Migration Literature Review

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Magnetic Navigation

Papers: Alerstam 2003, Boles & Lohmann 2003, Gould 2008, Johnsen & Lohmann 2005, Klimley et al. 2005, Lohmann et al. 2008, Meyer et al. 2005, Phillips et al. 2002, Wiltschko & Wiltschko 2005

Johnsen & Lohmann (2005) provide a good summary of magnetic field perception abilities in animals: there are 3 hypotheses for how magnetoreception works in animals, electromagnetic induction, magnetic field-dependent chemical reactions and biogenic magnetite, for none of which direct evidence exists. The earth's magnetic field can provide 2 types of information: compass information, which allows an animal to maintain a particular heading (i.e. head north) and geographical position, which allows an animal to navigate complex routes or find home and could be based on inclination angle or field intensity or the animal learning the 'magnetic map' (local anomalies) in their location. Electromagnetic induction is believed to be used by elasmobranch fish by means of detecting the Lorentz force of a charged particle moving though a magnetic field where the electric circuit is formed by the seawater as the conducting medium. The induction mechanism can detect polarity, but is probably not sensitive enough to be used as a magnetic map. The chemical magnetoreception mechanism relies on an electron transfer in a radical pair induced by light absorption. It is believed to be used by birds, newts, and flies, in which changes in magnetic orientation have been observed in response to specific in wavelengths of light. The chemical mechanism cannot detect polarity (merely the poleward direction rather than north or south) and cannot detect very small changes in field intensity necessary for a magnetic map. The biogenic magnetite mechanism comes in 2 types: single-domain magnetite, which are permanently magnetized crystals and will rotate into alignment with the earth's magnetic field, and superparamagnetic magnetite, which are smaller crystals and not permanently magnetized so they won't rotate, but the crystal's magnetic axis tracks the ambient field's axis. There is evidence of single-domain magnetite in fish noses, superparamagnetic magnetite in the upper beak of pigeons and other birds, and magnetite receptions in other animals such as turtles and mole rats. Single-domain magnetite mechanisms could detect polarity, though superparamagnetic magnetite mechanisms could not, though both could detect small changes in intensity to function as a magnetic map sense. Wiltschko & Wiltschko (2005) cover the 3 hypothesized magnetoreception mechanisms as well and also discuss field inclination and/or intensity being used as a 'signpost' in navigation with examples of birds and turtles. Gould (2008) turns to the evolution of magnetic sense stating with certain micro-aerobic bacteria containing chains of magnetite which serve to align them which the earth's magnetic field (and thus swim down away from the oxygen-laden surface). He considers the diversity of map and compass systems, and suggests that the chemical mechanism has evolved at least twice as a (partial) replacement for a magnetite mechanism based on the discovery of a vestigial fixed-direction compass in robins.

Additionally, several papers discuss evidence of magnetic navigational capabilities. Boles & Lohmann (2003) show that spiny lobsters (Panulirus argus) move in a homeward direction after being displaced, deprived of visual and magnetic cues during displacement, and having their eyes covered. When tested with magnetic fields replicating the locations ~400 km N and S of the testing site, the lobsters moved in the direction home would have been, had they been at these locations, showing a magnetic map sense. Alerstam (2003) places the work of Boles & Lohmann (2003) is a larger context with the history of considering animals using the earth's magnetic field for navigation on open future questions. Similarly, Phillips et al. (2002) showed evidence of a magnetic map sense in newts (Notophthalmus viridescens) sensitive to small differences in the magnetic field; displaced newts navigated towards home when subjected to a magnetic inclination simulating -0.5° from home, and did not display a significant directional orientation when the magnetic field simulated that of their home pond. Klimley et al. (2005) used telemetry to track bat rays (Myliobatis californica) to show the bat rays moved in a straight-line highly directional manner indicative of a compass or piloting sense. Meyer et al. (2005) showed sharks (Carcharhinus plumbeus and Sphyrna lewini) could detect an earth-strength magnetic field using conditioning for a food reward.

