Timing of Flowering and Seed Production in
Three California Oaks1
Walter D. Koenig,2 Johannes M.H. Knops,3 and William J. Carmen4
Abstract
We examined the importance of pollen limitation to variation in acorn production of three
species of California oaks (Quercus lobata, Q. douglasii, and Q. agrifolia) by testing for
relationships between phenology and acorn production. Within years, trees flowering closer to
the mean flowering date of the population produced significantly more acorns in two of the
species. Assuming that more pollen is available when more conspecifics are blooming, this
result is consistent with pollen limitation affecting individual variation in acorn productivity.
Across years, relatively warm, dry conditions during the peak of flowering correlated with
larger acorn crops the following fall in all three species. Assuming that such conditions favor
either increased pollen movement or increased fertilization, this is consistent with the
hypothesis that pollen limitation plays a significant role in the highly variable seed crops
characteristic of masting in these species. Overall, the proportion of total variance in the acorn
production of individual trees explained by these two indices of pollen availability ranged
from 28 to 38 percent. These results support the hypothesis that pollen limitation plays an
important role in causing variance in seed production in these wind-pollinated oaks.
Keywords: Acorn production, masting, phenology, pollen limitation.
Introduction
Wind-pollinated trees cover huge areas throughout temperate and boreal regions and
have vast economic and environmental importance. Many wind-pollinated trees are
also notable for producing seed crops that combine high variability among
individuals within years, high variability among years, and synchronized production
over large geographic areas, the latter two features characterizing masting or mastseeding (Norton and Kelly 1988; Koenig and Knops 1988; Kelly and Sork 2002).
Of central interest is the role that pollen limitation plays in these phenomena.
Theoretical models have demonstrated that pollen limitation, in conjunction with
environmental fluctuations, can potentially play a pivotal role in producing highly
variable and synchronized patterns of seed production in wind-pollinated species
(Satake and Iwasa 2000, 2002). Empirically, prior work has found that weather
conditions during flowering can have a significant influence on subsequent seed
production in various wind-pollinated trees (Sharp and Sprague 1967; Sork and
others 1993; Koenig and others 1996; Koenig and Knops 2002), a finding that is
likely to be due to effects of weather on pollen flow, although this has yet to be
1
An abbreviated version of this paper was presented at the California Oak Symposium: Today’s
Challenges, Tomorrow’s Opportunities, October 9-12, 2006, Rohnert Park, California.
2
Research Zoologist, Hastings Reservation and Museum of Vertebrate Zoology, University of
California Berkeley, 38601 E. Carmel Valley Road, Carmel Valley, CA 93924. e-mail:
koenigwd@berkeley.edu
3
Associate Professor, School of Biological Sciences, 348 Manter Hall, University of Nebraska, Lincoln,
NE 68588.
4
145 Eldridge Ave., Mill Valley, CA 94941.
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GENERAL TECHNICAL REPORT PSW-GTR-217
definitively demonstrated (Koenig and Ashley 2003). To the extent that similar
weather conditions affect all trees in a population, it is further possible that pollen
limitation plays an important role in masting behavior.
Pollen limitation may also play an important role in causing variation in seed
production among individuals within a population, as suggested by a correlation
between spacing and seed production in European beech (Fagus sylvatica) and yew
(Taxus canadensis) (Nilsson and Wästljung 1987; Allison 1990b), increased seed
production with the addition of supplemental pollen in low-density stands of yew
(Allison 1990a), and, more recently, a correlation between the number of pollenproducing neighbors and seed production in blue oaks (Quercus douglasii) (Knapp
and others 2001). These studies all suggest that some of the variation in seed
productivity among individuals may be due to differences in pollen availability.
Here we approach this issue by examining the relationship between flowering
phenology and subsequent acorn production in three species of California oaks with
the goal of estimating the potential importance of pollen limitation as a cause of
variation in acorn production. We also analyze the relationship between mean annual
acorn production and environmental conditions during the spring flowering period as
a measure of the potential importance of annual differences in pollen transfer in
determining year-to-year variability in acorn production.
