[advances in marine biology] advances in marine biology volume 22 volume 22 || growth in barnacles

Growth in Barnacles

D. J. Crisp

Natural Environment Research Council, Unit of Marine Invertebrate Biology, Marine Science Laboratories,

Menai Bridge, Gwynedd, United Kingdom

and

E. Bourget

Dkpartement de Biologie, Universitk Laud, QuPbec, Canada

I. Evolution of Barnacles and Their Shells . . . . , ,

11. Mechanisms of Growth . . . . . . . . . . , . A. Growth of individual shell plates . . . . . . . . B. Primordial valves . . . . . . . . . . . . C. Orientation of barnacles at settlement and during growth

111. Modification of Shape . . . . . . A. Effects of crowding . . . . . . B. Influence of substratum on shape . . C. Influence of salinity on shape . .

IV. Factors Influencing Growth Rate. . . . A. Temperature . . . . . . . . B. Light . . .. . . . . . . C. Current, tidal level, and nutrition . . D. Surface contour . . . . . . E. Orientation to current .. . . F. Population density . . . . . . G. Competing organisms. . . . . . H. Parasites . . . . . . . . I. Reproduction . . . . . . . .

V. Age and Growth-the Growth Curve . .

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200 203 203 204 207 208 208 209 211 211 215 216 216 217 217 217 219 219 219 220

ADVANCES IN MARINE BIOLOGY. VOL. 22 Copyrighl 8 19x5. hy Academic Press Inc. tl.ondon) Ltd. All rights of reproduction in any fbrm re\ervcd.

ISBN 0- IZ-O?hl22-7

200 D. J. CRISP AND E. BOURGET

VI. Growth Rates of Various Species . . . . . . . . . . . . Histology and Fine Structure of the Integument: Growth and Ecdysis . .

VIII. Shell Structure in Relation to Function . . . . . . . . . . . . IX. Cyclical Factors in Growth.. . . . . . . . . . . . . . .

A. Tidal influences.. . . . . . . . . . . . . . . . . B. Daily influences.. . . . . . . . . . . . . . . . . C. Other lunar influences . . . . . . . . . . . . . . . . D. Annual influences . . . . . . . . . . . . . . . .

F. Frequency, scale, and precision of measurement . . . . . . . . References . . . . . . . . . . . . . . . . . . . .

VII.

E. Other cyclic influences . . . . . . . . . . . . . .

22 1 222 227 234 234 236 237 237 238 238 239

1. Evolution of Barnacles and Their Shells

All three orders of cirripedes, the parasitic Rhizocephala, the burrowing Acrothoracica, and the sessile Thoracica, have a nauplius stage with frontal horns and an antennulary fixation mechanism, but only the Thora- cica have an external armament of calcareous plates. The earliest known cirripede, Cyprilepas, was a stalked, unarmoured epizoite of eurypterids dating from the upper Silurian (Wills, 1963), clearly a forerunner of the suborder of stalked barnacles, the Lepadidae (Fig. 1). The development of the calcareous armature of the capitulum, protecting the body, mouthparts and cirri, was probably necessary for the early Lepadidae to have become independent of the protection offered by an epizoic life, for modern epizoic barnacles often remain poorly armoured in comparison with intertidal forms. During the evolution of the Lepadidae, or stalked barnacles, there was first an increased calcification of plates surrounding the aperture-the paired scuta and terga-then the addition of an unpaired carinal plate (Fig. lA), and finally a surrounding defence of numerous smaller plates at the top of the stalk, one of which, the rostral, was to become of greatest size and importance (Fig. 1B and C). Whereas the floating and often epizoic lepadomorphs such as Lepas, Conchoderma, Octolasmis, etc., are still relatively thin shelled, with naked stalks, benthic scalpellids (Fig. 1B and C) and the intertidal Pollicipes have become well armed against predators by this further array of plates reinforced by chitinous scales over a short leathery stalk. The Verrucidae and Balani- dae, or sessile barnacles, have further shortened the stalk to a mere cemented disc and have reduced in number but increased in size the wall plates (parietes) surrounding the tergum and scutum.

The Balanomorpha, which are the most advanced thoracicans, dating from the upper Cretaceous, have thus evolved through a basic pattern of two paired opercular plates (scutum and tergum) and eight wall plates, two unpaired (carina and rostrum) and six paired (Fig. 1D). These are

GROWTH IN BARNACLES 20 1

A

5- plated lepadomorphs

hypothetical scutum tergum balanomorph

FIG. I . Shell plates of lepadomorph (A-C) and hypothetical eight-plated balanomorph (D- F). Abbreviations: s, scutum; t, tergum; c , carina; cap, capitulum; pe, peduncle or stalk, not visible in adult balanomorphs; ps, peduncle scales; r, rostrum; 1, rl, ul, cl, sc, other small shell plates developed around the base of the capitulum in benthic forms (the rostrum, r, becomes dominant in balanids); E, F, the inner surface of the opercular valves of balanomorphs; ar, adductor ridge; ad, insertion of adductor muscles; a, ala; r, radius at upper edges of each of the parietes, p, or shell plates r, rl, cl and c; cd, Id, rd, insertion of depressor muscles; oc, occludent margin of scuturn; am, articular margins where terga and scutum fit closely interlocking at the articular furrow, af, and articular groove, arg; bm, basal margins joined to the opercular membrane; cm, carinal margin of tergum; ax, apices, that of the tergum often produced into a beak; sp, spur of tergum (after Foster, 1978).

fused in various ways to produce the families as classified by Darwin (1854) and little modified since. Some species have also calcified the base, but whether membranous or calcified, the base must be perforated by the ducts of the cement glands in order to provide it with the adhesive mechanism by which it remains fixed to the substratum as it continues to grow outwards (Crisp, 1973). The cement, in Balanus at least, is a viscous material which relaxes under pressure and so allows barnacles to slide along the substratum under the force provided by surrounding growing individuals (Crisp, 1960a). It has nothing like the strength sometimes attributed to it (see Yule and Walker, 1984).

Cyprids of the balanomorphs show clear evidence of recapitulation. Immediately after settlement they retain a broad, flexible peduncle which can be pulled out when exposed to strong currents (Crisp and Stubbings, 1957), but within a few days the animal is drawn down onto the substratum, to which its basal region adheres (Yule and Walker, 1984). Im- mediately after metamorphosis, the scuta and terga of the young barnacle are greatly exaggerated in size, as in the Lepadidae, with the wall plates


relatively small. However, during early growth the shape rapidly changes to that of the typical balanomorph (Bourget and Crisp, 1975a).

Balanomorphs have evolved features which have rendered them highly successful in occupying the intertidal zone. These modifications not only seal them from desiccation but also protect them from predators. As we have seen, the vulnerable stalk has disappeared, the wall plates have become interlocked so that they invest the soft parts completely, and the opercular plates which seal the orifice, instead of being exposed to attack, are sunk below the crown of the barnacle. These plates usually fit rigidly against the parietes and are held closed by powerful muscles. The opening between the pairs of opercular plates is clamped by the adductor muscle of the scutum (Fig. l), and the occludent margin of the plates is covered by leathery strips or “flaps” so that, when the operculum is closed, the mantle cavity is completely sealed. When required, however, it can be ventilated through a tiny hole or micropyle left between the flaps (Barnes and Barnes, 1957). The opercular plates must clearly be mobile to allow the cirri to emerge and so are suspended by a tough flexible membrane attached to an overhang which projects downwards from the upper end of the paries. This additional calcareous ring was termed by Darwin “the sheath.” Thus, as the barnacle grows and the crown apex extends up- ward, the downward growth of the sheath keeps the opercular aperture well protected below (Fig. 2).

ou TER SURFACE

OPERCUL

HYPODERMIS (inner surface)

F I X AT ION F I BR’ES

BASAL MEMBRANE

.UM

FIG. 2. Section through wall plate (paries) of a balanornorph to show disposition of sheath and operculurn.

