Journal of Tropical Ecology (2012) 28:233–242. © Cambridge University Press 2012
doi:10.1017/S0266467412000119
Demography of Cycas micronesica on Guam following introduction
of the armoured scale Aulacaspis yasumatsui
Thomas E. Marler∗,1 and John H. Lawrence†
∗
Western Pacific Tropical Research Center, CNAS, University of Guam, UOG Station, Mangilao, Guam 96923, USA
† United States Department of Agriculture, Natural Resources Conservation Service, Mongmong, Guam, 96910, USA
(Accepted 4 February 2012)
Abstract: Following the 2003 invasion of the armoured scale Aulacaspis yasumatsui to Guam, changes to population
traits of the dominant Cycas micronesica were determined. Belt transects with a width of 4 m and an average length of
120 m were established in October 2004 to document plant mortality until January 2011. Stem height, basal diameter
and leaf number were also measured for each plant and used to determine density, demography and allometric
relationships. Allometric traits and a left-skewed demographic structure of the pre-invasion C. micronesica habitat
documented a thriving population with high recruitment potential. Aulacaspis yasumatsui dispersed into the study site
4 mo after the initial census. All seedlings were killed within 9 mo and all juvenile plants were killed within 40 ±
10 mo. Mortality reached 92% by 6 y after chronic scale infestations. Allometry and demography of the 2011 survivors
described a collapsing C. micronesica population of stressed and reproductively challenged trees with no recruitment.
This classic example of the enemy release hypothesis has resulted in a homogeneous decline in plant density from
2007–2011. The trend predicts extirpation of C. micronesica from west Guam habitats by 2019.
Key Words: Cycadaceae, endangered species, Guam, invasion ecology, oceanic islands, population dynamics, survival
INTRODUCTION
Populations of many island endemic species are
threatened by human-induced environmental changes.
The challenge confronting island ecologists is to clearly
identify causal mechanisms and unambiguous metrics to
measure and document changes in population viability.
The unintentional introduction of alien species to insular
areas is one means by which human activity disrupts
ecological processes, and small oceanic islands are exceedingly vulnerable to these disruptions. Specialist arthropod
herbivore invaders are particularly threatening to plants
in insular areas because the native plants lack a shared
evolutionary history with the invader (Elton 1958), and
the invaders are not constrained by the natural pressures
of their native range (Keane & Crawley 2002).
The armoured specialist scale Aulacaspis yasumatsui
was described from collections in Thailand (Takagi 1977)
and is known to attack several cycad genera. It was
unintentionally introduced into southern Florida about
20 y ago (Howard et al. 1999). Florida was a major
1
Corresponding author. Email: tmarler@uguam.uog.edu
producer and exporter of Cycas revoluta Thunb., an
economically significant landscape standard globally.
Exportation of C. revoluta resulted in the sequential
dispersal of A. yasumatusi in numerous settings globally.
Aulacaspis yasumatsui was documented in Hawaii in 1998
(Heu et al. 1999), in Guam in 2003, and its dispersal
from the initial outbreak site within urban landscapes
into native limestone forest habitat was confirmed in early
2005 (Terry & Marler 2005).
The endemic range for Cycas micronesica (Hill 2004)
extends from some islands in the Republic of Palau as the
southern boundary through Yap State in the Federated
States of Micronesia, Guam, and Rota in the Marianas
as the northern boundary. Forest inventories in 2002
revealed C. micronesica was the most abundant tree species
in Guam’s various habitats (Donnegan et al. 2004). Cycas
micronesica is the only native host of A. yasumatsui on
Guam, raising concerns about a possible decline of the
cycad and its mutualists, as well as potential negative
cascading ecosystem responses (Moir et al. 2011). The
unique attributes and dominant status of this cycad validate the prediction that its removal from native forests will
exert manifold ecological changes. These changes require
experimental and conceptual effort to be fully understood.
