Comparative Notes on Postlarvae and Pelagic Juveniles of the Rocklings Gaidropsaurus Mediterraneus, Rhinonemus Cimbrius, Ciliata Mustela and C. Septentrionalis

J. mar. biol. Ass. U.K. (1985), 65, 801-839

801

Printed in Great Britain

COMPARATIVE NOTES ON POSTLARVAE AND PELAGIC JUVENILES OF THE ROCKLINGS GAIDROPSAURUS MEDITERRANEUS, RHINONEMUS CIMBRIUS, CILIATA MUSTELA AND C. SEPTENTRIONALIS NECLA DEMIR Department of Biology, University of Istanbul, Vezneciler-Istanbul, Turkey

A. J. SOUTHWARD AND P. R. DANDO The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PLi 2PB (Figs. 1-9)

A full series of development stages is described for Gaidropsaurus mediterraneus, Rhinonemus cimbrius, Ciliata mustela and C. septentrionalis from the early postlarval to the late stage of pelagic life, based on samples collected from British waters. In the early postlarval stages, up to 9-10 mm standard length, the four species can be separated on characters provided by body pigmentation, the relative length of the pelvic fins and the relative length of the pigmented part of the pelvic fins. The absence or presence of temporal spines, and their size when present, can be an especially useful character, but fails to separate C. mustela and C. septentrionalis. During later stages of development, the numbers of barbels, their relative length and the size of the postlarvae when they first appear offer important distinguishing features. From about 5 to 7 mm in length, the numbers of either total or pre-caudal vertebrae also help to separate the four species from one another. The seasonal occurrences of the postlarvae and pelagic juveniles of these species in the Plymouth area suggest that spawning of G. mediterraneus and R. cimbrius probably takes place in May-October. Spawning of C. mustela and C. septentrionalis may occur between March and September, but it is probable that most of the spawning of these species occurs in the earlier half of this period. The distribution of rockling postlarvae and juveniles in the plankton off Plymouth does not indicate much geographical separation of the species. INTRODUCTION

Five species of rockling: Gaidropsaurus vulgaris (Cloquet), G. mediterraneus (L.)j Rhinonemus (Enchelyopus) cimbrius (L.), Ciliata mustela (L.) and C. septentrionalis (Collett), are commonly recorded from British waters. With the exception of G. mediterraneus, which has not been recorded from the North Sea, the other four species occur all round the British coasts. Two additional species have recently been added to the list of British fishes, Antonogadus macrophthalmus (Giinther), a southern boreal species and Onogadus argentatus (Reinhardt), a northern boreal species (Wheeler, 1969; Russell, 1976). The identity of adult A. macrophthalmus is, however, still in confusion. It is not clearly known if it is a different species from A. megalokynodon Kolombotovic (a species which occurs in the Mediterranean and adjacent Atlantic waters), since both of them are

802

N. D E M I R , A. J. SOUTHWARD AND P. R. DANDO

considered as synonyms of G. biscayensis (Collett) (Bini, 1970; Tortonese, 1970; Svetovidov, 1973). Cohen & Russo (1979) have since relegated Onogadus and Antefiogadus to synonyms of Gaidropsaurus, though the exact number of species is uncertain. Descriptions of rockling postlarvae from the North-east Atlantic have been given for R. cimbrius and C. mustela by M'Intosh & Prince (1890), Brook (1890), Ehrenbaum & Strodtmann (1904). Ehrenbaum (1905-9), Mielck (1925), and Schnakenbeck (1928). A 3 mm postlarva of C. mustela was illustrated by Arbault & Lacroix-Boutin (1969). Russell (1976), basing his argument on pigment pattern, distinguished and illustrated two types ('mustela' type and 'cimbrius' type) of rockling postlarvae. Recently the description of a full series of development stages has been summarized for R. cimbrius of the North-west Atlantic by Fahay (1983). Cunningham (1889) remarked that two specimens of a young fish 17 mm long collected from the neighbourhood of Plymouth agreed with descriptions given of the young Motella tricirrata, i.e. G. vulgaris. Eighteen postlarvae between 3 and 7 mm in length collected from Killeany Bay, Aran Islands, were referred to G. vulgaris by Fives (1970). The postlarvae of Gaidropsaurus species have more precisely been described from the Mediterranean. D'Ancona (1933) gives the descriptions of postlarvae and juveniles of G. mediterraneus and G. vulgaris of 75-60 mm and 10-265 mm in total length respectively. A full series of development stages has been described for G. mediterraneus and G. biscayensis (i.e. A. megalokynodon) from the early postlarvae to the late stage of pelagic life based on samples collected from the Sea of Marmara (Demir, 1982). A juvenile of O. argentatus 23 mm in standard length from the Labrador Sea was described tentatively as G. vulgaris by Hubbs (1955). The postlarvae and pelagic juveniles of C. septentrionalis and A. macrophthalmus (if it is a different species from A. megalokynodon) have never been described. Most recently, Dunn & Matarese (1984) have summarized knowledge of larval gadids and presented illustrations of Rhinonemus {Enchelyopus) cimbrius, and Ciliata sp., and noted the presence of temporal spines in Ciliata. The published illustrations of C. mustela postlarvae are in some confusion. Postlarvae 10 mm (pi. xvin, fig. 5) and 5, 7-5, 85 mm in length (pi. xn, figs, d, e, f) attributed to C. mustela by M'Intosh & Prince (1890) and Schnakenbeck (1928) respectively, apparently belong to C. septentrionalis. The postlarvae illustrated as 'mustela' type (fig. 38a-c) and 'cimbrius' type (fig. 38d-f) by Russell (1976) probably belong to C. septentrionalis and C. mustela respectively. Of the postlarvae referred to Phycis blennoides by the same author, the smaller one (43 mm) also figured by Dunn & Matarese (1984) as P. blennoides, obviously belongs to C. mustela, and the larger one to C. septentrionalis. Some of the postlarvae (fig. 9a-c) attributed to G. vulgaris by Fives (1970) also probably belong to C. septentrionalis, and some others (fig. 9d-e) to C. mustela. The main purpose of this work is to provide a basis for identifying rockling postlarvae and pelagic juveniles which commonly occur in British waters, especially in the Plymouth area, by giving comparative descriptions for a complete series of development stages.

COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

803

M A T E R I A L S AND M E T H O D S The material came from two main sources. One hundred and fifteen of the rockling postlarvae (2 G. mediterraneus, 2 R. cimbrius, 20 C. mustela, 91 C. septentrionalis) were obtained from samples collected at the routine stations L3, L4, and L5 at almost weekly intervals from March to October 1980 (Fig. 1). Approximately 400 postlarvae (12 G. mediterraneus, 19 R. cimbrius, 30 C. mustela and approximately 340 C. septentrionalis) and 17 pelagic juveniles (4 G. mediterraneus, 10 C. mustela, 3 C. septentrionalis) were obtained from ichthyoplankton collections of the Plymouth Laboratory taken mainly off Plymouth between the years 1969 and 1983, including the 1969-70 inshore fish egg and young fish survey (Southward & Demir, 1972). An additional 90 postlarvae (1 G. mediterraneus, 13 R. cimbrius, 8 C. mustela, 68 C. septentrionalis) and 11 pelagic juveniles (2 R.

J_ 40'

30

20

10

Z,°W

50

Fig. 1. Routine stations off Plymouth sampled for young fish in 1980.

cimbrius, 9 C. septentrionalis) were provided by the Dunstaffhage Laboratory of the Scottish Marine Biological Association, collected from the Tiree Passage (560 27' N, 6° 43' W), Ardalanish Bay (56°i6'N, 6 ° n ' W ) and Bloody Bay (56° 39' N, 6° 06'W) in the years 1975-6. In 1980 collections of the postlarvae from the routine stations were made by oblique tows of approximately 20 min duration, mainly with 1 m square net with a terylene mesh of 700 fim. Most of the specimens larger than 17-18 mm were obtained from special near-surface tows off Plymouth Sound, often in the 'coastal fronts' that develop in the warmer half of the year, demarcating near-shore and estuarine water from offshore water. Such fronts are made obvious by 'streamlines' of drifted seaweed, among which the young rocklings are found. A number of different types of net (1 m round terylene net, 3 m surface net, 2 m stramin net, 20 cm tow-nets) with meshes varying from 300 to 800 /im, were used for collections of the other specimens which belong to different years. Developmental series were established for the species dealt with in this paper by the method of working backwards from adults and juveniles to the early stage of postlarvae. The postlarval period is considered to end at the completion of all fin ray formation. Since the first dorsal fin is last to develop in rocklings, the specimens are classed as postlarvae until all rays of this fin are formed, and thereafter as juveniles. Measurements of the specimens were made using an ocular micrometer in a stereo-microscope. For meristic counts, specimens were cleared with a solution of potassium hydroxide, 1-3 ° 0 w/v according to size, and stained with alizarin red S using a modification of the method described by Hollister (1934). All vertebrae were counted, including the two ural centra. The descriptions and illustrations of the postlarvae and juveniles are based on material preserved in 5 ° 0 aqueous solution of commercial 4O°O formaldehyde buffered with hexamine or borax.

(513-629) — — — — — (44-5-46-5) (45-8-46-0) —

(488-581) (500-54-9) — (51-7-522) (500-511) — — —

(54-1-58-3) (476-600) (52-9-61-1) (542-545) (51-7-53-8) (486-492) (467-47-2) _

(50-0-55-6) (48-8-55-0) (47-1-52-9) (457-518) (453-49-6) — (42-9-47-7) — — —

52-8 — 53 4 ± 4 7 532 ±2-8 50-6 — 52-0 + 0-4 5O-5±o-6 500 — 48-0 — 465 —

56o±2-i 55 9 ± 7 2 561 + 2-4 544 ± 0 2 523 ± i - o 48-9+0-4 470+0-4 47-4 —

53-2 + 2-1 51-8 + 2 5 50-0 + 2-9 478 ±2-0 474±i-3 459 — 44 9 ± 2 5 45 2 — 45-6 — 473 —

35-3-9 4-0-4-4 5-0-5-4 80-89 110-119 18-0-18-9 21-0-21-9 270-279 29 0-29-9

35-3-9 40-4-4 50-5-4 80-89 110-119 18-0-18-9 21 0-21-9 25-0-259

3-5-39 4-0-4-4 5O-54 80-89 110-119 18-0-18-9 210-21-9 25-O-259 270-279 3OO-3O9

(

55'5±55 53 5 — 547 — 53-7 — 50-8 — 486 — 455 ±1-4 459±oi 459 —

Snout to anus length

3 5-39 4-0-4-4 50-54 80-8-9 110-119 18-0-18-9 21-0-21-9 260-269 300-30-9

Size group (mm)

—

27-8+2-7 27-7 ±2-6 290+ 1-3 28-8± 1-4 27 3 + o-S 243 — 246+ 1-8 236 — 233 — 24-3 —

3i-i±2-4 28-3 + 4-4 3O-6± 17 30-4+0-4 28-2+0-7 26-4± 0-6 249+0-5 239 —

30-8 + 0-6 294 — 28-8± 2 5 26-i±0-8 24-1 — 236 22-9 —

293 ± 3 5

27-8

28-6+2-1 29-1 — 330 — 31-7 — 297 — 260 — 246 + 0-9 22'4± 0-4 21-6 —

— — —

(23-3-26-6)

—

(250-308) (25-0-31-8) (27-5-30-0) (26-2-31-3) (26-4-28-8)

—

(286-33-3) (23-8-32-5) (280-333) (30-1-30-7) (27-6-29-1) (25-9-26-8) (245-252)

