Estuarine, Coastal and Shelf Science (1983) 17, 357-363

An Annual Cycle of Recruitment, Growth and Production in a Malaysian Population of the Trochacean Gastropod Umbonium vestiurium (L.)

A. J. Berrya and Zamri bin Othmanb aDepartment of Biological Science, Stirling University, Stiriing, U. K. and bSchooi of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia

Received 10 October I982 and in revised form I7 December ! 982

Keywords: Gastropoda; production; annual cycles; recruitment; Malaysia coast.

From July 1981 to July 1982 Umbonium vestiarium (L.) on a north Penang sand shore numbered 573-l 1077 m-2 (mean 4126 or 53.1 g dry tissue) near MLWN and 2164-12 414m-2 (mean 6500 or 59.8 g dry tissue) further downshore. Heavy recruitment of young became evident in June and July 1982 and a closely corresponding cohort of young was present in July 1981. Progression of this cohort indicated that young settling in May-June grew to full size ( 1 l-l 3 mm diameter) by January-March the following year and that virtually all died during their second year, presumably having spawned in March-May. Recruitment of young was chiefly on the lower shore but adults came to be more abundant and predominant on the upper shore. There is some evidence of migration upshore during growth.

Production is estimated at 105.4 g dry tissue m-2 y-1 (2118 kj) at the lower shore level and this is almost double the 58.8 g m-2 y-1 (1176.6 kj) at the higher level. These values represent almost the entire secondary production across much of the sand flats.

Possible causes of such a marked annual cycle in the very weakly seasonal tropics of the Malacca Strait are considered and it is suggested that monsoonal changes in wind, wave action and salinity might be involved.

Introduction

The humid tropics of Malaysia lack the dominant annual fluctuations of temperature and daylength that mark seasons in higher latitudes (Dale, 1963). Even changes in rainfall and relative humidity are far less marked and less seasonally regular in the Malacca Strait than in many other equatorial regions (Dale, 1959). In the absence of such powerful influences, many marine animals are known to breed and grow without close regard for the calendar (e.g. Braley, 1982 for a Guam oyster; Giese and Pearse, 1974, for invertebrates more generally). Continuous or near-continuous breeding with weak fluctuations have been reviewed for Malaysian aquatic and terrestrial molluscs and compared with other inverte- brates and lower vertebrates by Berry (1975). Several of these cases of fluctuating repro- ductive condition and population size-composition were related to weakly and variably seasonal rainfall, and others to non-annual features of tidal regimes. They contrast with

357 0272-7711/83/090357-t07 f&03.00/0 G 1983 Academic Press Inc. ‘Londun~ Lunltd

358 A. J. Bert-y & Z. bin Othman

well defined annual cycles among some higher vertebrates including, for example, some Malaysian bats (Medway, 1972). Broom (1982) refers to the long recognized seasonal spawning of the Malaysian cockle Anadara and presents further evidence suggestive of seasonality in populations of mudflat bivalves and gastropods. He proposes a relationship with seasonal changes of inshore salinity similar to that in some Indian oysters (Stephen, 1980). None of these invertebrate examples comprises a clearly marked definite annual cycle of breeding and subsequent population change.

Some clean sandy Malaysian shores support dense populations of the trochacean snail Umbonium vestiarium (L.) hidden 0.5-l ‘5 cm deep in clean sand and, near the N. W. extremity of Penang island, they dominate the fauna completely on most of the lower sand flats below about M.L.W.N. Aspects of the functional morphology of Umbonium are de- scribed by Fretter (1975) who described filter feeding and suggests they may also feed on organic deposits in the soil. Berry (1982; 1983) has described such a population during July-September 1981 with special reference to predation by naticid snails (and, less, by a starfish) for which Umbonium forms the only source of food. That study indicated that in July-September (a) the population comprised groups of small and of large snails in two distinct components, (b) the small group increased steadily in size during those 3 months and (c) the larger Umbonium tended to form a greater proportion of the population upshore while the smaller ones were more abundant downshore.

One of the authors (Z.O.) was able to continue counts on the same site at the Field Station of Universiti Sains Malaysia, Penang, with the aim of following changes in abundance and size-composition through a complete year.

Site, materials and methods

The location, profile and composition of clean sand flats from about 1.1 m above chart datum to lowest tides at Telok Aling, Penang, are described for mid-1981 by Berry (1982). During the subsequent observations (till July 1982) the horizontal extent of the upshore

TABLE 1. Numbers of Umbonium m-2 in year-group 0 and year-group I (with percentages of total) at 35 m and 45 m downshore during July 1981-July 1982. Each count comprised 2-6 pooled 10 cm diameter cores

35 m downshore 45 m downshore

Date Group 0 Group 1 % Group I Total Group 0 Group I % Group 1 TOtd

25 May 1982 0 22 June 1982 63.7 19 July 1982 1527.8 16 July 1981 191 .o 15 August 1981 7193.6 10 September 1981 4742.7 28 October 1981 191.0 25 November 1981 3596.5 25 December 1981 445.6 27 January 1982 732.1 24 February 1982 2864.7 30 March 1982 4010.6 28 April 1982 1718.8

