American Journal of Botany 98(4): 698703. 2011.

A FIELD TEST OF INVERSE MODELING OF SEED DISPERSAL1

Jose M. Contreras Snchez2, David F. Greene3,4, and Mauricio Quesada2
2Centro

de Investigaciones en Ecosistemas, Universidad Nacional Autnoma de Mxico, Apartado Postal 27-3 (Xangari) 58089 Morelia, Michoacan, Mexico; and 3Department of Geography, Planning and Environment, 1455 de Maisonneuve Blvd. West, Montral, Qubec H3G 1M8 Canada

Premise of the study: Seed dispersal distancea key process in plant population dynamicsremains poorly understood because of the difculty of nding a source plant so well isolated from conspecics that seeds or seedlings can be unambiguously attributed to it. Inverse modeling (IM) of seed dispersal, a simple statistical technique for parameterizing dispersal kernels, has been widely used since 1992; surprisingly, however, this approach has never been veried in the eld. Methods: We released from 20 nearby trees the winged seeds of a liana species, Entada polystachya, near the coast in a tropical, dry forest in Jalisco, Mexico. Key results: With a two-parameter log-normal function, we found that IM predicted both the shape and scale parameters well as long as we used the entire data set. When, however, we subsampled (thus simulating the use of transects for seedlings or an array of seed traps), the estimates of the scale and shape parameters were often more than double the real values. The problem was due to the marked anisotropy (directional bias; in this case, in the direction of the diurnal sea breeze) of the individual dispersal curves. When we randomized the direction of dispersal of individual seeds from the trees (keeping dispersal distances unchanged), predictions of parameter values were excellent. Conclusions: Inverse modeling must include directional parameters when dealing with areas where strong anisotropy is to be expected, e.g., for wind dispersal of seeds near coasts or pollination by any vector where a plant species is limited to a strongly linear habitat such as river banks.

Key words: anemochory; anisotropy; inverse modeling; seed dispersal. Seed dispersal is crucial for understanding metapopulation persistence (Freckleton and Watkinson, 2002), the mobility of invasive species (Higgins et al., 2001), density-dependent losses at the recruitment stage (Nathan and Muller-Landau, 2000; Uriarte et al., 2005), and the maximum migrational velocity of a species attempting to track rapid climate change (Pitelka, 1997; Vellend et al., 2003). Nonetheless, the dispersal kernel (i.e., the probability distribution of seeds or seedlings as a function of distance from a maternal parent) of no plant species is empirically known beyond very short distances (Cain et al., 2000; Higgins et al., 2003; Vellend et al., 2003); indeed, for distances exceeding a few hundred meters, we know essentially nothing about dispersal. As argued by Greene and Calogeropoulos (2002), Greene et al. (2004), and others, our lack of knowledge about the shape and scale of dispersal is due completely to formidable methodological constraints. The inevitably contagious distribution of conspecic plants means that the seeds or seedlings one nds in a stand could be attributed to any number of potential mothers. There are two approaches available to us as we attempt to disentangle these overlapping dispersal curves. The rst, using genetic markers, is expensive and, especially where the markers for a species remain to be established, tedious (Jones et al., 2005). Further, if one hopes to understand dispersal out to at least some distance x from the area where recruits were sampled, then all potential mothers lying within the radius x must be tissue-sampled; in consequence, the distances examined, at least for mid-latitude examples, have tended to be quite short (e.g., Pairon et al., 2006). Thus far, examination of dispersal to distances as great as several hundred meters has been limited to tropical species precisely because the limited number of potential parents makes the approach more tractable (Jones et al., 2005; Hardesty et al., 2006). The alternative approach, pioneered by Ribbens et al. (1994), is inverse modeling (IM). It is far cheaper (both in money and time) than a genetic study (Greene and Calogeropoulos, 2002). Further, rather than measuring the Cartesian coordinates and size of potential mothers far from the recruit-sampling area, one could use a simulated set of maternal parents at some reasonable density at the larger distances (Clark et al., 1998; Canham and Uriarte, 2006); although, as stressed by Jones and Muller-Landau (2008), it is better to have at least a rough sense of the spatial variation of these outer source plants. While many published studies have now employed IM for seed dispersal (e.g., Clark et al., 1999; LePage et al., 2000; Stoyan and Wagner, 2001; Greene et al., 2004) or even leaf dispersal (Staelens et al., 2003; Jonard et al., 2006), there were no tests of the approach until Canham and Uriarte (2006) used simulations (rather than empirical data) with a log-normal kernel to test the capacity of IM to recover known kernel parameter values. Recently, there have been two eld tests using genetic data to test IM. The rst, by Pairon et al. (2006) with the tree Prunus serotina, was hampered by the fact that they did not have potential 698

Manuscript received 28 April 2010; revision accepted 20 December 2010.