See also Friedland et al. as discussed under Navigation / Foraging Behavior.

Further investigation:

  • Kalmijn, A. J. 1982 Electric and magnetic field detection in elasmobranch fishes. Science 218, 916–918.
  • Walker, M. M. et al. Structure and function of the vertebrate magnetic sense. Nature 390, 371–376 (1997).
  • Diebel, C. E. et al. Magnetite defines a vertebrate magnetoreceptor. Nature 406, 299–302 (2000).
  • Quinn, T. P. et al. Magnetic field detection in sockeye salmon. J. Exp. Zool. 217, 137–142 (1981).
  • Mann S, Sparks NHC, Walker MM, Kirschvink JL (1988) Ultra-structure, morphology and organization of biogenic magnetite from Sockeyes salmon, Oncorhynchus nerka: implications for magnetoreception. J Exp Biol 140:35–49
  • Quinn TP (1980) Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J Comp Physiol 137:243–248291:433–434
  • Quinn TP, Brannon EL (1982) The use of celestial and magnetic cues by orienting sockeye salmon smolts. J Comp Physiol 147:547–552

Navigation / Foraging Behavior

Papers: Humston et al. 2004, Lohmann et al. 2008, Naug & Arathi 2006, Odling-Smee & Braithwaite 2003, Warburton 2003, Friedland et al. (2001)

Odling-Smee & Braithwaite (2003) discuss how learning affects fish orientation. Possible orientation mechanisms include landmarks (most evidence comes from lab studies which doesn't necessarily translate to the wild), compass orientation (including a sun-compass or a magnetic compass, but probably not polarized light), water movements (probably more applicable to fish that live near stationary objects or in rivers), inertial guidance & internal clocks (i.e. paying attention to their own movements & use their internal circadian clock to be at particular locations at particular times of day), and social cues (following other fish). One interesting point is the importance of the fish's ecological environment in what is learned (i.e. landmark use of shallow vs. open-water dwelling fish). The paper includes a section on salmon, mostly focused on homing to find their natal river, but briefly mentioning ocean migration mechanisms of pheromone tracking and celestial and magnetic compasses. Lohmann et al. (2008) address long-distance ocean migration (not confining themselves to fish) with respect the the navigational clues available, and discusses the advantages and disadvantages to various methods of studying ocean migration (lab experiments, ocean experiments, and telemetry data). Salmon are known to possess magnetic compasses and perhaps also magnetic maps. Magnetic anomalies might actually be used as landmarks, rather than being problematic for magnetic navigation (evidence from sharks and whales). Salmon can use chemical/olfactory clues to find their natal river, including from estuary or coastal environments where the salmon can sample the differences between water is stratified in vertical layers; however, ocean navigation most likely involves non-olfactory mechanisms. Other cues involve hydrodynamics such as wave direction and current. Hatchling sea turtles use wave direction to orient offshore and salmon might use waves similarly, though there is currently no evidence of this, and could possibly also use wave direction in the open ocean due to seasonally consistent winds. Currents are used by many animals in shallow water, but probably aren't useful for open ocean navigation. Salmon might also be able to use skylight polarization patterns or a sun compass. Finally, there are interesting similarities between sea turtle and salmon navigation (open ocean followed by natal homing at 2 different spatial scales with probably 2 different mechanisms), where open ocean navigation is better understood in sea turtles and natal homing better understood in salmon.

[also cognition] Warburton (2003) discusses learning from a foraging rather than orientation perspective, looking at factors that affect learning and thus foraging success. Memory windows seemed to vary based on the predictability of food availability with "significant interspecific and interpopulation differences correlated with ecology." Performance can increase due to motivation or learning, example of coho (Oncorhynchus kisutch) increasing prey capture ability with experience.

