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First published online May 19, 2008
Journal of Experimental Biology 211, 1719-1728 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015792
Novel sensory modalities for navigation and other behaviours |
The sensory ecology of ocean navigation
Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA
* Author for correspondence (e-mail: klohmann{at}email.unc.edu)
Accepted 31 March 2008
Summary
How animals guide themselves across vast expanses of open ocean, sometimes to specific geographic areas, has remained an enduring mystery of behavioral biology. In this review we briefly contrast underwater oceanic navigation with terrestrial navigation and summarize the advantages and constraints of different approaches used to analyze animal navigation in the sea. In addition, we highlight studies and techniques that have begun to unravel the sensory cues that underlie navigation in sea turtles, salmon and other ocean migrants. Environmental signals of importance include geomagnetic, chemical and hydrodynamic cues, perhaps supplemented in some cases by celestial cues or other sources of information that remain to be discovered. An interesting similarity between sea turtles and salmon is that both have been hypothesized to complete long-distance reproductive migrations using navigational systems composed of two different suites of mechanisms that function sequentially over different spatial scales. The basic organization of navigation in these two groups of animals may be functionally similar, and perhaps also representative of other long-distance ocean navigators.
Key words: navigation, orientation, migration, magnetic, hydrodynamic, chemical, olfactory, sea turtle, fish, whale, salmon
Introduction
Considerable progress has been made in characterizing the mechanisms of
orientation and navigation used by diverse animals. Most work has focused on
terrestrial groups such as insects and birds, which are readily accessible and
provide favorable subjects for studies both in the field and in the laboratory
(reviewed by Wiltschko and Wiltschko,
1995
; Wiltschko and Wiltschko,
2003; Wehner et al.,
1996; Wehner,
1998; Åkesson and
Hedenström, 2007). Significantly less is known, however,
about how animals guide themselves over the 70% of the Earth's surface that is
covered by ocean.
Animals that migrate long distances through the sea, and especially pelagic species like sea turtles and cetaceans that travel across deep water, inhabit a sensory environment fundamentally different from that of the terrestrial world. Below the air–sea interface light diminishes rapidly with depth. The light field is transformed by absorption, scattering, refraction and the constant movement of waves across the ocean surface. Visual landmarks are absent and, except in unusually clear and calm water immediately below the surface, celestial cues such as the position of the sun and stars cannot be perceived.
At the same time, the marine environment provides animals with numerous
potential cues that do not exist on land. In many oceanic regions, waves
driven by steady winds propagate through the sea in seasonally constant
directions (Hogben and Lumb,
1967; Lohmann,
1992). Water pressure can convey information about depth
(Fraser and Macdonald, 1994).
Distinctive chemical cues emanating from estuaries provide salmon
(Dittman and Quinn, 1996), and
perhaps other animals, with markers of ecologically important locations. Sound
and electrical currents travel more readily through the sea than through air,
and some marine animals are adept at detecting each
(Harley et al., 2003;
Kalmijn, 1971). Clearly,
animals navigating through the ocean have access to a suite of navigational
cues which differs from that of their terrestrial counterparts.
A second difference between the terrestrial and open-ocean environment lies
in the degree to which animals can control their paths. Caribou migrating
across tundra, or insects crawling across the ground, can be reasonably
assured of moving in the same direction in which they walk. Even birds, which
can be blown off course by winds while migrating, can often mitigate drift by
maintaining visual contact with the ground and by landing when conditions are
adverse (Richardson, 1991;
Erni et al., 2002).
Circumstances differ for pelagic migrants. In the open sea, the movements of
animals are continuously susceptible to the influence of currents; animals
also lack stationary visual references against which drift can be gauged and
cannot opt out by grounding themselves.
This difference in the ability of terrestrial and pelagic animals to
control their paths has significant implications for navigation. On land, some
navigational strategies depend on an expectation that the direction and
distance traveled approximately reflect the direction and duration of an
animal's attempted movements; examples include the path integration of desert
ants (Wehner et al., 1996) and
the clock-and-compass orientation that guides many young birds during their
first migration (Wiltschko and Wiltschko,
2003). Such strategies are unlikely to be successful for migrants
in the open ocean, where swimming movements are permanently uncoupled from
solid substrate. For pelagic migrants traveling long distances to specific
target areas, navigational systems must therefore accommodate continuous drift
and correct for errors that will inevitably arise.