— — —

(27-0-30-5) (25-4-26-9)

—

(25 0-326) (30-2-31-4)

—

(23-9-25-2) (22-1-22-6)

— — — — —

(263-31-4)

Head length n ] SL

— —

R. cimbrius 45-0 —

1-2 — — —

465+3-6 43-2±3-2 399+23 37 3 ±2-1 31 1 — 30-4+1-4 288 — 286 — 260 —

C. septentrionalis 45-3 + 3-0

444+ 24 43-5 ±3-4 39-5 ±o-8 374± 18 320+ 1-0 305 ±04 300 —

424 ± 2 3

C. mustela

306+ 294 27-7 279

— — —

(293-320)

—

(409-50-0) (41-7-50-0) (40-0-46-4) (36-5-41-3) (350-41-4)

—

(409-45-0) (41-7-46-2) (382-500) (389-400) (35-3-39-1) (31-3-32-7) (30-2-30-8)

— — —

(298-31-9)

4 4 5 ± 4 5 (39-3-500) 44 8+ 1-8 (43-8-46-9) — 400 — 36-o±3-8 (33-3-38-7)

(29-1-29-4) (292-293)

— —

— 1-2 17 — 14 0-7 — — —

28-3±2-7 28-7+2-1 29-0+ 13 243 + o-6 21-3 + 0-8 189 — i8-7±o-9 180 — 178 — 1R0 —

3i-i±2-4 291 + 0-8 302 + 0-9 263 + 0-3 24-7 + 0-7 19-9 + 0-2 20-2+ 02 17-9 —

292 28-3± 28-8± 24-7 22-7± 20-1 + 198 193 18-9

161 + o-i 164 —

16 8±o-3

— —

23-8±o 8

(38-5-40-4)

— —

220 18-8

290+ 29 27-9 — 27-4 —

(17-7-19-3)

—

(250-308) (26-2-31-8) (27-5-3O-O) (233-253) (20-7-22-5)

(28-6-333) (286-300) (29-4-31-5) (26-1-26-5) (24-1-25-6) (19-7-20-0) (20-0-20 3)

— — —

(21-7-23-7) (19-4-20-6)

—

(27-3-30-0) (26-9-302)

—

—

(16-4-17-0) (16-0-16-2)

— —

(23-2-244)

— —

(25-0-31-4)

Body depth SL

(40-9-45-5)

441 ± 2 1 440 — 400 — 39 5± 13 35-7 — 298 — 2 9 2 + 0-2 29 3 ± o i 27-3 —

G. mediterraneus

Eye width Head length

Proportions expressed as x + s.D.; figures in parentheses show ranges.

5-4 + 0-2 5-5 ±0-6 6-3 + 0-6 83 ±0-7 100+0 8 135 — 13-1 + 0-6 134 — 141 —

7-0 — 7-2 + 0-2 8-8+1-3 94 — i3-4± 1-6 155 + 0-5 14-7 + 0-6 143 —

56 5-9 ± 0 3 6-7+ 0-2 8-2 — 129+0-2 16-3 ± 0 3 14-6 — 149 — 148 —

5'7±o-5 6-5 — 8-5 11-6+0-8 144 — 149 — 137 + o-6 129 + 0-4 131 —

— —

(12-6-13-8)

—

(51-5-6) (5-0-6-1) (5-9-6-9) (7-1-9-3) (8-6-n-i)

(11-6-14-7) (151-15-8) (14-3-15-1)

(71-7-5) (7-4-10-0)

—

—

(12-7-13-0) (16-1-167)

(5-7-6-3) (6-6-6-9)

—

—

(12-6-13-2)

D > Z a 0

50

z0

0 >

JO

>

X

a

0

JO > (133-141)

1—'

—

aw

z

2

oo

—

(110-12-2)

(5-3-6-4)

Pectoral nn length SL

Table 1. Comparison of body proportions of postlarvae and pelagic juveniles of four rockling species

Size

4-0-4-4 5-0-5-4 8-0-8-9 11-0-11-9 18-0-18-9 21-0-21-9 250-259 270-279 30-0-30-9

3-5-39

11-0-11-9 18-0-18-9 210-21-9 250-25-9

35-39 40-4-4 5-0-5-4 80-89

5-0-5-4 80-89 11-0-11-9 18-0-18-9 21-0-21 9 270-279 290-29 9

4-0-4-4

3-5-39

5-O-5-4 8-0-8-9 110-119 180-18-9 21-0-21-9 260-26 9 300-309

40-4-4

3 5-39

group (mm)

—

18-4 i6-8± 14 152 — 152 — 147 —

246+ 4 0 256+ 2-8 28-3± 10 31-6+ 1-6 26-8+ 1-4

17-6+ 1-5 15-1 —

i8-8±o 5

357+0-6 294 ±2-4

4i-2± 15 39-6 + 2-5 399±i-8

25-0 — 264 ± 3 2 30-8 ± 17 282 — 29'2±l-7 2i-8± 0 4 203 — 171 — 158 -

131

18-2 — 149+O-9 1 4 0 + 0'4

320+ 16 326 340 — 28-7±2-6 21-2 —

SL

(15-7-18-3) — — —

(19-4-28-2) (21-4-29-5) (27-5-29-4) (29-6-338) (245-28-8) —

(40-0-43-2) (381-425) (370-426) (35-2-36-1) (27-6-32-1) (18-4-191) (16-5-18-6) —

—

—

—

— (22-5-302) (28-8-32-1) — (280-304) (21-5-22-2)

(137-143) —

(308-34-3) — — (26-8-305) — — (14-2-15-5)

v [i;

Pelvic fin lengthy

— — — —

— — — —

— — — — —

— — — — 16 10-2

— — — —

7-8 10-8± 11-9 111 17-8

— 1-2 — — —

i-3±o-4

— — — —

n-4+2-5 133 —

— — —

275 262 324

i9-7±2-3

3-8±i-4

— — — 1-2

23 — 64 — 8-9± 1-6 12-7+0-8 16-7 -

— — — —

— —

—

— — — — (0-9-1-7) — (lOO-12-l)

