Some observations in tetraclita squamosa rufotincta Pilsbry

J. exp. mar. Biol. Ecol.. 1978. Vol. 31. pp. 315-324 Q Elsevier/North-Holland Biomedical Press

SOME OBSERVATIONS IN TETRACLITA

SQUAMOSA

RUFOTINCTA

Pilsbry

Y. ACHITUV The Department

of Life Sciences, Ban-llan University,

Ramat-Gan.

Israel

and

H. BARNES The DamtaffnageMarineResearch Laboratory,

Oban. ArgyN. Scotland

Abatraet: Aspects of the biology of Tetraclita squamosa rufotincta Pilsbry were investigated. Although a tropical species, on the shores at Elat, Israel, its breeding is virtually restricted to the colder winter months. The causal factors are considered and the results of some experimental work relative to temperature control given. For a cirripede, T.s. rufotincta has a remarkably large ‘egg’ - unusual in a tropical or even warm-water species. The egg size is compared with that of other species and the survival value of large size considered; excess nutrients are carried over from the embryo to at least the first planktonic larva, and may aid survival in a relatively nutrient poor environment. The animals do not become sexually mature until the second year after their settlement. Growth takes place largkly in the colder winter months and is seasonally separated from the period when gonadal tissue is developed.

The pattern of reproductive behaviour in cirripedes varies with the species. In boreo-arctic species such as the littoral Bulunus balunoides and the largely sublittoral B. bulunus a single brood is developed synchronously in any given population each year, and for the final maturation of the gonads the temperature must fall below = 10°C (Barnes, 1.963; Barnes & Barnes, 1967 ; Crisp & Patel, 1969). In warm-temperate species such as B. perforutus and Chthumulusstellatus a minimum critical temperature must be exceeded before the gonads will develop (Pate1 & Crisp, 1960). There are varying degrees of eurythermy ; Eiminius modestus begins to breed at relatively low temperatures and does so with increasing intensity as the temperature is raised (Crisp & Davies, 1955). Little is known of breeding in tropical barnacles. Tetruclitu squumosu rufotinctu Pilsbry is a common littoral animal on rocky substrata on the shores at Elat (Israel) where it forms a well-defined belt in the centre of the narrow (90 and 20 cm, maximum and minimum predicted range, but markedly under the influence of meteorological conditions) littoral zone (Achituv, 1972; see also Safriel & Lipkin, 1964); it thrives best under wave action like other Tetrucfitu 315

316

k’.

;\CHITUV.AND H. BARNES

sp. (Barnes. 1959). Some aspects of the biology, particularly rufbtincta have now been investigated.

the breeding, of T.s.

MATERIALAND METHODS The animals were collected from intertidal rocks at Elat. During parts of 1970-72 the percentage of animals containing egg lamellac - irrespective of the stage of their development - was determined at frequent intervals. Subsequently. the egg lamellae from a series of individual animals were removed and, after treating with protease to remove the outer membranes (Barnes & Barnes, 1977) the separated eggs were counted in a Bogorov tray; the ‘bodies’ of the same animals were dissected from the valves and their individual oven dry weights determined. Growth rates were determined by the measurement (vernier calipers) of a population of spat settled on newly exposed boulders. or panels. Individual animals were not followed; a random sample was measured on each occasion.

RESULT-SAND DISCUSSION BREEDINGSEASON It is evident from Fig. 1 that, although a few animals may be found with egg lamellae at any time of the year, breeding of T.s. rufotincta at Elat is markedly seasonal. Breeding begins in October, reaches its maximum in November-December, and then rapidly declines; at other times of the year less than 0.5”, of the population has egg lamellae. Although there is an isolated record for Teneriffe, Canary Islands (NilssonCantell, 1921) the centre of distribution of this species is the Arabian Sea. It has been well recorded from the Gulf of Suez, Aden, and the Red Sea (Pilsbry, 19 16 ; Kolosvary, 1941). Nilsson-Cantell (1928) recorded it from Muscat at the entrance to the Persian Gulf and its occurrence in “India” (Koiosvary, 1943) could well refer to the northeastern Arabian Sea. It extends southwards from the Arabian Sea as far as Madagascar (Nilsson-Cantell, 1921). There can be little doubt that T.s. rufotincta is a markedly tropical species. It is perhaps somewhat surprising to find a distinct seasonal breeding cycle in a tropical species - unless related to monsoons and the effect of lowered salinity neither of which is relevant to Elat. There is a seasonal trend in sea surface temperature (Reiss et al., t976); Table I gives monthly mean sea surface temperatures for their Station A at the head of the Gulf of Elat (single values or means for 1975-76 according to the data available). Breeding begins when the temperature begins to fall (October) and continues during November and December when temperatures remain low (Fig. 1). It is clearly not synchronous throughout the whole population since not more than x60% of the animals in a sample have egg

