and suspension-feeding benthic bivalves - Springer Link

Marine Biology

Marine Biology 100, 227-240 (1989)

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| Springer-Verlag 1989

Siphon size and burying depth in deposit- and suspension-feeding benthic bivalves L. Z w a r t s 1 and J. W a n i n k 2 1 Rijksdienst voor de IJsselmeerpolders, P.O. Box 600, 8200 AP Lelystad, The Netherlands 2 Zoological Laboratory, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands

Abstract

This paper analyses the significance of siphon investment in the life strategy of benthic bivalves. It describes the relationships between siphon weight, burying depth and shell size in Mya arenaria, Cerastoderma edule. Scrobicularia plana and Macoma balthica. All data were collected on an intertidal flat in the Dutch Wadden Sea during seven successive winter and summer periods. The four species have in common that (1) the increase of depth in relation to size can be described with an S-curve; (2) there is a linear relationship between log siphon weight and log shell size; (3) siphon investment is maximal for the size classes with the greatest increase in their depth; (4) siphon weight, in proportion to total body weight, decreases gradually for the larger size classes whose depth does not increase; (5) burying depth increases with siphon weight if individuals within a same size class are compared, but burying depth levels off above a certain siphon weight. Macoma balthica and Scrobicularia plana live twice as deep in winter as in summer, although siphon weight for both seasons is about the same. In summer both species use a part of the siphon to graze the surface around the burrow, whereas deposit feeding does not occur in winter. This might explain the seasonal variation in burying depth. On the other hand Cerastoderma edule and Mya arenaria, which are both suspension feeders, show hardly any increase of depth in winter as compared to summer. For benthic bivalves the risk of being taken by a predator decreases with depth. The burying depth levels off where individuals reach the depth refuge (though in winter Scrobicularia plana live at greater depth). The conclusion is that siphon size is one of the main factors determining the burying depth of benthic bivalves and thus plays a critical role in their survival.

tees maximal survival and high offspring numbers. The deeper the burrow, the lower the risk of being washed out (Baggerman 1953, Kristensen 1957, Matthiesen 1960, Breum 1970, Hughes 1970a, Mosher 1972, Hulscher 1973, Ratcliffe et al. 1981, Sutherland 1982 a), of being exposed to extreme temperatures (Thamdrup 1935, Brafield 1964, Johnson 1965, de Wilde 1975, de Wilde and Berghuis 1979, Ratcliffe et al. 1981) or of being taken by a predator. Predation risk is maximal for infauna living near the surface, because (with some exceptions e.g. some predatory worms) predators creep or walk on the surface or swim above it and do not usually dig for prey. Exclosure experiments show that the predation pressure on shallow-living species is much higher than on species which bury deeper (Virnstein 1979, Holland et al. 1980, Reise 1985). Moreover, it has been shown that within a species, individuals living at greater depth in the substrate experience a decreased risk of being eaten by a predator (Table 1). If a deep burrow offers a safe refuge, there must be one or more counterforces which might explain why within a species some individuals risk their lives by living more shallowly. Bivalve species have a siphon with which they consume oxygen and food from the surface and overlying water, so in these species minimization of costs associated with investment in siphon mass might be one of the counterforces. This

Table 1. Studies showing that predation risk of benthic animals

decreases for individuals living at greater depth Predator

References

Starfish

Kim 1969, van Veldhuizen and Phillips 1978, Allen 1983 Reise 1979, Virnstein 1979, Blundon and Kennedy 1982b, Pearson et al. 1981, Haddon et al. 1987 Commito 1982 Kelso 1979 Reise 1978 Myers et al. 1980, Zwarts and Wanink 1984, Richardson 1985, Wanink and Zwarts 1985

Crab Introduction

It must be an essential part of the life-strategy of estuarine macrozoobenthos to select a burying depth which guaran-