976.1 4965.5 4774.5 5092 8 3883.3 1559.7 1273.2 795.8 127.3

31.8 0 0 0

100 976.1 0 4392.5 100 4392.5 98.7 5029.1 10 121.9 2291.8 18-5 12 413.7 75.8 6302.3 4583.5 2100.8 31.4 6684.3 96.4 5283.8 5283.8 2132.6 28.8 7416.4 35.1 11 076.8 8657.8 2037.1 19-o 10 694.9 24.7 6302.3 7957 5 1464.2 Ii 5 9421.7 87.7 1464.2 3755.9 572.9 13 2 4328 9 18.1 4392.4 5920.4 318.3 5.1 6238.7 22.2 573.0 2546.4 127.3 4.8 2673.7

4.2 763.9 2610.1 0 0 2610.1 0 2864 7 4201.6 0 0 4201 .6 0 4010.6 6047.7 0 0 6047.7 0 1718.8 2164.4 0 0 2164.4

Annual cycle of Umbonium vestiarium 359

coarse sand slope varied between 18 and 22 m from the upshore edge of terrestrial vegetation. Although further profiles were not surveyed, the lower sand flats also shifted such that, as an extreme example, a point 52m downshore coincided with a low tide of 0.4m in March 1982 but with a low tide of 0.8 m in July 1982. It is not clear if these shifts in the profile are of regular occurrence, are accompanied by changes in soil composition of if they might be of significance to the fauna.

Preliminary counts of Umbonium at five shore levels in July-September 1981 were reported earlier (Berry, 1982). Counts were continued subsequently at monthly intervals on low tides (by 2.0.) from October 1981 until July 1982 at two representative levels (a) on slightly raised sand at 35 m downshore (Z 1.1 m above chart datum, just below M.L.W.N.) and (b) at 45 m downshore (0.5-0.8m above C.D., commonly just above M.L.W.S.). On each occasion at least two 1Ocm diameter cores were taken, and up to six cores when numbers were visibly low. Umbonium were recovered from the sand in a sieve of 1.5-2 mm mesh. Greatest diameters of all Umbonium were measured and counted into l-mm size classes and the cores were pooled to give one count for each level each month.

Population and production

The Umbonium population across five shore levels at the north Penang site during July- September 1981 comprised generally larger numbers and mostly smaller snails downshore but higher proportions of larger snails upshore (Berry, 1982). Dry tissue weight during that period was related to maximum shell diameter as follows:

log, g dry tissue = 2.47 x log, mm diameter - 9.84.

Further collections confirmed that from July 1981-July 1982, Umbonium was more abun- dant on the downshore sand (45 m) with an overall mean of 6500.1 m-2 (59.82 g dry tissue), than on the higher sand (35 m) with a mean of 4125.8 m-2 (53.12 g). The only exception was in August 1981 when upshore numbers slightly exceeded those downshore. Totals were generally highest in JuneSeptember and lowest in December-January (Table 1).

Consideration of size classes indicates a clear annual cycle. In June 1982, 10 121.9 m-2 young of 26.9 mm diameter occurred downshore with far smaller numbers upshore (Table 1, Figures 1 and 2). By July 1982 this group grew to 4583.5 m-2 young of 3-7.9 mm down- shore and 1528 m-2 of 4-6.9 mm upshore. Closely corresponding groups of young of 4-7.9 mm at 45 m, and of 5-6.9 mm at 35 m occurred in the lirst counts (July 1981) and the fastest of these grew to = 8 mm (9.06 mg dry tissue) by September 1981 when the mean diameter of the group was 6-7 mm (4.5-6.5 mg). Maximum sizes (11-13 mm, < 30 mg) were reached by January-March 1982 after which little further growth occurred (Figure 2).

Two cohorts coexisted in June-July 1982 and July-November/December 1981 but by December-May the growing young comprised virtually the entire population. These pre- sumably produced the spawn leading to recruitment of the young detected in June 1982. It appears that after the presumed spawning, numbers of adults diminished during August- December and that none (or very few) complete a second year (Figures 1, 2).

Annual production of dry tissue, following the second method of Crisp (1971), totalled 105.39 g m-2 y-l on the downshore sand. This comprised 102.6 g in the younger cohort (year-group 0, May-April) and only 2.79 g in the older cohort (year-group 1). Higher

360 A. J. Berry & 2. bin Othman

C!L--l

L -

dl

61 ?I dl dl

Annual cycle of Umbonium vestiarium 161 ---

. I\

Group 0

May JUI Se0 Nov JfXl MClr 3

Figure 2. Monthly numbers of Umbonium mm* in year-groups 0 and 1 during July 1981 to July 1982 reordered to begin before major recruitment of young (May 1982). 0 and 1 were distinguished by inspection of counts depicted in Figure 1 (-, 35 m downshore; ----, 45 m downshore).

