Marine Biology (2006) 149: 1567–1576 DOI 10.1007/s00227-006-0308-2

RESEARCH ARTICLE

Heather M. Lamson · Jen-Chieh Shiao · Yoshiyuki Iizuka Wann-Nian Tzeng · David K. Cairns

Movement patterns of American eels (Anguilla rostrata) between salt- and freshwater in a coastal watershed, based on otolith microchemistry

Received: 5 August 2005 / Accepted: 15 March 2006 / Published online: 8 April 2006© Springer-Verlag 2006

Abstract Otolith strontium:calcium ratios were used totrace lifetime movements of American eels (Anguillarostrata) captured in salt-water bays and adjoining fresh-water ponds in Prince Edward Island, Canada. Eels wereclassiWed into migratory contingents based on theirmovement patterns. A pond with a pool-and-weir salmo-nid Wshway and a pond drained by a low-gradient chan-nel contained eels that had entered freshwater at all ages,but a pond with a 2.2 m vertical spillway contained onlyeels that had entered freshwater in the elver year. Salt-water residents were the dominant migratory contingentin salt-water bays (85% of 39), which overturns the para-digm of obligate catadromy for this species. Freshwaterresidency was the sole pattern found in the pond with thevertical spillway (100% of 12) and the majority contin-gent in the pond with the low-gradient channel (54% of24). Inter-habitat shifting was the dominant migratorycontingent in eels sampled from the pond with the pool-and-weir Wshway (85% of 20). Resident eels were estab-lished in salt- and freshwater habitats by the year after

their arrival in continental waters. Eels that shiftedbetween habitats increased their rate of inter-habitatshifting with age. The high degree of plasticity in habitatuse found in this study is consistent with worldwideAnguillid patterns as revealed by Sr:Ca.

Introduction

Anguillid eels are viewed as textbook catadromous spe-cies, spawning in the open sea, migrating to freshwaterhabitats to rear, and returning to the ocean to completetheir life cycle. There is, however, great variability in con-tinental habitat use, and anguillid eels in continentalwaters may be found in habitats ranging from full-strength salt-water to freshwater (Morrison et al. 2003;Daverat et al. 2004).

Analysis of strontium:calcium ratios of eel otolithshas greatly expanded our knowledge of eel movementpatterns, showing that some eels settle and remain in salt,brackish, or freshwater during their continental lives,while others shift among these habitats (Morrison et al.2003; Tzeng et al. 1997, 2000; Tsukamoto and Arai2001). In European (Anguilla anguilla) and Japanese(Anguilla japonica) eels, Sr:Ca data have revealed thatsome eels spend their entire lives in salt-water (Tsukam-oto et al. 1998; Arai et al. 2003). These species can thusno longer be regarded as obligate catadromous Wsh, butinstead use catadromy as a facultative life history option.

Sr:Ca studies on American eels (Anguilla rostrata) atthree locations have shown a variety of inter-habitatmovement patterns. However, none of these investiga-tions has sampled eels in full-strength salt-water. Ameri-can eels are commonly found in continental salt-waterduring their yellow (growth) phase, but it has not beendemonstrated that American eels can complete their lifecycles in the marine environment.

Secor (1999) noted that estuarine and diadromousWshes commonly exhibit varying movement patternsamong salt, brackish, and freshwater. He termed thesegroups “migratory contingents.” Tosi et al. (1988) and

Communicated by R.J. Thompson, St. John´s

H. M. LamsonBiology Department, University of New Brunswick, Fredericton, NB E3B 6E1, Canada

J. C. ShiaoInstitute of Zoology, Academia Sinica, Nankang, Taipei 11529, Taiwan, ROC

Y. IizukaInstitute of Earth Sciences, Academia Sinica, Nankang, Taipei, 11529, Taiwan, ROC

W. N. TzengInstitute of Fisheries Sciences, National Taiwan University, Taipei 10617, Taiwan, ROC

D. K. Cairns (&)Department of Fisheries and Oceans, Box 1236, Charlottetown, PE C1A 7M8, CanadaE-mail: cairnsd@dfo-mpo.gc.caTel.: +1-902-5667825Fax: +1-902-5667948

1568

Édeline and Élie (2004) found that glass eels sampledfrom marine waters showed distinct salinity preferencesin laboratory trials, some choosing salt-water while oth-ers preferred fresh. This implies that membership inmigratory contingents may be determined before arrivalat the coast. Eels which attempt to ascend rivers mayencounter natural or artiWcial obstacles. Eels under10 cm long are able to creep up wet vertical surfaces(Legault 1988). Hence dams or waterfalls where watertrickles down vertical walls may impose an age-depen-dent barrier to migration, with upstream movement pos-sible only for young eels (Cairns et al. 2004).

We used the Sr:Ca technique to investigate the ontog-eny, frequency, and directions of American eel move-ments between salt- and freshwater in a small watershedin eastern Canada. To permit the examination of eVectsof obstacle type on movement patterns, we chose a studyarea consisting of salt-water bays and adjacent freshwa-ter ponds which were formed by dams of three diVerenttypes: earthen dam with a vertical spillway, concrete damwith a salmonid Wsh ladder, and earthen dam with a low-gradient outlet channel. Patterns of movement betweensalinity zones, as indicated by Sr:Ca proWles, are used totest the following predictions:

1. Ponds formed by dams with vertical water drops (sal-monid Wsh ladder, vertical spillway) will contain onlyeels that entered at a small size, but the pond drainedby a low-gradient channel will contain eels thatentered at all sizes.

