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REVIEWS
Experimental tests of sex-allocation
theory in plants
Diane R. Campbell
T
hree-quarters of flowering
A general explanation for diversity in plant
Estimating the parameters
plant species have hermaphbreeding systems is offered by sex-allocation
of fitness gain functions
roditic flowers; however, the
theory. This theory assumes a trade-off
The first choice in describing fitremaining species illustrate a
between allocation of resources to the two
ness gain functions is deciding
tremendous variety of breeding sexual functions. It explains the high frequency how to measure resource allosystems. These include not only
of hermaphroditism in angiosperms by
cation (r). In the classic form of the
separate sexes (dioecy), and popudiminishing fitness returns on investment of
model, r refers to the proportion
lations with unisex individuals
more resources in a single function. Recent
of resources invested by the plant
and hermaphrodites, but also sepexperimental studies provide tests of this
in stamens rather than in pistil or
arate unisex and hermaphroditic
theory by measuring male and female fitness
seed maturation2,3. More recent
flowers on the same individual.
gains, and examining the trade-off
elaborations separate allocation
This diversity has fascinated evoassumption. These studies show how fitness
at the time of flowering from seed
lutionary biologists for a long
responds to shifts in allocation. Allocation
production, to allow for differtime. Darwin1 noted that reduced
traits often show heritable variation, but
ences in the timing of investinvestment in one reproductive
support for a trade-off remains weak.
ment10 and/or to include allofunction could be compensated
cation to attractive structures,
for if it left additional resources
such as the corolla11. Furthermore,
Diane Campbell is at the Dept of Ecology and
for the other sexual function.
allocation can differ depending on
Evolutionary Biology, University of California, Irvine,
This idea of a trade-off in resource
whether it is measured in units of
CA 92697, USA ([email protected]).
use was elaborated in evolutionbiomass, carbon or nutrients, and
arily stable strategy (ESS) modon whether it takes into account
els developed by Charlesworth
photosynthesis and respiration
and Charlesworth2, Charnov3 and
by reproductive structures12,13.
4
Lloyd . According to this theory, the ESS sex allocation The shapes of the fitness gain functions will differ dependdepends on the shape of fitness gain functions relating ing on the currency chosen, unless different currencies
male and female fertilities to the proportion of resources have a linear relationship. Thus, it is problematical to
invested in male function (Box 1). One major dichotomy measure fitness gains as a function of one trait, such as
addressed by the theory is the distinction between dioecy flower number, and use that function to suggest the shape
and hermaphroditism. Although it was well understood of fitness gains for other traits, such as biomass allocation.
that separation of sexes could be favored by high selfing
This property should not interfere with the model’s
and inbreeding depression, this model illustrated another ability to predict an ESS for the currency chosen by the
selective mechanism that would also apply to outcrossing investigator, provided the underlying assumption of a
species. Accelerating fitness returns on investment of re- trade-off in allocation is met. However, different currencies
sources in a single sexual function would favor separate could lead to conflicting predictions about the stability of a
sexes, whereas diminishing returns on investment would breeding system. To describe sex allocation, an approfavor hermaphroditism. The theory had a major impact on priate measure is one comparing allocation to male strucplant reproductive biology, because it could explain diversity tures (e.g. stamens) with total allocation by the plant
of not only breeding systems but also resource allocation to female and male structures, using a currency, such as
within a population of hermaphrodites.
biomass, that shows a trade-off.
However, testing the theory proved difficult because
Another difficulty is presented by the need to estimate
the parameters are notoriously hard to estimate. Until re- male and female fitness in the field. Here, it is assumed that
cently, most tests relied on qualitative comparisons of investigators start by observing sex allocation in a mature
species. For example, selfing species were predicted to plant. For such a plant, production of offspring surviving to
show lower investment in male function than outcrossing reproductive maturity provides a reasonable index of fitspecies5,6. Furthermore, sex allocation was often expected ness, particularly for species without variation in age at
to depend on the size of an individual plant7.
reproduction. In natural populations, female fitness is usuRecent studies illustrate how to test the model experi- ally estimated by seed production. However, the shape of
mentally by estimating the fitness gains themselves. Devel- the female gain curve might be influenced by differential
opments in paternity analysis8 now permit estimation of success of seed crops that vary in size3. If seeds compete
relative male fertility, and studies of seedling stages permit with their siblings for a limited number of safe sites, this
more accurate estimation of realized female fertility9. local resource competition will saturate female fitness
These advances are leading to the first attempts to quan- gains (Box 2). The process requires low seed dispersal.
tify fitness gain functions. At the same time, quantitative Density-dependent population growth is not sufficient to
genetics has been applied to testing the basic assumption cause diminishing fitness gains (Box 2). To test for the
of a trade-off in allocation. This article revisits the evidence importance of this phenomenon we need to follow the sucfor sex-allocation theory, as applied to outcrossing plants, cess of offspring from individual plants and determine how
now that these new approaches are available.
many survive to reproduce.
TREE vol. 15, no. 6 June 2000
0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(00)01872-3
227
REVIEWS
likelihood to estimate male
fertilities from the set of
offspring genotypes and
Male fertility (m) (solid line) and female fertility (f ) (broken line) are considered power functions of the proportion of
resources put into male function (r):
genotypes of potential parents8,17,18. The goal is to obb
m = km r
f = kf (1 − r )c
tain estimates of relative
male fertilities that have low
bias and low variance. Alwhere km and kf are constants. An exponent (b or c) ,1 generates a function with diminishing returns, whereas an
exponent .1 generates accelerating returns. These exponents determine the evolutionarily stable strategy (ESS)
though adding sufficient loci
breeding system. (a) Both exponents b and c ,1, and the ESS is hermaphroditism. Plotting m versus f would lead
to exclude all but one genetto a convex (bowed out) fitness set. (b) Both b and c .1 corresponding to accelerating fitness gains, and the ESS
ically possible father of a
is dioecy.
seed is appealing19, sampling
(a)
(b)
more offspring is usually
b = 0.4, c = 0.6
b = 1.5, c = 2.5
easier and leads to a greater
kf
km
kf
km
reduction in sampling variance for a fixed total number
of assays20. One caution is
f
m
m
f
that with low exclusion probabilities, the likelihood estimation tends to underestimate the fitness of highly
successful males8. It remains
unclear how much this bias
alters the apparent shape of
the male gain curve. Studies
taking this approach should,
therefore, attempt to estimate the bias through com0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
puter simulation21,22. Another
r
r
potential source of bias that
Proportion of resources to male function
(Online: Fig. I)
could flatten the male gain
Trends in Ecology & Evolution
curve is cryptic gene flow17.
