Download Density-dependent seed set in the Haleakala silversword: evidence

Oecologia (2003) 136:551–557
DOI 10.1007/s00442-003-1295-3
POPULATION ECOLOGY
Stacey A. Forsyth
Density-dependent seed set in the Haleakala silversword:
evidence for an Allee effect
Received: 23 December 2002 / Accepted: 15 April 2003 / Published online: 29 May 2003
Springer-Verlag 2003
Abstract Plant species may be subject to Allee effects if
individuals experience a reduction in pollination services
when populations are small or sparse. I examined
temporal variation in reproductive success of the monocarpic Haleakala silversword (Argyroxiphium sandwicense subsp. macrocephalum) over five years, to
determine if plants flowering out of synchrony with most
of the population (i.e., in low flowering years) exhibited
lower percent seed set than synchronously-flowering
plants (i.e., those flowering in high flowering years).
Through two pollination experiments conducted over
multiple years, I also measured pollen limitation and selfincompatibility in this species. The number of flowering
plants varied greatly among years, as did reproductive
success. Percent seed set was significantly correlated with
the number of plants flowering annually, such that plants
flowering in high flowering years (1997 and 2001)
exhibited significantly higher percent seed set than did
plants flowering in low flowering years (1998–2000). In
the 3-year pollen limitation study, plants flowering
asynchronously were pollen-limited, whereas plants flowering synchronously were not. This species is strongly
self-incompatible. Results of this study demonstrate that
the Haleakala silversword experiences reduced reproductive success in low flowering years, and suggest that this
Allee effect is pollinator-mediated. Allee effects in plants
are an understudied yet potentially important force with
implications for the population dynamics and conservation of rare species.
Keywords Argyroxiphium · Monocarpy · Pollen
limitation · Self-incompatibility · Synchronous flowering
S. A. Forsyth ())
Department of Ecology and Evolutionary Biology,
Biological Sciences West 310,
University of Arizona,
Tucson, AZ 85721, USA
e-mail: [email protected]
Tel.: +1-520-6213458
Fax: +1-520-6219190
Introduction
Theoretical and empirical work in conservation biology
suggests that small populations are more likely to go
extinct than are larger populations, in part due to chance
fluctuations in population size (Shaffer 1981; Gilpin and
Soule 1986). Small populations may also suffer additional
disadvantages due to Allee effects, in which individuals
experience reduced survival and/or fertility at low population sizes (Allee 1931, 1938). In species exhibiting
Allee effects, individual fitness is reduced as population
size decreases, with extinction becoming more likely as a
population declines. Allee effects may be due to a variety
of genetic, demographic, and/or ecological factors, including increased levels of inbreeding depression or
genetic drift, skewed sex ratios, reduced availability of
mates, and decreased hunting success with smaller pack
size (Allee 1938; Courchamp et al. 1999; Stephens et al.
1999; Courchamp and MacDonald 2001). Although the
role of Allee effects in the ecology and conservation of
animals has received much consideration (Kuussaari et al.
1998; Courchamp et al. 1999; Courchamp and MacDonald 2001), their importance in plants is poorly documented and requires further study (Lamont et al. 1993;
Hackney and McGraw 2001). Such studies are particularly important for rare plants, for which the evaluation of
Allee effects should be an essential component of
conservation efforts (Groom 1998).
In animal species, reproductive success may decline in
small populations because individuals in these populations are mate-limited (Allee 1931, 1938; Kuussaari et al.
1998; Courchamp et al. 1999). Similar effects can occur
in small or isolated plant populations, particularly in
species that depend on animal vectors for pollination
(Groom 1998). Plant abundance and/or density may
impact plant-pollinator interactions, and therefore plant
reproductive success, by affecting both the quantity and
quality of pollination services received (Kunin 1993;
Lamont et al. 1993; Ingvarsson and Lundberg 1995;
Groom 1998; Hackney and McGraw 2001). Small and/or
isolated plant populations may be less apparent or
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attractive to pollinators, resulting in a lower number of
pollinator visits to plants in these populations (Schemske
1980; Jennersten 1988). Lower visitation rates may lead
to insufficient pollen transfer, and therefore to decreased
seed set, for plants located in these areas. In cases where
pollinator visitation is not affected by population size or
density, plants in small populations may still suffer
reduced seed set if the effectiveness of pollination, due to
pollen quality, declines (Kunin 1993; Lamont et al. 1993;
Wolf and Harrison 2001). This may occur through the
deposition of foreign rather than conspecific pollen, or
through the transfer of incompatible pollen, if a selfincompatibility mechanism is present (Feinsinger et al.
