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1 Department of Environmental Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Received for publication May 12, 1998. Accepted for publication May 20, 1999.
ABSTRACT
We examined the effects of wind speeds on pollen capture by megastrobili of jack pine (Pinus banksiana). We found that, when wind speed increased from 1.3 to 7.5 m/s, the relative capture efficiency (Er) did not change significantly (P 
0.206) and remained below 12%. However, total capture rates increased linearly with wind speed and atmospheric pollen density. Because theoretical models of capture efficiency predict the Er to increase to ~80% asymptotically, our findings suggest that receptive megastrobili are equally adept at capturing pollen at all naturally occurring wind speeds.
Key Words: anemophily • jack pine • megastrobili • Pinaceae, Pinus banksiana; • pollen capture • pollination
Anemophily is thought to be a risky means of pollination (Whitehead, 1983
) preventing many ovules from becoming seeds (Fenner, 1985
). Anemophilous plants increase the chances of reproductive success by producing vast amounts of pollen with aerodynamic characteristics such as air sacs and low settling velocities (Whitehead, 1983
; Di-Giovanni, Kevan, and Nasr, 1995
). The ratio of the number of pollen grains to ovules produced is often three or more times greater for wind- pollinated plants than for insect-pollinated plants (Niklas, 1985
). Wind-pollinated plants such as grasses and conifers usually grow together as clones (unusual in conifers), clumps, or as monospecific stands, which increase the source strength of pollen. A few conifers are clonal, but most tend to grow in monospecific stands. This increases the efficacy of pollen dispersal and capture by having pollen near the receptive megastrobili. Further, the reproductive organs are usually situated at the ends of the branches or stems of the crown. This increases exposure to pollen flow and also reduces the filtration of pollen by vegetation (Di-Giovanni and Kevan, 1991
).
For conifers it has been shown that the shape of scale bracts in open, receptive megastrobili creates small eddies that cause pollen of the same species to be preferentially captured by the micropylar arms (Niklas and Paw U, 1983
; Niklas, 1984
). Erickson and Buchmann (1983)
noted that electrostatic attraction between receptive megastrobili and pollen grains is an added force. Further, but at the population level, synchronicity between pollen release and megastrobilus receptivity is strong (Whitehead, 1983
; Di-Giovanni, Kevan, and Caron, 1996
). However, synchronicity does not necessarily occur within a single tree in which asynchronicity increases outbreeding. The biggest factor in successful transfer of pollen between anemophilous plants has been suggested to be wind speed (Whitehead, 1983
).
Wind speed influences the numbers of particles captured by artificial objects in wind tunnels. Theoretical and experimental studies (Chamberlain, 1975
) have shown that when spheres (or objects of other shapes) are exposed to a stream of airborne pollen, the amount of pollen captured depends mainly on two factors: wind speed and the sizes of the pollen grains (Gregory, 1973
). The higher the wind speed the more inertia the pollen grain has so that, as the wind is deflected by the sphere, the pollen grain continues on a straighter course and collides with the sphere. Generally, the larger the pollen grain is, the heavier it is and the more inertia it has (somewhat contrary to generalizations about anemophilous pollen), and the less likely it is to deviate from its initial path. Thus heavier pollen is more likely to impact a receptive megastrobilus (Whitehead, 1983
). Also, around smaller objects, wind streamlines deviate more markedly so that a carried pollen grain would have to be deflected more from the air streamline to miss collision. Thus, at given wind speeds and pollen sizes, pollen is more likely to collide with a unit area of smaller obstacles than of larger ones. Larger objects may have increased capture efficiency by subdivisions of their surfaces (Whitehead, 1983
) to increase area but not diameter (e.g., the micropylar arms on strobili).
