J. Zool., Lond. (1973) 171, 499-512

Deposit feeding in Abra ternis (Bivalvia : Tellinacea)

T. G. HUGHES Dove Marine Laboratory, Cullercoats, Northumberland, England

(Accepted 12 June 1973)

(With 7 figures in the text)

Deposit feeding in Abru tenuis is described in terms of the size of particles utilized. Material is collected by the inhalant siphon performing a circular motion sucking in

sediment from beneath and on the surface. The size distribution of silica admitted into the mantle cavity is described and shown to

be controlled by physical parameters, The density of a particle does not affect its uptake by the inhalant siphon. The size distribution of the sediment affects the size distribution of particles admitted to the mantle cavity.

No selection of material for ingestion in terms of size occurs after it has been taken into the mantle cavity. Thus the range of material ingested is ultimately controlled by a physical parameter, the inhalant opening.

Contents Page

Introduction. . . . . . . . . . . . . . . . . . . . . . 499 Analysis of the sediment of the natural habitat of Abra tenuis . . . . . . 501 Siphonal activities . . . . . . . . . . . . . . . . . . . . 501 Inhalant aperture width and maximum size of silica particles admitted to the mantle

Analysis of silica admitted to the mantle cavity . . . . . . . . . . 504 A model of inhalant siphon action . . . . . . . . . . . . . . 507 The effect of the density of a particle on its uptake by the inhalant siphon .. 508 Analysis of silica within the stomach . . . . . . . . . . . . . . 509 Discussion . . . . . . . . . . . . . . . . . . . . . . 510 References . . . . . . . . . . . . . . . . . . . . . . 511

cavity . . . . . . . . . . . . . . . . . . . . . . 503

Intraductian The occurrence of deposit feeding in bivalved molluscs is well known. Yonge (1949)

has given a general picture of that occurring in the Tellinacea. Recently Hughes (1969) investigated the feeding of Scrobicularia plana more closely, giving quantitative data while Pohlo (1969) reclassified bivalves loosely grouped as deposit feeders into more clearly defined categories on a basis of their exact feeding behaviour.

There has been no previous reference to the feeding of Abra tenuis (Montagu) and only a few casual observations have been made on other members of the genus. Petersen & Boysen Jensen (191 1) observed that Abra alba sucked up the uppermost layers of sediment and Yonge (1949) described it as “actively pulling in sediment”. The present study investigates deposit feeding in Abra tenuis and, in particular, attempts to quantify the material utilized.

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DEPOSIT FEEDING IN A B R A TENUZS 501

Analysis of the sediment of the natural habitat of Abvu tenuis Specimens were collected from the sand flats of Holy Island, Northumberland. A

sediment analysis of the material within which A . tenuis occurred (top 5 cm) was carried out as outlined by Buchanan (1971). This gave the frequency distribution of the sediment in terms of weight (Fig. l(a)). An additional analysis was carried out in which the minimum dimension of 249 randomly selected silica particles was measured and the results plotted as a frequency histogram (Fig. l(b)). The relative abundance of small particles made measuring those less than 30 pm in minimum dimension impractical. The weight analysis, using the Wentworth scale, is unimodal (at approximately 200 pm). The percentage

Substrate surface lnhclent siphon

Sediment surface !.I 0 5 m m u

0 5mm u (Cl

FIG. 2. (a) Abru tenuis posture when burrowed; (b) inhalant siphon at rest; (c) inhalant siphon showing feeding action.

weight of the silt fraction, that passing through a 62 pm sieve, is 3.1 %. The silica particle analysis is bimodal; the peak of the second mode is also at approximately 200 pm. It is the latter analysis that is of greater significance to the animal, because it reflects the availability of various size ranges of particles.

Siphonal activities Abra tenuis was allowed to burrow in Holy Island sediment and the activity of the

siphons was observed using a binocular microscope. An animal 5-6 mm in shell length

502 T. G . HUGHES

0 . 0 2 -

I I I I I I 2 3 4 5 6 7 0

1 Shell length (rnrn)

FIG. 3. (a) The relationship between inhalant aperture width and shell length; (b) the relationship between the maximum minimum dimension of silica particle admitted to the mantle cavity and shell length.