BIOLOGY OF TETRACLITA

317

lamellae at any one time; each animal probably produces more than one brood during this period. Yet breeding has virtually ceased by January even though sea surface temperatures then remain ‘low’, viz.. less than the value in October, until March. It does not seem to be sea temperature which, directly at least, determines the breeding season. Furthermore, it would hardly be expected that a sea surface temperature in July of 27.O’C would inhibit breeding in a tropical species. Pate1 & Crisp (1960) found that Bufunus umphitrire would readily breed between 22 and 32 C. Tetracfira s. rufotincta is, however, a littoral species; Achituv (1972) has given an

=: ;

40.

9

t

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30.

c .i * PO. ;i E

‘Z q

I

IO. 0

NOW0-c

1970

I

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JM 1971

MW

Mar

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act

I

Y

D*C

40. * : = B 3o 2 I c .‘. 20. 3 r a ‘E a:

10.

I

0 s:, 1972

Fig.

1. Tewacliru

10

20

s. ruforincra:

OL

10

20

Nl”

IIL_ 11 0

20

31

reproductive state of adult animals during 1970-72 ; % animals with egg lamellae at different times of the year.

318

1’. ACHITW

AND TULE

Mean sea surface Jan.

temperatures

H. BARNES

I

( C) at Elat (from Reiss c[ trf.. 1976).

Feb. 21.8

March 14.9

April

May 33.3

June ‘4.8

Aug. 25.4

Sept. 24.8

Oct. 24.2

NOV.

Dec. 22.8

21.5

23.3

July 27.0

account of its distribution in the Gulf of Elat where it is conspicuous in the narrow littoral zone, particularly where the rocks are exposed to some wave action: for a considerable part of the time Tetracliro is emmersed and, therefore. exposed to air temperature. These are much higher than the sea surface temperatures and the daily variations far greater. The temperature of the animals will depend upon whether they are exposed at night or day - but even so. air temperatures reach high values much earlier in the year than do sea temperatures. Achituv & Eorut (1975) have investigated the relation between air temperature. rock temperature, and that in the mantle cavity of Tetraclita. Selecting days when low tide was during the hottest part of the day they found that the mantle cavity temperature was higher than the ambient (up to +9’C) and was much closer to that of the rock. The mean in situ temperatures found in these investigations are given in Table II.

Mean temperature

June August

( C) of the free air. rock surfxe. Elat (from Achituv

and within the mantle & Borut. 1975).

cavity

of T.s. rufolirrrru

at

Air

Rock surface

Mantle cavity

38.1 37.0

41.0 39.7

41.7 42.3

It seems that the regime of air temperature may be responsible for the restricted breeding season. Whether high temperatures regulate the reproductive cycle through a general effect on metabolism or whether through some specific target organ or system - possibly hormonal - is not known. it is well known that breeding activity is closely related to nutrition (Pate1 & Crisp. 1960). There is little evidence for a marked difference in the availability of plankton throughout the year and none which would be expected to affect the metabolism. Much of the nutrient may, indeed. always be in the form of detritus arising from inshore material, rather than living plankton. In view of the apparent relation of breeding activity to temperature, an attempt was made to induce breeding by experimental control of the latter. Clumps of animals were detached from the rocks at Elat in June; none had egg lamellae and the ovary was little developed. They were transported to Oban (8th June); maintained at 15 ‘C in aerated sea water. and fed liberally (always, unless stated otherwise) with

