Ecology, 84(9), 2003, pp. 2476-2492
0 2003 by the Ecological Society of America
LONG-TERM PATTERNS OF ACORN PRODUCTION FOR FIVE OAK
SPECIES IN XERIC FLORIDA UPLANDS
WARREN G. ABRAHAMSON'.2.3AND JAMES N. LAYNE'
'Archbold Biological Station, P.0. Box 2057, Lake Placid, Florida 33862 USA
2Department of Biology, Bucknell University, Lewisburg, Pennsylvania 17837 USA
Abstract. The number of seeds produced by a population of woody plants can vary
markedly from year to year. Unfortunately, knowledge of the patterns and causes of cropsize variation is limited, and most studies have examined only single species in a single
mesic environment. We examined long-term patterns of acorn crop sizes for five species
of shrubby oaks in three xeric upland vegetative associations of south-central peninsular
Florida for evidence of regular fruiting cycles and in relation to winter temperature and
precipitation. Counts of acorns on two white oak species (Quercus chapmanii and Q.
geminata) and three red oak species (Q. inopina, Q. laevis, and Q. myrtifolia) were conducted annually from 1969 to 1996 (except in 1991) on grids in southern ridge sandhill,
sand pine scrub, and scrubby flatwoods associations. As the result of the dissimilar timing
of reproductive events in species of red and white oaks and individual species responses
to climatic variables, annual acorn production of red and white oak species in a given
vegetation association were not synchronized, which dampened the variability of combined
annual acorn production. Consequently, acorns were produced with reasonable abundance
every year by at least one species. Oaks of nearly closed-canopy scrub produced fewer
acorns than similar-sized oaks of the same species in the more open-canopied sandhill and
scrubby flatwoods, suggesting light limitation. We identified regular cycles of acorn production that ranged from 2 to 2.4 yr for white oak species and from 3.6 to 5.5 yr for red
oak species and found evidence that annual acorn production is affected by the interactions
of precipitation, which is highly variable seasonally and annually in peninsular Florida,
with endogenous reproductive patterns. Multiple regression models using precipitation variables accounted for as much as 74% of crop-size variation in Q. inopina, 65% in Q. laevis,
60% in Q. chapmanii, and 44% in Q. geminata, but only 29% for Q. myrtifolia. In contrast,
acorn production showed no significant association with minimum winter temperatures. Of
the various hypotheses offered to explain supra-annual variation in seed crops, our data
are most compatible with the nonadaptive resource-matching hypothesis.
Key words: acorn; crop size; Florida; mast fruiting; precipitation effects on reproduction; Quercus; resource-matching hypothesis; sandhill; sand pine scrub; scrubby Jutwoods.
I NTRODUCTION
The numbers of seeds produced by individual longlived plants can vary markedly according to species
and site (e.g., Norton and Kelly 1988, Smith et al. 1990,
Lalonde and Roitberg 1992, Crawley and Long 1995,
McKone et al. 1998, Kelly et al. 2000, Koenig and
Knops 2000, Kelly and Sork 2002, Shibata et al. 2002).
For example, we would expect that plants growing in
resource-limited sites would produce smaller numbers
of seeds than individuals of the same species and size
living in more optimal sites. Crop sizes in the same
site also can be affected by climatic variables (Sork et
al. 1993, Houle 1999). Favorable temperature and/or
precipitation levels in certain years can promote greater
photosynthate production resulting in above-average
seed production in that year or in subsequent years
Manuscript received 17 December 2001; revised 5 August
2002; accepted 13 December 2002; final version received 21 January 2002. Corresponding Editor: T. P. Young.
Corresponding author (at Bucknell University address).
(Norton and Kelly 1988, Smith et al. 1990). Conversely, factors such as adverse temperature, humidity, or
wind at the time of pollination or seed development
can reduce flowering or seed set in one year and thus
conserve resources that could influence flowering or
fruiting levels positively in a subsequent year. Such
influences on endogenous reproductive patterns of
plants could produce a tendency towards periodic population synchrony of flowering or seeding (Sork et al.
1993 and references therein, Houle 1999). The interactions of endogenous reproductive rhythms with climatic factors could potentially yield patterns of no reproduction or small seed crops interspersed with the
periodic production of large seed crops that may be
synchronous over large areas (Janzen 1971, 1976,
1978, Silvertown 1980, Waller 1979, Sork et al. 1993,
McKone et al. 1998, Keeley and Bond 1999).
The importance of climatic variables to acorn crop
variation may rest in their ability to produce a tendency
towards population synchrony of flowering and/or
fruiting (Lalonde and Roitberg 1992, Waller 1993, Kel-
2476
September 2003
LONG-TERM ACORN PRODUCTION PATTERNS
ly 1994, McKone et al. 1998). However, climate-generated synchrony in and of itself does not establish that
annual fluctuations in crop size represent an evolved
reprod
variable reproductive crops.
Yet, once fruit crop synchrony is initiated, it is possible
that other factors could favor the evolution of a strategy
of variable annual crop sizes. Consequently if acorn
crop synchrony is identified, it is important to determine whether this variation is related to non-adaptive
causes such as resource availability and climatic variation or an evolved response to factors such as losses
to seed predators or enhancement of pollination/fertilization success.
,
Documented examples of long-lived woody plants
that exhibit seed production patterns with periodic
large crops include species of hickory (Sork 1983,
1993a, McCarthy and Quinn 1989), cycad (Ballardie
and Whelen 1986), ash (Tapper 1996), fir, maple, birch
(Houle 1999), and oak (Downs and McQuilkin 1944,
Matschke 1964, Beck and Olson 1968, Goodrum et al.
1971, Wolgast 1972, Beck 1977, Wolgast and Stout
1977, Moody 1985, Sork 19936, Sork et al. i993, Koenig et al. 1994, 1996, Crawley and Long 1995, Healy
et al. 1999, Abrahamson and Layne 2002a, b). In spite
of the relatively large number of studies, few data sets
allow direct comparisons of multiple species within the
same genus across different vegetative associations
within the same geographic region (see Kelly et al.
2000 for an example with species of the grass Chionochloa). Furthermore, we have limited knowledge of
the causes of supra-annual variation in seed production
in spite of the ecological and evolutionary significance
of crop-size fluctuations to the demography of the
plants themselves as well as of the animals that consume the seeds. The study reported here describes patterns of variation in annual acorn production of five
shrubby oak species, including members of both the
white and red oak sections with markedly different reproductive biologies, occurring in three xeric upland
associations of peninsular Florida that differed in light
availability. Because of a mix of multiple red and white
oak species in each vegetation association, the patterns
of fruiting for congeners with similar and markedly
different reproductive biologies could be compared in
the same and different vegetative associations. In addition, the variability of seasonal and annual precipitation on the Florida peninsula provided an opportunity
to examine the relationships between $ariation in annual seed production and rainfall. Our examination of
climate effects on seed production suggests that seasonal preciphation plays an appreciable role in determining crop size.
Extensive reviews of woody-plant crop sizes by Herrera et al. (1998) and Kelly and Sork (2002) indicate
that supra-annual variation in crop size is the rule
among iteroparous woody plants, yet understanding of
the proximate and ultimate causes of seed-crop variation is extremely limited. Attempts to explain supra-
2477
annual variation in crop size have generated a number
of hypotheses including nonadaptive interpretations
such as the resource-matching or weather-tracking hypothesis as well as the evolved responses of predator
satiation, enhancement of wind-pollination success, animal pollination and dispersal enhancement, and environmental prediction, as reviewed by Kelly (1994),
Koenig et al. (1994), Yamauchi (1996), Kelly et al.
(2001), Kelly and Sork ( 2 0 0 3 ,andVander Wall (2002).
Although the long-term data reported here do not include information about variables such as rates of seed
predation and pollen flow needed to critically test all
of the seed-crop size hypotheses, these data do provide
a basis for evaluating nonadaptive vs. adaptive explanations for compatibility with seed production patterns
in Florida's shrubby oaks.
Specifically, we address the following questions:
1) To what extent is acorn production synchronous
within a species in different but nearby vegetative associa
2)
nt is acorn production' synchronous
among species within a vegetative association?
3) To what extent do species within the same oak
section have parallel acorn production patterns?
4) Do shrubby oaks of the Florida peninsula exhibit
regular cycles of acorn production?
5) To what extent do climatic factors, namely precipitation and temperature, account for variation in
acorn production?
METHODS
Study site
The study site (Archbold Biological Station) lies near
the southern terminus of the Florida peninsula's Lake
Wales Ridge (12 km south of the town of Lake Placid,
27'11' N,81'21' W). Residual sandhills, relic beach
ridges, and paleo-sand dunes shape the landscape
(Brooks 1981) with elevations ranging from 38 to 65
m above mean sea level (USGS Childs, Florida, 7.5'
quadrangle). The lowest elevations (41-44 m) commonly occupied by the oaks in the study grids are in
scrubby flatwoods on well-drained soils; while the
highest elevations (59-65 m) inhabited by oaks are in
southern ridge sandhill vegetation on excessively welldrained sands. Elevations at which oaks occur in sandpine scrub are intermediate (42-50 m) (Abrahamson et
al. 1984, Abrahamson and Abrahamson 1996a, 6, Menges and Hawkes 1998; see Plate 1).