Although the study of long-distance navigation in ocean animals is still at an early stage, research has begun to provide insight into how a few species maintain consistent headings through the ocean and navigate to specific target areas. In this paper we highlight recent advances and emerging principles. Our examples are selective rather than exhaustive, and we focus primarily on sea turtles and salmon, two iconic long-distance ocean migrants whose navigational systems have been the subject of considerable study and speculation. We begin by briefly reviewing methods for studying ocean navigation, highlight three sets of environmental cues that ocean migrants are known to use, and conclude by suggesting that long-distance navigation in the sea is often (and perhaps always) accomplished through the sequential use of different suites of guidance mechanisms that operate over different spatial scales.
Studying ocean navigation
Three basic approaches can be used to study the navigation of ocean animals. First, behavioral studies can be conducted in the lab. Second, experiments can be carried out in the ocean. Finally, migratory routes can be analyzed for insight into navigational processes. Each of these approaches has a different set of advantages and limitations.
Laboratory experiments provide an opportunity to test hypotheses under
controlled conditions in which one variable at a time can be manipulated. This
approach has been particularly powerful in demonstrating the existence of
various guidance mechanisms and has been used successfully with hatchling sea
turtles (e.g. Lohmann and Lohmann,
1996a; Lohmann and Lohmann,
2003), immature fish (e.g.
Quinn, 1980;
Quinn and Brannon, 1982),
invertebrates (Rudloe and Herrnkind,
1980; Boles and Lohmann,
2003), and other small animals. One limitation is that such
experiments do not always reveal the circumstances under which each mechanism
is used in nature. For example, showing that an animal has a magnetic compass
does not by itself indicate where and when this ability is used.
Under favorable conditions, experiments conducted in the ocean can reveal
which sensory cues are used and when (e.g.
Lohmann and Lohmann, 1992;
Luschi et al., 2007). An
important caveat, however, is that numerous sources of directional and
positional information are always simultaneously present in the sea and many
animals switch among these when the need arises
(Able, 1993). Thus,
interpreting the results of field experiments can often be difficult. For
example, if covering the eyes of a migrating animal does not cause it to
change course, this does not necessarily imply that visual cues are not used;
it might mean only that alternative cues were available under the test
conditions.
The third method involves analyzing the tracks of animals. Satellite
telemetry has provided hundreds of tracks of marine animals migrating long
distances (e.g. Nichols et al.,
2000; Le Boeuf et al.,
2000; Bonfil et al.,
2005), and various attempts have been made to relate such tracks
to specific oceanographic, geophysical and topographic features.
Unfortunately, knowing the track of an animal is not the same as knowing how
the animal navigates; correlations alone are insufficient to demonstrate the
involvement of any particular cue (Fig.
1). Nevertheless, careful analyses of tracks can sometimes provide
ideas about potential navigational strategies that have not previously been
considered (e.g. Alerstam et al.,
2001).
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The minimal information needed by an animal to guide itself through the sea
depends largely on the nature and duration of the movement, the complexity of
the route, and whether there is a specific goal that the animal is trying to
reach. In some cases, orientation in a constant direction is sufficient. For
example, blue crabs scuttling from shallow water to the safety of deeper areas
(Nishimoto and Herrnkind,
1978) and hatchling sea turtles migrating from their natal beaches
to deep water (Lohmann and Lohmann,
1996a; Lohmann and Lohmann,
2003) move toward broad, offshore areas rather than toward
specific destinations. Under such conditions, all that is needed is a way to
maintain a consistent offshore heading.
In contrast, salmon returning from thousands of kilometers away to the
mouth of a specific river need more than a simple directional or compass
sense. Animals capable of homing to particular locations are often said to
possess both a map and a compass. According to this model, the map sense
enables the animal to determine its position relative to the goal (or at least
the direction in which it should travel), while the compass sense is used to
maintain a heading in the appropriate direction
(Kramer, 1961;
Able, 2001). In principle,
other ways also exist to locate distant targets. For example, animals might
search over a large area, or follow simple rules or algorithms that lead them
into the vicinity of a goal (e.g. swim west until a coastline is encountered;
swim south if the water temperature is cold).