DEPOSIT F E E D I N G I N A B R A TENUIS 503

will burrow 1-2 cm below the substrate surface (Fig. 2(a)). The exhalant siphon usually remains still beneath the sediment surface. It is the inhalant siphon that is the more active showing two main activities. In the first it extends level with or just above the surface where it remains open but relatively still (Fig. 2(b)). Suspended material can be seen entering. The second movement is that associated with deposit feeding. In this the siphon bends at the end and twists round to describe a circle (Fig. 2(c)). This action occurs both beneath and at the sediment surface and can take place in both the vertical and horizontal plane. During sweeping motions sand grains and other material are sucked in through the inhalant aperture. Sweeping activities are intermittent; the inhalant siphon extends to the surface sweeping, sweeps on the surface and again on descending. Following

01 I I I I I I 1 2 3 4 5 6 7

Shell length (nim)

FIG. 4. Regression lines for the inhalant aperture width/shell length (0 ) and maximum dimension of silica particle admitted to the mantle cavity/shell length (0) and their 95 % confidence regions plotted together.

this there is a period of inactivity (5-20 minutes) followed by another sweeping cycle if feeding is to continue. The return to the surface can be at the same or in a different place.

Inhalant aperture width and maximum size of silica particles admitted to the mantle cavity

The observations were carried out on animals burrowed in sediment kept at 15°C. The diameter of the inhalant siphon aperture was measured by means of an eyepiece micro- meter, measurements being taken when the siphons were still and open. The micrometer measurements were only accurate to approximately f10 pm. The inhalant siphon width was plotted against shell length (Fig. 3(a)).

504 T. G . HUGHES

To determine the maximum size of silica particle admitted to the mantle cavity animals were kept in Holy Island sediment for two days. They were then transferred to a 50 : 50 mixture of Holy Island sediment and pure silica of an appropriate size distribution relative to the size of the animal. Thus animals of shell length 5-7 mm were put into sediment containing 50 % pure silica of size range 250-500 pm (measured as the minimum dimension of a particle). In this way the animal was subjected to a high proportion of silica whose size overlapped that of the expected inhalant aperture. It was found necessary to mix the pure silica with natural sediment as the animals were unable to burrow in pure silica alone. Having burrowed they were observed to feed for at least two minutes. They were then removed as soon as feeding activity stopped and fixed. The silica from the mantle cavity was removed and the largest size of particle (measured as the minimum dimension) admitted was found. This was plotted against shell length.

The plot of inhalant aperture width and shell length (Fig. 3(a)) shows that the relation- ship is linear; the regression equation being y = 0.01 560f0.05181~. It can be seen that the inhalant siphon width varies from 70 pm in animals of 1 mm shell length to 380 pm in those of 7 mm shell length. These values represent the largest minimum dimension of silica particle that theoretically can be admitted to the mantle cavity of an animal of a particular shell length. Figure 3(b) shows the maximum size of silica actually admitted to the mantle cavity. Again the relation in shell length is linear and the regression equation is y = 0.07626+0.03107~.

The two regression lines plotted together with their 95% confidence limits (Fig. 4) shows that the confidence regions overlap up to shell lengths of 4 mm. Above this point they diverge. A test for equality between the slopes of the two revealed that they were significantly different (P = 0.01).

