The occurrence of Acanthurus monroviae (Perciformes: Acanthuridae) in the south-western Atlantic, with comments on other eastern Atlantic reef fishes occurring in Brazil

Abstract

The presence of ‘vagrants’ of the eastern Atlantic surgeonfish Acanthurus monroviae is confirmed for the south‐eastern coast of Brazil. Three other species, Aulostomus strigosus(Aulostomidae), Parablennius pilicornis(Blenniidae) and Epinephelus marginatus(Serranidae) have apparently also crossed the Atlantic from east to west, whereas the great majority of ‘amphi‐Atlantic’ species appears to have their origin in the western Atlantic.

Full text

The occurrence of Acanthurus monroviae (Perciformes:
Acanthuridae) in the south-western Atlantic, with
comments on other eastern Atlantic reef fishes
occurring in Brazil
O. J. LUIZ-JU
´NIOR*†, S. R. FLOETER‡, J. L. GASPARINI§,
C. E. L. FERREIRA{AND P. WIRTZ**
*Instituto Laje Viva, Rua Aure
´lio So
´rio, 346, Praia do Guaiu
´ba, Guaruja
´, SP,
11421-130, Brazil, ‡National Center for Ecological Analysis and Synthesis, University
of California, Santa Barbara 735 State Street, Suite 300 Santa Barbara, CA
93101-5504, U.S.A., §Universidade Federal do Espı´rito Santo, Depto. de Ecologia e
Recursos Naturais, Vito
´ria, ES, 29060-900, Brazil, {Instituto de Estudos do Mar
Almirante Paulo Moreira (IEAPM), Departamento de Oceanografia, Rua Kioto
253, Arraial do Cabo, RJ, 28930-000, Brazil and **Centro de Cie
ˆncias do Mar,
Universidade do Algarve, Campus de Gambelas, 8000-17, Faro, Portugal
(Received 12 May 2003, Accepted 8 July 2004)
The presence of ‘vagrants’ of the eastern Atlantic surgeonfish Acanthurus monroviaeisconfirmed
for the south-eastern coast of Brazil. Three other species, Aulostomus strigosus (Aulostomidae),
Parablennius pilicornis (Blenniidae) and Epinephelus marginatus (Serranidae) have apparently also
crossed the Atlantic from east to west, whereas the great majority of ‘amphi-Atlantic’ species
appears to have their origin in the western Atlantic. #2004 The Fisheries Society of the British Isles
Key words: Acanthurus monroviae; amphi-Atlantic; biogeography; reef fishes.
Virtually all reef fishes have a pelagic larval stage (Johannes, 1978; Leis, 1991)
with a quite variable duration, ranging from a few days to several months (Leis,
1991). This life-history theoretically provides a powerful means of dispersal
among marine animals (Scheltema, 1968; Lessios et al., 1998). Geographic
barriers and ecological factors, however, may limit dispersal, reducing gene
flow between populations and promoting speciation (Palumbi, 1994; Rocha
et al., 2002). This creates areas with distinct species composition and levels of
endemism, known as biogeographic regions (Briggs, 1974; Floeter & Gasparini,
2000). The mid-Atlantic barrier, a broad expanse of open and deep water,
divides the tropical Atlantic Ocean into a western and eastern region (Briggs,
1974, 1995; Muss et al., 2001). Some species are occasionally seen outside their
†Author to whom correspondence should be addressed. Tel.: þ55 13 97211093; fax: þ55 11 40566514;
email: osmarluizjr@ig.com.br
Journal of Fish Biology (2004) 65, 1173–1179
doi:10.1111/j.1095-8649.2004.00519.x,availableonline at http://www.blackwell-synergy.com
1173
#2004 The Fisheries Society of the British Isles

normal geographic range, but without establishing viable populations in the
new area. These are referred to as ‘vagrants’ (Joyeux et al., 2001).
