Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 November 2024 | 16(11): 26150–26162
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.9110.16.11.26150-26162
#9110 | Received 19
April 2024 | Final received 27 August 2024 | Finally accepted 30 October 2024
Decades of IUCN recommendations
for biocontrol of invasive pest on the Guam cycad: you can lead policy-makers
to conservation proposals but you cannot make them
follow
Thomas E. Marler
1, Anders J. Lindström 2
, L. Irene Terry
3 & Benjamin E. Deloso 4
1 Philippine
Native Plants Conservation Society Inc., Ninoy Aquino Parks and Wildlife
Center, Elliptical Road, Quezon City 1101, Philippines.
2 Global Biodiversity Conservancy,
144/ 124 Moo 3, Soi Buathong,
Bangsarae, Sattahip, Chonburi 20250, Thailand.
3 School of Biological Sciences,
257 South 1400 East, University of Utah, Salt Lake City, UT 84112 USA.
4 International Center of Tropical
Botany, Institute of Environment, Department of Biological Sciences, 3959
Douglas Road, Florida International University, Miami, FL 33133 USA.
1 thomas.marler@gmail.com
(corresponding author), 2 ajlindstrom71@gmail.com, 3 irene.terry@utah.edu,
4 bdelo005@fiu.edu
Editor: Mike Maunder, Biodiversity, Restoration and
Conservation, Crediton, United Kingdom.
Date of publication: 26
November 2024 (online & print)
Citation: Marler, T.E., A.J. Lindström,
L.I. Terry & B.E. Deloso (2024). Decades of
IUCN recommendations for biocontrol of invasive pest on the Guam cycad: you can
lead policy-makers to conservation proposals but you
cannot make them follow. Journal of Threatened Taxa 16(11): 26150-26162. https://doi.org/10.11609/jott.9110.16.11.26150-26162
Copyright: © Marler et al. 2024. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use,
reproduction, and distribution of this article in any medium by providing
adequate credit to the author(s) and the source of publication.
Funding: None.
Competing interests: The authors declare no competing interests.
Author details & contributions: : Thomas Marler is a conservation physiologist who has studied terrestrial plant species in western Pacific island nations for 30+ years. He has pioneered adaptive management research of the endangered Cycas micronesica, and wrote the original draft of the manuscript. Anders Lindström is a cycad taxonomist and curator of the Living Plant Collections at Nong Nooch Tropical Botanical Garden, Chonburi, Thailand, was directly involved in manuscript conceptualization, and reviewed and edited several versions of the manuscript. Irene Terry is a pollination and conservation biologist who has studied the chemistry of cycad cone volatiles involved with pollination for 20+ years, including research on pollination and conservation of Cycas micronesica, and she worked on several drafts of the manuscript. Benjamin Deloso is a botanist pursuing his PhD degree at Florida International University and is broadly interested in cycad biology and taxonomy, as well as the flora of the Pacific. He worked on several drafts of the manuscript. All four authors are contributing members of the Cycad Specialist Group of the IUCN Species Survival Council and have conducted in situ and ex situ research addressing Cycas micronesica biology, conservation, and ecology.
Acknowledgements: We thank John Donaldson and Patrick Griffith
for able administration of the Cycad Specialist Group, and all contributing
members who have devoted their time and knowledge toward the advancement of
cycad conservation.
Abstract: Guam’s cycad known as Cycas micronesica has been threatened by a coalition of
invasive herbivore species, and the armored scale Aulacaspis
yasumatsui has emerged as the primary threat.
This lethal cycad pest invaded Guam in 2003, and the Species Survival Council
of the International Union for Conservation of Nature (IUCN) began publishing
recommendations addressing protection of the cycad population in 2005.
Sustained epidemic mortality caused the addition of C. micronesica to the United States Endangered Species
Act in 2015. The need to establish a sustainable coalition of biological
control organisms has been the constant advice throughout almost two decades of
recommendations, yet the decision-makers who controlled the direction of policy
and funding have not responded to the advice with success. Therefore, we
describe the history of publications in which the IUCN has asserted that this
singular conservation action is urgently required to save the cycad species. We
then summarize contemporary recommendations to address the ongoing threats to
this and other insular cycad species.
Keywords: Aulacaspis
yasumatsui, biological control, conservation
science, Cycas micronesica, Rhyzobius lophanthae.
Abbreviations: CAS—Aulacaspis
yasumatsui, Cycad Aulacaspis
Scale | CSG—Cycad Specialist Group, Species Survival Council, IUCN | ESA—United
States Endangered Species Act | GBF—The Kunming-Montreal Global Biodiversity
Framework | IUCN—International Union for Conservation of Nature | USFWS—United
State Fish & Wildlife Service.
Introduction
The cycad Cycas micronesica
K.D.Hill grows among numerous disjunct ecological
niches in the Mariana Islands, the Federated States of Micronesia, and the
Republic of Palau (Hill 1994, Figure 1). The arborescent cycad species exhibits
morphological traits that are typical of cycads, with large pinnately compound
leaves radiating from the stem apex (Image 1). The species was the most
abundant tree on Guam in 2002 when an estimated 1.57 million healthy mature
trees existed (Donnegan et al. 2004). At that time,
there were no identifiable threats throughout its indigenous range.
The absence of threats changed in 2003–2005 when Guam was
invaded by the armored scale Aulacaspis
yasumatsui Takagi (Cycad Aulacaspis
Scale, CAS), the leaf miner Erechthias sp.,
and the Cycas-specific butterfly Luthrodes
pandava Horsfield (Deloso et al. 2020). These specialist herbivorous insects
arrived in Guam without their natural predators, finding an abundant population
of hosts that evolved in the absence of native leaf herbivores. The rapid
decreases in health of the attacked cycad trees generated unprecedented
infestations by the native longhorn beetle Acalolepta
marianarum Aurivillius,
which employs the common stem borer behavior of
preferentially attacking unhealthy trees (Marler
2013).
Plant mortality in the urban landscape was immediate, and
plant mortality among in situ habitats began in 2005 (Marler
& Lawrence 2012). A 2013 forest survey revealed only 624,000 C. micronesica trees remained alive, and most of these
were heavily infested with CAS at the time (Lazaro et al. 2020). These findings
indicated 60% of the mature tree population was killed within an eight year
period. Cycas micronesica was listed as
‘Endangered’ under the IUCN Red List in 2006 (Bösenberg
2022a), only three years after the invasion. Members of the Cycad Specialist
Group (CSG) within the Species Survival Commission of the IUCN have provided
informal and formal published recommendations concerning the threats to and
recovery needs of C. micronesica since
2005 when the CAS population began spreading into forest habitats on Guam. The
decades of publications since the beginning of the invasion carry a common
theme: exploit the successes of classical introduction biological control
(Hoddle et al. 2021) of CAS has always been and continues to be the most
important conservation action required for this species recovery.
