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Shell growth in some New Zealand cymathdae (Gastropoda: Prosobranchia)
J. exp. mar. Biol. Ecoi., 1970, Vol. 4, pp. 250-260; North-Holland
Publishing Company, Amsterdam
SHELL GROWTH IN SOME NEW ZEALAND CYMATIIDAE (GASTROPODA : pRoso~RANcHhi) J. H. LAXTON r Department
of Zoology,
University
of Auckland,
Auckland,
New Zealand
Abstract: The growth pattern of some New Zealand Cymatiidae is described and the growth rate of marked individuals of two populations of Cabestana spengleri (Perry) calculated by plotting the increase in length on recapture one year later against the initial length on tagging. Juveniles of the Mill Bay population reached 50-70 mm in length in their first year and grew a further 1S-40 mm in their second year. In their third year some individuals of this population increased in length by another 20-30 mm to reach the maximum adult size for the Mill Bay area. At Ahipara juveniles reached 17-35 mm in length in their first year after hatching and grew a further 5-35 mm by the end of their second year. Some individuals grew another 10-l 5 mm in their third year to reach the maximum size recorded at Ahipara.
The molluscan shell is formed by the advancing mantle edge. By an increased or decreased rate of shell deposition at various points around the circumference of the mantle, different shell types are formed. The deposition of calcareous material may be regular throughout the life span producing a shell without any marked lines or evidence of discontinuous growth, or irregular, giving shells with marked growth lines. Both types of growth are found in the Gastropoda. In temperate or cold water gastropods the irregularities of shell secretion may be seasonal, the lines corresponding to retarded growth during the winter. In some other gastropods shell lines are formed after each small increase in size irrespective of season, and this would appear to be the most common type of gastropod growth. The extreme examples of this type of discontinuous growth are found in the families which form varices after each growth period. Members of the Cymatiidae and probably the Bursidae and Muricidae may add up to three-quarters of a whorl to their shells in a few weeks, after which a flared lip is produced. These lips persist in the shells as varices. In the Cymatiidae this period of rapid growth may be followed by a dormant period which may last for several years or by the addition of another half whorl to the shell. The purpose of this work was to compare the growth patterns in Mayena australasia (Perry), Monoplex australasiae Perry, and Charonia species and to determine the growth rate of marked individuals of Cabestana spengleri (Perry) under different environmental conditions. ’ Present Address: Department
of Zoology, University of Queensland, 250
Brisbane, Australia.
SHELL GROWTH IN CYMATIIDAE
251
MATERIALS AND METHODS
The cymatiids examined were collected both intertidally and sublittorally in the North Auckland region and maintained in fresh circulated sea water in the laboratory. Growth rates were estimated in natural and laboratory populations of C. spengleri by the release and recovery of marked individuals. The animals were tagged with small numbered plastic discs. Two holes were drilled (l/16 in. in diameter) in the outer lip in the region of the exhalant siphon. The tag was tied on with mono-~lament nylon. Pearly nacre was soon secreted over the nylon on the inside of the shell preventing irritation and at the same time holding the tag firmly in place. The growth curves of individuals during a half whorl addition to the shell were determined in the laboratory. At weekly intervals the length, breadth, weight, and -
_
I
PARENGARENGA
I
N
Fig. 1. Map of North Auckland showing the areas investigated.
252
J. H. LAXTON
angular increment of shell added (measured about the inhalant siphon) were measured. Care was taken to drain the water out as for as possible before the animals were weighed: slight fluctuations in the weight inurements in successive weeks were caused by water in the mantle cavity at the time of weighing. Two localities were chosen for the growth rate experiments representing two widely different ecological situations each with large populations of C. spengleri. The first, Mill Bay, lies in the relatively sheltered Manukau Harbour on the west coast of Auckland (Fig. l), where the C. speng~eri population lives on silty ascidiancovered rocks at low tide. The ascidian M&ocosmus kura Brewin, covered 50-60 % of the rock surface at low tide and was the major food of Cabestana spengleri in this area. At Ahipara, on the exposed west coast, C. spengieri was confined to a narrow band sandwiched between the barnacle zone (Chamaesipho brunnea (Moore)) and the mussel zone (Perna cana~~cu~us(Gmelin)). This region was covered by patches of an unidentified ascidian upon whr:h Cabestana speng~eri feeds. At this locality the food was far less abundant compared with the apparently super-abundant food supply at Mill Bay.
RESULTS GENERAL GROWTH PATTERN IN THE CYMATIIDAE
Three growth patterns were found among the New Zealand Cymatiidae typified by the genera Mayena, Cabestana, and Monoplex. Mayena australasia The first varix in Mayena australasia is formed about half a whorl from the protoconch and subsequent varices occurred at half whorl intervals. An adult Mayena austrai~ia may have up to fourteen variees. At the onset of growth a thin flexible layer of organic material, the periostracum, grows out from the lip, beginning at the centre. On the inside of this velvety periostracum calcareous material is deposited, conferring some rigidity to the growing edge. Organic and calcareous material is laid down quickly forming a complete half-whorl before the growing edge turns outwards to form a new hp. At this stage the new shell is still flexible. After the new half-whorl has been completely moulded into its final shape and the new si~hona1 canal constructed, final calcification begins. The initial form of the shell took onIy a month to complete but calcification may take several months. A half-whorl was added twice in one year in some individuals. Charonia capax Finlay, C. rubicunda (Perry); Annaparenna oerrucosa (Sowerby); Austrosassia parkinson~a (Perry); Argobuccjnu~n rane~i~rmis tumidum (Dunker); Fusitrition /audandum Finlay, and RaneIla olearium (L,) are cymatiid species found in New Zealand waters which exhibit a similar growth pattern.
