| Ch eck Lis t biodiversity data > PENSUFT. NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (2): 379-385 https://doi.org/10.15560/14.2.379 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) Johnatas Adelir-Alves,' ? Marcelo Soeth,”? Raul Renno Braga,* Henry Louis Spach!-? 1 Programa de Pés-Graduacao em Zoologia, Universidade Federal do Parana, Campus Politécnico, Curitiba, PR, Brazil. 2 Programa de Pos- Gradua¢ao em Sistemas Costeiros e Oceanicos, Universidade Federal do Parana, Pontal do Parana, PR, Brazil. 3 Laboratorio de Ecologia de Peixes, Centro de Estudos do Mar. Universidade Federal do Parana, Pontal do Parana, PR, Brazil. 4 Laboratorio de Ecologia e Conserva¢ao, Depto de Engenharia Ambiental, Universidade Federal do Parana, Curitiba, PR, Brazil. Corresponding author: Johnatas Adelir-Alves, johnatas_alves@yahoo.com Abstract 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. Keywords Bioinvasions; reef fish; Bannerfish; Azores Chromis; citizen science; Brazil. Academic editor: Arturo Angulo | Received 13 December 2017 | Accepted 3 February 2018 | Published 23 March 2018 Citation: Adelir-Alves J, Soeth M, Braga RR, Spach HL (2018) 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). Check List 14 (2): 379-385. https://doi.org/10.15560/14.2.379 Introduction natural or anthropic processes (Wallace 1876, Carlton 1987). The introduction of non-native species by anthro- pogenic vectors is widely acknowledged to be one of the major threats to biodiversity and ecosystem function globally (Sutherland et al. 2010), including marine envi- 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 Junior et al. 2008, the journal of Leite et al. 2009, Anderson et al. 2015, Sampaio et al. 2016). Additionally, there are records of range expan- sions 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 ronments (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), Copyright Adelir-Alves et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unre- stricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 380 naturally distributed throughout the Indo-Pacific, has recently been recorded twice in Brazilian waters (Luiz et al. 2014). In addition, the Azores Chromis, Chromis lim- bata (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 popu- lations 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 (Fer- reira 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. acumina- tus 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 col- lected 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 bibliog- raphy from the Brazilian coast and the eastern Atlantic (native population). Results Order Perciformes Family Chaetodontidae Heniochus acuminatus (Linnaeus, 1758) New record. Brazil: off Parana state (PR), shipwreck, depth 27 m (25°53'50.47" S, 048°08'44.53" W), Eros Roberto, 4 March 2017, underwater video, 1 individual. Identification. The elongated fourth dorsal spine of spe- cies of the Heniochus Cuvier, 1816 distinguishes them from other chaetodontids (Tsadok et al. 2015). The spe- cies was identified by a combination of the body shape and coloration pattern (Fig. la): 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 pos- terior part of anal fin usually not extending anteriorly to longest soft ray; caudal fin and posterior part of dorsal fin yellow (Randall 1995, Froese and Pauly 2017). We do Check List 14 (2) not use the morphology (e.g. number of dorsal fin spines and finrays) because no specimen was collected. How- ever, 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 1s widespread throughout the Indo-Pacific Ocean. Remarks. The recent sighting of 1 individual of 4. acuminatus in Brazilian waters, reported here as a new record, was made by a recreational scuba diver (Fig. 1A). The first record in Brazil was 1n 1999 from Armacao dos Buzios (22°46'18.47" S, 041°53'11.53" W), state of Rio de Janeiro (RJ) (Moura et al. 2000). The second record, in 2013, was from Laje de Santos (SP) (24°19'11.62" S, 046°10'54.17" W) (Luiz et al. 2014). This is the south- ernmost one for this species in Brazil; it is approximately 300 km southwest of Laje de Santos (SP) and 800 km southwest of Armacao dos Buzios (RJ) (Fig. 2). Order Perciformes Family Pomacentridae Chromis limbata (Valenciennes, 1833) New records. Brazil: off Sao Paulo state (SP), ship- wreck of Laje de Santos, depth 22 m (25°53'50.47" S, 048°08'44.53" W), Antonio Pinna Neto, January 2017, underwater video, 1 individual. Santa Catarina state (SC), Tamboretes Archipelago, rocky reef, depth 10 m (26°22'45.20" S, 