The GlasgowNaturalist (2008) Volume 25, Part 1, 57-74 New records of copepods associated with ascidians from Scottish waters, including the description of a new species, Enterocola ooishiae n.sp. (Cyclopoida, Ascidicolidae), from a simple ascidian. Myles O’ Reilly Scottish Environment Protection Agency 5 Redwood Crescent, Peel Park, East Kilbride G74 5PP E-mail: [email protected] ABSTRACT the investigations of Thomas Scott for the Fishery New records are presented for over 20 species of Board of Scotland around one hundred years ago, copepods associated with ascidians, collected from which he summarised in a presentation to the Scottish waters over the last 20 years. These include Edinburgh Field Naturalist and Microscopical Society nine species of Notodelphyidae, seven of in 1907. Considerable knowledge of the ascidicolous Ascidicolidae, and six of Lichomolgidae. Among copepods from British waters has since been provided these Bonneriella altera, Bonneriella filipes, by Viv Gotto who produced the first identification key Botryllophilus aspinosus, Lichomolgidium cynthiae, in 1960 and subsequently added numerous new records Lichmolgus canui, and Zygomolgus didemni are to British and Irish waters as well as describing four recorded for the first time from Scottish waters. new species. Gotto’s synopsis (1993) of copepods Botryllophilus aspinosus has not been reported associated with marine invertebrates from the British anywhere since its type description in 1922. A note of Isles and surrounding seas included revised keys to an apparently new species ofBotryllophilus is provided over 60 ascidian-infesting species from the area. along with a revised key to the adult female Botryllophilus from British seas. A new species of The copepods recorded below were collected, mostly Enterocola collected from the Firth of Clyde is by the author, in the course of marine monitoring described. The genus Enterocola is reviewed and the surveys of benthic sediments. These surveys have key morphological features of the 21 species are already revealed a number ofcopepods associated with tabulated. A differential diagnosis ofthe new species, other invertebrates (O’Reilly 1995a,b, 1999, 2000a,b, Enterocola ooishiae, is given to distinguish it from 2001, O’Reilly et al. 2001). Ascidians were recovered similar species in the genus. The nomenclature of from rocks or sediment as an accidental by-catch of genderendings within the genus is also discussed. sampling by grab or trawl. The ascidians were identified as far as possible using Millar (1970) though specific identification of juvenile specimens was not INTRODUCTION always possible. Copepods have long been known as associates of ascidians. The Italian naturalist Francesco Redi All ascidians were fixed with formalin and observed such parasites inside ascidians as long ago as subsequently transferred to alcohol prior to laboratory 1684 (Damkaer, 2002,p.24-5). Since their initial dissection to search for copepods. Copepods were discovery, a diverse array of species have been examined in alcohol under a stereo microscope and, described inhabiting the branchial sac or the alimentary where necessary, were mounted in lactic acid and tract of both simple and compound ascidians. In many transferred to a compound microscope for more instances the copepods are visible through the body detailed observations. Permanent mounts were made of wall of their hosts. Several copepod species may some specimens in polyvinyl lactophenol. All occupy the same individual ascidian, along with other drawings were done with the aid of a camera lucida crustacean or bivalve co-habitees, prompting Gotto drawing tube. Accession numbers are shown for (1959b) to coin the term ascidian “hotel”. In a recent material deposited in the National Museum of study in the Ionian Sea, Pastore (2001), found 13 Scotland, Zoology (NMSZ). Classification used here copepod species representing five families and eight follows Gotto (1994) although some major revision of genera associated withjust two species ofascidian. ordinal and familial classification of copepods has & subsequently been undertaken by Boxshall Halsey In his account of the Crustacea of Norway, Sars (2004). (1917,1921) presented descriptions and detailed figures of 36 copepod species from ascidian hosts. Most records ofcopepods from Scottish ascidians stem from 57 ) ) Twenty one ovigerous females (NMSZ;2004.057.0001 New records ofasddicolous copepods from 16 Ciona intestinalis (also with 11 Lichomolgus furcillatus) collected in Ayr Bay, 30 Sept 1993 (SEPA OrderCyclopoida Stn.l3, 55°27.25’N, 04°40.3rw, depth 19m). Family Notodelphyidae Six ovigerous females (NMSZ:2004.057.0002) from Ascidiella aspersa trawled in Irvine Bay, 10 April 2002 Notodelphys agilis Thorell, 1859 (SEPA Stn.H, 55°35.92’N, 04°47.40’W, depth 38m). One ovigerous female and five juveniles from two In the Ayr Bay specimens the external seta on the Ascidiella aspersa, (also with 22 Doropygella psyllus, caudal ramus is positioned about one-third (rather then three Ascidicola rosea) collected in Barcaldine Bay, two-fifths) from the end. In the Irvine Bay material the Loch Creran, 21 June 1988, (SEPA Stn.DS, brood pouch is distended posteriorly into two 56“32.22’N, 05“18.63’W, depth 11m). pronounced symmetrical lobes (Fig. lb). In Scottish waters N.caerulea is recorded only from Shetland, by One mature female (NMSZ:2004.055.0001) found Brady (1878), although he did not consider its detached from host among sieve debris ofgrab sample separation from N.allmani well justified. Ciona collected at St Abbs sewage disposal grounds, Forth intestinalis appears to be a new host species for Sea area, 1990 (Stn.l, Sb^Ob-SG’N, 02°07.25’W, depth N.caerulea and the minor setal variation mentioned 50m). above may be anotherexample ofa host form. Four ovigerous females and two males Doropygellaporcicauda (Brady, 1878) (NMSZ:2004.055.0002) from two Ascidiella aspersal (also with 17 Lichomolgus albens) collected in Ayr One ovigerous female from Corella parallelogramma? Bay, 29 Sept 1993 (SEPA Stn.l, 55"28.88’N, (see above under N.agilis) collected in Irvine Bay, 28 04"04.40’W, depth 10m). Oct.1993 (SEPA Stn.Q2, 55°35.92’N, 04‘’44.15’W, depth 20m). Three ovigerous females and four males (NMSZ;2004.055.0003) from Corella parallelo- Two ovigerous females and one juvenile female grammal (also with one female Doropygella (NMSZ:2004.058.0001) from three Corella porcicaiida) collected in Irvine Bay, 28 Oct. 1993 parallelogramma? trawled in Irvine Bay, 10 April (SEPA Stn.Q2, 55°35.92’N, 04°44.15’W, depth 20m). 