SHELL
GROWTH
253
IN CYMATIIDAE
Cabestana spengleri The first varix
of Cabestana spengleri is formed
either
two, three,
four
or five
whorls from the protoconch, depending on the amount of food available during the initial stages of growth, and subsequent varices occur at half-whorl intervals. Addition of new shell follows the same pattern
described
for Mayena australasia. Cabestana
waterhougei segregata Powell has a similar growth pattern to C. spengleri. The mantle edge of juvenile C. spengleri is drawn out into a row of very fine projections which are responsible for secretion of the periostracum at the growing edge of the shell. Raised ridges of this horny material are formed during each temporary halt to growth prior to the formation of the first varix. These ridges are comparable with the horny fringes of the periostracum of Monoplex australasiae. Monoplex australasiae The growth pattern of Monoplex australasiae is different from that of either Mayena australasia or Cabestana spengleri. The first varix is laid down three, four or five whorls from the protoconch, probably depending on the conditions in which the animals live. Each cessation of growth is marked by the production of horny fringes of periostracum which are secreted by the pallial tentacles, the spacing between fringes being indicative of the growth rate. Short distances indicated a slow rate, while longer distances denoted rapid growth. Monoplex australasiae grows either immediately after the deposition of a fringe or stops growing. If growth is halted a major fringe is formed and a new lip secreted which becomes the labial varix. Heavy calcification of the shell does not occur until after the first varix has been formed. Further growth usually begins slowly, fringes being formed every few mm. After about quarter of a whorl has been added there is a sudden increase in the deposition rate which ends with the formation of a major fringe and a heavy lip. Cabestanimorpha exarata (Reeve) is another species with pallial tentacles a growth pattern similar to Monoplex australasiae.
which has
GROWTH CURVES OF INDIVIDUALS DURING THE GROWING PERIOD
Before a complete growth curve from juvenile to adult can be constructed the rate of growth during each half-whorl addition to the shell and the interval between such additions had to be measured. Figs 2, 3A, B show the growth rate during a half-whorl addition to the shell for Cabestana spengleri, Mayena australasia, and Monoplex australasiae. The curves for Cabestana spengleri and Mayena australasia were similar in shape while those of Monoplex australasiae proceeded in a series of steps, each plateau of the growth curve corresponding to a temporary halt to growth while a horny fringe was secreted.
Cobestana
spergleri / .--e-.-.-.-.-*-.--C.-
180
140 l
60
20
1
2
3
4
6
5
7
8
9
10
11
12
13
14
15
16 17
18
Weeks Fig. 2. Growth curve of Cubeslana spengleri during the addition of one half-whorl showing the increase in shell length, breadth (measured across the aperture), weight, and the angle of the shell added (measured about the inhalant siphon).
.- 160
2
4
6
8
x)
12
Weeks B
Mmoplex
austrolasiae.
+ 30--
2
4
6
8
10
12
60
14
Weeks Fig. 3. Growth
of a half-whorl
curves of Mayena australusiu (A) and Monoplex australasiae (B) during the addition showing the increase in shell length, breadth, weight and the angle of shell added.
SHELL
Growth rates of Cabestana
GROWTH
255
IN CYMATIIDAE
spengleri
The cymatiid habit of secreting a varix at the end of each growth period suggests that varices may be used to estimate the age of these molluscs and hence the growth rate, in the same way that the winter rings were used by Hancock (1965) for the bivalve Cardium edule. The secretion of a varix had long been considered an annual phenomenon
by some conchologists.
Mackenzie
(1960) has shown,
however,
that
this is not the case in Eupleura caudata (Muricidae). Vat-ix production in the New Zealand cymatiids studied differed widely from genus to genus as well as between individuals of the same species living in the same area. For example, in the population of Cabestana spengleri living at Mill Bay, some individuals grew up to four varices in one year, while others remained over two years without adding another varix. Application of the Ford-Walford and Manzer-Taylor plots for the estimation of growth parameters (Hancock, 1965) in C. spengleri led to certain difficulties. The most serious was the error incurred by using data drawn from a limited range of ages and the use of the length increment during the first year of life. Since C. spengleri reached its full adult size in three years it was impossible to overcome these difficulties. Thus for the Mill Bay and Ahipara populations the increase in length over a one year period of each marked individual (tagged during the breeding season of November 1966) was plotted against its initial length when tagged. Juveniles which hatched from
Cabestana spenqicri - Mill Bay
o juveniles measured 1 year after hatching
.
. ..
0
10 20
30405060
70
.