Scrubby flatwoods consist of a low (1-2 m) shrubby
association of predominantly evergreen, xeromorphic
oaks including Quercus inopina (Archbold oak), Q.
chapmanii (Chapman oak), and Q. geminata (sand live
oak), as well as abundant understory Serenoa repens
(saw palmetto) and Sabal etonia (scrub palmetto). Tree
presence is variable, typically comprised of widely
scattered Pinus elliottii var. densa (south Florida slash
pine) and P. clausa (sand pine). Sand pine scrub (hereafter referred to as scrub) designates a three-tiered com-
2478
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
Ecology, Vol. 84, No. 9
PLATE 1. (Top left) Southern ridge sandhills are composed of xerophytic oaks, scattered south Florida slash pine, and
understories of wiregrass, scrub and saw palmettos, and herbs. (Right) Sand pine scrubs are comprised of dense to scattered
sand pine with understories dominated by oaks. (Bottom left) Scrubby flatwoods have a low shrubby growth of xerophytic
oaks with widely scattered south Florida slash pines and sand pines. Photographs are by Warren Abrahamson.
munity characterized by a canopy of nearly even-aged
P. clausa, an intermediate canopy of Carya jloridana
(scrub hickory), Q. myrtifolia (myrtle oak), Q. geminata, and Q. chapmanii, and an understory of the same
oaks plus Serenoa and Sabal palmettos. Southern ridge
sandhill (hereafter referred to as sandhill), also a threelayered community, has an overstory of P. elliottii var.
densa, a lower deciduous canopy of Q. laevis (turkey
oak) and C. jloridana, and a shrub and understory layer
composed of Q. myrtifolia, Q. geminata, Q. chapmanii,
both Serenoa and Sabal palmettos, and Aristida stricta
(wiregrass) and forbs (Abrahamson et al. 1984, Abrahamson and Hartnett 1990, Myers 1990, and Abrahamson and Abrahamson 1996a, b, Menges 1999). Quercus
laevis of the southern Lake Wales Ridge express a
stunted growth form, as they do not develop the heights
and broad crowns of their more northerly counterparts.
Multiple measurements of photosynthethically active
radiation (PAR) in these associations showed that available PAR is highest in scrubby flatwoods, intermediate
in sandhill, and lowest in sand pine scrub (Abrahamson
and Rubinstein 1976).
Hot, wet summers and mild, dry winters characterize
the climate of the study area. The highest monthly mean
temperature (27.5"C) occurs in August and the lowest
(16°C) in January. The rainy season normally extends
from June through September, with -60% of the annual
precipitation (1357 mm, 65-yr mean, 1932-1997) fall-
ing during this 4-mo wet season (Abrahamson et al.
1984; for regional climate information, see Chen and
Gerber 1990).
Natural history of oak species
The five species of oak sampled in our study are the
most abundant of the nine Quercus species that occur
within our study area. Two species, Q. chapmanii Sargent and Q. geminata Small, are representatives of the
white oak group (Quercus section Quercus), while
three species, Q. myrtifolia Willdenow, Q. inopina
Ashe, and Q. laevis Walter are members of the r e d
black oak group (Quercus section Lobatae) (Jensen
1997, Nixon and Muller 1997).
Members of the white oak section produce flowers
in spring that, if fertilized, develop into mature fruit
in autumn of the same year. However, staminate floral
buds are initiated in the spring of the year prior to
flowering and pistillate floral buds are initiated in late
summer of the year prior to flowering (Sork et al. 1993
and references therein). Consequently, full acorn development spans 2 yr. Red/black oaks produce staminate and pistillate flowers during the spring of one year,
but ovules are fertilized and the fruit mature in the
following year. As with white oaks, the staminate and
pistillate floral buds are initiated in the spring and summer and late summer, respectively, of the year prior to
flowering (Sork et al. 1993 and references therein).
-.
September 2003
LONG-TERM ACORN PR ODUCTION PATTERNS
Thus, full fruit development in red/black oaks spans 3
Yr.
Acorn size varies among the five oaks. The fresh
masses of acorns for the oaks ranked from smallest to
largest in the order: Q. myrtifolia < Q. inopina < Q,
geminata < Q. chapmanii < Q. laevis (Abrahamson
and Abrahamson 1989). Abrahamson and Layne
(2002b) found that the small-fruited Q. myrtifoZia had
the highest numbers of acorns per bearing ramet while
the large-fruited Q. laevis (two to four times heavier
within the same vegetative association) had the lowest
numbers of acorns per bearing ramet.
Quercus geminata is common in sandhill, scrub, and
scrubby flatwoods. Quercus chapmanii is common in
sandhill and scrub, but is often most abundant in scrubby flatwoods. Quercus myrtifolia is frequent in sandhill
and scrub but uncommon in scrubby flatwoods. The
central Florida endemic Q. inopina, a highly clonal
shrub, is dominant in scrubby flatwoods but does not
occur in the other two associations. Quercus laevis is
common in sandhill but infrequent in the other vegetative associations (Abrahamson et al. 1984, Givens et
al. 1984, Menges et al. 1993, Abrahamson and Abrahamson 1996a, b).
Monitoring of acorn production
Annual counts of acorns for each species were initiated in 1969 on four 2.7-ha grids (counts for Q. inopina and Q. myrtifolia were combined from 1969 to
1971, with separate counts for these oaks beginning in
1972). The grids were placed in representative stands
of scrubby flatwoods, scrub, and sandhill (two grids,
one of which was prescribed burned in 1993) as well
removed as possible from adjacent associations. Because there is only one grid for scrubby flatwoods and
one for scrub, and because the patterns of acorn production for each oak species in the two grids of sandhill
were so similar prior to the prescribed burn, only data
from the unburned sandhill grid are presented in the
analyses included here. Consequently, differences
among vegetation associations conceivably could be
due to site-to-site variation unrelated to vegetation.
However, given that the precipitation and temperature
differences among associations are slight, it is most
likely that the differences are related to vegetation (e.g.,
canopy cover). The distance between the nearest
boundaries of the grids ranged from 870 to 1130 m
(mean = 1003 m). With the exception of 1991, all grids
were censused through 1996.
Acorn counts were conducted in the autumn at a time
when the,nuts were well enough developed to allow
normal and aborted individuals to be distinguished but
before they were ripe enough to be harvested in significant numbers by birds and rodents. Acorns were
counted on one ramet (stems) in each of the four quadrants at 15 stations located 30 m from one another
within the same row and 60 m from one another within
the same column within a grid. Consequently, 60 ra-
2479
mets of each species were sampled on each grid except
for Q. laevis on the scrub grid for which only 30 ramets
were sampled because of its scarcity. The acorn-sampling stations were the same as those used in vegetation
surveys in 1969, 1979, and 1989 (Givens et al. 1984,
Menges et al. 1993).
Because of the small size of Lake Wales Ridge oaks,
we were able to make absolute counts of all acorns
present on each sampled oak ramet. At each station,
the nearest ramet of each species in each quadrant was
selected subject to the following qualifications: (1) ramets within 1 m of the path between stations were not
sampled to exclude individuals that might have been
damaged by foot traffic or trimming and obviously
damaged and abnormal individuals away from paihs
also were avoided; (2) only one ramet of a given clone
was sampled at a given station; (3) no more than five
individuals of the same species in the smallest size class
(0.3-0.8 m) were sampled, as only very rarely did oaks
of that size produce acorns.
For large ramets, the same individual ramet had a
relatively high probability of being counted from year
to year, except for the occasional death of a ramet.
However, there was a much lower probability of repeated sampling of the same ramets in smaller size
classes because of the relatively high rate of ramet
mortality (Givens et al. 1984, Menges et al. 1993, Johnson and Abrahamson 2002). Consequently year-to-year
production variation for individual ramets cannot be
analyzed since ramets were not marked.
The height of ramets sampled was recorded to the
nearest 0.3 m. As acorn production is related to ramet
size (Abrahamson and Layne 2002a, b), mean number
of acornslramet was a weighted value based on counts
for different size classes and the proportion of each
size class in the population as determined by vegetation
surveys in 1969, 1979, and 1989 (Givens et al. 1984,
Menges et al. 1993), with adjustment for any changes
in the distribution of size classes between 10-yr censuses on the assumption that they were linear.
In order to properly weight acorn numbers, we analyzed the changes in oak densities in each grid over
the 20-yr period represented by the vegetative surveys.
The trends were similar in all associations, each exhibiting an overall decline in ramet density from 1969
to 1979 followed by an increase in ramet density from
1979 to 1989. Density in 1989 in sandhill and scrub
exceeded that of 1969 by 8% and 22%, respectively,
while that of scrubby flatwoods was 11% below the
1969 level. All differences between censuses for numbers of ramets in ground, shrub, and tree layers within
each association were significant (x2 tests of 1 X 3
contingency tables of total frequencies in samples for
each vegetation layer: P < 0.001) except for the ground
layer in scrubby flatwoods and the tree layer in scrub.
The trend of decline in overall ramet density from 1969
to 1979 and increase from 1979 to 1989 was mostly
due to changes in the ground and shrub layers, reflect-
2480
WARREN G. ABRAHAMS3N AND JAMES N.LAYNE
ing thinning in the first 10-yr interval (Givens et al.
