Biogeography of tropical reef ®shes: the SouthAtlantic puzzleJ.-C. Joyeux1*, S. R. Floeter2, C. E. L. Ferreira3 and J. L. Gasparini1 1Departamento de

Ecologia e Recursos Naturais, Universidade Federal do EspõÂrito Santo, Av. Fernando Ferrari

S/N, VitoÂria, ES 29060-900, Brazil, 2LaboratoÂrio de CieÃncias Ambientais, Universidade

Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ

28015-620, Brazil, and 3Departamento de Oceanogra®a, IEAPM, Rua Kioto 253, Arraial do

Cabo, RJ 28930-000, Brazil

Abstract

Aim To reveal underlying distributional mechanisms of tropical reef ®shes in the SouthAtlantic.

Location The tropical South Atlantic, with emphasis on the Brazilian province.

Methods The disjunct distributions of thirty-®ve reef ®sh species occurring in theBrazilian Province were analysed to allow a better understanding of present biogeo-graphical patterns. To avoid potential bias because of taxonomic problems ormisidenti®cation, we only included families taxonomically well documented, withconspicuous species, and relatively easy to identify.

Results The low-level differentiation between Caribbean and Brazilian species/popula-tions, as well as the presence of restricted populations of a few northern or southernspecies on the opposite side of the Amazon River, clearly indicate that this barrier todispersion can be occasionally bridged. Transoceanic dispersal appears to be frequentand to occur along three routes: from the Caribbean to North East Atlantic, fromnorthern Brazil to the Gulf of Guinea, and from Africa to southern Brazil. Intermediatestepping-stones are apparently not required along transatlantic routes because of therarity of consecutive colonizations. However, intermediate stopovers are persistentlyused along short routes. In all cases, the long-term success of colonists, i.e. theestablishment of stable local populations, appears to depend upon ecological factors.

Main conclusions The puzzling patterns of distribution found in the South Atlanticseem primarily the outcome of allopatric speciation and of the interaction of longdistance dispersal abilities and ecological processes. Successfulness of the colonization ofremote sites appears to be less dependent from dispersal ability than upon persistenceability or settlement preferences.

Keywords

Dispersal, islands, disjunct, colonization, speciation, Amazon barrier, Brazilian prov-ince, distribution.

INTRODUCTION

The South Atlantic Ocean has some peculiar biogeograph-ical and ecological characteristics. The most obvious is the

freshwater out¯ow from the Amazon River that apparentlyacts as a major biogeographical barrier separating the shore®sh faunas of Brazil and the Caribbean (Briggs, 1995;Floeter & Gasparini, 2000). The oceanic islands of thetropical South Atlantic are widely scattered and supportshelf faunas that exhibit reduced species diversity and othereffects of isolation (Floeter & Gasparini, 2000). Consideringthat the islands vary in age, size and distance from othershores, comparative studies of their faunas can reveal

*Correspondence: Departamento de Ecologia e Recursos Naturais,

Universidade Federal do EspõÂrito Santo, Av. Fernando Ferrari S/N, Vito ria,

ES 29060-900, Brazil. E-mail: joyeux@npd.ufes.br

Journal of Biogeography, 28, 831±841

Ó 2001 Blackwell Science Ltd

considerable information about general patterns of evolutionand distribution (cf. Robertson, 2001). St Helena is the ofone the world's most isolated tropical islands (located from1270 km Ascension and 1870 km from Africa). Others lyingfar out from shore are Ascension, Trindade and St Paul'sRocks (Fig. 1a). Closer to the continental shores, but still farenough to demonstrate the effects of isolation, are otherisland groups located on both sides of the tropical SouthAtlantic. In addition to the oceanic islands, there aresubmerged seamounts (the Fernando de Noronha and theVito ria-Trindade chains) that remain to be explored.

Until recently, the tropical western South Atlantic presen-ted a conspicuous gap in our knowledge of the distributionof tropical reef ®shes (cf. Sale, 1991). In the late 1990s, anincrease in exploration and specimen collection resulted inthe publication of considerable new information about thegeographical distribution of many species (e.g. Moura et al.,1999; Floeter et al., 2001), the description of new species(e.g. Sazima et al., 1998; Rocha & Rosa, 1999; Heiser et al.,2000; Burgess, 2001; Moura et al., 2001), the ®rst compre-hensive collections for certain sites (e.g. Rosa & Moura,1997; Rocha et al., 1998; Gasparini & Floeter, 2001), andthe ®rst works on phylogeography (Bernardi et al., 2000;Bowen et al., 2001; Muss et al., 2001). Also, there is nowavailable new work on the tectonic, eustatic, climatic andoceanographic characteristics of the tropical Atlantic (e.g.Zebiak, 1993; Arz et al., 1999; Knoppers et al., 1999;Stramma & Schott, 1999). These recent advances permit usto draw a ®rst picture of some aspects of the biogeography ofthe region.

