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Is Chinese Tallowtree, Triadica sebifera, an Appropriate Target for Biological Control in the United States?

Published online by Cambridge University Press:  20 January 2017

Gregory S. Wheeler*
Affiliation:
U.S. Department of Agriculture/Agricultural Research Service, Invasive Plant Research Lab, 3225 College Avenue, Fort Lauderdale, FL 33314
Jianqing Ding
Affiliation:
Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden/Institute, Chinese Academy of Sciences, Moshan, Wuhan, Hubei Province 430074, China
*
Corresponding author's E-mail: greg.wheeler@ars.usda.gov

Abstract

Biological control is one of the most common approaches used to manage invasive weeds of wetlands and other natural areas. Before candidate agents can be released, research is conducted to support biological control, which can be protracted and expensive, leading to a scientific and potentially lengthy regulatory review. To increase biological control safety, efficacy, and transparency, we suggest that during the early phases of a weed project, the feasibility of the invasive plant as a target should be studied explicitly. Our purpose here is to summarize information of an important invasive weed that can serve to judge whether the project is appropriate. Chinese tallowtree, Triadica sebifera, is one of the worst invasive species invading coastal wetlands and other riparian areas of the southeastern United States. Current management practices have not controlled the spread of this weed into these sensitive habitats. Initial surveys in the plant's native Chinese range for potential biological control agents have recovered several herbivore species that could be developed. These potential agents include defoliators, root and foliage feeders, and gall formers, whose biology, apparent host specificity, and impacts on plant fitness suggest that biological control offers great promise against Chinese tallowtree. When conducted during the initial phase of a project, this type of feasibility study can address potential conflicts of interest and risks, ultimately producing projects that are more effective and safer for biological control.

Type
Research Article
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Adams, CK, Saenz, D (2012) Leaf litter of invasive Chinese tallow (Triadica sebifera) negatively affects hatching success of an aquatic breeding anuran, the Southern Leopard Frog (Lithobates sphenocephalus). Can J Zool 90:991998 Google Scholar
APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105121 Google Scholar
Baldwin, MJ, Barrow, WC, Jeske, C, Rohwer, FC (2008) Metabolizable energy in Chinese tallow fruit for yellow-rumped warblers, northern cardinals, and American robins. Wilson J Ornithol 120:525530 Google Scholar
Bernays, EA, Chapman, RF (1994) Host-Plant Selection by Phytophagous Insects. New York. Chapman & Hall. 312 pGoogle Scholar
Bingtao, L, Esser, H-J (2008) TRIADICA Loureiro, Fl. Cochinch. 2: 598, 610. 1790. Flora of China 11:284285 Google Scholar
Blossey, B, Hunt-Joshi, TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521547 Google Scholar
Blossey, B, Nötzold, R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887889 Google Scholar
Boldor, D, Kanitkar, A, Terigar, BG, Leonardi, C, Lima, M, Breitenbeck, GA (2010) Microwave assisted extraction of biodiesel feedstock from the seeds of invasive Chinese tallow tree. Environ Sci Technol 44:40194025 Google Scholar
Bower, MJ, Aslan, CE, Rejmánek, M (2009) Invasion potential of Chinese tallowtree (Triadica sebifera) in California's Central Valley. Invasive Plant Sci Manage 2:386395 Google Scholar
Bruce, KA, Cameron, GN, Harcombe, PA (1995) Initiation of a new woodland type on the Texas coastal prairie by the Chinese tallow tree (Sapium sebiferum (L.) Roxb.). Bull Torrey Bot Club 122:215225 Google Scholar
Bruce, KA, Cameron, GN, Harcombe, PA, Jubinsky, G (1997) Introduction, impact on native habitats, and management of a woody invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb. Nat Areas J 17:255260 Google Scholar