The authors thank Gumersindo Snchez, Bonnie Hayden, Nancy Calderon, Luis Escalera, Victor Rosas, and Julia Astegiano for eld assistance. Financial support was provided by an NSERC Discovery grant and by grants from the Secretaria de Educacin Pblica (SEP) and Consejo Nacional de Ciencia y Tecnologa (CONACyT) (grants SEP-CONACYT 2005-CO1-51043 and 2005-CO1-50863) and the Direccin General de Asuntos del Personal Acadmico de la Universidad Nacional Autnoma de Mxico (grant IN221305). 4 Author for correspondence (e-mail: greene@alcor.concordia.ca), fax: 514-848-2032 doi:10.3732/ajb.1000152

American Journal of Botany 98(4): 698703, 2011; http://www.amjbot.org/ 2011 Botanical Society of America

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source plants (either real or simulated) outside the small area where the traps were located. They concluded that IM poorly expressed frugivorous dispersal by birds relative to the genetic results. The second genetic test, by Jones and Muller-Landau (2008) with the tropical wind-dispersed tree Jacaranda copaia, concluded that IM was robust so long as information on source trees outside the mapped area was included in the analysis. But there is another possible type of eld test for IM, one which has never been performed. One could articially release seeds from adjacent maternal plants. Thus, one would have overlapping dispersal curves but know exactly which seeds came from which plant because, unlike genetic analyses, there would be no potential error in assigning maternal parents, no sample size constraint, nor any problem with immigrant seeds derived from off-plot maternal parents. By attempting to emulate natural anemochorous abscission processes in relation to relative humidity and wind speed, this approach would be distinguished from a simulation because one could emulate the real natural variability in space for each single source as well as among the conspecic sources. Our main objective in this study then was to evaluate in the eld, using articial releases that imitate real abscission and dispersal processes, the capacity of IM to recover the underlying dispersal parameters when we have overlapping dispersal curves from multiple conspecic sources. MATERIALS AND METHODS
At Careyes (Jalisco, Mexico) in a deciduous forest in the dry season (March 2007), we articially released from trees using seeds of the liana species Entada polystachya. Although a few dried, curled leaves still remained on branches, the stand, occupying a broad hilltop 2 km from the Pacic Ocean, was essentially leaess. Lianas were common. As is typical of drought-deciduous, tropical forests, values of basal area per area (nearly 10 m2/ha) and canopy height (about 9 m) were low. Nonetheless, the total density of woody elements above the ground was quite large; this will enhance collisions by diaspores with woody elements and thus sharply reduce dispersal distances (Pounden et al., 2008). Indeed, dry season woody area index (WAI) is within the range reported for mid-latitude deciduous hardwood stands (with summed basal area per hectare two to three times greater than at Careyes) in the winter (Breda, 2003). Natural seed dispersal at this site is strongly directional with the great majority of seeds abscising during the period 1000 to 1600 hours when the sea breeze (i.e., a wind from the sea moving inland) is both strong and consistent (Greene et al., 2008). We chose to imitate that strong diurnal abscission bias by only releasing seeds from 1000 to 1600 hours each day. Over the course of 2 weeks, 100 seeds were released from a ladder midcrown in a set of 21 contiguous trees whose mean nearest neighbor distance was 3.5 m. The 100 seeds were released (and found) from each tree before we released from the next tree. The release height for each tree averaged 6.9 m, ca. 75% of the canopy height (Table 1). (This height was used because 75% is the typical mean value for the release height of mid-latitude tree diaspores according to Greene and Johnson (1996). Lianas of course would tend to release seeds near the top of the canopy.) As with real diaspores (Greene, 2005; Greene et al., 2008), seeds were never released unless there was at least some wind. Each seed was released by hand with a slight twist (as would be caused by a windinduced abscission) to hasten the entrance into autorotation We brightly spray-painted the woody diaspore of each seed to facilitate following its ight trajectory and then subsequently nding it in the dried leaf litter. Indeed, because of the high terminal velocity (1.71 ms1 for the painted seeds; about 15% greater than for unpainted seeds) and numerous collisions, distances were sufciently short that all 2100 seeds were found. We analyzed the eld data in ve successive steps. First, for each of the 21 trees separately, we assumed a log-normal distribution of deposition distances and calculated the median distance and the standard deviation of the logarithms of the distance traveled. Given that we never released seeds unless there was at least some horizontal wind, the log normal is the most likely two-parameter dispersal function (Greene et al., 2004). We also calculated these two parameters for the ensemble of 2100 distances. For subsequent comparison with IM results, in all cases, we rounded the real dispersal distance of a seed as the Cartesian

