diversity Opinion Persistent Gaps of Knowledge for Naming and Distinguishing Multiple Species of Crown-of-Thorns-Seastar in the Acanthaster planci Species Complex Gerhard Haszprunar 1,2,*, Catherine Vogler 3 and Gert Wörheide 3,4 1 Staatliche Naturwissenschaftliche Sammlungen Bayerns (SNSB)-Zoological State Collection, Münchhausenstraße 21, D-81247 Munich, Germany 2 Department Biology II and GeoBio-Center, Ludwig-Maximilians-Universität München, D-80539 Munich, Germany 3 Department of Earth and Environmental Sciences, Paleontology & Geobiology, and GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Straße 10, D-80333 Munich, Germany; [email protected] (C.V.); [email protected] (G.W.) 4 SNSB-Bavarian State Collections of Palaeontology and Geology, D-81827 Munich, Germany * Correspondence: [email protected]; Tel.: +49-89-8107-104 Academic Editors: Morgan Pratchett and Sven Uthicke Received: 19 September 2016; Accepted: 9 May 2017; Published: 12 May 2017 Abstract: Nearly a decade ago, DNA barcoding (partial mitochondrial COI gene sequences) showed that there are at least four species in the Indo-Pacific within what was previously conceived to be a single Crown-of-Thorns-Seastar (COTS) species, Acanthaster planci. Two of these species—A. planci Linnaeus, 1758, distributed in the North Indian Ocean, and A. mauritiensis de Loriol, 1885, distributed in the South Indian Ocean—have been already unequivocally named. In contrast, the Pacific COTS (proposed name: A. solaris (Schreber, 1795) and the COTS from the Red Sea (still to be named) require further taxonomic work. COI barcoding sequences and Barcode Identification Numbers (BINs) are available for all four COTS species in the global Barcode of Life Database (BOLD). We recommend depositing voucher specimens or tissue samples suitable for DNA analyses when studying any aspect of COTS, and use BINs to identify species, to ensure that no information is lost on species allocation until unequivocal Linnean names are available for the Pacific and Red Sea species as well. We also review the differences between COTS species with respect to morphology, ecology, and toxicity. Future studies should widen the current biogeographic coverage of the different COTS species by strategically sampling neglected areas, especially at the geographic distribution limits of each species, to enhance our understanding of the diversity of this reef coral predator. Keywords: COTS; taxonomy; Linnean names; DNA-barcodes; Barcode Index Numbers; biogeography 1. Introduction There is little doubt that the Crown-Of-Thorns-Seastar (COTS), usually referred to as Acanthaster planci (Linnaeus, 1758), with its corallivorous lifestyle and strong tendency to mass outbreaks, is one of the most serious threats to coral reefs throughout the Indo-Pacific marine biome, and numerous studies over the last decades have addressed all aspects concerning this point (reviewed in [1]). These circumstances have led to Acanthaster planci’s being the most researched and cited of all echinoderm species. For more than 250 years, researchers have noticed morphological differences among specimens of COTS from different geographical areas. Indeed, a number of taxa have been proposed, and these have Diversity 2017, 9, 22; doi:10.3390/d9020022 www.mdpi.com/journal/diversity Diversity 2017, 9, 22 2 of 10 circumstances have led to Acanthaster planci’s being the most researched and cited of all echinoderm species. Diversity 2017, 9, 22 2 of 10 For more than 250 years, researchers have noticed morphological differences among specimens of COTS from different geographical areas. Indeed, a number of taxa have been proposed, and these subsequentlyhave subsequently been merged been merged again or again split or further split furt (forher a review, (for a review, see [2]). see Currently, [2]). Currently, only one only other one species other asidespecies from asideAcanthaster from Acanthaster planci is uniformly planci is uniformly accepted asaccepted valid within as valid the within genus, Acanthasterthe genus, Acanthaster brevispinus Fisher,brevispinus 1917 Fisher, [3]. This 1917 species [3]. This does species not does feed not on coralfeed on and coral thus and does thus not does threaten not threaten coral coral reefs. reefs. Yet duringYet during the lastthe 30last years, 30 years, various various molecular molecular datasets datasets have have suggested suggested that thatAcanthaster Acanthaster planciplanci mightmight bebe more more than than a a single single species species [ 4[4–8].