The reproductive cycles of Chthamalus stellatus (Poli) and C. montagui Southward in south-western Ireland

Journal

ELSEVIER

of Experimental Marine Biolonv 190 (1995) 17-38 -.

The reproductive and C. montagui Ruth Department Received

cycles of Chthamalus stellatus (Poli) Southward in south-western Ireland

M. O’Riordan*,

of Zoology, 25 October

and EcoloavI_

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Alan A. Myers,

Thomas

F. Cross

University College Cork, Lee Maltings, Prospect Row, Cork, Ireland 1994; revised

received

27 January

1995; accepted

8 February

1995

Abstract

The reproductive cycles of two intertidal barnacles, Chthamalus stellatus (Poli) and C. Southward, were studied at Lough Hyne Marine Reserve, Cork, Ireland, over 28 months. In both species there were seasonal trends in development of the male and female reproductive organs with, for example, the ovaries regenerating while eggs were being brooded. Breeding occurred mainly during June-August but also at other times. The sizes of the ova and eggs of the two species were compared and the timing of the cycles relative to other areas considered.

montagui

Keywords: Barnacle; Brooding; size; Reproductive organs

Chthamalus

montagui;

Chthamalus

stellatus; Ova and egg

1. Introduction

Prior to the recognition of Chthamalus stelfutus (Poli) and C. montagui Southward as separate species (Southward, 1976) extensive research work was carried out on various aspects of the reproductive cycle of C. stellutus agg., including the breeding season (Bassindale, 1936; Crisp, 1950; Southward and Crisp, 1954; Daniel, 1958; Le Reste, 1965; Barnes, 1972) variation in the percentage of adults with egg masses at different shore levels (Klepal & Barnes, 1975) and at different latitudes (Crisp and Fischer-Piette, 1959), the number of annual broods (Crisp, 1950; Barnes & Crisp, 1956; Pate1 & Crisp, 1960a; Barnes, 1963) asynchronous reproduction of the population (Pate1 & Crisp, 1960a; Barnes, 1972) egg size (Powell, 1954; Pate1 & Crisp, 1960b; Barnes & Barnes, 1965), the

* Corresponding

author.

0022-0981/95/$09.50 @ 1995 Elsevier SSDZ 0022-0981(95)00029-l

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B.V. All rights

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R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (lY95)

17-38

effect of temperature on egg size (Pate1 & Crisp, 1960b), and the rate of development of eggs (Pate1 & Crisp, 1960a). Klepal & Barnes (1975) examined ovum size, as well as egg production, while Barnes & Barnes (1968) investigated variation in egg production with tidal level and with latitude. Barnes & Crisp (1956) and Barnes & Barnes (1958) discussed the capability of C. stellarus agg. (probably C. montagui, from the degree of exposure of the shores involved) to self-fertilize, while Southward & Crisp (1954) and Daniel (1958) commented on the age at first breeding. Barnes (1972) carried out detailed work on the seasonal changes in body weight and biochemical composition of adult C. stellarus agg., while other authors examined the lipid composition of the bodies (Morris & Barnes, 1975) and the relationship between the time of copulation and ecdysis (Crisp & Patel, 1958; Pate1 & Crisp, 1961). Pate1 & Crisp (1960b) examined the upper temperature limits for breeding. Since the recognition of C. stellatus and C. montagui as distinct species, most of the work on their reproductive biology has been concerned with their breeding seasons. In this study, the terms reproductive cycle and breeding season are used sensu Bousfield (1954), i.e. the reproductive cycle encompasses the entire period from the incipient development of ova and sperm in the gonads to the time of attachment and metamorphosis of the cyprid-stage larvae, whereas the breeding season embraces that part of the reproductive cycle concerned with the deposition, fertilization, development, and hatching of the egg in the mantle cavity. The term ovum applies to an unfertilized egg in the ovary, the term egg to a fertilized ovum. Eggs, containing developing embryos, are incubated in the mantle cavity in masses known as egg lamellae. Southward (1976) suggested, from preliminary data, that the two species may differ in their periods of breeding, with C. stellarus beginning to breed in the spring 1 or 2 months earlier than C. montagui. Crisp et al. (1981) on the other hand, found that the species showed little difference in their breeding periods, both being summer-breeders in SW Britain, with a peak in the numbers containing developing eggs in July and August. The breeding seasons of both C. stellatus and C. montagui have been studied in SW Britain (Burrows, 1988; Burrows et al., 1992), SE Ireland (Healy, 1986) northern Spain (Miyares, 1986) the Ligurian Sea (Relini & Matricardi, 1979; Relini, 1983) and in other parts of the Mediterranean Sea (Crisp et al., 1981). In addition, the breeding season of C. montagui was studied in Scotland (Lewis, 1986; Barnes, 1992) and in mid-Wales (Kendall & Bedford, 1987) and that of C. stellatus on the Mediterranean coast of Israel (Mizrahi & Achituv, 1990). Burrows (1988) and Burrows et al. (1992) determined the fecundity of the two species at MTL at Plymouth in the United Kingdom. These authors also investigated egg size and on one occasion the development of the ovary in animals with and without egg masses. They estimated the number of broods produced per year indirectly by combining information on the rate of development of the eggs, to give the time each brood was retained in the mantle cavity and the proportion of time individuals spent brooding per year. The number of broods produced annually and variation in egg numbers between species and within a species at different shore levels have been discussed by

R.M. O’Riordan

et al. I J. of Exp. Mar.

