g. comp. Physiol. 97, 329--338 (1975)
9 by Springer-Verlag 1975
Jet-Propulsion in Anisopteran Dragonfly Larvae
P. J. Mill and 1~. S. Pickard*
Department of Pure ~nd Applied Zoology, University of Leeds, England
Received December 17, 1974
Summary. Jet-propulsion in dragonfly larvae is achieved by the rapid ejection of water
from a specialised rectal chamber via the anus, at a frequency of up to 2.2 eycles/s. Movement,
forward thrust and muscular activity have been recorded in restrained and free-swimming
larvae. Forward thrusts of up to 1.5 g wt result from the expiratory phases of cycles lasting
0.1 to 0.4 s. Swimming velocities are in the order of 10 cm/s. The following muscles are shown
to be active during expiratory phases of jetting: anterior, posterior and respiratory dorsoventrals; primary and secondary longitudinal tergals; lateral primary longitudinal sternopleural; dorso-ventral oblique; ventral adductors of the anal appendages. The sub-intestinal
muscle is active during the inspiratory phases of jetting. Activity recorded is compared with
that found during normal ventilation. The larval jet-propulsive mechanism is compared with
that of certain cephalopods and found to be very effective for the larva's relatively small size.
Introduction
Jet-propulsion in insects is unique to dragonfly larvae, although certain
aquatic species do use surface active secretions to produce an expansion thrust for
locomotion (e.g. Stenus, Staphylinidae; Hughes, 1958). Isolated examples of jetpropulsion as an aid to locomotion have been described in other animals (e.g. in the
mollusc, Notarchus (Martin, 1966) and in certain teleosts (Breder, 1926)) and the
best known example is probably t h a t seen in the cephalopods (Packard, 1972).
Locomotion b y jet-propulsion requires a considerable expediture of energy and is
usually reserved for escape from predators. Cephalopods have particularly
exploited this means of escape and provide an interesting comparative study with
the anisopteran larva. I n Onycoteuthis, one of the hooked squids, rigorous escape
often results in the animal actually shooting several metres from the water surface
into a gliding flight (Morton, 1964). Some mechanical aspects of jet-propulsion
have been looked at in cephalopods (Trueman and Packard, 1968; Johnson et al.,
1972; Packard, 1972; Ward, 1972), and in lamellibranehs (u
1936; Trueman,
1967). The basic mechanical study of anisopteran jetting in recent years is t h a t of
Hughes (1958). Hughes used cine photography .to relate abdominal movements to
forward thrust on the animal as determined with an I~CA transducer. Simultaneous records of thrust and pressure changes in the respiratory chamber were
also taken. Mechanical problems associated with tidal jet-propulsion are usually
ones concerning the production of a greatly increased expiratory thrust; a shortest
possible inspiratory recovery with minimum retardation of movement; rapid
acceleration; streamlining; and directional control.
* Present address: Department of Zoology, University College, Cardiff, Wales.
330
P . J . Mill and R. S. Pickard
Jet-propulsionin anisopteran larvae is essentially the result of hyperventilation
(Hughes, 1958; Hughes and Mill, 1966; Olesen, 1972). I n normal ventilation
(Vn) and jetting (Vs) tidal water exchange of a modified region of the hind gut, the
branchial chamber, occurs via the anus (Tonner, 1936; Hughes and Mill, 1966;
Mill and Pickard, 1972 a, b ; Pickard and Mill, 1974). The roles of various abdominal
muscles involved in ventilatory behaviour, other t h a n swimming, have been
described b y Mill and H u g h e s (1966) and Pickard and Mill (1972, 1975). The
present account is concerned with the roles of particular abdominal muscles during
swimming and a comparative consideration of jet-propulsive locomotion.
Materials and Methods
Recordings were made of movement, propulsive forces and muscular activity during jetpropulsion. An isometric strain gauge {Lewis, 1969) was used to record expiratory thrusts in
restrained and chronic preparations. In both cases an aluminium cylinder, 5 mm high and
2 mm in diameter, was fixed to the larval wing buds with epoxy resin. In the restrained
preparations this cylinder was rigidly attached to a vertical lever using aluminium jointing
compound. This compound is brittle at room temperature and yet melts quickly with slight
heat, allowing rapid attachment of the animal to the lever with a minimum amount of discomfort. The larva was then lowered into a water bath supported only by the lever attached
to the wing buds. The strain gauge was hooked up to the other end of the lever (Fig. 1 a). By
tapping the bench or touching the paraprocts, the larva could be encouraged to jet. In some
preparations the aluminium cylinder was connected directly to the strain gauge (Fig. 1 b) so
that the larva was allowed some degree of movement both vertically and laterally. On some
occasions spring levers were used to "load" the strain gauge, sensitising it to the onset of each
jetting thrust, by taking up "slack" in the recording system.