–8]. The The most most thorough thorough molecularmolecular andand phylogeographicphylogeographic studystudy thatthat includedincludedAcanthaster Acanthaster planci plancispecimens specimens acrossacross itsits entireentire Indo-PacificIndo-Pacific distributiondistribution rangerange (from(from thethe RedRed SeaSea to to Mauritius Mauritius and and the the Eastern Eastern Pacific) Pacific) revealedrevealed nonoless less thanthan fourfour deeplydeeply divergentdivergent cladesclades [[9].9]. TheThe “barcoding“barcoding fragment” fragment” of of the the mitochondrial mitochondrial COI COI gene gene showed showed high high inter-clade inter-clade divergence divergence (8.8–10.6%) (8.8%– compared10.6%) compared to <0.7% intra-cladeto <0.7% intra-clade divergence, divergence, strongly suggesting strongly thatsuggestingAcanthaster that planciAcanthasterrepresents planci a speciesrepresents complex a species with complex four different with four species different instead spec ofies a singleinstead one of a [9 single]. These one species [9]. These (and species we use (and the termwe use “species” the term henceforth) “species” showhenceforth) distinct show geographical distinct geographical distribution patternsdistribution across patterns the Indo-Pacific: across the oneIndo-Pacific: species might one species be restricted might be to restricted the Red Sea, to the one Red occurs Sea, one in the occurs Northern in the Northern Indian Ocean, Indian another Ocean, oneanother mainly one in mainly the Southern in the Southern Indian Ocean Indian (with Ocean the (with exception the exception of Northern of Northern Oman), Oman), and the and fourth the speciesfourth showsspecies a shows pan-Pacific a pan-Pacific distribution distribution (Table1 ;(Table Figure 1;1 ,Figure references 1, references [ 9–11]). [9–11]). Moreover, Moreover, the Pacific the speciesPacific showsspecies some shows internal some phylogeographic internal phylogeograp structurehic [12 structure–14], accordingly [12–14], itacco cannotrdingly be excludedit cannot that be additionalexcluded (sub-)speciesthat additional be discovered(sub-)species here be indiscov the futureered here using in higher-resolution the future using molecular higher-resolution markers, suchmolecular as SNPs. markers, such as SNPs. Figure 1. Geographic distribution of COI-barcoded species and of type localities of names (combined andFigure modified 1. Geographic from [2 distribution] and [9–11 ]:of COI-barcoded red—Red Sea spec (RS)ies species; and of type blue—South localities Indianof names Ocean (combined (SIO) speciesand modified (A. mauritiensis from [2]); and yellow—North [9–11]: red—Red Indian Sea Ocean (RS) species; (NIO) species blue—South (A. planci Indian); green—Pacific Ocean (SIO) species Ocean (PO)(A. mauritiensis species (A.); solarisyellow—North). Location Indian of type Ocean localities (NIO) ofspecies nominal (A. (sub-)species:planci); green—Pacific asterisk— OceanA. planci (PO); cross—speciesA. (A. echinites solaris;). triangle— Location A.of solaristype localities, square— ofA. nominal mauritiensis (sub-)species:; circle—A. asterisk— ellisii pseudoplanciA. planci; ;cross— “?”—theA. typeechinites locality; triangle— of A. ellisiiA. wassolaris not, square— specified:A. in mauritiensis South American; circle— watersA. ellisii of the pseudoplanci East Pacific.; “?”—the type locality of A. ellisii was not specified: in South American waters of the East Pacific. Diversity 2017, 9, 22 3 of 10 Table 1. Summary of Linnean nomenclature, Biological Index Number (BIN) and distribution of currently recognized Organismic Taxonomic Units (OTUs) of the Acanthaster planci species complex based on Vogler et al. [9–11] and Haszprunar & Spies [2]. See text for details. OTU (Vogler et al., NIO Species SIO Species Pacific Species Red Sea Species 2008 [9]) A. mauritiensis de Name [proposed] A. planci (Linnaeus, 1758) [A. solaris (Schreber, 1795)] NN (not yet named) Loriol, 1885 off Goa, Type locality off Mauritius Magellan Street, Philippines - West Indian coast BIN (BOLD) AAA1633 AAA1631 AAA1630 AAA1632 Synonyms [A. echinites (Ellis & A. ellisii (Gray, 1840) - - [proposed] Solander in Watt, 1786)] A. e. pseudoplanci Caso, 1962 South Indian Pacific Ocean and West Distribution North Indian Ocean Ocean (except West Red Sea Australian coast Australian coast ) Outbreak ability Yes yes Yes yes number of arms max. 23 max. 23 max. 23 max. 13–14 gray-green to gray-green to gray-purple, Specific color “electric-blue“ light blue to rusty gray-purple, bulls-eye bulls-eye appearance appearance Harmfulness to harmful harmful very harmful less harmful humans 2. Nomenclatorical Status and Problems When established in 2008, Vogler et al. [9–11] did not correlate the four species with any Linnean taxon names. This could explain why their results have not been considered in most studies on COTS biology and ecology published since then, despite the potential implications of these findings for COTS research and conservation. This unfortunate situation