Most nations do not possess the financial resources to
lead the way in invasion biology adaptive management research. When a wealthy
nation such as the United States experiences a consequential invasion that
foreshadows similar invasions in other nations, the global community looks to
that wealthy nation for knowledge that evolved from their early adaptive
management iterative learning process. Three recent documents highlight how
misdirection of conservation activities since the 2003 Guam invasion has led to
a failure to fully establish biological control of CAS. First, the United
States Fish & Wildlife Service (USFWS) is required to publish a national
recovery plan and five-year status reports informing taxpayers about how the
Endangered Species Act (ESA) is being honored for
each ESA-listed species. Cycas micronesica was
added to the ESA in 2015 (USFWS 2015). The national recovery plan for C.
micronesica has not been formulated to date
despite published documentation of widespread ongoing mortality, and the first
status report for C. micronesica was
published in 2020 (USFWS 2020). This status report described the death of an
estimated 947,556 Guam trees between 2002 and 2012 and highlighted the need for
more research to reduce the impact of cycad pests. Unfortunately, the report
did not list any ongoing or planned conservation actions addressing the
emergency need to establish adequate biological control of CAS. Second, the United
States military owns more land on the island of Guam than any other party, and
the United States Sikes Act requires the publication of a multi-year Integrated
Natural Resource Management Plan to steer conservation efforts. This plan
guides federal resource managers with top-down directives that are used for
developing funded projects. The current plan does not include any information
concerning the emergency need to establish effective biological control of CAS
in Guam (DON 2022). Third, a Habitat Conservation Plan for Guam is being
developed by biologists in the island’s territorial government agencies, and
updates of the draft document are available for review
(http://www.guamhcp.com). The current draft describes numerous expensive C.
micronesica conservation actions including
plant translocations and nursery operations, the need for more research on how
to manage CAS, but again no plans for exploiting the heavily communicated best
available science to establish an effective biological control program. Moreover,
this plan includes the proposed creation of C. micronesica
plants that are genetically resistant to CAS herbivory. While genetic
resistance is a possible explanation for why some of Guam’s C. micronesica trees are still alive today, this has
not been verified to date. The current status of knowledge indicates that
intraspecific or interspecific genetic resistance to CAS herbivory within the Cycas
genus has never been identified. In all countries where CAS is native, no
genetic resistance among the host population has been detected. The CAS is
always controlled by native predators and parasitoids
in its native states. Clearly, the federal and territorial decision-makers who
have been empowered to define the direction of Guam’s recent and impending conservation
actions have steered planning toward activities that have not honored the recommendations from the CSG since 2005.
These Guam developments have created a case study where
the best available science has been ignored and evidence available to inform
urgent conservation actions has been disregarded (Lindström
et al. 2023). The recent invasion of Japan by CAS (Takagi 2023) has caused a
repeat of the initial years following the Guam invasion, with entire crowns of
leaves of the host Cycas revoluta Thunb. population being killed by the CAS herbivory as the
first step in the process that ends in plant death (Image 2). We predict there
will be sustained plant mortality that will endanger C. revoluta
if the Japan decision-makers follow in the footsteps of the Guam
decision-makers by failing to heed the IUCN’s recommendation to establish
immediate biological control of CAS.
Our objective herein is to plainly outline what was
communicated within each of the publications that included germane
recommendations from CSG members since the 2003 invasion in order to
reemphasize that sustainably managing a classical biological control program of
CAS remains the most important conservation endeavor
needed to enable persistence of C. micronesica.
Every citation within the chronological review contained at least one member of
the CSG on the authoring team, ensuring the collective knowledge from the
international experts representing the IUCN directly informed the
recommendations. Thereafter, we provide contemporary recommendations for
funding informative adaptive management conservation actions that acknowledge
the current best management practices based on evidence from the best available
science.
Chronological
review of recommendations prior to ESA-listing
2005
The invasions of Taiwan and Guam by CAS generated the
first two case studies in which a native Cycas species was threatened by
non-native CAS herbivory (Tang & Cave 2016). The threats to Taiwan’s Cycas
taitungensis C.F.Shen, K.D.Hill, C.H.Tsou & C.J.Chen and Guam’s C. micronesica
led the CSG to form a new subgroup in 2005 to address the growing threat to
wild cycad populations posed by the artificial spread of insect pests and
pathogens affecting cycads. This new subgroup immediately published a
recommendation paper in hopes of informing decision-makers in Guam and other
locations (Tang et al. 2005). In addition to respecting the need for employing
methods that reduce the risk of spreading CAS, the need for immediate
identification of biological control organisms was discussed in detail as the
most important permanent response for establishing classical biocontrol in the
location of every new CAS invasion.
A commentary style article was authored by several
resident biologists from Guam (Moore et al. 2005). This article detailed the
initial attempts at establishing introduction biological control on Guam with
the successful establishment of the predator Rhyzobius
lophanthae Blaisdell and the unsuccessful
introduction of the parasitoid Coccobius
fulvus Compere & Annecke.
The authors included the mandate that ultimate construction of effective
multi-species biological control of CAS was the only conservation action that
could ensure the survival of C. micronesica.
A second commentary style article communicated the predicted demise of Guam’s
forests if CAS persisted without biological control into the future, the
unfortunate lack of initial response by the conservation community which
allowed the CAS population to become so well established by 2005, and that a
multi-pronged approach rooted in biological control of CAS would be required to
save the insular cycad species (Terry & Marler
2005).
2012
The Guam community operated during the first few years of
conservation actions without local evidence or relevant data from other
countries. Although numerous countries outside of the native range of CAS had
been invaded prior to 2003 (Marler et al. 2021), no
in situ Cycas habitats had been invaded prior to the Guam invasion.
Several adaptive management projects were initiated which began to inform the
conservation decisions by 2012. The first look at plant mortality from
benchmarked permanent plots in northern Guam was published (Marler
& Lawrence 2012), revealing 92% plant mortality within the first six years
of CAS herbivory. This article pointed to the fact that in situ Cycas
species that thrive within the native range of CAS do not experience lethal threats
because of native biological control, and that ex situ C. micronesica plants growing in Thailand where CAS is
controlled by natural enemies do not exhibit a decline in health despite
experiencing CAS herbivory. The first of numerous recommendations to establish parasitoid biocontrol of CAS on Guam to augment the
predator biocontrol was outlined.