The fitness of a rare mutant i is the average of its relative female and male fertilities, and can be written as37:
This refers to siring of seeds
by a plant from outside the
mi
wi = f i + f
reference population that
m
goes undetected because a
where f and m are average female and male fertilities in the whole resident population. Substituting the power
genetically possible father
functions into this expression yields:
also exists inside the population. It is possible to eliminkmrib
c
c
wi = kf (1 − ri ) +
k (1 − r )
b f
ate bias as a result of cryptic
kmr
gene flow by simultaneously
The ratio rib/rb expresses the fraction of seeds in the population as a whole that are sired by the mutant. Following
estimating gene flow and
standard techniques4 the ESS value for r is b/(b1c). The condition for hermaphroditism to be an ESS is: b1c .2bc.
male fertilities23.
These results mean that the ESS breeding system is determined by just the exponents of the fitness gain funcOnce estimates of male
2,6
tions and not the scaling factors km and kf. Similar methods can be used to model sex allocation in partial selfers .
fertilities have been obtained,
regression methods could
be used to fit a function reThree recent studies provide some clues. In the orchid lating male fitness to sex allocation. Alternatively, it is
Tolumnia the number of seedlings recruited to the popu- possible to integrate estimation of parameters describing
lation correlated positively with the number of fruits pro- a fitness function into the maximum-likelihood model18.
duced experimentally by augmenting pollination9. In the This method (Box 3) has statistical properties making it
thistle, Cirsium canescens, plants setting more seed especially suitable for describing male gain curves.
because of lower insect herbivory also had more surviving
offspring14. Finally, in the borage Cynoglossum officinale, The shapes of fitness gain functions
biomass of surviving seedlings increased linearly with During the past 15 years, attention to the male side of reseed production15. Only the last case provides sufficient production has led to increasingly sophisticated studies of
information to describe the shape of the fitness function, plant fitness. However, only recently have attempts been
but for all three species local resource competition was made to estimate either male or female fitness gains as a
not so extreme that the advantage to producing more seed function of sex allocation per se. Three studies explored fitwas eliminated.
ness gains as a function of a trait thought to reflect sex alloLocal seed competition will not affect the male gain cation and, in so doing, tested aspects of the theory. Elle
curve, at least not for outcrossers that disperse pollen to a and Meagher (unpublished) used state-of-the-art paternity
large set of mates16. This makes the number of seeds sired analysis18 to estimate male fertility in the andromonby an individual (male fertility) an excellent measure of male oecious horsenettle Solanum carolinense and found that it
fitness. Recent years have seen the development of reliable increased with an increasing proportion of male flowers on
analytical methods for estimating male fertility from the plant, while female fertility decreased24. This result
molecular data (Box 3). The latest methods use maximum supports a basic assumption of the theory: male fitness
Fertility
Box 1. The classic model of sex allocation for outcrossing species
228
TREE vol. 15, no. 6 June 2000
REVIEWS
Fitness estimate
Fitness estimate
increases with additional alBox 2. Local resource competition and female fitness gains
location to male function.
The two other studies
Local resource competition can cause the female gain curve to saturate4. The process requires low seed dispersal
so that seeds compete with siblings. Density-dependent survival or reproduction is not sufficient.
also support this assumption
and, in addition, provide inThe figure contrasts the case of low (a) and high (b) seed dispersal in populations with density-dependent survival. From left to right are the spatial distribution of seeds in a population, the spatial distribution of progeny surformation on shapes of
viving to reproduce, and female fitness plotted against allocation to male function (r ). Seeds are produced by two
the gain functions. For the
genotypes differing in allocation: females (closed symbols) and hermaphrodites (open symbols). Progeny of three
bumblebee-pollinated hermindividuals of each genotype are shown. The hermaphrodites allocate half their resources to male function (r 5 0.5)
aphroditic herbs C. officinale
and produce half as many seeds as females, which allocate no resource to male function (r 5 0). Survival is
density-dependent; the high-density population produces more seeds than the low-density population, but no
(hound’s tongue) and Echium
more seeds survive to reproduce.
vulgare (viper’s bugloss),
Rademaker and de Jong25
Seeds
Surviving offspring
Female fitness gain
defined allocation (r) as
(a)
Low
seed
dispersal
the ratio of flowers to seeds,
a choice justified by the
Surviving
2
physiological trade-off beoffspring
High
tween these traits. This
density
Seeds
study is unusual in considering how local resource
1
competition influences the
female gain curve. Female fitness was estimated by comLow
paring seedling growth and
0
density
survival around plants that
0
1
r
varied in the number of
seeds produced15. Male fit(b) High seed dispersal
ness was estimated by mecha2
nistic studies of pollen
Surviving
High
export and, because these
offspring
density
species are partially selfing,
or seeds
of selfing rate and inbreed1
ing depression. Estimated
pollen export increased with
flower number26, supporting
Low
the idea that investing more
0
density
in male function benefits
0
1
male fitness, provided pollen
r
export represents male ferTrends in Ecology & Evolution
(Online: Fig. I)
tility. The male gain curves
showed linear or diminish(a) Seed dispersal is low so that seeds lie in clusters of siblings and progeny compete only with siblings to yield a
ing returns and plotting male
single survivor. Even though one genotype makes more seed it does not have more surviving offspring and relative
versus female fitness profitness measured by the number of surviving offspring is one. The function relating female fitness to allocation levels
off (solid line). The diminishing returns on allocation make hermaphroditism more likely to be evolutionarily stable.
duced convex fitness sets
as predicted in the case
(b) Seeds are dispersed further so that they also compete with nonsiblings. Relative female fitness of the two
genotypes estimated by surviving progeny is two, and the fitness gain function is linear.
when hermaphroditism is
Although only two extreme genotypes are shown here, the same principles apply in a population of hermaphrothe ESS (Ref. 25).
dites differing quantitatively in sex allocation. Cases (a) and (b) could be separated using genetic markers to follow
A study of hummingthe success of progeny produced by plants with different sized seed crops.
bird-pollinated scarlet gilia
(Ipomopsis aggregata) is unusual in measuring sex allocation in units of biomass, allowing exploration of gain curves female gain curve so that the number of seeds is a poor
as specified in the classic theory22. Sex allocation was defined measure of female fitness, or if no trade-off in biomass
as the ratio of biomass in the stamens versus the pistil and allocation exists.
seeds. Male fertility, estimated with a genetic paternity
In summary, these initial studies suggest that male fitanalysis, increased with increasing allocation to male func- ness responds to increased allocation to male function. In
tion. When fitted to a gain function the relationship was addition, fitness gains for hermaphroditic herbs are qualibest described by diminishing returns (Fig. 1), although tatively consistent with theoretical expectations for that
with considerable scatter. Female fitness, estimated by breeding system, but there are quantitative discrepancies
seed production, showed accelerating returns on invest- between observed and expected sex allocation that remain
ment. Taken together, the shapes of the two fitness func- to be explained.