Burger, W, Huft, M (1995) Family 113 Euphorbiaceae. 36 ed. Chicago Field Museum of Natural History. 169 pGoogle Scholar
Cameron, GN, LaPoint, TW (1978) Effects of tannins on the decomposition of Chinese tallow leaves by terrestrial and aquatic invertebrates. Oecologia 32:349366 Google Scholar
Center, TD, Purcell, MF, Pratt, PD, Rayamajhi, MB, Tipping, PW, Wright, SA, Dray, FA. Jr (2012) Biological control of Melaleuca quinquenervia: an Everglades invader. Biocontrol 57:151165 Google Scholar
Conway, WC, Smith, LM, Bergan, JF (2002) Avian use of Chinese tallow seeds in coastal Texas. Southwest Nat 47:550556 Google Scholar
Costanza, R, D'Arge, R, De Groot, R, Farber, S, Grasso, M, Hannon, B, Limburg, K, Naeem, S, O'Neill, RV, Paruelo, J, Raskin, RG, Sutton, P, Van Den Belt, M (1997) The value of the world's ecosystem services and natural capital. Nature 387:253260 Google Scholar
Cotten, TB, Kwiatkowski, MA, Saenz, D, Collyer, M (2012) Effects of an invasive plant, Chinese tallow (Triadica sebifera), on development and survival of anuran larvae. J Herpetol 46:186193 Google Scholar
Davis, DR, Fox, MS, Hazen, RF (2013) Systematics and biology of Caloptilia triadicae (Lepidoptera: Gracillariidae), a new species of leaf-mining moth of the invasive Chinese tallow tree (Triadica sebifera (L.) Euphorbiaceae). J Lep Soc 67:281290 Google Scholar
Dewalt, SJ, Siemann, E, Rogers, WE (2011) Geographic distribution of genetic variation among native and introduced populations of Chinese tallow tree, Triadica sebifera (Euphorbiaceae). Am J Bot 98:11281138 Google Scholar
Dodd, AP (1940) The Biological Campaign against Prickly Pear. Brisbane, Australia Commonw. Prickly Pear Board Google Scholar
Duke, JA (2013) Handbook of Energy Crops. http://www.hort.purdue.edu/newcrop/duke_energy/dukeindex.html. Accessed March 5, 2013Google Scholar
Ehrlich, PR, Raven, PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586608 Google Scholar
Engelhardt, KAM, Ritchie, ME (2001) Effects of macrophyte species richness on wetland ecosystem functioning and services. Nature 411:687689 Google Scholar
Esser, HJ (2002) A Revision of Triadica Lour. (Euphorbiaceae). Harvard Papers Bot 7:1721 Google Scholar
Esser, HJ, Van Welzen, P, Djarwaningsih, T (1997) A phylogenetic classification of the Malesian Hippomaneae (Euphorbiaceae). Syst Bot 22:617628 Google Scholar
[FLEPPC] Florida Exotic Pest Plant Council Plant List Committee (2009) Florida Exotic Pest Plant Council's 2009 List of Invasive Species. Wild Weeds 12:1316 Google Scholar
Forero, L, Nader, G, Craigmill, A, DiTomaso, JM, Puschner, B, Maas, J (2011) Livestock-Poisoning Plants of California. http://anrcatalog.ucdavis.edu, University of California Agriculture and Natural Resources. Accessed March 5, 2013Google Scholar
Fox, M, Hazen, R, Wheeler, GS, Davis, DR (2012) Using internet images to gather distributional data for a newly discovered Caloptilia species (Lepidoptera: Gracillariidae) specializing on Chinese tallow in North America. Am Entomol 58:3235 Google Scholar
Geiger, JH, Pratt, PD, Wheeler, GS, Williams, DA (2011) Hybrid vigor for the invasive exotic Brazilian peppertree (Schinus terebinthifolius Raddi., Anacardiaceae) in Florida. Int J Plant Sci 172:655663 Google Scholar
Govaerts, R, Dransfield, J, Zona, SF, Hodel, DR, Henderson, A (2013) World Checklist of Euphorbiaceae. Facilitated by the Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp/. Accessed March 5, 2013Google Scholar
Grace, JB (1998) Can prescribed fire save the endangered coastal prairie ecosystem from the Chinese tallow invasion? Endangered Species Update 15:7076 Google Scholar
Hansen, RW, Richard, RD, Parker, PE, Wendel, LE (1997) Distribution of biological control agents of Leafy Spurge (Euphorbia esula L.) in the United States: 1988–1996. Biol Control 10:129142 Google Scholar
Hoffmann, JH, Moran, VC (1998) The population dynamics of an introduced tree, Sesbania punicea, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia 114:343348 Google Scholar
Hosking, JR, Conn, BJ, Lepschi, BJ (2003) Plant species first recognised as naturalised for New South Wales over the period 2000–2001. Cunninghamia 8:175187 Google Scholar