234
Demographic studies are an important tool for
evaluating the condition of plant populations and
monitoring changes in population status over time
(Schemske et al. 1994). Our objective in this study
was to assess recent changes in the demography of
Guam’s C. micronesica population, monitoring what
started as a healthy, stable cycad population. We
quantified size-based patterns of mortality and changes
to the demography and allometric traits of this
population after successive migrations of A. yasumatsui.
Long-term infestations of this armoured scale lead
to sequential defoliation events with each successive
flush of leaves generating fewer and smaller leaves, a
process that ultimately results in plant death (Terry
& Marler 2005). The roots and pachycaul stems of
healthy cycads are comprised mostly of live parenchyma
tissues containing abundant starch (Marler et al. 2010,
Norstog & Nicholls 1997). Therefore, our hypothesis
was the initial pool of non-structural carbohydrate as
dictated by size of the plant correlates with length
of time from initial infestation until plant death. Our
results will inform ecological principles of rare plant
populations in small islands and fragmented continental
populations.
THOMAS E. MARLER AND JOHN H. LAWRENCE
Plot establishment and multi-trophic developments
We established four belt transects with a width of 4 m
and an average length of 120 m (range 102–142 m) in
October 2004. The initial number of plants within the
transects was 687. We re-visited the study site weekly
thereafter to ensure accurate assessment of the initial
dispersal of A. yasumatsui within the study site. This
occurred in January 2005. We purposely introduced the
armoured scale predator Rhyzobius lophanthae Blaisdell
(Coleoptera, Coccinellidae) to Guam in November 2004,
and made a release at the study site in February
2005 (Moore et al. 2005). We also discovered Chilades
pandava Horsfield, a Cycas-specific butterfly that feeds
on young, expanding tissues, in the study site in 2005
(Moore et al. 2005). Its discovery validated yet another
problematic alien introduction to Guam. An ephemeral
irruption of Dihammus marianarum Aurivillius (Marler &
Muniappan 2006) occurred within the study site in late
2007. This native longhorn beetle is a borer that feeds
on C. micronesica stems, primarily on stressed plants.
A temporary decline in the R. lophanthae population
occurred in late 2008, which initiated a secondary
irruption of A. yasumatsui. This epidemic was also shortlived.
METHODS
Measurements and data analysis
Study site
We visited the site approximately annually to conduct a
type I right-censoring approach (Pyke & Thompson 1986)
in which we documented plant mortality to January
2011. Plants in the initial census were tagged to ensure
accuracy during subsequent data collection. In addition
to the survival data, we measured stem height, basal
diameter and leaf number for each individual plant. As an
estimation of reproductive effort, sex was assigned to each
individual using any signs of reproductive structures.
This approach included documenting any persistent
reproductive structures from past reproductive events,
not just the current season’s structures.
We calculated the density of plants from each census
within height categories. The data were organized as
a two-factor (height category × month of census)
ANOVA using SAS Proc GLIMMIX with AR(1) covariance
structure, with month treated as a repeated-measures
variable. In addition, we organized juvenile plants less
than 100 cm in height into four size categories then
recorded the number of months required for each
height category to reach 100% mortality. A singlefactor ANOVA was performed using SAS Proc GLM. We
compared 2004 and 2011 frequency data among various
size categories for stem height, stem diameter and leaf
number with the Wilcoxon rank-sum test (Wilcoxon
1945) using SAS Proc NPAR1WAY. For describing size
Following the 2003 unintentional introduction of A.
yasumatsui to Guam, we scouted various native forest
habitats to locate a representative study site where we
could determine population-level responses to anticipated
migrations of A. yasumatsui. We selected a high-density,
healthy population in western Guam where Cycas
micronesica stem density was in excess of 3500 plants
ha−1 . This site resides within the federally managed
Guam National Wildlife Refuge, centred at 13.645278◦ N,
144.858333◦ E. The complex of soils is dominated by
a clayey-skeletal, gibbsitic, non-acid, isohyperthermic
Lithic Ustorthents (Young 1988). This soil supports
most of the highest-density cycad habitats on Guam.