— — — — — — (9-6-13 2)

—

— — — — (2-8-48) (180-21-3) — —

— — — — — — (78-100) (12-1-13-3) —

Head length

Length of first ray of first dorsal fin

—

153 159 164

— — —

C. septentrionalis — — — — — — — — 6-1 + 0-7 111 — 138+1-3

l7-6± 1-8 i 8 i ± 1-6 200 —

6-6 ±09

3 1

C. mustela — — — — — —

R. cimbrius — — — — — — 6-0 — 9 0 + 10 16-7 ±2-2 19 6 — 23 1 — 22" 1 —

11-7 — 13- 7 ±O1 19 5 ± 0 7 22-7 —

G. mediterraneus — — — — — — 19 — — —

(47-6-7) — (12-5-15-0) — — —

— — — —

— — — — (5-9-7-6) (163-18-8) (17-0-19-2) —

—

(8-3-9-7) (14-9-19-1) — —

—

—

—

—

—

— — — — — — (13-6-13-7) (190-200)

Head length

chin barbel /,()

Length of

Table 1. (Cont.)

— —

4-3 53

—

—

— — — — — (43-6-4) — —

(6-9-8-2) (10-0-10-3) —

_ —

— — — —

95 110

— —

— — — — — — — 1-6 — 33 — 5-8 ± 0 3 8-5 -

— —

— — — — — — (54-6-0) -

— — — — — — — — — — — — 31 — — 108 ±2-0 (9-4-12-2) 1 2 4 + 12 (11 5-132) 15-8 -

n-8

— — — — — — — — 2-8 — 5-6±i-i 8-8 — 108 —

7-6 + 0-9 10-2+0-2 136 —

— — — —

— — — 0-8

Head length

Length of nostril barbel

— — — —

— — — — — — — — —

— — — — —

—

— —

—

1-7 1-6 27

— — —

— — — — — — — — — — — — 1-3 + 0 6

100

47±o-6 5-8±o-i

— — — — —

51

39 4-6

1-4 — 21 + 0 1

— — — —

— — — — — — — — —

— — — — — — — — —

(0-9-2-0) — — —

— —

— —

(4-2-5-0 (5-7-5-8) —

—

—

00

Z 0

r

O

O

71

HJ

n

2;

—

—

0

0

• <

0

r0

O

X

•"3

s, O

td

H

I>

73

!>

O

CJ

—

—

—

—

— — — — — (2-O-2-1)

Head length

Length of upper lip barbel

806

N. D E M I R , A. J. S O U T H W A R D AND P. R. DANDO

DEVELOPMENT OF G. MEDITERRANEUS,1 R. CIMBRIUS, C. MUSTELA AND C. SEPTENTRIONALIS

Body proportions (Figs. 2-7)

All rockling postlarvae have a similar characteristic appearance. In the early postlarval stage up to about 10-12 mm, they are deep-bodied and stubby in form with large rounded head and snout, although the caudal portion of the body is slender at the beginning of this stage. In the late postlarval and juvenile stages, which are known as 'mackerel midges', however, they become slimmer and moderately elongate in shape, with smaller head and pointed snout. Full details of measurements made on 19 specimens of G. tnediterraneus, 34 specimens of R. cimbrius, 67 specimens of C. mustela and 221 specimens of C. septentrionalis are given in Tables 4-7. Their body proportions at comparable sizes are shown in Table 1. The average body depth as a percentage of standard length progressively decreases in each species and shows slight differences among them. In the postlarval stage between 3 5 and 12 mm in length, however, C. mustela, which has an average relative depth ranging from 31 % SL to 25 % SL, is deeper-bodied than the other three species, which have an average relative depth ranging from about 28-29% SL to 21-23% SL respectively. At 18-19 mm m length the average relative depth is about 19-20% SL in all these rocklings. In more advanced stages of development, G. tnediterraneus, which has a relative depth of 16-17% SL, becomes slimmer-bodied than the other three species, which have an average relative depth of about 18-20% SL. In all rockling species under consideration, at the beginning of postlarval development (at 2-8-3-6 mm), the ventral primordial fin, as usual in gadiformes, is not traversed by the rectum and in correspondence with this the anus opens laterally to this fin and does not become vertical until postlarvae reach about 6-8 mm. At 3-5—5-5 mm postlarvae, the average relative snout-anus length is about 50-53 % SL in C. septentrionalis, 53 % SL in R. cimbrius, 54-55 % SL in G. tnediterraneus, 56% SL in C. mustela. At 11-12 mm, it decreases to about 47% SL in C. septentrionalis and to 51-52% SL in the other three species. At 21-22 mm it becomes about 45% SL in C. septentrionalis, 46% SL in G. mediterraneus, 47% SL in C. mustela and 50% SL in R. cimbrius. In more advanced stages of development the relative snout-anus distance varies between about 46 and 48 % SL in all of them. It can be concluded that during the postlarval stage the anus is generally more anteriorly situated in C. septentrionalis than in the other three species, being generally in front of the middle of SL after a length of about 7-8 mm is reached in C. septentrionalis and behind it in the other species until a length of about 18-20 mm. 1 We have observed considerable differences between the development of G. mediterraneus of the Atlantic and that of the Mediterranean G. mediterraneus in body proportions, pigmentation, temporal spines, rates of development and seasonal occurrence. We hope to discuss this problem after obtaining more postlarval specimens of G. mediterraneus from the Atlantic and after examination of the proteins of the adult stages by gel electrophoresis.