Methods
Study Site and Species
We conducted the study at Hastings Reservation in central coastal California, where
we have long-term data on acorn production by oaks since 1980. Weather records
were taken from reserve headquarters, within 1.5 km and 100 m elevation of trees
included in the analyses. Species included in the study were Q. lobata (valley oak)
and Q. douglasii (blue oak), both members of the “white oak” subgenus Quercus, and
Q. agrifolia (coast live oak), a member of the “black oak” subgenus Erythrobalanus.
All three of these are “1-year species” requiring a single season to mature acorns.
Thus, acorns counted were in all cases fertilized the prior spring.
Acorn Survey
We estimated relative acorn abundance for 86 Q. lobata, 56 Q. douglasii, and 63 Q.
agrifolia every fall between 1980 and 2002 (23 years) using visual surveys conducted
in early September. At each tree, two observers scanned different parts of the canopy
and counted as many acorns as they could in 15 s. Counts were added and logtransformed to reduce the correlation between the mean and variance (Sokal and
Rohlf 1981). Details of these methods are given elsewhere (Koenig and others 1994a,
1994b; Garrison and others 2008).
Phenological Survey
We performed phenological surveys on a subset of 67 trees (25 Q. lobata, 23 Q.
douglasii, and 19 Q. agrifolia) during the six years from 1991 and 1996. We focused
on male flowers (catkins), which we visually surveyed weekly starting in early March
until the end of flowering in May. We recorded the date on which each tree was first
in bloom as indicated by the presence of pendant male catkins and expanded flower
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Timing of Flowering and Seed Production in Three California Oaks—Koenig
buds, the date on which each tree ended male flowering as indicated by the absence
of catkins shedding pollen, and the date when flowering peaked. Because female
flowers are cryptic, we did not survey them directly. In general, however, female
flowering in oaks is correlated with the period catkins are present, with the former
appearing 5 to 10 days after catkins (Sharp and Sprague 1967).
In order to look for a potential effect of pollen limitation on annual acorn
production, we extended prior analyses correlating overall acorn production with
environmental conditions during the main flowering period the prior spring,
specifically the month of April, during which 72 percent of flowering takes place in
this population (Koenig and others 1996). As a comparison of the relative importance
of pollen limitation vs. endogenous energy reserves in determining the mean annual
acorn crop, we performed multiple regressions of environmental conditions in April
and the prior year’s acorn crop on the current year’s acorn production.
Statistical Methods
We tested for consistency among the phenology of individuals across years using
Kendall’s coefficient of concordance. In order to test for pollen limitation within
years, we looked for a relationship between phenology and acorn productivity of
individual trees. Specifically, we assumed that there would be less pollen early and
late in the season and thus tested whether trees flowering in the middle of the season
produced more acorns than trees flowering early/late. We did this by using the
number of standard deviations before or after the mean date individual trees flowered
(the absolute value of standard deviation, |SD|) as a measure of how far from the
presumed peak of pollen availability each tree flowered, regardless of whether it
flowered earlier or later than the peak itself. We then performed ANOVAs with (logtransformed) acorns counted as the dependent variable, year as a main factor, and
|SD| as a covariate in order to test whether acorn production of individual trees was
influenced by phenology.
To compare the relative importance of conditions during pollination vs.
endogenous energy reserves related to the prior year’s crop, we compared the
significance and change in R2 values for regressions of the mean (log-transformed)
acorn crop on mean conditions during April and the prior year’s mean acorn crop
separately and together using all 23 years of data and all individuals surveyed on the
study site. We used analogous regressions of relative date of initial flowering and
mean maximum April temperature on the subsequent acorn crops of individual trees
combining the six years of phenological data to estimate the overall proportion of
variance in acorn production potentially explainable by pollen limitation.
Results
Variation in Flowering
For all species, the three phenology variables (date of first flowering, date of
maximum flowering, and last date of flowering) were highly correlated (nine
pairwise correlations, all rs > 0.70, all P < 0.001). Thus, except where noted, we
present only results using the date of first flowering.