Group 0 and I

Group 0

Figure 3. Monthly producrlon (g dry tissue m 2 month ~1) of year-groups 0, I and total (0 + 1). Dates reordered as in Figure 2.

362 A. J. Berry & Z. bin Othman

on the sand (35 m), annual production of the older cohort was slightly greater (3.53 gj but that of year-group 0 was only 55.27 gm-* y-1 giving a total of only 58.8gm-2y-1. Production rose highest in the young cohort during June-November, appeared to fall steeply in January-February and to rise in March before finally declining to low levels in the diminishing adult cohort (Figure 3).

Numbers and monthly production varied with broad similarity at the two shore levels (Figures l-3), and mean sizes (and tissue weights) of the separate cohorts also coincided closely (Figure 1). Yet the younger cohort were always more abundant downshore than upshore and always comprised a much greater proportion of the total counts there (Table 1). Conversely, the older cohort were always more abundant upshore than downshore except in May 1982 which was the first month they arbitrarily entered year-group 1 (Table 1, Figure 2). The reversal in concentration of large animals after May (Figure 2) resulted partly from a continuing decline in their numbers downshore but, more especially, from a marked increase in their numbers upshore in June-August prior to a final decline matching that downshore (Figure 2).

The foregoing values for yearly production and mean biomass indicate values for P/B of1.762at45mandl.l06at35m.

Discussion

The present findings indicate a cycle of reproduction and population change that is more pronounced and more distinctly annual than those reviewed by Berry (1975) for animals living in generally more sheltered habitats nearer the equator or those indicated for Malacca Strait mudflat molluscs by Broom (1982). Yet there is at present no supporting evidence in terms of changing reproductive condition or the seasonal occurrence of veliger larvae in Umbonium. It remains conceivable, though unlikely, that the observed pattern was merely the result of briefly favourable settlement or survival conditions in mid-year.

The annual pattern is complicated by some irregular variation with strikingly low numbers in December 1981-January 1982 and again in April 1982. November-January marks the height of the N.E. monsoon when northerly winds prevail and reach maximum strength in the northern part of the Malacca Strait. Winds are lightest and variable in direc- tion, by contrast, in May-August (Dale, 1956). These monsoonal changes lead to increased wave action especially on north facing shores in November-January which might well have led to disturbance of the Telok Aling sand and some dispersion of Umbonium with perhaps a redistribution towards sub-tidal levels: certainly numbers were most drastically reduced at the higher shore level in December-January (Figure 1). Wave action is usually minimal in May-September and such calm conditions might particularly favour the settlement and establishment of young.

Rainfall at Penang is also irregularly seasonal with a maximum typically in September- November as the N.E. monsoon begins, and a lesser peak in May, while the driest month is February (Dale, 1959). This heavy rain normally leads to marked reduction of salinity throughout the Malacca Strait in October-November and to a lesser depression in May (Selvarajah, 1961). It is possible that such seasonal low salinity somehow contributed to the losses of Umbonium from the shore in December-January and, less clearly, in April- May. It is also possible that changing salinity affects the onset of reproduction in Umbonium as proposed by Broom (1982) for mudflat molluscs further south in the Malacca Strait and by others (e.g. Stephen, 1980) for other tropical molluscs.

Monsoonal changes in temperature are slight and only irregularly seasonal (Dale, 1963) and daylength at Penang (latitude 5’25 ‘N) varies only some 35 min throughout the year.

Annual cycle of Umbonium vestiarium 363 __-~-

It seems unlikely that these factors exert strong direct influences on reproductive activity in littoral molluscs.

Different counts at the two shore levels strongly imply that settlement of young occurred predominantly on the lower shore. This could be the direct result of longer tidal cover downshore. Lower numbers of young might also have been caused by severer mortality after settlement at high shore levels. Changing numbers at the two levels also imply that Umbonium moved upshore as they approached full size, especially from June when numbers of large snails upshore came to exceed greatly the numbers downshore. It is poss- ible that minimal wave action in mid-year favours upshore movement in contrast to the effects of strong wave action in December-January.

Annual production downshore of 105.4g dry tissue m-2 y-1 (2118 kj) is certain to

have comprised the great majority of all secondary production on the lower shore where Umbonium made up some 89% of total benthic biomass in July-September 1981 (Berry, 1983). Similarly, 58.8 g (1176.6 kj) m-2 y-i must represent virtually all the secondary production at 35 m downshore where, during the same period, Umbonium comprised more than 98% of total biomass. Therefore, while these are high values for production in a littoral gastropod, they are to be compared with the entire secondary production on other shores where single species rarely dominate faunas so completely. P : B ratios are not particularly high.

It is not known how much food is taken by Umbonium nor what proportions are filtered from the water as indicated by Fretter (1975) or taken from deposits in the soil.

Acknowledgements

A. J. B. gratefully acknowledges grants from the Royal Society under the Marshall and Orr Bequest and from the Carnegie Trust for the Universities of Scotland which made work possible in Malaysia during July-October 1981 and, also, the assistance and facilities made available in that period by Universiti Sains Malaysia, Penang.

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