Publishedin collaboration with the University of Bergenand the Institute of Marine Research,Norway

Re-descriptionsof Caprellalinearis (Linnaeus,1767) and C.septentrionalis Kro¨yer,1838 (Crustacea: Amphipoda: Caprellidea) from Scotland, with an on- togeneticcomparison between the species anda studyof theclinging behaviour

Jose´ManuelGuerra-Garc ´a SARSIA Guerra-Garc ´aJM.2002. Re-descriptions of Caprellalinearis (Linnaeus,1767) and C.septentrionalis Kro¨yer,1838 (Crustacea: Amphipoda:Caprellidea) from Scotland, with an ontogenetic comparison between thespecies anda studyof theclinging behaviour. Sarsia 87:216–235.

Caprellalinearis (Linnaeus,1767) and C.septentrionalis Kro¨yer,1838 are re-describedbased on specimens collectedfrom the coasts ofScotland. Mature males of C. linearis differclearly fromthose of C.septentrionalis mainlyin the features ofantenna1 andgnathopod 2. The pair of lateral projections presenton pereonite 5 infemales of C. linearis is lackingin females of C.septentrionalis . The gnathopod2 propodusis widerand the genital openings more setose infemales of C.septentrionalis than in C. linearis.Thearrangement ofthebody projections and the abdomen during development is quitesimilar in C. linearis and C.septentrionalis .Forboth species thepredominant mode of attachment tothesubstrate is theupright posture and feeding is byŽ ltering,frequently using grooming behaviour. These species presentbasically the same geographicaldistribution, along the North Atlantic, Boreal andArctic regionsand they are notvery speciŽ c inchoosingtheir substrate.

J.M. Guerra-Garc ´a,Laboratoriode Biolog ´aMarina,Departamento de Fisiolog ´a y Biolog´a Animal, Facultadde Biolog ´a,Universidad de Sevilla,Apdo. 1095, E-41080, Sevilla, Spain. E-mail:jmguerra@ us.es

Keywords: Caprellalinearis ; Caprellaseptentrionalis ;Caprellidea;re-descriptions; clinging beha- viour;ecology; biogeography; Scotland.

INTRODUCTION subspeciŽc variants.Although C. linearis and C. septentrionalis havebeen found frequently in North Duringa shortstay at the Gatty Marine Laboratories, St Atlanticwaters, they have never been described in Andrews,Scotland, several samples of theCaprellidea detail.Furthermore, from the extensive literature, only fromthe east and west coasts of Scotland(Fig. 1) were thedescriptions of McCain (1968) as part of a general collected.The intertidal rocky areas of St Andrews, studyof the Caprellidea of thewestern North Atlantic, Boarhillsand Kingsbarns (east coast) were exclusively areof most signiŽ cance. inhabitedby Caprellasepten trionalis Kro¨yer,1838. On Todifferentiate C. linearis from C.septentrionalis thewest coast (Clachan Seil, near Oban) an important completedescriptions with detailed Ž guresof antennae, populationof C. linearis (Linnaeus,1767) was found. mouthparts,gnathopods, pereopods and abdomen are Thenomenclature of C. linearis and C.septentrio- necessary.These descriptions, based on the material nalis hastraditionally been one of the most confused in collectedalong the Scottish coasts, are included in the theCaprellidea literature. McCain & Steinberg(1970) presentpaper. Furthermore, Ž guresof thelateral view, pointedout that these species were easily confused and, gnathopod2 andabdomen during the different stages of therefore,many of the references could be questionable. developmentand data on clinging behaviour are Smaldon(1990) reported that no simple distinction presentedhere with the purpose of comparisonbetween couldbe made between the two species. For C. thetwo species. septentrionalis ,avarietyof body forms based mainly onthebody projections have been recognized since its MATERIALAND METHODS originaldescription. Mayer (1890, 1903) considered the differentforms as variants of the same species. Never- Samplesof various types of substrata on which theless,Stephensen (1940) treated several of these caprellidswere expected to inhabit were carefully formsas distinctspecies or subspecies.McCain (1968) detachedfrom rocks of intertidal areas along the east foundnumerous intergradations between the forms and andwest coasts of Scotland (Fig. 1). The intertidal suggestedthat they probably represented only infra- zonesat St Andrews,Boarhills and Kingbarns (56 °15’N

# 2002Taylor & Francis Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 217

clingingbehaviour was also studied. For the behaviour- alstudies, 10 mature specimens (Ž ve males and Ž ve females)of each species were selected prior to preservationand individuals were placed in a Petridish Žlledwith seawater. The methods used for measuring theclinging behaviour in the present study are explainedin detail in Takeuchi & Hirano(1995). TheŽ gureswere drawn using a binocularmicroscope withthe aid of acameralucida. Permanent preparations ofthe mouthparts were made using polyvinyl lactophe- nol.Fifty mature males and 50 maturefemales of each specieswere measured under the microscope. The body lengthwas calculated as the sum of the head and pereonitelengths. Specimens of bothspecies have been depositedin the Museo Nacional de CienciasNaturales, Spainwith the follow catalogue numbers: MNCN 20.04/4660for C.septentrionalis and20.04/ 4661for C. linearis.Withthe purpose of comparison, the type material(syntypes from Greenland) of C.septentrio- nalis fromthe Zoological Museum, University of Copenhagen(ZMUC-CRU-8059) was consulted. Type materialdoes not exist for C. linearis.Inthiscase, non- typematerial from Nordso ¨en,O ¨ rsted,Denmark (ZMUC uncatalogued)was examined.