1991; Kunin 1993; Aizen and Feinsinger 1994; Groom
1998; Ramsey and Vaughton 2000). Essentially, the
efficiency of pollination, in terms of both the quantity and
quality of pollen received, declines as patches become too
small or the distance between plants becomes too great
(Courchamp et al. 1999). Obligate outcrossers that rely on
animal vectors for pollination are most likely to be
affected by Allee effects (Huenneke 1991).
Previous studies that have examined Allee effects in
plants have focused on reproductive success in differentsized populations or in patches of varying density
(Lamont et al. 1993; Groom 1998; Hackney and McGraw
2001). Some of these studies have manipulated plant
population size or density and examined subsequent
effects on pollinator behavior and/or efficiency (Feinsinger et al. 1991; Kunin 1993, 1997; Bosch and Waser
2001; Hackney and McGraw 2001; Mustajrvi et al.
2001), whereas others have taken advantage of existing
variation in plant population size or density (Lamont et al.
1993; gren 1996; Roll et al. 1997; Groom 1998; Bosch
and Waser 1999; Mavraganis and Eckert 2001). However,
in many species, the abundance of flowering plants varies
greatly among years, even if overall population size
remains fairly constant. This is particularly true for longlived species exhibiting synchronized flowering, in which
years of abundant flowering are separated by one to a few
years of little or no flowering (Janzen 1976; Taylor and
Inouye 1985; Kelly 1994). In these species, temporal
variation in flowering plant abundance and density may
affect reproductive success via the mechanisms described
above.
The Haleakala silversword (Argyroxiphium sandwicense subsp. macrocephalum; Asteraceae: Madiinae)
is a long-lived, monocarpic rosette plant endemic to
Haleakala volcano on the Island of Maui, Hawaii. As is
the case with many other monocarpic plant species, A.
sandwicense subsp. macrocephalum (subsequently, silversword) flowering exhibits a boom and bust pattern,
with years of abundant flowering separated by one to a
few years of very little flowering (Loope and Crivellone
1986). In this study, I use the natural annual variation in
the abundance of flowering plants, combined with
observations and pollination experiments, to test for an
Allee effect in the Haleakala silversword. I quantify
silversword seed set over five years and examine the
relationship between annual flowering plant abundance
and reproductive success. Specifically, I address the
following questions:
1. To what degree does seed set vary among years?
2. Does among-year variation in seed set correlate with
annual variation in flowering plant abundance?
3. Is the silversword pollen-limited?
4. To what degree is the silversword self-incompatible?
Questions 1 and 2 test for the presence of an Allee
effect; questions 3 and 4 examine a potential mechanism
underlying this effect. Following these analyses, I discuss
the conservation implications of an Allee effect in this
species.
Materials and methods
Study site
I conducted this research at Haleakala National Park (HALE),
Maui, Hawaii (20440 N, 156130 W). This area is comprised of
alpine desert (>3,000 m) and subalpine shrubland (2,000–3,000 m)
habitats, which are characterized by low annual precipitation, large
diurnal variation in temperature, and relatively bare cinder and ash
soils (Juvik and Juvik 1998). Vegetation in this area is sparse and
primarily comprises a few dominant species, in addition to the
silversword. Annual precipitation at Haleakala summit (3,341 m)
averages 500–800 mm, with the majority of rainfall occurring
between November and April (Kobayashi 1973; Juvik and Juvik
1998). Precipitation is slightly greater in the silversword habitats
(2,000–3,100 m), due to the cloud layer associated with a trade
wind inversion (Loope and Medeiros 1994).