Although numerous sources of directional and positional information are potentially available to long-distance migrants in the sea, recent work has highlighted the importance of three particular types of cue: geomagnetic, chemical and hydrodynamic. These three sources of information, perhaps supplemented in some cases by celestial cues, may provide the fundamental building blocks for much of the navigational repertoire of ocean migrants. We will briefly consider each in turn.
Magnetic maps and compasses
The Earth's magnetic field is a pervasive environmental feature that is
present throughout the day and night, remains unaffected by weather and
season, and exists in all parts of the ocean, from shallowest to deepest.
Animals can evidently extract at least two distinct types of information from
the geomagnetic field (Wiltschko and
Wiltschko, 1995; Johnsen and
Lohmann, 2005). The simplest of these is directional or compass
information, which enables an animal to maintain a consistent heading in a
particular direction such as north or south. The list of marine animals known
to possess magnetic compasses includes isopods
(Ugolini and Pezzani, 1995),
spiny lobsters (Lohmann et al.,
1995a), sea turtles (Lohmann,
1991; Lohmann and Lohmann,
1993), rays (Kalmijn,
1978) and salmon (Quinn,
1980; Quinn et al.,
1981).
In addition to providing a source of compass information, the Earth's field
also provides a potential source of positional or `map' information (reviewed
by Lohmann et al., 2007).
Several geomagnetic elements vary in a predictable way across the surface of
the Earth and might, in principle, be used to assess geographic location
(Fig. 2). For example, at each
location on the globe, the magnetic field lines intersect the Earth's surface
at a specific inclination angle. At the magnetic equator, the field lines are
parallel to the Earth's surface, but become progressively steeper as one moves
toward the magnetic poles. Thus, inclination angle varies predictably with
latitude, and an animal able to detect this field element may be able to
determine whether it is north or south of a particular area. Similarly, the
intensity of the total field, or the intensity of the horizontal and vertical
field components, might also hypothetically be used in position finding. For
animals that can perceive the direction of true geographic north (for example,
by using star patterns to determine the location of the north pole), still
other magnetic parameters such as declination (the difference between true
north and magnetic north) are potentially available.
|
Hatchling loggerhead turtles (Caretta caretta) detect both
magnetic inclination angle (Lohmann and
Lohmann, 1994) and field intensity
(Lohmann and Lohmann, 1996b).
Furthermore, when hatchlings were subjected to magnetic fields that exist at
three widely separated locations along their open-sea migratory pathway, they
responded by swimming in directions that would, in each case, facilitate
movement along the migratory route (Fig.
3) (Lohmann et al.,
2001). These results imply that young turtles have a `magnetic
map' in which regional magnetic fields function as navigational markers and
elicit changes in swimming direction at appropriate geographic locations
(Lohmann et al., 2007).
Moreover, these responses appear to be inherited, inasmuch as the hatchlings
tested had never been in the ocean.
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;
Lohmann et al., 2007). In one
experiment, juvenile green turtles (Chelonia mydas) were captured in
feeding grounds along the Florida coast, placed in an orientation arena, and
exposed to magnetic fields that exist at locations approximately 340 km north
or south of the capture site (Lohmann et
al., 2004). Turtles exposed to the field from the northern area
swam south, whereas those exposed to the field from the southern location swam
north (Fig. 4). Thus, turtles
swam in directions that would have led them home had they actually been
displaced to the locations where the two fields exist.
|
;
Lohmann, 2007). These results
imply that adult turtles use a magnetic map, a magnetic compass, or both while
navigating to their nesting grounds.