GROWTH IN BARNACLES 203

II. Mechanisms of Growth

A. Growth of Individual Shell Plates

When Darwin wrote his monograph, the mechanism by which a sessile barnacle grew was thought puzzling, as it still is by the uninitiated, who believe the wall plates to be sealed on to the substratum. Darwin beauti- fully unravelled the mystery (Darwin, 1854, pp. 33-61), showing that the individual shell plates can grow at their edges where they overlap each other, yet maintain complete protection of the underlying parts. The over- lapping shell margin he called the radius and the underlapping of the adjacent plate the ala (Fig. 1). Clearly each must be separated from the other by thin slips of living tissue in order to allow growth to continue. The wall plates grow at their lower edges and the base at its periphery, so these also must be separated by two layers of hypodermis, which add to the paries above and to the base below. We shall term this important region the basal suture, following Darwin's apt nomenclature. How then, since there is no solid seal at the suture between paries and base, is the shell held in place? The answer must lie in the numerous fixation fibres (see Crisp, 1965), demonstrated by Gutmann (1960) in Balanus balanoides (L.)' and present, as far as we know, in other balanomorphs (Fig. 2). These are long, fine tendons attached to the inner surface of each paries and expanded into a very short piece of striated muscle, joined again to the basis by a much shorter tendon. Thus the barnacle shell is not itself cemented to the substratum, but, like the shell of a limpet, is held by tendon and muscle to that part of the animal which does adhere to the substratum-the cemented base of the barnacle-which can be compared with the foot of the limpet held by mucus (Crisp, 1973; Grenon and Walker, 1981). No one has yet demonstrated the role of the muscles of the fixation fibers, but we believe that they allow the deposition of thin laminae of shell when they relax and cause it, while still malleable, to conform to the substratum when they contract. There can be no doubt that barnacles are able to chisel the shell into the substratum. Fouling species thus strip off paint films, causing corrosion (Woods Hole Oceanographic Insti- tution, 1952) while epizoic species such as Chelonobia resrudinaria and Coronula diadema drive their shells into the substance of their turtle and

I In this article we are retaining the scientific names used in the original publications, so as to avoid confusion, except where an actual mistake in identity was made. Newman and Ross (1976) have raised the former subgenus Semibalanus to generic rank, and refer to B . balanoides as Semibalanus balanoides. Southward (1976) has divided Chrhamalus stellarus (Poli) into true C. stellatus and another species called Chthamalus montagui; it is likely that most experimental work on C. stellatus, referred to here, was actually carried out with C . montagui.

204 D. J . CRISP AND E. BOURGET

cetacean hosts. In many barnacles with calcareous bases, the junction between wall plate and base is reinforced by a closely interlocking series of holes and projections, as described on p. 227.

Exceptionally, in some species the various shell plates have lost their capacity for independent growth and have become effectively fused. Some Chthamalus species, especially those belonging to the hembeli group (Euraphia), show this tendency. Older specimens of Chthamalus hembeli and Chthamalus intertextus have a fused or nearly fused tergum and scutum, while the basal margin of the parietes becomes tucked in below the base, forming a calcareous ledge which prevents further growth in diameter. The compartments of old specimens of Chthamalus stellatus, and probably of many other species of this genus, become so strongly bound that they can no longer enlarge. Similarly, in some genera, such as Acasta and Pyrgoma, the parietes become fused so that the shell can increase in diameter only at the base, causing the aperture to remain small. Increase in girth, with commensurate increase in orifice diameter, can then be achieved only by abrasion or disintegration of the crown. Darwin noted that in two species, Tetraclita purpurascens (Wood) and Balanus perforatus (Bruguike), in which the aperture was usually en- larged by erosion, specimens in which the shell remained intact had indeed well-developed radii, and so had succeeded in enlarging the circumference and orifice. As he writes, “It appeared, but of course erroneously, as if the lateral growth of the compartments had been sub- jected to the will of the animal” (Darwin, 1854, p. 56).

B. Primordial Valves

In the primitive thoracican Lepas, the cyprid, or settling stage, already contains the primordia of the five calcareous valves, scuta, terga, and carina, though before its attachment to a substratum they are without trace of calcareous matter. They can be seen through the carapace as a single layer of cells which, according to Darwin, are hexagonal in outline, 1/6000-2/6000 in. (4-8 pm) across. Almost immediately after settlement calcification begins, and the characteristic form of the five most primitive shell plates can clearly be seen under light-field, dark-field, or phase- contrast illumination if the tissues of the cyprid are cleared away with a strong solution of sodium hydroxide (Figs. 3 and 4A-C). Under high magnification with polarizing filters, the hexagonal patterns mentioned by Darwin can be seen to be composed of interlocking garlands of tiny calcite crystals with variously orientated crystal axes (Fig. 3D), alternately spar- kling as the plane of polarisation is changed. A primordial shell lies at the umbones of each of the five major plates of lepads, and can be distinctly

FIG. 3. Primordial valves of Lepas cyprid, under dark-field illumination, showing primordial scuta (s), terga (t) and canna (c); cyprid 1.5 mm long.

GROWTH I N BARNACLES 207

identified in the adult shell by their peculiar patterning. The mature shell is laid down around the primordial shell with marks that indicate the position of the growing edge at each progressive growth episode (Fig. 4D). It is interesting that, in Lepadidae with numerous plates, only the most primitive five have primordial elements.

Darwin claimed to have seen traces of these primordial valves in Chtha- malus, a primitive balanomorph, but not in the more advanced Balanidae. However, a distinct element at the apex of the paries (Bourget and Crisp, 1975c), primordial in the sense of being laid down at or very soon after metamorphosis, can be identified in balanids.

Contrary to the views of Kuhn and Fuchs (1954), there are no calcareous deposits in the unmetamorphosed larval stages. Yule et al. (1982), by analytical methods, found that, as in the lepad cyprid, calcite is laid down only after metamorphosis in Balanus. The white crystalline deposits thought by Kuhn and Fuchs to be calcium carbonate were described by Walley (1969) and are probably organic, like those in the limbs of the adult barnacle, in which there are white deposits of guanine (Waite and Walker, 1984).

C. Orientation of Barnacles at Settlement and during Growth

At settlement the last act of the still mobile cyprid is to orientate itself to three environmental influences-the contour of the surface, the direction of light, and the current. These influences form a hierarchy to which the cyprid reacts in that order (see Crisp, 1975). The strongest influence is the direction of surface grooves or furrows (Crisp and Barnes, 1954). The cyprid is capable of aligning to the long axis of a cylindrical cavity whose radius of curvature is many times the length of the cyprid itself, though narrow grooves into which it can fit snugly are preferred. These situations clearly offer protection during the period immediately after metamorphosis.

Secondly, the cyprid responds to face the direction of light (Barnes et al., 1951). Forbes et al. (1971) examined the shading response to light coming from various directions and found that the rostra1 area of the adult barnacle, beneath which lie the paired eyes, was the most sensitive. When it orientates to light at settlement, the cyprid places this sensitive com-

FIG. 4. (A) Detail of primordial scutum of cyprid under normal illumination; f , food body and associated pigment; (B) detail under phase contrast; (C) detail under polarised light; (D) fully calcified primordial valve forming the umbone of the scutum of a juvenile Lepas. Note the similar hexagonal pattern within the primordial valve and the growth banding in the growing shell. Valve length ca. 0.5 mm [cf. (A)].


partment away from the light. However, it is from this direction that predatory fish learn to attack, so that the orientation adopted is likely to be of survival value.

Thirdly, the response to current is so weak that it is difficult to demon- strate in the laboratory unless the first two influences are eliminated by experimenting on smooth surfaces and in darkness (Crisp and Stubbings, 1957). However, the reaction may nevertheless be important in barnacles that settle on swimming animals such as portunid crabs (Forbes er a[., 1971), turtles, and whales (Crisp and Stubbings, 1957). The orientation displayed to current, which causes the posterior end of the cyprid to point upstream, is that which allows the cirral flet, after metamorphosis, to fish into the current with least distortion of the animal’s posture. If, after settlement, the orientation is otherwise, it can readjust during growth and optimise its orientation. This process of “torsion” was shown by Crisp (1953) to result from constant exposure to unidirectional or prevalent currents. In barnacles with radial canals in the calcareous base, for example, Balanus improvisus (Darwin) or Balanus amphitrite (Darwin), the evidence of torsion remains behind as a spiral twist in the canals. How- ever, B. balanoides, which has a membranous base, also reorientates in the expected sense (Crisp, 1953; contra Moore, 1933). It is not known how the prevailing current causes the torsion, whether the animal senses the current and can change the direction of growth accordingly, or whether the orientation is a passive result of mechanical forces. The current, which causes the extended cirri to twist, may thereby apply a torque to the base.

111. Modification of Shape

The morphology of a barnacle has great plasticity, so that its form may be much modified during growth without greatly hindering its vital activities. Although there have been attempts to relate shape to environment (Abel, 1926; Neu, 1935), only three main factors have been well documented as causing modification in shape: first, the forces produced by the growth of surrounding individuals; secondly, the shape of the surface on which the barnacle is growing; and thirdly, salinity.

A. Effects of Crowding

An isolated barnacle grown on a smooth flat plate might be expected to extend symmetrically about its point of attachment. In an experiment to test this, Bourget and Crisp (1975a) found that although there was com-


plete symmetry in lateral extension, extension along the rostral exceeded that along the carinal direction in Elminius modestus (Darwin), while in Balanus balanoides there was considerable variation in eccentricity along the rostrocarinal axis. We suspect that, since in most species the rostral compartment makes the more acute angle to the substratum, the rostrum should grow faster, as in Elminius.

