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Controlling the fly’s gyroscopes Roland Hengstenberg
rue flies — such as hoverflies or the blow fly Calliphora vicina — have breathtaking aerobatic capabilities due to a very elaborate flight apparatus. Not only do they beat their wings up to 150 times per second, but they have a gearbox with three gears in the wing joint1, and use non-stationary aerodynamics to generate exceptionally large flight forces2. These flies also show masterly control as they fly around obstacles and through turbulent air, and the way in which they do this is revealed in part by Chan et al.3 in Science. The authors report unexpected features of the ‘gyroscopic’ sense organs that tell the fly about its rotations in space. Most insects have four wings, consisting of the thin wing blade spread between a framework of stiff veins that also carry touch and strain receptors4. Wings are, therefore, usually mechanical effectors and sense organs at the same time. The wings of true flies are driven by two kinds of specialized muscle. First, two large ‘power’ muscles (which fill most of the fly’s thorax) contract antagonistically at wing-beat frequency, in mechanical resonance with the thoracic box5. They produce several contraction cycles for each impulse from a motor neuron, so they are also called ‘asynchronous’ muscles5. Second, 13 small ‘control’ muscles, operating synchronously, act on the wing joint to extend and retract the wings, and to modify the wing kinematics for steering5. During evolution, the hind wings from the ancestors of true flies were transformed into the so-called halteres6–8. These are small, club-shaped organs, buried in the cleft between the fly’s thorax and abdomen (Fig. 1a). During flight they oscillate up and down around a hinge joint (Fig. 1b), through an angle of about 180° and in antiphase with the wings. Because of their small size and shape, as well as their location, they can hardly be expected to have any aerodynamic effect. Instead, they have been shown to act as highly specialized ‘gyroscopic’ sense organs, measuring rotations of the fly in space6–8. An oscillating haltere tends to preserve its angular momentum. When the fly turns, a periodic Coriolis force is generated perpendicular to the plane of the oscillation. The Coriolis force means that a mass moving in a rotating system is accelerated perpendicular to its motion and to the axis of rotation. This force acts mainly on the haltere knob (Fig. 1b), and its amplitude is proportional to the vector product of the haltere’s linear velocity and the fly’s angular velocity. So, halteres sense angular velocity directly — unlike the vertebrate semicircular canals, which integrate angular acceleration.
T
NATURE | VOL 392 | 23 APRIL 1998
The frequency of the Coriolis force depends on the direction in which the fly is turning. For pitch turns around the transverse axis, the force has the same frequency as the wing beat. But for yaw turns around the vertical axis, the force has twice the wingbeat frequency6,8. Moreover, although a single haltere is ‘blind’ for rotations around the axis of its oscillation9, roll turns of the fly around the longitudinal body axis can still be sensed because the two halteres are arranged obliquely (Fig. 1a). The necessary distinction of pitch and roll turns is achieved by bilateral processing of the signals from the two halteres6–10, probably in the ventral cord (the insects’ analogue of the spinal cord). The reactive force acting on the centre of mass — that is, on the haltere knob — is transmitted along the stiff stalk (Fig. 1b) to the base of the haltere, where it produces a very complicated spatio-temporal strain pattern in the insect’s cuticle. This pattern is encoded by about 335 cuticular strain receptors, most of which are clustered in five neatly ordered fields around the base of the haltere (Fig. 1b)11. The central nervous pathways that process the signals from these mechanoreceptors are poorly understood. But behavioural studies have shown that flies use the information from their halteres to stabilize the orientation of their head in space7–10, to maintain flight equilibrium12 and to follow their intended course13. Because Calliphora oscillates its halteres as it walks — when the wings are held perfectly still — each haltere must be moved by its own set of muscles. Until now, this has been thought to involve either one or two
