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Alternative predation tactics of a tropical naticid gastropod
J. Exp. Mar. Biol. Ecol., 1987, Vol. 111, pp. 109-119 Elsevier
109
JEM 00925
Alternative predation tactics of a tropical naticid gastropod Alan D. Ansell’ and Brian Morton2 ‘Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, Oban, Argyll. U.K., ‘Department of Zoology, University of Hong Kong. Hong Kong
(Received 12 March 1987; revision received 6 April 1987; accepted 24 April 1987) Abstract: Aquarium observations of naticid gastropods from Hong Kong show that different species attack their bivalve prey in different ways. Natica gualteriana and Glossaulax didyma appeared always to use
conventional modes of boring, i.e., through one shell valve, before consuming the prey, but some larger prey of C. didyma with incomplete borings were consumed after having apparently suffocated before boring was complete. In contrast, Polinices tumidus prey may be side-bored, edge-bored (i.e., through the commisure of the valves) or suffocated and consumed without boring. The frequency of each of these modes of attack vary with different prey species. Non-boring predation, in aquarium experiments, accounted for 14.7-54.9% of attacks with different species of prey. Suffocated prey were found to be enwrapped in a thick, viscous coat of mucus, which in partially consumed prey showed a round hole overlying the ventral shell gape marking the entrance hole made by the proboscis. The observations reveal considerable flexibility in predation behaviour in this tropical naticid and have important implications in the interpretation of naticid predation rates in recent and fossil dead shell assemblages. Key words: Predation; Naticid gastropod; Bivalve
INTRODUCTION
Naticid gastropods, which are regular components of benthic infaunal communities at all latitudes (Taylor & Taylor, 1977) are specialist predators of shelled prey, most commonly bivalve molluscs, but also in certain areas gastropods (Berry, 1981, 1984; Hughes, 1985) or ostracods (Reyment, 1966). The commonest and most familiar mode of attack involves the use, alternately, of the radula and accessory boring organ, to bore through the shell of the prey, at a point away from the shell margin, forming a circular hole which has a characteristic countersunk appearance. This predation behaviour, especially the handling of the prey, is stereotyped, with the result that the boreholes in the prey are often closely grouped in characteristic distributions on the shell for particular predator-prey combinations, while differences in these groupings for different prey species indicate differences in the way each is handled by the predator. Recently, Taylor (1980), Vermeij (1980) and Ansell & Morton (1985) have described cases of naticids which bore certain bivalve prey species through the commisure of the Correspondence address: A. D. Ansell, Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, P.O. Box 3, Oban, Argyll PA34 4AD, U.K.
110
A.D.ANSELLANDB.MORTON
valve margins, rather than through either shell valve. Such edge-boring behaviour has been described only for certain tropical species of Polinices, where it is used mainly in attacking thicker shelled prey, or prey protected by heavy shell sculpture. Although boring seems to be an obligatory phase in the stereotyped predation behaviour of most naticid species, it has also been recognized that other species may consume some types of prey without first boring through the shell, or may act as scavengers. Thus, Polinices duplicatus from North America will consume the razor clam Ensis directus without first boring, entry being possible because the E. directus shell does not completely seal the mantle cavity when the adductors contract and the naticid can insert its radula through the pedal or siphonal gape (Edwards, 1975; Schneider, 1981). Polinices lewisi employs a similar strategy in attacking Tresus nutalli (Reid & Fiesen, 1980). Similarly, gastropods may be attacked through the aperture (Edwards, 1969; Hughes, 1985), the proboscis and radula forcing an entry around the flexible margins of the operculum. Here we describe a further example, in which a naticid consumes prey bivalves which can close completely without first boring through the shell. The naticid species involved, P. tumidus, is one which has previously been shown to employ both conventional side-boring and edge-boring techniques when attacking different prey. During previous experiments in which P. tumidus and other naticid predators from waters around Hong Kong were kept with various potential prey in the aquarium (Ansell & Morton, 1985) it was noted that many of the bivalves used as prey with P. tumidus, but not with other species, were found gaping and empty of tissue, but lacking a borehole. In some individual experiments, the number of such prey, presumed to have been eaten, but not bored, could be > 50% of the total consumed, whilst in concurrent experiments with other naticids, only very low numbers of dead unbored prey were found, presumably resulting from mortality from other causes than predation. Vermeij (1980) recorded similar results in experiments using P. tumidus at Guam: in his experiments 3 1y0 of the bivalves consumed by P. tumidus were eaten without injury to the shell. Vermeij assumed that suffocation of the bivalve occurred “while being enveloped by the predator’s foot before drilling has proceeded very far”. The observations described here confirm that P. tumidus does indeed suffocate many of its prey and add new information on this aspect of naticid predation behaviour.
MATERIALS AND METHODS
The aquarium experiments reported here were carried out in a similar manner to those described earlier (Ansell & Morton, 1985). Each combination of predator and prey was maintained in a small (0.05 m2) aquarium in the recirculating sea water system of the Zoology Department, University of Hong Kong, at a temperature of 2 1 k 1 ‘C. A layer of natural sand in each aquarium provided a sediment in which the animals could burrow. Each aquarium was examined daily to determine which prey had been attacked,
111
PREDATION TACTICS OF A NATICID GASTROPOD
and bored prey were removed and usually replaced by equivalent size individuals of the same species. The main series of experiments were designed to explore some aspects of choice of prey by P. tumidu~. The detailed results of these will be described elsewhere; here on& the observations relevant to discussion of the mode of attack on different prey will be described. A limited number of observations were also made on Gloss&ax didyma, and these together with some previously unpublished results with ~at~c~ ~a~te~a~a are also reported. P. tumidus were collected from the lower intertidal of the beach at Hoi Sing Wan (Starfish Bay), New Territories, and the species of bivalve used as prey were also collected there, but over a wider area of the intertidal. G. didyma and N. ~alte~~a~a were collected by dredging from Mirs Bay.