It is well known that when barnacles grow in close proximity, their shells become elongated and the base narrow (Trusheim, 1932; Schafer, 1938, 1948). Whether the species possesses a membraneous or a calcareous base, the shell-secreting tissue of the basal suture in such elongate specimens must become distorted; the parietes, instead of progressively thickening towards the base, are there reduced to thin slips of shell with greatly reduced adhesion. In contrast, growth of the opercular plates, the sheath and the summits of the radii and alae continues apace. As a result, the upper parts of the individuals expand and fan out, producing hum- mocks which are strengthened on the outside by the interlocking of the compartments (Gutmann, 1960) but are fragile within. Eventually, the hummock disrupts (Barnes and Powell, 1950). When individuals grow in this hummock form, the opercular plates are often a better guide to size and age than the shell as a whole. Nevertheless, if barnacles grow on a smooth surface with sufficient space outside the group in which to expand, even though the individuals come to touch one another, they will continue to adhere. The outer ones will slide along the surface centrifu- gally, and the whole group will continue to grow with little elongation upwards (Crisp, 1960a).

Clearly barnacles compete avidly for whatever space is free, and only when there is no more space in which to spread are they distorted into the columnar form. Some species, such as Chthamulus depressus (Poli) and E. modestus, have a naturally flattened shape with a low angle of contact with the substratum; these can form only slightly elongated columns when crowded. Others, such as Balanus humeri (Ascanius) or Chamaesipho columna (Spengler), readily and naturally develop tall individuals.

B. Influence of Substratum on Shape

Gregg (1948) noticed how surface irregularities left their impression on the walls of barnacles and of other organisms that grew in close conformity to the surface. Gutmann (1960) described how isolated individuals of Bala- nus balanoides were modified, those settling in hollows becoming flattened, while those growing near an edge had to extend the shell plates in order to allow them to arch over it. Small individuals lying in grooves would become elongated in the direction of the groove. He interpreted

210 D. J. CRISP A N D E. BOURGET

these modifications in terms of the necessity for the shell to remain in contact with the substratum.

Crisp and Patel (1967) saw the analogy between the shape of a barnacle on a surface and that of a droplet of water. Thus a droplet in a groove becomes similarly orientated along the length of the groove. This is not due merely to its remaining in contact with the surface, but rather because it maintains a constant angle of contact at all points at the periphery, as a result of which its shape is modified. Crisp and Patel calculated, on this basis, how the shape of a barnacle would be modified when grown on surfaces of positive (convex) and negative (concave) curvature. Their observations agreed well with mathematical prediction, both for B. bulunoides with its conical form, and for E. modestus with its more complex, flatter shape. Fig. 5A and B illustrates the variation in shapes observed

CONCAVE PLANE CONVEX FIG. 5. Variation in shape with surface contour. Left to right: concave, plane, and convex

substratum. (A) E. modesfus in side view, all of equal age; (B) E. modestus in plan view, all of equal age; (C) shell plates of B . balanoides, all of equal age (from Crisp and Patel, 1967, reproduced by courtesy of Marine Biological Association of India).

GROWTH IN BARNACLES 21 I

when the latter species is grown on concave and convex surfaces. Crisp and Patel also noted that, when barnacles grow on concave surfaces, the weight of dry tissue relative to the total, including shell, was larger than when grown on convex surfaces, probably because of the greater capacity of the hollowed-out base, while the opercular valves and parieties were reduced. In absolute size, however, the individuals on convex surfaces grew more rapidly, probably because they had the advantage, due to their exposed position, of greater access to water flow. In both Balanus and Elminius the shorter and narrower parietes formed on the concave surfaces were distinctly more crenulated than those on convex surfaces (Fig. 5B, C). There is probably a morphogenetic norm for the surface area/ volume ratio, so that the reduction in area caused by the concave shape of the substratum is compensated by folding and crenulation of the paries at the basal margin. Another example of morphometric compensation was seen in the size of the lateral compartments. Thus, when there was a large left compartment it would usually be compensated for by a small right one and vice versa (Crisp and Patel, 1967).

C. Influence of Salinity on Shape

Barnes and Barnes (1962a) noted that in the region of the Danish Belts, where B. balanoides reached its salinity limit, individuals have fragile shells and become unusually flat, the measure of height/basal diameter falling to 0.2 in Jutland, compared with values of 0.4-0.5 on the North Sea coasts. The euryhaline barnacle B. irnprouisus, however, showed no com- parable change in shape (Barnes and Barnes, 1961) nor, in our experience, does the cosmopolitan species B. amphitrite.

IV. Factors Influencing Growth Rate

Since the Lepadidae are oceanic and only occasionally found washed up alive, growth studies depend on serendipity. Most of our information on barnacle growth, in consequence, relates to the Balanomorpha, and in particular to B . balanoides. This species has a highly synchronized settlement in spring, so that a single cohort can be followed readily. All individuals of a year class have been exposed to broadly similar seasonal conditions of water temperature, salinity and suspended nutrients. The effects of local factors, such as wave action and water flow, can be isolated quite easily. Table I summarizes growth data for B. balanoides, and Table I1 includes data for other species.

TABLE I. B. balanoides GROWTH DATA

Location

Approximate

temperature carinal diameter annual monthly Mean rostro-

range (sea and at end of first Conditions air average, "C) pnlday season (mm) Reference

Spitzbergen Herdla, Norway Millport, Scotland

Port Erin, Isle of Man Liverpool Menai Straits

St. Malo

St. Andrews, New Brunswick Woods Hole, Rocky Beach Woods Hole, Buzzards Bay

Intertidal Midlittoral Raft (cleaned) Midlittoral Piles, midlittoral Raft (cleaned) Midlittoral, piles Several levels

and exposures

Midlittoral Raft (submerged

and cleaned)

4.2- 13.7 6-13.9

6.8-13.4 6.3-14.3 5.0-16.1 6.1-15.4 5.5-15.5 7.0-17.1

18--2 24- 4- 2 22-4-4

25 26

120- I30

23 120-160

158 63 33

36 44 75

7-9 13-14 17.5 5.3 5.9

12-17 5-7

2.5-4.0

Ca. 9 Ca. 10

Feyling-Hanssen (1953) Runnstrom (1925) Barnes and Powell (1953)

Moore (1934) Corlett (1948) D.J. Crisp (unpublished) D.J. Crisp (unpublished) Hatton (1938)

Bousfield (1954) Barnes and Barnes (1959b) Barnes and Barnes (1959b)

TABLE 11. GROWTH RATES I N VARIOUS SPECIES~

Species

Daily growth Approximate Linear rate in linear maximum + half

phase (pm) size (mm) maximum size Reference

C . stellatus St. Malo HW exposed

MTL exposed Brixham HWS

HWN MTL LWN

Millport Continuous immersion (raft) Continuous immersion after

keeping at HW

E . modestus Menai Straits

Millport, raft Millport, high intertidal Stranraer, low intertidal

Balanus glandula (Darwin) Pacific Coast, intertidal

(raft-continuous immersion)

10 I5 21.4 37.5 50 55

12-14

50

138 113 25 42

51

12 12 12 12 12 12

12

12

17 17 17 17

25

1.67 2.5 3.57 6.25 8.33 9.71

2.0-2.33

8.33

16.2 13.3 2.9 5.0

4.1

Hatton (1938)

D.J. Crisp (unpublished)

Barnes (1956)

Barnes (1956)

D.J. Crisp (unpublished) Barnes and Barnes (1962b) Barnes and Barnes (1962b) Barnes and Barnes (1962b)

Barnes and Barnes (1956)

(continued)

TABLE 11. GROWTH RATES IN VARIOUS SPECIES~ (CONTINUED)

Species

Daily growth Approximate Linear rate in linear maximum + half

phase (wn) size (mm) maximum size Reference

B . amphitrite Shoreham Harbour, Portslade 245

Power Station, panels on wall of cooling pond

Balanus perforatus Brixham intertidal Raft

Balanus crenatus (Bruguiere) Millport, raft Menai Straits, raft

Verruca stroemia (Miiller) Millport, raft

14 122

220 284

25 19.6 Crisp (unpublished)

35 35

25 25

0.8 Emily Clay (unpublished) 6.97 Emily Clay (unpublished)

17.6 Barnes and Powell (1953) 22.12 D.J. Crisp (unpublished)

Balanus balanus (L.) Millport, raft

Two fast-growing individuals 130 Average first year 36 Beaumaris Bay, sublittoral 70

50 8 12.5 Barnes (1958)

43 43 43

6.05 Barnes and Barnes (1954) 1.7 Barnes and Barnes (1954) 3.26 Crisp (1954) as Balanus

porcatus (Da Costa)

Balanus humeri Isle of Man 33h 31* 2.12 Moore (1935)

a For B . balanoides, see Table 1. Derived from volume measurements and Bertalanffy equation

GROWTH I N BARNACLES 215

Although it is the soft tissues that are responsible for growth, the shell is so much easier to measure and weigh that the greater part of our knowledge relates to length or weight of the shell. It is assumed that a relationship exists between shell and body weight, although seasonal influences must be large for a species such as B . balanoides, which sheds its gametes in autumn and then stops feeding and moulting for some time (Crisp and Patel, 1960, 1969; Ritz and Crisp, 1970). For this species Barnes and Barnes (1959a,b) have provided a large amount of data on seasonal changes in wet weight and nitrogen content of the “body” (prosoma and thorax) in relation to shell size. It should be noted that these weights are difficult to relate to those of other investigators where tissue weight includes the depressor muscles and other parts adhering to the shell and basis, as well as prosoma and thorax. Thus Barnes and Barnes show a wet weight of tissue comprising 7-10% of the total of shell and tissue, whereas Crisp and Patel (1967) and Fradette and Bourget (1980) found the dry weight of all tissues to be as high as 7-10% of the total weight in B . balanoides and as high as 15% in Elminius, which has a thinner shell.

