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Upwind Movement of Achenes ofCentaurea eriophoraL. on the Ground
Annals of Botany 78 : 431–436, 1996
Upwind Movement of Achenes of Centaurea eriophora L. on the Ground A L L A N W I T Z T U M*, K A L M A N S C H U L G A S S ER† and S T E V E N V O G E L‡ * Department of Life Sciences, † Pearlstone Center for Aeronautical Studies, Department of Mechanical Engineering, Ben Gurion Uniersity of the Nege, P.O.B. 653, Beer Shea, Israel and ‡ Department of Zoology, Duke Uniersity, Durham, NC 27708, USA Received : 20 November 1995
Accepted : 6 March 1996
The lightly compressed achenes of Centaurea eriophora L. bear a pappus composed of stiff bristles at their apex and have an elaiosome appendage at their base. The pappus is ineffective in keeping the achene wind-borne but does serve to regulate the movement of the achene on the ground in response to wind. In wind the achene swivels like a weather vane with the base of the achene pointing into the wind. In weak wind the pappus bristles prevent the achene from blowing away. In stronger wind the bristles move due to their flattened, flexible, hinge-like bases and act like ratchets against the substratum, thus enabling the achene to move upwind. In either case achenes remain in groups. Ants are attracted to the elaiosome and disperse the achenes. Wind-induced movement was explored by testing achenes on various substrata in a wind tunnel at free-stream speeds between 2 and 7 m s−". #1996 Annals of Botany Company Key words : Wind dispersal, Centaurea eriophora, seeds, achenes.
INTRODUCTION
OBSERVATIONS
Centaurea eriophora L., a recent inadvertent introduction to Israel, probably from Morocco (Witztum, 1989), releases compressed achenes approx. 4±0–4±5 mm long, 2±3–2±4 mm wide, brown and shiny in appearance, with sparsely distributed hairs on their surface. An achene bears a lateral elaiosome at its base, where it was attached to the receptacle. The apex of the achene bears a crown-like inner pappus and an outer pappus of toothed bristles of varying lengths, with the longest approaching 6–7 mm. The longer bristles of the pappus are flattened and curved where they emerge from the body of the achene (Figs 1–8). Achenes of Centaurea eriophora L. (Compositae) do not fall far from the mother plant. The pappus does not keep the achene airborne for long and at best may serve as a guide parachute, providing orientation rather than substantial drag. Burrows (1986), citing Hoerner (1965), noted that diaspores with guide parachutes have high terminal velocities and do not undergo much wind-induced lateral movement. On the ground, achenes of C. eriophora are still more resistant to lateral displacement by wind than when airborne. Curiously, though, what movement they make is inevitably upwind, at least in our observations under both casual and controlled conditions in the laboratory. Passive movement directly into the wind has not previously been reported in connection with seed dispersal ; for that matter it is not known in biology and is not an ordinary part of human technology. This paper explores the conditions under which this behaviour can be elicited and its apparent mechanical basis.
If achenes on the ground are exposed to wind, they swivel so the body of the achene points upwind and the pappus points downwind. The stiff bristles of the pappus bear tooth-like cells (Figs 1, 4, 7 and 8). The tips of some of these bristles as well as other pappus teeth contact the soil, as has been described for other dispersal units of similar structure (Kerner von Marilaun, 1895). Pointing away from the body, the bristles and teeth prevent motion of the achene toward the pappus, and thus downwind, with little effect on upwind movement. Thus any random shaking results in unidirectional motion, and an achene that is shaken by wind passing over it ratchets along in a consistently upwind direction. The phenomenon is easily observed by placing one on a piece of paper. Any shaking of an achene sufficient to move it, whether by wind or simply by tapping or vibrating the substratum, makes it move with pappus behind, as the pappus bristle tips and marginal teeth engage the microscopic wood fibres. A minimum wind speed appears necessary to induce movement, while achenes are blown away at very high wind velocities ; thus the upwind movement occurs within a specific, if fairly wide, speed range. Observations with a dissecting microscope, aided by a video camera, show that in winds sufficient to move them, an achene rocks from side to side, so contact between the pappus bristles and the substratum is continuously changing. Movement of the longer bristles is due to their flexible, flattened, and curved hinge-like base (Figs 2, 3 and 6). The space between the rigid base of the crown-like inner pappus and the inflexible short pappus bristles on the outer rim of the achene apex determines the range of movement of the longer pappus bristles with the thin flattened bases (Fig. 3).
