The first record of the African Sergeant, Abudefduf hoefleri (Perciformes: Pomacentridae), in the Mediterranean Sea
© The Author(s) 2016
Received: 10 February 2016
Accepted: 22 February 2016
Published: 22 March 2016
This article has been peer reviewed and accepted at the previous publisher. The article was originally submitted on 18th October 2015, and originally accepted on 10th December 2015.
Alien fish species are increasing in the Mediterranean Sea, urging closer monitoring of coastal habitats and biodiversity towards achieving timely assessment and management. Among the alien fish species found in Maltese waters there are members of the Abudefduf genus.
Research work undertaken with the cooperation of fishermen allows for additional monitoring effort to record the presence of alien species and their possible impacts. One such alien fish specimen collected from Maltese waters in January 2014 was studied through morphological, meristic and genetic analyses. Mitochondrial DNA barcoding analyses were undertaken to confirm the species' identity given that the specimen found belonged to the genus Abudefduf which is composed of a number of congeners that have similar morphological characters.
Results and conclusion
This research led to the identification of the first record of the African Sergeant, Abudefduf hoefleri (Steindachner 1881) (Perciformes: Pomacentridae), in the Mediterranean Sea. This alien tropical species is native of the East Atlantic and may aggressively compete with native Mediterranean reef species for territories and resources.
KeywordsAfrican sergeant Abudefduf hoefleri Alien Morphometrics mtDNA barcoding Mediterranean Sea Malta
The Pomacentridae is a highly diverse family of reef fishes that primarily inhabit tropical and temperate shallow waters around the world (Allen & Woods 1980; Allen 1991; Bessa et al., 2007; Cooper et al., 2009; Feitosa et al., 2012; Litsios et al. 2012; Froese and Pauly 2013). Till a few years ago, the only representative of this Family in the Mediterranean Sea was the native Chromis chromis (Linnaeus 1758) which is distributed from the eastern Atlantic along the coast of Portugal to the Gulf of Guinea and throughout the Mediterranean Sea (Dulčić 2005; Froese & Pauly 2013). However, in the past two decades, alien species have been on the increase in the Mediterranean Sea (Coll et al., 2010; Golani et al., 2014), including species that are not natural migrants from neighbouring waters (Vacchi et al., 2010; Lipej et al., 2014; Vella et al., 2015 and 2015). Recent records of non-native Pomacentridae members in the Mediterranean include Chrysiptera cyanea (Quoy and Gaimard 1825) that was collected from the Gulf of Trieste, North Adriatic Sea (Lipej et al., 2014) and Stegastes variabilis (Castelnau 1855) that was recently caught from Maltese waters (Vella 2014a and 2014b; Vella et al., 2015a), in the central Mediterranean Sea.
The genus Abudefduf (Linnaeus, 1758) was first recorded in the Mediterranean in 1957 (Tardent, 1959), with several more recent records of A. vaigiensis (Goren & Galil, 1998; Vacchi & Chiantore, 2000; Golani et al., 2014; Vella 2014a and 2014b), and A. saxatilis (Azzurro et al., 2013; Vella 2014a and 2014b; Deidun & Castriota 2014; Tsadok et al., 2015) at various coastal locations around the Mediterranean. However, there have been no records of the African sergeant, A. hoefleri in this region. This fish is native to the tropical Eastern Atlantic region, ranging from Senegal to Benin, including Ilheu das Rolas, Sao Tome and Cape Verde (Loris & Rucabado 1990; Edwards et al., 2001; Cooper et al., 2009; Cowman & Bellwood, 2013), with its most northern records being the Canary Islands (Cooper et al., 2009; Triay-Portella et al., 2015).
Results and discussion
Measurements for the Abudefduf hoefleri specimen caught in Malta
A. hoefleri Specimen
Total length (mm)
Fork length (mm)
83.5 % TL
Standard length (mm)
73.1 % TL
Maximum body depth (mm)
54.3 % SL
Length of dorsal fin base (mm)
58.4 % SL
Pectoral fin base (mm)
10.2 % SL
Anal fin base (mm)
25.3 % SL
Pre-pelvic length (mm)
31.1 % SL
Pre-anal length (mm)
61.7 % SL
Pre-pectoral length (mm)
24.7 % SL
Head length (mm)
28.0 % SL
Pre-orbital length (mm)
8.1 % SL
Eye diameter (mm)
8.2 % SL
Depth of caudal peduncle (mm)
15.4 % SL
Meristics for the Abudefduf hoefleri specimen caught in Malta
Parameters measured for A. hoefleri specimen
Dorsal fin spines
Dorsal fin soft rays
Ventral fin spines
Ventral fin soft rays
Anal fin spines
Anal fin soft rays
Pectoral fin soft rays
Lateral line scales
Ongoing monitoring may verify the spread or loss of this non-indigenous species in these waters. The already at risk Mediterranean fish species (Coll et al. 2010) are being faced with increasing threats from alien species (Coll et al., 2015). As a member of the genus Abudefduf, this new alien can be aggressively competitive towards other fishes, therefore like other alien species its occurrence can have detrimental effects to coastal fishes communities with potential negative repercussions on marine conservation of local species.
