Predatory behavior of the paguroid Dardanus venosus (H. Milne-Edwards, 1848) (Anomura: Diogenidae) on the snail Aurantilaria aurantiaca (Lamarck, 1816) (Gastropoda: Fasciolariidae)

Abstract

Paguroids are usually detritivorous organisms and the occurrence of predation on mollusks is very unusual. This contribution reports the occurrence of a predatory behavior of the paguroid Dardanus venosus (H. Milne Edwards, 1848) on the snail Aurantilaria aurantiaca (Lamarck, 1816). Single specimen of paguroid was found attacking the snail in a sea grass meadow dominated by Halodule wrightii Ascherson on the coast of Ceará, northeastern Brazil. The paguroid and gastropod specimens were brought to the laboratory and placed in an aquarium and the behavior was recorded by photos. Paguroid behavior was characterized by sequencial movements of chelipeds in the attack to the snail when the snail was hold by paguroid ambulatory legs. External lip of shell aperture, operculum and foot of the gastropod were severely damaged.

Key words
Hermit crab; behavior; gastropod; predation; feeding; Brazil

Paguroids comprise dense populations in intertidal environments. They use empty gastropod shells to protect themselves against predators, desiccation, and other environmental stresses (Reese, 1969; Bertness, 1981; Hazlett, 1981). In spite of the extensive literature on their behavior, most studies focus on how paguroids use their shelter, namely shell selection and assessment (Reese, 1963; Hazlett, 1966; Elwood and Neil, 1992; Mesce, 1993; Garcia and Mantelatto, 2001; Dominciano and Mantelatto, 2004; Turra and Leite, 2004; Biagi et al., 2006; Mantelatto et al., 2007; Meireles et al., 2008), shell fighting (Hazlett, 1981; Briffa et al., 1998), reproductive behavior (Hazlett, 1966; 1968a; 1972; 1986; Turra, 2005), and clustering behavior (Turra and Leite, 2000a).

However, other aspects of paguroid biology, such as feeding behavior, have not been addressed. Most of paguroid species are defined as generalist in diet and opportunistic in their feeding habits, with an omnivore-detritivore feeding style (Orton, 1927; Roberts, 1968; Caine, 1975, 1976; Hazlett, 1981; Benvenuto et al., 2003). The available data indicate that paguroids have a wide range of feeding strategies (Schembri, 1982a). They can be classified as detritivores (Orton, 1927; Roberts, 1968; Greenwood, 1972; Caine, 1975; 1976); mesograzers (Ruesink, 2000); microphagous, scavengers and predators (Kunze and Anderson, 1979; Hazlett, 1981a). Moreover, a single species is able to feed in different ways according to the food available at the time (Kunze and Anderson, 1979; Schembri, 1982a). Paguroids diet can change seasonally and include other marine invertebrates such as ophiuroids, bivalves, amphipods, shrimps, and small hermit crabs (Hunt, 1925).

Dardanus venosus (H. Milne Edwards, 1848) is a colorful paguroid species that typically occurs in the intertidal zone up to a depth of 100 m, and is commonly found among rocks, shells, coralline algae (Rieger, 1997; Melo, 1999) or even in sea grass meadows constituted by species Thalassia testudinum Banks ex König and Syringodium filiforme Kuetz (Bauer, 1985). This paguroid species is distributed in the western Atlantic, from Florida to Brazil (from the state of Pará to state of São Paulo, including the Rocas atoll and the Fernando de Noronha archipelago) (Mantelatto et al., 2001).

