Journal of Experimental Marine Biology and Ecology, L 240 (1999) 213±228

Hunger rapidly overrides the risk of predation in the subtidal scavenger siquijorensis (: ): an energy budget and a comparison with the intertidal Nassarius festivus in Hong Kong

B. Morton* , K. Chan The Swire Institute of Marine Science, The University of Hong Kong, Cape d'Aguilar, Shek O, Hong Kong Received 4 January 1999; received in revised form 23 April 1999; accepted 1 May 1999

Abstract

This study shows that, as with its intertidal counterpart, Nassarius festivus, the rate at which subtidal Nassarius siquijorensis moves towards food bait is similar for starved and well-fed individuals. This study also investigates another facet of nassariid nutrition related to the degree of hunger, i.e. the effect of simulated predation upon a feeding assemblage. Individuals which fed within 7 days, cease feeding and depart palatable food if crushed conspeci®cs are added. Between 7 and 13 days since its last meal, however, N. siquijorensis will feed when food is available, despite the possibility of predation. For the intertidal N. festivus, the critical time for hunger to override the risk of predation is between 14 and 21 days. The difference between subtidal and intertidal may be due to a difference, in terms of days, that a meal can provide for their energy expenditure, particularly with regard to respiration. The bigger, subtidal, N. siquijorensis needs to feed more frequently than the smaller, intertidal, N. festivus.  1999 Elsevier Science B.V. All rights reserved.

Keywords: Carrion; Scavenging; Nassarius; Hong Kong; Energy budget; Predation risk; Respira- tion

1. Introduction

Due to the unpredictable supply of carrion in the sea, there are probably no obligate scavengers, only facultative (opportunistic) species which would normally pursue a

*Corresponding author. Tel.: 1852-2809-2179; fax: 1852-2809-2197. E-mail address: [email protected] (B. Morton)

