Omobranchus punctatus (Teleostei: Blenniidae), an exotic blennyin the Southwestern Atlantic

Springer 2006

Biological Invasions (2006) 00:1–6 DOI 10.1007/s10530-005-5104-2

Invasion note

Omobranchus punctatus (Teleostei: Blenniidae), an exotic blenny in the Southwestern Atlantic Leopoldo Cavaleri Gerhardinger1,*, Matheus Oliveira Freitas1, A´thila Bertoncini Andrade1 & Carlos Augusto Rangel2 1

Instituto Vidamar, Sa˜o Francisco do Sul, Santa Catarina, 89240-000, Brazil; 2Departamento de Biologia Marinha, Universidade Federal Fluminense, Rua Outeiro Sa˜o Joa˜o Batista, S/N, C.P.100.644 Nitero´i, Rio de Janeiro, Brazil cep 24001-970; *Author for correspondence (e-mail: leocavaleri@gmail.com)

Received 1 November 2005; accepted in revised form 14 November 2005

Key words: alien species, ballast water, mariculture, offshore oilrigs, Omobranchus punctatus, ship fouling Abstract The muzzled blenny Omobranchus punctatus (Valenciennes), native to the Indo-Pacific region, is recorded in the Southwestern Atlantic coast, inhabiting natural and artificial substrates in the proximities of three large Brazilian seaports (states of Bahia, Rio de Janeiro and Santa Catarina). Due to its habitat and habits, the introduction of this species was probably by ship or oil rigs, presumably associated within fouling. It is also argued that the muzzled blenny can maintain populations in natural and artificial (mariculture facilities) coastal environments in the Southwestern Atlantic.

Abbreviations: MHNCI – Museu de Histo´ria Natural Capa˜o da Imbuia; LNEP-UFF – Laborato´rio de Ne´cton e Ecologia Pesqueira – Universidade Federal Fluminense

Introduction The muzzled blenny Omobranchus punctatus (Valenciennes) (Perciformes: Blenniidae) (Figure 1) is a coastal and brackish water benthic fish that can be found inhabiting the interstices of rock substrates and mangroves (Ismail and Clayton 1990). Its original distribution was presumed to be the Indo-Pacific region, ranging from Japan and Australia to the Persian Gulf (Golani 2004). Since the first record outside its presumed original distribution, in Trinidad and Tobago (Springer and Gomon 1975), the species has been identified in several other localities in the Atlantic Ocean such as Panama and Venezuela (Bath 1980; Lasso et al. 2004), as well

as in the Mediterranean Sea (Golani 2004) and in the Indian Ocean (Carlton 1985).

Wonham et al. (2000) attributed the invasive success of blennies and gobies to their cryptic behavior, as both seek refuge and lay eggs in small holes, which may predispose them to inhabit areas inside and around ports. These characteristics, together with their tolerance to salinity variations, allow them to take advantage of ballast-intake holes on ship hulls and offshore oilrigs.

Herein we report several recently found specimens of O. punctatus in the Southwestern Atlantic (Brazil) and comment upon the possible means of invasion and population maintenance in this region.

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Figure 1. Omobranchus punctatus (44.2 mm standard length; MHNCI 10776), collected from aquaculture structures near of the port of Sa˜o Francisco do Sul, Babitonga Bay, Southern Brazil. Photo by A. B. Andrade.

Materials and methods

Results

Specimens were collected in Ilha Grande Bay (22 50¢–23 20¢ S, 44 00¢–44 45¢ W), Rio de Janeiro state, Brazil, and Babitonga Bay (26 00¢– 26 40¢ S, 48 28¢–49 00¢ W), Santa Catarina state, Brazil (Figure 2). Vouchers are deposited at the ‘‘Museu de Histo´ria Natural Capa˜o da Imbuia’’ (MHNCI) and ‘‘Laborato´rio de Ne´cton e Ecologia Pesqueira – Universidade Federal Fluminense’’ (LNEP-UFF).

The Babitonga Bay represents one of the largest estuarine systems of Southern Brazil, encompassing a wide range of coastal habitats such as mangroves, salt marshes and rocky shores. The bay shelters one of the oldest and busiest ports of Southern Brazil, active since 1912.

The Ilha Grande Bay is a wide embayed coastal region sheltering several sandy beaches, rocky shores, mangroves and estuaries. This region encompasses a commercial port (active since 1923), oil and ore terminals, two nuclear plants and a shipyard. There is also an intense traffic of oilrigs that are brought to this area for repairing.

In April 2004, two specimens of Omobranchus punctatus were collected in shallow brackish and murky waters of a rocky shore near to a small mangrove at Ilha Grande Bay. The occurrence of this exotic species is relatively common at this mangrove area, co-inhabiting in the same habitat type with the frillfin goby Bathygobius aff. soporator (C. E. L. Ferreira, personal observation). In June/August 2004, six specimens of O. punctatus were collected from mussel culture structures (Perna perna), at depths of 1–2 meters in Babitonga Bay (Gerhardinger et al. 2005) (Figure 3).

