Behaviour and energetics of whelks, Buccinum undatum (L.), feeding on animals killed by beam trawling

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Journal of Experimental Marine Biology and Ecology,

ELSEVIER

197 (1996) 51-62

Behaviour

and energetics of whelks, Buccinum undutum (L.), feeding on animals killed by beam trawling Paul L. Evans”, Michel J. Kaiserb’*, Roger N. Hughes”

“Ecology Group, School of Biological Sciences, University of Wales, Bangor, Gwynedd, LL57 ZUW, UK “Minimy of Agriculture, Fisheries and Food, Dire&orate of Fisheries Research, Fisheries Laboratory, Benarth Road, Conwy, Gwynedd, LL34 SUB, UK

Received 20 February 1995; revised 23 June 1995; accepted

11 August

1995

Abstract Whelks, Buccinum undutum, are potentially important scavengers of animals damaged or killed as a result of beam trawling. In order to assess the ability of whelks to scavenge these moribund animals, and the consequences of this to energy flow, we presented them with four different species that were either damaged on the seabed or died as a result of capture by beam trawling. Whelks ate swimming crabs, Liocarcinus depurutor, purple heart urchins, Spatangus purpureus, and a gadoid fish, the pouting, Trisopterus minutus, but not plaice, Pleuronectes plutessu. Whelks moved most rapidly towards swimming crabs, suggesting that these were the most preferred prey type. Although the rate of energy intake was highest when whelks fed on sea urchins, when fed to satiation they acquired most energy from swimming crabs. When presented with whole animals, whelks fed preferentially on different body tissues, e.g. they consumed the eyes of pouting first, and never ate the gills or carapace of swimming crabs. Absorption efficiency was highest when fed a diet of swimming crabs (93%) and lowest when fed pouting (83%). Whelks are able to efficiently utilise animals killed by beam trawling, and our results indicate that they prefer the most energetically rich species. In areas of intense beam trawling, such as the southern North Sea, dead or moribund animals which result from these activities could constitute a considerable proportion of whelk diets.

Keywords:

Whelks;

Scavenging;

Beam trawl; By-catch;

Energy-flow

1. Introduction The

benthic

*Corresponding

communities

of coastal

shelf

areas

are subject

author. Fax: (44) (1492) 59-2123.

0022-0981/96/$15.00 0 1996 Elsevier SSDI 0022-0981(95)00144-l

Science B.V. All rights reserved

to various

sources

of

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natural and anthropogenic disturbance, extensively reviewed by Hall (1994). The arrival of scavengers after such disturbance is often dramatic, for example scavenging amphipods (Anonyx sp.) increased to densities 20-30-times greater than those in surrounding areas after grey whales fed on dense mats of tube-building amphipods (Oliver and Slattery, 1985) and, in another study, juvenile gadoids arrived within 10 min at pits recently excavated by crabs, Cancer pagurus (Hall et al., 1993). Scavengers can indeed be an important pathway for energy transfer (Dayton and Hessler, 1972; Stockton and De Laca, 1982; Hall, 1994; Britton and Morton, 1994). Fishing has been recognised as an increasingly important source of benthic disturbance, particularly in areas of intensive exploitation such as the southern North Sea (Bergman and Hup, 1992; de Groot and Lindeboom, 1994). To date, studies have mainly concentrated on the direct effects on the animals intimately associated with the sediment (van der Veer et al., 1985; Rumohr and Krost, 199 1; Bergman and Hup, 1992; Kaiser and Spencer, 1993). Few studies have examined the behaviour of scavengers following these disturbance events although Kaiser and Spencer, 1994 and Kaiser and Spencer, 1996 have demonstrated that some demersal fish feed on disturbed and damaged animals in recently trawled areas. Highly mobile scavengers such as fish and crabs quickly arrive at sites of disturbance (minutes to hours), feed and then disperse (Nickel1 and Moore, 1992; Kaiser and Spencer, 1996). Other, less mobile scavengers, such as whelks and starfish, arrive several hours or even days after the disturbance event (Sainte-Marie and Hargrave, 1987; Nickel1 and Moore, 1992; Kaiser and Spencer, 1996). In the seas of north-west Europe, beam trawling has been suggested as one form of disturbance that has contributed to changes in benthic communities (Pearson et al., 1985; de Groot and Lindeboom, 1994; Lindley et al., 1995). Commercial beam trawls weigh up to 10 tonnes out of water and are fitted with tickler chains or chain matrices which are designed to disturb sole, buried in the sediment, resulting in their capture. A large proportion of the catch (up to 80%) is composed of a by-catch of invertebrates and non-commercial fish species which are then discarded (de Groot and Lindeboom, 1994). This takes no account of the animals which are not retained in the codend but pass through the meshes, or remain exposed or damaged on the seabed. Discards, usually gadoids, from trawlers have already been shown to be an important source of food for seabirds (Fumess, 1982). Those animals not eaten by seabirds sink to the sea bed where they are consumed by a variety of scavengers (Wassenberg and Hill, 1987). It is important to identify which species are important scavengers in different communities, as this may enable us to explain or predict shifts in community structure and energy flow. Scientists from the Ministry of Agriculture, Fisheries and Food (MAFF) have been studying the short- and long-term effects of beam trawling at a site off the north east coast of Anglesey, Wales (Kaiser and Spencer, 1994). This is also a site of a fishery for whelks, Buccinum undutwrz (L.), that are common in the area. Whelks are carnivorous and will scavenge moribund prey as well as a variety of live prey including polychaetes, such as Lanice conchilega, and bivalves (Neilsen, 1975; Taylor, 1978). Whelks are sensitive to odour trails carried by currents (Carr, 1967; Pearce and Thorson, 1967; Walker, 1988) resulting in movement towards bait (Sainte-Marie and Hargrave, 1987; Nickel1 and Moore, 1992). We speculated that whelks could be potentially important