Study species
The Haleakala silversword, a member of the Hawaiian silversword
alliance, is one of five species in the genus, and one of two
subspecies. The other, the Mauna Kea silversword (Argyroxiphium
sandwicense subsp. sandwicense), is endemic to the Island of
Hawaii. The Haleakala silversword occurs on the cinder cones and
lava flows within Haleakala crater (2,000–3,000 m), as well as on
the outer slope near the volcano’s summit (3,000–3,341 m). After
growing for many years as a basal rosette, individuals produce a tall
flowering stalk (capitulescence) bearing hundreds of capitula, and
die after setting seed. Capitulescence length and number of capitula
are both strongly correlated with rosette diameter (Forsyth 2002).
Flowering occurs throughout the summer months, typically peaking
in July; during this time, flowering individuals are frequently
visited by native and alien bees, wasps, flies, and moths (Forsyth,
unpublished data). Nearly all pollination is effected by diurnal
visitors, primarily native yellow-faced bees (Hylaeus spp.; Forsyth,
unpublished data). Due to its extensive interactions with pollinators, herbivores and seed predators, the silversword is likely a key
component of HALE’s high-elevation ecosystem (Loope and
Medeiros 1994).
Once common throughout Haleakala crater, the silversword
suffered severe population declines in the late 1800s and early
1900s, primarily due to browsing by introduced goats and cattle, as
well as human vandalism (Loope and Crivellone 1986). Following
federal protection from these threats, the population rebounded to
an estimated size of 48,000 individuals by 1982 (Loope and
Crivellone 1986). A silversword monitoring study conducted from
1982 to 2002, however, suggests that the population may once
again be in decline (Forsyth 2002). A current threat to the
silversword is the invasive Argentine ant (Linepithema humile), a
predator of native insect species, including Hylaeus spp. (Cole et al.
553
1992; Loope and Medeiros 1994). The Haleakala silversword was
federally listed as threatened in 1992 (USFWS 1992).
Silversword flowering
I obtained long-term silversword flowering records from the U.S.
Geological Survey, Biological Resources Division, Haleakala
National Park. With the exceptions of 1977 and 1981, flowering
surveys have been conducted every year since 1969. Surveys are
conducted in October, following the flowering season, in order to
quantify the number of silverswords flowering in each area of
HALE, as initially delineated by Kobayashi (1973). I used the total
number of plants flowering throughout HALE as an estimate of
flowering for each year, because annual flowering densities in each
of the four areas used in this study reflected flowering intensity
crater-wide (Loope and Forsyth, unpublished data).
Temporal variation in seed set
In order to assess temporal variation in seed set, I collected achenes
(fruits) from flowering individuals every year from 1997 to 2001.
Achenes were collected from plants located in four areas of HALE
crater: Sliding Sands Trail (2,700 m), Silversword Loop (2,400 m),
Puu Kauaua (2,400 m), and Kalahaku (3,050 m). These sites were
selected based on relatively high densities of silverswords in these
areas. For each plant, I measured rosette diameter and collected
three naturally-pollinated capitula, in order to quantify seed set.
Capitula were collected in late September, approximately 8–
10 weeks after flowering, when achenes were mature and close to
dispersal. I examined achenes under a dissecting microscope and
used the proportion of all dissected achenes that contained a filled
embryo as a measure of percent seed set for that plant. Within each
year, seed set estimates from the four areas were pooled together,
due to low numbers of flowering plants in some years, and average
annual percent seed set was compared to the number of plants
flowering that year.
Pollen limitation and self-incompatibility experiments
I conducted pollen limitation and self-incompatibility experiments
on individuals located throughout HALE crater from 1997 to 1999.
In order to limit damage to cinder cones, the majority of study
plants were located at Silversword Loop, Puu Kauaua, and
Kalahaku. In all years, access to flowering plants limited sample
sizes in these experiments. In 1997, 1998, and 1999, I conducted
pollen limitation experiments on 6, 8, and 16 individuals, respectively. Self-incompatibility experiments were conducted in 1998
and 1999 on 8 and 13 individuals, respectively. Heavy seed
predation by Rhynchephestia rhabdotis (Lepidoptera: Pyralidae)
reduced sample sizes in these experiments to 5, 4, and 13 plants
(pollen limitation) and 5 and 10 plants (self-incompatibility),
respectively.
