Seed Size and Dispersal Potential of Acer rubrum (Aceraceae) Samaras Produced by Populationsin Early and Late Successional EnvironmentsAuthor(s): Patricia A. PeroniSource: American Journal of Botany, Vol. 81, No. 11 (Nov., 1994), pp. 1428-1434Published by: Botanical Society of AmericaStable URL: http://www.jstor.org/stable/2445316Accessed: 28/09/2010 19:41

Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available athttp://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unlessyou have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and youmay use content in the JSTOR archive only for your personal, non-commercial use.

Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained athttp://www.jstor.org/action/showPublisher?publisherCode=botsam.

Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printedpage of such transmission.

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact support@jstor.org.

Botanical Society of America is collaborating with JSTOR to digitize, preserve and extend access to AmericanJournal of Botany.

http://www.jstor.org

American Journal of Botany 81(11): 1428-1434. 1994.

SEED SIZE AND DISPERSAL POTENTIAL OF ACER RUBRUM (ACERACEAE) SAMARAS PRODUCED BY

POPULATIONS IN EARLY AND LATE SUCCESSIONAL ENVIRONMENTS1

PATRICIA A. PERONI2

Department of Botany, Duke University, Durham, North Carolina 27006

In order to determine if red maple dispersal potential or seed size change during secondary succession, samaras were collected from five populations located in early successional environments and five populations located in late successional environments. Wing loading ratios (samara mass-mg/samara area-cm2), which are inversely proportional to dispersal ability, were computed for all samaras, and seeds were excised from each samara and weighed. Samaras from the early successional red maples showed slightly but significantly lower wing loading ratios than those from the late successional environments. This result corresponds with the conclusions reached by several theoretical investigations of seed dispersal evolution that predict that recently founded populations will show greater dispersal abilities than more established populations. The earlier successional populations had slightly heavier seeds than the later successional populations, which suggests that the changes in community composition and dynamics that occur during this successional sequence do not select for heavier seeds in older red maple populations. Coefficients of variation for wing loading and seed size showed no consistent trends with successional stage, which indicates that variation in these characters does not decrease as succession proceeds.

Seed size and the dispersal structures of plant propa- gules can influence the ability of plant populations to colonize new habitats and to persist at these sites. As succession proceeds at a site, selection on propagule char- acters may change in ways that can result in the evolution of these traits. Although several theoretical treatments offer predictions regarding the potential evolutionary ef- fects of successional changes on dispersal structures of fruits (Van Valen, 1971; Levin, Cohen, and Hastings, 1984; Olivieri and Gouyon, 1985), Olivieri and Gouyon's (1985) analysis of propagule polymorphisms in two het- erocarpic species of Carduus represents the only published investigation that compares dispersal potential across a successional sequence. Several investigators have studied variation in seed size of herbaceous species in successional habitats (Reinartz, 1984; Aarssen and Turkington, 1985; Hartnett, Hartnett, and Bazzaz, 1987), but similar studies on woody plant species are lacking.

The current study represents part of a larger investi- gation into genetic change and persistence of red maple (Acer rubrum L.) during old field succession in North Carolina piedmont forests. The winged fruits of red maple colonize fields soon after abandonment, and these pop- ulations persist throughout the remainder of the succes- sional sequence. The unit of dispersal is a samara (a single seed attached to a wing), and the mass, area, and shape of these samaras vary greatly within populations (Town- send, 1972).

In this study, I compared samaras produced by early

1 Manuscript received 6 July 1993; revision accepted 16 May 1994. The author thanks J. Antonovics, N. L. Christensen, R. K. Peet, and

S. Mazer for comments on initial drafts of this manuscript. Support for this study was provided by a Sigma Xi Grant-in-Aid of Research and a Sigma Delta Epsilon Graduate Women in Science Grant-in-Aid.

2 Current address: Department of Biology, Davidson College, David- son, NC 28036.

and late successional red maple populations in order to evaluate the following questions:

1) Do samaras produced by red maple populations in early and late successional environments differ in dis- persal potential? Hypotheses based on the theoretical work of Van Valen (1971), Levin, Cohen, and Hastings (1984), and Olivieri and Gouyon (1985) predict that propagules produced by populations in early successional habitats will show greater dispersal potential than those produced by populations at older sites, and that the magnitude of the difference in dispersal potential observed between ear- ly and late successional populations will be greatest in those landscapes where the rate at which new sites become available for colonization and the probability of extinc- tion for established populations are both moderate.