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53

scavengers of beam-trawl discards or of those animals which are damaged by the trawl but are never removed from the sea bed. Thus the aim of the present study was to determine the preference, handling time, satiation ration and absorption efficiency of whelks fed four different types of animals found in the by-catch of a 4 m beam trawl. This in turn would enable us to judge the importance of whelks in determining the fate of beam trawl discards in terms of community energy flow.

2. Experiment

1

2.1. Methods 2.1.1. Collection and maintenance of whelks and discards Whelks were collected in July 1993 from a site off the north east coast of Anglesey using standard French-pattern pots (Kideys et al., 1993) baited with dogfish, Scyliorhinus canicula. Whelks were maintained in glass tanks (45 X 25 X 25 cm) supplied with aerated, continuously flowing seawater (32%0) in a closed recirculating system with an in-line biological filter. The entire system was housed in a constant temperature room at lOS”C, the mean bottom seawater temperature, with a 12 h photoperiod. Four contrasting species that are frequently injured and die as a result of capture in a commercial 4 m beam trawl (Kaiser and Spencer, 1995); plaice, Pleuronectes platessa; bib, Trisopterus luscus; swimming crabs, Liocarcinus depurator; purple heart urchin, Spatangus purpureus, were sorted from the catches of a 4 m beam trawl and immediately blast frozen in 400 g batches. These were stored frozen prior to feeding trials in the laboratory. Whelks were allowed to acclimatise for two weeks prior to any experiments. Individual whelks were labelled using permanent marker pen and divided into four different size-classes defined by shell length (50-59 mm small, 60-69 medium, 70-79 large, and 2 80 mm). Prior to the beginning of a feeding trial all whelks were fed to satiation on a mixture of mussel, Mytilus edulis, and scallop, Pecten maximus, flesh and then deprived of food for 7 days. At the end the study the shell length of each whelk was determined to the nearest 0.1 mm and the soft tissues of the animal were removed from the shell and dried at 100°C for 24 h. 21.2. Food preference The response of whelks to odour trails may differ depending on the type of odour encountered. We tested the responses of different sized whelks to the four different discards. Different sized whelks were selected randomly from the stock tanks according to random number tables which were also used to decide the sequence of prey presentation. The raceway was made from an opaque 60 cm long, 15 cm diameter plastic pipe sealed at both ends apart from a 1.5 cm diameter inlet and outlet pipe. A 4 cm wide slit was cut along the full length of the upper edge of the pipe to allow direct observation of whelk behaviour. A 1 mm mesh panel was fixed 10 cm from the end of the pipe, nearest the seawater inlet, and served as the prey chamber. Individual whelks were