Humston et al. (2004) created a spatiotemporally dynamic population model including heterogeneity of biotic and abiotic conditions. They investigate 3 movement behaviors: random-walk, kinesis, and restricted-are search (gradient response). They found restricted-area search very sensitive to initial conditions with grater variability among cohorts as fish tended to get stuck in local maxima and not move much (the model did not include prey depletion or density-dependence), and they recommend minimalistic movement models where there is no empirical evidence for complex behaviors at the appropriate spatiotemporal scale of the model. In a different vein, Naug & Arathi (2006) investigate decision rules used by honey bees (Apis cerana) to optimally forage in patches with multiple dynamic options.

Further investigation:

  • STABELL OB, HOMING AND OLFACTION IN SALMONIDS - A CRITICAL-REVIEW WITH SPECIAL REFERENCE TO THE ATLANTIC SALMON, BIOLOGICAL REVIEWS OF THE CAMBRIDGE PHILOSOPHICAL SOCIETY 59 : 333 1984
  • DITTMAN AH, Homing in Pacific salmon: Mechanisms and ecological basis, JOURNAL OF EXPERIMENTAL BIOLOGY 199 : 83 1996
  • QUINN TP AND GROOT, ORIENTATION OF CHUM SALMON (ONCORHYNCHUS-KETA) AFTER INTERNAL AND EXTERNAL MAGNETIC-FIELD ALTERATION, CANADIAN JOURNAL OF FISHERIES AND AQUATIC SCIENCES 40 : 1598 1983
  • QUINN TP AND DITTMAN AH, PACIFIC SALMON MIGRATIONS AND HOMING - MECHANISMS AND ADAPTIVE SIGNIFICANCE, TRENDS IN ECOLOGY & EVOLUTION 5 : 174 1990
  • PASZKOWSKI CA, FORAGING BEHAVIOR OF HATCHERY-PRODUCED COHO SALMON (ONCORHYNCHUS-KISUTCH) SMOLTS ON LIVE PREY, CANADIAN JOURNAL OF FISHERIES AND AQUATIC SCIENCES 42 : 1915 1985

Magnetic compass:

  • Quinn, T. P. (1980). Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J. Comp. Physiol. 137, 243-248.
  • Quinn, T. P., Merrill, R. T. and Brannon, E. L. (1981). Magnetic field detection in sockeye salmon. J. Exp. Zool. 217, 137-142.

Magnetic maps:

  • Quinn, T. P. (1984). Homing and straying in Pacific salmon. In Mechanisms of Migration in Fish (ed. J. D. McCleave, G. P. Arnold, J. J. Dodson and W. H. Neil), pp. 357-362. New York: Plenum.
  • Walker, M. M., Diebel, C. E., Haugh, C. V., Pankhurst, P. M., Montgomery, J. C. and Green, C. R. (1997). Structure and function of the vertebrate magnetic sense. Nature 390, 371-376.

No magnetic map:

  • Yano, A., Ogura, M., Sato, A., Sakaki, Y., Shimizu, Y., Baba, N. and Nagasawa, K. (1997). Effect of modified magnetic field on the ocean migration of maturing chum salmon, Oncorhynchus keta. Mar. Biol. 129, 523-530.
  • Døving, K. B. and Stabell, O. B. (2003). Trails in open waters: sensory cues in salmon migration. In Sensory Processing in Aquatic Environments (ed. S. P. Collin and N. J. Marshall), pp. 39-52. New York: Springer Verlag.
  • Walker, M. M., Diebel, C. E. and Kirschvink, J. L. (2003). Detection and use of the earth’s magnetic field by aquatic invertebrates. In Sensory Processing in Aquatic Environments (ed. S. P. Collin and N. J. Marshall), pp. 53-74. New York: Springer.