Among years, the mean date of first flowering ranged from March 4 to 29 in Q.
lobata (26 days), March 3 to April 3 in Q. douglasii (31 days), and March 5 to April
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GENERAL TECHNICAL REPORT PSW-GTR-217
16 in Q. agrifolia (41 days). Within years, estimated date of first flowering among
individuals differed by 21 to 35 days in Q. lobata, 21 to 30 days in Q. douglasii, and
15 to 43 days in Q. agrifolia. Across years, however, all three measures of flowering
phenology were highly significantly concordant for all three species (nine tests,
Kendall’s W >0.44, all P <0.001). Thus, trees tended to flower in the same relative
temporal order from one year to the next, despite differences in flowering among
years.
Effect of Spring Conditions on Acorn Production
Across the entire 23 years of the study, the mean acorn crop was significantly
correlated with conditions during April, the peak of the flowering period, for both Q.
lobata and Q. douglasii, with larger acorn crops occurring in warmer and drier
springs (table 1). Spring conditions were not significantly correlated with acorn
production in Q. agrifolia. The prior year’s acorn crop was inversely correlated with
the current crop in all three species, significantly so for Q. lobata and Q. douglasii.
Table 1—Spearman rank correlations of the mean acorn crop vs. environmental conditions
during the prior April and the mean acorn crop the prior year1
Variable
Mean max. temp.
Mean min. temp.
Mean ave. temp.
Mean rainfall
Prior year’s crop
1
Q. lobata
(N = 86)
0.80***
0.60**
0.78***
-0.42*
-0.47*
Q. douglasii
(N = 56)
0.60**
0.43*
0.59**
-0.34
-0.50*
Q. agrifolia
(N = 63)
0.31
0.07
0.26
-0.01
-0.36
N = 23 years (22 for the prior year’s acorn crop). * P < 0.05; ** P < 0.01; *** P < 0.001
Using the environmental factor most strongly correlated with acorn production
(mean maximum April temperature), environmental conditions were far more
important as an explanatory variable of the current acorn crop than the prior year’s
acorn crop in both Q. lobata and Q. douglasii (table 2; neither variable was
significant for Q. agrifolia, which is not included in the table). Adding the prior
year’s acorn crop to a regression of the current acorn crop on mean maximum April
temperature increased R2 values by only 3.5 percent (Q. lobata) and 6.4 percent (Q.
douglasii), while adding the mean maximum April temperature to a regression of the
current acorn crop on the prior year’s acorn crop increased R2 values by 43.2 percent
(Q. lobata) and 33.3 percent (Q. douglasii)(table 2).
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Timing of Flowering and Seed Production in Three California Oaks—Koenig
Table 2—Results of multiple regressions examining the effects of mean maximum April
temperature and the (log-transformed) mean prior year’s acorn crop on subsequent mean
acorn production (N = 23 years)
Species (N
individuals)
Q. lobata
Prior year’s acorn crop only
Adjusted
R2
0.188
(86)
Mean max. April temp. only
0.585
Both variables
0.620
Model
Prior year’s acorn crop
Mean max. April temp.
t-value
P-value
2.4
0.025
5.5
<0.001
1.7
0.106
4.9
<0.001
Q. douglasii
Prior year’s acorn crop only
0.152
2.2
0.041
(56)
Mean max. April temp. only
0.421
4.0
0.001
Both variables
0.485
Prior year’s acorn crop
1.8
0.083
Mean max. April temp.
3.7
0.001
Individual Variation, Phenology, and Acorn Production
For Q. lobata and Q. agrifolia, but not Q. douglasii, timing of flowering relative to
the population at large was significantly related to subsequent acorn production by
individual trees after controlling for differences among years (table 3). In both
species where it was significant, acorn production increased as trees flowered closer
to the overall mean flowering date. However, the proportion of variance explained by
the timing of flowering was small in comparison to differences among years.