2002 (SEPA Stn.H, 55°35.92’N, 04‘’47.40’W, depth 38m). Of these one ovig. female accompanied by a N.agilis is widely recorded in British Waters. Scott female Ascidicola rosea and the single juvenile female (1907) highlighted previous records from both the accompanied by two male Lichomolgus canui. Firths ofClyde and Forth, and from Shetland. D.porcicauda is readily identified by the very long Notodelphys allmani Thorell, 1859 flexible caudal rami. In the Irvine Bay specimens these are gently curved (rather than curled as depicted by A single ovigerous female (NMSZ:2004.056.0001 Sars, 1921) but the copepods exhibit the characteristic from an Ascidiella spl, collected off Ironotter Point, dorsal ridges on thoracic segments 1-3. In one Greenock, 23 April 1992, (SEPA Stn.Hl, 55°58.29’N, specimen these ridges are very pronounced and bent 04°48.35’W, depth 22m, see O’Reilly etal. 1997). forwards and have numerous stalked ciliate protozoans attached (Fig. Ic). Scott (1900, 1907) cites the The Greenock specimen has an unusually prominent occurrence ofD.porcicauda in Loch Fyne and the Firth process on the inside ofthe seta on the distal extension ofForth. ofbasal segment ofthe fifth leg, and numerous (13-16) spinules on the inner margin (Pig. la). These features Doropygellapsyllus (Thorell, 1859) are very similar to N.allmani f.spinulosa, a variety described by Bocquet & Stock (1960), but the Twenty ovigerous females, two males and 1 1 juveniles elongated first endopodite segment of ''forma (NMSZ:2004.059.0001) from three Ascidiella spinulosa" is not evident. Although the specimen aspersa?, (also with four Ascidicola rosea and six would key as N.rufescens in Gotto (1993), it is N.agilis), collected in Barcaldine Bay, Loch Creran, 21 emphasized by Gotto that there may be considerable June 1988, (SEPA Stn.DS, 56°32.22’N, 05°18.63’W, difficulty in distinguishing different host forms among depth 1 Im). the "allmani-rufescens” complex Indeed as long ago . as 1878 some authors, such as Brady, regarded Two ovigerous females (NMSZ:2004.059.0002) from N.allmani and N.rufescens as synonymous. Clearly Ascidiella aspersa collected at Poll na Gile, Shuna further study in this area is required. Island, Loch Melfort, May 94. Notodelphys caerulea Thorell, 1859 58 Three ovigerous females from Ascidiella sp., collected A.typicus. It seems probable that these and other at Tobermory, Mull, Aug. 2001 (also with one Agnathaner records represent unknown males of ovigerous femaleAscidicola rosea.) various notodelphyids. Although the validity of the genus is doubtful, it has been retained by some authors Three ovigerous females from Ascidiella aspersa until the status of the various forms is clarified (see collected at Linne Mhurich, Loch Sween, November Holmes & Gotto, 2000). 2005. Botachus cylindratus Thorell, 1859 In Scotland Doropygella psyllus is known only from a single record (see Gotto, 1957). The record derives Sixteen gravid females, 10 immature females (NMSZ: from A.aspersa collected by Dr R.B.Pike from Loch 2006.111.0001), from Ascidiella aspersa collected in Sween, Kintyre in August 1946 (Gotto, pers.com.). Invasion Bay, Loch Sunart, 2003. Copepods found by Superficially Doropygella psyllus closely resembles P. Garwood. Doropygus pulex which has been recorded in Scotland from Shetland, Oban, Loch Fyne, and Millport (Scott, Widely distributed in Scottish waters. Scott (1907) 1907). The diagnostic feature distinguishing the two cites its occurrence in Shetlands, Orkneys, Oban, and species is the presence in the former ofsix setae (rather Loch Fyne. than two) on the endopodite ofthe maxillule (Mx.l) as figured by Sars (1921). However the D.psyllus from Bonnierilla altera Stock, 1967 Loch Creran appear to differ in that the endopodite of the maxillule is two-segmented with a total of seven Twenty four gravid females and 10 copepodites setae and the basis has only three (rather than four) (NMSZ:2004.061.0001) in Pyura microcosmus, 1 inner setae (Fig. Id). In practice D.psyllus can be more gravid female and 40 copepodites in a second readily separated from D.pulex, without examination of P.microcosmus (along with two Lichomolgidium the mouthparts, by the rounded (not pointed) brood cynthiae copepodites, see below), and 33 copepodites pouch, and by the minute (rather than prominent) (NMSZ:2004.061.0002) in a third P.microcosmus. terminal claw on the second antennae. Al! collected from South Shian, Loch Creran, Aug. 2001 (SEPA Stn. 100m Sth., 56"31.25’N, 05‘’23.86’W, Hamond (1973) provided a brief description of a new depth 7m). Doropygus-Wkt copepod which he called “Haplostome A” collected from Sidnyum turbinatum, from West In British waters B.altera is known only from the west Runton, Norfolk in 1957. Although the description is of Ireland (Holmes & Gotto, 1987). P.microcosmus is incomplete the cephalic and thoracic appendages are a new host species. quite different from both Doropygus and Doropygella. It is more primitive than most haplostomes and Bonnierillafilipes Stock, 1967 probably represents a new genus. As the single specimen no longer exists, its systematic position will One ovigerous female (NMSZ:2004.062.0001) from a remain uncertain until new material is discovered. Dendrodoa grossularia collected off Dipple, Girvan, However the postulate that it might be the (then Oct 2002 (SEPA Stn. LSO, 55°!7.25’N, 04"51.12’W, unknown) female of the genus Agnathaner now seems depth 15m). The host ascidian was examined shortly very unlikely (see discussion below under Pachypygus after fixation in formalin. The bright orange ova in the gibber). brood sac of the copepod made it clearly visible through the wall of the ascidian. The orange colour Pachypygusgibber (Thorell, 1859) faded after a few days. One mature female (NMSZ:2004.060.0001) from This species was initially described and figured from Ciona intestinalis