Non-native reef fishes in the Southwest Atlantic Ocean : a recent record of Heniochus acuminatus ( Linnaeus , 1758 ) ( Perciformes , Chaetodontidae ) and biological aspects of Chromis limbata ( Valenciennes , 1833 ) ( Perciformes , Pomacentridae )

In the present paper, we document a recent record of the Bannerfish, Heniochus acuminatus, an Indo-Pacific species, in the southwest Atlantic Ocean and comment on biological aspects of the Azores Chromis, Chromis limbata, an invasive reef fish in the western Atlantic Ocean. We suggest that investigations of invasive species along the Brazilian coast can use data provided by citizen science, strengthening the non-native reef fish control strategies.


Introduction
Recent geographic range expansions of reef fishes from the northwestern Atlantic Ocean, the eastern Atlantic Ocean, and oceanic islands have been reported along the Brazilian coast (Luis et al. 2004, Vaske Júnior et al. 2008, Leite et al. 2009, Anderson et al. 2015, Sampaio et al. 2016).Additionally, there are records of range expansions for endemic Brazilian reef fishes into the northern and southern portions of the Brazilian biogeographic province and into the eastern Atlantic (Freitas et al. 2014, Anderson et al. 2015, Almeida et al. 2016).
Expansions of geographic ranges can occur through natural or anthropic processes (Wallace 1876, Carlton 1987).The introduction of non-native species by anthropogenic vectors is widely acknowledged to be one of the major threats to biodiversity and ecosystem function globally (Sutherland et al. 2010), including marine environments (Molnar et al. 2008).However, because of the connectivity of the ocean habitat, differentiating between natural long-distance dispersal and species introductions is not trivial (Luiz et al. 2014).
Whether they arrive by natural or anthropic vectors, new records of reef fish in Brazil still occur.For example, the Bannerfish, Heniochus acuminatus (Linnaeus 1758), naturally distributed throughout the Indo-Pacific, has recently been recorded twice in Brazilian waters (Luiz et al. 2014).In addition, the Azores Chromis, Chromis limbata (Valenciennes 1833), a native of the Macaronesian Islands and the west coast of Africa, was first recorded in Brazil in 2008 and has now successfully established populations in the western Atlantic (Leite et al. 2009, Anderson et al. 2017).These new records may be a result of the more intensive research efforts currently underway (Ferreira et al. 2009), which have increased our knowledge of the Brazilian reef fish fauna significantly in recent years.
Here, we describe a recent sighting of the H. acuminatus along the Brazilian coast and the update of C. limbata geographic distribution in the south western Atlantic Ocean.We then comment on the need for monitoring the occurrence and establishment of invasive species and their spread into Brazilian coastal waters.

Methods
Records of H. acuminatus and C. limbata were obtained through underwater visual censuses randomly distributed at various locations in southern Brazil (between 25°S and 28°S), published and unpublished data, and image records.Additional data were collected through videos posted on YouTube (see Kousha et al. 2012).Video and photographic authors were contacted for details and for permission to use their images.
For C. limbata, we checked the morphology of a collected and deposited specimen, reference MHNCI 12327 (Leite et al. 2009), and developed an external diagnosis for use with field observations.The biological data were based on underwater images and the available bibliography from the Brazilian coast and the eastern Atlantic (native population).
Identification.The elongated fourth dorsal spine of species of the Heniochus Cuvier, 1816 distinguishes them from other chaetodontids (Tsadok et al. 2015).The species was identified by a combination of the body shape and coloration pattern (Fig. 1a): body deep and snout pointed (longer than eye); ventral profile of head almost straight; dorsal spine very long; anal fin round; caudal fin truncate; snout and interorbital space black; body white with 2 pairs of diagonal black bands; black area on posterior part of anal fin usually not extending anteriorly to longest soft ray; caudal fin and posterior part of dorsal fin yellow (Randall 1995, Froese andPauly 2017).We do not use the morphology (e.g.number of dorsal fin spines and finrays) because no specimen was collected.However, the body and coloration pattern of this individual is consistent with that reported by previous authors for H. acuminatus off the Brazilian coast (Luiz et al. 2014) and this approach was adequate to confirm the identification.
Distribution.This species is widespread throughout the Indo-Pacific Ocean.

Chromis
Distribution.This natural range of this species includes the Macaronesian Islands and the west coast of Africa.
Remarks.The compilation of C. limbata records in southwestern Atlantic Ocean extend more than 800 km along the coast of Brazil, from Cabras Island (23°49′50.88″S, 045°23′36.02″W) to Parcel de Torres (29°34′50.10″S, 048°07′56.70″W) (Fig. 2).Complementary data on the biological aspects (e.g.depth range) observed for the Brazilian population agree with descriptions for the population in its native range compiled from the literature (Table 1).