RESULTS AND CONCLUSIONS N. GUALTEHANA
The results of the Iimited experiments with iV. ~aIte~ana carried out in 1983-84 are summarized in Table I. Over a 21-wk period, two N. gwlteriana attacked a total of 14 prey, all of which were conventionally side-bored. TABLE
I
Prey consumed in individual experiments with Natica gualteriana confined with different prey. Percentage of the total prey (N) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB). Prey
N
S
E
NB
Tapes philippinarum Anomalocard~a squamosa Aractodea striara
5 4 5
100 100
0 0
0 0
100
0
0
The results of observations on two G. didyma made in 1986 are summarized in Table II. The majority of attacks made were by side-boring near the umbone, but a varying proportion of prey were suffocated. The G. dia’ymawere large (4.7 and 5.2 cm shell length) and were often observed in the aquarium inactive, with single prey held in a pouch-like invagination formed in the underside of the posterior region of the foot (Fig. 1). Tapes p~ii~~~na~rn were generally attacked by these P. d~dyma by side-boring, but, with the largest individual prey (30-39 mm shell length), most attacks resulted in only incomplete borings. Nonetheless, the bivalves died, and were consumed, and when removed from the aquarium were found to be covered with a coating of clear mucus.
A.D. ANSELL AND B. MORTON
112
Although limited, these observations are of interest since they show non-boring predation by suffocation occurriug as an alternative predation strategy in a G~~ssu~~x species which otherwise attacks prey only by conventional side-boring (Ansell & Morton, 1983). TABLE II
Prey consumed in individual experiments with single Gfossaufax didyma confined with different prey. Percentage of the total prey (N) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB). Prey
Tapes phif~pina~m Caecella chinensis Atactodea stn’ata Glauconome chinensis AaQmafo~a~diasq~amasa
Individual predator A
B
61.6 -
0 13.0 25.0 57.1 77.8
N
S
E
NB
16 23 4 7 9
50.0 87.0 75.0 42.9 22.2
0 0 0 0 0
50.0’ 13.0 25.0 57.1 77.8
* Includes some incompletely side-bored (see text).
shell
propodium
proboscis Fig. 1. Glassaulax didyma. A, diagrammatic section to illustrate method of “holding” or “carrying” prey; B and C, views illustrating position adopted when boring prey.
PREDATION TACTICS OF A NATICID GASTROPOD
113
They also indicate that incomplete naticid boreholes in bivalve shells from death assemblages do not necessarily imply that the prey survived the attack. P. TUMIDUS The incidence of conventional side-boring, edge-boring and non-boring predation with different prey in experiments with P. tumidus in 1986 is summarized in Table III. There was wide variation in the incidence of non-boring predation both between different prey, and between individual P. tumidus preying on the same prey species. For individual P. tumidus attacking the same prey species, the percentage of the total attacks observed which were non-boring ranged from 0 to 90.9. There is some suggestion in the results that the incidence of non-boring predation may increase as the naticid grows, since both of the individuals in which a low incidence was recorded were small (A and E, Table III). For different prey species, the mean percentage of total attacks observed which were non-boring ranged from 14.7% for the thin-shelled venerid Gluuconome chinensis to 54.9% for T. philippinarum. There was no clear relationship between shell thickness, or degree of shell ornamentation, and the percentage of non-boring attacks. The two species which showed the highest rate of non-boring attacks (T. phil@pinarum and Anomalocardia squamosa) were both species which are readily available as prey to P. tumidus in its normal habitat in Hong Kong. These results confirm the indications in earlier experiments (Vermeij, 1980; Ansell & Morton, 1985) that many of the prey consumed by P. tumidus are not bored before being consumed. By removing more frequently both predators and prey from the experimental aquaria than in 1983-84 we were able to observe the means by which this result was achieved. Many individual bivalves recovered were found to be enwrapped in a thick, highly viscous, coat of mucus, which formed a complete envelope around the closed shell. In others, the shell within this envelope was gaping, and the tissue partially or completely consumed. In these latter, overlying the region of the ventral gape of the shell, there was a round hole in the mucous envelope through which the proboscis of the naticid had clearly been extended. In a few cases, this hole was accompanied by a slight chipping of the shell margins immediately under the hole in the mucous envelope, but rarely was the shell damaged sufficiently for it to have been recognizable as a case of edge-boring predation in the absence of the mucous envelope. Our conclusion is that non-boring predation by P. tumidus is the result of suffocation of the bivalve principally arising from the presence of the surrounding mucous envelope secreted by the predator. Most naticids which have been observed attacking their prey use mucous secretions to immobilize and attack the prey to the foot prior to boring, and can crawl over the surface and burrow with the prey attached in this way (Ziegelmeier, 1954). The complete mucous envelope secreted by P. tumidus would seem to be a development of this secretion. The results of these aquarium experiments therefore strongly suggest that non-boring predation must make a significant contribution to overall predation by P. tumidus in this
Tapes ~hjlip~~~a~rn Caecella chinensb Atactodea striata Donax faba Glauconome chinensis Anomalocardia squamosa
Prey
64.5 16.7
41.2 24.3 -
20.0
2
53.3
-
22.2
40.0
(;I 90.9
75.0
ck 25.0 25.0 0 0
33.3
$1
Individual predator
0 0 60.0 0
0 -
25.0
0 0 0 -
0
t:, 44.9 21.4
31.6 32.4 0
19 34 23
13.4
52.9 56.5
52.6
34.7 64.3
31.7
S (total x,”
49 28
142
N
43.5
54.9
NB
Prey consumed in individual experiments with single (1) or pairs (2) of Polinices tumidus confined with different choices of prey. Percentage of the total prey (A’) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB).
TABLE III
3 m
F
E
?2
? P
PREDATION TACTICS OF A NATICID GASTROPOD
115
and other areas. They also highlight the flexibility of predatory behaviour in P. tumidus which is widely dist~buted and often ab~d~t in steeds and shallow sheltered sandy shore communities throughout the Indo-Pacific.