midpoint of an imaginary 1 m2 (i.e., 1 1 m2) seed trap. That is, the entire area within which seeds fell (roughly 40 35 m2) was viewed as a set of contiguous seed traps, and each seed within a trap was assigned to the trap midpoint. Second, we used the global optimization parameter estimation algorithm (as in Greene et al., 2004) to see whether IM could arrive at the observed parameter values for each tree. Seeds per trap were assumed to be Poisson-distributed as with Ribbens et al. (1994) and Greene et al. (2004). We set the fecundity parameter to a constant value as all trees produced 100 seeds in our eld exercise; that is, we need only solve for the two parameters of the log-normal dispersal function. The area examined was the area in which seeds dispersed but with an extra 5 m added to each compass direction. This parameter estimation program had no directionality parameter. Third, we accounted for a potential bias in directionality as follows. We randomly assigned negative or positive values to each Cartesian coordinate (x, y) for each set of 100 seeds. That is, distances from individual tree to trap were the same as originally observed, but the direction traveled was now, with respect to the source tree, randomized. We then repeated step 2, using the algorithm to solve for the two dispersal parameters. The fourth step in the analysis was to adopt the more typical eld method associated with IM for the analysis of both seeds and seedlings and to use only parallel transects (in effect, uniform subsampling) to evaluate the diaspore dispersal, i.e., unlike before, now we were dealing with all trees simultaneously and the maternal parent was (we pretend) not known. As shown in Fig. 1, there were 11 of these sampling designs, each of which is merely a different way of sampling the 1-m2 traps from the real eld site. Among the sampling designs, the number of 1-m-wide transects varied from 4 to 31; in all cases, except sampling design 2, the transects were oriented parallel to the abscissa. The nal step was to account for the potential bias in directionality as we examined dispersal from all trees simultaneously. We did this by repeating step 4 but rst randomly assigning negative or positive values to each Cartesian coordinate (x, y) for each set of 100 seeds (as in step 3). That is, distances from an individual tree to a trap were the same as originally observed, but the direction traveled was now, with respect to the source tree, randomized. The parameter estimation program was then used on the resulting 2100 seed ensemble using the same 11 sampling designs as before.

RESULTS The location of traps (i.e., 1-m2 sections of the study area) containing at least one seed are shown in Fig. 3, along with the location of the 21 trees. Given the large terminal velocity, the numerous collisions [almost ve collisions per seed: Pounden et al. (2008)], and the short stature of the trees, the median distances traveled from each tree were not great, ranging as only 2.2 to 4.9 m. No seed traveled more than 17 m (Fig. 2). The right-skewed dispersal results (all seeds) are shown in Fig. 2 (N = 2100). The estimated median dispersal distance and standard deviation for the log normal were 3.3 and 0.46 m, respectively (Table 1). The seeds dispersed primarily in the prevailing direction of the sea breeze (for this hilltop, roughly from the lower left corner toward the upper right corner in Fig. 3). The mean angle of dispersal for these 21 sets of 100 seeds varied only from 18.3 to 91.6 (Table 1), while the angular standard deviations varied narrowly from 15.8 to 36.3. Lumping all 2100 seeds (and thus 2 weeks of releases), the relative amount of angular dispersion remained remarkably small; the mean angle was 58 with a standard deviation of 33. The log normal was a reasonable approximation for these 21 data sets with a signicant Pearson correlation between observed and predicted seed numbers per distance category in every case (P < 0.001; N = 10 distance categories in all 21 cases; Table 1). Not surprisingly, given the strong anisotropy of the dispersal curves, randomizing the azimuths of the seeds around each maternal parent resulted in signicantly higher likelihoods for individual trees (2 test; p < 0.000001 in all cases; df = 1). The improvement in the likelihood ranged from 7 to 34% with

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Fig. 1. The 11 transect arrays superimposed on the eld site. Open circles represent the 21 source trees.