power muscles, like those that control the wings. My own observations show that there are two, a depressor and a levator, as proposed by Schneider14. But Chan et al.3 claim that there is only one power muscle, as proposed 50 years ago by Pringle6. Furthermore, the authors describe a set of 11 tiny control muscles, which had never been seen before, at the base of the haltere. Eight of them originate on the hard body wall, and are inserted at various points on minute sclerites of the haltere joint. From these sites of attachment, the authors infer that each is homologous to the corresponding muscle of the wing joint. The mechanosensory function of the halteres therefore seems to be adjustable by commands from the fly’s nervous system. This might involve adaptations to different usage of the halteres when either walking or flying, or it may be a sign of fine tuning of the haltere kinematics. Or, as proposed by Chan et al., it may be a means of particularly efficient flight control, to modulate signals from the halteres that converge on some of the flight control muscles. The most surprising new finding is that at least two of the eight control muscles receive input from the visual system. Chan et al. recorded (extracellularly) the spike activity of the control muscles B2 and I1 in resting flies, while moving striped patterns were presented in the frontal visual field of the experimental fly. They found that the impulse activity of the muscles was modulated by the pattern motion in a directionally specific manner. For example, whereas B2 was maximally excited when the pattern moved downwards and a little to the side of the recorded muscle, I1 responded best to motion 45° upwards and to the same side. The significance of these directional specificities is not yet clear, and the different effects of visual inputs on the two mechanosensory axes of the haltere still have
8
Figure 1 Halteres, the ‘gyroscopic’ sense organs of the blow fly Calliphora vicina. During walking and flight, the halteres oscillate in a vertical plane around a proximal hinge, and Chan et al.3 have now shown that they are under both neural and visual control. a, The halteres (arrowhead) are found between the thorax and abdomen of a fly. b, Left haltere from above. Most of the mass of the haltere is in the knob (left). A thin, stiff stalk leads to a base that houses about 335 cuticular strain receptors. Nature © Macmillan Publishers Ltd 1998
757
news and views to be worked out. But, because halteres sense rotatory self-motions, it seems reasonable to assume that the observed visual motion sensitivities must be interpreted in this context. Thus, although the halteres have been thought of as an extremely specialized, hardwired and purely mechanosensory system, Chan et al.3 have forced us to reconsider the fly’s ‘gyroscopes’ as sense organs that are under neural and visual control. Roland Hengstenberg is at the Max-Planck-Institut für Biologische Kybernetik, Spemannstrasse 38, D-72076 Tübingen, Germany, and at the Institute for Advanced Study, Wallotstrasse 19, D-14193 Berlin, Germany. e-mail: [email protected]
1. Nalbach, G. J. Comp. Physiol. 165, 321–331 (1989). 2. Lehmann, F.-O. & Dickinson, W. H. J. Exp. Biol. 200, 1133–1144 (1997). 3. Chan, W. P., Prete, F. & Dickinson, W. H. Science 280, 289–292 (1998). 4. Dickinson, M. H. J. Exp. Biol. 169, 221–233 (1992). 5. Dickinson, M. H. & Tu, M. S. Comp. Biochem. Physiol. 116A, 223–238 (1997). 6. Pringle, J. W. S. Phil. Trans. R. Soc. Lond. B 233, 347–384 (1948). 7. Hengstenberg, R. J. Comp. Physiol. 163, 151–165 (1988). 8. Nalbach, G. J. Comp. Physiol. 173, 293–300 (1993). 9. Nalbach, G. Neuroscience 61, 149–163 (1994). 10. Nalbach, G. & Hengstenberg, R. J. Comp. Physiol. 175, 695–708 (1994). 11. Gnatzy, W., Grünert, U. & Bender, M. Zoomorphology 106, 312–319 (1987). 12. Faust, R. Zool. Jahrb. Physiol. 63, 325–366 (1952). 13. Heide, G. in Insect Flight (ed. Nachtigall, W.) 35–52 (G. Fischer, Stuttgart, 1983). 14. Schneider, G. Z. Vergl. Physiol. 35, 416–458 (1953).
Climate change
The past as guide to the future Gabriele Hegerl
e know that in recent years the Earth’s climate has been getting warmer. But is this warming unusual relative to low-frequency variations in temperature? If it is, then how much of it has been caused by anthropogenic changes in the composition of the atmosphere? On page 779 of this issue1, Mann et al. provide a reconstruction of past temperature back to the year AD 1400, extending previous records further into the past, and deriving annual temperature anomaly patterns over large parts of the globe. As examples, the authors have produced reconstructions of the ‘year without summer’ (1816), which was probably influenced by the eruption of Mount Tambora in Indonesia, and of 1791 when a strong El Niño is known to have occurred. Such reconstructions are poten-
W
tially useful for interpreting the warming trend in the twentieth century. For example, the reconstructed record for the Northern Hemisphere suggests that the warming is unprecedented, at least since 1400. Also, from a multivariate correlation between the reconstructed temperature time-series for the Northern Hemisphere and external climate influences, it seems that increases in greenhouse gases have been the main forcing in the twentieth century, whereas natural climate forcing by changes in solar irradiance and volcanism dominate the early part of the record. Mann et al. use a quite original and promising method to produce their reconstructions, employing data from tree rings, ice cores, ice melt indices and long historical records of temperature and precipitation.