A
loo
Species
B
m
Side-bored
0
Edge-bored
m
Non-bored
A
8 0
C
D
E
F
C
D
E
F
1.0
1
100 f
Species
Q
A
Fig. 2. Proportions of side-boring, edge-boring and non-boring attacks on different prey species by A, Polinices tumidus, and B, GIossuulux didyma, in aquarium experiments in 1986. The ratios of edge and non-boring predation/total attacks (0) and of edge-boring predation/edge + side-boring attacks (V) are also shown. Prey species: A, Caecella chinensis; B, Donaxfaba; C, Glauconome chinensis; D, Ataeiodea striata; E, Tapes phil~p~~~~rn; F, Anorn~i~rd~ squamosa.
DISCUSSION
P. tumidus has now been shown to adopt at least three different tactics in dealing with bivalve prey: conventional side-boring, edge-boring, and non-boring predation. None of these is used exclusively against any particular prey, at least not under aquarium conditions, but the frequency of occurrence of a p~cul~ method differs with different prey (Fig. 2A). Conventional side-boring is the method adopted most frequently against thin-shelled prey, such as the mesodesmatid Caecella chinensis. The proportion of edge to side-boring attacks increases in thicker-shelled prey (Ansell & Morton, 1985) and in some species, e.g., A. squamosa, side-boring is rarely or never attempted. Non-boring
+ Wk 2-6 only; * wk 2-18.
1.20 0.40 2.50 1.50
1.65 0.55 3.00 1.00
-
2.10 0.95 3.50 2.50
0.75 (1.5)
-
1.90 (4.5)
(t)
2.3 1.85 4.50 4.00
(mean) NB (mean) (max) NB (max)
0.60 (1.5)
1.35 (2.5)
0.85 (2.5)
0.80 (1.5)
2.25 0.75 3.00 1.00
D’ (2)
Total Total Total Total
Z)
0.40 (1.5)
0.60(1.5)
(i)
1.35 0.24 4.00 1.00
0.12 (1.0) 0.47 (2.0)
0.24 (1.0) 0.18 (1.0)
0.35 (2.0)
FE
1.85 0.18 3.00 1.00
0.24 (1.0)
0.24 (1.0)
0.35 (1.0) 0.29 (1.0)
0 (0)
z;
Mean (max) no. of prey attacked *predator - ’ . wk - ’
Tapes philippinarum CaeceNa chinens& Atactodea striata Donax faba Glauconome chinensis Anomalocardia squamosa
Prey
1.10 0.30 2.50 1.oo
-
-
1.10 (2.5) -
1.29 0 3.00 0
0.18 (1.0) 0.06 (1.0) 1.oo(3.0)
0.06 (1.0)
The mean and maximum rates of predation by Polinices tumidus when confined with different prey choices in aquarium experiments at 21 “C (Wk 2-11).
TABLE IV
PREDATION TACTICS OF A NATICID GASTROPOD
117
attacks account for m 15% of attacks in most species. There is no clear relationship between shell thickness or degree of shell ornamentation and the percentage of non-boring attacks, but it is interesting to observe that the highest percentage of non-boring attacks concerned the two species of prey most readily available to P.~midu~ at the site from which the experimental animals were collected, i.e., T. ~~il~~i~u~rn and A. squ~musu. Non-boring predation accounted for 54.9 and 43.5%) respectively, of all attacks observed on these two species. Hughes (1985) suggested that learning may be important in modifying attack behaviour in naticids, so that predators which have coexisted with prey which can be consumed without drilling would show a higher incidence of non-drilling predation than those which lack previous experience. The P. tumidus used in these experiments, and all the bivalves, were collected from Starfish Bay (Hoi Sing Wan), New Territories, but only T. phiiippi~~m and A. ~q~rno~~ ase readily available to the shallow burrowing predators in the lower zone of the intertidal beach where P. tumidus is abundant. The process of boring through the shell of the prey accounts for a high proportion of total prey handling time in naticids (Kitchell et al., 1981; Hughes, 1985) as it does in other boring gastropods. Non-boring predation methods will be relatively advantageous where the time required for entry without boring is signitlcantly reduced compared with that required for boring. Suffocation seems unlikely to present much advantage in this respect since many bivalves withst~d extended periods of oxygen depletion without gaping. No information on tolerance of anoxic conditions is available for the species used as prey for P. tumidus either in these or earlier experiments, but Day (1980) showed that in T. philippinarum the valves gaped within a few hours of emersion, perhaps indicating a low tolerance in this one species. Non-boring predation, by suffocation might be selectively advantageous, also, if (a) it were energetically less demanding, or (b) it allowed search for further prey to continue during periods which would normally be spent in boring through the shell of pre~ous~y captured prey. Both seem plausible hypotheses, but cannot be further explored with the data currently available. The mean and maximum rates of predation recorded in the present experiments for P. tumidus preying on a range of different bivalves show no consistently higher rates for non-boring predation compared with either edge-boring or side-boring (Table IV), although the highest numbers (9 and 9) of bivalves found predated in any single period both included high numbers (7 and 8) of unbored prey. The immediate cause of gaping of the prey is interpreted here as suffocation, but it is also possible that the process is facilitated by the presence in the pedal mucus or other secretion of the predator of a narcotizing toxin. Such a toxin has been implicated in predation by thaidid gastropods on barnacles (Huang, 1971, 1972; Palmer, 1982). Although there is no evidence for the presence of a narcotizing toxin in either the pedal or salivary secretion of naticids, the possibility of such a toxin being involved in cases of non-boring predation deserves further consideration. Evidence for the exploitation of the type of non-bo~ng predation described here by naticid gastropods other than P. tumidus remains equivocal (Table V), and its origin can
A.D. ANSELL
118
AND B. MORTON
only be a subject of speculation. Presumably non-boring predation by naticid-like gastropods preceded the evolution of the boring habit in the group, but non-boring predation in recent species may be a secondary development. In P. tumidus the habit seems to be closely linked with that of edge-boring, but the observations on G. &yma TABLE V
Predation strategies adopted by four naticid gastropod species from the Indo-Pacific region: S, side-boring; E, edge-boring; NB, non-boring predation-suffocation. Authority
Species
S
E
NB
&z&a ~aite~ana GIossaulax didyma Folinices melanostoma PO&ices tumidus
+ + + +
-
? +
3-4
t
?