.
l
80901001lO120130140150
Initial Length (mm). Fig. 4. Increase
in length
on recapture against
after one year for Cabesrana the initial length on tagging.
spengleri from
Mill Bay plotted
J. H. LAXTON
256
Cabestana
2
535
.-:
5 -0 C-30 zx ;25
.. .. . -a :.. *.
u 920 5 F El5
spengleri - Ahipara
.
1year after hatching. .
. . .
. .
. .
. . ... : .-
-:’ :. . -
..
.
.* .. .
.
$ -10 .s ?: t85
* - juveniles measured
.
-
.
-
. ,
, 0
10
20
..I..
. ..
.
l **
.
-c
em
. .
30 Initial
..*....%I 40
. 50
.I
60
.
.
.
I
70
.
. 4
60
length (mm).
Fig. 5. Increase in length on recapture after one year for Cabestana spengleri from Ahipara plotted against their initial length on tagging.
egg capsules laid in November 1966 were marked with red nail varnish as soon as they appeared on the shore and remeasured in November 1967. This gave the growth rate during the first year of life for individuals of both populations. These juvenile one-year olds were then tagged in November 1967, liberated again, and remeasured the following year along with the animals originally tagged in November 1966. All the tagged animals plus juveniles from the 1967 breeding season were remeasured in November 1968 giving information over a three year period. No difference in growth rate was found between the sexes or from year to year in animals of the same age so the results were combined to give Figs 4 and 5.
Age and growth in Cabestana
spengleri.
According to Haskin (1954) the methods of age determination in molluscs employed to date may be grouped into three categories: 1) size frequency studies; 2) the interpretation of growth interruption lines on shells or other parts of the animal; 3) experiments involving the release and recapture of marked individuals. In cymatiids the size frequency method showed no segregation into distinct age classes, but a first year class could be recognized by inspection in C. spengleri. At
SHELL
Mill Bay the juveniles
GROWTH
first became
25-l
IN CYMATHDAE
noticeable
on the shore in February
and March
when they had reached 20-30 mm in length, some 334 months after the breeding period. These small animals were marked with nail varnish, measured after one year and tagged in the manner
already
outlined.
They grew rapidly
in their first year and
some reached 70 mm in length with a class average of 55 mm. Between one and four varices were laid down during this period. Animals from this locality which were tagged at an initial length of 5&60 mm in November grew to 110-120 mm in the course of a year and added another two or three varices to their shells (Fig. 6).
Fig. 6. Growth in Cubestuna splengleri from Mill Bay: note the tags which are partly buried in the shell sometimes with only the monofilament nylon still showing. These three animals were tagged at the age of one year and recaptured a year later; three varices have been added in the centre animal and two in the others since they were tagged.
The number of varices laid down in the first year depended on the number of whorls grown before a major interruption caused the first varix to be formed. An annual increment of 50-60 mm for the first two years produced animals which, if they were to grow another half-whorl the following year, would reach 140 mm. This is close to the maximum size recorded for C. spengleri at Mill Bay. A large proportion of the tagged population at Mill Bay ranging from 80-140 mm, however, failed to grow at all during the two-year period of observation. The majority of these animals were between 90-120 mm in length and potentially able to add a further half-whorl to their shells. This lack of growth could not be explained by a food shortage since they were living in an area where ascidians covered 4&60 % of the rock surface. Moore (1936) showed that growth in Purpura lapillus ceased at the onset of sexual maturity. This was definitely not the case in Cabestana spengleri since individuals which have been observed copulating and egg-laying during the breeding
258
J. H. LAXTON
season later commenced
growing.
It appeared
that growth stopped earlier in some indi-
viduals than in others, although reproductive ability was not affected. In C. spengleri sexual maturity of the males was reached in the first year. They have been observed copulating at this age. It is not known whether the females also reached maturity in the first year. The Ahipara population showed an annual increment of 28 mm in the first year and a further
20 mm in the second year. On the basis of this study it appeares
that
C. spengleri takes three years to reach its maximum size under ideal food conditions. The growth curves for individuals of C. spengleri from Mill Bay are shown in Fig. 7 indicating that aging by varix counts was impossible. Aging by counting opercular rings (Kubo, 1953) was also of little value in C. spengleri.
120
Cabestana
spengleri
-
80
0
2
4
6
8
10
12
14
16
18
20
Time (months)
Fig. 7. Age-growth curves of Cubestana spengleri from Mill Bay. A, Individual with four whorls before the first varix. B, Individual with five whorls before the first varix. C, Individual with three whorls before the first varix (v = varix). The curves were constructed as follows. Each curve represents a single tagged animal living unconfined on the shore. The points on each curve show the amount of shell growth that had occurred prior to the animal’s recapture. The shape of the growth curve between each observation of an animal could be deduced from knowledge obtained from other animals living in the same area that the addition of a half-whorl from one varix to the next took a month to complete. Once the particular half-whorl was complete there was no further increase in length until calcification was finished giving the ‘stepped’ growth curve.