tions were consistent with the expectation for a hermaphrodite (Fig. 1). However, the ESS allocation to male Is there a trade-off in allocation?
function was lower than observed in nature, and pheno- Theory of sex allocation assumes a trade-off in allocation
typic selection through male and female functions did not of resources, such that plants investing more in male funccancel as expected if the population is at an ESS (Ref. 27). tion retain less for female function. The classic model is
This discrepancy is explainable if variation in seed quality even more restrictive in assuming a linear trade-off beor local resource competition cause a flattening of the tween resources invested in the two sexual functions. If no
TREE vol. 15, no. 6 June 2000
229
REVIEWS
Box 3. Estimating male fitness gains using paternity analysis
Current methods for determining male fertility from genetic data make use of likelihood estimation. These methods can be used with dominant markers (RAPDs) or codominant markers (isozymes or microsatellites). The discussion here assumes codominance. Multilocus genotypes are obtained for a sample of progeny, their known
maternal parents and all possible fathers in the population. The probability of observing a particular offspring genotype, given the genotypes of its mother and a candidate father, depends on mendelian segregation. Exclusion of all
but one possible father means this probability is zero for all other candidates. Complete exclusion for all progeny is
typically not possible. Instead, the procedure estimates the vector of male fertilities for all putative fathers in the
population, which maximizes the likelihood for obtaining the entire array of offspring genotypes8,17.. This requires
either assuming that relative male fertilities are the same for all female mates or assaying a sufficient sample of
progeny per female to estimate fertilities separately for each seed crop. Recently, Smouse et al. showed how
to incorporate estimation of a regression parameter relating male fertility to a phenotypic trait into the likelihood
analysis18. This method has low bias and could be applied to determine the shape of a male gain curve by estimating
linear and quadratic terms for male fertility regressed on sex allocation.
(b)
Relative seeds sired per flower (m)
4.0
3.0
m = 1.93 r 0.48
2.0
1.0
0.0
0.0
0.2
0.4
0.6
0.8
1.0
Relative seeds produced per flower (f)
(a)
4.0
f = 3.02 (1 – r )3.69
3.0
2.0
1.0
0.0
0.0
0.2
0.4
r
0.6
0.8
1.0
r
Proportion of resources to male function
Trends in Ecology & Evolution
Fig. 1. Estimated fitness gain functions in scarlet gilia (Ipomopsis aggregata)22. An increase in r (biomass allocation to stamens versus pistil and seeds) led to a significant increase in relative seeds sired per flower (a) and a
significant decrease in relative seeds produced per flower (b). Total seed production was linearly related to seeds
per flower, giving female gain curves, based on both measures, similar shapes. Power functions were fitted using
nonlinear regression to obtain the exponents that determine ESS sex allocation in the classic model. The exponents b 5 0.48 (95% CI 5 0.07–0.89) and c 5 3.69 (95% CI 5 2.82–4.55) make hermaphroditism the ESS
because b1c .2bc, with an expected allocation of r 5 0.12. The observed allocation of 0.28 (95% CI 5 0.25–0.31)
is less strongly female biased. Reproduced, with permission, from Ref. 22.
Table 1. Genetic correlations between sex-allocation traits obtained from
crossing studies
Species
Traits
Heritable
variation?
Genetic
correlation
Zea mays
Tassel mass and seed mass
Yes
20.83 a
a
Refs
38
Lythrum salicaria
Stamen mass and pistil mass
In short-styled
morph only
0.87
39
Begonia semiovata
Male flower mass and female
flower mass
Yes
0.88a
40
Ipomopsis aggregata
Stamen mass and pistil mass
Yes
0.40a and 0.38a,b
30
Mimulus guttatus
Pollen number and ovule number
Yes
20.32, 0.28, 0.36 c and
20.27c
31
a
P , 0.05.
Partial genetic correlation factoring out variation in flower number.
c
Partial genetic correlations factoring out variation in corolla size. The two estimates correspond to two populations.
b
230
trade-off exists, hermaphroditism could be favored even
when gain functions do not
show diminishing returns3.
A trade-off should generate a negative genetic correlation between allocation by
a whole plant into two sexual
functions28. However, plants
can also vary genetically in
their ability to acquire resources, which tends to generate positive correlations in
allocation characters. The
sign of the net genetic correlation will depend on both
sources of genetic variation29. The few quantitative
genetic studies of sex allocation, in which male and
female function were measured in a common currency,
have all uncovered some
genetic variation (Table 1).
However, three of the four
studies found positive genetic correlations between
allocation to male versus
female function. Positive
correlations are not surprising given genetic variation in
acquisition of resources used
for reproduction. If a tradeoff still exists, it should show
as a negative genetic correlation when the influence of
total reproductive biomass is
factored out to find a partial
correlation between allocation to male versus female
function29. Two studies30,31
have used multivariate methods to adjust estimated
correlations for other traits
and still found zero or positive genetic correlations
(Table 1). These initial results
suggest that genetic variation
in sex allocation is often
small compared with variation in traits related to resource acquisition and
vigor31, perhaps because
flowers can draw on different
resource pools for male and
female parts, as suggested
by physiological studies13.
Future tests of genetic correlations between allocation
traits should benefit from
the potentially powerful approach of artificial selection32,33. An open question
is whether negative correlations are stronger for
certain currencies, such as
nitrogen or biomass.
TREE vol. 15, no. 6 June 2000
REVIEWS
Prospects: designing a study of fitness gains
Describing how sex allocation influences fitness gains in
plants has only just begun. To date, no single study has
combined a measure of sex allocation directly related to
the theory, an estimate of female fitness that includes variation in survival of seeds to reproductive maturity and an
accurate estimate of male fitness. How can future studies
be designed to do so efficiently?
In a natural population it is difficult to estimate male
fertility with the precision necessary to describe a gain
function. A more powerful approach would involve constructing an artificial isolated population in which both
genotype and biomass allocation to male versus female
function can be manipulated. Such an approach has many
advantages that offset a probable cost to realism. An isolated population would be free from problems introduced
by cryptic gene flow. The investigator could choose multilocus genotypes to maximize statistical power in estimating male fertility. The ability to manipulate allocation
would eliminate the possibility that apparent fitness gains
are the result of a trade-off with an unmeasured character
with a hidden effect on the shape of the gain curve.