Fig.1. Location of the sampling stations on the coasts of RESULTSAND DISCUSSION Scotland. SYSTEMATICS

Caprellalinearis (Linnaeus,1767) 02°30’W)areareas exposed to waveaction. The algae Cancerlinearis (Linnaeus1767: 1056) communityis dominated by the brown seaweed Fucus Oniscusscolopendroides (Pallas1772: 80, plate 4, Ž g. serratus Linnaeus,1753 and several species of the 15 a–c) genera Polysiphonia and Ceramium.ClachanSeil, Squillalobata (Mu¨ller1776: 197) alongthe west coast, is a verysheltered tidal strait of Squillaquadrilobata (Abildgaard1788: 21– 22, plate approximately30 mwideand 1 kmlong separating Seil 56, Ž gs 4–6) Island (56°20’N 05°35’W)fromthe Argyll mainland. Gammarusquadrilobatus (Abildgaard1789: 58, plate Thereare tidal sills at bothends of thenarrows, and as a 114,Ž gs11,12) result,the spring tides ebb to the same level between the Cancer(Gammarellus) linearis (Herbst1793: 142– 144, sillsirrespective of the open coast  uctuations;hence, plates99, 106) theenclosed narrows are never immersed. The domi- Cancerlinnearis (Linnaeus1800: 761) nantalga is also F. serratus;largeamounts of Caprellalinearis (Mayer1882: 58– 62, Ž gs17– 19, plate bryozoans(principally Electrapilosa Linnaeus,1767) 4,Ž g.32;Koehler 1885: 98– 99, 117;Sokolowsky 1900: andhydroids are attached to thesurface of theseaweed 162,plate 3, Žg.16; Chevreux & Fage1925: 456– 457, andare considerably more abundant than at St Žg.434;McCain 1968: 30– 33, Ž gs14,22, 51; Laubitz Andrews,Boarhills and Kingsbarns. 1972:35– 37, plate 7; Smaldon 1990: 448, Ž g.9.48; Thecollected material was brought back to theGatty Larsen1998: 82, Ž g.2) MarineLaboratories and transferred into a shallow Caprellalaevis (Goodsir1842: 189– 190, plate 3, Žgs4, trainerŽ lledwith seawater. The caprellids were hand 5) pickedand Ž xedin a 10%seawater– formalin solution Caprellalobata (Bate1856: 60; 1862:354, plate 55, Žg. andthen preserved in 70%ethanol. 8) Inan attempt to elucidate if the method of attachment Caprellalinearis f. gullmarensis (Mayer1903: 112, tothe substrate could differentiate these species, the plate8, Žg.20) 218 Sarsia 87:216-235– 2002

Fig. 2. Caprellalinearis (Linnaeus,1767) from Scotland. Lateral view.a. Male.b. Female. Scale bars:1 mm.

Caprellalinearis f. distalis (Mayer1903: 113, plate 4, Materialexamined Ž gs 27, 28) Eightmature males, seven mature females, seven prematurefemales and one juvenile collected from Typelocality hydroidsattached to the seaweed F. serratus at the “Habitatin Oceano Europaeo” (Linnaeus 1767). intertidalarea of ClachanSeil, west coast of Scotland, May 2000.

Typematerial Additionalmaterial examined Notdesigned. Non-typematerial (12 mature males, three mature Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 219

Fig. 3. Caprellalinearis (Linnaeus,1767) from Scotland. Male. a. Antenna1. b.Antenna2. c. Gnathopod1. d.Gnathopod2. Scale bars:A: 1mm (a); B:1mm (b);C: 0.3mm (c); D: 1 mm (d).

