molecules Article Insecticidal and Attractant Activities of Magnolia citrata Leaf Essential Oil against Two Major Pests from Diptera: Aedes aegypti (Culicidae) and Ceratitis capitata (Tephritidae) † Ngoc Anh Luu-Dam 1,2, Nurhayat Tabanca 3,* , Alden S. Estep 4 , Duy Hung Nguyen 1 and Paul E. Kendra 3,* 1 Vietnam Academy of Science and Technology (VAST), Graduate University of Science and Technology, No. 18 Hoang Quoc Viet Road, Cau Giay District, Hanoi 100803, Vietnam; [email protected] (N.A.L.-D.); [email protected] (D.H.N.) 2 Vietnam National Museum of Nature, Vietnam Academy of Science and Technology (VAST), No.18 Hoang Quoc Viet Road, Cau Giay District, Hanoi 100803, Vietnam 3 United States Department of Agriculture-Agricultural Research Service (USDA-ARS), Subtropical Horticulture Research Station (SHRS), 13601 Old Cutler Rd., Miami, FL 33158, USA 4 United States Department of Agriculture-Agricultural Research Service (USDA-ARS), Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Gainesville, FL 32608, USA; [email protected] * Correspondence: [email protected] (N.T.); [email protected] (P.E.K.) † This work was produced by US government employees and is in the public domain in the US. Abstract: In this study, Magnolia citrata Noot and Chalermglin (Magnoliaceae) essential oil (MCEO) Citation: Luu-Dam, N.A.; was evaluated for insecticidal activity against the yellow fever mosquito Aedes aegypti and attractant Tabanca, N.; Estep, A.S.; activity for the Mediterranean fruit fly Ceratitis capitata. The leaves of Magnolia citrata (Giổi chanh) Nguyen, D.H.; Kendra, P.E. were collected from northwestern Vietnam, and the water-distilled MCEO was analyzed by gas- Insecticidal and Attractant Activities of chromatography and mass spectrometry (GC-MS). The major constituents of MCEO were identified Magnolia citrata Leaf Essential Oil as linalool 19%, geranial 16%, citronellal 14%, neral 14%, and sabinene 12%. MCEO showed 100% against Two Major Pests from Diptera: µ µ Aedes aegypti (Culicidae) and mortality at 1 g/ L against 1st instar larvae of Ae. aegypti (Orlando strain, ORL), and the oil Ceratitis capitata (Tephritidae) . exhibited 54% (ORL) and 68% (Puerto Rico strain) mortality at 5 µg/mosquito against Ae. aegypti Molecules 2021, 26, 2311. https:// adult females. Initial screens showed that MCEO had weak insecticidal activity compared to the doi.org/10.3390/molecules26082311 positive control permethrin. In bioassays with sterile male C. capitata, MCEO exhibited moderately strong attraction, comparable to that observed with a positive control, Tetradenia riparia essential oil Academic Editors: Ladislav Kokoska (TREO). Herein, the insecticidal and attractant activities of MCEO are reported for the first time. and Laura De Martino Keywords: Magnoliaceae; mosquito; medfly; fruit fly; GC-MS; aliphatic aldehydes; citronellal; Received: 22 March 2021 geranial; citral Accepted: 14 April 2021 Published: 16 April 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- The extensive and long-term application of pesticides has resulted in an accumula- iations. tion of residues in food, water, soil, and other environmental components. The negative impact of pesticides on biodiversity, and increasing pesticide resistance, have prompted more research on alternative control strategies using botanicals, biological, cultural, and other sustainable methods for integrated management of existing and invasive pests [1–6]. Plants synthesize a diverse array of molecules that can be exploited to develop novel Copyright: © This work was pro- pest control agents [7–9]. Vietnam is a tropical Asian country with extraordinarily rich duced by US government employees plant biodiversity, and many of the indigenous plants are known to have medicinal prop- and is in the public domain in the US. Sub-mitted for possible open access erties; the country’s rich forest ecosystems provide an abundant opportunity to search publication under the terms and for phytochemicals with potential applications for the management of major insect pest conditions of the Creative Com-mons species [10–12]. Aedes aegypti L. (Diptera: Culicidae) mosquitoes are the major vector for Attribution (CC BY) license (https:// the transmission of several uncontrolled, life-threatening viral diseases, which are more creativecommons.org/licenses/by/ frequent in hot and humid climate regions [13,14], and thus effective mosquito control 4.0/). of both larval and adult stages can reduce the impact of vector-borne diseases. As an Molecules 2021, 26, 2311. https://doi.org/10.3390/molecules26082311 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 10 Molecules 2021, 26, 2311 2 of 10 both larval and adult