Capture efficiency, E(%), is defined as the number of particles impacted upon a surface divided by the number of particles passing through the same area projected horizontally (Di-Giovanni, 1989
) and varies between 0 and 100%. Pollen capture is the impaction and retention of pollen landing on a projecting surface. Thus, for a given pollen type, an increase in wind speed should increase the capture efficiency of receptive megastrobili (Chamberlain, 1975
). There are also other factors that influence capture efficiency, such as rebound and stickiness of pollen and obstacle surfaces. Rebounded particles are those that are not retained after bouncing from a surface (Chamberlain, 1975
). Stickiness of an obstacle's surface greatly diminishes blow-off (Gregory, 1973
) or rebound, and therefore increases capture efficiency. Scales on receptive megastrobili are often moist, and micropylar arms are sticky. Receptive megastrobili of conifers also secrete sticky pollination drops (Ho, 1991
).
Despite theory and models, it is not known how capture efficiency in receptive megastrobili of conifers is affected by wind speed even though positive correlation would be expected from the above discussion. Because of the complex surface of receptive megastrobili, the exact relationship between wind speed and capture efficiency by the micropylar arms is probably different from that for smooth spheres. Although the megastrobilus seems to have evolved to favor impaction by conspecific pollen (Niklas, 1983
), there are no data linking wind speed to the amount of pollen deposited on the micropylar arms. Our aim was to test the null hypothesis (H0) that wind speed does not affect pollen capture efficiency on the stigmatic area of megastrobili of jack pine (Pinus banksiana, Lamb.) and to explore the idea that the cones have evolved with mechanisms, or structures, or both, to be equally accessible to pollen grains at any and all usual wind speeds. The alternative hypothesis tested by linear regression is the expected one that efficiency increases with increasing wind speed (H1).
MATERIALS AND METHODS
To test the hypotheses, we used fresh receptive megastrobili placed at the exit of a contraction cone (Sage Action, Inc., P.O. Box 416, Ithaca, New York 14850) inserted at the end of a wind tunnel borrowed from K. Niklas (Cornell University) from which measured amounts of pollen were blown at variable wind speeds (Fig. 1).
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) (Fig. 2).
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Each receptive megastrobilus was placed at the wind tunnel's exit on another plasticine stub and was exposed to a stream of jack pine pollen supplied from the wind tunnel. Dimensions of the wind tunnel extraction cone were 15 by 15 cm. The wind tunnel motor was adjusted for each exposure to provide various wind speeds from 1.3 to 7.5 m/s, chosen as typical of those to which megastrobili are exposed in nature. Wind speed was measured with a DVA 6000 T vane anemometer (Airflow Developments Limited, Missisauga, Ontario, Canada).
During exposure, a rotating Rotorod® pollen sampler head (taken from a model 92 Rotorod®, Sampling Technologies, Minnetonka, Minnesota, USA) powered by a 12- V motor, was placed 10 cm downwind of the receptive megastrobilus to sample the aerial concentration of the pollen cloud emanating from the tunnel (Fig. 3). This distance was thought to be the minimum distance from the receptive megastrobilus to ensure that the Rotorod® did not have an effect on the receptive megastrobilus' aerodynamics because of turbulence induced by the Rotorod®'s spinning arm (see Fig. 2 in McCartney, Filt, and Schmechel, 1997
). The megastrobili also did not have an effect on the rotorod because all megastrobili diameters were <1 cm (
= 3.62 mm), and so the downwind effect was <10 cm. The rate of rotation was checked stroboscopically (Strobatec type 1531-AB, Radio Company, Concord, Massachusetts, USA). Attached to the rotating arms were perpendicular I-rods made sticky with a 50 : 50 mixture of silicone gel and hexane. These I-rods were the sampling surface of the Rotorod® instrument.
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Each megastrobili was exposed to a given wind speed. Wind speeds used were 1.3, 1.9, 2.25, 3.0, 4.0, 5.5, 6.0, 7.0, and 7.5 m/s. At each sample the wind speed was tested with the anemometer to insure accurate measurements.
Each receptive megastrobilus was exposed for 2 min of continuous pollen release (timed by stop-watch).This period of time was thought to be sufficiently long to accommodate expected small-scale turbulent anomalies and short enough to avoid overloading the cone surfaces. Pollen release from the wind tunnel, Rotorod® operation, and exposure of a receptive megastrobilus were all started simultaneously to minimize possible atmospheric contamination within the experimentation room. Error in time measurement was approximately ± 2 s and was insignificant).