2) Does the size of seeds produced by red maple pop- ulations vary with the successional maturity of a popu- lation's habitat? Several investigators have extended Abrahamson and Gadgil's (1973) hypotheses regarding life history differences among successional species to life history evolution within species that inhabit successional environments (for a review see Gray, 1987). In the case of seed size, these models predict that phenotypes that produce small seeds will dominate colonizing popula- tions, while populations in more mature habitats will be dominated by phenotypes that produce heavier seeds.

MATERIALS AND METHODS

Old field succession in piedmont forests-In the North Carolina piedmont, widespread abandonment of agri- cultural land during the late nineteenth and early twentieth centuries initiated secondary forest succession across much of the region. Herbs and grasses dominate fields in the years immediately following the cessation of cultivation (Keever, 1950), but within 3-5 yr after abandonment, pines (primarily Pinus taeda) begin to overtop and shade

1428

November 1994] PERONI-CHANGES IN DISPERSAL OF RED MAPLE DURING SUCCESSION 1429

this grassy/herbaceous cover. A pine forest with a hard- wood understory develops and eventually forms a closed canopy. As these forests reach 80-100 yr of age, the pines begin to senesce (Peet and Christensen, 1987). Since pine seedlings show poor survival in the low light and high litter environments created by their parents, hardwood species gradually replace the pines. Within 200-300 yr after abandonment, this transition is complete, and a hardwood forest dominated by various oak (Quercus) and hickory (Carya) species occupies the former field. These hardwood forests are relatively stable and self-perpetu- ating, and Oosting (1942) designated them the climax community for the piedmont old field successional se- quence. Oosting (1942) and Peet and Christensen (1987) provide detailed descriptions of old field succession in the North Carolina piedmont.

Red maple-General description -Under forest condi- tions red maple is classified as a short to medium-lived understory and subcanopy tree (Fowells, 1965). Although stem turnover may be relatively high (Peet and Christen- sen, 1979), genetic individuals may be extremely long- lived since red maple shows a great capacity to stump sprout (Wilson, 1968). Despite its prodigious sprouting abilities, red maples apparently do not survive cultivation since sprouts are absent from recently abandoned fields in the study area (personal observation).

Although wind dispersal of red maple samaras assures that many seeds reach recently abandoned old fields, most of these colonization events prove unsuccessful due to extremes of the physical environment and the action of seed predators and herbivores (DeSteven, 1991 a, b). The age structure of red maple in young pine stands located in the North Carolina piedmont indicates that the ma- jority of red maple in these forests established during a relatively discrete phase that occurred 9-15 yr after the sites were released from cultivation (Peroni, 1991). After this period of successful colonization and establishment, seedling densities of red maple remain low until the initial cohort of red maple reach reproductive maturity at 30- 40 yr of age (Peet and Christensen, 1987; personal ob- servation). Long-term data gathered from permanent plots indicate that red maples continue to recruit into the adult portions of populations throughout the remainder of the old field successional sequence in this region (Peet and Christensen, 1987).

Red maple-Dispersal biomechanics-The red maple fruit is a double samara, and the two samaras that form the fruit are united at their bases (i.e., seed end; Harlow et al., 1991). The pedicel attaches to the fruit at the apex of this union. As the fruit ripens, an abscission layer forms between the two samaras. Upon maturity, the samaras separate from each other and are released from the pedicel. The individual samara serves as the dispersal unit.

Upon release, a maple samara falls freely for a short distance, but then begins to rotate. The rotation of the samara wing produces lift, which slows its descent (Green, 1980). Eventually, the velocity of the falling samara reach- es the terminal velocity (Green, 1980). The dispersal po- tential of a samara is directly proportional to the height of release, and inversely proportional to its terminal ve- locity (Guries and Nordheim, 1984).

Research into the aerodynamics of winged fruits in- dicates that terminal velocity depends upon the relation- ship between the mass of the dispersal unit and the size of the wing (Green, 1980). Guries and Nordheim (1984) investigated the aerodynamic properties of red maple samaras and found that the square root of the wing loading ratio (mass of dispersal unit/area of the wing) explained 83% of the variation in terminal velocity for samaras released from a common height. Since the components of the wing loading ratio are relatively easy to measure, this ratio provides a means for comparison of the dispersal potential of different samaras.