Biol. and Ecol. 190 (1995) 17-38

19

O’Riordan et al. (1991, 1992). For C. stellutus, Achituv & Barnes (1976) and Mizrahi & Achituv (1991) examined changes in general biochemical composition of the eggs during development, while Mizrahi & Achituv (1990) studied seasonal changes in body weight and biochemical components in Mediterranean adults. Despite the work on C. stellatus and C. montugui during the last few years (Healy, 1986; Lewis, 1986; Kendall and Bedford, 1987; Burrows, 1988; Barnes, 1992; Burrows et al., 1992) there is still considerable confusion over the breeding seasons of the two species, because studies were not carried out throughout the year. Cross, Southgate & Myers (unpubl. data) reported either or perhaps both species (from SW Ireland) releasing embryos in January, soon after being brought into the laboratory and held at 4°C. In the present study, C. stellutus and C. montugui were examined throughout the year, at sites representative of their preferred habitats and shore levels (see Crisp et al., 1981), to determine more precisely the breeding seasons and the factors governing them, and to establish what changes occur in the male (testes, vesiculae seminales and penis) and female (ovary) reproductive organs. Egg and ova size were also examined.

2. Materials and methods The study was carried out at Lough Hyne Marine Nature Reserve, west Cork, Ireland (.51”31’N, YlO’W). C. stellatus was collected from an exposed site, the lower shore at Carrigathorna Rock which is about 2-3 on the Ballantine’s Scale (Ballantine, 1961), while C. montugui was collected from the higher shore at the Rapids (see O’Riordan, 1992). This latter site does not readily conform to Ballantine’s Scale, being sheltered but experiencing a strong current. These sites and shore levels were selected as being representative of the preferred habitats of each species (see Crisp et al., 1981). Collections, of 46-60 individuals of each species, were made monthly, from December 1988 to March 1991 inclusive, except when adverse weather conditions prevented collecting from the exposed site (January, February and March 1989 and January, February, March and October 1990). Chips of rock bearing adult barnacles were brought back to the laboratory and examined within 24 h. Only barnacles which, from the appearance of the shells, were at least 2 yr old were used, although both species are able to produce embryos in their first year (O’Riordan et al., 1992). Isolated specimens were excluded, despite the fact that the genus Chthamalus is known to be capable of self-fertilization (Crisp, 1954; Barnes & Crisp, 1956; Barnes & Barnes, 1958; Pannacciulli, pers. comm.). Individual barnacles were removed from the rock and the rostro-carinal diameter (RCD) was measured, using the ocular micrometer of a dissecting microscope. The body (soma only, excluding ovary, retractor muscles and tissue lining the mantle cavity) was removed and placed in a drop of seawater on a slide with a sample of ovarian tissue and egg lamella, if present. The presence/absence of the penis was noted in all specimens. The testes, vesiculae seminales and ovary and egg lamella were scored for their stage of development,

20

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

using a modification of the scales described by Crisp (1954) and Burrows (1988) and Achituv & Barnes (1976) respectively (see Table 1). Twelve barnacles per sample were selected and the size (length and breadth at the widest section) of 10 ova (dissected out of the ovarian tubule and allowed to “round off” in seawater) and 10 eggs per barnacle were measured. The mean of 10 measurements (length and breadth) within each measured barnacle ovary/brood was calculated, in order to acquire a single value per ovary/brood. Air and seawater temperatures were recorded on each sampling occasion, at high tide at the Rapids, where there is a mixing of sea and Lough waters, in order to investigate whether there was a correlation between the time of breeding and temperature.