Gastropods are also widely distributed and abundant in intertidal environments (Veras et al., 2013) and have different feeding habits. Their feeding habits are extremely varied and include herbivory, detritivory, suspensivory, carnivory and parasitism (Taylor et al., 1980; Hughes, 1986; Meirelles and Matthews-Cascon, 2003). Predatory gastropods are represented by species with tremendous adaptive success. Species of the family Fasciolariidae Gray, 1853 are usually predators of other gastropods and bivalves (Matthews-Cascon et al., 1989). This group preys on shell chipping that it uses to reach the soft parts of the prey (Hughes, 1986). Aurantilaria aurantiaca (Lamarck, 1816) is commonly found on the bottoms with calcareous algae and corals at shallow waters of the northeastern Brazil. The reproductive period of this species in that region is from August to December, and the egg masses are found under the rocks (Meirelles and Matthews-Cascon, 2005).

Paguroids have not been recognized as important predators in the intertidal environments, and they often obtain empty shells from the environment without killing gastropods. Therefore, the aim of this paper is to report for the first time a predatory behavior of the paguroid D. venosus on the snail A. aurantiaca.

A sample represented by one single specimen of D. venosus and one of A. aurantiaca was collected on the bottom covered by sea grass meadows mainly dominated by the species Halodule wrightii Ascherson at the coastal waters of the municipality of Icapuí, state of Ceará, northeastern Brazil (04º41’00”S 37°21’00”W) (Fig. 1). The sampling area is part of the Barra Grande estuarine system and covers approximately 540 ha; its bottom structure consists mostly of extensive sand/mud banks (Carlos et al., 2010). The paguroid was found showing aggressive behavior, moving chelipeds into the shell aperture. For this reason, the sample was brought to the laboratory and placed in an aquarium containing 10 L of seawater from the collection site and maintained under constant aeration for three days. Subsequently, the sample was cryo-anesthetized and fixed.

Figure 1
Location of the sea grass meadow (Banco dos Cajuais), on the east coast of the state of Ceará, northeastern Brazil.

The gastropod shells of the snail and that occupied by the paguroid were identified based on Rios (2009) and measured for aperture length (SAL) and width (SAW). The hermit crab was identified according to Melo (1999) and sexed by the presence of genital pores (on the basis of third pereiopods in females and of the fifth in males). The paguroid was then measured to establish shield length (SL), which is the distance from the edge of the rostrum to the V-shaped groove in the posterior margin. All measurements were made using a vernier caliper (0.01 mm accuracy).

The specimen of D. venosus was deposited in the Carcinological Collection of the Departamento de Zoologia, Universidade Federal do Rio Grande do Sul (catalogue number: UFRGS 5912), and the specimen of A. aurantiaca was deposited in the Coleção Malacológica Professor Henry Ramos Matthews série B (catalogue number: CMPHRM B 4082). The aggressive behavior of D. venosus on P. aurantiaca was observed during three days (3h/day: one hour during the morning, one in afternoon and one in the night). On the fourth day, the paguroid died, possibly because of the stress. Main aspects of this behavior were recorded by photos using a Sony WX30 digital camera.

The paguroid was a male of D. venosus (SL = 11.16 mm), occupying a shell of Voluta ebraea Linnaeus, 1758 (SAL = 63.53 mm; SAW = 15.47 mm) in good conditions (without severe cracks or perforations) but covered by some ectosymbiont groups: bryozoans, barnacles, calcareous algae, calyptraeid gastropods and polychaete worm tubes. The individual of A. aurantiaca (SAL = 56.02 mm; SAW = 14.40) had a shell in very good conditions (without cracks, perforations and ectosymbionts).

The paguroid reestablishes its aggression immediately after it was placed in the aquarium with the snail and stayed all the time attacking the mollusk during the observation time. Predatory behavior was characterized by the use of pereiopods and mouth parts. The second and third pairs of pereiopods (ambulatory legs) were used to hold laterally the shell in the spire region and in the siphonal chanel of the gastropod (Fig. 2A, B). The first pair of pereiopods (chelipeds) was projected into the shell aperture and moved alternately to hit the gastropod hard structures. The left cheliped (major chela) was used mainly to break the shell and the operculum of A. aurantiaca and the right cheliped (minor chela) to tear apart pieces of snail flesh (Fig. 2A-C). When enough material was accumulated in the fingers, this was brought to the third pair of maxillipeds that were used to manipulate and select the pieces, and push them towards the mandible. In addition, the right cheliped of D. venosus is covered by long setae and it helped the paguroid to obtain small pieces of snail flesh occasionally trapped in the setae and then, these pieces were moved to the mouthparts. All pieces of snail flesh were chopped by the mandibles and then ingested with the aid of the mandibular palps. Part of the external lip of shell aperture was broken and the operculum and foot of the gastropod were severely damaged (Fig. 2D).