this elimination of the azimuthal bias. Lumping all seeds, the IM estimate of the median distance traveled (2.9 m) was within 12% of the real value (3.3 m). Similarly, for the standard deviation of the logarithms of the distances traveled, the IM estimate (0.48) was within 6% of the observed value (0.46). Nonetheless, given the large sample size, the IM expectation for the standard deviation was outside of the 95% condence interval from the earlier data set where all seeds were included (Table 1; one-sample t test, t = 9.06; N = 2100; P < 0.000001). What happens when we use parallel transects instead of the entire sampled area (Fig. 1)? While the IM t to the observed data for all of the 11 sampling designs was signicant (Pearson correlation; Table 1) likelihood ratios; P < 0.05)), the estimated median distances for seed dispersal (Table 2) were far more variable than what we had estimated previously using the entire seed data set. The ratio of the estimated median distance for transects to the estimate based on the entire area (3.3 m) varied as 0.9 to 2.2. For the standard deviations, the ratio of the values from the transects relative to our earlier estimate for the entire area (0.46) varied even more: as 0.3 to 3.4 (Table 2). The ve sampling designs where all trees were included (sampling design 6 through 9 and 11) within the sampled area, had ve of the six best estimates of the true median, and ve of the six best estimates of the true standard deviation. This inaccuracy as we switched to transects was clearly due to the anisotropy of the dispersal. Removing the anisotropy (i.e., randomizing the directionsbut not distancesof travel for the seeds around each tree), resulted in ratios of program estimate to

overall estimate that were far more muted: 0.9 to 1.2 for the median distance and 0.8 to 1.0 for the standard deviation (Table 2). Not surprisingly, the r2 for the observed vs. predicted seed frequencies of the randomized data (averaging 0.32) in the transects was much higher than for the anisotropic data (average = 0.10). DISCUSSION While the dispersal distances seem short relative to the empirical records of wind-dispersed tree species (cf. Greene and Calogeropoulos, 2002), this is primarily because of the short height of the trees in this seasonally dry, tropical forest. The median

Fig. 2. The observed distribution of distances traveled (all diaspores lumped: N = 2100).

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Table 1.

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Results from the eld site. All data are in meters except for angles which are in degrees. Note that the angular data are based on the coordinate system used in Fig. 1; i.e., an angle of 90 indicates the abscissa to the right of the origin. To switch these angles to compass directions, one must subtract about 40from each angle; then, for example, 90 would indicate a (wind) direction from west to east. Also shown are the likelihood and the estimated median distance (m) from the parameter estimation program with and without randomization of the azimuths of the seeds around each of the 21 trees. For the correlations (with P in parentheses) of predicted (log normal) and observed frequencies, N = 10 distance categories.
Tree height (m) 9 (7) 10 (6.8) 8.5 (6.8) 9 (7.5) 8.3 (6.8) 9.3 (7.4) 9 (6.7) 9.5 (7.2) 9.2 (6.8) 9.5 (7.1) 8.2 (6.7) 8.5 (6.3 9.2 (7.1) 9 (6.8) 9.2 (6.7) 11.5 (6.8) 7.5(6.8) 11.5(6.9) 10.8(7.3) 7.5(6.8) 9.2(6.8) 9.2(6.9) Median 2.9 3.8 3.9 2.8 2.2 3 2.7 4.9 3.8 4.5 2.9 2.4 2.3 3.5 3.4 4.1 4.2 3.3 3.2 2.9 3.3 3.3 SD 0.6 0.3 0.4 0.5 0.4 0.3 0.5 0.3 0.3 0.3 0.4 0.5 0.5 0.3 0.4 0.5 0.3 0.5 0.4 0.5 0.3 0.5 Mean angle 75.4 74.7 45.6 91.6 71 53.6 77.7 35.1 40.8 28.8 27.5 60.6 48.4 81.6 89 56.7 31.3 18.3 51.1 85.5 62.4 57.8 Angular SD 27.5 15.8 28.2 25.5 30.5 29.3 31.8 23.1 22.7 20.6 32.2 24.7 33.2 20.2 20.3 36.3 19.1 33.8 29.4 24.7 18.1 33.4 L (actual) 194 250 212 197 138 182 193 243 190 234 186 171 154 213 218 240 240 200 194 218 202 L (random) 167 200 160 162 100 120 160 200 146 188 124 125 111 167 172 192 176 176 149 178 140 r2 (P) 0.89 (0.00004) 0.88 (0.00006) 0.94 (<0.00001) 0.87 (0.00008) 0.95 (<0.00001) 0.88 (0.00006) 0.84 (0.00019) 0.91 (0.00002) 0.96 (0.00002) 0.92 (0.00001) 0.90 (0.00003) 0.86 (0.00011) 0.89 (0.00004) 0.91 (0.00002) 0.88 (0.00006) 0.89 (0.00004) 0.91 (0.00002) 0.89 (0.00004) 0.85 (0.00015) 0.82 (0.00031) 0.91 (0.00002) Program: Median (randomized) 2.2 3.4 3.5 2.3 1.9 2.6 2.2 4.4 3.4 4.1 2.6 1.9 2 3.1 3 3.5 3.7 2.8 2.7 2.3 3 2.8 Program: Median (not randomized) 2.3 3.4 3.5 2.3 1.9 2.6 2.3 4.4 3.6 4.1 2.6 1.9 2 3.2 3 3.5 3.7 2.8 2.7 2.3 3 2.9