Table 1 Scale for scoring stage of development from Crisp (1954) and Burrows (1988)

of male and female gonads and egg masses, and Achituv & Barnes (1976), respectively

Testes development Absent Poorly developed, visible only on dissection or teasing out Moderately developed, occupying a small part of the body and just visible through the cuticle, transparent to slightly white/opaque in colour Well developed, occupying much of the body cavity and clearly visible from the outside, transparent to slightly white/opaque in colour Vesiculae seminales development Absent or present as thin strands of tissue Thin linear sacs with little sperm Moderately developed. sacs cylindrical of diameter about equal to that of the gut, clearly visible through the cuticle, opaque white in colour Well developed, sacs large and bloated, exceeding the gut in diameter, seminal fluid readily expelled, opaque white in colour Ovarian development Absent, no ovary/ova visible Poorly developed, rudimentary ovary, grey to off-white, only a thin layer in the basal membrane, ova minute, few cells Ovary moderately developed, filling about a third of the mantle cavity, ova multicellular, having a smooth appearance, but not of full size nor completely filling the tubules, orange in colour Well developed ovary, filling the greater part of the mantle cavity, ova with a clearly defined shape, often rounded or slightly oval, orange in colour and filling the ovarian tubules Egg masses Early, from newly laid to a few cells Multicellular From the appearance of limb buds to the presence of limbs and spines From the presence of the naupliar eye to hatching Those which hatched upon removal from the mantle cavity

modified Score 0 1 2 3

0 1 2 3

0 1

2

3

1 2 3 4 4h

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

21

3. Results 3.1. The male reproductive

organs

3.1.1. C. stellatus

The testes and vesiculae seminales both showed annual cycles of development (Fig. 1). The greatest proportion with well developed testes (Stage 3) was recorded during mid-summer, with peaks in July in 1989 (86%) and in June in 1990 (78%). Well developed vesiculae seminales (Stage 3) were present from May to August in 1989 and from April to November in 1990. Barnacles with moderately developed testes and vesiculae seminales (Stage 2) were found in all months examined. The testes were at a minimum stage of development in October in 1989 (60% of the samples were Stage 0) and in November in 1990 (26% ), after which they began to regenerate. The maximum number with absent or very poorly developed vesiculae seminales (Stage 0) was found in December in both 1989 and 1990. 3.1.2. C. montagui As in C. stellatus,

the testes and vesiculae seminales of C. montagui showed annual cycles of development (Fig. 2) and moderately developed testes and vesiculae seminales were found in all months examined. The highest proportion of individuals with well developed testes and vesiculae seminales was recorded in mid-summer. However, in June 1990 only 28% had well developed testes compared with 78% in C. stellatus. In C. montagui, the highest proportion of individuals with no visible evidence of testes was in November in both 1989 and 1990. In January-March 1991 (the sole year for which we have data for C. stellatus in these months), the vesiculae seminales and testes were less welldeveloped in C. montagui than in the C. stellatus population. In May 1990, both species showed a decrease in the percentage with well developed testes and vesiculae seminales in comparison with the preceding months. In both species a measurable penis was found to be present, throughout the year, in all specimens. 3.2. The female

reproductive

system

3.2.1. The ovary

The ovary of both C. stellatus and C. montagui showed seasonal changes (Fig. 3a,b, respectively). These data are for brooding and non-brooding barnacles combined. In both species, ovaries were more well developed (Stage 3) during the “summer months” than at other times, but throughout the year less well developed ovaries could be found. In C. stellatus, well developed ovaries were recorded from April-August 1989 (maximum 12% in June and August), and again in April-September 1990 (maximum 22% in April), as well as in November and December 1989 (4 and 2% respectively) and March 1991 (4%). In C.

22

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995)

17-38

* * 7

7

F‘MAMJJASONDJ

DJ

FMAMJJASC

1989

1988

bNDJFM

1990

1991

MONTH/ YEAR

a) Testes

* T

D .J F MAMJJAikNb; 1988

b) Vex KEY: Fig. 1. The developmental

percentage stages.

1989 ill;

se seminales

NDJFM

FMAMJJAS0

1990

MONl-H/Y EAR

I n STAGEO q STAGEI of C. stellarus with

(a) testes

STAGEZ

and

(b)

q

1991

STAGE3 1 * = NO data

vesiculae

seminales

in different

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

23

90 80 70 60 50 40 30 20 10 0 DJFMAMJJASONDJFMAMJJASONDJFM 1991

1990

1989

1988

MONTH/YEAR a) Testes

90 80

60 50 40 30 20 10 0 ONDJFM

DJFMAMJJASONDJ.FMAMJJAs 1989

1988

b) Vesiculae KEY: Fig.

2. The

developmental

percentage

stages.

1991

1990

MONTH/YEAR

seminales W

STAGE0

of C. montagui

q

STAGE 1

with

q

(a) testes

STAGE2

q

and

vesiculae

(b)

STAGE3

seminales

in different

R.M. O’Riordan

24

et al. I J.

of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

100

90

80

70

60

% 50

40

30

20

10

* * * 0

-TT

D J

*

*

-r

l-

-I

F hl

1988

A M

J

J

A

S 0

K

D

J

F hl

A M

J

J

A

S

0

fi

D

J

F M

1990

1989

hlONl-H~YI3.K

a) Chttmmulu.~ stellatrrs

90

80

70

60

% 50

40

30

20

10

0

DJFMAMJJASONDJFMAMJJASONDJFM 1989

1988

MONTH/YEAR.