females,14 premature females, 11 juveniles) from setaeon peduncular articles 3 and4. Flagellum two- Nordso¨en,O ¨ rsted,Denmark. articulate.Proximal article with six pairs of swimming Description(mature male “ a”from Clachan Seil, setae. Scotland).Lateral view (Fig. 2a). Body length 10.1 mm. Gnathopod1 (Fig.3c) basis a littleshorter than Headwith a smallmid-dorsal rounded projection. ischiumto carpus combined. Carpus with a pairof Pereonites1 and2 elongate.Pereonite 2 thelongest. proximalgrasping spines. Grasping margin of palm Pereonite3 witha roundtubercle posteriorly. Pereonite propodusand dactylus serrated. Dactylus biŽ d distally 5withtwo pairs of small round projections. Pereonites carryinga simpleseta. 6and7 withone pair of small acute projections. Gills Gnathopod2 (Fig.3d) basis inserted posteriorly on elongate,length about 3.3 times width. pereonite2, about0.7 times as long as pereonite2 and Antenna1 (Fig.3a) nearly 0.5 the body length. 0.2the body length. Basis with a distalacute projection. Articles2 and3 ofpeduncle setose. Article 2 the Propodusslender, length about 3.0 times width, bearing longest,about 1.5 times longer than article 1. Articles1 amid-dorsalseta. Palm setose, with a proximal and3 subequal.Flagellum composed of 11articles. projectioncarrying a graspingspine, an accessoryspine Antenna2 (Fig.3b) equal in length to peduncular andtwo distal projections separated by a deepcleft. articles1 and2 ofantenna 1. Ten pairs of swimming Dactyluscurved and setose distally. 220 Sarsia 87:216-235– 2002

Fig. 4. Caprellalinearis (Linneus,1767) from Scotland. Female. a. Antenna1. b.Antenna 2. c. Gnathopod 1.d.Gnathopod2. e. Genitalopenings. f. Dorsal viewof pereonites5– 7 showinglateral projectionson pereonite5. Scale bars:A: 1mm (a, b);B: 0.3mm (c); C:0.5mm (d);D: 0.3mm (e); E:1mm (f). Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 221

Fig. 5. Caprellalinearis (Linnaeus,1767) from Scotland. a– d. Male.a. Pereopod5. b.Pereopod 6.c. Pereopod7. d. Abdomen.e. Female abdomen.Scale bars:A: 1mm (a, b,c); B:0.2mm (d, e).

Pereopods5– 7 (Fig.5a– c) similar in feature but littlelonger than the inner plate, bearing four setae increasingin length. Palm of propodus with a pairof apically,three teeth and two setae medially. Palp setose. graspingspines. Dactyluswith two rows of Ž nesetae in the inner Abdomen(Fig. 5d) with a pairof one-articulate margin. appendages,a pairof lateral lobes and a singledorsal Description(mature female “ b”from Clachan Seil, lobe.Appendages curved medially, length about 3.0 Scotland).Lateral view (Fig. 2b). Body length 5.1 mm. timeswidth, carrying a pairof setaeapically. Pereonites1 and2 notelongated. Pereonites 2– 4 witha Upperlip of mouthparts (Fig. 6a) symmetrically pairof tuberclesdorsally. Pereonite 5 withtwo pairs of bilobed,setose apically. smalldorsal round projections and a pairof acute lateral Mandibles(Fig. 6d, e) without palp. Molar process ones(Fig. 4f). Genital openings (Fig. 4e) scarcely strong.Incisor and lacinia mobilis Ž ve-toothed.A row setose.Pereonites 6– 7 witha pairof roundprojections ofthreesetae on theleft mandible and two setae on the dorsally. right.Molar  akesmall, present on theright mandible. Antenna1 (Fig.4a) longer than 0.5 the body length. Lowerlip of mouthparts(Fig. 6b) with well-marked Pedunculararticles 2 and3 notsetose,  agellum10- innerlobes. Inner and outer lobes densely pubescent articulate. apically. Antenna2 (Fig.4b) with six pairs of swimmingsetae Maxilla1 (Fig.6f) outer lobe carrying six stout teeth onpeduncular article 3 andeight pairs on peduncular apically.Palp two-articulate, distal article of the palp article 4. withnine distal marginal spines and a rowof Žvesetae Gnathopod1 (Fig.4c) as inmale. medially. Gnathopod2 (Fig.4d) inserted on the anterior half of Maxilla2 (Fig.6g) outer and inner lobe carrying 11 pereonite2. Palm without large distal projection setaeapically. followedby notch, sparsely setose. Dactylus not setose. Maxilliped(Fig. 6c) inner plate with two simple and Abdomen(Fig. 5e) with a pairof laterallobes with an fourplumose setae and two small teeth. Outer plate, a apicalsetae and a singledorsal lobe. 222 Sarsia 87:216-235– 2002

Fig. 6. Caprellalinearis (Linnaeus,1767) from Scotland. Male. a. Upperlip. b. Lowerlip. c. Maxilliped.d. Rightmandible. e. Left mandible.f. Maxilla 1. g.Maxilla 2. Scale bars:0.2 mm. A(a, b),B(c, d,e), C(f,g).