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F 1–4. Achenes of Centaurea eriophora L. F. 1. Upper part of achene with pappus bristles. Note shorter bristles at the rim of the achene apex. ¬20. F. 2. Longitudinal section through broad face of the achene. Note crown-like inner pappus. ¬20. F. 3. Flattened bases of the long pappus bristles, and base of crown-like inner pappus. ¬150. F. 4. Portions of pappus bristles. ¬220. All figures reproduced here at 80 %.
The ratchet action and the role of vibration were demonstrated in the absence of wind in the following manner. Achenes were placed in the fold of a sheet of paper inclined at 45° with the pappus bristles pointed down-
wards and the achene body upwards. When the paper was vibrated (by attachment to a test tube stirrer) the achenes rapidly moved up the inclined paper groove. In this case orientation is imposed by the groove, forward movement is
Witztum et al.—Upwind Moement of Achenes on the Ground
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F 5–8. Achenes of Centaurea eriophora L. F. 5. Centre of pappus from above. ¬35. F. 6. Section through flattened bases of long pappus bristles. ¬1500. F. 7. Cut and uncut pappus bristles. ¬400. F. 8. Tip of pappus bristle. ¬500. All figures reproduced here at 80 %.
due to the vibrations of the bristle-like pappus, and retrogression is prevented by those bristle tips which are in contact with the substrate at any given instant. Achenes of Centaurea hyalolepis Boiss., which are much
smaller and lighter but which also have a pappus, behave similarly but are easily blown away at wind speeds at which C. eriophora achenes lock into position or move into the wind. Similarly, achenes of C. crocodylium L., which are
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heavier than those of C. eriophora but where the achene body is covered with hairs, are more easily blown away. (Achenes of C. hyalolepis have small elaiosomes while those of C. crocodylium lack them altogether.) On a windy day, groups of five achenes from each of the above three species of Centaurea were placed on a relatively smooth concrete surface. As wind direction changed achenes of all three species swiveled into the wind. After some minutes in a wind of fluctuating speed the small achenes of C. hyalolepis as well as the heavier but hairy achenes of C. crocodylium were blown away. By contrast, the achenes of C. eriophora moved in group formation, swiveling uniformly and either remaining stationary or moving into the wind. After 30 min the groups were still intact. C. eriophora achenes placed in areas where harvester ants (Messor sp.) were active were grasped by their elaiosomes and carried off. EXPERIMENTAL PROCEDURES Achenes (entire or cut with a razor blade) were mounted on stubs, grounded with silver paste, sputter-coated with gold}palladium, and examined in a field emission SEM (Hitachi S-800 FESEM) at an accelerating voltage of 10 kV. A small wind tunnel (Fig. 9) permitted estimation of the wind speeds required to move the achenes of C. eriophora. Wind was drawn in an upper and lower channel across a flat plate 42 mm beneath the top and above the bottom of the tunnel ; it then passed through a perforated metal grid into a fan box and thence upward through the blades of the fan. The latter, 180 mm in diameter, was driven by a 50 W motor and a proportional speed control (Minarik SL-32). Exploration with a stream of smoke revealed no gross fluctuations or turbulence in the stream. For calibration, centre-channel speed was determined by dangling a Teflon sphere, 6±35 mm in diameter, from a fine thread and noting the horizontal deflection of the thread ; a drag coefficient of 0±5 (with respect to frontal area) was assumed, from Vogel (1994). Speeds between 2±0 and 10±6 m s−" could be produced
with a systematic error of less than³5 % and a repeatability of less than³2 %. It should be born in mind that speeds cited here refer to the centre of the upper channel ; achenes downstream from the upstream edge of the flat plate were exposed wholly or in part to a velocity gradient (the ‘ boundary layer ’) and substantially lower average winds. The flat plate could be covered with paper or other thin substrata, while the panel that formed the top of the tunnel was transparent for observations and measurements.