In each experiment, I randomly selected experimental capitula,
although capitula exhibiting signs of R. rhabdotis infestation were
replaced by nearby uninfested capitula. To determine if seed set
was pollen-limited, I conducted a pollen augmentation experiment.
If seed production in pollen-augmented flowers is increased relative
to naturally pollinated flowers, the plant is considered to be pollenlimited at that place and time (Hainsworth et al. 1985; Zimmerman
and Pyke 1988). I selected six experimental capitula on each plant
and randomly assigned each to one of two treatments, for a total of
three capitula per treatment per plant: open-pollinated with no
supplemental pollen added (OPEN), or open-pollinated with
supplemental pollen added (AUGMENT). In the AUGMENT
treatment, the supplemental pollen was a mix of pollen collected
from at least three other individuals. I collected donor pollen in a
vial by gently brushing the vial against several pollen-bearing
capitula, and applied pollen to recipient capitula using a paintbrush
to cover all receptive stigmas. This procedure was repeated twice
for each capitulum, in order to pollinate the maximum number of
stigmas. Each experimental capitulum was marked with a colorcoded thread to distinguish treatment and permitted to mature.
Achenes were collected and analyzed as described above.
If seed production is limited by resources as well as pollen, seed
set in pollen-augmented flowers may occur at the expense of nonaugmented flowers on the same plant, as resources are reallocated
to flowers that receive more pollen (Lee 1988; Zimmerman and
Pyke 1988). To evaluate this effect in the silversword, in 1999 I
compared seed set in open-pollinated capitula on plants that
received the augmentation treatment (n=9 plants) to seed set in
open-pollinated capitula on control plants that did not receive the
augmentation treatment (n=7 plants). For each plant, openpollinated seed set was the proportion of all dissected achenes
(pooled from three capitula per plant) that were filled. Achenes
from open-pollinated capitula on treatment and control plants were
collected and analyzed as described above.
Previous evidence suggests that some species in the Hawaiian
silversword alliance (Argyroxiphium, Dubautia, and Wilkesia) are
self-incompatible (Carr et al. 1986). To measure self-incompatibility in the silversword, I conducted a pollinator exclusion
experiment using nylon mesh bags to prevent pollinators from
visiting experimental capitula. This method effectively excludes
insect visitors but does not alter the microclimate surrounding the
developing capitulum (Kearns and Inouye 1993). I selected nine
capitula per plant and randomly assigned each to one of the
following three treatments, for a total of three capitula per
treatment per plant: unbagged and pollinated naturally (OPEN);
bagged, with no pollen added (BAG); or bagged, with self-pollen
added (SELF). BAG and SELF capitula were enclosed in mesh
bags as soon as they were distinct from the flowering stalk. Selfpollen was collected from at least three other capitula on the same
plant and applied to receptive stigmas as described above.
Experimental capitula were collected after achene maturation and
analyzed as previously described.
Statistical analyses
Percent seed set data were logit transformed for statistical analyses.
Among-year variation in seed set was examined with a one-way
analysis of variance; Tukey-Kramer tests were used to evaluate
significant differences between all pairs of years. To examine the
relationship between flowering plant abundance and percent seed
set, I plotted the average percent seed set (€1 SE) for each of the
five years against the number of plants that flowered in that year. I
used the transformation
Y ¼ lnð1 f =fmax Þ
ð1Þ
where f equals the average percent seed set for each year and fmax
equals the maximum fertility observed in the 5-year period, or 0.45,
in order to linearize the relationship. I then used linear regression to
analyze the relationship between annual flowering plant abundance
and percent seed set.
In order to examine other factors potentially related to plant
seed set, I used linear regression. Specifically, I tested whether
individual seed set was dependent on plant size (rosette diameter),
and whether average annual percent seed set was correlated with
annual precipitation. Annual precipitation records for HALE were
obtained from the Western Regional Climate Center.
To analyze the results of the pollen limitation and selfincompatibility experiments, I used two-way ANOVAs, with
treatment and year as the main effects. In the pollen limitation
experiment, I compared two treatments (OPEN and AUGMENT)
and three years (1997–1999), and in the self-incompatibility
experiment, I compared three treatments (OPEN, BAG, and SELF)
and two years (1998 and 1999). Open-pollinated seed set data from
augmented and non-augmented plants were logit-transformed and
compared with a student’s t-test. All statistical analyses were
performed with JMPin software (SAS 2000).
