Eee Review

7/31/2019 Eee Review

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Lo ng -distanc e n avigation in se a turtle s

K.J. L OHMANN 1 , J.T. H E S T E R 2 and C.M.F. L OHMANN 1

1 Departm en t of Bio logy, Un iv ers it y of N orth Carolin a, Ch ap el H ill, N orth Carolin a27599-3280, U.S.A. (E-mail address: [email protected])2 Departm en t of Bio m edical E n gin eerin g, Un iv ers it y of N orth Carolin a, Ch ap el H ill,

N orth Caro lin a 27 599 U.S .A.

R eceiv ed 31 March 19 98 , accep ted 21 May 19 98

Adult sea tur t les of several species m igrate across vast expanses of oceanto arr ive at specif ic nest ing areas and feeding si tes. Two hypotheses have beenproposed to account for th is remarkable naviga t ion . The f i r s t i s tha t chemicalcues emanating from target areas guide turt les to their dest inat ions. The secondis that turtles can approximate their position relative to target regions using fea-tures of the ear ths m agnetic f ield. Because an imals often rely on m ult iple cueswhile migrating, the two hypotheses are not mutually exclusive.

Satel l i te t racking experiments have revealed that migrat ing turt les oftenswim directly to distant goals, even when traveling perpendicularly to water cur-rents . Because animals usually change course frequently while seeking thesource of a chemical p lume, the cons is tency of headings cas ts doubt on thehypothesis that turt les fol low such plumes over great distances. Chemical cuesmay nevertheless play a role in enabling turtles to recognize a target area in thefinal stages of a long migration.

The magnetic navigation hypothesis is based on the f inding that hatchlingloggerhead turt les can detect two different features of the geomagnetic f ield(inclina t ion an gle an d inten si ty) tha t vary across th e earth s sur face. Hatchlingsfrom Florida, U.S.A., respond to magnetic features found along their migratoryroute by swimming in d i rec t ions tha t may he lp keep them safe ly wi th in theNorth Atlantic gyre, a circular warm-water current system favorable for growthand development. These results suggest that young turt les can derive posi t ionalinform at ion f rom fea tures of the ear ths f ie ld , and tha t such inform at ion m ayplay an imp ortant role in guiding tran s-oceanic migrat ions.

Adults might also exploit geomagnetic features in long-distance navigation.In p rinciple, turt les nest ing on coast lines might locate the a ppropr iate region byreturning to an area marked by the intersect ion of the shorel ine and a magneticisoline (e.g. , a part icular incl inat ion angle or intensi ty) . Turt les that migrate toremote is lands may be able to exploit bicoordinate magnetic maps for posi t ion-f inding , a l though secular var ia t ion and o ther fac tors may l imi t the condi t ionsunder which such a system can be used.

K EY W OR DS : s ea t u r t le s, Caretta caretta , Chelonia m ydas , orientat ion, navigation,chemical, olfactory, magnetic, magnetoreception, migration.

E th ology Eco logy & Evolu ti on 11: 1-23, 1999


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2 K.J. Loh m an n , J.T. H ester and C.M.F. Lohm an n

In troduct ion . . . . . . . . . . . . . . . . . 2Chem ica l cues and n aviga t ion . . . . . . . . . . . . 3Magn et ic n aviga t ion h ypoth esis . . . . . . . . . . . . 5Fu tu re direct ions . . . . . . . . . . . . . . . . 18Ackn owledgm ents . . . . . . . . . . . . . . . 19

Referen ces . . . . . . . . . . . . . . . . . 19

INTRODUCTION

Most sea turtles migrate intermittently throughout their lives. As hatchlings,the tur t les swim f rom the i r na ta l beaches in to the open ocean (F RICK 1976, S AL -MO N & W YNEKEN 1987), often taking refuge in circular current systems (gyres) thatserve as moving, open-sea nursery grounds (C ARR 1986, B OLTEN et al. 1998). As

ju ven iles, m an y take u p r esid en ce in coasta l a r eas bu t m igra te seaso n ally betwee nsummer and win te r hab i t a t s (M USICK & L IMPUS 1997). Finally, as adults, turtlesperiodically leave their feeding grounds and migrate to mating and nesting areas,af ter which many return to their individual feeding si tes (L IMPUS et al. 1992,M USICK & L IMPUS 1997). The itinerant lifestyle characteristic of sea turtles is thusinextr icably l inked to an abi l i ty to navigate accurately across large expanses of seemingly featureless ocean.

In some populat ions, migratory performance reaches extremes. The total dis-tances certain green turt les ( Chelonia m ydas ) and loggerheads ( Caretta caretta ) t ra-verse over the span of their lifetimes exceed tens of thousands of kilometers, sever-al t imes the diam eter of the tur t les hom e ocean basin (C ARR 1984, M ORTIMER &P ORTIER 1989, B OWEN et al. 1995). For examp le, green tu rtles tha t n est on AscensionIsland in th e South Atlant ic regularly m igrate between th eir n est ing beach and Bra-zilian feeding grounds, a straight-line distance of more than 2,000 km (C ARR 1975,1984). Even more impressively, loggerheads that hatch on Japanese beaches appar-ently traverse the entire Pacific Ocean to Baja California before returning to Japanto nest (B OWEN et al. 1995).

Researchers have long hypothes ized tha t adul t tur t les nes t on or near thesame beaches where they themselves emerged as hatchl ings (M ROSOVSKY 1983).Genetic analyses have now confirmed that the adults of at least some populat ionsdo indeed re turn to the i r na ta l reg ion for nes t ing af te r f i r s t migra t ing to d is tan t

oceanic areas (M EYLAN et al. 1990; B OWEN et a l. 1993, 1994, 1995).Sea turt les can also pinpoint small , isolated feeding areas. Loggerheads and

green turt les that nest along the Great Barrier Reef, for examp le, return af terward sto specific , widely dispersed feeding groun ds th at a re som etimes located h un dredsor thousands of ki lometers from their nest ing si tes (L IMPUS et al. 1992). Althoughthe feeding grounds of different individuals may l ie in nearly any direct ion fromthe nest ing region, adult tur t les show great f idel i ty to both their feeding and nest-ing areas and m igrate between them at a ppropr iate t im es.

Satellite tracking experiments have revealed that turtles can navigate to suchdistant sites with remarkable efficiency. Paths of migrating turtles often lead nearly

straight across the open sea to dest inat ions h und reds of kilometers away (B ALAZS etal. 1994, P API et al. 1995, P API & L USCHI 1996). Such unwavering courses seem toimply that turtles possess an awareness of their position, the location of the distantgoal , and the direct ional relat ionship between the two (P API & L USCHI 1996, L OH -MANN et a l. 1997).