Other variations in tissuehhell weight ratios may well be found, in addition to seasonal changes. For example, barnacles growing at high tide levels, under nutritional stress, would be expected to have a relatively low ratio of tissue weight to shell weight. Conversely, the ratio should increase in low salinity habitats where the shell is obviously less well calcified. However, we are not aware of any researches expressly di- rected to these aspects of growth of barnacles.

A. Temperature

It is usually assumed that temperature will enhance growth rates, since the cirral beat, which represents the potential rate of food gathering, has been shown by several authors to be strongly temperature-dependent (e.g., Southward, 1955, 1957). Thus it is scarcely valid to attempt to isolate the effects of temperature from those of food supply. Seasonal variations in growth rates involve a complex set of factors, including the physiological state of the animal, as well as environmental temperature, nutrient levels and racial differences, none of which can readily be disen- tangled, as can be seen from the study by Barnes and Barnes (1959a,b). Temperature may well have differential effects on assimilative and respi- ratory metabolism, growth and gametogenesis being determined as the net gain to the animal of these processes. Wu and Levings (1978, 1979) compiled an energy budget for individual and population growth, respectively, over the annual cycle of Baianus glandula.


B. Light

Neither we nor Barnes (1953), in a careful study where other factors were eliminated, could find any evidence of an influence of light on growth, despite the claims of Klugh and Newcombe (1935) (see also p. 236).

C. Current, Tidal Level, and Nutrition

Sessile organisms such as barnacles generally reach their greatest size when growing in estuaries, in tidal rapids, or on headlands exposed to swell, since they can receive greater quantities of suspended food under such conditions. Hatton (1938) demonstrated this effect by transplanting barnacles from still to flowing water, while Hatton and Fischer-Piette (1932) and Moore (1934) found faster growth at wave-exposed localities. By growing B. balanoides on panels in the same current flow but with some individuals protected by baffles, Crisp (1960b) showed that those directly exposed to current not only grew larger, but their rate of growth steadily rose to reach double that of those behind the baffles. The faster growth rate was attributed to the extending of the cirri beyond the bound- ary layer into the freely flowing current. Currents not only transport more food to the barnacle, but also stimulate cirral activity. Cirral activity is also stimulated by the presence of food particles and soluble organics in the water (Crisp and Southward, 1961; Crisp, 1967; Allison and Dorsett, 1977).

The higher the tidal level occupied, the more is the food supply re- stricted by periods of emersion, as shown by Barnes and Powell (1953) (see also Table IV). If their data are reinterpreted as growth rate per daily submergence time, there is only a small influence of tidal level, those at high water growing slightly faster. Crisp (1960b) explained this effect by suggesting that those at high tidal levels would benefit from greater wave exposure. However, Southward (1955) showed that the feeding mode of cirral activity (fast beat) was more prevalent in high water animals, while Barnes (1956) found that Chthamalus previously kept at high levels grew faster (Table 11). Ritz and Crisp (1970) demonstrated that high water B. balunoides fed more avidly than those accustomed to live at lower tidal levels. Thus, higher ingestion and growth rate per unit of feeding time may be explained as an adaptation to nutritional stress-subjectively, to hunger-in those individuals which have shorter periods of immersion.

In Balanus bulunoides the influence of current, wave exposure, and tidal level appears greatly to outweigh latitudinal temperature influences, as can be seen from Table I.


D. Surface Contour

Hatton (1938) noted that barnacles settled in hollows grew more slowly than those on an exposed surface. Cyprids of B. balanoides, settled in pits only slightly larger than themselves, not only showed slower metamorphosis (Gamble, private communication) but also slower growth during the first 15 days. After this time, having outgrown the dimensions of the pit, they fed, respired, and grew normally.

E. Orientation to Current

A heavy board suspended from an anchored chain on swivels, such that it always swung with the tide, provided natural conditions of growth with unidirectional current flow. Spat of B. balanoides that had settled within a few days of each other were arranged at various orientations to the current flow and measured at the end of the season's growth. Those with the rostra1 end towards the current source could collect plankton simply by extending the cirral net (see Crisp and Southward, 1961), but those with the lateral plates or the carina towards the current source had to twist the cirral net through 90 or 180" in order to set it across the current. A small but significant advantage in growth of approximately 10% by weight or 3% by linear dimension accrued to the former (Crisp, 1960b).

F. Population Density

Since barnacles settled together on a surface remove particulate material from the same water mass, they compete for the same food resource. When sufficiently close, they may also interfere with each other's cirral activity. This latter possibility was investigated by comparing with single individuals, pairs of barnacle spat settled adjacent to each other so that they might interfere. Pairs and singletons with otherwise ample space from which to draw food grew at equal rates; hence their mutual interference was negligible (Crisp, 1960b). However, growth rates of populations of B. balanoides set up at increasing densities starting from 0.25/cm2 began to compete for space as soon as they touched. Beyond that point, growth in diameter almost ceased, but individual dry weight and volume continued to increase by growth in height. Above l/cm2, however, the growth rate by weight gradually fell with increasing density of settlement.

In a further examination of intraspecific competition, Crisp (1964) compared dry weights of B. balanoides at the end of the season at various population densities and in three different situations:

218 D. J . CRISP A N D E. BOURGET

1. The most favourable: on a raft in the Menai Strait 2. On an intertidal support and 3 . In an enclosed box with limited water flow and planktonic food

When expressed as a fraction of the weight of individuals grown in isolation, growth at given population densities was identical in all situations, though the absolute growth in situations (2) and ( 3 ) was only about one- third and one-tenth, respectively, of the raft individuals' (Fig. 6). More- over, the total biomass per unit area was limited by insufficient settlement density only below five individuals/cm2. Above this critical settlement density, competition was such that any increase in food assimilation by the extra individuals was subtracted from that obtained by the others. The average weight to which the group occupying unit area would grow by the end of the season was therefore independent of the number of individuals settled per unit surface area. Since these barnacle populations came to monopolise the surface area at densities >5/cm2, the rate of food capture was maximal and strictly depended only on the rate at which the moving water could transport particles into the waving sheet of cirri below. The hydrodynamics of this system deserve further study. To carry particles toward the surface where the extended cirri capture them, the flow must be nonlaminar with velocity components normal to the surface. More- over, this regime of turbulent flow must be uniform both up- and down- stream of an array of barnacles, since there was little difference in growth

supply

BOO 100

5c

<, .5,.0 I o,.o I5.,0

a a W

6

t z 3

-

a

a W

s' w 3 m ul

b-

> 0

-

a

I N I T I A L S E T T L E M E N T D E N S I T Y [ern-'] FIG. 6. The relationship between total oven-dry biomass at the end of the first growing

season and initial settlement density, in each of three environments (from Crisp, 1964, by courtesy of Blackwell Scientific Publications, Oxford).


rate between the leading and trailing edges of the population (Crisp, 1960b).

G. Competing Organisms

Many sessile barnacles form part of the primary fouling community settling on otherwise bare surfaces, usually after the primary film has been established. They grow best on wave-exposed shores where limpets control algal growth, or in dark, plant-free situations. Barnes (1955) documents reduced growth of submerged B . balanoides and Balanus crenatus (Bruguikre) when filamentous algae are present, since they reduce water flow and possibly interfere with cirral activity. Enteromorpha intestinalis is frequently abundant in eutrophic estuaries, especially in the cooler months, and similarly reduces the growth of E. modestus. The presence of foliaceous animal fouling, such as hydroids, bryozoans, etc., must similarly reduce growth, while secondary fouling by space monopolisers such as mussels, anemones, compound ascidians and sponges will at first depress barnacle growth and ultimately smother the settlements alto- gether (Scheer, 1945).

H. Parasites

The cryptoniscid isopod Hemioniscus balani lives usually singly in the mantle cavity of a number of species (see Crisp and Fischer-Piette, 1959), where it destroys the ovary and reduces somatic growth (Crisp, 1960b). Barnacles are also host to a number of rhizocephalan parasites, but their effects on growth have not been researched. Examples are Chthama- lophilus delagei, which is exceptional in being ectoparasitic (Bocquet- VCdrine, 1957), and Boschmaella, often present as a multiple parasite, which attaches to the internal mantle lining of balanids such as B. improuisus (Bocquet-VCdrine, 1969). Intertidal barnacles are often heavily in- fected with the metacerceria of trematodes; these cysts distort the body but, being passive, are unlikely to influence its growth seriously.