2. Eels will show a variety of migratory contingents,including residence in salt-water, residence in freshwa-ter, and movements between these habitats.

3. Some eels will show salt-water residence only, indicat-ing an exclusively marine life cycle.

4. Eels choose their migratory contingents upon arrivalin continental waters, so that colonization of salt-water and of adjacent freshwater ponds occurs simul-taneously or nearly so.

Methods

This study was conducted on the north shore of PrinceEdward Island in Brackley and Covehead Bays and asso-ciated ponds (Fig. 1). Both bays have full-strength salt-water (>28 ppt) and their combined watersheds total81 km2. Four streams entering these bays are blocked bydams at head of tide, forming freshwater impoundments.Water exits McCallums Pond to Brackley Bay by fallingvertically 2.2 m from a wooden spillway set in an earthendam (Fig. 2). Cass Pond on Covehead Bay has a 5-cham-ber pool-and-weir salmonid Wshway through whichwater drops 0.9 m over a horizontal distance of 12.2 m.Chambers are 1.8 m wide, 1.8–4.3 m long, and 0.7–1.3 mdeep. Water also leaves Cass Pond over a vertical con-crete spillway 5 m wide. Marshalls Pond drains intoCovehead Bay by a low-gradient channel with a rockybottom that falls 5.0 m over a horizontal distance of

303 m (1.7% slope). Parsons Pond connects to CoveheadBay via a culvert with wooden baZes on its Xoor that areintended to aid Wsh movement. The sole unimpoundedstream in the Brackley–Covehead system runs throughthe bed of the former McMillans Pond, whose damwashed out in 1996.

Eels were Wshed by fyke net in Brackley and Cove-head Bays, associated ponds, and the stream runningthrough McMillans Pond bed in May–November 2003.Eels were anaesthetized with clove oil, measured for totallength, weighed, and frozen until the otoliths wereremoved.

One otolith per eel was subject to microchemical anal-ysis. Otoliths were embedded in epoWx resin, then groundand polished until the primordium was exposed. Theotoliths were then carbon coated under a high vacuumevaporator prior to analysis with an electron probe mic-roanalyzer. Using a JEOL JXA-8900R system equippedwith wavelength dispersive X-ray spectrometers, Sr andCa concentrations were measured at 10 �m intervalsfrom the primordium to the otolith edge. Beam condi-tions were an acceleration voltage of 15 kV, a current of3 nA and a 5£4 �m rectangular scanning beam. A syn-thetic aragonite (CaCO3) and strontiantite (SrCO3NMNH R10065) were used for standard calibrations. Srconcentrations were measured for 80 s at Sr L� peakpositions and 20 s at both the lower and upper sides ofthe baseline. Ca was measured for 20 s at the Ca K� peakand for 10 s at both sides of the baseline. After Sr:Caratio analysis the otolith was polished to remove the car-bon layer and etched for 1–2 min with 5% EDTA toreveal annular rings for age determination.

Sr:Ca reference levels were established to identifyoccupancy of fresh, salt, and inter-habitat transitionwaters, on the basis of eels from the present study thatoccupied only one habitat type after age 1 (see Results).For each specimen, a Wve-point running mean was usedto smooth short-term Xuctuations in Sr:Ca ratios thatare likely due to otolith surface Xaws or analytic artifacts(Kotake et al. 2003). Smoothed Sr:Ca ratios that wereless than the mean +2 SD of smoothed measurements ofage 1+ eels from McCallums Pond were considered toindicate freshwater occupancy (F). Smoothed Sr:Caratios that were greater than the mean ¡2 SD ofsmoothed measurements of 15 salt-water resident age 1+eels from Brackley Bay were considered to indicate salt-water occupancy (S). Sr:Ca ratios intermediate betweenthese reference levels were considered to indicate transi-tion between habitat types (T).

Eels were assigned to one of three migratory contin-gents (freshwater residents, salt-water residents, andinter-habitat shifters) on the basis of habitat occupancypatterns. Criteria for identifying residents allowed forbrief excursions from the habitat of residence, or slightdelays in the arrival of young eels in freshwaters. An eelwas classed as a freshwater resident if its combinedsmoothed Sr:Ca ratios after age 1 were >97% F, or>92% F, ·8% T and 0% S. Salt-water residents includedeels whose post-age 1 Sr:Ca ratios were >97% S, or

1569

>92% S, ·8% T and 0% F. Eels that fell into neither ofthese categories were termed inter-habitat shifters.

The proportions of measurements in F, S, and Tand the mean Sr:Ca ratio were calculated fromsmoothed values within each year for each eel. Eel-years in F, S, and T were calculated by summing thewithin-year proportions of these categories across allyears.

Changes in an eel’s smoothed Sr:Ca ratio between Fand S after age 1 were considered to indicate inter-habi-tat shifts. Shifts did not include transfers to T. Shifts wereonly counted if they were at least four Sr:Ca samplepoints (40 �m) past the year one marker.