Pereopodsand mouthparts as in male. 1–3 (p.268); McCain 1968: 44– 49, Ž gs19– 22, 51; Caprellaseptentrionalis Kro¨yer,1838 Laubitz1972: 48– 53, plate12; Smaldon 1990: 488, Ž g. Caprellaseptentrionalis (Kro¨yer1838: 318; Herklots 9.48;Larsen 1998: 84) 1861:43; Bate 1862: 355, plate 56, Ž g.3;Mayer1882: Caprellacercopoides (White1852, Ž g.1) 62–64, Ž gs20– 22; 1890: 65– 68, plate 2, Ž gs26– 33, Caprellarobusta (Stimpson1854: 44; Mayer 1882: 66; plate4, Ž g.31, plate 6, Ž g.38; Sars 1895: 659– 660, 1890: 73) 700,plate 237, Ž g.1; Mayer 1903: 120– 123, plate 5, Caprellapunctata (Boeck1861: 676– 677; Stephensen Žgs19–21, plate 8, Žg.24;Stephensen 1928: 384– 386, 1928:385, Ž g.92) Žg.92;Oldevig 1933: 266– 269, Ž gs1–2 (p.267), Ž gs Caprellaseptentrionalis (Herklots1861: 43) Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 223

Fig. 7. Caprellalinearis (Linnaeus,1767) from Denmark (non-typematerial). Lateral view.a. Male.b. Female. Scale bar:1 mm.

Caprellastimpsoni (Bate1862: 361) femalesfrom Boarhills, east coast of Scotland, May Caprellalongicornis (Boeck1871: 274– 275) 2000;two mature males, one mature female, one juvenile Caprellaseptentrionalis f. typica (Mayer1890: 66) fromKingsbarns, east coast of Scotland, June 2000; one Caprellaseptentrionalis f. longicornis (Mayer1890: maturemale, one mature female, four premature females 66,plate 2, Ž gs26, 27, 33, plate 4, Ž g.31) fromSt Andrews,east coast of Scotland, May 2000. All Caprellaseptentrionalis f. nodigera (Mayer1890: 66) thespecimens were collected from algae, especially Caprellaseptentrionalis f. polyceros (Mayer1890: 66, Polysiphonia sp.,at the intertidal zone. plate2, Ž g.32) Caprellaseptentrionalis f. parva (Mayer1890: 66, plate Additionalmaterial examined 2,Žgs28–31) Caprellaseptentrionalis f. spinigera (Hansen1895: Syntypes(31 mature females, Ž veyoungmales). 130) Description(mature male “ a”from Boarhills, Scot- land).Lateral view (Fig. 8a). Body length 10.9 mm. Typelocality Headwith a patentmid-dorsal rounded projection. Pereonites2 and3 witha roundtubercle dorsally. Greenland(Kro ¨yer1838). Pereonite4 witha medialand a posteriortubercle. Pereonites5– 7 withtwo pairs of dorsal small round Typematerial projections.Pereonites 2, 3 and4 subequalin length. Syntypes(ZMUC-CRU-8059). Gillsoval– elongate, length 2.8 times width. Antenna1 (Fig.9a) about 0.3 of body length. Materialexamined Pedunculararticles not setose. Peduncular article 2 thelongest. Peduncular article 3 theshortest, about 0.5 Sevenmature males, four mature females, two premature thelength of article2. Flagellum nine-articulate. 224 Sarsia 87:216-235– 2002

Fig. 8. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Lateral view.a. Male.b. Female. Scale bar:1 mm.

Antenna2 (Fig.9b) a littlelonger than peduncle of Gnathopod2 (Fig.9d) basisinserted in the middle of antenna1. Ten pairs of swimming setae present on pereonite2, about 0.25 the length of pereonite 2 and pedunculararticles 3 and4. Flagellum two-articulate. 0.05the body length. Basis with a distalacute Proximalarticle with six pairs of swimming setae. projection.Propodus wide, length about 1.7 times Gnathopod1 (Fig.9c) basis a littleshorter than width.Palm scarcely setose with a proximalprojection ischiumto carpus combined. Carpus with a pairof carryinga graspingspine, an accessory spine and two proximalgrasping spines. Grasping margin of palm smalldistal projections separated by a cleft.Dactylus propodusand dactylus serrated. Propodus wider and curvedwithout setae. carpusmore setose than in C. linearis. Pereopods5– 7 (Fig.11a– c) increasingin length, less Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 225

Fig. 9. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Male. a. Antenna1. b. Antenna 2.c. Gnathopod1. d. Gnathopod 2. Scale bars:A: 1mm (a, b);B: 0.5mm (c); C:1mm (d).

setosethan those in C. linearis.Palmof propoduswith a teethapically. Distal article of thepalp with six spines pairof graspingspines. anda rowof foursetae medially. Abdomen(Fig. 11d) with a pairof one-articulate Maxillae2 (Fig.12g) outer lobe with 11 setae appendages,a pairof lateral lobes and a singledorsal distally,inner lobe shorter but wider than outer lobe, lobe. with12 setae apically. Upperand lower lips of mouthparts (Fig. 12a, b) Maxilliped(Fig. 12c) inner plate carrying six simple morphologicallysimilar to those in C. linearis but less setaeand two small teeth distally. Outer plate bearing pubescentapically. threeteeth and several setae. Article 2 ofthe palp Mandibles(Fig. 12d, e) similar to thosedescribed for scarcelysetose. Article 3 setose.Article 4 acutedistally. C. linearis exceptlacinia mobilis four-toothed. Description(mature female “ b”from Boarhills, Scot- Maxillae1 (Fig.12f) outer lobe carrying Ž vestout land).Lateral view (Fig. 8b). Body length 7.2 mm. 226 Sarsia 87:216-235– 2002

Fig. 10. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Female. a. Antenna1. b. Antenna2. c. Gnathopod1. d. Gnathopod 2. e. Genitalopenings. f. Dorsal viewof pereonites5– 7. Scale bars:A: 1mm (a, b);B: 0.3mm (c); C:1mm (d);D: 0.2mm (e); E: 1 mm (f).