Because flower number is particularly easy to manipulate,
such a study would be easiest to perform in species where
variation in sex allocation results partly from variable
flower number26. In other species, manipulation might be
possible using selective application of soil nutrients34 or
hormonal treatments to adjust within-flower sex allocation. To measure female fitness as the number of seed
offspring surviving would require the use of parentage
analysis to identify the mother and father of seedlings35, or
setting up a separate study using genetic markers to examine the relationship of seed production to realized female
fitness (Box 2).
Such experimental studies of fitness gains will be far
more informative if they are combined with efforts to
determine the mechanisms underlying them. Several hypotheses have been proposed to explain saturating male
gain curves and thus the prevalence of hermaphroditism in
animal-pollinated flowers. One idea is that presenting more
pollen leads to diminishing returns on pollen removal and
export to other flowers, particularly if pollinators become
saturated with pollen or lose much pollen to grooming. In
addition, increasing pollen production can increase the
fraction of pollen moved to other flowers on the same plant
(geitonogamous selfing) at the expense of outcrossing26,36.
Alternatively, if pollen dispersal is highly localized, pollen
grains might show local mate competition with sib pollen
that lands on the same stigma, again generating diminishing fitness returns4. One way to separate these hypotheses
is to measure fitness gains separately during pollen removal, pollen export and post-pollination. Effects on pollen
removal are probably the most easily addressed, because
they can be studied by presenting plants differing in sex
allocation to captive pollinators. Effects on pollen export
could be separated from post-pollination effects by simultaneously tracking pollen dispersal and estimating
male fertility. Comparing fitness gains based on these two
measures would indicate the stage at which any curvature
is produced.
Perhaps the most fruitful systems for such experimental tests will be genera in which there are two or more
related species that differ in breeding systems. Ascertaining whether the shapes of fitness gain curves differ between those species in the direction expected, and the key
step in the life cycle at which this happens, would provide
a powerful test of sex-allocation theory.
TREE vol. 15, no. 6 June 2000
Acknowledgements
I am grateful to Tom J. de Jong and Peter G.L. Klinkhamer
for many helpful discussions. I also thank Ann K. Sakai,
Nickolas M. Waser and Stephen G. Weller for encouraging
me to pursue this topic and for comments on this article.
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35 Meagher, T.R. and Thompson, E.A. (1987) Analysis of parentage for
naturally established seedlings of Chamaelirium luteum. Ecology
68, 803–812
36 Harder, L.D. and Barrett, S.C.H. (1995) Mating cost of large floral
displays in hermaphrodite plants. Nature 373, 512–515
37 Morgan, M.T. and Schoen, D.J. (1997) The role of theory in an emerging
new plant reproductive biology. Trends Ecol. Evol. 12, 231–234
38 Garnier, P. et al. (1993) Costly pollen in maize. Evolution 47, 946–949
39 O’Neil, P. and Schmitt, J. (1993) Genetic constraints on the
independent evolution of male and female reproductive characters in
the tristylous plant Lythrum salicaria. Evolution 47, 1457–1471
40 Agren, J. and Schemske, D.W. (1995) Sex allocation in the monoecious
herb Begonia semiovata. Evolution 49, 121–130
Pulsed resources and community
dynamics of consumers in
terrestrial ecosystems
Richard S. Ostfeld and Felicia Keesing
R
ecently, the field of commuMany terrestrial ecosystems are characterized
resources permeate through food
nity ecology has integrated
by intermittent production of abundant
webs is a major challenge for
the notions of ‘top-down’
resources for consumers, such as mast seeding
community ecology. Tracing the
and ‘bottom-up’ influences on comand pulses of primary production following
impacts of pulsed resources on
munity organization1–5. According
unusually heavy rains. Recent research is
communities incorporates both
to this framework, populations ocrevealing patterns in the ways that consumer
bottom-up and top-down influcupy positions in a food web and communities respond to these pulsed resources. ences, but requires ecologists to
their abundance or biomass can
Studies of the ramifying effects of pulsed
incorporate the concepts of
be controlled by populations at
resources on consumer communities integrate
disturbance, time delays and
higher trophic levels (e.g. top‘top-down’ and ‘bottom-up’ approaches to
mobility of organisms into condown effects of predators on prey),
community dynamics, and illustrate how the
siderations of how populations
lower trophic levels (e.g. bottomstrength of species interactions can change
affect one another.
dramatically through time.
up effects of biotic resources on
Conceptual underpinnings
consumers) or the same level
Recently, far-reaching effects of
(more traditional competitive inRichard Ostfeld is at the Institute of Ecosystem
pulsed seed production have
teractions). The top-down bottomStudies, Millbrook, NY 12545, USA
been documented in several terup approach is sympathetic to the
([email protected]); Felicia Keesing is at Siena
restrial habitats. Mast seeding
notion that interactions between
College, Loudonville, NY 12211, USA, and the
populations might be either direct Institute of Ecosystem Studies, Millbrook, NY 12545, occurs in many terrestrial ecosystems, including boreal, temperate
(e.g. a predator controlling prey
USA ([email protected]).
and tropical forests, as well as
density) or indirect (e.g. a primary
grasslands and deserts7,12–14. If
producer enhancing a parasitoid
the trees, shrubs or herbaceous
population by increasing popuplants that synchronously prolation growth of a herbivore host).
Recently, temporal fluctuations in the strengths of inter- duce large fruit or seed crops (i.e. mast) are highly abunactions among species have been of great interest to ecolo- dant, even dominant, members of their communities, the
gists6, but these fluctuations have not been integrated into result is an extraordinary flush of nutritious foods for consumers (Box 1). Pulses of seed production can be elicited
the top-down bottom-up paradigm2.
Many terrestrial (and aquatic) ecosystems are charac- by regional or global climatic fluctuations, including El
terized by pulsed resources – the temporary availability of Niño southern-oscillation (ENSO) events, which can cause
dramatically higher than normal levels of resources, which unusually high rainfall or solar radiation (potentially
then become depleted with time. Examples include mast important abiotic resources). In arid ecosystems, plant
fruiting by trees and herbs7,8, periodic irruptions of palat- communities typically respond to heavy rainfall with
able insects9, and storm-induced transport of marine re- explosive production of seeds and vegetative tissues15–17. In
sources (e.g. whale carcasses) to terrestrial systems10 or of moist, tropical forest systems, trees might respond to either
terrestrial resources (organic nitrogen or phosphorus) to unusually heavy rain or unusually dry, sunny conditions
aquatic systems11. Determining how the effects of pulsed with heavy fruit production18–20 (Table 1).