554
Results
From 1997 to 2001, the number of flowering silverswords
ranged from a low of 167 (~0.33% of the total population)
in 1998 to a high of 2,687 (~5.37% of the total
population) in 1997. Consistent with the annual variation
in flowering, percent seed set differed significantly
among years (F4, 48=6.788, P=0.0002). Seed set was
significantly greater in 1997 and 2001, both high flowering years, than in 1998, 1999, and 2000, all low
flowering years (Tukey-Kramer test, a=0.05). Average
annual percent seed set was positively correlated with
flowering plant abundance, reaching a maximum of about
45% seed set in 1997 (Fig. 1A). After transformation
(Eq. 1), the number of plants flowering each year
explained 99.5% of the variation in seed set among years
(Fig. 1B).
There was no relationship between plant size (rosette
diameter) and percent seed set, for all years combined, as
well as for each year, 1997–2001 (Fig. 2). Average annual
percent seed set was not correlated with annual precipitation (R2=0.554, df=4, P=0.149).
In the pollen limitation experiment, treatment (F1,38=
20.677, P<0.0001), year (F2,38=9.426, P=0.0005), and the
treatment by year interaction (F2,38=3.963, P=0.0273)
were significant effects. Pollen augmentation significant-
Fig. 2 Percent seed set of open-pollinated silversword capitula
(1997–2001) and plant size. Symbols distinguish the five years,
with clear symbols indicating individuals that flowered in highflowering years (1997 and 2001), and filled symbols indicating
individuals that flowered in low-flowering years (1998, 1999, and
2000)
Fig. 3 Average percent seed set (€1 SE) for open-pollinated and
pollen-augmented silversword capitula, 1997–1999. 1997: n=5
plants; 1998: n=4 plants; 1999: n=13 plants. Letters indicate
statistical differences: the pollen augmentation treatment significantly increased seed set in 1998 and 1999, but not in 1997
Fig. 1. A Raw and B transformed (relative to fmax) percent seed set
of open-pollinated silversword capitula for each year, 1997–2001,
as a function of the number of plants that flowered that year (n).
Markers represent average percent seed set (€1 SE) for each year.
n=6 (1997); 5 (1998); 15 (1999); 7 (2000); 20 (2001). Transformed
percent seed set =ln (1f/fmax), where f = average percent seed set
for each year, 1997–2001, and fmax=0.45 (maximum percent seed
set observed in the 5-year period). R2=0.995; F=602.380, P<0.0001
ly increased seed set in 1998 and 1999, but not in 1997
(Fig. 3). This suggests that the silversword was strongly
pollen-limited in 1998 and 1999, both low flowering
years, but not in 1997, a high flowering year. The pollen
augmentation treatment produced consistent results across
years, yielding 35–40% seed set in all years (1997:
38.92€3.63; 1998: 34.80€5.99; 1999: 36.72€4.87). Openpollinated seed set did not differ between augmented and
non-augmented plants (t=0.278, df=14, P=0.7854), indicating that the pollen augmentation treatment did not
affect seed set in open-pollinated capitula on the same
plant.
The self-incompatibility experiment demonstrated that
the silversword is strongly self-incompatible (Fig. 4).
555
Fig. 4 Average percent seed set (€1 SE) for open-pollinated,
bagged, and self-pollinated silversword capitula, 1998–1999. 1998:
n=5 plants; 1999: n=10 plants. Letters indicate statistical differences: in both years, seed set was significantly greater in openpollinated capitula than in bagged and selfed capitula
There was a highly significant treatment effect (F2, 39=
17.329, P<0.0001), but no effect of year (F1, 39=1.594,
P=0.2140) or the treatment by year interaction (F2, 39=
0.262, P=0.771). In both 1998 and 1999, percent seed set
in bagged and selfed capitula was significantly lower than
percent seed set in open-pollinated capitula (Fig. 4). Seed
set in the BAG and SELF treatments were statistically
indistinguishable, averaging 0.31€0.12% and 0.40€0.13%
across years, respectively, whereas seed set in openpollinated capitula in these two years averaged 5.99€
1.13%.