0022-0981/99/$ ± see front matter  1999 Elsevier Science B.V. All rights reserved. PII: S0022-0981(99)00060-X 214 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 predatory life style (Britton and Morton, 1993, 1994a). Taylor (1980) identi®ed 93.3% of the gut contents of the subtidal nassariid gastropod Nassarius siquijorensis (A. Adams, 1852) in Hong Kong as comprising ®sh bones and scales and unidenti®able tissue. Later, Taylor and Shin (1990) showed gut contents to comprise 26.7% sediment, 9.7% ®sh bones and scales, 8.6% unidenti®able tissue, 5.4% crustacean fragments, 18.3% ophiuroid ossicles but also identi®able fragments from a variety of polychaetes, identi®ed by their setae. N. siquijorensis may, thus, consume living prey, i.e. possibly polychaetes and ophiuroids but is, largely, a consumer of carrion. Britton and Morton (1994b) pointed out that subtidal Nassarius mendicus from Monterey Bay, California, recognized and consumed carrion, but had limited powers of distance chemoreception, i.e. from a maximum distance of 10 cm. Liu and Morton (1994) demonstrated that N. siquijorensis recognized carrion, moved purposefully towards it and consumed it. The distance for the majority of N. siquijorensis to detect food was 35 cm. N. siquijorensis is dominant in soft subtidal habitats in Hong Kong because of an ability to withstand anoxia for periods of up to 8.5 days (Chan and Morton, 1997) and because of the ready availability of trawler-damaged carrion (Morton, 1996). Intertidal nassariids live on gently sloping beaches of sand and mud experiencing moderate wave action, a moderate to large tidal range and slowly receding tides. Tidal waters, ¯owing slowly over stranded carrion pick up chemical cues which nassariids are able to detect. Such scavengers normally lie quiescent in the sediment, only the siphon protruding above it, but emerge quickly once a chemical cue from carrion is received. Distance chemoreception takes them unerringly to its source. They can arrive from considerable distances, i.e. between 1.5 to 2.5 m for small intertidal species, e.g. Nassarius pyrrhus and Nassarius festivus from Western Australian and Hong Kong shores, respectively (Morton and Britton, 1991; Britton and Morton, 1992). Contact chemoreception completes the detection process and eversion of the proboscis (the `proboscis search reaction'; Kohn, 1983) initiates feeding. Nassariids move towards food rapidly and consume large quantities quickly, i.e. between 50 and 60% of the body weight for the intertidal Nassarius festivus (Morton, 1990; Cheung, 1994) and 61% of the body weight for the subtidal Nassarius siquijorensis (Liu and Morton, 1994) in feeding bouts lasting for an average of 8 and 12 min, respectively. After feeding, they depart the food and reburrow quickly. Snails clustered around moribund ¯esh constitute a potentially attractive source of food for larger predators, e.g. portunid (Stenzler and Atema, 1977) and xanthid crabs (Zipser and Vermeij, 1978), the latter attracted to the leaking body ¯uids of the object of nassariid interest and thus to the snails themselves. Tryon (1882) made the ®rst brief mention of the escape reaction of the genus Nassarius when he stated that some `Nassas' spring up and throw themselves over when disturbed whilst feeding. When the metapodial tentacles of ( 5 Nassarius) reticulata are stimulated by contact with the sea star Astropecten bispinosus, it exhibits a ¯ipping reaction of a series of somersaults. Weber (1924; in Carthy, 1958) illustrates the movement of Nassarius mutabilis as a twisting, side-to-side, forward leap rather than a somersault. Hoffman (1913, in Kohn, 1961) showed that chemicals such as chloroform, similarly elicit an escape reaction in Nassa reticulata. Gonor (1965) described a predator±prey relationship involving Nassarius luteostoma and its predator Natica B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 215 chemnitzii. A comparison of the literature for N. luteostoma, N. reticulata, and N. mutabilis shows that the escape response is somewhat similar in all three species. It differs only in whether the snail either somersaults or leaps diagonally forward. Nassarius vibex also utilizes an escape reaction when it is stimulated by either the sea star Luidia alternata or by the gastropods Fasciolaria hunteria and F. tulipa (Gore, 1966). Other examples of escape responses among gastropods are seen when potential prey comes into close proximity with a predator (Field, 1977; Parsons and Macmillan, 1979; Vermeij et al., 1987; Dix and Hamilton, 1993). When a Mediterranean trail-following opisthobranch, Haminoea navicula, is either molested or injured, conspeci®cs following its mucous trail exhibit an alarm response upon encountering the location where the trauma occurred (Cimino et al., 1991). Species of the sand-dwelling gastropod Umbonium perform twisting and leaping movements in the presence of potential predators (Kiruchi and Dol, 1987). The presence of either conspeci®c tissues or body ¯uids in water may also initiate either an escape or an alarm response. Within 10 min after introduction of water containing body ¯uids of crushed conspeci®cs, a signi®cant number of tide-pool inhabiting Littorina littorea moved to shelter, with some quadrupling their crawling speed immediately after exposure to the contaminated water (Hadlock, 1980). The mud snail Nassarius obsoletus [ 5 Ilyanassa obsoleta] moves toward and feeds upon crushed mussels (Modiolus [Geukensia] demissus) and snails (Littorina littorea), but departs rapidly when placed in the vicinity of crushed conspeci®cs (Atema and Burd, 1975). Stenzler and Atema (1977) expanded these observations by showing that three species, i.e. N. obsoletus, Nassarius vibex and Nassarius trivittatus, all responded negatively to crushed conspeci®cs, but that the escape response was diminished by hunger. This study was designed to determine: (a) whether or not Nassarius siquijorensis possesses either an alarm or escape response to the presence of dead conspeci®cs; (b) if so, how long after introduction of crushed conspeci®cs to a feeding group do individuals invoke such a response, and (c) to what extent can an alarm response be over-ridden by hunger, as expressed by 28 days starvation post-satiation. A similar study has been carried out with the intertidal species, Nassarius festivus (Morton et al., 1995), so that the last objective (d) was to compare these subtidal and intertidal species and to obtain an explanation for any differences identi®ed in terms of energy expenditure.