Guam’s urban landscape contained many Cycas revoluta Thunb. plants at the
time of the 2003 invasion. The stem apex of this popular cycad species is
covered with dense tomentum. This plant trait allowed CAS individuals to become
established on cataphyll surfaces because the tomentum excluded the R. lophanthae predators (Marler
2012). The results verified that most Cycas plants contain microsites on
various organ surfaces within which CAS can become established where R. lophanthae cannot physically navigate (Marler et al. 2021). The recommendation to introduce a
smaller biological control organism such as a parasitoid
species was the primary actionable recommendation from this research, as these
smaller CAS enemies may be able to navigate to all CAS infestation sites.
The failures to adequately pursue biological control of
CAS led to the publication of a commentary article in which the ongoing
negative cycad population developments were discussed (Marler
& Terry 2012). Some of the limitations of the R. lophanthae
predator were outlined along with the emergency recommendation of establishing
at least one parasitoid species to augment the
established R. lophanthae predation.
2013
The levels of infestation of CAS, L. pandava, Erechthias,
and A. marianarum were followed from
2005-2013 and the interplay among the four arthropod herbivores became more
fully understood (Marler 2013a). Increases in CAS
damage led to subsequent increases in A. marianarum
damage and subsequent decreases in Erechthias
damage. Alternatively, increases in CAS damage led to concurrent decreases in L.
pandava damage. The need for a parasitoid biological control organism was reiterated,
along with the prediction that future improvements in CAS control may lead to
increases in L. pandava damage.
Experimental elevation of container-grown C. micronesica seedlings within in situ forest settings
revealed that the predator R. lophanthae
was more effective at controlling CAS at higher strata and less effective at
lower strata (Marler et al. 2013). The findings were
discussed along with the recommendation of establishing parasitoid
biological control organisms which may not be constrained by the same stratification
issues.
A commentary article analyzed
various issues regarding stratification of R. lophanthae
predation success (Marler 2013b). The reasons for the
persistence of greater prevalence of CAS on C. micronesica
leaves close to the soil surface were discussed in length. Accurate sampling
methods are required to fully assess biocontrol efficacy, and the vertical
heterogeneity in CAS incidence one decade after the Guam invasion indicated R.
lophanthae biocontrol efficacy was clearly
impaired when cycad leaves persisted close to the soil surface.
A comprehensive listing of known biological control
agents was published to provide the Guam decision-makers the names of the
organisms that could be pursued for immediate introduction to Guam (Cave et al.
2013). The need to introduce at least one parasitoid
to augment the R. lophanthae biological
control was repeated.
2014
The sustained lack of concern toward the need to
biologically control CAS was addressed in another commentary style article (Marler & Lindström 2014).
This opinion article proposed approaches to address stakeholder apathy or
outright objection to the need for urgent conservation interventions when a
native tree species is threatened with extinction. The limitations of R.
lophanthae biological control were discussed
in the context of global invasion science, whereby the Guam case study unfolded
as an example that may inform conservation efforts in other invaded islands
within which initial biological control efforts were unsuccessful.
Summation of
recommendations prior to ESA-listing
Preemptive conservation endeavors may be highly effective for ensuring a proposed
species is not ultimately added to a national endangered list such as the ESA (Treakle et al. 2023; Stanley et al. 2024). The CAS invasion
that caused the ultimate ESA-listing of C. micronesica
was predicted in 2000 (Marler 2000) and occurred in
2003 (Deloso et al. 2020; Marler
et al. 2021). As outlined above, the formal recommendations explicating the
emergency conservation actions required to save C. micronesica
from extinction risk began in 2005 and continued throughout the years prior to
the ESA-listing. Moreover, the United States military was the landowner with
the greatest number of C. micronesica
plants within their custody at the time of the invasion. The deciders
responsible for management decisions concerning federal lands are required by law
to use evidence-based management decisions that respect the best available
science. These deciders who controlled the policy and budget directions were
provided a full decade of IUCN recommendations based on best available science
prior to the ESA-listing. The decisions instead directed planning and
considerable funding into conservation actions that did not address the
recommended biological control of CAS, ensuring the addition of C. micronesica to the ESA.
Chronological
review of recommendations after the ESA-listing
Cycas micronesica was added to the United States ESA in 2015 (USFWS 2015).
Based on United States Forest Service surveys of mature tree populations,
almost 100,000 of Guam’s C. micronesica
trees died each year within one decade after the CAS invasion (Donnegan et al. 2004; Lazaro et al. 2020) and during a
timeframe in which the CSG had been recommending emergency establishment of
multi-species biological control of CAS (Marler &
Terry 2005; Moore et al. 2005; Tang et al. 2005). These explicit biocontrol
recommendations from the scientific community continued into the years
following the ESA-listing.
2016
The need to provide another detailed listing of potential
biological control organisms led to another publication that enumerated the
available CAS predators and parasitoids along with
their attributes and limitations (Tang & Cave 2016). This publication provided
the Guam deciders with the latest adaptive management recommendations derived
from global biocontrol research concerning which organisms carried the greatest
potential for introduction to save C. micronesica
from continued CAS-induced mortality.
2017
The first project designed to evaluate methods of
salvaging mature trees from military construction sites resulted in a
description of the moderate success in producing adventitious roots on large C.
micronesica stem cuttings obtained from
CAS-damaged trees (Marler & Cruz 2017). In
discussing the conservation implications, the authors noted the emergency need
of establishing effective biological control of CAS on Guam, and due to limited
conservation funds all available public funds should not be spent on expensive
salvage projects unless efficacious classical biological control is first
established.
The sustained lack of concern for the need to establish
biological control of CAS was addressed in another opinion style article in
which the ill-informed focus on salvage of C. micronesica
trees from construction sites was discussed (Marler
& Lindström 2017). Again, recommendations to
refrain from spending more conservation funding on plant translocation projects
were communicated along with the assertions that redirecting those funds to
expanded biological control efforts such that “…the plant mortality will cease
and the species can be removed from the ESA-listing.” The need to collect parasitoids within the native range of CAS was discussed
along with how to maneuver through the problem that
many of these parasitoids would be new to science
which would require that they be described and named prior to introduction to
Guam.
2018
The ongoing inability of R. lophanthae
to adequately control Guam’s CAS population led to an olfactometer study which
demonstrated the preferential navigation of the predator toward mature leaves
infested with CAS (Marler & Marler
2018). Guam’s C. micronesica seedling
population was rapidly killed by CAS herbivory (Marler
& Lawrence 2012; Marler & Krishnapillai
2020), and the results of the olfactometer study illuminated another potential
explanation for why the established predator had been ineffective in stopping
the seedling mortality. The findings were discussed in the context that parasitoid biocontrol was urgently needed on Guam because parasitoids may not be constrained by the same issues that
caused the predator biocontrol to be inadequate.