Lateralprojections on pereonite 5 absent(Fig. 10f). Gnathopod1 (Fig.10c) as inmale. Pereonite6 withonly a pairof dorsal round projections. Gnathopod2 (Fig.10d) slender; propodus palm Pereonite7 smooth.Genital openings (Fig. 10e) setose. almoststraight. Antenna1 (Fig.10a) longer than 0.5 the body length. Abdomen(Fig. 11e) with a pairof lateral lobes Flagellum10-articulate. carryingthree apical setae and a singledorsal lobe. Antenna2 (Fig.10b) with nine pairs of swimming Pereopodsand mouthparts as inmale. setaeon peduncular articles 3 and4. Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 227

Fig. 11. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. a– d. Male.a. Pereopod5. b. Pereopod6. c. Pereopod7. d.Abdomen.e. Female abdomen.Scale bars:A: 1mm (a, b,c); B: 0.2mm (d,e).

REMARKS dactylus in C. linearis isprovided with setae in the innermargin. Other minor but constant differences Thebody lengths of the males of both species are havebeen found between the two species: pereonites 1 similar,while the females of C.septentrionalis are and2 areelongate and the pereopods are more setose largerthan the femalesof C. linearis (Table1). Mature dorsallyin adult males of C. linearis.Thelacinia males of C. linearis differfrom those of C. septen- mobilisis Ž ve-toothedin C. linearis andfour-toothed trionalis mainlyin the features of antenna 1 and in C.septentrionalis .Theupper and lower lips are gnathopod2. In adult males of C. linearis, the moresetose in C. linearis.Distalsetae on the inner pedunculararticles 2 and3 ofantenna 1 bearshort plateof themaxilliped are plumose in C. linearis and setae.Regarding gnathopod 2, the basis is almost as simple in C.septentrionalis .Thepropodus of gnatho- longas pereonite2 in C. linearis whilebeing about one pod2 iswiderand the genital openings more setose in third in C.septentrionalis .Furthermore,the propodus females of C.septentrionalis than in C. linearis. isclearlyslender in C. linearis (lengthabout 3.0 times Furthermore,a pairof lateral projections in pereonite width)while in C.septentrionalis thepropodus is 5,present in C. linearis,arelacking in C.septentrio- wider(length about 1.7 times width). Moreover, the nalis.Themorphologica ldifferencesbetween the 228 Sarsia 87:216-235– 2002

Fig. 12. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Male. a. Upperlip. b. Lower lip.c. Maxilliped.d. Left mandible.e. Rightmandible. f. Maxilla 1. g. Maxilla2. Scale bars: 0.2mm. A(a, b),B(c, d,e, f,g).

Table1. Comparison of selected morphologicalcharacteristics in Caprellalinearis and C.septentrionalis .Data ofaverage length (mm) formature males andfemales are alsoincluded. Fifty mature males and50 mature females ofeach species were measured. Numbers inparentheses indicatethe range. The results of theone-way ANOVA formales andfemales are included. C. linearis C.septentrionalis F Bodylength (males) 8.2(6.8– 10.1) 8.3(6.0– 11.9) 0.01 ns Bodylength (females) 5.1(4.0– 6.1) 8.1(6.0– 11.2) 7.01* Peduncleof antenna1 (males) Setose Not setose Basis ofgnathopod2 length(males) Aboutpereonite 2 One thirdof pereonite2 Length/widthratio of propodusof gnathopod2 (males) 3:1 1.7:1 Pereonites1 and2 (males) Elongate Non-elongate Lacinia mobilis(males andfemales) Five-toothed Four-toothed Genitalopenings (females) Scarcely setose Very setose Lateral projectionson pereonite5 (females) Present Absent ns,not signiŽ cant. * p < 0.05. Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 229

Fig. 13. Caprellaseptentrionalis Kro¨yer,1838 from Greenland (ZMUC-CRU-8059, syntypes). Lateral view.a. Maturefemale. b.Young male. Scale bar:1 mm.