SHELL GROWTH IN CYMATIIDAE
259
DISCUSSION The type of discontinuous growth characteristic of cymatiids has not previously been described for molluscs. This type of growth may also be found in other gastropod families
in which
varices
are produced,
such as some muricids
and the Bursidae,
although Gostan (1966) has shown that the rate of shell growthin the rissoid, Rissoa parva, is uninterrupted during the formation of ribs and varices. The fact that R. parva is annual and that muricids, bursids, and cymatiids are long lived may give rise to some difference in growth pattern. The shells of adult Cabestana spengleri with up to seven or eight varices have marked shell shape variations depending on the number of whorls before the first varix (Laxton, 1968). The amount of food available has been shown to influence the growth in the initial stages, and may explain why interruptions occur in rapidly growing individuals. At Mill Bay some animals may grow up to 70 mm in their first year and produce only one varix, while others may reach the same size in the same period but produce either two, three, or four varices. Since the annual increment is the same in both cases one group of animals must have grown continuously while the other suffered interruption. The reason for this difference may be that shell growth exceeds tissue growth, so that periodic halts occur while balance is restored, and during this time a varix is laid down. Since there is a volume increase of about 75 % with every half-whorl added to the shell (Laxton, 1968) tissue growth must be very rapid to keep up with this increase. In continuously growing animals this requires a constant supply of food. The only other alternative in areas where food is less abundant is for growth in stages, each terminated by the formation of a varix. The number of varices, and the size of the first year animals reflects the food conditions of an area. This view is supported by the observation that juveniles with only three whorls before the first varix are found highest on the shore where their ascidian food is scarce. Young C. spengleri found lower on the shore among the densest ascidians grow continuously for five whorls before a varix is secreted. It must be remembered, however, that for C. spengleri it is the food supply prior to the formation of the first varix which has the greatest influence on the ultimate adult shell shape since subsequent varices are invariably formed at half whorl intervals. As the animal grows its power of locomotion increases and it is able to migrate to regions where food is more abundant. When rapidly growing animals are removed from areas of abundant food to regions where it is scarce they continue to complete the half-whorl in the process of secretion but do not add any further half-whorls to their shells. Contemporary animals left in areas where food is abundant continue adding to their shells. This confirms the supposition that rapid growth during the first year requires a super-abundant food supply. Growth in later years, however, is slower and when shell is being added the animals conceal themselves and fast so preventing damaging the new growth. A comparison of the growth rates of the Mill Bay and Ahipara populations of C. spengferi poses an interesting problem. While animals from both populations reach the maximum size recorded for the respective areas in three years, the actual amount
260
J. H. LAXTON
of shell growth for the Mill Bay animals is about twice that of the Ahipara animals for the same period. While the growth rate in terms of reaching maturity is the same in both groups, the rate of increase in biomass of the Ahipara population is half that of the Mill Bay population. This difference is important from the point of view of productivity and the energy required to reach adult size. The ability of the Ahipara population to reach sexual maturity at a smaller size may be an adaptation to the environment of the area. In this region the ascidian food is scarce and very restricted in its vertical distribution. If this food source is to be used efficiently by a large number of individuals sexual maturity will have to be reached at a smaller size. Where food is unlimited and widespread as at Mill Bay, sexual maturity is attained at a greater size and growth may continue after it has been reached. This suggestion is consistent with other populations investigated. Breeding individuals are between 60-70 mm long at Urquhart’s Bay, Whangarei Heads, where food covers less than 2 ‘A of the rock surface at low tide. C. spengleri takes approximately three years to reach its maximum size and judging from the number of tagged animals in the Mill Bay population which did not grow during the two-year observation period, the age of some of the larger individuals must be at least 5 years. The question of longevity can only be satisfactorily answered by continued observation of the marked animals. 14 of the 1’71initially tagged animals were known to have died during the period and the shells of a small number of newly dead unmarked animals were found during the same period, Most of the shells were of fully grown adults. Nothing is known of the mortality between the time they appear on the shore and the age of one year. Only one animal within this age group was found dead. Larval mortality must be very high since each egg capsule contains at least one thousand embryos and one female may lay up to two hundred capsules a season. ACKNOWLEDGEMENTS
I wish to thank Professor J. E. Morton for help and guidance during this study. I am grateful for the use of the facilities of the Leigh Marine Research Laboratory and wish to acknowledge the valuable suggestions and comments of Dr. W. J. Ballantine. REFERENCES
GO~TAN, G., 1966. Aspects cyclique de la morphogenhe de la coquille de Rissoa parva da Costa (Gastropode Prosobranche). Vie ~il~ei~, T 17. pp. 9-86. HANCOCK,D. A., 1965. Graphical estimation of growth parameters. J. Cons. perm. int. Explor. h&r, Vol. 29, pp. 340-351. HASKIN, H. H., 1954. Age determination in molluscs. Trans. N.Y. Acad. Sci., Vol. 16, pp. 300-304. KUBO, I., 1953. Age determination of Babylonica japonica (Reeve) an edible marine gastropod, basing on the operculum. J. Tokyo Univ. Fish., Vol. 34, p. 199. LAXTON,J. H., 1968. The anatomy, feeding, growth and reproduction of some New Zealand cymatiids M. SC. Thesis, University of Auckiand, N.Z., 104 pp. MACKENZIE,C., 1960. Interpretation of varices and growth ridges of EupIeura caudato. Ecology, Vol. 41, pp. 783-784. MOORE, H. B., 1936. The biology of Purpuru Zapillus. 1. Shell variation in relation to environment. J. mar. biol. Ass. U.K., Vol. 21, pp. 61-86.