3,4
f
+
L&3,4
134
1 = Taylor, 1980; 2 = Vermeij, 1980; 3 = Ansell & Morton, 1985; 4 = this paper.
suggest strongly that in this species suffocation often follows only from prolonged, ultimately incomplete side-boring. Whatever the origin, however, it is clear that in some tropical species, non-boring predation is a frequently adopted alternative predation tactic. In contrast, colder water species seem normally to bore the shells of their prey, a conclusion reached by Kitchell et al. (1986) which is in accord with our own concIusions from observations on European naticids. The obse~ations recorded here, and other recent observations on a variety of naticid species from different geographical regions show, however, that there is more diversity of predation behaviour between species, than was previously believed. The evidence remains too small for any generalizations to be made. One consequence is that uncertainties will remain in the interpretation of recent death assemblages of bored, unbored and incompletely bored shells, and of similar palaeontological material, especially where these derive from tropical or subtropical habitats.
We gratefully acknowledge a grant from the Jeffreys Association Ltd., which enabled A. D. Ansell to make a research visit to the University of Hong Kong. We are also grateful for the help of Ms. K.Y. Chan for help in maintaining the laboratory experiments. REFERENCES ANSELL,A. D. & B. MORTON,1985. Aspects of naticid predation in Hong Kong with special reference to the defensive adaptations of Bassina (Callanaitis) calophylla (Bivalvia). In, Proceedings of the Second international Workshop on Malacofaa~a of Hong Kong and Southern China, Hong Ibrtg, 1983, edited by B. Morton & D. Dudgeon, Hong Kong University Press, Hong Kong, pp. 635-660.
PREDATION TACTICS OF A NATICID GASTROPOD
119
BERRY, A.J., 1984. Umbonium vestiutium (L.) (Gastropoda, Trochacea) as the food source for naticid gastropods and a starfish on a Malaysian sandy shore. J. MON. Stud., Vol. 50, pp. l-7. BERRY,A. J., 1985. Predation by Narica maculosa Lamarck (Naticidae : Gastropoda) upon the trochacean gastropod Umbonium vestiurium (L.) on a Malaysian shore. J. Exp. Mar. Biol. Ecol., Vol. 64, pp. 71-89. DAY, J. E., 1980.Correlation ofgill physiology, emersion survival, and intertidal distribution ofthree bivalves from Hong Kong. In, Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1977, edited by B. S. Morton, Hong Kong University Press, Hong Kong, pp. 211-217. EDWARDS, D.C., 1969. Predation of Olivella biplicata including a species specific predator avoidance response. Vehger, Vol. 11, pp. 326-333. EDWARDS,D. C., 1975. Preferred prey of Polinices duplicatus in Cape Cod inlets. Am. Malacol. Union Inc. Bull., Vol. 40, pp. 17-20. HUANG, C. L., 1971. Pharmacological properties of the hypobranchial gland of Thais haemastoma (Clench). J. Pharm. Sci., Vol. 60, pp. 1842-1846. HUANG, C.L., 1972. Pharmacological investigations of the salivary gland of Thais haemastoma (Clench). Toxicon, Vol. 10, pp. 111-l 17. HUGHES, R.N., 1985. Predatory behaviour ofNatica unifasciata feeding intertidally on gastropods. J. MON. Stud., Vol. 51, pp. 331-335. KITCHELL,J. A., C. H. BOGGS, J. F. KITCHELL& J. A. RICE, 1981. Prey selection by naticid gastropods: experimental tests and application to the fossil record. Paleobiol., Vol. 7, pp. 533-552. KITCHELL,J. A., C. H. BOGGS,J. A. RICE, J. F. KITCHELL,A. HOFFMAN& J. MARTINELL,1986. Anomalies in naticid predatory behaviour; a critique and experimental observations. Mulucol., Vol. 27, pp. 291-298. PALMER,A. R., 1982. Predation and parallel evolution: recurrent parietal plate reduction in balanomorph barnacles. Palaeobiol., Vol. 8, pp. 31-44. REID, G. B. & J. A. FEISEN, 1980. The digestive system ofthe moon snail Polinices lewisii(Gould, 1847) with emphasis on the role of the oesophageal gland. Veliger, Vol. 23, pp. 25-34. REYMENT,R.A., 1966. Preliminary observations on gastropod predation in the western Niger delta. Palaeogeogr. Palaeoclimalol. Palaeoecol., Vol. 2, pp. 81-102. SCHNEIDER,D., 1981. Escape response of an infaunal clam Ensis directus Conrad 1843 to a predatory snail, Polinices duplicatus Say 1822. Veliger, Vol. 24, pp. 371-372. TAYLOR,J.D., 1980. Diets and habitats of shallow water predatory gastropods around To10 Channel, Hong Kong. In, Proceedings of the Firs? International Workshop on the Malacofauna of Hong Kong and southern China, Hong Kong, 1977, edited by B. Morton, Hong Kong University Press, Hong Kong, pp. 163-180. TAYLOR,J.D. & C.M. TAYLOR, 1977. Latitudinal distribution of predatory gastropods on the eastern Atlantic shelf. J. Biogeogr., Vol. 4, pp. 73-81. VERMEIJ,G. J., 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacol. Int. J. Malacol., Vol. 19, pp. 329-334. ZIEGELMEIER,E., 1954. Beobachtungen tiber den Nahrungswerb bei der Naticidae Lunatia nitida Donovan (Gastropoda: Prosobranchia). Helgol. Wiss. Meeresunters., Vol. 5, pp. l-33.