The possibility that salmon and other fish possess magnetic maps has been
discussed by several authors including Quinn
(Quinn, 1984) and Walker and
colleagues (Walker et al.,
1997). Walker and colleagues
(Walker et al., 1997)
conditioned rainbow trout (Oncorhynchus mykiss) to respond to
magnetic fields imposed on them in the laboratory, confirming magnetic
sensitivity in this species. However, because the magnetic stimulus altered
the intensity, inclination, direction, and gradient of the field
simultaneously, the precise element or elements of the field detected by the
fish could not be determined.
In a different experiment, four chum salmon (Oncorhynchus keta)
were tracked as they swam through the sea near the coast of Japan for a period
of hours while the magnetic field around them was intermittently disrupted
(Yano et al., 1997). No
obvious change in orientation behavior was observed when the magnetic field
was altered. However, as noted previously (see `Studying ocean navigation'),
interpreting experimental results can be difficult when animals are deprived
of one type of cue but are tested in the ocean where numerous alternative cues
exist. Although the findings of Yano et al.
(Yano et al., 1997) have been
interpreted by some as evidence against magnetic maps in salmon (e.g.
Døving and Stabell,
2003), others consider the results to be inconclusive (e.g.
Walker et al., 2003).
Use of magnetic anomalies?
In some oceanic regions, rocks rich in magnetic minerals produce local
magnetic anomalies (Skiles,
1985). Such anomalies are typically small (<1% of the total
field at the surface of the ocean)
(McElhinny and McFadden,
1999), but in principle might disrupt the field sufficiently to
impair the navigation of animals using magnetic maps. On the other hand, the
difficulty might be easily solved, given that a fast-moving animal may pass
rapidly through such areas just by maintaining a consistent heading for a
short time (Lohmann and Lohmann,
1996b; Lohmann et al.,
2007).
Although magnetic anomalies have often been viewed as potential problems
for magnetically sensitive species
(Walcott, 1978), an
interesting possibility is that anomalies might sometimes serve as useful
markers. For example, many islands and seamounts generate significant
anomalies, which might hypothetically provide a useful signal to animals
searching for such locations. Interestingly, analysis of hammerhead shark
movements near seamounts has led to the suggestion that this species might
sometimes follow features of the local magnetic topography
(Klimley, 1993).
An unusual pattern of magnetic anomalies exists on the ocean bottom in
seafloor-spreading zones (areas where continental plates diverge). As the
plates move apart, molten material continually seeps out along the ocean floor
and, as it cools, acquires magnetization parallel to the direction of the
Earth's field. Because the polarity of the Earth's field has reversed at
irregular intervals over geologic time, stripes of ocean floor formed during
periods of opposite geomagnetic polarity are magnetized in opposite directions
(Skiles, 1985;
McElhinny and McFadden, 1999).
The magnetic signal of each stripe either adds to the local geomagnetic field,
enhancing the total field slightly (creating magnetic maxima), or opposes the
present Earth's field (resulting in magnetic minima).
Analyses have suggested that whales tend to be found along these magnetic
pathways more often than should occur by chance
(Walker et al., 1992) and that
whales in some geographic areas tend to become stranded where magnetic minima
pathways intersect land (Kirschvink et
al., 1986). One interpretation is that whales follow these weak
magnetic pathways as they migrate
(Kirschvink et al., 1986). If
so, the benefits of this strategy relative to other methods of navigation are
not immediately apparent (Wiltschko and
Wiltschko, 1995).
Chemical cues and navigation
Numerous marine species have well-developed chemical senses that facilitate
the detection of food sources over relatively small spatial scales, which
often range from centimeters to tens of meters (e.g.
Carr, 1988;
Weissburg and Dusenbery, 2002;
Wyeth et al., 2006). In at
least a few cases, however, long-distance migrants have evolved the ability to
exploit chemical signals in navigation.