collected off Ironotter Point, the Mediterranean by Illg & Dudley (1961), who Greenock, 23 April 1992. (SEPA Stn.Hl, 55“58.29’N, erroneously referred it to the African/Australian 04°48.35’W, depth 22m, see O’Reilly etal. 1997). species "'B.armata Schellenberg, 1922”. Stock (1967) realised that the Mediterranean copepods were in fact a The only previous Scottish record is from Tarbert new species which he named B.filipes. It was Bank, Loch Fyne (Scott, 1900). In a study of subsequently discovered on the west coast of Ireland morphological variation of P.gibber males, Hipeau- by Holmes & Gotto (1987). The Girvan specimen is Jacquotte (1980) realised that the atypical male form the first Scottish record. Although the eggs of the was identical toAgnathanerminutus Canu, 1892. Girvan specimen were orange, Illg & Dudley described the embryos in the brood sac as green. The genus Agnathaner was established by Canu in 1891 for A.typicus, and he added A.minutus the Family Ascidicolidae following year. Both were based on male specimens recovered from ascidians at Boulonnais, France. Ascidicola rosea Thorell, 1859 Hamond’s A.freemani, collected from Norfolk, was also based on a male which closely resembled 59 Five females (NMSZ:2004.063.0001) from several Two mature females from two Ciona intestinalis Ascidiella sp? collected at Bell Rock sewage disposal collected off Ironotter Point, Greenock, 23 April 1992. grounds, Forth Sea area, 27 Nov. 1987 (Stn.l3 & (SEPA Stn.Hl, 55“58.29’N, 04“48.35’W, depth 22m, Stn.C, see O’Reilly etah, 2001). see O’Reilly etal. 1997). H.eruca is a rarely recorded copepod initially described Three females and one juvenile from Shetland and subsequently found in the Firth of (NMSZ:2004.063.0002) from three Ascidiella Forth by T. & A. Scott (1892) and in southern Norway aspersa?, (also with 30 D.psylliis and six N.agilis, see by Sars (1921). Gotto (1959a) recovered a single above), collected in Barcaldine Bay, Loch Creran, 21 specimen from Strangford Lough, Northern Ireland, June 1988, (SEPA Stn.DS, 56“32.22’N, 05°18.63’W, and discussed some of the taxonomic confusion depth 1 1m). surrounding this species. The Clyde material is the first record in Scottish waters for 100 years and forms One female (NMSZ:2004.063.0003) from Ascidiella the basis of a re-description by Ooishi & O’Reilly spl, collected off Ironotter Point, Greenock, 23 April (2004). Three other Haplostoma species from British 1992, (SEPA Stn.Hl, 55°58.29’N, 04°48.35’W, depth waters have been re-described by Ooishi (1994, 22m, see O’Reilly etal. 1997). 2004a,b). Three females (NMSZ:2004.063.0004) from Ascidiella Botryllophilus aspinosus Schellenberg, 1922 scabra trawled in Ayr Bay, 30 Sept. 1992. Three mature females and two juveniles from five One female (NMSZ:2004.063.0005) from Ascidiella specimens of Polycarpa spl collected in Bay of aspersa, Loch Spelve, Mull, 1996 Puldrite, (approx. 59°02.7’N, 03“00.2’W, around 15 m deep), north of Kirkwall, Orkney Isles, June 2003 . One female (NMSZ:2004.063.0006) separated from The copepods were recovered by P.R. Garwood. host in sieve debris, Braer Survey, St. Magnus Bay, Shetland, collected 4 May 1993 (Stn.3, 60‘’23.44’N, B.aspinosus was originally recovered from Polycarpa 01°33.84”W, depth 146m) by Sue Hamilton. pomaria collected in Plymouth and also from Styela hupferi from Angola. It is rather poorly described and One female (NMSZ:2004.063.0007) from Ascidiella has never been seen since. Hence it was excluded from sp. (also with 1 Lichomolgus albens), Bogany Point, Gotto’s synopsis (1993). However, Illg & Dudley Rothesay, Isle of Bute, 6 June 2001, (SEPA Stn. 5, (1980), considered it well characterised and regarded it 55'’50.7rN, OS^OLSEW, depth 15m). as a valid species, although a modem redescription is needed. The discovery of new material has confirmed One female ovigerous from Ascidiella sp., Tobermory, their supposition and provided an opportunity to Mull, Aug. 2001 (also with three D.psyllus). present a full description. This will be the subject ofa future publication. One female ovigerous (NMSZ;2004.063.0008) from Ascidiella sp., collected off Dipple, Girvan, Oct 2002 Botryllophilus macropus Canu, 1891 (SEPA Stn. LSO, 55°17.25’N, 04°5L12’W, depth 5m). One mature female and two juveniles (copepodids) 1 from a solitary tunicate {Molgula complaiiatal) Thirteen ovigerous females from 38 Ascidiella aspersa, collected at Bell Rock sewage disposal grounds. Forth five ovigerous females from 37 Ascidiella scabra, and Sea area, Nov.1987 (Stn.13, 56"25’N, 02°10’W, depth one female from Corella parallelogramma?, all 56m). The only previous record of B.macropus from trawled in Irvine Bay, 10 April 2002 (SEPA Stn.H, British waters is from Langstone Harbour, Hampshire 55"35.92’N, 04°47.40’W, depth 38m). (Schmidt, 1984). The Forth Sea specimens are the first from Scotland and were described in detail by Ooishi Three ovigerous females (NMSZ:2004.063.0009) from (1996). Ascidiella aspersa collected by C.Milner, 0.8km north ofPort a Bheachan, Loch Craignish, 13 August 2003. Botryllophilus norvegicus Schellenberg, 1921 Ascidicola rosea is one of the most widespread of the One mature female found among sieve debris from a ascidicolous copepods occurring in a variety of hosts. grab sample collected at St.Abbs sewage disposal Scott (1907) mentioned its presence in Orkney (Scapa grounds, Forth Sea area, Jun. 1988, (Stn.27, Flow), Shetland, the Firth of Forth, and on the west 56"05.9rN, 02"04.72’W, depth 52m). Both of the coast at Oban and in Loch Fyne. A detailed re- known hosts, Pelonaia corrugata and Polycarpa description of the female is provided by Ooishi fibrosa, were present in the sample. One specimen of (2007a). the former ascidian had been tom open during sampling and may have been the actual host in this Haplostoma eruca (Norman, 1869) case. B.non’egicus is known from Norway, Greenland, eastern Canada and U.S.A., and Alaska. The Forth Sea specimen is the first record from the British Isles and 60 was illustrated, along with B.macropus, by Ooishi mauve (but usually greenish) were ascribed to B..sarsi. (1996). These included records from Strangford Lough (Gotto, 1954), Sheephaven, County Donegal (Gotto, 1961a), Botryllophilus