Foraging by marine scavengers: Effects of relatedness, bait damage and hunger

267

Journal of Sea Research 36(3/4): 267-273 (1996)

FORAGING BY MARINE SCAVENGERS: EFFECTS OF RELATEDNESS, BAIT DAMAGE AND HUNGER P.G. MOORE 1 AND J. HOWARTH 2 I University Marine Biological Station, Millport, Isle of Cumbrae, Scotland KA28 OEG, UK 2Faculty of Applied Sciences, University of the West of England, Frenchay Campus, Coldharbour Lane, BristoI,BS16 1QY, UK

ABSTRACT Field studies using fish-baited creels have confirmed that Carcinus maenas, Necora puber and Pagurus bernhardus (Crustacea: Decapoda), Buccinum undatum (Gastropoda) and Asterias rubens (Echinodermata) are prominent scavenging species in shallow waters in the Clyde Sea area. Capture rates of these species by creels baited with dead fish plus variously damaged C. maenas were examined in the field. The addition of substantially fractured C. maenas significantly reduced the capture of conspecifics, but significantly enhanced the capture of the taxonomically unrelated species A. rubens. The remaining crustacean taxa (of the above) were unaffected by this treatment. The magnitude of the response was related strongly to the extent to which C. maenas were damaged. The effects of hunger on these responses were tested in a laboratory experiment in which the responses of starved and fed batches of C. maenas were investigated. Starved crabs remained attracted to fish bait, despite the proximity of dead conspecifics. Conversely, crabs of the fed batch were significantly more reluctant to enter creels containing damaged conspecifics. The localized presence of odours emanating from dead conspecifics did not cause crabs to remain inactive in shelter. We conclude that taxonomic relatedness to bait, degree of carcass damage and hunger of the scavenger all interact in determining foraging decision-making even by so-called generalist scavengers.

Keywords: Scavenger, foraging behaviour, food selection, Carcinus, Necora, Pagurus, Buccinum, Asterias, Clyde Sea, Scotland.

1. INTRODUCTION Dead conspecifics often act as a deterrent to trap entry by epibenthic scavenging species. Chapman & Smith (1974) reported that the addition of recently killed edible crabs, Cancer pagurus L., to fish bait reduced the catch of live C. pagurus in creels by 54%. Hancock (1974) reduced the catch of shore crabs, Carcinus maenas (L.), and increased the catch of whelks, by adding dead C. maenas to traps. Shelton (in Hancock, 1974), however, reported that crushed C. maenas was a first-class bait for conspecifics in maze trials. Richards & Cobb (1987) deployed crushed spider crabs effectively to keep worthless conspecifics out of traps set for commercial American lobster and crab species. Miller (1990) has extensively reviewed the literature on the effectiveness of crab and lobster traps, and confirms that dead deca-

pods in traps generally reduce catches of conspecifics. Earlier, he (Miller, 1977) noted that dead snow crabs, Chionoectes opilio (O. Fabricius), were ineffective at attracting the same species off Newfoundland, although cannibalism (inter alia) in this species has been reported recently (Wieczorek & Hooper, 1995). Inhibition of feeding in response to crushed conspecifics has also been noted in the pebble crab, Philyra laevis, by McKillup & McKillup (1992). Similar avoidance of, and alarm responses to, dead conspecifics have been reported among scavenging gastropod molluscs, e.g. the whelks Ilyanassa obsoleta (Say) (Atema & Burd, 1975) and Nassarius dorsatus Recling (McKillup & McKillup, 1994). The intertidal herbivorous snail Planaxis sulcatus (Born) has also been reported by McKillup & McKillup (1993) to shun crushed conspecifics.