The C. micronesica population is the most genetically
isolated population on Guam, and deserves paramount
conservation efforts (Cibrián-Jaramillo et al. 2010).
Several ecological studies have been conducted at this site,
providing a more robust understanding of the site than
many other candidate sites. Its vegetation is classified as
secondary limestone forest, with Aglaia, Ficus, Meiogyne,
Macaranga, Neisosperma, Ochrosia, Pandanus, Premna and
Pisonia being the common native genera. In addition to
invasive insects, this habitat is severely threatened by two
feral ungulate species and invasive plants.
Scale insect invasion alters cycad demography
235
Figure 1. Demographic characteristics of Guam’s Cycas micronesica population in October 2004 (left column, n = 687) 4 mo prior to the establishment
of the invasive Aulacaspis yasumatsui in the study area and in January 2011 (right column, n = 57) after 72 mo of scale infestation. Percentage of
individuals within height categories in 2004 (a) and 2011 (b). Percentage of individuals within stem diameter categories in 2004 (c) and 2011 (d).
Percentage of individuals within total leaf number categories in 2004 (e) and 2011 (f).
distributions, we calculated the skewness and kurtosis
(Groeneveld & Meeden 1984, Joanes & Gill 1998) then
employed the Lilliefors goodness-of-fit test for normality
(Lilliefors 1967). For allometric relations, we used log10 transformed data to determine log-log linear relationships
between stem height and diameter, stem height and leaf
number, and stem diameter and leaf number for the 2004
and 2011 data. First we determined the slope of each
regression for each transect. Thereafter a dataset was
created with the slope as the response variable and a
single-factor ANOVA was performed using SAS Proc GLM.
diameter and total leaf number (Figure 1, Table 1). The
degree of skewness and kurtosis was greatest for leaf
number. Variation in plant density over time revealed the
main effects of height category (F = 31.0, df = 5,126, P ≤
0.0001) and census date (F = 128, df = 6,126, P ≤
0.0001) were significant, as was their interaction (F =
40.1, df = 30,126, P ≤ 0.0001). The initial decline
in density of seedling and juvenile plants 1–100 cm
in height was extreme, whereas the decline in density
of plants above 100 cm in height was more gradual
(Figure 2). All seedlings within the transects were killed
within 9 mo after the initial A. yasumatsui infestation.
RESULTS
Timing of juvenile mortality
Population demography
The 2004 C. micronesica population presented a leftskewed frequency distribution for stem height, stem basal
The number of months required for juvenile plants to
reach 100% mortality differed among four 25-cm height
increments (F = 6.4, df = 4,15, P ≤ 0.0033). Mortality of
236
THOMAS E. MARLER AND JOHN H. LAWRENCE
Table 1. Characteristics of frequency distributions among size categories
for Cycas micronesica stem height, stem diameter and leaf number in
October 2004, 4 mo prior to the establishment of Aulacaspis yasumatsui
in the study area (Before) and in January 2011, 72 mo following the
invasion event (After).
Table 2. Time required for juvenile Cycas micronesica
plants to suffer 100% mortality following Aulacaspis
yasumatsui establishment, as documented by 25-cmincrement height categories, P ≤ 0.0033, n = 4
transects. Least square means with the same letter
are not significantly different.
Characteristic
Stem height
Lilliefors test statistic
Skewness
Kurtosis
Stem diameter
Lilliefors test statistic
Skewness
Kurtosis
Leaf number
Lilliefors test statistic
Skewness
Kurtosis
Before
After
0.444
1.99
6.56
0.328
0.601
3.47
0.425
1.66
4.61
0.247
−0.635
2.67
Size category (cm)
0.517
3.78
17.8
0.450
158
27 000
1–25
26–50
51–75
76–100
Time (mo)
25 A
31 AB
34 AB
40 B
that for the 2004 population (Figure 3). Additionally, the
range of the data for all three regressions in 2011 was
severely constricted by the plant mortality after 6 y of A.
yasumatsui infestations.
