First Record of the Polychaetous Annelid Diopatra Micrura Pires Et Al., 2010 in the Mediterranean Sea A

Short Communication Mediterranean Marine Science Indexed in WoS (Web of Science, ISI Thomson) and SCOPUS The journal is available on line at http://www.medit-mar-sc.net DOI: http://dx.doi.org/10.12681/mms.377

First record of the polychaetous annelid Diopatra micrura Pires et al., 2010 in the Mediterranean Sea A. ARIAS1 and H. PAXTON2,3

1 Departamento de Biología de Organismos y Sistemas (Zoología), Universidad de Oviedo, Oviedo 33071, Spain 2 Department of Biological Sciences, MacquarieUniversity, Sydney, NSW 2109, Australia 3 Australian Museum, 6 College Street, Sydney, NSW 2010, Australia Corresponding author: [email protected] Handling Editor: Carlo Nike Bianchi

Received: 3 March 2013; Accepted: 25 June 2013; Published on line: 29 July 2013

Abstract

Until now the only recognised species of the onuphid genus Diopatra in the Mediterranean Sea was D. neapolitana. This paper reports on the presence of another species, D. micrura, in the western Mediterranean, occurring in shallow waters along the coasts of south-eastern Spain.

Keywords: Onuphidae, Iberian Peninsula, biodiversity, western Mediterranean.

Introduction Costa in Clarapède, 1868, previously described species for the Mediterranean, are considered subjective syno- Until very recently, the onuphid polychaete genus nyms of D. neapolitana (Read & Fauchald, 2013). Diopatra Audouin & Milne-Edwards, 1833 was thought Here we are reporting on the presence of D. micrura to be represented in Europe by only one species, D. nea- in the Mediterranean Sea, constituting the easternmost politana Delle Chiaje, 1841. These large worms are val- distribution for this species. We are presenting a diagno- ued as fish bait (Pires et al., 2012a) and have become sis of D. micrura, its relative abundance at the new lo- an exploited natural resource (Arias & Anadón, 2012), cality and compare the depths and substrate preferences stimulating a tremendous increase in biological research. of its original Portuguese habitat and the new Mediter- Diopatra species are ecosystem engineers, thought to un- ranean sites. Furthermore, we discuss and tabulate the dergo range shifts in Western Europe (Wethy & Woodin, distinguishing characteristics between D. micrura and D. 2008; Berke et al., 2010). Diopatra marocensis Paxton neapolitana. et al., 1995, previously only known from the Moroccan Atlantic coast, was reported from the coasts of Portugal (Rodrigues et al., 2009; Berke et al., 2010) and northern Materials and Methods Spain (Arias et al., 2010). The reproductive biology of D. neapolitana and D. marocensis was studied by Pires et al. In March 2012, a series of surveys were carried out (2012b; 2012c respectively) and Arias et al. (2013) who at an intertidal sandy cove near Cape Gata (36º57’N demonstrated that the Spanish Villaviciosa population 01º53’W), SE Spain, Mediterranean Sea (Fig. 1). Col- of the brooding D. marocensis was a simultaneous her- lected specimens were transported alive to the labora- maphrodite. With all this research activity, new species tory, anaesthetized in a 7.5% MgCl2 solution isotonic were discovered. Diopatra micrura Pires et al., 2010 was with seawater and extracted from their tubes (Fig. 2B); described from the western and southern coast of Portu- then, they were pre-fixed in 10% buffered formalin and gal (Pires et al., 2010), while D. biscayensis Fauchald preserved in 70% ethanol for later taxonomical analysis. et al. (2012) was described from western France and D. All specimens were measured (body length and width of cryptornata Fauchald et al. (2012) from the south-west- the 10th chaetiger) with callipers. Voucher specimens of ern Iberian Peninsula, increasing the number of Europe- D. micrura from these collections have been deposited at an Diopatra species to five (Fauchaldet al., 2012). the Invertebrate Collection of the Department of Biology Despite the recent increase of Diopatra species in of Organisms and Systems at the University of Oviedo Europe, D. neapolitana is the only Mediterranean rep- (Spain) (BOS-EUN 21; BOS-EUN 22). resentative, as D. baeri Grube, 1840 and D. iridicolor Five paratypes of D. micrura from Portugal, depos-

