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Locomotory Modes in the Larva and Pupa of Chironomus Plumosus

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Locomotory Modes in the Larva and Pupa of Chironomus Plumosus Journal of Insect Physiology 46 (2000) 1517–1527 www.elsevier.com/locate/jinsphys Locomotory modes in the larva and pupa of Chironomus plumosus (Diptera, Chironomidae) John Brackenbury Department of Anatomy, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK Received 2 October 1999; received in revised form 6 April 2000; accepted 6 April 2000 Abstract The locomotory kinematics of Chironomus plumosus larvae and pupae were investigated in order to determine how different locomotory techniques may be related to (a) possible underlying patterns of muscle activation and (b) the particular lifestyles and behaviours of these juvenile stages. Larvae display three independent modes of motile activity: swimming, crawling and whole- body respiratory undulation. Swimming and respiratory undulation involve the use of metachronal waves of body bending which travel in a head-to-tail direction. Whereas swimming is produced by side-to-side flexures of the whole body, respiratory undulation employs a sinusoidal wave. Crawling appears to result from an independent programme of muscle activation. Instead of a longitudi- nally transmitting metachronal wave of body flexure, a simultaneous arching of the body, combined with the alternating use of the abdominal and prothoracic pseudopods as anchorage points, produces a form of locomotion analogous to caterpillar-looping. Larval swimming has a set speed and rhythm and is an ‘all-or-nothing’ locomotory manoeuvre, but the neural programme controlling larval crawling is adaptable; switching from a less to a more slippery substrate resulted in a shorter, faster stepping pattern. The pupa displays two swimming modes, somersaulting and eel-like whole-body undulation, the former being principally a brief, escape manoeuvre, the latter being a faster form of locomotion employed to deliver the pupa to the surface prior to adult emergence. Comparison with the pupa of the culicid Culex pipiens shows that this insect also uses the somersault mechanism but at a higher cycle frequency which produces a faster swimming speed. This appears to be related to differences in lifestyle; the surface-living culicid pupa is exposed to greater predator threat than the bottom-dwelling chironomid pupa, and consequently needs a faster escape. 2000 Elsevier Science Ltd. All rights reserved. Keywords: Kinematics; Swimming; Crawling; Somersaulting; Respiratory undulation; Muscle activation sequences; Locomotory control; Ecology 1. Introduction achronism is still recognisable in the walking patterns of modern-limbed hexapods (Hoyle, 1976). Kinematic studies on animal locomotion can serve a Free-living invertebrates with elongated, worm-like dual purpose, providing not only a description of mech- bodies display two characteristic forms of motile anical events but also rudimentary evidence on the way activity: whole-body sinusoidal undulations, as practised in which the locomotory control system may be organ- by aquatic nemertine, nematode and annelid worms ised. In view of the paucity of direct information on (Gray, 1968; Trueman, 1975; Full, 1997), and telescopic locomotory control in simple, soft-bodied invertebrates peristalsis, found in earthworms (Gray and Lissmann, compared with existing knowledge on the control of 1938), caterpillars (Barth, 1937; Hughes, 1974; Casey, walking patterns in limbed arthropods (Huber, 1974; 1991; Brackenbury, 1999a) and the wood-burrowing lar- Hoyle, 1976; Delcomyn, 1981; Eaton, 1985), indirect vae of longhorn beetles (personal observation). Both studies of this nature can be particularly useful. As a kinds of activity involve serial recruitment of the loco- group, the juvenile stages of Diptera lend themselves to motory musculature, in the form of a metachronal wave such an approach since they share a common body plan which travels either tailwards, as in worms and centi- (limbless, segmented, elongate) but occupy a variety of pedes (Manton, 1977; Anderson et al., 1995), or head- niches and have evolved a corresponding diversity of wards (caterpillars, Barth, 1937; saw-fly larvae, personal locomotory styles. The latter range from telescopic observation). Being of extremely ancient lineage, met- crawling (terrestrial maggots, Berrigan and Lighton, 0022-1910/00/$ - see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S0022-1910(00)00079-2 1518 J. Brackenbury / Journal of Insect Physiology 46 (2000) 1517–1527 1993; Berrigan and Pepin, 1995), sinusoidal undulation a normal frame rate of 25 sϪ1. By using a stroboscope (aquatic ceratopogonids, Nachtigall, 1961) and side-to- (Drelloscop 1018, Drelloscop, Germany) at 50 Hz, it was side flexure (chironomid, culicid and corethrid larvae possible to