232
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TREE vol. 15, no. 6 June 2000
Experimental tests of sex-allocation
theory in plants
Diane R. Campbell
T
hree-quarters of flowering
A general explanation for diversity in plant
Estimating the parameters
plant species have hermaphbreeding systems is offered by sex-allocation
of fitness gain functions
roditic flowers; however, the
theory. This theory assumes a trade-off
The first choice in describing fitremaining species illustrate a
between allocation of resources to the two
ness gain functions is deciding
tremendous variety of breeding sexual functions. It explains the high frequency how to measure resource allosystems. These include not only
of hermaphroditism in angiosperms by
cation (r). In the classic form of the
separate sexes (dioecy), and popudiminishing fitness returns on investment of
model, r refers to the proportion
lations with unisex individuals
more resources in a single function. Recent
of resources invested by the plant
and hermaphrodites, but also sepexperimental studies provide tests of this
in stamens rather than in pistil or
arate unisex and hermaphroditic
theory by measuring male and female fitness
seed maturation2,3. More recent
flowers on the same individual.
gains, and examining the trade-off
elaborations separate allocation
This diversity has fascinated evoassumption. These studies show how fitness
at the time of flowering from seed
lutionary biologists for a long
responds to shifts in allocation. Allocation
production, to allow for differtime. Darwin1 noted that reduced
traits often show heritable variation, but
ences in the timing of investinvestment in one reproductive
support for a trade-off remains weak.
ment10 and/or to include allofunction could be compensated
cation to attractive structures,
for if it left additional resources
such as the corolla11. Furthermore,
Diane Campbell is at the Dept of Ecology and
for the other sexual function.
allocation can differ depending on
Evolutionary Biology, University of California, Irvine,
This idea of a trade-off in resource
whether it is measured in units of
CA 92697, USA ([email protected]).
use was elaborated in evolutionbiomass, carbon or nutrients, and
arily stable strategy (ESS) modon whether it takes into account
els developed by Charlesworth
photosynthesis and respiration
and Charlesworth2, Charnov3 and
by reproductive structures12,13.
4
Lloyd . According to this theory, the ESS sex allocation The shapes of the fitness gain functions will differ dependdepends on the shape of fitness gain functions relating ing on the currency chosen, unless different currencies
male and female fertilities to the proportion of resources have a linear relationship. Thus, it is problematical to
invested in male function (Box 1). One major dichotomy measure fitness gains as a function of one trait, such as
addressed by the theory is the distinction between dioecy flower number, and use that function to suggest the shape
and hermaphroditism. Although it was well understood of fitness gains for other traits, such as biomass allocation.
that separation of sexes could be favored by high selfing
This property should not interfere with the model’s
and inbreeding depression, this model illustrated another ability to predict an ESS for the currency chosen by the
selective mechanism that would also apply to outcrossing investigator, provided the underlying assumption of a
species. Accelerating fitness returns on investment of re- trade-off in allocation is met. However, different currencies
sources in a single sexual function would favor separate could lead to conflicting predictions about the stability of a
sexes, whereas diminishing returns on investment would breeding system. To describe sex allocation, an approfavor hermaphroditism. The theory had a major impact on priate measure is one comparing allocation to male strucplant reproductive biology, because it could explain diversity tures (e.g. stamens) with total allocation by the plant
of not only breeding systems but also resource allocation to female and male structures, using a currency, such as
within a population of hermaphrodites.
biomass, that shows a trade-off.
However, testing the theory proved difficult because
Another difficulty is presented by the need to estimate
the parameters are notoriously hard to estimate. Until re- male and female fitness in the field. Here, it is assumed that
cently, most tests relied on qualitative comparisons of investigators start by observing sex allocation in a mature
species. For example, selfing species were predicted to plant. For such a plant, production of offspring surviving to
show lower investment in male function than outcrossing reproductive maturity provides a reasonable index of fitspecies5,6. Furthermore, sex allocation was often expected ness, particularly for species without variation in age at
to depend on the size of an individual plant7.
reproduction. In natural populations, female fitness is usuRecent studies illustrate how to test the model experi- ally estimated by seed production. However, the shape of
mentally by estimating the fitness gains themselves. Devel- the female gain curve might be influenced by differential
opments in paternity analysis8 now permit estimation of success of seed crops that vary in size3. If seeds compete
relative male fertility, and studies of seedling stages permit with their siblings for a limited number of safe sites, this
more accurate estimation of realized female fertility9. local resource competition will saturate female fitness
These advances are leading to the first attempts to quan- gains (Box 2). The process requires low seed dispersal.
tify fitness gain functions. At the same time, quantitative Density-dependent population growth is not sufficient to
genetics has been applied to testing the basic assumption cause diminishing fitness gains (Box 2). To test for the
of a trade-off in allocation. This article revisits the evidence importance of this phenomenon we need to follow the sucfor sex-allocation theory, as applied to outcrossing plants, cess of offspring from individual plants and determine how
now that these new approaches are available.
many survive to reproduce.
TREE vol. 15, no. 6 June 2000
0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(00)01872-3
227
REVIEWS
likelihood to estimate male
fertilities from the set of
offspring genotypes and
Male fertility (m) (solid line) and female fertility (f ) (broken line) are considered power functions of the proportion of
resources put into male function (r):
genotypes of potential parents8,17,18. The goal is to obb
m = km r
f = kf (1 − r )c
tain estimates of relative
male fertilities that have low
bias and low variance. Alwhere km and kf are constants. An exponent (b or c) ,1 generates a function with diminishing returns, whereas an
exponent .1 generates accelerating returns. These exponents determine the evolutionarily stable strategy (ESS)
though adding sufficient loci
breeding system. (a) Both exponents b and c ,1, and the ESS is hermaphroditism. Plotting m versus f would lead
to exclude all but one genetto a convex (bowed out) fitness set. (b) Both b and c .1 corresponding to accelerating fitness gains, and the ESS
ically possible father of a
is dioecy.
seed is appealing19, sampling
(a)
(b)
more offspring is usually
b = 0.4, c = 0.6
b = 1.5, c = 2.5
easier and leads to a greater
kf
km
kf
km
reduction in sampling variance for a fixed total number
of assays20. One caution is
f
m
m
f
that with low exclusion probabilities, the likelihood estimation tends to underestimate the fitness of highly
successful males8. It remains
unclear how much this bias
alters the apparent shape of
the male gain curve. Studies
taking this approach should,
therefore, attempt to estimate the bias through com0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
puter simulation21,22. Another
r
r
potential source of bias that
Proportion of resources to male function
(Online: Fig. I)
could flatten the male gain
Trends in Ecology & Evolution
curve is cryptic gene flow17.