ruber Hesse, 1864 Norfolk (Hamond, 1973) as well as some from east and south-west Scotland. One mature female found among sieve debris from a A revised key to Botryllophilus females from waters grab sample collected in the Sound of Jura, Jun. 2007 around the British Isles can be constructed: (SEPA Stn. SJl, 55°50.507’N, 05°46.829’W, around 10 km east of the Small Isles, depth 174m). B.ruber 1. Urosome 5-segmented, exopods ofleg pairs 1-4 was comprehensively re-described by Ooishi (1999) strongly asymmetric 2 based on new material collected at Roscoff, in Brittany, Urosome 8-segmented, exopods ofleg pairs 1-4 and morphological differences between females of weakly asymmetric 3 B.ruber and B.macropus were clarified for the first 2. Fifth leg narrow, long, curved, hook-like time. The definitive hosts of B.ruber are the botryllid B.norvegicus ascidians Botryllus schlosseri and Botrylloides leachi. Fifth leg narrow, short, straight B.sarsi Ooishi considered the B. ruber records of Scott (1901) (syn. B.brevipes Sars,1921) from Loch Fyne and the Moray Firth, and that ofGotto Fifth leg broad, long, lamellate (1954) from Strangford Lough, as reliable. In the Botryllophilus n.sp? second edition of his synopsis Gotto (2004) reviewed 3. Fifth leg strongly curved, hook-like other British Botryllophilus records and ascribed those B.aspinosiis from botryllid hosts, lacking true developed eyes, and Fifth leg gently curved, but not hooked with mauve eggs to B.ruber. This included records 4 from Devon (Norman & Scott, 1905), Norfolk 4. Fifth leg short, less than 1/2 urosome length, legs (Hamond, 1973) and Mayo, West Ireland (Holmes & 1-4 exopods shorter than endopods B.ruber Gotto, 2000). Fifth leg long, more than 3/4 urosome length, legs 1-4 exopods longer than Endopods Botryllophilus n.sp.? ...B.macropus One mature female, 1.5mm long, removed from a Order Poecilostomatoida small (4mm diameter) solitary ascidian, {Molgula spl), from a grab sample collected in the Sound ofJura, Jun. Family Lichomolgidae 2007 (SEPA Stn. SJl, 55°50.507’N, 05°46.829’W, around 10 km east of the Small Isles, depth 174m). Lichomolgidium cynthiae (Brian, 1924) The single female appears to be attributable to the genus in the form or the cephalic appendages, Two copepodites (NMSZ:2004.065.0001-2) from one asymmetric legs 1-4, and five-segmented urosome. Pyura microcosmus (also with 41 B.altera) collected However leg five which, in this genus, is usually from South Shian, Loch Creran, Aug.2001 (SEPA Stn. narrow and lanceolate, is in this specimen very large, 100m Sth., 56°31.25’N, 05°23.86’W, depth 7m). broad, and lamellate. A full description of this new species is planned fora future publication. The immature copepodites were just under 1mm in length. They appear to be different stages as one had The genus Botryllophilus Hesse, 1964 has been the the second and third segments of the leg rami fused subject of considerable confusion. Illg & Dudley while the rami in the other specimen were clearly (1980) reviewed the status of all named species and three-segmented. The second antennae and maxilliped dismissed many as indeterminable. Much of the appear similar to the adult although the caudal rami are confusion surrounding the genus Botryllophilus in much shorter. The fine spinulation on the posterior European waters has been resolved by detailed studies ventral margin of the urosomal segments and the ofOoishi (1988, 1996, 1999, 2002b, 2006). In addition peculiar structure of the outer principal caudal seta {ie. to the four species above, one other species is now weakly sclerotized on the inner side) illustrated by known to occur in British waters. Humes & Stock (1973, Fig.24) were observed on the copepodites. This species, B.sarsi Ooishi, 2002, was formerly known as “fi. brevipes Sars, 1921”. As Gotto (1993) L.cynthiae has only been recorded once before in noted, the name “B.brevipes” had previously been used British waters from Styela clava collected at Plymouth by Brement, in 1909, for a different Mediterranean (Gotto,196lb). The genus Lichomolgidium was species, and a new name was required for Sars’ transferred from the Sabelliphilidae to the species. Ooishi (2002b) provided the new name, Lichmolgidae by Humes & Boxshall (1996). B.sarsi, and a detailed redescription of new material from the clavelinid ascidian Polycitor vitreus collected Lichomolgus albens Thorell, 1859 at Lofoten, Norway. In Gotto’s synopsis (2004), British Botryllophilus records from various Seventeen females ovigerous and one male (1 1 ) aplousobranchiate ascidians, with eggs not coloured (NMSZ:2004.066.0001 from two Ascidiella aspersal ) 61 (also with six N.agilis) collected in Ayr Bay, 29 Sept Lichomolgusforficula Thorell, 1859 1993 SEPA Stn.l, 55‘’28.88’N, 04‘’04.40’W, depth ( 10m). Two ovigerous females, two mature females, and three males (NMSZ:2006.1 12.0001) from Ascidiella aspersa Seven females (five ovigerous) from one Ascidiella Invasion Bay, Loch Sunart, 2003. The copepods were scabra collected in Ayr Bay, 30 Sept 1993, found by P. Garwood. (SEPA Stn.l3, 55‘’27.25’N, 04‘’40.3rW, depth 19m). Widely distributed in Scottish waters. Scott (1907) One female from Ascidiella sp., (also with one cited its occurrence in Shetlands, Orkneys, Oban, and A.rosea), Bogany Point, Rothesay, Isle of Bute, June Loch Fyne. 2001, (SEPA Stn. 5, 55“50.7rN, 05"0I.8rW, depth 15m). Lichomolgusfurcillatus Thorell, 1859 One immature female? from Ascidiella sp., collected Three ovigerous females, and eight juveniles off Dipple, Girvan, Oct 2002 (SEPA Stn. LSO, (NMSZ;2004.068.0001) from 16 Ciona intestinalis 55“17.25’N, 04"51.12’W, depth 15m). (also with 21 N.caerulea) collected in Ayr Bay, 30 Sept 1993, (SEPA Stn.l3, 55° 27.25’N, 04°40.3rW, Examination of the caudal rami is perhaps the easiest depth 19m). way to distinguish the various Lichomolgus species from ascidians. L.albens is characterised by peculiar The relatively short and stout caudal rami help truncated apical seta. The ovisacs of fixed specimens distinguish L.furcillatus from other species of are rather fragile and often break up as the copepod is Lichomolgus in British waters. In Scotland there are extracted from its host. The ovisacs of one of the several