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Bull Mar Sci. 90(0):000–000. 2014
http://dx.doi.org/10.5343/bms.2013.1046
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Far away from home: the occurrence of the
Heniochus acuminatus
Department of Biological
Sciences, Macquarie University,
NSW 2109, Sydney, Australia.
1
Instituto Laje Viva, Santos, SP,
Brazil.
2
Corresponding author email:
<[email protected]>.
*
Submitted: 29 May, 2013.
Accepted: 18 July, 2013.
Available Online: 3 September, 2013
Osmar J Luiz 1,2 *
Eric J Comin 2
Joshua S Madin 1
ABSTRACT.—The occurrence of the Indo-Pacific reef
fish Heniochus acuminatus (Linnaeus, 1758) is confirmed
for the southwestern Atlantic. A single adult individual
was photographed in a marine reserve off the southeastern
coast of Brazil. Two hypotheses explaining the species
occurrence are discussed: an aquarium release on the
Brazilian coast, and a long-distance dispersal from the
Indian Ocean into the Atlantic via South Africa.
Species invasion is a natural process that ultimately shapes the distribution
of life on earth (Elton 1958). Nevertheless, two emblematic cases of unnatural,
human-assisted reef fish invasions, the lionfish in the northwest Atlantic (Albins
and Hixon 2008) and the Lessepian fishes in the Mediterranean Sea (Belmaker et
al. 2013), have raised many questions about the detection of species outside their
natural ranges and their ecological impacts.
Here we provide the first photographic evidence of the longfin bannerfish,
Heniochus acuminatus (Linnaeus, 1758) (Perciformes: Chaetodontidae), in the
Atlantic Ocean, which was recorded in the Laje de Santos Marine Park, a marine
protected area located 36 km off the southeast coast of Brazil (Fig. 1). Heniochus
acuminatus is native to the Indo-Pacific region, where it is widespread and ranges broadly into subtropical and warm temperate zones (Kuiter 2002). A single
adult individual of approximately 20 cm total length was repeatedly observed and
photographed over several days at a depth of about 15 m at the same reef area.
The local setting is a transitional tropical-subtropical environment (Perry and
Larcombe 2003), where the reef habitat consists of granitic boulders covered by
patches of brown and red algae and a varied assemblage of sessile invertebrates,
including sparsely spaced colonies of the scleractinian corals Madracis decactis
(Lyman, 1859) and Mussismilia hispida (Verrill, 1902). This photographic record
validates a poorly-documented sighting of H. acuminatus made approximately
500 km northeast of our study site (Moura 2000).
Over the last decade, several Indo-Pacific reef fish species have been found
along the coast of Florida (USA), presumably as a consequence of aquarium releases (Schofield et al. 2009). Despite the presence of three other Heniochus species in Florida, H. acuminatus remains unrecorded in the northwest Atlantic. It is
Bulletin of Marine Science
© 2014 Rosenstiel School of Marine & Atmospheric Science of
the University of Miami
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Bulletin of Marine Science. Vol 90, No 0. 2014
Figure 1. An adult individual of the Indo-Pacific bannerfish Heniochus acuminatus (approximately 20 cm TL) recorded in February 2013 in the Laje de Santos Marine Park,
southeast Brazil and southwest Atlantic Ocean (24 15´S, 46 10´W).
therefore unlikely that the individual found in Brazil results from secondary dispersal from an established invasive population in the Atlantic. Two other mechanisms explaining the species presence are possible: (1) an aquarium release on
the Brazilian coast, which is plausible given the popularity of this species in the
aquarium trade worldwide, or (2) a long-distance dispersal of larval and/or postlarval stage individuals from the Indian Ocean into the Atlantic via South Africa.
Brazil is one of the five leading tropical aquarium fish exporters in the world
(Gasparini et al. 2005). The availability of native aquarium species means that
aquarium imports are uncommon, although imports do occur to supply specialized aquarium shops in major Brazilian cities. The observation of a single H. acuminatus adult, the lack of juveniles, and the proximity (approximately 150 km) of
the Laje de Santos Marine Park to São Paulo, the largest city in Brazil, provides
compelling evidence for the aquarium release hypothesis. However, this does not
invalidate the dispersal hypothesis. Previous records of non-native aquarium vagrants on the Brazilian coast are non-existent, which suggests that cheaper and
readily available native species are more popular than imported species. On the
other hand, recent transoceanic occurrences of vagrant adults of species that
are not associated with the aquarium trade have been detected in the southwest
Atlantic (Luiz et al. 2004, Leite et al. 2009), suggesting that shore fishes do occasionally breach the barrier imposed by the mid-Atlantic oceanic expanse (Luiz
et al. 2012).
Heniochus acuminatus is very common in the southwest Indian Ocean and
recorded far south off the east coast of South Africa, where it is found in great
numbers (Heemstra and Heemstra 2004). Exchanges of tropical marine organisms between the Indian and Atlantic oceans around the tip of South Africa were
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tightly constrained following the establishment of the Benguela upwelling system (about 2 Ma), which forms a cold-water barrier along the Atlantic coast of
southern Africa (Rocha et al. 2005). However, dispersal of reef fishes from the
Indian Ocean into the Atlantic has occurred, likely during warm interglacial periods (Rocha et al. 2005, Bowen et al. 2006). Planktonic larvae may be transported
westward in warm gyres that bud off from the Agulhas Current and become entrained in the northward-moving Benguela Current. These fast-moving gyres are
long lived and may facilitate the transport of warm-water species into the Atlantic
(Rocha et al. 2005). Phylogeographic analysis of two reef fish species groups that
have crossed from the Indian Ocean recently point to the existence of a dispersal
route into the Atlantic. This route typically extends to the mid-Atlantic islands
and often directly to the Brazilian coast (Rocha et al. 2005, Bowen et al. 2006).