BIOLOGY

OF TETRACLITA

319

newly hatched Artemiu (San Francisco) larvae. Throughout the experiments the water was changed twice weekly and at each change a small amount of chloramphenicol was added to inhibit bacterial growth. During the first week (to 15th June) a few animals died - but subsequent mortality was negligible; in those cases where, however, a dead animal was found especial care was taken to remove all remains. On 24th June a further two experimental groups were set up at 25 and 30°C; every time the water was changed the temperature was adjusted to the appropriate value before transferring the animals. In view of the limited amount of material more animals were maintained at 15’C and these were sampled more frequently and in greater numbers. On 7th July, i.e., about one month after initiation of the experiment the animals at 15°C had well-developed ovaries which, in some cases, after removal from the mantle cavity, released oocytes which rounded-off on standing. The vesiculae seminales were gorged with semen which was readily expressed under sea water to give very active spermatozoa. The oviducal sacs could easily be expressed from the base of the first cirri. It was anticipated that within days the animals would fertilize. Some three weeks later, however, (27th July) the animals were in a similar state - perhaps somewhat ‘riper’. Ovary was also reasonably well developed in the animals maintained at 25 and 30°C - but the oocytes were not readily released nor could ripe oviducal sacs be easily obtained. There was, nevertheless, much semen which gave active spermatozoa. Unfortunately the animals could not be examined again until 31st August; on that date the ovary appeared less-well developed in all cultures - oocytes were not released, oviducal sacs could not be expressed and yet active spermatozoa were readily obtained. The impression gained was that there had probably been regression of the gonads perhaps followed by renewed development. There were no egg lamellae nor any evidence that the animals had fertilized. On 15th September the gonads were better developed but had not reached the state seen on the 27th July; there was little difference on 10th October. Clearly the attempt to induce breeding had not been successful and with the few remaining animals two changes were made. Since it has been suggested that continued feeding may tend to delay fertilization no food was given. After 21 days (31st October) under this regime no animals were fertilized and, as far as could be judged from the small samples, there had been some regression. Temperature ‘shock’ is a characteristic inducing breeding in many animals; on 31st October some of the animals previously at 15°C were transferred to water at 10°C from 17.00 h-09.00 h each day for 5 days being returned to 15 “C for the rest of each day. This did not induce breeding over the next three weeks. Unless a brood was missed in August - and there is little evidence that this was the case since it seems unlikely that all the animals would have fertilized, developed, and released their nauplii in complete synchronization during that month - all the efforts to induce breeding failed, and it would seem that the simple hypothesis of temperature control put forward above is inadequate. There is no doubt that the animals were in good condition at all three temperatures throughout the whole

320

Y ACHITUV

AND

H. BARNES

6 months of the experiment. It is well known in other species that development of the reproductive organs can take place outside the temperature limits required for the final stages of gamete maturation - and some other controlling factors must be sought. Even before the experiments had ended the shore population examined at Elat on 5th October had 50% with egg lamellae. The ‘quality’ of the experimental diet may have been inadequate. On the other hand. some endogenous rhythms triggered by variable conditions in the environment may have been suppressed by holding the animals at a constant temperature and continuously immersed. There is. however. no evidence from the few other littoral species which have been examined that constant immersion. even though it may delay fertilization. ever inhibits it. provided other controlling factors are held at the appropriate levels. It is. perhaps. worth noting that all the above attempts to induce breeding were related to the suggestion that high temperatures inhibit it and the assumption that. consequently, lowering temperature would remove the inhibition. In spite of the fact that the assumption was invalid it may still be true that high temperatures do inhibit breeding. It would be interesting to have data from other areas. THE SIZE AT MATURITY

In November, 1977, the population was sampled in order to determine at what size (basal diameter) maturity was reached. This was at the height of the breeding season (see Fig. 1). Each animal was measured and then broken open to determine whether egg lamellae were present. The results are given in Table III from which it is seen that z IS16 mm basal diameter is the size at which the animals mature. It is interesting to note that in the animals maintained in the laboratory and abundantly fed those with a basal diameter of 12-14 mm had pome ovary and a fully developed penis; this suggests that nutrient conditions on the shore at Elat may have been suboptimal. These results taken together with those on the growth rate (see Fig. 3) indicate that at Elat the animals do not mature until their second year from settleT.OLE III

Terraclita s. ruforincra: percentage, .of animals with egg lamellae at any stage of development;

littoral

population present on boulders: Elat. 28th Novimber. 1977. Size group. basal diameter (mm)

‘,.‘owith egg lamella

8-11 12-15. 16-19 20-23 24-27 28-3 I, 32-15

0 0 14.9 32.4 38.9 33.3 51.5 60.0

_

--.

3540’

BIOLOGY

OF TETRACLITA

321

ment, and that during this second year ovarian tissue is not laid down until after the main growing season since in a sample of the adult population collected in June little ovarian tissue was present. SIZE AND