records from Scott: from Shetland, from above females were measured (through the host body Inchkeith and the Isle of May in the Firth ofForth, and mm wall prior to extraction) as 1.1 long, extending from Inverary, Loch Fyne (for record details see well beyond the caudal rami. These are much longer Humes & Stock, 1973, p.l93). that those illustrated by Sars (1917) and superficially resemble, in size and shape, the ovisacs figured by Zygomolgusdidemni (Gotto, 1956) Gotto (1961b) for L.diazonae Gotto, 1961. The only previous record of L.albens in Scottish waters is that One ovigerous female (NMSZ:2004.069.0001) from mentioned by Scott (1907) from Otter Spit, Loch Fyne. Diplo.soma listerianum colonies scraped off fish farm nets in Loch Kishom, April 2002, by Sally Davies. Lichmolgus canid Sars, 1917 At present, this species is known only from its type Ten females (five ovigerous) (NMSZ:2004.067.0001) locality in Strangford Lough, Northern Ireland. collected from 38 Ascidiella aspersa and two males D.listerianum represents a new host species for this (NMSZ:2004.067.0002) from Corella parallelo- copepod but the same ascidian may also act as a host to gramma? (also with D.porcicauda) trawled in Irvine an allied species, Z.tenuifurcatus (Sars, 1917), known Bay, 10 April 2002 (SEPA Stn.H, 55“35.92’N, from Norway and Ireland. 04‘’47.40’W, depth 38m). Description of a new copepod species from the Two females (ovigerous) from Ascidiella aspersa genus Enterocola van Beneden, 1860, Family collected near Lappock Rock, Irvine Bay, 16 April Ascidicolidae. 2004 (SEPA Stn.100m u/s IVS, 55°34.98’N, 04‘’41.46’W, depth 10m). Enterocola ooishiae n.sp. Two ovigerous females, one mature female, and one Material examined: one ovigerous female (Holotype) male from the non-native ascidian, Styela clava, removed from intestinal tract of a juvenile Ascidiella collected in Ardrossan harbour, Firth of Clyde, April sp? (ascidian about 1cm long), collected off Ironotter 2006. Point Greenock, May 1995 (SEPA Stn.H750, , 55°57.99’N, 04°48.7LW, depth 20m). Specimen in vial L.canui is new to Scotland. Around the British Isles it deposited in National Museum of Scotland has only been recorded from the southern North Sea (NMSZ:2004.064.0001-2) with some cephalic (i.e. The Netherlands, Stock, 1960) and Irish waters appendages mounted separately on a slide. (Gotto,1961b, Holmes & Gotto,1992). The male is figured by Costanzo (1968) and the female has recently Etymology: The new species is named in honour of been re-described by Conradi & Lopez-Gonzalez my colleague Shigeko Ooishi, of the Friday Harbour (1994). Laboratory, Washington State, USA, in recognition of her considerable contribution to the study of ascidicolous copepods over many years. Description: 62 Lamellae almost hemi-sphaerical, enclosing pair of Female (Fig. 2a-d): Body 2.4mm total length from dorsal protuberances to which ovisacs attach. Ovisacs, anterior of cephalosome to end of caudal rami. Body strongly curved, 2.7mm long, multiseriate (Fig. 2c). comprising cephalosome with antennae and Remainder of urosome relatively short, possibly with mouthparts, four-segmented metasome with sclerotized four segments, articulation obscure and difficult to plates dorsally and fourpairs oflegs ventrally, distinguish joints from wrinkles. Caudal rami clearly and urosome with pair of conspicuous lateral lamellae articulated with urosome, cylindrical, without on first segment and terminating in two simple caudal ornamentation. rami. Enterocola ooishiae is known only from the single Cephalosome (Fig. 3b) about 0.5mm broad, without female holotype specimen. The male remains to be rostrum. discovered. Antennules (A.l) (Fig. 3b,c) - elongate, cylindrical, perhaps 2-3 segmented but articulation obscured, about Review ofthe genusEnterocola three times as long as wide, of uniform width throughout with rounded end, anterior edge with six Illg & Dudley (1980) in their review of the setae, distally with three setae and three small setules. Ascidicolidae treated Enterocola in some detail, Antenna (A.2) (Fig. 3a,b) two-segmented, basal describing developmental stages, the form ofthe male, segment unarmed, apical segment elongate armed with as well as some intra-specific morphological variation short seta on inner margin, three long terminal setae in of females from different hosts. They accepted 15 group, and two long setae on outer margin. named species as valid and figured ten species in all, Labrum (La) (Fig. 3b) - semi-circular plate with five ofthem new. They provided a key to the females spinulose palps extending posteriorly from lateral of all 15 named species, the males being excluded as comers. they were known for only four species. Since 1980, Maxillule (Mx.l) (Fig. 3b,d) - proximal portion two species have been added from the Straits of forming large, heavily sclerotized, blunt tooth, and Gibraltar; E.gottoi Conradi et a/.1992 and E.africamis armed on anterior surface with seta and tiny Lopez-Gonzalez et a/.1993, and more recently another accompanying setule. Distal palp extends ventrally, three species; E.dicaudatus, E.monnioti and with five stout spinulose setae distally, and single seta E.parapterophorus have been described by on outer margin. Marchenkov & Boxshall (2005) from Tanzania, Bahrain, and Djibouti respectively. Ooishi (2007b) Maxilla (Mx.2) (Fig. 3b,e) - two-segmented with presented a detailed re-description of the type species, massive proximal segment, bearing at distal medial E.fulgens van Beneden, I860, and provided new comer an articulated digitiform, spinulose endite. insight regarding its morphology. She synonymised Distal segment narrower, heavily sclerotized, bifid E.megalova Gotto, 1964 with E.fulgens. distally with anterior process shorter that the posterior one. Irregular unsclerotized area on posterior surface All, except five, of the 20 named Enterocola species with small spine. occur in European waters and (excepting E.ooishiae) their distribution in Europe is summarised by Lopez- Legs 1-4 (Fig 4a-d) - two-segmented protopodite and Gonzalez et al. (1992). E.africanus described from the 1-segmented rami. First segment of protopodite African side of the Straits of Gibraltar can effectively (coxopodite) broad, without