Abstract
Assessing the impact of temperature changes on insect population and overwintering on nontarget hosts is important for prediction of nontarget effects in weed biological control. Agasicles hygrophila is a beetle used for biological control of the invasive plant alligator weed, Alternanthera philoxeroides, with nontarget damage to a native plant, Alternanthera sessilis. In this study, we monitored plant growth and phenology along with beetle population and overwintering on these two hosts along a latitudinal gradient from subtropical to temperate climates (Guilin, Wuhan and Kaifeng) in China. We found only annual A. sessilis seedlings in temperate Kaifeng, but both annual seedlings and perennial ramets of A. sessilis were found in Guilin and Wuhan. However, in winter, living A. sessilis plants were found in only subtropical Guilin. Beetles at the Guilin site could successfully maintain their populations and overwinter on A. sessilis. Although the beetle could sustain its populations on A. sessilis at the other two higher-latitude sites during the growing season, it failed to overwinter on either species, indicating that the temperatures in different climate zones may directly and/or indirectly affect the development of insect biological control agents and their population sizes on nontarget hosts. Therefore, it is important to consider the shifting plant–insect interactions induced by climate when assessing potential nontarget effects of species introduced as biological control agents.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bale JS, Hayward SAL (2010) Insect overwintering in a climate change. J Exp Biol 213:980–994. https://doi.org/10.1242/jeb.037911
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Stat Method) 57:289–300. https://doi.org/10.2307/2346101
Coulson JR (1977) Biological control of alligatorweed, 1959–1972. A review and evaluation. Agricultural Research Service, United States Department of Agriculture, p 1547
Ding J, Wang Y, Jin X (2007) Monitoring populations Galerucella birmanica (Coleoptera: Chrysomelidae) on Brasenia schreberi and Trapa natans (Lythraceae): implications for biological control. Biol Control 43:71–77. https://doi.org/10.1016/j.biocontrol.2007.06.010
Guo JY, Fu JW, Xian XQ, Ma MY, Wan FH (2012) Performance of Agasicles hygrophila (Coleoptera: Chrysomelidae), a biological control agent of invasive alligator weed, at low non-freezing temperatures. Biol Invasions 14:1597–1608. https://doi.org/10.1890/14-1092.1
Ismail M, Brooks M (2016) The impact of geographical origin of two strains of the herbivore, Eccritotarsis catarinensis, on several fitness traits in response to temperature. J Therm Biol 60:222–230. https://doi.org/10.1016/j.jtherbio.2016.07.008
Ismail M, Compton SG, Brooks M (2017) Interaction between temperature and water nutrient levels on the fitness of Eccritotarsus catarinensis (Hemiptera: Miridae), a biological control agent of water hyacinth. Biol Control 106:83–88. https://doi.org/10.1016/j.biocontrol.2017.01.001
Jamieson MA, Schwartzberg EG, Raffa KF, Reich PB, Lindroth RL (2015) Experimental climate warming alters aspen and birch phytochemistry and performance traits for an outbreak insect herbivore. Global Change Biol 21:2698–2710. https://doi.org/10.1111/gcb.12842
Jang T, Rho MS, Koh SH, Lee KP (2015) Host-plant quality alters herbivore responses to temperature: a case study using the generalist Hyphantria cunea. Entomol Exp Appl 154:120–130. https://doi.org/10.1111/eea.12261
Julien MH, Broadbent JE, Harley KLS, Medd RW, Auld BA (1979) The current status of biological control of Alternanthera philoxeroides in Australia. In: Proceedings of the 7th Asian-Pacific weed science society conference, pp 231–233
Julien MH, Skarratt B, Maywald GF (1995) Potential geographical-distribution of alligator weed and its biological-control by Agasicles Hygrophila. J Aquat Plant Manage 33:55–60
Knapp M, Knappová J (2013) Measurement of body condition in a common carabid beetle, Poecilus cupreus: a comparison of fresh weight, dry weight, and fat content. J Insect Sci 13:1–10. https://doi.org/10.1673/031.013.0601
Lencioni V (2004) Survival strategies of freshwater insects in cold environments. J Limnol 63:45–55. https://doi.org/10.4081/jlimnol.2004.s1.45
Lu JJ, Zhao LL, Ma RY, Zhang PP, Fan RJ, Zhang JT (2010) Performance of the biological control agent flea beetle Agasicles hygrophila (Coleoptera: Chrysomelidae), on two plant species Alternanthera philoxeroides (alligatorweed) and A. sessilis (joyweed). Biol Control 54:9–13. https://doi.org/10.1016/j.biocontrol.2010.02.012
Lu JJ, Zhao LL, Ma RY, Fan RJ, Zhang JT, Wang R (2012) Non-target plant testing of the flea beetle Agasicles hygrophila, a biological control agent for Alternanthera philoxeroides (alligatorweed) in China. Biocontrol Sci Techn 22:1093–1097. https://doi.org/10.1080/09583157.2012.708019
Lu X, Siemann E, Shao X, Wei H, Ding J (2013) Climate warming affects biological invasions by shifting interactions of plants and herbivores. Global Change Biol 19:2339–2347. https://doi.org/10.1111/gcb.12244
Lu X, Siemann E, He M, Wei H, Shao X, Ding J (2015) Climate warming increases biological control agent impact on a non-target species. Ecol Lett 18:48–56. https://doi.org/10.1111/ele.12391