The fitness of a rare mutant i is the average of its relative female and male fertilities, and can be written as37:
This refers to siring of seeds
by a plant from outside the
mi
wi = f i + f
reference population that
m
goes undetected because a
where f and m are average female and male fertilities in the whole resident population. Substituting the power
genetically possible father
functions into this expression yields:
also exists inside the population. It is possible to eliminkmrib
c
c
wi = kf (1 − ri ) +
k (1 − r )
b f
ate bias as a result of cryptic
kmr
gene flow by simultaneously
The ratio rib/rb expresses the fraction of seeds in the population as a whole that are sired by the mutant. Following
estimating gene flow and
standard techniques4 the ESS value for r is b/(b1c). The condition for hermaphroditism to be an ESS is: b1c .2bc.
male fertilities23.
These results mean that the ESS breeding system is determined by just the exponents of the fitness gain funcOnce estimates of male
2,6
tions and not the scaling factors km and kf. Similar methods can be used to model sex allocation in partial selfers .
fertilities have been obtained,
regression methods could
be used to fit a function reThree recent studies provide some clues. In the orchid lating male fitness to sex allocation. Alternatively, it is
Tolumnia the number of seedlings recruited to the popu- possible to integrate estimation of parameters describing
lation correlated positively with the number of fruits pro- a fitness function into the maximum-likelihood model18.
duced experimentally by augmenting pollination9. In the This method (Box 3) has statistical properties making it
thistle, Cirsium canescens, plants setting more seed especially suitable for describing male gain curves.
because of lower insect herbivory also had more surviving
offspring14. Finally, in the borage Cynoglossum officinale, The shapes of fitness gain functions
biomass of surviving seedlings increased linearly with During the past 15 years, attention to the male side of reseed production15. Only the last case provides sufficient production has led to increasingly sophisticated studies of
information to describe the shape of the fitness function, plant fitness. However, only recently have attempts been
but for all three species local resource competition was made to estimate either male or female fitness gains as a
not so extreme that the advantage to producing more seed function of sex allocation per se. Three studies explored fitwas eliminated.
ness gains as a function of a trait thought to reflect sex alloLocal seed competition will not affect the male gain cation and, in so doing, tested aspects of the theory. Elle
curve, at least not for outcrossers that disperse pollen to a and Meagher (unpublished) used state-of-the-art paternity
large set of mates16. This makes the number of seeds sired analysis18 to estimate male fertility in the andromonby an individual (male fertility) an excellent measure of male oecious horsenettle Solanum carolinense and found that it
fitness. Recent years have seen the development of reliable increased with an increasing proportion of male flowers on
analytical methods for estimating male fertility from the plant, while female fertility decreased24. This result
molecular data (Box 3). The latest methods use maximum supports a basic assumption of the theory: male fitness
Fertility
Box 1. The classic model of sex allocation for outcrossing species
228
TREE vol. 15, no. 6 June 2000
REVIEWS
Fitness estimate
Fitness estimate
increases with additional alBox 2. Local resource competition and female fitness gains
location to male function.
The two other studies
Local resource competition can cause the female gain curve to saturate4. The process requires low seed dispersal
so that seeds compete with siblings. Density-dependent survival or reproduction is not sufficient.
also support this assumption
and, in addition, provide inThe figure contrasts the case of low (a) and high (b) seed dispersal in populations with density-dependent survival. From left to right are the spatial distribution of seeds in a population, the spatial distribution of progeny surformation on shapes of
viving to reproduce, and female fitness plotted against allocation to male function (r ). Seeds are produced by two
the gain functions. For the
genotypes differing in allocation: females (closed symbols) and hermaphrodites (open symbols). Progeny of three
bumblebee-pollinated hermindividuals of each genotype are shown. The hermaphrodites allocate half their resources to male function (r 5 0.5)
aphroditic herbs C. officinale
and produce half as many seeds as females, which allocate no resource to male function (r 5 0). Survival is
density-dependent; the high-density population produces more seeds than the low-density population, but no
(hound’s tongue) and Echium
more seeds survive to reproduce.
vulgare (viper’s bugloss),
Rademaker and de Jong25
Seeds
Surviving offspring
Female fitness gain
defined allocation (r) as
(a)
Low
seed
dispersal
the ratio of flowers to seeds,
a choice justified by the
Surviving
2
physiological trade-off beoffspring
High
tween these traits. This
density
Seeds
study is unusual in considering how local resource
1
competition influences the
female gain curve. Female fitness was estimated by comLow
paring seedling growth and
0
density
survival around plants that
0
1
r
varied in the number of
seeds produced15. Male fit(b) High seed dispersal
ness was estimated by mecha2
nistic studies of pollen
Surviving
High
export and, because these
offspring
density
species are partially selfing,
or seeds
of selfing rate and inbreed1
ing depression. Estimated
pollen export increased with
flower number26, supporting
Low
the idea that investing more
0
density
in male function benefits
0
1
male fitness, provided pollen
r
export represents male ferTrends in Ecology & Evolution
(Online: Fig. I)
tility. The male gain curves
showed linear or diminish(a) Seed dispersal is low so that seeds lie in clusters of siblings and progeny compete only with siblings to yield a
ing returns and plotting male
single survivor. Even though one genotype makes more seed it does not have more surviving offspring and relative
versus female fitness profitness measured by the number of surviving offspring is one. The function relating female fitness to allocation levels
off (solid line). The diminishing returns on allocation make hermaphroditism more likely to be evolutionarily stable.
duced convex fitness sets
as predicted in the case
(b) Seeds are dispersed further so that they also compete with nonsiblings. Relative female fitness of the two
genotypes estimated by surviving progeny is two, and the fitness gain function is linear.
when hermaphroditism is
Although only two extreme genotypes are shown here, the same principles apply in a population of hermaphrothe ESS (Ref. 25).
dites differing quantitatively in sex allocation. Cases (a) and (b) could be separated using genetic markers to follow
A study of hummingthe success of progeny produced by plants with different sized seed crops.
bird-pollinated scarlet gilia
(Ipomopsis aggregata) is unusual in measuring sex allocation in units of biomass, allowing exploration of gain curves female gain curve so that the number of seeds is a poor
as specified in the classic theory22. Sex allocation was defined measure of female fitness, or if no trade-off in biomass
as the ratio of biomass in the stamens versus the pistil and allocation exists.
seeds. Male fertility, estimated with a genetic paternity
In summary, these initial studies suggest that male fitanalysis, increased with increasing allocation to male func- ness responds to increased allocation to male function. In
tion. When fitted to a gain function the relationship was addition, fitness gains for hermaphroditic herbs are qualibest described by diminishing returns (Fig. 1), although tatively consistent with theoretical expectations for that
with considerable scatter. Female fitness, estimated by breeding system, but there are quantitative discrepancies
seed production, showed accelerating returns on invest- between observed and expected sex allocation that remain
ment. Taken together, the shapes of the two fitness func- to be explained.