Publishing Company, Amsterdam
SHELL GROWTH IN SOME NEW ZEALAND CYMATIIDAE (GASTROPODA : pRoso~RANcHhi) J. H. LAXTON r Department
of Zoology,
University
of Auckland,
Auckland,
New Zealand
Abstract: The growth pattern of some New Zealand Cymatiidae is described and the growth rate of marked individuals of two populations of Cabestana spengleri (Perry) calculated by plotting the increase in length on recapture one year later against the initial length on tagging. Juveniles of the Mill Bay population reached 50-70 mm in length in their first year and grew a further 1S-40 mm in their second year. In their third year some individuals of this population increased in length by another 20-30 mm to reach the maximum adult size for the Mill Bay area. At Ahipara juveniles reached 17-35 mm in length in their first year after hatching and grew a further 5-35 mm by the end of their second year. Some individuals grew another 10-l 5 mm in their third year to reach the maximum size recorded at Ahipara.
The molluscan shell is formed by the advancing mantle edge. By an increased or decreased rate of shell deposition at various points around the circumference of the mantle, different shell types are formed. The deposition of calcareous material may be regular throughout the life span producing a shell without any marked lines or evidence of discontinuous growth, or irregular, giving shells with marked growth lines. Both types of growth are found in the Gastropoda. In temperate or cold water gastropods the irregularities of shell secretion may be seasonal, the lines corresponding to retarded growth during the winter. In some other gastropods shell lines are formed after each small increase in size irrespective of season, and this would appear to be the most common type of gastropod growth. The extreme examples of this type of discontinuous growth are found in the families which form varices after each growth period. Members of the Cymatiidae and probably the Bursidae and Muricidae may add up to three-quarters of a whorl to their shells in a few weeks, after which a flared lip is produced. These lips persist in the shells as varices. In the Cymatiidae this period of rapid growth may be followed by a dormant period which may last for several years or by the addition of another half whorl to the shell. The purpose of this work was to compare the growth patterns in Mayena australasia (Perry), Monoplex australasiae Perry, and Charonia species and to determine the growth rate of marked individuals of Cabestana spengleri (Perry) under different environmental conditions. ’ Present Address: Department
of Zoology, University of Queensland, 250
Brisbane, Australia.
SHELL GROWTH IN CYMATIIDAE
251
MATERIALS AND METHODS
The cymatiids examined were collected both intertidally and sublittorally in the North Auckland region and maintained in fresh circulated sea water in the laboratory. Growth rates were estimated in natural and laboratory populations of C. spengleri by the release and recovery of marked individuals. The animals were tagged with small numbered plastic discs. Two holes were drilled (l/16 in. in diameter) in the outer lip in the region of the exhalant siphon. The tag was tied on with mono-~lament nylon. Pearly nacre was soon secreted over the nylon on the inside of the shell preventing irritation and at the same time holding the tag firmly in place. The growth curves of individuals during a half whorl addition to the shell were determined in the laboratory. At weekly intervals the length, breadth, weight, and -
_
I
PARENGARENGA
I
N
Fig. 1. Map of North Auckland showing the areas investigated.
252
J. H. LAXTON
angular increment of shell added (measured about the inhalant siphon) were measured. Care was taken to drain the water out as for as possible before the animals were weighed: slight fluctuations in the weight inurements in successive weeks were caused by water in the mantle cavity at the time of weighing. Two localities were chosen for the growth rate experiments representing two widely different ecological situations each with large populations of C. spengleri. The first, Mill Bay, lies in the relatively sheltered Manukau Harbour on the west coast of Auckland (Fig. l), where the C. speng~eri population lives on silty ascidiancovered rocks at low tide. The ascidian M&ocosmus kura Brewin, covered 50-60 % of the rock surface at low tide and was the major food of Cabestana spengleri in this area. At Ahipara, on the exposed west coast, C. spengieri was confined to a narrow band sandwiched between the barnacle zone (Chamaesipho brunnea (Moore)) and the mussel zone (Perna cana~~cu~us(Gmelin)). This region was covered by patches of an unidentified ascidian upon whr:h Cabestana speng~eri feeds. At this locality the food was far less abundant compared with the apparently super-abundant food supply at Mill Bay.
RESULTS GENERAL GROWTH PATTERN IN THE CYMATIIDAE
Three growth patterns were found among the New Zealand Cymatiidae typified by the genera Mayena, Cabestana, and Monoplex. Mayena australasia The first varix in Mayena australasia is formed about half a whorl from the protoconch and subsequent varices occurred at half whorl intervals. An adult Mayena austrai~ia may have up to fourteen variees. At the onset of growth a thin flexible layer of organic material, the periostracum, grows out from the lip, beginning at the centre. On the inside of this velvety periostracum calcareous material is deposited, conferring some rigidity to the growing edge. Organic and calcareous material is laid down quickly forming a complete half-whorl before the growing edge turns outwards to form a new hp. At this stage the new shell is still flexible. After the new half-whorl has been completely moulded into its final shape and the new si~hona1 canal constructed, final calcification begins. The initial form of the shell took onIy a month to complete but calcification may take several months. A half-whorl was added twice in one year in some individuals. Charonia capax Finlay, C. rubicunda (Perry); Annaparenna oerrucosa (Sowerby); Austrosassia parkinson~a (Perry); Argobuccjnu~n rane~i~rmis tumidum (Dunker); Fusitrition /audandum Finlay, and RaneIla olearium (L,) are cymatiid species found in New Zealand waters which exhibit a similar growth pattern.