Samara collection - Samaras were collected from five hardwood stands and five 50-60-yr pine stands located in the Durham and Korstian Divisions ofthe Duke Forest, Durham and Orange Counties, North Carolina. Stands with extreme aspects and novel soil types (e.g., diabase) were excluded as seed collection sites. Historical stand maps of the Duke Forest (Duke Forest Archives) were used to determine the minimum distance from the center of each of the 50-60-yr-old pine stand sites to the edge of the closest stand that could have served as a seed source for red maple at the time the field was abandoned.

The majority of fruiting red maple in the 50-60-yr pine stands established between 9 and 15 yr after abandon- ment, and, therefore, represent early successional indi- viduals. Since historical records (Duke Forest Archives) and tree ring data (N. L. Christensen, Duke University, unpublished data) indicate that the hardwood stands used in this study are very old (i.e., >400 yr), the majority of fruiting red maples in these populations are assumed to have established under later successional conditions, al- though a few extremely long-lived early successional in- vaders may have been able to persist at these sites via vegetative reproduction.

All sites covered areas of at least 1 ha, and all site boundaries were located at least 30 m away from trails, roads, or adjoining stands of different successional status. At each site, bulk samples of samaras were collected from 225 samara traps deployed on a 5-m grid. Each trap con- sisted of a plastic greenhouse flat (52 x 25.5 cm) and was secured to the forest floor with a 16 penny nail.

In 1990, red maple seed dispersal commenced in late March and samaras were collected from the traps at each site every 7-10 d during the dispersal period. The majority of the seeds collected from the seed traps were ripe. Upon return from the field, samaras from the various sites and censuses were placed into separate Zip-Loc bags and stored at 4 C. At the end of the dispersal period, the samara samples obtained from the various censuses at each site were pooled to obtain a single bulk sample for each site. Each bulk sample was placed in a Zip-Loc bag and stored at 4 C.

Dispersal potential and seed mass -Fifty samaras with filled ovules were selected at random from each popu- lation's bulk sample, with the exception of one of the 50- 60-yr pine stands from which only 31 samaras were se- lected. In order to uniquely identify each samara and to prevent desiccation, each samara was placed into a labeled microcentrifuge tube. The tubes were sealed, placed in a random array, and allowed to come to abient laboratory

1430 AMERICAN JOURNAL OF BOTANY [Vol. 81

temperature (20-22 C) prior to measurement of samara and seed characters.

Each samara was weighed to the nearest 0.1 mg, and its area was calculated to the nearest 0.01 cm2 by taking the mean of three passes through a leaf area meter. The seed was then removed from each samara and weighed to the nearest 0.1 mg.

Height of release and effects of tree size on samara mor- phology - The dispersal potential of a samara depends upon the height at which it is released as well as its aero- dynamic properties. In order to determine if mean height of fruiting red maples differed between early and late successional habitats, all the fruiting red maples at one early and one late successional seed source site were mapped and scored for fecundityjust prior to the initiation of seed dispersal. The height of each fruiting red maple that produced > 1,000 samaras was measured using a clinometer (N = 13-26 trees per site).

These data were pooled with height data obtained from two additional early successional stands and two addi- tional late successional populations. In 1988, as part of another, unpublished investigation, 1-ha plots were es- tablished in two 80-90-yr pine stands (earlier succes- sional) and two hardwood stands located in the Duke Forest. At each of these sites, all female red maple that produced > 1,000 samaras were cut at ground level to facilitate seed collection (N = 15-19 trees per site). The height of each tree was determined after cutting by mea- suring the distance from the base of the stem to the furthest branch tip.

In order to determine if samara morphology varies among trees within populations or with tree size, the areas of four samaras from each of the trees cut in the 1988 investigation described above were measured to the near- est 0.01 cm2 by taking the mean of three passes through a leaf area meter. At the time of collection, samaras on different trees were at varying stages of maturity, but the wings were fully formed. All trees were measured for diameter breast high (DBH) just prior to cutting.

In order to ascertain if samara morphology varies within trees as a function of height on the stem, samara samples were collected from the lowest fruiting branch off of the main trunk and the next highest branch (1 .1-2.5 m higher) for 7 red maples in the study region. Ten samaras from each branch on each tree were measured to the nearest 0.01 mm for samara length and maximum wing width using digital calipers.

Data analysis-Wing loading ratios were used as in- dicators of dispersal potential. A wing loading ratio was calculated for each samara by dividing its mass in mg by its area in cm2. The wing loading ratios were square root transformed and then subjected to ANOVA. Separate ANOVAs also were conducted for the samara mass, sa- mara area, seed mass, and tree height data. A regression analysis was performed to determine if mean wing loading ratios for the five early successional sites correlated with the distance from a suitable seed source at the time of abandonment.