METHODS

This study is based on the recorded occurrences of thirty-®ve tropical teleost species primarily associated with hardsubstrata (rocky shores, coral and coralline algae reefs),here referred to as `reef ®shes', in the South Atlanticcontinental shelf and oceanic islands (Fig. 1a). To avoidpotential bias caused by taxonomic problems or misiden-ti®cation, we only included families taxonomically welldocumented (e.g. Pomacanthidae, Labridae, Scaridae), withconspicuous (e.g. generally common, large, non-cryptic,colourful, etc.) species, and relatively easy to identify(Table 1). Species not presenting disjunct distributions (i.e. present on the coast while absent in all islands, orendemic to one lone island) were excluded because such`even' distributions are unlikely to bring much insight. Thedistribution patterns have been determined primarilythrough original studies by the authors and colleagues, aswell as compilation of data from the literature (e.g.Lubbock, 1980; Lubbock & Edwards, 1981; Edwards,1990; Afonso et al., 1999; Smith-Vaniz et al., 1999). Thespecies were considered to be resident at a particularlocation if they were suf®ciently abundant to have estab-lished self-recruiting populations or to be vagrants ifexceedingly rare and probably recruited from other sites.Although the Manuel Luis Reefs are not considered to be anoceanic island, they were included as such in this study for

their ecological and biogeographical signi®cance, as theyare the ®rst reef formation south of the Amazon plume(Rocha & Rosa, 2001a).

RESULTS AND DISCUSSION

Distribution patterns

The South Atlantic reef ®sh biogeography proved to be anintricate tapestry (Fig. 1). The thirty-®ve selected speciesdisplayed intriguing distribution patterns. The wrasseHalichoeres bathyphilus and the damsel®sh Chromis ¯avic-auda present strongly accentuated antitropical distributions(Fig. 1c). Other species such as the groupers Epinephelusniveatus and Mycteroperca microlepis and the parrot®shSparisoma atomarium show discontinuous distribution onAmerican coastal reefs (Fig. 1c). The tropical extinctiontheory (the loss of the centre of distribution) is commonlyevoked to explain this type of distribution pattern (TheÂel,1886; Briggs, 1995). Three species found in the south-westare presumed immigrants from African waters the trumpet-®sh Aulostomus strigosus, the grouper Epinephelus margin-atus and the surgeon®sh Acanthurus monroviae (Fig. 1d).Twenty-one species are indistinguishable from their Carib-bean counterparts (Fig. 1e±i). The remaining six species(Fig. 1c and i) are southern endemics the butter¯y®shPrognathodes brasiliensis, the damsel®sh Stegastes fuscus,the wrasses Bodianus insularis, Halichoeres brasiliensis andThalassoma noronhanum, and the parrot®sh Sparisomaaxillare, with close relatives in the northern or easternAtlantic [respectively, P. aculeatus, S. imbricatus, B. pul-chellus/B. rufus, H. radiatus, T. bifasciatum, and S. rubrip-inne (Table 1)].

The south-western Atlantic is overall characterized byhigh endemism, about 18±20% for reef ®shes (Floeter &Gasparini, 2000). However, differences between the Carib-bean and the Brazilian provinces are at the species orsubspecies level, with no genus restricted to the south-western Atlantic. Brazilian corals, in contrast, show a levelof endemism of 33%. Twenty-three percent of thesescleractinian species are considered relict forms onlyremotely related to recent Caribbean species (Laborel,1970; LeaÄo, 1983; J. Laborel, pers. comm.). It has beenargued that the observed differentiation with respect to reef®shes is too low to be accounted for the initial establishmentof a connection of the Amazon River system to the Atlanticin the late Miocene (5±6 Ma) (cf. Hoorn et al., 1995). Wesuspect that `complete' vicariance or allopatric speciationwith stabilizing selection could not have produced suchgeneral closeness between north and south-western Atlanticichthyofaunas across the whole spectrum of ®sh species andlife histories. Thus, vicariance through parapatric speciation(separation with occasional contact) seems the most parsi-monious hypothesis to explain the low morphologicaldifferentiation in spite of the wide and old Amazon barrier(cf. Briggs, 1995; Bowen et al., 2001). The Amazon River®rst created a ®lter, not a full barrier, to dispersal withina once widespread distribution. During the Pliocene