ornamentation. Second be regarded as European. segment (basipodite) broadly conical, armed with pair of minute setae laterally, surmounted laterally with In their assessment of some older species which have exopodite and terminally with endopodite. Exopodites at some stage been attributed to Enterocola, Illg & with granular protuberances laterally at base, and about Dudley (1980) dismissed as indeterminable Biocryptus midway along length. Exopodites of first, second, and flavus and B.roseus both Hesse, 1865 and B.calthaeus fourth legs terminate with pointed dome-like element. Hesse 1872, all from the Erench coast. The status of Exopodite of third leg terminates with smooth the '"Enterocola sp.” briefly described by Claus (1875) styliform process. Endopodites longerthan exopodites, without a given locality (but possibly from European around twice as long as broad, armed with two terminal waters) and "Enterocola sp.A Chatton & Brement, setae. Endopodite setae well spaced apart, outer 1909” from Naples (originally referred to E.fulgens generally a little longer than inner and longer than van Beneden, 1860 by della Valle,1883), remains endopodite segment. Well developed plates present uncertain as the original descriptions and figures are of between each pair of legs projecting posteriorly. poorquality. Simple plate between first pair, but plate between second, third, and fourth legs distinctly bilobed to form Scott (1900) figured "Enterocola (?) fulgens van two mammiform processes (Fig. 2b). Beneden” from the Eirth of Clyde. While he realised that his specimens differed somewhat from van Urosome with pediform projections on first segment Beneden’s he preferred to regard them as a variety of comprising pair of curved lateral lamellae each with E. fulgens rather than a new species. However, two tiny setules on posterior margin (Fig. 2d). Chatton & Brement (1909) regarded Scott’s Enterocola 63 & as a distinct entity and referred to it as “Enterocola setae. E.laticeps Illg Dudley 1980 from Washington sp.B”, a view re-iterated by Illg & Dudley (1980). and British Columbia also has a similar antennule to However, Scott’s description and figures lack E.ooishiae but with more numerous setae. sufficient detail to establish a new species and a full re- description is required based on new material. Another The antenna (A2) of E.ooishiae has a fairly typical 2- inadequately described species Enterocola beaumonti segmented spatulate structure. However, the possession Scott & Scott, 1895, from Valentia, Ireland has long of a distinct terminal group of 3 setae is shared only since been transferred to Haplostomides, and more with E. petiti Guide,1964 and E.fertilis Illg «fe Dudley, recently Ooishi (2002a, 2005) has indicated it should 1980 both from the Mediterranean, and also E. be regarded as synonymous with H.scolti Chatton & brementi Illg & Dudley, 1980 from the Channel coast Harant (1924). ofFrance. The genus Enterocola is poorly represented in British The oral appendages are of little taxonomic value in waters with only scant records. Ofthe seven species in Enterocola. It has generally been assumed that Gotto’s synopsis (1993) only four actually occur within mandibles are absent but Marchenkov & Boxshall the British Isles (one of which has since been (2005) described a pair of setulose elements concealed submerged as a synonym); the others being recorded beneath the labral palps in all three oftheir new species from the Channel coast of France. Apart from which they considered as representing mandibles. “Enterocola sp.B” mentioned above the only other Ooishiae (2007b) figured similar appendages in her records from Scottish waters are an unpublished record recent study of E.fulgens, but regarded them as derived in 1901 from the Millport Marine Station for paragnaths. No attempt has been made to locate such E.fidgens in the intestines of small ascidians dredged structures in E.ooishiae in order to avoid damage to the at Tarbert Bank (Loch Fyne), and Gotto’s citation of holotype specimen. E.fulgens (1960) from the Isle ofJura. The occurrence ofmammiform processes only between Almost all the known hosts of Enterocola species are legs 2-4 in E.ooishiae is also exhibited by E.clavelinae compound ascidians with the exception of E.laticeps Chatton & Harant, 1924 from France, E.precarius Illg Illg & Dudley 1980, from western USA and Canada, & Dudley, 1980 from Naples, Italy, and E.africanus one of the most primitive species in the genus, which from the Straits ofGibraltar. was found in a simple ascidian. Enterocola species have been observed in the pharynx, stomach, or The basic leg structure in E.ooishiae with the dome- intestine of their hosts. Brement (1911) provided like elements on exopods of legs 1, 2, and 4, is similar various illustrations ofthe orientation ofE.pterophorus to most other species. However, the endopod terminal Chatton & Brement, 1909 within the stomach of its setae are well separated on all legs (compared with compound ascidian host. several other species where they are closely adjacent), the setae are relatively long {i.e. much longer than The key morphological characters ofthe 20 Enterocola length of the endopod), and the outer seta is species (plus “Enterocola sp.B”) are summarised in consistently longer than the inner. This combination Table 1. They are derived from published descriptions ofcharacteristics is unusual within the genus, with only but should be used as a guide only as some features, E.bilamellatus Sars, 1921, from Norway, appearing to & such as the setal arrangement of the antenna (A2), and be similar. In E.hessei Chatton Harant 1924, the , the setal lengths of the leg endopodites may show setae are spaced and long but both inner and outer setae intra-specific variation in different hosts. are around the same length. The distinguishing features of the new species The possession of cylindrical, articulated, caudal rami E.ooishiae are; elongate cylindrical antennule (Al), in E.ooishiae is shared with 10 other species, the antenna (A2) with apical group of 3 long setae, remainder have conical or lobed rami usually fused mammiform processes at the base of legs 2-4 (leg 1 with the last urosome segment. with