1984) and recruitment of new ramets by these clonal
oaks in the second decade (Menges et al. 1993). Treesized oaks exhibited a progressive increase in density
from 1969 to 1989 in all three associations. However,
only three of the 12 populations exhibited significant
long-term patterns of change and none of these patterns
were congruent with the expected consequences of the
density changes described above. A linear regression
on the natural log-transformed numbers of acorns per
ramet of Q. chapmanii found increases in sandhill
(Y = 0.12X - 8.59, r2 = 0.20, P = 0.03) and scrub
(Y = 0.07X - 4.97, r2 = 0.16, P = 0.053). The third
population, Q. myrtifolia in scrubby flatwoods. exhibited
decreasing acorn production during approximately the
first third of the 27-yr study before increasing during
the last third of the study (Y = -2.04X + 0.01S
86.36, rz = 0.33, P = 0.02). Additional details of the
sampling protocols are available in Abrahamson and
Layne (2002a, b). One might argue that changes in oak
ramet-size distributions or densities during the course
of the study, with consequent changes in mean numbers
of acornshamet, could have influenced the patterns of
acorn production over time. However, as our sampling
protocol controlled for ramet-size changes (Abrahamson
and Layne 2002a), mean ramet size remained essentially
constant throughout the 28-yr period.
+
Statistical analyses
SPSS Version 10 statistical software was used for all
analyses (SPSS, Chicago, Illinois, USA) except for the
spectrum (Fourier) analyses which were performed using Statistica Version 5 (Statsoft, Tulsa, Oklahoma,
USA). Data on the percentages of ramets bearing
acorns (the incidence of acorn production) were arcsine-square-root transformed prior to statistical analyses. For ANOVAs, correlation, and regression analyses, natural-log transformed numbers of acorns per
ramet were used to reduce the amplitudes of production
variation over time. However, coefficients of variation
(cv) were calculated from the absolute numbers of
acorns per ramet. One-way, two-way, and three-way
ANOVAs with Bonferroni multiple-comparison posthoc tests to adjust significance levels for multiple comparisons were used to determine differences in the number of acorns per ramet and the incidence of acorn
production across oak species and vegetative associations. In all cases where multiple correlations are made,
significance levels were adjusted using the sequential
Bonferroni procedure to ensure contrast-wide significance of at least P = 0.05 (Rice 1989).
Because of the length (27 yr) of our data set, annual
crop sizes of each oak could be examined for cyclical
production behavior using time-series spectrum (Fourier) analyses. Spectrum analysis breaks down a complex time series containing cyclical components into a
few underlying sinusoidal functions of specific lengths
(Bloomfield 1976). We explored the correlations of
Ecology, Vol. 84,No. 9
numbers of acorns per ramet with winter temperatures
and with annual, monthly, and various monthly combinations of precipitation that reflected time periods
within the wet or dry season considered to have a potential effect on particular stages of the oak reproductive cycle. Both numbers of acorns per ramets and precipitation variables were natural log-transformed prior
to analysis and precipitation variables were lagged up
to 3 yr in order to explore the correlation of rainfall
with the timing of floral-bud initiation, flowering, fertilization, and acorn development because each of these
events potentially influences the number of acorns produced. Because of the large number of contrasts involved, the significance of the resultant Pearson correlation coefficients was adjusted using the sequential
Bonferroni procedure (Rice 1989) to ensure significance of at least P 5 0.05 within a species in a given
association. We also report (Table 5) correlations that
were initially significant at least at P 5 0.01 but were
nonsignificant according to the sequential Bonferroni
procedure. These latter correlations are reported only
to help identify precipitation variables that may be useful predictors of acorn production.
Stepwise multiple linear regression analysis was
used to develop models for each oak species that used
precipitation variables to predict the natural-log-transformed numbers of acorns per ramet. The data for all
associations in which a given oak occurred were combined €or this analysis because crops of individual oak
species were typically correlated across associations.
The stepwise criterion for variable entry was P 5 0.05
for F and that for variable removal was P 5 0.10.
RESULTS
Variation across vegetation associations
and among species
Annual acorn production was frequently synchronized within an oak species across vegetation associations (Table 1, also see Abrahamson and Layne
2002a, b). The numbers of acorns per ramet (the annual
acorn production) were positively correlated for six of
the 10 comparisons of the same species across associations. Quercus laevis,'with consistently low acorn
production, exhibited the strongest correlation of acorn
production across associations.
Acorn production of oak species within the same
section (Le., red vs. red oak species) was also synchronized in several instances likely due to their similarities in reproductive phenology. In three of six comparisons, the levels of annual acorn production for species within the same section were positively and significantly related. Numbers of acorns per ramet for Q.
chapmanii and Q. geminata, both white oaks, were positively correlated in scrub ( r = 0.63, P < 0.001) and
scrubby flatwoods ( r s 0.58, P = 0.002), but were not
related in sandhill. Among red oaks, annual acorn production of &. myrdifolia and Q. laevis was correlated
September 2003
LONG-TERM ACORN PRODUCTION PATTERNS
248 1
TABLE 1. Pearson correlation coefficients for natural-log-transformed annual acorn production
(number of acorns per ramb) within oak species that occur in two or more xeric upland
vegetation associations in south-central Florida.
Species
White oaks
Q. chapmanii
Q. geminata
Red oaks
Q. myrtifolia
Sandhill vs.,Sand
pine scrub
Sandhill vs. Scrubby
flatwoods
Sand pine scrub vs.
Scrubby flatwoods
0.84""
. 0.36NS
0.43NS
0.83""
0.57**
0.57**
0.44NS
O.3lNs
0.69**
Notes: N = 27 yr for all correlations except N = 24 yr for Q. myrtifolia in scrubby flatwoods.
Significance levels were adjusted using the sequential Bonferroni procedure to ensure significance at the P 5 0.05 level within a species across associations.
P < 0.01; Ns, not significant; .-, not applicable.
in sandhill ( r = 0.60, P = O.OOl), but not in scrub; and
annual acorn production of Q. myrtifolia and Q. inopina
was not correlated in scrubby flatwoods. As expected,
there were no significant correlations of acorn production between oak species of different sections within
the same vegetation association.
A two-way ANOVA followed by a Bonferroni multiple comparison post-hoc test showed that annual
acorn production varied significantly according to vegetation association and oak species, and that the interaction between association and oak species was significant (Table 2, Fig. l). Overall, oaks i n scrub bore
significantly fewer acorns per ramet (2.6 2 0.3, mean
t 1 SE) than oaks in sandhill (10.4 2 1.2) or scrubby
flatwoods (9.6 2 1.2) (association, F2,306= 43.6, P <
0.001; species, F4,306 = 15.2, P < 0.001; interaction
TABLE 2.
term, F5,306= 2.5, P = 0.032). The highest producer,
Q. myrtifolia, averaged more than five times as many
acorns per ramet in sandhill and scrubby flatwoods than
in scrub (Table 2), while ramets of Q. geminata averaged six to nine times more acorns per ramet in scrubby flatwoods and sandhill, respectively, than in scrub.
Variation over time and correlation
of acorn-production components
Acorn production varied markedly from year-to-year
for each species within a vegetative association, however, the patterns of variation differed by species (Fig.
1). Among species across all vegetative associations
(Fig. 2), Q. myrtifolia produced the highest mean number of acorns per ramet (13.4 2 2.3) followed by Q.
chaprnanii (8.8 ? l.o), Q. geminata (4.5 -C 0.6), Q.
Numbers of acorns per ramet (rank in parentheses) and coefficients of variation
(%) for the numbers of acorns per ramet (rank in parentheses) for oak species in three xeric
upland vegetation associations in south-central Florida.
-.
Association
and species
Q. chapmanii
Q. geminata
Q. myrtifolia
Q. laevis
No. acorns
per ramet?
(rank)
9.6
7.4
19.6
5.1
41.8
i 1.51
2 1.17
-i- 3.5
2 1.01
2 4.35
(2)
(3)
(1)
(4)
cv of no.
acorns per
81.2
82.5
92.5
101.9
54.0
(4)
(3)
(2)
(1)
Combined
Sand pine scrub
3.5 i 0.57 (1)
84.1 (4)
Q. chapmanii
Q. geminata
0.8 t 0.16 (4)
104.9 (1)
3.5 t 0.65 (1)
96.7 (3)
Q. myrtifolia
Q. laevis
2.6 ? 0.52 (3)
103.5 (2)
Combined
10.4 2 1.27
63.7
Scrubby flatwoods
Q. chapmanii
13.2 S 1.60 (2)
63.2 (4)
5.4 t 0.85 (3)
82.2 (2)
Q. geminata
Q. myrtifolia
18.0 i 4.02 (1)
,
109.5 (1)
1.9 i 0.26 (4)
66.3 (3)
Q. inopina
Combined
34.2 2 4.36
66.2
Note: N = 27 yr forall correlations except N = 24 yr for Q. myrtifolia and Q. inopina in
scrubby flatwoods.
I Mean t 1 SE.
2482
Ecology, Vol. 84, No. 9
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
-A-
Q. myrtifolia
Q. laevis
~
'
"
"
'
'
'
'
'
-
FIG. 1. Mean numbers of acorns per ramet for five oak species including two members of the white oak section (Q.
chapmanii and Q. geminuta) and three members of the red oak section (Quercus myrtlfoliu, Q. laevis, and Q. inopinu) in
three xeric upland vegetative associatlons in south-central Florida over the 28-yr period 1969-1996 (no observations were
made in 199i).