Analysis of silica admitted to the mantle cavity For this experiment only animals of shell lengths 5-6 mm were used. These were kept

at least 12 hours in one of two sediments at 15°C. One, the natural sediment, is that whose size distribution is shown in Fig. l(a) and (b). The second is a mixture of natural sediment and of specially made up silica sand whose size distribution is shown in Table I. Using the Kolmogorov-Smirnov test (Siegel, 1956) it is significantly different in distribution from that of the natural sediment (P=O.Ol). The two modes of the pure silica sand are less pronounced and, by using this, it was hoped to see if a change in the size distribution of the sediment could effect a change in that of the silica within the mantle cavity. Animals seen to have been feeding for at least two minutes were removed and fixed after feeding motions ceased. The mantle cavity silica was then numerically analysed for size distribution ; again particles less than 30 pm in the first series and less than 60 pm in the second were not analysed. In the second series only pure silica was measured.

Five specimens were used in the first experiment and four in the second. Using natural sediment the pooled frequency distribution of silica within the mantle cavity is shown in Fig. 5. The Kolmogorov-Smirnov test used to see if there was any variation between the specimens showed that two were significantly different, but these were only marginal at the 1 % level. The mantle cavity contents, though, were significantly different (P = 0.01) from the Holy Island sediment (Fig. l(b)). Particles varying in size from 30 pm (and less) to 270 pm are taken into the mantle cavity of animals 5-6 mm in shell length. Particles admitted in greatest number are those 60 pm or less in minimum dimension. This may

DEPOSIT FEEDING IN A B R A TENUIS 505

reflect that these are the sizes most readily available in the sediment. However, the mantle cavity distribution is unimodal as compared with the bimodal distribution of the sediment. The mode around 200 pm, present in the latter is absent in the silica from the mantle cavity.

TABLE I Size distribution ofpure silica sediment ( N = 200)

Size group (pm) Absolute frequency

60-90 0220 90-120 0.220

120-1 50 0.060 150-1 80 0.060 180-210 0.115 210-240 0.110 24&270 0.120 270-300 0,080 3W330 0.020 330-360 0.005 360-390 0.005 39M20 0.005

The pooled size distribution of the pure silica within the mantle cavity of animals from the second experiment is shown in Table 11. There is no significant difference between the specimens ( P = 0-01), but all are significantly different ( P = 0.01) from the pure silica sediment (Table I). The pooled size distribution of pure silica from the mantle cavity is

Minimum dimension ( p m ) FIG. 5. Pooled size distribution (5 specimens) of natural sediment admitted to the mantle cavity (figures in

brackets are absolute frequencies if the 30-60 pm size class is discounted).

506 T. G . HUGHES

significantly different (P = 0.01) from that of silica from the mantle cavity of animals feeding on natural sediment. For comparison the distribution of the latter was cut off at 60 pm. The main difference lies with the 90-120 pm group which is greater in the pure

TABLE I1 Pooled size distribution (4 specimens) of pure silica sediment admitted to the mantle cavity

( N = 350)

Size group (pm)

60-90 90-120

120-1 50 150-1 80 180-210 210-240

270-300 240-270

Absolute frequency

0.531 0.283 0.089 0.054 0.026 0.006 0.009 0.003

silica (0.283) than in the Holy Island sediment (0.159). This probably reflects the greater abundance of this size range in the pure silica sediment (0.200) as compared with 0.083) and would indicate that silica admitted to the mantle cavity is dependent to some extent on the size distribution of the sediment the animal is sampling.

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FIG. 6 Diagram of the model Abru siphon.

DEPOSIT FEEDING I N A B R A TENUIS 507

A model of inhalant siphon action To test whether or not the size distribution of particles taken into the mantle cavity is

controlled purely by physical factors, a model of the inhalant siphon was constructed. This is shown diagrammatically in Fig. 6. A glass tube has an aperture of 300 pm which corresponds to the theoretical inhalant aperture of an animal 5.5 mm in shell length (Fig. 4). Water and sand are drawn through the opening into a sand trap by suction induced by the outflow of water from a reservoir. The operation was repeated four times using natural sediment and the sand collected was subsampled and analysed as before. The suction applied throughout each run was made comparable with the others by allowing the water in the reservoir to fall between two predetermined levels. The analysis of silica from the model was compared with a similar analysis of the same sediment taken into the mantle cavity of four specimens of Abra tenuis (shell length 5-6mm).