plate but no processes), leg endopods with long, unequal, well spaced setae (of which the outer are E.ooishiae keys out to couplet 7 (in the Illg & Dudley longer than the endopod), and cylindrical caudal rami key) or couplet 4 (in Gotto’s synopsis key) but which clearly articulate with the urosome. proceeds no further as the choice is for an apical group of 2 or 4 (or more) setae on the antennae (A2), whilst The antennule (Al) in most Enterocola species is E.ooishiae has an apical group of three setae. Of the & usually rather short, unsegmented or vaguely bimerous, species described since Illg Dudley’s review, often bulbous with a sharply tapered tip. The elongate E.gottoi is distinguished from E.ooishiae by its short antennule of E.ooishiae is unusual being of uniform bulbous antennule, antenna with 2 apical setae, width and with a rounded end. It bears some mammiform processes between all the legs, adjacent resemblance to that of two Mediterranean species. Of subequal endopod setae, and conical caudal rami fused these E. pterophorus appears to have a shorter with urosome. E.africanus has some features in antennule with fewer setae, and in E. mammiferiis common with E.ooishiae but has a short bulbous Chatton & Harant, 1922 the antennule is devoid of antennule, antenna with apical row of four setae, and 64 closely adjacent endopod setae. E.dicaudatus and appropriate to that person, and personal names can be E.parapterophoms differ in the structure of the regarded as nouns in apposition. antennae and antennules, and have very short closely adjacent endopod setae. E.monnioti has different Lopez-Gonzalez et al (1999) commented on the antennae, antennules, endopod setae, and caudal rami nomenclature in the genus Enterocola. Although they and lacks processes orplates between the legs. realised that Enterocola had traditionally been treated as feminine they proposed that the genus should be Conradi et ai (1992) recommended that any new regarded as masculine and that those species names species ofEnterocola is based on numerous specimens, with feminine endings {e.g. E.pterophora, to avoid confusion by variable host forms. However, E.bilamellata, E.mammifera, E.setifera, E.precaria, Marchenkov & Boxshall (2005) suggested that the host E.ianthina) should be amended to a masculine form forms previously described for E. pterophorus may {i.e. E.pterophorus, E.bilamellatus, E.mammiferus, represent a species complex. In the case ofE.ooishiae, E.setiferus, E.precarius, E.ianthinus). the combination of several distinct morphological features appears to be sufficient to allay such concerns They argued that generic names of other parasitic and warrants the establishmentofa new species. copepods with the suffix “-icokr (such as Doridicola Leydig, 1853, Modiolicola Aurivillius,1882 and Nearly all the species of Enterocola have been Synapticola Voigt, 1892) have been regarded as recovered from compound ascidians. The occurrence masculine and hence Enterocola should be considered ofE.ooishiae in a simple ascidian is of interest as only in the same manner. one species, E.laticeps, has previously been observed in a solitary ascidian. The hosts of E. bilamellatus However, on the grounds ofmaintaining nomenclatural from Norway and E.setiferus Hansen, 1923 from stability, the Code also allows the form of a generic Iceland are unknown but Illg & Dudley (1980) name to be conserved ifthere has been a long tradition suggested that as these share some ancestral features of use of the name in a particular form, even if the with E.laticeps (such as multi-segmented antennules) original construction is later shown to be erroneous. they may also utilise simple ascidians as hosts. It is This would certainly be the case with Enterocola not clear whether “Enterocola sp.B” of Scott, 1900 is which has generally been treated as feminine by almost from a solitary ascidian but Scott’s subsequent (1907) ail authors for well over 100 years. There seems to be comment that “only one copepod was noticed in each only a few exceptions; in a resume of parasitic single ascidian” implies that a solitary ascidian may be copepods from Southern Africa (Barnard, 1955) involved. Moreover the multi-articulated ancestral transgendered the name E. bilamellata to E. form of both the antennules and antennae depicted by bilamellatus, and E.africanus was constructed in a Scott appears to be unique within the genus. Although masculine form by Lopez-Gonzalez et al. (1993). E.ooishiae and “Enterocola sp.B” may occupy similar However, Marchenkov & Boxshall (2005) in a brief hosts within the same geographical area, they are very mention ofE.pterophora changed the gender ending to different morphologically. Re-descriptions ofsome of E.pterophorus, bluntly stating that the genus the poorly known Enterocola species would greatly aid Enterocola is masculine and that such a change is understanding of morphological variation within the mandatory. Hence they also used masculine endings genus. It seems likely that diligent searching of for their three new species, E.dicaudatus, E.monnioti, ascidians will reveal further new species ofEnterocola and E.parapterophoms. More recently Ooishi (2007b) both in British waters and elsewhere. followed suit and treated the genus as masculine. Nomenclatural footnote Some light can be cast on the proposal of Lopez- Gonzalez et al (1999) and the statement of The names of six of the Enterocola species have Marchenkov & Boxshall (2005) if the original recently changed their endings from feminine form to description of Enterocola is re-examined. The first masculine. To fully understand the etymology of described species of the genus Enterocola was E. scientific names and some recent discussion on the fulgens van Beneden, 1860. The genus name correct form of species names within Enterocola Enterocola is derived from Enteron (Greek for gut) requires delving into the rather esoteric world of combined with the latin suffix -cola (meaning zoological nomenclature. The Code of Zoological inhabitant). Enteron is neuter {i.e. common gender Nomenclature (ICZN, 1999) states that generic names form which may be either masculine or feminine derived from greek or latin words should maintain the