Huang, W, Carrillo, J, Ding, J, Siemann, E (2012) Interactive effects of herbivory and competition intensity determine invasive plant performance. Oecologia 170:373382 Google Scholar
Huang, W, Siemann, E, Wheeler, GS, Zhou, J, Carrillo, J, Ding, J (2010) Resource allocation to defense and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:11571167 Google Scholar
Huang, W, Wheeler, GS, Purcell, MF, Ding, J (2011) The host range and impact of Bikasha collaris (Coleoptera: Chrysomelidae), a promising candidate agent for biological control of Chinese tallow, Triadica sebifera (Euphorbiaceae) in the United States. Biol Control 56:230238 Google Scholar
Invasive.org (2013) Invasive.org Center for Invasive Species and Ecosystem Health. www.invasive.org. Accessed March 5, 2013Google Scholar
Jamieson, G, McKinney, R (1938) Stillingia oil. J Am Oil Chem Soc 15:295296 Google Scholar
Jones, RH, McLeod, KW (1989) Shade tolerance in seedlings of Chinese tallow tree, American sycamore, and cherry bark oak. Bull Torrey Bot Club 116:371377 Google Scholar
Jongejans, E, Sheppard, AW, Shea, K (2006) What controls the population dynamics of the invasive thistle Carduus nutans in its native range? J Appl Ecol 43:877886 Google Scholar
Jubinsky, G, Anderson, LC (1996) The invasive potential of Chinese tallow-tree (Sapium sebiferum Roxb.) in the Southeast. Castanea 61:226231 Google Scholar
Keane, RM, Crawley, MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164170 Google Scholar
Lankau, RA, Rogers, WE, Siemann, E (2004) Constraints on the utilisation of the invasive Chinese tallow tree Sapium sebiferum by generalist native herbivores in coastal prairies. Ecol Entomol 29:6675 Google Scholar
Lavergne, S, Molofsky, J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. PNAS 104:38833888 Google Scholar
Leonard, NE (2005) Tadpoles of early breeding amphibians are negatively affected by leaf litter from invasive Chinese tallow trees. Eos Trans AGU 86: Abstract NB14A-05Google Scholar
Lieux, M (1975) Dominant pollen types recovered from commercial Louisiana honeys. Econ Bot 29:8796 Google Scholar
Lonsdale, WM, Briese, DT, Cullen, JM (2001) Risk analysis and weed biological control. Pages 185210 in Wajnberg, E, Scott, JK, Quimby, PC, eds. Evaluating Indirect Ecological Effects of Biological Control. New York CABI Publishing Google Scholar
Louda, SM, Pemberton, RW, Johnson, MT, Follett, PA (2003) Nontarget effects—the Achilles' heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365396 Google Scholar
Mack, RN, Simberloff, D, Lonsdale, WM, Evans, H, Clout, M, Bazzaz, FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689710 Google Scholar
Manrique, V, Diaz, R, Cuda, JP, Overholt, WA (2011) Suitability of a new plant invader as a target for biological control in Florida. Invasive Plant Sci Manage 4:110 Google Scholar
Matlack, GR (2002) Exotic plant species in Mississippi, USA: critical issues in management and research. Nat Areas J 22:241247 Google Scholar
McCormick, CM (2005) Chinese Tallow Management Plan for Florida. http://www.fleppc.org/publications.htm. Accessed March 5, 2013Google Scholar
McEvoy, PB, Coombs, EM (1999) Why things bite back: unintended consequences of biological weed control. Pages 167194 in Follett, PA, Duan, JJ, eds. Nontarget Effects of Biological Control. Boston Kluwer Academic Google Scholar
McEvoy, P, Cox, C, Coombs, E (1991) Successful biological control of ragwort, Senecio jacobaea, by introduced insects in Oregon. Ecol Appl 1:430442 Google Scholar
Miller, ML, Aplet, GH (2005) Applying legal sunshine to the hidden regulation of biological control. Biol Control 35:358365 Google Scholar
Mitter, C, Farrell, B (1991) Macroevolutionary aspects of insect-plant interactions. Pages 3578 in Bernays, E, ed. Insect–Plant Interactions. Boca Raton, FL CRC Press Google Scholar
Moran, VC, Hoffmann, JH, Zimmermann, HG (2005) Biological control of invasive alien plants in South Africa: necessity, circumspection, and success. Front Ecol Environ 3:7783 Google Scholar
Nelson, G (2011) The Trees of Florida. 2nd edn. Sarasota, FL Pineapple Press Google Scholar