After exposure, each megastrobilus was gently returned to the petri dish so that pollen grains would not fall from the cone. The megastrobilus was brought to a stereo microscope where the micropylar arms were examined at 40x magnification. The cones were dissected scale by scale and the pollen grains deposited on all the upwind micropylar arms were counted. Only the upwind side was used to measure the Relative Efficiency (ER) in order to avoid double counting any pollen grain. By cutting the megastrobilus in half we were able to determine that in most cases the pollen counts were zero or insignificant on the downwind side. Pollen grains in clumps were ignored because of difficulties in determining the actual number of pollen in the clumps. In any case, the aerodynamics of clumped pollen are different from those of single grains (Di-Giovanni and Kevan, 1994
), and, in this and related field experiments (Roussy, unpublished data), very few clumps were found. The petri dishes were also scanned for fallen and contaminant pollen grains, but none were found.
The upwind surface area of each megastrobilus was determined by measuring its length and width. These values were used to calculate average dimensions, which were used to estimate the surface area of an equivalent hemisphere for each receptive megastrobilus. Area was calculated as follows by using the length and width to create an average diameter for each individual megastrobili. We then used this average diameter in the formula for the surface of a sphere: 
d2. We used the total upwind surface area of the receptive megastrobilus as an easily measured estimator for the upwind surface area of the micropylar arms. Therefore, we are assuming, for the purposes of this study, that the area of the micropylar arms is proportional to the total upwind surface area of the receptive megastrobilus and, therefore, that our efficiency measurements are relative measures, denoted ER.
Rotorod® analysis followed standard procedure (Sampling Technologies, 1989
; Banks and Di-Giovanni, 1993
). The two I-rods on the Rotorod arms were placed on an I-rod holder with the sticky, exposed side up, and then placed and examined under a microscope. Pollen grains were counted on both I-rods. The airborne concentration was then calculated as follows: concentration (no./m3) = total pollen on both rods (no.)/total volume of air sampled (m3) by both rods. Multiple (minimum 6) exposures were made at the various wind speeds between 1.3 and 7.5 m/s.
We estimated relative capture efficiency by measuring the ratio of the amount of pollen intercepted by the micropylar arms on the receptive megastrobili to the amount of pollen passing through the area had the receptive megastrobilus not been there, as follows
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RESULTS
Our data showed that the average diameter for jack pine megastrobili was 3.623 mm and the average surface area for the megastrobili was 41.227 mm for a sample size of 42. Although we found, as expected, a positive correlation between pollen fluxes of 164 000 to 160 000 000 grains and pollen capture by receptive megastrobili (r2 = 0.63; P 0.0001) (Fig. 4), there proved to be no significant relation between wind speed and pollen capture efficiency by the micropylar arms (P 0.206). The relative efficiencies of jack pine micropylar arms were low and varied from 0.72 to 12% (Fig. 5). Over the same range of wind speeds and particle and object size, theory predicts efficiency should rise to ~80% as calculated by Aylor's (1982)
empirical formulation:
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measurements for a cylinder or ribbon (Fig. 4).
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Gregory (1961)
and Chamberlain (1975)
showed that small, light airborne particles slowly approaching a sphere are deflected around it by the streamlines of air flow because of their lack of inertia. At higher speeds, such particles have higher inertia and thus continue towards the object, crossing the boundary layer, and impacting the sphere. It has been shown, in previous studies (Gregory, 1973
; Chamberlain, 1975
), that increasing wind speeds also increases capture efficiency for smooth spheres and other objects (Fig. 5). Meanwhile, in our study we found no significant relationship between wind speed and capture efficiency of jack pine pollen by the micropylar arms on receptive megastrobili of jack pine (Fig. 5).
The spread of the data points at each wind speed was quite wide, probably caused by randomness of the experimental pollen cloud, small errors in pollen counts on micropylar arms, concentration estimates, wind speed measurements, and in measuring the size of receptive megastrobilus. We did not count pollen impacted onto the scales and other parts of the cone because such pollen is lost to reproduction and potential seed set and restricted our attention to the micropylar arms. Nevertheless, we would expect, by theory, increasing efficiency with wind speed, but our results did not follow the same pattern as theoretical predictions. The results of our experiments indicate that the belief that receptive megastrobili follow the pattern described by Gregory (1961)
and Chamberlain (1975)
is not true in this case.
