Physiology & Behavior 68 (2000) 543–547 0031-9384/00/$ – see front matter © 2000 Elsevier Science Inc. All rights reserved. PII: S0031-9384(99)00216-4 Effect of aging on manipulative behavior in the cuttlefish, sepia M.P. Halm, V. Agin, M.P. Chichery, R. Chichery* Laboratoire de Psychophysiologie, Université de Caen, 14032 Caen Cedex, France, and Station Marine (CREC), 14530 Luc sur Mer, France Received 29 July 1998, received in revised form 28 September 1999; accepted 27 October 1999 Abstract The cuttlefish is an active predator that is able to catch crabs of a size that is large relative to its own. The capture is followed by a com- plex manipulative behavior leading to paralysis of the prey by injection of a cephalotoxin. This manipulative behavior is relatively stereo- typed, and earlier research has shown that the cuttlefish concentrates its bite on the articular basi-ischiocoxopodite membrane of the crab’s fifth pair of pereiopods. By placing mechanical constraints on the base of the fifth pereiopods, we were able to demonstrate that this manipulative behavior presents a marked degree of stereotypy but is not rigidly fixed. Substantial behavioral differences, however, were observed between subadult and senescent cuttlefish. The existence of a reduction in behavioral flexibility in the older animals in re- action to the constraints is discussed. © 2000 Elsevier Science Inc. All rights reserved. Keywords: Sepia officinalis; Cephalopods; Predation; Manipulative behavior; Behavioral flexibility; Aging 1. Introduction Many studies have provided an insight into the major characteristics of the predatory behavior of the cuttlefish. There are two capture strategies: tentacle strikes used gener- ally for prey capable of a rapid escape (shrimps, fishes), and the “jump” mode used for less mobile prey (crabs) [1–3]. From a motor control point of view, two stages may be distinguished, contrasting posturokinetic motor activities that correspond, first, to the movement of the body and/or ejection of the tentacles for prey capture; second, manipula- tive motor activities allow the paralysis of the prey before its ingestion [4]. However, up until now, little is known about the control of this manipulative behavior. It appears to be especially complex in the “jumping mode,” following the capture of large-sized crabs with claws that may injure the predator. Such prey is often captured in the “jumping mode”: the cuttlefish jumps forward at its prey and covers it with its eight arms [2]. The crab is then moved to the buccal bulb and manipulated by the cuttlefish’s arms in such a way that the pereiopods of the crab cannot clinch to the substra- tum [5]. Two clear manipulative phases are observed. Prey capture is followed by an initial, very rapid manipulative phase that moves the cephalothorax–abdomen junction of the crab to the mouth of the cuttlefish. In this position, the cuttlefish can inflict a wound. The salivary toxins are proba- bly injected into this wound and cause a paralysis of the prey about 55 s after capture. The examination within 20 s after the capture of the crabs shows that this wound is gen- erally localized in the proximal joints of the hind pereiopods [5]. The second manipulative phase reorientes the crab to facilitate its ingestion [5]. The limited variability of the ap- pearance of the first indications of paralysis (fibrillation time latency) and the preferential location of the wound on the fifth pereiopod speak for a stereotyped organization of this behavior. This stereotypy is also found in other behav- iors of cephalopods, such as body patterns and digging in Sepia; however, the latter is relative flexible [6]. In addition, in Octopus, different experimental studies have shown a nonrandom location of drill holes on different species of snails [7] and a large flexibility in the choice of opening the shells either by force or by drilling. These results suggest some complexity in the manipulative behavior of Octopus. One might stress here the surprising learning capacities of the cephalopods [8–11]. In cuttlefish, Wells [12] and Messenger [13] showed that this animal can quickly learn to inhibit its predatory behavior towards shrimps enclosed in a glass tube. Visual or tactile learning have been described in Octopus. Blind octopuses are clearly able to learn to dis- criminate between objects that differ by their surface tex- ture; in contrast, they failed to learn to discriminate by touch between objects of different sizes, shapes, or weights. Thus, Octopus does not seem to use haptic information, as this species does not integrate proprioceptive with surface con- tact information [11]. These data seem inconsistent with the * Corresponding author. Tel.: (33) 2 31 56 55 19; Fax: (33) 2 31 56 56 00 E-mail address: Chichery@scvie.unicaen.fr