2. Materials and methods

Samples of subtidal Nassarius siquijorensis were collected using a trawl from Hong Kong waters at depths of between 10 and 30 m in April 1998. They were removed from the sediment while aboard ship and returned to the Swire Institute of Marine Science where they were maintained in aquaria with ¯owing seawater. Prior to experimentation, four sets of 240 individuals of N. siquijorensis were isolated in separate tanks and all fed to satiation with shrimps, one of their preferred food items (Liu and Morton, 1994). During the subsequent 28 days, the four isolated sets of N. siquijorensis were fed at pre-determined times, i.e. experimental meals were provided only on days 7 (for group 1), 14 (for group 2), 21 (for group 3) and 28 (for group 4) post-initial satiation on day 0. 216 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228

2.1. Feeding experiments

For each feeding experiment, six sets of 40 individuals of Nassarius siquijorensis, i.e. a total of 240 individuals, were placed in 40 cm 3 40 cm experimental trays with non-¯owing seawater. The 40 individuals in each tray were arranged in a 24-cm- diameter circle around three shrimps placed in the centre. For each of the six trays, the numbers of individuals feeding upon the shrimps were recorded each minute for 40 min. When 20 (50%) individuals had arrived at the bait, 5 g of coarse, shell, sand was sprinkled upon two of the feeding groups to simulate the mechanical but not chemical part of the stimulus introduction (Stenzler and Atema, 1977). For the second two feeding groups, the bodies of 10 crushed Monodonta labio (an intertidal gastropod N. siquijorensis would never have encountered and to simulate non-conspeci®c predation) were scattered upon the feeding nassariids. For the third two feeding groups, the bodies of 10 crushed N. siquijorensis (to simulate conspeci®c predation) were scattered upon them. Regardless of whether sand, crushed Monodonta or crushed conspeci®cs was added to each feeding cluster, feeding individuals were permitted to feed without other disturbance for the duration of the experiment, i.e. 40 min. Because few satiated Nassarius siquijorensis were attracted to the bait at time zero, a second experiment was conducted using different individuals in which six groups of 20 N. siquijorensis were placed initially upon the shrimps. After all individuals were so situated, two control groups received sand, two more groups received 10 crushed Monodonta while the two ®nal groups received the bodies of 10 crushed N. siqui- jorensis. In this case, the numbers of individuals remaining at the site of the bait, but not necessarily feeding, were recorded every minute for 40 min. From these experiments it has been possible to calculate the times taken for 50% of each group of control and experimental individuals to (a) ®nd the bait and (b) ascertain how long they remained feeding upon it, if at all, when sand or either crushed Monodonta or crushed conspeci®cs were added after increasingly long periods of starvation.

2.2. Activity

Forty individuals of Nassarius siquijorensis were each placed in separate 55-ml pots containing seawater and sand into which they could burrow. One group of 20 individuals was fed daily to satiation and the other group was starved for 8 days. The activity pattern of each individual was recorded from 06:00 to 16:00 h. Observations were made for 10 min each hour and the times spent moving, resting and buried in the sand in each observation period was recorded for each individual. The mean % time spent moving/ individual in the two groups in a 10-h cycle was compared by a Mann±Whitney rank sum test using arcsine transformed data (Zar, 1984).

2.3. Respiration rate

Ten individuals of Nassarius siquijorensis (shell lengths of between 10.4 and 18.5 mm) were placed in separate 55-ml plastic vials. The vials were ®lled with ambient B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 217 seawater and covered underwater with lids without trapping any air bubbles. All vials were placed in a large tank ®lled with seawater at a temperature of 208C (the average sea-bed temperature in Hong Kong). The N. siquijorensis were forced to move continuously by inverting the vials when they reached the tops. The experiment lasted for 20 min so that dissolved oxygen levels inside the vials would not fall below 30% saturation. Dissolved oxygen levels in each vial were measured by a YSI model 33 S-C-T oxygen meter at the start and at the end of the experiment. Ten more vials were ®lled with seawater without N. siquijorensis and served as controls. Ten individuals of Nassarius siquijorensis (shell lengths of between 10.9 and 18.4 mm) were put into separate 55-ml plastic vials. Sand from the beach outside the Swire Institute of Marine Science was dried in an oven at 808C for 2 days to halt microbial activity and 16.5 g were added to each vial. The experiment started only when all individuals were buried with their siphons protruded. The determination of respiration rate was as above. Differences in respiration rate during resting and moving were compared by a Student t-test. Energy expended on respiration was calculated using a 21 conversion factor of 13.98 J mg O2 (Ivlev, 1934).