The difference (Fig. 5) between pollen capture efficiency of receptive megastrobili vs. that of smooth spheres (Aylor, 1982
) presumably reflects the effects of the particular surface shape of the megastrobili. Because the receptive megastrobili have scales with both the outer and inner sides exposed, the overall surface area is greater than a comparable sphere with the same diameter. The shape modifies wind flow patterns (Niklas, 1984
), and our results indicate that at all natural and usual wind speeds the strobili are equally efficient at pollen capture. The shapes of megastrobili may have evolved so that reproductive fitness is equally good in varying and various environments. Our results support Niklas' (personal communication, 1994) idea that receptive cones take an active part in individual reproductive fitness by preferentially entrapping pollen over a range of naturally occurring wind speeds.
The capture efficiency for jack pine megastrobili to pollen is rather low so we would like to speculate that jack pine megastrobili may have taken the route of the turtle in that slow and steady wins the race. Another explanation could be that rebound and reentrainment have a significant effect on pollen capture by megastobili. Paw U and Braaten (1992)
showed that at higher wind speeds there are more particles that bounce and therefore become unavailable for reentrainment, thus in fact lowering capture efficiency at these higher wind speeds.
In another experiment Paw U (1983)
demonstrated that it was the particle type, in this case pollen, that was significant in rebound speed and not the surface type. This may indicate that the stickiness of the micropylar arms does not significantly affect the rebound rate of the pollen grains. Future work should be done concentrating at the lower wind speeds.
Recent work by Sorensen and Webber (1997)
has shown that seed set rises to an asymptote of maximum values at relatively low values of airborne pollen concentration. Physical or physiological mechanisms that explain this finding were not discussed by Sorensen and Webber (1997)
. However, we suggest that our results do explain this finding. If the shape of the megastrobili has evolved so that pollen capture efficiency is equally good at all wind speeds, then one would see a minimum increase, if any, of pollen deposition.
Our overall low efficiency could also have been caused by the pollen grain themselves. We used pollen that had been frozen from the previous year. At a scale that we could not detect, the pollen might have been altered by freezing, i.e., shrinkage.
This result also has implications in the field of pollen contamination research for forestry tree improvement (Di-Giovanni and Kevan, 1991
). Much work in pollen contamination research is based on the use of sticky microscope slides, exposed in the seed orchard, to indicate the amount of, or potential for, contaminant (nonselected) pollen entering a seed orchard (e.g., Greenwood and Rucker, 1985
). The implicit assumption used is that these slides capture pollen in the same manner that megastrobili do and therefore represent the amount of contaminant pollen that would be captured by megastrobili. However, it is well known that the capture efficiency of sticky for airborne biological particles varies markedly with wind speed (Gregory, 1973
). Our study indicates no appreciable variation in efficiency with wind speed, and therefore, the two sampling surfaces cannot capture pollen with the same efficiency. Therefore, sticky slides do not mimic the capturing ability of megastrobili.
Although our hypotheses were tested on only one species, only through similar research on more species can the phenomena we describe be shown to be generally applicable and used to describe the evolution of anemophilous megastrobilus structures and interaction with wind.
FOOTNOTES
1 The authors thank K. Niklas of Cornell University, Ithaca, New York, USA, for supplying the wind tunnel. Support for this research was granted by the Ontario Ministry of Natural Resources, grant OMNR-ORRRG (010-91), grant from NSERC/Forestry Canada Research Partnerships (696-006/91), NSERC Operating Grant (A8098, awarded to Kevan) and Environment Canada. 
2 Current address: R.R. #1, Shelburne, Ontario L0N 1S5, Canada.
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Ho, R. H. 1991 A guide to pollen- and seed-cone morphology of black spruce, white spruce, jack pine and eastern white pine for controlled pollination. Ministry of Natural Resources, Ontario Forest Research Institute.
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) and predicted efficiency (•) using data on cone sizes and calculations based on Aylor's (1982)