RESULTS Achenes moved upwind quite satisfactorily and about equally well on coarse paper, dry soil, or brick (the upper surface of these latter coplanar with the floor of the tunnel). Conversely, they were reluctant to travel across sandpaper of any coarseness between 40 and 220 grit, and moved only a little faster on beach sand dusted onto a sticky (via a coating of petroleum jelly) substratum. The threshold wind speed for initial orientation, though, was largely independent of the specific character of the surface. A series of six achenes on coarse construction paper all faced into a wind of 2±4³0±2 m s−" when placed 140 mm back from the upstream edge of the substratum, and upwind motion was detectable at 3±0³0±2 m s−". Differences among achenes with respect to both variables were thus notably low. Figure 10 gives the results of measurements of the average speed at which the same six achenes advanced from 30 to 10 mm back from the upstream edge as a function of centrechannel wind speed. An alternative view consists of a linear regression of logarithms of the data (used since the logarithmic versions showed no evident curvature) and gives the following equation, where wind speed (x) is in m s−" and achene speed (y) is in mm s−" : y ¯ 0±00335 x%±"&, r# ¯ 0±973
Since the retarding effect of a surface on wind across it increases with distance from an upstream edge (see Vogel,
Achene speed (mm s–1)
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Wind direction
Achene direction
Elaiosome
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0 F. 9. Wind tunnel used in present work. Airflow is from lower left to upper right, above and below a thin Plexiglass board that divides the channel.
(1)
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5 6 Wind speed (m s–1)
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F. 10. Speed of upwind motion of achenes vs. mid-channel speed ; error bars give standard deviations for six seeds.
Witztum et al.—Upwind Moement of Achenes on the Ground
about 2 mm or more, they literally dove into it ; they crossed fissures of smaller width. Casual observations of stored specimens (New Mexico State University Herbarium) show that achenes of Centaurea americana Null. move upwind in a manner similar to those of C. eriophora.
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DISCUSSION
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50 70 90 110 Distance downstream (mm)
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F. 11. Speed of upwind motion of an achene vs. distance from upstream edge of the substratum ; averages and standard deviations for four tests at 6±0 m s-".
1994), at any given centre-channel wind speed an achene further downstream is in effect in a less windy environment. Figure 11 gives the results of measurements of the speed of an achene as a function of distance from the upstream edge, at a wind speed of 6±0 m s−" ; the particular achene was one of the six used previously and was thus demonstrably typical. Linear regression of logarithms of the data, with achene speed (y) in mm s−" and downstream distance (x) in mm, gives : (2) y ¯ 21±14 x−!±($(, r# ¯ 0±960 The pappus of bristles on the achenes appears to stabilize them in wind rather than, by raising drag or upward lift, increasing their tendency to be dislodged and carried downwind. Intact achenes in almost all cases when they lost purchase and blew downwind, did so when they reached the upstream edge, whatever the tunnel speed. By contrast, six achenes in which the bristles had been trimmed back as far as possible with iridectomy scissors, placed 20 mm downstream, failed to orient or travel upwind and dislodged at 6±7³0±7 m s−". Any device placed near the upstream edge of the tunnel that increased the irregularity of the air stream decreased the threshold speeds for both orientation and movement and increased the speed of movement. It is uncertain whether the immediate agent is steepening of the velocity gradient near the surface (at which the wind speed is, of course, zero) and thus exposure of achenes to greater wind, or increasing turbulence and thus greater shaking of the seeds, or both. If a lateral gradient of wind speed is provided, by partial blocking of the channel downstream from an achene, it moves toward the greater wind speed. The mechanism appears trivial : greater drag on the side of the achene exposed to the greater wind pushes the bristles on that side farther downwind, causing the achene to rotate toward the greater wind ; and achenes always moved in the same direction relative to their orientation. If in their movement upwind in the channel, achenes encountered a cross-wind trench or fissure with a width of