NUMBER

OF EGGS

The eggs of the Hat population of T.s. rufirincta are very large. By the time they are eyed they are 477 pm long and 363 pm wide.; assuming the egg to be an ellipsoid of revolution about its major axis gives a volume of 32.7 x 1O-6 ml for an egg. This is far greater than the volume of an ‘egg’ (largely estimated from the dimensions of stage I nauplii) of any other species so far investigated (Barnes & Barnes, 1965. 1968). Other Tetracfita species have much smaller eggs, viz., T. squamosa, 6.07 x 10S6 ml, T.s. rubescens, 3.28 x 1O-6 ml, T. serrata, 3.63 x 1O-6 ml. Wide differences in egg size even within a genus seem to be common in other genera for which data are available; the maximum in Balanus is between B. hameri and B. algicofa (ratio 13.7: 1) which is greater than the volume ratio for the largest and smallest Tetracfita, namely 10 : 1 ( T.s. rufotincta and T.s. rubescens). The size of the eggs at various subsequent stages are given in Table IV; from this it is evident that there is little change during embryonic development, except for an increase in width (+ 14%) in the eyed stage. This is unusual; between the early and late stages in warm-temperature species there is usually an increase of 1619% in length at high temperatums (Crisp & Patel, 1960). In general, egg size within a genus tends to decrease from north to south and it is surprising to find that the eggs of T.s. rufotincta are so large, exceeding those for the boreo-arctic Balanus balanoides and B. balanus, 8.74 x 1O-6 ml and 8.45 x 10db ml, respectively. The planktotrophic larvae of many northern species are larger than their southern counterparts and in the case of cirripedes this has been usually associated with the necessity for the larvae to feed on large phytoplanktonic organisms characteristic of colder waters..The plankton .of the Gulf of Hat is poor and the nauplii may feed mainly on large, non-living particles. TABLE

IV

Size of eggs at four stages of embryonic development i values in pm f s.D.; Stage I. 2. 3. 4.

Few cells Many cells Limbed Eyed

n

Length

66 58 60 60

464k40 470 f 21 482 f 20 477 f 21

n, number of samples. Maximum width 316 f 316* 313 f 362 f

12 11 15 16

The relation between egg number and body weight is shown in Fig. 2. In order to compare the ‘efficiency’ of egg production between a variety of species the increase in the number of eggs/50 c(g oven dry body wt (N) has been used (Barnes & Barnes.

322

Y. ACHlTUV

AND

H. BARNES

(1968); the value for T.s. rufbrincru, 1.61 is very low. It is. however, a very large egg and in terms of metabolic efficiency of production, NV where Y is the volume of the egg is better used for comparison. Taking N as 1.62 and P’ as 32.7 ~1 gives NV = 53. This is very much lower than for many other species, particularly those from northern waters, but does come within the range given by Barnes & Barnes (foe. cir.). Since, however, not only is NV small but breeding takes place only over a restricted period. what has been termed the annual metabolic efficiency of egg 9000.

8000

,000

6000

;

5000

:

,000.

‘c

e 3000. 2000 1000

50

Fig. 3. Tt-rraclira s. rr&fbti;~cra: relation

150

1CO Body

w.**llt

,or.n

200

250

dry, Ills

between the total number

of eggs produced

(_r‘) and body size

(x, dry wt. mg): j = 151.8 + 32.4 x.

production, i.e., NV x number of broods, is low; withrn the breeding season preliminary estimates suggest any animal may give two or three successive broods. In terms of its population ecology it must, however, be pointed out that T.s. rufotincra grows rapidly and is apparently long-lived so that the population at Elat has a high proportion of very large animals, many between 100-150 mg oven dry body wt; each of these will give x 3,400-5,000 eggs. Even so, in terms of competition where the rate of production of Ehe number of potential offspring is often more important than their size, T.s. rufutincra is not highly favoured. GROWTH

RATE

The growth rate as indicated by measurements of the basal diameter has been foilowed for one and a half years on a clearly defined population settled on boulders and panels in the winter of 1970 (Fig. 3). Growth is clearly seasonal. It is rapid immediately after settlement in winter but by *March is beginning to decrease; during the summer there is little growth even in the first year. The pattern is repeated in the second year and by the end of the second growing season the animals have reached

323

BIOLOGY OF TETRACLITA

a basal diameter of ~20 mm; this is far from maximum size, x50 mm. Growth may be partially reduced by the extremely high summer temperatures but probably more by the metabolic demands of the developing reproductive organs (see above). It is known that young spat and juvenile animals are more sensitive to dessication than adults: Tetruclita appears to be no exception since in the upper part

MW 1070

Jul

Au2

OCt

lo71

1972

Fig. 2. Terrackr s. ruforincra: growth of a newly settled population followed over one and a half years: basal diameter, mm; numbers are number of animals measured: vertical bars, SE.

of the Tetraclira zone at Elat small dead animals are easily found. The winter breeding and settlement followed by rapid growth - still in the colder part of the year - will allow the animals to reach a size by the summer at which they can withstand the strong dessication stress consequent upon high temperatures.