The African surgeon fish Acanthurus monroviae Steindachner is a conspicuous
reef fish that inhabits the tropical eastern Atlantic. It is known from the coast of
Morocco to South Africa (Randall, 1956; Desoutter, 1986), including the archi-
pelagos of Cape Verde [Fig. 1(a)] (Reiner, 1996), the Canaries (Brito et al., 2002)
and the island of Sa
˜o Tome
´in the Gulf of Guinea (Afonso et al., 1999). In the
last two decades, vagrants of A. monroviae were found in the western Mediter-
ranean, off the Spanish coast (Crespo et al., 1987), and in the eastern Mediter-
ranean on the coast of Israel (Golani & Sonin, 1996).
Recently, vagrant individuals of the African surgeonfish were detected at the
south-eastern coast of Brazil (Moura, 2000; O.J. Luiz-Ju´ nior, pers. obs.). In this
paper, the first photographic record for this species in the western Atlantic is
given [Fig. 1(b)]. The photograph was taken in the Parque Estadual Marinho da
Laje de Santos (Laje de Santos Marine State Park), a marine protected area
located 36 km south of the city of Santos, Sa
˜o Paulo State, Brazil (24150S;
46100W). The presence of A. monroviae in the south-western Atlantic Ocean
extends the known range of the species by >3900 km. The single individual of
c. 35–40 cm standard length (L
S
) was repeatedly observed at the main island of
the Laje de Santos Marine State Park. All encounters were in the same reef area
of c.50m
2
, suggesting a relatively small home range for this individual.
Although normally solitary, this particular animal was also seen joining a
school of Acanthurus chirurgus (Bloch) and feeding together with the members
of this group. The formation of interspecific groups is a common behaviour
among acanthurids (Lawson et al., 1999; Dias et al., 2001).
Despite the presence of the mid-Atlantic barrier, there are some species of
reef fishes that occur with established populations on both sides of the tropical
Atlantic (Briggs, 1974; Bernardi et al., 2000; Bowen et al., 2001; Joyeux et al.,
2001; Muss et al., 2001; Carlin et al., 2003). The geographic separation of such
populations may be explained by one of the two hypotheses: 1) at some point in
time the populations were continuous and subsequently separated by the for-
mation of unsuitable habitats inside their distributional range (vicariance) with-
out speciation, or 2) migrants from one population founded the other via long
distance dispersal (Platnick, 1976). The earliest fossil remains of acanthurids are
dated to the Lutetian (up to 52 million years ago) (Patterson, 1993), which
would have been when the Atlantic was quite young (Rosen, 1975). There is no
evidence, however, to show that A. monroviae was already present early on in
the development of the Atlantic. It is highly unlikely that the present day
populations were originally a single, continuous population before the separa-
tion between Africa and South America and that their species identity has been
maintained for such a long time without recent gene flow.
Assuming that the observed disjunct distributions are a result of dispersal
across the central Atlantic barrier, the origin of these ‘amphi-Atlantic’ fishes
(Briggs, 1974) may be inferred by analysing the distributional range of the
species. It is commonly assumed that the place of origin of a particular species
is where it reaches the largest area of occurrence (Briggs, 1974, 1995; Joyeux
et al., 2001; Moura & Sazima, 2003; Rocha, 2003). From an analysis of a
database of reef-associated amphi-Atlantic fishes (S.R. Floeter, pers. comm.),
1174 O. J. LUIZ-JU
´NIOR ET AL.
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179

FIG. 1. Reef-associated fishes which have migrated from the east to west Atlantic. (a) Acanthurus
monroviae from the Cape Verde Archipelago, eastern Atlantic (16000N; 24000W). November
1996. 10 m depth. (b) Acanthurus monroviae from the Laje de Santos Marine State Park, south-
eastern Brazil (24150S; 46100W). June 2002. 12 m depth. (c) Aulostomus strigosus at Cape Verde
Archipelago, eastern Atlantic (16000N; 24000W). September 1988. 15 m depth. (d) Aulostomus
strigosus from St Paul’s Rocks, an isolated island off north-eastern Brazil (00550N; 29210W).
November 1999. 20 m depth. (e) Epinephelus marginatus at Madeira Island (33800N; 17160W).