The structure of the achene in the genus Centaurea was described in detail by Dittrich (1968) and a concise summary was provided by Roth (1977). In some species of Centaurea the presence of an elaiosome is accompanied by loss of the pappus (van der Pijl, 1972). Elaiosomes attract ants, and dispersal is myrmecochorous. Achenes of Centaurea eriophora L. are avidly carried off by ants attracted to the elaiosome at the base of the achene. Thus the presence of the pappus is enigmatic. It does not keep the achene windborne and at best may serve as a guide parachute. The present results suggest that it retains a function in dispersal, through the peculiar upwind movement of achenes on the ground for which it is a crucial component, or by preventing scattering by wind. Both phenomena may ultimately result in ‘ planting ’ of the achenes. While the speeds of movement are slight, they may serve to propel achenes until they enter a crack in the soil surface. The mechanism of movement consists of orientation in the manner of a weather-vane and conversion of random shaking into unidirectional motion by permitting slippage in only one direction. It is simple and not especially demanding with respect to either wind speed or inclination or roughness of the substratum. Nor does it depend on appreciable modification of achene structure typical of the group of plants. The flattened and curved hinge-like base of the longer pappus bristles facilitates bristle movement in wind. Poor performance on sand paper and pure sand most likely reflects the reduced number of contacts between achenes and these substrata. The aerodynamic behaviour of the achenes may enhance myrmecochory as well, primarily by keeping achenes in a group even in strong winds until they are discovered by ants. As the group moves, those that encounter fissures will be self-planted, while the remaining ones may be planted by ants. The latter eat the nutritive tissue of the elaiosome but cannot chew through the hard achene itself. The tactic should be most effective if achenes are released during the day, when ants are active, and kept in a group near the mother plant, thus minimizing predation by nocturnal rodents, as noted for the Cape flora by Bond, Yeaton and Stock (1991). It is of interest that the involucral bracts of the capitulum open most widely during the heat of the day facilitating achene release and are more closed at night. Shmida (1985) has discussed the mixed dispersal strategy of Compositae that have an inconsistently deciduous pappus. Plitmann (1986) studied mixed dispersal strategies in numerous Compositae from Turkey. Some of these taxa had a dispersal strategy which combined myrmecochory with another mode of dispersal. Under conditions of changing humidity hygroscopic bristles in some species of Centaurea perform movements that may help in achene dispersal (van der Pijl, 1972). The hindrance of dispersal
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(antitelechory) is well known in the Compositae (Zohary, 1962). The function of the pappus in preventing dispersal of achenes in weak wind and keeping them together as they move upwind in stronger wind facilitates their more effective removal by ants once a group of achenes has been discovered. ‘ Although ant manipulation may not be foolproof, the evidence is that it can be effective ’ (Beattie, 1985). For biological entities in contact with the substratum, movement in the direction of fluid flow is extremely common and movement at some angle to the direction of the flow has been reported in a few cases (Vogel, 1994). The present case, as far as we are aware, is the first report of movement directly opposite the direction of the flow. It is uncertain to what extent the phenomenon reflects novel structural arrangements selected for this behaviour rather than behaviour incidental to pre-existing structure. The uncertainty results largely from the apparent simplicity of the scheme. Vibrations induced by the wind, unidirectional slippage of the pappus, and the weather-vane orientation of the entire achene propel achenes into the wind and keep them together even in strong winds, enabling both selfplanting and effective myrmecochory. A C K N O W L E D G E M E N TS This collaboration was made possible by a Dozor Visiting Professorship given to SV by Ben-Gurion University of the Negev. We thank Tina M. Weatherby, Biological Electron Microscope Facility, University of Hawaii at Manoa, for her help with the SEM, and Richard Spellenberg, New Mexico State University, for suggesting and providing C.
americana. We are grateful to Drs Ronny Shneck and Olga Nabutovskaya of the Department of Material Sciences, Ben-Gurion University of the Negev, for their SEM work and suggestions. LITERATURE CITED Beattie AJ. 1985. The eolutionary ecology of ant-plant mutualisms. Cambridge : Cambridge University Press. Bond WJ, Yeaton R, Stock WD. 1991. Myrmecochory in Cape Fynbos. In : Huxley CR, Cutler DF, eds. Ant–plant interactions. Oxford : Oxford University Press, 448–462. Burrows FM. 1986. The aerial motion of seeds, fruits, spores and pollen. In : Murray DR, ed. Seed dispersal. Sydney : Academic Press, 1–47. Dittrich M. 1968. Karpologische Untersuchungen zur Systematik von Centaurea und verwandten Gattungen. Botanische Jahrbuch 88 : 70–162. Hoerner SF. 1965. Fluid-dynamic drag. Vancouver WA : Hoerner Fluid Dynamics. Kerner von Marilaun A. 1895. The natural history of plants. London : Blackie & Son. van der Pijl L. 1972. Principles of dispersal in higher plants, 2nd Edn. Berlin : Springer-Verlag. Plitmann U. 1986. Alternative modes in dispersal strategies, with an emphasis on herbaceous plants of the Middle East. Proceedings of the Royal Society of Edinburgh 89B : 193–202. Roth I. 1977. Fruits of angiosperms. Berlin : Gebru$ der Borntraeger. Shmida A. 1985. Why do some Compositae have an inconsistently deciduous pappus ? Annals of the Missouri Botanical Garden 72 : 184–186. Vogel S. 1994. Life in moing fluids. Princeton NJ : Princeton University Press. Witztum A. 1989. Contributions to the flora of Israel and Sinai. IV.Centaurea eriophora L. in Israel. Israel Journal of Botany 38 : 59–62. Zohary M. 1962. Plant life of Palestine. New York : Ronald Press.