tions were consistent with the expectation for a hermaphrodite (Fig. 1). However, the ESS allocation to male Is there a trade-off in allocation?
function was lower than observed in nature, and pheno- Theory of sex allocation assumes a trade-off in allocation
typic selection through male and female functions did not of resources, such that plants investing more in male funccancel as expected if the population is at an ESS (Ref. 27). tion retain less for female function. The classic model is
This discrepancy is explainable if variation in seed quality even more restrictive in assuming a linear trade-off beor local resource competition cause a flattening of the tween resources invested in the two sexual functions. If no
TREE vol. 15, no. 6 June 2000
229
REVIEWS
Box 3. Estimating male fitness gains using paternity analysis
Current methods for determining male fertility from genetic data make use of likelihood estimation. These methods can be used with dominant markers (RAPDs) or codominant markers (isozymes or microsatellites). The discussion here assumes codominance. Multilocus genotypes are obtained for a sample of progeny, their known
maternal parents and all possible fathers in the population. The probability of observing a particular offspring genotype, given the genotypes of its mother and a candidate father, depends on mendelian segregation. Exclusion of all
but one possible father means this probability is zero for all other candidates. Complete exclusion for all progeny is
typically not possible. Instead, the procedure estimates the vector of male fertilities for all putative fathers in the
population, which maximizes the likelihood for obtaining the entire array of offspring genotypes8,17.. This requires
either assuming that relative male fertilities are the same for all female mates or assaying a sufficient sample of
progeny per female to estimate fertilities separately for each seed crop. Recently, Smouse et al. showed how
to incorporate estimation of a regression parameter relating male fertility to a phenotypic trait into the likelihood
analysis18. This method has low bias and could be applied to determine the shape of a male gain curve by estimating
linear and quadratic terms for male fertility regressed on sex allocation.
(b)
Relative seeds sired per flower (m)
4.0
3.0
m = 1.93 r 0.48
2.0
1.0
0.0
0.0
0.2
0.4
0.6
0.8
1.0
Relative seeds produced per flower (f)
(a)
4.0
f = 3.02 (1 – r )3.69
3.0
2.0
1.0
0.0
0.0
0.2
0.4
r
0.6
0.8
1.0
r
Proportion of resources to male function
Trends in Ecology & Evolution
Fig. 1. Estimated fitness gain functions in scarlet gilia (Ipomopsis aggregata)22. An increase in r (biomass allocation to stamens versus pistil and seeds) led to a significant increase in relative seeds sired per flower (a) and a
significant decrease in relative seeds produced per flower (b). Total seed production was linearly related to seeds
per flower, giving female gain curves, based on both measures, similar shapes. Power functions were fitted using
nonlinear regression to obtain the exponents that determine ESS sex allocation in the classic model. The exponents b 5 0.48 (95% CI 5 0.07–0.89) and c 5 3.69 (95% CI 5 2.82–4.55) make hermaphroditism the ESS
because b1c .2bc, with an expected allocation of r 5 0.12. The observed allocation of 0.28 (95% CI 5 0.25–0.31)
is less strongly female biased. Reproduced, with permission, from Ref. 22.
Table 1. Genetic correlations between sex-allocation traits obtained from
crossing studies
Species
Traits
Heritable
variation?
Genetic
correlation
Zea mays
Tassel mass and seed mass
Yes
20.83 a
a
Refs
38
Lythrum salicaria
Stamen mass and pistil mass
In short-styled
morph only
0.87
39
Begonia semiovata
Male flower mass and female
flower mass
Yes
0.88a
40
Ipomopsis aggregata
Stamen mass and pistil mass
Yes
0.40a and 0.38a,b
30
Mimulus guttatus
Pollen number and ovule number
Yes
20.32, 0.28, 0.36 c and
20.27c
31
a
P , 0.05.
Partial genetic correlation factoring out variation in flower number.
c
Partial genetic correlations factoring out variation in corolla size. The two estimates correspond to two populations.
b
230
trade-off exists, hermaphroditism could be favored even
when gain functions do not
show diminishing returns3.
A trade-off should generate a negative genetic correlation between allocation by
a whole plant into two sexual
functions28. However, plants
can also vary genetically in
their ability to acquire resources, which tends to generate positive correlations in
allocation characters. The
sign of the net genetic correlation will depend on both
sources of genetic variation29. The few quantitative
genetic studies of sex allocation, in which male and
female function were measured in a common currency,
have all uncovered some
genetic variation (Table 1).
However, three of the four
studies found positive genetic correlations between
allocation to male versus
female function. Positive
correlations are not surprising given genetic variation in
acquisition of resources used
for reproduction. If a tradeoff still exists, it should show
as a negative genetic correlation when the influence of
total reproductive biomass is
factored out to find a partial
correlation between allocation to male versus female
function29. Two studies30,31
have used multivariate methods to adjust estimated
correlations for other traits
and still found zero or positive genetic correlations
(Table 1). These initial results
suggest that genetic variation
in sex allocation is often
small compared with variation in traits related to resource acquisition and
vigor31, perhaps because
flowers can draw on different
resource pools for male and
female parts, as suggested
by physiological studies13.
Future tests of genetic correlations between allocation
traits should benefit from
the potentially powerful approach of artificial selection32,33. An open question
is whether negative correlations are stronger for
certain currencies, such as
nitrogen or biomass.
TREE vol. 15, no. 6 June 2000
REVIEWS
Prospects: designing a study of fitness gains
Describing how sex allocation influences fitness gains in
plants has only just begun. To date, no single study has
combined a measure of sex allocation directly related to
the theory, an estimate of female fitness that includes variation in survival of seeds to reproductive maturity and an
accurate estimate of male fitness. How can future studies
be designed to do so efficiently?
In a natural population it is difficult to estimate male
fertility with the precision necessary to describe a gain
function. A more powerful approach would involve constructing an artificial isolated population in which both
genotype and biomass allocation to male versus female
function can be manipulated. Such an approach has many
advantages that offset a probable cost to realism. An isolated population would be free from problems introduced
by cryptic gene flow. The investigator could choose multilocus genotypes to maximize statistical power in estimating male fertility. The ability to manipulate allocation
would eliminate the possibility that apparent fitness gains
are the result of a trade-off with an unmeasured character
with a hidden effect on the shape of the gain curve.