Salmon are the iconic example. Although tremendous variation exists in the
life history and migratory patterns of salmon, all hatch in rivers and
streams; the young of some species and populations subsequently enter the
ocean and disperse across hundreds or thousands of kilometers of open sea
(Fig. 5)
(Dittman and Quinn, 1996;
Quinn, 2005). Several years
later, as adults, the fish use chemical cues to help locate their natal rivers
once they have arrived in the general vicinity of the river mouth; such cues
also help guide salmon up the correct branches of rivers as they migrate to
their spawning grounds (Johnsen,
1982; Johnsen and Hasler,
1980; Døving et al.,
1985; Dittman and Quinn,
1996). That the salmon actually imprint on the chemical cues of
their natal rivers and streams has been demonstrated through experiments in
which young fish were exposed to specific chemicals during development and
subsequently released to undergo their normal migrations. These artificially
imprinted salmon returned to breed in streams that had been scented with the
imprinting chemical (e.g. Hasler and
Scholtz, 1983; Dittman et al.,
1996; Nevitt and Dittman,
1998).
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As salmon complete the ocean phase of their migration and draw close to the
mouths of their natal rivers, they often enter estuaries, fjords, or other
coastal environments where masses of fresh water encounter seawater. In such
areas, the water column sometimes contains multiple layers that remain
vertically stratified due to density differences
(Døving et al., 1985;
Dusenbery, 1992;
Moore and Crimaldi, 2004).
Salmon move vertically through these layers and, by doing so, may sample
differences in chemical cues in the different water masses
(Døving et al., 1985).
It has been proposed, but not yet demonstrated, that salmon can also detect
the relative movements of neighboring layers of water and thus infer the
direction in which each water mass is moving
(Døving and Stabell,
2003).
Stratified water masses might transport chemical cues from rivers over
considerable distances in fjords and other favorable settings where limited
vertical mixing occurs. However, such cues cannot persist and extend across
more than a thousand kilometers of ocean, the distances over which some
populations of salmon are known to migrate
(Dittman and Quinn, 1996). For
this reason, most authors have concluded that salmon navigation in the open
sea is likely to involve a different suite of mechanisms that are not
olfactory (e.g. Hasler, 1971;
Quinn, 1990;
Quinn, 2005;
Dittman and Quinn, 1996;
Yano et al., 1997;
Hinch et al., 2006). The
nature of the open-ocean navigation system in salmon, although subject to much
speculation, remains unknown.
Hydrodynamic cues: wave direction
Ocean waves are ubiquitous in the open-sea environment and also along exposed continental coastlines. In such coastal areas, wave direction typically provides a reliable indicator of the offshore direction because of wave refraction. As waves approach a coast from the open sea, the leading edge of a wave encounters the ocean bottom first, slowing its forward progress and providing the remainder of the wave crest with an opportunity to catch up. Eventually, the wave approaches the beach directly (i.e. the wave crest is approximately parallel to the shore while moving toward it).
Hatchling sea turtles emerge from underground nests on sandy oceanic
beaches, scramble into the sea, and migrate offshore. By swimming into
refracted waves, hatchlings launching from the beach can quickly establish
courses toward the open sea (Lohmann and
Lohmann, 1996a; Lohmann and
Lohmann, 2003). Both laboratory
(Lohmann et al., 1990;
Wyneken et al., 1990) and
field experiments (Salmon and Lohmann,
1989; Lohmann et al.,
1990; Lohmann and Lohmann,
1992) have demonstrated that hatchlings swim into waves.
Additional experiments have demonstrated that hatchlings detect the direction
of waves by monitoring the sequence of accelerations that occur within wave
orbits below the water's surface (Lohmann
et al., 1995b). For example, a turtle facing into oncoming waves
is accelerated upward, backward, downward and then forward with each wave
cycle, whereas a turtle oriented in the direction of wave movement is
accelerated upward, forward, downward and then backward
(Fig. 6).
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)
and arthropods (Nishimoto and Herrnkind,
1978; Rudloe and Herrnkind,
1980), orient to waves or to wave surge. Salmon have been
hypothesized to detect and use waves in much the same way that turtles do
(Cook, 1984), although
experimental confirmation is lacking. An interesting possibility is that
marine mammals might also exploit such cues. Seals can detect slight
fish-generated water movements (Dehnhardt
et al., 2001), so an ability to perceive water movements
associated with waves appears plausible.