Ocean navigation:

  • Dittman, A. H. and Quinn, T. P. (1996). Homing in Pacific salmon: mechanisms and ecological basis. J. Exp. Biol. 199, 83-91.
  • Quinn, T. P. (1990). Current controversies in the study of salmon homing. Ethol. Ecol. Evol. 2, 49-63.
  • Quinn, T. P. (2005). The Behavior and Ecology of Pacific Salmon and Trout. Seattle: University of Washington Press.
  • Hasler, A. D. (1971). Orientation and fish migration. In Fish Physiology (ed. W. S. Hoar and D. J. Randall), pp. 429-510. New York: Academic.
  • Hinch, S. G., Cooke, S. J., Healey, M. C. and Farrell, A. P. (2006). Behavioral physiology of fish migrations: salmon as a model approach. In Fish Physiology. Vol. 24 (ed. A. P. Farrell and C. J. Brauner), pp. 239-295. Amsterdam: Elsevier.

Wave direction:

  • Cook, P. H. (1984). Directional information from surface swell: some possibilities. In Mechanisms of Migration in Fishes (ed. J. D. McLeave, G. P. Arnold, J. J. Dodson and W. H. Neill), pp. 79-101. New York: Plenum Press.

Sun/polarization compass:

  • Quinn, T. P. (1982). A model for salmon navigation on the high seas. In Salmon and Trout Migratory Behavior Symposium (ed. E. L. Brannon and E. O. Salo), pp. 229-337. Seattle: School of Fisheries, University of Washington.
  • see also Quinn 1980 above

Friedland et al. (2001) analyze temperature data from data storage tags to determine possible migration routes for chum salmon (Oncorhynchus keta) tagged in the Bering Sea migrating to Japan. They found that fish tended to make more directed progress (as determined by crossing isotherms) during the day when they also exhibited mode diving behavior, while at night temperatures tended to remain constant with the fish presumably near the surface. They found this supports a light-based orientation mechanism, such as a sun compass, with the daytime dives and ascents possibly related to finding/maintaining heading (maybe using polarization which would be robust to varying light conditions), though some form of magnetic navigation and/or thermal gradients may also be used in some way.

Interesting references:

  • Dat CG, Leblond PH, Thomson KA, Ingraham WJ (1995) Computer simulations of homeward migrating Fraser River sockeye salmon—is compass orientation a sufficient direction finding mechanism in the Northeast Pacific Ocean. Fish Oceanogr 4:209–216
  • Flamarique IN, Hawryshyn CW (1993) Spectral characteristics of salmonid migratory routes from Southern Vancouver Island (British Columbia). Can J Fish Aquat Sci 50: 1706–1716
  • Hansen LP, Jonsson N, Jonsson B (1993) Oceanic migration in homing Atlantic salmon. Anim Behav 45:927–941
  • Haugh CV, Walker MM (1998) Magnetic Discrimination Learning in Rainbow Trout (Oncorhynchus mykiss). J Navigation 51:35–45
  • Hiramatsu K, Ishida Y (1989) Random movement and orientation in pink salmon (Oncorhynchus gorbuscha) migrations. Can J Fish Aquat Sci 46:1062–1066
  • Nordtug T, Berg OK, Melo TB (1994) Directional light transmission in the pineal window of Atlantic salmon (Salmo salar L.) may be used for solar orientation. J Exp Zool 269: 403–412
  • Ogura M, Ishida Y (1992) Swimming behavior of coho salmon, Oncorhynchus kisutch, in the open sea as determined by ultrasonic telemetry. Can J Fish Aquat Sci 49:453–457
  • Ogura M, Ishida Y (1995) Homing behavior and vertical movements of four species of Pacific salmon (Oncorhynchus spp.) in the central Bering Sea. Can J Fish Aquat Sci 52:532–540
  • Ogura M, Kato M, Arai N, Sasada T, Sakaki Y (1992) Magnetic particles in chum salmon (Onchorhynchus keta): extraction and transmission electron microscopy. Can J Zool 70:874–877
  • Quinn TP, Groot C (1984) Pacific salmon (Oncorhynchus) migrations: orientation versus random movement. Can J Fish Aquat Sci 41:1319–1324
  • Radchenko VI, Glebov II (1998) On vertical distribution of Pacific salmon in the Bering Sea, collected by trawling data. J Ichthyol 38:603–608
  • Saila SB, Shappy RA (1963) Random movement and orientation in salmon migration. J Cons Int Explor Mer 28: 153–166
  • Stepanov AS, Churmasoc AV, Cherkashin SA (1979) Migration direction finding by chum salmon according to the sun. Sov J Mar Biol 5:92–99
  • Ueno Y (1992) Deepwater migrations of chum salmon (Oncorhynchus keta) along the Pacific coast of northern Japan. Can J Fish Aquat Sci 49:2307–2312
  • Wada K, Ueno Y (1999) Homing behavior of chum salmon determined by an archival tag (NPAFC Doc. 425) Hokkaido National Fisheries Research Institute, Hokkaido