Morphological patterns and meristic counts of the specimens collected in Brazil (Table 1) agree with the description of O. punctatus provided by Springer and Gomon (1975). All collected specimens of O. punctatus have the following diagnostic morphologic characteristics: small gill openings restricted to the sides of the head above the dorsal most level of the pectoral-fin base; head profile steep without cirri or crest; body elongated and compressed, with horizontal stripes.

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Figure 2. Several sites along the Brazilian coast where Omobranchus punctatus was registered near ports areas.

Discussion The introduction of O. punctatus in Trinidad and Tobago has been related to species transfer by slave boats from India to the West Indies in the early 19th Century (Springer and Gomon 1975). From this site on the species was considered to spread presumably in ballast water to the eastern entrance of the Panama Channel and to Venezuela (Walford and Wicklund

1973; Golani 2004). In the Mediterranean Sea its occurrence was presumed to be associated to ballast water, bilge water or ship fouling (Golani 2004). In this case, only one specimen was collected in Israel, and no stable population is known to exist. The occurrence of a population of O. punctatus in Mozambique was also considered to be a result of an introduction mediated by ballast water (Springer and Gomon 1975).

Table 1. Morphometric and meristic data from Omobranchus punctatus specimens collected in Brazil. Measurements are expressed as percentages of standard length, except orbit diameter (expressed as percentages of head length).

Museum numbers Location

Standard Head length Orbit Pectoral Pelvic Dorsal Anal Pectoral length (mm) (% SL) diameter fin length fin length soft rays soft rays rays

LNEP-UFF a 150 LNEP-UFF 150 MHNCI b 10764 MHNCI 10764 MHNCI 10776 MHNCI 10776 MHNCI 10776 MHNCI 10776

46.00 37.00 49.12 34.60 29.93 44.22 56.50 56.50

a b

Ilha Grande Bay Ilha Grande Bay Babitonga Bay Babitonga Bay Babitonga Bay Babitonga Bay Babitonga Bay Babitonga Bay

19.82 21.23 19.91 21.01 24.65 19.78 17.69 19.02

24.34 22.81 21.98 26.27 20.32 26.85 14.00 24.93

19.78 20.27 18.79 21.24 22.51 18.50 15.75 18.03

10.97 11.83 10.11 9.53 14.76 11.26 7.78 9.43

19 20 20 21 – 19 19 20

Speciments deposited at the Laborato´rio de Ne´cton e Ecologia Pesqueira – Universidade Federal Fluminense.

Specimens are deposited the Museu de Histo´ria Natural Capa˜o da Imbuia.

22 22 21 21 21 23 20 23

13 12 13 13 13 13 13 14

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Figure 3. Mussel maricultre field (Perna perna) where the specimens of Omobranchus punctatus were collected. Babitonga Bay shelters one of the busiest ports in the Southern Brazil. Photo by M. O. Freitas.

Mendonc¸a et al. (2005) reported on the occurrence of O. punctatus at Todos os Santos Bay, northeast coast of Brazil (they collected 90 specimens in 2002). They suggested that ballast water was the source of introduction at the Todos os Santos Bay. We indeed believe that ship fouling should be considered to a much greater extent as a potential vector in all three accounts of this exotic blenny in Brazil. Biofouling in ship hulls and oilrigs is receiving increasing concern as a source of exotic species introductions in the marine realm (Gollasch 2002).

In fact, Ferreira et al. (in press) cite that 22 out of 118 benthic species found in the fouling of drill-ships, oilrigs and cargo ships in Brazil were exotic to the Brazilian coast. C.E.L. Ferreira (personal communication) alerts that Brazilian native blennies such as Parablennius pilicornis were observed inhabiting ship hulls going to Argentina and Africa. We also hypothesize that the tessellated blenny Hypsoblennius invemar, which is very abundant around oilrigs and a few coastal sites (Hostim-Silva et al. 2002), might consist of an introduced species in the Brazilian coast. This species also has a cryptic nature, and is usually found hiding and nesting in empty barnacles (Megabalanus tintinabulum). This life trait

may facilitate invasion success as both adults and eggs sheltered inside empty barnacles may find favorable conditions to travel long distances.

It is reasonable to consider that geographical range extension may follow the introductions. To investigate this hypothesis, areas with similar habitats and areas close to other Brazilian ports should be monitored in order to verify O. punctatus occurrence. Its presence was not yet seen along the stretch of coastline between the infected sites and all three records in Brazil are close to large ports. Thus, we are inclined to suggest that this blenny was introduced by ship mediation.