TABLE 111 Size distribution of the sediment used for the model siphon experiments ( N = 200), that taken into the mantle caviiy of 4 animals ( N = 200) and that taken up

by the model (N = 260)

Absolute frequencies Size group (pm) Sediment Mantle cavity Model siphon

30-60 60-90 90-120

12&150 150-180 180-210 2 1 0-240 240-270 270-300 3W330 330-360 360-390 390-420

0.325 0.170 0.065 0.040 0.140 0.105 0.090 0.025 0.025 0.005 0905 0.000 0.005

0.525 0.275 0.090 0.025 0.045 0.030 0.005 0.005

0.512 0.242 0.077 0.035 0.054 0.054 0.015 0008 0.004

These, as before, were observed to feed for at least two minutes (temperature constant at I5OC) and then removed and fixed.

The frequency distributions of silica taken in by the model siphon and animals are shown in Table 111. The frequency distribution of the sediment used is also shown in Table 111. A Kolmogorov-Smirnov test done on the silica size distributions of the model and mantle cavity shows no significant difference between them (P=O.O5). The largest particle admitted by the model was 273 pm (minimum dimension) which com- pares favourably with that of 255 pm admitted by the animal. Thus selection appears to be by purely physical means and is a result of drawing sediment through a narrow orifice. Whether the factor limiting the size of particle admitted to the mantle cavity is the dia- meter of the inhalant opening or the force of suction is not shown by the above.

508 T. G . HUGHES

The effect of the density of a particle on its uptake by the inhalant siphon If the limiting factor in determining the maximum size of particle admitted to the

mantle cavity is the suction applied, less dense particles may be expected to be preferen- tially taken. To investigate this animals were put into a mixture of 50 % carborundum, 50% pure silica diluted with Holy Island sediment. The carborundum and silica had similar size distributions of 120-260 pm and 140-240 pm (Table IV) respectively. The animals were fed for two minutes and removed and fixed. The distribution of carborundum and the silica/carborundum ratios within the mantle cavity and the sediment were found.

TABLE IV Size distributions of silica ( N = 120) and carborundum (N= 120) used in the density experiment and that of carborundum taken info the mantle cavity of 5 animals ( N = 106)

Size group (pm)

100-120 120-140 140-160 160-1 80 180-200 200-220 220-240 240-260

Silica in sediment

Absolute frequencies

in sediment mantle cavity Carborundum Carborundum from

0408 0.233 0.325 0350 0.083

0.033 0.083 0.117 0.333 0.300 0.125 0008

0.028 0.057 0.151 0160 0.283 0.245 0.047 0.028

TABLE V Ratios of silicalcarborundum particles from random counts on

the sediment and mantle cavity contents

No. Sediment N Mantle cavity N ~

1 2 3 4 5 6 7 8

~

1.016 389 0.692 22 0.792 215 1 Qoo 38 1.037 444 0.741 47 0.838 430 1 .OOO 34 1.007 287 0.833 55 0.903 607 0.905 40 0.938 500 0.637 72 0.932 425

The distribution of carborundum within the mantle cavity (Table IV) is not signi- ficantly different from that in the sediment (P= 0-05) and the Kruskal-Wallis test (Siegel, 1956) showed no variation between the carborundum in the mantle cavities of the five specimens (P= 0-05). The ratios of silica/carborundum are shown in Table V. A Mann- Whitney U test (Siegel, 1956) shows no significant difference between those of the sediment and the mantle cavity (P=0.05). Thus although silica (density 2.635 g cm-2) is lighter than carborundum (density 3.217 g cm-2) it is not taken up preferentially, suggesting the suction of the siphon is not the limiting factor in determining the maximum size of particle taken into the mantle cavity.