Migration Models

Papers: Booker et al. 2008 and more

Booker et al. (2008) model the trajectories of 15 Atlantic salmon (Salmo salar) with known release (west coast of Ireland) and recapture (at sea north of the British Isles) points. The first part of the paper is devoted to validating the OCCAM model of ocean currents used with data from drifter buoys. For the salmon model, they investigated 3 direction-finding mechanisms, random-walk, rheotaxis (aligning to the prevailing current), and thermotaxis (moving to the preferred temperature along the temperature gradient), all with a constant velocity. They found that both rheotaxis and thermotaxis performed much better than random-walk, with rheotaxis more closely corresponding to recapture sites than thermotaxis. They measured the difference between the observed and simulated data (100 trajectories for each salmon) in 3 ways: difference between observed and simulated recapture on actual date of recapture, minimum distance between recapture location and any point on the simulated trajectory, and number of days between observed recapture date and minimum distance date. There were still discrepancies between modeled trajectories and recapture locations, which could also be explained by incorrectly estimating swimming speed or delays between tagging and the salmon entering the ocean.

Also, proposed migration routes for chum salmon migrating from the Bering Sea to Japan in Friedland et al. (2001) (discussed above under Navigation / Foraging Behavior).

Salmon using ocean currents/North Pacific Gyre: THOMSON 1992, PEARCY 1992

Vertical position in water column (superseded by modern tagging data?):QUINN 1989, OGURA 1992, RUGGERONE 1990

Navigation (celestial, magnetic, rheotaxis): HEALEY 1987, QUINN 1990, QUINN 1990, FRAENKEL 1961, ROYCE 1968, HAMILTON 1986, HEALEY 2000, YANO 1997, FRIEDLAND 2001

Comparison of OCCAM and drifters in Pacific: SAUNDERS 1999

Ocean conditions

Papers: Carmack 2007, McGowan et al. 1998, Wells 2008, and more

Carmack (2007) recommends using the alpha/beta ocean distinction a a conceptual framework for understanding physical and biological processes. Alpha oceans are found at subtropical latitudes and are characterized by being stratified by temperature, while beta oceans are found at subarctic latitudes and are instead stratified by salinity. The boundary corresponds roughly to the 10° winter isotherm at about 44°N in the North Pacific. Salmon are only found in beta oceans where temperatures are 6°-10° or colder, and it it hypothesized that they use another feature of beta oceans to aid in migration: "the system of contiguous buoyancy boundary currents along the coast of British Columbia and Alaska." Though Welch et al. (1995, 1998) argue that physiological factors keep salmon in colder waters, Carmack supposes it could also be the importance of the "special suite of environmental cues-maintained by freshwater mixtures in and above the permanent haloclineseas" to navigation. The paper also discusses nutrient availability in alpha and beta oceans.