Figure 2
A-C, Sequence of attacks of Dardanus venosus on Aurantilaria aurantiaca; D, damages in A. aurantiaca after the attack. White arrows indicates the damages in the operculum (op), foot (fo) and external lip (exl).

This report is an important record of the uncommon feeding behavior of hermit crabs since they are mainly omnivorous detritivores (Caine, 1975; 1976) and rarely show predatory behavior. Paguroids usually acquire gastropod shells without killing, being attracted to sites where gastropods are sick or dying (Pezzuti et al., 2002). Predatory behavior in paguroids has been recorded in Pagurus traversi (Filhol, 1885), Diacanthurus rubricatus (Henderson, 1888), Pylopagurus sp. and Sympagurus dimorphus (Studer, 1883) (Schembri, 1982a; 1982b). These paguroid species usually capture small gastropods and can break shells using the teeth of the cutting edge of the major chela. Paguroids have more success when the prey is small (Schembri, 1982b). The cheliped structure in paguroids may be useful to indicate if one species is feeding on large pieces of food or entire animals. Among paguroids that display predatory behavior, the cutting edges of the fingers are usually sharp and one of chelipeds is larger (Caine, 1975), as found in D. venosus. Sharp fingers can also be used to cut and reduce the size of food (Caine, 1975). The morphology of chelipeds and fingers of D. venosus together with the damages found in the shell indicate that this paguroid was, in fact, trying to predate the snail.

Paguroids usually do not attack and kill healthy gastropods (Lancaster, 1988), but there are records of hermit crabs attacking sick or injured snails (Scully, 1983). In this contribution, the snail specimen was apparently healthy and there was no evidence of past injury or sickness. Even in hermit crabs that filter feed on suspended matter, as Diogenes brevirostris Stimpson, 1858, Diogenes pugilator (Roux, 1829) and Paguristes hummi Wass, 1955, can feed on macroscopic pieces of dead or wounded organisms when available (Hazlett, 1968b). Predatory habits in paguroids may have evolved from casual feeding on small invertebrates, which they disturb while foraging amongst algae (Schembri, 1982b).

Aurantilaria aurantiaca is classified as a generalist predator in intertidal environments and may compete with hermit crabs to obtain food. These generalist predators play an important role in the community structure. Aurantilaria aurantiaca can be classified as a key predator in marine intertidal environments. It preys on several other gastropods, such as Pisania pusio (Linnaeus, 1758), Tegula viridula (Gmelin, 1791), and Stramonita brasiliensis Claremont & Reid, 2011 in the intertidal zone (Meirelles and Matthews-Cascon, in prep.).

Finally, we consider that there are few studies concerning the feeding habits of hermit crabs in Brazil and this report brings relevant new information of one record of predation of a hermit crab on a gastropod that plays an important role in the intertidal food chain. We think that the studies to be carried out in the future on the feeding behavior of paguroids can help determine all aspects of food obtainment by predatory action.

Acknowledgments

The authors would like to thank the undergraduate Biology student Victor M. Azevedo for his help during sampling, Cipriana Leme for correcting the English text and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for grant a Master of Science Scholarship to FBR (Ciências do Mar - Processo 0532/2010) and support for sampling (Ciências do Mar II - Processo 2005/2014 - 23038.004308/ 2014-14).

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Publication Dates

• Publication in this collection
  2017

History

• Received
  14 June 2016
• Accepted
  02 Dec 2016