The results of a second study that refined methods to
improve adventitious root formation on large stem cuttings were published (Marler 2018). The findings verified that reduced stem
carbohydrates resulting from long-term CAS infestations were correlated with
reduced asexual propagation success. Again, the recommendations included the
need to refrain from expending human and budgetary resources on expensive
salvage projects, as these resources should instead be spent on sustainably
controlling the ubiquitous CAS infestations using classical biological control
protocols.
2020
The influence of inadequate biological control of CAS on
Guam was shown to reduce C. micronesica
height increment among surviving trees (Marler et al.
2020). These data were combined with population-level mortality data to
estimate that at least 70 years of demographic depth had been removed from
Guam’s C. micronesica population by
2020. Recommendations that developed from the study included the cessation of
funding expensive salvage projects and that use of all available funds to “…launch
biological control of the primary threats would establish the road to species
recovery.”
A comprehensive look at island-wide C. micronesica survival was published from benchmarked
permanent plots (Marler & Krishnapillai
2020). The results confirmed the complete mortality of seedlings, saplings, and
juveniles shortly after CAS herbivory, and 96% population mortality by 2020.
The primary recommendation was to “…establish a complex integrated biological
control program under the direction of scientists with appropriate
international expertise” as the only conservation action that may enable
recovery of C. micronesica.
The adaptive management literature from Guam had
continued to accumulate throughout the years since 2003, and the first of
several formal review articles was published as a comprehensive outline of
herbivore and omnivore threats to C. micronesica
survival (Deloso et al. 2020). Although the list of
cycad consumers had grown by this time, CAS was identified as the single
greatest threat to Guam’s cycad population. The need for the conservation
community to stop funding salvage projects and instead invest unreservedly into
classical biological control of CAS was repeated.
2021
A detailed look at how the Guam CAS invasion fit into the
chronology and geography of CAS invasions throughout numerous countries was
published (Marler et al. 2021). Enemy release occurs
when an invasive species thrives within its invaded locations as a result of
the lack of native biological control by enemies found within its native range
(Heger et al. 2024). The long list of CAS invasions
has revealed that the lack of natural enemies allowed CAS to kill its host
plants until local biologists established biological control. Recommendations
indicated that a dedicated search for fortuitous biological control organisms
within newly invaded locations should be combined with the purposeful
introduction of predators and parasitoids from other
managed biocontrol programs which could provide advice and rapid responses.
2023
The results from another asexual propagation study were
published which revealed that a CAS-infested plant may be killed by the added
stress of transplantation or the take of stem cuttings for adventitious root
formation (Marler 2023a). The findings indicated that
salvage and propagation of CAS-damaged C. micronesica
comprise an ill-informed conservation agenda and implementing sustainable
biological control of CAS as recommended in 2005 remained the most important
conservation agenda.
The fact that CAS herbivory reduces non-structural
carbohydrates and this response to the herbivory decreases asexual propagation
success was exploited to demonstrate that a visual starch stain technique could
be useful for identifying CAS-damaged host trees that would yield the best
chances of propagation success during salvage programs (Marler
2023b). The discussion of relevant conservation issues reiterated that
“…species recovery would ensue without the need for expensive propagation and
translocation rescue projects” if conservationists would stop spending funds on
salvage and nursery projects and instead direct all available funds to
establishing a multi-species classical biocontrol program.
The influence of the Guam CAS invasion on C. micronesica female tree behavior
was studied following benchmarked pre-invasion data, and revealed reproductive
effort and output remained constrained two decades after the invasion (Marler & Terry 2023). The outcomes revealed that, if
adequate establishment of classical biocontrol of CAS were to be achieved,
species recovery may require conservation practitioners to proactively manage
population-level regeneration and recruitment behaviors.
The implementation of a coalition of biological control organisms to stop the
CAS-induced population damage was discussed as the most important conservation
agenda.
The May 2023 Typhoon Mawar
imposed the strongest tropical cyclone windspeeds on Guam since the 2003 CAS
invasion. A coalition of CSG members responded to this stochastic event by
discussing how the tropical cyclone caused damage to the in situ C. micronesica population & interacted with the
history of funded conservation actions (Lindström et
al. 2023). The recommendations indicated that “…a dedicated multi-step
procedure for establishing classical biological control” remained the most
important conservation action for saving C. micronesica,
and that a serious response to the 2005 biocontrol recommendations (Moore et
al. 2005; Tang et al. 2005; Terry & Marler 2005)
would have likely preemptively mitigated the CAS
threat such that C. micronesica would
have never been ESA-listed.
2024
Disparities in biotic and abiotic stressors among the
Guam and Rota habitats that were invaded by CAS from 2005-2010 were exploited
to reveal the C. micronesica population
response to nascent CAS damage was remarkably homogeneous (Marler
& Cruz 2024). The results indicated that all co-occurring threats can be
ignored by conservationists who should focus exclusively on establishing
immediate classical biocontrol of CAS to remove the primary threat to species
survival.
Summation of
recommendations after ESA-listing
The general tone of the recommendations within CSG
publications during the years following the ESA-listing was essentially a
continuation of the decade of recommendations that were published prior to the
ESA-listing. Funding from the U.S. military for C. micronesica
conservation activities within Guam’s forests was initiated in 2012, a project
described by Marler & Cruz (2017). The amount of
funding increased dramatically following the ESA-listing, resulting in the
investment of more funds for cycad conservation than in any other location
worldwide. These expensive projects were designed without any of the available
public funds directed toward expanding biological control of CAS. Therefore, a
new theme that began to define the CSG publications was the unfortunate
misdirection of the millions of dollars of federal funding toward activities
that were of no consequence to the primary threat of CAS herbivory.
Parallels
This devastating pest has steadily expanded its invasive
range during the antecedent three decades. When CAS invaded Taiwan, the threat
to the endemic C. taitungensis was
immediate (Marler et al. 2021). Several years of CAS
population expansion were required before CAS infested the in situ C. taitungensis localities, and the resulting plant
mortality reached 62% by 10 years after the initial invasion (Liao et al.
2018). As a result, the status of this endemic island cycad was changed from
Vulnerable to Endangered in 2010 (Bösenberg 2022b).
The parallels to the Guam case study were striking, as the C. micronesica threat status was changed from Near
Threatened to Endangered in 2006 (Bösenberg 2022a).