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3Sea turtle navigation

For logist ical reasons, most s tudies on orientat ion and navigat ion in sea tur-t les have focused on hatchl ings rather than adults . Adults are powerful animalsthat often exceed one hundred ki lograms in weight; they are also diff icul t to keepin captivity, and migrate only intermittently. In contrast, hatchlings are small, sea-

sonally abundant , easy to manipulate in laboratory and f ield s tudies, and stronglymotivated to migrate offshore. In recent years , considerable progress has beenmade in characterizing the orientat ion cues that guide hatchl ings during their off-shore migration (reviewed by L OHMANN & L OHMANN 1996a, L OHMANN et al. 1997).

Relat ively l i t t le is known, however, about how adult tur t les navigate overlong distances or how they relocate their natal region for mating and nesting. Fornow, hypotheses of adult navigat ion are based primari ly on inferences fromstudies with hatchlings and juveniles, from analyses of migratory routes, and fromtheoretical considerations. In this paper we review and discuss two major hypoth-eses of long-distance navigat ion. The f irs t is that chemical cues emanating fromtarget areas guide turt les to their dest inat ions. The second is that tur t les canapproximate their global position and navigate to nesting and feeding areas usingfeatures of th e earth s m agnetic f ield. Because long-distan ce m igran ts frequen tlyuse multiple cues in navigation (A BLE 1991), the two hypotheses are not mutuallyexclusive.

CHE MICAL CUE S AND NAVIGATION

The discovery that chemical cues play a cr i t ical role in enabling salmon to

recognize the t r ibutaries in which they hatched (H ASLER & W ISBY 1951, H ASLER etal. 1978, H ASLER & S CHOLZ 1983, N ORTHCOTE 1984) prompted speculat ion that s imi-la r cues may be impor tant in sea tur t le naviga t ion . The chemica l impr in t inghypothesis for sea turt les proposes that ha tchl ings impr int on chemical cues uniqueto their natal beach and u se this inform ation as adults to return to tha t same beachfor nest ing and m ating (C ARR 1984, G RASSMAN 1993).

Relat ively l i t t le evidence has been obtained to ei ther support or refute thishypothesis. Behavioral experiments have revealed that sea turtles, l ike most aquaticanim als (C ARR 1988), can detect chemicals dissolved in water (M ANTON et al. 1972a,1972b; G RASSMAN & O WENS 1982). Whether such cues play a role in navigat ion or

natal beach recognition, however, remains to be determined.The spat ial scale over which chemical cues are proposed to funct ion is animpor tant cons idera t ion in an oceanic envi ronment where waves , cur rents , andeddies rapidly disrupt chemical gradients . Salmon, for example, appear to usechemica l cues only a t th e end of the i r m igra t ions wh en th e f ish h ave m oved in tocoastal waters an d dr awn close to the n atal r iver (H ASLER et al. 1978). Different, asyet unidentif ied cues are thought to guide salmon during the open-ocean phase of their m igrat ion (Q UINN 1984).

Some researchers , however, have hypothesized that sea turt les guide them-selves over hundreds or thousands of ki lometers of open sea by homing in on thesource of a par t icu lar odor p lume (K OC H et al. 1969, C ARR 1972). Others havespeculated that turtles, l ike salmon, may use chemical cues only to identify a finaltarget area af ter other cues have already brought the animals into close proximityof the goal (L OHMANN & L OHMANN 1996b). We will consider the two possibilitiesseparately.


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Chem osensory cues in lon g-distance navigation

In an a t tempt to expla in the remarkable migra t ion of green tur t les f rom thecoast of Brazil to Ascension Island, K OCH et al. (1969) hypothesized that green tur-

t les in Braz i lian waters d e tect a chemica l p lume th a t or ig ina tes a t the i s land andthen fol low i t across more than 2,000 km of ocean to i ts source. The putat ivechemica l markers would need to pers i s t in the sea wi thout degrading for a t leas tseveral weeks, and a suff icient gradient would need to exist so that tur t les in dis-tan t loca t ions could de tec t not only the chemica l but the d i rec t ion of increas ingconcentrat ion (C ARR 1972, 1984).

As the m igrator y paths of turt les have become bet ter ch aracterized, however,evidence against the use of such cues in long-distance navigat ion has begun toaccumulate. Satel l i te t racking experiments have revealed that tur t les often fol lowessentially straight paths to target sites hundreds of kilometers away (B ALAZS et al.1994, P API & L USCHI 1996, L USCHI et al. 1996), even when swimming directly acrosswater cur rents (P API et al . 1995). Because animals orient ing in a chemical plumeare seldom able to move directly to the source without employing a search strategythat involves frequent course changes (B AKER 1985, D USENBERY 1992), the consis-tency of the headings casts doubt on the hypothesis that turtles follow such plumesover great distances (P API et a l. 1995, P API & L USCHI 1996).

In addit ion, tur t les in many geographic areas appear to approach their nest-ing and feeding si tes from direct ions that are seemingly independent of currentdirect ion. For example, green turt les that nest at Tortuguero, Costa Rica, appar-ently converge on their nest ing si tes from feeding grounds that are both upcurrentand downcur ren t (C ARR 1984). The sam e app ears to be t r ue for Kem ps r idleys

( Lepidochelys kem pi ) that nest at Rancho Nuevo, Mexico (C ARR 1963), loggerheadsthat nest in the United States (M EYLAN et al. 1983) and in South Africa (H UGHES1995), and green turt les and loggerheads that nest along the Great Barrier Reef (L IMPUS et al. 1992). Oceanographic analyses have also suggested that currents atAscens ion Is land move eas tward dur ing the t ime when tur t les migra te to theisland from Brazi l (B ROWN 1990). If this is t rue, then an odor plume originat ingat the i s land would presumably move toward Afr ica and could not guide tur t lesapproaching from the west .

Chem ical cu es and recognition of the n atal beach region

Even if chem ical cues ar e not involved in long-distance na vigation, they m ightst i l l enable turt les to recognize a specif ic nest ing area af ter other navigat ionalmechanisms have brought the turtles into the vicinity. Some limited evidence existsto support this hypothesis, but results are not yet conclusive.