Lu X, Siemann E, He M, Wei H, Shao X, Ding J (2016) Warming benefits a native species competing with an invasive congener in the presence of a biocontrol beetle. New Phytol 211:1371–1381. https://doi.org/10.1111/nph.13976
Ma RY (2001) Ecological adaptation for the intruduced biocontrol agent, Agasicles hygropghila, for Alligatorweed, Alternanthera philoxeroides, in China. Dissertation, Chinese Academy of Agricultural Sciences, Beijing
Ma RY, Ding JQ, Li BT, Wu ZQ, Wang R (2003) The pupation adaptability of Agasicles hygrophial on different ecotypes alligator weed. Chin J Biol Control 19:54–58
Ma RY, Hao SG, Kong WN, Sun JH, Kang L (2006) Cold hardiness as a factor for assessing the potential distribution of the Japanese pine sawyer Monochamus alternatus (Coleoptera: Cerambycidae) in China. Ann For Sci 63:449–456. https://doi.org/10.1051/forest:2006025
Maddox DM, Andres LA, Hennessey RD, Blackburn RD, Spencer NR (1971) Insects to control alligatorweed: an invader of aquatic ecosystems in the United States. Bioscience 21:985–991. https://doi.org/10.2307/1296135
McEvoy PB (1996) Host specificity and biological pest control—how well is research on host specificity addressing the potential risks of biological control. Bioscience 46:401–405. https://doi.org/10.2307/1312873
McEvoy PB, Higgs KM, Coombs EM, Karaçetin E, Starcevich LA (2012) Evolving while invading: rapid adaptive evolution in juvenile development time for a biological control organism colonizing a high-elevation environment. Evol Appl 5:524–536. https://doi.org/10.1111/j.1752-4571.2012.00278.x
Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biol Invasions 10:859–874. https://doi.org/10.1007/s10530-008-9238-x
Myers JH, Cory JS (2017) Biological control agents: invasive species or valuable solutions? In: Vilà M, Hulme PE (eds) Impact of biological invasions on ecosystem services. Springer International Publishing, Berlin, pp 191–202. https://doi.org/10.1007/978-3-319-45121-3_12
Pan XY, Jia X, Zeng J, Sosa A, Li B, Chen JK (2011) Stem tissue mass density is linked to growth and resistance to a stem-boring insect in Alternanthera philoxeroides. Plant Spec Biol 26:58–65. https://doi.org/10.1111/j.1442-1984.2010.00307.x
Posledovich D, Toftegaard T, Wiklund C, Ehrlén J, Gotthard K (2015) The developmental race between maturing host plants and their butterfly herbivore—the influence of phenological matching and temperature. J Anim Ecol 84:1690–1699. https://doi.org/10.1111/1365-2656.12417
Raghu S, Dhileepan K, Scanlan JC (2007) Predicting risk and benefit a priori in biological control of invasive plant species: a systems modelling approach. Ecol Model 208:247–262. https://doi.org/10.1016/j.ecolmodel.2007.05.022
Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol 28:46–54. https://doi.org/10.1111/1365-2435.12135
Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integr Zool 5:132–142. https://doi.org/10.1111/j.1749-4877.2010.00196.x
Stoeckli S, Hirschi M, Spirig C, Calanca P, Rotach MW, Samietz J (2012) Impact of climate change on voltinism and prospective diapause induction of a global pest insect—Cydia pomonella (L.). PLoS ONE 7:e35723. https://doi.org/10.1371/journal.pone.0035723
Uelmen JA Jr, Lindroth RL, Tobin PC, Reich PB, Schwartzberg EG, Raffa KF (2016) Effects of winter temperatures, spring degree-day accumulation, and insect population source on phenological synchrony between forest tent caterpillar and host trees. For Ecol Manag 362:241–250. https://doi.org/10.1016/j.foreco.2015.11.045
Wang R, Wang Y, Zhang GC, Li JX (1988) The host specificity test of Agasicles hygrophila. Chin J Biol Control 4:14–17. https://doi.org/10.16409/j.cnki.2095-039x.1988.01.006
Wu ZQ, Cai YC, Guo ZX, Wang TB (1994) Host specificity tests for Agasicles hygrophila (Coleoptera: Chrysomelidae), a biological control agent of alligator weed. J Biosafety 3:98–100
Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10. https://doi.org/10.1111/j.1461-0248.2009.01402.x
Zhao LL, Jia D, Yuan XS, Guo YQ, Zhou WW, Ma RY (2015) Cold hardiness of the biological control agent, Agasicles hygrophila, and implications for its potential distribution. Biol Control 87:1–5. https://doi.org/10.1016/j.biocontrol.2015.02.007
Zhu Z, Zhou CC, Yang J (2015) Molecular phenotypes associated with anomalous stamen development in Alternanthera philoxeroides. Front Plant Sci 6:1–10. https://doi.org/10.3389/fpls.2015.00242
Acknowledgements
We would like to thank Saichun Tang, Yumei Pan, Chunqiang Wei, Baoliang Tian, Xiao Sun, Xiangqin Li, Li Xiao, Jia Liu, Zhenzhen Yu, Zhen Liu and Shunliang Feng for field and laboratory assistance. Edits and comments by Roy Van Driesche, Emmet Van Driesche, Springer Nature Author Services as well as the journal editor and reviewers improved earlier versions of this manuscript. This work was supported by the National Key Research and Development Program (2017 YFC 1200100).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by M. Traugott.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, Y., Ismail, M., Huang, W. et al. Population dynamics and overwintering of a biological control beetle, Agasicles hygrophila, on a nontarget plant Alternanthera sessilis, along a latitudinal gradient. J Pest Sci 92, 835–845 (2019). https://doi.org/10.1007/s10340-018-1031-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-018-1031-8