BIOLOGY 457/657 PHYSIOLOGY OF MARINE & ESTUARINE ANIMALS

1. BIOLOGY 457/657PHYSIOLOGY OF MARINE & ESTUARINE ANIMALS May 5, 2004 MIGRATION IN THE SEA

2. INTRODUCTIONCues for Migration Marine Animals Use Every Available Sensory Modality to Orient Their Migrations, Both Short and Long-Distance

3. INTRODUCTIONCues for Orientation Light (visual systems; eyes) Sound (auditory senses) Gravity (mechanical systems) Pressure (several receptor types) Chemical gradients (chemosenses) Currents (mechanoreception) Wind (mechanoreception) Wave surge (acceration receptors; gravity sense) Temperature (thermal sense) Celestial cues (visual systems) Electrical fields (electroreception) Magnetic fields (magnetoreceptors) Landmarks (visual systems)

4. INTRODUCTIONTypes of Navigation Piloting - Navigation involving the use of landmarks. “Dead Reckoning” - Navigation involving compass and distance cues. True Navigation - Navigation requiring a reliable map sense; requires 2 independent sets of coordinates. As animals migrate, they often combine all possible strategies during their travels. For instance, they may usetrue navigation to figure out where they are, dead reckoning to get near their destination, and piloting to reach the exact point they want to go. In fact, this is what a human navigator often does!

5. INTRODUCTIONTypes of Migration Definition: “The act of moving from one spatial unit to another (Robin Baker, 1978).” Accidental Migration vs Non-accidental Migration Removal Migration vs Return Migration Periodic Migration vs Ontogenetic Migration Homing Behavior

6. INTRODUCTIONBiological Features of Migration Is species characteristic. Generally involves a large fraction (frequently all) of the individuals in a population. Is multimodal. Involves the use of diverse cues for orientation and navigation. Is periodic. Periodicity may be ontogenetic, annual, lunar or semilunar, diel, or tidal. Has physiological aspects. Includes sensory, internal drive, and orientational/navigational components.

7. Migrations in the SeaShort-Range Migrations: Diel Vertical Migration • Common patterns: • Nocturnal (animals at surface at night, by far the most common pattern) • Twilight (animals at surface at dawn and dusk; a modification of the nocturnal pattern) • Reverse (animals at surface during the day) • Tidal (keyed to to tides; phase shifts with regard to L:D cycle) • Substrate-Water Column (common for animals that are riding tidal currents or only feeding for part of the day) • Patterns may vary with age, sex, season, mating condition, and presence of food or predators. • Diel vertical migration is considered the greatest mass movement of animals on earth that takes place each day!

8. Diel Vertical Migration

9. Vertical Migration: Mechanisms Light plays a central role in all but tidal vertical migration. Does not involve phototaxis (an oriented swimming response to light). Light orientation may be modified by other depth-related factors. Two Major Hypotheses: (1) Preferendum Hypothesis - the animals follow a “preferred” level of light (a particular isolume). (2) Rate-of-Change Hypothesis - the migration is stimulated by changing light conditions. For instance, a decrease in light intensity might cue upward swimming, while an increase could initiate downward swimming.

10. Vertical Migration: Mechanisms Isolume-following by the “deep scattering layer” at sunrise (left) and sunset (right). Notice that the layer seems to stay with a particular level of light. But also notice that this apparent “following” behavior could be caused by changes in light intensity.

11. Vertical Migration: Mechanisms Isolume-following by crab larvae in an estuary. Note that while the larvae often stay with a particular isolume, they also migrate in response to other (less obvious) cues.

12. Vertical Migration: Mechanisms

13. Vertical MigrationAdaptive Significance “Optimal light value” - old idea, but what does it mean??? Photoprotection Accidental byproduct of station-keeping. Enhancement of dispersal by currents at different levels. Predator avoidance (***) Metabolic advantages (feed in warm water, digest and assimilate in cold) Feeding advantages (chlorophyll and photosynthetic products are highest at sunset)

14. Migrations in the SeaShort-Range Migrations: Y-Axis Orientation Animals on beaches commonly orient towards the water. This is called “y-axis” orientation, since it is perpendicular to the beach. There is evidence that the preferred orientation (with respect to the sun) is inherited, at least in beach amphipods. www.gla.ac.uk/ibls/DEEB/honsproj/ izzie_2/graphics/tal.jpg

15. Migrations in the SeaIntermediate-Range Migrations Example: The spiny lobster Panulirus argus in the Bahamas (research done by William Herrnkind and collaborators) The migration is unusual in that the lobsters actually travel in single-file “queues”. Queuing reduces drag.

16. Migrations in the SeaIntermediate-Range Migrations stevegoldfarb.com/bvi/ art/spinylobster.gif

17. Summary of migration: Premigration. Lobsters move independently. Buildup. In autumn, lobsters move into the migration pathway. Mass migration. Lobsters begin to form long cues, moving southward along the margins of the island. Post-migration. Following the migration, lobsters disperse into available cover. The migration may prepare the animals for cold water conditions in winter. (Summarized from Herrnkind) Migrations in the SeaIntermediate-Range Migrations

18. Migrations in the SeaIntermediate-Range Migrations

19. Migrations in the SeaIntermediate-to-Long Range Migrations Spiny lobsters also can orient back to their homes if displaced by several 10s to 100s of miles. Boles & Lohmann 2003

20. Migrations in the SeaIntermediate-to-Long Range Migrations The navigation system is based on detection and orientation within the earth’s magnetic field.