In one s tudy (G RASSMAN et al. 1984), Kem ps ridley tur tle eggs from Ran choNuevo, Mexico, were incubated in sand from Padre Island, Texas, U.S.A. Afteremerging f rom the i r eggs , ha tchl ings were permi t ted to c rawl across the PadreIs land beach and swim through the sur f . They were then recaptured and he ld incaptivi ty for 4 months, af ter which the turt les were tested in a water-f i l led arenaconsist ing of four compa rtm ents . One contained a solut ion m ade from Padre Is landsand and sea water, a second contained a s imilar solut ion made from sand and seawater from a d ifferen t location (Galveston, Texas, U.S.A.), and two ot hers conta inedun treated sea water. The t ime th at tur t les spent in each compar tm ent af ter entering


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was monitored, and resul ts indicated that tur t les spent s ignif icantly more t ime perentry in th e Padre Is land com partm ent than they spent in an y of the others .

Althou gh th ese results are su ggestive, all tur tles tested in th is initial stud y hadbeen imprinted to Padre Is land sand and water; no at tempt was made to test the

responses of tur t les tha t had been s imi lar ly impr in ted to water f rom anotherlocation. Thus, the possibility remained that turtles preferred Padre Island water tothe alternatives for reasons unrelated to early experience. A second experiment wastherefore car r ied out to de termine whether tur t les impr in ted to e i ther PadreIs land or Rancho Nuevo prefer red water f rom the i r respec t ive na ta l beaches(G RASSMAN & O WENS 1989). No such preferences could be discerned, but poorheal th of the turt les may have adversely affected their performance (G RASSMAN &O WENS 1989).

In an add it iona l expe r imen t , G RASSMAN & O WENS (1987) incubated green tur-tle eggs in sand that was scented with one of two chemicals (morpholine or 2-phen-ylethanol) that do not exist in the natural habitat. After the eggs hatched, each tur-t le was held for 3 months in water containing the same chemical to which the tur-t le had been exposed as an embr yo. After 2 a ddit ional mon ths without exposure toe i ther chemica l , the tur t les were tes ted in a compar tmenta l ized arena conta in ingsolutions of morpholine, 2-phenylethanol, and untreated sea water. Turtles that hadpreviously been exposed to morpholine preferred morpholine to 2-phenylethanol ,whereas the opp osite was tru e for turt les that h ad b een exposed to the 2-phenyleth-anol . Inter est ingly, however, addit iona l groups of tur t les that had been exposed tothe chem ica ls only whi le in th e nes t ( for a bout 2 m onths) or only af te r emergingfrom the nest ( i .e . , while l iving in the water of the holding tank for 3 months)failed to sh ow th ese preferences.

These resul ts provide addit ional evidence that tur t les can detect chemicalcues. Moreover, they demonstrate that , during at least certain developmental peri-ods, turtles can retain the ability to recognize a chemical for at least 2 months. Thesignificance of these findings, however, is not yet clear. Only turtles exposed to thechemica ls for about 5 months dura t ion (approximate ly 2 months in the nes t , fo l -lowed by 3 months in water ) acqui red the preference . Under na tura l condi t ions ,hatchl ings migrate beyond the waters of their n atal beach within a few hour s af teremerging f rom the i r nes ts (F RICK 1976, I RELAND et al. 1978). Thus, if exposure tothe chemical for 3 months af ter hatching is essential for the response to develop,then i t is diff icul t to envision how such a process could occur during the offshore

migration. Nevertheless, the initial results are intriguing, and additional studies areclearly n eeded.

MAGNETIC N AVIGATION H YPOTHE SIS

Hatchl ing sea tu r t les possess a m agnet ic compa ss sense tha t enables them toestablish and m ainta in cour ses relative to th e earth s m agnetic field (L OHMANN 1991;L IGHT et al. 1993; L OHMANN & L OHMANN 1993, 1994a; G OF F et al. 1998). For animalstha t m igrate long distances, the ear ths field provides not on ly a sou rce of directionalinform at ion , but a p otent ia l source of pos i t ional inform at ion as well (G OULD 1985,1998; W ILTSCHKO & W ILTSCHKO 1995). The possibility ther efore exists tha t tu rtles canappr oximate the i r pos i t ion wi th in the ocean , and the i r pos i t ion re la t ive to a goal,using geom agnetic field featu res (L OHMANN & L OHMANN 1994b, 1996b, 1998).


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Positional inform ation in the earths m agnetic field

Several featur es of the earth s f ield vary in a predictab le way across th e sur -face of the earth and might, in principle, be used in position-finding (S KILES 1985).

For example, at each location on the globe, the geomagnetic field lines intersect theear th s surface a t a specific an gle of inclinatio n (Fig. 1). Becau se inclinat ion a nglesvary with latitude, an animal able to distinguish between different field inclinationsm ight , in principle, determ ine i ts appr oximate lat itude.

In addi t ion to inc l ina t ion angle , a t leas t three o ther magnet ic parameterscould hypothet ical ly be used in assessing posi t ion (Fig. 1) . These include: (1) theintensity (strength) o f the tot al field; (2) the inten sity of the hor izontal field; (3) theintensi ty of the vert ical f ield. Addit ional magnetic features such as decl inat ionpotentially exist for an animal that can detect geographic north as well as magneticnor th (Q UINN 1984, G OULD 1985). For sea turtles, however, l imited visual abilitiesprobably preclude the use of s tar pat terns and other celest ial cues that might con-ceivably be used to determine geographic north (E HRENFELD & K OCH 1967).

Field parameters at a given locat ion are usual ly defined in terms of an incl i-nat ion angle and a total f ield intensi ty. Specifying any two of the four parameterslisted ab ove, however, defines a local field.

inclination

surface of the earth

angle

verticalcomponent

horizontal component

t o t a l f

i e l d

i n t e

n s i t y

Fig. 1. Left: Diagram of the ear ths m agnet ic field il lustr atin g how field lines (repr esented byarrows) intersect t he earth s surface, and how inclination angle (the an gle formed between the fieldlines and the earth) varies with latitude. At the magnetic equator (the curving line across the earth),field lines are pa rallel to the ear ths surface an d th e inclination an gle is 0 . An animal migrat ingnorth from the magnetic equator to the magnetic pole encounters progressively steeper inclinationangles along its journey. At the magnetic pole, field lines are directed straight down into the earthand the inclination angle is 90 .Right: Diagram illustrating four features of geomagnetic field vectors that might, in principle, pro-vide sea tur t les or other long-dis tance migrants with posi t ional information. The f ie ld present a teach location on earth can be described in terms of a total field intensity and an inclination angle.The total intensity of the field can be resolved into two vector components: the horizontal fieldintensity and the vertical field intensity. (Whether animals are able to resolve the total field intovector com ponent s, however, is not known).