stages can reduce the impact of vector-borne diseases. As an eco- nomically important agricultural pest, the Mediterranean fruit fly, Ceratitis capitata economically important agricultural pest, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), is one of the most serious invasive pests in tropical (Wiedemann) (Diptera: Tephritidae), is one of the most serious invasive pests in tropical and subtropical regions around the world [15]. [15]. It It attacks attacks a a wide wide range range of of fruits fruits and and vege- veg- etables,tables, with with larval larval infestation infestation causing causing severe severe damage to manymany commerciallycommercially importantimportant tropicaltropical andand subtropicalsubtropical cropscrops [[16,17].16,17]. Thus,Thus, identificationidentification ofof effectiveeffective attractantsattractants forfor earlyearly detection and suppression ofof C.C. capitatacapitata populationspopulations isis criticalcritical forfor managingmanaging thisthis pestpest andand reducingreducing cropcrop losses.losses. The genus genus MagnoliaMagnolia L.L. (Magnoliaceae) (Magnoliaceae) is one is one of the of ol thedest oldest families families of flowering of flowering plants plants[18]. The [18 ].genus The genus comprises comprises about about 245 245taxa taxa occurring occurring in intemperate temperate and and tropical tropical areas areas ofof Southeast andand EastEast Asia, Asia, North North America, America, the the Antilles, Antilles, and and Central Central and and South South America America [19]. Magnolia[19]. Magnoliaspecies species have have attracted attracted a great a great deal deal of research of research interest interest due due to theto the presence presence of biphenolicof biphenolic phytochemicals phytochemicals magnolol magnolol and an honokiol,d honokiol, which which possess possess diverse diverse pharmacological pharmaco- properties,logical properties, including including inhibition inhibition of the central of the nervous central nervous system, preventionsystem, prevention of cardiovascular of cardi- disease,ovascular anti-inflammatory, disease, anti-inflammatory, antimicrobial, antimicrobial, antioxidative, antioxidative, and free radical and scavengingfree radical activ-scav- ityenging [20– 22activity]. Magnolia [20–22].extracts Magnolia and extracts their bioactive and their chemicals bioactive have chemicals been evaluated have been for evalu- their promisingated for their insecticidal promising activity. insecticidal A lignan, activity epimagnoline. A lignan, A,epimagnoline was isolated A, from was flower isolated buds from of M.flower fargesii buds(Finet of M. and fargesii Gagnep.) (Finet [23 and]. Larvicidal Gagnep.) activity [23]. Larvicid of differental activity solvent of extracts different of solventM. sali- cifoliaextractsMaxim. of M. showedsalicifolia good Maxim. to moderate showed good effect to on moderate fourth instar effect larvae on fourth of Aedes instar aegypti larvae[24 of]. EssentialAedes aegypti oils from[24]. EssentialM. grandiflora oils fromL. were M. testedgrandiflora for insecticidal L. were tested and bitingfor insecticidal deterrent and activity bit- againsting deterrentAe. aegypti, activityand against the seed Ae. aegypti, oil exhibited and the biting seed deterrenceoil exhibited similar biting todeterrence the standard sim- insectilar to the repellent standard DEET insect (N ,repellentN-diethyl-3-methylbenzamide) DEET (N,N-diethyl-3-methylbenzamide) [25]. Tests for insecticidal [25]. Tests sus- for ceptibilityinsecticidal to susceptibility ethanol extracts to ethanol from M extracts. dealbata fromZucc. M. dealbata [26] and Zucc.M. schiedeana [26] and M.Schltl. schiedeana were carriedSchltl. were out against carried the out tephritid against the fruit tephritid fly Anastrepha fruit fly ludens Anastrepha(Loew) ludens [27]. Sarcotesta (Loew) [27]. extract Sar- fromcotestaM .extractdealbata from[26], M as. welldealbata as the [26], seed as and well sarcotesta as the seed extracts and fromsarcotestaM. schiedeana, extracts fromshowed M. potentialschiedeana, insecticidal showed potential activity insecticidal against adults activity of A. against ludens adults[27]. Magnolia of A. ludens citrata [27].Noot Magnolia and Chalermglincitrata Noot and is an Chalermglin evergreen tree is an (Figure evergreen1) that tree grows (Figure naturally 1) that in grows three localitiesnaturally inin Thai-three landlocalities and atin oneThailand locality and in Vietnamat one locality [28–30 in]. LeavesVietnam are [28–30]. locally knownLeaves asare Gi locallyổi chanh’ known due toas strongGiổi chanh’ citrus due or lemongrass to strong citrus odor or and lemongrass used as