Current transport from Africa to Brazil is estimated to take about 70 d (Bowen
et al. 2006), which is longer than the 40-d larval duration estimated for H. acuminatus (Wilson and McCormick 1999). However, association with floating rafts
can greatly enhance long-distance oceanic crossings (Luiz et al. 2012). Juveniles
of H. acuminatus have been observed swimming among floating seaweed mats in
Indonesia (R Kuiter, Zoonetics, Australia, pers comm), and the presence of drifting kelp rafts of South African origin among the mid-Atlantic islands (Edwards
and Glass 1987) confirms the availability of this dispersal route for raft-associated
species.
It is not currently possible to discern if the presence of H. acuminatus in Brazil
is the result of human-assisted introduction or rare long-distance dispersal. In
any case, the species is unlikely to become established, given the apparently low
frequency of migration or release. If the bannerfish were to become established
in Brazil, its presence is unlikely to have significant ecological impacts on native
species. Being a planktivore, H. acuminatus will not consume native fishes and,
because zooplankton is plentiful in the region, it is also unlikely to competitively displace native planktivores. Continuous monitoring of the individuals at the
study site will provide important information on the fate of expatriated tropical
marine fish species in Brazilian reefs.
ACKNOWLEDGMENTS
We thank R Kuiter and G Allen for confirming the identification of the species, R Kuiter
for providing unpublished information, and R Arévalo for the photograph used in this paper.
We also thank JE Serafy and three anonymous reviewers for comments in the manuscript.
LITERATURE CITED
Albins MA, Hixon MA. 2008. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser. 367:233–238. http://dx.doi.
org/10.3354/meps07620
Belmaker J, Parravicini V, Kulbicki M. 2013. Ecological traits and environmental affinity
explain Red Sea fish introduction into the Mediterranean. Global Change Biol. 19:1373–
1382. PMid:23505033. http://dx.doi.org/10.1111/gcb.12132
Bowen BW, Muss A, Rocha LA, Grant WS. 2006. Shallow mtDNA coalescence in Atlantic
pygmy angelfishes (genus Centropyge) indicates a recent invasion from the Indian Ocean.
J Hered. 97:1–12. PMid:16394255. http://dx.doi.org/10.1093/jhered/esj006
4
Bulletin of Marine Science. Vol 90, No 0. 2014
Edwards AJ, Glass CW. 1987. The fishes of Saint Helena Island, South Atlantic Ocean. I.
The shore fishes. J Nat Hist. 21:617–686. http://dx.doi.org/10.1080/00222938700770381
Elton C. 1958. The ecology of invasions by animals and plants. Methuen: London.
Gasparini JL, Floeter SR, Ferreira CEL, Sazima I. 2005. Marine ornamental trade in Brazil.
Biodivers Conserv. 14:2883–2889. http://dx.doi.org/10.1007/s10531-004-0222-1
Heemstra P, Heemstra E. 2004. Coastal fishes of Southern Africa. NISC/SAIAB:
Grahamstown.
Kuiter RH. 2002. Butterflyfishes, bannerfishes and their relatives: a comprehensive guide to
Chaetodontidae e Microcanthidae. TMC Publishing: Chorleywood, UK.
Leite JR, Bertoncini AA, Bueno L, Daros F, Alves J, Hostim-Silva M. 2009. The occurrence
of Azores Chromis, Chromis limbata in the south-western Atlantic. Mar Biodiv Rec.
2:e145. http://dx.doi.org/10.1017/S1755267209990637
Luiz OJ, Floeter SR, Gasparini JL, Ferreira CEL, Wirtz P. 2004. The occurrence of Acanthurus
monroviae (Perciformes: Acanthuridae) in the south-western Atlantic, with comments
of other eastern Atlantic reef fishes occurring in Brazil. J Fish Biol. 65:1173–1179. http://
dx.doi.org/10.1111/j.0022-1112.2004.00519.x
Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR. 2012. Ecological traits
influencing range expansion across large oceanic dispersal barriers: insights from
tropical Atlantic reef fishes. P Roy Soc B, Biol Sci. 279:1033–1040. PMid:21920979.
PMCid:PMC3259933. http://dx.doi.org/10.1098/rspb.2011.1525
Moura RL. 2000. Non-indigenous reef fishes in the southwestern Atlantic. Abstracts of the
9th Int Coral Reef Symp 1, 288.
Perry CT, Larcombe P. 2003. Marginal and non-reef-building coral environments. Coral
Reefs. 22:427–432. http://dx.doi.org/10.1007/s00338-003-0330-5
Rocha LA, Robertson DR, Rocha CR, Van Tassell JL, Craig MT, Bowen BW. 2005. Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol. 14:3921–3928.
PMid:16262848. http://dx.doi.org/10.1111/j.1365-294X.2005.02698.x
Schofield PJ, Morris JA Jr, Akins L. 2009. Field guide to nonindigenous marine fishes of
Florida. NOAA Tech Mem NOS NCCOS 92.
Wilson ST, McCormick MI. 1999. Microstructure of settlement-marks in the otoliths of
tropical reef fishes. Mar Biol. 134:29–41. http://dx.doi.org/10.1007/s002270050522
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