Compared to analyses in which year alone was included in the model, R2 values
increased by only 1.1 percent in Q. lobata and 1.3 percent in Q. agrifolia when
timing of flowering was included in the analysis. Timing of flowering did not
significantly correlate with subsequent acorn production without controlling for year.
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GENERAL TECHNICAL REPORT PSW-GTR-217
Table 3—Results of ANOVAs examining the effects of year and date of initial flowering
(relative to the overall distribution) on subsequent acorn production of individual trees using
the phenological subsample of trees, 1991–1996
Species (n
individuals)
Q. lobata
(25)
Adjusted R2
F-value (df)
P-value
Year only
0.474
27.9 (5,144)
<0.001
Flowering date only
0.002
1.3 (1,148)
0.26
Both variables
0.485
Year
28.7 (5,143)
<0.001
Flowering date
4.0 (1,143)
0.048
Model
Q. douglasii
Year only
0.356
16.2 (5,132)
<0.001
(23)
Flowering date only
0.000
0.5 (1,136)
0.49
Both variables
0.357
Year
16.2 (5,131)
<0.001
Flowering date
1.0 (1,131)
0.31
Q. agrifolia
Year only
0.598
34.6 (5,108)
<0.001
(19)
Flowering date only
0.015
2.7 (1,112)
0.10
Both variables
0.611
Year
35.4 (5,107)
<0.001
Flowering date
4.7 (1,107)
0.033
An estimate of the overall importance of pollen limitation at both the annual and
individual levels can be made by regressing acorn production of individual trees on
the relative date of flowering and mean maximum April temperature across the six
years of the study. Results indicate that 28.4 to 38.2 percent of the overall variance in
acorn production is potentially explained by pollen limitation (table 4). The majority
of this is due to the relatively high explanatory power of mean maximum April
temperature. After controlling for this variable, pollen limitation at the individual
level as indexed by date of initial flowering was only significant for Q. agrifolia.
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Timing of Flowering and Seed Production in Three California Oaks—Koenig
Table 4—Results of multiple regressions examining the effects of date of initial flowering
(relative to the overall distribution) and mean maximum April temperature on subsequent
acorn production of individual trees using the phenological subsample (N = 6 years)
Species
(N individuals)
Variable
R2
F-value
(df)
0.309
34.3 (2,147)
t-value
P-value
Q. lobata
Full model
(25)
Flowering date only
1.4
0.154
Mean max. April temp.
8.2
<0.001
0.284
<0.001
Q. douglasii
Full model
(23)
Flowering date only
1.0
0.33
Mean max. April temp.
7.5
0.001
0.382
28.1 (2,135)
<0.001
Q. agrifolia
Full model
35.9 (2,111)
<0.001
(19)
Flowering date only
2.0
0.045
Mean max. April temp.
8.2
<0.001
Discussion
Our results support the hypothesis that pollen limitation plays a role affecting both
individual and annual variation in acorn production. With respect to the former, Q.
lobata and Q. agrifolia trees flowering closer to the mean date of flowering produced
more acorns than those flowering either earlier or later than the peak. This is
expected if pollen is limited such that trees have greater pollination success and
subsequently produce more acorns if they flower when more conspecifics are
flowering as well.
However, our results also suggest that the role of pollen limitation, although
significant in two of the species, may be a relatively minor cause of differences in
acorn productivity. Annual differences, independent of environmental variation
during flowering (year), explained a far higher proportion of the variance in
individual acorn production than did differences in flowering phenology.
With respect to annual variation (masting), our results are consistent with prior
studies both in this population (Koenig and others 1996) and in other species in the
“white oak” subgenus (Sork and others 1993; Koenig and Knops 2002) that warm,
dry conditions during the spring flowering season correlate with subsequent acorn
production. In our data, such conditions were considerably more important than an
index of endogenous energy reserves (the prior year’s acorn crop) in predicting the
subsequent mean acorn crop using the complete 23-year dataset. Because the species
considered here produce mature acorns in a single year, this is consistent with pollen
availability playing an important role in determining the size of the acorn crop.