The reconstruction is based on large-scale patterns of temperature fluctuations in the twentieth century as recorded by instruments. The authors derived an empirical relationship between the strength of these patterns in the twentieth century and the palaeoclimate indices, which were then used to estimate the magnitude of the same patterns in times before instruments were used to record temperature. This approach differs from that taken in producing local temperature reconstructions, on which other reconstructions of global-scale temperature are based (see, for example, refs 2 and 3), and enables use of instrumental data other than temperature and of proxy data influenced by more than temperature. For example, treering data may reflect, among other influences, a combination of temperature and precipitation. Mann and colleagues attempt to use the relation of such variables with atmospheric dynamics to reconstruct largescale temperature patterns. Given the novelty of this approach, it is not surprising that the uncertainties need more investigation4. As the authors acknowledge, climate reconstructions can only be as good as the underlying data. The value of different data as temperature proxies3 varies, which should also influence the pattern reconstructions. Similarly, problems in dating some records may decrease the quality of the reconstruction. Also, we need to know more about the influence of non-resolved patterns on global-scale averages, about the validity of the assumption that proxy and temperature data are related linearly, and about the quality of the reconstruction in the earlier part of the record where data are sparser. Still, when Mann and colleagues’ reconstruction is compared with other new recon-
8
100 YEARS AGO from 21 April 1898.
50 YEARS AGO from 24 April 1948.
758
Nature © Macmillan Publishers Ltd 1998
NATURE | VOL 392 | 23 APRIL 1998
Controlling the fly’s gyroscopes Roland Hengstenberg
rue flies — such as hoverflies or the blow fly Calliphora vicina — have breathtaking aerobatic capabilities due to a very elaborate flight apparatus. Not only do they beat their wings up to 150 times per second, but they have a gearbox with three gears in the wing joint1, and use non-stationary aerodynamics to generate exceptionally large flight forces2. These flies also show masterly control as they fly around obstacles and through turbulent air, and the way in which they do this is revealed in part by Chan et al.3 in Science. The authors report unexpected features of the ‘gyroscopic’ sense organs that tell the fly about its rotations in space. Most insects have four wings, consisting of the thin wing blade spread between a framework of stiff veins that also carry touch and strain receptors4. Wings are, therefore, usually mechanical effectors and sense organs at the same time. The wings of true flies are driven by two kinds of specialized muscle. First, two large ‘power’ muscles (which fill most of the fly’s thorax) contract antagonistically at wing-beat frequency, in mechanical resonance with the thoracic box5. They produce several contraction cycles for each impulse from a motor neuron, so they are also called ‘asynchronous’ muscles5. Second, 13 small ‘control’ muscles, operating synchronously, act on the wing joint to extend and retract the wings, and to modify the wing kinematics for steering5. During evolution, the hind wings from the ancestors of true flies were transformed into the so-called halteres6–8. These are small, club-shaped organs, buried in the cleft between the fly’s thorax and abdomen (Fig. 1a). During flight they oscillate up and down around a hinge joint (Fig. 1b), through an angle of about 180° and in antiphase with the wings. Because of their small size and shape, as well as their location, they can hardly be expected to have any aerodynamic effect. Instead, they have been shown to act as highly specialized ‘gyroscopic’ sense organs, measuring rotations of the fly in space6–8. An oscillating haltere tends to preserve its angular momentum. When the fly turns, a periodic Coriolis force is generated perpendicular to the plane of the oscillation. The Coriolis force means that a mass moving in a rotating system is accelerated perpendicular to its motion and to the axis of rotation. This force acts mainly on the haltere knob (Fig. 1b), and its amplitude is proportional to the vector product of the haltere’s linear velocity and the fly’s angular velocity. So, halteres sense angular velocity directly — unlike the vertebrate semicircular canals, which integrate angular acceleration.