3. Results

3.1. Feeding experiments

At the start of the feeding experiment, satiated Nassarius siquijorensis were clearly not interested in the food provided (Fig. 1). When afforded the opportunity to seek a further meal, on day zero, typically less than 5% did feed (Fig. 1A). Even when placed upon the shrimps, many moved off them (Fig. 1B). Although the presence of crushed conspeci®cs at the bait site may have helped drive away members of this group, illustrated in Fig. 1B by downward-pointing triangles, there was no signi®cant difference between these and the control individuals receiving sprinkled sand and crushed Monodonta (closed and open circles, respectively) with respect to the numbers remaining in the vicinity of the bait (Wilcoxon matched pairs signed ranks test, P 5 0.0652). The speed at which experimental and control groups of Nassarius siquijorensis approached the food is given in Table 1. Analysis of variance (ANOVA) indicated no signi®cant difference between two or more of the groups at the a 5 0.05 level with respect to rate of movement towards the food prior to additions of either sand, crushed Monodonta or crushed conspeci®cs (df 5 3, F 5 1.37, P 5 0.321). Despite the variance between some groups, when movement rates for experimental and control groups are combined (Table 1, Grand means), the mean values of 4.60 cm min21 , 2.06 cm min21 and 4.50 cm min21 for all individuals, indicate that there was no difference in the attractiveness of the bait between experimental and control groups, prior to the addition of crushed conspeci®cs, crushed Monodonta and sand, respectively. On day 7, the mean arrival time at the food for 50% of the Nassarius siquijorensis individuals was 6 min for the control group and 5 and 7 min for the crushed conspeci®c and crushed Monodonta experimental groups, respectively (Fig. 2A). A mean maximum 218 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228

Fig. 1. Feeding responses of recently (within 2 h) satiated Nassarius siquijorensis. (A) Percentage numbers of individuals reaching the bait from a distance of 24 cm. (B) Percentage numbers of individuals remaining at the bait, but not necessarily feeding, after being placed upon it. Filled triangles represent individuals exposed to crushed conspeci®cs and food; un®lled circles represent individuals exposed to crushed Monodonta and ®lled circles represent individuals exposed to sand.