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Migratory rou te of Florida loggerhead s

Hatchling loggerheads from the east coast of Florida, U.S.A., enter the seaand swim from their natal beach to the Gulf Stream current . This offshore migra-

t ion, however, is just the f i rs t s tep in a much longer t ransoceanic journey. Youngloggerheads evidently remain for at least several years in the North Atlant ic gyre,the c i rcu lar cur rent sys tem tha t enc i rc les the Sargasso Sea (C ARR 1986, H AYS &M ARSH 1997). During this time many cross to the eastern side of the Atlantic Ocean(B OLTEN et al. 1994, 1998) before returning to the vicinity of the southeastern Unit-ed States to take up residence in coastal feeding grounds (C ARR 1987, S EARS et al.1995, M USICK & L IMPUS 1997).

Young loggerheads in the open sea m ay benefi t f rom oriented m ovements thatserve to keep them within oceanic regions favorable for growth and development.For example, whereas the warm waters of the Gulf Stream provide a suitable envi-ronment for young tur t les , s t ray ing beyond the la t i tudina l ex t remes of the Nor thAtlant ic gyre can be fatal . As the northern edge of the gyre approaches Portugal ,the east-flowing curr ent divides. The n orthern bran ch continu es past Great Bri tainand the water temperature decreases rapidly. Loggerheads swept north in this cur-rent soon die from the cold (C ARR 1986, 1987; H AYS & M ARSH 1997). Similarly, tur-t les that venture south of the gyre r isk being swept into the south Atlant ic currentsystem and carried far from their normal range. An ability to recognize the latitudi-nal extremes of the gyre, and to respond by orient ing in an appropriate direct ion,might therefore have considerable adaptive value.

Detect ion of m agn etic in clin at ion an gle

The geomagnetic parameter most strongly correlated with latitude is field lineinclination (S KILES 1985). To determ ine if loggerheads can distinguish betw een dif-ferent inclination angles, hatchlings were tethered in a water-filled arena surround-ed by a computerized coil system (Fig. 2) that was used to generate earth-strengthfields with different inclinations (L OHMANN & L OHMANN 1994b). Hatchlings exposedto a f ield with an inclinat ion an gle foun d along the nor thern boun dary of the NorthAtlantic gyre swam south-southwest (Fig. 3). In contrast, hatchlings exposed to aninc l ina t ion angle found near the southern boundary of the gyre swam in a nor th-

easterly direction (Fig. 3). Tur tles exposed to inclina tion a ngles they do not nor m al-ly encounter ( i .e . , f rom north or south of the North Atlant ic gyre) , or to a f ieldinclinat ion found well within the n orthern and southern extrem es of the gyre, werenot significan tly oriented .

These resul ts dem onstrate that loggerheads can dist inguish b etween differentm agnetic inclinat ion an gles. In ad dit ion, inclinat ion an gles found near the n orthernand southern gyre boundaries el ici ted orientat ion that would, in each case, directturt les approximately toward the gyre center. The resul ts are therefore consistentwith the hypothesis that specif ic incl inat ion angles in effect warn turt les that theyhave reached the lat i tudinal extremes of the gyre and must swim toward the gyrecenter to avoid s t ray ing out of the warm-water cur rent sys tem (L OHMANN & L OH -MANN 1994b). For turtles that are safely within the gyre, drifting passively presum-ably poses no danger of displacement into undesirable areas. The absence of adirect ional preference amon g turt les exposed to an inclinat ion an gle found near thegyres latitudin al center is con sistent with this int erpr etation.


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Detect ion of m agn etic field in ten si ty

A second geomagnetic feature that varies across the surface of the earth isfield intensity. To determine if hatchling loggerheads can perceive differences in

intensity that they experience along their migratory route, hatchlings were exposed

Fig. 2. Diagram of the orientation arena, magnetic coil system, and data acquisition system usedin s tudies of hatchl ing responses to magnet ic f ie ld features (af ter L OHMANN & L OHMANN 1994b).Each hatchling was tethered to a rotatable lever-arm mounted on a digital encoder (located insidethe central post of the orientation arena). The lever arm tracked the direction toward which the tur-

tle swam; signals from the encoder were relayed to the data acquisition computer, which recordedthe or ientation of the turtle every 10 sec. The a rena was enclosed by a m agnetic coil system consist-ing of two different coi ls arra nged or th ogonal ly. One coi l control led th e horizonta l compon ent of the field while the oth er controlled the vertical com ponent .

Fig. 3. Orientation of hatchling loggerheads tested in magnetic fields of the same intensity butdifferent inclinations (data from L OHMANN & L OHMANN 1994b). Turtles exposed to a 60 inclinationangle (an an gle found n ear th e norther n edge of the North Atlantic gyre) were significantly orientedtoward the south-southwest, whereas those exposed to an inclination angle of 30 ( found near thesouthern border of the gyre) swam in a northeaster ly direct ion. Dashed l ines represent the 95%confidence interval for the mean bearing.


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to one of two intensi t ies that they normally encounter during their f i rs t months inthe sea (L OHMANN & L OHMANN 1996b). The incl inat ion angle of the f ield was heldconstan t in these tr ials. Tur tles tested in a field of 52,000 nT (a field 10.6% stron gerthan the natal beach f ield, and one that hatchl ings f i rs t encounter near South and

North Carolina, USA) swam eastward (Fig. 4). Those exposed to a 43,000 nT field(a f ield 8.5% weaker than the natal beach f ield, and one f irs t encountered on theeastern side of the Atlantic near Portugal) swam westward (Fig. 4).

These results demonstrate that hatchlings can distinguish between field inten-si t ies that occur in different locat ions along their migratory route. Moreover,because eas tward or ien ta t ion near South Carol ina and wes tward or ien ta t ion near

Fig. 4. Top: Generalized diagram of the North Atlantic gyre (after G ROSS 1977, C ARR 1986) indi-cating the only location within the gyre where the field intensity is 52,000 nT (marked by a) andthe locat ion where Flor ida loggerheads in the gyre presumably f i rs t encounter a f ie ld intensi ty of 43,000 nT (marked by b).Bottom : Orientation of h atchling loggerheads tested in a ma gnetic field of 52,000 nT (left) and 43,000nT (right). Conventions as in Fig. 3. Diagram s are m odified from L OHMANN & L OHMANN (1996b).