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The capacity of crustaceans to discriminate between closely related species on the basis of chemical cues has been well established in other contexts, e.g. for settling cyprid larvae (Knight-Jones, 1955; Larman & Gabbott, 1975; Dineen & Hines, 1994), yet the question - Just how closely related do scavenging species need to be in order to be deterred by, rather then attracted to, a particular carcass? seems not to have been subjected to detailed systematic analysis. Field observations, using fish-baited creels, have reinvestigated (cf. Nickell & Moore, 1991) the composition of, and possible 'live' interactions between, an assemblage of scavenging megabenthic invertebrates living in shallow waters in the Clyde Sea area. To test the importance of the degree of taxonomic relatedness to scavenger attraction vs deterrence at bait, field experiments (using fish-baited or fish plus dead C. maenas-baited creels) have investigated the responses of five invertebrate species: the shore crab (C. maenas), the velvet swimming crab (N. puber), the hermit crab (Pagurus bernhardus (L.)), the edible whelk (Buccinum undatum L.) and the common starfish (Asterias rubens L.) to assess the influence on those responses of proximity to dead crabs (C. maenas). Carcinus maenas and N. puber are both representatives of the family Portunidae within the Crustacea: Decapoda: Brachyura. Pagurus bernhardus represents a different decapod infraorder (Anomura), while B. undatum (Mollusca, Gastropoda) and A. rubens (Echinodermata, Asteroidea) represent different phyla. Inhibitions towards consumption of conspecifics are traditionally regarded as only being overcome by extreme hunger (Stenzler & Atema, 1977; McKillup & McKillup, 1995; but note Smith, 1966, p.31). Shortage of food for scavengers, however, may be a natural feature of some environments (e.g. intertidally, see McKillup & McKillup, 1994). Cannibalism does seem to be a feature of the behaviour both of P. bernhardus (Lancaster, 1988) and C. maenas (Shelton, in Hancock, 1974), although its prevalence in C. maenas has been stated to be low (Ropes, 1968). Far from being an aberrant practice though, cannibalism must be accepted as a normal (if minority) facet of population regulatory processes in a wide range of organisms (Smith, 1966), especially among resource-monopolists like flour beetles or termites (references in Allee et aL, 1949). Cannibalism may also be initiated by injury (Allee et al,, 1949), especially in hungry animals (McKillup & McKillup, 1995). Therefore, the degree to which hunger and carcass damage might influence the attractiveness to C. maenas of conspecific carrion was also tested in the laboratory. Trials comparing the effect on catch of the five species above of adding C. maenas with differing degrees of carapace damage to fish bait were also accomplished in situ.

2. MATERIAL & METHODS 2.1. FIELD DATA Standard west coast Nephrops creels (base 40 x 55 cm; two hard-eyed entrances, 7.5 cm diam. diagonally opposed; mesh size 3.5 cm across stretched diagonal; deployed in 2 fleets, 1 of 9, 1 of 10 creels) were deployed in the field over a sandy bottom near Fairlie, Firth of Clyde (lat. 55°44.04 ' N; long. 4°53.07'W). These were baited with half a salted mackerel (ca 100 g) and fished at a water depth of 3 to 4 m (with various soak times; weather- and ship availability-dependent). The catch of the five species above was monitored on five occasions between 12 Oct. and 6 Nov. 1995 to provide baseline data. Current speeds were not measured, but typically are <0.3 m.s -1 locally (Nickell & Moore, 1992b). On five subsequent dates (6 - 10 Nov. 1995), experimental deployments of creels were accomplished in which, in addition to the usual half mackerel bait, a single, freshly killed C. maenas (carapace substantially fractured) was added to alternate creels in each fleet. The numbers of the five species under consideration subsequently captured were recorded for 'fish-baited' and for 'fish plus dead C. maenas-baited' creels for comparison. A further series of five experimental creel deployments (14 - 20 Nov. 1995) compared the effect of adding freshly killed C. maenas with different degrees of carapace damage (to fish-baited creels) on catches of the five species above. Alternate creels in each fleet were baited either with 'bait plus minimally damaged C. maenas' or 'bait plus substantially fractured C. maenas' for comparison of the catches of the five species above. Minimally damaged crabs were pithed using the recommended technique for humane killing of crabs: using an awl inserted through the mouthpart bundle and disrupting the nerve ring (Edwards, 1979). Substantially damaged crabs were struck once mid-carapace with a peen. 2.2. LARGE TANK EXPERIMENT A large, outdoor tank (fibreglass; 300 x 90 cm) filled to a depth of 35 cm with sea water and shaded beneath removable planking was used for this experiment (20 - 27 Nov. 1995). Two ranks of five shelters, constructed from house bricks, were placed along the tank's sidewalls. Two Nephrops creels were submerged longitudinally along the midline of the tank, one between each opposed rank of shelters. Each day, creels were freshly baited with ca 50 g of a standard fish bait (chunks of tinned tuna, brine preserved) placed inside a cylindrical (7.0 [diam.] x 5.0 cm), screw-cap container with lightly perforated lid and base. A constant flow of sea water was maintained through the tank, entering at one end and exiting via a standpipe at the other. The incoming water

ASPECTS OF FORAGING BEHAVIOUR OF MARINE SCAVENGERS

269

TABLE 1 Summary of field catches of five scavenger species over 19 fish-baited creels in baseline series of samples (1995), see text for site details. Mean sea (surface) temperature 12.2"C. Overall percentages in parentheses with totals. C. maenas N. puber B. undatum P. bernhardus A. rubens