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 831±841

832 J.-C. Joyeux et al.

Figure 1 Distribution patterns of selected south-western Atlanticreef ®shes. The letter `v' beside a number indicates that thecorresponding species is a vagrant. (a) Location of sites (excludingGough and Tristan da Cunha), (b) oceanic-scale currents,(c) antitropical distributions and an endemic of mid-Atlantic ridgeislands, (d) colonizers of the south-western Atlantic of Africanorigin. Brazilian Aulostomus is genetically similar to A. strigosus butshows intermediate morphology between A. strigosus and A.maculatus (Bowen et al., 2001), (e) colonizers of the eastern Atlanticof Caribbean or Brazilian origin 1 African population, (f) colonizersof north-eastern Brazil of Caribbean origin, (g) caribbean speciesrestricted to South Atlantic islands. 1 Although vagrant on the coastof Brazil, this species is relatively common in the Vito ria-Trindaderidge and in Trindade Island, (h) widely distributed western Atlanticspecies, and (i) south-western Atlantic endemics and species withrestricted Caribbean distribution. 1 Including subspecies S. fuscustrinidadensis. 2 Including S. lubbocki [Novelli (1998) reviewedmeristic data from all the Stegastes occurring in Brazil and found noconsistent difference between S. pictus and S. lubbocki].

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 831±841

Biogeography of tropical reef ®shes 833

(5.3±1.6 Ma) onwards, the delta experienced a rapidseaward growth caused by a major uplift and erosion ofthe Andes (Hoorn, 1994). Thus, it is possible that the ®lterinterrupted faunal interchange for the most salinity orsediment sensitive species (Muss et al., 2001), but that otherspecies breached the barrier on occasion. We hypothesize adrastic but intermittent interruption of passage during highfreshwater out¯ow periods (i.e. at the end of each glacialperiod). Another non-excluding possibility is that genetic¯ow would be completely severed during low sea-levelperiods (cf. Maslin & Mikkelsen, 1998; Arz et al., 1999;Knoppers et al., 1999). During one of the recent loweststands ()50/70 m at 12.7±11.2 ka BPBP) (Arz et al., 1999), theAmazon freshwater and material was directly exported tothe upper shelf slope (present day shelf break is at 75±80 m).This event coincided with high sedimentation rates, possibly

cutting-off passage of shallow-water forms between the twobiogeographical provinces.

It should be noted that the Brazilian province seemsisolated from the Caribbean province because of the direc-tion of prevailing currents, but that the reverse is possiblynot true (Fig. 1b). It is conceivable that species unitybetween western Atlantic, the Brazilian and the Caribbeanprovinces may be maintained in some cases through genetic¯ow from south to north. For instance, some wide-rangingBrazilian species can only be found in the southern tip of theCaribbean (Fig. 1i). The grunt Anisotremus moricandi(Ranzani), the ¯ameback angel®sh Centropyge aurantono-tus, the yellowtail damsel®sh S. pictus and the Brazilianpuffer Canthigaster sp.n., among others, distribute accord-ing to this surprising pattern (Humann, 1996; L.A. Rocha,pers. comm.). On the other hand, some Caribbean species

Figure 1 Continued.

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 831±841

834 J.-C. Joyeux et al.

Tab

le1

Geo

grap

hic

range

and

endem

ism

leve

lfo

rth

ere

efsp

ecie

sse

lect

edfo

rth

epre

sent

study.

More

det

ails

on

the

south

-wes

tA

tlan

tic

range

are

give

nin

the

®gu

res.

Exac

tra

nge

exte

nsi

on

inth

eC

arib

bea

nPro

vince

and

along

the

Afr

ican

coas

tis

only

pro

vided

insp

eci®

cca

ses.

Vouch

erre

fere

nce

sfo

rB

razi

lian

spec

imen

sca

nbe

obta

ined

atth

eB

iobas

ePro

ject

(htt

p//

:ww

w.b

iobas

e.org

/)

Spec

ies

Geo

grap

hic

range

Lev

elof

endem

ism

Ref

eren

ces*

Puta

tive

sist

ersp

ecie

sG

eogr

aphic

range

Aulo

stom

idae

Aulo

stom

us

stri

gosu

sV

alen

cien

nes

,1842

WIn

dia

n+

EA

tlan

tic+

Oce

anic

Isl.+

Bra

zili

anpro

vince

Bow

enet

al.