1. Reproduction

Energy expended in reproduction cannot be available for growth, and vice versa. Crisp and Pate1 (1961) prevented breeding in E . modestus, an obligate cross-fertilizing hermaphrodite, by isolation. They compared growth of isolated individuals with paired individuals well spaced apart to reduce mechanical or competitive interaction, but which were nevertheless able to breed. The two sets grew at equal rates during the period


before the majority acquired mature ova (less than 6 mm; 0-52 days), but after breeding had begun (more than 5 mm; 38-157 days) growth rates diverged significantly, the breeding individuals growing more slowly. Lest this result should have arisen from competition between pairs, in a second experiment Elminius was paired either with its own species or with a faster growing species with which it could not breed. After 6 months the tissue weight of the breeding specimens had been reduced to about half that of virgin individuals. The loss of tissue was shown to correspond reasonably closely with that of the broods of nauplius larvae that had been liberated.

The effects of reproduction in reducing growth rate have not been tested on barnacles with a single annual brood such as B . balanoides, where, in Europe, feeding and growth normally ceases in winter. Such an investigation would be of special interest since Barnes (1 962) attributed anecdysis and other aspects of reduced activity characterising the winter condition of B . balanoides (Crisp and Patel, 1960) to low environmental food levels and postbreeding “debilitation” rather than to a physiological change under hormonal control (Crisp and Patel, 1969). If laboratory- maintained animals are supplied with food during the winter, then the period of anecdysis is reduced and growth continues, although other factors regulating the seasonal cycle are present (Barnes et af., 1963). Barnes (1962) and Barnes et al. (1963) also detected an arrest of growth not entirely dependent on feeding, coinciding with the time when the ovary was initiated.

V. Age and Growth-the Growth Curve

As in most invertebrates, the rate of growth of juvenile barnacles at first accelerates and then, with increasing age and maturity, slows down. Thus, whatever the initial growth rate, a given species tends towards the same ultimate size if allowed long enough to reach it.

Some authors have quoted “specific growth rates” or “relative growth rate,” (dx/dt)/x or d logs/dt. Since, except for exponentially growing cultures, this quantity declines even more rapidly with age than absolute growth rate, the concept has little to recommend it. In seeking a more useful function by which to describe the change in growth with age, it must be borne in mind that the curve representing absolute growth will depend critically on the units employed, whether linear, superficial or volumetric. Crisp (1960b) suggested that the linear increase in diameter was the most appropriate, since not only was it easily measured, but it also remained relatively constant over much of the animals’ early growth.

GROWTH I N BARNACLES 22 1

For that part of the growth curve beyond maturity in which growth rates are falling, the Bertalanffy equation is probably better.

Crisp (1960b) suggested that, since for an isometrically growing barnacle the area of cirral net should increase as the square of a linear dimension L, so also would food uptake if the net captured suspended particles by extending passively in a steady current. He assumed that the rate of volume increase would therefore rise as Lz. This would, in turn, imply a constant increase in the linear dimensions of the animal, as is in fact observed in the rate of increase of basal diameter over a considerable part of the growth curve. Dr. R. N. Hughes has drawn to our notice that assimilated energy must be partitioned between increase in biomass and respiration. Fortunately, this correction does not influence the conclu- sion. The equations for the energy budget should be prefaced in terms of biomass (B) proportional to length3 (L3).

B = KpL3 (1)

Production (P) is increase in biomass with time:

P = dB1dt = 3KpL2dL/dt ( 2 )

Respiration (R) is approximately proportional to L2 (the well-known “area law”):

R = K R L ~ (3)

Assimilation (A) (Crisp, 1960b) is assumed proportional to food uptake and to cirral net area:

A = KAL2 (4)

By the first law of thermodynamics,

dBldt = P = A - R

Substituting for P , R , and A from Eqs. (2), (3) and (4):

dLldt = (K*-KR)/3KP = a constant ( 5 )

Barnacles would offer a suitable subject on which to test these relations.

VI. Growth Rates of Various Species

The best records of growth rate have been made on sessile barnacles responsible for fouling (e.g., Barnes and Powell, 1953), or by repeated measurements in autecological investigations (e.g., Moore, 1934). Other, less reliable, data have been obtained from measurements of the maxi-


mum dimensions of individual barnacles found on ships’ hulls after the completion of a voyage or on buoys left at sea for a known period. Table I, for a single species, B . balanoides, illustrates how much variation exists. Measurements apply only to the location and to the season quoted, although perhaps there is an optimal rate, characteristic of the species, which is approached when ideal conditions of temperature, current and food availability obtain. Table I1 supplements Table I, giving recorded growth rates of certain other species. In comparing species, Barnes (1958) sought to minimise the effects of differences in size by measuring relative growth rate at half maximum size. A simpler comparison, giving similar results, is shown in Table I1 by dividing the rate of linear growth by one- half the maximal size. It can be seen that:

1. 2.

Growth rates are low in large species Species growing on rafts, in flowing channels, or in the shallow sublittoral give the highest rates, those at high tide levels the low- est, and

3. Chthamalus, often a high shore barnacle, grows relatively slowly.

The few available observations on growth rates of lepadomorphs indicate fast growth despite the alleged paucity of plankton at the surface of oceanic waters. Dalley and Crisp (1981) fitted observed growth of Con- choderma aurita and Conchoderma uirgatum to the Bertalanffy equation, obtaining initial growth rates of the capitulum of 0.83 and 1.17 mm/d, respectively. Tropical and subtropical sessile barnacles grow, mature and breed faster than cool temperate species (e.g., Paul, 1942; Daniel, 1954).

VII. Histology and Fine Structure of the Integument: Growth and Ecdysis

In cirripedes, most of the hypodermis has retained the ability to produce a flexible and frequently replaced uncalcified skeleton. However, the hypodermis underlying the shell plates can lay down an organic matrix containing calcium carbonate in the form of calcite crystals, while the outer surface of the shell is covered by a cuticle. The animal, like all other anthropods, is totally surrounded by a cuticle and epicuticle. However, unlike other crustaceans where the chitin-protein integument may be impregnated by calcium carbonate, in barnacles there is a complete separation between the outer cuticle and the accreted layers of calcite. Whereas in most crustaceans with calcified exoskeletons the mineral portion, before ecdysis, is either resorbed, often into a gastrolith, or shed with the old integument, in cirripedes the shell is a permanent structure


continuously added to during each period of intermoult. “A cirripede,” wrote Darwin of the Thoracica, “cannot like a crab crawl into some crevice and remain protected till its shell becomes hardened; hence, probably, it is that the shell is never wholly moulted.” The hypothesis put forward by Darwin (1854), that the shell was deposited by a hypodermis lying below previously formed layers of shell, has been widely accepted. Only Gruvel (1893) and Davadie (1963) thought that the epidermis lay immediately below the cuticular elements on the outer surface of the shell and that the shell was formed by addition of material from outside the preexisting shell. Newman et al. (1967) effectively disposed of this error. As noted by Darwin, there is evidence within the shell of frequently deposited laminae (1854, p. 57), which we now know as being formed at each tidal immersion (Bourget and Crisp, 1975b; Crisp and Richardson, 1975), as well as evidence on the surface of the shell of less frequent episodes of ecdysis.

It must be emphasised at this point that we have insufficient information regarding the composition and origin of the shelled integument of barnacles to be able to homologise with certainty the various layers with the more usual structures in arthropods (Neville, 1975). The outermost horny layer, which is often lost, was called by Darwin the “epidermis”; it probably corresponds to epicuticle plus cuticle in whole or in part but is, in any case, excessively thin. The organic components of the shelly layers secreted by the underlying hypodermis may also represent part of the endocuticle. The amount of material is sparse (Barnes et al., 1976), yet often highly complex (see below). In Chthamalus, Klepal and Barnes (1975a,b) consider that this material includes persistent epicuticle left at each moult. It probably combines an arthropodin-like protein (Crisp and Meadows, 1962, 1963) with chitin in various proportions (Barnes et al., 1976). However, it is best not to assume any certain homology with classi- cal cuticle at this stage, and in referring to the outer horny layer as “cuticle” we imply none.