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the coast of Portugal would both function to keep young turtles within the gyre, theresults imply that turtles can derive positional information from geomagnetic fieldfeatures.

Secular variation and responses of hatchlings

In these experiments , hatchl ings responded to magnetic f ield features thatthey had never before encountered. The responses to such featur es therefore app earto be ful ly funct ional when the turt les f i rs t emerge from their nests . Indeed, thismay be essential because turt les swept out of the gyre usual ly die before they canregain entry (C ARR 1986, H AYS & M ARSH 1997). Thus, young turtles probably cannotlearn to recognize dangerous geographic areas because entering such regions is initself fatal.

Although hatchlings evidently respond to specific magnetic features, the fieldthat marks a given locat ion changes gradually over t ime (S KILES 1985). In light of this secular variat ion, how can hatchl ings respond appropriately to magnetic f ieldfeatur es that m ay differ s ignificantly from those tha t th eir ancestors encountered?

One possibi l i ty is that s trong select ive pressure acts to ensure a continuousmatch between the responses of hatchl ings and the f ield features that exist at anypoint in t im e. For exam ple, natur al select ion p resum ably rem oves from the popu la-t ion those young Florida loggerheads that s tray out of the gyre, while favoringthose with orientation responses that keep them safely inside. As the magnetic val-ues m arking th e gyre b oun daries chan ge, tur t les tha t fai l to respond correct ly tothe new field condit ions wil l be quickly el iminated and replaced by other turt les

with s l ight ly different responses that enhance the l ikel ihood of survival under thenew conditions. In this way, the responses of hatchlings may evolve rapidly to com-plement the continuously changing field.

Precedents exist for the rapid evolution of similar migratory adaptations. Forexample, monarch butterf l ies were introduced into Austral ia only about a centuryago but now have a migra t ion in which the t iming and d i rec t ion are a l te red by 6months and 180 relat ive to the North American populat ion from which they prob-ably descended (J AMES 1993, B ROWER 1996). Par t of the cent ra l Eu ropean p opula-t ion of a migratory bird, the blackcap Sylvia atricapilla , evolved a new migrat ionroute to the British Isles within only three decades (B ERTHOLD et al. 1992). In black-

caps, the direction of first migration appears to be encoded by at most a few genes(H ELBIG 1991, 1996), and the new route appears to be based on a novel, geneticallyprogrammed wes tnor thwester ly or ien ta t ion preference tha t i s spreading rapid lythrough the popula t ion (B ERTHOLD et al. 1992, H ELBIG 1996). These examples, andmany o thers (T ERRILL 1991, D INGLE 1996), highlight the evolutionary flexibility of migratory adaptat ions and the rapidi ty with which changes in orientat ion behaviorcan a rise.

N av igation in adu lt tu rtles

The movements of hatchl ings differ from those of adults in that the dest ina-t ion for young turt les is a large oceanic region rather than a relat ively restr ictednest ing or feeding area. Thus, al though hatchl ings appear to derive at least someposi t ional inform ation from the ear ths field, wheth er th ey can n avigate with th e


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same precision as adults is not known. Hatchlings might conceivably emerge fromtheir nests program m ed only to swim towar d specific direct ions in r esponse to par-t icular magnetic features found along the migratory route. For example, magneticparameters along the far northern border of the gyre might el ici t southward orien-

tat ion, whereas features along the southern border of the gyre might el ici t north-ward swimm ing. Thus, young tu rt les might r emain within a favorable gyre or oth eroceanic region without possessing the navigational abilities needed to locate specif-ic nesting and feeding areas.

Adult tur t les , however, can return to nest ing si tes fol lowing forced displace-ments (L USCHI et a l. 1996, P API et al. 1997). Moreover, adults often follow essentiallys t ra ight courses both d ay and n ight whi le migra t ing to spec if ic des t ina t ions h un -dreds of kilometers away (B ALAZS et al. 1994, P API et al. 1995, P API & L USCHI 1996).Such pr ecise tar geting of specific destinations over im m ense distan ces is difficult toexplain without hypothesizing an abi l i ty to determine geographic posi t ion relat iveto th e goal (G OULD 1985, P API et a l. 1995, P API & L USCHI 1996, L OHMANN et a l. 1997).

Although the nature of the sea turt le posi t ion-f inding system remains un-known, one hypothesis is that adult tur t les use geomagnetic f ield features such asincl inat ion and intensi ty to assess posi t ion during long-distance migrat ions (L OH -MANN & L OHMANN 1994b, 1996b; L OHMANN et al. 1997). Geomagnetic field featurescould potential ly be used by migrat ing adults in several different ways dependingon th e navigat ional task and the n atur e of the environm ent. Below we dra w on sev-eral examples to outl ine how turt les might , in principle, use incl inat ion and inten-sity to locate: (1) specific nesting regions along continental coastlines, and (2) iso-lated islan ds th at serve as rookeries.

Magn etic cu es as m ark ers of con tin en ta l n estin g beaches

Many m ajor sea turt le rookeries are located on continental coast lines that ar ealigned approximately north-south (e.g., Mexico, Costa Rica, the southeastern Unit-ed States, and Africa). For turtles that feed in shallow coastal areas along the samecontinent on which they nest , the problem of navigat ing from a feeding area to aspecif ic nest ing region may be reduced to one of swimming north or south along acoast l ine unti l the nest ing locat ion is reached and recognized. Thus, tur t les mightneed only to detect a single feature that varies latitudinally to discriminate between

different coa stal regions.In principle, the abi l i ty to detect ei ther incl inat ion angle or intensi ty couldallow turtles to identify a particular area of a continental beach. Inclination angle,in part icular, is s t rongly correlated with lat i tude; thus, for shorel ines runningapproximately north -south, each beach segm ent is m arked by a u nique an gle (L OH -MANN & L OHMANN 1994b).

Loggerhead turt les that nest in KwaZulu-Natal , South Africa, provide oneexam ple of a pop ulation t ha t m ight plausibly use such a str ategy. Most turtles tag-ged while nest ing in this area have been recovered at widely dispersed locat ionsalong the African east coast (H UGHES 1995), suggest ing that many adults in thispopulat ion u ndertake m igrat ions th at p aral lel the African coast l ine for h un dreds of kilometers. Four turtles tracked by satellite did indeed swim along the coast as theytraveled between their nesting beaches and feeding areas (P API et a l. 1997).