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placed in the raceway, which contained static sea water, furthest away from the food chamber. After 10 min, 60 g (wet weight) of the selected discard, enclosed in a muslin bag, was added to the prey chamber. The time taken, from the moment the whelk passed a start line to the moment it reached the bait (50 cm) was recorded using a stopwatch. Each trial was run for a maximum of 1 h. To remove any scent from the previous trial, the raceway was thoroughly cleaned with a scouring pad and fresh sea water passed through the system for 10 min. Data were subjected to analysis of covariance (ANCOVA), with whelk shell length as covariate. Having shown that the slopes were not significantly different, a posteriori comparisons among adjusted means were made using the Tukey-Kramer test.

2.2. Results 2.2.1. General observations of whelk feeding behaviour Whelks were never attracted to plaice discards and showed no behavioural responses even to dead freshly caught plaice. However, whelks readily consumed all other discards, even though some were relatively difficult to handle (see below). When presented with any of these discards, whelks immediately everted their proboscis, to probe the water column and substratum and then moved towards the prey with the siphon raised and proboscis still everted. On reaching the prey, whelks explored the surface of the item with the proboscis and tentacles, finally gripping it with the foot ready for feeding. Whelks were unable to penetrate the carapace of intact crabs, but gained access to the flesh through breaks in the carapace or through the site of missing appendages. However, one whelk (90 mm shell length) used its foot to crush a crab’s carapace. Whelks preferentially ate the muscle, gonad and gut tissues, but did not eat crab gills or eggs. When feeding on pouting, whelks bored through the skin, using their radula, before eating the flesh. They fed only on the muscle tissues and eyes, leaving the bones, gut and skin. Whelks fed voraciously on damaged sea urchin, eating all the soft tissues but leaving the test and spines. Once feeding had ceased, whelks would move away from the prey, and remain withdrawn into their shell for several days.

2.2.2. Food preference The percentage of whelks that moved 50 cm towards the different prey was greatest when swimming crabs were offered (88%), and lowest for pouting (54%). In the control experiment using no bait, 10% of the whelks reached the feeding chamber. When moving towards the prey, whelks often paused or even returned to the start of the chamber. Whelks which moved directly towards the bait moved at a mean?SE speed of 6.920.9 cm mini’, with a maximum speed of 10.6 cm min-‘. There was no significant interaction between shell length and rate of movement (ANCOVA, F_3,2x= 0.18, P = 0.91). Whelks moved at a similar speed towards sea urchins and pouting, but moved more quickly towards swimming crabs (Table 1).

55

P.L. Evans et al. I J. Exp. Mar. Biol. Ecol. 197 (1996) 51-62 Table 1 Mean?SE distance moved (cm) and the mean?SE the opposite end of the raceway

time taken (min) for whelks to reach each of the discards at

Discard

n

Time to reach bait (min)

Distance moved (cm)

Liocarcinus depurator (swimming crab) Spatangus purpureus (sea urchin) Trisopterus minutus (pouting)