(2001)

A.

mac

ula

tus

(Val

enci

ennes

,1837)

+A

.ch

inen

sis

(Lin

nae

us,

1766)

Car

ibbea

npro

vince

Indo-P

aci®

c

Ser

ranid

ae

Der

mat

ole

pis

iner

mis

(Val

enci

ennes

,1833)

Wes

tern

Atl

anti

c

Epin

ephel

us

mar

ginat

us

(Lin

nae

us,

1758)

Med

iter

ranea

n+

Eas

tA

tlan

tic+

Bra

zili

anpro

vince

E.

niv

eatu

s(V

alen

cien

nes

,1828)

Wes

tern

Atl

anti

c+

Eas

tern

Pac

i®c

Myc

tero

per

cam

icro

lepis

(Goode

&B

ean,

1879)

Wes

tern

Atl

anti

c

Par

anth

ias

furc

ifer

(Val

enci

ennes

,1828)

Eas

tA

tlan

tic+

WA

tlan

tic+

Eas

tern

Pac

i®c

Afo

nso

etal

.(1

999)

Haem

uli

dae

Hae

mulo

nch

rysa

rgyr

eum

(Gu Ènth

er,

1859)

Car

ibbea

npro

vince

+B

razi

lian

isla

nds

Chaet

odonti

dae

Chae

todon

oce

llat

us

(Blo

ch,

1787)

Wes

tern

Atl

anti

c

C.

seden

tari

us

(Poey

,1860)

Wes

tern

Atl

anti

cSa

nto

set

al.

(1997)

C.

stri

atus

(Lin

nae

us,

1758)

Wes

tern

Atl

anti

cP

rogn

athodes

bra

sili

ensi

s(B

urg

ess,

2001)

Bra

zili

anpro

vince

Spec

ies

Burg

ess

(2001)

P.

acule

atus

(Poey

,1860)

Car

ibbea

npro

vince

Pom

aca

nth

idae

Cen

tropyg

eau

ranto

notu

s(B

urg

ess,

1974)

Bra

zili

anpro

vince

+S

Car

ibbea

npro

vince

C.

argi

(Woods

&K

anaz

awa,

1951)

Car

ibbea

npro

vince

H.

cili

aris

(Lin

nae

us,

1758)

Wes

tern

Atl

anti

c

StPau

l's

rock

s

Spec

ies

Morp

hs

Lubbock

&E

dw

ards

(1981);

B.

Fei

toza

,per

s.co

mm

.

H.

tric

olo

r(B

loch

,1795)

SEB

razi

lian

pro

vince

Popula

tion

J.L

.G

aspar

ini,

per

s.obs.

NE

Bra

zili

anpro

vince

+C

arib

bea

npro

vince

Popula

tion

Pom

acan

thus

par

u(B

loch

,1787)

Wes

tern

Atl

anti

c+

Oce

anic

isla

nds

P.

arcu

atus

(Lin

nae

us,

1758)

Wes

tern

Atl

anti

c

Pom

ace

ntr

idae

Chro

mis

¯av

icau

da

(Gu Ènth

er,

1880)

Bra

zili

anpro

vince

Spec

ies

?Sm

ith-V

aniz

etal

.(1

999)

C.

¯av

icau

da

Ber

muda

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 831±841

Biogeography of tropical reef ®shes 835

Tab

le1

(Conti

nued

)

Spec

ies

Geo

grap

hic

range

Lev

elof

endem

ism

Ref

eren

ces*

Puta

tive

sist

ersp

ecie

sG

eogr

aphic

range

Chro

mis

scott

i(E

mer

y,1968)

Car

ibbea

npro

vince

+B

razi

lian

pro

vince

Smit

h-V

aniz

etal

.(1

999);

Gas

par

ini

&Flo

eter

(2001);

Roch

a&

Rosa

(2001a)

Mic

rosp

athodon

chry

suru

s(C

uvi

er&

Val

enci

ennes

,1830)

Wes

tern

Atl

anti

c

Steg

aste

sfu

scus

(Cuvi

er&

Val

enci

ennes

,1830)

Bra

zili

anco

ast

Tri

ndad

eis

land

(S.

f.tr

indad

ensi

s)

Spec

ies

Subsp

ecie

sA

llen

(1991);

Gas

par

ini

etal

.(1

999)

S.im

bri

catu

s(J

enyn

s,1840)

+S.

vari

abil

is(C

aste

lnau

,1855)

Afr

ican

coas

t+

isla

nds

Bra

zili

anpro

vince

S.pic

tus

(Cas

teln

au,

1855)

Bra

zili

anpro

vince

+T

rinid

ade

&T

obag

oSp

ecie

sN

ove

lli

(1998);

L.A

.R

och

a,per

s.C

om

m.

