Colchicum Autumnale) Bulb Powder on Red Imported Fire Ants (Solenopsis Invicta
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toxins Article Toxicity and Sublethal Effects of Autumn Crocus (Colchicum autumnale) Bulb Powder on Red Imported Fire Ants (Solenopsis invicta) Sukun Lin 1, Deqiang Qin 1, Yue Zhang 1, Qun Zheng 1, Liupeng Yang 1, Dongmei Cheng 2, Suqing Huang 3, Jianjun Chen 4,* and Zhixiang Zhang 1,* 1 Key Laboratory of Natural Pesticide and Chemical Biology of the Ministry of Education, South China Agricultural University, Guangzhou 510642, China; [email protected] (S.L.); [email protected] (D.Q.); [email protected] (Y.Z.); [email protected] (Q.Z.); [email protected] (L.Y.) 2 Department of plant protection, Zhongkai University of Agricultural and Engineering, Guangzhou 510225, China; [email protected] 3 College of Chemistry and Chemical Engineering, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China; [email protected] 4 Department of Environmental Horticulture and Mid-Florida Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Apopka, FL 32703, USA * Correspondence: jjchen@ufl.edu (J.C.); [email protected] (Z.Z.) Received: 18 September 2020; Accepted: 17 November 2020; Published: 21 November 2020 Abstract: Autumn crocus (Colchicum autumnale L.) is a medicinal plant as it contains high concentrations of colchicine. In this study, we reported that the ground powder of autumn crocus bulb is highly toxic to invasive Solenopsis invicta Buren, commonly referred to as red imported fire ants (RIFAs). Ants fed with sugar water containing 5000 mg/L of bulb powder showed 54.67% mortality in three days compared to 45.33% mortality when fed with sugar water containing 50 mg/L of colchicine. Additionally, the effects of short-term feeding with sugar water containing 1 mg/L of colchicine and 100 mg/L of autumn crocus bulb powder were evaluated for RIFAs’ colony weight, food consumption, and aggressiveness, i.e., aggregation, grasping ability, and walking speed. After 15 days of feeding, the cumulative colony weight loss reached 44.63% and 58.73% due to the sublethal concentrations of colchicine and autumn crocus bulb powder, respectively. The consumption of sugar water and mealworm (Tenebrio molitor L.) was substantially reduced. The aggregation rates decreased 48.67% and 34.67%, grasping rates were reduced to 38.67% and 16.67%, and walking speed decreased 1.13 cm/s and 0.67 cm/s as a result of the feeding of the two sublethal concentrations of colchicine and autumn crocus bulb powder, respectively. Our results for the first time show that powder derived from autumn crocus bulbs could potentially be a botanical pesticide for controlling RIFAs, and application of such a product could be ecologically benign due to its rapid biodegradation in the environment. Keywords: autumn crocus; Colchicum autumnale; colchicine; invasive species; pest control; red imported fire ant (RIFA) Key Contribution: This study found that colchicine in autumn crocus (Colchicum autumnale L.) bulb powder was 0.3%, and solutions made from the bulb powder or commercial colchicine were toxic to the red imported fire ant (Solenopsis invicta Buren), a notorious invasive pest. Our results suggest that autumn crocus bulb powder could be potentially used as a botanical pesticide for control of red imported fire ants. Toxins 2020, 12, 731; doi:10.3390/toxins12110731 www.mdpi.com/journal/toxins Toxins 2020, 12, 731 2 of 12 1. Introduction Solenopsis invicta Buren, commonly known as the red imported fire ant (RIFA), is a dominant and detrimental invasive species [1–3]. RIFA is native to South America [4], and was discovered in southern Alabama in the 1930s [5] and subsequently in Australia [6,7], New Zealand [8], Malaysia [9], Taiwan [10,11], and mainland China [12]. A mature RIFA colony contains a single queen or multiple queens with a large number of workers ranging from 200,000 to 400,000 [13]. They are extremely aggressive andToxins voracious 2020, 12, x FOR feedersPEER REVIEW and can quickly disrupt ground fauna, causing2 the of 12 imbalance of specific natural ecosystems [14]. Fire ant workers sting relentlessly when their mound is disturbed. 