Table 1 Mean rates (cm min21 ) at which 50% of experimental, Monodonta and control groups of Nassarius siquijorensis moved towards the bait, after 7, 14, 21 and 28-day periods of starvation Day Control Monodonta Experimental groups group group 7 2.00 1.71 2.40 14 4.00 2.40 6.00 21 6.00 2.40 6.00 28 6.00 1.71 4.00 Grand means 4.50 2.06 4.60 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 219 crushed . Closed after: (A) 7 days; (B) 14 days; (C) 21 days and (D) 28 days post initial satiation. (All experimental groups were Nassarius siquijorensis after 50% of each group commenced feeding. Fig. 2. Feeding responses of circles represent individualsMonodonta exposed to sprinkled sand after 50% of each group commenced feeding and open circles represent individuals exposed to placed 24 cm from the bait at time 0.) Filled triangles represent individuals exposed to crushed conspeci®cs after 50% of each group commenced feeding 220 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 of 20 experimental (50%) arrived at the bait on day 7, with this feeding density lasting less than 1 min. When crushed conspeci®c tissue was added, individuals began to move off it immediately. Three minutes later, 11 individuals (27%) of the experimental groups remained feeding whereas 5 min later, nine individuals (22.5%) were still at the bait. Animals continued to leave the bait until the end of the experiment. A mean maximum of 32.5 individuals (81.25%) of the sand and 34 (85.0%) of the crushed Monodonta control groups clustered around the bait. The feeding density in these two groups remained at . 20 individuals for 21 min after addition of sand and 26 min after addition of crushed Monodonta. An average of 14 (35.0%) feeding individuals remained in the sand control group even at the end of the experiment (40 min), as did 16.5 (41.25%) of the Monodonta control group. On day 14, the mean arrival time at the food for 50% of the individuals was 2 min for the sand control group and 2 and 5 min for the conspeci®c and Monodonta control groups, respectively (Fig. 2B). The addition of crushed conspeci®cs to the experimental groups did not, however, elicit an escape response, as it had on day 7. A mean maximum of 22.5 conspeci®c in¯uenced animals (56.25%) clustered about the bait on day 14, with feeding densities ¯uctuating around 50% of the test animals remaining after 27 min. Similarly, a mean maximum of 36.5 sand control and 34 Monodonta in¯uenced individuals (91.25 and 85.0%) clustered around the bait, with feeding densities of . 50% remaining after 28 and 29 min, respectively. On day 21, the mean arrival time at the food by 50% of the individuals was 2 min for the sand control group and 2 and 5 min for the conspeci®c and Monodonta in¯uenced groups, respectively (Fig. 2C). As on day 14, feeding individuals in the experimental groups did not depart the bait when crushed conspeci®cs were added to it. A maximum of 24 experimental animals (60.0%) clustered about the bait on day 21, with feeding densities of . 50% of the test animals remaining after 27 min. A mean maximum of 39.5 sand control individuals (98.75%) and 36 (90.9%) of the Monodonta in¯uenced individuals clustered around the bait, with feeding densities of . 50% remaining for 23 and 32 min, respectively. On day 28, the mean arrival time at the food for 50% of the sand control individuals was 2 min and 3 and 7 min, respectively for the conspeci®c and Monodonta in¯uenced groups (Fig. 2D). As on the previous days, the addition of crushed conspeci®cs to the experimental groups did not elicit an escape response. A mean maximum of 24 experimental animals (60.0%) clustered around the bait on day 28, with a feeding density of . 50% of the test animals remaining after 18 min. Similarly, a mean maximum of 34 sand control and 33.5 Monodonta in¯uenced individuals (85.0% and 83.75%) clustered around the bait, with feeding densities of . 50% remaining after 28 and 27 min, respectively. Two different patterns become clear when the data are re-organized and plotted from the times either sand or crushed Monodonta or crushed conspeci®cs were added to the control and experimental groups, respectively (Fig. 3). First, the responses of the sand-sprinkled group to the presence of food in the absence of crushed conspeci®cs or Monodonta tissue appear variable but, in fact, suggest a simple pattern. One week following a meal in which all individuals were fed to satiation, i.e. day 7, there was a slight interest in feeding again (Fig. 3A, circles). After another week, day 14, more B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 221

Fig. 3. Percentage numbers of Nassarius siquijorensis feeding after 50% of each set had commenced feeding on the bait and either: (A) after sand was added to the feeding assemblage; (B) crushed Monodonta or (C) crushed conspeci®cs were added. (The days after initial satiation are indicated by the following symbols: day 7, circles; day 14, down-pointing triangles; day 21, squares; day 28, diamonds). 222 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 control individuals spent time feeding than they did on day 7 (Fig. 3A, downward- pointing triangles). By day 21, the majority of the group had gone 2 weeks without feeding, which is re¯ected in the highest (almost 100%) percentage number of individuals joining the feeding cluster on this day (Fig. 3A, squares). Finally, by day 28 (Fig. 3A, diamonds), there was a further, slight, decreased interest in feeding. A similar pattern to the above was seen with the feeding individuals exposed to crushed Monodonta. One week following the `fed to satiation' meal, i.e. day 7, there was a renewed interest in feeding again (Fig. 3B, circles). By day 14, fewer individuals initially showed an interest in feeding again (Fig. 3B, downward pointing triangles) but did return to the food eventually. By day 21, most individuals (| 90%) showed an interest in feeding (Fig. 3B, squares) and by day 28 (Fig. 3B, diamonds), the same numbers as seen on day 7 were feeding. The second pattern is even clearer. With the addition of crushed conspeci®cs to the feeding cluster on day 7 (Fig. 3C, circles), a signi®cant percentage of Nassarius siquijorensis left it. As this did not happen with the control and Monodonta in¯uenced groups, we must assume that the addition of damaged nassariid tissue triggered an alarm response in some feeding individuals. By day 14, hunger overrode the risk of predation, suggested by the presence of crushed conspeci®cs. Even with the addition of conspeci®c tissue, however, the feeding clusters on day 14 (Fig. 3C, downward pointing triangles) remained on the food. A similar pattern was repeated on days 21 and 28 (Fig. 3C, squares and diamonds, respectively). The percentages of N. siquijorensis remaining on the food, even after 14, 21 and 28 days were, overall, well below the numbers remaining on the sand control and crushed Monodonta-in¯uenced food on the same days (| 50± 60% versus 80±100%).