A generalized linear mixed model was employed toexamine changes in rate of inter-habitat shifting with ageand changes in habitat occupancy with age. Individualeels were treated as the random eVect because measure-ments within individuals were not independent. All mod-els were Wt in the R 2.1.1 (R Development Core Team2004) statistical program using the GLMM routine(Bates and Sarkar 2005).

Results

We caught eels at all Wshing locations except McMillansPond bed (Table 1). We encountered excessive lethalbycatch of white perch (Morone americana) in ParsonsPond and stopped Wshing before obtaining the targetminimum sample size (12). Otoliths from 95 eels cap-tured in Brackley and Covehead Bays and McCallums,Cass, and Marshalls Ponds were analyzed for Sr:Caratios. Sr:Ca ratios peaked during the oceanic phase, fellas eels arrived in continental waters, and then showed avariety of patterns (Fig. 3). Overall frequency distribu-tions of smoothed Sr:Ca ratios in age 1+ eels were bimo-dal in samples from both salt- and freshwater sites(Fig. 4). Modal values were <0.5£10¡3 and 5£10¡3. Thehigh mode dominated salt-water samples and the lowmode dominated freshwater samples.

Some Sr:Ca trajectories of individual eels were stablenear one of the two modes, while others varied widely(Fig. 3). All 12 eels from McCallums Pond showed low

Fig. 1 Brackley and Covehead Bays, Prince Edward Island (a) and associated freshwater impoundments; McCallums Pond (b) and Cass and Marsh-alls Ponds (c)

0 250 500

m

c

CassPond

Damwith fishladder Dam with

run-aroundoutlet

MarshallsPond

250 500

m

0

Dam withverticaloverspill

McCallums Pond

Brackley BayCovehead Bay

Parsons Pond

MarshallsPond

Cass PondMcMillanspond bed

McCallumsPond

Gulf of St.Lawrence0 1 2

km

a

b

63˚10’W46˚25’N

1570

and stable Sr:Ca ratios, with a mean of 0.57£10¡3

(SD=0.61£10¡3). We considered these eels to be fresh-water residents (F), and set the upper boundary forfreshwater occupancy to be the McCallums mean +2 SD(1.8£10¡3). In Brackley Bay, 15 eels showed high andstable Sr:Ca ratios (mean=5.24£10¡3, SD=1.28£10¡3)and one eel showed a variable ratio. We considered the15 Brackley eels with high and stable ratios to be salt-water residents (S), and set the lower boundary for salt-water occupancy to be their mean ratio ¡2 SD(2.7£10¡3). Smoothed ratios between 1.8£10¡3 and2.7£10¡3 were considered to indicate inter-habitat tran-sition (T).

The proportion of age 1+ eels that were freshwaterresidents, salt-water residents, and inter-habitat shiftersdiVered signiWcantly among ponds (G test, G=43.4,P<0.001) but not between bays (G=1.92, P>0.05;

Table 2). Failure to detect diVerences between bays mayhave been due to low statistical power (power=0.14).Salt-water residents dominated samples from bothBrackley (93.8%) and Covehead Bays (78.3%). All eelssampled from McCallums Pond were freshwater resi-dents. Most (85%) eels sampled from Cass Pond were

Fig. 2 Schematic proWles of pond outlets, showing the vertical spill-way at McCallums Pond (a), the concrete salmonid Wshway at CassPond (b), and the low-gradient channel at Marshalls Pond (c)

a

b

c 303 m

5.0m

12.2 m

0.9 m

2.2 m

Table 1 Catch and catch rates of American eels in fyke nets in theBrackley–Covehead system

Site Number of eels caught

Number of gear-days

Number caught per gear-day

Brackley Bay 32 46 0.696Covehead Bay 31 52 0.596McCallums Pond 12 61 0.197McMillans Pond bed 0 44 0.000Cass Pond 20 89 0.225Marshalls Pond 30 50 0.600Parsons Pond 6 5 1.200

Fig. 3 Mean within-year Sr:Ca ratios versus age for American eelsfrom Wve sites. For inter-habitat shifters (eels that moved betweenhabitat types at least once after age 1), lines represent individual eels.For eels that remained resident in either salt or freshwater after age1, symbols represent means, with N indicating the number of eels

01234567

Covehead Bay

Brackley Bay

01234567

N=18

McCallums Pond

01234567

0

0

1

1

2

2

3

3

4

4

5

5

6

6

7

7

Marshalls Pond

Age0

0

0

0

5

5

5

5

1

1

1

1

0

0

0

0

1

1

1

1

5

5

5

5

2

2

2

2

0

0

0

0

N=8

Mea

n S

r:C

a ra

tio (

x10

)-3

Mea

n S

r:C

a ra

tio (x

10)

-3M

ean

Sr:

Ca

ratio

(x1

0)

-3M

ean

Sr:C

a ra

tio (

x10

)-3

Mea

n S

r:C

a ra

tio (

x10

)-3

1571

inter-habitat shifters. Marshalls Pond samples were54.2% freshwater residents and 33.3% salt-water resi-dents. When habitat use was measured in eel-years, a sig-niWcant diVerence was found between the bays(G=12.31, P<0.01), though salt-water use dominatedsamples from both bays (Brackley 98.9%; Covehead87.5%). Freshwater use was the sole pattern in McCal-lums Pond samples. Eels from Cass Pond spent slightlymore time in freshwater (52.5%) than in salt-water

Tab

le2

Salin

ity

hist

ory

and

rate

of i

nter

-hab

itat

shi

ftin

g of

Am

eric

an e

els

capt

ured

in s

alt-

and

fres

hwat

er s

ites

See

text

for

deW

niti

ons

a P

ropo

rtio

n of

eel

s w

ith

diV

eren

t sal

init

y hi

stor

ies

did

not d

iVer

sig

niW

cant

ly b

etw

een

bays

(G

=1.