In order to determine if early and late successional habitats showed significant differences in levels of vari- ation within populations, coefficients of variation (stan-

TABLE 1. Means (? standard deviation) for morphological characters of red maple samaras collected from populations in early and late successional environments. Wing loading = samara mass (mg)/ samara area (cm2). Sample size = 5 populations/successional stage and 50 seeds per population, with the exception of one early suc- cessional population where N = 31. For each samara character, means with different lowercase letters differ significantly between the two successional stages.

Successional Square root Samara Samara Seed stage wing loading area (cm2) mass (mg) mass (mg)

Early 3.91a 0.92a 13.92a 9.21a (0.10) (0.08) (1.16) (0.72)

Late 3.99b 0.88b 13.78a 9.05a (0.07) (0.04) (0.74) (0.46)

dard deviation as % of mean) were calculated for each samara character in each population following the ex- ample of Hartnett, Hartnett, and Bazzaz (1987). Separate ANOVAs were conducted using the coefficients of vari- ation for each character.

A nested ANOVA was performed in order to determine if samara area varied significantly among cut trees within the populations. Separate Pearson and Spearman corre- lations were performed for each population to determine if samara area varied as a linear function of either tree height or diameter. In addition, the data from the four populations were pooled and subjected to correlation analysis. The effect of branch height on samara mor- phology was analyzed using a paired sample t-test.

RESULTS

Samaras produced by late successional populations dis- played slightly higher wing loading ratios than samaras obtained from the early successional habitats (Table 1). This difference was significant when tested against the model mean square error, but the P value increased to 0. 16 5 8 when the population within successional stage mean square was used as the error term (Table 2). Wing loading ratios also varied significantly among populations within each successional stage (Tables 2, 3). The minimum dis- tance from the center of each of the early successional samara collection sites to the nearest seed source at the time of abandonment showed no correlation with the mean wing loading ratios obtained for each of these pop- ulations (r2 = 0.01693 1, P= 0.8348, N = 481 samaras).

Samaras from early successional populations had slight- ly larger wings than those from late successional popu- lations (Table 1). This difference was significant when tested against the model mean square error, but the P value rose to 0.275 12 when tested against the populations within successional stage mean square (Table 2). Early successional samaras also were slightly heavier and con- tained slightly larger seeds than the late successional prop- agules (Table 1), but these differences were not significant (Table 2). Samara mass, samara area, and seed mass all varied significantly among populations within each suc- cessional stage (Tables 2, 3).

The coefficient of variation data obtained from the early and late successional populations were similar for the wing loading as well as the other samara characters, and yielded no significant or consistent trends (Tables 4, 5).

Fruiting red maples measured in the late successional

November 1994] PERONI-CHANGES IN DISPERSAL OF RED MAPLE DURING SUCCESSION 1431

TABLE 2. Results of univariate ANOVAs on morphological characters of red maple samaras collected from populations in early and late successional environments. Wing loading = samara mass (mg)/samara area (cm2).

f (P)

Square root Samara Samara Seed Source df Error MS wing loading area mass mass

Successional stage 1 Model error 5.62 6.37 0.28 0.49 (0.0182) (0.0120) (0.5951) (0.4821)

Population w/in 2.32 1.37 0.05 0.14 stage (0.1658) (0.2751) (0.8231) (0.7141)

Population w/in 8 Model error 2.42 4.64 5.30 3.43 stage (0.0145) (0.0001) (0.0001) (0.0007)

Error 457

sites were slightly taller (mean = 16.9 m ? 3.2 m, N= 3 populations) than those measured in the early succes- sional sites (mean = 15.8 m ? 1.5 m, N = 3 populations). However, these differences were not significant (ANOVA, df= 1, 93, F= 2.32, P= 0.1312).

Samara area differed significantly among trees within populations (Table 6). However, none of the correlation analyses detected any significant linear relationship be- tween samara area and either tree height or diameter (only one P value was < 0.22), and correlation coefficients ranged from -0.34 to + 0.38. Samara samples obtained from the higher branches of trees showed slightly greater mean lengths than samples obtained from lower branches in four of the seven trees sampled. Mean samara width for samples from higher branches was slightly greater than mean widths from lower samples in five of the seven trees sampled. However, these differences were not significant (mean of length differences = 0.47 mm ? 1.34, t = 0.82, df = 6, P = 0.22; mean of width differences = 0.338 ? 0.726, t = 1.2339, df= 6, P = 0.13).