1990

1991

b) Chttuzmalus montagui KEY:

Fig. 3. The [lercentage stag es.

1

n

STAGEO

H

SAGES

ilB

STAGEZ

a

STAGES

1 * = Nodata

of (a) C. stellatus and (b) C. montagui with the ovary in different

develc

mtal

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

25

montagui well developed ovaries were present from February to September in 1989 and in January, March to July 1990, with a maximum of 40% in July in 1989 but only 14% in April of 1990. In 1989 the maximum proportion of the population lacking any evidence of an ovary (Stage 0) was in October (62% in C. stellutus, 28% in C. montugui). No data are available for C. stellatus in October 1990, but 18% of C. montugui lacked any evidence of an ovary. 3.3. The percentage

of the population

brooding

egg masses

The percentage of C. stellatus and C. montagui bearing eggs containing embryos of different developmental stages is illustrated in Fig. 4. In both 1989 and 1990, C. stellarus brooded throughout the summer with the number of gravid barnacles reaching a maximum in July (90% ) in 1989 and June (94% ) in 1990. All four stages of egg development were found from MaySeptember 1989 and April-August 1990. In 1990, brooding seems to have commenced earlier (in April 1990, 56% of the samples had egg masses, in comparison with 0% in April 1989) and probably lasted for at least as long as in 1989, because whilst no data are available for October 1990, in September 1990 90% of the population still had egg masses (38% in 1989). Two percent of the samples contained what appeared to be viable eggs (Stage 2) in December 1988. C. montagui also brooded during the summer, with the number of gravid barnacles reaching a maximum (72%) in mid-summer (July in 1989 and August in 1990) and all four stages of egg development being found from May to August 1989 and June-September 1990 inclusive. Furthermore, a low level of brooding was observed in C. montagui during the “off” season. In 1989, egg masses were first found in April (5%, Stage 1 and 2), but in 1990, 2% were gravid in February (Stage 4/4h), 4% in March (Stage 2 and 4/4h), as well as 2% in April (Stage 3), but none in May, in comparison to 50% in May 1989. By October (of both years) only 2% of the population contained eggs and by November, no egg masses were present. In 1991, no eggs were found in either species in the 3 months sampledJanuary, February or March. In July 1990, there were decreases in the number of both C. stellatus and C. montagui brooding eggs. Two months previously, there were decreases in the proportion with well developed testes and vesiculae seminales in both species. Temperatures reached a maximum in July-August and a minimum from December to February (see Fig. 5). Brooding was at a maximum in both C. stellatus and C. montagui in July 1989, when the mean seawater and air temperatures reached maxima. In 1990, there was a decrease in the percentage of both species brooding eggs in July (compared with June and August), which may be related to a drop in both air and seawater temperatures in the previous month. The egg masses of both species are similar in coloration. They can remain bright orange in all stages of development, or alternatively, they may darken slightly with development, becoming fawn or brown. Stage 1 egg masses are always coloured orange. The egg masses of the first three stages of development have a firm texture and are not easily broken apart. Stage 4/4h eggs are distinguished by

26

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995)

17-38

100

90 80 70 60 % 50 40 30 20 10 Ii

0

*

*

I

*

-

-

DJFMAMJJASONDJFMAMJJASONDJFM 1988

1991

1990

1989 MOWH/YEAR

a) Chthurnalus stellatus

100

90 80 70 60 %

50 40 30 20 10 0 DJFMAMJJASONDJFMAMJJASONDJFM 1989

MONTH/YEAR

1990

b) Chthamalus montagui KEY:

* = No data Fig. 4. The percentage of (a) C. stellatus and (b) C. montagui developmental stages from December 1988 to March 1991.

bearing

embryos

of different

R.M. 0 ‘Riordan et al. / J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

27

20

15

TEiMr.

(‘C) 10

5

0

-

AIR

-

SEA-WATER

i DJFMAJJASNDJFMAMJJASONDJFM 1988

1990

1989

1991

hdONTH/YEAR Fig. 5. Air and surface seawater recorded at the Rapids.

temperatures

at Lough

Hyne.

Data

points

are mean

monthly

values

the presence of distinct darkly coloured eyespots and the egg masses are fragile. At the hatching stage, eggs are readily separated from one another. The minimum rostro-carinal diameter (RCD) of adults with egg masses was 2.8 mm in 1 + C. sfelfatus (range of RCD in collections: 2.2-11.0 mm) and 4.5 mm in 1 + C. montagui (range of RCD: 3.5-12.6 mm). There was normally a pair of egg masses lying in the mantle cavity. In C. stellatus there were four cases (out of 437) in which just one egg mass was found, while a single case of three egg masses, instead of a pair, was also recorded. In C. montagui, in two cases (out of 234) a single egg mass, instead of a pair, was recorded. Embryos within an egg mass were all found to be at the same stage of development.