Population trait changes
Figure 2. The influence of plant height size categories (cm) on survival of
Cycas micronesica following the establishment of Aulacaspis yasumatsui
in western Guam. The x-axis refers to January of each calendar year.
Arrow on x-axis marks the initial infestation of A. yasumatsui in the
study habitat.
the 1–25-cm category required about 2 y, while that of the
76–100-cm category required a mean of more than 3 y
(Table 2). The census confirming ultimate loss of the final
juvenile plant was the January 2010 census. At this stage
when all of the juvenile plants had been killed, the mature
plants above 100 cm in height were at 73% mortality.
Allometric patterns
Differences in the slope of the 2004 versus 2011
populations of C. micronesica were apparent for stem
height versus diameter (F = 55.9, df = 1,6, P ≤ 0.0003),
stem height versus leaf number (F = 130, df = 1,6, P ≤
0.0001) and stem diameter versus leaf number (F =
143.3, df = 1,6, P ≤ 0.0001). The 2011 population
exhibited a slope for height versus diameter that was 40%,
a slope for height versus leaf number that was 10%, and
a slope for diameter versus leaf number that was 13% of
The distribution of size categories in the 2004 population
differed significantly from that in the 2011 population
for stem height (Wilcoxon statistic = 37, P ≤ 0.0301),
stem diameter (Wilcoxon statistic = 40, P ≤ 0.0061),
and leaf number (Wilcoxon statistic = 36, P ≤ 0.0453).
Following 6 y of A. yasumatsui damage this population
of C. micronesica exhibited a unimodal pattern for stem
height (Figure 1). The degree of skewness declined to 30%
of the 2004 values, and the degree of kurtosis declined to
about half of the 2004 values (Table 1). The left-skewed
2004 distribution of stem diameter was reversed by
6 y of damage to become a right-skewed pattern
(Table 1, Figure 1). The left-skewed 2004 distribution
of leaf numbers was retained in the 2011 population
(Figure 1). In fact, this skewed pattern was magnified
by the response to years of A. yasumatsui damage
as evidenced by a 42-fold increase in skewness
(Table 1). The lowest leaf number category increased
from c. 75% of the 2004 population to more than
90% of the 2011 population. Furthermore, the three
largest leaf number categories from the 2004 census
declined to zero by the 2011 census. The lowest
leaf number categories in 2004 were due to the
prevalent seedling and juvenile populations. In contrast,
the 2011 data did not include any plants less than
100 cm in height, so the trend of declining leaf number per
plant occurred within a remaining population exclusively
comprised of mature plants. Lilliefors test statistic revealed
strong evidence against normality for every population
test (Table 1). The 2011 results portray the absence
of seedling and juvenile plants and predict imminent
population decline.
In order to increase our understanding of how 6 y of A.
yasumatsui attack changed the C. micronesica populations,
we calculated mean ± SE for several before–after variables
(Table 3). Total plant density declined to 8% of initial
Scale insect invasion alters cycad demography
237
Table 3. Characteristics of Guam’s Cycas micronesica population in
October 2004, 4 mo prior to the establishment of Aulacaspis yasumatsui
in the study area (Before) and in January 2011, 72 mo following the
invasion event (After). n = 4 transects, mean ± SE.
Characteristic
Plant density (stems ha−1 )
Mean mature tree leaf number
Mean mature tree height (cm)
Total stem basal area (m2 ha−1 )
Quotient sexed trees
Before
After
3580 ± 153
85 ± 8
244 ± 10
93.7 ± 12.5
0.49 ± 0.04
290 ± 63
20 ± 3
258 ± 5
28.2 ± 6.3
0.33 ± 0.09
The male/female quotient among these sexed individuals
was 0.73 in 2004 and 0.63 in 2011, signifying an
increase in the ability to identify signs of female plants
relative to that of male plants.