[NYBG] New York Botanical Garden (2013) http://www.nybg.org. Accessed March 5, 2013Google Scholar
Pattison, RR, Mack, RN (2008) Potential distribution of the invasive tree Triadica sebifera (Euphorbiaceae) in the United States: evaluating CLIMEX predictions with field trials. Global Change Biol 14:813826 Google Scholar
Pattison, RR, Mack, RN (2009) Environmental constraints on the invasion of Triadica sebifera in the eastern United States: an experimental field assessment. Oecologia 158:591602 Google Scholar
Pratt, PD, Center, TD (2012) Biocontrol without borders: the unintended spread of introduced weed biological control agents. Biocontrol 57:319329 Google Scholar
Rawlins, KA, Griffin, JE, Moorhead, DJ, Bargeron, CT, Evans, CW (2013) EddMaps—Early Detection & Distribution Mapping Systems. Tifton, GA The University of Georgia–Center for Invasive Species and Ecosystem Health. www.eddmaps.org. Accessed March 15, 2013Google Scholar
Rayamajhi, MB, Pratt, PD, Center, TD, Tipping, PW, Van, TK (2009) Decline in exotic tree density facilitates increased plant diversity: the experience from Melaleuca quinquenervia invaded wetlands. Wetlands Ecol Manage 17:455467 Google Scholar
Rejmánek, M (2000) Invasive plants: approaches and predictions. Aust Ecol 25:497506 Google Scholar
Richardson, DM, Pyšek, P, Rejmánek, M, Barbour, MG, Panetta, FD, West, CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93107 Google Scholar
Riina, R, Berry, PE (coordinators) (2013) Euphorbia Planetary Biodiversity Inventory database. Available from Tolkin. http://app.tolkin.org/projects/72/taxa. Accessed March 5, 2013Google Scholar
Russell, LH, Schwartz, WL, Dollahite, JW (1969) Toxicity of Chinese tallow tree (Sapium sebiferum) for ruminants. Am J Vet Res 30:12331238 Google Scholar
Scheld, H, Cowles, J (1981) Woody biomass potential of the Chinese tallow tree. Econ Bot 35:391397 Google Scholar
SEEPPC (2001) Invasive Exotic Pest Plants in Tennessee. Published by the Tennessee Exotic Pest Plant Council. http://www.se-eppc.org. Accessed March 5, 2013Google Scholar
Sheppard, AW, Hill, R, De Clerck-Floate, R, McClay, A, Olkers, T, Quimby, PC, Zimmermann, HG (2003) A global review of risk–benefit–cost analysis for the introduction of classical biological control agents against weeds: a crisis in the making? Biocontrol News Inf 24:91N108N Google Scholar
Siemann, E, Rogers, WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4:514518 Google Scholar
Siemann, E, Rogers, WE (2003) Herbivory, disease, recruitment limitation, and success of alien and native tree species. Ecology 84:14891505 Google Scholar
Smith, GF, Nicholas, NS, Zedaker, SM (1997) Succession dynamics in a maritime forest following Hurricane Hugo and fuel reduction burns. For Ecol Manag 95:275283 Google Scholar
Stevens, PF (2011) Angiosperm Phylogeny Website. http://www.mobot.org/mobot/research/APweb/. Accessed March 5, 2013Google Scholar
Strong, DR, Pemberton, RW (2001) Food webs, risks of alien enemies and reform of biological control. Pages 5779 in Wajnberg, E, Scott, JK, Quimby, PC, eds. Evaluating Indirect Ecological Effects of Biological Control. New York CABI Publishing Google Scholar
Sutherst, RW, Maywald, GF, Yonow, T, Stevens, PM (1999) CLIMEX: Predicting the Effects of Climate on Plants and Animals. Victoria, Australia CSIRO Publishing Google Scholar
Texas Invasives.org (2013) www.texasinvasvies.org. Accessed March 5, 2013Google Scholar
Texas Parks and Wildlife Department (2013) Nongame and Rare Species Program: Federal/State Threatened and Endangered Species. www.tpwd.state.tx.us/huntwild/wild/wildlife_diversity/texas_rare_species/listed_species/.Accessed April 15, 2013Google Scholar
The Plant List (2013) Version 1. http://www.theplantlist.org/ Accessed March 5, 2013Google Scholar
Thorpe, P (1996) Evaluation of Alternatives for the Control of Invasive Exotic Plants in Lake Jackson, Florida. Havana, FL Northwest Florida Water Management District, Water Resources Special Report. 51 pGoogle Scholar