12 Oct+

25 Oct.

1 Nov.

3 Nov.

6 Nov.

Total

273 13 48 64 22

132 49 26 102 18

262 4 0 51 55

330 4 1 51 91

196 22 0 87 28

1193 (62.6) 70 (3.7) 75 (3.8) 355 (18.6) 214 (11.2)

stream was split such that a symmetrical flow of water past the creels was achieved along the floor of the tank. A batch of adult C. maenas was split into two stock groups (n = 60+ each) regardless of crab size (range 50-75mm carapace diam.) or sex. One stock tank was fed ad libitum (on chopped fresh cod) for one week before beginning the experiment and feeding continued for the week of the experiment, the other continued without food for the same period. The reactions to bait of these crabs were then sequentially tested (20 - 27 Nov. 1995) in the experimental tank, according to a randomized experimental protocol, comparing the responses of 20 crabs to 'bait only', 'bait plus freshly killed, minimally damaged C. maenas', or 'bait plus freshly killed, substantially fractured C. maena~ treatments for both fed and unfed groups. Individual crabs were used only once. Daylength was approximately 8L:16D during the course of this trial. Seawater temperatures varied between 9 and 11"C (mean 10.6°C, n = 12). Mean current speed was 0.03 m's

.

2.3. STATISTICAL ANALYSES Field catch data of the five species above were transformed using IOgl0(X + 1) to stabilize the variance prior to Pearson correlation analysis of the baseline data, or analysis of the field experimental data using the MINITAB general linear model (GLM) of ANOVA for unbalanced designs, in which transformed catches were analysed against three factors (bait, fleet and date) and their interactions. The laboratory experiment was analysed using Chi-squared testing of appropriate sub-category 2 x 3 contingency tables.

3. RESULTS 3.1. FIELD STUDIES a) Baseline data and species interactions (all alive) Table 1 shows that the five species investigated remain among the dominant invertebrate species captured in baited creels in shallow water locally (cf. Nickell & Moore, 1991), confirming the ecological relevance of their selection. Table 1 also highlights the general consistency in relative abundance of most of these five species between five sampling dates. The exception was B. undatum; the catches of which declined with time. Table 2 displays the correlation matrix of transformed catch data for individual creels between C. maenas, N. puber, B. undatum, R bernhardus and A. rubens for the baseline series of samples taken with fish-baited creels. There were significant correlations only between C. maenas catches and those of R bemhardus and A. rubens, and between N. puber and R bernhardus catches. b) Effect of dead C. maenas on field captures of five scavenging species Field data (Table 3) revealed significantly reduced (P<0.05) attraction of C. maenas, and very highly significantly enhanced (P<0.001) attraction of A. rubens to those creels to which a substantially fractured C. maenas had been added. Catches of N. puber, B. undatum and R bernhardus were not significantly (P>O.05) affected by this treatment (as mentioned above, the catches of B. undatum declined severely as time progressed, see Table 1). The GLM analyses, unsurprisingly, revealed vari-

TABLE 2 Matrix of Pearson product moment correlation coefficients derived from individual creel catches of five scavenging species in the baseline field data (transformed), 92 d.f., * = P<0.05, ** = P<0.01, ns = not significant at P = 0.05. N. puber B. undatum R bernhardus A. rubens

C. maenas

N. puber

B. undatum

R bernhardus

-0.155ns 0.091 ns 0.273 0.218*

0.199 ns 0.290 -0.024 ns

0.192ns -0.082ns

-0.98 ns

270

RG. MOORE & J. HOWARTH

TABLE 3 Descriptive statistics (mean per creel)(F and P values derived from GLM analyses done on transformed [loglo (n+l)] data) of five scavenger species captured in fish-baited creels to which a substantially fractured C. maenas was either added (N = 50) or not (N = 45). Mean sea (surface) temperature 11.5°C. *** = P<0.001, * = P<0.05, ns. = not significant at P = 0.05. Species C, maenas N. puber B. undatum A. rubens R bernhardus

with C. maenas

no C. maenas

F(1,94)

P

9.64 0.46 0.50 13.84 5.34

12.13 0.53 0.09 2.98 4.27

6.96 }.00 :~68 d0.90 (}.64

0.01 * 0.97ns 0.06ns 0.00 0.43ns

ously significant effects attributable to fleet identity and sampling date, together (often) with significant interaction terms between bait treatment, fleet identity and sampling date. These have been ignored presently, however, since they do not bear directly on the current investigation. Their simultaneous consideration in the analyses, however, enhances our confidence in the particular statistics derived for bait treatment.

