Abstract
One of the main obstacles of classical biological control is that biological control organisms cannot be recalled once they are released in nature. It is particularly true for the flowerhead weevil, Rhinocyllus conicus Frölich, which was released as a biological control organism for the invasive musk thistle, Carduus nutans L. (MT). While weevils successfully suppressed introduced populations of musk thistles and other invasive thistle species, non-target attacks have been reported on multiple native thistles including federally listed threatened and endangered (T&E) thistle species. To investigate the foraging behavior of female weevils on invasive and native thistles, we examined volatile organic compounds (VOCs) emitted from MT and a T&E plant species, Sacramento Mountains thistle, Cirsium vinaceum Wooton & Standley (SMT) in the Lincoln National Forest, New Mexico. We used a dynamic headspace volatile collection system and gas chromatography-mass spectrometry to compare volatile profiles between MT and SMT. Female weevils reacted to 7 electrophysiologically active chemical compounds in the blends based on gas chromatography-electroantennography. The behavioral response of female weevils was indifferent when VOCs from both thistles were offered in y-tube olfactometry experiments. Yet, they preferred VOCs collected from MT to purified air. The searching time of female weevils was longer to VOCs collected from SMT over controls. Investigating signals during the initial host recognition of released biological control organisms may open new opportunities to reduce non-target attacks on T&E plant species.
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References
Ancheta J, Heard SB (2011) Impacts of insect herbivores on rare plant populations. Biol Conserv 144:2395–2402
Blossey B, Dávalos A, Simmons W, Ding J (2018) A proposal to use plant demographic data to assess potential weed biological control agents impacts on non-target plant populations. Biocontrol 63:461–473
Briese D (1999) Open field host-specificity tests: is 'natural' good enough for risk assessment? In: Withers TM, L. Barton Browne, J. Stanley (eds.) Host specificity testing in Australasia: Towards improved assays for biological control. Department of natural resources, Coorparoo, Queensland, Australia, pp 44–59
Bruce TJ, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects–finding the right mix. Phytochemistry 72:1605–1611
Catton HA, Lalonde RG, De Clerck-Floate RA (2015) Nontarget herbivory by a weed biocontrol insect is limited to spillover, reducing the chance of population-level impacts. Ecol Appl 25:517–530
Corella-Madueño MA, Harris MK, Fu-Castillo AA, Martínez-Téllez MA, Valenzuela-Soto EM, Gálvez-Ruiz JC, Vargas-Arispuro I (2011) Volatiles emitted by Carya illinoinensis (Wang.) K. Koch as a prelude for semiochemical investigations to focus on Acrobasis nuxvorella Nuenzig (Lepidoptera: Pyralidae). Pest Manag Sci 67:1522–1527
Dueñas M-A, Ruffhead HJ, Wakefield NH, Roberts PD, Hemming DJ, Diaz-Soltero H (2018) The role played by invasive species in interactions with endangered and threatened species in the United States: a systematic review Biodivers Conserv 27:3171–3183
Gassmann A, Louda SM (2001) Rhinocyllus conicus: Initial evaluation and subsequent ecological impacts in North America. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Oxon, UK, pp 147–183
Havens K, Jolls CL, Marik JE, Vitt P, McEachern AK, Kind D (2012) Effects of a non-native biocontrol weevil, Larinus planus, and other emerging threats on populations of the federally threatened Pitcher’s thistle, Cirsium pitcheri. Biol Conserv 155:202–211
Hinz HL, Winston RL, Schwarzländer M (2019) How safe is weed biological control? A global review of direct nontarget attack. Q Rev Biol 94:1–27
Knolhoff LM, Heckel DG (2014) Behavioral assays for studies of host plant choice and adaptation in herbivorous insects. Annu Rev Entomol 59:263–278
Li N, Li S, Ge J, Schuman MC, Wei JN, Ma RY (2017) Manipulating two olfactory cues causes a biological control beetle to shift to non-target plant species. J Ecol 105:1534–1546
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 48:365–396
Louda SM, Rand TA, Arnett AE, McClay AS, Shea K, McEachern AK (2005) Evaluation of ecological risk to populations of a threatened plant from an invasive biocontrol insect. Ecol Appl 15:234–249
Miller JR, Strickler KL (1984) Finding and accepting host plants. In: Bell WJ, Carde RT (eds) Chemical ecology of insects. Sinauer Associates, Boston, MA, pp 127–157
Park I, Eigenbrode SD, Cook SP, Harmon BL, Hinz HL, Schaffner U, Schwarzländer M (2018) Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment. Biocontrol 63:377–389
Raghu S, Wilson JR, Dhileepan K (2006) Refining the process of agent selection through understanding plant demography and plant response to herbivory. Aust J Entomol 45:308–316
Rand TA, Louda SM (2006) Invasive insect abundance varies across the biogeographic distribution of a native host plant. Ecol Appl 16:877–890
Rand TA, Russell FL, Louda SM (2004) Local- vs. landscape-scale indirect effects of an invasive weed on native plants. Weed Technol 18:1250–1254
Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931
Russell FL, Louda SM, Rand TA, Kachman SD (2007) Variation in herbivore-mediated indirect effects of an invasive plant on a native plant. Ecology 88:413–423
Schiestl FP (2015) Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytol 206:571–577
Seybold SJ, Bentz BJ, Fettig CJ, Lundquist JE, Progar RA, Gillette NE (2018) Management of western North American bark beetles with semiochemicals. Annu Rev Entomol 63:407–432
Tewari S, Leskey TC, Nielsen AL, Piñero JC, Rodriguez-Saona CR (2014) Use of pheromones in insect pest management, with special attention to weevil pheromones. In: Abrol DP (ed) Integrated pest management: current concepts and ecologiacl perspective. Academic Press, San Diego, CA, pp 141–168
Acknowledgements
We thank Kathryn Kennedy (USFS) and Mary Pruitt (USFWS) for granting the research permits and Daniela Roth (EMNRD) for providing us the GPS coordinates of thistle populations to collect VOCs in the Lincoln National Forest. Two anonymous reviewers, an editorial member, and Mark A. Burgman (Imperial College) provided helpful comments to improve and clarify the manuscript’s earlier drafts.
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Park, I., Thompson, D.C. Host recognition by Rhinocyllus conicus of floral scents from invasive and threatened thistles. Biol Invasions 23, 1663–1668 (2021). https://doi.org/10.1007/s10530-021-02477-9
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DOI: https://doi.org/10.1007/s10530-021-02477-9