August 1990. 20 m depth. (f) Epinephelus marginatus from the Laje de Santos Marine State Park,
south-eastern Brazil (24150S; 46100W). May 2001. 6 m depth. (g) Female Parablennius pilicornis
from the Baleares Islands, Mediterranean Sea (38460N; 01260E). May 1994. 4 m depth. (h)
Female Parablennius pilicornis from the Laje de Santos Marine State Park, south-eastern Brazil
(24150S; 46100W). 10 m depth.
ACANTHURUS MONROVIAE IN THE WESTERN ATLANTIC 1175
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179

only four (37%) out of 106 that occur on hard bottoms (i.e. coral or rocky
reefs) appear to have migrated from east to west. Besides A. monroviae, the
other three species are: Aulostomus strigosus Wheeler, Epinephelus marginatus
(Lowe) and Parablennius pilicornis (Cuvier) (Fig. 1).
The best-documented case of westward migration across the Atlantic is that
of trumpetfish A. strigosus [Fig. 1(c), (d)]. A phylogeographic study of the genus
based on mtDNA analysis (Bowen et al., 2001) indicated that the Brazilian
trumpetfish are genetically identical to the eastern Atlantic trumpetfish, contra-
dicting previous studies which assumed that the Brazilian trumpetfish was the
Caribbean species Aulostomus maculatus Valenciennes (Wheeler, 1955; Lubbock
& Edwards, 1981; Randall, 1996). Wide ranging in the eastern Atlantic, from
Madeira to South Africa (Wheeler, 1955; Maul, 1959), A. strigosus established
large populations in the western Atlantic at the St Paul’s Rocks (Lubbock &
Edwards, 1981; Feitoza et al., 2003), an oceanic rocky formation off north-
eastern Brazil, and also on the coast of Espı
´rito Santo State (J.L. Gasparini &
S.R. Floeter, pers. obs.), in south-eastern Brazil. Individuals from both loca-
tions were analysed in the study by Bowen et al. (2001).
The second, more conspicuous and better-known putative east-to-west
migrant is the dusky grouper E. marginatus [Fig. 1(e), (f)] with records for the
Brazilian coast dating from the 19th century (Eschmeyer, 1998). The dusky
grouper occurs in almost all of the eastern Atlantic, from the British Isles to
South Africa, Mozambique in the Indian Ocean and in the Mediterranean Sea
(Heemstra & Randall, 1993). In the western Atlantic, its range is restricted to
the southern coast of South America, from Rio de Janeiro State south to
Argentina (Riguelet & Aramburu, 1960; Figueiredo & Menezes, 1980; Rico &
Acha, 2003). Heemstra (1991) examined specimens of E. marginatus from both
the eastern Atlantic and Brazilian coast and found no morphological differ-
ences. The northernmost established population of E. marginatus in the western
Atlantic is found in the Cabo Frio region (23440S), c. 150 km north of Rio de
Janeiro (Ferreira et al., 2001).
The ringneck blenny P. pilicornis [Fig. 1(g), (h)] is the fourth reef fish that is
probably a westward migrant. Its range includes the western Mediterranean Sea
and the eastern Atlantic Ocean, from the Bay of Biscay, Spain to South Africa,
(Zander, 1986; Bath, 1990; Almada et al., 2001). Bath (1977) revised the family
Blennidae and examined specimens of P. pilicornis from both the eastern
Atlantic and Brazilian coasts, including type specimens of Blennius ater Sauvage
and Blennius pantherinus Valenciennes, which are junior synonyms of P. pilicornis.
Bath (1977) found no morphological differences between the specimens
from the eastern and western Atlantic. In the western Atlantic, the range of
P. pilicornis is also limited to the southern South American region, including
Rio de Janeiro (Bath, 1977; Rangel, 1998), Sa
˜o Paulo and Santa Catarina
states (Barreiros et al., 2004; O.J. Luiz-Ju´ nior, pers. obs.) south to Patagonia
(Bath, 1977). Parablennius pilicornis is one of the most abundant fish species
in some shallow rocky reefs and tide pools of south-eastern Brazil (Ferreira
et al., 2001; Barreiros et al., 2004).
