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Electrolocation-Communication Discharges of the Fish Gymnotus Carapo L

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Electrolocation-Communication Discharges of the Fish Gymnotus Carapo L SleepBrazilian in electricJournal fishof Medical and Biological Research (1999) 32: 1223-1228 1223 ISSN 0100-879X Short Communication Electrolocation-communication discharges of the fish Gymnotus carapo L. (Gymnotidae: Gymnotiformes) during behavioral sleep R.M. Stopa and Departamento de Ciências Biológicas, Faculdade de Ciências, K. Hoshino Universidade Estadual Paulista, Bauru, SP, Brasil Abstract Correspondence Technical problems have hampered the study of sleep in teleosts. The Key words R.M. Stopa electrical discharges of Gymnotus carapo L. (Gymnotidae: Gymnoti- · Sleep · Departamento de Ciências Biológicas formes) were monitored to evaluate their ease and reliability as Fish Faculdade de Ciências, UNESP · parameters to study sleep. The discharges were detected by electrodes Electric discharges Av. Eng. Luiz Edmundo C. Coube, s/n · Cannibalism immersed in a glass aquarium and were recorded on a conventional 17033-360 Bauru, SP · Antipredation mechanism Brasil polygraph. G. carapo showed conspicuous signs of behavioral sleep. During these periods, opercular beat rates were counted, electric Publication supported by FAPESP. discharges recorded, and the sharp discharge increase (SDI) of the orienting reflex was investigated. All 20 animals monitored main- tained electrical discharges during behavioral sleep. The discharge frequencies during sleep (50.3 ± 10.4 Hz) were not significantly Received September 24, 1998 Accepted July 26, 1999 different from those observed when the fish was awake and inactive (57.2 ± 12.1 Hz) (Wilcoxon matched-pairs signed-ranks test, P>0.05). However, the SDI, which was prevalent in the awake fish, was not observed during periods of behavioral sleep. Additional observations showed that the species had cannibalistic habits. When presented with electrical discharges from a conspecific, the sleeping fish showed an initial decrease or pause in discharge frequency, while the awake fish did not have this response. We conclude that the electrical discharges of G. carapo were not conspicuous indicators of behavioral sleep. Discharges may have been maintained during sleep for sensory pur- poses, i.e., conspecific detection and avoidance of cannibalistic at- tacks. The heuristic value of comparative stud- ria, and the universal occurrence of sleep in ies for sleep research is widely recognized, the group is still questioned (2,3). but many animal groups have received little Gymnotus carapo L. (Gymnotidae: Gym- attention. Fish, in particular, have been ne- notiformes), popularly called tuvira, is a glected because of the technical difficulties low voltage electric pulse triggering fish, and in obtaining and interpreting conventional may be a potentially valuable species for electrographic recordings (1). As pointed out sleep research. It uses electric organ dis- by others (1-6), existing studies of sleep in charges (EOD) to interact with its environ- fish are based primarily on behavioral crite- ment, e.g., to communicate with conspecif- Braz J Med Biol Res 32(10) 1999 1224 R.M. Stopa and K. Hoshino ics and to scan its habitat (7-9). Since re- vibration of the aquarium, etc). Another 20 duced interaction with the environment is a fish were observed to determine the occur- marked characteristic of sleep, the electrical rence of behavioral sleep. For this purpose, discharges of G. carapo would be expected each animal was left undisturbed (except for to change during a sleep-activity cycle. To the placement of worms in the tank) in the investigate this hypothesis, in the present experimental aquarium for 7 days. Several study we determined the occurrence of be- times a day, the fish were observed for signs havioral sleep in G. carapo and then ob- of behavioral sleep, i.e., prolonged immobil- served if the state was correlated with changes ity in a particular posture, reduced fin move- in EOD. The electrical discharges of this ment, and reduction of the frequency of cy- species oscillate between 40 and 100 Hz and clic opercular movements. EOD recordings can be measured continuously and easily by were carried out when signs of behavioral a noninvasive technique. sleep were apparent and during the orienting G. carapo individuals of both sexes from reflex test, characterized in the awake ani- the Paraná River basin were used during the mal by a sharp discharge increase (SDI) in study. Size ranged from 50 to 400 mm stan- response to a plastic rod immersed and stirred dard length. Ten groups of 15 animals were in the vicinity of the fish. Near the end of the kept in aerated water tanks (1,000-l capac- behavioral sleep recording periods, the ity) under ambient temperature and light aquarium wall was knocked upon to induce conditions. The fish were fed earthworms locomotion by the fish and to confirm the daily in amounts corresponding to approxi- reversibility of the behavioral