16 16 16

21.551.3* 35.65 1.3 37.82 1.3

44.1 *1.4* 32.85 1.4 31.4 21.4

Significant

differences

3. Experiment

were determined

using the Tukey-Kramer

multiple comparison

test * PsO.05

2

3. I. Methods 3. I. 1. Satiation ration and handling time After acclimatisation in separate tanks, each of 5 whelks from each size-class was presented a pre-weighed portion (approximately 10 g wet weight after blotting dry) of one of the four discard species. Sea urchin tests had to be broken by hand to allow the whelks access to the internal tissues, these would normally be broken by beam trawls on contact with the gear. Handling time, defined as the moment the whelk’s proboscis touched the food to the moment the whelk ceased to feed, presumably having reached satiation, was recorded to the nearest second using a stop watch. Once the whelk had moved away from the food, the remains were collected by siphoning onto blotting paper, weighed, and dried in an oven at 60°C for 24 h and re-weighed. Twenty samples of each discard type were also weighed wet and then dried at 60°C for 24 h and reweighed to obtain conversion factors as follows: swimming crab dry weight = 31.84% wet weight; sea urchin dry weight = 13.30% wet weight; pouting dry weight = 18.18% wet weight. 3.1.2. Gut evacuation and faecal production Whelks (5 individuals from each of the four size-classes) were fed to satiation, as before, but this time the discards were dyed with carmine (Rozin and Mayer, 1964). After consumption of the initial meal, the whelks were fed food that contained no dye. Thereafter coloured faeces of individual whelks were collected every 24 h until no more faeces were produced. The time elapsed from feeding to the emergence of the last coloured faeces was defined at the gut-evacuation time. Faecal strings were collected using a pipette, dried at 60°C for 24 h and weighed. Dried faeces were stored frozen in micro centrifuge tubes ready for biochemical and calorific analysis. Evacuation rate was calculated as g dried faeces h- ’ . 3.1.3. Consumption rate The weight of food required for each of four whelks from each of the four size-classes to reach satiation was estimated as before. Subsequently, each whelk was presented successive pre-weighed amounts of food, noting the time until the complete return of appetite. This enabled the consumption rate to be calculated in terms of dry weight, g

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h- ’ , for different sized whelks. Consumption rate was then expressed as J h- ’ after determination of the energetic content of the discards (see below). Data were subjected to ANCOVA. Differences among adjusted means for different discards were tested for significance using the Tukey-Kramer procedure. 3.1.4. Energy content of discards and faeces The energy content (J g-‘) of both discards and whelk faeces was measured by wet oxidation (Johnson, 1949; Slobodkin and Richman, 1961). Whelks ate only certain tissues from each of the discards, hence samples of these tissues, rather than preparations from whole animals, were analysed. Samples and faeces were dried for 24 h at 60°C. The energy content was determined for triplicate 1 mg samples of each tissue. Since the oxidation of protein is incomplete (Slobodkin and Richman, 1961), a correction was obtained by separately measuring the nitrogen content of triplicate subsamples using the Macro-Kjeldhal method (Slobodkin and Richman, 1961), and the coefficient of 20.1 kJ a correction allowing for the total nitrogen content and g -’ of protein. Subsequently thence protein content of discards and faeces could be calculated for all samples. Incomplete absorption of some foods in the gut means that a certain proportion of the energy is lost in the faeces. When the energy content of the consumed food and consequent faeces is known, the percentage of energy absorbed can be determined. This is the assimilation efficiency, or digestibility coefficient (D) given by: Digestibility Where C=energy

(D) = lOO(C - F)IC (J g-‘)

consumed

and F =energy

content of the faeces produced (J

g-l). 3.2. Results 3.2.1. Satiation ration, handling time and ingestion rate For all three prey-types satiation ration and ingestion rate increased with whelk dry weight (Table 2). Adjusted-mean satiation rations for pouting and sea urchin were similar (pouting 0.416?0.04 g, n=20; sea urchin 0.448-+0.05 g; T-K PzO.O5), but were significantly greater for swimming crab (swimming crab 0.636-+0.09 g, n ~20, T-K PsO.001). Adjusted mean handling time was longest for pouting and shortest for sea urchins (Table 3, T-K P~O.001). Accordingly, ingestion rate was greatest for sea urchin and lowest for pouting (Table 3, T-K P~O.001). 3.2.2. Gut-evacuation time and rate As whelks increased in size their gut-evacuation rate (g h-‘) increased regardless of prey type (Table 2). Gut-evacuation rate was highest when whelks fed on swimming crabs (n=20, meantSE=0.00754~0.0013 g hh’) and lower when fed urchin (n =20, 0.0059~0.0004 g h-‘) and pouting (n =20, 0.0052+0.0005 g hh’). Gut-evacuation time increased with whelk dry weight when whelks fed on sea urchin ((g g- ’ h- ’ ) mean?SE=69.1%3.9 h) or pouting (mean?SE=83.6?3.9 h). No such relationship