On the 4th of January 2014 a specimen of A. hoefleri (Figs. 1 and 2) was caught in shallow coastal waters close to Delimara, Malta [GPS: 35.835260 N, 14.562635E] (Fig. 4) during sport-fishing being monitored by researchers from the Conservation Biology Research Group of the University of Malta. Upon capture the whole specimen was kept for scientific analyses. The diagnostic features that were used in the morphological identification of the specimen were analysed according to Allen (1991), Edwards et al. (2001), and Froese & Pauly (2013). All length measurements were taken to the nearest 0.1 mm using electronic calipers and mass was recorded to the nearest 0.01 g.
Tissue samples were collected from this specimen and preserved in 95 % ethanol. The specimen was subsequently deposited in the ichthyological collection of the Conservation Biology Research Group laboratory at the University of Malta with reference code number CBRG/F.140104/AH001. For genetic analyses, the tissue was digested with Proteinase K and the total DNA was extracted using AccuPrep® Genomic DNA Extraction Kit (Bioneer). PCR amplifications were carried out for: cytochrome c oxidase I gene (COI) using FishF2 and FishR2 primers (Ward et al., 2005); ATP synthase subunit 6 and its flanking protein coding genes (ATPase) using L8331 (Meyer 1993) and H9236 primers (Quenouille et al., 2004); NADH dehydrogenase subunit 3 and its flanking tRNA genes (nd3) using nd3-F270 and nd3-R750 primers (Cooper et al., 2009); cytochrome b (cytb) using GluDG-L14724 and CB3H-15560 primers (Martin and Palumbi 1993); and 12S to 16S ribosomal RNA genes (12S-16S) using 12SA and 16SA primers (Palumbi 1996). The amplification for each primer set was performed using an initial denaturation at 95 °C for 5 min, followed by 35 cycles of denaturation at 94 °C for 45 s, annealing at 52 °C for 45 s and extension at 72 °C for 40 s and a final extension at 72 °C for 10 min, except 12S-16S where an annealing temperature of 48 °C was used. The PCR products were purified and sequenced via ABI3730XL sequencer using both the forward and reverse primers. The sequences, at both nucleotide and amino acid level, were analyzed using Geneious v6.1.6 (http://www.geneious.com, Kearse et al., 2012). The sequences obtained were deposited in GenBank accession numbers KT374287-91 for COI, ATPase, nd3, cytb and 12S-16S respectively. These sequences were compared to other sequences available in genomic databases using BLASTn.
Various COI gene sequences for different Abudefduf species available in GenBank and BOLD, allowed for phylogenetic analyses of this specimen. The sequences were aligned using Geneious v6.1.6 (http://www.geneious.com, Kearse et al., 2012). A 549 bp sequence representing the smallest homologous COI sequence was selected and genetic divergences were calculated using the Kimura 2-parameter distance model (Kimura 1980), while the phylogenetic tree was constructed using 1500 bootstraps with Maximum Likelihood utilizing MEGA v5.2.1 Tamura et al. (2011).
Availability of supporting data
The genetic sequence data supporting the results of this article are available in GenBank, as accession numbers KT374287-91 for COI, ATPase, nd3, cytb and 12S-16S respectively.