92, P

>0.

05),

but d

iVer

ed s

igniW

cant

ly a

mon

g po

nds

(G=

43.4

, P<

0.00

1)b

Pro

port

ion

of e

el-y

ears

wit

h diV

eren

t sa

linit

y hi

stor

ies

diV

ered

sig

niW

cant

ly b

etw

een

bays

(G=

12.3

1, P

<0.

01)

and

amon

g po

nds

(G=

119.

3, P

<0.

001)

c E

els

wit

h ed

ge m

ism

atch

are

tho

se w

hose

oto

lith

edge

Sr:

Ca

rati

o in

dica

ted

fres

hwat

er b

ut w

hich

wer

e ca

ptur

ed in

sal

t-w

ater

, and

tho

se w

hose

oto

lith

edge

Sr:

Ca

rati

o in

dica

ted

salt

-w

ater

but

whi

ch w

ere

capt

ured

in f

resh

wat

er

Num

ber

of e

els

Salin

ity

hist

ory

by n

umbe

raSa

linit

y hi

stor

y by

eel

-yea

rsb

Num

ber

wit

h ed

ge

mis

mat

chc

Num

ber

of

inte

r-ha

bita

t shi

fts

per

eel

Fre

shw

ater

re

side

nts

Inte

r-ha

bita

t sh

ifte

rsSa

lt-w

ater

re

side

nts

Fre

shT

rans

itio

nSa

ltM

ean

SDR

ange

Num

ber

%N

umbe

r%

Num

ber

%E

el-y

ears

%E

el-y

ears

%E

el-y

ears

%

Bra

ckle

y B

ay16

00.

01

6.3

1593

.80.

30.

30.

70.

886

.098

.90

0.12

0.49

0–2

Cov

ehea

d B

ay23

00.

05

21.7

1878

.312

.09.

63.

72.

911

0.3

87.5

10.

350.

780–

3M

cCal

lum

s P

ond

1212

100.

00

0.0

00.

015

9.0

100.

00.

00.

00.

00.

00

0.00

0.00

0–0

Cas

s P

ond

202

10.0

1785

.01

5.0

66.2

52.5

4.5

3.6

55.3

43.9

31.

751.

120–

4M

arsh

alls

Pon

d24

1354

.23

12.5

833

.320

0.0

79.7

1.9

0.7

49.2

19.6

100.

210.

590–

2

Fig. 4 Frequency distribution of Sr:Ca ratios measured in otolithsof age 1+ American eels captured in salt-water (a) and freshwater (b)sites

0

100

200

300

0 2 4 6 8 10

Brackley BayCovehead Bay

0

200

400

600

800

0 2 4 6 8 10

Sr:Ca ratio (x 10 )-3

McCallums Pond

Cass Pond

Marshalls Pond

Num

ber

of m

easu

rem

ents

Num

ber

of m

easu

rem

ents

b

a

Fig. 5 Rate of movement between salt- and freshwater of eels sam-pled in Cass Pond which shifted between habitat types. Sample size(number of eel-years) is given at the top of the graph

0.6

0.4

0.2

0.0

0.2

0.4

0.6

0.8

1

16 1616

432

16

5

13

6

9

7

4

8

3

Age

Num

ber

of s

hifts

per

eel

-yea

rT

o sa

lt w

ater

To

fres

h w

ater

1572

(43.9%) and Marshalls Pond eels spent the majority(79.7%) of their time in freshwater. Proportion of timespent in the various habitats diVered signiWcantly amongponds (G=119.3, P<0.001).

Eels from all sites except McCallums Pond showedinter-habitat shifts (Table 2). Mean rate of shifting didnot diVer between samples in the bays (Brackley 0.13shifts per eel, Covehead, 0.35 shifts per eel; ANOVA,F=1.02, P>0.05). Rate of shifting diVered among pondsamples (ANOVA, F=28.2, P<0.0001), with highestrates found in Cass Pond (1.75 shifts per eel).

The number of shifts from salt to freshwater per eel-year for inter-habitat shifters sampled in Cass Pondincreased signiWcantly with age (GLMM, F=7.44,P<0.01; Fig. 5). Rate of shifting from fresh to salt-waterdid not diVer signiWcantly with age (GLMM, F=0.33,P>0.05). Overall rate of shifting between habitatsincreased with age (GLMM, F=7.07, P<0.05). Figure 6

plots the percent of time spent in salt, transition, andfreshwaters versus age by inter-habitat shifters. For shift-ers captured in Covehead Bay, percent of time in salt-water increased, and percent of time in freshwaterdecreased, with age (salt: GLMM, F=39.6, P<0.001;fresh: F=5.268, P<0.05; n=29 eel-years). For shiftersfrom Cass Pond, percent of time in salt-water decreased,and percent of time in freshwater increased, with age(salt: GLMM, F=13.9, P<0.001; fresh: F=7.95,P<0.01; n=29). Percent time allocated to salt and freshhabitats by shifters captured in Marshalls Pond did notshow signiWcant trends with age (salt: GLMM, F=3.969,P>0.05; fresh: F=0.715, P>0.05; n=21).