Recruitment
Figure 3. Allometric relations of Guam’s Cycas micronesica population in
October 2004, 4 mo prior to the establishment of the invasive Aulacaspis
yasumatsui in the study area and in January 2011, after 72 mo of scale
infestation. Height versus diameter slope was 1.62 for 2004 and 0.65
for 2011 (a). Height versus leaf number was 1.28 for 2004 and 0.11 for
2011 (b). Diameter versus leaf number was 0.71 for 2004 and 0.09 for
2011 (c).
plant density, and mean leaf number for mature plants
declined to 24% of initial leaf number. Range in leaf
number for mature plants was 21–229 in 2004 and 1–72
in 2011. These characteristics of changes in leaf number
explain the drastic changes in the regressions of height
versus leaf number and diameter versus leaf number
(Figure 3). In 2004 all of the individuals with few leaves
were seedlings and small juveniles, so the y-intercept was
near the origin as both factors scaled together. In contrast,
the y-intercepts for both height and diameter were quite
large for 2011 plants because all of the individuals with
few leaves were large mature specimens.
Mean height of mature trees exhibited a non-significant
increase following 6 y of A. yasumatsui damage, while
total stem basal area declined to 30% of the initial basal
area during the same period (Table 3). About half of the
mature tree population could be sexed in 2004, but only
about a third of the 2011 population could be sexed
(Table 3), indicating a decline in reproductive effort
among the few remaining C. micronesica plants on Guam.
This site contained C. micronesica seedlings at the density
of 602 ha−1 in 2004. These were all killed within 9 mo
of scale infestation, and the census in 2005 revealed a
complete lack of seedlings. As the R. lophanthae predator
began to exert some biological control of the damage by A.
yasumatsui, but before the mature plant health declined
substantially, a few new seedling recruits were apparent
in this habitat. This was revealed as 118 seedlings ha−1
in January 2007 and 28 seedlings ha−1 in January 2008.
All of these seedlings were killed by direct A. yasumatsui
damage before the three-leaf stage. As mature plant
health continued to decline with each passing year, seed
production and quality declined. As a result, no new
seedlings have been observed persisting in this habitat
since 2008.
An unusual increase in recruitment into the 1–100cm height category occurred in 2010. This was not
the normal growth increment increase that promoted
a cohort of individuals from the seedling category into
the juvenile category. Instead, it occurred because many
mature plants lost most of their stem height due to
the D. marianarum tunnelling that peaked in 2007–
2008. This is the typical historical response to this
pest where the entire upper portion of the stem and
leaves dies back to about 1 m height. The phenomenon
decreased calculated plant density within some of the
taller categories, but not due to mortality. It also increased
plant density in the 1–100-cm category, but not due to
normal growth increment recruitment. This also partly
explains the atypical height versus diameter slope for the
2011 population by constricting the height range without
a parallel constriction of the diameter range (Figure 3).
DISCUSSION
We present a north-western Pacific island case study
describing the consequences of a predicted invasion that
238
empirically supports the contention that island-endemic
plant populations are acutely susceptible to invasive
herbivores (Meyer & Butaud 2009). This is also a classic
example of the enemy release hypothesis (Elton 1958,
Liu & Stiling 2006, Norghauer et al. 2011). First, A.
yasumatsui populations within the scale’s native range cooccur with healthy native Cycas populations that exhibit
scale infestations but are not severely threatened (Tang
et al. 1997). Second, many mature C. micronesica trees died
during less than 1 y of A. yasumatsui infestation before R.
lophanthae became well-established, but after its effective
establishment the R. lophanthae predator has allowed
many trees to survive 6 y of A. yasumatsui infestation.
Third, C. micronesica plants growing in ex situ plantings
in Thailand where A. yasumatsui is controlled by various
natural enemies do not exhibit greater susceptibility to A.
yasumatsui infestations than other congeneric plants (A. J.