3.2. Activity

Well-fed individuals of Nassarius siquijorensis were more active than starved individuals. Three out of 20 individuals moved within the 10 h of the study period while only one of the starved individuals was active. For the rest of the time, however, both the well-fed and starved individuals remained resting and buried in the sand. The mean % time spent moving per individual was 1.563.67 and 0.562.24 for well-fed and starved individuals, respectively. A Mann±Whitney rank sum test, however, showed no signi®cant difference between the two groups (T 5 430, P 5 0.595), that is, regardless of its level of hunger, N. siquijorensis is an `await' scavenger. It rarely forages.

3.3. Respiration rate

The mean respiration rate of resting individuals of Nassarius siquijorensis 21 21 (0.12560.0407 mg O2 h individual ) was signi®cantly lower (T 5 1211.0, P , 21 21 0.0001) than moving individuals (0.18760.0479 mg O2 h individual ). When dry tissue weights were used in calculating respiration rate, the mean values for resting and 21 21 moving individuals were 0.07060.022 mg O2 h g dry weight and 0.09960.023 mg 21 21 O2 h g dry weight, respectively. There was, again, a signi®cant difference between the two groups (T 5 1195.0 P , 0.0001). B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 223

3.4. Energy budget

As no data on absorption ef®ciency and energy expenditure on mucus production and excretion have been obtained, it is not possible to calculate a complete energy budget for Nassarius siquijorensis. Notwithstanding, the great majority, | 80%, of nassariid energy is thought to be spent on respiration, hence their typically quiescent life style in the absence of food (Cheung, 1994). The calculation used to determine energy expended on respiration (J day21 ) was as follows:

Energy expended on respiration day21 individual21 when moving 5 Respiration rate 3 conversion factor 3 % time moving 3 24 h 21 21 21 5 0.187 mg O22 h individual 3 13.98 J mg O 3 0.015 3 24 h 5 0.94 J day21 individual21

Energy expended on respiration day21 individual21 when buried 5 Respiration rate 3 conversion factor 3 % time buried 3 24 h 21 21 21 5 0.125 mg O22 h individual 3 13.98 J mg O 3 0.985 3 24 h 5 41.31 J day21 individual21

The total energy expended on respiration by Nassarius siquijorensis was, thus, 42.25 J individual21 day21 of which 97.78% was expended when buried, the remainder whilst moving (Table 2). Liu and Morton (1994) have calculated for Nassarius siquijorensis the mean time spent feeding on a single meal (19.14 min individual21 ) and the mean amount of food eaten during a single meal individual21 (0.090 g dry weight). The mean dry tissue weight of N. siquijorensis of the same size range as used in this experiment was calculated to be 0.335 g and using the above information the mean consumption rate min21 can, therefore, be calculated as 0.014 g dry weight g dry weight21 min21 . The energy intake (J meal21 ) for Nassarius siquijorensis was calculated as follows: mean calori®c value of shrimp (Penaeus setiferus; 80 kcal 100 g21 (Spotte, 1992), i.e. 1 cal54.1868 J)3mean consumption rate3feeding time meal21 (min)5(80 000/100)3 4.1868 J g21 30.014 g dry weight g dry weight21 min21 30.335 g dry weight319.14 min5300.67 J meal21 .

Table 2 The energy budget of Nassarius siquijorensis Buried Moving Percentage of time spent (%) 98.50 1.50 21 21 Respiration rate (mg O2 h individual ) 0.125 0.187 Energy expended on respiration (J day21 ) 41.31 0.94 42.25 (Total) Mean feeding time meal21a (min) 19.14 Energy intake (J meal21 ) 300.67 a After Liu and Morton (1994). 224 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228

Table 3 A comparison of the energy budgets calculated for Nassarius siquijorensis and Nassarius festivus N. siquijorensis N. festivusa Total energy expended on respiration (J day21 ) 42.25 7.09 Energy intake (J meal21 ) 300.67 144.20 Average energy cost of existence day21 (% of the energy ingested meal21 ) 14 5 Ingested food containing the energy needed for 24 h of existence (times) 7 20 a After Cheung (1994).