Tree 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 All trees

distance traveled was ca. 50% of our release height; for mid-latitude forests (say, 30 m tall with a mean release height at 75% of the total height), this would scale up to a median dispersal distance of 11 m. In addition, the terminal velocity of this liana species (even without the paint) is very high relative to mid-latitude (Greene and Johnson, 1993) or other tropical (Augspurger, 1986) anemochorous species.

This represents the rst eld test of inverse modeling for recruitment function parameterization where we know the maternal parent without error. Using the log-normal dispersal function and the full data set, IM performed admirably with strongly anisotropic data; estimates of the median and standard deviation for the seeds were good either for individual trees

Fig. 3. The imaginary 1-m2 traps that contained one or more seeds are shown as light gray dots. The Cartesian grid is in meters. Note that the prevailing seed breeze (from the west) in the early afternoon would be roughly from the lower left corner toward the upper right corner of the graph. The 21 source trees are depicted with large black circles.

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Table 2.

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Results using transects for the median distance (m) and standard deviation of the logarithms of the distances traveled, for both the actual and the randomized azimuths. The ratio of the algorithm value to the observed value (bottom row, where we used all possible 1-m2 quadrats) is shown in parentheses. The sampling designs are as in Fig. 1. For the isotropic (randomized) designs, all P-values for the correlation (N = number of 1-m2 quadrats in the nal column) of observed vs. predicted seed densities were <0.00001.
Median (m) Standard deviation (m) IM Anisotropy 0.4 (0.9) 0.1 (0.3) 1.0 (2.2) 1.6 (3.4) 1.1 (2.4) 0.6 (1.3) 0.6 (1.4) 0.6 (1.3) 0.4 (0.8) 1.1 (2.3) 0.6 (1.3) 0.46 IM Isotropy 0.3 (0.7) 0.5 (1.1) 0.5 (1.1) 0.5 (1.1) 0.5 (1.0) 0.5 (1.1) 0.5 (1.1) 0.5 (1.0) 0.4 (0.8) 0.5 (1.1) 0.5 (1.1) r2 IM Anisotropy (P) 0.1041 (0.00099) 0.1525 (0.00006) 0.0564 (0.00132) 0.0351 (0.00247) 0.0425 (0.00012) 0.1247 (<0.00001) 0.1021 (<0.00001) 0.1021 (<0.00001) 0.0715 (0.00038) 0.0384 (0.00006) 0.1121 (<0.00001) 0.2323 IM Isotropy 0.4502 0.3291 0.2818 0.26 0.2776 0.3657 0.3535 0.3484 0.3445 0.2712 0.3514 Transect number 5 5 9 13 17 16 15 23 9 21 31 Total sampled area m2 (% of area examined) 101 (22.9) 100 (22.7) 181 (41.0) 260 (59.0) 343 (77.8) 328 (50.4) 302 (49.6) 465 (76.6) 179 (29.4) 424 (96.1) 631 (96.9)

Design 1 2 3 4 5 6 7 8 9 10 11 All trees (Table 1)

IM Anisotropy 3.7 (1.1) 7.3 (2.2) 4.3 (1.3) 6.7 (2.0) 5.6 (1.7) 3.1 (0.9) 3.4 (1.0) 3.3 (1.0) 4.4 (1.4) 5.9 (1.8) 3.2 (1.0) 3.26