Discussion

EVect of obstacle type on upstream movement

Eels cannot swim directly against strong currents, butthose smaller than 10 cm can creep up damp verticalwalls (Legault 1988). We therefore expected that eelswould colonize ponds with vertical water drops (McCal-lums, Cass) only at young ages, while colonization ofMarshalls Pond, which drains by a low-gradient channel,would occur at all ages. This was conWrmed for McCal-lums Pond, where Sr:Ca ratios showed that all capturedeels had entered freshwater in their elver year (Fig. 3).The dam at this site, with its 2.2 m vertical water drop,evidently posed an obstacle to upstream migration ofpost-elver eels. Contrary to prediction, eels of all agesmoved between salt-water and Cass Pond, indicatingthat the pool-and-weir salmonid Wshway at that site didnot impede upstream migration. Eels of all ages alsomoved between salt-water and Marshalls Pond, showing,as expected, that that pond’s low-gradient channel couldbe readily ascended by eels.

Movement patterns

This study identiWed three migratory contingents ofAmerican eels. Salt-water residents dominated samplesin two salt-water bays (84.6% of 39). Freshwater resi-dents were the sole contingent found in McCallumsPond, which is accessible only to eels in their Wrst conti-nental year. Inter-habitat shifters were found in all studysites except McCallums Pond. Shifters comprised of 85%of samples in Cass Pond and 12.5% in Marshalls Pond,whose dams did not impede inter-habitat movement.

Sr:Ca life history data are now available for the conti-nental phases of naturally reared Anguilla eels of six spe-cies at 39 locations worldwide (Table 3; Fig. 7). Ingeneral, reported Sr:Ca studies show that plasticity ofhabitat usage is the norm among eel populations. For allspecies combined, 27 of 39 (69%) samples contained eelsthat had shifted from the habitat where they were cap-tured. Fidelity to habitat type was the commonest infreshwater studies, where one half (7 of 14) of samples

Fig. 6 Allocation of time in habitat categories during each year, byeels which shifted habitat at least once after age 1. Samples are fromCovehead Bay (a), Cass Pond (b), and Marshalls Pond (c)

0%

20%

40%

60%

80%

100%

1 2 3 4 5 6 7 8

Per

cent

of t

ime

B

0%

20%

40%

60%

80%

100%

1 2 3 4 5 6

Per

cent

of t

ime

Fresh

Transition

Salt

A

0%

20%

40%

60%

80%

100%

1 2 3 4 5 6 7Age

Per

cent

of t

ime

C

1573

Tab

le3

Hab

itat

occ

upan

cy p

atte

rns

of w

ild (n

on-s

tock

ed)

yello

w a

nd s

ilver

Ang

uilla

eel

s af

ter

arri

val i

n co

ntin

enta

l wat

ers,

as

infe

rred

fro

m o

tolit

h Sr

:Ca

rati

os

a M

: on

spaw

ning

mig

rati

on, N

: not

on

spaw

ning

mig

rati

onb

S: s

alt,

B: b

rack

ish,

F: f

resh

c T

ype

B o

ccup

ancy

his

tory

may

als

o in

clud

e ty

pes

SB, B

F, a

nd S

BF

Stud

y lo

cati

onE

els

sam

pled

in s

alt-

wat

erE

els

sam

pled

in b

rack

ish

wat

erE

els

sam

pled

in fr

eshw

ater

Ref

eren

ces

Sam

plin

g ha

bita

tM

igra

tion

aN

Per

cent

occ

upan

cy

hist

oryb

Sam

plin

g ha

bita

tM

igra

tion

aN

Per

cent

occ

upan

cy

hist

oryb

Sam

plin

g ha

bita

tM

igra

tion

aN

Per

cent

occ

upan

cy

hist

oryb

SSB

BB

FF

SBF

SSB

BB

FF

SBF

SSB

BB

FF

SBF

A. r

ostr

ata

Gul

f of

St

. Law

renc

eE

stua

ryN

1310

0Im

poun

dmen

tN15

100

Cai

rns

etal

. (20

04)

Gul

f of

St

. Law

renc

eC

oast

al b

ays

N39

8515

Impo

undm

entN

5616

4836

D. K

. Cai

rns

etal

. (t

his

pape

r)N

ova

Scot

iaR

iver

N29

8317

Jess

op e

tal

. (20

02)

Nov

a Sc

otia

Riv

erM

6472

28Je

ssop

et

al. (

2002

)N

ova

Scot

iaR

iver

N10

729

71Je

ssop

et

al. (

2006

)H

udso

n R

iver

Est

uary

N29

3565

Riv

erN

1410

0M

orri

son

etal

. (20

03)