Snail Fish Shrimp Bird

228

L. Zwarts and J. Wanink: Siphon size and burying depth in benthic bivalves

supposition is based on two assumptions: depth is a function of siphon mass and the investment in siphon mass competes with somatic growth and gonad production. This paper focuses on the question of how much an animal has to invest in siphon mass to reach the depth refuge. We therefore compare depth and siphon mass in species with different feeding methods, and within each species the different size classes. It has already been suggested by Ansell (1962) and Trueman et al. (1966) that siphon length might determine the maximal burying depth. Green (1967) observed that a Scrobicularia plana died when it was buried so deeply that the inhalent siphon could not reach the surface anymore, and Jackson and James (1979) showed that Cerastoderma edule did not survive a burial below their natural living depth. If it is true that siphon length determines the maximal burying depth, it is to be expected that burying depth in deposit-feeding bivalves is more variable than in suspension feeders. Suspension feeders have to reach the surface only, but deposit feeders use a part of the inhalent siphon to graze the surface around their burrows. Zwarts (1986) describes the burying depth of the deposit-feeding bivalve Scrobicularia plana as a compromise between feeding and avoidance of predation: the deeper the burrow the smaller the radius for deposit feeding. Hence the burying depth is maximal if the feeding radius is nil and the feeding mode is reduced to suspension feeding. This paper investigates the relationships between burying depth, siphon weight and shell size in two suspension feeders, Cerastoderma edule and Mya arenaria, and two species which are able to graze on the surface for deposit: Macoma balthica and S. plana.

and it is necessary to make a correction for the loss of the surface layer. Therefore we usually used a pin which was pushed into the substrate just to the surface before the core was taken. The "core sampling method" is accurate (see also Hulscher 1973), but bivalves of < ca. 5 mm are easily overlooked. Therefore we twice took additional core samples, which were cut into slices and sieved apart. This "slice technique", which was also used by Reading and McGrorty (1978), Ratcliffe et al. (1981) and Blundon and Kennedy (1982b), gives the number per depth category. The mean depth of each category indicates in this technique the distance between the surface and a point about halfway between the upper and lower edge of the shell. The slices were cut at 0.75, 1.25 cm, 1.75 cm and so on, to make the depth of spat (4 6 mm) comparable with the depth classes 0.5, 1 cm, 1.5 cm and so on, used in our core sampling method. The core sampling technique was also convenient for determining the siphon width of Mya arenaria. The siphon of this species leaves in the mud a well-marked circular corridor, which can be measured easily, if the core is broken.

Laboratory The collected bivalves were stored in fresh sea water of 4 ~ for max. 24 h. The length of the bivalves was measured along the anterio-posterior axis to the nearest mm. The flesh was removed from the gaping shell after a short immersion in boiling water. The inhalent siphons of Cerastoderma edule, Macoma balthica and Scrobicularia plana were cut off to be weighed separately from the body (Fig. 1). Since the inhalent and exhalent siphon of Mya arenaria are fused, in this species the total siphon was removed.

Materials and methods

Field work The study was performed on intertidal mudflats along the mainland coast of Friesland, the Dutch Wadden Sea (53o25' N, 6004` E). Most samples were taken at one study site, which was situated at mean sea level and where the clay content (fraction < 2 #m) amounted to 6.5%. The burying depth of the four bivalve species was measured once or twice a month during 7 yr, 1980 to 1986. We used a circular corer (1/56 m 2) which was thrust 40 cm into the substrate. The core was then placed horizontally and broken carefully. Depth was defined as the distance between the surface of the mud and the upper edge of the shell and measured to the nearest 0.5 cm. The depth measurement is systematically too low if the upper layer is lost during the handling of the core. A comparison between the "core sampling method" (as described above) and depth measurement by means of a thin thread attached to the shell revealed an average underestimation of nearly 0.5 cm (Zwarts 1986). The amount lost is variable, however, since it depends on how semi-fluid the surface layer is. After a storm the bottom is firm and nothing gets lost, but after a calm weather period the surface layer is soft

Cerastoddrma edule

Mya arenaria

Scrobicularia plana

Macoma balthica

Fig. 1. The way in which the total siphon of Mya arenaria and inhalent siphon of three other species were removed


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Analysis

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All analyses in this p a p e r pertain to a winter (Nov.-March) and a summer period (July to September) during which, according to a preliminary analysis, the bivalves remained at a similar depth. SPSS (Nie et al. 1975) was used for all statistical analyses.