Darwin (1854, p. 59) describes how, as a result of shell expansion in three regions of sutures-between the opercular valves and the sheath, between the lateral edges of the parietes, and between the base and the shell wall-the adherent cuticle splits “at each period of exuviation.” This membrane “which when well preserved invests the walls of the shell is made up . . . of successive adherent slips which originally covered the lines of the sutures.” He also states that “little bristles . . . which arise from the slip of membranes left adherent to the opercular valves, sheath and walls stand in rows; a row corresponding to each period of exuviation . . . ” Darwin had clearly seen and appreciated the significance of the relationship between shell growth and moulting long before others had


redescribed it (von Bahls, 1903; Costlow, 1956; Costlow and Bookhout, 1953, 1956; Bocquet-VBdrine, 1963, 1964, 1965, 1966a,b; Bourget and Crisp, 1975c; Klepal and Barnes, 1975a). Darwin was not equipped to investigate the processes at work in these sutures at the cellular level. Histological studies carried out by Bocquet-VCdrine (1963, 1964, 1965, 1966a) on various operculates have shown that the activity of the hypodermis wedged in the basal suture is discontinuous, the events being synchronised with the animals’ moulting cycle. Klepal and Barnes (1975a) repeated these observations on C . depressus without demurring from Bocquet-VCdrine’s conclusions. Bubel (1975) made further advances by describing at the fine structure level the opercular hinge and the basal suture. According to Bubel and Bocquet-Vedrine, during each intermoult period the cells located here lay down first new epicuticle, then endocuticle, both within the previously formed cuticular membrane.

The new layers are folded and contrast sharply with the older stretched layers beneath (Fig. 7). In order to lay down the increased length of membrane which will allow for subsequent growth, the surfaces of the secreting cells are greatly folded. Electron micrographs of the hypodermis underlying the opercular hinge of E. modestus show this folding clearly

0

FIG. 7. Distribution of continuous shell growth during the intermoult period: Mean, with standard error bars, of cumulative percentage growth during the intermoult period plotted against the percentage of time elapsed during the intermoult period (from Bourget and Crisp, 1975c, by courtesy of the Marine Biological Association).


(Bubel, 1975). According to Bocquet-VCdrine, secretory activity starts at the extreme corner of the basal suture where the hypodermis abuts the rim of the calcareous shell and proceeds centripetally along the basal layer of hypodermis. The process begins at stage C of the ecdysis cycle (Drach, 1939), as judged by the condition of moulting of the limbs and body. The formation of the epicuticle is followed by secretion of cuticle at moult stage D2. At this point the limbs and body moult, but clearly nothing can be shed from beneath the persistent wall plates. During the premoult stages A and B, Bocquet-VCdrine (1965) states that the hypodermal cells deposit calcium on the older portion of the shell, thereby extending the length of the parietes and the circumference of the shell, so breaking the old cuticle and unfolding the new. Unfortunately, Bocquet-Vedrine does not record the time intervals of the various moult stages.

Bourget and Crisp (1975b,c) in B. balanoides and Crisp and Richardson (1975) in E. modestus, one of the species studied by Bocquet-VCdrine (1963, demonstrated that discrete layers of calcium carbonate are formed whenever the barnacle is immersed. This appears to be so whatever the interval between immersions, so that deposition must be virtually continuous as long as sea water is supplied to the mantle cavity. Bourget and Crisp (1975b) found by direct observation of young immersed barnacles that there was little variation in the rate of shell growth throughout the moulting cycle, other than a slight increase during the first half and a small reduction towards the latter end of the intermoult period (Fig. 7). It follows that, if Bocquet-VCdrine is correct in assuming that epicuticle, cuticle and calcareous shell are laid down consecutively, the length of stage C to D2 for cuticle formation must be very short indeed compared with the premoult and intermoult stages of the cycle, when the shell is being produced.

Bourget and Crisp (1975b) proposed a slightly different mechanism to account for the two distinct processes: cuticle formation and shell deposition. They agree that the epicuticle and cuticle must be secreted first, and are gradually stretched at the basal perimeter of the shell as shell is being laid down. Calcite is secreted periodically during tidal immersions by the hypodermis beneath the parietes, mainly towards the outer edges. These authors suggested that haemolymph pressure controlled by the muscles of the prosoma, together with adjustments made by the small muscular elements of the fixation fibres that join the shell plates to the base, periodically force the still plastic shell matrix down into the substratum, the pressure causing the new cuticle to form an annular bulge at the edge of the shell (Fig. 8).

In B. balanoides these bulges are figured by Bourget and Crisp (1975~) as smaller ridges which do not coincide with tidal growth increments nor


D'

Ce

FIG. 8. Growing edge of a barnacle: Abbreviations: A, A', calcium carbonate-secreting area of hypodermis (maximum secretion); B, B', calcium carbonate-secreting area of hypodermis (minimum secretion); C, C', basal cuticle-secreting area of hypodermis (premoult only), not exuviated; Ce, cement; Cuo, Ep,, remains of cuticle and epicuticle formed during a previous intermoult; Cu, , Ep , , old cuticle and epicuticle which will become broken by stretching; Cu2, Ep,, new folded cuticle and epicuticle; D, D', nonsecreting area of hypodermis; E, E', mantle lining hypodermis secreting a normal thin cuticle exuviated at each ecdysis; h, hair of hirsute ridge; G , , G2 , tidal growth increments separated by growth lines; r,, large moulting ridge or hirsute ridge; r , , rz. rl. ridges formed during growth; F, fixation fibre; M, muscle of fixation fibre. (Modified from Bourget and Crisp, 1975c.)

with the larger ridges and hairs (hirsute ridges) associated with moulting (Fig. 8). Klepal and Barnes (1975b) illustrated similar configurations in C . depressus. Eventually, as Darwin stated, shell growth so stretches the old underlying cuticle that it breaks, but the new folded cuticle continues to accommodate the enlarging shell until the next moult occurs.

As the parietes grow from below, the new cuticle appears to move up the external surface of the shell, as on a conveyor belt, carrying the torn annular remnant representing the epidermis formed at the previous moult, together with the hirsute ridge, to occupy a position higher on each paries. These hirsute ridges can be seen at intervals up the shell, defining the occasion of a previous moult (Fig. 8).

An important difference between the typical arthropod and the barnacle results from the separation of the cuticle from the largely calcite shell, each apparently being laid down by different parts of the hypodermis. In normal arthropod cuticle, the hypodermal cells elongate to a columnar form with a wavy surface to accommodate further growth at the onset of ecdysis. They lay down first an epicuticle; then, after secretion of moulting fluid and resorption of the old integument, the exo- and endocuticle are formed beneath the epicuticle by the same cells (Wigglesworth, 1962).


It is implied by Bocquet-VCdrine (1964, 1965, 1966a) and Bubel (1975), that barnacles differ fundamentally in having specialised hypodermal cells for each function. Elongated cuticle-secreting cells are found in the basal suture, and variously modified hypodermal cells underlie the basis, the opercular membrane, and the shell plates. However, we know nothing of the origin of these modifications. Do the cuticle-secreting cells remain permanently lodged within the suture? If so, before the onset of each ecdysis, the increased areas of hypodermis must have been made good by a multiplication of basis-secreting and shell-secreting cells on either side of the cuticle-secreting cells. Alternatively, do all the cells slide along the basement membrane, occupying successively basis-secreting, epidermis- secreting and calcite-secreting positions and modifying their structure and function accordingly?

VIII. Shell Structure in Relation to Function

The thin laminae deposited along the inner surfaces of the shell of many species may be seen in radial sections (Fig. 9). These are the growth increments of Bourget and Crisp (1975b,c) which form at each tidal immersion. Darwin (1854) had observed these layers: “if now a section of one of the shelly zones of growth be carefully examined, it can in some cases be distinctly seen to be formed of successive, excessively fine laminae . . . ” They were noted also by Gutmann (1960) and Bassindale (1964), both of whom confused them with ecdysal marks on the outside of the shell and so wrongly associated them with ecdysis. The thickness of these laminae indicate where maximum deposition takes place; the regions of growth in balanids comprise the lower outer edge of the basis and lower parts of the paries, meeting at the basal suture, the downward protruding region of the sheath, the margins of the opercular plates, and the radii and alae (Darwin, 1854). These areas of enhanced shell deposition were also evident from autoradiograms obtained by Bourget and Crisp (1975b) after immersing living animals in 45Ca-treated sea water (Fig. lo). Younger individuals show a more general and intense pattern of deposition, but in older individuals deposition is more clearly concen- trated in the regions identified above. In most balanids the sheath is a separate entity, but in the chthamalids a paries is a single entity with very thin zones of deposition laid down parallel to the inside of the shell (Fig. 8A). The chthamalid shell, therefore, increases in total thickness towards the apex. Intermediate forms, such as Elminius spp., show reduced growth rates between two regions of deposition, one at the basal suture


cc -

osh +!

osu

gs gs

A B C D FIG. 9. Diagram of radial sections of shell plates from different species illustrating banding

and layering of shell: (A) one-layered type of shell (Chthamalus sp.); (B) two-layered type of shell (Balanus sp.); (C) change in shell banding of a very young barnacle showing the developing discontinuity of the bands and enlargement of the more basal increments; (D) section of Tetraclita squarnosa stalactifera (Lamarck), showing sublayered inner layer, Abbreviations: bs, base of sheath; cc, cuticular covering; d, discontinuity; gb, growth bands; gs, growing surface; il, inner layer; is, inner surface; is-I, inner sub-layer; mb, membranous base; 01, outer layer; osh, organic sheet; 0s-I, outer sub-layer; osu, outer surface; ps, primordial shell.

and the other at the base of a pseudosheath, the paries being a single element without discontinuity (Fig. 9C).

