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
DOI:
https://doi.org/10.11609/jott.9110.16.11.26150-26162Keywords:
Aulacaspis yasumatsui, biological control, conservation science, Cycas micronesica, Rhyzobius lophanthaeAbstract
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.
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.
Published
Issue
Section
License
Copyright (c) 2024 Thomas E. Marler, Anders J. Lindström, L. Irene Terry, Benjamin E. Deloso

This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors own the copyright to the articles published in JoTT. This is indicated explicitly in each publication. The authors grant permission to the publisher Wildlife Information Liaison Development (WILD) Society to publish the article in the Journal of Threatened Taxa. The authors recognize WILD as the original publisher, and to sell hard copies of the Journal and article to any buyer. JoTT is registered under the Creative Commons Attribution 4.0 International License (CC BY), which allows authors to retain copyright ownership. Under this license the authors allow anyone to download, cite, use the data, modify, reprint, copy and distribute provided the authors and source of publication are credited through appropriate citations (e.g., Son et al. (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969. https://doi.org/10.11609/jott.2785.8.7.8953-8969). Users of the data do not require specific permission from the authors or the publisher.