3.4. Ovarian

regeneration

Table 2A,B illustrates ovarian regeneration in mature individuals of C. stellatus and C. montagui by classifying gravid individuals as a function of the stage of development of the previous brood (Crisp & Patel, 1961). In both species, when embryos were Stage 1 to 3 the greatest proportion of the population had Stage 1 ovaries, but when the embryos were eyed (Stage 4) or hatching (Stage 4h) the when embryos were greatest proportion had Stage 2 ovaries. Furthermore, hatching, over 11% of the C. stellatus population and greater than 18% of the C. montagui population had well developed ovaries (Stage 3) thus the ovary was seen to regenerate as the embryos developed, reaching a maximum when the

28

R.M. O’Riordan

Table 2 Ovarian regeneration

in mature

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995)

of (A) C. stellatus and (B) C. montagui

individuals

Stage of development of embryos within egg mass

17-38

Percentage of individuals with egg masses column 1 in which the ovary is at Stage:

as in

0

1

2

3

(A) C. stellatus 1 2 3 4 4h

5.71 13.71 0.95 6.98 2.27

65.72 58.87 53.33 17.83 18.18

25.71 26.61 45.71 68.99 68.28

2.86 0.81 0.00 6.20 11.36

(B) C. montagui 1 2 3 4 4h

9.37 2.33 2.56 1.39 6.25

87.50 65.11 56.41 18.06 16.67

3.13 30.23 41.03 70.83 58.33

0.00 2.33 0.00 9.72 18.75

embryos were at the hatching ready to be fertilized.

stage,

and thus some of the population

were again

3.5. The size of ova and eggs The mean length and breadth were calculated for each stage of development in each species and are given in Table 3A,B for ova size and Table 4A,B for egg size. Kruskal-Wallis single factor analyses of variance (Zar, 1984) showed that, within each species, there were significant differences between the length and breadth, for both ova and eggs, at each developmental stage, for C. stellatus and C. montagui. Subsequent non-parametric multiple comparison tests showed that in both species, both the length and breadth of the ova increased significantly with each stage of development (i.e. Stage 3 > 2 > 1). The mean length and breadth of the eggs did not increase significantly during the first three stages of development, Table 3 Ova size of (A) C. stellatus and (B) C. montagui Stage

No. of barnacles

Mean length -t

Mean breadth 2

ss (ran&( pm)

ss (raage)( pm)

Ratio of mean length:mean breadth

(A) C. stellutw 1 38 2 120 3 45

50.0 + 1.74 (29.4-67.5) 85.6 ? 1.09 (60.8-11.6) 112.1 ? 1.81 (91.7 + 148.3)

45.5 t 1.59 (26.8-63.4) 76.0 + 0.92 (54.1-105.5) 98.2 2 1.93 (76.7-140.6)

l.lO:l 1.13:1 1.14:1

(B) C. montugui 1 45 2 142 3 41

46.1 + 1.70 (30.4-76.7) 82.3 2 1.08 (50.8-117.1) 103.2 5 1.58 (85.9-139.2)

42.4 t 1.52 (26.8-66.4) 74.1 + 0.91 (47.2-99.5) 90.8 + 1.69 (74.2-133.7)

1.09:1 l.ll:l 1.14:1

R.M. O’Riordan

et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-38

29

Table 4 Egg size of (A) C. stellatus and (ES) C. montagui Stage

No. of barnacles

Mean length ?

Mean breadth _f

sE (rangc)(pm)

SE (range)( pm)

Ratio of mean 1ength:mean breadth

(A) C. stellatus 1 19 2 54 3 45 4 58 4h 14

173.3 2 3.31(138.2-198.3) 177.8 f 1.82 (146.3-208.1) 180.1 t 1.80 (159.7-215.3) 201.2 2 1.74 (174.6-241.5) 202.4 t 2.40 (188.5-219.4)

87.3 2 87.9 2 88.6 ? 99.3 2 100.4 f

0.93 (79.9-93.7) 0.65 (78.3-97.9) 1.07 (79.3-112.3) 1.10 (80.3-123.6) 1.69 (94.0-116.4)

1.991 2.02:1 2.03:1 2.03:1 2.02:l

(B) C. montagui 1 20 2 20 3 25 4 40 4h 23

157.7 +- 3.54 (106.0-181.3) 165.9 2 2.46 (147.8-187.4) 168.2 k 2.05 (154.5-194.7) 186.0 -t 1.85 (164.8-220.4) 184.4 f 2.24 (161.2-210.6)

82.1 k 83.2 + 82.6 2 92.3 k 93.7 t

0.94 (74.9-90.5) 1.01 (77.8 t 97.3) 0.76 (76.2-89.1) 0.97 (79.8-111.2) 1.65 (81.9-110.2)