SHELL
GROWTH
253
IN CYMATIIDAE
Cabestana spengleri The first varix
of Cabestana spengleri is formed
either
two, three,
four
or five
whorls from the protoconch, depending on the amount of food available during the initial stages of growth, and subsequent varices occur at half-whorl intervals. Addition of new shell follows the same pattern
described
for Mayena australasia. Cabestana
waterhougei segregata Powell has a similar growth pattern to C. spengleri. The mantle edge of juvenile C. spengleri is drawn out into a row of very fine projections which are responsible for secretion of the periostracum at the growing edge of the shell. Raised ridges of this horny material are formed during each temporary halt to growth prior to the formation of the first varix. These ridges are comparable with the horny fringes of the periostracum of Monoplex australasiae. Monoplex australasiae The growth pattern of Monoplex australasiae is different from that of either Mayena australasia or Cabestana spengleri. The first varix is laid down three, four or five whorls from the protoconch, probably depending on the conditions in which the animals live. Each cessation of growth is marked by the production of horny fringes of periostracum which are secreted by the pallial tentacles, the spacing between fringes being indicative of the growth rate. Short distances indicated a slow rate, while longer distances denoted rapid growth. Monoplex australasiae grows either immediately after the deposition of a fringe or stops growing. If growth is halted a major fringe is formed and a new lip secreted which becomes the labial varix. Heavy calcification of the shell does not occur until after the first varix has been formed. Further growth usually begins slowly, fringes being formed every few mm. After about quarter of a whorl has been added there is a sudden increase in the deposition rate which ends with the formation of a major fringe and a heavy lip. Cabestanimorpha exarata (Reeve) is another species with pallial tentacles a growth pattern similar to Monoplex australasiae.
which has
GROWTH CURVES OF INDIVIDUALS DURING THE GROWING PERIOD
Before a complete growth curve from juvenile to adult can be constructed the rate of growth during each half-whorl addition to the shell and the interval between such additions had to be measured. Figs 2, 3A, B show the growth rate during a half-whorl addition to the shell for Cabestana spengleri, Mayena australasia, and Monoplex australasiae. The curves for Cabestana spengleri and Mayena australasia were similar in shape while those of Monoplex australasiae proceeded in a series of steps, each plateau of the growth curve corresponding to a temporary halt to growth while a horny fringe was secreted.
Cobestana
spergleri / .--e-.-.-.-.-*-.--C.-
180
140 l
60
20
1
2
3
4
6
5
7
8
9
10
11
12
13
14
15
16 17
18
Weeks Fig. 2. Growth curve of Cubeslana spengleri during the addition of one half-whorl showing the increase in shell length, breadth (measured across the aperture), weight, and the angle of the shell added (measured about the inhalant siphon).
.- 160
2
4
6
8
x)
12
Weeks B
Mmoplex
austrolasiae.
+ 30--
2
4
6
8
10
12
60
14
Weeks Fig. 3. Growth
of a half-whorl
curves of Mayena australusiu (A) and Monoplex australasiae (B) during the addition showing the increase in shell length, breadth, weight and the angle of shell added.
SHELL
Growth rates of Cabestana
GROWTH
255
IN CYMATIIDAE
spengleri
The cymatiid habit of secreting a varix at the end of each growth period suggests that varices may be used to estimate the age of these molluscs and hence the growth rate, in the same way that the winter rings were used by Hancock (1965) for the bivalve Cardium edule. The secretion of a varix had long been considered an annual phenomenon
by some conchologists.
Mackenzie
(1960) has shown,
however,
that
this is not the case in Eupleura caudata (Muricidae). Vat-ix production in the New Zealand cymatiids studied differed widely from genus to genus as well as between individuals of the same species living in the same area. For example, in the population of Cabestana spengleri living at Mill Bay, some individuals grew up to four varices in one year, while others remained over two years without adding another varix. Application of the Ford-Walford and Manzer-Taylor plots for the estimation of growth parameters (Hancock, 1965) in C. spengleri led to certain difficulties. The most serious was the error incurred by using data drawn from a limited range of ages and the use of the length increment during the first year of life. Since C. spengleri reached its full adult size in three years it was impossible to overcome these difficulties. Thus for the Mill Bay and Ahipara populations the increase in length over a one year period of each marked individual (tagged during the breeding season of November 1966) was plotted against its initial length when tagged. Juveniles which hatched from
Cabestana spenqicri - Mill Bay
o juveniles measured 1 year after hatching
.
. ..
0
10 20
30405060
70
.
.
l
80901001lO120130140150
Initial Length (mm). Fig. 4. Increase
in length
on recapture against
after one year for Cabesrana the initial length on tagging.
spengleri from
Mill Bay plotted
J. H. LAXTON
256
Cabestana
2
535
.-:
5 -0 C-30 zx ;25
.. .. . -a :.. *.
u 920 5 F El5
spengleri - Ahipara
.