IM Isotropy 3.5(1.1) 3.2(1.0) 2.9(0.9) 2.9(0.9) 3.0(0.9) 2.7(0.8) 2.9(0.9) 2.7(0.8) 3.9(1.2) 3.0(0.9) 2.8(0.9)

(N = 100 seeds) or for the entire population (N = 2100 seeds). Anisotropy merely led to low correlations. However, as we sampled the seeds with transects, estimates of the dispersal parameters were often quite poor and tended toward dramatic exaggeration of distances traveled. In the worst case, with both the median and standard deviation badly overestimated, the dispersal distance for the 99th percentile of the crop enlarged from the observed value of 9.5 to 253 m (Fig. 1: sampling design 4). Scaling up to tree (taller release height) species with diaspores possessing much lower terminal velocity, clearly one should worry about extrapolating long-distance dispersal events from a short-distance empirical record if strong anisotropy were suspected. The problem was clearly due to the directional bias because the IM parameter estimates were far closer to the real values when we reanalyzed the transect data using randomized (with respect to maternal parent tree) azimuths. The worst estimates of the median distance traveled were for those sampling designs where we did not sample part of the area that included source trees and/or sampled at a very low intensity (<190 1-m2 quadrats). The idea that accuracy with IM requires sampling well beyond the mapped potential source trees has already been broached by Clark et al. (1998), Canham and Uriarte (2006), and Jones and Muller-Landau (2008). The sensible point these authors made was that immigrant recruits from outside the area sampled for parents around the recruit plots/traps needed to be accounted for. In particular, using computer simulations and a lognormal function, Canham and Uriarte (2006) argued that the investigator employing IM needed to include source plants (mapped or simulated) at a distance at least one or two times the median dispersal distance. But here, we had no immigrants; and thus we conclude there is another reason to nest the sampled recruits within a larger area of potential sources: it increases the capacity of IM to recover the underlying dispersal function parameters when there is strong ansiotropy. While one can certainly include directionality parameters (mean and standard deviation of angles) in an IM model (for leaves: Staelens et al., 2003; Jonard et al., 2006; for seeds: Wagner et al., 2004; Canham and Uriarte, 2006), one wonders how frequently dispersal data as strongly anisotropic as that presented here will arise. As argued by Greene et al. (2008), the interaction of a local diurnal circulation (sea/land breezes along

coasts; valley/mountain winds in heavily dissected terrain) and xerochasty (bias toward low relative humidity in seed abscission) will lead to marked anisotropy of pollen or seed dispersal by wind because the great bulk of dispersal will occur in the period from roughly 1000 to 1600 hours. That is, the strong directionality exhibited by our articial midday releases was (purposefully) quite typical of real seed dispersal curves along a tropical coast (Greene et al., 2008). We note further that wind dispersal is hardly limited to midlatitudes; ca. 30% of the woody plants of the dry, tropical ora possess wind-dispersed seeds (Quesada et al., 2009). We recommend therefore that any investigator employing IM to quantify the dispersal of pollen, seeds, or leaves by the wind in a coastal or mountain environment should most certainly use a function with directionality parameters (mean and standard deviation of angles). When else might anisotropy be pronounced at the scale of say a few multiples of the median dispersal distance? Whenever there are linear arrays of conspecics one can expect strong anisotropy; and the most common case would be a species in a river valley where adult conspecics are conned to narrow contour bands because of, presumably, the interaction of moisture availability and relative competitiveness. The valley would need to be well dissected if the topographically determined band of conspecic adult abundance were narrow relative to dispersal capacity. This expected strong anisotropy would hold for the movement of both pollen reaching stigmas (say, fertilized ovules) and seeds reaching suitable seedbeds (i.e., established seedlings, not seeds) and would not be limited to those species whose pollen or seeds were moved by wind. By contrast, in most other environments, where conspecic density will not greatly vary by direction, any bias in directionality for anemochorous or anemophilous dispersal of pollen and seeds (or leaves) by the wind is expected to be more modest because the prevailing azimuth is independent of time of day. Thus, one may well detect an azimuthal bias, but the effect will be primarily on the strength of the likelihood rather than the accuracy of the parameter estimates (Staelens et al., 2003; Wagner et al., 2004; Canham and Uriarte, 2006; Jonard et al., 2006). We conclude that IM is remarkably robust as a parameter estimation approach even where strong anisotropy exists if the locale terrain is exhaustively sampled for seeds, pollen, seedlings,

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