Medit. Mar. Sci., 15/1, 2014, 5-8 5 Fig. 1: Diopatra micrura - current distribution along the Ibe- rian Peninsula. Portuguese sites: A: Aveiro estuary; B: Nazaré; C: Tagus estuary; D Guadiana estuary (Pires et al., 2010). Spanish sites: E: Gata Cape; F: Valencia Harbour. ited at the National Museum of Natural Sciences, Ma- drid, Spain (MNCN 16.01/11627-16.01/11631) were examined to confirm identification of the Cape Gata specimens. Preserved specimens in the collections of the MNCN (MNCN16.01/1942-MNCN16.01/1961; MNCN16.01/2045- MNCN1601/2056; MNCN16.01/2641; MNCN16.01/2665; MNCN16.01/2671; MNCN1601/4339; MNCN1601/5942), previously identified as Diopatra neapolitana from the Spanish Mediterranean coast, between San Antonio Cape Fig. 2: (A) Anterior end of Diopatra micrura, dorsal view. (B) (38º48’N 00º08’W) and Valencia Harbour (39º27’N General view of D. micrura tubes, with attached shell frag- 00º19’W), collected on soft substrata (from muddy to fine ments and vegetal material. (C) Anterior end of live Diopatra neapolitana, dorsal view; (D) Dorsal colour pattern of anterior sands) from 5 m to 50 m depth (Redondo & San Martin, chaetigers of D. neapolitana. (E) D. neapolitana with it tube. 1997), were re-examined and identified asDiopatra micrura. Scale bars: A: 2 mm; B: 5 mm; C-D: 10 mm; E: 10 cm.

Results ish colour; antennostyles and palpostyles with conspicu- Diopatra micrura Pires et al., 2010 (Fig. 2A, B; Table 1) ous transverse iridescent white and brown bands, 12–15 Diopatra neapolitana – Rendondo & San Martín, brown ceratophoral rings; nuchal organs crescentic; sub- 1997; not Delle Chiaje, 1841 ulate to ovate ventral parapodial lobes on setigers 5 to Diagnosis: Small species; living specimens of green- 14–20; four pairs of modified parapodia with bidentate

Table 1. Comparison of diagnostic features between Diopatra micrura and D. neapolitana. Feature Diopatra micrura (Figure 2A, B) Diopatra neapolitana (Figure 2C-E) Maximum length of complete pre- 5 cm 60 cm served specimens Maximum width at chaetiger 10 4.5 mm 10 mm styles with transverse iridescent white and brown Colour pattern of palps and antennae styles with brown spots bands Colour pattern of peristomium darker than subsequent segments same colour as other segments Colour pattern of anterior chaetigers with two dorsal lateral brown patches each with one median brown bar Shape of nuchal grooves crescentic almost circular Appearance of subacicular hooks 8–13 19–25 Level of emergence of tube from sedi- several cm above sediment sediment level ments Ornamentation of tube shell fragments and seaweed incorporated into tube smooth silty, sandy tube