COMPARATIVE MORPHOLOGY OF YOUNG R O C K L I N G S

807

The average head length as a proportion of standard length, which is about 28-31 % SL at 3-5-3-9 mm, increases to 29-33 % SL at 5—5-5 mm, but decreasing progressively during later stages of development becomes about 22-24 % SL after a length of 22 mm is reached in all rockling species included in this report. The average relative head length is, however, generally smaller in C. septentrionalis, larger in C. mustela (especially at 3-5-45 mm) and G. mediterraneus (especially between 5-13 mm) and intermediate in R. cimbrius. In all these species, the mean eye width as a percentage of head length is about 42-45 % HL in the early postlarvae at 3-5-4 mm in length, but it gradually declines to 28-30 % HL in late stage of pelagic life between 25 and 28 mm in length. It is noteworthy that the body proportions mentioned above are not of particular value in distinguishing among these species, since they vary considerably from specimen to specimen within each species. Fins Pelvic fins

The most salient characteristic of rockling postlarvae is their large blackpigmented pelvic fins, which develop after the larval pectoral fins. Four rays of these fins with the pigmented membranes between them have already formed in the smallest specimens of G. mediterraneus, R. cimbrius, C. mustela and C. septentrionalis at 2-8, 36, 3 3 and 3-3 mm respectively. The fully developed pelvic fins of G. mediterraneus have 7-8 rays (both left and right pelvic with an average of 7286, mode 7). Development of these fins has not been properly followed in this species, since the specimens especially between 5-18 mm in length are very few in number. In the specimens at 53 mm, 8-2 mm and 11 -8 mm in length, however, the fifth, sixth and seventh rays of the pelvics, respectively, have already been formed. The adult complement of pelvic rays is 5-6 in R. cimbrius (left pelvic with an average of 5875, right pelvic average 575, mode 6). The fifth ray of the pelvics starts to develop at about 7 mm and the sixth ray at 10 mm in length in this species; 5-6 pelvic rays, as usual for G. mediterraneus of the Mediterranean, have, however, been reported for G. mediterraneus of the Atlantic (personal communication A. Wheeler, British Museum (Natural History) London) and 7 rays for R. cimbrius (Fahay, 1983). The full complement of pelvic rays is also 7-8 in C. mustela and C. septentrionalis (left pelvic average 7-3, right pelvic average 7-2, mode 7 and left pelvic average 7364, right pelvic average 7454, mode 7 respectively). In both species, the fifth ray of these fins begins to form at about 6-5-7 mm, the sixth at 8-8-5 m m an£ l the seventh at 11 5-12 mm. The size at which the eighth ray begins to develop could not be determined, but eight pelvic rays have already been formed in specimens larger than 17 mm in both species. Of the other rockling species which may occur in the area investigated, G. vulgaris has 7-8, O. argentatus 8 and A. macrophthalmus 5 pelvic rays (Svetovidov, 1948; Hubbs, 1955; Tortonese, 1970). That is, the number of pelvic fin rays is not particularly useful in separating the rockling species of the North-east Atlantic, but it is one of the main features for

5-0-5-4 5-5-5-9 6-0-6-9 7-0-7-9 80-89 9-0-9-9 10-0-10-9 11-0-11-9 12-0-12-9 140-14-9 15-0-15-9 16-0-16-9 17-0-17-9 18-0-18-9 21-0-21-9 26-0-26-9 28-0-28-9

group (mm)

Size

—

42-4 320

— —

61-3 + 9 5

8-9

(54-5-68-O)

—

Length of pigmented part of pelvics Pelvic length

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(32-4-37-5)

35-o±3-6

— — (70-8-100) — — (600-781) (71-4-75-8) _ (40-5-52-7)

— —

79-7+13-9 75-0 — 640 — 69-1 + 12-8 73-6±3-i 694 _ 468 + 6-1

100 100

Length of pigmented part of pelvics Pelvic length

R. cimbrius

— — — (66-7-100) (56-7-64-5)

(40-6-66-7)

— (25-0-27-3)

— 100 100 — 100 — 83-4123-5 60-6 + 5-5

50-9+13-9

290 — 26-2+1-6

Length of pigmented part of pelvics Pelvic length

C. mustela

Lengths expressed as x + s.D.; figures in parentheses show ranges.

92-9112-4 818+ 188 59-7+11-8 5O-o±59 45-4+59 393±52 38-7 + 4-9 37O± 6-1 33-2+30 — 40-1 31-8+8-7 31-8+2-1 — 303 32-4 — 36-1 + 1-5 28-6 — 200 —

(786-100) (55-6-100) (37-5-833) (333-63-6) (35-7-520) (32-1-48-1) (321-500) (28-1-46-7) (29-4-36-4) — (24-2-45-7) (3O3-333) — — (35-0-37-1) —

Pelvic length

Length of pigmented part of pelvics

C. septentrionalis

Table 2. Comparison of the length of pigmented part of the pelvic fins of four rockling species ecies

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COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