Discussion
Both species reported here are invasive reef fish that have been recorded previously from Brazilian waters (Leite et al. 2009, Luiz et al. 2014).We present the third record of H. acuminatus (Fig. 1a) for southwestern Atlantic waters and data on the distribution of the Brazilian population of C. limbata (Fig. 1b, c).
Heniochus acuminatus is distributed all over the Indo-Pacific Ocean.The occurrence of this species in Brazilian waters is possibly due to a natural dispersal via South Africa or an aquarium release (Luis et al. 2014).The long distance from the Indo-Pacific to Brazil weakens the natural-dispersal hypothesis.The aquarium trade is the most reasonable hypothesis, as this species is commonly commercialized, and the sightings were near large Brazilian aquarium centers (Sampaio et al. 2015).All species of the genus Heniochus are allowed in the Brazilian aquarium trade (IBAMA 2008), and H. acuminatus is one of the most commonly traded butterflyfish species in the aquarium industry (Rocha et al. 2010).
Maintaining marine ornamental fish in aquaria is a popular hobby, and many aquarium owners are reluctant to kill their pets, so they end up releasing them into natural environments (Semmens et al. 2004).If this is the major vector of invasion, H. acuminatus could also soon be found in other places along the Brazilian coast.A recently established population of Heniocus sp. was   reported in the Mediterranean (Tsadok et al. 2015), and H. acuminatus is also considered to be new to Arabian Gulf waters (Jawad et al. 2014).
The western Atlantic Ocean is separated from the Caribbean by the freshwater outflow from the Orinoco and Amazon rivers (Amazon-Orinoco river plume).In addition, a large and deep oceanic barrier (the Mid-Atlantic Barrier) separates the western and eastern Atlantic Ocean, and the cold waters to the south of Africa, in concert with the Benguela Current, act as a barrier separating the Atlantic Ocean from the southern Indian Ocean (Luis et al. 2012, Floeter et al. 2008).While these barriers can be breached by reef fishes (Luis et al. 2004, Freitas et al. 2014) through natural (Rocha et al. 2005) or artificial dispersal mechanisms (Pajuelo et al. 2016), crossing these barriers via larvae dispersal or rafting with floating debris seems unlikely for an Indo-Pacific species.
The presence of C. limbata along the Brazilian coast has been reported since 2008 (Leite et al. 2009, Silva et al. 2009), with population establishment, increased abundance, and dispersion to new sites (Figs 1c,2).A large increase in the population density from 0 to 6.4 individuals m 2 occurred between 2010 and 2014 (Anderson et al. 2017).Viable populations of C. limbata along the Brazilian coast may be supported by the biological conditions observed in the underwater surveys.Populations of these species have been expanding both in numbers and range and it would not be surprising if additional increases in both range and population density along the Brazilian coast were observed in the next few years.
The introduction of C. limbata can be attributed to the movement of oil platforms between South America and the Canary Islands.Introduced non-native species have been reported on oil platforms around the world (Friedlander et al. 2014, Pajuelo et al. 2016).However, we cannot dismiss the possibility of a natural colonization, as is seen in other amphi-Atlantic species of pomacentrids (Wirtz et al. 2007, Occhipinti-Ambrogi et al. 2011).Chromis limbata is reported to have colonized new areas, expanding its geographic range into the eastern Atlantic by natural and anthropic processes (Vasco-Rodrigues et al. 2016, Pajuelo et al. 2016).
Chromis limbata represents a new case of the successful introduction of reef fish reported from the western Atlantic.The most disastrous and successful marine colonization ever documented in the Caribbean is that of the Indo-Pacific lionfish, Pterois miles (Bennett, 1828) and P. volitans (Linnaeus, 1758) (Morris and Whitfield 2009), while the most recent introduction reported is that of an Indo-Pacific damselfish Neopomacentrus cyanomos (Bleeker, 1856) (Robertson et al. 2016).Special concern should be given to aquatic species such as these, since once established, they become almost impossible to eradicate (Gozlan et al. 2010), as was seen with the establishment of Eastern Pacific coral species along the Brazilian coast (Sampaio et al. 2012).
Around the world, non-native species typically receive attention and are studied only after they have settled into a new environment (Alves et al. 2007).There are, however, a few studies about bioinvasions in the marine environments of Brazil that describe the occurrence and discuss the patterns of introduction (Gerhardinger et al. 2006, Ferreira et al. 2009).There is a trend towards an increasing number of bioinvasion events and, consequently, a need to monitor invasive species in natural areas in Brazil (Ferreira et al. 2009, Vitule 2012).Using underwater images taken by recreational divers and posted on the web (e.g.Youtube) and engaging the public in citizen science are low-cost monitoring strategies to collect data on invasive species (Cambell andSalagrama 2001, Kobori et al. 2015).These types of participatory research programs are being developed in many scientific disciplines with relevant applications to the marine sciences (Cambell and Salagrama 2001).
The first record of lionfish in Brazil was made by citizen volunteers (Ferreira et al. 2015).Lionfish species are among the most alarming invasive species in the Caribbean Region of the western Atlantic Ocean, and the data provided by citizen volunteers were effective in filling information gaps (Schofield 2009, Scyphers et al. 2015).Trained volunteer divers have been engaged in the control of lionfish by spearfishing off Bonaire and reducing the biomass of lionfish by a quarter, which has been demonstrated to be a tool for controlling the populations of this invasive species (León et al. 2013).
Research are needed to assess the distribution and abundance of non-native reef fish species.Monitoring the effects of non-native reef fishes on marine biodiversity, such as competition with native species, is also necessary.Increased knowledge can ensure the correct management of bioinvasions.We suggest data provided by citizen science can be an effective tool to monitor non-native reef fish along the Brazilian coast.

Table 1 .
Comparison of biological data for C. limbata between its occurrence areas in the Atlantic Ocean.Note: SL (standard length), D (number of dorsal fin spines and rays), A (number of anal fin spines and rays), P (number of pectoral fin rays) and V (number of ventral fin spines and rays).