Despite observations of restricted gene flow across the mid-Atlantic barrier in
some shore fish species (Muss et al., 2001, Carlin et al., 2003) the lack of genetic
differences between the eastern and western populations of A. strigosus and the
1176 O. J. LUIZ-JU
´NIOR ET AL.
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179

recent recruitment of A. monroviae to south-eastern Brazil suggest that migra-
tion from east to west across the Atlantic can occur. Further genetic investiga-
tions on E. marginatus and P. pilicornis from both sides of the Atlantic are
required to test whether the morphologically similar specimens on each side of
the Atlantic are also genetically similar. Finally, the oceanographic barriers to
dispersal in the tropical Atlantic Ocean are expected to be variable in their
effectiveness over geological time (Rocha, 2003), and the effects of stochastic
climatic events on the ocean currents (Philander, 1986, Venegas et al., 1996,
Joyeux et al., 2001, Carlin, et al., 2003) could promote periods of favoured
dispersion alternating with periods of isolation.
We are very grateful for the invaluable field assistance provided by C. Benno de
Carvalho and the Centralmar Dive Center. L.A. Rocha, J.-C. Joyeux, C.A. Rangel and
J.P. Barreiros critically read the manuscript. We thank M. Augustowski for encouraging
the scientific investigation in Laje de Santos Marine Park. R. Patzner kindly provided the
photograph in Fig. 1(g). I. Harrison and two anonymous reviewers provided comments
that greatly improved the manuscript.
References
Afonso, P., Porteiro, F., Santos, R., Barreiros, J. P., Worms, J. & Wirtz, P. (1999).
Coastal marine fishes of Sa
˜o Tome
´Island (Gulf of Guinea). Arquipe
´lago 17A,
65–92.
Almada, V. C., Oliveira, R. F., Gonc¸ alves, E. J., Almeida, A. J., Santos, R. & Wirtz, P.
(2001). Patterns of diversity of the north-eastern Atlantic Blennid fauna (Pisces:
Blennidae). Global Ecology and Biogeography 10, 411–422.
Barreiros, J. P., Bertoncini, A., Machado, L., Hostim-Silva, M. & Santos, R. S. (2004).
Diversity and seasonal changes in the ichthyofauna of rocky tidal pools from Praia
Vermelha and Sa
˜o Roque, Santa Catarina, Brazil. Brazilian Archives of Biology
and Technology 47, 291–299.
Bath, H. (1977). Revision der Blenniini. Senckenbergiana Biologica 57, 167–234.
Bath, H. (1990). Blennidae. In Check-list of the Fishes of the Eastern Tropical Atlantic
(Que
´ro, J. C., Hureau, J. C., Karrer, C., Post, A. & Saldanha, L., eds), pp. 905–915.
Lisboa: JNICT.
Bernardi, G., Robertson, D. R., Clifton, K. E. & Azzurro, E. (2000). Molecular systematics,
zoogeography, and evolutionary ecology of the Atlantic parrotfish genus Sparisoma.
Molecular Phylogenetics and Evolution 15, 292–300.
Bowen, B. W., Bass, A. L., Rocha, L. A., Grant, W. S. & Robertson, D. R. (2001).
Phylogeography of the Trumpetfishes (Aulostomus): ring species complex on a
global scale. Evolution 55, 1029–1039.
Briggs, J. C. (1974). Marine Zoogeography. New York: McGraw-Hill.
Briggs, J. C. (1995) Global Biogeography. Amsterdam: Elsevier.
Brito, A., Pascual, P. J., Falcon, J. M., Sancho, A. & Gonzalez, A. (2002). Peces de las
Islas Canarias. Tenerife: Francisco Lemus Editor.
Carlin, J. L., Robertson, D. R. & Bowen, B. W. (2003). Ancient divergences and recent
connections in two tropical Atlantic reef fishes Epinephelus adscencionis and
Rypticus saponaceus (Percoidei: Serranidae). Marine Biology 143, 1057–1069.