The Ilha Grande Bay embraces a rich fauna and flora and is a sanctuary of singular biodiversity, located between the two largest metropolises of South America (Rio de Janeiro and Sa˜o Paulo). The region receives a large amount of cargo and oil ships. This environment can be perfect for invasions of a great number of organisms, such as the Indo-Pacific exotic coral of the genus Tubastrea Lesson, which was probably introduced in the area by ship or oilrig mediation (Figueira de Paula and Creed, 2004).

The Perna perna mussel is cultivated in Southern Brazil in vertical ropes displaced from the

5 water surface to approximately 2-meters depth.

These structures form a ‘‘novel habitat’’ which provides a complex and suitable substrate for recruitment and protection of small fishes and other marine organisms (Gerhardinger in press).

Golani (2004) has also registered O. punctatus in artificial substrates of fish culture placed in the proximity of a port in Israel.

We suggest that the identification of the ichthyofauna associated to artificial aquaculture structures near ports is an efficient means of obtaining data on fish invasions. Hewitt and Martin (2001) also point out the importance of surveying marine aquaculture facilities. They have showed that these structures have been responsible for the detection of 6–10% of the overall number of introduced species.

In contrast with the individuals collected in Babitonga Bay, specimens recorded in Ilha Grande Bay and in Northeastern Brazil were found in natural shallow waters. The high number of individuals collected in Northeastern Brazil (90 specimens on a broad range of size classes) also suggests that this species is capable of self-maintenance in natural environments. If this hypothesis is confirmed, mariculture structures in Babitonga Bay may be playing an important role in supporting populations of this species in natural environments. This is due to the increased availability of reproductive suitable habitats for the reproduction of blennies in mussel culture fields, such as empty mussel shells (Gerhardinger in press).

Omobranchus punctatus is highly tolerant to adverse environmental conditions. In Venezuela, Lasso et al. (2004) reported a self-reproducing population living between rocks in natural oil seeps, which were considered by them an ‘‘interesting fact from a physiological and ecological perspective’’. Despite the traditional invasive success of blennies (and in particular that of O. punctatus), we have no strong evidence to conclude whether this species is maintaining its population in Babitonga and Ilha Grande bays.

Brazil still does not have data or control of the volume of ballast water purged in it’s ports. It is estimated that about 40 thousand ships are circulating and 40 million tons of water are purged per year (Silva and Souza 2004). Ballast water has been responsible for the introduction of crus-

taceans, bivalve molluscs and corals (Silva and Souza 2004).

However, the lack of basic surveys in several natural environments, as well as in harbors and similar artificial substrates, makes a precise evaluation of the processes of exotic species introduction in Brazil difficult (Ferreira et al. in press).

According to Walford and Wicklund (1973), recording invasions is unavoidably occasional, because it depends in each instance on a systematic biologist of a particular specialty being at the right place at the right time. This old statement seems still to be valid in the Brazilian context of poor research effort directed towards exotic marine species.

The tremendous increase in shipping traffic since World War II and the increase in the speed of ships seem to coincide with the appearance of many exotic species throughout the globe (Walford and Wicklund 1973). Nowadays, there are world-wide debates on this very important topic.

Brazil was the second country to sign the ‘‘Convention for the Control and Management of Ships’ Ballast Water and Sediments’’. In order to anticipate the effects of the convention, which will take several years to be triggered, the Brazilian Navy is about to publish a new NORMAN (Brazilian Navy Authority Norms). This regulation will require ships to change ballast water at 200 nm from the coast and at 200 m depth, aiming to reduce the risks of introducing alien high success species into Brazilian waters.

Recently, surveyed sites in South America (Venezuela, Lasso et al. 2004) have already identified other exotic marine fish species introduction (e.g., the mud sleeper Butis koilomatodon: Eleotridae and the naked goby Gobiosoma bosc: Gobiidae) – two cryptic benthic species that may be considered as potential Brazilian invaders.

Thus, taxonomic surveys are urgently demanded, in and around harbors, as a mean to identify species introductions.

Acknowledgements We would like to thank ven by the aquaculture staff. We acknowledge Springer and Christine

all the field support giowners and respective Daniel Golani, Victor Marie V. Casal for

6 providing the relevant literature and invaluable help in the identification process. This manuscript was greatly improved by discussion and comments from Ricardo Corbetta, Alfredo Carvalho Filho, Carlos Eduardo Leite Ferreira, Hanson Leech, Fabrice Le Lorec, Mauricio HostimSilva, Vinicius Abilhoa and three anonymous referees. We acknowledge the field support from volunteers at Instituto Vidamar (http://www.vidamar.org.br) and financial support given by PROBIO, BIRD/GEF, MMA, CNPq to the project ‘‘Ilha Grande: um levantamento da biodiversidade’’.

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