DEPOSIT F E E D I N G I N ABRA TENUIS

TABLE VI Size distributions of sediment used for the stomach contents analysis ( N = 200), that admitted to the mantle cavity ( N = 200) and that taken into the stomach

(N = 250)

509

Absolute frequency Size group (pm) Sediment Mantle cavity Stomach

30-60 60-90 90-120

120-150 150-180 180-210 210-240 240-270 270-300 300-330 330-360 360-390

0.390 0.585 0.628 0140 0.250 0.280 0.040 0.060 0.044 0.020 0.035 0.008 0075 0.030 0.020 0105 0.030 0.016 0.125 0.010 0.004 0.050 0.035 0.015 0.OOO 0.005

Analysis of silica within the stomach Again, only animals of shell length 5-6 mm were used. The stomachs were emptied by

starving them for 24 hours at 15°C after which the five specimens were allowed to burrow in natural sediment. Each was observed to feed for 15 minutes and then removed and fixed. The stomach contents were carefully dissected out, the silica separated in chromic acid and all particles larger than 30 pm measured. In addition, a repeat analysis of the

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510 T. G . H U G H E S

silica in the mantle cavity was carried out because the sediment proved to be of a slightly different composition to that used previously. The result of the sediment analysis and the pooled size distribution of silica from the mantle cavity are shown in Table VI. A similar pooled size distribution of silica from the stomach is also shown in Table VI. A Kruskal- Wallis test for homogeneity between the specimens of the latter showed that at the 1 % level they were not significantly different from each other. Also no significant difference was found (P = 0.05) on comparing the material from the mantle cavity with that from the stomach. Thus, in terms of size, there is no difference between the silica taken into the mantle cavity and that ingested.

The external diameter of the oesophagus of 16 preserved specimens of shell length 5-6 mm was measured (Fig. 7). Oesophageal diameter in this size range is only loosely correlated with shell length; the correlation coefficient, r = 0.4485. The external diameter values do not approach the minimum dimension of the largest particle admitted to the stomach (240 pm), however, it has been observed that in living specimens the oesophagus can distend to accommodate large particles.

Discussian Feeding activity similar to that exhibited by the inhalant siphon of Abra tenuis has been

observed in several other species of the Tellinacea and according to Reid (1971) is charac- teristic of species feeding on sand grains. It has been observed in Macoma brota and M. lipara (Reid & Reid, 1969), M. nasuta (Pohlo, 1966), Tellina buttoni (Maurer, 1967), Abra alba (Yonge, 1949) and Scrobicularia plana (Hughes, 1969). Of these Macoma nasuta, Tellina buttoni, Abra alba and Scrobicularia plana were observed actively drawing in sedi- ment and this is the case in Abra tenuis. This specialized mechanism enables them to utilize a broad size range of particles and is in contrast to animals classed by Reid (1971) as fine deposit feeders (e.g., M . calcarea) whose siphons only pick up fine material on the sediment surface.

The occurrence of deposit feeding in tellinaceans is well documented, but in contrast to filter feeding few attempts have been made to quantify the process. Hughes (1969) made estimates of gut clearance and filtering rates in Scrobicularia plana but the nature of the material ingested was not investigated. Hunt (1925) observed that tellinaceans, including Abra alba and A. prismatica, ingested sand and detritus and Yonge (1949) noted that the stomach contents of Macoma balthica, Abra alba and Scrobicularia plana consisted mainly of sand grains. Reid & Reid (1969) reported that although Macoma secfa does not show the rotating action of the inhalant siphon it ingested many sand grains of 300 pm average size.

The size of the inhalant aperture is an obvious limitation to the size of particles taken into the mantle cavity of a deposit feeding bivalve. In Abra tenuis there is a linear relation- ship between the size of the inhalant aperture and the shell length, but the size of this aperture, in itself, does not account for the actual size of particles taken into the mantle cavity. In larger animals this is less than the diameter of the inhalant aperture. The size distribution of silica particles taken into the mantle cavity is markedly different from that of the sediment on which the animal is feeding. When the silica of the mantle cavity is compared with that taken in by a model siphon of corresponding dimensions the size distributions of the two are very similar. This suggests that material is taken into the mantle cavity purely as a result of the dimensions of the inhalant orifice and the rate of

