A PERSISTENT DIURNAL RHYTHM IN CHAOBORUS LARVAE. II. ECO LOGICAL SIGNIFICANCE
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1 A PERSISTENT DIURNAL RHYTHM IN CHAOBORUS LARVAE. II. ECO LOGICAL SIGNIFICANCE Edward J. LaRow2 Department of Zoology, Rutgers University, New Brunswick, NJ ABSTRACT- When Chaoborus larvae (Diptcra:Culicidae) were kept under constant light conditions within sediment cores their distribution exhibited a 24-hr periodicity. There was a gradual upward movement of larvae in the sediments; the greatest percentage (5 = 90% ) was consistently found in the O-l-cm stratum at solar sunset. The data indicate the larvae test the light conditions at the mud-water interface at solar sunset, When the light intensity was below some critical threshold value, the larvae emerged and became planktonic. When the light intensity was above this value, the larvae recntercd the sediments. The depth to which they burrowed was a function of the light intensity to which they were exposed. A method of resetting the endogenous rhythm in nature is proposed. INTRODUCTlON The larval instars of Chaoborus undergo a diurnal vertical migration (Juday 1921; Eggleton 1931; Wood 1956; LaRow 1965). Typically the first two instars are entirely planktonic, while the third and fourth ( mature larvae) are benthic during the day and planktonic at night. All four instars migrate to the surface waters and return to the hypolimnion (1st and 2nd instars) or the sediments ( 3rd and 4th instars) shortly before sunrise. The stimulus causing the cmcrgence of the mature larvae from the sediments to coincide closely with the setting sun has been discussed (Juday 1921; Eggleton 1931; Wesenbcrg-Lund 1943), but it has not been explained how larvae buried in the sediments could dctcct the difference bctwcen day and night at the surface. LaRow ( 196Sa) dcmonstratcd a persistcnt diurnal rhythmicity in the cmcrgence of Chaoborus larvae from the sediments. However, this did not preclude the necessity of the benthic larvae receiving some light stimulus from the setting sun, since the offset of light was shown to be the Zcitgebcr for this rhythm. Further cxperimcnts indicate that the larvae were not 1 This research was supported by National Science Foundation Grant GB Present address: Department of Biology, Siena College, Loudonville, N. Y am indebted to Dr. R. Loveland for his interest and criticism. responding directly to a light stimulus because overhead lights in the laboratory failed to penetrate the sediments and establish a light gradient. METIIODS Sediment cores were used to determine the activity patterns of the larvae in the sediments as well as the effect of light on these larvae. Opaque plastic cores ( 10 cm long, 2.5-cm I.D.) were filled with sediments so that each core contained 9 cm of sediment with 1 cm of water on top. Fifty larvae (4th instar) of Chaoborus punctipennis Say were put in each core and exposed to varying light conditions at 2OC. To determine the distribution of the larvae, the cores were instantly frozen by placing them in supercooled acetone. When solid, they were cut into l-cm sections, which were then thawed, and the larvae recovered and counted. RESULTS Eleven cores were kept under constant overhead illumination. Every 2 hr during a 24-hr period a core was frozen. This experiment was repeated three more times. The cores processed during the solar day had the greatest concentration of larvae in the l-2-cm stratum (2 = 42% ) with another 20% of the population located in the 2-3-cm stratum ( Fig. 1). There was a gradual increase in concentration at the 213
2 214 EDWARD J, LAROW t 19 FIG. 1. Diurnal movement of larvae in sediments constantly illuminated. Values expressed are mean values for four replicate experiments ( 50 larvae/replicate). Numerals on the depth scale refer to the lower lines. R = 5% of larval population. t 06 O-l-cm stratum, and at 2000 hours, 52% of the larvae were there, The greatest fraction (90%) of larvae occurred in the O-l-cm stratum at 2100 ( natural sunset), and no larvae were recovered at that time below 2 cm. In the 1-hr interval between 2000 and 2100 hours, there was a 38% increase of larvae in the O-l-cm stratum; the greatest concentration was found there in the cores processed after solar sunset. In the remaining samples, an average of 58% of the larvae were in this stratum. The major change observed in the cores processed after sunset was the increase in larvae below 5 cm. Cores for the 3 hr after natural sunset averaged 16% of the larvae below 5 cm, although none were found below 5 cm in the four cores processed before natural sunset. The response of the larvae under varying