double the imaging rate to 50 fields sϪ1, two and/or pupae, Nachtigall 1961, 1962). Dixid larvae swim separate images being obtained for each binary field nor- like chironomid larvae (lateral flexure) and also modify mally making up a single frame. Data were recorded on the same technique to skate on the water surface a video cassette player equipped with a single field (Brackenbury, 1999b). The larvae of certain cecidomyi- advance facility for detailed image measurement. Body ids and the Mediterranean fruit-fly Ceratitis capitata profiles and swimming trajectories were traced by hand (Maitland, 1992) show the most intriguing locomotion directly from the video screen. The mechanics of larval of all—jumping using elastic energy stored in the integu- crawling underwater was investigated in two experi- ment. mental conditions, the substrate at the bottom of the con- It could justifiably be said that juvenile Diptera, as an tainer being provided either by glass or sand (particle assemblage, have exploited the design capabilities of the sizeϽ0.8 mm). Crawling and swimming appear to be simple, segmented elongated body to their maximum kinematically distinct kinds of locomotion but in order potential. Between-species comparisons of locomotory to determine whether or not there may be gradations techniques show the degree to which specific designs between them observations were made on larvae swim- can be adapted to different physical environmental cir- ming in water in which the viscosity had been artificially cumstances. But an additional dimension can be gained increased by the addition of small amounts of gelatine. by examining individual species which display not one The viscosity of the resulting media was not quantified but several locomotory patterns, since they may provide but at its maximum was sufficient to halt forward information on the organisation and versatility of the motion, without stopping locomotory movements of the locomotory control system. The present study began body. Experimental values are quoted as means±1 stan- from field observations by the author that the aquatic dard error. Paired values were compared for significant stages of Chironomus plumosus display between them differences using the ‘t’-test at a significance level of at least five distinct patterns of motile activity. Further 5%. In total, approximately 50 larvae and 20 pupae were patterns of motor behaviour, for instance tube-building examined with an average of 3–4 measurements per by the larvae, may exist independently of the motile sys- parameter per animal, although it was not practical to tems, but they are not considered here. The objectives obtain data for all locomotory techniques in every indi- of the study were (a) to identify, from kinematic analy- vidual. sis, any evidence of the employment of similar patterns of body flexure to generate different types of loco- motion, and (b) to relate the various types of locomotion 3. Results identified in the larvae and pupae to their respective lifestyles. 3.1. Larval movements In open water the larva uses the familiar ‘figure-of- 2. Materials and methods eight’ style of swimming, produced by side-to-side flexion of the body (Fig. 1A). The hydrodynamics of Chironomus plumosus larvae (final stage) and pupae chironomid larval locomotion has previously been ana- were collected from local rain-pools in early summer and lysed by Nachtigall (1961) and the present study concen- kept in tanks in the laboratory in daylight conditions at trates on evidence that the kinematics of swimming may ambient temperatures of 20–22°C, which were in general reveal about underlying patterns of muscle recruitment. only one or two degrees above outside temperatures for Viewing the larva from its dorsal aspect it can be seen the time of year. The pupae are exclusively bottom- that successive half-strokes rotate the longitudinal axis dwellers, only attempting brief swimming sorties when of the body back and forth through 180° (Fig. 1A). As disturbed or during the final ascent to the surface in a result, the head and abdominal tip trace out double anticipation of adult emergence. Once brought into the cycloidal paths through the water, on alternate sides of laboratory, the larvae readily constructed tunnels in the the mean forward swimming line (Fig. 1B). Throughout detritus at the bottom of the container and showed nor- the cycle, axial length remains constant, indicating the mal behaviour including whole-body respiratory undu- absence of any telescoping of body segments (Fig. 1C). lation, crawling and open-water swimming. Videography Plotting successive body profiles during the half- of larval and pupal movements was performed with a stroke in head-fixed co-ordinates allows the changes in NAC 400 high-speed video system (NAC Inc., Japan) body shape and the resultant motion of the abdominal with
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