Upwind Movement of Achenes of Centaurea eriophora L. on the Ground A L L A N W I T Z T U M*, K A L M A N S C H U L G A S S ER† and S T E V E N V O G E L‡ * Department of Life Sciences, † Pearlstone Center for Aeronautical Studies, Department of Mechanical Engineering, Ben Gurion Uniersity of the Nege, P.O.B. 653, Beer Shea, Israel and ‡ Department of Zoology, Duke Uniersity, Durham, NC 27708, USA Received : 20 November 1995
Accepted : 6 March 1996
The lightly compressed achenes of Centaurea eriophora L. bear a pappus composed of stiff bristles at their apex and have an elaiosome appendage at their base. The pappus is ineffective in keeping the achene wind-borne but does serve to regulate the movement of the achene on the ground in response to wind. In wind the achene swivels like a weather vane with the base of the achene pointing into the wind. In weak wind the pappus bristles prevent the achene from blowing away. In stronger wind the bristles move due to their flattened, flexible, hinge-like bases and act like ratchets against the substratum, thus enabling the achene to move upwind. In either case achenes remain in groups. Ants are attracted to the elaiosome and disperse the achenes. Wind-induced movement was explored by testing achenes on various substrata in a wind tunnel at free-stream speeds between 2 and 7 m s−". #1996 Annals of Botany Company Key words : Wind dispersal, Centaurea eriophora, seeds, achenes.
INTRODUCTION
OBSERVATIONS
Centaurea eriophora L., a recent inadvertent introduction to Israel, probably from Morocco (Witztum, 1989), releases compressed achenes approx. 4±0–4±5 mm long, 2±3–2±4 mm wide, brown and shiny in appearance, with sparsely distributed hairs on their surface. An achene bears a lateral elaiosome at its base, where it was attached to the receptacle. The apex of the achene bears a crown-like inner pappus and an outer pappus of toothed bristles of varying lengths, with the longest approaching 6–7 mm. The longer bristles of the pappus are flattened and curved where they emerge from the body of the achene (Figs 1–8). Achenes of Centaurea eriophora L. (Compositae) do not fall far from the mother plant. The pappus does not keep the achene airborne for long and at best may serve as a guide parachute, providing orientation rather than substantial drag. Burrows (1986), citing Hoerner (1965), noted that diaspores with guide parachutes have high terminal velocities and do not undergo much wind-induced lateral movement. On the ground, achenes of C. eriophora are still more resistant to lateral displacement by wind than when airborne. Curiously, though, what movement they make is inevitably upwind, at least in our observations under both casual and controlled conditions in the laboratory. Passive movement directly into the wind has not previously been reported in connection with seed dispersal ; for that matter it is not known in biology and is not an ordinary part of human technology. This paper explores the conditions under which this behaviour can be elicited and its apparent mechanical basis.
If achenes on the ground are exposed to wind, they swivel so the body of the achene points upwind and the pappus points downwind. The stiff bristles of the pappus bear tooth-like cells (Figs 1, 4, 7 and 8). The tips of some of these bristles as well as other pappus teeth contact the soil, as has been described for other dispersal units of similar structure (Kerner von Marilaun, 1895). Pointing away from the body, the bristles and teeth prevent motion of the achene toward the pappus, and thus downwind, with little effect on upwind movement. Thus any random shaking results in unidirectional motion, and an achene that is shaken by wind passing over it ratchets along in a consistently upwind direction. The phenomenon is easily observed by placing one on a piece of paper. Any shaking of an achene sufficient to move it, whether by wind or simply by tapping or vibrating the substratum, makes it move with pappus behind, as the pappus bristle tips and marginal teeth engage the microscopic wood fibres. A minimum wind speed appears necessary to induce movement, while achenes are blown away at very high wind velocities ; thus the upwind movement occurs within a specific, if fairly wide, speed range. Observations with a dissecting microscope, aided by a video camera, show that in winds sufficient to move them, an achene rocks from side to side, so contact between the pappus bristles and the substratum is continuously changing. Movement of the longer bristles is due to their flexible, flattened, and curved hinge-like base (Figs 2, 3 and 6). The space between the rigid base of the crown-like inner pappus and the inflexible short pappus bristles on the outer rim of the achene apex determines the range of movement of the longer pappus bristles with the thin flattened bases (Fig. 3).