state. mately 10 g/animal. They were allowed to Recordings for the first 10 animals at 23- acclimate for 7 days and then one animal 25oC showed that inactive, awake fish emit- was singled out and transferred to the exper- ted very regular pulse discharge frequencies imental chamber, an aerated glass aquarium ranging from 42 to 68 Hz (mean ± SD of 53.5 (250 x 500 x 250 mm) surrounded by a visual ± 12.1 Hz) (Figure 1). Discharge amplitude isolation fence and containing a thermom- changed with animal position in relation to eter. The bottom of the aquarium was filled the electrodes and the maximum voltage with a 10-mm deep layer of washed sand. A observed was 1 mV. The frequency of pulses shelter made with a piece of PVC tubing (24 increased during swimming, reaching 75.5 ± to 40 mm in diameter, 50 to 280 mm in 16.0 Hz (mean ± SD of 15 randomly selected length) was positioned in the sand so that the episodes). No relationship was observed be- animal could be observed through a sight tween animal size or previous swimming hole from outside the visual isolation fence. and the frequency of discharge. The mean Electrical cables with 20-mm non-insulated and standard deviation of the SDI frequency tips were immersed and fixed on the oppo- was 71.4 ± 12.8 Hz. SDI was elicited by site longitudinal walls of the aquarium to rapidly moving shadows and unexpected light transmit and record electric organ discharges changes, observer approximation, knocks on via the electromyography channel of an EM the aquarium wall, or immersion and slow polygraph (Electronics for Medicine, Hous- movement of a plastic rod. EOD frequency ton, TX, USA). decreased and increased directly with tem- Preliminary observations were made on perature, but ceased outside the 9-32oC range. 10 animals to evaluate recording quality, Near the extremes of this range, the fish lost baseline discharge frequencies, the effect of their natural posture and showed EOD arrest temperature, and the response to presenta- for 3-10 s in response to painful pinching. tions of some environmental stimuli (light There were clear signs of behavioral sleep flash, moving shadows, sounds, mechanical for G. carapo. Sleep was characterized by a Braz J Med Biol Res 32(10) 1999 Sleep in electric fish 1225 motionless posture with the tail down (touch- ful stimulation (pinching). G. carapo emit- ing the sand) and the head up (30 degrees ted electrical discharges throughout the above with respect to the bottom of the aquarium), behavioral sequence, and then stopped them reduction in amplitude and frequency of oper- 5-20 min after quiescence had begun. Be- cular movements, and ventral fin immobil- cause EOD was maintained after behavioral ity. Plastic rod immersion into the aquarium responses had ceased, it is likely to be con- during these periods did not evoke an SDI, trolled independently. EOD was recovered indicating a reduction in the vigilance level. after 5-10 min in the original aquarium, con- However, the more extreme stimulus of a comitantly with postural and swimming nor- knock on the aquarium wall woke the fish up malization. as indicated by generalized body movements Interactions with conspecifics were in- and undulations of the ventral fins. EOD vestigated in order to determine the func- recordings unexpectedly showed that elec- tional role played by the sleep EOD of G. trical discharges were maintained during carapo. Small size class G. carapo (50-90 behavioral sleep periods. Discharge frequen- mm) were introduced into an aquarium with cies (50.3 ± 10.4 Hz) were not significantly a larger resident animal, which was awake different from those recorded during inac- and had been starved for two days (the resi- tive awake periods (57.2 ± 12.1 Hz) (Wil- dent fish was at least 30 mm longer than the coxon matched-pairs signed-ranks test, intruder fish). A brief period of attentive P>0.05). Amplitude remained constant dur- behavior of the resident animal was observed, ing sleep and waking periods if the fish did followed by a rapid exit from the PVC shel- not change its position in the aquarium. ter, pursuit and capture of the intruder fish, To determine if electrical discharges oc- and immediate cannibalism (within 2 to 5 curred during sleep via mechanisms inde- min). Alternatively, in two cases (15.4%), pendent of those that control other aspects of the smaller fish was killed within the first 5 sleep, behavior and EOD were monitored in min, but ingestion was delayed for up to 5 h. anesthetized fish. Thirteen fish were anes- The ingestion latencies were shown to in- thetized for the experiment individually by crease up to 24 h if a second or more intrud- immersion in an aquarium containing 200 ers were introduced (16 observations). mg/l of compound MS-222. Later, they were These observations suggest the possibil- returned to their original aquarium and moni- ity that G. carapo uses its EOD during sleep tored to assess the reversibility of anesthetic- to detect conspecifics and to avoid cannibal- induced sleep compared with natural sleep.
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