Discussion
In the 5-year study period, the number of silverswords
flowering annually varied greatly among years, with three
low flowering years (1998–2000) bracketed by two high
flowering years (1997 and 2001). The 30-year flowering
record suggests that this among-year variation is typical
for the silversword; relatively high flowering years are
commonly separated by one to three low flowering years,
with the number of plants flowering annually ranging
from zero in 1970 to nearly 7,000 in 1991 (L.L. Loope,
personal communication). It is currently unknown what
triggers silverswords to flower; attempts to correlate
annual flowering abundance with precipitation, El Nio,
and other environmental factors have been unsuccessful
(Loope and Crivellone 1986; Rundel and Witter 1994).
Synchronous flowering at multi-year intervals has been
observed in other long-lived monocarpic species (Janzen
1976; Foster 1977; Taylor and Inouye 1985; Kelly 1994),
and in general, the causes for such flowering synchrony
are rarely understood (Taylor and Inouye 1985).
Annual variation in flowering was highly correlated
with significant variation in percent seed set among years.
Although the observed among-year variation in seed set
could be due to other, potentially confounding factors,
attempts to correlate seed set with other variables were
not successful. For example, percent seed set may vary
among individuals as a function of plant size, due to
differences in resource availability or pollinator attraction. In this study, however, there was no correlation
between plant size and percent seed set, both when data
from the five years were pooled together (n=49 plants), as
well as when data from each year were examined
separately. In addition, annual precipitation was not
correlated with average annual percent seed set and does
not appear to be a confounding factor in this system. This
is also implied by the consistent results of the pollen
augmentation experiment: from 1997 to 1999, pollen
augmentation consistently yielded seed set levels of about
35–40%, despite differences in annual precipitation
among these three years. This suggests that reproductive
success is determined by factors related to pollination,
such as flowering plant abundance, rather than by
precipitation. Although it would be ideal to manipulate
flowering plant abundance or density, to confirm that this
factor is responsible for the observed variation in percent
seed set, such experimental manipulation is not feasible
due to the conservation status of this species.
Kunin (1993) suggested that most self-incompatible
plants will have a critical minimum population density
threshold, below which pollen limitation is likely to
become an important factor influencing reproductive
success. Pollen limitation in small or sparse populations
can occur via effects on the quantity and/or quality of
pollen received (Kunin 1993; Lamont et al. 1993; Bosch
and Waser 2001). In poor flowering years, low densities
of flowering plants may attract fewer pollinators than
larger flowering displays, which can result in reduced
visitation, and consequently pollen limitation (Sih and
Baltus 1987; Groom 1998; Ramsey and Vaughton 2000).
In addition, individuals flowering in low flowering years
are less likely to overlap in time with nearby flowering
plants. This is particularly true for the silversword, for
which the flowering season extends across several months
but the flowering period of an individual is only one to
three weeks (Forsyth, unpublished data). Flowering
individuals, especially those flowering at the beginning
or end of the flowering season, may be isolated in both
time and space from any other flowering plant. In such
cases, there is little outcross pollen available and the
probability that receptive stigmas will receive compatible
outcross pollen declines as the number of flowering plants
decreases.
Similarly, if flowering plants are sparsely distributed,
pollinators are more likely to forage on multiple flowers
within one plant, instead of visiting several different
plants (de Jong et al. 1993; Bosch and Waser 2001). This
is particularly true for species exhibiting a “big bang”
flowering habit, in which large numbers of flowers within
a plant are on display simultaneously (Augspurger 1980).
Several studies have noted that pollinators tend to visit
more flowers in larger inflorescences (Klinkhamer et al.
1989; Mustajarvi et al. 2001). Such an increase of withinplant foraging would reduce the amount of outcross
pollen deposited on a plant, while increasing the amount
556
of geitonogamous (within-plant) self-pollination (de Jong
et al. 1993; Harder and Barrett 1995; Bosch and Waser
2001). Given the silversword’s strong self-incompatibility
mechanism, geitonogamous pollination would lead to low
seed set (reduced female fitness) as well as pollen
discounting (reduced male fitness).