Although neither the prior year’s acorn crop nor mean maximum April
temperature was significantly related to mean annual acorn production in Q. agrifolia
using the complete dataset, results with this species nonetheless suggest a significant
role for pollen limitation using the six-year phenological subset of data, in which
both date of initial flowering and mean maximum April temperature were
significantly related to acorn production. Overall, about one-third of the total
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GENERAL TECHNICAL REPORT PSW-GTR-217
variance in acorn productivity among individuals and across years was explainable
by the two variables potentially indicative of pollen limitation. In all three species,
this was primarily due to the relationship between spring conditions and subsequent
acorn productivity.
The significance of pollen limitation within years supports the earlier finding of
Knapp and others (2001) that the number of conspecifics flowering within the
vicinity of individual trees correlates with subsequent acorn production, at least in
some years. Surprisingly, our support for this hypothesis did not come from Q.
douglasii (the species studied by Knapp), but rather from the other two species
studied here.
Our results also indicate that availability of locally-produced pollen may limit
reproduction in some species of California oaks, and thus are consistent with data
from Q. alba and Q. lobata that average pollen dispersal occurs on a very small
geographic scale (Smouse and others 2001; Sork and others 2002). Such small-scale
pollen dispersal implies that reproduction in oaks and possibly other wind-pollinated
species may be impaired by fragmentation or other alterations to the spatial structure
of their populations that reduces the availability of pollen. However, the small
proportion of variation between productivity explainable by phenological differences
among individuals does not preclude the possibility that considerable pollen flow
occurs over much larger distances, as indicated by parentage analysis using
microsatellite markers in several species (Dow and Ashley 1998a, 1998b; Streiff and
others 1999). Clearly this issue deserves additional study.
In contrast, a relatively large proportion of the variance in annual acorn
production by all three species appears to be due to differences in pollen availability
among years correlated with environmental conditions. As with the within-year
effects, the direction of the relationship implicates pollen limitation, as in all
significant cases crop size was greater when conditions were more favorable for
pollen flow. Primarily because of this relationship, up to 38 percent of total variance
in acorn productivity is explainable by factors potentially reflecting pollen limitation.
At the proximate level, this supports the hypothesis that differences in pollen
availability among years plays an important role in determining annual variability in
acorn production, either through fertilization or subsequent ovule development (Sork
and others 1993).
What remains unclear is the ultimate cause of this pattern. A close correlation
between environmental conditions favoring pollen dispersal and subsequent seed
production is predicted by the hypothesis that wind pollination is an important
driving force in the evolution of masting behavior, as suggested by several authors
(Smith and others 1990; Satake and Iwasa 2000, 2002). However, regardless of the
ultimate factors selecting for masting, trees are likely to be using some environmental
cue to synchronize reproductive effort. Thus, even if masting is exclusively an
adaptation to some other evolutionary challenge such as predation, a close correlation
between acorn production and the environment would be predicted. The fact that this
environmental variable is often one that is likely to have a strong influence on pollen
flow is consistent with, but not strong evidence for, wind pollination per se being an
important factor selecting for masting behavior in these species.
Regardless of the ultimate significance of the relationship between pollen
availability and masting, pollen limitation appears to play at least a small role in
causing differences in seed production among individuals and a larger role in
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Timing of Flowering and Seed Production in Three California Oaks—Koenig
producing differences in seed production among years, explaining as much as 38
percent of the overall variance in acorn productivity. Additional work is needed to
clarify the spatial dimensions of pollen flow in wind-pollinated trees and clarify the
role that pollen limitation plays in the evolution of masting behavior.
Acknowledgments
We thank Dick Sage, who suggested we examine the relationship between phenology
and acorn production, and the reviewers for their comments. We also thank Lisa
Gleboff for helping to collect the phenology data, Mark Stanback for his participation
in the acorn surveys, and Mary Ashley for commenting on the manuscript and
helping research the topic of pollen dispersal. Support was provided by the
University of California Integrated Hardwood Range Management Program and by
the National Science Foundation.
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