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JEM 00925
Alternative predation tactics of a tropical naticid gastropod Alan D. Ansell’ and Brian Morton2 ‘Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, Oban, Argyll. U.K., ‘Department of Zoology, University of Hong Kong. Hong Kong
(Received 12 March 1987; revision received 6 April 1987; accepted 24 April 1987) Abstract: Aquarium observations of naticid gastropods from Hong Kong show that different species attack their bivalve prey in different ways. Natica gualteriana and Glossaulax didyma appeared always to use
conventional modes of boring, i.e., through one shell valve, before consuming the prey, but some larger prey of C. didyma with incomplete borings were consumed after having apparently suffocated before boring was complete. In contrast, Polinices tumidus prey may be side-bored, edge-bored (i.e., through the commisure of the valves) or suffocated and consumed without boring. The frequency of each of these modes of attack vary with different prey species. Non-boring predation, in aquarium experiments, accounted for 14.7-54.9% of attacks with different species of prey. Suffocated prey were found to be enwrapped in a thick, viscous coat of mucus, which in partially consumed prey showed a round hole overlying the ventral shell gape marking the entrance hole made by the proboscis. The observations reveal considerable flexibility in predation behaviour in this tropical naticid and have important implications in the interpretation of naticid predation rates in recent and fossil dead shell assemblages. Key words: Predation; Naticid gastropod; Bivalve
INTRODUCTION
Naticid gastropods, which are regular components of benthic infaunal communities at all latitudes (Taylor & Taylor, 1977) are specialist predators of shelled prey, most commonly bivalve molluscs, but also in certain areas gastropods (Berry, 1981, 1984; Hughes, 1985) or ostracods (Reyment, 1966). The commonest and most familiar mode of attack involves the use, alternately, of the radula and accessory boring organ, to bore through the shell of the prey, at a point away from the shell margin, forming a circular hole which has a characteristic countersunk appearance. This predation behaviour, especially the handling of the prey, is stereotyped, with the result that the boreholes in the prey are often closely grouped in characteristic distributions on the shell for particular predator-prey combinations, while differences in these groupings for different prey species indicate differences in the way each is handled by the predator. Recently, Taylor (1980), Vermeij (1980) and Ansell & Morton (1985) have described cases of naticids which bore certain bivalve prey species through the commisure of the Correspondence address: A. D. Ansell, Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, P.O. Box 3, Oban, Argyll PA34 4AD, U.K.
110
A.D.ANSELLANDB.MORTON
valve margins, rather than through either shell valve. Such edge-boring behaviour has been described only for certain tropical species of Polinices, where it is used mainly in attacking thicker shelled prey, or prey protected by heavy shell sculpture. Although boring seems to be an obligatory phase in the stereotyped predation behaviour of most naticid species, it has also been recognized that other species may consume some types of prey without first boring through the shell, or may act as scavengers. Thus, Polinices duplicatus from North America will consume the razor clam Ensis directus without first boring, entry being possible because the E. directus shell does not completely seal the mantle cavity when the adductors contract and the naticid can insert its radula through the pedal or siphonal gape (Edwards, 1975; Schneider, 1981). Polinices lewisi employs a similar strategy in attacking Tresus nutalli (Reid & Fiesen, 1980). Similarly, gastropods may be attacked through the aperture (Edwards, 1969; Hughes, 1985), the proboscis and radula forcing an entry around the flexible margins of the operculum. Here we describe a further example, in which a naticid consumes prey bivalves which can close completely without first boring through the shell. The naticid species involved, P. tumidus, is one which has previously been shown to employ both conventional side-boring and edge-boring techniques when attacking different prey. During previous experiments in which P. tumidus and other naticid predators from waters around Hong Kong were kept with various potential prey in the aquarium (Ansell & Morton, 1985) it was noted that many of the bivalves used as prey with P. tumidus, but not with other species, were found gaping and empty of tissue, but lacking a borehole. In some individual experiments, the number of such prey, presumed to have been eaten, but not bored, could be > 50% of the total consumed, whilst in concurrent experiments with other naticids, only very low numbers of dead unbored prey were found, presumably resulting from mortality from other causes than predation. Vermeij (1980) recorded similar results in experiments using P. tumidus at Guam: in his experiments 3 1y0 of the bivalves consumed by P. tumidus were eaten without injury to the shell. Vermeij assumed that suffocation of the bivalve occurred “while being enveloped by the predator’s foot before drilling has proceeded very far”. The observations described here confirm that P. tumidus does indeed suffocate many of its prey and add new information on this aspect of naticid predation behaviour.
MATERIALS AND METHODS
The aquarium experiments reported here were carried out in a similar manner to those described earlier (Ansell & Morton, 1985). Each combination of predator and prey was maintained in a small (0.05 m2) aquarium in the recirculating sea water system of the Zoology Department, University of Hong Kong, at a temperature of 2 1 k 1 ‘C. A layer of natural sand in each aquarium provided a sediment in which the animals could burrow. Each aquarium was examined daily to determine which prey had been attacked,
111
PREDATION TACTICS OF A NATICID GASTROPOD
and bored prey were removed and usually replaced by equivalent size individuals of the same species. The main series of experiments were designed to explore some aspects of choice of prey by P. tumidu~. The detailed results of these will be described elsewhere; here on& the observations relevant to discussion of the mode of attack on different prey will be described. A limited number of observations were also made on Gloss&ax didyma, and these together with some previously unpublished results with ~at~c~ ~a~te~a~a are also reported. P. tumidus were collected from the lower intertidal of the beach at Hoi Sing Wan (Starfish Bay), New Territories, and the species of bivalve used as prey were also collected there, but over a wider area of the intertidal. G. didyma and N. ~alte~~a~a were collected by dredging from Mirs Bay.