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Witztum et al.—Upwind Moement of Achenes on the Ground
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F 1–4. Achenes of Centaurea eriophora L. F. 1. Upper part of achene with pappus bristles. Note shorter bristles at the rim of the achene apex. ¬20. F. 2. Longitudinal section through broad face of the achene. Note crown-like inner pappus. ¬20. F. 3. Flattened bases of the long pappus bristles, and base of crown-like inner pappus. ¬150. F. 4. Portions of pappus bristles. ¬220. All figures reproduced here at 80 %.
The ratchet action and the role of vibration were demonstrated in the absence of wind in the following manner. Achenes were placed in the fold of a sheet of paper inclined at 45° with the pappus bristles pointed down-
wards and the achene body upwards. When the paper was vibrated (by attachment to a test tube stirrer) the achenes rapidly moved up the inclined paper groove. In this case orientation is imposed by the groove, forward movement is
Witztum et al.—Upwind Moement of Achenes on the Ground
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F 5–8. Achenes of Centaurea eriophora L. F. 5. Centre of pappus from above. ¬35. F. 6. Section through flattened bases of long pappus bristles. ¬1500. F. 7. Cut and uncut pappus bristles. ¬400. F. 8. Tip of pappus bristle. ¬500. All figures reproduced here at 80 %.
due to the vibrations of the bristle-like pappus, and retrogression is prevented by those bristle tips which are in contact with the substrate at any given instant. Achenes of Centaurea hyalolepis Boiss., which are much
smaller and lighter but which also have a pappus, behave similarly but are easily blown away at wind speeds at which C. eriophora achenes lock into position or move into the wind. Similarly, achenes of C. crocodylium L., which are
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heavier than those of C. eriophora but where the achene body is covered with hairs, are more easily blown away. (Achenes of C. hyalolepis have small elaiosomes while those of C. crocodylium lack them altogether.) On a windy day, groups of five achenes from each of the above three species of Centaurea were placed on a relatively smooth concrete surface. As wind direction changed achenes of all three species swiveled into the wind. After some minutes in a wind of fluctuating speed the small achenes of C. hyalolepis as well as the heavier but hairy achenes of C. crocodylium were blown away. By contrast, the achenes of C. eriophora moved in group formation, swiveling uniformly and either remaining stationary or moving into the wind. After 30 min the groups were still intact. C. eriophora achenes placed in areas where harvester ants (Messor sp.) were active were grasped by their elaiosomes and carried off. EXPERIMENTAL PROCEDURES Achenes (entire or cut with a razor blade) were mounted on stubs, grounded with silver paste, sputter-coated with gold}palladium, and examined in a field emission SEM (Hitachi S-800 FESEM) at an accelerating voltage of 10 kV. A small wind tunnel (Fig. 9) permitted estimation of the wind speeds required to move the achenes of C. eriophora. Wind was drawn in an upper and lower channel across a flat plate 42 mm beneath the top and above the bottom of the tunnel ; it then passed through a perforated metal grid into a fan box and thence upward through the blades of the fan. The latter, 180 mm in diameter, was driven by a 50 W motor and a proportional speed control (Minarik SL-32). Exploration with a stream of smoke revealed no gross fluctuations or turbulence in the stream. For calibration, centre-channel speed was determined by dangling a Teflon sphere, 6±35 mm in diameter, from a fine thread and noting the horizontal deflection of the thread ; a drag coefficient of 0±5 (with respect to frontal area) was assumed, from Vogel (1994). Speeds between 2±0 and 10±6 m s−" could be produced
with a systematic error of less than³5 % and a repeatability of less than³2 %. It should be born in mind that speeds cited here refer to the centre of the upper channel ; achenes downstream from the upstream edge of the flat plate were exposed wholly or in part to a velocity gradient (the ‘ boundary layer ’) and substantially lower average winds. The flat plate could be covered with paper or other thin substrata, while the panel that formed the top of the tunnel was transparent for observations and measurements.
RESULTS Achenes moved upwind quite satisfactorily and about equally well on coarse paper, dry soil, or brick (the upper surface of these latter coplanar with the floor of the tunnel). Conversely, they were reluctant to travel across sandpaper of any coarseness between 40 and 220 grit, and moved only a little faster on beach sand dusted onto a sticky (via a coating of petroleum jelly) substratum. The threshold wind speed for initial orientation, though, was largely independent of the specific character of the surface. A series of six achenes on coarse construction paper all faced into a wind of 2±4³0±2 m s−" when placed 140 mm back from the upstream edge of the substratum, and upwind motion was detectable at 3±0³0±2 m s−". Differences among achenes with respect to both variables were thus notably low. Figure 10 gives the results of measurements of the average speed at which the same six achenes advanced from 30 to 10 mm back from the upstream edge as a function of centrechannel wind speed. An alternative view consists of a linear regression of logarithms of the data (used since the logarithmic versions showed no evident curvature) and gives the following equation, where wind speed (x) is in m s−" and achene speed (y) is in mm s−" : y ¯ 0±00335 x%±"&, r# ¯ 0±973
Since the retarding effect of a surface on wind across it increases with distance from an upstream edge (see Vogel,
Achene speed (mm s–1)
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Wind direction
Achene direction
Elaiosome
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0 F. 9. Wind tunnel used in present work. Airflow is from lower left to upper right, above and below a thin Plexiglass board that divides the channel.