The average energy cost of existence day21 is thus: (41.3110.94)/300.6731005 14.05% of the energy ingested meal21 . Energy intake for Nassarius siquijorensis was, thus, 300.67 J individual21 meal21 . The energy intake during a single meal can, therefore, provide seven times the energy required for survival. Table 3 compares the calculated energy budgets for Nassarius siquijorensis and Nassarius festivus (the latter after Cheung, 1994). N. siquijorensis expended more energy on respiration than N. festivus. Although the energy intake for N. siquijorensis is higher than that for N. festivus, the average energy cost of existence day21 is higher for the former than the latter. At a single meal, N. siquijorensis can ingest food containing seven times the energy needed for 24 h of existence while N. festivus can ingest food containing 20 times.

4. Discussion

Like its intertidal counterpart, Nassarius festivus, this study suggests that, for Nassarius siquijorensis, hunger is not re¯ected in speed to food, that is, individuals always move at a relatively constant rate. The time taken for 50% of the experimental animals to reach the food, however, differed with the state of hunger. This observation is, we believe, a measure of an individual's decision about whether or not to seek the sensed food. It thus seems that each individual responds to the scent of food and makes a decision about whether or not to ®nd it. This is probably related to the strength of the stimulus, as a re¯ection of its proximity, and the degree of individual hunger. When nassariids feed, they do so to satiation and voraciously. Morton (1990) and Cheung (1994) estimated that Nassarius festivus eats between 50 and 60% of its body weight in a single meal, as does the subtidal Nassarius siquijorensis (Liu and Morton, 1994). Once fed to satiation, however, subsequent meals are smaller (Liu and Morton, 1994; Cheung, 1994). Nassariids thus have degrees of hunger. Cheung (1994) has calculated that for N. festivus fed to satiation, the energy obtained would provide it with |20 days of expenditure. The energy obtained for N. siquijorensis, however, would provide it with only |7 days of expenditure. It thus seems that the subtidal N. siquijorensis needs to feed more frequently than the intertidal N. festivus. Since nassariids do not usually forage for food, except species of Bullia on high wave energy B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 225 beaches (Brown, 1971, 1982), most metabolic energy is required for respiration while quiescent. Cheung (1997), however, showed that the oxygen consumption rate of active N. siquijorensis was 74% higher than for resting animals and an equivalent ®gure of 50% has been obtained in this study. Nassariids can survive periods of starvation much greater than 20 days, i.e. at least 100 days for N. festivus (Morton, 1990). Nassarius obsoletus similarly can survive up to 120 days without food (Curtis and Hurd, 1979) although this species is an obligate omnivore, requiring both plant and material in its diet if growth and reproduction are to be maintained (Brown, 1982). There is no estimate of the maximum number of days that N. siquijorensis can survive without food, but a recent study of the tolerance of this species to anoxia showed that it can survive periods of starvation for .30 days (Chan and Morton, 1997). The proximity of dead and dying conspeci®cs surely signals the likely presence of a predator at a point food source, as was demonstrated for the tide-pool-inhabiting Littorina littorea (Hadlock, 1980). Experimental re-creation of this scenario by Atema and Burd (1975) and Stenzler and Atema (1977) for Nassarius obsoletus [5Ilyanassa obsoleta] also suggested this was true. The latter authors also showed that when nassariids were denied food for several days and then fed carrion, they were markedly less-inclined to leave the meal in the presence of water exposed to crushed conspeci®cs than well-fed individuals presented with the same choice. The study by Morton et al. (1995) extended the scope of the above scenario and showed that for starvation periods of up to 14 days there was a marked propensity for Nassarius festivus to cease feeding. Following 21 and 28 days starvation, however, individuals continued to feed, despite the presence of crushed conspeci®cs. The critical time for hunger to override the perceived risk of predation for this species was thus deemed to lie between 14 and 21 days. In this study, it has been shown that for periods of starvation of up to 7 days, Nassarius siquijorensis would cease feeding if crushed conspeci®cs were added to the food, i.e. they would leave the meal in the likelihood of the presence of a predator suggested by the proximity of dead and dying conspeci®cs. After 14 days of starvation, however, hunger