A. a

ngui

llaSw

eden

Coa

stal

w

ater

sN

310

0T

zeng

et

al. (

1997

)

Swed

enC

oast

al

wat

ers,

es

tuar

iesN

1872

28T

zeng

et

al. (

2000

)

Swed

enE

stua

ries

M8

8813

Tze

ng e

tal

. (20

00)

Bal

tic

Sea

exit

Coa

stal

wat

ersM

636

6216

16L

imbu

rg e

tal

. (20

03)

Ger

man

yO

pen

sea

M, N

1810

0R

iver

N9

100

Tsu

kam

oto

etal

. (19

98)

Fra

nce

Bay

N10

100

Est

uary

N12

842

50R

iver

N7

100

Dav

erat

et

al. (

2004

)A

. jap

onic

aJa

pan

Bay

N19

7426

Kot

ake

etal

. (20

04)

Japa

nB

ays

M, N

650

1733

Ara

i eta

l. (2

003)

Japa

nC

oast

al w

ater

sM25

2852

20K

otak

e et

al. (

2003

)Ja

panc

Bay

M42

2359

18T

zeng

et

al. (

2003

a)Ja

pan

Bay

M45

2220

58T

zeng

et

al. (

2003

b)Ja

pan

Riv

erN

1010

0T

suka

mot

o et

al. (

1998

)Ja

pan

Coa

stal

wat

ersM

, N39

2856

15E

stua

ries

N15

780

13R

iver

M, N

714

86T

suka

mot

o an

d A

rai (

2001

)E

ast

Chi

na S

eaO

pen

sea

M12

100

Tsu

kam

oto

etal

. (19

98)

Pea

rl R

., C

hina

Riv

erM

7410

0T

zeng

et

al. (

2003

a)T

aiw

anE

stua

ryM

, N58

521

6014

Riv

erM

, N18

5050

Shia

o et

al. (

2003

)T

aiw

anE

stua

ryM

, N58

521

6014

Riv

er6

100

Tze

ng e

tal

. (20

02)

Tai

wan

cE

stua

ryM

1813

807

Tze

ng e

tal

. (20

03a)

Tai

wan

cE

stua

ryN

339

6427

Tze

ng e

tal

. (20

03a)

A. m

arm

orat

aT

aiw

anE

stua

ryM

, N7

8614

Riv

erM

, N79

2575

Shia

o et

al. (

2003

)A

. aus

tral

isN

ew Z

eala

ndC

oast

al

lago

onM

2055

2025

Ara

i eta

l. (2

004)

A. d

ieV

enba

chii

New

Zea

land

Coa

stal

la

goon

M20

2575

Ara

i eta

l. (2

004)

1574

showed freshwater residency only. The exclusivity of thiscontingent at many locations may be due to long dis-tances to other salinity zones (Hudson River, USA: Mor-rison et al. 2003; Pearl River, China: Tzeng et al. 2003a),or to dams which impede upstream movements of eels atpost-elver ages (Cairns et al. 2004; D. K. Cairns et al.,this paper). Most samples of eels from brackish and salt-water contained eels that had used other habitats (brack-ish: 13 of 15, 87%; salt: 7 of 10, 70%). Movement patternsshown by American eels in the Brackley–Covehead sys-tem reXect the highly plasticity of Anguillid habitat useworldwide. Although available Sr:Ca studies are suY-cient to portray the broad strokes of Anguilla movementpatterns, it must be emphasized that uncertainty aboutrepresentativity of study sites and limited sample sizespreclude robust statistical conclusions.

Sr:Ca studies have demonstrated that some Europeanand Japanese eels never leave salt-water (Tsukamotoet al. 1998; Arai et al. 2003). This study is the Wrst to mea-sure Sr:Ca ratios of American eels sampled in salt-water.Our Wnding that most eels from Brackley and CoveheadBays had an exclusive salt-water Sr:Ca proWle indicatesthat American eels can likewise complete their life cyclein the sea. The catadromy paradigm for the American eelis thus overturned. Like European and Japanese eels,American eels must now be considered as species where

catadromy is a facultative life history option. The highrepresentation of exclusive salt-water residency in eelsfrom bay samples (84.6%) also suggests that non-catadr-omy may be an important and common pattern forAmerican eels.

Tosi et al. (1988) and Édeline and Élie (2004) foundthat European glass eels have distinct individual salinitypreferences. This implies that young eels separate intomigratory contingents upon arrival on the coast, withsalt-seeking eels remaining in marine waters while fresh-seekers ascend into freshwaters. The freshwater ponds inthe Brackley–Covehead system are adjacent to salt-waterbays, and all are within 5 km of the open sea. Given asalinity preference that is activated on arrival in coastalwaters and an upstream ascent rate of 0.6 km/day (Whiteand Knights 1997), we hypothesized that there would belittle time lag between the colonization of salt-water byeels destined to be salt residents, and colonization offreshwaters by eels destined to be fresh residents. Consis-tent with expectation, salt- and freshwater residents wereestablished in their respective habitats by age 1 (Fig. 3).Early movement to settlement areas may have an adap-tive basis. Because of their superior climbing ability,young eels can overcome vertical barriers to upstreammigration (such as the dam at McCallums Pond) andreach habitats that are inaccessible at older ages.