RESULTS AND CONCLUSIONS N. GUALTEHANA
The results of the Iimited experiments with iV. ~aIte~ana carried out in 1983-84 are summarized in Table I. Over a 21-wk period, two N. gwlteriana attacked a total of 14 prey, all of which were conventionally side-bored. TABLE
I
Prey consumed in individual experiments with Natica gualteriana confined with different prey. Percentage of the total prey (N) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB). Prey
N
S
E
NB
Tapes philippinarum Anomalocard~a squamosa Aractodea striara
5 4 5
100 100
0 0
0 0
100
0
0
The results of observations on two G. didyma made in 1986 are summarized in Table II. The majority of attacks made were by side-boring near the umbone, but a varying proportion of prey were suffocated. The G. dia’ymawere large (4.7 and 5.2 cm shell length) and were often observed in the aquarium inactive, with single prey held in a pouch-like invagination formed in the underside of the posterior region of the foot (Fig. 1). Tapes p~ii~~~na~rn were generally attacked by these P. d~dyma by side-boring, but, with the largest individual prey (30-39 mm shell length), most attacks resulted in only incomplete borings. Nonetheless, the bivalves died, and were consumed, and when removed from the aquarium were found to be covered with a coating of clear mucus.
A.D. ANSELL AND B. MORTON
112
Although limited, these observations are of interest since they show non-boring predation by suffocation occurriug as an alternative predation strategy in a G~~ssu~~x species which otherwise attacks prey only by conventional side-boring (Ansell & Morton, 1983). TABLE II
Prey consumed in individual experiments with single Gfossaufax didyma confined with different prey. Percentage of the total prey (N) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB). Prey
Tapes phif~pina~m Caecella chinensis Atactodea stn’ata Glauconome chinensis AaQmafo~a~diasq~amasa
Individual predator A
B
61.6 -
0 13.0 25.0 57.1 77.8
N
S
E
NB
16 23 4 7 9
50.0 87.0 75.0 42.9 22.2
0 0 0 0 0
50.0’ 13.0 25.0 57.1 77.8
* Includes some incompletely side-bored (see text).
shell
propodium
proboscis Fig. 1. Glassaulax didyma. A, diagrammatic section to illustrate method of “holding” or “carrying” prey; B and C, views illustrating position adopted when boring prey.
PREDATION TACTICS OF A NATICID GASTROPOD
113
They also indicate that incomplete naticid boreholes in bivalve shells from death assemblages do not necessarily imply that the prey survived the attack. P. TUMIDUS The incidence of conventional side-boring, edge-boring and non-boring predation with different prey in experiments with P. tumidus in 1986 is summarized in Table III. There was wide variation in the incidence of non-boring predation both between different prey, and between individual P. tumidus preying on the same prey species. For individual P. tumidus attacking the same prey species, the percentage of the total attacks observed which were non-boring ranged from 0 to 90.9. There is some suggestion in the results that the incidence of non-boring predation may increase as the naticid grows, since both of the individuals in which a low incidence was recorded were small (A and E, Table III). For different prey species, the mean percentage of total attacks observed which were non-boring ranged from 14.7% for the thin-shelled venerid Gluuconome chinensis to 54.9% for T. philippinarum. There was no clear relationship between shell thickness, or degree of shell ornamentation, and the percentage of non-boring attacks. The two species which showed the highest rate of non-boring attacks (T. phil@pinarum and Anomalocardia squamosa) were both species which are readily available as prey to P. tumidus in its normal habitat in Hong Kong. These results confirm the indications in earlier experiments (Vermeij, 1980; Ansell & Morton, 1985) that many of the prey consumed by P. tumidus are not bored before being consumed. By removing more frequently both predators and prey from the experimental aquaria than in 1983-84 we were able to observe the means by which this result was achieved. Many individual bivalves recovered were found to be enwrapped in a thick, highly viscous, coat of mucus, which formed a complete envelope around the closed shell. In others, the shell within this envelope was gaping, and the tissue partially or completely consumed. In these latter, overlying the region of the ventral gape of the shell, there was a round hole in the mucous envelope through which the proboscis of the naticid had clearly been extended. In a few cases, this hole was accompanied by a slight chipping of the shell margins immediately under the hole in the mucous envelope, but rarely was the shell damaged sufficiently for it to have been recognizable as a case of edge-boring predation in the absence of the mucous envelope. Our conclusion is that non-boring predation by P. tumidus is the result of suffocation of the bivalve principally arising from the presence of the surrounding mucous envelope secreted by the predator. Most naticids which have been observed attacking their prey use mucous secretions to immobilize and attack the prey to the foot prior to boring, and can crawl over the surface and burrow with the prey attached in this way (Ziegelmeier, 1954). The complete mucous envelope secreted by P. tumidus would seem to be a development of this secretion. The results of these aquarium experiments therefore strongly suggest that non-boring predation must make a significant contribution to overall predation by P. tumidus in this
Tapes ~hjlip~~~a~rn Caecella chinensb Atactodea striata Donax faba Glauconome chinensis Anomalocardia squamosa
Prey
64.5 16.7
41.2 24.3 -
20.0
2
53.3
-
22.2
40.0
(;I 90.9
75.0
ck 25.0 25.0 0 0
33.3
$1
Individual predator
0 0 60.0 0
0 -
25.0
0 0 0 -
0
t:, 44.9 21.4
31.6 32.4 0
19 34 23
13.4
52.9 56.5
52.6
34.7 64.3
31.7
S (total x,”
49 28
142
N
43.5
54.9
NB
Prey consumed in individual experiments with single (1) or pairs (2) of Polinices tumidus confined with different choices of prey. Percentage of the total prey (A’) attacked by side-boring (S), edge-boring (E), or non-boring predation (NB).
TABLE III
3 m
F
E
?2
? P
PREDATION TACTICS OF A NATICID GASTROPOD
115
and other areas. They also highlight the flexibility of predatory behaviour in P. tumidus which is widely dist~buted and often ab~d~t in steeds and shallow sheltered sandy shore communities throughout the Indo-Pacific.