TABLE 3. Population means (? standard deviation) for morphological characters of red maple samaras. Populations GT4, GYD, KR5, K1 4, and PSP were located in early successional environments. The other populations were located in late successional environments. Wing loading = samara mass (mg)/samara area (cm2). Sample size = 50 samaras per population with the exception of population GT4 where N = 31.

Samara Square root Samara mass Seed mass

Population wing loading area (cm2) (mg) (mg)

GT4 3.89 0.90 13.11 8.86 (0.46) (0.30) (3.37) (2.50)

GYD 4.04 0.88 14.1 9.28 (0.32) (0.18) (2.58) (1.91)

KR5 3.97 0.88 13.74 9.14 (0.35) (0.16) (2.52) (1.81)

K14 3.79 0.91 12.87 8.41 (0.31) (0.19) (2.13) (1.44)

PSP 3.86 1.06 15.80 10.34 (0.31) (0.24) (3.95) (3.13)

BOR 4.04 0.91 14.75 9.77 (0.42) (0.20) (3.12) (2.43)

CIR 4.08 0.85 14.02 9.22 (0.33) (0.19) (2.79) (2.07)

D60 3.96 0.83 12.99 8.72 (0.42) (0.19) (3.35) (2.87)

K29 3.94 0.86 13.07 8.62 (0.36) (0.20) (2.48) (1.90)

K40 3.93 0.92 14.06 8.97 (0.41) (0.19) (2.39) (1.91)

DISCUSSION

Variation between successional stages-The wing load- ing results suggest that samaras produced by early suc- cessional red maple populations will show greater dis- persal potential than samaras produced in later successional sites. This trend agrees with the findings of theoretical investigations that predict that selection in colonizing populations will favor characters that enhance dispersal, but that selection against long-distance dispersal will operate within established populations (Van Valen, 1971; Levin, Cohen, and Hastings, 1984; Olivieri and Gouyon, 1985). The differences in dispersal potential de- tected for red maple in this study are much smaller than those documented by Olivieri and Gouyon (1985) for early and later successional populations of C. pycnoceph- alus and C. tenuiflorus. Red maple displays continuous variation in samara characters that influence dispersal potential, while propagules produced by the Carduus spe- cies fall into discrete dispersing and nondispersing classes. These contrasting patterns of variation may account in part for the more modest differentiation in dispersal po- tential observed between early and late successional red maple populations. However, the theoretical investiga- tions of both Van Valen (1971) and Olivieri and Gouyon (1985) predict that variation between early and late suc- cessional population means for dispersal potential will be greatest in landscapes where the extinction probability of established populations and the rate at which new sites become available for colonization are both modest. They also predict that variation between early and late succes- sional populations for dispersal will be lowest in situations that involve either many colonization opportunities and high population extinction rates or low rates of both col- onization and local population extinction. Prior to the introduction of agriculture to the piedmont of south- eastern North America in the early 18th century, most of the landscape consisted of mature hardwood-dominated forests (Delcourt and Delcourt, 1987). Data on red maple population dynamics collected from mature hardwood stands that escaped clearing suggest that the extinction probabilities of red maple populations in such forests are extremely low (Christensen, 1977). If extinction rates were similarly low in the presettlement piedmont landscape, then much of the variation for long-distance dispersal potential may have been purged from these populations during this period. For species that persist throughout a successional sequence, Olivieri and Gouyon (1985) sug- gest that selection for dispersal within individual popu-

1432 AMERICAN JOURNAL OF BOTANY [Vol. 81

TABLE 4. Means (?standard deviation) of coefficients of variation for morphological characters of red maple samaras collected from populations in early and late successional environments. Wing load- ing = samara mass (mg)/samara area (cm2). Sample size = 5 pop- ulations/successional stage, with 50 samaras per population with the exception of one early successional population where N = 31.

Mean coefficient of variation

Successional Square root stage wing loading Samara area Samara mass Seed mass

Early 8.99 23.20 20.79 23.23 (1.56) (6.14) (4.23) (5.71)

Late 9.69 22.30 20.55 24.72 (1.15) (1.28) (3.27) (4.76)

lations may play a larger role in maintaining variation in dispersal characters than the landscape's disturbance re- gime. Since rodent predation of red maple seeds is intense (Peroni, 1991) in these piedmont forests and appears to be density-dependent (Peroni, unpublished data), mod- erate levels of dispersal may be selectively advantageous within these populations (Howe and Smallwood, 1982).