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Results 35 Burying depth and shell size

Fig. 3. Cerastoderma edule. Frequency distribution of depth per size class in winter (grey histograms; n = 453) and in summer (black histograms; n = 835). Mean depth indicated. Table 2 gives statistical analysis The flesh was dried at 70 ~ for a m i n i m u m of 24 h before the dry weight was determined. The samples were burned in a furnace at 550 ~ for 2 h to compute the ash-free dry weight ( A F D W ) by subtracting ash weight from dry weight. A F D W was not determined for all inhalent siphons. F o r the latter the average relative weight loss during burning

The depth measurements of M y a arenaria are given in Fig. 2. The relation between burying depth and shell size can be described by an S-curve. M. arenaria < 10 m m live in the upper 2 cm of the substrate. They increase their depth when they grow from 10 to 40 m m and remain at the same depth level when > 50 mm. In winter M. arenaria live 10% deeper than in summer. Cerastoderma edule remain near the surface, but there is an increase o f depth with size and their burying depth in winter is larger than in summer (Fig. 3).

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Table 2. Results of 4 two-way analyses of variance (ANOVA) to test effect of shell size and season on depth distribution (same data as in Figs. 2-5) Species

Size

Mya arenaria Cerastoderma edule Maeoma balthica Scrobieularia plana

Season

R2

p

R2

p

R2

p

76.4% 21.3 1.8 5.1

0.001 0.001 0.001 0.001

0,6% 0.7 33.3 50.2

0,001 0,001 0.001 0,001

0.7% 1.3 0.4 0.2

0,001 0,002 0,001 0.001

g

Number of cases 2 528 1 288 8 320 8 336

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winter (Fig. 5). Depth increases with size in the range of 10 to 30 m m length. Smaller individuals were not found because there was no new spatfall during the study period. The depth/size relationship is significant in all four species (Table 2). There is a large difference between winter and summer depth in the deposit feeders. Macoma balthica and Scrobicularia plana, but not in the suspension feeders, Mya arenaria and Cerastoderma edule. In all species there is rem a r k a b l e variation in burying depth for a given size class, especially in the 2 deposit-feeding species.

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Fig. 5. Scrobiculariaplana. Frequency distribution of depth per size class in winter (grey histograms; n = 3 082) and in summer (black histograms; n = 5 254). Mean depth indicated. Table 2 gives statistical analysis Large Macoma balthica live deeper in the substrate than smaller ones, but the depth remains the same for all animals > 10 m m (Fig. 4). In summer M. balthica > 10 m m live at a depth of 2 cm c o m p a r e d to an average of 5 cm in winter. Scrobiculariaplana which pass the limit o f 30 m m remain at a b o u t the same depth, 6 cm in summer and 11 cm in

The increases of siphon weight and total b o d y weight with size in the four species are shown in Fig. 6. There is a large variation in b o d y and siphon weight on different sampling dates within the summer and winter periods, which explains why the exponential increase of b o d y weight with size does not have as perfect a linear correspondence on a log-log scale as it does for each sampling date separately. The increase o f siphon weight with size is also exponential for all four species, though there is a leveling off in the siphon weight for the larger individuals (Fig. 6). Burying depth and siphon weight Siphon weight was measured instead of siphon length since length is very difficult to measure. C h a p m a n and Newell

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Number of cases 1 816 237 2700 6178

Sanchez-Salazar et al. 1987b). It is not yet clear to what degree size and depth offer protection against these shallowfeeding predators. In any case, quick growth is apparently a first priority, to be followed by increase in siphon mass to make possible a greater burying depth. It has been suggested that reproduction in these benthic bivalves is delayed in order to divert its resources into rapid early growth (Lammers, /967 for Macoma balthica; Seed and Brown 1978 for Cerastoderma edule, Brousseau, 1979, Commito 1982 for M y a arenaria). Table 6 shows that maximal siphon growth also takes place before sexual maturity is reached. The three priorities during the course of the life of

238


a b e n t h i c bivalve therefore seem to be: (1) to grow fast; (2) to increase b u r y i n g depth; a n d (3) to p r o d u c e offspring. Acknowledgement. Most of the bivalves used for this study were handled in the field as well as in the laboratory by T. van Dellen. We are grateful to him and to B. Toxopeus, J. L. Straat and many others who made it possible to establish this data base. We also thank R. H. Drent for his supervision, R. M. Drent, B. J. Eus and T. Piersma for their comments on the draft manuscript, and D. Visser for his preparation of the figures.

