Circadian Migratory Behavior of a Cestode Symbiote in the Rat Host

Abstract

Under specified experimental conditions, Hymenolepis diminuta exhibits a longitudinal circadian migration in the small intestine of the rat. This was shown by changes in distribution of total worm tissue and of scolices in the gut at different times of the day in hosts on a 15-hr feeding schedule. Maximum numbers of scolices and amounts of worm tissue were in the anterior 10 inches of the small intestine during the 12 to 4 AM period, and lowest quantities at 4 to 5 PIM. There were accompanying inverse worm distribution changes in the posterior part of the small intestine. Short periods of host starvation delayed anteriad migration. In a limited number of combinations, migration occurred in infections of one to 30 worms, 10 to 21 days of age. The timing of migration was changed by altering the feeding pattern of the host. Fluoroscopic study of the rat gut during and after killing indicated that the migration was not an artifact produced by violent gut movements. In the course of other experiments on the strobilate stage of the rat tapeworm, Hymenolepis diminuta, it was noted that the worms appeared to be in different parts of the host small intestine at different times of the day. This has been examined in a more systematic fashion to determine whether there is a regular pattern of movement of the strobila and whether or not the scolex migrates during the course of a day. MATERIALS AND METHODS Young male rats of the Sprague-Dawley strain (Holtzman Rat Co.) were infected with cysticercoids of Hymenolepis diminuta; unless otherwise specified, each host received 30 worms. Ten days after infection, at specified times of the day, groups of four rats were weighed; each rat was killed by a blow on the head and the small intestine rapidly removed. With minimal stretching, the small gut was cut into three sections; the first two portions were 10 inches long, and the posteriormost third varied in length. The worm tissue in each of the three sections of the gut was flushed out with Ringer's solution. The worm tissue was blotted on hard filter paper, the wet weight of the tissue determined, and the number of scolices in each of three samples was counted. In experiments in which the procedure was modified, this is described in the context of the experiment. Unless otherwise stated, the rats were given an excess of food (Purina Lab Chow) each day at 5 PM and food was removed from the cages each morning at 8 AM throughout the 10-day period of worm development. Water was available to the animals at all times. RESULTS AND DISCUSSION In the first experiments (Expt. 1, Table I), Received for publication 10 January 1969. * This work was supported in part by grants from the NIH, U. S. Public Health Service (AI 01384 and 2E-106). real differences were apparent in the distribution of worm tissue and of scolices from hosts killed at four times during the day. There appeared to be a posteriad movement of worms during the post-feeding period, this repositioning being maximal at 5 PM. Next, the worms moved anteriorly and, shortly after midnight, the distribution of worm tissue and scolices resembled that seen at 8 AM. In a second experiment (Expt. 2, Table I), the afternoon shift in worm distribution was examined more closely by killing groups of animals at 4 PM and at 6:30 PM, as well as at other times of the day. The shift in position in the gut was again obvious. At 4 PM, about half of the worms were in the posterior part of the small intestine. At 6:30 PM, 1.5 hr after host feeding began, there was an increase in the number of worms in the anterior small intestine. At 9 PM, this anteriad movement was apparently still in progress. The data of Experime ts 1 and 2 have been combined and are presented graphically in Figure 1. Special mention may be made of the changes in tissue and scolex distribution in the second 10-inch section of the small gut. The fluctuations in worm weight in this region closely paralleled those seen in the anterior section. However, in the middle region the maximum number of scolices was found about 4 hr later than in the first section and several hours before the peak was attained in the posterior zone. In Experiment 2, food was withheld from two groups of animals at the regular 5 PM feeding. At 9 PM, one group was killed and food was given to the second group which was then killed 2 hr later. In the starved 9 PM