P.L. Evans et al. I J. Exp. Mar. Biol. Ecol. I97 (1996) 51-62 Table 2 Linear regression

equations

Satiation amount (g) Ingestion rate (g h.‘) Gut evacuation rate (g h-‘) Gut evacuation rate (g g-’ h ‘) Gut evacuation time (h) (satiation ration) Gut evacuation rate (g h-‘) (satiation ration) Faecal weight (g)

Faecal production

(g)

Return of appetite (h) Consumption

rate

(g h-‘) Consumption (j hh’)

rate

Consumption (j g-’ h-‘)

rate

Linear regression and (g g-’ h-l), time (h) and rate (g h-l), (J h-‘)

57

df

Food type

Regression

19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 19 15 15 15 15 15 15 15 15 15 15 15 15

L s T L s T L s T L s T L s T L s T L s T L s T L s T L s T L s T L s T

log,(y)= log,(y)= log,(y)= log,(y) = log,(y)= log,(y)= log,(y)= log,(y) = log,(y) = log,(y)= loge(y)= log,(y)= log,(y) = log,(y)= log,(y)= log,(y)= log,(y)= log,(y)= log,(y)= log,(y) = log,(y) = log,(y) = log,(y)= log(y)= loge(y)= log,(y)= log,(y)= log,(y) = log,(y)= log,(y)= log,(y) = log,(y)= log,(y)= log,(y)= log,(y)= log,(y)=

equation -2.48+ 1.2210gcDW - 1.90+0.621og,DW - 1.81+0.55log,DW - 1.25 + 0.731og,DW -0.62+0.4010geDW - 1.44+0.39log~DW -6.38+ 1.261ogDW - 5.54 + 0.24log,DW -6.11 +0.49log,DW -6.98 +0.26log,DW -5.54 +0,76log
SE (slope)

F

P

0.038 0.028 0.04 0.05 0.04 0.09 0.03 0.03 0.03 0.03 0.03 0.03 0.01 0.02 0.02 0.01 0.02 0.02 0.07 0.05 0..05 0.07 0.05 0.05 0.03 0.01 0.03 0.06 0.03 0.03 0.06 0.03 0.03 0.06 0.03 0.03

51.4 24.5 38.4 10.4 6.5 6.8 87.3 4.1 10.6 3.7 39.8 11.7 0.2 23.3 11.7 394.9 47.6 109.5 8.1 40.0 0.1 8.3 21.3 0.1 3.2 20.3 41.6 6.4 32.2 4.5 6.4 32.2 4.4 1.8 5.7 16.3

0.0001 0.0001 0.01 0.004 0.02 0.02 0.0001 0.05 0.004 ns 0.0001 0.03 ns 0.0001 0.003 0.0001 0.0001 0.0001 0.01 0.0001 ns 0.01 0.0001 “S ns 0.0001 0.01 0.02 0.0001 0.05 0.02 0.0001 0.05 ns 0.03 0.001

equations (loge) for; satiation amount (g). ingestion rate (g h ‘), gut evacuation rate (g h- ‘) faecal weight (g) and faecal production (g h-‘) on whelk dry weight (g), and gut evacuation (g h-l) on satiation amount dry weight (g), and return of appetite (h) and consumption rates and (J g-’ h-‘) on whelk dry weight (g).

existed, however, for swimming crabs (mean?SE= 8.5.352.6) (Table 2). Gut-evacuation rate increased with increasing satiation ration (SA) for sea urchin and pouting but not for swimming crab (Table 2). Faecal production increased with increasing whelk size when fed either swimming crabs or sea urchin, however, no such relationship was found for pouting (Table 2).

58

P.L. Evans et al. I .I. Exp. Mar. Biol. Ecol. 197 (1996) 51-62

Table 3 A summary table of mean+SE satiation amount (g dry wt), handling time (h), ingestion rate (.I he’), time to return of appetite (h), consumption rate (J h-‘) and % body weight consumed day ’ for each of the different prey-types for whelks between 5-10 cm shell length Species

n

Satiation

L. depurator s. purpureus T. luscus

20 20 20

0.636+0.088 0.4161-0.04 0.448?0.054

0.739-t0.111 0.4221-0.040 0.971-+0.097

Return of appetite

Consumption

L. depurator S. purpureus T. luscus

16 16 16

25.31% 1.93 27.83 2 1.23 38.99e4.48

281.4230.7 198.8222.0 128.0-t-13.1

Handling

amount

time

Ingestion

rate

IO 9662237 13434kl522 5689t455 rate

% Body wt day

’