Lindström, unpubl. data). Our results empirically validate
the designation of endangered status for C. micronesica by
the International Union for Conservation of Nature and
Natural Resources.
Initial establishment of A. yasumatsui in the study site
preceded that of R. lophanthae. This enabled a brief period
of A. yasumatsui infestation without biological control.
Unfortunately the size differential between R. lophanthae
and A. yasumatsui limits ongoing efficacy of biological
control, as the scale is able to find locations on the
Cycas plant body that the predator cannot access (Marler
& Moore 2010). Regardless, the long-term protection
afforded by this predator is undoubtedly responsible for
the mature trees that are still alive today.
Size-related impacts
The first year of C. micronesica mortality following
A. yasumatsui infestation was comprised primarily of
seedlings. As time passed the loss of seedlings was
sequentially followed by 100% mortality of plants within
the height range 1–25 cm, 26–50 cm, 51–75 cm, and
finally 76–100 cm. These results for seedling and juvenile
plants up to 100 cm in height were consistent with
our hypothesis. Moreover, they lend evidence for the
hypothesis that carbon limitations and starvation are
universal mechanisms of tree decline following biotic or
abiotic stresses (McDowell et al. 2008).
Unlike juvenile plant mortality, the mature plants
appeared to exhibit no overt relationship of size category
to survivorship. First, the mean height of mature trees
did not change during the time frame of this study
(Table 3), despite mortality and removal from the
population of 75% of the mature trees. Second, 19%
of the mature trees in excess of 100 cm in height died
within 9 mo of A. yasumatsui infestation, and these plants
were distributed randomly among mature size categories
THOMAS E. MARLER AND JOHN H. LAWRENCE
rather than showing a left-skewed trend whereby the
smallest mature trees were preferentially killed. Third,
although we cannot determine the timing of 100%
mortality for any of the mature tree size categories to
date, we can determine the time to reach 50% mortality.
The transition to at least 50% mortality occurred in
the January 2007 census for 101–200-cm, 201–300cm and 401+ cm categories. This level of mortality for
the 301–400-cm category was evident in the January
2009 census. Therefore, the benefits of being large are
very clear for juvenile plants, but less clear for mature
plants. Other factors may explain which mature trees are
most susceptible to A. yasumatsui damage, such as the
available pool of carbon reserves at the time of initial
infestation (Galiano et al. 2011).
Determining the influences of climatic, edaphic, biotic
and demographic factors on stand-level die-back may
aid in understanding the underlying causes of tree death
(Mueller-Dombois 1986, 1987). Mortality of the mature
plants in our study appears to conform to Manion’s conceptual model of tree disease (Manion 1981). This model
posits that pre-disposing factors render an individual more
or less vulnerable to subsequent stresses, which then
decrease vigour and increase vulnerability prior to imposition of the next stress. Ultimately a newly imposed stress
can cause a final vigour decline and subsequent death.
The chronic attack by A. yasumatsui imposed the major
stress factor that contributed to this ongoing phase of
mature C. micronesica plant mortality. However, other biological factors contribute to the compilation of stressors.
Contributing factors adding to the A. yasumatsui
pressure include the chronic pressure of Chilades pandava
(Moore et al. 2005) and Erechthias sp. (Marler &
Muniappan 2006) infestations. The combination of these
three alien arthropod pests, all of which are very recent
unintentional introductions on Guam, does not allow C.
micronesica plants the time to adequately recover carbon
from the naturally long-lived leaves following initial
leaf construction. This forces the plant into a chronic
state of carbon deficit. In addition to these leaf feeders,
the stem borer D. marianarum (Marler & Muniappan
2006) is a native longhorn beetle that preferentially
attacks stressed plants, a behaviour common among
other Cerambycidae stem borers. Feral ungulates are also
threatening the health of remaining plants, as the pig (Sus
scrofa L.) consumes stems and the deer (Cervus mariannus
Desmarest) consumes leaves and reproductive organs,
adding to the multiple compounding insults from alien
pests to this island endemic.