A
loo
Species
B
m
Side-bored
0
Edge-bored
m
Non-bored
A
8 0
C
D
E
F
C
D
E
F
1.0
1
100 f
Species
Q
A
Fig. 2. Proportions of side-boring, edge-boring and non-boring attacks on different prey species by A, Polinices tumidus, and B, GIossuulux didyma, in aquarium experiments in 1986. The ratios of edge and non-boring predation/total attacks (0) and of edge-boring predation/edge + side-boring attacks (V) are also shown. Prey species: A, Caecella chinensis; B, Donaxfaba; C, Glauconome chinensis; D, Ataeiodea striata; E, Tapes phil~p~~~~rn; F, Anorn~i~rd~ squamosa.
DISCUSSION
P. tumidus has now been shown to adopt at least three different tactics in dealing with bivalve prey: conventional side-boring, edge-boring, and non-boring predation. None of these is used exclusively against any particular prey, at least not under aquarium conditions, but the frequency of occurrence of a p~cul~ method differs with different prey (Fig. 2A). Conventional side-boring is the method adopted most frequently against thin-shelled prey, such as the mesodesmatid Caecella chinensis. The proportion of edge to side-boring attacks increases in thicker-shelled prey (Ansell & Morton, 1985) and in some species, e.g., A. squamosa, side-boring is rarely or never attempted. Non-boring
+ Wk 2-6 only; * wk 2-18.
1.20 0.40 2.50 1.50
1.65 0.55 3.00 1.00
-
2.10 0.95 3.50 2.50
0.75 (1.5)
-
1.90 (4.5)
(t)
2.3 1.85 4.50 4.00
(mean) NB (mean) (max) NB (max)
0.60 (1.5)
1.35 (2.5)
0.85 (2.5)
0.80 (1.5)
2.25 0.75 3.00 1.00
D’ (2)
Total Total Total Total
Z)
0.40 (1.5)
0.60(1.5)
(i)
1.35 0.24 4.00 1.00
0.12 (1.0) 0.47 (2.0)
0.24 (1.0) 0.18 (1.0)
0.35 (2.0)
FE
1.85 0.18 3.00 1.00
0.24 (1.0)
0.24 (1.0)
0.35 (1.0) 0.29 (1.0)
0 (0)
z;
Mean (max) no. of prey attacked *predator - ’ . wk - ’
Tapes philippinarum CaeceNa chinens& Atactodea striata Donax faba Glauconome chinensis Anomalocardia squamosa
Prey
1.10 0.30 2.50 1.oo
-
-
1.10 (2.5) -
1.29 0 3.00 0
0.18 (1.0) 0.06 (1.0) 1.oo(3.0)
0.06 (1.0)
The mean and maximum rates of predation by Polinices tumidus when confined with different prey choices in aquarium experiments at 21 “C (Wk 2-11).
TABLE IV
PREDATION TACTICS OF A NATICID GASTROPOD
117
attacks account for m 15% of attacks in most species. There is no clear relationship between shell thickness or degree of shell ornamentation and the percentage of non-boring attacks, but it is interesting to observe that the highest percentage of non-boring attacks concerned the two species of prey most readily available to P.~midu~ at the site from which the experimental animals were collected, i.e., T. ~~il~~i~u~rn and A. squ~musu. Non-boring predation accounted for 54.9 and 43.5%) respectively, of all attacks observed on these two species. Hughes (1985) suggested that learning may be important in modifying attack behaviour in naticids, so that predators which have coexisted with prey which can be consumed without drilling would show a higher incidence of non-drilling predation than those which lack previous experience. The P. tumidus used in these experiments, and all the bivalves, were collected from Starfish Bay (Hoi Sing Wan), New Territories, but only T. phiiippi~~m and A. ~q~rno~~ ase readily available to the shallow burrowing predators in the lower zone of the intertidal beach where P. tumidus is abundant. The process of boring through the shell of the prey accounts for a high proportion of total prey handling time in naticids (Kitchell et al., 1981; Hughes, 1985) as it does in other boring gastropods. Non-boring predation methods will be relatively advantageous where the time required for entry without boring is signitlcantly reduced compared with that required for boring. Suffocation seems unlikely to present much advantage in this respect since many bivalves withst~d extended periods of oxygen depletion without gaping. No information on tolerance of anoxic conditions is available for the species used as prey for P. tumidus either in these or earlier experiments, but Day (1980) showed that in T. philippinarum the valves gaped within a few hours of emersion, perhaps indicating a low tolerance in this one species. Non-boring predation, by suffocation might be selectively advantageous, also, if (a) it were energetically less demanding, or (b) it allowed search for further prey to continue during periods which would normally be spent in boring through the shell of pre~ous~y captured prey. Both seem plausible hypotheses, but cannot be further explored with the data currently available. The mean and maximum rates of predation recorded in the present experiments for P. tumidus preying on a range of different bivalves show no consistently higher rates for non-boring predation compared with either edge-boring or side-boring (Table IV), although the highest numbers (9 and 9) of bivalves found predated in any single period both included high numbers (7 and 8) of unbored prey. The immediate cause of gaping of the prey is interpreted here as suffocation, but it is also possible that the process is facilitated by the presence in the pedal mucus or other secretion of the predator of a narcotizing toxin. Such a toxin has been implicated in predation by thaidid gastropods on barnacles (Huang, 1971, 1972; Palmer, 1982). Although there is no evidence for the presence of a narcotizing toxin in either the pedal or salivary secretion of naticids, the possibility of such a toxin being involved in cases of non-boring predation deserves further consideration. Evidence for the exploitation of the type of non-bo~ng predation described here by naticid gastropods other than P. tumidus remains equivocal (Table V), and its origin can
A.D. ANSELL
118
AND B. MORTON
only be a subject of speculation. Presumably non-boring predation by naticid-like gastropods preceded the evolution of the boring habit in the group, but non-boring predation in recent species may be a secondary development. In P. tumidus the habit seems to be closely linked with that of edge-boring, but the observations on G. &yma TABLE V
Predation strategies adopted by four naticid gastropod species from the Indo-Pacific region: S, side-boring; E, edge-boring; NB, non-boring predation-suffocation. Authority
Species
S
E
NB
&z&a ~aite~ana GIossaulax didyma Folinices melanostoma PO&ices tumidus
+ + + +
-
? +
3-4
t
?