speciesare also present in the specimens belonging to females of C. linearis arealso very similar to females thetype material of C.septentrionalis fromGreenland of C.septentrionalis .Althoughthe length/ widthratio of (Fig.13) and the non-type material of C. linearis from thepropodus of gnathopod 2 inmales seems to be Denmark(Fig. 7). Consequently ,theconsistent and constantduring development in C.septentrionalis (Fig. constantmorphologic aldifferences existing between 17),it changes in C. linearis.Inthe more advanced thesetwo species (Table 1) support the idea of stagesof development,this length/ widthratio increases, consideringthem as two valid species. thepalm becomes more setose and some setae appear onthe dactylus (Fig. 16). No differences in the abdomenbetween the two species were found during ONTOGENETIC DEVELOPMENT ontogeneticdevelopment. The penes and the appen- Thearrangement of the body projections during dagesincrease in size during development for both developmentis quite similar in both species (Figs 14, species(Figs 16, 17). 15).Juvenile stages are indistinguishable between the Inseveral species of Caprella theontogeny of the twospecies. Nevertheless, it seems that the rounded abdominalappendages has been studied (see Mori projectionon the head appears earlier during develop- 1999).Sakaguchi (1989) described the post-marsupia l mentin specimens of C. septentrionalis . Mature developmentof C.scauradiceros Mayer,1890, reared 230 Sarsia 87:216-235– 2002

Fig. 14. Caprellalinearis (Linnaeus,1767) from Scotland. Different stages inthe lateral viewof males (above)and females (below)during development. Scale bar:1 mm.

inthe laboratory. All the hatchlings had paired CLINGING BEHAVIOUR abdominalappendages bearing a singleseta, as shown here for C. linearis (Fig.16). These appendages were Thepredominant mode of substrate attachment was atŽ rstone-articulat eandsmall, becoming larger and theupright posture for both C. linearis and C. two-articulatein the older specimens of C. scaura. septentrionalis (Table2). Both species grasp the Takeuchi(1989) described the post-marsupia ldevel- substratewith pereopods 5– 7 withthe anterior somites opmentof theabdominal appendages of C.danilevskii heldaway from the substrate. Both of the second Czerniavski,1868, C. okadai Arimoto,1930 and C. gnathopodsare usually extended laterally. Grooming generosa Arimoto,1977, reared in the laboratory. In wasfrequent in both species in comparison with data thesethree species, all the early juveniles had paired reportedby Takeuchi& Hirano(1995), using the same abdominalappendages bearing a singleapical seta. methodologyas for other species of Caprellidea . Theappendages grew larger in the males, whereas Groomingbehaviour has been traditionally associated theywere reduced in the females, as in C. scaura withŽ lteringsuspended material (Patton 1966; Caine diceros. 1974).The rows of setaepresent ventrally on antenna 2favourthis type of feeding. Therefore, both species Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 231

Fig. 15. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Different stages inthe lateral viewof males (above)and females (below)during development. Scale bar:1 mm.

seemto Ž lterfeed, standing in the upright posture. inhabitsubstrates subject to heavy wave exposure Althoughthey have been found in areas exposed to (Takeuchi& Hirano1995). In theparallel posture the waveaction, especially C.septentrionalis , neither caprellidstrongly grasps the substrate with both of the specieshas adopted the parallel posture as predomi- Žrstgnathopods and pereopods 5– 7, with the body nantbehaviour and scraping as a feedingstrategy. somitesstraight and parallel to the substrate, thus Somespecies of thegenus Caprella,consideredas one avoidingdisplacement by the currents or the wave ofthe most apomorphic genera of the Caprellidea action. (Takeuchi1993), such as C. penantis Leach,1814 and C.danilevskii ,presentthis parallel posture in associa- ECOLOGY tionwith feeding by scraping the substrate, and have developedcharacters that speciŽ cally enable them to Theintertidal rocky areas of St Andrews,Boarhills 232 Sarsia 87:216-235– 2002

Fig. 16. Caprellalinearis (Linnaeus,1767) from Scotland. Different stages inA. gnathopod2 andB. theabdomen in males. Scale bars:A: 1mm; B:0.2mm.

andKingsbarns(east coast) were exclusively inhabited foundit on Bryozoaand reported that C.septentrionalis by C.septentrionalis ,attachedmainly to thered algae sometimesinhabits among the seaweed Corallina sp. in Polysiphonia sp.Onthewest coast (Clachan Seil, near rockpools. The temperature range for C. linearis is Oban)an important population of C. linearis was establishedbetween 7.1 and 8.2 °C and for C. septen- foundclinging to thehydroids growing on F. serratus. trionalis between0 and7.9 °C(Larsen1998). The depth Othercaprellid sfoundliving on these substrate were rangeis 0–1000 m for C. linearis and0– 1026 m for C. Phtisicamarina Slabber,1719 and C.acanthifera septentrionalis (Larsen1998). Leach,1814. Bothspecies, C. septentrionalis and C. linearis, do DISTRIBUTION notappear to be very substrate speciŽ c, having been collectedfrom brown, green and red algae, sea grass, Theknown distribution of C. linearis and C. septen- sponges,hydroids, alcyonarians and tunicates (McCain trionalis ispresented in Fig. 18. Both species share 1968).Ohlin (1895) reported C. linearis from Asterias basicallythe same area of distribution which occurs sp.collected off Newfoundland and Mayer (1903) also mainlyalong the North Atlantic, Boreal and Arctic reportedit from the asteroid Solaster sp.which was regions.The most occidental localities for C. linearis collectedfrom Scotland. Harrison (1944) pointed out arein Alaska. In Greenland, C.septentrionalis is more thepresenceof C. linearis on Zostera sp., Laminaria sp. abundantthan C. linearis (Laubitz1972). The presence and oatingwreckage and buoys. Smaldon (1990) also of C. linearis hasalso been reported along the Atlantic Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 233

Fig. 17. Caprellaseptentrionalis Kro¨yer,1838 from Scotland. Different stages inA. gnathopod2 andB. theabdomen in males. Scale bars:A: 1mm; B:0.3mm.