I f tur t les learn the inc lina t ion angle of the i r hom e beach as ha tchlings, anadult at tempting to return to the area might need only to swim along the African


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coast unt i l the appropriate angle is encountered (Fig. 5) . Such turt les might alsoassess whether th ey are north or south of the goal by determ ining if the incl inat ionangle is smaller or larger than that of the natal beach region. A similar processbased on other magnetic features that vary lat i tudinal ly (e .g. , total intensi ty, hori-

zontal field intensity, or vertical field intensity) could also hypothetically be used.

Islan d-fin din g an d bicoordin at e m agn etic m aps

Turt les that nest on small , remote is lands cannot fol low a coast l ine unti l theappropriate dest inat ion is reached. However, the abi l i ty to perceive two f ieldparameters, such as inclination and intensity, might provide turtles with the senso-ry abi l i t ies necessary to approximate posi t ion using a bicoordinate magnetic map(L OHMANN & L OHMANN 1996b). In most oceanic regions, isocl inics ( l ines of equalf ield incl inat ion) and isodynamics ( l ines of equal f ield intensi ty) vary in differentdirections. Thus, each area within an ocean is usually marked by a different combi-nat ion of magnetic featur es.

Fig. 5. Isoclinics along the African coast. Each region of the eastern coastline is marked by a dif-ferent inclination angle; a similar situation exists for the west coast. Adjacent isoclinics representdifferences in inclination of 2 , while dark lines are spaced 10 apart. Isoclinics were derived fromthe IGRF 1995 m odel (C AMPBELL 1997) for the year 1995.


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The migrat ion of green turt les from the Brazi l ian coast to Ascension Islandprovides an examp le of how a bicoordinate m agnetic map m ight p erm it navigat ionover a large oceanic region. Isoclinics and isodynamics form a nonorthogonal gridbetween South America and Africa, so that al l locat ions between feeding grounds

in Brazi l and nest ing beaches at Ascension Island are defined by unique combina-tions of inclination and intensity (L OHMANN & L OHMANN 1996b; Fig. 6). A migratingturt le using a bicoordinate map based on these two parameters might therefore beable to approximate i ts posi t ion anywhere along i ts route, provided i t had learnedthe magnetic features of Ascension and the gradients of inclination and intensity inthe South Atlantic.

A similar s i tuat ion exists at Tromelin Is land in the Indian Ocean (Fig. 7) .Green turt les tagged while nest ing at Tromelin have been recaptured in feedinggrounds a t var ious d is tan t i s lands and a long the coas t of Madagascar (H UGHES1995). Because green turt les show great f idel i ty to both feeding areas and nest ingsites (C ARR & C ARR 1972, L IMPUS et al . 1992), tur t les at Tromelin, l ike those atAscension, apparently migrate across hundreds of ki lometers of open sea to arr iveat a t iny, remote is land. The isocl inics and isodynamics in this region also form agrid that might , in principle, enable turt les to determine their posi t ion relat ive tothe goal (Fig. 7).

Although the Ascension and Tromelin Island examples are useful to illustratethe concept of a bicoordinate map, some elements of these maps cannot be gener-

Ascension

20

S

10

S

0

30

S

10

N

40 W W 0 10 E

50 W 30 W60 W 1020

W

Fig. 6. Isoclinics and isodynam ics in th e oceanic region surr ound ing Ascension Island. Isoclinicsin this region are aligned approximately northeast-southwest. Adjacent isoclinics represent differ-ences in incl inat ion of 2 . Isodynamics are a l igned approximately northwest-southeast and areshown in increments of 1 ,000 nT. The two geomagnet ic features form a non-orthogonal gr id thatmight, in principle, provide Ascension Island turtles with a bicoordinate position-finding system asthey migrate between Ascension and the Brazilian coast. Isoclinics and isodynamics were derivedfor the year 1995 from t he IGRF 1995 m odel (C AMPBELL 1997).


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alized to all locations. In p art icular, the an gle of intersection betw een isoclinics andisodynamics varies great ly between widely separated geographic areas. Thus,al though the two sets of isol ines are nearly perpendicular in parts of the southAtlantic (Fig. 6) and Indian Ocean (Fig. 7), this pattern is not universal; the inter-

sect ion angle is smaller in other oceanic regions such as the North Atlant ic andapproaches 0 (parallel isolines) in a few locations (L OHMANN & L OHMANN 1996b).Bicoordinate maps based on incl inat ion and intensi ty may therefore be of variableutility in different parts of the world, and indeed, might be exploited only by popu-lations that inhabit geographic regions with the most favorable grids.

Magnetic features could hypothet ical ly be exploi ted in several other ways(reviewed by W ILTSCHKO & W ILTSCHKO 1995, G OULD 1998). For example, fieldparameters might provide only one coordinate of a bicoordinate map that involvesa second, as yet unidentif ied, cue (P HILLIPS 1996). An interest ing navigat ionalmodel involving total field intensity and the direction of the intensity gradient hasalso recently been proposed (W ALKER 1998).

20

S

40

E 50

E 60

E 70

E

30

S

10

S

30

E

0

Tromelin

Fig. 7. Isoclinics and isodynamics in the Indian Ocean surrounding Tromelin Island. Isoclinicsrun approximately east-west in this region and are shown in 1 contours. Isodynamics run approxi-mately north-south and are represented in 1,000 nT increments. As is the case at Ascension, the twosets of isolines form a nonorthogonal grid that might, in principle, be used in position-finding. Iso-clinics and isodynam ics were derived for th e year 1995 from the IGRF 1995 m odel (C AMPBELL 1997).


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Magn etic im prin tin g hypoth esis

The nesting sites of sea turtles possess certain, specific attributes. For exam-ple , the beach must cons is t of sand ra ther than rock or mud, and the sand must

possess qual i t ies favorable for nest construct ion and egg incubation (M ORTIMER1990, H ENDRICKSON 1995). The area must be free of steep inclines, mangrove front-age, and other insur m ounta ble obstacles that block access from the sea (H ENDRICK -SO N 1958, M ORTIMER 1995). Appropriate temperatures for incubation and sex deter-mination are also required (A CKERMAN 1997), as are low densities of egg predators(M ORTIMER 1995) and c lose proximi ty to ocean currents tha t can he lp t ranspor thatchlings to suitable developmental habitats (M USICK & L IMPUS 1997).

Given th is suite of environ m enta l factor s, i t is clear th at n esting areas are creat -ed an d destr oyed rapid ly over evolution ary tim e. Cha nges in sea level and clima te, aswell as s torm s and erosion, quickly render favorable areas u nu sable and p roduce sui t-able sites wher e non e existed p reviously (H ENDRICKSON 1958, B OWEN et a l. 1989).