1. Introduction To control RIFAs, many contact insecticides, including chlorpyrifos and pyrethroid, have been widely Solenopsis invicta Buren, commonly known as the red imported fire ant (RIFA), is a dominant used [15]. However,and detrimental the use invasive of synthetic species [1–3]. insecticides RIFA is native may to South cause America environmental [4], and was discovered contamination in and are also prone to insecticidesouthern Alabama resistance. in the 1930s Thus, [5] and naturally subsequently occurring, in Australialow-resistant, [6,7], New Zealand and [8], ecologicallyMalaysia friendly control methods[9], haveTaiwan been [10,11], explored and mainland for RIFAChina [12]. management A mature RIFA [16 colony,17]. Amongcontains a them,single queen biological or pesticides multiple queens with a large number of workers ranging from 200,000 to 400,000 [13]. They are or biopesticidesextremely are valuable aggressive alternatives and voracious tofeeders synthetic and canpesticides quickly disrupt [18 ground]. fauna, causing the Biopesticidesimbalance are of natural specific natural products ecosystems derived [14].from Fire ant living workers organisms sting relentlessly including when their microbes, mound nematodes, is disturbed. To control RIFAs, many contact insecticides, including chlorpyrifos and pyrethroid, and plants thathave canbeen limitwidely orused reduce [15]. However, pest the populations use of synthetic [19 insecticides,20]. Biopesticides may cause environmental are usually unique and complexcontamination and have diandff erentare also modesprone to insecticide of action; resistance. thus, Thus, pests naturally are less occurring, likely low-resistant, to develop resistance. Biopesticides areand generallyecologically friendly safer than control synthetic methods have ones been to explored the environment for RIFA management as they [16,17]. can be Among quickly degraded, them, biological pesticides or biopesticides are valuable alternatives to synthetic pesticides [18]. and they are alsoBiopesticides more friendly are natural to nontarget products derived organisms from living [21,22 organisms]. The useincluding of biopesticides microbes, has been increasing globallynematodes, each and year. plants North that can America limit or reduce is the pest largest populations biopesticide [19,20]. Biopesticides market, are accounting usually for 44% of the market valueunique [23 and]. complex and have different modes of action; thus, pests are less likely to develop resistance. Biopesticides are generally safer than synthetic ones to the environment as they can be Autumnquickly crocus degraded, (Colchicum and they autumnale are also moreL.), friendly also knownto nontarget as organisms meadow [21,22]. saff ron,The use is of an herbaceous perennial plantbiopesticides in the familyhas been Colchicaceaeincreasing globally and each isyear. cultivated North America as anis the ornamental largest biopesticide plant [24,25] and market, accounting for 44% of the market value [23]. medicinal herb [26Autumn]. Its crocus flowers (Colchicum arise autumnale from underground L.), also known bulbsas meadow without saffron, leavesis an herbaceous and often achieve a height of 20 toperennial 25 cm plant (Figure in the1 A).family All Colchicaceae organsof and the is cultivated plant are as toxican ornamental and contain plant [24,25] alkaloids, and of which colchicine contributesmedicinal herb 50–70% [26]. Its offlowers the arise total from alkaloid underground content bulbs [ 25without]. These leaves alkaloidsand often achieve withstand a storage, height of 20 to 25 cm (Figure 1A). All organs of the plant are toxic and contain alkaloids, of which drying, and heatcolchicine treatment. contributes Colchicine 50–70% of the is total a medication alkaloid content used [25]. to These treat alkaloids gout andwithstand Bechet’s storage, disease [27,28]. It can inhibit microtubuledrying, and heat treatment. formation Colchici in cellne is mitosis,a medication thus used inducing to treat gout polyploid and Bechet’s disease plants [27,28]. [29,30 ]. However, autumn crocusIt can and inhibit colchicine microtubule have formation been in rarely cell mitosis, reported thus inducing to have polyploid any insecticidalplants [29,30]. However, activities. autumn crocus and colchicine have been rarely reported to have any insecticidal activities. Figure 1. Autumn crocus (Colchicum autumnale) plants at the time of flowering (A), underground bulbs (B), sliced bulb (C), ground bulb powder (D), HPLC chromatogram of colchicine standard at 10 mg/L (E) and autumn crocus bulb powder sample (F). The fourth (far right) peak in (F) had the same UV-Vis spectra as the peak of colchicine (E). Toxins 2020, 12, 731 3 of 12 Toxins 2020, 12, x FOR PEER REVIEW 3 of 12 In ourFigure studies 1. Autumn with RIFAs,crocus (Colchicum we found autumnale that) autumnplants at the crocus time of had flowering toxic (A e),ff undergroundects on RIFAs. Thus, this study wasbulbs intended (B), sliced bulb toanalyze (C), ground colchicine bulb powder levels (D), HPLC in autumn chromatogram crocus of colchicine bulb and standard determine at 10 toxic and sublethal effmg/Lects (E of) and colchicine autumn crocus and bulb autumn powder crocussample (F bulb). The fourth powder (far right) on RIFAs, peak in (F including) had the same the mortality, UV-Vis spectra as the peak of colchicine (E). colony weight, food consumption,