September 2003
Q. inopina
LONG-TERM ACORN PRODUCTION PATTERNS
2483
I
FIG. 2. Summed mean numbers of acorns per ramet for five oak species including two members of the white oak section
(Q. chapmanii and Q. geminata) and three members of the red oak section (Quercus myrtifolia, Q. laevis, and Q.inopina)
for three xeric upland vegetative associations in south-central Florida over the 28-yr period 1969-1996 (no observations
were made in 1991). Horizontal dashed lines represent the long-term mean.
TABLE 3. Pearson correlations ( 7 ) of the incidence of acorn
production (arcsine square-root transformed percentage of
ramets bearing acorns) with the amount of acorn production
(mean number of acorns per bearing ramet).
Species
White oaks
Q. chapmanii
Q. geminata
Red oaks
Q. myrtifolia
Q. inopina
Q. laevis
Ecology, Vol. 84, No. 9
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
2484
Sandhill
Sand pine
scrub
Scrubby
flatwoods
0.66""
0.53**
0.73**
0.63**
0.61**
0.43NS
0.55**
0.70""
0.79**
0.80**
0.52**
0.26Ns
...
...
...
Notes: N = 27 yr for all correlations except N = 24 yr for
Q. myrtifolia and Q. inopina in scrubby flatwoods. Significance levels were adjusted using the sequential Bonferroni
procedure to ensure significance at the P 5 0.05 level for all
comparisons within a species.
P < 0.01; NS, not significant; ..., not applicable.
*%
laevis (3.9 ? 0.7), and Q. inopina (1.9 2 0.3) (one= 16.9, P < 0.001). Bonferroni
way ANOVA, F4,124
multiple-comparison post-hoc tests found all species
comparisons were significant with the exception of Q.
geminata and Q. inopina ( P = 0.077) and Q. laevis
and Q. inopina ( P = 0.53).
Quercus chapmanii consistently exhibited the least
variation in annual crop size compared to the other
species, while the species with the most variable crop
size differed according to association (Table 2). Whatever factors determined annual acorn production of
these oaks affected both the frequency with which ramets produced acorns and the number of acorns per
bearing ramet. In all but two cases, the percentage of
bearing ramets and the number of acorns per bearing
ramet were significantly correlated (Table 3).
Acorn production by all species of oaks combined
within each association (Fig. 3) was correlated significantly with that in other associations (sandhill vs.
scrub, r = 0.79, P < 0.001; sandhill vs. scrubby flatwoods, r = 0.57, P = 0.004; scrub vs. scrubby flatwoods, r = 0.71, P < 0.001).
At least one oak species had modest acorn production
in every year. Consequently, there was no year of complete acorn failure in any association (Figs. 1, 2, and
3). The differences in trends and magnitude of annual
acorn production among species in part reflect the effects of external factors, most likely precipitation, acting on different stages of acorn development in a given
year as a consequence of the different reproductive
schedules of individual oak species
The patterns of variation over time suggest differences in the magnitude of year-to-year fluctuations at
different periods during the course of the study, with
greater fluctuations during the first and last thirds of
the 27-yr span than during the middle interval (Figs.
1 and 2). However, the differences were significant only
for the red oaks Q. myrtifolia and Q. laevis in sandhill,
with coefficients of variation for acorn production of
Q. myrtifolia of 80% for 1969-1979, 62% for 19801989, and 104% for 1990-1996 and for Q. laevis, 101,
51, and 88%, respectively (three-way ANOVA on species, F4,282= 23.3, P c 0.001; association, F2,282=
34.1, P < 0.001; and time period, F2,282 = 3.9, P =
0.02). Only the 1980-1989 and 1990-1996 periods
were significantly different ( P = 0.005) according to
Bonferroni post-hoc tests with adjustment for multiple
comparisons. The two-way interactions of species and
association (F5,282
= 4.6, P < 0.001) and species with
time period (F8,282= 3.1, P = 0.002) were significant,
as was the three-way interaction of species, association,
and time interval (Fi,,282= 3.4, P < O.OOl), suggesting
that the various oak species were reacting differently
according to association and time period.
Cycles of acorn production
Ten of the 12 species by association populations exhibited significant cyclical patterns in annual crop sizes
(Table 4). White oaks had shorter cycles of acorn production than did red oaks. Quercus chapmanii had significant 2-yr periodicities in sandhill and scrubby flatwoods but expressed a slightly longer 2.4-yr cycle in
light-limited scrub. Similarly, Q. geminata had a significant 2-yr cycle for annual crop size in scrubby flatwoods and a longer 2.4-yr periodicity in scrub. The red
oaks had periodicities ranging from 3 to 5 yr. For example, cycles for Q. Zaevis were 3.7 yr in sandhill but
4.4 yr in scrub. Quercus myrtifolia expressed 3.6 and
3.7-yr periodicities in scrubby flatwoods and sandhill,
respectively, but had a much prolonged 5.5-yr cycle in
the closed-canopy scrub.
Variation due to winter temperature
Of all temperature variables, minimum winter temperatures were predicted a priori to have the greatest
potential impact on acorn production through their effect on flower buds or immature stages of developing
acorns. January is the coldest of the winter months at
Archbold Biological Station and over the period of the
TABLE 4. The periodicities of cycles (yr) for annual acorn
production according to spectrum (Fourier) analysis
(Bloomfield 1976).
Sand pine
Species
White oaks
Q. chapmanii
Q. geminata
scrub
Sandhill
2**
3.INS
2.4**
2.4~~
Red oaks
Q. myrtifolia
Scrubby
flatwoods
2**
2x*
3.7**
5.5**
3.6*
Q. inopina
...
...
2.6NS
3.7**
4.4**
...
Q. laevis
Notes: The period shown is the highest periodogram peak
representing cycle length in years (Uhighest spectral density
frequency). Significance was tested by Barlett's Kolomogorov-Smirnov D (one-sample test).
* P 5 0.05; ** P 5 0.01; NS, not significant; ..., not applicable.
\
LONG-TERM ACORN PRODUCTION PATTERNS
September 2003
1201
cn
E
I
I
I
I
I
,
A
I
I
I
I
I
I
I
,
,
,
,
, \ ,
,
2485
,
,
,
,
,
,
,
,
-4- Scrubby flatwoods
-w-
Scrub
0
m
K
m
E"
FIG. 3. Summed mean numbers of acorns per ramet for all oak species occurring i n each of three xeric upland vegetative
associations in south-central Florida over the 28-yr period 1969-1996 (no observations were made in 1991).
study accounted for 68.3% (P< 0.001) of the variation
in minimum winter temperature compared with 12.6%
(P < 0.01) for December (stepwise multiple regression
of December, January, and February minimum temperatures vs. the three-month combined mean). The
most severe freeze in the 27 yr of monitoring occurred
in December 1989, with the lowest minimum temperature (-7.8"C) recorded from 1932 to 1998.
Correlations were calculated between mean numbers
of acorns per ramet and mean minimum temperatures
in December, January, and February and for the three
months combined (winter) with up to 3-yr lags for each
oak species across associations. No correlations were
significant after significance levels were adjusted by a
sequential Bonferroni procedure to ensure contrastwide significance of at least P = 0.05. This finding
suggests the absence of a linear relationship between
patterns of acorn production and winter temperatures.
However, winter temperatures may have a threshold
effect on acorn production (when freezing temperatures
kill reproductive tissues) rather than a linear effect. The
unusually severe freeze in December 1989 did consid' erable damage to a number of woody plants in the
region, including at least two native species (Ximenia
americana and Licania michauxii), two exotics (Melquinquenervia and Schinus terebinthifolius),
ltivated citrus (Citrus spp.). Nevertheless, the
only oak species observed with frost damage was Q.
chapmanii in low-lying areas, and the level of acorn
production by this species in the autumn following the
freeze was the third highest in the 27 yr of monitoring.
Quercus geminata also produced above average numbers of acorns in autumn 1990. These results suggest
that south-central Florida winter temperatures have little impact on acorn production by scrub oaks.
Variation in acorn crop size correlated
with precipitation
Annual precipitation on the Florida peninsula is
highly variable. Extreme amounts at Archbold Biological Station during the period of our study (1968-1996)
were 1643 mm during 1969 and 930 mm in 1980. Mean
precipitation was 1318 2 33 mm with the majority
(58%) of the total annual precipitation falling during
the four-month summer wet season (June through September). Mean rainfall during our study was below the
long-term mean (65 yr, 1932-1997, less 1941) of 1357
t 29 mm. The cumulative departure of annual rainfall
(the sum of the yearly departures from the 65-yr mean)
in the study area during the 1942-1996 period increased from a cumulative deficit of - 213 mm in 1942
to a peak of + 1825 mm in 1960, remained high (+ 1387
to +1819) until 1970, declined to +64 mm by 1991,
and varied from -1-215 to +450 mm from 1992-1996.
Thus, the major portion of the study occurred during
the period of a pronounced decline in cumulative departure of annual rainfall from the long-term mean.
Regardless, the long-term record of acorn production
showed no significant trend related to the marked decline in cumulative rainfall for any species or association (Figs. 1, 2, and 3).
Monthly precipitation is also highly variable on the
Florida peninsula. For example, January, a dry-season
month, had only 2 mm of precipitation in 1976 compared with 203 mm just 3 yr later; and rainfall in September, a wet-season month, ranged from 363 mm in
1979 to only 18 mm in 1996.