1.92:1 1.991 2.04:1 2.021 1.97:l

but Stage 4 eggs were significantly longer and wider than those of Stage 3. Hatching eggs (Stage 4h) were not significantly different in size from Stage 4 eggs. The Wilcoxon-Mann-Whitney test (Zar, 1984) showed that there was no significant difference between the species in the length of Stage 1 ova, but Stage 2 and 3 ova of C. stellutus were significantly longer than those of the corresponding stages of C. montagui. Only Stage 3 C. stellatus ova were significantly wider than those of C. montagui. The eggs of C. stellatus were significantly longer and wider, at each of the five stages of development, than those of C. montugui. When the ratios of mean ova 1ength:mean ova breadth are examined, it is seen that the ova of both species become narrower (in comparison to length) as they develop. A similar situation is seen for the first three developmental stages of the eggs, but not for Stage 4/4h.

4. Discussion At Lough Hyne, the male and female reproductive organs of C. stellatus and C. did not totally degenerate at any time of year, so that a small percentage of each population was capable of producing broods at times other than the summer months. This agrees with the findings of Barnes (1989) that in some Chthamalus spp. the male gonads may remain active throughout the year and ovaries may carry mature ova or ova available for final maturation as soon as conditions are favourable. In warm-temperate species the whole generation time, from the renewed ovarian development to the hatching of the nauplii, may take only a few weeks under optimal conditions (Barnes & Barnes, 1965; Anderson, 1994). Barnes (1972) commented that at the centre of the distribution of C. stellatus agg. reproductive tissue is presumably constantly produced. At Lough Hyne, only mature Chthamalus were examined and a measurable montagui

30

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penis was always found, throughout the year. Barnes (1992) on the contrary, reported a high percentage of C. montugui (24%) and C. stellutus (20%) with penis stumps in October samples from Loch Sween, Scotland and Arcachon, France, respectively. C. stellatus and C. montagui are both able to produce several broods in a season (Burrows et al., 1992; O’Riordan et al., 1992). At Lough Hyne C. stellatus and C. montugui, from their preferred habitats and shore levels, were shown to have similar breeding seasons. In both species, breeding occurred mainly during JuneAugust, but as in France (Le Reste, 1965), Italy (Relini, 1983) and Yugoslavia (Klepal & Barnes, 1975) low levels also occurred at other times (see Table 5). The only other published record of C. stellatus agg. bearing embryos in the winter months in the British Isles is in the Plymouth Marine Fauna (1931). Burrows (1988) and Healy (1986) found that the breeding seasons of C. stellatus and C. montagui were alike. They did not observe any breeding in the “off” season, but Burrows (1988) only sampled from April to October. The suggestion by Southward (1976) that C. stellatus may begin to breed in the spring 1 or 2 months earlier than C. montugui, was not confirmed at Lough Hyne. Similarly, Crisp et al. (1981) found that the two species showed little difference in their breeding periods. Crisp (1950) suggested that in C. stellatus agg. breeding commenced later with increasing latitude and with easterly longitude in the United Kingdom and that it started earlier on the lower shore, but Barnes (1989) pointed out that the effect of latitude on the onset of breeding is difficult to separate from the effect of temperature. According to Hines (1978), the length of the breeding season is usually broadly defined by temperature, and during the season the production of broods is only limited by food availability and by the temperature-dependent development rate of the brood in the mantle cavity. Burrows (1988) found that the onset of breeding at Plymouth coincided with a rise in sea temperature above 10°C. Temperature may be correlated with the onset of breeding in C. montugui at Lough Hyne in February in 1990, following mean seawater temperatures of 10°C in December 1989. At Lough Hyne, temperatures were recorded at the Rapids, which should reflect seawater temperatures both inside and outside the Lough. Both air and surface seawater temperatures were recorded because barnacles are exposed to the influence of both (Southward & Crisp, 1954). Klepal & Barnes (1975) attributed the presence of egg lamellae in C. stellatus agg. in February to abnormally high air temperatures in that month (mean air and sea surface temperatures 7.6 and 10.8”C, respectively). Barnes (1992) reported that at Arcachon (France), breeding begins in C. stellatus in April, when mean air and seawater temperatures are 11-12”C, and maximum air temperature around 14°C. She also suggested that reproductive activity declined at an upper thermal threshold of 20-21°C (water) and 24-25°C (air). Pate1 & Crisp (1960b) brought specimens of C. stellutus agg. [probably C. montagui according to Burrows (1988)] into the laboratory during the winter, to try to induce them to breed outside the normal breeding period of the natural population (see also Barnes, 1992). Despite having scarcely any gonad develop-