A remote ex situ germplasm collection of Guam’s C.
micronesica genotypes was constructed on the
island of Tinian beginning 2006 and consisted of ≈ 1200 healthy plants in 2018
(Brooke et al. 2024). The Implementation Plan for managing this valuable
germplasm exploited the concepts of “proactive biological control” (Hoddle et
al. 2018). This biological control approach differs from classical biological
control in that available natural enemies are pre-selected and permitted for
introduction and release prior to an anticipated invasion of a target invasive
pest. Development of proactive biological control programs are analogous to
purchasing insurance, since the initial lag phases of classical biological
control are avoided (Hoddle 2024). The scale predator R. lophanthae was established on the nearby island of
Rota at the time, and collection, transport to Tinian, and release in Tinian
had been pre-approved in the event that CAS invaded Tinian at some time in the
future. The plan mandated the cessation of all management activities until
immediate introduction of R. lophanthae
to Tinian had been successful, a process that should have required no more than
24–48 h. Unfortunately, the military biologists responsible for managing this
germplasm and the practitioners contracted to protect the germplasm did not
follow the mandates of the plan, allowing the nascent CAS infestation to become
firmly established. The lack of concern for following through with the
proactive biological control plan caused 83% mortality of the germplasm within
four years of the invasion (Brooke et al. 2024).
Recent invasions persist that threaten more iconic
endemic Cycas species. For example, the 2006 predictions that an
armoured scale invasion to India would threaten the endemic Cycas circinalis L. (Muniappan
& Viraktamath 2006) have come to pass with the
2023 invasion of the closely related Aulacaspis
madiunensis Zehnter
(Joshi et al. 2023). Similarly, Amami-Oshima Island
was invaded by CAS in 2022 (Takagi 2023), and the subsequent invasions of other
Ryukyu Islands and initial mortality of the endemic C. revoluta populations have been alarming developments
(Deloso et al. 2024).
The continuing expansion of the invasive range of CAS
underscores the value of the lessons learned from Guam, where a native Cycas
species was threatened by non-native armoured scale herbivory for the first
time. These lessons call for resident scientists and conservation agents in
newly invaded countries to embrace the recommendations from international
experts and implement immediate adaptive management endeavors
addressing every facet of biological control.
Contemporary
observations and recommendations from Guam
Benchmarked permanent plots throughout Guam revealed 245
stems per ha were alive in some 2015 habitats when C. micronesica was federally listed (Marler & Krishnapillai 2020).
These same plots revealed 157 stems per ha were alive in 2020 when the five-year
species recovery status report was published (USFWS 2020), indicating 36%
mortality of the 2015 population occurred during these five years of federal
protection. All available evidence indicated that 100% of this mortality was a
direct result of herbivory by CAS and the resulting increases in damage by
native stressors such as A. marianarum
(Marler 2013a) and tropical cyclone winds (Marler et al. 2016). These native stressors were not
damaging to the cycad population prior to the plant damage imposed by the CAS
invasion. Yet the USFWS reviewed the first five years of ESA protection (USFWS
2020) with no mention of any biological control efforts designed to address the
CAS threat. Similarly, the contemporary Integrated Natural Resource Management
Plan crafted to define the ongoing conservation actions of the U.S. military
(DON 2022) failed to mention any plans to expand biocontrol of CAS on Guam.
This Guam case study has unfolded to inform conservationists in other regions
of the world that apathy toward recommendations of international specialists
concerning the need for immediate biocontrol of CAS can rapidly impose
irreversible damage to in situ Cycas populations and the ecosystem
services that they provide.
What is needed to more fully understand the current
status of C. micronesica population
survival and desired species recovery? We recommend that biologists within
federal funding and permitting agencies at least minimally begin to connect
with knowledgeable input from international experts. The many mistakes made in
the heavily funded conservation projects on Guam could have been avoided if the
funding agencies had followed this recommendation. For example, the U.S.
military has spent millions of U.S. dollars on C. micronesica
conservation in the past decade, numbers that dwarf the amount of cycad
conservation funding from all other sources worldwide, yet none of these funds
have been devoted to expanding the coalition of predator and parasitoid species to enhance the control of CAS on Guam.
Therefore, a fundamental shift in culture of the empowered conservation
decision-makers will be required to enable a respect for the need to embed
adaptive management research by qualified specialists within every conservation
project. As early as 2008 this Guam case study was being highlighted as an
example in which the lack of rapid establishment of biological control of a new
herbivorous insect invasion could cause irreversible damage to ecosystems
(Messing & Watson 2008), and yet today the lack of adequate CAS biological
control continues to be the greatest threat to C. micronesica
survival.
Parasites comprise an ancient life form that remains
prevalent today (Poulin 2014). Parasitism is an integral component of ecosystem
function (Hatcher et al. 2012). The exploitation of highly specific parasitoids as endoparasites to control damaging herbivore
arthropods has been a successful component of managed biological control
programs for decades (Eggleton & Belshaw 1992). We continue to believe that the managed
construction of a coalition of biological control organisms that includes parasitoids will actively suppress Guam’s CAS population
and passively engineer the recovery of the C. micronesica
population. The list of biocontrol organisms that are available to introduce to
Guam is extensive (Cave et al. 2013; Tang & Cave 2016; Marler
et al. 2021).
Numerous attempts to introduce the parasitoids
C. fulvus and Aphytis
lingnanensis Compere to Guam from Florida and
Hawaii were unsuccessful (Marler & Lindström 2017). The reasons for the lack of success remain
elusive, but there was no parasitoid specialist
included in those Guam activities. We recommend the inclusion of a parasitoid specialist to oversee a repeat of these endeavors, as both parasitoid
species are readily available within the U.S.A. Dedicated trips to rear parasitoids from CAS-infested Cycas leaves within
the CAS native range has led to collection of parasitoids
that have not been described (Marler & Lindström 2017). These organisms cannot be imported to Guam
until a taxonomist places a binomial on the animal, which is a prerequisite to
applying for mandatory import permits. We have recommended a multi-stage
program within which these parasitoids are described
and named by taxonomic experts as part of the initial funding (Marler & Lindström 2017; Lindström et al. 2023), and we repeat this recommendation
here. These conservation actions could have been completed between the 2003
invasion and the 2015 ESA-listing with a fraction of the funds that have been
spent on C. micronesica salvage,
transplantation, and nursery endeavors.
The fortuitous improvement in health of Guam’s in situ C.
micronesica population has been
reported in the past few years (Lindström et al.
2023; Marler & Terry 2023). Some contemporary
trees exhibit healthy leaves with no signs of herbivory, which is something
that has not occurred since 2005. These observations point to a pivotal time
period in which conservationists need to identify why reduced CAS herbivory is
fortuitously occurring. Numerous geographic regions are characterized by native
Cycas species, native CAS, and native biocontrol organisms coexisting in
harmony. In these settings, the host plants are typically infested with CAS but
remain unthreatened (Marler & Lindström
2017). Some C. micronesica trees in
various Guam habitats exhibit general appearance that mimics the Cycas
trees in these regions where native CAS is controlled by native natural
enemies. These observations indicate that the likely cause of the recent
decrease in CAS herbivory on Guam is a fortuitous improvement in biological
control of the resident CAS population. An experienced cycad biologist would
possess the wherewithal to experimentally determine if currently unidentified
biocontrol of CAS has developed in recent years on Guam. The team of deciders
empowered to define future conservation actions on Guam should include at least
one cycad specialist who has worked within habitats containing sympatric native
Cycas, CAS, and CAS enemies, as these biologists understand the gestalt
traits of the cycad and CAS populations under these sustainably controlled
conditions.