Electrodes were inserted into various abdominal muscles (Pickard and Mill, 1975) (Fig.2)
to record their activity in both restrained and completely free-swimming larvae. The latter
were also photographed with a Bolex cine camera. Larvae of Anax imperator Leach were used
and the muscle terminology is that of Mill (1965).
Results
I n the free-swimming state larvae will jet-propel when (a) vigorously disturbed
(b) in water without a foothold (c) striking at prey.
Mechanics
The Vn cycle usually extended over a period of 0.8 to 2.3 s, whereas the V8 cycle
usually only lasted for 0.1 to 0.4 s. The overall velocity t h a t can be achieved is
largely proportional to the amplitude of the expiratory thrusts of individual
ventilatory cycles, the m e a n frequency of these cycles and the magnitude of
drag forces. J e t t i n g frequencies varied from single spontaneous cycles to 2.2
cycles/s. Swimming sequences began either abruptly, with one or two vigorous
expiratory thrusts (Fig. 3 a) or gradually with cycles of increasing amplitude (Fig.
3 b). The former t y p e is indicative of an escape reaction. Sequences usually ended
gradually with cycles of decreasing amplitude and frequency. M a x i m u m t h r u s t
forces of 1 to 1.5 g wt (1 g wt : 9 . 8 1 • 10-a 1~) were recorded for individual cycles.
These figures have not been corrected for inertia effects but the recording system
allowed v e r y little acceleration to occur. M a x i m u m swimming velocities measured
from cine film were in the order of 10 cm/s over a distance of 10 cm, for final instar
larvae 45 to 55 m m in length.
Jet-Propulsion in Dragonfly Larvae
331
a,
~ "
Starling
FI~
~
Pulley
Weights
Thread
\
I . A[uminium lever
jJ
C
Resin
Water
T
b.
J
A,um,.,urod
Water
Fig. 1 a and b. Recording expiratory thrusts during Vs. (a) larva fully restrained, (b) larva
partially restrained. C aluminium cylinder; F fulcrum; G strain gauge; J aluminium jointing
compound; S adjustable screw stop; Sc semi-conductor; Sp spring; T terylene cord. Inset
(a) : method of gauge calibration. E aluminium extension piece, replaces larva at the aluminium
joint
Muscular Co-Ordination
a) Dorso-Ventral Muscles
W h e n respiratory dorso-ventral muscle (RDV) activity a n d jetting are recorded simultaneously, the RD V is seen t o be involved in producing the locomotory
(expiratory) thrusts (Fig. 3b). I n the free-swimming preparations jetting often
continued for up to 15 s. During maintained jetting the expiratory bursts v a r y
332
P . J . Mill and R. S. Pickard
Fig. 2. Diagram of the right side of the ninth and tenth abdominal segments. A8, eighth
abdominal ganglion; a apodeme; n4, n 5 fourth and fifth lateral nerves; snp, snlo ninth and
tenth median nerves. Muscles: adv anterior dorso-ventral; al alary; atp anterior tergo-pleural;
dabe dorsal abductor of the epiproet; dad dorsal adductor of the paraproct and epiproct;
davr dorsal anal valve retractor; ddv dorsal dilator of the vestibule; dvo dorso-ventral oblique;
labp~, labp2 primary and secondary lateral abductors of the paraproct; lavr lateral anal valve
retractor; ldv lateral dilator of the vestibule; lia lamina inffa-analis; Isa lamina supra-analis;
It1, Ite primary and secondary longitudinal tergals; pdv posterior dorso-ventral; rdv respiratory
dorso-ventral; vadp ventral adductor of the paraproct; vavr ventral anal valve retractor; vdv
ventral dilators of the vestibule; vra ventral retractor of the anus
a.
]l
[ 1 g wt
Thrust
]S
b. [ I g w t
!
.~w~,
-.r . .
.
o.5 s
Thrust
.
!
~T~,-
~
-~ ' -
~l
~ .....
".fl~
~1 " ~
-~'"
~T r
~tf-
-
~
.. . . . . .