Our examination of annual acorn production and precipitation found a number of significant correlations of
numbers of acorns per ramet in different species and
associations with monthly or seasonal precipitation
(Table 5), which suggests that precipitation affects re-
Ecology, Vol. 84, No. 9
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
2486
TABLE 5. Pearson correlations of natural-log-transformed mean numbers of acorns per ramet with natural-log-transformed
precipitation variables lagged up to 3 yr for species across associations.
Red oaks
Q. myrtifolia
Rainfall
variable
Annual
Jan
Feb
Mar
Jul
Oct
Jan-May
Feb-Apr
Mar-Apr
Jun-Aug
Jun-Sep
Sep-Jan
Oct-May
Dec-May
Sandhill
Scrub
Scrubby
flatwoods
Q. inopina
Q. laevis
Sandhill
Scrub
-0.49 (-3)
0.43 (-I)
-0.47 ( - 3 )
Scrubby
flatwoods
0.65 (-2)
0.55 (-2)
-0.58 (-2)
-0.56 (-2)
0.60 (0)
0.61 (- 2)
0.64 (-3)
-0.47 (-2)
-0.57 (-3)
-0.54 (-3)
0.48 (-3)
-0.58 (-3)
-0.56 (-3)
Notes: Correlations shown in bold were significant after a sequential Bonferroni procedure to ensure significance of at
least P = 0.05 within a species in a given association (Rice 1989). Other correlations shown were initially significant at
least at P 5 0.01 prior to the sequential Bonferroni procedure. These latter values are reported only to help identify precipitation
variables that may be useful predictors of acorn production given that 85 correlations were performed for each species within
a given association. The number of years lagged is shown for each coefficient in parentheses. N = 27 for each correlation,
except N = 24 for Q. myrtifololia and Q. inopina in scrubby flatwoods.
production in scrub oaks. Acorn production by the red
oak Q. laevis had the greatest number o f sequentialBonferroni-determined significant correlations with
precipitation. Numbers of acorns per ramet were negatively associated with wet season (July) rainfall two
years previous and with rainfall during the dry season
(October through May) three years previous in each
association where this oak occurred. Similarly, the
combined acorn crops of Q. laevis from all associations
correlated negatively with wet season (July) rainfall
two years previous (-0.58) and with dry season rain
lhree years previous (October through May, -0.59; December through May, -0.56).
Acorn production for Q. inopina, which occurs only
in scrubby flatwoods, was positively correlated with
spring (February through April) rainfall two years previous, with the months of February and March showing
the strongest effects. Acorn crops of Q. myrtifolia were
positively correlated with the previous October’s rainfall in scrub and with June through August precipitation
three years previous in sandhill and for all associations
combined (0.56).
Acorn production of the white oak Q. chapmanii was
positively correlated in at least one association with
rainfall during the preceding late dry season (March)
and negatively with rainfall during the preceding July.
Acorn production by this oak in all associations combined was positively correlated with precipitation during the preceding dry season (October through May,
0.59; February through April, 0.55; March through
April, 0.56). Similar to Q. chapmanii, the other white
oak Q. geminata showed a negative relationship with
the previous year’s July rainfall in scrub and a positive
correlation with September rainfall one year previous
(0.60) when all associations were combined.
Regression models of crop size and precipitation
Because annual acorn production of individual species was typically correlated across associations, we
used stepwise multiple regressions to predict the numbers of natural-log-transformed acorns per ramet for
each of the five oaks in combined association samples
employing precipitation variables found significant in
the correlation analyses (but prior to the sequential
Bonferroni adjustment) (Table 6). Models for four oaks
explained 44-74% of the variation in acorn crop size,
however, the model for Q. myrtijolia explained only
29% of the crop-size variation. The fact that 1 1 different precipitation variables loaded into the five models suggests complexity in the interactions of precipitation with acorn crop sizes. But then again, some of
the variables used in the models for different oaks are
correlated with one another (e.g., annual rainfall one
year previous with October through May rainfall three
years previous, I = -0.61, P = 0.001). Furthermore,
the timing of events in reproductive development (e.g.,
flower initiation, anthesis) in red 17s. white oak species
differs substantially, as does the reproductive phenology of even closely related oaks within the same section (Q. inopina and Q. myrtifolia, Johnson and Abrahamson 1982). Consequently precipitation at various
times could have markedly different results depending
on the oak species.
The annual acorn production of red vs. white oak
species reacted as would be predicted from their respective reproductive biologies to precipitation. Acorn
September 2003
LONG-TERM ACORN PRODUCTION PATTERNS
2487
TABLE 5. Extended.
Q. chapmanii
Q. geminata
Sandhill
Scrub
Scrubby
flatwoods
0.46 (0)
0.53 (0)
0.44 (0)
0.48 (0)
-0.58 (- 1)
-0.45 (-1)
0.61 (-1)
-0.51 (-1)
SandhilL
Scrub
-0.58 (-1)
0.46 (0)
0.45 ( 0 )
0.52 (0)
0.47 (0)
0.46 (0)
0.44 (0)
0.48 (0)
Scrubby
flatwoods
0.53 (0)
0.48 (0)
0.42 (0)
0.45 (0)
production of white oaks was more frequently related
to precipitation one or two years previous whereas red
oak acorn production was more frequently related to
precipitation two or three years previous. For example,
previous-year precipitation variables accounted for
40% of the measures used in models for white oaks as
compared with 14% in red oak production models,
whereas precipitation variables three years previous accounted for only 20% of the measures entered into
models for white oaks versus 43% for red oak models.
In summary, the patterns of correlations and multiple
regression models for acorn production and precipitation, which influence ground water availability and
ultimately the moisture status of individual oak ramets,
differed among oak species and to a lesser extent vegetative associations. The variability in the effects of
both amount and timing of precipitation on acorn production among species and associations, probably reflects, in part, innate species-specific differences in water requirements, as well as differences among vegetative associations in such factors as soil type, development of the litter layer, relative humidity, and air
flow that in turn affect soil moisture. However, the
correlations and models broadly agree with predictions
of the effect of precipitation on acorn production based
on the reproductive biology of the oaks.
DISCUSSION
Crop sizes
There was no year of complete acorn crop failure
during the 27 yr of monitoring. At least a modest acorn
crop was produced each year by one or more oak species. This relationship is reflected in the lower cvs of
total acorn production in sandhill (54%), scrub (64%),
and scrubby flatwoods (66%) compared to the ranges
for individual species within each association (8 1102%, 84-105%, and 63-1 lo%, respectively). Such
differences in the annual yields of different species in
0.44 (0)
0.43 (0)
0.44 (0)
a given year are likely a consequence of the phenological differences in reproductive biology among oak
species, and especially of the differences between
members of the white versus red oak sections of Quercus. Such variations in annual acorn crops in mixed
oak species stands have been documented in several
other studies (e.g., Beck and Olson 1968, Goodrum et
al. 1971, and Beck 1977).
Coefficients of variation for annual acorn crops in
our study ranged from a low of 63% for Q. chupmanii
to a high of 110% for Q. myrtifolia in scrubby flatwoods, with an overall mean for all species in combined associations of 89% (Table 2 ) . Reviews of seedcrop variation data sets by Herrera et al. (1998), Koenig
and Knops (2000), and Kelly and Sork (2002) indicate
that the cvs we determined for the shrubby Florida
oaks are low. Furthermore, these cvs are relatively low
compared to those for other Quercus species (see Fig.
1 of Kelly et al. 2000). The reduced crop-size variation
found in our study may result from the small size of
the shrub-sized ramets and the consequent low numbers
of acorns produced per ramet.
Acorn production was related to vegetation association. Mean numbers of acorns of species growing in
scrub were consistently reduced compared to levels in
sandhill or scrubby flatwoods. We suspect that this reduction is a consequence of the reduced light availability in scrub. Canopy coverage is nearly complete
in scrub as a consequence of the dense overstory of
Pinus clausa, which translates into scrub having the
lowest available light of the associations studied (Abrahamson and Rubinstein 1976, Abrahamson et al. 1984,
Abrahamson 1995, 1999). Sandhill is intermediate in
canopy coverage and hence light level, and scrubby
flatwoods is the most open canopied of the three associations studied. However, in spite of the variations
in environmental conditions across vegetation associations, individual oak species exhibited a moderate de-
'
Ecology, Vol. 84, No. 9
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
2488
TABLE 6. Stepwise multiple linear regression models of natural-log-transformed numbers of
acorns per ramet for each oak species (all associations combined) ( Y ) using the natural-logtransformed precipitation variables found significant for the given oak species in the correlation analyses (significance prior to the sequential Bonferroni procedure).
Species
White oaks
Q. chuprnanii
Q. geminata
Red oaks
Q. myrtifolia
Q. luevis
Q. inopina
Equation
ANOVA
Y = -0.17X1 i: 0.19X2 - 0.10X3 + 4.54
v2 = 0.60
Y = -0.1.5X3 + 0.15X4 + 2.17
rz = 0.44
F3,23= 11.5, P < 0.001
Y = O.O7X, + 1.66
r2 = 0.29
Y =- -0.16X6 - 0.16X7 - 0.06X8 + 5.19
r2 = 0.65
Y = O.llX, + O.O7X,,
O.O5X,, - 5.39
rz = 0.74
F,,, = 9.2, P
F*,= = 9.4, P = 0.001
F3,3
+
=
=
0.006
14.2, P < 0.001
F3,20= 19.2, P < 0.001
Notes: Variables are shown in order of their entry into the regression model. XI, July rain
1 yr previous; X,, April rain 3 yr previous; X,, September rain 2 yr previous; X,, September
rain 1 yr previous; X,, July-August rain 3 yr previous; X,, July rain 2 yr previous; X,, August
rain 2 yr previous; X,, October-May rain 3 yr previous; X,, February-April rain 2 yr previous;
XI,, June-September rain 3 yr previous; XI,, annual rain 1 yr previous.