light conditions immediately before and after sunset was then investigated (Fig. 2). The top half of Fig. 2 shows, in essence, a duplication of part of the previous experiment. The cores were kept in continuous light, and at solar sunset they showed a sharp increase in the number of larvae (92%) in the O-l-cm stratum; none were recovered below 2 cm. One hour after sunset the larvae in the O-l-cm stratum had decreased to 64% and were prcsent for the first time below 5 cm. When the lights were turned off 1 hr before sunset, 40% of the larvae became planktonic at sunset and 52% were found in the O-l-cm stratum (Fig. 2, bottom). The next core in this experiment was similarly treated; however, the lights were turned on again at sunset, and it was processed after 1 hr of light exposure. In this case, no larvae were planktonic and most were found in the l-2-cm stratum, with 14% below 4 cm. That the greatest concentration of larvae in the O-l-cm stratum occurs at natural sunset was also demonstrated in the next experiment ( Fig. 3). When the lights were turned off at sunset and remained off, 56% of the larvae were planktonic 1 hr after sunset No larvae were found below 4 cm ( Fig. 3, top). A core receiving the same treatment, but having the lights
3 DIURNAL 1~IIYTHM IN CHAOBORUS 215-3cm - 1 cm - 2cm 3cm 4cm 5cm Ocm 1 cm 2cm 3cm 4cm f 5cm L D DL FIG. 2. Distribution of larvae in the scdimcnts under varying light conditions. Time at which the cores were frozen is given at the top (SS = solar sunset). Symbols at the bottom designate light conditions for the preceding hour(s), Values expressed are mean values for four replicate experiments (50 larvae/replicate), R = 10% of larval population. R turned on 1 hr after sunset, was processed off, 22% of the population became plank- 1 hr later. All the larvae had reentered tonic 1 hr after sunset, 84% were plankthe sediments; the greatest concentration tonic 2 hr after sunset, and none were (68%) was in the O-l-cm stratum, and below 2 cm. 20% were found below 4 cm. DISCUSSION The light conditions for the final core The results of these experiments indicate experiment closely resembled natural con- that the larvae wcrc testing the light conditions : The lights were turned off at ditions at the mud-water interface. Thus, solar sunset and rcmaincd off (Fig. 3, they become planktonic only if the light bottom). Again, the greatest percentage intensity is below some threshold value. (80%) of larvae was in the O-l-cm stratum If the light intensity is above this value, at solar sunset. When the lights were the larvae reenter the sediments. The turned off at solar sunset and remained depth to which they burrow is a function
4 216 EDWARD J. LAROW LD 0 cm 1 cm 2cm 11 3cm 4cm cm LD FIG. 3. Distribution of larvae in the scclimcnts under varying light conditions. Time at which the cores were frozen is given at the top (SS = solar sunset). Symbols at the bottom designate light conditions for the preceding hour ( s ). Values expressed are mean values for four replicate experiments ( 50 larvae/replicate). R = 10% of larval population. of the intensity of the light stimulus. The core experiment that sampled larvae exposed to constant overhead illumination for a 24-hr period showed that their distribution within the sediments changed with time. Before natural sunset, there was a gradual movement of larvae toward the mud-water interface. This vertical movemcnt within the sediments would, in nature, place a high percentage of the population where they could easily test the light conditions at the mud-water interface at natural sunset. Since the greatest percentagc of the larvae kept under constant conditions was consistently found at the mud-water interface at sunset, chaoborid larvae must have some clock mechanism regulating their movements within the sediments. The experiments illustrated in Figs. 2 and 3 demonstrated that the larvae test the stratum above the sediments at sunset. If the overhead light was on then, there was a large pcrcentagc of larvae below 5 cm in the cores processed after sunset. Those cores proccsscd before solar sunset never had larvae below 5 cm. This sudden appearance of larvae below 5 cm can be