Steg

ates

par

titu

s(P

oey

,1868)

+St

egas

tes

lubbock

iA

llen

&Sm

ith,

1992

Car

ibbea

npro

vince

Asc

ensi

on

Labri

dae

Bodia

nus

insu

lari

s(G

om

on

&L

ubbock

,1979)

Mid

-Atl

anti

cri

dge

isla

nds

Spec

ies

Gom

on

&L

ubbock

(1980)

B.

rufu

s(L

innae

us,

1758)

+B

.pulc

hel

lus

(Poey

,1860)

Wes

tern

Atl

anti

c

Wes

tern

Atl

anti

c+

SaÄo

Tom

e ÂH

alic

hoer

esbat

hyp

hil

us

(Bee

be

&T

ee-V

an,

1932)

Bra

zili

anpro

vince

Spec

ies

?Sm

ith-V

aniz

etal

.(1

999)

H.

bat

hyp

hil

us

(Bee

be

&T

ee-V

an,

1932)

Ber

muda

H.

biv

itta

tus

(Blo

ch,

1791)

Wes

tern

Atl

anti

cH

.bra

sili

ensi

s(B

loch

,1791)

Bra

zili

anpro

vince

Spec

ies

Roch

a&

Rosa

(2001b)

H.

radia

tus

(Lin

nae

us,

1758)

Car

ibbea

npro

vince+

NE

Bar

azil

ian

isla

nds

Thal

asso

ma

noro

nhan

um

(Boule

nge

r,1890)

Bra

zili

anpro

vince

Spec

ies

Roch

aet

al.

(2001)

T.

bif

asci

atum

(Blo

ch,

1791)

Car

ibbea

npro

vince

Sca

ridae

Spar

isom

aat

om

ariu

m(P

oey

,1861)

Wes

tern

Atl

anti

c

S.ax

illa

re(S

tein

dac

hner

,1878)

Bra

zili

anpro

vince

Spec

ies

Ber

nar

di

etal

.(2

000);

Moura

etal

.(2

001)

S.ru

bri

pin

ne

(Val

enci

ennes

,1839)

+Sp

aris

om

aaf

f.R

ubri

pin

ne

(Val

enci

ennes

,1839)

Car

ibbea

npro

vince

Eas

tern

Atl

anti

c

Aca

nth

uri

dae

Aca

nth

uru

sbah

ianus

(Cas

teln

au,

1855)

Bra

zili

anpro

vince

Car

ibbea

npro

vince

Popula

tion

Popula

tion

Bri

ggs

&C

aldw

ell;

(1957);

Roch

aet

al.,

per

s.co

mm

.A

.ra

ndal

li(B

rigg

s&

Cal

dw

ell,

1957)

Eas

tern

Gulf

of

Mex

ico

A.

chir

urg

us

(Blo

ch,

1787)

Wes

tan

dE

ast

Atl

anti

cA

.co

erule

us

(Blo

ch&

Schnei

der

,1801)

Wes

tern

Atl

anti

c

A.

monro

viae

(Ste

indac

hner

,1876)

Eas

tern

Atl

anti

cQ

ue Âr

oet

al.

(1990);

Gola

ni

&So

nin

(1996);

Moura

(2000);

C.E

.L.

Fer

reir

a,per

s.obs.

*G

ener

alre

fere

nce

suse

dfo

rth

eW

este

rnA

tlan

tic

are

Bo Èhlk

e&

Chap

lin

(1968),

Hum

ann

(1996)

and

Ran

dal

l(1

996),

and

for

the

Eas

tern

Atl

anti

car

e:Q

ue Âr

oet

al.

(1990),

Deb

eliu

s(1

997)

and

Edw

ards

etal

.(2

001).