-
~
. . . .
.....
-
"
I RDV 7
Fig. 3. (a) Jet propulsive thrusts produced by a partially restrained larva during V s. (b)
Simultaneous recording of propulsive thrusts and activity in the left R D V of segment seven of
a fully restrained larva during Vs. (Upward movement of the force traces indicates increasing
thrust; oscillations after each thrust are products of the recording systems)
b o t h in d u r a t i o n a n d pulse frequency, t h e s h o r t e r b u r s t s a p p e a r i n g in c o n j u n c t i o n
w i t h g r e a t e r t h r u s t s (Fig. 3 b). T h e differences b e t w e e n V~ a n d V~ a c t i v i t y can be
seen in Fig. 4 a . As t h e l a r v a p r e p a r e s t o j e t t h e overall f r e q u e n c y of e x p i r a t o r y
Jet-Propulsion in DragonflyLarvae
333
bursts increases rapidly and successive ventilatory cycles become confluent. The
gradual build-up of pulse frequency characteristic of Vn bursts gives way to a
uniformly high frequency. At a critical point in the preparatory process large
potentials appear in the expiratory bursts and it is at this stage that jetting
thrusts are first observed. Although these larger potentials could reflect the firing
of a second motor axon, they could also be the result of muscle-potential summation
and hence related to pulse frequency. After jetting, the expiratory bursts lengthen
once again but high pulse frequency per burst and high ventilatory rate are maintained for several cycles before the normal ventilatory rhythm is restored. Although
jetting serves to increase respiratory capability as well as to provide locomotion,
this is probably not sufficient to cater for the greatly increased muscular activity,
since deep ventilation always occurs after swimming.
When left and right RDVs of the same segment are recorded from during
V~the precise symmetry of activity seen in V~is not as evident but the expiratory
bursts still begin and end together (Fig. 4 b). No obvious relationship was ovserved
between the large potentials in the expiratory bursts of the two muscles. Many of
the differences between the bursts are probably due to the problems of recording
during exaggerated abdominal movement. Not only are the muscles themselves
contracting vigorously; the segments are telescoping rapidly during jetting and
postural changes are occurring as the larva moves rapidly around the chamber.
Muscles in adjacent segments showed little difference in activity during Vs
(Fig. 4c). Prior to jetting the contraction of the expiratory bursts is accompanied
by loss of the sequential burst initiation usually recorded in V~. Pulse frequency
differences in the expiratory bursts also tend to disappear both before and during
Vs. RD Vs in segments five to eight all showed synchronous activity during jetting.
The anterior dorso-ventral muscles (AD Vs) were also extremely active during
V~, with bursts coinciding closely with those of the RDVs. RDVs and ADVs in the
same segment were always recorded from simultaneously to check for cross-talk
artifacts (Fig. 5 a). As with the RD V, the AD V bursts had increased pulse frequency prior to swimming and the jetting bursts were also eharacterised by the presence
of larger potentials. The third dorso-ventral muscle, the posterior (PDV), was
never found to be active during Vn (Pickard and Mill, 1975) but it was active
during jetting (Fig. 5b). Pulse frequency was found to be low in short periods of
moderate jetting, but high in vigorous expiratory thrusts. The large PD V potentials were always clearly recorded but showed no direct phase relationship with
potentials of either the RD V or the AD V of the same segment or adjacent segments.
However, potentials in the PDV did only appear when large potentials were
present in the RDV and A D V of the same segment, perhaps illustrating that the
PDV comes into action at a particular point of stress or demand for increased
expiratory thrust. It is interesting to note that the PDV is innervated by the
third lateral nerve unlike the A D V and RDV (which are both innervated by the
second lateral nerve), and this anatomical distinction may be related to the
observed functional differences between the muscles.
b) Longitudinal and Oblique Muscles
The primary and secondary longitudinal tergal (LT 1 and LT2), lateral primary
longitudinal sterno-pleural (LLSP1) , and dorso-ventral oblique (DVO) muscles
23
•. comp. Physiol., Vol. 97
334
P . J . Mill and R. S. Piekard
a,
lllnlillLJJlllillllll[lU$111llllil
i
0.58
.
.
.
.
;..
hlIJlllil]JildlUlllii,l~HI.
a
--
:
.