overrode the perceived risk of predation and individuals continued to feed despite the presence of crushed conspeci®cs. The critical time for hunger to override the perceived risk of predation for this species thus seems to lie between 7 and 14 days. The above laboratory studies have been con®rmed in the ®eld for seven species of Australian nassariid and buccinid intertidal scavengers (McKillup and McKillup, 1995) with supporting evidence from laboratory studies (McKillup and McKillup, 1994, 1995). These authors argue that food availability in¯uences not only scavenger growth and reproduction but also population size. Assuming that the availability of carrion is naturally limiting (Britton and Morton, 1994b), it is likely that hunger will typically override the risk of predation, at least intertidally. The difference discerned here between the subtidal Nassarius siquijorensis and the intertidal Nassarius festivus and their reactions to the presence of dead conspeci®cs is probably due to a difference in the days that a meal can provide for their respective energy expenditures. Table 3 shows that the total amounts of energy expended on respiration by N. siquijorensis and N. festivus are 42.56 and 7.09 J day21 , respectively. Innes (1981) in a review of energy consumption by intertidal gastropods has shown that mid and low shore species have similar oxygen consumption rates in air and water, a 226 B. Morton, K. Chan / J. Exp. Mar. Biol. Ecol. 240 (1999) 213 ±228 difference only being detected when, in the former situation, the mantle cavity is drained of water (Houlihan, 1979). N. festivus is a middle to low shore species that, by burrowing, is always immersed (Britton and Morton, 1992). This suggests that the difference between the two species is a real one and that N. siquijorensis has a six times higher respiration rate than N. festivus. Although the average energy intake during a meal is 300.67 J meal21 , the average energy cost of existence day21 is |14% of the energy ingested meal21 , which implies that the animal can, at a single meal, ingest food containing only seven times the energy needed for 24 h survival. Conversely, N. festivus can ingest food containing 20 times the energy needed for 24 h survival (Cheung, 1994). A similar value (18 times) was obtained for the similarly intertidal Bullia digitalis (Brown, 1981). It thus seems that the subtidal N. siquijorensis needs to feed more frequently than the intertidal N. festivus. The subtidal Nassarius mendicus, from California, fed more frequently than the intertidal Bullia digitalis from South Africa, the former averaging 3.14 days (Britton and Morton, 1994b) between meals, whereas the latter fed every 7±10 days (Stenton-Dozey and Brown, 1988). Liu and Morton (1994) showed that starvation caused N. siquijorensis to feed for longer and to ®nd food more quickly. This was also shown on days 14 and 21 of this study. Fig. 2B and C have steeper initial slopes (black triangles) than Fig. 2A, i.e. the food was found more quickly by more individuals and a higher percentage of them remained feeding with time. Although the length of time nassariids feed is a re¯ection of the time since the last meal and the degree of achieved satiation at it, it may also be a re¯ection of the individual's hunger-driven need to consume, opportunistically, what it can in order to survive in the face of potential predation. For a nassariid, therefore, there are both advantages and risks involved in pursuing a scavenging mode of life. The bene®t of being able to exploit carrion, albeit an ephemeral food resource, is tempered by two costs: (a) being exposed to possible predation while feeding and (b) the possibility of greater time intervals between meals. Both costs affect survival. The perceived risk of predation overrides hunger when starvation is not an important consequence of abandoning food in the presence of potential predation. Hunger overrides the risk of predation when an important consequence of abandoning a meal is death by starvation, even if continued presence at the food may result in death by predation. In the latter case, the probability of being consumed by a predator is no greater and, likely, less than the probability of starvation, if the meal is abandoned. For scavenging nassariids, hunger overrides the risk of predation when the likely alternative is starvation (Morton et al., 1995). This general conclusion seems to be true for both subtidal, as shown in this study, and intertidal species (Morton et al., 1995). In the former, i.e. N. siquijorensis, however, hunger overrides risk more quickly because it has to feed more often to balance the demands of an energy budget that spends more on respiration than the latter, i.e. N. festivus.

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