DEPOSIT FEEDING I N A B R A T E N U I S 511

flow through it and not because the animal is actively selecting material. The inhalant siphon does not take silica particles in preference to heavier carborundum particles suggesting that the limiting factor is not the rate of flow but the dimensions of the inhalant orifice. The discrepancy between the diameter of the inhalant aperture and the maximum minimum dimension of particle admitted may be a result of the low probability of getting a particle of minimum dimension approaching the diameter of the aperture in the correct alignment for it to pass through. This discrepancy is seen in animals larger than 4 mm shell length.

As the size distribution of silica admitted to the mantle cavity is controlled by the size of the inhalant orifice, the size distribution would be expected to change with changing size distribution of the sediment. This is so. The general shape of the distribution remains unimodal although the group proportions change. How critical the size distribution of the sediment is to the functioning of the animal is not known but clearly certain limits must

Analysis of stomach contents have shown that in terms of size there is no difference between these and the contents of the mantle cavity. Thus the size range of silica ingested by Abra tenuis is governed by the diameter of the inhalant aperture. The gills and palps do not appear to alter the size distribution of particles in the range 30-300 pm. The oeso- phagus, although its dimensions empty are much less than those of the largest particles admitted to the stomach, does not form a physical barrier to material passing into the stomach. However, not all the material taken into the mantle cavity is ingested. The palps can be seen to reject material and this accumulates under the mantle fold as pseudofaeces.

Yonge (1949) concludes that the large size of the palps in Abra sp. is concerned with taking over selective processes from the reduced gills. Selection, if it occurs in A . tenuis, cannot be concerned with selection of material in terms of size. Reid & Reid (1969) also concluded that there was no selection of particulate material by the pallial organs of Macoma secta. They suggested that differences between this and other species of Macoma could be due to the amount of mucus secreted by the gills and palps. Whether any other form of selection occurs by the pallial organs is not known. In terms of size though, the gills and palps of these animals seem little more than a conveyor system transporting material to the stomach.

apply-

This work was carried out during the tenure of a Research Studentship awarded by the Science Research Council. I would like to thank Dr J. A. Allen for help in the manuscript preparation.

REFERENCES Buchanan, J. B. (1971). Sediments. In Methodsfor the study ofmarine benthos: 30-52. Holme, N. A, and McIntyre,

A. D. (Eds). Oxford and Edinburgh: Blackwell Scientific Publications. I. B. P. Handbook No. 16. Hughes, R. N. (1969). A study of feeding in Scrobicularia plana. J. mar. biol. Ass. U.K. 49: 805-823. Hunt, 0. D. (1925). The food of the bottom fauna of the Plymouth fishing grounds. J. mar. biol. Ass. U.K. 13:

Maurer, D. (1967). Mode of feeding and diet, and synthesis of studies on marine pelecypods from Tomales Bay,

Petersen, C. J. G. & Boysen Jensen, P. (1911). Valuation of the sea. I. Animal life of the sea bottom, its food and

Pohlo, R. (1969). Confusion concerning deposit feeding in the Tellinacea. Proc. maluc. SOC. Lond. 38: 361-364.

560-599.

California. Veliger 10: 72-76.

quantity. Rep. Dan. biol. Stn 20: 3-76.

512 T. G . HUGHES

Reid, R. G. B. (1971). Criteria for categorizing feeding types in bivalves. Veliger 13: 358-359. Reid, R. G . B. & Reid, A. (1969). Feeding processes of members of the genus Macoma (Mollusca: Bivalvia).

Seigel, S. (1956). Nonparametric statisfics for the behaviourul sciences. New York: McGraw-Hill. Yonge, C. M. (1949). On the structure and adaptations of the Tellinacea, deposit-feeding Eulamellibranchia.

Can. J. ZooI. 47: 649-657.

Phil. Trans. R. SOC. (B.) 234: 29-76.