_
..
l]alll~l]dlail~lu&lli~a~
__
llilllanldJl~.~-~-:'i
- V N -
I
Vn
b.
i I
is
,
~, ,
~,.
i,
IRDVz
I RDV5
_ Vs_
Vn
rRDV5
C.
r RDV5
,
3ooms
,
-
s-
Vn
IRDV7
Fig. 4a--c. Expiratory muscle activity in unrestrained larvae. (~) left R D V of segment seven,
(b) left and right R D Vs of segment six, (e) right R D V of segment six and left R D V of segment
seven. (Fn normal ventilation; ~ swimming)
a.
r R D V 2'
vn
IADV7
b.
i
300
ms
,
I AOVz
lIJ
f
i:.
_
,
vn
,
I PDV Z
Fig. 5 a and b. Expiratory muscle activity in unrestrained larvae. (a) right R D g and left A D Y
of segment seven, (b) left A D V and P D V of segment seven. (lZn normal ventilation; other
activity during swimming)
are all active during ~ in synchrony with R D V activity (Figs. 6, 7). However,
whereas the L T 1 and L T 2 are also active during ~ and other types of ventilation
(Pickard and Mill, 1975) the L L S P 1 and D V O are not (Figs. 6b, 7a). Again no
constant phase relationships could be established between potentials recorded
from different muscles. Although these longitudinally orientated muscles act
with the dorso-ventral muscles in ventilatory behaviour, they are capable of independent action (e.g. in lateral curling of the abdomen during defensive behaviour;
Pickard and Mill, 1975). Clearly, the increased expiratory thrust necessary for
jet-propulsion is achieved in two ways. Firstly, muscles active in both Vn and
Jet-Propulsion in Dragonfly Larvae
335
a.
ILT25
,
30d~'s ,,
T
b.
0.5S
i
-
i
Vn"
Vn
r RDV 6
Vn
":=~--r L'LSPt 7
Vn
Fig. 6a and b. Expiratory muscle activity in unrestrained larvae. (a) left LT~s of segments
five and seven, (b) right RDV of segment six and I~LSPz of segment seven. (Vn normal ventilation; other activity during swimming)
a.
r RDV,
.
.,,,,..-. 9 - . - - -
.
9
,1111 ...........:"?'-':_.,
,,,
_
I DV0 B
9
o.s
$
,
b.
r RDV,
i
I DVOs
I
o.5s
C.
r RnV5
. . . . . . . . . . .
rz
'
|~
i
=S
,i
--
..r~---\-__.:.2_~
B E
-
Vs
L J
.
]L1]i[ti
V8
.
.
.
.
j
:6
.
E.[[
E;~[~;
rDVO~
,
Vs
Fig. 7 a--o. Activity in various D VOs compared with that in the right RD V of segment six in
an unrestrained larva during (a) normal ventilation, (b) maintained swimming, (c) bouts of
swimming, ~ and continued normal ventilation
show m u c h higher pulse frequencies per burst during Vs. Secondly, muscles n o t
active during Vn are recruited for Vs. Dorso-ventral contraction during Vs is thus
stronger t h a n t h a t in V~ and haemocoelic pressure is intensified b y longitudinal
contraction. The D VOs contribute to contraction in both dimensions 9
e) Transverse Muscles
The sub-intestinal muscle (SIM) runs transversely across the tergal arch of
segment six. I t was found to be active during the inspiratory phase of each Vs
cycle (Fig. 8a). The bursts consist of m u c h higher frequency potentials and
double pulsing is not as obvious as in Vn (Pickard and Mill, 1975). This m a y be
simply a function of the reduced burst duration or it m a y reflect a closer coupling
between the two axons innervating the muscle.
23*
336
P.J. Mill and R. S. Pickard
|
3oo ms
SIM
b.
I RDV5
c.
I RDV5
3o0 ms
~
X
Fig. 8. Activity in the left RDV of segment five during jet propulsive swimming compared
with that in the (a) SIM, (b) left VADP and muscles at recording position 'X' (see text), and
(c) muscles at recording position 'X'
d) Muscles Associated with the Posterior Region
of the Branchial Apparatus and the Anal Appendages
Activity in the adductor muscles of the paraprocts was clearly evident during
jetting and deep ventilation (Fig. 8b). Recordings from position 'X' (Fig. 8b, c)
were consistent between different individuals and the potentials denote activity in
either the ventral retractor muscle of the anus and/or the ventral dilator muscles
of the vestibule (Pickard and Mill, 1975). All of this activity is synehronised with
R D V expiratory bursts. Adduction of the paraprocts and epiproct during an
expiratory thrust channels the expired water into a narrow jet. B y bending the
abdomen the larva can direct this jet of water with the appendages and so, to
some extent, determine the direction of propulsion.