6 Medit. Mar. Sci., 15/1, 2014, 5-8 pseudocompound hooks with moderately long pointed for the Mediterranean representatives. In the intertidal re- appendages; pectinate chaetae with 5–10 long teeth; low- gion of the Aveiro estuary, D. micrura occurs sympatri- er limbate chaetae replaced by two bidentate subacicular cally with D. marocensis and D. neapolitana (Pires et al., hooks from chaetiger 8–13. Tube typical of genus. 2010), whereas in the Mediterranean study sites D. micru- Remarks: Specimens identified asD. neapolitana in ra was not found with other Diopatra species. the collections of the MNCN (registration numbers listed The presence of D. micrura in south-eastern Spain above) have been examined and re-identified as Diopat- brings the number of identified Mediterranean Diopatra ra micrura, thus demonstrating that the species has been species to two. However, Çinar et al. (2012) reported an present in the Mediterranean since at least 1996, the col- unidentifiedDiopatra sp. from Mersin Harbour and Sey- lection date. han estuary (Turkey), where it reaches high densities (ca. The material sampled in March 2012 near Cape Gata 90 specimens /m2). We expect that D. micrura is more was from an intertidal-shallow subtidal (2 m depth) fine widely distributed in the Mediterranean Sea and has at to medium sand community, where D. micrura reached times been misidentified as young specimens of D. nea- a density of ca. 4 individuals/m2. The size range of com- politana. A widespread sampling campaign and exami- plete specimens varied from 29 to 44 mm, and the av- nation of museum holdings would be required in order erage length was 35.9 mm (N= 10; SD= 4.41); average to document the real distribution of this species in the width of 10th chaetiger (without parapodia) was 1.58 mm Mediterranean Sea. (N=10; SD= 0.16). A key to the five European Diopatra species can be Acknowledgements found in Fauchald et al. (2012). Here we are focusing on the distinguishing characteristics between D. micrura We thank the two reviewers for their constructive and D. neapolitana (Table 1). The two species are closely criticism. A. A. is supported by a Severo Ochoa fellow- related and thus share a number of diagnostic parapodial ship from the FICYT Foundation (Principado de Astu- and chaetal characteristics. However, they can easily be rias, Spain). distinguished in that Diopatra micrura is a much smaller, slenderer species than D. neapolitana, which can reach at maximum size of 68 cm length (authors’ pers. obs.), References and in that their colour patterns are strikingly different. Diopatra micrura has antennae with iridescent white and Arias, A., Anadón, N., 2012. First record of Mercenaria mercenaria (Bivalvia: Veneridae) and Ensis directus (Bivalvia: brown bands, a brown peristomium that differs sharply Pharidae) on Bay of Biscay, Iberian Peninsula. Journal of from the immediate segments and two dorsal lateral Shellfish Research, 31, 57-60. brown patches on each of the anterior chaetigers (Fig- Arias, A., Anadón, N., Paxton, H., 2010. New records of Dio- ure 2A), while D. neapolitana has antennae with brown patra marocensis (Annelida: Onuphidae) from northern spots, a peristomium of the same colour as the subse- Spain. Zootaxa, 2691, 67-68. quent segments, and anterior chaetigers with one short Arias, A., Richter, A., Anadón N., Paxton, H., 2013. Evidence transverse mid-dorsal brown bar (Figure 2C-D). Other of simultaneous hermaphroditism in the brooding Diopat- differences concern the construction and ornamentation ra marocensis (Annelida: Onuphidae) from northern of their tubes, and the level of emergence from the sedi- Spain. Journal of the Marine Biological Association of ment. Diopatra micrura tubes stand out a few centime- the United Kingdom. In press. http://dx.doi.org/10.1017/ S002531541300012X tres from the sediment (with tube-cap) and are highly Berke, S.K., Mahon, A.R., Lima, F.P., Halanych, K.M., Wethey, ornamented with foreign material, mainly shells, shell- D.S. et al., 2010. Range shifts and species diversity in fragments and seaweeds, for most of the length of the marine ecosystem engineers: patterns and predictions for tube (Fig. 2B). On the other hand, D. neapolitana builds European sedimentary habitats. Global Ecology and Bio- its tubes at sediment level (without tube-cap) with scarce- geography, 19, 223-232. ly any ornamentation and they consist mostly of silt and Çinar, M.E., Katagan, T., Öztürk, B., Dagli, E., Açik, S. et fine sand, but may include some larger foreign material al., 2012. Spatio-temporal distributions of zoobenthos in near the opening (Fig. 2E). Mersin Bay (Levantine Sea, eastern Mediterranean) and the importance of alien species in benthic communities. Marine Biology Research, 8(10), 954-968. Discussion Fauchald, K., Berke S.K., Woodin S.A. 2012. Diopatra (Onu- phidae: Polychaeta) from intertidal sediments in south- Diopatra micrura occurs along the western and south- western Europe. Zootaxa, 3395, 47-58. ern Portuguese coasts, commonly in shallow waters of Pires, A., Freitas R., Quintino, V., Rodrigues, A.M., 2012a. Can mouths of major estuaries (Pires et al., 2010) (Fig. 1). The Diopatra neapolitana (Annelida: Onuphidae) regenerate Portuguese population seems to have a preference for fine body damage caused by bait digging or predation. Estua- rine, Coastal and Shelf Science, 110, 36-42. sand and shallow waters and the same seems to hold true Pires, A., Gentil, F., Quintino, V., Rodrigues, A.M., 2012b. Re-

Medit. Mar. Sci., 15/1, 2014, 5-8 7 productive biology of Diopatra neapolitana (Annelida, February 2013) Onuphidae), an exploited natural resource in Riade Aveiro Redondo, M. S., San Martín, G., 1997. Anélidos Poliquetos de (Northwestern Portugal). Marine Ecology, 33, 56-65. la costa comprendida entre el cabo de San Antonio y el Pires, A., Paxton, H., Quintino, V., Rodrigues, A.M., 2010. Puerto de Valencia. Publicaciones Especiales del Instituto Diopatra (Annelida: Onuphidae) diversity in European Español de Oceanografía, 23, 225-233. waters with the description of Diopatra micrura, new spe- Rodrigues, A.M., Pires, A., Mendo, S., Quintino, V., 2009. cies. Zootaxa, 2395, 17-33. Diopatra neapolitana and Diopatra marocensis from the Pires, A., Quintino V., Gentil F., Freitas R., Rodrigues, A.M., Portuguese coast: morphologicaland genetic comparison. 2012c. Reproductive biology of a brooding Diopatra spe- Estuarine, Coastal and Shelf Science, 85, 609-617. cies: Diopatra marocensis Paxton et al., 1995. Estuarine, Wethey, D.S., Woodin, S.A., 2008. Ecological hindcasting of Coastal and Shelf Science, 110, 85-92. biogeographic responses to climate change in the Euro- Read, G., Fauchald, K., 2013. World Polychaeta database. pean intertidal zone. Hydrobiologia, 606, 139-151. http://www.marinespecies.org/polychaeta (Accessed 27

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