3.2. LARGE TANK EXPERIMENT While there was no significant difference among bait treatments (different degrees of conspecific damage) for the starved crabs (XL= 1.68, 2df, ns), there was a significant difference for fed crabs (X2 = 10.00, P<0.01) (table 5). 4. DISCUSSION

c) Effect of degree of damage to dead C. maenas on field catches of five scavenging species Table 4 details the analysis of the field catch data for C. maenas, N. puber, B.undatum, A. rubens and P. bernhardus in fish-baited creels to which either a substantially fractured C. maenas, or a minimally damaged (freshly killed) C. maenas, was added. The resultant catch of C. maenas was very highly significantly (P<0.001) reduced in creels with substantially damaged, compared with minimally damaged, conspecifics. Conversely, A. rubens were very highly significantly (P<0.001) elevated in creels to which heavily damaged C. maenas had been added. Catches of the other three species recorded were unaffected by this difference in treatment (P>0.05). However, as before, low catch numbers may be responsible for the lack of significance in the B. undaturn data.

The five co-existing species investigated consistently feature among the shallow-water marine invertebrates most commonly caught in baited traps, or filmed in situ, both locally (see Nickell & Moore, 1991, 1992a,b) and further afield (Eriksson et al., 1975). Clearly, their scope for interactions (see Richards et aL, 1983; Lapointe & Sainte-Marie, 1992; Miller & Addison, 1995) will have direct and indirect influences on what species combinations occur in particular traps. Our field catch data suggested that in some cases, species' abundances in creels were related to the live presence of others. Thus catches of C. maenas in the baseline series of samples were significantly (positively) associated, inter alia, with those of R bernhardus (Table 2). However, Eriksson et al. (1975) reported that R bernhardus will "stay at a distance' when C. maenas is present. Lancaster (1988) also

TABLE 4 Descriptive statistics (mean per creel)(F and P values derived from GLM analyses of transformed [Iogle (n+l)] data) of five scavenger species captured in fish-baited creels to which either a substantially fractured (N = 50), or a minimally damaged (N = 45) C. maenas was added. Mean sea (surface) temperature 11.7°C. *** = P<0.001, ns. = not significant at P = 0.05 Species

max.damaged

min.damaged

FI ~.94)

P

C. maenas

16.46

22.44

10.39

0.00"**

N. puber

1.32

1.31

0.00

0.94ns

B, undatum

0.82

0.44

3.23

0.07ns

A. rubens

10.74

4.87

1(].84

0.00"**

R bernhardus

7.12

5.47

0.91

0.34ns

ASPECTS OF FORAGING BEHAVIOUR OF MARINE SCAVENGERS

271

TABLE 5 Catch data for C. maenas (starved vs fed) in large tank experiment; see text for details. Treatment

starved

fed

captured

not captured

captured

not captured

bait only bait + substantially fractured

17

3

18

2

C. maenas

18

2

9

8

5

15

bait +minimally fractured C. maenas

X2 P

15

1.68 0.4317

noted that R bernhardus is fed upon by brachyuran crabs; Cancer pagurus especially. Yet hermit crab numbers (all animals undamaged) were positively correlated with both brachyuran species presently encountered. A possible explanation may, however, be indirect: that feeding by the dominant crab species (C. maenas) fragments bait and disperses carrion odours more rapidly thus attracting other highly mobile species, like N. puber, R bernhardus and A. rubens. So direct interactions might still only be slight: for instance, Nickell & Moore (1992b) reported that the few interspecific encounters observed in situ (using underwater TV) between A. rubens and other species were generally characterized by mutual disinterest. Correspondingly, it was maintained by Hancock (1955) and Crothers (1968) that C. maenas does not eat A. rubens. On the other hand, however, it should be recalled that Mackie et aL (1968) have described avoidance reactions of B.undatum to A. rubens, and live B. undatum is known to be preyed upon by crabs and starfish, including Asterias (Thomas & Himmelman, 1988). Also, in spite of being primarily algivorous (Choy, 1986; Norman & Jones, 1992), N.puber will consume small C. maenas (ap Rheinallt & Hughes, 1985). Scope for intraspecific agonistic interactions limiting trap entry, particularly among aggressive crab and hermit crab species (Lancaster, 1988; Nickell & Moore, 1992b; Cyr & Sainte-Marie, 1995), however, remains an additional agency influencing directional choices at particular creels [and may be the agency responsible for the generally solitary N. puber recorded per creel; this species being particularly aggressive (Smith et aL, 1994)] after recognition of the impact of any interspecific interactions. The rank order of abundance of these species captured overall in the field (C. maenas> P. bernhardus> A. rubens > N. puber> B. undatum) will relate both to the summation of such biological interactions and to the different mobilities of the species considered, as well as to considerations of habitat suitability. Thus, C. maenas and R bernhardus are known to respond more rapidly to the presence of bait than B. undatum and A. rubens (Eriksson et aL, 1975; Himmelman,