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 831±841

836 J.-C. Joyeux et al.

are restricted to a few sites south of the Amazon (e.g. thedamsel®sh Chromis scotti and the wrasse Halichoeresradiatus), generally on isolated locations (Fig. 1g). Suchdistributions are a clear indication that the isolation betweenBrazil and the Caribbean is occasionally bridged ± one wayor the other. Periods of isolation can be interrupted bysporadic gene ¯ow through larval transport by currents,active swimming abilities (Stobutski & Bellwood, 1997),rafting (Mora, 2001) or even through the colonization ofdeep-water sponge habitats under the Amazon River plume(Collette & Rutzler, 1977; Uyeno et al., 1983; Rocha et al.,2000).

Long-distance dispersal

Larvae of a number of species can successfully travelenormous distances before reaching suitable settling groundand colonizing new areas. Five species have thus apparentlymade the eastward transatlantic crossing. Two of them(Chaetodon sedentarius at Azores and Madeira, and theangel®sh Pomacanthus paru in the Gulf of Guinea) wereonly found vagrants in the East Atlantic, presumablyindicating recent arrival (Fig. 1e). The other three (Creole-®sh Paranthias furcifer, B. pulchellus and Sparisomaaff. rubripinne) established restricted populations (Afonsoet al., 1999; Bernardi et al., 2000) (Fig. 1e). Two specieswith now resident western populations most probablycrossed the other way (cf. Bowen et al., 2001) (Fig. 1d).However, as shown by the relative commonness of vagrantsfrom distant source populations, the establishment offounding populations appears much rarer than recruitment.In addition to the two recorded stray species in the EastAtlantic, the African acanthurid Acanthurus monroviae wasrecently found as a vagrant in south-east Brazil (Moura,2000; C.E.L.F. pers. obs.) and in the eastern Mediterranean(Golani & Sonin, 1996) (Fig. 1d). Other examples includethe thirteen species that were recorded only as juveniles inBermuda (including Chromis scotti; Fig. 1g) (Smith-Vanizet al., 1999). This pattern (comparative number of speciescrossings, limited distribution in colonized areas) ®ts withmodern and fossil records for shell-bearing mollusks(Vermeij & Rosenberg, 1993). Invaders of the East Atlanticcould have crossed the ocean from northern Brazil to theGulf of Guinea via the Equatorial Under Current (Stramma& Schott, 1999; Muss et al., 2001) (Fig. 1b and e), possiblyfavoured by ENSO-type or ENSO-induced events (Venegaset al., 1996; Stramma & Schott, 1999). Alternatively, otherspecies [e.g. C. sedentarius and Adudefduf taurus (MuÈ ller &Troschel)] (Debelius, 1997; Edwards et al., 2001) appear tohave crossed from the Caribbean to the Macaronesianislands off northern African via the Gulf Stream. In spite ofthe westward ¯owing South Equatorial Current, invasionsfrom Africa to the west are rarer, as evidenced by thelimited present distribution of the few putative colonizers ofSouth America (Fig. 1d). Stepping stones do not appearnecessary for transatlantic passage in either direction. Theinsular hog®sh B. insularis is endemic and the lone memberof its genus on the mid-Atlantic Ridge islands (Fig. 1c),

although its sister species B. pulchellus crossed the tropicalAtlantic (Fig. 1e). It is unlikely that two or more consecu-tive and successful colonizations can occur. The presence ofvarious species at oceanic islands is thus to be seen asre¯ecting the species' ability to disperse and colonize, not asa pre-requisite for further transport.

There has been an increasing attention given to theevolutionary signi®cance of dispersal and retention of earlylife-history stage (e.g. Jones et al., 1999; Swearer et al.,1999). Overall, reef ®sh seem to have evolved and success-fully dealt with the dispersion/retention duality. As evi-denced by established populations at geologically recentvolcanic islands such as Ascension (1.5 Myr) and bytransoceanic vagrants, species may be dispersed far away,thus colonizing new areas and avoiding extinction. How-ever, mass recruitment is essentially local (Jones et al., 1999;Swearer et al., 1999). Recruitment in isolated environmentsnot only allows the persistence of endemic populations(Robertson, 2001), but also may permit allopatric speci-ation. A notable example is the possibly on-going differen-tiation of Holacanthus ciliaris (Fig. 2a±b) and Chromismultilineata (Guichenot) through possible founder effectsand inbreeding at St Paul's (cf. Edwards & Lubbock, 1983).It would be of interest to know if H. ciliaris colour morphsperceive themselves as different `species', as they apparentlyoccupy different microhabitats (B. Feitoza and Osmar LuizJr, pers. comm.).