1year after hatching. .
. . .
. .
. .
. . ... : .-
-:’ :. . -
..
.
.* .. .
.
$ -10 .s ?: t85
* - juveniles measured
.
-
.
-
. ,
, 0
10
20
..I..
. ..
.
l **
.
-c
em
. .
30 Initial
..*....%I 40
. 50
.I
60
.
.
.
I
70
.
. 4
60
length (mm).
Fig. 5. Increase in length on recapture after one year for Cabestana spengleri from Ahipara plotted against their initial length on tagging.
egg capsules laid in November 1966 were marked with red nail varnish as soon as they appeared on the shore and remeasured in November 1967. This gave the growth rate during the first year of life for individuals of both populations. These juvenile one-year olds were then tagged in November 1967, liberated again, and remeasured the following year along with the animals originally tagged in November 1966. All the tagged animals plus juveniles from the 1967 breeding season were remeasured in November 1968 giving information over a three year period. No difference in growth rate was found between the sexes or from year to year in animals of the same age so the results were combined to give Figs 4 and 5.
Age and growth in Cabestana
spengleri.
According to Haskin (1954) the methods of age determination in molluscs employed to date may be grouped into three categories: 1) size frequency studies; 2) the interpretation of growth interruption lines on shells or other parts of the animal; 3) experiments involving the release and recapture of marked individuals. In cymatiids the size frequency method showed no segregation into distinct age classes, but a first year class could be recognized by inspection in C. spengleri. At
SHELL
Mill Bay the juveniles
GROWTH
first became
25-l
IN CYMATHDAE
noticeable
on the shore in February
and March
when they had reached 20-30 mm in length, some 334 months after the breeding period. These small animals were marked with nail varnish, measured after one year and tagged in the manner
already
outlined.
They grew rapidly
in their first year and
some reached 70 mm in length with a class average of 55 mm. Between one and four varices were laid down during this period. Animals from this locality which were tagged at an initial length of 5&60 mm in November grew to 110-120 mm in the course of a year and added another two or three varices to their shells (Fig. 6).
Fig. 6. Growth in Cubestuna splengleri from Mill Bay: note the tags which are partly buried in the shell sometimes with only the monofilament nylon still showing. These three animals were tagged at the age of one year and recaptured a year later; three varices have been added in the centre animal and two in the others since they were tagged.
The number of varices laid down in the first year depended on the number of whorls grown before a major interruption caused the first varix to be formed. An annual increment of 50-60 mm for the first two years produced animals which, if they were to grow another half-whorl the following year, would reach 140 mm. This is close to the maximum size recorded for C. spengleri at Mill Bay. A large proportion of the tagged population at Mill Bay ranging from 80-140 mm, however, failed to grow at all during the two-year period of observation. The majority of these animals were between 90-120 mm in length and potentially able to add a further half-whorl to their shells. This lack of growth could not be explained by a food shortage since they were living in an area where ascidians covered 4&60 % of the rock surface. Moore (1936) showed that growth in Purpura lapillus ceased at the onset of sexual maturity. This was definitely not the case in Cabestana spengleri since individuals which have been observed copulating and egg-laying during the breeding
258
J. H. LAXTON
season later commenced
growing.
It appeared
that growth stopped earlier in some indi-
viduals than in others, although reproductive ability was not affected. In C. spengleri sexual maturity of the males was reached in the first year. They have been observed copulating at this age. It is not known whether the females also reached maturity in the first year. The Ahipara population showed an annual increment of 28 mm in the first year and a further
20 mm in the second year. On the basis of this study it appeares
that
C. spengleri takes three years to reach its maximum size under ideal food conditions. The growth curves for individuals of C. spengleri from Mill Bay are shown in Fig. 7 indicating that aging by varix counts was impossible. Aging by counting opercular rings (Kubo, 1953) was also of little value in C. spengleri.
120
Cabestana
spengleri
-
80
0
2
4
6
8
10
12
14
16
18
20
Time (months)
Fig. 7. Age-growth curves of Cubestana spengleri from Mill Bay. A, Individual with four whorls before the first varix. B, Individual with five whorls before the first varix. C, Individual with three whorls before the first varix (v = varix). The curves were constructed as follows. Each curve represents a single tagged animal living unconfined on the shore. The points on each curve show the amount of shell growth that had occurred prior to the animal’s recapture. The shape of the growth curve between each observation of an animal could be deduced from knowledge obtained from other animals living in the same area that the addition of a half-whorl from one varix to the next took a month to complete. Once the particular half-whorl was complete there was no further increase in length until calcification was finished giving the ‘stepped’ growth curve.