Stand structure
Understanding the structure of a plant population enables
the assessment of regeneration processes and reflects on
Scale insect invasion alters cycad demography
the population health. The left-skewed size structure of
Guam’s C. micronesica population prior to A. yasumatsui
damage is often called reverse-J shape, conforming to
a Type III curve according to Deevey (1947) or Type I
curve according to Bongers et al. (1988). This structure
suggests copious fecundity and favourable site conditions
for establishment and survival of seedlings. Indeed, only
one-third of the 2004 population was comprised of
mature trees greater than 100 cm in height. The leaf
number size class distribution exhibited more asymmetry
and a broader peak in the distribution curve than did
the stem height or stem diameter size class distribution,
as evidenced by the extent of skewness and kurtosis
(Groeneveld & Meeden 1984, Joanes & Gill 1998).
The ability of larger plants to delay mortality following
A. yasumatsui infestation generated extreme changes
in population structure. Therefore, only 6 y after A.
yasumatsui migrated into the study site a left-skewed
C. micronesica population exhibiting healthy trees with
bountiful active recruitment, this same population was
transformed into a unimodal stem height structure and
a right-skewed stem diameter structure comprised of
unhealthy trees exhibiting no recruitment.
Although the general trend of the 2004 population was
clearly left-skewed, this cycad population exhibited more
than twice as many trees within the 201–300-cm height
category than within the 101–200-cm height category
(Figure 2). This anomaly in what would have otherwise
been a smooth curve may signify an ephemeral pulse in
recruitment at some historical period that enabled the
greater number of 201–300-cm trees, or alternatively a
more recent decline in recruitment that resulted in the
smaller number of 101–200-cm trees. Perhaps habitat
destruction during establishment of copra plantations in
the 20th century and as a result of military operations
and construction during and following World War II,
or the cumulative impacts of these events combined
with natural climatic events may explain these results.
Alternatively, the extent of ecosystem destruction during
the direct hit of several major typhoons striking Guam
in the past century may partly explain the anomaly.
Unfortunately, no reliable historical records are available
that permit us to definitively establish any single cause
or any series of events that influenced C. micronesica
demography or the subsequent recovery of this
habitat.
Death of a portion of juvenile C. micronesica plants
shortly after the A. yasumatsui invasion caused significant
changes on allometric relations for the juvenile survivors
(Niklas & Marler 2008). Here we have extended the
results to include the changes in allometry for the entire
population after 100% removal of the juveniles and 75%
removal of the mature plants. The slope and range in
data were severely decreased by the selective removal of
C. micronesica plants by the invasive pest.
239
Other cycads
Cycads are the most threatened group of plant
species on Earth (Hoffmann et al. 2010). Despite this
unfortunate conservation condition and the importance
of demographic studies to assess population status, only
a few of the c. 300 described cycad species (Donaldson
2003) have been the subject of demographic studies.
Merely one of these focused on a congeneric of our
study species, when Keppel (2001) determined height
class distribution of one Cycas seemannii population. Other
relevant studies included Ceratozamia matudae (PérezFarrera & Vovides 2004a, 2004b), Ceratozamia mirandae
(Pérez-Farrera & Vovides 2004b, Pérez-Farrera et al.
2006), Dioon edule (Vovides 1990), Dioon merolae (LázaroZermeño et al. 2011), Zamia debilis (Negron-Ortiz &
Breckon 1989) and Zamia soconuscensis (Pérez-Farrera &
Vovides 2004b).
Without exception, these studies revealed populations
that generally conformed to the classic left-skewed size
class structure. Our report, therefore, stands out as the
first to describe a unimodal population status for a cycad
habitat as evidence of a severely threatened population.