In some oceanic areas, winds sweep steadily over large expanses of open
water and generate waves with long periods and wavelengths, which are known as
swells (Bascom, 1980;
Bearman, 1989). Because
seasonal wind patterns are often relatively constant, the direction of ocean
swells is also often seasonally consistent and might, in principle, be used as
a directional cue by open-sea migrants
(Cook, 1984;
Lohmann, 1992). To migrate in
different directions, such animals would presumably need to swim at fixed
angles relative to waves rather than orienting directly into them as hatchling
turtles do. Whether any animal has such a `wave compass' is not known, but
hatchling turtles do have the minimal sensory abilities required, inasmuch as
they can distinguish among waves approaching from different angles
(Lohmann et al., 1995b). Thus,
an interesting speculation is that the tendency of hatchlings to swim directly
into waves is supplanted in juvenile and adult turtles by a more versatile
ability to use waves as a reference for maintaining any course.
Information in ocean waves might also be used to locate targets in some
cases. For example, waves are refracted as they pass around islands, creating
characteristic interference patterns on the leeward side
(Fig. 7). Traditional
Polynesian navigators used such wave patterns to detect the presence of
islands too far away to be seen (Lewis,
1978); turtles or other marine animals might do the same. Although
no direct evidence for this ability presently exists in animals, a finding of
potential interest is that female green turtles captured while nesting on an
island and displaced to the leeward side returned more rapidly to the nesting
area than turtles displaced an equivalent distance on the windward side
(Hays et al., 2003). These
results were interpreted initially as evidence that turtles detect windborne
odors, but an alternative possibility is that the turtles perceived a change
in wave patterns on the downwind (and downwave) side of the island
(Fig. 7)
(Lohmann et al., 2008).
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Numerous animals use water currents as a directional cue when crawling
short distances or swimming in shallow water. For example, sea slugs
(Wyeth et al., 2006), crabs
(Weissburg and Dusenbery,
2002) and lobsters (Horner et
al., 2004) crawl into water currents in response to chemical cues
from prey or potential mates, a response that leads them toward the source of
the odor. These animals are thought to monitor current direction by
maintaining contact with the substrate, either directly or visually
(Dusenbery, 1992). Open-sea
migrants, however, lack these stationary reference points and thus are
probably unable to use oceanographic currents as directional references.
Indeed, analyses of tracks of sea turtles have indicated that, when turtles
encounter currents, they do not alter their movements to preserve the original
direction of travel; instead currents typically deflect turtles away from
their original courses (Girard et al.,
2006; Luschi et al.,
2007).
Other cues
Although celestial cues are used in orientation and navigation by diverse
terrestrial animals (e.g. Wehner et al.,
1996; Wiltschko and Wiltschko,
2003; Åkesson and
Hedenström, 2007), few studies have investigated these
mechanisms in marine species. To our knowledge, no evidence exists for a star
compass in any ocean migrant. However, at least a few marine animals are
thought to exploit skylight polarization patterns, a sun compass, or both
(Quinn, 1980;
Quinn, 1982;
Avens and Lohmann, 2003). Such
cues are presumably available only to animals that swim at or near the
air–water interface. The ability of whales to produce sounds that travel
long distances, and that might potentially reflect off distant land masses,
also provides the basis for interesting speculation, but the logistical
obstacles to investigating such a possibility are formidable.
Natal homing and biphasic navigation
Despite their phylogenetic differences, sea turtles and salmon have both
evolved the ability to exploit disparate, widely separated habitats at
different times of their lives. Great diversity exists in the life histories
of different populations and species of both groups
(Groot and Margolis, 1991;
Buskirk and Crowder, 1994;
Lutz and Musick, 1997;
Quinn, 2005); thus, no general
description accurately portrays all members (and indeed, some non-migratory
species and populations exist in each case). Nevertheless, some interesting
parallels exist among the salmon and sea turtles that undergo the longest
oceanic migrations.
The salmon of interest in this context are those that enter the sea from
their natal streams and rivers and disperse across hundreds or thousands of
kilometers of offshore waters before returning several years later to their
natal tributaries to spawn (Dittman and
Quinn, 1996; Quinn,
2005). In the Pacific northwest, this description applies to some
populations of sockeye salmon (Oncorhynchus nerka), chinook salmon
(O. tshawytscha) and chum salmon (O. keta), among others.
