Sublethal Effect of Imidacloprid on Solenopsis Invicta
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Sublethal Effect of Imidacloprid on Solenopsis invicta (Hymenoptera: Formicidae) Feeding, Digging, and Foraging Behavior Author(s): Lei Wang, Ling Zeng, and Jian Chen Source: Environmental Entomology, 44(6):1544-1552. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1093/ee/nvv127 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. BEHAVIOR Sublethal Effect of Imidacloprid on Solenopsis invicta (Hymenoptera: Formicidae) Feeding, Digging, and Foraging Behavior 1 1 2,3 LEI WANG, LING ZENG, AND JIAN CHEN Environ. Entomol. 44(6): 1544–1552 (2015); DOI: 10.1093/ee/nvv127 ABSTRACT There is increasing evidence that exposure to neonicotinoid insecticides at sublethal levels impairs colonies of honeybees and other pollinators. Recently, it was found that sublethal contamination with neonicotinoids also affect growth and behavior of ants. In this study, we exposed red imported fire ants, Solenopsis invicta Buren, to sublethal dosages of dietary imidacloprid and investigated its effect on ant feeding, digging, and foraging behavior. S. invicta consumed significantly more sugar water con- taining 0.01 lg/ml imidacloprid than untreated sugar water. Ants fed with 0.01 lg/ml imidacloprid also showed significantly increased digging activity than ants fed with untreated sugar water. However, imidacloprid at 0.25 lg/ml significantly suppressed sugar water consumption, digging, and foraging behavior. These results indicate that imidacloprid at sublethal concentrations may have a significant and complicated effect on S. invicta. KEY WORDS Solenopsis invicta, neonicotinoid, sublethal concentration, feeding, recruitment Neonicotinoids are widely used insecticides (Jeschke were also detected in bee pollen (Mullin et al. 2010, et al. 2011). Imidacloprid, a common neonicotinoid in- Blacquie`re et al. 2012). secticide, was routinely used on rice, sunflower, maize, Worldwide population declines of many pollinators potatoes, vegetable, sugar beets, fruit, cotton, hops, and may be caused by the extensive use of neonicotinoids turfs as seed dressing, soil treatment, and foliar spray (Decourtye and Devillers 2010). Neonicotinoids at sub- (Elbert et al. 2008). Residues and degradation of imida- lethal levels can effect learning and memory of honey- cloprid in soils, vegetable, food, and water have been bees (Decourtye et al. 2004, Aliouane et al. 2009), and well investigated. The half-life of imidacloprid can decrease their foraging success (Blacquie`re et al. 2012, range from 28.7 to 47.8 d in three different soil types— Henry et al. 2012). After feeding on dietary imidaclo- Gangetic alluvial soil, lateritic soil, and coastal alkaline prid at 6 to 12 ppb for 2 wk, the growth rate and queen soil (Sarkar et al. 2001). In vineyard, 86 d after the ap- production of colonies of the bumble bee, Bombus ter- plication at recommended and double the recom- restris (L.), were significantly reduced (Whitehorn et al. mended dosages (Confidor 200SL at 400 and 800 g 2012). On exposure to field-realistic doses of imidaclo- haÀ1 1,000 literÀ1 of water, 0.008 and 0.016% a.i.), the prid, pollen foraging efficiency, wax pot production, and residue level of imidacloprid in soil reached 0.12 and nectar storage of bumblebees, Bombus spp., were re- 0.22 mg/kg, respectively (Arora et al. 2009). When the duced (Felttham et al. 2014, Scholer and Krischik field was treated with imidacloprid (seed dressing), imi- 2014), and foraging preferences for the flower types dacloprid was detected at the end of the cultivation in were altered (Gill and Raine 2014). the soils with various compositions (mean ¼ 12 lg/kg; Among the few studies on ants, it was found that Bonmatin et al. 2003). In a study on the residues of exposure to sublethal neonictinoids can change ant be- imidacloprid in vegetables, fruits, and water samples havior and colony fitness. For instance, interspecific ag- collected from the West Bank, Palestine, the highest gressive behavior and colony fitness of Southern ants, and lowest imidacloprid concentrations were found in Monomorium antarcticum (Smith), and Argentine ants, eggplant (0.46 mg/kg) and green beans (0.08 mg/kg), re- Linepithema humile (Mayr), were altered after feeding spectively (Daraghmeh et al. 2007). Neonicotinoids on aqueous honey solution containing 1.00 lg/ml imida- cloprid (Barbieri et al. 2013). Imidacloprid at 10 ng/ant reduced self-grooming behavior of Acromyrmex subter- We declare that no conflict of interests exists. Mention of trade raneus subterraneus (Forel) (Galvanho et al. 2013). In names or commercial products in this publication is solely for the pur- this study, we investigated the effect of dietary imidaclo- pose of providing specific information and does not imply recommen- dation or endorsement by the U. S. Department of Agriculture. prid at concentrations ranging from 0.01 to 1.0 lg/ml on 1 College of Agriculture, South China Agricultural University, 483 feeding, digging, and foraging behavior of red imported Wushan Rd., Guangzhou, Guangdong 510642, P. R. China. 