The type of spawning mode and the larval duration of theplanktonic phase are often assumed to be major constraintson the dispersal abilities of marine species (see review inSale, 1991, for a counter-example see Victor & Wellington,2000). Among the Brazilian endemic reef ®shes, 74% aresmall benthic demersal spawners, which evidently could notreadily transgress the Amazon barrier (Floeter & Gasparini,2000). A duality is readily apparent on oceanic islandswhere benthic spawners are more frequently endemic(through lack of genetic input), and pelagic spawnersproportionately more speciose (through higher dispersal),than at continental shelves (Floeter & Gasparini, 2000).Recent expeditions to St Paul's Rocks (B. Feitoza et al.,unpubl. data) noted the rarefaction of the semi-albinoticsH. ciliaris, and the comparatively higher abundance of thelocal blue morph (Fig. 2a) (cf. also Lubbock & Edwards,1981). That such island populations can undergo large¯uctuations within a few years appears to illustrate thatreversal to ancestral population composition is unlikelywithout integrating new immigrants. Thus, concurrentlywith the high-observed frequency of vagrants, we infer thatlong-distance dispersal processes are more common thangenerally predicted. For both pelagic and benthic spawners,however, short route dispersal would be eased by thepresence of stepping stones, and the south-western Atlanticis no exception to the rule. Trindade Island presents higherreef ®sh diversity than would be expected from its distancefrom the coast because of the seamounts of the Vito ria-Trindade chain (Gasparini & Floeter, 2001). Further north,St Paul's Rocks' ichthyofauna could be considered as animpoverished caricature of Fernando de Noronha (Fig. 1h),

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Biogeography of tropical reef ®shes 837

thus showing the dependency of the former's fauna to thelatter's colonization.

Long-term success of colonists

Some of the observed features cannot easily be linked todispersal abilities or possible routes. Of special interest is theabsence of the family Acanthuridae (surgeon®shes) fromSt Paul's Rocks, probably the only tropical island in theworld missing this conspicuous reef associated family(Floeter et al., 2001). Similarly, the wide-ranging butter¯y-®sh Chaetodon striatus and the hog®sh B. pulchellus werenot recorded at Atol das Rocas while both are present inneighbouring Fernando de Noronha. These local absencescould be related to the small size of the islands, and thushabitat availability together with possible post-settlement

dif®culties. The genus Scarus (family Scaridae), which occursat oceanic sites in the Indo-Paci®c and North Atlantic(Smith-Vaniz et al., 1999), is absent from the South Atlanticoceanic islands. On the other hand, all four scarid speciesthat do occur on South Atlantic oceanic islands belong to thegenus Sparisoma. This pattern could re¯ect the broaderfeeding habits of this genus (Bernardi et al., 2000). TheFrench angel®sh P. paru is common in the Caribbean, on theBrazilian coast, Atol das Rocas, Fernando de Noronha andSt Paul's Rocks. Surprisingly, on Trindade Island this speciesis apparently replaced by H. tricolor. The island is the onlyone in the South Atlantic that harbors a resident H. tricolorpopulation (Gasparini & Floeter, 2001). These pelagic-spawning species certainly do not have larval dispersalrestrictions, because the acanthurids, C. striatus, B. pulchel-lus and P. paru have successfully colonized very isolated sites

Figure 2 Holacanthus ciliaris colourmorphs from St Paul's Rocks: (a) blue morph,and (b) semi-albinotic morph. In situ photo-graphs by Osmar Luiz Jr.

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838 J.-C. Joyeux et al.

such as Ascension, Bermuda, and Africa. Thus, specialecological requirements for proper larval or post-settlementdevelopment, including habitat and predation rates, pre-sumably determine the long-term success of colonists.

It has been argued that competition could hinder orprevent colonization of high diversity locations. EasternPaci®c ®sh and gastropod species have apparently beenunable to colonize the Indo-western Paci®c, while theopposite is frequent (Vermeij & Rosenberg, 1993; Briggs,1995). As is known from shell-bearing mollusks (cf. Vermeij& Rosenberg, 1993), western Atlantic ®shes that havecolonized Africa generally have extremely limited distribu-tions in the eastern Atlantic (Briggs, 1995) (Fig. 1d and e),most often occurring on the offshore islands of Cape Verdeand SaÄo Tome archipelago, where competition is probablylower.