Patterns of deposition, however, become more complicated when a thickened calcareous base interlocks with the lower end of the paries at the basal suture. Both may have evolved a complex system of canals in which secondary calcite is sometimes laid down. In such species the basal and parietal hypodermis must meet on each side of the interlocking parts and lay down calcite crystals perpendicular to the plane of suture. If the base and paries are rudely separated these interlocks are often broken, suggesting that in some instances, where one member forms a neck into which the opposing member fits, dissolution of shell may have to accom- pany growth. Such complex interlocks greatly strengthen the shell (Mur- dock and Currey, 1978), especially if the joints merit the accolade of being “workmanlike. ”

If, at any point, there is a fold in the opposed sheets of hypodermal cells, the axes of the crystals formed by them will not lie parallel to each other but meet at a disjunction which is visible in the section of shell as a


FIG. 10. Autoradiograms of young (A) and older (B) specimens of B . bdanoides after immersion in sea water containing 45Ca. Abbreviations: bm, basal margin; op, opercular plate; os, outer surface of shell; sh, sheath; sp, shell plate (from Bourget and Crisp, 1975b, by courtesy of the Marine Biological Association).

discontinuity. The canals, separated by septa with their secondary teeth, are all formed by an infolding of hypodermis at the basal suture. The lines of teeth become gradually embedded in secondary deposition as they are moved up the shell by its growth from the base. Hence, higher up in the paries the inner wall becomes smoothed by secondary growth as the canals become embedded within it together with septa, teeth, and their lines of crystal discontinuity. These patterns, which can be seen in Fig. 1 1 A, were termed interlaminate figures by De Allessandri (1895) and were later studied exhaustively in many species by Cornwall (1956, 1958, 1959, 1960, 1962), Davadie (1963), Newman et al. (1967), and Bourget (1977). Some species with canals in the parietes (e.g., Tetraclita, B . perforatus, B . amphitrite) may also have complicated structures associated with sec-


FIG. 11. (A) Tranverse section near the apex of a shell plate of B . perforatus seen in polarised light (with crossed polars), showing filled canals and ovoid interlaminate figures (above); (B) fractured shell plate showing the ropelike organic fibers forming the tangential organic sheets of C. sfellatus (scale = 50 pm); (C) transverse bridges of organic material joining the ropelike fibers of the tangential organic sheets of C. stellatus (scale = 1 pn); (D) decalcified shell plate of T . squamosa stalactifera showing the concentric organic sheets present in the longitudinal canals (scale = 200 pm).

ondary deposition within the canals, so that often the upper portion of the canal forms a column of infilled shell material (Fig. 11A and D). Elminius simplex and Elminius plicatus (Epopella group-Foster, 1978) have calcareous pillars depending from the inner side of the paries in radial series. Their origin lies just below the first formed outermost layers of shell, and they become embedded in the later formed inner layers through which they pass. The vertical bundles of shell crystals constituting a pillar are sharply defined from the ordinary laminae and must therefore be formed by specialised cells of the hypodermis.


Within the calcareous laminae of most barnacles may also be found various arrangements of organic material in the form of plane sheets, sheets enveloping crystals, or, as in many chthamalids, large or small threads or twisted ropelike bundles of fibres (Fig. 11B and C). Bourget (1977) examined the layering and orientation of the crystals, classifying them into the different crystalline types. He depicted the arrangement of the organic sheets within the shell matrix and was able to relate shell microstructure to shell function and cirripede classification.

The microstructural features of the parietes are summarised for various taxa in Table 111. The table shows how these features are adapted to the mechanical function of the shell, for example, to resist the impact of floating objects, abrasion by particulate matter, attack by predators, competition by adjacent barnacles, crushing by grazers, or invasion by boring algae. The importance of biological factors was discussed by Palmer (1982). He provides evidence that easier access by predatory gastropods near the region of apposition of the parietes and at the margins of the opercular plates may account for the reduction in the number of plates and the development of thick external ribbing of the shell in some balanomorphs during evolution. Bourget (1977) suggested that the thin and highly orientated layer of crystals at the outer surface of the alae and radii might serve to give additional strength in the regions most exposed to attack by borers and to wear by abrasive particles. These suggestions call for experimental verification.

Shell characteristics likely to increase the strength and resistance of the shell are

1 . Increased thickness to give added strength 2. Organic layers surrounding the crystallites to increase flexibility and

strength by arresting the propagation of cracks (see Currey, 1964; Taylor and Layman, 1972; Murdock and Currey, 1978)

3. Laminated structures as in chthamalids, similarly increasing tough- ness and flexibility

4. Longitudinal canals which lighten the shell and, if surrounded by annuli of orientated fibrillar crystals or filled with columns of secondary calcite invested in organic matrix (Fig. l lD), give even greater strength than a solid block

Currey (1964) and Wainwright et al. (1976) show how hollow canals in bone structure can interrupt the spread of cracks; a similar function could be argued for the parietal canals in barnacle shell. The rather crude tests made by Barnes et al. (1970) and Murdock and Currey (1978) indicate that strength per unit weight of shell is relatively greater in the species with canals than in those with solid shells.

TABLE 111. SUMMARY OF OBSERVATIONS ON THE SHELL MICROSTRUCTURE OF SOME BARNACLESO ~~~~~~ ~ ~

Number of species Number

Taxon examined of layers Structure of the parietes Potential advantages for resisting damage

Verruca 1

Chthamalus 6

Balanus 9

1 Orientated microcrystals; plates heavily

1 corrugated

The parietes are stratified by alternate regions of thick organic sheets and fibrils and irregular prisms; Chthamalus rhizophorae (C. hembeli group) differ from those of the C . stellatus group in having a thin stratum of convergent fibrils on the outer surface of the shell, and a wedge-shaped region of elongated transparent prisms delimiting the pseudosheath from the outer region of the shell plate

Mainly composed of small disorientated crystals (granular structure and/or orientated microcrystals and prisms arranged in and around the interlaminate figures and sheath); the structure of the outer layer reflects the complexity of the shells; B . amphitrite and B . perforatus have filled canals

2

Corrugations may increase shell strength

Many Chthamalus species do not have thick shells but live in high-water, wave-beaten areas; the laminated structure may allow relative movement between layers and hold the shell intact after minor breakage

Discontinuities around and in interlaminate figures, hollow or filled canals could serve to stop the propagation of cracks; crystallites of the longitudinal septa separating the canals are well orientated; the zone of tangential orientation around each canal probably compensates for the loss of solid material inside it; canals secondarily filled with radially orientated crystals and organic sheets within a tangentially orientated cylinder are expected to be highly resistant; these columns of shell material are usually the last to disintegrate

Acasta

Pyrgoma

Elminius

Tetraclita

Chelonobia

1

2

1

4

2

2

2

2

Mainly granular, but also orientated

Mainly granular, but also orientated prisms

prisms as well as orientated microcrystals; the shell is made of one circular piece

Outer layer mainly granular but inner layer (sheath) with large prisms

Granular structure constitutes the basic structure of the parietes. Depending ridges of E . simplex and E . plicatus consist of crystallites arranged in long bundles, each bundle encased in an organic sheath; the bundles are secondarily associated in prisms invested in organic sheets; the shell contains a considerable amount of organic material

2

Pseudosheaths

2

2

Outer layer with small irregular disorientated crystals (granular structure), but longitudinal septa and inner laminae consist of orientated crystals packed into lamellar sheets; canals are secondarily filled with layers of large lamellar crystals tangentially arranged to the surface of the canals and separated by concentric organic sheets; some Terraclita have sublayered sheaths

(lamellae and fibrils) surrounded by small crystallites disorientated in C. testudinaria but convergent in Chelonobia patula; the sheath extends downwards to the base

Pillars of convergent crystallites

E. simplex has organic ribbons extending through the shell; E . plicatus, E. kingii have thick organic sheets as well as pillars of oriented crystals; this organic material might hold the shell intact after minor breakage, allowing relative movement of the shell laminae; specimens of E . plicatus with exposed organic layers on the outer surface are not uncommon and suggest a possible barrier against disintegration

Columns of shell material tangentially orientated to the sides of the canals presumably create a ply structure highly resistant to forces in all directions; these columns of radially orientated prisms are clearly visible as ridges on heavily eroded shells, indicating their resistance to erosion: boreholes are also less common in the orientated structures of the columns than in the matrix surrounding them

Bourget, 1977.