Because nest ing areas are ephemeral , posi t ional information specif ic to par-t icular s i tes is probably learn ed by turt les rather than inheri ted (B OWEN et al. 1989,B OWEN & AVISE 1995). If the cr i t ical information involves magnetic features, theninheritance is also effectively precluded by the gradual change in field parameters;the f ield that exists at a nest ing local i ty at any point in t ime usual ly differs fromthe f ield that existed there during earl ier generat ions. These considerat ions implythat i f tur t les do indeed rely on magnetic features to recognize the natal region,then each tur t le must learn the appropr ia te magnet ic fea tures dur ing i t s l i fe t ime(L OHMANN & L OHMANN 1994b, 1996b, 1998).

One possibi l i ty is that tur t les imprint on the magnetic features of their natal

beach as hatchl ings (L OHMANN & L OHMANN 1994b, 1996a). Such a process wouldenable each turt le to begin i ts journey with knowledge of the f ield features thatmarked i ts natal region at the t ime i t entered the sea. During i ts pelagic years aturt le might then learn how the various f ield parameters vary over a large oceanicregion, so that eventually, as an adult, the animal is able to assess its position rela-tive to its natal area.

Such magnetic imprinting, if i t occurs, may represent the first of several occa-sions when a turt le learns the magnetic features that mark a specif ic locat ion. Forexample, turtles might subsequently learn the features of feeding areas so that theycan return to such si tes af ter reproductive migrat ions. The f lexibi l i ty inherent in

such a system might also enable turt les to update their knowledge of the featuresin important areas each t ime they visi t so as to minimize navigat ional errors thatm ight otherwise accrue from secular variat ion (L OHMANN & L OHMANN 1998).

Secular variation an d n atal beach h om ing

If tur t les do indeed impr int on the m agnetic featur es of the na tal region, thenthe ch ange in th e geomagnetic f ield th at occur s du ring a turt les absence from thearea might cause naviga t ional e r rors dur ing re turn migra t ions (L OHMANN & L OH -MANN 1998). Whether secular change poses a significant obstacle to magnetic navi-ga t ion presumably depends on numerous fac tors , some of which vary grea t lybetween species, populations, and geographic regions. Among critical variables are:(1) the magnetic feature(s) used; (2) the way in which such features are exploited;(3) the nature of the nest ing area (e .g. , continental coast l ine or is land); (4) the


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length of time a turtle is gone from a region; (5) the rate of field change in the crit-ical area; (6) the navigational error represented by the change; (7) whether a turtlecan update i ts knowledge of magnetic features when i t returns to a s i te or region;(8) whether a turt le can est imate secular change or compensate for i t ; and (9) the

distance from which a tu rt le can locate the target area using nonm agnetic cues.At present, insufficient data exist to permit a reliable assessment for any situ-at ion. Analyses suggest , however, that the effects of secular change should beexpected to differ great ly depending on precisely how magnetic features are usedand on wh ether th e target areas are a long continental coast lines or on islands.

Continental nesting areas and secular change

For loggerheads and o ther spec ies tha t nes t predominant ly on coas t l ines ,potential effects of secular change may be mit igated by the tendency of turt les toreturn to na tal regions rath er th an to highly specific natal s i tes . Both th e pat tern of population genetics and the nesting locations of individual loggerheads suggest thatal though females return to nest within the general geographic region of their natalbeach, they may select nest sites anywhere within a considerable area (R ICHARDSON1982, B JORNDAL et a l. 1983, B OWEN & AVISE 1995, M ILLER 1997).

If hatchl ings learn th e ma gnetic environm ent of their hom e region in term s of a specific isoline intersecting the coast (Fig. 5), then the shoreline can function asone coordinate, so that drift in the critical feature results only in the perceived tar-get area moving sl ight ly along the coast in one direct ion or the other. Under suchconditions, the limited field change that typically occurs between the time a turtle

leaves an area and when it returns is unlikely to result in a navigational error thatdisplaces the animal beyond its natal region. Indeed, the effect of such drift may beinconsequential i f magnetic features near the home beach serve mainly as a land-mark to turt les indicat ing the general area in which to begin searching for ei ther:(i) any suitab le nesting site, or (ii) distinctive local cues th at perm it fine-scale local-ization of particular nesting locations.

Bicoordin at e m aps an d secu lar ch an ge

Secular variat ion may impose more signif icant constraints on the condit ionsunder which bicoordinate magnetic maps can be used (L OHMANN & L OHMANN 1998).In cases of island-finding (e.g., Figs 6-7), a turtle cannot exploit a coastline to re-duce the navigational task to one of detecting a single magnetic feature. Thus, theproblem of dr i f t i s magni f ied by the change in two fea tures ra ther than one , andthe gr id i s gradual ly d is tor ted over t ime so tha t the magnet ic coordina tes tha tinitially ma rked t he island m ove pr ogressively fart her away.

As a f i rs t s tep toward invest igat ing possible effects of secular variat ion onislan d-findin g, we exam ined h ow r ecent ch an ges in the earth s f ield at AscensionIsland and Trom elin Is land m ight affect at tem pts to locate each island u sing a m ag-net ic map. For our analysis we assumed that tur t les use a bicoordinate map basedon incl inat ion and intensi ty (e .g. , Figs 6 and 7) . We further assumed that : (1)search pat terns that might assis t in locat ing the is land are not used; (2) turt les areunable to compensate for secular change in any way; (3) navigation is based exclu-sively on the m agnetic map (no supplemental , nonm agnetic cues are used).