Thanks are due to sport fishermen, in particular to Mr. S. Zammit who has cooperated with this research.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Allen GR. Damselfishes of the world. Melle, Germany: Mergus Publishers; 1991. 271.Google Scholar
- Allen GR, Woods LP. A review of the damselfish genus Stegastes from the Eastern Pacific with description of a new species. Records of the Western Australian Museum. 1980;8:171–98.Google Scholar
- Azzurro E, Broglio E, Maynou F, Bariche M. Citizen science detects the undetected: the case of Abudefduf saxatilis from the Mediterranean Sea. Management of Biological Invasions. 2013;4:167–70.View ArticleGoogle Scholar
- Bessa E, Dias JF, de Souza AM. Rare data on a rocky shore fish reproductive biology: sex ratio, length of first maturation and spawning period of Abudefduf saxatilis (Linnaeus, 1758) with notes on Stegastes variabilis spawning period (Perciformes: Pomacentridae) in São Paulo, Brazil. Braz J Oceanogr. 2007;55:199–206.View ArticleGoogle Scholar
- Coll M, Piroddi C, Steenbeek J, Kaschner K, Frida Ben Rais F, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T, Danovaro R, Estrada M, Froglia C, Galil BS, Gasol JM, Gertwagen R, Gil J, Guilhaumon F, Kesner-Reyes K, Kitsos MS, Koukouras A, Lampadariou N, Laxamana E, Lopez-Fede la Cuadra CM, Lotze HK, Martin D, Mouillot D, Oro D, Raicevich S, Rius-Barile J, Saiz-Salinas JI, San Vicente C, Somot S, Templado J, Turon X, Vafidis D, Villanueva R, Voultsiadou E. The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE. 2010;5:e11842.Google Scholar
- Coll M, Steenbeek J, Ben Rais Lasram F, Mouillot D, Cury P. 'Low-hanging fruit' for conservation of marine vertebrate species at risk in the Mediterranean Sea. Global Ecology and Biogeography. 2015;22:226–239.View ArticleGoogle Scholar
- Cooper W, Smith LL, Westneat MW. Exploring the radiation of a diverse reef fish family: phylogenetics of the damselfishes (Pomacentridae), with new classifications based on molecular analyses of all genera. Mol Phylogenet Evol. 2009;52:1–16.View ArticleGoogle Scholar
- Cowman PF, Bellwood DR. Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers. Proc R Soc Lond B Biol Sci. 2013;280:20131541.View ArticleGoogle Scholar
- Deidun A, Castriota L. First record of Abdudefduf cfr saxatilis Linnaeus, 1758 (Perciformes:Pomacentridae) from the Maltese Islands (Central Mediterranean). BioInvasions Records. 2014;3:53–6.View ArticleGoogle Scholar
- Dulčić J. Biometric properties of damselfish, Chromis chromis (Osteichthyes: Pomacentridae) from the middle Adriatic. Acta Adriat. 2005;46:91–8.Google Scholar
- Edwards AJ, Gill AC, Abohweyere P.O. A Revision of Irvine's Marine Fishes of Tropical West Africa. Darwin Initiative Report 2, Ref. 162/7/451. 2001. p. 157. http://www.ncl.ac.uk/tcmweb/tmr/Irvines_Marine_Fishes.PDF. Accessed 10th April 2013.
- Enemalta. Prediction of the Spread and Dilution of Cooling Water from Delimara Power Station; SLR global environmental solutions Report Ref. 403.0082.00022; 2011. 41. URL http://www.mepa.org.mt/lpgdocuments/thermal%20Model.pdf. Accessed 20th August 2015
- Feitosa JLL, Concentino AM, Teixeira SF, Ferreira BP. Food resource use by two territorial damselfish (Pomacentridae: Stegastes) on South-Western Atlantic algal-dominated reefs. J Sea Res. 2012;70:42–9.View ArticleGoogle Scholar
- Froese R. and Pauly D. FishBase. 2013. URL http://www.fishbase.org. Accessed 10th April 2013
- Galil BS. Shipwrecked – Shipping impacts on the biota of the Mediterranean Sea. Chapter 3. In: Davenport J, Davenport JL, editors. The Ecology of Transportation: Managing Mobility for the Environment. The Netherlands: Springer publishers; 2006. p. 392.Google Scholar
- Golani D. Colonization of the Mediterranean by Red Sea fishes via the Suez Canal- Lessepsian migration. In: Golani D, Appelbaum-Golani B, editors. Fish Invasions of the Mediterranean Sea: Change and Renewal. Sofia-Moscow: Pensoft Publishers; 2010. p. 145–88.Google Scholar
- Golani D, Orsi-Relini L, Massutí E, Quignard JP. CIESM - Atlas of Exotic Fishes - List [WWW Document]. 2014. URL http://www.ciesm.org/atlas/appendix1.html. Accessed 20th August 2015.
- Goren M, Galil BS. First record of the Indo-Pacific, coral-reef fish Abudefduf vaigiensis (Quay & Gaimad, 1825) in the Levant. Isr J Zool. 1998;44:57–9.Google Scholar
- Kalogirou S, Azzurro E, Bariche M. The Ongoing Shift of Mediterranean Coastal Fish Assemblages and the Spread of Non-Indigenous Species, Chapter 11. In A.G. Lameed (ed) Biodiversity Enrichment in a Diverse World, InTech;2012. 263–280. http://www.intechopen.com/books/biodiversity-enrichment-in-a-diverse-world/the-ongoing-shift-of-mediterranean-coastal-fish-assemblages-and-the-spread-of-non-indigenous-species. Accessed 20th August 2015
- Katsanevakis S, Coll M, Piroddi C, Steenbeek J, Ben Rais Lasram F, Zenetos A, Cardoso AC. Invading the Mediterranean Sea: biodiversity patterns shaped by human activities. Frontiers in Marine Science. 2014. doi:10.3389/fmars.2014.00032.
