An electric sense in crayfish?

A variety of aquatic vertebrates, including teleost and non-teleost fish, amphibians, and monotreme mammals, are sensitive to low-frequency electric signals with thresholds of low nanovolts per centimeter to high microvolts per centimeter, have specialized detectors for these signals, and use electroreception to locate food or orient in their environment (1–9). Although invertebrates would similarly benefit from an electric sense (10), none are known to use it. A recent report concluded that the freshwater crayfish species Cherax destructor responds to electric fields (11). Some years ago, we investigated whether another species of freshwater crayfish, Procambarus clarkii, has an electric sense and uses it to find prey. Weak fields were produced across water-bridge electrodes spaced 1–5 cm apart, and exploratory feeding behaviors such as touching, grabbing, and tugging at the electrodes using the claws, legs, and mouthparts were examined. Our results show that P. clarkii responds to fields with intensities of 20 mV/cm and greater. We also recorded from sensory neurons in P. clarkii legs and claws and found that the only field-sensitive cells had similarly high thresholds and were also responsive to chemical and mechanical stimuli. We conclude that P. clarkii does not have a high-sensitivity, specialized electric sense used in locating food. Male and female freshwater crayfish (Procambarus clarkii), 55–80 mm total length, were shipped from Atchafalaya Biological Supply Co. (Louisiana), kept in our laboratory, and fed shrimp pellets. A week before behavioral assays, animals were isolated without food in holding aquaria under a photoperiod of 12 h light to 12 h dark. We assumed that if P. clarkii has an electric sense, these crayfish would use it in a context in which many electroreceptive animals normally use it—to identify prey animals on the basis of small, weak dipole fields generated by those prey species. Thus, we examined the feeding behavior of the crayfish when we presented such fields. Animals were tested in a 404020-cm aquarium (Fig. 1A). Dipole electric fields were generated by applying DC or sinusoidal voltages across a pair of water-bridge electrodes. Field strength and direction were measured with a pair of electrodes held a fixed distance apart and moved and rotated to determine field strength and orientation around the dipole source (Fig. 1B; Supplemental Fig. 1, http://www.biolbull.org/supplemental/). Animals were tested in the dark phase of the light:dark cycle under dim red light, to which they are minimally sensitive. Each animal was tested twice, first in the absence of an electric field (control) and then a few days later in the presence of an electric field. At the beginning of a trial, the animal was secured in a shelter located 3 cm from the electrodes. After 45 min, the shelter door was opened and the behavior of the animal was videotaped for 2 h. Behaviors elicited close to the dipole source (i.e., within 0.5 cm of the electrodes spaced 1 cm apart or within 2.5 cm of the electrodes spaced 5 cm apart) were quantified by an observer unaware of the experimental treatment. Behaviors analyzed were exploratory and appetitive feeding behaviors typical of crustaceans (12), including the following: (1) Pass-by: crayfish passed close to the electrodes with its first two pairs of legs or claws. (2) Touch: crayfish repeatedly touched the electrodes with its first pair of legs or kept its first pair of legs in contact with the electrodes. (3) Active behavior on the electrodes with claws down: crayfish touched the electrodes and brought one or both claws down close to them. (4) Tug: crayfish tugged the electrodes with its mouthparts. (5) Grab: Crayfish grabbed the electrodes with one or both claws. The cumulative duration of all four “active” behaviors in proximity to the electrodes (i.e., touches, claws down, tugs, and grabs) was also used as a Received 28 February 2007; accepted 1 May 2007. * To whom correspondence should be addressed. E-mail cderby@ gsu.edu 1 Current address: Centre de Neurosciences Psychiatriques, Département de Psychiatrie, CHUV 1008 Prilly-Lausanne, Switzerland. E-mail: [email protected] Reference: Biol. Bull. 213: 16–20. (August 2007) © 2007 Marine Biological Laboratory