809

distinguishing rockling postlarvae larger than about 7 mm from those of P. blennoides. According to D'Ancona (1933), P. blennoides also has large blackpigmented pelvics with four rays in the early postlarval stage, but after a length of about 10 mm is reached, the fourth ray of the pelvics is reduced and only three pelvic rays remain until 46 mm. The fully developed pelvics of this species have a single branched ray. In postlarvae at 3-5-5-5 mm in length, the mean pelvic length as a proportion of standard length is 40-41 % SL in C. mustela, 32-34 % SL in G. mediterraneus, 25-31 % SL in R. cimbrius and 25-28% SL in C. septentrionalis. With development decreasing progressively it becomes about 36% SL, 29% SL, 28% SL, 32% SL at 8-89 mm and 29% SL, 21 % SL, 29% SL, 27% SL at 11-11-9 m m respectively. At 18-189 mm, the average relative length of pelvics is about 18-19% SL in C. mustela, G. mediterraneus and C. septentrionalis, 22% SL in R. cimbrius. In later stages of development (between 21 and 30 mm), it is shorter in G. mediterraneus (13-15% SL), longer in R. cimbrius (16-20% SL) and intermediate in C. mustela and C. septentrionalis (15-18% SL). As mentioned above, the black pigmentation on the membranes between the upper four rays of the pelvic fins covers their entire length in early postlarvae, but with development it progressively becomes restricted to the distal part only and is not generally retained in late stages of pelagic life (see below). In R. cimbrius and C. mustela, the membranes between the pelvic rays are entirely pigmented until postlarvae attain a length of abut 7-8 mm, in G. mediterraneus and C. septentrionalis until 5-6 mm. In the latter two species the average length of the pigmented part, as a proportion of pelvic length, is about 89 % VL and 93 % VL at 5-5-5 mm respectively. It is considerably shorter in 8-8-9 mm and i 1 - 1 i 9 mm postlarvae of C. septentrionalis (45 % VL, 37 % VL respectively) than those of the other three species (75% VL, 74% VL in R. cimbrius, 61% VL, 42% VL in G. mediterraneus and 61 % VL, 51 % VL in C. mustela respectively). Since pigmentation of the pelvicfinscan easily be rubbed off during collection, especially in the specimens larger than 15 mm, we could only observe that at 17-18 mm the average relative length of the pigmented part of pelvics is shorter in C. mustela (26 % VL), longer in R. cimbrius (35 % VL) and intermediate in C. septentrionalis (30-32% VL). The black pigment remains on the pelvic fins of C. septentrionalis until a length of about 29 mm is reached (see Table 2). It can be concluded that the relative lengths of the pelvics, together with the proportions of the pigmented part, are very useful characters in separating postlarvae (especially early postlarvae up to 9-10 mm) of the above-mentioned rockling species, provided that the pigment is not rubbed off during collection. Caudal fin

In rocklings, the third fin to develop is the caudal.The differentiation of its rays is initiated on hypurals, after postlarvae are 3-5-4 mm long, before the notochord flexion which starts at about 4-4-5 mm and approximately 10 mm and longer postlarvae have fully formed caudal rays. In the rockling species considered in

8l0

N. DEMIR, A. J. SOUTHWARD AND P. R. DANDO

this report, the fully developed caudalfinis associated with the last eight or nine vertebrae. The numbers of caudal rays supported by posterior and ultimate hypurals (i.e. hypurals 4-6 and 2-3 of Matarese, Richardson & Dunn, 1981, respectively) are 4-5 and 2 in G. mediterraneus, 5 and 2 in R. cimbrius and C. mustela, 4-5 and 1-2 in C. septentrionalis respectively. After a length of about 10 mm is reached, this characteristic is valuable in distinguishing rockling postlarvae from those of Phycis species which, according to D'Ancona (1933) and Markle (1982), have 6 rays associated with hypurals 4-6 and 3 rays with hypurals 2-3. The total number of caudal rays and those of superior procurrent and inferior procurrent rays are 30-36, 13-15 and 13-16 in G. mediterraneus, 32-36, 13-15 and 14-16 in R. cimbrius, 34-36, 14-15 and 15-16 in C. mustela, 33-36, 14-15 and 15-16 in C. septentrionalis respectively. That is, neither superior and inferior procurrent rays nor total rays of caudalfinmarkedly differ among these rockling species as far as their numbers are concerned. Their numbers are, however, rather different from those of O. argentatus, which has 41-44 total caudal rays, of which 17-19 are superior procurrent rays and 19-20 inferior procurrent rays (Markle, 1982). Second dorsal and anal fins

In the postlarvae of the rockling species dealt with in this paper, at a length of about 4-5 mm, the bases of the second dorsal and anal fins begin to form simultaneously, but no ray is ossified. Postlarvae 11-12 mm and larger have the adult complement of rays in both fins. According to meristic counts made on 10 specimens of G. mediterraneus, 10 specimens of R. cimbrius, 16 specimens of C. mustela and 34 specimens of C. septentrionalis, the fully developed second dorsal and anal fins have 54-59 rays (average 564) and 45-48 rays (average 468, mode 47) in G. mediterraneus, 44-48 rays (average 457, mode 45) and 38-40 rays (average 388) in R. cimbrius, 45-52 rays (average 4875) and 39-44 rays (average 41-75) in C. mustela, 44-50 rays (average 47588, mode 48) and 38-45 rays (average 40912, mode 40) in C. septentrionalis respectively. In the other rockling species and P. blennoides, which are the most probable sources of confusion with the four rockling species in the area investigated, the adult complements of the second dorsal and anal fin rays are 56-64, 46-52 in G. vulgaris, 53-59,45-50 in A. macrophthalmus, 52-62,43-49 in O. argentatus and 60-64, 50—55 in P. blennoides respectively (Wheeler, 1969). That is to say, the three-bearded rocklings (G. mediterraneus, G. vulgaris, A. macrophthalmus, O. argentatus) have a considerably higher number of second dorsal and anal fin rays than four-bearded (R. cimbrius) and five-bearded rocklings (C. mustela and C. septentrionalis). The second dorsal and analfinray counts are of use in distinguishing the postlarvae of these two groups of rocklings from each other, especially after these fins are fully formed, although they are not of particular value in separating the species within each group. Pectoral fins

As mentioned previously, the larval pectoral fins are present in the smallest specimens of each species included in this report. They consist of a fleshy base

COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

811

and an undifferentiated membrane without rays. The rays of the pectoral fins appear when the postlarvae attain a length of about 5-7 mm. Postlarvae 10-12 mm and larger have the adult complement of 16-17 rays (left pectoral average 16889, right pectoral average 167, mode 17) in G. mediterraneus, 14-17 rays (left pectoral average 15143, right pectoral average 15286) in R. cimbrius, 15-17 rays (left pectoral average 165, right pectoral average 16778, mode 17) in C. mustela and 15-19 rays (left pectoral average 1668, right pectoral average 1684, mode 17) in C. septentrionalis. The pectoral fin ray counts are not particularly useful distinguishing characters even after full complement of rays are formed, but after a length of about 10-12 mm is reached they are more satisfactory in separating the rest from G. vulgaris,A. macrophthalmus and O. argentatus, which have 20-22, 21-23, 22-24 pectoral rays respectively (Wheeler, 1969). In the rockling species included in this paper, the mean relative length of pectoral fins, which is approximately 5-5-7% SL in 3-5-4-5 mm postlarvae, progressively increases to a maximum of 14-16% SL at 18-18-9 mm, that is by the end of the postlarval stage. In later stages of development it gradually decreases, and becomes about 13-15% SL at 29-30 mm in length. The mean relative length of the pectoral fins does not generally much differ among species; it is, however, longer in G. mediterraneus than the other three species between about 8 and 12 mm in length and slightly smaller in C. septentrionalis than in the other three species, especially between about 9 and 18 mm in length (see Table 1). First dorsal fin

The fully developed first dorsalfinof rocklings, in contrast to that of Phycis which has 8-9 normal rays, has a single long ray followed by a series of shorter separate rays in a shallow groove. Thisfinstarts to develop with the appearance of its first ray at 8-5-9 m m m R- cimbrius and after 10-11 mm is reached in the other three species. The differentiation then proceeds posteriorly and the full complement of 73-79 rays in G. mediterraneus, 50-53 rays in R. cimbrius, 50-60 rays in C. mustela and 45-59 rays in C. septentrionalis is formed after respective lengths of about 22 mm, 22 mm, 19 mm and 25 mm are reached. Thus only G. mediterraneus can be separated by the number of first dorsalfinrays. (No report exists on the full complement of rays of first dorsalfinof the other rocklings of the North-east Atlantic.) In rocklings the length of the first ray of the first dorsalfinas a percentage of head length progressively increases during development, being more rapid in R. cimbrius than in the other three species. The mean relative length of this ray, which is 1 2 % HLat 8-5 mm in/?, cimbrius, increases to 3 8 % HLat 11-11-9 m m when it is between 13 and 2 3 % HL in the other three species, and attains 275 % HL at 21-21-9 m m and 324% HL at 29-29-9 mm, becoming about 2-3 times longer than that of the other species at comparable sizes (see Table 1 and Figs. 2D-E, 4D-F, 5F-G, 7E-G). That is to say, starting at about 8-5-9 m m > R. cimbrius postlarvae are separable from those of the other three species on the basis of the relative length of the first ray of the first dorsal fin.

812

N. DEMIR, A. J. SOUTHWARD AND P. R. DANDO

COMPARATIVE MORPHOLOGY OF YOUNG ROCKLIMGS

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COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

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Pigmentation (Figs. 2-7) Distribution of pigment

In the rockling species included in this report, starting from the early postlarval stage until the end of pelagic life, pigment is found on the head (on the top of the head, on the preorbital region, on the tip of the upper jaw, along the mandible, on the opercle, pre-opercle and gular regions), body (on the peritoneum, on the surface of the body and around the neural tube and vertebral column) and pelvic fins. In later stages of pelagic life, melanophores are not retained on the pelvic fins (see pelvic fins), but they appear on the fleshy base of the pectoral fin starting from a length of 115-16 mm according to species. The pigmentation of the head and the peritoneum differs among the species mainly in concentration, and follows a sequence of development similar to that of the Mediterranean species of Gaidropsaurus described by Demir (1982). The embedded melanophores, which are arranged in a row on the neural tube, in a row ventral to the vertebral column and in a row dorsal to the vertebral column, follow similar sequences of development in all rockling species. At about 4-5 mm in length, soon after, the row of melanophores on the neural tube starts to develop both behind the head and at about the midtail simultaneously, the row of melanophores ventral to the vertebral column appear at about the midtail, while the row of melanophores dorsal to the vertebral column appears at about the midtail by 7 mm. As development proceeds, melanophores are formed progressively, so that the rows of melanophores on the neural tube and dorsal to the vertebral column continuously extend from behind the head to the base of the caudal fin and the row of melanophores ventral to the vertebral column from the peritoneal pigment to the base of caudal fin. These rows of melanophores, which are illustrated in R. cimbrius and C. mustela postlarvae by Ehrenbaum (1905-9) and Schnakenbeck (1928) are not shown in Figs 2-7, to prevent confusion with characteristic body pigmentation. The melanophores which appear around the posterior 8-9 caudal vertebrae after 10-11 mm is reached, are however, shown with broken lines in thesefigures.The pigment patterns on the body surface of these species are rather different from one another until approximately 8-10 mm. After this size is reached they become similar to those of the Mediterranean G. mediterraneus and follow a similar sequence of development. Some differences are present among the pigmentation of the species, especially as far as the concentration and size of melanophores are concerned. In all rockling species, after the postlarvae attain a length of approximately 9-10 mm, when they are known as 'mackerel midges', their bodies become silvered, and in freshly preserved specimens the colour is greenish-blue on the back and silvery on the sides and belly. The development of pigmentation of the species under consideration is fully illustrated in Figs. 2-7. The characteristic pigment pattern of each species in the early postlarval stage will be discussed here briefly, because of its importance in separating the species. It is also noteworthy that from the early postlarval stage melanophores show considerable variations in size, number and location from specimen to specimen at comparable sizes.