Pollen, however, does not appear to be the only factor
limiting silversword reproduction. Even in high flowering
years, seed set did not exceed 45%, suggesting that
silversword seed set is limited by factors other than
compatible pollen in all years. Resource limitation is also
suggested by the pollen augmentation experiment, which
consistently produced only 35–40% seed set in each of the
three years in which the experiment was conducted. These
levels of seed set (<40%) suggest that silversword seed set
is limited by resources as well as by pollen.
The observed effect of flowering plant abundance on
reproductive success may help to explain the synchronized flowering pattern observed in this species. The
evolution of flowering synchrony to maximize reproductive success has been hypothesized for other long-lived
monocarpic species, including Swertia radiata, a longlived gentian (Taylor and Inouye 1985). Synchronized
flowering may also affect levels of seed predation, as
predicted by the predator satiation hypothesis (Janzen
1976). This hypothesis, that synchronized flowering
serves to minimize seed predation by swamping seed
predators with an abundance of seed in good flowering
years, and starving them in poor flowering years, has been
proposed for other long-lived plant species (Janzen 1976;
Augspurger 1981; Kelly 1994). Although not addressed in
this study, previous observations suggest that this interaction may occur with the silversword. In some years, a
large proportion of silversword achenes are lost to two
native predispersal seed predators, but in good flowering
years, seed predation may be less than 50% (Kobayashi
1973; Loope and Medeiros 1994). Alternating years of
synchronized flowering with low flowering years may
help to minimize seed predation over the long term.
Conservation implications
The presence of an Allee effect in the Haleakala
silversword has important implications for the persistence
of this species, because at small population sizes, low
numbers of flowering plants will lead to reduced reproductive success for most individuals. This will in turn
likely impact future population size. Although the link
between seed production and recruitment is not precisely
known, due to seed dormancy, population monitoring
studies indicate that recruitment is greater following years
of high flowering (Forsyth and Loope, unpublished data).
The mechanism underlying this Allee effect suggests that
population persistence is not only dependent on population size, but also on the spatial distribution of flowering
plants, annual flowering patterns, and pollinator activity
and efficiency as well. Also, a pollinator-mediated Allee
effect could be exacerbated by reduced pollinator abun-
dance or efficiency, which in this system is a likely
consequence of the current Argentine ant invasion (Cole
et al. 1992; Forsyth 2002).
Density-dependent seed set in the Haleakala silversword also has important implications for restoration
efforts on the Hawaiian volcano, Mauna Kea. The
critically endangered Mauna Kea silversword (A. sandwicense subsp. sandwicense) is currently the focus of a
large-scale reintroduction effort on the Island of Hawaii
(Robichaux et al. 2000). Because the Mauna Kea
silversword is also strongly self-incompatible (Carr et
al. 1986), low densities of individuals will likely exhibit
reduced reproductive success. Outplanting individuals at
higher densities may serve to alleviate the negative effects
of density-dependent seed set.
In combination, results of this study provide strong
evidence for a pollinator-mediated Allee effect in the
Haleakala silversword. Allee effects may be prevalent in
plants, particularly in self-incompatible species that rely
on animal vectors for pollination. As plant population
sizes begin or continue to decline, due to factors such as
habitat fragmentation, harvesting, or invasive species,
extinction risks may be heightened due, in part, to Allee
effects. Such possibilities point to the need to better
understand factors influencing plant reproduction, particularly for rare and endangered species, including how
reproductive success is affected by changes in population
size. Evaluating Allee effects and determining threshold
population sizes, below which individual reproduction is
reduced, should be a critical step in the management and
conservation of rare plant species.
Acknowledgements I thank Clare Aslan for assistance in the field
and laboratory, and Regis Ferriere for inspiring discussion. Much
thanks to Lloyd Loope and Ron Nagata for logistical support at
Haleakala National Park. Rob Robichaux, Judie Bronstein, Lucinda
McDade, Molly Hunter, Nick Waser and an anonymous reviewer
provided valuable feedback on earlier drafts of this manuscript.
This project was funded by the National Science Foundation
(Graduate Research Fellowship), the National Parks Conservation
Association, and the Department of EEB at the University of
Arizona. This manuscript was submitted to the University of
Arizona in partial fulfillment of requirements for the degree of
Doctor of Philosophy.
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