Fig.18. Geographical distribution of C. linearis and C.septentrionalis .Data fromMcCain (1968), McCain & Steinberg(1970), Laubitz(1972), Larsen (1998),Smaldon (1990) and Guerra-Garc ´a(unpublisheddata). 234 Sarsia 87:216-235– 2002

Table2. Average time spentin each clingingtype of behaviour, scraping and frequency of grooming. Data are givenas a percentage ofthetotal observation time (10min), except for the grooming frequency which is givenas thenumber of times per 10minobservation period. The numbers in parentheses indicatethe range. Ten specimens ofeach species were observed. Clingingbehaviour Feeding Moving Upright BendingParallel ScrapingGrooming (%) (%) (%) (%) (%) (times) Caprellalinearis 1.1 96.5 1.9 0.5 0 20 (0.0–3.0) (85.0– 100.0) (0.0– 4.0) (0.0– 2.0) (5.0–28.0) Caprellaseptentrionalis 0.7 93.5 2.5 3.3 0 22.5 (0.0–5.0) (76.0– 100.0) (0– 10) (0.0–7.0) (2.0–32.0)

coastof the Iberian Peninsula. Inside the British Isles, ACKNOWLEDGEMENTS C. linearis iscommon on all British coasts while C. Iam verygrateful to Dr ChristopherTodd and Helen Gurney- septentrionalis isa northerndistributed species, occur- Smithfor their hospitality and kindness during my stay at the ringin Scottish waters, but is notknown further south GattyMarine Laboratories (Scotland). Special thanks to Dr (Smaldon1990). Harrison (1944) pointed out the JorgenOlesen forthe loan of the specimens andto three presence of C.septentrionalis onthe east coast of reviewers fortheir valuable comments onthemanuscript. This studywas partiallysupported by a grant(AP98 28617065, Scotland,at Clyde and St Andrews,the locality where “Acciones Integradas”) fromthe Spanish Government (Minis- thepresent material was collected. teriode Educacio ´n,Cultura y Deporte).

REFERENCES

AbildgaardPC. In: Mu ¨ller OF.1788. Zoologiadanica, sev Hansen HJ. 1895.Pycnogonider og Malacostrake Krebsdyr. AnimaliumDaniae et Norvegiaerariorum ac minus Meddelserom Gro¨nland 19:121–132. notorumdescriptiones et historia,Vol. 2 .Havniae.56 p. HarrisonRJ. 1944. Caprellidea (Amphipoda, Crustacea). AbildgaardPC. In: Mu ¨ller OF.1789. Zoologiadanica, sev Synopsesof theBritish Fauna 2:1–27. AnimaliumDaniae et Norvegiaerariorum ac minus Herbst JFW.1793. Versucheiner Naturgeschichteder notorumdescriptiones et historia,Vol. 3 .Havniae.71 p. Krabbenund Krebse, nebsteiner Systematischen Bate CS.1856.On the British Edriophthalma. Part 1. The Bescreibungihrer verschiendenArten .Berlin.p 99– Amphipoda.Report on the25th Meeting of the British 146. Associationfor the Advancement of Science. p18–62. HerklotsJA. 1861. Symbolaecarcinologicae. I. Cataloguedes Bate CS.1862. Catalogueof the specimens ofamphipodous crustace´squiont servi debase au syste ´me carcino- Crustaceain the collection of the British Museum . logiquede M. W.deHaan,re ´dige´d’apre ´slacollection London.p 349–365. duMuse´edePays-Baset les crustace´sdelaFaune du BoeckA. 1861.Bemaerkninger angaaende de vedde norske Japon.Leyde.p 1–43. Kyster forekommendeAmphipoder. Forhandlingerved Kro¨yerH. 1838.Gro ¨nlandsamphipoder beskrevne af Henrik deSkandinaviske Naturforskeres 8.Møde .Copenhagen. Kro¨yer. Danske VidenskabsSelskabet Naturviden- p 631–677. skabeligeog Mathematiske Afhandlinger 7:229–326. BoeckA. 1871.Crustacea Amphipodaborealia et arctica. Larsen K.1998.Caprellidea (Crustacea: Amphipoda)from ForhandlingerVidenskabs Selskabet i Christiania FaroeIslands waters, witha keyto the north-Atlantic 1870:83– 280. species. Fro´dskaparrit 46:81–90. Caine ED.1974. Comparative functional morphology of LaubitzD. 1972.The Caprellidae (Crustacea: Amphipoda)of feedingin three species ofcaprellids (Crustacea, Atlanticand Arctic Canada. Publicationsin Biological Amphipoda)from the northwestern Florida gulf coast. Oceanography,National Museum of Natural Sciences Journalof Experimental Marine Biology and Ecology 4:1–82. 15:81–96. LinnaeusC. 1767.Systema naturae,12th edn. Holmiae 1:533– ChevreuxE, FageL. 1925. Amphipodes.Faune de France , 1327. Vol.9. Paris. 488 p. LinnaeusC. 1800. Ageneralsystem ofnature, through the GoodsirHDS. 1842. On a new genus,and on sixnew species of three grandkingdoms of animals, vegetables and Crustacea, withobservations on thedevelopment of the minerals:systematically dividedinto their several eggand on the metamorphoses of Caligus,Carcinus , classes, orders,genera, species, andvarieties, with and Pagurus.Edinburg New PhilosophicalJournal theirhabitations, manners, economy, structure and 33:174–192. peculiarities. Swansea. 761p. Guerra-Garc ´a–Comparisonbetween Caprellalinearis and C. septentrionalis 235