Crespo, J., Rey, J. C. & Garcia, A. (1987). Primera cita de Acanthurus monroviae
Steindachner, 1876 y de Diodon eydouxii Brissout de Barneville, 1846 para la
ichthyofauna de Europa. Miscella
`nia Zoolo
`gica 11, 271–275.
Desoutter, M. (1986). Acanthuridae. In Fishes of the North-eastern Atlantic and the
Mediterranean, Vol. II (Whitehead, P. J. P., Bauchot, M. L., Hureau, J. C.,
Nielsen, J. & Tortonese, E., eds), pp. 262–263. Paris: Unesco.
ACANTHURUS MONROVIAE IN THE WESTERN ATLANTIC 1177
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179

Dias, T. L. P., Rosa, I. L. & Feitoza, B. M. (2001). Food resource and habitat sharing
by the three western south Atlantic surgeonfishes (Teleostei: Acanthurus) off
Paraı
´ba coast, north-eastern Brazil. Aqua, Journal of Ichthyology and Aquatic
Biology 5, 1–10.
Eschmeyer, W. N. (1998). Catalog of Fishes. San Francisco, CA: California Academy of
Sciences.
Feitoza, B. M., Rocha, L. A., Luiz-Ju´ nior, O. J., Floeter, S. R. & Gasparini, J. L. (2003).
Reef fishes of St. Paul’s Rocks: new records and notes on biology and zoogeography.
Aqua, Journal of Ichthyology and Aquatic Biology 7, 61–82.
Ferreira, C. E. L., Gonc¸ alves, J. E. A. & Coutinho, R. (2001). Community structure of
fishes and habitat complexity on a tropical rocky shore. Environmental Biology of
Fishes 61, 353–369.
Figueiredo, J. L. & Menezes, N. A. (1980). Manual de Peixes Marinhos do Sudeste do
Brasil: III. Teleostei (2).Sa
˜o Paulo: Museu de Zoologia da Universidade de Sa
˜o
Paulo.
Floeter, S. R. & Gasparini, J. L. (2000). The southwestern Atlantic reef fish fauna:
composition and zoogeographic patterns. Journal of Fish Biology 56, 1099–1114.
doi: 10.1006/jfbi.2000.1231
Golani, D. & Sonin, O. (1996). The occurrence of the tropical west African marine fishes
Acanthurus monroviae (Acanthuridae) and Arius parkii (Ariidae) in the Levant.
Aqua, Journal of Ichthyology and Aquatic Biology 2, 1–3.
Heemstra, P. C. (1991). A taxonomic revision of the eastern Atlantic groupers (Pisces:
Serranidae). Boletim do Museu Municipal de Funchal 43, 5–71.
Heemstra, P. C. & Randall, J. E. (1993). Groupers of the world. FAO Fisheries Synopsis
125, 1–124.
Johannes, R. E. (1978). Reproductive strategies of coastal marine fishes in the tropics.
Environmental Biology of Fishes 3, 65–84.
Joyeux, J.-C., Floeter, S. R., Ferreira, C. E. L. & Gasparini, J. L. (2001). Biogeography of
tropical reef fishes: the South Atlantic puzzle. Journal of Biogeography 28, 831–841.
Lawson, G. L., Kramer, D. L. & Hunte, W. (1999). Size-related habitat use and schooling
behaviour in two species of surgeonfish (Acanthurus bahianus and A. coeruleus)on
a fringing reef in Barbados, West Indies. Environmental Biology of Fishes 54, 19–33.
Leis, J. M. (1991). The pelagic stage of reef fishes: larval biology of coral reef fishes. In
The Ecology of Fishes on Coral Reefs (Sale, P. F., ed.), pp. 183–230. San Diego, CA:
Academic Press.
Lessios, H. A., Kessing, B. D. & Robertson D. R. (1998). Massive gene flow across the
world’s most potent marine biogeographic barrier. Proceedings of The Royal
Society of London, Series B 265, 583–588.
Lubbock, R. & Edwards, A. (1981). The fishes of St. Paul’s Rocks. Journal of Fish Biology
18, 135–157.
Maul, G. E. (1959). Aulostomus, a recent spontaneous settler in Madeiran waters.