According to Bourget (1977), species with obviously strong, thick shells (e.g., Balanus balanus (L.), Balanus psittacus, Balanus amaryllis, and B . perforatus) are not necessarily those found at high water in wave- beaten habitats where physical damage is most likely to occur. Indeed, of the two genera found in such regions, Chthamalus and Tetraclita, only the latter has a strong and thick shell. However, Tetraclita spp. are found somewhat below the levels of Chthamalids in the tropics and are probably more likely to be attacked by large boring gastropods or by fish well adapted to chipping the coral. The chthamalids are often too high upshore to be vulnerable to marine predators. Another obviously weak-shelled form, E. modestus, is highly prolific (Crisp and Davies, 1955) and may thus compensate for losses due to mechanical damage, but Verucca stroemia would appear very vulnerable unless it has other means of defence. On balance, it seems probable that strong shells have been evolved as a defence against predators rather than against the elements. More refined measurements of barnacle shell strength and hardness in relation to its physical structure would repay further effort.

IX. Cyclical Factors in Growth

Shell growth in barnacles is usually measured as an increment over a given period of time, resulting from a series of influences, some endogenous, some exogenous. The factors that influence growth may act over a short or long term; they may operate only once or recur periodically. These will be considered and their magnitude assessed.

Growth has usually been measured in various species at defined sites or geographical areas or the effect of individual factors examined under given conditions. However, growth is a dynamic process, and if we could evaluate all the periodic and aperiodic influences, then a more compre- hensive picture could be put forward. Cyclical factors likely to influence growth at various periodicities are summarised in Fig. 12 for the well- studied species B. balanoides. The figure clearly shows that a given factor may influence growth at several periodicities, of which the chief are tidal and annual.

A . Tidal Influences

When shell growth at the edge of the barnacle B. balanoides, was measured very precisely (k l pm) at hourly intervals under a microscope, a stepwise deposition was found to take place (Fig. 13). The animals grew


moulting

reproduction

Q 6h j< 1 2 h j i 24h\< lwki< 2wki4 lmoj< 4mo/< l y r

-

FXOGENOUS FACTORS j

illumination

tidal regime

temperature

food

*- I

FIG. 12. Relative importance of cyclical factors likely to influence growth at various periodicities.

when in sea water but ceased soon after they became emersed. The periodicity of deposition was later traced within the shell structure as growth increments separated by darker bands in both B. balanoides (Bourget and Crisp, 197%) and E. modestus (Crisp and Richardson, 1975). By allowing these two species to grow for short periods in calcium-rich sea water, thereby forming thick increments as time marks, these workers were able to show that under tidal conditions each increment corresponded with a

Wet

f I I I I

6 12 18 24 30 Hours

FIG. 13. Hourly changes in the position of the growing edge of B . balanoides settled on a coverglass and viewed from below with a high-power oil-immersion objective (from Bourget and Crisp, 197513, by courtesy of the Marine Biological Association).


TABLE IV. EFFECT OF TIDAL LEVEL ON GROWTH RATE AND

GROWTH INCREMENT WIDTH I N B . balanoides AT MENAI BRIDGE, NORTH WALES

Number of Mean growth Mean increment Condition individuals rate (mm/day) width (pm)

~ ~ ~

Raft 5 0.0602 31.24 LWN 3 0.0400 22.46 HWN 3 0.0243 13.33

semidiurnal period of tidal immersion. The width of the increments was directly correlated with the duration of immersion. Moreover, when shells from different tidal conditions were compared, those immersed continuously formed diffuse bands of circa-tidal frequency, whereas those immersed intertidally all gave distinct bands of precisely tidal frequency. The banding was much more distinct in animals from higher tidal levels, despite the fact that the increments were narrower (Table IV). Sometimes, in barnacles living at or above the level of high water of neap tides, fewer than the theoretical number of bands were laid down because they were not always immersed. Some individuals at this level were marked and followed during 23 successive tidal periods. These were found to have certain bands missing and replaced by a darker “stress” band, notably when an unduly long period of emersion was associated with long insolation and high air temperature. Thus, shell deposition may temporarily cease during periods of heat stress (Bourget and Crisp, 1975~). Reduced growth at high tide level is evident from Tables I and 11, pp. 212, 214.

B. Daily Influences

We have already noted the suggestion by Klugh and Newcombe (1935) that direct sunlight reduced growth in B . balanoides. Barnes (1953) and Crisp and Pate1 (1960) showed that light did not influence growth, and any reduced growth observed in illuminated conditions probably resulted from interference by algae. Costlow and Bookhout (1956) measured growth every 24 h in “B. amphitrite niveus” [B. amphitrite amphitrite, actually (Ed.)] kept in the laboratory. They obtained faster growth in darkness. This question was further examined by Bourget and Crisp (1975b) by measuring very precisely the basal diameter of a group of newly metamorphosed B . balanoides kept under a 12-h light/l2-h dark regime. They were unable to show any significant effect of illumination on


growth in the laboratory. Possibly Costlow and Bookhout’s results may have resulted from a nightly carbon dioxide accumulation in the algal culture, which could stimulate cirral activity (Southward and Crisp, 1965). On the other hand, Trump and Bourget (1980), in reexamining the results of Bourget and Crisp (1975b), found slightly greater increments during daytime than at night. They suggested that in uncontrolled field situations sea surface and air temperatures would probably have been higher during the day and so increased the rate of feeding and growth. No influence on the regular production of tidal bands in the laboratory could be detected when the light regime was modified. Animals kept either under continuous illumination or in alternating 12-h lighti12-h dark periods, as well as animals kept since metamorphosis in a light-tight box in the field, continued to produce the usual two equal increments per day. Thus, any effect that light might have over a 24-h periodicity must be very small. However, where the tidal regime has a strong diurnal component, it might impose a daily (23.8 h) rhythm of growth, as was found by Evans (1972) in the cockle Clinocardiurn nuttalli growing on the Pacific Coast of the USA.

C . Other Lunar Influences

Since the thickness of the tidal growth increment is correlated with the duration of tidal immersion, it follows that differences in the semidiurnal growth increment should be observed between the spring and neap periods of the lunar cycle (14 days), as Bourget and Crisp (197%) have shown. Similarly, the smaller differences in the new and full moon cycle (28 days) and the semiannual solar-lunar effect must also be present, although probably too small to be detected.

D. Annual injhences

The tidal cycles of growth, other than semidiurnal, might not be easily separated from the seasonal cycle of growth which, for example in B. balanoides, is annual and characterised by a maximum in the spring, a reduction during summer, possibly a rise in autumn, and a virtual cessa- tion during winter (Hatton and Fischer-Piette, 1932; Moore, 1934; Hatton, 1938; Barnes and Barnes, 1959a,b; Barnes, 1961, 1962; Ritz and Crisp, 1970). The annual cycle of growth is clearly evident in shell sections from the much thinner bands laid down during winter. In some species the annual cycle is also evident from discontinuities on the outer form of the shell (e.g., B. porcatus = B. balanus, Crisp, 1954; B . balanoides, Bourget, 1980).


E. Other Cyclic Influences

The moulting cycle, at least in B . balanoides, will impose a further, but somewhat irregular, periodicity, since growth is maximal in the immedi- ate postmoult period. The moulting frequency is itself increased by greater feeding and growth of the animal (Crisp and Patel, 1960), although the animal continues to moult even when not growing (Crisp and Patel, 1958), possibly to remove small organisms that settle and grow on the cuticle.

Breeding, which competes with growth for resources (Crisp and Patel, 1961), is likely to have quite different effects on high-latitude species which breed once a year than on those which liberate broods continuously over the breeding season or those from low latitudes which breed continuously.

F. Frequency, Scale, and Precision of Measurement

From Fig. 12, which illustrates the periodic factors influencing barnacle growth, it can be seen how some factors, notably immersion and emersion, are effective at several periodicities. The most important factors influence growth over 12-h tidal and yearly cycles. Most growth studies have been carried out using weekly or monthly measurements, and at precisions of approximately 1 mm. These time scales are too short to register annual effects and too long to register tidal changes. The precision of most measurements would also preclude any possibility of observ- ing increases at tidal intervals.

Since each successive growth band width is a short-term and accurate method of recording growth rate, Trump and Bourget (1980) suggested the use of these patterns to separate the influence of the various periodic and aperiodic effects by time-series analysis. Sufficiently long-term records were not available, but the technique was applied to an artifically created series of band widths and immersion periods, so that after filtering out the shorter term periodicities, it should be possible to isolate and describe long-term variations in growth rates, such as the annual cycle, the moulting cycle or the reproductive cycle, and to isolate and describe residual aperiodic events, such as unique periods of high or low temperature, spills of pollutants, or eutrophic algal blooms. By the development of such methods, the information locked within the shells of barnacles and other organisms such as corals, bivalves, gastropods and chitons, not forgetting fossil shells, could be of great practical and academic importance.


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