21. Migrations in the SeaLong-Range Migrations I: Tunas Bluefin tuna (Thunnus thynnus) make long-distance (trans-oceanic) migrations. To study this, tuna were tagged with “implantable archival tags” (recovered at the triangles) and “pop-up satellite archival tags” (recovered at the circles). These tags monitored location, depth, and temperature.

22. Migrations in the SeaLong-Range Migrations I: Tunas Individual tuna swam vertically down as much as 1000 m, but often less deep at night (see the blue trace, right). Body temperature (red) was relatively constant and almost always higher than sea temperature outside the fish (black lines; the red dots are maximum body temperature, and the black dots are minimum environmental temperature).

23. Migrations in the SeaLong-Range Migrations I: Tunas Fish often stayed resident in the western Atlantic, and many made transoceanic return migrations at least once. Panel A shows data from 19 fish that migrated only slightly. The fish in panel B migrated to the Gulf of Mexico and back. C shows several fish that crossed the ocean and returned. The bottom panel (D) illustrates a fish that stayed near North America in 1999 (black) and then crossed to the east (where it was caught).

24. Migrations in the SeaLong-Range Migrations II: Eels Fish migrations between sea & rivers fall into two general types: Catadromous migrations. Adults live in fresh water, but breed in the open sea. The best examples are the anguillid eels, which live in rivers (in Europe or Asia) as adults, but breed in the sea (in the case of the Atlantic population, Anguilla anguilla, in the Sargasso Sea). Anadromous migrations. Adults live in seawater, but spawn in fresh (or estuarine) waters. Excellent examples are salmon, lampreys, and striped bass (“rockfish”). Navigational mechanisms are unknown, but it is clear that chemical cues play major roles. Almost certainly, geomagnetic senses are involved too.

25. Migrations in the SeaLong-Range Migrations II: Eels

26. Migrations in the SeaLong-Range Migrations II: Eels The Japanese counterpart of Anguilla anguilla (A. japonica) was also known to exhibit a catadromous migration, but it was only in 1991 that the location of the reproductive center was located in the Philippine Sea. Boles & Lohmann 2003

27. Migrations in the SeaLong-Range Migrations III: Whales

28. Migrations in the SeaLong-Range Migrations III: Whales In sperm whales (Physeter catodon), only the males carry out the long-distance migrations. Females and juveniles remain in temperate or tropical latitudes all year long. homepage1.nifty.com/surara/ pbooks/kujira/sperm.jpg

29. Migrations in the SeaLong-Range Migrations III: Whales In humpbacks (Megaptera novaeangeliae), both sexes carry out the long-distance migrations. Because the northern and southern hemispheres have different seasons, the two hemispheres have populations that are mostly reproductively isolated. home.earthlink.net/~jimmrc/whale/ whalenews0102/w18.html

30. Migrations in the SeaLong-Range Migrations III: Whales In gray whales (Eschrichtius gibbosus), the migration occurs along the coastline from Alaska to Baja California, generally within sight of land. The animals “spy-hop” during the migration, perhaps to spot landmarks along the way.

31. Migrations in the SeaLong-Range Migrations IV: Sea Turtles Sea turtles (like the green turtle, Chelonia mydas, illustrated here) often nest on tiny, isolated islands (here, Ascension Island) or single beaches (photo, Heron Island, Great Barrier Reef). How do the adults find their way back to the beach? How do the nestlings make their way to the sea and eventually return “home”?

32. Migrations in the SeaLong-Range Migrations IV: Sea Turtles Emerging hatchlings (1) find their way to the water using visual cues (the location of a bright, open horizon), (2) continue offshore by swimming into approaching waves, and (3) eventually orient in the open ocean using geomagnetic cues.

33. Migrations in the SeaLong-Range Migrations IV: Sea Turtles1. Visual Cues The initial orienting cue is the sight of an open, typically bright horizon. Hatchlings will orient to a darker horizon if the bright one is elevated (as would occur on a moonlit night). However, in cases where the horizon is roughly equally flat in all directions, they run towards the brightest part. This is why artificial lighting is so destructive to sea turtles.

34. Migrations in the SeaLong-Range Migrations IV: Sea Turtles2. Wave Orientation Once the hatchlings reach the water, they orient by swimming into waves. Since most waves refract when they approach beaches so that they approach roughly perpendicular to the shore, wave travel direction is usually a reliable cue for the direction offshore when near shore.

35. Migrations in the SeaLong-Range Migrations IV: Sea Turtles3. Magnetic Orientation The final orienting cue is the earth’s geomagnetic field. Turtles have an internal “map” sense – they know what direction to swim from their current location to get to a given destination. The strength and direction of the earth’s field is used for this orientation.

36. Migrations in the SeaLong-Range Migrations IV: Sea Turtles3. Magnetic Orientation This figure illustrates the 2 components just mentioned (field strength and field direction) that together produce a “map” in the north Atlantic Ocean that provides a unique identification for each location. Turtles probably don’t “know” where they are in the sense that a human navigator would, but they know which way to swim to get to their destination.