ACKNOWLEDGEMENTS

One of us (Y. A.) wishes to acknowledge partial financial support from The Fund for Encouragement of Research (Hahistadrut) General Federation of Labour in Israel. H. B. wishes to thank The Hebrew University of Jerusalem for their invitation to serve as a Visiting Professor which gave the opportunity to take part in this work.

REFERENCES ACHITUV. Y.. 1972. The zonation of Terrachrhamalus

oblirrerarus Newman, and Terraclira ruforincra Pilsbry in the Gulf of Elat, Red Sea. J. exp. mar. Bid. Ecol., Vol. 8, pp. 73-81. ACHITUV. Y. & A. BORUT, 1975. Temperature and water relations in Terraclira squamosa ruforincra Pilsbry (Cirripedia) from the Gulf of Elat (Red Sea). In. Proc. Ninrh European Marine Biology S,vnposium. edited by H. Barnes, Aberdeen University Press, Aberdeen. pp. 95-108.

324

Y. ACHITUV AND H. BARNES

BARNES,H., lY59. Stomach contents and micro-ferding of some common cirripedes. C‘rr~r.J. Zoo/.. Vol. 37. pp. 231-236. BARNES.H.. 1%3. Light, temperature and the breeding of f?ukmus bahnoides. J. mar. biol. Ass. U.K.. Vol. 43. pp. 7 17-727. BARNES,H. & M. BARNES,1965. Egg size, nauplius size and their variation with local, geographical and specific factors in some common cirripedes. J. Anim. Ecol.. Vol. 34. pp. 391-402. BARNES.H. & M. BARNES.1967. The effect of starvation and feeding on the time of production of eggmasses in the boreo-arctic cirripede &/anus bahoides (L.). J. exp. mar. Biol. Ecol.. Vol. I, pp. l-6. BARNES.H. & M. BARNES,196%.Egg numbers, metabolic eMiciency of egg production and fecundity: local and regional variations in a number of common cirripedes. J. e.rp. mar. Biol. Ecol.. Vol. 2. pp. 135-153. BARNES,H. & M. BARNES,1977. Studies on the reproduction of cirripedes. 11. Setting of the lamellae; action of protease and disintegration of the oviducal sac. J. exp. mar. Biof. Ecol.. Vol. 27, pp. 219-231. CRISP, D. J. & P. A. DAVIES,1955. Observations in viw on the breeding of Elminius modestus grown on glass slides. J. mot-. biol. Ass. U.K.. Vol. 34. pp. 357-380. CRISP, D. J. & B. PATEL. 1%9. Environmental control of the breeding of three boreo-arctic cirripedes. Mur. Biol.. Vol. 2, pp. 283-295. KOLOSVARY, G. von, 1941. Revisionedella collezione di Balanidi del Museo Zoologico della R. Universita di Firenze. lUonirone Zoologico Italiuno. T. 53. pp. 183-195. KOLOSVARY. G. VON,1943. Cirripedia Thoracica in der Sammlung des Ungarischen National-Museums. Ann. Hisr.-Nat. Musei National. Hwgarici. purs Zoologica. Bd 36, S. 67-120. NILSSON-CANTELL, C. A., 1921. Cirripedien-Studien. Zur Kenntnis der Biologie, Anatomieund Systematik dieser Gruppe. Zool. Bidr. Upps.. Bd 7, S. 75-378. NILSSON-CANTELL, C.A., 1928. Studies on cirripedes in the British Museum (Natural History). Ann. Mug. Nut. Hisr.. Ser. 10, Vol 2, pp. I-39. PATEL,B. & D. J. CRISP. 1960. The influence of temperature on the breeding and moulting activities of some warm-water spexies of operculate barnacles. J. mar. biol. Ass. U.K., Vol. 39, pp. 667-679. PILSBRY.H.. 1916. The se&e barnacles (Cirripedia) contained in collections of the U.S. National Museum including a monograph of the American species. Bu//. U.S. narn. Mus., No. 93, 366 pp. REISS,Z., C. KROPACH,1. LEVANON,J. KLINKER,H. HARP.~Z,Y. SHAPIRO&Z. BEN-AVRAHAM,1976. Data-collecting program in the Gulf of Ekdt - report No. 3. In. Fijfh Report of~rke H. Sreinirz Marine Biofogy Laborarory. Elaf, by Z. Reiss & I. Papema. Hebrew University of Jerusalem, pp. 22-28 and Tables. SAFRIEL,U. & Y. LIPKIN, 1964. Note on the intertidal zonation of the rocky shores of Elat (Red Sea, Israel), Isruel J. Zool., Vol. 13, pp. 187-190.