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Although each of these assumptions may be incorrect , the resul ts of thisworst-case analysis (Fig. 8) illustrate several points. First, considerable differ-ences exist between different geographic regions. The field at Ascension, for exam-ple, is presently changing more rapidly than the field at Tromelin. Second, the navi-

gat ional error that resul ts from secular change over a few years is not large, atleas t not in the context of t ransoceanic migra t ions tha t may span thousands of kilometers. Thus, a 2 or 3-year absence from a nesting area, as is probably typicalfor adult female green turt les (C ARR 1975, B JORNDAL et al. 1983, M ILLER 1997),would resul t in a navigat ional error of about 20-30 nautical miles (NM) at Ascen-sion; an identical absence from Tromelin would resul t in an error of only about5-10 NM. If adult males return every year to the region for mating, as the males of some popula t ions apparent ly do (M ILLER 1997) , then such tur t les may encountereven less drif t between visi ts (about 10 NM at Ascension and 3 NM at Tromelin) .We conclude that the f ield change presently occurring between successive migra-

0 5 10 150

25

50

75

100

125

150

Tromelin

Ascension

D i s t a n c e

f r o m

t a r g e t

( N M )

Fig. 8. Estimates of worst-case navigational error due to secular change at Ascension Island andTromelin Island. Potential error is graphed as a function of time away from each island; distancesare in nautical miles (1 NM = 1.852 km). The analysis assumes that turtles: (1) rely exclusively on abicoordinate map based on incl inat ion angle and total intensi ty; (2) are unable to compensate forsecular change; (3) do not use search strategies or any nonmagnetic cues to locate the island at theend of the migrat ion; and (4) re turn to the exact magnet ic coordinates that marked the is land thelast t ime the tur t le was there . To calculate error, we f i rs t mapped the magnet ic gr id that exis tedaround each island in 1995 (Figs 6-7) using the IGRF 1995 model (C AMPBELL 1997). We then usedthe model to determine the inclination and intensity that marked each island during each previousyear back to 1980. The magnetic coordinates (inclination and intensity) for each year were plottedon the 1995 magnet ic gr id map, and we then measured the dis tance between each set of coordi-nates and the position of the island. The error thus represents how far from the island the magneticcoordinates that marked the location at various times between 1980 and 1995 had drifted by 1995.For example, a female tur t le that nested at Ascension in 1992 and next re turned to the is land in1995 would miss the is land by about 25-30 NM if she returned to the magnet ic coordinates thatm arked t he island in 1992; a similar 3-year a bsence from Tromelin Island, however, would result inan error of only about 10 NM.


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tions of adult tur t les does not appear to pr eclude u sing magnetic grid m aps in n avi-gat ion, especial ly i f supplemental cues or search pat terns aid turt les in local izingthe is land at th e end of the m igrat ion.

Whereas the field change that occurs over 1-3 years may cause litt le difficulty

for adults once they begin making regular reproductive migrat ions, greater drif tm ay occur du ring th e period of a tur t les li fe tha t precedes i ts fi rs t retu rn to th enatal region. Little is known about the length of this interval, but it can be consid-erably less than the t ime to sexual maturi ty (S EARS et al. 1995). In addition, greatvariation probably exists between different populations and species (M USICK & L IM -PU S 1997), so that no general ized assessment can be made of the f ield change thatoccurs before a first return migration. For now, we can only conclude that if turtlesrely exclusively on bicoordinate maps, and if they cannot compensate for f ieldchange, then navigat ional errors wil l general ly increase with increasing periodsaway from the natal region (Fig. 8).

Under n atur al condit ions, however, a m agnetic map m ay fun ction a s only onepart of a repertoire of navigat ional mechanisms (S ALMON & W YNEKEN 1994). Thu s,diverse cues or behavioral s trategies might normally assis t tur t les in locat ing anis land a t the end of a migra t ion (C ARR 1984, L OHMANN et al. 1997). Among poten-tially useful cues are wave diffraction patterns around an island (L EWIS 1978), pher -omones f rom nes t ing or mat ing conspeci f ics (E HRENFELD & E HRENFELD 1973),chemical cues unique to a natal beach area (G RASSMAN et al. 1984), chemical cuessuch as dimethyl sulf ide that may signal nearby shal low water areas (T URNER &L ISS 1985, N EVITT et al . 1995), long-range visual landmarks such as mountains(C ARR 1984), and the sounds of waves breaking (M ROSOVSKY 1972, L USCHI et al .1996). Mechanisms involving interact ions with other turt les are also possible(O WENS et al . 1982), inasmuch as turt les that have navigated into the appropriateregion for the f i rs t t ime might encounter other members of the populat ion that aremigrating to the same goal; thus, following an experienced conspecific at the end of a m igrat ion could lead an inexperienced tu rt le to an appr opriate nest ing site (H E N -DRICKSON 1958). Search pa t terns ini t iated at th e end of a m igrat ion m ight also helpa turt le to locate an is land, just as searching behavior enables desert ants to over-come accumulated errors and locate a t iny nest entrance at the end of long forag-ing trips (W E H N E R & S RINIVASAN 1981).

We tentat ively conclude that , a t least under favorable condit ions, a turt leabsent for even a decade or more could plausibly use magnetic features to navigate

into the general vicini ty of an is land, close enough for local cues to permit f inallocal izat ion of the target . Once the is land has been located, such a turt le wouldpresumably need to update i t s knowledge of the magnet ic fea tures and regionalgrid in prepara t ion for i ts next m igrat ion.

FUTURE DIRECTIONS

Conducting experiments to test hypotheses of open-sea navigat ion in adultturtles will be challenging. The large size of adults precludes the relatively simplelaboratory manipulations that have proven successful with hatchlings. Field experi-ments a re poss ib le , ye t the des ign must take in to account the fac t tha t long-distance migrants often exploi t mult iple cues in orientat ion and navigat ion (A BLE1991, G OULD 1998). Thus, eliminating even a preferred source of information from


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the na tura l habi ta t may fa i l to d is rupt migra tory headings i f a l te rna t ive cues a reavailable (A BL E 1993). These potential pitfalls, along with the relative infrequencyof adult migrations and the large distances involved, pose significant logistical andexperimental obstacles.

Such difficulties notwithstanding, satellite tracking procedures now provide apossible avenue for experimen tat ion with a dults in the natu ral habitat (L USCHI et al.1996, M ORREALE et al. 1996, P API et al . 1997). The continuing ref inement of suchtracking may eventually permit rudimentary tests of navigational hypotheses in tur-t les and other m igratory anim als (N OWAK & B ERTHOLD 1991).

For now, experiments with hatchl ings and juveniles have provided a f i rs tgl impse into the sensory cues that adult tur t les may have at their disposal . Howadults navigate across vast expanses of seemingly featureless ocean, however,rem ains an endur ing mystery.

ACKNOWLEDGMENTS

We than k Mike Salm on, Jean ette Wyneken, Bil l I rwin, an d Lar isa Avens forassistance with our research and for their many helpful insights. We are also grate-ful to Wolfgang Wiltschko, Floriano Papi , and Kimberly Delemos for their com-ments on ear l ie r draf t s of the manuscr ip t . Our research has been suppor ted bygrants from the National Science Foundation (IBN 9120338 and IBN 9419993).

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