5

10.00 0.0067

1988; Nickell & Moore, 1992b; Kaiser & Spencer, 1996) and so would be expected to dominate field catches in baited traps (as found here) for this reason alone. These realizations apart, we have not sought to elucidate further the interactions between the five investigated species when alive. Our field experimental data support the idea that the degree of taxonomic relatedness between a scavenger and an item of carrion modifies the attraction of otherwise acceptable bait. [Note: Van Engel (1958) noted that oily fish are a preferred bait for blue crabs; see also Ropes (1968) on C. maenas.] Thus the presence of dead C. maenas with substantial wounds significantly depressed the attraction of fish bait to conspecifics, when compared with the alternatives tested, Le. absence of dead C. maenas or presence of minimally damaged C. maenas. The other decapod crustaceans considered (N.puber, Rbernhardus) were not influenced in their choice of creels by either of these alternative bait treatments, neither was the gastropod B.undatum (but see below). By contrast, the taxonomically unrelated (to C. maenas) species, A. rubens, showed the opposite trend to that shown by C. maenas, i.e. the presence of substantially fractured C. maenas additional to the fish bait significantly enhanced the attractiveness of that bait to starfishes [note also that the data for B.undatum, which is equally unrelated to C. maenas, revealed the same trend, with differences between treatments only marginally failing to reach statistical significance]. B. undatum has been reported by others to be attracted to dead crabs in the field (Sch&fer, 1972; Hancock, 1974; Martel et aL, 1986; Himmelman, 1988; Moore & Wong, 1995a), as has A. rubens (Moore & Wong, 1995a; see above). Chapman & Smith's (1974) value of 54% depression of catch of Cancer pagurus, brought about by insertion of a recently killed conspecific into fish-baited traps (see also Richards & Cobb, 1987), is considerably larger than our field findings (21% reduction) for Carcinus maenas catches in creels with substantially fractured, freshly killed C. maenas compared with creels having no added conspecific. This difference, plus the comment by Shelton (in Hancock,

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1974), that crushed C. m a e n a s was a first-class bait for conspecifics in maze trials, suggests that cannibalism features more widely in the diet of C. m a e n a s than in that of the edible crab, perhaps reflecting differences in population pressures and/or food availabilities (see Introduction). It also, however, raises the question: how hungry were the crabs investigated by different authors (see below)? It was clear from the laboratory experiment, both that past feeding history exerted considerable control on the extent to which C. m a e n a s is inhibited from foraging due to the presence of dead conspecifics, and that only substantially damaged conspecifics deterred welt-fed shore crabs from foraging (see also McKillup & McKillup, 1995). The fact that, in the field, C. m a e n a s did show significant inhibition towards substantially damaged conspecifics infers that this shallow-sublittoral population of C. m a e n a s (cf. McKillup & McKillup, 1994 on intertidal systems) is not short of food, at any rate at the time of year studied. This inference is further substantiated by the results of the laboratory experiment. The degree to which epibenthic scavengers may be inhibited from, or encouraged in, foraging by the perception of carrion signals in their vicinity can thus be seen to depend on a variety of factors, like degree of decomposition of carrion (Ropes, 1968; Hancock, 1974; Zimmer-Faust & Case, 1982; Lokkeborg & Johannessen 1992; Moore & Wong, 1995b), extent of taxonomic relatedness between scavenger and carrion, degree of damage to carrion (see also Zimmer-Faust & Case, 1982) and food availability; the outcome of which all depends on the hunger of the scavenger (see herein). Clearly, being a generalist omnivore does not preclude a scavenger from having a capacity for dietary discrimination.

Acknowledgements.--We are most grateful to the staff of the Specimen Sales department at UMBS Millport for allowing us to use (and temporarily modify) their holding facilities, and to the skipper and crew of RV 'Aplysia' for help with collecting data at sea. Dr J.M. Hills is thanked for discussions on experimental design and computation. Dr R.J.A. Atkinson and Dr MJ. Kaiser kindly helped us with references to pertinent literature and gave their critical comments on an earlier draft of the manuscript. The helpful comments of two anonymous referees eliminated further errors.

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(accepted 7 May 1996)