\
gree of synchrony from association to association. For
these shrubby oaks living in a region of highly seasonal
and variable precipitation, such synchrony likely results from similar responses to environmental factors
that influence acorn production.
Temperatures, precipitation, and crop sizes
There was no evidence that low winter temperatures
affected the acorn crop via either linear or threshold
influences on developing flower buds or acorns. This
finding may reflect the relatively infrequent occurfence
and very short duration Of below-freezing temperatures
at our south-central Florida study site.
In contrast, there was substantial evidence that precipitation levels during specific time periods influenced
the acorn
sizes Of the shrubby oaks. The particular
combination of precipitation variables correlated with
acorn production vaned by species but accounted for
74% of crop-size variation in Q. inopina and 65, 60,
and 44% for Q. laevis, Q. chapmanii, and Q. geminata
respectively (Table 6 ) . Previous studies involving a
number of woody species have also identified weather
variables conelated with crop sizes (e.g., Sork et al.
1993, Crawley and Long 1995, Dominguez and Dirzo
1995, Cecich 1997, Cecich and suliivan 1999, ~~~l~
1999, and Shibata et al. 2002). However, other studies,
even with oaks, have shown little or no correlation of
crop sizes with weather variables. Koenig et al. (1994,
but see Koenig et al. 1996) and Goodrum et al. (1971),
for example, found little evidence of weather effects
on acorn production.
The fact that precipitation variables correlated with
acorn production for the shrubby Florida oaks may be
a consequence of the high variability in annual and
monthly rainfall on the Florida peninsula and sandy
soil substrates. Limited amounts of rainfall during the
winter dry season lead to drought stress (Menges and
Gallo 1991, Abrams and Menges 1992, Menges 1994),
which in turn may influence oak flowering ih the current or a subsequent year. The combination of highly
variable annual and seasonal precipitation with excessively well-drained, nutrient-poor sandy soils likely
cause rainfall events to have unusually profound effects
on the remoduction of these shrubby oaks.
Differ&ces in the reproductive phenologies (e,g.,
Johnson and Abrhamson 1982) and endogenous reproductive cycles of oak species likely interact in v ~ ious ways with external factors such as precipitation,
soil-moisture availability, and/or canopy coverage to
generate patterns of annual acorn production that vary
from oak species to species
associations. As a
consequence, we should expect the
that the
influencesof
on acorn production differed con by oak species. Furthermore it is possible that
siderably
correlates of precipitation such as ground-water availability, rather than precipitation per se, may be more
strongly coupled to acorn production because of a tighter link with plant water relations. Thus, the effect of
On acorn production at a
a given amount Of
given point in the reproductive cyc1e
vary from
site to site depending on the root water uptake, which
in turn is
to soil type. surface drainage, development of litter layer, competition with other plants,
and Other
factors.
Whether the precipitation correlates identified in our
study affect staminate andlor pistillate flower initiation,
rates of pollination, fertilization rates and/or rates of
acorn abortion await experimental testing. Nevertheless, the correlations that were identified suggest that
precipitation at particular times may influence specific
stages in the acorn production cycle and point the way
for subsequent experimental studies. High rainfall during the summer wet season may influence the initiation
September 2003
LONG-TERM ACORN PRODUCTION PATTERNS
of pistillate flowers, the maturation of acorns, and rates
of acorn abortion while abundant precipitation during
the previous winter and spring dry season may affect
staminate flower initiation, flowering, pollination, and
ovule fertilization. For example, the negative correlations of July rainfall, a wet-season month, with acorn
production in the red oak Q. laevis and the white oaks
Q. chapmanii and Q. geminata suggest that July rainfall
can impact pistillate flower initiation. But to more fully
understand the impacts of precipitation on acorn production, we need to know how rainfall in different seasons affects root water uptake profiles, water stress,
carbon gain, and different stages in the reproductive
cycle from flower bud initiation to mature acorn. Experimental studies comparing control plants that receive ambient levels of rainfall with ramets supplemented with irrigation at prescribed times would aid
in developing models that more accurately describe and
predict oak reproductive responses to rainfall.
The variability of both rainfall and acorn production
as well as the effects and interactions of current and
historical environmental factors (e.g., ground-water reserves) that may potentially influence plant productivity greatly complicate teasing out any relationships between climate variables and seed production. Because
the production of an acorn crop requires two years for
white oaks and three years for red oaks, optimal weather conditions throughout the duration of acorn development probably occur only periodically in the xeric
upland associations in this study. Thus, a favorable
effect of weather conditions on one stage of the acorn
development cycle, such as flower bud initiation, may
be cancelled out by unfavorable conditions at a later
stage, such as fertilization or acorn maturation. Similarly unfavorable conditions at the time of flower bud
initiation cannot be fully compensated by favorable
conditions at the time of fertilization. Despite the complex interactions of factors potentially influencing
acorn production that may tend to obscure the influence
of weather, unusually favorable or unfavorable weather
conditions may periodically synchronize production in
all species, as suggested by our data for the period
1994-1996 (Figs. 1 and 2).
Weather may cue high seed years by providing favorable conditions for reproduction (Smith et al. 1990,
Lalonde and Roitberg 1992, Waller 1993, Kelly 1994,
McKone et al. 1998, Shibata et al. 2002). For example,
the occurrence of favorable weather conditions promotes greater photosynthate production andlor less
stressful conditions that enable plants to produce more
fruits (Sork et al. 1993). For the shrubby oaks in our
study, when acorn production was correlated with precipitation of the current year the relation was positive
and typically involved rainfall during the winter and
spring dry season (Table 5). Furthermore, the majority
of these correlations occurred in the white oaks, Q.
chapmanii and Q. geminata, with shorter reproductive
cycles than red oaks. Annual acorn crops of the red
2489
oaks were more often correlated with precipitation two
or three years earlier, suggesting a stronger influence
of precipitation on early stages of flower development.
\
Endogenous cycles and external influences
The length of our 27-yr data set enabled us to use
spectrum (Fourier) analyses to discover evidence of
regular cycles of acorn production that ranged from 2
to 2.4 yr for white oak species and from 3.6 to 5.5 yr
for red oak species. The regular reproductive cycles
identified for each oak match well with predicted periodicities based on differences in the reproductive biology of white vs. red oak species. However, the annual
acorn production patterns in this study suggest that the
intrinsic reproductive rhythms of these shrubby oaks
are influenced by the effects of external factors including resource limitation (Le., light and nutrient
availability) and rainfall, each of which can affect carbon storage (Campbell and Valentine 1972, Gdttschalk
1990, Lalonde and Roitberg 1992, Sork et al. 1993,
Waller 1993, McKone et al. 1998, Keeley and Bond
1999, Abrahawon and Layne 20024 b). The cycles of
annual acorn production for a given- oak species, for
example, were consistently longer in light-limited
scrub than compared to more open-canopied sandhill
and scrubby flatwoods.
Plants in less productive habitats are expected to
show more pronounced masting because lower productivity increases the time required to accumulate resources between high seed crops (Kelly and Sork
2002). If true, resource limitation in Florida’s xeric
uplands shouId foster years of low vs. high acorn production given the very low productivity due to the nutrient-poor conditions and water stress during the winter dry season (Abrahamson et al. 1984, Abrahamson
and Hartnett 1990, Myers 1990, Menges and Gallo
1991, Abrams and Menges 1992, Menges 1994, 1999).
The lifetime fitness of plants growing in resource-limited environments, such as these oaks, would likely
increase if reproduction during less favorable times is
postponed in order to survive unfavorable conditions,
gain vegetative mass to facilitate greater future reproductive output, or accumulate the resources necessary
to produce a more sizeable fruit crop in a subsequent
year (Abrahamson and Gadgil 1973, Abrahamson
1979, Waller 1979, Silvertown 1980, Sork 19936, Sork
et al. 1993). Indeed, an examination of biomass allocation in Q. inopina, the most clonal of the five oaks
studied, found that on average only - 25% of each ramet’s mass is allocated to aboveground organs (Johnson et al. 1986). This allocation pattern is one that
implies the importance of mass accumulation and longevity. However, in spite of the potential selective advantages, the shrubby oaks in our study show low cvs
in acorn production compared to other species including tree-size oaks. It is possible that the small stature
of these shrubby oaks limits the extent of variation
possible.
2490
WARREN G. ABRAHAMSON AND JAMES N. LAYNE
Must-seeding hypotheses
.
A comparison of the acorn production patterns for
these Florida shrubby oaks with the predictions of the
several hypotheses generated to explain supra-annual
variation in crop sizes suggest that several of the hypotheses can be rejected. For example, the relatively
low level of inter-annual crop variability in these Florida shrub oaks suggests that predator satiation, which
states that large intermittent seed crops reduce losses
to seed predators, is an unlikely significant factor driving crop-size variability. Furthermore, the synchronization of acorn production that we identified within
white oak species and within red oak species when
coupled with differences in periodicities of annual
acorn yields among oak species resulted in at least
moderate-sized seed crops each autumn of our 27-yr
study.