Although the wing loading data suggest that the dis- persal potential of red maple in early and late successional environments differs, the question of whether this poten- tial is realized remains. Established models of samara flight clearly indicate that the height of release can have profound effects on the actual distance a samara travels (Green, 1980; Guries and Nordheim, 1984). The differ- ences in height measured between the early and late suc- cessional populations were not significant, but the data suggest a trend for slightly taller trees in the late vs. the early successional populations that may compensate for the higher wing loading potentials detected in these more mature habitats. In addition, most existing biomechanical models of seed dispersal apply only to situations that involve nonturbulent air. Since air turbulence is likely to be common in nature, and since patterns of air flow may vary among sites that differ in species composition and topography, the ecological implications of the differen- tiation in wing loading detected between the early and late successional populations in this study could be min- imal.

Models of genetic change during succession that are based upon life history evolution theory predict that later, presumably more competitive, successional environ- ments will select for large seeds (Gray, 1987). However, the seed mass results obtained in this and similar studies (Reinartz, 1984; Aarssen and Turkington, 1985; Hartnett, Hartnett, and Bazzaz, 1987) do not agree with these pre- dictions. In fact, the trends that emerge from these studies suggest the either no differences in seed size exist along successional gradients (e.g., Reinartz, 1984) or that the earlier successional populations of a given species actually produce larger seeds than populations in more succes- sionally mature sites (Aarssen and Turkington, 1985; Hartnett, Hartnett, and Bazzaz, 1987). Although maternal environment effects may account for some ofthe variation in red maple seed size detected between early and late successional populations in this study, the seed size data reported in these other studies were all obtained from common garden experiments.

The trend toward slightly larger seeds in earlier rather

TABLE 5. Results of univariate ANOVAs on coefficients of variation for morphological characters of red maple samaras collected from early and late successional environments. Data were square root transformed prior to analysis.

f (P)

Square root Source df wing loading Samara area Samara mass Seed mass

Successional stage 1 0.64 0.01 0.01 0.20 (0.4464) (0.7570) (0.9232) (0.6650)

Error 8

than later successional environments that emerges from these studies suggests that the assumption that compe- tition constitutes the major selective force in successional habitats may not apply to seed size. The extremes in temperature, irradiance, and water availability encoun- tered in many recently disturbed habitats may impose considerable selection on populations that inhabit these environments. Schimpf (1977) documented a significant negative correlation between seed size in Amaranthus ret- roflexus L. and soil moisture availability, which suggests that selection may favor large seeds in drier soils. Ap- parently, large seed size can accelerate the penetration of radicles into the soil and the emergence of seeds buried at greater depths (Baker, 1972).

The small differences in seed size detected in these experiments suggest that factors such as low heritabilities for seed size or negative genetic correlations between seed size and other fitness components may limit natural se- lection on this character in successional habitats. Mazer (1987) found no evidence of significant additive genetic variation for seed size in wild radish despite the fact that seed size was correlated with fitness and varied 20-fold within the populations studied. In a similar investigation, Schwaegerle and Levin (1990) found no significant her- itability for seed size in a population of Phlox drum- mondii. At present, no published data on negative genetic correlations between seed size and other fitness compo- nents exist for undomesticated plants.

The results of this experiment provide no support for adaptive explanations that assume changes in the intensity of selection occur during succession. Gray (1987) suggests that genetic variation within populations may decrease during succession in response to increased competition or decreased environmental heterogeneity. If changes in the intensity of selection varied between the early and late successional habitats considered in this study, then, for a given character, the mean coefficient of variation for the early successional stage should be greater than the

TABLE 6. Results of ANOVA to examine the effects of population and matemal tree within population on variation in area of red maple samaras. Sample size = 4 samaras per matemal tree, 15 to 19 trees per population, 4 populations. When the population effect is tested using the matemal tree within population mean square as the error term the f ratio drops to 1.10 (P = 0.3985).