Fig. 7 Percentage of sampled Anguilla eels which showed movements out of the habitat type where they were captured, based on Sr:Ca anal-ysis. The habitat type given in each panel is the habitat where captured. All species includes A. marmorata, A. australis, and A. dieVenbachii.See Table 3 for data sources

Percent of eels which showed movement out of the habitat type where they were captured

A. rostrata,salt water

0

1

0 1-33 34-66 >67

Num

ber

ofst

udie

s A.rostrata,brackish

water

0

1

0 1-33 34-66 >67

A. rostrata,fresh water

0

1

2

0 1-33 34-66 >67

A. rostrata,all habitats

0

1

2

3

0 1-33 34-66 >67

A. anguilla,salt water

0

1

2

0 1-33 34-66 >67

Num

ber

ofst

udie

s

A. anguilla,brackish

water

0

1

2

0 1-33 34-66 >67

A. anguilla,fresh water

0

1

2

0 1-33 34-66 >67

A. anguilla,all habitats

0

1

2

3

4

5

0 1-33 34-66 >67

A. japonica,salt water

0

1

2

3

0 1-33 34-66 >67

Num

ber

ofst

udie

s A.japonica,brackish

water

0

1

2

0 1-33 34-66 >67

A. japonica,fresh water

0

1

2

3

0 1-33 34-66 >67

A. japonica, all habitats

0

1

2

3

4

5

0 1-33 34-66 >67

All

speciesspecies,

,salt

water

0

1

2

3

4

0 1-33 34-66 >67

Num

ber

ofst

udie

s AllAll species,

brackishwater

0

1

2

3

4

5

0 1-33 34-66 >67

fresh water

0

2

4

6

0 1-33 34-66 >67

All species,all habitats

0

246

81012

0 1-33 34-66 >67

1575

Eels may choose among salinity zones, and they mayalso choose between sedentary and mobile lifestyles(Feunteun et al. 2003). Some eels in the Brackley–Cove-head system shifted between habitats only once and thenremained in the new habitat. This could be interpreted assearching for suitable habitat, and then settling therewhen they Wnd it (Fig. 3). However, others shifted contin-uously, suggesting that nomadic behavior is an inherentproperty of some eels.

Implications for conservation

Prince Edward Island has over 800 artiWcial impound-ments (MacFarlane 1999), and most streams areblocked by one or several dams. Our results suggestthat eels can readily reach ponds formed by damsequipped with pool-and-weir salmonid Wshways or low-gradient channels. These passage facilities thus permitthe natural spatial behavior that is characteristic of thehabitat-shifting eel contingent. In contrast, small damswith vertical spillways and no passage facilities mayblock the normal behavior of habitat-shifting eels bylimiting upstream passage to young ages. This mayhave negative eVects on populations in systems wheresuch dams occur.

Recent declines in eel abundance indices haveprompted eVorts to devise management schemes thatwould assure adequate escapement to the spawninggrounds (Richkus and Whalen 2000; ICES 2003). Suchschemes must recognize contributions of escaping silvereels from unWshed, as well as Wshed areas. In much ofeastern North America eel exploitation is restricted tocoastal and estuarine waters. Our results suggest thatWshing in marine waters may aVect eel populations innearby freshwaters, due to movement between the twohabitats. Neither marine populations nor those of adja-cent freshwater are discrete. Population models that esti-mate escapement of silver eels from salt, brackish, andfreshwater habitats must account for these movements.

The relative importance of marine and freshwaters tothe eel’s life cycle, and patterns of migration betweenthese habitats, are vital issues in eel biology and conser-vation. The Sr:Ca technique will Wnd wide employ as thekey to their understanding.

Acknowledgments This study received support from the NationalScience Council, ROC (NSC 91¡2313-B-002-291 and 92-2313-B-002-057). We thank Angus McLennan, Corey Muttart, ValérieTremblay, Noella McDonald, and Robbie Moore for assistance inthe laboratory and Weld, and Mark Grimmett for measuring chemi-cal concentrations in water samples. Tillmann Benfey and AllenCurry provided valuable advice at all stages and improved the man-uscript with their comments.

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Bates D, Sarkar D (2005) Linear mixed eVects models using S4 mod-els. LME 4 package for R. Available at http://www.micro-arrays.unife.it/CRAN/doc/packages/lme4.pdf

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Mar Biol (2006) 149:1587–1588 DOI 10.1007/s00227-006-0418-x

123

ERRATUM

Movement patterns of American eels (Anguilla rostrata) between salt- and freshwater in a coastal watershed, based on otolith microchemistry

Heather M. Lamson · Jen-Chieh Shiao · Yoshiyuki Iizuka · Wann-Nian Tzeng · David K. Cairns

Published online: 26 June 2006© Springer-Verlag 2006

Mar Biol (2006) DOI 10.1007/s00227-006-0308-2

Unfortunately Table 3 contained errors. The correctTable 3 is shown below.

The online version of the original article can be found at http://dx.doi.org/10.1007/s00227-006-0308-2.