We believe the CAS invasions of Guam in 2003, Rota in
2007, and Palau in 2008 were enabled by the frequent international flights in
these three airports, flights from regions that contained Cycas
populations that were heavily infested with CAS. We also believe that the
infrequent flights to the Yap airport explain why Yap remains uninvaded by CAS
to date, despite a thriving C. micronesica
population. New investments of United States national security funding into Yap
will likely ensure a CAS invasion of Yap in the near future. Indeed, an
estimated US$37 million is being spent to expand the Yap Island airport (Island
Times 2023) and an estimated US$3.3 billion will be spent on Yap and other FSM
islands over next 20 years (Island Times 2024). The resulting increases in
human travel to Yap indicate that C. micronesica
conservationists need to be on the lookout for the probable Yap invasion by CAS
in the near future.
The Guam and Rota cycad populations were decimated by the
CAS invasions of those islands because of apathy toward the need to rapidly
establish biocontrol. Yap’s conservation community has an opportunity to be
ready to construct the biological control program that will be required to save
Yap’s C. micronesica population from
being decimated by CAS. Similarly, the conservation communities within the
recently invaded C. circinalis and C.
revoluta habitats have an opportunity to
construct the biological control program that will be required to save these
iconic cycad species. In so doing, they can emerge as the first location where
successful conservation actions were implemented in compliance with
evidence-based approaches based on the best available science as communicated
by the CSG.
Global
Biodiversity Targets
Lessons
from every conservation case study are integral for informing the global
biodiversity crisis. Legal instruments that create opportunities for
international cooperation are useful for addressing declines in genetic
diversity, compromises in ecosystem services, and the risk for localized
ecosystem collapse. The Kunming-Montreal Global Biodiversity Framework (GBF)
has been developed to operationalize global biodiversity targets (Convention on
Biological Diversity 2022). Single species case studies in isolated island
communities do not operate in isolation from global crises, and goals of the
GBF will not be possible without commitments for compliance in these isolated
biodiversity cases.
The GBF’s
four goals and 23 targets provide guidelines to mobilize resources to maintain
the Earth’s biodiversity. This Guam case study falls directly in line with
species and ecosystem conservation in goal A, with attention on threats that
are driven by human activities. Implementation of this goal requires local
conservationists to identify the factors that are known to threaten each
species as the baseline for progress. As outlined in this review, the threats
to C. micronesica are clearly
understood and have been pointedly communicated in the primary literature for
decades. Recovery actions in target 4 for species that require urgency
necessitates the identification of the root causes of human-induced extinction.
The consistent and ongoing expansion of the invasive range for CAS (Marler et al. 2021) has emerged as one of the greatest
threats to cycad conservation (Tang et al. 2005), and the root causes of the
threats are unambiguously understood as transport of CAS-infested plant
materials and phoresis of CAS crawlers through human
travel. This Guam case study falls directly under target 6 which calls for
combatting the consequences of invasive species. The demise of Guam’s 2005 C.
micronesica population when CAS began killing
in situ plants has been documented with 96% mortality as of 2020 (Marler & Krishnapillai
(2020), and as outlined herein the causes have been a failure to implement a
classical multi-species biological control program to mitigate the CAS threat.
Goals and
targets are integral parts of the international solution to guide biodiversity
policy reforms. Successful implementation, however, cannot occur without
learning from past programs which provide successful and unsuccessful case studies.
Bureaucracy and politics have been identified as institutional barriers, and
staff turnover and limited use of available knowledge have been identified as
organizational barriers to successful recovery of endangered species (Guerrero
et al. 2024). Guam’s government agency bureaucracy, inter-agency politics, lack
of collaboration with international experts, violation of human rights of
Guam’s indigenous peoples, rapid turnover of consequential decision-makers,
failures to respect the value of adaptive management, and waste of resources on
inconsequential projects have been discussed as barriers to conservation of C.
micronesica and as root causes of
environmental destruction (Marler 2014, 2019; Marler & Lindström 2014,
2017; Marler & Cruz 2017, 2024; Lindström et al. 2023; Brooke et al. 2024; Deloso et al. 2024). These barriers have been successfully
exploited to marginalize international experts from having a seat at Guam’s
decision-making table. They have also generated public condemnation by the United
Nations of the violations of human rights of Guam’s indigenous peoples (United
Nations Commission on Human Rights 2021) and an ongoing lawsuit from the Center for Biological Diversity for systemic violations of
the tenets of the ESA (Center for Biological
Diversity 2023). The contributions of this case study to future cycad
conservation endeavors in particular and the GBF in
general will require deciders in other countries which are invaded by CAS to
avoid these same barriers.
Summation
The 2003 CAS invasion of Guam created a case study that
held the potential to develop mitigation protocols through biocontrol adaptive
management research that could inform conservation planners in other nations
where subsequent CAS invasions threatened native Cycas species. The
deciders who hold power over the planning and funding of Guam’s conservation
actions have not exploited this opportunity. There is an urgent need to
overhaul the manner in which Guam’s policy and funding deciders view the input
of relevant specialists. This Guam case study informs conservationists in other
regions of the world that apathy toward inputs from international specialists
concerning the need for immediate biocontrol of CAS can rapidly impose
irreversible damage to in situ Cycas populations.
For
figure & images - - click here for full PDF
REFERENCES
Bösenberg, J.D. (2022a). Cycas micronesica. In The IUCN Red List of Threatened Species; 2022;
e.T61316A68906033. International Union for Conservation of Nature, Gland,
Switzerland. https://doi.org/10.2305/IUCN.UK.2022-1.RLTS.T61316A243418579.en.
Accessed on 23 August 2024.
Bösenberg, J.D. (2022b). Cycas taitungensis. The IUCN Red List of Threatened Species
2022: e.T42067A243420506. International Union for Conservation of Nature, Gland,
Switzerland. https://doi.org/10.2305/IUCN.UK.2022-1.RLTS.T42067A243420506.en.
Accessed on 23 August 2024.
Brooke, A., L.I. Terry & T.E. Marler
(submitted). Conception, construction, and
initial development of the Tinian ex situ Cycas micronesica
(Cycadaceae) germplasm. Plant Species Biology (submitted).