Source df SS MS f P

Population 3 0.3162 0.1054 8.23 0.0001 Matemal tree

w/in population 49 5.1380 0.1049 8.19 0.0001 Error 149 1.9081 0.0128

November 1994] PERONI-CHANGES IN DISPERSAL OF RED MAPLE DURING SUCCESSION 1433

mean coefficient of variation calculated for the late suc- cessional stage, provided no other evolutionary forces influence the character. However, the data from this study provide no evidence of such differences. Although reports of decreased genetic variation along successional gradients exist (McNeilly and Roose, 1984; Gray, 1985), most other investigations have not detected this pattern (Hayward, 1970; Hayward, Gottlieb, and McAdam, 1978; Aarssen and Turkington, 1985; Hartnett, Hartnett, and Bazzaz, 1987; Peroni, 1991). The existing literature suggests that the intensity of selection does not necessarily increase during succession, or that the effects of such intensified selection may be balanced by increases in environmental heterogeneity during succession or the effects of gene flow.

Variation among populations - Significant variation ex- isted among populations within each successional stage for all of the samara characters measured. The absence of any correlation between the early successional popu- lation means for wing loading and the distances from seed sources at the time these sites were colonized suggests that selection for long-distance dispersal did not produce the variation in wing loading that exists among these popu- lations. Since the red maples that bordered each field probably accounted for the majority of seeds that colo- nized these sites, many of the red maples in these early successional stands may be the progeny of a relatively small number of parents. Thus, founder effects may ac- count for much of the variation in wing loading and wing area detected among populations within each successional stage.

Seed mass also varied significantly among populations within each successional stage. Although the magnitude of these differences was small, such subtle variation po- tentially could create more substantial differentiation among populations for survival and growth in competitive environments (Howe and Richter, 1982; Stanton, 1984, 1985). Differential selection among sites that is unrelated to successional change could account for the differences in seed mass detected among populations within each stage. However, founder effects or maternal environment effects constitute equally likely sources for this variation.

Heritability of samara characters-The evolutionary interpretations provided in this discussion assume that at least part of the variation in samara characters observed in the red maple populations studied is heritable. Maternal environment effects or ontogenetic factors could account for all of the differences in samara characters observed among populations. Because of the difficulties involved in conducting sufficiently controlled experiments to de- termine the relative importance of such nonheritable vs. heritable sources of variation in tree populations, direct estimates of heritabilities for red maple samara characters are not available. Such data would be particularly difficult to obtain for characters such as samara area since the wing develops from the ovary wall and reflects the maternal rather than the seed phenotype.

However, several lines of evidence suggest that heritable variation may exist for at least one of these characters, samara morphology. The identity of the maternal tree explained a significant amount of the variation in samara morphology within red maple populations, but this vari-

ation was not related to tree size, nor was there a clear relationship between branch position and samara size. Since tree diameter and height are variables that reflect the quality of the local environment and to a lesser extent tree age, this result suggests that some of the variation in samara area may be heritable. Townsend (1972) also not- ed that samara size showed little variation within the progeny of an individual red maple, but varied signifi- cantly among maternal families from the same popula- tion. Guries and Nordheim (1984) determined that wing loading ratios did not vary significantly among canopy locations within the same red maple. These data suggest that samara architecture remains relatively constant among different locations within the maternal tree. More con- clusive evidence regarding the heritability of samara char- acters will not be available until long-term studies of these characters are conducted in provenance testing planta- tions.

LITERATURE CITED

AARSSEN, L. W., AND R. TURKINGTON. 1985. Within species diversity in natural populations of Holcus lanatus, Lolium perenne, and Tri- folium repens from four different-aged pastures. Journal of Ecology 73: 869-886.

ABRAHAMSON, W. G., AND M. D. GADGIL. 1973. Growth form and reproductive effort in goldenrods (Solidago, Compositae). American Naturalist 107: 651-661.

BAKER, H. F. 1972. Seed weight in relation to environmental conditions in California. Ecology 53: 997-1010.

CHRISTENSEN, N. L. 1977. Changes in structure, pattern and diversity associated with climax forest maturation in piedmont, North Car- olina. American Midland Naturalist 97: 176-188.

DELCOURT, P. A., AND H. R. DELCOURT. 1987. Long-term forest dy- namics of the temperate zone. Springer-Verlag, New York, NY.

DESTEVEN, D. 1991 a. Experiments on mechanisms of tree establish- ment in old field succession: seedling emergence. Ecology 72: 1066- 1075.

1991b. Experiments on mechanisms oftree establishment in old field succession: seedling survival and growth. Ecology 72: 1076- 1088.

FOWELLS, H. A. 1965. Silvics offorest trees ofthe United States. USDA Handbook 271. U.S. Government Printing Office, Washington, DC.