Extinctions are usually believed to be rare events occurringonly on a long time-span. Even in the smallest and mostisolated islands, endemic ®shes have survived through evolu-tionary time under very restricted areas in high-risk situations(Robertson, 2001). However, local extinction processes ofapparently established populations are probably more fre-quent than generally expected. Historical disappearance orsevere decline of population of reef ®sh species caused bynatural (e.g. El NinÄo) or man-made disturbance (e.g. reefdegradation, intensive aquarium collection, over®shing) isnow documented (Smith-Vaniz et al., 1999; Hawkins et al.,2000), and has been related to the restricted geographicalrange of the species (Hawkins et al., 2000). The survival ofpotentially valuable morphs or endemic species on south-western oceanic islands is under serious threat as theaquarium trade is moving in (J.L. Gasparini & S.R. Floeter,pers. obs.). Present-day distribution patterns may or may notprovide indications of the local long-term history of species.An interesting feature found in the western Atlantic is that ofspecies present in the entire Caribbean Basin but restricted tooffshore localities in the south-western Atlantic (Fig. 1i).Assuming the latter are relict populations from a oncewidespread distribution, the pattern does not ®t with theobservation that generally the northern component of adisjunct antitropical or antiequatorial population is the ®rstto disappear (Briggs, 1995). However, one can argue thatinferences from observations in the Paci®c are dif®cult totranspose into the Atlantic because the West Indies areconsiderably more extensive and diverse than the Brazilianprovince and thus more ef®cient at providing tropical habitatsafter range reduction, especially during glacial periods.

CONCLUSIONS

The puzzling patterns of distribution found in the SouthAtlantic seem primarily the outcome of allopatric speciationand of the interaction of long distance dispersal abilities andecological processes. One emerging idea is that persistenceability or settlement preferences (see OÈ hman et al., 1998) aremore important than dispersal ability. Given enough timemany species can reach extremely isolated reefs. Thedocumented arrival of vagrants clearly indicates this capa-

bility, even within the short period of recent scienti®cinvestigations. However, not all vagrants can complete theirlife history there. No stepping stones are required alongtransoceanic routes because of the rarity of consecutivecolonizations. However, intermediate stopovers are persist-ently used along short routes. Finally, some patterns cannotbe given a satisfactory explanation. For example, why thespot®n hog®sh B. pulchellus is present at the SaÄo TomeÂarchipelago when its closest relative (Sazima & Gasparini,1999), and always sympatric, the Spanish hog®sh B. rufus isnot? Just chance?

The puzzle will certainly remain unclear for a long time. Agreat effort will be required to resolve central issues such asthe importance of speciation, long distance transport,colonization success, etc. that shaped the biogeography ofSouth Atlantic reef ®shes.

ACKNOWLEDGMENTS

This study is dedicated to John C. Briggs for his lifetimecontribution to the science of biogeography and for inspiringmany generations of researchers. The work greatly bene®tedfrom discussions or comments on earlier drafts from thefollowing colleagues: John Brigg, Alasdair Edwards, Benja-min Victor, Brian Bowen, Julian Caley, Phil Munday, andHoward Choat. Unpublished information was kindly provi-ded by Bertran Feitoza (Universidade Federal da ParaõÂba,JoaÄo Pessoa, PB, Brazil), Osmar Luiz Jr, Luiz Rocha(University of Florida, Department of Fisheries and AquaticSciences, Gainesville, FL, USA), and Jacques Laborel (Che-min des grands Bassins, La Ciotat, France).

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BIOSKETCHES

Dr Jean-Christophe Joyeux is Professor of Ecology at theUniversidade Federal do EspõÂrito Santo and is currentlyleading various projects on larval ®sh ecology.

Sergio R. Floeter is a PhD candidate at the UniversidadeEstadual do Norte Fluminense. He is currently leading anmulti-institutional team to build a reference data base forthe tropical Atlantic reef ®shes.

Dr Carlos Eduardo L. Ferreira works as marine resear-cher at IEAPM Institute (Brazilian Navy), and has beendealing with various aspects of the ecology of Brazilianreefs and ®shes for more than a decade.

JoaÄo Luiz Gasparini is af®liated to the UniversidadeFederal do EspõÂrito Santo, and has worked for the last15 years on the taxonomy, systematics and naturalhistory of Brazilian reef ®shes.

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