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.Google Scholar
- Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–20.View ArticleGoogle Scholar
- Lipej L, Mavri B, Dulcic J. First record of Chrysiptera cyanea (Quoy and Gaimard, 1825) (Perciformes: Pomacentridae) in the Mediterranean Sea. J Appl Ichthyol. 2014;30(5):1–3.View ArticleGoogle Scholar
- Litsios G, Pellissier L, Forest F, Lexer C, Pearman PB, Zimmermann NE, and Salamin N. Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae). Proc R Soc B Biol Sci. 2012;279:3662–9.Google Scholar
- Loris D, Rucabado J. Pomacentridae. In: Quéro JC, Hureau JC, Karrer C, Post A, Saldanha L, editors. Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). Volume 2. Lisbon: JNICT; 1990. p. 842–50. SEI, Paris; and UNESCO, Paris.Google Scholar
- Martin AP, Palumbi SR. Protein evolution in different cellular environments: cytochrome b in sharks and mammals. Mol Biol Evol. 1993;10:873–91.Google Scholar
- Meyer A., 1993. Evolution of mitochondrial DNA in fishes. In: Hochachka PW, Mommsen TP (Eds.), Biology Frontiers, Biochemistry and Molecular Biology of Fishes, vol. 2. Elsevier Science, Amsterdam, pp. 1–38.Google Scholar
- Occhipinti-Ambrogi A, Galil B. Marine alien species as an aspect of global change. Adv Oceanogr Limnol. 2010;1:199–218.View ArticleGoogle Scholar
- Occhipinti-Ambrogi A, Marchini A, Cantone G, Castelli A, Chimenz C, Cormaci M, Froglia C, Furnari G, Gambi MC, Giaccone G, Giangrande A, Gravili C, Mastrototaro F, Mazziotti C, Orsi-Relini L, Piraino S. Alien species along the Italian coasts: an overview. Biol Invasions. 2011;13:215–37.Google Scholar
- Palumbi SR. Nucleic Acids II: The Polymerase Chain Reaction. In: Hillis DM, Moritz C, Mable BK, editors. Molecular Systematics. Massachusetts: Sinauer Associates; 1996. p. 205–47.Google Scholar
- Quenouille B, Bermingham E, Planes S. Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol. 2004;31:66–88.View ArticleGoogle Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.View ArticleGoogle Scholar
- Tardent P. Capture d'un Abudefduf saxatilis vaigiensis Q. und G. (Pisces, Pomacentridae) dans le Golfe de Naples. Rev Suisse Zool. 1959;66:347–51.View ArticleGoogle Scholar
- Triay-Portella R, Pajuelo JG, Manent P, Espino F, Ruiz-Diaz R, Lorenzo JM, Gonzalez JA. New records of non-indigenous fishes (Perciformes and Tetraodontiformes) from the Canary Islands (north-eastern Atlantic). Cybium. 2015;39(3):163–74.Google Scholar
- Tsadok R, Rubin-Blum M, Shemesh E, Tchernov D. On the occurrence and identification of Abudefduf saxatilis (Linnaeus, 1758) in the easternmost Mediterranean Sea. Aquat Invasions. 2015;10:101–5.View ArticleGoogle Scholar
- Vacchi M, Chiantore MC. Abudefduf vaigiensis (Quoy & Gaimard, 1825): a tropical damselfish in Mediterranean Sea. Biologia Marina Mediterranea. 2000;7:841–3.Google Scholar
- Vacchi M, Psomadakis PN, Repetto N, Würtz M. First record of the dog snapper Lutjanus jocu in the Mediterranean Sea. J Fish Biol. 2010;76:723–8.View ArticleGoogle Scholar
- Vella A. Conservation research reports new alien species and declining local species in our sea. 2014a. The Maritime Directory Website news: http://www.maritimedirectory.com.mt/newsread.asp?l=e&ID=3037 issued on the 16th of January 2014. Accessed 10th May 2015.
- Vella A. Conservation research reports new alien species and declining local species in our sea. 2014b. The University of Malta Website news: http://www.um.edu.mt/newsoncampus/researchinitiatives/archive/newaliendeclininglocalspecies. Accessed 10th May 2015.
- Vella A, Agius Darmanin S, Vella N. Morphological and genetic barcoding study confirming the first Stegastes variabilis (Castelnau, 1855) report in the Mediterranean Sea. Marine Mediterranean Science. 2015a;16:609–12.View ArticleGoogle Scholar
- Vella A, Vella N, Agius Darmanin S. First record of Lutjanus fulviflamma (Osteichthyes: Lutjanidae) in the Mediterranean Sea. J Black Sea/Mediterranean Environment. 2015b;21:307–15.Google Scholar
- Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN. DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci. 2005;360:1847–57.View ArticleGoogle Scholar