GRAY, A. J. 1985. Adaptation in perennial coastal plants-with par- ticular reference to heritable variation in Puccinellia maritima and Ammophila arenaria. Vegetatio 61: 179-188.

. 1987. Genetic change during succession in plants. In A. J. Gray, M. J. Crawley, and P. J. Edwards [eds.], Colonisation, suc- cession, and stability, 273-293. 26th Symposium of the British Ecological Society, Blackwell, Oxford.

GREEN, D. S. 1980. The terminal velocity and dispersal of spinning samaras. American Journal of Botany 67: 1218-1224.

GURIES, R. P., AND E. V. NORDHEIM. 1984. Flight characteristics and dispersal potential of maple samaras. Forest Science 30: 434-440.

HARLow, W. M., E. S. HARRAR, J. A. HARDIN, AND F. M. WHITE. 1991. Textbook of dendrology, 7th ed. McGraw-Hill, New York, NY.

HARTNETT, D. C., B. B. HARTNETT, AND F. A. BAzzAz. 1987. Persis- tence of Ambrosia trifida populations in old fields and responses to successional changes. American Journal of Botany 74: 1239-1248.

HAYwARD, M. D. 1970. Selection and survival in Lolium perenne. Heredity 25: 441-447.

, L. D. GOTTLIEB, AND N. J. McADAM. 1978. Survival of allo- zyme variants in swards of Lolium perenne L. Zeitschriftfiir Pflan- zenziichtung 81: 228-234.

HOwE, H. F., AND W. M. RICHTER. 1982. Effects of seed size on seedling size in Virola surinamensis: a within and between tree analysis. Oecologia 53: 347-351.

AND J. SMALLWOOD. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13: 201-228.

1434 AMERICAN JOURNAL OF BOTANY [Vol. 81

KEEVER, C. 1950. Causes of succession in old fields of the piedmont, North Carolina. Ecological Monographs 20: 230-250.

LEVIN, S. A., D. COHEN, AND A. HASTINGS. 1984. Dispersal strategies in patchy environments. Theoretical Population Biology 26: 165- 191.

MAZER, S. J. 1987. The quantitative genetics of life history and fitness components in Raphanus raphanistrum L. (Brassicaceae): ecological and evolutionary consequences of seed weight variation. American Naturalist 130: 891-914.

MCNEILLY, T., AND M. L. RooSE. 1984. The distribution of perennial ryegrass genotypes in swards. New Phytologist 98: 503-513.

OLIVIERI, I., AND P. H. GOUYON. 1985. Seed dimorphism fordispersal: theory and implications. In J. Haeck and J. W. Woldendorp [eds.], Structure and functioning in plant populations, vol. 2, Phenotypic and genotypic variation in plant populations, 77-90. North Holland Publishing, Amsterdam.

OOSTING, H. J. 1942. An ecological analysis of the plant communities of piedmont, North Carolina. American Midland Naturalist 28: 1- 126.

PEET, R. K., AND N. L. CHRISTENSEN. 1979. Succession: a population process. Vegetatio 43: 131-140.

, AND -. 1987. Competition and tree death. BioScience 37: 586-595.

PERONI, P. A. 1991. Genetic change and persistence of red maple (Acer rubrum L.) during secondary succession in North Carolina piedmont forests. Ph.D. dissertation, Duke University. Durham, NC.

REINARTZ, J. A. 1984. Life history variation of common mullein (Ver- bascum thapsus). III. Differences among sequential cohorts. Journal of Ecology 72: 927-936.

SCHIMPF D. A. 1977. Seed weight ofAmaranthus retroflexusin relation to moisture and length of growing season. Ecology 58: 450-453.

SCHwAEGERLE, K. E., AND D. A. LEVIN. 1990. Quantitative genetics of seed size variation in Phlox. Evolutionary Ecology 4: 143-148.

STANTON, M. L. 1984. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65: 1105- 1112.

. 1985. Seed size and emergence time in a stand of wild radish (Raphinus raphanistrum L.): the establishment of a fitness hierarchy. Oecologia 67: 524-531.

TowNsEND, A. M. 1972. Geographic variation in fruit characteristics of Acer rubrum. Bulletin of the Torrey Botanical Club 99: 122-126.

VAN VALEN, L. 1971. Group selection and the evolution of dispersal. Evolution 25: 591-598.

WILSON, B. F. 1968. Red maple stump sprouts: development the first year. Harvard Forest Paper No. 18. Harvard University, Boston, MA.