The Box Crab Calappa hepatica as a Nuclear Species for the Opportunistic Foraging Behaviour of the Flowery Flounder, Bothus mancus, in the Indo-Pacific

Abstract

Some predatory fishes may exhibit opportunistic feeding behaviour by exploiting potential prey that is distracted, displaced, or exposed by the activities of a third party that acts as a ‘nuclear’ species. Other fishes mostly perform the role of ‘nuclear’ species, but benthic invertebrates, such as octopuses, have also been reported. Crabs are rarely observed in this role, with only a few records from the tropical Atlantic Ocean. Here, we report the temporary association between two specimens of the flowery flounder, Bothus mancus (family Bothidae), and a box crab, Calappa hepatica (family Calappidae), from the Philippines, representing the first record of a crab–fish feeding association in the Indo-Pacific region.

Interspecific temporary associations are common as part of feeding strategies among predatory marine fishes [1,2,3]. Some species are capable of complex coordinated hunting for mutual benefits (e.g., the cooperation between Gymnothorax javanicus and Plectropomus pessuliferus that allows them to attack potential preys both inside and outside reef crevices, which requires referential elaborate gesture communication and precise movement coordination) [4,5]. However, the most widespread interspecific association is the ‘following and scavenging’ strategy (also known as ‘following behaviour’), where one or more ‘associate’ fish opportunistically follow a ‘nuclear’ species to exploit the potential prey that is distracted, displaced, or exposed by its presence, movement, or feeding activities [1,2,3,6,7,8]. Usually, there is minimal overlap between the dietary preferences of the species in this partnership, which therefore can be considered commensalism, but cases of food pilfering are also known [1]. This peculiar association is mainly widespread among benthic and benthopelagic fishes but is also known among semi-pelagic species [9].

The role of nuclear species is usually carried out by other fishes, such as those of the family Mullidae (e.g., Mulloidichthys dentatus, Mulloidichthys martinicus, Mullus surmuletus, Parupeneus barberinus, Pseudupeneus maculatus), which stir soft substrata to detect their invertebrate preys and commonly attract numerous invertivorous and piscivorous benthic and benthopelagic fishes, including some species of Labridae, Epinephelidae, and Carangidae [1,2,3,9]. On the other hand, some species of Muraenidae (e.g., Gymnothorax castaneus, Gymnothorax funebris, Gymnothorax vicinus, Muraena pavonina, Siderea grisea) and Ophichthidae (Myrichthys breviceps, Myrichthys ocellatus), which stalk their preys inside holes and crevices, often attract piscivorous fishes (mainly belonging to the families Epinephelidae, Labridae, Serranidae, and Carangidae) that exploit fishes trying to escape from their refuges [1,3,6,10,11].

Nevertheless, benthic invertebrates that enter crevices or those that perturbate soft substrata during their movements and feeding activities can assume the role of nuclear species as well. Octopuses are well-known representatives of this role [1,7,12,13,14], but other invertebrates, including crabs, have infrequently been reported as such. Among crabs, in particular, the calappids Cryptosoma cristatum Brullé, 1837, Cryptosoma balguerii (Desbonne, 1867), and Calappa ocellata Holthuis, 1958 can act as nuclear species for the hunting activities of various fish species along both sides of the Atlantic Ocean [15,16]. Calappidae species mainly live in soft substrata and quickly bury themselves in the sand using their large chelipeds when threatened [17]. This activity can disturb and expose small fish and invertebrates living on and inside the sediments, which then might become easy prey for the associated fishes. Flounders belonging to the families Bothidae and Cyclopsettidae (Pleuronectiformes) are among the associated species, as they are benthic predators of invertebrates that dwell on and in soft bottoms [16].

The lack of records of a crab–fish ‘following and scavenging’ association in the Indo-Pacific was puzzling since this region, and in particular, the area known as the Coral Triangle (including Philippines, Malaysia, Indonesia, Papua New Guinea, the Solomon Islands, and Timor-Leste), hosts the highest marine biodiversity in the world [18]. This anomaly can plausibly be explained by the relative scarcity of scientific observations carried out on soft substrate communities in the proximity of coral reefs [19,20,21,22]. Here, we report the observation of an opportunistic behaviour shown by two adult males (about 25 cm long) of the flowery flounder Bothus mancus (Broussonet, 1782) (Pleuronectiformis: Bothidae), strictly following a specimen of the smooth box crab, Calappa hepatica (Linnaeus, 1758) (Decapoda: Calappidae) in the Philippines (Figure 1).

The fish identification was based on its general morphology, a large triangular protuberance on the anterior of the ocular-side maxillary, and small blue spots and white blotches larger than the ventral eye diameter. The presence of spines visible on orbitals allowed gender identification [23]. The crab was identified by its colour and the roughness of its carapace and chelipeds [24].

The observation was conducted in the central area of the northern coast of Maricaban Island, close to Tingloy Port (13.662279 N, 120.878500 E), in a dive spot known as ‘Coconut’ (Figure 2a,b), characterised by a dark grey sand slope developing from the shore. The coasts of the Calumpan Peninsula (Luzon Island) and Maricaban Island (about 2.3 km south of the peninsula), usually referred to as the Anilao diving area, are considered to be among the world’s best ‘muck diving’ areas [25,26]. The term ‘muck diving’ indicates scuba diving activities performed on soft-sediment habitats with limited landscape features, with the explicit goal of observing or photographing rare, unusual, or cryptic species seldom seen on coral reefs [27,28].

On 21 February 2017, on a sandy bottom at about 10 m depth, a large individual of Calappa hepatica was observed from a distance when it was patrolling the substratum, followed at close distance by two individuals of Bothus mancus. Disturbed by the presence of divers, the crab moved rapidly on the seafloor across a distance of about 10 m before partially burying itself in the sand. The two flounders darted in the same direction and stopped abruptly a few centimetres behind the crab and then patiently waited for it to move again (Figure 1). After about a minute, the crab re-emerged and moved again for a few meters before burying again, always closely followed by the two fish. The fish never attempted to attack the crab or tried to make it move.

The persistence of the association, the presence of two individuals performing the same actions, and the rapidity of the fish’s tracking in response to the crab fleet suggest the existence of a ‘following and scavenging’ foraging behaviour. The crab acts as a nuclear species by stirring up sediment, which is caused by its walking and its burying behaviour on the sea floor, while the flounders act as associated species, feeding on the small invertebrates and fishes disturbed by the crab’s activities. This represents the first record of this kind of opportunistic feeding behaviour from the Indo-Pacific region involving a crab as a nuclear species. Because of shared soft-bottom environments and the common occurrence of stalking fish behaviour, we do not know if the similar commensalistic relationship between Calappa and Bothus species in the Caribbean and the Indo-Pacific is based on common ancestry or convergent evolution. This would require a phylogenetic study involving all Calappa species and fishes participating in this kind of relationship. At minimum, we know now that this relationship is not limited to the Atlantic Ocean, which adjusts a preliminary conclusion of a recent study [16].