Likewise. our data do not support the animal-dispersal hypothesis in which the level of functional response by animal-dispersal agents should be higher in
years of large seed crops. The vertebrates that disperse
acorns via scatter or larder hoarding ’have relatively
stable populations in xeric Florida uplands that interact
with acorn crops year-after-year and there is no evidence to suggest that acorn predators differ appreciably
by oak species. The importance of acorns as winter
food to scatter-hoarding scrub jays, for example, suggests that they collect and cache a high proportion of
the seed crop each year regardless of crop size
(DeGange et al. 1989). Consequently, the acorn crops
of these mixed oak communities experience relatively
high predation/dispersal each year.
Our observations also suggest rejecting the environmental-prediction hypothesis in which large crops represent the prediction of optimal years for seedling survival. Acorn germination and seedling establishment
are generally rare events in these xeric upland associations and do not appear to vary with crop size (Abrahamson and Layne 2002a, b).
Our findings agree most closely with the non-adaptive explanation of the resource-matching or weathertracking hypothesis in which seed-crop sizes mirror the
availability of resources. The extent of acorn crop reduction in light-limited associations and the correlations of precipitation at various periods with acorn crop
sizes suggest that light and water availability at crucial
times can influence any or several of the reproductive
stages from flower bud initiation to mature acorns.
Thus, our findings suggest that variation in the sizes
of annual seed crops in Florida’s shrubby oaks results
from interactions of their intrinsic reproductive cycle
with extrinsic environmental factors as soil nutrients,
light availability, and weather variables and points up
the need to focus on both the ultimate and proximate
causes of seed-crop variation. Testing these conclusions will require detailed knowledge of the interaction
of light, rainfall, and other environmental variables
Ecology, Vol. 84, No. 9
with such factors influencing acorn production as root
water uptake, ramet water stress, ramet carbon gain,
flower production, pollen flow, pollination, fertilization, seed abortion, and seed predation. Experimental
studies in which quantitative reproductive data (e.g.,
timing of reproductive events, rates of pollen flow, pollination success, mortality of flowers, and immature
fruits) are collected along with measures of plant water
balance and potentially relevant environmental variables are needed to improve our understanding of reproductive synchrony in plants and its importance to
the evolution and ecology of plant reproduction. In
addition to the population-level results reported here,
studies that track the production of individual shrubby
oaks over time are needed to tease out the factors that
influence annual fluctuations in crop size.
The oak species in this study appear to be more dependent on clonal expansion than acorn production for
local population maintenance and expansion, as occursence of seedlings is rare and not related to the size
of the acorn crop in a given year (Givens et al. 1984,
Menges et al. 1993, Abrahamson and Abrahamson
1996b). The adaptive advantage of maintenance of
acorn production in these long-lived, clonal oaks in
relatively stable vegetation associations may be to facilitate long-distance dispersal via acorn-caching birds
and perhaps small mammals to sites with potential oak
habitats that are unoccupied or understocked. For example, C. S . Adkisson (personal communication) has
documented long-distance dispersal of acorns by Blue
Jays (Cyanocittu cristuta) from the sandhill in the vicinity of our study site to citrus groves > I km away,
with as many as 5000 nuts per bird being transported
in autumn. Florida Scrub Jays (Aphelocomu coerulescens) also often carry and bury acorns from oak-dominated associations to human-modified, oak-free sites
such as lawns, pastures, or grassy road-shoulders (R.
Bowman, personal communication); and we have observed long-term colonization of old fields adjacent to
our study area by oaks whose source could only have
been acorns transported by birds, most likely blue jays.
On a geological time-scale, acorn dispersal by animals
has no doubt played an important role in establishing
Florida’s shrubby oaks in primary bare sandy sites such
as dunes, former sand bars, and beaches created by
fluctuating sea levels during Pliocene and Pleistocene
glacial cycles.
ACKNOWLEDGMENTS
We especially thank Fred E. Lohrer and Chet E. Winegarner
for their long-term support of annual field surveys. J. F. Douglass, L. C. Layne, M. McCanley (Connor), A. Stinchfield, R.
D. Jennings, C. W. Harris, S . Craft, A. E Johnson, C. R.
Abrahamson, D. R. Smith, D. Fleck, P. A. Frank, K. R. Lips,
N. Stotz, S. Denton, and L. K. Harb provided additional field
assistance. We thank P. Heinrich for statistical advice and two
anonymous reviewers for their comments on earlier drafts.
The Archbold Biological Station and the Burpee Chair endowment of Bucknell University supported this work.
September 2003
LONG-TERM ACORN PRODUCTION PATTERNS
LITERATURE CITED
Abrahamson, W. G. 1979. Patterns of resource allocation in
wildflower populations of fields and woods. American Journal of Botany 66:71-79.
Abrahamson, W. G. 1995. Habitat distribution and compete neighborhoods of two Florida palmettos. Bulletin of
the Torrey Botanical Club 122:l-14.
Abrahamson, W. G. 1999. Episodic reproduction in two fireprone palms, Serenoa repens and Sabal etonia (Palmae).
Ecology 8O:lOO-115.
Abrahamson, W. G., and C. R. Abrahamson. 1989. Nutritional quality of biotically dispersed fruits in Florida sandridge habitats. Bulletin of the Torrey Botanical Club 116:
2 15-228.
Abrahamson, W. G., and C R. Abrahamson. 1996a. Effects
of fire on long-unburned Florida uplands. Journal of Vegetation Science 7:565-574.
Abrahamson, W. G., and J. R. Abrahamson. 19966. Effects
of a low-intensity winter fire on long-unburned Florida sand
pine scrub. Natural Areas Journal 16:171-183.
Abrahamson, W. G., and M. Gadgil. 1973. Growth form and
reproductive effort in goldenrods. American Naturalist 107:
651-661.
Abrahamson, W. G., and D. C. Hartnett. 1990. Pine flatwoods
and dry prairies.'Pages 103-149 in R. L. Myers and J. J.
Ewel, editors. Ecosystems of Florida. University of Central
Florida Press, Orlando, Florida, USA.
Abrahamson, W. G., A. F. Johnson, J. N. Layne, and P. A.
Peroni. 1984. Vegetation of the Archbold Biological Station, Florida: an example of the southern Lake Wales Ridge.
Florida Scientist 47:209-250.
Abrahamson, W. G., and J. N. Layne. 2002~.Post-fire recovery of acorn production by four oak species in southern
ridge sandhill association in south-central Florida. American Journal of Botany 89:119-123.
Abrahamson, W. G., and J. N. Layne. 2002b. Relation of
ramet size to acorn production in five oak species of xeric
upland habitats in south-central Florida. American Journal
of Botany 89:124-131.
Abrahamson, W. G., and J. Rubinstein. 1976. Growth forms
of Opuntia compressa (Cactaceae) in Florida sandridge
habitats. Bulletin of the Torrey Botanical Club 103:77-79.
Abrams, M. D., and E. S. Menges. 1992. Leaf ageing and
plateau effects on seasonal pressure-polume relationships
in three sclerophyllous Quercus species in south-eastern
USA. Functional Ecology 6:353-360
Ballardie, R. T., and J. Whelen. 1986. Masting seed dispersal
and seed predation in the cycad Mucrozamia communis.
Oecologia 70: 100-105
Beck, D. E. 1977. Twelve-year acorn yield in southern Appalachian oaks. USDA Forest Service Research Note SE244.
Beck, D. E., and D. F. Olson, Jr. 1968. Seed production in
southern Appalachian oak stands. USDA Forest Service
Research Note SE-91.
Bloomfield, I? 1976. Fourier analysis of time series: an introduction. Wiley, New York, New York, USA.
Brooks, H. K. 1981. Physiographic divisions of Florida. Florida Cooperative Extension Service, Institute of Food and
Agricultural Science, University of Florida (map and
guide), Gainesville, Florida, USA.
Campbell, R. W., and H. T. Valentine. 1972. Tree condition
and mortality following defoliation by the gypsy moth.
USDA Forest Service Research Paper NE-236.
.
Cecich, R. A. 1997. The influence of weather on pollination
and acorn production. Pages 252-261 in K. W. Gottschalk
and S. L. C. Fosbroke, editors. Proceedings of the 10th
central hardwoods forest conference. USDA Forest Service
General Technical Report NE- 197.
2491
Cecich, R. A., and N. H. Sullivan. 1999. Influence of weather
at time of pollination on acorn production of Quercus alba
and Quercus velutina. Canadian Journal of Forest Research
29: 1817-1823.
Chen, E., and J. E Gerber. 1990. Climate. Pages 11-34 in R.
L. Myers and J. J. Ewel, editors. Ecosystems of Florida.
University of Central Florida Press, Orlando, Florida, USA.
Crawley, M. J., and C. R. Long. 1995. Alternate bearing,
predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83:683-696.
DeGange, A. R., J. W. Fitzpatrick, J. N. Layne, and G. E.
Woolfenden. 1989. Acorn harvesting by Florida Scrub
Jays. Ecology 70:348-356.
Dominguez, C. A., and R. Dirzo. 1995. Rainfall and flowering synchrony in a tropical shrub: variable selection on
the flowering time of Erythroxylum havanense. Evolutionary Ecology 9:204-216.