14.16tl.85 8.08 k-o.62 6.40 to.97

3.2.3. Energy content of discards and faeces The energy content of pouting was similar to that of sea urchin (T-K, P~0.3) and was higher than that for swimming crab (T-K, P50.001). The energy content of the faeces produced was ranked poutingzsea urchinrswimming crab (Table 4). The energy content of faeces was similar from all size classes of whelk (T-K Pr0.05). 3.2.41 Digestibility coefficient (0) Larger whelks absorbed less energy per unit dry mass of sea urchin than small whelks but absorbed more energy from pouting. This was derived from the relationship between the d(digestibility coefficient) (D) (arcsin transformed) and log, whelk dry weight (g) (sea urchin; D = 1.46 - 0.132 dry weight; pouting; D = 0.97 +O. 12 1 dry weight). There was no effect of whelk size on the absorption efficiency of whelks fed swimming crabs (Pr0.05). Mean (&SE) absorption efficiency was greatest for swimming crabs (93.4+1.0%)>sea urchin (90.15 1.6%) and lowest for pouting (83.6?3.7%). 3.25 Consumption rate and return of appetite The time taken for appetite to return differed significantly among the alternative prey-types (ANCOVA, F=9.57, PSO.001). Return of appetite increased from a mean of 25 h when fed swimming crab to 39 h when fed pouting (Table 3). As whelks increased in size, the time taken for appetite to return increased when sea urchin and pouting were eaten but did not vary significantly when swimming crab was eaten (Table 2).

Table 4 MeantSE energy content (kJ g-’ dry weight), corrected and faeces (n = 4) consequently produced by whelks Species

L. depurutor S. pui-pureus T. luscus

for protein content,

of different

prey types (n = 3).

Energy content (kJ g ‘) Food

Faeces

10.96kO.23 12.38+0.1 I 12.08+0.33

6.9620.22 ll.O2t-0.32 17.44?0.19

P.L. Evans et al. I J. Exp. Mar. Biol. Ecol. 197 (1996) 51-62

59

Consumption rate for different size-classes of whelk differed with only marginal significance among prey-types (ANCOVA, F =3.01, P=O.O6). However, the mean consumption rate, corrected for whelk size, differed significantly among all prey-types (T-K P
4. Discussion 4.1. Feeding

behaviour

and energetics

It is clear from our studies that whelks will feed on some animals discarded from, or killed as a result of, beam trawling (Kaiser and Spencer, 1995, 1996; and present study). However, although whelks are apparently capable of eating a wide range of prey, they were not attracted to plaice. This is contrary to Dakin (1912) who recorded whelks feeding on plaice tangled in set nets. Such plaice may have been in a state of decomposition, therefore perhaps more attractive than those used in our study which were either fresh or fresh-frozen (M. Fonds and S. Groenewold, personal communication). On the other hand, pouting were readily eaten, perhaps owing to the difference in flesh texture or rate of decomposition. Whelks were strongly attracted to the swimming crabs, reaching the food chamber more quickly than when either sea urchin or pouting were presented. Despite this, swimming crabs contained the least energy per g dry weight. Handling time to reach satiation was least when whelks consumed sea urchin, but longest for pouting. Hence the rate of energy intake to reach satiation (calculated from Table 1) was ranked sea urchin (13.4 kJlh)rswimming crabs (10.8 Id/h)? pouting (5.7 kJ/h). Although whelks were able to obtain the greatest short-term rate of energy intake by eating sea urchin, in the longer term they were able to consume a meal with a higher energy value by eating swimming crabs. This is explained by the lower percentage water content of crab flesh (68%) than of sea urchin tissues (86%). The ingestion rate of whelks feeding on pouting remained fairly constant (58 min/meal) independent of whelk size, as compared with Buccinum lutosa which fed for 15 mm/meal on fish carrion (Morton, 1990). However, B. lutosa only consumed 4% of its body weight of prey as opposed to an average of 6.4% in our study. As expected, gut-evacuation time increased with the size of meal. It was also dependent on the prey-type consumed, being longest for swimming crabs (85 h) and shortest for sea urchin (69 h). Gut-evacuation time did not vary with whelk size when either swimming crabs or pouting were eaten, but increased with whelk size when sea urchin was consumed. This may be attributed to the presence/absence of suitable enzymes in the gut of smaller whelks. Whelks had a higher absorption efficiency when fed swimming crabs (93%) as opposed to sea urchins (90%) or pouting (83%). Although these absorption efficiencies are high, they are by no means exceptional. The mean