Furthermore, ours is the first study to our knowledge
that has quantified the size-structure response of a cycad
population to a biotic or abiotic disturbance by comparing
pre- and post-disturbance status within the same habitat.
Prognosis
Our results provide empirical evidence that supports
the endangered status of C. micronesica and highlight
concerns about ecosystem processes that will be impacted
by the loss of this native cycad. Gestalt comparison
of a Guam forest before and after the consequences of
this invasion (Figure 4) reveals immeasurable changes
to biotic and abiotic characteristics. An immediate
research focus on changes to habitat- and ecosystemlevel processes that result from the epidemic mortality of
this species is warranted, as the changes in population
density are of such great magnitude and speed. The
window of opportunity to quantify these rapid changes
has already been compromised for this island population,
highlighting the importance of securing data prior to
predicted disturbances to serve as benchmarks.
Compounding negative impacts visited on this and
other native plant communities are anticipated with
future waves of biological invasions associated with the
nascent military build-up on Guam (Marler & Moore
2011). Guam’s dominant native trees are ecologically
well adapted to local soils and climate, and have
fundamental cultural and economic significance. The
continued loss of ecologically significant plants and
habitat will continue to be disastrous for the island,
240
THOMAS E. MARLER AND JOHN H. LAWRENCE
predicts a typhoon event will occur prior to the predicted
2019 extirpation. The poor health status of remaining
trees indicates that the natural resilience of this taxon
to typhoon damage has been decreased by the chronic A.
yasumatsui damage, a contention that has yet to be tested.
In contrast to these factors that may increase mortality
rate, a factor that has the potential to ward off extirpation
is the purposeful introduction of a second and hopefully
more effective biological control agent. A parasitoid would
be a better candidate for a second biological control agent,
as a second predator species may be impaired by the
same limitations that prevent R. lophanthae from being
completely effective.
During the time frame of this Guam study, A. yasumatsui
invaded Rota in 2007 and Palau in 2008. Our striking
results serve as a benchmark for comparative purposes as
the influence of this pest on the C. micronesica populations
in Rota and Palau should be determined in the future.
ACKNOWLEDGEMENTS
Figure 4. General appearance of a high density Cycas micronesica habitat
prior to the invasion of Aulacaspis yasumatsui (a). General appearance of
the same habitat 29 mo after the initial infestation of A. yasumatsui (b).
underscoring the importance of empirical studies to
inform conservation decisions.
The surviving C. micronesica population on Guam is
rooted in an expiring timer to a bomb of unknown
ecological impacts, with a short but uncertain amount of
time left on the timer. If the ongoing negative population
density trajectory established over the past 4 y is
sustained, extirpation will occur in 2019. However, an increase in biotic disturbances would likely reduce this time
frame, an outcome that may materialize as the invasion
of yet another Cycas pest or as another irruption of one of
the existing pests. Abiotic disturbances that may similarly
shorten the time frame include damage by a tropical
cyclone or a severe dry season. Concerns about the threat
of tropical cyclone damage are especially warranted for
Guam habitats, as the average return time for typhoons
over a 54-y monitoring period was 4.7 y (Guard et al.
1999). Endemic species such as C. micronesica cannot escape damage during the more powerful typhoons (Marler
& Hirsh 1998). However, in the absence of subsequent
disturbances a healthy C. micronesica plant is resilient
to typhoon damage (Hirsh & Marler 2002). Guam has
not experienced a major typhoon since the unintentional
introduction of A. yasumatsui in 2003, so probability
This project was made possible in part by National Science
Foundation SGER No. 0646896, USDA CSREES Project
No. 2003-05495, US Forest Service Project No. 06-DG11052021-206, No. 09-DG-11052021-173 and No. 10DG-11059702-095 to TEM. This material was made
possible, in part, by a Cooperative Agreement from the
United States Department of Agriculture’s Animal and
Plant Health Inspection Service (APHIS). It may not
necessarily express APHIS’ views.
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