3,4
f
+
L&3,4
134
1 = Taylor, 1980; 2 = Vermeij, 1980; 3 = Ansell & Morton, 1985; 4 = this paper.
suggest strongly that in this species suffocation often follows only from prolonged, ultimately incomplete side-boring. Whatever the origin, however, it is clear that in some tropical species, non-boring predation is a frequently adopted alternative predation tactic. In contrast, colder water species seem normally to bore the shells of their prey, a conclusion reached by Kitchell et al. (1986) which is in accord with our own concIusions from observations on European naticids. The obse~ations recorded here, and other recent observations on a variety of naticid species from different geographical regions show, however, that there is more diversity of predation behaviour between species, than was previously believed. The evidence remains too small for any generalizations to be made. One consequence is that uncertainties will remain in the interpretation of recent death assemblages of bored, unbored and incompletely bored shells, and of similar palaeontological material, especially where these derive from tropical or subtropical habitats.
We gratefully acknowledge a grant from the Jeffreys Association Ltd., which enabled A. D. Ansell to make a research visit to the University of Hong Kong. We are also grateful for the help of Ms. K.Y. Chan for help in maintaining the laboratory experiments. REFERENCES ANSELL,A. D. & B. MORTON,1985. Aspects of naticid predation in Hong Kong with special reference to the defensive adaptations of Bassina (Callanaitis) calophylla (Bivalvia). In, Proceedings of the Second international Workshop on Malacofaa~a of Hong Kong and Southern China, Hong Ibrtg, 1983, edited by B. Morton & D. Dudgeon, Hong Kong University Press, Hong Kong, pp. 635-660.
PREDATION TACTICS OF A NATICID GASTROPOD
119
BERRY, A.J., 1984. Umbonium vestiutium (L.) (Gastropoda, Trochacea) as the food source for naticid gastropods and a starfish on a Malaysian sandy shore. J. MON. Stud., Vol. 50, pp. l-7. BERRY,A. J., 1985. Predation by Narica maculosa Lamarck (Naticidae : Gastropoda) upon the trochacean gastropod Umbonium vestiurium (L.) on a Malaysian shore. J. Exp. Mar. Biol. Ecol., Vol. 64, pp. 71-89. DAY, J. E., 1980.Correlation ofgill physiology, emersion survival, and intertidal distribution ofthree bivalves from Hong Kong. In, Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1977, edited by B. S. Morton, Hong Kong University Press, Hong Kong, pp. 211-217. EDWARDS, D.C., 1969. Predation of Olivella biplicata including a species specific predator avoidance response. Vehger, Vol. 11, pp. 326-333. EDWARDS,D. C., 1975. Preferred prey of Polinices duplicatus in Cape Cod inlets. Am. Malacol. Union Inc. Bull., Vol. 40, pp. 17-20. HUANG, C. L., 1971. Pharmacological properties of the hypobranchial gland of Thais haemastoma (Clench). J. Pharm. Sci., Vol. 60, pp. 1842-1846. HUANG, C.L., 1972. Pharmacological investigations of the salivary gland of Thais haemastoma (Clench). Toxicon, Vol. 10, pp. 111-l 17. HUGHES, R.N., 1985. Predatory behaviour ofNatica unifasciata feeding intertidally on gastropods. J. MON. Stud., Vol. 51, pp. 331-335. KITCHELL,J. A., C. H. BOGGS, J. F. KITCHELL& J. A. RICE, 1981. Prey selection by naticid gastropods: experimental tests and application to the fossil record. Paleobiol., Vol. 7, pp. 533-552. KITCHELL,J. A., C. H. BOGGS,J. A. RICE, J. F. KITCHELL,A. HOFFMAN& J. MARTINELL,1986. Anomalies in naticid predatory behaviour; a critique and experimental observations. Mulucol., Vol. 27, pp. 291-298. PALMER,A. R., 1982. Predation and parallel evolution: recurrent parietal plate reduction in balanomorph barnacles. Palaeobiol., Vol. 8, pp. 31-44. REID, G. B. & J. A. FEISEN, 1980. The digestive system ofthe moon snail Polinices lewisii(Gould, 1847) with emphasis on the role of the oesophageal gland. Veliger, Vol. 23, pp. 25-34. REYMENT,R.A., 1966. Preliminary observations on gastropod predation in the western Niger delta. Palaeogeogr. Palaeoclimalol. Palaeoecol., Vol. 2, pp. 81-102. SCHNEIDER,D., 1981. Escape response of an infaunal clam Ensis directus Conrad 1843 to a predatory snail, Polinices duplicatus Say 1822. Veliger, Vol. 24, pp. 371-372. TAYLOR,J.D., 1980. Diets and habitats of shallow water predatory gastropods around To10 Channel, Hong Kong. In, Proceedings of the Firs? International Workshop on the Malacofauna of Hong Kong and southern China, Hong Kong, 1977, edited by B. Morton, Hong Kong University Press, Hong Kong, pp. 163-180. TAYLOR,J.D. & C.M. TAYLOR, 1977. Latitudinal distribution of predatory gastropods on the eastern Atlantic shelf. J. Biogeogr., Vol. 4, pp. 73-81. VERMEIJ,G. J., 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacol. Int. J. Malacol., Vol. 19, pp. 329-334. ZIEGELMEIER,E., 1954. Beobachtungen tiber den Nahrungswerb bei der Naticidae Lunatia nitida Donovan (Gastropoda: Prosobranchia). Helgol. Wiss. Meeresunters., Vol. 5, pp. l-33.