Literature cited Allen, P. L. (1983). Feeding behaviour of Asterias rubens (L.) on soft bottom bivalves: a study in selective predation. J. exp. mar. Biol. Ecol. 70:79 90 Ansell, A. D. (1962). Observations on burrowing in the Veneridae (Eulamellibranchia). Biol. Bull. mar. biol. Woods Hole 123: 521-530 Bachelet, G. (1980). Growth and recruitment of the tellinid bivalve Macoma balthica at the southern limit of its geographical distribution, the Gironde estuary. Mar. Biol. 59:105-117 Baggerman, B. (1953). Spatfall and transport of Cardium edule L. Arch Neerl. Zool. 10:315-342 Beukema, J. J., de Bruin, W. (1977). Seasonal changes in dry weight and chemical composition of the soft parts of the tellinid bivalve Macoma balthiea in the Dutch Wadden Sea. Neth. J. Sea Res. 11:42-55 Beukema, J. J., Meehan, B. W. (1985). Latitudinal variation in linear growth and other shell characteristics of Macoma balthica. Mar. Biol. 90:27-33 Blundon, J. A. Kennedy, V. S. (1982a). Mechanical and behavioral aspects of blue crab, Callinectus sapidus (Rathbun), predation on Chesapeake Bay bivalves. J. exp. mar. Biol. Ecol. 65:47-65 Blundon, J. A., Kennedy, V. S. (1982b). Refuges for infaunal bivalves from blue crab, Callinectus sapidus (Rathbun), predation in Chesapeake Bay. J. exp. mar. Biol. Ecol. 65:67-81 Brafield, A. E. (1964). The oxygen content of interstitial water in sandy shores. J. Anim. Ecol. 33:97-116 Brafield, A. E., Newell, G. E. (1961). The behaviour of Macoma balthica (L.). J. mar. biol. Ass. U.K. 41:81-87 Breum, O. (1970). Stimulation of burrowing activity by wave action in some marine bivalves. Ophelia 8:197-207 Brousseau, D. J. (1978). Population dynamics of the soft-shell clam Mya arenaria. Mar. Biol. 50:63-71 Brousseau, D. J. (1979). Analysis of growth rate in Mya arenaria using the Von Bertalanffy equation. Mar. Biol. 51:221-227 Burton, P. J. K. (1974). Feeding and the feeding apparatus in Waders. British Museum, London Caddy, J. F. (1967). Maturation of gametes and spawning in Macoma balthica (L.). Can. J. Zool. 45:955-965 Cain, D. J., Luoma, S. N. (1986). Effect of seasonally changing tissue weight on trace metal concentrations in the bivalve Macoma balthica in San Francisco Bay. Mar. Ecol. Progr. Ser. 28: 209-217 Chambers, M. R., Milne, H. (1975). The production of Macoma balthica (L.) in the Ythan Estuary. Estuar. cstl mar. Sci. 3: 443 -455 Chambers, M. R., Milne, H. (1979). Seasonal variation in the condition of some intertidal invertebrates of the Ythan estuary, Scotland. Estuar. cstl mar. Sci. 8:411-419 Chapman, G., Newell, G. E. (1956). The role of the body fluid in the movement of soft-bodied invertebrates II. The extension of the siphons of Mya arenaria L. and Serobieularia plana (da Costa). Proc. R. Soc. B. 145:564-580 Commito, J. A. (1982). Effects of Lunatia heros predation on the population dynamics of Mya arenaria and Maeoma balthiea in Maine, USA. Mar. Biol. 69:187-193