048°31'23.99" W), Johnatas Adelir- Alves, December 2015, dive survey, many individuals; Lobos Island, rocky reef, depth 17 m (26°30'53.05" S, 048°33'43.72" W), Johnatas Adelir-Alves, 1 July 2012, dive survey, | individual; Tacami Island, rocky reef, depth 12 m (28°21'07.31" S, 048°36'03.89" W), Johnatas Adelir-Alves, January 2017, dive survey, many indi- viduals; Parcel do Campo Bom, rocky reef, depth 10 m (28°42'21.30" S, 048°59'53.45" W), Daniel Marques, 24 August 2016, underwater video, many individuals. Rio Grande do Sul state (RS), Parcel de Torres, rocky reef, depth 30 m (29°34'50.10" S, 048°07'56.70" W), Hen- rique Santos Junior, 27 February 2017, underwater video, many individuals. Identification. Chromis limbata is identified by its color pattern (Table 1; Fig. 1b). Other diagnostic characters are listed in Table 1. Both morphological (Ichthyological Collection of the Museu de Historia Natural Capao da Imbuia no. 12327) and genetic (GenBank accession no. KT844434 to KT844464) studies confirmed the species occurrence in southwestern Atlantic waters (Leite et al. 2009, Anderson et al. 2017). Distribution. This natural range of this species includes the Macaronesian Islands and the west coast of Africa. Remarks. The compilation of C. /imbata records in south- western Atlantic Ocean extend more than 800 km along the coast of Brazil, from Cabras Island (23°49'50.88" Adelir-Alves et al. | Non-native reef fishes in the Southwest Atlantic Ocean 381 Figure 1. Heniochus acuminatus and Chromis limbata. A. H. acumi- natus (left/white arrow); photograph: Eros Roberto. B, C. C. limbata, reef at 30 m deep, Parcel de Torres, January 2015 (B) and January 2017 (C); photographs: Henrique Santos Junior. 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 litera- ture (Table 1). 25S} 24°S 26°S 28°S 30°S 52°W 50°W 48°W 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 weak- ens the natural-dispersal hypothesis. The aquarium trade is the most reasonable hypothesis, as this species is com- monly commercialized, and the sightings were near large Brazilian aquarium centers (Sampaio et al. 2015). All species of the genus Heniochus are allowed in the Brazil- ian 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 reluc- tant 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 Atlantic Ocean 46°W 44°W 42°W Figure 2. Records of Heniochus acuminatus: Armacao dos Buzios (RJ), Lage de Santos (SP), and Dianka shipwreck (PR), and the geographical distribution of Chromis limbata along Brazilian coast. 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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-Atlan- tic Barrier) separates the western and eastern Atlantic Ocean, and the cold waters to the south of Africa, in con- cert 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 dis- persal 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. /imbata along the Brazilian coast has been reported since 2008 (Leite et al. 2009, Silva et al. 2009), with population establishment, increased abun- dance, and dispersion to new sites (Figs lc, 2). A large increase in the population density from 0 to 6.4 individu- als m? occurred between 2010 and 2014 (Anderson et al. 2017). Viable populations of C. /imbata along the Brazil- ian 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. /imbata 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 (Fried- lander et al. 2014, Pajuelo et al. 2016). However, we cannot dismiss the possibility of a natural colonization, as 1s seen in other amphi-Atlantic species of pomacen- trids (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 suc- cessful 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 cya- nomos (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, conse- quently, 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 and Salagrama 2001, Kobori et al. 2015). These types of participatory research programs are being developed in many scientific disciplines with relevant applications to the marine sci- ences (Cambell and Salagrama 2001). The first record of lionfish in Brazil was made by citizen volunteers (Ferreira et al. 2015). Lionfish spe- cies 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 reduc- ing the biomass of lionfish by a quarter, which has been demonstrated to be a tool for controlling the populations of this invasive species (Leon 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 sci- ence can be an effective tool to monitor non-native reef fish along the Brazilian coast. 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