MayerP. 1890.Die Caprellidendes Golfes vonNeapel undder diceros (Crustacea, Amphipoda,Caprellidae). II. Hyogo angrenzendenMeeres-Abschnitte. Faunaund Flora des Biology 9:280–285. Golfesvon Neapel 17:1–55. Sars GO. 1895. Anaccount of theCrustacea of Norway,Vol. 1, MayerP. 1903.Die Caprellidaeder Siboga-Expedition. Amphipoda.Christiania.711 p. Siboga-Expeditie 34:1–160. SmaldonS. 1990.Suborder Caprellidea. In: Hayward PJ, McCainJC. 1968. The Caprellidae (Crustacea: Amphipoda)of RylandJS, editors. Themarine fauna of theBritish Isles thewestern NorthAtlantic. BulletinUnited States andnorth-west Europe. I. Introductionand protozoans NationalMuseum 278:1–147. toarthropods .Oxford.p 482–488. McCainJC, Steinberg JE. 1970. Amphipoda I. CaprellideaI. StephensenK. 1928.Storkrebs II. Ringkrebs I. Tangloper Fam. Caprellidae.In: Gruner HE, Holthuis LB, editors. (AmŽpoder). DanmarksFauna 32. DanskNaturhis- CrustaceorumCatalogus .Paris.p 1–78. toriskForening. 399 p. MoriA. 1999. Caprellakuroshio ,anew species (Crustacea: StephensenK. 1940.Marine Amphipoda. Zoologyof Iceland Amphipoda:Caprellidea), with a redescriptionof 3:69–75. Caprellacicur Mayer,1903, and an evaluation of the StimpsonW. 1854.Synopsis of the marine Invertebrataof genus Metacaprella Mayer,1903. Proceedingsof the GrandManan: or theregion about the mouth of theBay BiologicalSociety of Washington 112:722–738. ofFundy,New Brunswick. SmithsonianContributions Mu¨ller OF.1776. Zoologiædanicæ prodromus, seu Animalum toKnowledge 6:44–45. daniæet norvegiæindigenarum characteres, nomina, et TakeuchiI. 1989.Taxonomic and ecological studies of the synonymaimprimis popularium .Hafniae. 274p. Caprellidea(Crustacea, Amphipoda)inhabiting the OhlinA. 1895.Bidrag till Ka ¨nnedomenom Malakostrakfau- nani BafŽn Bayoch Smith Sound. ActaUniversitas Sargassum zone.Graduate Schoolof Agriculture, Lundensis 31:60–65. Universityof Tokyo.244 p (unpublishedPhD thesis). OldevigH. 1933.Sveriges Amphipoder. Go¨teborgsVetensk. TakeuchiI. 1993.Is theCaprellidea a monophyleticgroup? Vitterhets-Sa¨mhallesHandl .3:261–270. Journalof NaturalHistory 27:947–964. Pallas PS.1772. Spilicilegiazoologica quibus novae imprimis TakeuchiI, HiranoR. 1995.Clinging behaviour of the et obscuraeanimalium species iconibus,descriptioni- epifaunalcaprellids (Amphipoda) inhabiting the Sar- bus,et quecommentariis illustrantur .Berlin.p 1–86. gassum zoneon the PaciŽ c coast ofJapan, with its PattonWK. 1966.Feeding habitats, behavior and host evolutionaryimplications. Journalof CrustaceanBiol- speciŽcity of Caprellagrahami ,anamphipod commen- ogy 15:481–792. sal withthe starŽ sh Asteriasforbesi. Biological Bulletin WhiteA. 1852.Crustacea. In:Sutherland PC, editor. Journal 134:148–153. ofa voyagein BafŽ n’ sBayand Barrow Straits in the SakaguchiM. 1989.New knowledgeof Caprellascaura years 1850–1851 . London.

Accepted14 March 2001 – Printed20 September2002 Editorialresponsibility: Tore Hø isœ ter