1 U.S. Department of Agriculture (USDA), Agricultural Research Service (ARS), U.S. Arid Land Agricultural Research Center, Maricopa, AZ, United States of AmericaFind articles by
1 U.S. Department of Agriculture (USDA), Agricultural Research Service (ARS), U.S. Arid Land Agricultural Research Center, Maricopa, AZ, United States of AmericaFind articles by
The western tarnished plant bug, Lygus hesperus Knight (Hemiptera: Miridae) and the whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) are key hemipteran pests of numerous crop plants throughout the western United States and Mexico. Management in the U.S. currently relies on only a few insecticides and is threatened by the evolution of resistance. New chemistries or alternative management strategies are needed to reduce selection pressure on current insecticides and enhance control. Here, we investigated the bio-insecticidal toxicity of the French marigold, Tagetes patula Linnaeus (Asterales: Asteraceae), against both L. hesperus and B. tabaci. Assays indicated significantly reduced survival of both pest species on T. patula plants, and in diet incorporation assays containing aqueous and methanolic marigold foliar extracts. Mortality was concentration-dependent, indicating the presence of one or more extractable toxicants. These data suggest that T. patula plants have insecticidal constituents that might be identified and developed as novel alternatives to conventional chemical treatments.
Many plants exhibit resistance to insect attack that typically arises from one or more mechanisms; tolerance, non-preference, or antibiosis [1–4]. Antibiosis (where plant defenses affect pest biology) is often facilitated by phytotoxins, some of which have been developed as botanical pesticides. Pyrethrum, nicotine, neem oil, essential oils, and rotenone are examples of phytochemicals used as commercial botanical pesticides [5–7]. Several more recently investigated plant extracts and essential oils also show promising activity as bio-insecticides [8–12] or repellents [13,14].
Several species of marigold (Tagetes spp.) are known to contain phytochemicals with pesticidal activity. For example, numerous studies have shown insecticidal activity associated with Tagetes erecta L. (African marigold), T. minuta L. (Mexican marigold), or T. patula L. (French marigold) against mosquitoes [15–20], sand flies [21], a leaf hopper [22], grain/seed beetles [23–26], termites [27], human head lice [28], bed bug [29], an aphid [30], and several caterpillars [31,32]. These marigold species have also shown activity as acaricides [33,34] and nematocides [35–37].
Numerous insecticidal compounds have been isolated from essential oils and root extracts of Tagetes spp. [30,38]. Monoterpenoids, carotenoids, and flavonoids are the major biocidal constituents of volatile oils from aerial plant parts of Tagetes spp. [30,38]. Photoactive thiophenes, present primarily in roots and flowers, are also biologically active against several insect species [19,23,39–41]. Unfortunately, many of these active compounds have limited practical use because they are volatile and have poor persistence under field conditions [5].
The western tarnished plant bug, Lygus hesperus Knight (Hemiptera: Miridae) and the whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) are two major pests of cotton and other crops throughout the western United States [42–44]. Tarnished plant bug management typically relies on multiple applications of conventional insecticides of various chemical classes [45–46]. Whitefly control in the western U.S. is primarily dependent on insect growth regulators (IGRs) and neonicotinoids [46–47], although broad-spectrum insecticides are also used [46]. In Arizona, an Integrated Pest Management program has been implemented against both lygus and whitefly [44]. However, success of this program is dependent on the continued effectiveness of only a few insecticides [48]. Because these few chemicals have been widely used for many years and because both pest species have evolved resistance to numerous other insecticides [48–52], new control tactics are needed. Hence, the discovery of new compounds or complex mixtures of bioactive compounds with novel insecticidal modes of action are needed to reduce such selection pressure, and novel botanical insecticides could fill such pest management niches [9]. Here, we demonstrate that the marigold, T. patula, and its crude extracts, have toxicological activity against two important hemipteran pest species, revealing that future benefits might include use of foliar extracts for direct use as botanical insecticides as well as a resource for future isolation and development of beneficial compounds.
The vibrant colors and elegant blooms of African marigolds are a beloved addition to many gardens. However, the standing water that collects in trays under potted specimens provides an ideal breeding spot for mosquitoes. Allowing larvae to flourish puts you and your family at risk of mosquito-borne diseases. Getting rid of larvae in flower water takes some effort, but is crucial to ensure your health and continue enjoying these classic flowers.