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5 6 Wind speed (m s–1)
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F. 10. Speed of upwind motion of achenes vs. mid-channel speed ; error bars give standard deviations for six seeds.
Witztum et al.—Upwind Moement of Achenes on the Ground
about 2 mm or more, they literally dove into it ; they crossed fissures of smaller width. Casual observations of stored specimens (New Mexico State University Herbarium) show that achenes of Centaurea americana Null. move upwind in a manner similar to those of C. eriophora.
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Achene speed (mm s–1)
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DISCUSSION
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50 70 90 110 Distance downstream (mm)
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F. 11. Speed of upwind motion of an achene vs. distance from upstream edge of the substratum ; averages and standard deviations for four tests at 6±0 m s-".
1994), at any given centre-channel wind speed an achene further downstream is in effect in a less windy environment. Figure 11 gives the results of measurements of the speed of an achene as a function of distance from the upstream edge, at a wind speed of 6±0 m s−" ; the particular achene was one of the six used previously and was thus demonstrably typical. Linear regression of logarithms of the data, with achene speed (y) in mm s−" and downstream distance (x) in mm, gives : (2) y ¯ 21±14 x−!±($(, r# ¯ 0±960 The pappus of bristles on the achenes appears to stabilize them in wind rather than, by raising drag or upward lift, increasing their tendency to be dislodged and carried downwind. Intact achenes in almost all cases when they lost purchase and blew downwind, did so when they reached the upstream edge, whatever the tunnel speed. By contrast, six achenes in which the bristles had been trimmed back as far as possible with iridectomy scissors, placed 20 mm downstream, failed to orient or travel upwind and dislodged at 6±7³0±7 m s−". Any device placed near the upstream edge of the tunnel that increased the irregularity of the air stream decreased the threshold speeds for both orientation and movement and increased the speed of movement. It is uncertain whether the immediate agent is steepening of the velocity gradient near the surface (at which the wind speed is, of course, zero) and thus exposure of achenes to greater wind, or increasing turbulence and thus greater shaking of the seeds, or both. If a lateral gradient of wind speed is provided, by partial blocking of the channel downstream from an achene, it moves toward the greater wind speed. The mechanism appears trivial : greater drag on the side of the achene exposed to the greater wind pushes the bristles on that side farther downwind, causing the achene to rotate toward the greater wind ; and achenes always moved in the same direction relative to their orientation. If in their movement upwind in the channel, achenes encountered a cross-wind trench or fissure with a width of
The structure of the achene in the genus Centaurea was described in detail by Dittrich (1968) and a concise summary was provided by Roth (1977). In some species of Centaurea the presence of an elaiosome is accompanied by loss of the pappus (van der Pijl, 1972). Elaiosomes attract ants, and dispersal is myrmecochorous. Achenes of Centaurea eriophora L. are avidly carried off by ants attracted to the elaiosome at the base of the achene. Thus the presence of the pappus is enigmatic. It does not keep the achene windborne and at best may serve as a guide parachute. The present results suggest that it retains a function in dispersal, through the peculiar upwind movement of achenes on the ground for which it is a crucial component, or by preventing scattering by wind. Both phenomena may ultimately result in ‘ planting ’ of the achenes. While the speeds of movement are slight, they may serve to propel achenes until they enter a crack in the soil surface. The mechanism of movement consists of orientation in the manner of a weather-vane and conversion of random shaking into unidirectional motion by permitting slippage in only one direction. It is simple and not especially demanding with respect to either wind speed or inclination or roughness of the substratum. Nor does it depend on appreciable modification of achene structure typical of the group of plants. The flattened and curved hinge-like base of the longer pappus bristles facilitates bristle movement in wind. Poor performance on sand paper and pure sand most likely reflects the reduced number of contacts between achenes and these substrata. The