salmon homing. By recording the movements of animals in relation to potential navigation cues, evidence for and against the use of certain cues can be gained. For 56 years the return direction of sockeye salmon to the Fraser River has been recorded. In some years most salmon returned via the south of Vancouver Island while in other years most salmon returned via the northern route. This inter-annual variation in return path is linked to movement of the inclination and intensity of the Earth’s magnetic field, suggesting that salmon use the magnetic field to navigate. Circle: mouth of Fraser River; triangle: Vancouver Island. Red arrows indicate inferred return directions of salmon. Salmon illustration courtesy of the estate of Harry Heine.
moves by 50–60 km each year. Likewise other parameters of the Earth’s magnetic field, such as its intensity and inclination, constantly move, a phenomenon known as ‘secular variation’ [11]. So over time, a magnetic map based on the Earth’s magnetic inclination and intensity will shift and, consequently, any animals following this map should change their routes of travel accordingly. Putman et al. [5] showed that the proportion of salmon returning to the Fraser River via the northerly or southerly routes could be explained by this inter-annual movement of the magnetic map. So, salmon seem to be using the Earth’s magnetic field to navigate as they cross the open ocean towards their home river and then switch to using smell to find their specific home stream (Figure 1). These results parallel the conclusion for long-distance migration in sea turtles where it is thought that magnetic information may be one of the cues used in ocean crossings before a switch to more localised cues, including the smell of land, as they approach their target [12]. Thus, it appears that in diverse migrants, such as turtles and salmon, the geomagnetic map is rather crude, allowing animals to return to roughly the correct area, with fine-scale target
finding facilitated by other cues, such as smell [13]. So, what important questions remain unresolved? If the movement of the Earth’s magnetic field impacts the routes that migrating animals follow, then this may be a surmountable problem when animals migrate fairly regularly, as over only a few years the movement of the magnetic map may be relatively small. However, other animals may only complete their return journey to specific sites many decades after they completed the outward leg. For example, turtles may only return to breeding sites for the first time after more than 20 years [14]. Likewise freshwater eels, such as the Atlantic eel (Anguilla anguilla), may take decades to mature in river systems before they return to distant ocean sites to breed [15]. Over these long time-scales, movement of the Earth’s magnetic field may be considerable: possibly many 100s of km. In such circumstances how animals find specific targets, rather than ending up 100s of km away, remains enigmatic. While Charles Darwin would no doubt be pleased to learn of all the recent discoveries into the navigational cues used by long-distance migrants, he surely would still be intrigued by the unresolved questions. References 1. Wisby, W.J., and Hasler, A.D. (1954). Effect of occlusion on migrating silver salmon (Oncorhynchus kisutch). J. Fish. Res. Bd. Can. 11, 472–478. 2. Bowen, B.W., Meylan, A.B., and Avise, J.C. (1989). An odyssey of the green sea turtle – Ascension Island revisited. Proc. Natl. Acad. Sci USA 86, 573–576. 3. Klaassen, R.H.G., Hake, M., Strandberg, R., and Alerstam, T. (2011). Geographical and temporal flexibility in the response to crosswinds by migrating raptors. Proc. R. Soc. B 278, 1339–1346. 4. Darwin, C. (1873). Perception in the lower animals. Nature 7, 360.
5. Putman, N.F., Lohmann, K.J., Putman, E.M., Quinn, T.P., Klimley, A.P., and Noakes, D.L.G. (2013). Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon. Curr. Biol. 23, 312–316. 6. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A., and Swing, T. (2004). Geomagnetic map used in sea-turtle navigation. Nature 428, 909–910. 7. Putman, N.F., Endres, C.S., Lohmann, C.M.F., and Lohmann, K.J. (2011). Longitude perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21, 463–466. 8. Luschi, P., Benhamou, S., Girard, C., Ciccione, S., Roos, D., Sudre, J., and Benvenuti, S. (2007). Marine turtles use geomagnetic cues during open-sea homing. Curr. Biol. 17, 126–133. 9. Papi, F., Luschi, P., A˚kesson, S., Capogrossi, S., and Hays, G.C. (2000). Open-sea migration of magnetically disturbed sea turtles. J. Exp. Biol. 203, 3435–3443. 10. Scholz, A.T., Horrall, R.M., Cooper, J.C., and Hasler, A.D. (1976). Imprinting to chemical cues: the basis for home stream selection in Salmon. Science 192, 1247–1249. 11. Lohmann, K.J., Luschi, P., and Hays, G.C. (2008). Goal navigation and island-finding in sea turtles. J. Exp. Mar. Biol. Ecol. 356, 83–95. 12. Hays, G.C., A˚kesson, S., Broderick, A.C., Glen, F., Godley, B.J., Papi, F., and Luschi, P. (2003). Island-finding ability of marine turtles. P. Roy. Soc. Lond. B 270(suppl), S5–S7. 13. Luschi, P., Akesson, S., Broderick, A.C., Glen, F., Godley, B.J., Papi, F., and Hays, G.C. (2001). Testing the navigational abilities of ocean migrants: displacement experiments on green sea turtles (Chelonia mydas). Beh. Ecol. Sociobiol. 50, 528–534. 14. Scott, R., Marsh, R., and Hays, G.C. (2012). Life in the really slow lane: loggerhead sea turtles mature late relative to other reptiles. Funct. Ecol. 26, 227–235. http://dx.doi.org/10.1111/ j.1365-2435.2011.01915.x. 15. Aarestrup, K., Okland, F., Hansen, M.M., Righton, D., Gargan, P., Castonguay, M., Bernatchez, L., Howey, P., Sparholt, H., Pedersen, M.I., et al. (2009). Oceanic spawning migration of the European Eel (Anguilla anguilla). Science 325, 1660.
Department of Biosciences, College of Science, Swansea University SA2 8PP, UK. Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Warrnambool, Victoria 3280, Australia. *E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2013.01.025
Cytokinesis: Centralspindlin Moonlights as a Membrane Anchor The hardest working complex in animal cell division has a new gig. This extraordinary machine, the centralspindlin complex, works overtime, contributing to nearly every step in cytokinesis. It has now been shown to stabilize an association between the plasma membrane and the midbody microtubules prior to abscission. Michael Glotzer Centralspindlin is a stable heterotetramer consisting of a dimer of
the kinesin MKLP1 and a dimer of the accessory protein Cyk4 (also known as MgcRacGAP) [1] (Figure 1A). The MKLP1 subunit of centralspindlin is