depending on the context). The suffix -cola is gender of the original word, or where this word is of masculine or common gender and the species epithet common gender then the genus name should be fulgens (meaning shining or gleaming) is also neuter. considered as masculine, unless treated otherwise by Grammatically the stem of the word Enteron is Enter- the original author. The gender of specific names ed in combination with -cola the vowal ‘i’ is normally should, as adjectives, generally follow that ofthe genus inserted to make the name more rhythmic or although there are exceptions to this such as species pronouncable. Hence the name ought to have been named after a person which utilize the gender ending “Entericola”. However, on this point at least, there is 65 no imperative under the Code to amend such a trivial Nevertheless the Code must be applied consistently to grammatical error. all fauna and there the debate must rest. The type species Enterocolafulgens is thus constructed ACKNOWLEDGEMENTS in common gender form and there is no explicit A special tribute is due to the late Dr Viv. Gotto indication within the original decription of how the (Queen’s University, Belfast) who acted as my mentor author regarded the gender of the new genus. on copepod matters for nearly 20 years. Sadly, Dr Evidently van Beneden only had female specimens and Gotto died in April 2006. A review of his life and tells us that the name “shining” refers to the brilliant work is provided by O’Reilly & Boxshall, (2006). purple appearance ofthe ovisacs. With a specific name Thanks are also due to Dr Shigeko Ooishi (Friday based on a female holotype and referring to a Harbour Laboratories, University of Washington, specifically female feature it might be inferred that he USA) for assistance with my studies of ascidicoious effectively treated the genus as feminine when it was copepods and to Peter Garwood (Identichaet, established. However names are constructed strictly Newcastle-upon-Tyne), Sue Hamilton (Marine according to word gender and not sex of specimens. biological consultant, Edinburgh), Sally Davies Sex and word gender are entirely different concepts. (Scottish Sea Farms, Isle of Mull), and my colleagues Hence the suggestion of Lopez-Gonzalez et al (1999) at SEPA (Jeni Boyle, Stephen Nowacki, Kirsty Bauros, that no gender was inferred and that the genus should Carol Milner, and Paul Hallas) for supplying default to a male gender seems reasonable at first. specimens. However, it is also worth noting that the masculine REFERENCES examples presented by Lopez-Gonzalez et al (1999); Barnard, K.H. (1955). South African parasitic Doridicola, Modiolicola, and Synapticola, are all Copepoda. Annals of the South African Museum named after their respective hosts (the Sea Slug, Doris 41(5), 223-312. Linnaeus, 1758, the Horse Mussel Modiolus Lamarck, Bocquet, C. & Stock J.H. (1960). Copepodes parasites 1799, and the Sea Cucumber Synapta Eschscholtz, d’invertebres des cotes de France, 11. Le genre 1829) which themselves were all of feminine form. Notodelphys, de la famille des Notodelphyidae. (The Horse Mussel was called Modiola in the 1880’s Proceedings of the Koninklijke Nederlandse but has since reverted to its original masculine form akademie van Wetenschappen-Amsterdam, Series C, Modiolus). Thus the corresponding copepod genera 63(1), 123-136. should perhaps also have been treated as feminine. Boxshall, G.A. & Halsey, S.H. (2004). An Nevertheless, if there is now a long history of treating introduction to copepod diversity. London: the Ray them otherwise then this could be continued on the Society, 966pp. grounds ofmaintaining nomenclatural stability. Brady, G.S. (1878). A monograph of the free and semi-parasitic Copepoda of the British Islands. Similarly with Enterocola, its long historical treatment Vol.l, 148pp., 33 pis., Ray Society, London. as a feminine genus warrants, to some extent, the Brement, E. (1911). Sur la situation que peut affecter, maintenance ofsubsequent specific names as feminine. chez quelque Ascidies merosomes, le genre de Against this is the argument for rigid application ofthe Copepode Enterocola. (Note preliminaire.) Bulletin Code and defaulting to masculine forms. The latter du Museum d’Histoire naturelle, Paris, 17(2), 69-75. option was chosen by Lopez-Gonzalez et al (1999), by Canu, E. (1891). Les copepodes marines du Marchenkov & Boxshall (2005), and was followed by Boulonnais: V. Les semi-parasites. Bulletin Ooishi (2007b). This option has now also been Scientifique de la France etde la Belgique, Ser.4, 23, adopted here, albeit with some reluctance. 467-487. Canu, E. (1892). Les copepodes du Boulonnais: It is interesting from a socio-historical viewpoint that morphologie, embryologie, taxonomie. Travaux du the Code of Nomenclature displays a male gender bias Laboratoire de Zoologie Maritime de Wimereux- in that names should be regarded as masculine by Ambleteuse, 6, 1-354, pi.1-30. default. This may be appropriate to some of the major Chatton, E. & Brement, E. (1909). Sur un nouveau vertebrate groups where males may be physically Copepode ascidicole Enterocola pterophora n.sp. et dominant or may display more distinctive morphology sur le genre Enterocola P.J.van Beneden. Bulletin de or coloration. However, in many crustacean groups, la Socittt Zoologique de France, 34, 223-229. and among parasitic copepods in particular, females Chatton, E. & Harant, H. (1922). Notes on the tend to dominance in body size and longevity. The Copepodes ascidicoles. XL Enterocola betencourti males are often short-lived and of diminutive size. Canu, E.pterophora Ch. et Br., E.mammifera n.sp. Indeed for a considerable number of species the males Bulletin de la Soci6t6 Zoologique de France, 47, 146- remain unknown. In practice this means that females 156. are more frequently observed and the type descriptions Chatton, E. & Harant, H. (1924). Notes on the are generally based on female holotypes. Hence, in Copepodes ascidicoles. XV. Sur trios formes parasitic copepods at least, the code rule to default to nouvelles du genre Enterocola P. J. van Beneden. an assumed male gender may seem quite inappropriate. Etat actuel de la systematique des Enterocolinae 66