Boundary currents for migration:

  • Welch, D.W., Chigirinsky, A.I., Ishida, Y., 1995. Upper thermal limits on the oceanic distribution of Pacific salmon (Onchorhynchus spp.) in the spring. Canadian Journal of Fisheries and Aquatic Science 52, 489–503.
  • Welch, D.W., Ishida, Y., Nagasawa, K., Eveson, J.P., 1998. Thermal limits on the ocean distribution of steelhead trout (Oncorhynchus mykiss). North Pacific Anadromous Fisheries Commission, Bulletin 1, 396–404.

McGowan et al. (1998) examines the effect of climate variation on North Pacific ecosystems on an interannual and interdecadal scale. Daily sea-surface temperature (SST) are well correlated along the Pacific coast and don't show poleward propagation of warming predicted by coastally trapped Kelvin waves. They also looked at SST correlated with SOI (Southern Oscillation Index) and found warm anomalies (El Niños) and cool anomalies (La Niñas) laster 6-12 months with approximately equal and opposite amplitudes. The biological response to warming El Niños episodes was a northward shift of species an population declines (from zooplankton to kelp forests to fish to sea birds to seals). In 1976-77 a regime shift took place: " a deepening of the Aleutian Low, a drop in SST in the central Pacific, and a rise in SST in the California Current and the Gulf of Alaska." The California Current temperature increased while salinity decreased (previously positively correlated). In general a negative effect on California Current system and a mostly positive impact on Gulf Of ALaska (though less data there), and discussion of mechanisms.

Wells et al. (2008) correlate various measures of ocean conditions with Chinook salmon (Oncorhynchus tshawytscha) growth. They used scale sample to measure growth and number of ocean winters from (i) ocean-type Situk River, Alaska; (ii) stream-type Taku River, Alaska; (iii) ocean- (1980–2003, N = 1427) and (iv) stream-type Skagit River, Washington; and (v) ocean-type Smith River, California, where stream-type spend at least one winter in freshwater before migrating to sea while ocean-type migrate to sea before their first winter. They used 2 methods, path analysis and partial least squares regression, and found that, in general, Alaska fish do better with a strong Alaska current, California fish do better with a strong California Current (though not as well modeled), and Puget Sound fish do best when neither current dominates (also, stream-type fit transition zone conditions the first 2 years and Alaska conditions the 3rd year).

So many references, where to begin?

  • Beamish, R.J., McFarlane, G.A. and King, J.R. (2005) Migratory patterns of pelagic fishes and possible linkages between open ocean and coastal ecosystems off the Pacific coast of North America. Deep-Sea Res. Part 2 52:739–755.
  • Prey distribution (Juvenile-focused?):
    • Brodeur, R.D., Pearcy, W.G. and Ralston, S. (2003) Abundance and distribution patterns of nekton and micronekton in the northern California current transition zone. J. Oceanogr. 59:514–535.
    • Brodeur, R.D., Fisher, J.P., Teel, D.J., Emmett, R.L., Casillas, E. and Miller, T.W. (2004) Juvenile salmonid distribution, growth, condition, origin, and environmental and species associations in the Northern California Current. Fish. Bull. 102:25–46.
  • Hobday, A.J. and Boehlert, G.W. (2001) The role of coastal ocean variation in spatial and temporal patterns in survival and size of coho salmon (Oncorhynchus kisutch). Can. J. Fish. Aquat. Sci. 58:2021–2036.
  • Mueter, F.J., Ware, D.M. and Peterman, R.M. (2002) Spatial correlation patterns in coastal environmental variables and survival rates of salmon in the north-east Pacific Ocean. Fish. Oceanogr. 11:205–218.
  • Sackmann, B., Mack, L., Logsdon, M. and Perry, M.J. (2004) Seasonal and inter-annual variability of SeaWiFS-derived chlorophyl a concentrations in waters off the Washington and Vancouver Island coasts, 1998-2002. Deep-Sea Res. Part 2 51:945–965.
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