Earll, R. (1975). Temporal variation in the heart activity of Scrobicularia plana (Da Costa) in constant and tidal conditions. J. exp. mar. Biol. Ecol. 19:257-274 Gilbert, M. A. (1977). The behaviour and functional morphology of deposit feeding in Macoma balthica (Linne, 1758) in New England. J. moll. Stud. 4 3 : 1 8 - 2 7 Goss-Custard, J. D. (1969). The winter feeding ecology of the redshank, Tringa totanus. Ibis 111:338-356 Goss-Custard, J. D., Jones, R. E., Newherry, P. E. (1977). The ecology of the Wash I. Distribution and diet of wading birds (Charadrii). J. Appl. Ecol. 14:681-700 Green, J. (1967). Activities of the siphons of Scrobicularia plana (da Costa). Proc. malac. Soc. Lond. 37:339 341 Haddon, M., Wear, R. G., Packer, H. A. (1987). Depth and density of burial by the bivalve Paphies ventricosa as refuges from predation by the crab Ovalipes catharus. Mar. Ecol. 9 4 : 2 5 - 3 0 Hancock, D. A., Franklin, A. (1972). Seasonal changes in the condition of the edible cockle (Cardium edule L.). J. Appl. Ecol. 9: 567-579 Hancock, D. A., Urquhart, A. E. (1965). The determination of natural mortality and its causes in an exploited population of cockles (Cardium edule L). Fish. Invest. Minist. Agric. Fish Food Ser II, 2 4 : 1 - 4 0 Hibbert, C. J. (1976). Biomass and production of a bivalve community on an intertidal mud-flat. J. exp. mar. Biol. Ecol. 25: 249-261 Hodgson, A. N. (1982). Studies on wound healing, and an estimation of the rate of regeneration, of the siphon of Scrobicularia plana (da Costa). J. exp. mar. Biol. Exp. 6 2 : I ] 7 - 1 2 8 Hodgson, A. N., Trueman, E. R. (1981). The siphons of Scrobicularia plana (Bivalvia: Tellinacea). Observations on movement and extension. J. Zool., Lond. 194:445 459 Hotland, A. F., Mountford, N. K., Hiegel, M. H., Kaumeyer, K. R., Mihursky, J. A. (1980). Influence of predation on infaunal abundance in upper Chesapeake Bay, USA. Mar. Biol. 57: 221-235 Hughes, R. N. (1969). A study of feeding in Scrobieularia plana. J. mar. biol. Ass. U.K. 49:805-823 Hughes, R. N. (1970 a). Population dynamics of the bivalve Scrobicularia plana (Da Costa) on an intertidal mud-flat in North Wales. J. Anita. Ecol. 39:333-356 Hughes, R. N. (1970 b). An energy budget for a tidal-flat population of the bivalve Scrobieularia plana (Da Costa). J. Anim. Ecol. 39, 357-381 Hughes, R. N. (1972). Reproduction of Scrobicularia plana Da Costa in North Wales. Veliger 14:77-81 Hulscher, J. B. (1973). Burying-depth and trematode infection in Maeoma balthica. Neth. J. Sea Res. 6:141-156 Hulscher, J. B. (1976). Localisation of Cockles (Cardium edule L.) by the Oystercatcher (Haematopus ostralegus L.) in darkness and daylight. Ardea 64:292-310 Hulscher, J. B. (1982). The oystercatcher Haematopus ostralegus as a predator of the bivalve Maeoma balthica in the Dutch Wadden Sea. Ardea 70:89-152 Hummel, H. (1985). Food intake of Macoma balthica (Mollusca) in relation to seasonal changes in its potential food on a tidal flat in the Dutch Wadden Sea. Neth. J. Sea Res. 19:52-76 Jackson, M. J., James, R. (1979). The influence of bait digging on cockle, Cerastoderma edule, populations in North Norfolk. J. Appi. Ecol. 16:671-679 Jensen, K. T., Jensen, J. N. (1985). The importance of some epibenthic predators on the density of juvenile benthic macrofauna in the Danish Wadden Sea. J. exp. mar. Biol. Ecol. 89:157-174 Johnson, R. G. (1965). Temperature variation in the infaunal environment of a sand flat. Limnol. Oceanogr. 10:114-120 Kelso, W. E. (1979). Predation on soft-shell clams, Mya arenaria, by the common mummichog, Fundulus heteroclitus. Estuaries 2: 249 254 Kim, Y. S. (1969). Selective feeding on several bivalve molluscs by the starfish, Asterias amurensis. Bull. Fac. Fish. Hokkaido Univ. 19:244-249

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Date of final manuscript acceptance: July 26, 1988. Communicated by O. Kinne, Oldendorf/Luhe