8i6

N. DEMIR, A. J. SOUTHWARD AND P. R. DANDO

COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

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COMPARATIVE MORPHOLOGY OF YOUNG ROCKLINGS

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COMPARATIVE MORPHOLOGY OF YOUNG R O C K L I N G S

821

Pigmentation of the individual species

In the smallest specimen of G. mediterraneus the characteristic feature of the pigment pattern is the presence of a dorsal and a ventral stripe of melanophores along the dorsal and ventral body midline situated at about the midtail (75 % SL) and two pigment spots close to each other on the ventral side of the notochord tip on the finfold. The stripes are a single row of melanophores and composed of 3 and 2 melanophores respectively (Fig. 2A). At 3-5-4-3 mm postlarvae, the numbers of melanophores in both stripes increase to a maximum of 5. There are also 1 or 2 melanophores along the lateral line between these stripes and 2-4 ventral spots near the bases of the future caudal rays (Fig. 2 B). In a single specimen of 53 mm in length there were double rows of melanophores extending from behind the head to the base of the caudal fin on both sides of the dorsal midline along the bases of the second dorsal fin and a row of melanophores extended on the anterior two-thirds of the tail along the lateral line of the body. Scattered melanophores are found both dorsally and ventrally on the lateral surfaces of the tail, with the exception of its posterior third, and a continuous dorsolateral pigment band (which is characteristic of all rockling postlarvae and pelagic juveniles, but appears after a length of about 8-10 mm is reached in the other rockling species) has begun to be distinct, running from behind the head to near the end of the second dorsal fin. At 8-2 mm in length the body is almost entirely covered with melanophores with the exception of the posterior part of the tail tip. The nape especially is heavily pigmented (Fig. 2C). In the postlarvae of R. cimbrius at a length of 3-6-4-5 mm, there is generally only a dorsal stripe situated about the midtail, but some specimens show a spot at the ventral side of the notochord tip. The stripe is formed from a double row of melanophores (viewed dorsally) on both sides of the body along the dorsal midline, 3 or 4 melanophores on each side (Fig. 4A). A few melanophores appear behind the head on both sides of the dorsal midline by 4 5 mm. With development, melanophores are gradually formed between these melanophores and the dorsal stripe, becoming continuous with them by 5 mm. Approximately at this size a row of several melanophores appear along the lateral line of the body at about the midtail (below the dorsal stripe), where a number of scattered melanophores develop between this row and the dorsal row of melanophores by 6 mm (Fig. 4B-C). With further development, this pigmented area gradually widens with the formation of new melanophores, so that the body is covered with large branched melanophores except for the small area just above and behind the abdominal cavity and the tail tip. A continuous band of dorsolateral pigment from behind the head to the base of the caudal fin, which will remain to the end of pelagic life, becomes conspicuous at about 9-10 mm (Fig. 4D). The ventral side of the hypaxial region of the tail, however, remains free of melanophores up to about 8-9 mm. In C. mustela postlarvae at 3-3-4 mm in length, three characteristic ventral pigment spots exist on the tail on both sides of the ventral midline. The

822

N. DEMIR, A. J. SOUTHWARD AND P. R. DANDO

Fig. 7. Postlarvae of C. septentrionalis. (A) 42 mm. (B) 59 mm. (C) Another of 59 mm to show pigment variation. (D) 72 mm. (E) 102 mm. (F) Another of 102 mm to show pigment variation. (G) 222 mm (metamorphosing specimen).

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N. D E M I R , A. J. SOUTHWARD AND P. R. DANDO

anteriormost of these is situated behind the anus (on the 3rd~5th post-anal myomere), the posterior one is below the notochord tip on finfold and the middle one is located about midway between them (see Fig. 5 A). In some of the specimens, however, there are two spots on the ventral side of the notochord tip instead of a single one. At a length of 4-5-5 mm, beside a few scattered melanophores on the nape, double rows of melanophores appear on both sides of the body along the dorsal midline. These rows, which extend from the nape to beyond the midpoint of the standard length, progressively proceed more posteriorly and reach to the base of the caudal fin by 8 mm. Two anterior ventral spots on the tail begin to migrate upward on the lateral surface of the tail after 4-5-5 mm is reached, and 4 or 5 small melanophores replace the second of these spots by 6 mm. Starting at about 7 mm, a row of melanophores which begins to develop along the lateral line from just behind the anus progresses posteriorly and reaches the base of the caudal fin by 8-9 mm. Scattered melanophores, which are found between the base of the second dorsal fin and the ventral spots, progressively spread over lateral surfaces of the midtail. The continuous dorsolateral pigment band from behind the head to the base of the caudal fin becomes conspicuous after a length of about 8 mm is reached (Fig. 5B-E). In postlarvae of C. septentrionalis at 3-3-4 mm in length, melanophores arranged more or less in a single row along the ventral body midline extend from behind the anus (from the second or third post-anal myomere) to about 80 % SL (25th or 27th post-anal myomere). There is also a spot present on the ventral side of the notochord tip on the future hypural plate. Dando (1975) was able to hatch larval stages from artificially fertilized eggs. The pigment pattern of the living larva appeared to be similar to that of C. mustela: there was a spot on the ventral side of the notochord tip and two equally spaced bands of melanophores between the anus and the caudal spot. After fixation, however, Russell (1976) detected a ventral row of very small melanophores behind the posterior pigment band. At about 4-4-5 mm in length, the anteriormost 3 or 4 melanophores of the ventral series become embedded and progressively take place at the ventral side of the vertebral column, while the rest form double rows of melanophores (viewed ventrally) on both sides of the body along the ventral midline (Fig. 7 A). Although these rows of melanophores generally consist of 5-6 melanophores each, the numbers on each row are very variable, since with further development some of them begin to migrate upward on the lateral surfaces of the tail, while others become embedded. While this process occurs, some melanophores arranged in double rows (viewed dorsally) along the dorsal midline of the body appear both on the nape and on the midtail by 5 mm. Starting about this size, several melanophores arranged in a row along the lateral line of the body develop at about the midtail, together with 3-5 melanophores scattered both dorsally and ventrally (Fig. 7B). The dorsal rows of melanophores on the nape and on the midtail proceed progressively towards each other, becoming continuous and reaching to the base of the caudal fin, with the addition of new melanophores, by 6-7 mm. The row of melanophores on the lateral line, which progressively extends both

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