Tipping, PW, Martin, MR, Pierce, R, Center, TD, Pratt, PR, Rayamajhi, MB (2012) Post-biological control invasion trajectory for Melaleuca quinquenervia in a seasonally inundated wetland. Biol Control 60:163168 Google Scholar
U.S. Department of Agriculture–Natural Resources Conservation Service (2013) The PLANTS Database. http://plants.usda.gov. Accessed March 5, 2013Google Scholar
U.S. Fish and Wildlife Service Endangered Species Program (2006) http://ecos.fws.gov/tess_public/pub/ listedPlants.jsp. Accessed April 15, 2013Google Scholar
Van Driesche, RG, Carruthers, RI, Center, T, Hoddle, MS, Hough-Goldstein, J, Morin, L, Smith, L, Wagner, DL, Blossey, B, Brancatini, V, Casagrande, R, Causton, CE, Coetzee, JA, Cuda, J, Ding, J, Fowler, SV, Frank, JH, Fuester, R, Goolsby, J, Grodowitz, M, Heard, TA, Hill, MP, Hoffmann, JH, Huber, J, Julien, M, Kairo, MTK, Kenis, M, Mason, P, Medal, J, Messing, R, Miller, R, Moore, A, Neuenschwander, P, Newman, R, Norambuena, H, Palmer, WA, Pemberton, R, Perez Panduro, A, Pratt, PD, Rayamajhi, M, Salom, S, Sands, D, Schooler, S, Schwarzländer, M, Sheppard, A, Shaw, R, Tipping, PW, Van Klinken, RD (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54(Suppl 1):S2S33 Google Scholar
Van Driesche, RG, Hoddle, MS, Center, TD (2008) Control of Pests and Weeds by Natural Enemies. An Introduction to Biological Control. Malden, MA Blackwell Publishing. 484 pGoogle Scholar
Wang, HH, Grant, WE, Gan, J, Rogers, WE, Swannack, TM, Koralewski, TE, Miller, JH, Taylor, JW (2012a) Integrating spread dynamics and economics of timber production to manage Chinese tallow invasions in southern U.S. forestlands. PLoS One 7:e33877 Google Scholar
Wang, Y, Huang, W, Siemann, E, Zou, J, Wheeler, GS, Carrillo, J, Ding, J (2011) Lower resistance and higher tolerance of invasive host plants: biocontrol agents reach high densities but exert weak control. Ecol Appl 21:729738 Google Scholar
Wang, Y, Siemann, E, Wheeler, GS, Zhu, L, Gu, X, Ding, J (2012c) Genetic variation in anti-herbivore chemical defences in an invasive plant. J Ecol 100:894904 Google Scholar
Wang, Y, Zhu, L, Gu, X, Wheeler, GS, Purcell, M, Ding, J (2012b) Pre-release assessment of a noctuid Gadirtha inexacta ( = Iscadia inexacta) proposed as a biological control agent of Chinese tallow (Triadica sebifera) in the United States. Biol Control 63:304309 Google Scholar
Wapshere, AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201211 Google Scholar
Weaver, RE, Anderson, PJ (2010) Notes on Florida's endangered and threatened plants. Contribution No. 38, 5th edition. http://freshfromflorida.s3.amazonaws.com/fl-endangered-plants.pdf. Accessed December 31, 2013Google Scholar
Webster, GL (1994) Classification of the Euphorbiaceae. Ann. Missouri Bot. Gard. 81:332 Google Scholar
Wheeler, GS, Pemberton, RW, Raz, L (2007) A biological control feasibility study of the invasive weed-air potato, Dioscorea bulbifera L. (Dioscoreaceae): an effort to increase biological control transparency and safety. Nat Areas J 27:269279 Google Scholar
Wunderlin, RP, Hansen, BF (2008) Atlas of Florida Vascular Plants. http://www.plantatlas.usf.edu/. Accessed March 5, 2013Google Scholar
Wurdack, KJ, Davis, CC (2009) Malpighiales phylogenetics: Gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 96:15511570 Google Scholar
Wurdack, KJ, Hoffmann, P, Chase, MW (2005) Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) with the use of plastid rbcL and trnL-F DNA sequences. Am J Bot 92:13971420 Google Scholar
Zavaleta, E (2000) Valuing ecosystem services lost to Tamarix invasion in the United States. Pages 261300 in Mooney, HA, Hobbs, RJ, eds. Invasive Species in a Changing World. Washington, DC Island Press Google Scholar
Zedler, JB (2003) Wetlands at your service: reducing impacts of agriculture at the watershed scale. Front Ecol Environ 1:6572 Google Scholar
Zedler, JB, Kercher, S (2003) Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. Crit Rev Plant Sci 23:431452 Google Scholar
Zheng, H, Wu, Y, Ding, J, Binion, D, Fu, W, Reardon, R (2005) Invasive plants established in the United States that are found in Asia and their associated natural enemies. Volume 2. Morgantown, WV USDA Forest Service. 1174 Google Scholar