Cave, R.D., J.-T. Chao, B. Kumashiro,
T. Marler, J. Miles, A. Moore, R. Muniappan
& G.W. Watson (2013). Status and biological control of
cycad aulacaspis scale. Biocontrol News
Information 34(1): 1N–4N.
Center for Biological Diversity (2023). Center for Biological
Diversity and Prutehi Litekyan
versus United States Department of Defense; Carlos
del Toro; United States Fish and Wildlife Service; Haaland,
D. CIV 23-00019 (2003). Complaint for Declaratory and Injunctive Relief under
the Endangered Species Act, Administrative Procedure Act, and Freedom of
Information Act. United States District Court of Guam. 2023. https://www.biologicaldiversity.org/programs/biodiversity/pdfs/Camp-Blaz-Complaint.pdf.
Accessed on 23 August 2024.
Convention on Biological Diversity (2022). Decision adopted by the conference of the parties to
the convention on biological diversity 15/4. Kunming-Montreal global
biodiversity framework. https://www.cbd.int/doc/decisions/cop-15/cop-15-dec-04-en.pdf.
Accessed on 23 August 2024.
Deloso, B.E., L.I. Terry, L.S. Yudin
& T.E. Marler (2020). Biotic threats to Cycas micronesica
continue to expand to complicate conservation decisions. Insects 11:
888. https://doi.org/10.3390/insects11120888.
Deloso, B.E., J.S. Gutiérrez-Ortega, J.-T. Chang, Y. Ito-Inaba,
A.J. Lindström, L. I. Terry, J. Donaldson, W. Tang,
R.D. Cave, J.A. Gómez Díaz, V.M. Handley, M.P. Griffith & T.E. Marler (in press). Biological
invasion by the cycad-specific scale pest Aulacaspis
yasumatsui (Diaspididae)
into Cycas revoluta (Cycadaceae)
populations on Amami-Oshima and Okinawa-jima, Japan. Plant Species Biology 39 (in press).
DON (2022). Integrated
Natural Resources Management Plan for Joint Region Marianas. Prepared for Joint
Region Marianas and NAVFAC Marianas, Department of the Navy, Guam by Cardno, Honolulu, HI. https://www.mcbblaz.marines.mil/Environmental-Program/.
Accessed on 23 August 2024.
Donnegan, J.A., S.L. Butler, W. Grabowiecki,
B.A. Hiserote & D. Limtiaco
(2004). Guam’s forest resources, 2002. Portland, OR. p.
32. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research
Station.
Eggleton, P. & R. Belshaw (1992). Insect parasitoids: an
evolutionary overview. Philosophical Transactions of the Royal Society of
London. Series B: Biological Sciences 337: 1–20. https://doi.org/10.1098/rstb.1992.0079
Guerrero, A.M., I. Sporne &
K.A. Wilson (2024). A multilevel perspective to
understanding enablers and barriers to success in threatened species recovery
planning. Conservation Science and Practice 6(8): e13175.
https://doi.org/10.1111/csp2.13175
Hatcher, M.J., J.T. Dick & A.M. Dunn (2012). Diverse effects of parasites in ecosystems: linking
interdependent processes. Frontiers in Ecology and the Environment 10:
186–194. https://doi.org/10.1890/110016
Heger, T., J.M. Jeschke, M. Bernard-Verdier, C.L. Musseau & D. Mietchen (2024). Hypothesis
description: Enemy release hypothesis. Research Ideas and Outcomes 10:
e107393. https://doi.org/10.3897/rio.10.e107393
Hill, K.D. (1994). The Cycas rumphii complex (Cycadaceae)
in New Guinea and the Western Pacific. Australian Systematic Botany 7:
543–567.
Hoddle, M.S. (2024). A new
paradigm: proactive biological control of invasive insect pests. BioControl 69: 321–334. https://doi.org/10.1007/s10526-023-10206-5
Hoddle, M.S., E.C. Lake, C.R. Minteer
& K.M. Daane (2021). Importation biological control. pp. 67–89. In: Mason,
P.G. (ed.). Biological control—global impacts, challenges and future
directions of pest management. CSIRO Publishing, Victoria, 644 pp.
Hoddle, M.S., K. Mace & J. Steggall
(2018). Proactive biological control: a cost effective
management option for invasive pests. California Agriculture 72:
148–150.
Island Times (2023). U.S to
deploy air defence assets to Yap. https://islandtimes.org/u-s-to-deploy-air-defence-assets-to-yap/.
Accessed 23 August 2024.
Island Times (2024). U.S,
FSM begin exploring military training opportunities in Yap. https://islandtimes.org/u-s-fsm-begin-exploring-military-training-opportunities-in-yap/.
Accessed 23 August 2024.
Joshi, S., H. Bhaskar, K. Sachin, K. Aparna, K.A. Gokul,
G. Athira Menon & S.N. Sushil (2023). Aulacaspis madiunensis (Zehntner) (Hemiptera: Diaspididae)
– an additional danger to the endangered Cycas circinalis
L. Pest Management in Horticultural Ecosystems 29(2): 181–189.
Lazaro, M., O. Kuegler, S.
Stanton, A. Lehman, J. Mafnas & M. Yatskov (2020). Guam’s forest
resources: Forest Inventory and Analysis, 2013. Resource Bullettin
PNW-RB-270. U.S. Department of Agriculture, Forest Service, Pacific Northwest
Research Station, Portland, OR, 43 pp.
Liao, P.C., L.P. Ju, Y.Z. Ko, M.H.
Chen, Y.P. Cheng & Y.C. Chiang (2018). Using the genetic
variation of Cycas
taitungenesis, an endangered
Island cycad, to evaluate
ex situ conservation strategies.
Memoirs of the
New York Botanical Gardens 117: 205–229.
Lindström, A., I. Terry, B. Deloso, W. Tang, J. Donaldson
& T. Marler (2023). Typhoon Mawar enables an assessment of Cycas micronesica
conservation plans. Journal of Geography and Natural Disasters 13: 280.
Marler, T. (2000) Looking out for
scale insects. Pacific Sunday News 13 Feb. 2000, 24 pp.
Marler, T.E. (2012). Boomeranging
in structural defense: Phytophagous insect uses cycad
trichomes to defend against entomophagy. Plant Signaling
& Behavior 7: 1484–1487.