Downs, A. A., and W. E. McQuilkin. 1944. Seed production
of southern Appalachian oaks. Journal of Forestry 42:913920.
Givens, K. T., J. N. Layne, W. G. Abrahamson, and S. C.
White. 1984. Structural changes and successional relationships of five Florida Lake Wales Ridge plant communities. Bulletin of the Torrey Botanical Club 111:8-18.
Goodrum, P. D., V. H. Reid, and C. E. Boyd. 1971. Acorn
yields, characteristics and management criteria of oaks for
wildlife. Journal of Wildlife Management 35520-532.
Gottschalk, K. W. 1990. Gypsy moth effects on mast production. Pages 42-50 in C. E. McGee, editor. Proceedings
of the Workshop, Southern Appalachian Mast Management.
University of Tennessee, Knoxville, Tennessee, USA.
Healy, W. M., A. M. Lewis, and E. E Boose. 1999. Variation
of red oak acorn production. Forest Ecology and Management 116:l-11.
Herrera, C. M., I? Jordano, J Guitian, and A. Traveset. 1998.
Annual variability in seed production by woody plants and
the masting concept: reassessment of principles and relationship to pollination and seed dispersal. American Naturalist 152576-594.
Houle, G . 1999. Mast seeding in Abies balsamea, Acer saccharum, and Betula alleghaniensis in an old growth, cold
temperate forest of north-eastern North America. Journal
of Ecology 87:413-422.
Janzen, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465-492.
Janzen, D. H. 1976. Why bamboos wait so long to flower.
Annual Review of Ecology and Systematics 7:347-391.
Janzen, D. H. 1978. Seeding patterns of tropical trees. Pages
83-128 in P. B Tomlinson and M. H. Zimmerman, editors.
Tropical trees as living systems. Cambridge University
Press, Cambridge, UK.
Jensen, R. J. 1997. Quercus Linnaeus sect. Lobatae Loudon,
Hort. Brit., 385. 1830. Red or black oaks. Pages 447-468
in Flora of North America editorial committee, editors. Flora of North America North of Mexico. Oxford University
Press, New York, New York, USA.
Johnson, A. E, and W. G. Abrahamson. 1982. Quercus inopina: a species to be recognized from south-central Florida. Bulletin of the Torrey Botanical Club 109:392-395.
Johnson, A. E, and W. G. Abrahamson. 2002. Stem turnover
in the clonal scrub oak, Quercus inopina. American Midland Naturalist 147:237-246.
Johnson, A. E, W. G. Abrahamson, and K. D. McCrea. 1986.
Comparison of biomass recovery after fire of a seeder (Ceratiola ericoides) and a sprouter (Quercus inopina) species
from south-central Florida. American Midland Naturalist
116:423-428.
Keeley. J. E., and W. J. Bond. 1999. Mast flowenng and
semelparity in bamboos: the bamboo fire cycle hypothesis.
American Naturalist 154:383-391.
2492
WARREN G. ABRAHAMSON AND JAMES N. LAMVE .
Kelly, D, 1994. The evolutionary ecology of mast seeding.
Trends in Ecology and Evolution 9:465-470.
Kelly, D., D. E. Hard, and R. B. Allen. 2001. Evaluating the
wind pollination benefits of mast seeding. Ecology 82:117126.
Kelly, D., A. L. Harrison, W. G. Lee, I. J. Payton, P. R. Wilson,
and E. M. Schauber. 2000. Predator satiation and extreme
mast seeding in 11 species of Chionochloa (Poaceaej. Oikos 90~477-488.
Kelly, D., and V. L. Sork. 2002. Mast seeding in perennial
plants: why, how, where? Annual Review of Ecology and
Systematics 33:427-447.
Koenig, W. D., and J. M. H. Knops. 2000. Patterns of annual
seed production by northern hemisphere trees: a global perspective. American Naturalist 155:59-69.
Koenig, W. D., J. M, H. Knops, W. J. Carmen, M. T. Stanback,
and R. L. Mumme. 1996. Acorn production by oaks in
central coastal California: influence of weather at three levels. Canadian Journal of Forest Research 26: 1677-1683.
Koenig, W. D., R. L. Mumme, W. J. Carmen, and M. T.
Stanback. 1994. Acorn production by oaks in central coastal California: variation within and among years. Ecology
75~99-109.
Lalonde, R. G., and B. D. Roitberg. 1992. On the evolution
of masting behavior in trees: predation or weather? American Naturalist 139:1293-1304.
Matschke, G. H. 1964. The influence of oak mast on European wild hog reproduction. Proceedings of the Southeastern Association of the Game Fish Commission 18:3539.
NcCarthy, E. C., and J. A. Quinn. 1989. Within- and amongtree variation in flower and fruit production in two species
of Carya (Juglandaceae). American Journal of Botany 76:
1015-1023.
McKone, M. J., D. Kelly, and W. G. Lee. 1998. Effect of
climate change on mast-seeding species: frequency of mass
flowering and escape from specialist insect seed predators.
Global Change Biology 4:591-596.
Menges, E. S . 1994. Fog temporarily increases water potential in Florida scrub oaks. Florida Scientist 57:65-74.
Menges, E. S. 1999. Ecology and conservation of Florida
scrub. Pages 7-22 in R. C. Anderson, J. S. Fralish, and J.
Baskin, editors. The savanna, barren. and rock outcrop
communities of North America. Cambridge University
Press, UK.
Menges, E. S . , W. G. Abrahamson, K. T. Givens, N. P. Gallo,
and J. N. Layne. 1993. Twenty years of vegetation change
in five long-unburned Florida plant communities. Journal
of Vegetation Science 4:375-386.
Menges, E. S., and N. P. Gallo. 1991. Water relations of scrub
oaks on the Lake Wales Ridge. Florida Scientist 54:69-79.
Menges, E. S., and C. V. Hawkes. 1998. Interactive effects
of fire and microhabitat on plants of Florida scrub. Ecological Auulications 8:935-946.
Ecol&y, Vol. 84, No. 9
Moody, R. D. 1985. Mast production of certain oak species
in Louisiana. Proceedings of the Annual Conference of the
Southeastern Association of the Game and*Fish Commission 7:l-19.
Myers, R. L. 1990. Scrub and high pine. Pages 150-193 in
R. L. Myers and J. J. Ewel, editors. Ecosystems of Florida.
University of Central Florida Press, Orlando, Florida, USA.
Nixon, K. C., and C. H. Muller. 1997. Quereus Linnaeus
sect. Quercus. White oaks. Pages 471-506 in Flora of North
America Editorial Committee, editors. Flora of North
America north of Mexico. Oxford University Press, New
York, New York, USA.
Norton, D. A., and D. Kelly. 1988. Mast seeding over 33
,years by Dacyrdium cupressinum Lamb. (rimuj (Podocarpaceae) in New Zealand: the importance of the economies
of scale. Functional Ecology 2:399-408.
- .
Rice. W. R. 1989. Analyzing
- - tables of statistical tests.- Fvolution 43:223-225.
Shibata. M.. H. Tanaka. S . Iida. S. Abe, T. Masaki, K Nii- .__
yarna; and T. Nakashizuka. 2002. Synchronized annual
seed production by 16 principal tree species in a temperate
deciduous forest, Japan, Ecology 83: 1727-1742.
Silvertown, J. W. 1980. The evolutionary ecology of mast
seeding in trees. Biological Journal of the Linnean Society
14:235-250.
Smith, C. C., .J. L. Hamrick, and C. L. Kramer. 1990. The
advantage of mast years for wind pollination. American
Naturalist 136:154-166.
Sork, V. L. 1983. Mast-fruiting in hickories and availability
of nuts. American Midland Naturalist 109:81-88.
Sork, V. L. 1993a. Mammalian seed dispersal of pi'gnut hickory .during three fruiting seasons. Ecology 64: 10491056.
Sork, V. L. 1993b. Evolutionary ecology of mast-seeding in
temperate and tropical oaks (Quercus sp,p.). Vegetatio 1071
108:133-147.
Sork, V. L., J. Bramble, and 0. Sexton. 1993. Ecology of
mast-fruiting in three species of North American deciduous
oaks. Ecology 74:528-541.
Tapper, P. G. 1996. Long-term patterns of mast fruiting in
Fraxinus excelsior. Ecology 77:2567-2572.
Vander Wall, S . B. 2002. Masting in animal-dispersed pines
facilitates seed dispersal. Ecology 83:3508-35 16.
Waller, D. M. 1979. Models of mast fruiting in trees. Journal
of Theoretical Biology 80:223-232.
Waller, D. M. 1993. How does mast-fruiting get started?
Trends in Ecology and Evolution 8:122-123.
Wolgast, L. J. 1972. Oak mast production in scrub oak (Quercus ilicifolia) on the coastal plain in New Jersey. Final
Report, Project Number W-48-R, New Jersey Department
of Fish, 'Game, and Shell Fisheries, Trenton, New Jersey,
USA.
Wolgast, L. J., and B. B. Stout. 1977. Effects of age, stand
density, and fertilizer application on bear oak reproduction.
Journal of Wildlife Management 41:685-69 1.
Yamauchi, A. 1996. Theory of mast reproduction in plants:
storage-size dependent strategy. Evolution 50:1795-1805.