SHELL GROWTH IN CYMATIIDAE
259
DISCUSSION The type of discontinuous growth characteristic of cymatiids has not previously been described for molluscs. This type of growth may also be found in other gastropod families
in which
varices
are produced,
such as some muricids
and the Bursidae,
although Gostan (1966) has shown that the rate of shell growthin the rissoid, Rissoa parva, is uninterrupted during the formation of ribs and varices. The fact that R. parva is annual and that muricids, bursids, and cymatiids are long lived may give rise to some difference in growth pattern. The shells of adult Cabestana spengleri with up to seven or eight varices have marked shell shape variations depending on the number of whorls before the first varix (Laxton, 1968). The amount of food available has been shown to influence the growth in the initial stages, and may explain why interruptions occur in rapidly growing individuals. At Mill Bay some animals may grow up to 70 mm in their first year and produce only one varix, while others may reach the same size in the same period but produce either two, three, or four varices. Since the annual increment is the same in both cases one group of animals must have grown continuously while the other suffered interruption. The reason for this difference may be that shell growth exceeds tissue growth, so that periodic halts occur while balance is restored, and during this time a varix is laid down. Since there is a volume increase of about 75 % with every half-whorl added to the shell (Laxton, 1968) tissue growth must be very rapid to keep up with this increase. In continuously growing animals this requires a constant supply of food. The only other alternative in areas where food is less abundant is for growth in stages, each terminated by the formation of a varix. The number of varices, and the size of the first year animals reflects the food conditions of an area. This view is supported by the observation that juveniles with only three whorls before the first varix are found highest on the shore where their ascidian food is scarce. Young C. spengleri found lower on the shore among the densest ascidians grow continuously for five whorls before a varix is secreted. It must be remembered, however, that for C. spengleri it is the food supply prior to the formation of the first varix which has the greatest influence on the ultimate adult shell shape since subsequent varices are invariably formed at half whorl intervals. As the animal grows its power of locomotion increases and it is able to migrate to regions where food is more abundant. When rapidly growing animals are removed from areas of abundant food to regions where it is scarce they continue to complete the half-whorl in the process of secretion but do not add any further half-whorls to their shells. Contemporary animals left in areas where food is abundant continue adding to their shells. This confirms the supposition that rapid growth during the first year requires a super-abundant food supply. Growth in later years, however, is slower and when shell is being added the animals conceal themselves and fast so preventing damaging the new growth. A comparison of the growth rates of the Mill Bay and Ahipara populations of C. spengferi poses an interesting problem. While animals from both populations reach the maximum size recorded for the respective areas in three years, the actual amount
260
J. H. LAXTON
of shell growth for the Mill Bay animals is about twice that of the Ahipara animals for the same period. While the growth rate in terms of reaching maturity is the same in both groups, the rate of increase in biomass of the Ahipara population is half that of the Mill Bay population. This difference is important from the point of view of productivity and the energy required to reach adult size. The ability of the Ahipara population to reach sexual maturity at a smaller size may be an adaptation to the environment of the area. In this region the ascidian food is scarce and very restricted in its vertical distribution. If this food source is to be used efficiently by a large number of individuals sexual maturity will have to be reached at a smaller size. Where food is unlimited and widespread as at Mill Bay, sexual maturity is attained at a greater size and growth may continue after it has been reached. This suggestion is consistent with other populations investigated. Breeding individuals are between 60-70 mm long at Urquhart’s Bay, Whangarei Heads, where food covers less than 2 ‘A of the rock surface at low tide. C. spengleri takes approximately three years to reach its maximum size and judging from the number of tagged animals in the Mill Bay population which did not grow during the two-year observation period, the age of some of the larger individuals must be at least 5 years. The question of longevity can only be satisfactorily answered by continued observation of the marked animals. 14 of the 1’71initially tagged animals were known to have died during the period and the shells of a small number of newly dead unmarked animals were found during the same period, Most of the shells were of fully grown adults. Nothing is known of the mortality between the time they appear on the shore and the age of one year. Only one animal within this age group was found dead. Larval mortality must be very high since each egg capsule contains at least one thousand embryos and one female may lay up to two hundred capsules a season. ACKNOWLEDGEMENTS
I wish to thank Professor J. E. Morton for help and guidance during this study. I am grateful for the use of the facilities of the Leigh Marine Research Laboratory and wish to acknowledge the valuable suggestions and comments of Dr. W. J. Ballantine. REFERENCES
GO~TAN, G., 1966. Aspects cyclique de la morphogenhe de la coquille de Rissoa parva da Costa (Gastropode Prosobranche). Vie ~il~ei~, T 17. pp. 9-86. HANCOCK,D. A., 1965. Graphical estimation of growth parameters. J. Cons. perm. int. Explor. h&r, Vol. 29, pp. 340-351. HASKIN, H. H., 1954. Age determination in molluscs. Trans. N.Y. Acad. Sci., Vol. 16, pp. 300-304. KUBO, I., 1953. Age determination of Babylonica japonica (Reeve) an edible marine gastropod, basing on the operculum. J. Tokyo Univ. Fish., Vol. 34, p. 199. LAXTON,J. H., 1968. The anatomy, feeding, growth and reproduction of some New Zealand cymatiids M. SC. Thesis, University of Auckiand, N.Z., 104 pp. MACKENZIE,C., 1960. Interpretation of varices and growth ridges of EupIeura caudato. Ecology, Vol. 41, pp. 783-784. MOORE, H. B., 1936. The biology of Purpuru Zapillus. 1. Shell variation in relation to environment. J. mar. biol. Ass. U.K., Vol. 21, pp. 61-86.