H. M. LamsonBiology Department, University of New Brunswick, Fredericton, NB, Canada E3B 6E1

J.-C. ShiaoInstitute of Zoology, Academia Sinica, Nankang, Taipei 11529, Taiwan, ROC

Y. IizukaInstitute of Earth Sciences, Academia Sinica, Nankang, Taipei 11529, Taiwan, ROC

W.-N. TzengInstitute of Fisheries Sciences, National Taiwan University, Taipei 10617, Taiwan, ROC

D. K. Cairns (&)Department of Fisheries and Oceans, Box 1236, Charlottetown, PE, Canada C1A 7M8 e-mail: cairnsd@dfo-mpo.gc.ca

1588 Mar Biol (2006) 149:1587–1588

123

Tab

le3

Hab

itat

occ

upan

cy p

atte

rns

of w

ild (

non-

stoc

ked)

yel

low

and

silv

er A

ngui

lla e

els

afte

r ar

riva

l in

cont

inen

tal w

ater

s, a

s in

ferr

ed f

rom

oto

lith

Sr:C

a ra

tios

a R

efer

ence

s: 1

: Cai

rns

etal

. (20

04),

2: t

his

stud

y, 3

: Jes

sop

etal

. (20

02),

4: J

esso

p et

al. (

in p

ress

), 5

: Mor

riso

n et

al. (

2003

), 6

: Tze

ng e

tal

. (19

97),

7: T

zeng

eta

l. (2

000)

, 8: L

imbu

rg e

tal

. (20

03),

9: T

suka

mot

oet

al. (

1998

), 1

0: D

aver

at e

tal

. (20

04),

11:

Kot

ake

etal

. (20

04),

12:

Ara

i eta

l. (2

003)

, 13:

Kot

ake

etal

. (20

03),

14:

Tze

ng e

tal

. (20

03a)

, 15:

Tze

ng e

tal

. (20

03b)

, 16:

Tsu

kam

oto

and

Ara

i (20

01),

17:

Shi

ao e

tal

.(2

003)

, 18:

Tze

ng e

tal

. (20

02),

19:

Ara

i eta

l. (2

004)

b M

: on

spaw

ning

mig

rati

on, N

: not

on

spaw

ing

mig

rati

onc S:

sal

t, B

: bra

ckis

h, F

: fre

shd

Typ

e B

occ

upan

cy h

isto

ry m

ay a

lso

incl

ude

type

s SB

, BF

, and

SB

F

Stud

y lo

cati

onE

els

sam

pled

in s

alt w

ater

Eel

s sa

mpl

ed in

bra

ckis

h w

ater

Eel

s sa

mpl

ed in

fre

shw

ater

Ref

.a

Sam

plin

g ha

bita

tM

ig.b

NP

erce

nt o

ccup

ancy

hi

stor

ycSa

mpl

ing

habi

tat

Mig

.bN

Per

cent

occ

upan

cy

hist

oryc

Sam

plin

g ha

bita

tM

ig.b

NP

erce

nt o

ccup

ancy

hi

stor

yc

SSB

BB

FF

SBF

SSB

BB

FF

SBF

SSB

BB

FF

SBF

A. r

ostr

ata

Gul

f of

St. L

awre

nce

Est

uary

N13

100

Impo

undm

ent

N15

100

1

Gul

f of

St. L

awre

nce

Coa

stal

bay

sN

3985

15Im

poun

dmen

tsN

5616

4836

2

Nov

a Sc

otia

Riv

erN

2983

173

Nov

a Sc

otia

Riv

erM

6472

283

Nov

a Sc

otia

Riv

erN

107

2971

4H

udso

n R

iver

Est

uary

N29

3565

Riv

erN

1410

05

A. a

ngui

llaSw

eden

Coa

stal

wat

ers

N3

100

6Sw

eden

Coa

stal

wat

ers,

es

tuar

ies

N18

7228

7

Swed

enE

stua

ries

M8

8813

7B

alti

c Se

a ex

itC

oast

al w

ater

sM

636

6216

168

Ger

man

yO

pen

sea

M,N

1810

0R

iver

N9

100

9F

ranc

eB

ayN

1010

0E

stua

ryN

128

4250

Riv

erN

710

010

A. j

apon

ica

Japa

nB

ayN

1974

2611

Japa

nB

ays

M,N

650

1733

12Ja

pan

Coa

stal

wat

ers

M25

2852

2013

Japa

ndB

ayM

4223

5918

14Ja

pan

Bay

M45

2220

5815

Japa

nR

iver

N10

100

9Ja

pan

Coa

stal

wat

ers

M,N

3928

5615

Est

uari

esN

157

8013

Riv

erM

,N7

1486

16E

ast

Chi

na S

eaO

pen

sea

M12

100

9P

earl

R.,

Chi

naR

iver

M74

100

14T

aiw

anE

stua

ryM

,N58

521

6014

Riv

erM

,N18

5050

17T

aiw

anE

stua

ryM

,N58

521

6014

Riv

er6

100

18T

aiw

and

Est

uary

M18

1380

714

Tai

wan

dE

stua

ryN

339

6427

14

A. m

arm

orat

aT

aiw

anE

stua

ryM

,N7

8614

Riv

erM

,N79

2575

17A

. aus

tral

isN

ew Z

eala

ndC

oast

al la

goon

M20

5520

2519

A. d

ieV

enba

chii

New

Zea

land

Coa

stal

lago

onM

2025

7519