Discussion
The effectiveness of the jet-propulsion mechanism is largely dependent upon
(a) the velocity and mass of water ejected from the respiratory chamber, (b) the
mass of the whole animal, and (c) the magnitude of induced drag forces. Velocity
and mass of water ejection are affected by (i) the expiratory forces applied to the
chamber, (ii) the cross-sectional area of the expiratory aperture, and (iii) the
volume of the chamber. Packard (1969) points out that jet-propulsion favours
animals with a large body size and suggests that this may account for the rapid
growth rate in cephalopods. Dragonfly larvae employing jet-propulsion certainly
tend to be larger and stronger than larvae not doing so, but they are still much
smaller than all but very immature cephalopods.
Dragonfly larvae and cephalopods apply very different structures to achieve
common mechanical goals. The respiratory chambers in both types of animal can
each be likened to a collapsible cylinder where a decrease in circumference causes a
decrease in volume proportional to the square of the linear change, but a decrease
in length effects a volume change proportional only to the distance shortened
(Ward and Wainwright, 1972). Thus the circular mantle musculature surrounding
the mantle cavity in Coleoidea is ideally suited to providing the expiratory forces.
The dragonfly larva has been shown to employ both dorso-ventral and longitudinal
Jet-Propulsion in Dragonfly Larvae
337
contractions of the abdomen to produce its expiratory forces. Despite this, an
all-round pressure is still applied to the respiratory chamber by virtue of the
haemocoelie transmission, making good use of most of the abdominal musculature.
The method of reducing open anal valve area during expiration has been
described in the dragonfly larva (Mill and Pickard, 1972 b). Hughes (1958) estimated
an anal aperture of less than 0.01 mm 2 during jetting. This very small aperture
greatly enhances the effectiveness of the larva's propulsive mechanism. I t is
also a measure of the muscular power involved in jetting that such an aperture
can be utilised. Cephalopods also restrict funnel aperture during jetting (e.g.
250 g wet weight Sepia--l.5 em2; Trueman and Packard, 1968). Branchial chamber
pressures during single jet-propulsion cycles in dragonfly larvae rarely exceed
50 cm H20 (Aeshna; Hughes and Mill, 1966). But this relates to an animal
weighing about 1 g, whereas in a 250 g Sepia Trueman and Packard (1968) recorded
only 180 cm H20.
During inspiration, the area of intake is increased in Coleoidea by drawing water
in between mantle periphery and funnel, whereas the dragonfly larva simply
opens the anal valve to its fullest extent. Squid also utilise elastic restoring forces
during inspiration (Ward, 1972; Ward and Wainwright, 1972). Similarly, since
cutieular deformation has been shown to occur in dragonfly larvae during expiration in Vn (Pickard and Mill, 1974), it would seem likely that the emphasised
ventilatory movements in Vs would result in cuticular restoring forces considerably promoting inspiration. This conclusion is supported by the current study,
where only one abdominal muscle is found active during inspiration, the SIM.
Although the diaphragm may also be active (Pickard and Mill, 1975), it is
unlikely that even both muscles operating together could achieve the observed
speed and extent of inspiratory movement.
Clearly, the dragonfly larva compares extremely favourably with the cephalopods in the effectiveness of its unique jet-propulsion mechanism. Particularly so,
in view of its relatively small size. However, many cephalopods do have much
greater capacity than dragonfly larvae for sustained swimming, which may reflect
the different escape situations (migrations apart) of open water for squid compared
with weed or mud substrate for dragonfly larvae and/or that dragonfly jetpropulsion consumes relatively too much energy for prolonged use.
R. S. P. wishes to thank the Science Research Council for a studentship during the tenure
of which the above work was carried out.
References
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Hughes, G. 5L, Mill, P.J.: Patterns of ventilation in dragonfly larvae. J. exp. Biol. 44,
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Johnson, W., Soden, P. D., Trueman, E. R.: A study in jet propulsion: an analysis of the
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Martin, R. : On the swimming behaviour and biology of Notarchus punctatu8 Phillips (Gastropoda, Opisthobranchia). Pubbl. Staz. zool. Igapoli 85, 61-75 (1966)
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Dr. R. S. Pickard
Department of Zoology
University College
Cardiff, Wales, Great Britain