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absorption efficiency for carnivorous gastropods is 68% (Bayne and Newell, 1983; Hughes, 1985) and in carnivorous fish may reach values as high as 98% (Fange and Grove, 1979). Moreover, estimated absorption efficiencies could have been elevated by our analysis of only those tissues eaten by whelks. Those tissues not eaten, such as lish skin, contain high concentrations of lipids in comparison with muscle, which is mostly protein. Thus had we analysed homogenates of whole animals we may have obtained much lower absorption efficiencies. This is an important point when considering studies of feeding energetics. As demonstrated here, whelks are highly selective when feeding on whole corpses, and surprisingly avoided tissues with high energy values such as the liver of fish and the exoskeleton and gills of swimming crabs (cf. Stepien and Brusca, 1985; Moore, 1994) which may be difficult to digest. Small whelks consumed a larger proportion of their body weight per day than larger whelks, consistent with the effect of body size on metabolic rate (Hughes, 1985; Morton, 1990). The proportion of body weight consumed for each of the discards was greatest for swimming crabs (14.1%) and least for pouting (6.4%) (Table 3), values that are similar to whelks feeding on dogfish, Scyliorhinus canicula (9.5%) (Kideys et al., 1993). 4.2. Whelks scavenging

on fisheries

by-catch

Several studies have already shown that a variety of scavengers arrive at sites of disturbance within hours (Oliver and Slattery, 1985; Hall et al., 1993; Nickel1 and Moore, 1992; Kaiser and Spencer, 1994). These are usually highly mobile predators such as fish (Hall et al., 1990; Kaiser and Spencer, 1994) or crustaceans (Oliver and Slattery, 198.5; Nickel1 and Moore, 1992) whereas less mobile scavengers such as whelks and starfish may take up to several days to arrive (Kaiser and Spencer, 1996). Despite this delay, these animals will play an important role in the energy recycling of any moribund items missed or ignored by other scavengers. Whelks are well suited to capitalise on fisheries discards, as they are very responsive to chemosensory stimuli exuded from damaged or moribund animals (Himmelman, 1988). In addition, although they are often found in the by-catch of beam trawls, they are well protected by their shell and show 98% survival after capture (Kaiser and Spencer, 1996). Moreover, whelks, while selective, are capable of exploiting a wide variety of prey (present study), and in situations of natural disturbance where other scavengers compete with whelks, this flexible feeding behaviour will maximise the chance of procuring food. Natural disturbances may also attract predators of whelks such as the crab, Cancer irroratus, which has been shown to hinder whelk arrival (Lapointe and Sainte-Marie, 1992). Further investigations, therefore, are required to examine the interactions between whelks and their predators and competitors while feeding on discards. In areas where whelks are common, they have a potentially important role redirecting energy from dead and damaged animals produced as a result of fishing activity. In areas of sustained intense fishing, animals, such as whelks, which can utilize discards may gain a competitive advantage leading to a local increase in their numbers. The clearest example is the increase in certain species of seabirds in the North Sea (Furness, 1982). Indeed, in areas of intense beam trawling, such as the southern North Sea, scavengers

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such as common starfish, Aster& rubens, which survive capture by beam trawls, may become the dominant species. The incidence of beam trawling, which peaked between 1985 and 1990 correlates with the observation by Lindley et al., 1995 that echinoderm larvae (they suggest amphiuroid larvae) became dominant in the North Sea plankton after 1980. It is not unreasonable to assume that different communities may similarly contain scavengers with equivalent potential to increase in numbers as an indirect result of fishing activity.

Acknowledgments The authors wish to thank P. Geoff Moore for thoroughly helpful suggestions.

reading the manuscript

and

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