Dangers of Mosquitoes in the Garden
Mosquitoes transmitting serious illnesses like West Nile Zika dengue, chikungunya, and malaria are spreading farther geographically every year. Mosquito-borne diseases are becoming harder to avoid. Letting larvae propagate in your flower pots exponentially increases local disease risk. A single neglected tray filled with water could produce hundreds of dangerous adult mosquitoes within weeks. With some diligence and planning, you can grow gorgeous African marigolds pest-free.
Start by Eliminating Standing Water
The most basic step in controlling mosquito larvae is to remove potential breeding sites. This means getting rid of any standing water that lingers for more than a few days. For potted African marigolds, empty the trays under pots immediately after watering. Don’t allow water to stand for long periods. Adjust watering frequency and volume to avoid excess accumulation in saucers. Consider grouping several pots on an elevated, slatted rack so water freely drains away.
Introduce a Predator
Nature provides another way to knock down mosquito larvae—let predators eat them! Tiny fish like mosquito fish (Gambusia affinis) and guppies are voracious larvavores. Add a few to each flower pot’s water reservoir or saucer after watering. Just a handful of small fish can wipe out 100s of larvae daily. The fish stay contained and focused on their task while helping control mosquitoes. Make sure you research local regulations first, as mosquito fish are considered invasive in some areas.
Apply a Natural Larvicide
When standing water can’t be fully eliminated, using a natural larvicide is the next best step An effective microbial option is Bacillus thuringiensis israelensis. This bacterium releases toxins that specifically target and wipe out mosquito larvae upon ingestion. Bacillus thuringiensis israelensis, or Bti, has no effects on people, pets, birds, fish, or other wildlife, so it’s safe for use around African marigolds.
How to Apply Bacillus thuringiensis israelensis
Bti comes as a liquid concentrate or granules that you sprinkle into standing water. It’s available at most garden centers. For potted African marigolds, use the granular formulation labeled for fountains, ponds, and large planters. Follow label directions for dosage based on the amount of standing water. One application should provide mosquito control for 3-4 weeks. Reapply any time new water accumulates. Make sure to directly treat every possible mosquito breeding area.
Stop Mosquitoes at the Source
For a truly comprehensive mosquito management plan, also address potential breeding areas away from your flowers. Take steps like:
- Emptying or changing water in bird baths, pet dishes, and other containers weekly
- Removing excess foliage to eliminate water-holding pockets
- Filling ruts and puddles in yards
- Checking for trapped water in kids’ toys, tarps, tires, etc.
- Cleaning clogged gutters holding stagnant rainwater
- Ensuring proper drainage around structures
Enjoy Your Garden Pest-Free
Don’t let concerns over mosquito larvae stop you from including gorgeously colorful African marigolds in your garden design. With some basic diligence, you can readily prevent mosquitoes from breeding in flower pot water sources. Eliminate standing water, add natural predators, and apply targeted larvicides made just for mosquito control. Taking the time to incorporate these methods means you and your family can fully enjoy warm evenings among the marigolds without fear of mosquito bites. Pitting nature against itself, you’ll win the battle against these biting pests!
1 Marigold toxicity to Lygus hesperus
When L. hesperus adults were held on intact plants, mortality occurred more rapidly on marigolds compared with the common bean control ( ; ANCOVA F = 6.23; df = 1,22; P = 0.021). The rate of mortality (%/d) was higher for those on marigold (slope ± SE, 3.38 ± 0.209; intercept ± SE, 9.05 ± 1.66; R² = 0.960; F = 261.6; df = 1,11; P < 0.001) than for those on common bean (slope ± SE, 2.82 ± 0.080; intercept ± SE, 0.448 ± 0.634; R² = 0.991; F = 1245; df = 1,11; P < 0.001).
Materials and methods
Adult L. hesperus were obtained from a laboratory-reared colony maintained on common bean pods (Phaseolus vulgaris L.) and raw sunflower seeds (Helianthus annuus L.) as shown previously [53]. The colony was initiated from adults collected from alfalfa (Medicago sativa L.) on the University of Arizona Maricopa Agricultural Center farm, Maricopa, AZ. Because L. hesperus reared for more than three generations exhibit effects of laboratory selection [53], we examined only insects collected less than three generations from the field. Adults were collected from the colony within 24 h after adult eclosion.