5 DIURNAL RIIYTIIM IN CHAOBORUS 217 attributed to the fact that some larvae tested the aquatic environment and on receiving the light stimulus burrowed down into the core. If the overhead lights were off at solar sunset, the larvae became planktonic and none were below 3 cm. This testing behavior can explain how, under natural conditions, the cndogcnous rhythm of Chaoborus can be reset to coincide with the annual change in time of solar sunset. From 21 Deccmbcr to 21 June sunset is later each evening. During this period, the larvae emerge at a time set by their clock mechanism, and owing to the later sunsets, they eventually encounter a light stimulus above their thrcshold value. This light stimulus at the beginning of their activity period results in a phase shift delaying onset of activity (Bruce 1960). The rhythm of chaoborid larvae is thus continually reset to synchronize with the later sunsets. From 21 June to 21 August the sun sets earlier each evening and the period of darkness is less than 10 hr. The activity period for chaoborid larvae is 10 hr ( LaRow 1968b), so any natural dark pcriods shorter than that would apply a light stimulus to a portion of the chaoborid population late in the activity period (i.e., early morning ). Bruce ( 1960) observed that light signals occurring at or near the end of an activity period rcsultcd in advancing phase shifts. Thus, the rhythm of activity for the chaoborid larvae could be advanced along with the earlier sunsets. Neither of these phase-shift mechanisms arc possible during the interval from 21 August to 21 December, since the natural period of darkness is longer than 10 hr. Two solutions have been postulated to explain the role of the cndogenous rhythm during the autumnal period. First, once Chaoborus fails to receive a light stimu- lus at the beginning or at the end of its cycle, it could rigorously maintain a 24-hr rhythm. This 24-hr rhythm need be maintained only until the water temperature reaches 5C, since activity then ceases ( LaRow 1968a). In spring, when the water temperature rises above 5C, the rhythm can again be set by the method described above for 21 December to 21 June. A second solution is that after 21 August there is a continuous damping of the rhythm and the onset of activity becomes more random. If this occurs, a certain percentage of the population will, by chance alone, emerge from the sediments at the time of sunset and will receive the offset stimulus. This Zeitgebcr will then synchronize that portion of the population. Thus, a percentage of the population would be synchronized each night with the setting sun. To test these two hypotheses, larvae were collected the night of 26 October and transferred in darkness to two 152- X locm Pyrex glass columns containing lake water and sediments. The 325 larvae were kept in continuous darkness and were monitored with a red-filtered flashlight. Peak activity of Chaoborus larvae (i.e., the grcatcst number of planktonic larvae) occurs 2 hr after the offset stimulus (LaRow 1968a). If the first hypothesis is true and the larvae maintain a 24-hr rhythm from 21 August to 21 December, peak activity for 27 October should have occurred at about 2104 hours-2 hr after the 21 August sunset. If the second hypothesis is true, peak activity should have occurred at hr after sunset on the 26 October sampling date. Peak activity on 27 October for the larvae collcctcd on 26 October and maintaincd in constant darkness was at 2100 hours (49% planktonic)- hr after sunset, but only 2 hr after sunset for 21 August. These results indicate that the larvae do indeed maintain a 24:-hr rhythm based on the 21 August sunset. This maintenance of an exact 24-hr rhythm during the autumnal period may be the most important adaptive feature for the endogenous rhythm of Chaoborus larvae. In conclusion, the problem posed by Juday ( 1921) of how light reaches and affects Chaoborus larvae buried in the sediments can be understood in terms of the testing behavior described here. Light need not penetrate the sediments,
6 218 EDWARD J. LAROW The endogenous rhythmicity of Chaoborus Corethra pun&pen& Say. Biol. Bull., 40: places the larvae at the mud-water inter LAROW, E. J, Instar behavior of Chaoboface precisely at solar sunset, enabling them rus punctipennis Say. M.S. Thesis, Kansas to test the light conditions of the aquatic State University, Manhattan. 49 p. medium ~. A persistent diurnal rhythm in Chaoborus larvae. I. The nature of the REFERENCES BRUCX, V. G Environmental entrainment of circadian rhythms. Cold Spring Harbor Symp. Quant. Biol., 25: EGGLETON, F. E Limnetic distribution an d migration of Corethru larvae in two Michigan lakes. Papers Mich. Acad. Sci., 15 : JUDAY, C Observations on the larvae of rhythmicity. Limnol. Oceanog., 13 : b. Environmental factors regulating the diurnal vertical migration of Chaoborus larvae. Ph.D. Thesis, Rutgers University, New Brunswick, N.J. 148 p. WESENBF-RG-LUND, C Biologie der Siisswasserinsektcn. Springer, Berlin. 682 p. WOOD, K. G Ecology of Chaoborus (Diptera:Culicidae) in an Ontario lake. Ecology, 37 :
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