T
NATURE | VOL 392 | 23 APRIL 1998
The frequency of the Coriolis force depends on the direction in which the fly is turning. For pitch turns around the transverse axis, the force has the same frequency as the wing beat. But for yaw turns around the vertical axis, the force has twice the wingbeat frequency6,8. Moreover, although a single haltere is ‘blind’ for rotations around the axis of its oscillation9, roll turns of the fly around the longitudinal body axis can still be sensed because the two halteres are arranged obliquely (Fig. 1a). The necessary distinction of pitch and roll turns is achieved by bilateral processing of the signals from the two halteres6–10, probably in the ventral cord (the insects’ analogue of the spinal cord). The reactive force acting on the centre of mass — that is, on the haltere knob — is transmitted along the stiff stalk (Fig. 1b) to the base of the haltere, where it produces a very complicated spatio-temporal strain pattern in the insect’s cuticle. This pattern is encoded by about 335 cuticular strain receptors, most of which are clustered in five neatly ordered fields around the base of the haltere (Fig. 1b)11. The central nervous pathways that process the signals from these mechanoreceptors are poorly understood. But behavioural studies have shown that flies use the information from their halteres to stabilize the orientation of their head in space7–10, to maintain flight equilibrium12 and to follow their intended course13. Because Calliphora oscillates its halteres as it walks — when the wings are held perfectly still — each haltere must be moved by its own set of muscles. Until now, this has been thought to involve either one or two
power muscles, like those that control the wings. My own observations show that there are two, a depressor and a levator, as proposed by Schneider14. But Chan et al.3 claim that there is only one power muscle, as proposed 50 years ago by Pringle6. Furthermore, the authors describe a set of 11 tiny control muscles, which had never been seen before, at the base of the haltere. Eight of them originate on the hard body wall, and are inserted at various points on minute sclerites of the haltere joint. From these sites of attachment, the authors infer that each is homologous to the corresponding muscle of the wing joint. The mechanosensory function of the halteres therefore seems to be adjustable by commands from the fly’s nervous system. This might involve adaptations to different usage of the halteres when either walking or flying, or it may be a sign of fine tuning of the haltere kinematics. Or, as proposed by Chan et al., it may be a means of particularly efficient flight control, to modulate signals from the halteres that converge on some of the flight control muscles. The most surprising new finding is that at least two of the eight control muscles receive input from the visual system. Chan et al. recorded (extracellularly) the spike activity of the control muscles B2 and I1 in resting flies, while moving striped patterns were presented in the frontal visual field of the experimental fly. They found that the impulse activity of the muscles was modulated by the pattern motion in a directionally specific manner. For example, whereas B2 was maximally excited when the pattern moved downwards and a little to the side of the recorded muscle, I1 responded best to motion 45° upwards and to the same side. The significance of these directional specificities is not yet clear, and the different effects of visual inputs on the two mechanosensory axes of the haltere still have
8
Figure 1 Halteres, the ‘gyroscopic’ sense organs of the blow fly Calliphora vicina. During walking and flight, the halteres oscillate in a vertical plane around a proximal hinge, and Chan et al.3 have now shown that they are under both neural and visual control. a, The halteres (arrowhead) are found between the thorax and abdomen of a fly. b, Left haltere from above. Most of the mass of the haltere is in the knob (left). A thin, stiff stalk leads to a base that houses about 335 cuticular strain receptors. Nature © Macmillan Publishers Ltd 1998
757
news and views to be worked out. But, because halteres sense rotatory self-motions, it seems reasonable to assume that the observed visual motion sensitivities must be interpreted in this context. Thus, although the halteres have been thought of as an extremely specialized, hardwired and purely mechanosensory system, Chan et al.3 have forced us to reconsider the fly’s ‘gyroscopes’ as sense organs that are under neural and visual control. Roland Hengstenberg is at the Max-Planck-Institut für Biologische Kybernetik, Spemannstrasse 38, D-72076 Tübingen, Germany, and at the Institute for Advanced Study, Wallotstrasse 19, D-14193 Berlin, Germany. e-mail: [email protected]
