Acta Zoologica (Stockholm) 87: 113–119 (April 2006) SoundBlackwell Publishing Ltd production in two carapids (Carapus acus and C. mourlani) and through the sea cucumber tegument Eric Parmentier,1 Michael Fine,2 Pierre Vandewalle,1 Jean-Jacques Ducamp3 and Jean-Paul Lagardère4 Abstract 1Laboratoire de Morphologie Fonctionnelle Parmentier, E., Fine, M., Vandewalle, P., Ducamp, J.-J. and Lagardère, J.-P. et Evolutive, Institut de chimie, Bât. B6, 2006. Sound production in two carapids (Carapus acus and C. mourlani) Université de Liège, B-4000 Liège, and throught the sea cucumber teguments. — Acta Zoologica (Stockholm) 87: 2 Belgium; Department of Biology, Virginia 113–119 Commonwealth University, Richmond, VA 23284-2012, USA; 3Centre d’Etude Carapus acus and Carapus mourlani are able to live inside sea cucumbers and Biologiques de Chizé, CNRS, 79360 sea stars respectively. Unlike other carapids whose sounds have been recorded 4 Villiers-en-Bois, France; CREMA- (C. boraborensis, C. homei and Encheliophis gracilis), these two species have L’Houmeau (CNRS-Ifremer), BP 5, 17137 a central constriction in their swimbladder and are unlikely to encounter L’Houmeau, France heterospecific carapids within their hosts. We evoked sound production in Carapus acus and Carapus mourlani by adding several individuals to a tank with Keywords: a single host and found that their sounds differ substantially from the sounds Carapidae, soniferous, swimbladder emitted by other carapids in pulse length, peak frequency and sharpness of Accepted for publication: tuning (Q3 dB). Unlike the other carapids, C. mourlani and C. acus produce 9 January 2006 shorter and less repetitive sounds and do not produce sounds when they enter their host. Since sounds produced within a sea cucumber have the potential to be heard by distant carapids and are typically recorded outside the sea cucumber, we examined the effect of the sea cucumber tegument on acoustic transmission. Attenuation by the tegument was negligible at the frequencies within carapid sounds. Therefore, carapids have the potential to call from the relative safety of a sea cucumber without sacrificing the distance over which their transmissions are heard. Eric Parmentier, Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de chimie, Bât. B6, Université de Liège, B-4000 Liège, Belgium. E-mail: [email protected] (Smith 1964; Trott 1970; Trott and Trott 1972; Vanden Introduction Spiegel and Jangoux 1989). Of 257 Bohadschia argus Some pearlfish (Carapidae) enter and reside in invertebrate collected in Opunohu Bay (Moorea, French Polynesia), hosts such as sea stars, sea cucumbers or bivalves (e.g. Trott 83% contained different species of carapids but less than 1981; Parmentier and Vandewalle 2005). The host reduces 1% included heterospecific infestations (Parmentier and visual, chemical or tactile perception of both predators and Vandewalle 2005). Laboratory experiments and field studies congeners. The ability to communicate acoustically would be revealed that the fish do not appear to determine whether a an advantage during host colonization and reproduction, potential host is already occupied; the fish penetrates the and three species have been shown to produce species- first host it contacts. However, when C. boraborensis and specific sounds (Parmentier et al. 2003a). Sounds have only C. homei are inside the same holothurian, the interspecific been recorded when an individual has entered a sea cucumber confrontation is accompanied by short sound signals. that was already occupied. Intraspecific confrontations are associated with longer and In areas of the Pacific Ocean where they live in sympatry prolonged sounds. Interestingly, the first acoustic signals are (Markle and Olney 1990), Carapus boraborensis, C. homei and emitted as the inter- or intraspecific types without passing Encheliophis gracilis can inhabit the same host species but through an intermediate enquiry-type stage (Lagardère et al. heterospecifics are rarely found together in the same host 2005). © 2006 The Authors Journal compilation © 2006 The Royal Swedish Academy of Sciences Sounds in Carapini fishes • Parmentier et al. Acta Zoologica (Stockholm) 87: 113–119 (April 2006) The apparent silence of fish approaching a host is not with previously recorded species (C. boraborensis, C. homei understood. Since these species are capable of eating each and E. gracilis) to know (i) how the central constriction of the other, it could be advantageous to be discrete. However, the swimbladder can influence the sound and (ii) if the differ- meeting of two species does not automatically end in preda- ences in the ecology of both groups can be inferred from the tion because one of the fish may leave the host (Parmentier sounds produced. (2) In the second experiment, the goal was and Vandewalle 2005). Therefore, the entering fish appears to know if the tegument of the sea cucumber