Marler, T.E. (2013a). Temporal
variations in leaf miner, butterfly, and stem borer infestations of Cycas micronesica in relation to Aulacaspis
yasumatsui incidence. HortScience
48: 1334–1338. https://doi.org/10.21273/HORTSCI.48.10.1334
Marler, T.E. (2013b). Vertical
stratification in arthropod spatial distribution research. Communicative and
Integrative Biology 6: e25745. https://doi.org/10.4161/cib.25749
Marler, T.E. (2014). The intersection
of a military culture and indigenous peoples in conservation issues. Communicative
and Integrative Biology 7: e26665. https://doi.org/10.4161/cib.26665
Marler, T.E. (2018). Stem
carbohydrates and adventitious root formation of Cycas micronesica
following Aulacaspis yasumatsui
infestation. Horticultural Science 53: 1125–1128. https://doi.org/10.21273/HORTSCI13170-18
Marler, T.E. (2019). Tree
conservation can be constrained by agents from conservation permitting and
funding agencies. Communicative & Integrative Biology 12: 133–143. https://doi.org/10.1080/19420889.2019.1654348
Marler, T.E. (2023a). Infestations
of Aulacaspis yasumatsui
reduce asexual propagation and transplantation success of Cycas revoluta plants. Horticulturae
9: 1108. https://doi.org/10.3390/horticulturae9101108
Marler, T.E. (2023b). Visual starch
stain procedure assists cycad propagation decisions. Agronomy 13: 2815. https://doi.org/10.3390/agronomy13112815
Marler, T.E. & A.J. Lindström
(2014). The value of research to selling the conservation of
threatened species: the case of Cycas micronesica
(Cycadopsida: Cycadales: Cycadaceae). Journal of Threatened Taxa 6:
6523–6528. https://doi.org/10.11609/JoTT.o4098.6523-8
Marler, T.E. & G.N. Cruz (2017). Adventitious rooting of mature Cycas micronesica K.D. Hill tree stems reveals moderate
success for salvage of an endangered cycad. Journal of Threatened Taxa
9: 10565–10570. https://doi.org/10.11609/jott.3523.9.8.10565-10570
Marler, T.E. & G.N. Cruz (2024). Insular Cycas micronesica
habitats respond similarly to Aulacaspis yasumatsui invasion, regardless of co-occurring
consumers. Forests 15: 22. https://doi.org/10.3390/f15010022.
Marler, T.E. & I. Terry (2012). The continuing demise of Cycas micronesica.
The Cycad Newsletter 36(1): 22–26.
Marler, T.E. & J.H. Lawrence (2012). Demography of Cycas micronesica
on Guam following introduction of the armoured scale Aulacaspis
yasumatsui. Journal of Tropical Ecology 28:
233–242.
Marler, T.E. & L.I. Terry (2023). Cycas micronesica megastrobilus traits respond to chronic herbivory by Aulacaspis yasumatsui.
Ecologies 4: 371–384. https://doi.org/10.3390/ecologies4020024
Marler, T.E. & A.J. Lindström (2017). First,
do no harm. Communicative and Integrative Biology 10: e1393593. https://doi.org/10.1080/19420889.2017.1393593
Marler, T.E. & M.V. Krishnapillai
(2020). Longitude, forest fragmentation, and plant size
influence Cycas micronesica mortality
following island insect invasions. Diversity 12: 194. https://doi.org/10.3390/d12050194
Marler, T.E. & P.N. Marler (2018). Rhyzobius lophanthae behavior is
influenced by cycad plant age, providing odor samples
in a Y-tube olfactometer. Insects 9: 194. https://doi.org/10.3390/insects9040194
Marler, T.E., A.J. Lindström & G.W.
Watson (2021). Aulacaspis yasumatsui delivers a blow
to international cycad horticulture. Horticulturae 7:
147. https://doi.org/10.3390/horticulturae7060147
Marler, T.E., J.H. Lawrence & G.N. Cruz (2016). Topographic relief, wind direction, and conservation
management decisions influence Cycas micronesica
K.D. Hill population damage during tropical cyclone. Journal of Geography
and Natural Disasters 6: 178. https://doi.org/10.4172/2167-0587.1000178
Marler, T.E., M.P. Griffith & M.V. Krishnapillai
(2020). Height increment of Cycas micronesica
informs conservation decisions. Plant Signaling
and Behavior 15: e1830237. https://doi.org/10.1080/15592324.2020.1830237
Marler, T.E., R. Miller & A. Moore (2013). Vertical stratification of predation on Aulacaspis yasumatsui
infesting Cycas micronesica seedlings. HortScience 48: 60–62. https://doi.org/10.21273/HORTSCI.48.1.60
Messing, R.H. & T.K. Watson (2008). Response to Holland et al.; Biocontrol in Hawaii: more
bureaucracy is not the answer. Proceedings of the Hawaiian Entomological
Society 40: 85–87.
Moore, A., T. Marler, R.H.
Miller & R. Muniappan (2005). Biological control of cycad aulacaspis
scale on Guam. The Cycad Newsletter 28(4): 6–8.
Muniappan, R. & C.A. Viraktamath
(2006). The Asian cycad scale Aulacaspis
yasumatsui, a threat to native cycads in India. Current
Science 91(7): 868.
Poulin, R. (2014). Parasite
biodiversity revisited: frontiers and constraints. International Journal for
Parasitology 44: 581–589. https://doi.org/10.1016/j.ijpara.2014.02.003.
Stanley, A.E., R. Epanchin-Niell,
T. Treakle & G.D. Iacona
(2024). Attributes of preemptive
conservation efforts for species precluded from listing under the U.S.
Endangered Species Act. Conservation Biology 38: e14200. https://doi.org/10.1111/cobi.14200
Takagi, S. (2023) Outbreak of Aulacaspis yasumatsui
in Japan (Sternorrhyncha: Coccoidea:
Diaspididae). Insecta
matsumurana 79: 81–84. http://hdl.handle.net/2115/90638
Tang, W. & R.D. Cave (2016). Recent advances in the biological control of cycad aulacaspis scale. Encephalartos
123: 16–18.
Tang, W., J. Donaldson, J. Haynes & I. Terry (2005). International Union for Conservation of Nature Cycad
Specialist Group Report and Recommendations on Cycad Aulacaspis
Scale, Aulacaspis yasumatsui
Takagi (Hemiptera: Diaspididae). IUCN, Gland,
Switzerland.
Terry, I. & T. Marler
(2005). Paradise lost? Tipping the scales against Guam’s
Cycas micronesica. The Cycad Newsletter
28(4): 21–23.
Treakle, T., R. Epanchin-Niell &
G.D. Iacona (2023). Factors associated with preemptive
conservation under the U.S. Endangered Species Act. Conservation Biology
37: e14104. https://doi.org/10.1111/cobi.14104
United Nations Commission on Human Rights (2021). AL USA 7/2021. Available at: https://spcommreports.ohchr.org/TMResultsBase/DownLoadPublicCommunicationFile?gId=25885.
Accessed 23 August 2024.
United States
Fish and Wildlife Service (2020). Cycas micronesica (fadang, faadang). 5-year review summary and evaluation. Available
at: https://ecos.fws.gov. Accessed 23 August
2024.