Bocagiana 1, 1–18.
Moura, R. L. (2000). Non-indigenous reef fishes in the southwestern Atlantic. Abstracts
of the Ninth International Coral Reef Symposium 1, 288.
Moura, R. L. & Sazima, I. (2003). Species richness and endemism levels of the Brazilian
reef fish fauna. Proceedings of the Intenational Coral Reef Symposium 9, 956–959.
Muss, A., Robertson, D. R., Stepien, C. A., Wirtz, P. & Bowen, B. W. (2001).
Phylogeography of Ophioblennius: the role of ocean currents and geography in
reef fish evolution. Evolution 55, 561–572.
Palumbi, S. R. (1994). Genetic divergence, reproductive isolation, and marine speciation.
Annual Reviews of Ecology and Systematics 25, 547–572.
Patterson, C. (1993). Osteichthyes: Teleostei. In The Fossil Record, Vol. 2 (Benton, M. J.,
ed.), pp. 621–656. London: Chapman & Hall.
Philander, S. G. (1986). Unusual conditions in the tropical Atlantic Ocean. Nature 322,
236–238.
Platnick, N. (1976). Concepts of dispersal in historical biogeography. Systematic Zoology
25, 294–295.
1178 O. J. LUIZ-JU
´NIOR ET AL.
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179

Randall, J. E. (1956). A revision of the Surgeon Fish genus Acanthurus.Pacific Science 10,
159–235.
Randall, J. E. (1996). Caribbean Reef Fishes, 3rd edn. Neptune City, NJ: T.F.H.
Publications.
Rangel, C. A. (1998). Estudo Taxonoˆ mico da Famı
´lia Blennidae (Teleostei: Blennioidei)
em um trecho do Litoral Sudeste do Brasil, com o registro de duas novas ocorreˆ ncias.
Bs. Graduation Monography, Universidade Federal do Rio de Janeiro.
Reiner, F. (1996). Cata
´logo dos Peixes do Arquipe
´lago de Cabo Verde. Lisboa: Instituto
Portugueˆ s de Investigac¸ a
˜o Marı
´tima.
Rico, M. R. & Acha, E. M. (2003). Southernmost occurrence of Epinephelus marginatus
in the south-west Atlantic. Journal of Fish Biology 63, 1621–1624. doi: 10.1046/
j.1095-8649.2003.00271.x
Riguelet, R. A. & Aramburu, R. H. (1960). Peces marinos de la Republica Argentina.
Agro Publicacio
´nTe
´cnica 2, 1–141.
Rocha, L. A. (2003). Patterns of distribution and processes of speciation in Brazilian reef
fishes. Journal of Biogeography 30, 1161–1171.
Rocha, L. A., Robertson, D. R. & Bowen, B. W. (2002). Adult habitat preferences, larval
dispersal, and the comparative phylogeography of three Atlantic surgeonfishes
(Teleostei: Acanthuridae). Molecular Ecology 11, 243–252.
Rosen, D. E. (1975). A vicariance model of Caribbean biogeography. Systematic Zoology
24, 431–464.
Scheltema, R. S. (1968). Dispersal of larvae by equatorial ocean currents and its
importance to the zoogeography of shoal-water tropical species. Nature 217,
1159–1162.
Venegas, S. A., Mysak, L. A. & Straub, D. N. (1996). Evidence for interannual and
interdecadal climate variability in the south Atlantic. Geophysical Research Letters
23, 2673–2676.
Wheeler, A. C. (1955). A preliminary revision of the fishes of the genus Aulostomus.
Annual Magazine of Natural History, Zoology, Botany and Geology 12, 613–623.
Zander, C. D. (1986). Blennidae. In Fishes of the North-eastern Atlantic and the
Mediterranean, Vol. III (Whitehead, P. J. P., Bauchot, M. L., Hureau, J. C.,
Nielsen, J. & Tortonese, E., eds), pp. 1096–1112. Paris: Unesco.
ACANTHURUS MONROVIAE IN THE WESTERN ATLANTIC 1179
#2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 65, 1173–1179