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31

ment at the outset, they found that well-nourished specimens developed gonads within a short time and commenced breeding after being kept for 2-3 weeks at 1516°C with the percentage of animals breeding increasing with temperature, reaching an optimum rate between 24-25°C. C. stellatus agg. continued producing broods up to 30-32”C, but a lower proportion of the population was found to be carrying eggs at this temperature. Since, at Lough Hyne, the ovary of C. sfellatus is in a fairly advanced stage throughout the year, if the testes and vesiculae seminales are also well developed, as was the case in November and December 1990, the only limiting factors of reproduction would be temperature and food. In both C. stellatus and C. montagui, a connection exists between latitude and the commencement of breeding and/or the length of the breeding season (see Table 5). As suggested by Kendall & Bedford (1987) in the centre of the species range, i.e. Continental Europe, both species start breeding earlier and have longer breeding seasons than in the British Isles (Relini & Matricardi, 1979; Relini, 1983; Miyares, 1986), except in the eastern Mediterranean where C. stellatus breeds mainly in July and August, with just a small percentage breeding in May and June (Mizrahi & Achituv, 1990). Barnes (1989) commented that breeding in intertidal species begins at the shore level having the longest exposure to the changing controlling factors, such as temperature, light and food. C. stellatus agg. breeds earlier at a lower than higher tidal level (Crisp, 1950) and is controlled by temperature, while Balanus balanoides breeds first at higher and later at lower levels (Crisp, 1959) and may be controlled by light (Barnes, 1963) and possibly air temperature (Barnes & Barnes, 1976). At Asamushi, Japan, Luckens (1968) found that C. challengeri commenced breeding earlier on the lower than on the higher shore. Dando & Southward (1980) suggested that C. montagui and C. challengeri may possibly have been derived from a common circum-boreal ancestor. In the present study, embryos within an egg lamella were all found to be at the same stage of development. This supports the contention of Pate1 & Crisp (1960a), that in some species such as C. stellarus agg., which may have very small and thin egg lamellae, the eggs may develop uniformly (see also Groom, 1894). However, Relini (1983) working near Genoa, Italy, noted that in the same individual (of both C. stellatus and C. montagui), it was possible to find contemporarily different developmental stages of embryos. Sandison (1954) in her work on the reproduction of some South African barnacles, also occasionally found an individual in which the embryos were not all at the same stage of development. The barnacles examined by Relini (1983) and Sandison (1954) may have been larger than those used by Pate1 & Crisp (1960a) or in the present work and consequently may have had larger and thicker egg lamellae. Pate1 & Crisp (1960a) noted that in many species the outer eggs in the lamella develop faster than those inside. Three distinct egg lamellae, instead of the normal pair, were found in only one individual of C. sfellatus. The embryos were all at the same stage of development and were presumably the same brood. Klepal (1975) reported on the occurrence of “twinning” in C. depressus. Depending on which organs were “twinned” it

North Devon Brixham-Penzancc Plymouth. SW England

Lough Hyne. SW lrcland

Kintyre, Scotland Anglesey, Wales North Wales and Fyldc Aberystwyth, mid-Wales Carnsore Point, SE Ireland

C. montugui

stellatus

stellutus

C. stellatus

C. C. C. C.

agg.

agg.

&

agg. agg. stellatus agg. .stellatu.s agg.

C. stellatus

C. montagui

C. stellatus

C. montagui

C. montagui

C. stellatus

C. montagui

C. montapi

C. stellatus

C. montapi

Scotland

Millport.

to south

Later than further south: probably only 1 brood/year, succeeds only in especially warm summers June-end of August: peak in July (max. = 80%) Begins in early May July to October Probably all year Begins in late April Mid/late May to late August (max. = 90%) Mid-June to mid-September (max. - 55%) Early May to mid-September (max. - 70%) April to October (max. = 72% ); some in Feb./ March 1990 April to October (max. = 94%): some in December 1988 Begins in mid-April Begins first week of April (LTL) or late May (MHWS) January-March, August-September July to mid-September Late April to late September/early October (max. - 95%) Both breed in summer; peak in July and August

from north

C. montapi

arranged

N. Scotland

mcrntag~ri with latitude.

of breeding

of C. .stellrrt~s and C. Period

season

Snecies

in the time of the breeding

Location

Table 5 Variation

work Crisp, 1950 Crisp, 1950 Plymouth Marine Bassindale, 1936 Burrows, 1988 Crisp et al., 1981

The present

Fauna.