host could (or to be willing to risk an encounter to allow it to assess the size could not) disturb the propagation of sounds. of any other fish that might be present. Carapus mourlani is commonly found in the Indo-Pacific as The carapid sonic mechanism includes specialized an- a commensal of sea stars such as Culcita sp. and Acanthaster terior vertebrae, the swimbladder and associated muscles planci (Meyer-Rochow 1977, 1979; Trott 1981; Eeckhaut (Courtenay and McKittrick 1970; Markle and Olney 1990; et al. 2004). Carapus mourlani has been observed to swim Parmentier et al. 2000; Parmentier & Vandewalle 2003). The along the ambulacral groove of the sea star Culcita before anteriormost lateral surface of the swimbladder possesses a entering the stomach, tail first, through the oral cavity and horseshoe-shaped thinner zone, the swimbladder fenestra. finally reaching the general cavity (E. Parmentier, personal The fenestra is covered dorsolaterally by the swimbladder observation). Carapus acus lives in the Mediterranean Sea plate, an extension of the third epineural rib. The sonic and on the east coast of North Africa. It is usually found in muscles originate on the orbital roof of the skull and insert the sea cucumbers Stichopus regalis, Holothuria tubulosa and into the anterior wall of the swimbladder (Parmentier et al. Holothuria stellati, which it enters tail first or head first (Kloss 2003b). The action of the sonic muscles in sound generation and Pfeiffer 2000; Eeckhaut et al. 2004). could stimulate movement of the fenestra (Parmentier et al. 2003a, 2003b), which presses against the swimbladder plate. Materials and methods The swimbladder plate is broader, thinner and more regu- larly shaped in the Carapini tribe (Encheliophis and Carapus) Carapus mourlani than in free-living carapids. Parmentier et al. (2002) sug- gested that the large swimbladder plate of the Carapini could Thirty-two C. mourlani (total length 6–10 cm) were col- be related to their way of life because the teguments of the lected by scuba diving in the lagoon in front of Tulear host could disturb or attenuate sound propagation. (Mozambic canal, west coast of Madagascar) in June 2004. On the other hand, the genus Carapus can be divided They were found in the general body cavity of the sea star into two subgroups: subgroup 1 (C. acus, C. bermudensis and Choriaster granulatus (n = 40). Host and fish were stored in C. mourlani) possesses a central constriction of the swim- a community tank (3.50 × 0.7 × 0.2 m) with running sea bladder (Fig. 1), which is not present in subgroup 2 water. Recordings were made at 26 °C in a smaller tank (C. homei, C. boraborensis and C. dubius). Moreover, fishes of (1 × 0.5 × 0.6 m). A specimen of the host was placed in the subgroup 1 can only have conspecific encounters in their centre of the tank, and several individuals were introduced host whereas they can be heterospecifics for C. homei and successively into the aquarium. Sounds were recorded with C. boraborensis (Markle and Olney 1990; Parmentier et al. 2000). an Orca hydrophone (sensitivity: −186 dB re 1 V/µPa) con- The goal of this study was dual. (1) The sounds of C. acus nected via an Orca-made amplifier (ORCA Instrumentation, and C. mourlani were recorded for the first time and compared France) to a mini-disc recorder (JVC, XM−228BK). This system has a flat frequency response range (± 3 dB) between 10 and 23.8 kHz. The hydrophone was placed above the sea star. Carapus acus Thirty-two C. acus (total length of 8–12 cm) were collected from dissection of 87 Holothuria tubulosa and 129 Holothuria stellati obtained in front of the STA.RE.SO station (Calvi Bay, Corsica) in April 2004. Fish were stored in a community tank (0.6 × 0.6 × 0.4 m) with running sea water. Recordings were made at 19 °C in a smaller tank (0.4 × 0.4 × 0.31 m). A specimen of the host (H. stellati ) was first placed in the centre of the tank, and several individuals were introduced Fig. 1—Left lateral view of the swimbladder. —A. In Carapus successively into the aquarium. Sounds were recorded with mourlani —B. In C. boraborensis. White arrow: central constriction of an HTI 16 400 hydrophone coupled with a preamplifier and the swimbladder. Black arrow: localization of the sound-producing connected to a Sony TCD-D8 digital audio tape-recorder muscle. (recording band width: 20–22 000 Hz ± 1.0 dB). © 2006 The Authors Journal compilation © 2006 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 87: 113–119 (April 2006) Parmentier et al. • Sounds in Carapini fishes Fig. 2—Scheme of the experimental process used to study the transmission of sounds through the sea cucumber tegument. a large glass aquarium (2.48 × 0.7 × 0.7 m) (Fig. 2). A 8103 Sound analysis Brüel & Kjaer is used as a constant sound pressure trans- Sounds were digitized at 44.1 kHz (16-bit resolution) and mitter, and a B & K, type 8101 hydrophone was the receiver.