1. Nalbach, G. J. Comp. Physiol. 165, 321–331 (1989). 2. Lehmann, F.-O. & Dickinson, W. H. J. Exp. Biol. 200, 1133–1144 (1997). 3. Chan, W. P., Prete, F. & Dickinson, W. H. Science 280, 289–292 (1998). 4. Dickinson, M. H. J. Exp. Biol. 169, 221–233 (1992). 5. Dickinson, M. H. & Tu, M. S. Comp. Biochem. Physiol. 116A, 223–238 (1997). 6. Pringle, J. W. S. Phil. Trans. R. Soc. Lond. B 233, 347–384 (1948). 7. Hengstenberg, R. J. Comp. Physiol. 163, 151–165 (1988). 8. Nalbach, G. J. Comp. Physiol. 173, 293–300 (1993). 9. Nalbach, G. Neuroscience 61, 149–163 (1994). 10. Nalbach, G. & Hengstenberg, R. J. Comp. Physiol. 175, 695–708 (1994). 11. Gnatzy, W., Grünert, U. & Bender, M. Zoomorphology 106, 312–319 (1987). 12. Faust, R. Zool. Jahrb. Physiol. 63, 325–366 (1952). 13. Heide, G. in Insect Flight (ed. Nachtigall, W.) 35–52 (G. Fischer, Stuttgart, 1983). 14. Schneider, G. Z. Vergl. Physiol. 35, 416–458 (1953).
Climate change
The past as guide to the future Gabriele Hegerl
e know that in recent years the Earth’s climate has been getting warmer. But is this warming unusual relative to low-frequency variations in temperature? If it is, then how much of it has been caused by anthropogenic changes in the composition of the atmosphere? On page 779 of this issue1, Mann et al. provide a reconstruction of past temperature back to the year AD 1400, extending previous records further into the past, and deriving annual temperature anomaly patterns over large parts of the globe. As examples, the authors have produced reconstructions of the ‘year without summer’ (1816), which was probably influenced by the eruption of Mount Tambora in Indonesia, and of 1791 when a strong El Niño is known to have occurred. Such reconstructions are poten-
W
tially useful for interpreting the warming trend in the twentieth century. For example, the reconstructed record for the Northern Hemisphere suggests that the warming is unprecedented, at least since 1400. Also, from a multivariate correlation between the reconstructed temperature time-series for the Northern Hemisphere and external climate influences, it seems that increases in greenhouse gases have been the main forcing in the twentieth century, whereas natural climate forcing by changes in solar irradiance and volcanism dominate the early part of the record. Mann et al. use a quite original and promising method to produce their reconstructions, employing data from tree rings, ice cores, ice melt indices and long historical records of temperature and precipitation.
The reconstruction is based on large-scale patterns of temperature fluctuations in the twentieth century as recorded by instruments. The authors derived an empirical relationship between the strength of these patterns in the twentieth century and the palaeoclimate indices, which were then used to estimate the magnitude of the same patterns in times before instruments were used to record temperature. This approach differs from that taken in producing local temperature reconstructions, on which other reconstructions of global-scale temperature are based (see, for example, refs 2 and 3), and enables use of instrumental data other than temperature and of proxy data influenced by more than temperature. For example, treering data may reflect, among other influences, a combination of temperature and precipitation. Mann and colleagues attempt to use the relation of such variables with atmospheric dynamics to reconstruct largescale temperature patterns. Given the novelty of this approach, it is not surprising that the uncertainties need more investigation4. As the authors acknowledge, climate reconstructions can only be as good as the underlying data. The value of different data as temperature proxies3 varies, which should also influence the pattern reconstructions. Similarly, problems in dating some records may decrease the quality of the reconstruction. Also, we need to know more about the influence of non-resolved patterns on global-scale averages, about the validity of the assumption that proxy and temperature data are related linearly, and about the quality of the reconstruction in the earlier part of the record where data are sparser. Still, when Mann and colleagues’ reconstruction is compared with other new recon-
8
100 YEARS AGO from 21 April 1898.
50 YEARS AGO from 24 April 1948.
758
Nature © Macmillan Publishers Ltd 1998
NATURE | VOL 392 | 23 APRIL 1998