aerodynamic behaviour of the achenes may enhance myrmecochory as well, primarily by keeping achenes in a group even in strong winds until they are discovered by ants. As the group moves, those that encounter fissures will be self-planted, while the remaining ones may be planted by ants. The latter eat the nutritive tissue of the elaiosome but cannot chew through the hard achene itself. The tactic should be most effective if achenes are released during the day, when ants are active, and kept in a group near the mother plant, thus minimizing predation by nocturnal rodents, as noted for the Cape flora by Bond, Yeaton and Stock (1991). It is of interest that the involucral bracts of the capitulum open most widely during the heat of the day facilitating achene release and are more closed at night. Shmida (1985) has discussed the mixed dispersal strategy of Compositae that have an inconsistently deciduous pappus. Plitmann (1986) studied mixed dispersal strategies in numerous Compositae from Turkey. Some of these taxa had a dispersal strategy which combined myrmecochory with another mode of dispersal. Under conditions of changing humidity hygroscopic bristles in some species of Centaurea perform movements that may help in achene dispersal (van der Pijl, 1972). The hindrance of dispersal
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Witztum et al.—Upwind Moement of Achenes on the Ground
(antitelechory) is well known in the Compositae (Zohary, 1962). The function of the pappus in preventing dispersal of achenes in weak wind and keeping them together as they move upwind in stronger wind facilitates their more effective removal by ants once a group of achenes has been discovered. ‘ Although ant manipulation may not be foolproof, the evidence is that it can be effective ’ (Beattie, 1985). For biological entities in contact with the substratum, movement in the direction of fluid flow is extremely common and movement at some angle to the direction of the flow has been reported in a few cases (Vogel, 1994). The present case, as far as we are aware, is the first report of movement directly opposite the direction of the flow. It is uncertain to what extent the phenomenon reflects novel structural arrangements selected for this behaviour rather than behaviour incidental to pre-existing structure. The uncertainty results largely from the apparent simplicity of the scheme. Vibrations induced by the wind, unidirectional slippage of the pappus, and the weather-vane orientation of the entire achene propel achenes into the wind and keep them together even in strong winds, enabling both selfplanting and effective myrmecochory. A C K N O W L E D G E M E N TS This collaboration was made possible by a Dozor Visiting Professorship given to SV by Ben-Gurion University of the Negev. We thank Tina M. Weatherby, Biological Electron Microscope Facility, University of Hawaii at Manoa, for her help with the SEM, and Richard Spellenberg, New Mexico State University, for suggesting and providing C.
americana. We are grateful to Drs Ronny Shneck and Olga Nabutovskaya of the Department of Material Sciences, Ben-Gurion University of the Negev, for their SEM work and suggestions. LITERATURE CITED Beattie AJ. 1985. The eolutionary ecology of ant-plant mutualisms. Cambridge : Cambridge University Press. Bond WJ, Yeaton R, Stock WD. 1991. Myrmecochory in Cape Fynbos. In : Huxley CR, Cutler DF, eds. Ant–plant interactions. Oxford : Oxford University Press, 448–462. Burrows FM. 1986. The aerial motion of seeds, fruits, spores and pollen. In : Murray DR, ed. Seed dispersal. Sydney : Academic Press, 1–47. Dittrich M. 1968. Karpologische Untersuchungen zur Systematik von Centaurea und verwandten Gattungen. Botanische Jahrbuch 88 : 70–162. Hoerner SF. 1965. Fluid-dynamic drag. Vancouver WA : Hoerner Fluid Dynamics. Kerner von Marilaun A. 1895. The natural history of plants. London : Blackie & Son. van der Pijl L. 1972. Principles of dispersal in higher plants, 2nd Edn. Berlin : Springer-Verlag. Plitmann U. 1986. Alternative modes in dispersal strategies, with an emphasis on herbaceous plants of the Middle East. Proceedings of the Royal Society of Edinburgh 89B : 193–202. Roth I. 1977. Fruits of angiosperms. Berlin : Gebru$ der Borntraeger. Shmida A. 1985. Why do some Compositae have an inconsistently deciduous pappus ? Annals of the Missouri Botanical Garden 72 : 184–186. Vogel S. 1994. Life in moing fluids. Princeton NJ : Princeton University Press. Witztum A. 1989. Contributions to the flora of Israel and Sinai. IV.Centaurea eriophora L. in Israel. Israel Journal of Botany 38 : 59–62. Zohary M. 1962. Plant life of Palestine. New York : Ronald Press.