Adult B. tabaci were from a Middle East-Asia Minor One (MEAM1) laboratory colony maintained at the U.S. Arid Land Agricultural Research Center, Maricopa, AZ. Whiteflies were continuously reared on Brassica oleracea L. within a 35 x 35 x 85-cm mesh cage in a greenhouse maintained between 21-32°C with ambient photoperiod [54]. To synchronize ages of whiteflies for bioassays, uninfested broccoli plants were placed into the cage harboring our whitefly lab colony. After 24-48 h the infested plants were removed from the cage and adult whiteflies were removed by shaking plants and/or gently brushing with paint brush. The plants with newly oviposited eggs were held in new cage within greenhouse for 1-2 weeks until initiation of adult whitefly emergence. Adult whiteflies were again removed by shaking/brushing. Then, newly emerged adult whiteflies were collected by aspiration within 24 h and used immediately in diet and on-plant tests.
Seeds from the marigold, T. patula L. (Livingston Seed Co., Columbus, OH), were sown in pots containing filtered Sunshine Mix-1 (Sun Gro Horticulture, Agawam, MA) soil:sand mixture [9:5 soil:sand (v/v)]. Plants were grown in a greenhouse at 25 ± 8°C with 15-50% relative humidity (R.H.). Flowering marigold plants were harvested for leaf extractions or used for on-plant assays 3-5 months after seedling emergence. For on-plant assays, common bean (P. vulgaris L.) seed (Ferry-Morse, Norton, MA) and cotton (Gossypium hirsutum L.) seed (Bollgard II, Monsanto, St. Louis, MO) were sown and grown in the 9:5 soil:sand potting mix in a greenhouse using the conditions described above.
On-plant tests of L. hesperus survival were conducted in the greenhouse at 25 ± 8°C with a natural daylength of 10-12 h. Adults less than 24 h-old were collected, chilled on ice, and sorted into cohorts, each containing 20 males and 20 females. The 40 adults were simultaneously released into 37 x 37 x 61-cm plexiglass cages with mesh sides and a hole in the bottom that accepted a 3.8-liter pot ( ). Tap water was provided ad libitum in each cage via 30-mL vials sealed with foam plugs. Each of the three experimental repetitions included three each of T. patula test plants and three P. vulgaris control plants (six plants per repetition). Survival of the L. hesperus adults was recorded by counting the live and dead insects every 24 h for 13 d.
For B. tabaci on-plant assays, age-synchronized adults (<24-h old) of indeterminate sex were aspirated into 30-mL plastic vials and released into plexiglass cages (described above) containing test plants within a plant growth chamber (Conviron E8, Controlled Environments, Winnipeg, MB, Canada) at 26.0 ± 1.0°C, 40–60% R.H. under a 14:10 (L:D) h photoperiod. A total of 55-60 whiteflies were released into each cage. Survival of adults and numbers of eggs were counted every 24 h for 3 d. Each of the five experimental repetitions consisted of two each of the T. patula and two G. hirsutum plants per repetition.
For aqueous extractions, 10 g of fresh marigold leaves were removed from mature plants, rinsed under tap water, cut into pieces, and placed into a mortar containing 30 mL of ultrapure water. Leaf material was crushed with a pestle for 5 min. After adding 20 mL of ultrapure water to rinse the pestle, the slurry was transferred to Erlenmeyer flask and total volume was brought to 150 mL with ultrapure water. The flask was covered with Parafilm M (Pachiney Plastic Packaging, Chicago, IL) and the contents were mixed with a magnetic stirrer for 2-3 hr. Equal amounts of the slurry were poured into each of four 50-mL capped centrifuge tubes and centrifuged at 10,000 x g for 10 min. Supernatants were vacuum filtered through Whatman #2 filter paper, then evaporated to dryness at 40°C on a heated stir plate. The dried residue was resuspended in 12 mL of ultrapure water and transferred to a pre-weighed centrifuge tube. Aqueous extracts were lyophilized using a benchtop lyophilizer (FreeZone 6 Liter, Labconco, Kansas City, MO). The dry extract was weighed and stored at 4°C until used in feeding bioassays.
For methanol extractions, 10 g of fresh marigold leaves were crushed with mortar and pestle in 30 mL of methanol (Fisher Scientific, Waltham, MA). The slurry was transferred to an Erlenmeyer flask, brought to 150 mL with methanol, covered, and stirred for 2-3 hr. The slurry was centrifuged and filtered as indicated above. Filtered supernatants were evaporated to dryness overnight at 30°C on a heated stir plate. The dried residue was resuspended in 12 mL methanol, transferred to a pre-weighed centrifuge tube, and dried in a fume hood under an air stream. Once dry, tubes were weighed and stored at 4°C.
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