Because flower number is particularly easy to manipulate,
such a study would be easiest to perform in species where
variation in sex allocation results partly from variable
flower number26. In other species, manipulation might be
possible using selective application of soil nutrients34 or
hormonal treatments to adjust within-flower sex allocation. To measure female fitness as the number of seed
offspring surviving would require the use of parentage
analysis to identify the mother and father of seedlings35, or
setting up a separate study using genetic markers to examine the relationship of seed production to realized female
fitness (Box 2).
Such experimental studies of fitness gains will be far
more informative if they are combined with efforts to
determine the mechanisms underlying them. Several hypotheses have been proposed to explain saturating male
gain curves and thus the prevalence of hermaphroditism in
animal-pollinated flowers. One idea is that presenting more
pollen leads to diminishing returns on pollen removal and
export to other flowers, particularly if pollinators become
saturated with pollen or lose much pollen to grooming. In
addition, increasing pollen production can increase the
fraction of pollen moved to other flowers on the same plant
(geitonogamous selfing) at the expense of outcrossing26,36.
Alternatively, if pollen dispersal is highly localized, pollen
grains might show local mate competition with sib pollen
that lands on the same stigma, again generating diminishing fitness returns4. One way to separate these hypotheses
is to measure fitness gains separately during pollen removal, pollen export and post-pollination. Effects on pollen
removal are probably the most easily addressed, because
they can be studied by presenting plants differing in sex
allocation to captive pollinators. Effects on pollen export
could be separated from post-pollination effects by simultaneously tracking pollen dispersal and estimating
male fertility. Comparing fitness gains based on these two
measures would indicate the stage at which any curvature
is produced.
Perhaps the most fruitful systems for such experimental tests will be genera in which there are two or more
related species that differ in breeding systems. Ascertaining whether the shapes of fitness gain curves differ between those species in the direction expected, and the key
step in the life cycle at which this happens, would provide
a powerful test of sex-allocation theory.
TREE vol. 15, no. 6 June 2000
Acknowledgements
I am grateful to Tom J. de Jong and Peter G.L. Klinkhamer
for many helpful discussions. I also thank Ann K. Sakai,
Nickolas M. Waser and Stephen G. Weller for encouraging
me to pursue this topic and for comments on this article.
References
1 Darwin, C. (1859) On the Origin of Species, John Murray
2 Charlesworth, D. and Charlesworth, B. (1981) Allocation of resources to
male and female function in hermaphrodites. Biol. J. Linn. Soc. 15, 57–74
3 Charnov, E.L. (1982) The Theory of Sex Allocation, Princeton
University Press
4 Lloyd, D.G. (1984) Gender allocations in outcrossing cosexual plants. In
Perspectives in Plant Population Ecology (Dirzo, R. and Sarukhan, J., eds),
pp. 277–300, Sinauer
5 Charnov, E.L. (1987) On sex allocation and selfing in higher plants.
Evol. Ecol. 1, 30–36
6 de Jong, T.J. et al. (1999) How geitonogamous selfing affects sex
allocation in hermaphroditic plants. J. Evol. Biol. 12, 166–176
7 Klinkhamer, P.G.L. et al. (1997) Sex and size in cosexual plants.
Trends Ecol. Evol. 12, 260–265
8 Smouse, P.E. and Meagher, T.R. (1994) Genetic analysis of male
reproductive contributions in Chamaelirium luteum (L.) Gray
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Pulsed resources and community
dynamics of consumers in
terrestrial ecosystems
Richard S. Ostfeld and Felicia Keesing
R
ecently, the field of commuMany terrestrial ecosystems are characterized
resources permeate through food
nity ecology has integrated
by intermittent production of abundant
webs is a major challenge for
the notions of ‘top-down’
resources for consumers, such as mast seeding
community ecology. Tracing the
and ‘bottom-up’ influences on comand pulses of primary production following
impacts of pulsed resources on
munity organization1–5. According
unusually heavy rains. Recent research is
communities incorporates both
to this framework, populations ocrevealing patterns in the ways that consumer
bottom-up and top-down influcupy positions in a food web and communities respond to these pulsed resources. ences, but requires ecologists to
their abundance or biomass can
Studies of the ramifying effects of pulsed
incorporate the concepts of
be controlled by populations at
resources on consumer communities integrate
disturbance, time delays and
higher trophic levels (e.g. top‘top-down’ and ‘bottom-up’ approaches to
mobility of organisms into condown effects of predators on prey),
community dynamics, and illustrate how the
siderations of how populations
lower trophic levels (e.g. bottomstrength of species interactions can change
affect one another.
dramatically through time.
up effects of biotic resources on
Conceptual underpinnings
consumers) or the same level
Recently, far-reaching effects of
(more traditional competitive inRichard Ostfeld is at the Institute of Ecosystem
pulsed seed production have
teractions). The top-down bottomStudies, Millbrook, NY 12545, USA
been documented in several terup approach is sympathetic to the
([email protected]); Felicia Keesing is at Siena
restrial habitats. Mast seeding
notion that interactions between
College, Loudonville, NY 12211, USA, and the
populations might be either direct Institute of Ecosystem Studies, Millbrook, NY 12545, occurs in many terrestrial ecosystems, including boreal, temperate
(e.g. a predator controlling prey
USA ([email protected]).
and tropical forests, as well as
density) or indirect (e.g. a primary
grasslands and deserts7,12–14. If
producer enhancing a parasitoid
the trees, shrubs or herbaceous
population by increasing popuplants that synchronously prolation growth of a herbivore host).
Recently, temporal fluctuations in the strengths of inter- duce large fruit or seed crops (i.e. mast) are highly abunactions among species have been of great interest to ecolo- dant, even dominant, members of their communities, the
gists6, but these fluctuations have not been integrated into result is an extraordinary flush of nutritious foods for consumers (Box 1). Pulses of seed production can be elicited
the top-down bottom-up paradigm2.
Many terrestrial (and aquatic) ecosystems are charac- by regional or global climatic fluctuations, including El
terized by pulsed resources – the temporary availability of Niño southern-oscillation (ENSO) events, which can cause
dramatically higher than normal levels of resources, which unusually high rainfall or solar radiation (potentially
then become depleted with time. Examples include mast important abiotic resources). In arid ecosystems, plant
fruiting by trees and herbs7,8, periodic irruptions of palat- communities typically respond to heavy rainfall with
able insects9, and storm-induced transport of marine re- explosive production of seeds and vegetative tissues15–17. In
sources (e.g. whale carcasses) to terrestrial systems10 or of moist, tropical forest systems, trees might respond to either
terrestrial resources (organic nitrogen or phosphorus) to unusually heavy rain or unusually dry, sunny conditions
aquatic systems11. Determining how the effects of pulsed with heavy fruit production18–20 (Table 1).
232
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TREE vol. 15, no. 6 June 2000