Lewis, 1986 Barnes, 1972 Crisp, 1950 Lewis & Powell, 1960 Pate1 & Crisp, 1960a Crisp, 1950 Kendall & Bedford, 1987 Hcaly, 1986

Reference

1931

Spain

France

Adriatic Sea Naples, Italy Mediterranean Salobrena, W. Mediterranean Mediterranean Coast of Israel

Gulf of Marseilles,

northern

Sea, Italy

Ligurian

Santander,

C. stellatus agg.

France

Arcachon,

C. C. C. C.

stellatus agg. stellatus agg. stellatus agg. stellatus & C. mantagui C. stellatus

C. stellatus C. stellatus & C. montagui C. montagui C. stellatus C. stellatus agg.

C. stellatus agg. C. stellatus agg.

French Atlantic Coast Near Rovinj, Yugoslavia

Mizrahi

with

Mainly July to August, a small percentage embryos in May and June

1959

Le Reste,

& Achituv,

1965

1990

Klepal & Barnes, 1975 Barnes et al., 1972 Dessenoix, 1962 Barnes, 1992 Relini, 1983 Relini & Matricardi, 1979 Miyares, 1986

Kolosvary, 1947 Groom, 1894 Tenerelli, 1958, 1959 Crisp et al., 1981

Crisp & Fischer-Piette,

Broods until mid-September Mainly April to September (max. - 45%); some in October and February Does not breed during autumn and winter April to May Eggs from April to August All year except October and November Ready to release nauplii in March March/April to early October (max. - 50%) March to early October (max. - 60%) Larvae in plankton from mid-May to mid-October Some breeding in winter, but of little importance July to December Probably all year round March to October February to April

34

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I J. of Exp. Mar. Biol. and Ecol. 190 (1995) 17-S

could be possible to have more than two egg lamellae. Crisp & Davies (1955) noted that although only one pair of egg lamellae was usually found in the mantle cavity of C. stellutus agg., two pairs occurred in a few specimens out of several thousand C. stellatus agg. they examined. In such cases the egg lamellae were in different stages of development, the earlier ones being fully developed and the later ones were only just deposited. They suggested that since Chthamalus (C. montagui?) lives high in the intertidal zone it may only infrequently be submerged, and it is possible that one brood might be retained beyond the normal physiological time limit. At Lough Hyne the ovaries of both C. stellatus and C. montagui re-developed as each brood matured. This agrees with the findings of Crisp (1950), Barnes & Barnes (1977) and Burrows (1988). Barnes (1953) suggested that the rate of development of eggs or embryos within the parent may be as important a factor as the rate of development during the planktonic stages in determining the size of any given larval stage, while Pate1 & Crisp (1960b) suggested that the final size of the ripe embryo will depend upon the size of the ova from which it was developed and changes in size during the development of the embryo. In the present work, the third stage (i.e. ripe) ova of C. stellatus were significantly longer and wider than those of C. montugui, which carries through to the size of the eggs of the species. The egg measurements given by Bassindale (1936), Crisp (1954) and Southward (1964) could refer to either species. The eggs measured by Powell (1954) were probably C. stellutus and were longer (230 x 130 pm, for Stage 4/4h) than those in the present study, but they may have developed more slowly, due to lower temperatures in Fair Isle than in SW Ireland. Pate1 & Crisp (1960b) found that in C. stellatus agg. there was an inverse relationship between temperature and size, whereby the volumes of both early and late stage eggs increased inversely with the temperature at which they had developed as ova, and that although the breadth remained relatively constant, the length varied significantly. Their figures for the later stages at the lowest temperature (15’C) agree with measurements for the Stage 4h eggs of C. montugui in the present study. At Lough Hyne the eggs of C. stellatus were significantly larger at each developmental stage than those of C. montugui. Crisp (1987) suggested that since egg size is highly characteristic of a species it can be used as a taxonomic character, quoting C. stellatus and C. montagui as an example. Burrows (1988) pointed out that an approximately 50% greater biomass of the nauplii (resulting from the larger eggs) of C. stellatus than C. montngui. would result in a 20% increase in survival time and in addition, the larger larvae of C. stellarus would have a longer “pre-competent” (sensu Crisp, 1974) period in which to assimilate non-feeding cyprid stage (Lucas et al., 1979). energy for the “competent” Burrows (1988) further proposes that if C. stellatus had more stored energy in the form of oil cells this may allow it to extend further the competent phase beyond the 20% predicted and increase the chance of finding a suitable substratum. The presence of more oil cells has not, however, been confirmed and Moyse (1963) has pointed out that a long larval life might be unfavourable for shore barnacles,

R.M. 0 ‘Riordan et al. I J. of Exp. Mar. Biol. and Ecol. 190 (1995)

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35

increasing the danger of their dispersal seawards. Crisp (1987) suggested that, with the need for a longer pelagic life in an archipelago situation, a larger egg and larva might be needed and he proposed that perhaps this has happened in the case of C. stellatus and Euraphia depressa in contrast to the mainland coastal species C. montagui.

Acknowledgements

Thanks to S. Berrow, N. F. Ramsay, H. Wilkins for assistance and the Wildlife Service for granting permission to work at Lough Hyne Marine Nature Reserve. We are grateful to the two anonymous referees for their constructive comments on the manuscript.

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