Natal homing is very precise in that the vast majority of these fish return to
their river of origin and often to a particular river branch
(Quinn et al., 1999;
Quinn, 2005).
Sea turtles of most species migrate intermittently throughout their lives.
As hatchlings, turtles migrate offshore; as they grow, many follow complex,
population-specific migratory pathways that sometimes lead across entire ocean
basins and back (Lutz and Musick,
1997). Older juveniles of some species, such as loggerheads and
green turtles, eventually leave the open-ocean environment and take up
residence in neritic feeding grounds, sometimes migrating seasonally between
summer and winter habitats. As adults, turtles of nearly all species migrate
intermittently from their feeding grounds to specific mating and nesting areas
and back again. Genetic analyses have confirmed that the adults of many (and
perhaps most) populations return to their natal region for nesting
(Meylan et al., 1990;
Bowen et al., 1993;
Bowen et al., 1994;
Bowen et al., 1995). Although
some populations demonstrate exceedingly precise natal homing, others may only
home to regions of coastline several hundred kilometers in length
(Bjorndal et al., 1983;
Peare and Parker, 1996;
Lee et al., 2007); at a
minimum, natal homing is regional in nature
(Bowen and Avise, 1995;
Miller, 1997).
Although sea turtles and salmon have been investigated independently and
through somewhat different means, an interesting similarity has emerged: both
have been hypothesized to complete long-distance reproductive migrations using
navigational systems composed of two different suites of mechanisms that
function sequentially over different spatial scales
(Quinn, 2005;
Lohmann et al., 2008). In each
case, the first navigational system is thought to guide the animals across
large expanses of ocean and bring them into the general vicinity of the target
area. The second system is then thought to supplant the first and lead animals
to their final destination (the correct branch of a river for salmon and a
nesting area for sea turtles).
If this view is correct, then what is the basis of the dual navigational
systems in each of these groups of animals? In turtles, direct experimental
evidence for a magnetic map sense has been acquired
(Fig. 4)
(Lohmann et al., 2004) and
this mechanism might plausibly guide turtles over hundreds or thousands of
kilometers into the general vicinity of a nesting beach
(Lohmann et al., 1999;
Luschi et al., 2007). However,
the existence of magnetic anomalies, and the fact that the Earth's field
changes gradually over time, are likely to make the resolution of such a map
too imprecise to guide turtles to highly specific nesting areas
(Lohmann et al., 1999;
Lohmann et al., 2008). Thus,
the involvement of additional local cues must be hypothesized once a turtle
reaches the vicinity of its target (e.g.
Lohmann et al., 1999;
Hays et al., 2003;
Lohmann et al., 2008).
The situation with salmon differs from that of sea turtles in that it is
the second navigation system that is well characterized and the first that is
enigmatic. Much is known about how salmon use chemical cues to pinpoint their
natal rivers once they are near, but how they navigate into the correct
vicinity from hundreds of kilometers away remains a matter of speculation.
Techniques developed for studying navigation in sea turtles under laboratory
conditions (e.g. Lohmann et al.,
2001; Lohmann et al.,
2004) might provide a possible approach for gaining insight into
how salmon guide themselves in the open sea.
Given our present understanding, it seems possible that the navigational systems of sea turtles and salmon are more alike than different. Salmon might rely on a magnetic map like that of turtles to navigate into the vicinity of their natal rivers, close enough for chemical cues to be detected; sea turtles might use olfactory cues in the final stages of returning to their natal beaches. Both animals might use hydrodynamic cues (waves) as an orientation cue under appropriate conditions. If so, the basic navigational processes in these two seemingly different long-distance migrants might be very similar, and perhaps representative of other long-distance ocean navigators as well. Many additional studies will be needed to determine whether different migrants do indeed use similar navigational mechanisms and strategies, or whether each has evolved a different method of finding its way in the sea.
Acknowledgments
We thank Nathan Putman and Sönke Johnsen for helpful discussions. The research was supported in part by grants from the National Science Foundation (IOB-0344387 and IOS-0718991) to K.J.L. and C.M.F.L.
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