2 fire ants, Solenopsis invicta Buren, as these behaviors National Biological Control Laboratory, Southeast Area, Agricul- are essential to colony development. Due to its signifi- ture Research Service, United States Department of Agriculture, 59 Lee Rd., Stoneville, MS 38776. cance in public health, agriculture, and biodiversity, S. 3 Corresponding author, e-mail: [email protected]. invicta is considered as one of the worst invasive species Published by Oxford University Press on behalf of Entomological Society of America 2015. This work is written by US Government employees and is in the public domain in the US. December 2015 WANG ET AL.: SUBLETHAL EFFECT OF IMIDACLOPRID ON S. invicta 1545 in the world (Lowe et al. 2000). S. invicta has become contained 15 ml 5% sugar water and the other tube one of the most well studied ant species in the contained 15 ml sugar water with 0.01 lg/ml imidaclo- world (http://www.myrmecos.net/2009/01/25/the-most- prid. Ants were starved for 48 h before the experiment. studied-ant-species-are-either-trampy-or-european/, last The feeding tubes were weighed before and after the accessed 4 August 2015), making it an ideal model to 7-d feeding period and average daily consumption (mg evaluate the effect of neonicotinoid insecticides on ants. sugar water/gram ant/day) was calculated for each tube. Five colonies were used. Digging Bioassay. Digging is an intrinsic behavior Materials and Methods of S. invicta workers. They will dig whenever a suitable Insects. Red imported fire ant S. invcta colonies substrate is available. The effect of imidacloprid on ant were collected from Leroy Percy Wildlife Management digging effort was evaluated using the difference in the Area, Washington County, MS. Pesticide use is not amount of sand removed between ants fed on sugar allowed in this area. Species identity was confirmed water containing imidacloprid and those fed on using ant cuticular hydrocarbon characteristics (Ross untreated sugar water. Two bioassays were conducted: et al. 1987). Colonies were fed with 10% w/w sugar bioassay 1, in which sugar water supply in both control water and frozen crickets. All colonies were reared and imidacloprid treatments were unlimited before dig- under laboratory condition (28C and 45% relative ging bioassays, and bioassay 2, in which sugar water humidity [RH]) for at least 1 wk prior to experiment. supply in control but not in imidacloprid treatments Polygyne colonies were used in this study. were limited. In bioassay 1, fire ants were found to con- Insecticides and Sublethal Dosage. Imidacloprid sume significantly less sugar water containing (>99.9% purity, Sigma-Aldrich, St. Louis, MO) was 0.25 lg/ml imidacloprid than control. Because sugar directly dissolved in 5% w/w sugar water. Based on pre- intake itself might affect ant digging performance, to vious studies (Barbieri et al 2013, Galvanho et al 2013) evaluate the effect of imidacloprid, the possible effect and our preliminary experiments, five concentrations of of sugar intake must be minimized. To accomplish this, imidacloprid—0.01, 0.05, 0.25, 0.50, and 1.00 lg/ml— bioassay 2 was included. were selected for feeding and digging bioassays and For bioassay 1, subcolonies from the nonchoice feed- two concentrations—0.01 and 0.25 lg/ml—for foraging ing bioassays were used. Those subcolonies had fed on bioassays. Solutions were freshly prepared before each sugar water containing 0.00, 0.01, 0.05, 0.25, 0.50, or experiment. 1.00 lg/ml imidacloprid for 7 d. The digging bioassay Feeding Bioassay. The effect of imidacloprid on apparatus developed by Chen and Allen (2006) was sugar water consumption was evaluated in both non- used for the digging study. The apparatus consists of choice and choice bioassays. In nonchoice feeding bio- one Petri dish (9.0 by 2.0 cm2) and a capped Wheaton assay, a colony was divided into four subcolonies with liquid scintillation vial (2.8 by 6.1 cm2) right under- same weight, and each subcolony had at least one neath it (Supp. Fig. 1 [online only]). There was a 3-mm queen. Ants in these subcolonies were first starved for access hole between the Petri dish and the vial.