Hummingbird Neonicotinoid Pesticide Study

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PROJECT TITLE: Nontarget effects of neonicotinoids on Ruby-throated Hummingbird (Archilochus colubris)

PI: Vera Krischik, Department of Entomology, University of Minnesota, [email protected]

COOPERATORS: Pending

Abstract

Neonicotinyl insecticides are systemic, which means they are applied to the soil or on seeds and move from the soil to roots, leaves, pollen, and nectar. In the U.S., one-third of all crop (143 million acres / total 442 million acres) are treated with over 2 million pounds of neonicotinyl insecticides. The high use of neonicotinyl insecticides makes it probable that a foraging bee or hummingbird will consume nectar and pollen from a neonicotinoid-treated plant, which can reduce foraging, health, and perhaps increase mortality, although we do not know this until we do research.

We know that higher amounts of neonicotinoids are used on ornamental plants compared to field crops. In addition, even higher rates are used on trees when they are injected or have a soil drench of a neonicotinoid insecticide. We do not know if these higher levels of neonicotinoids found in ornamental plants affect hummingbirds. However, field relevant doses of neonicotinoid insecticides were shown to affect bee colony health, foraging, and queen production of native bees.

In ornamental flowering plants grown for residential and commercial landscapes, a soil application of imidacloprid is 300 mg for a 3-gallon pot (Marathon 1%G or Bayer Advanced Tree and Shrub, Bayer CropScience). This is a 230 times higher rate when compared to a seed treatment rate on corn (1.3 mg AI /seed), and a 75 times higher rate when compared to a field crop rate (4 mg AI /sg ft. rate). In trees, a soil surface drench under the canopy permits 14 g imidacloprid for a 25 cm (10 in) diameter at breast height (dbh) tree. If we calculate the area under a 25 cm dbh tree to be 10 sq. m, then the amount of imidacloprid applied is 1,400 mg/sq. ft. compared to 4 mg/sq. ft. in agriculture, a 350 times greater amount. If these higher amounts of insecticide used in urban landscapes are translocated to pollen and nectar, then nectar-feeding bees and hummingbirds may be affected.

Introduction

The research in our lab has focused on the effects of neonicotinoid insecticides on beneficial insects and bees. We know that higher amounts of neonicotinoids are used on ornamental plants compared to field crops. In addition, even higher rates are used on trees when they are injected or have a soil drench of a neonicotinoid insecticide. We do not know if these higher levels of neonicotinoids found in ornamental plants affect hummingbirds.

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There are six neonicotinoid active ingredients, imidacloprid, dinotefuran, thiamethoxam, and clothianidin, of which acetamiprid and thiacloprid are the least toxic to bees. The neonicotinoid class of insecticides is highly toxic to bees and kills them at around 40-180 ppb in flower nectar or pollen. However, sublethal doses of neonicotinoid insecticide starting around 10 ppb, causes bees to lose navigation and foraging skills. Research showed that bee brains have 40x more nicotinic receptors compared to other insects, as bees perform higher brain functions dealing with memory, spatial orientation, and learning. The longevity and amount of the neonicotinoid in the pollen and nectar will depend on application method, concentration applied, and binding capacity of the soil. More research is needed to determine residual levels from different applications.

Our research demonstrates that these levels cause mortality in beneficial insects and bumblebees. Currently we have a field study investigating the effects of the EPA NOEL (no observed effect level) of 25 ppb on bumblebees. In caged greenhouse studies and in current field studies by 3 weeks 25 ppb caused reduced foraging, reduced storing of nectar, and reduced reproduction. From numerous experiments we know the residue in landscape plants and trees from an approved application rate are high.

For instance, an imidacloprid soil drench (56g) of large 20in dbh (diameter breast height) linden trees, Tilia Americana, showed that flowers in yr. 2 had around 80 ppb imidacloprid,. Levels in the soil under the tree for 2 yrs. was 15,430 ppb; 5,956 ppb; 1634 ppb; and 534 ppb which would result in high levels in flowers growing under the trees. Based on data from other experiments, flowers would have around 3130 ppb, 900 ppb, 313 ppb, and 100 ppb imidacloprid, which are all high enough to kill foraging bees. (Data current, not published yet, cannot be quoted).

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Another example is the residue in Calibrachoa flowers. By 10 wk. post treatment, flowers in 1X treatments of imidacloprid (383 ppb) and dinotefuran (386 ppb, not on graph) contained similar amounts of residue. These residues could cause mortality in foraging bees. (Data current, not published yet, cannot be quoted).

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Research Objectives

Objective 1. Determine from a consumer landscape imidacloprid application the residue in soil, leaves, and flowers of two herbaceous plants, anise hyssop, Agastache foeniculum, and tropical milkweed, Ascelpias curassavica; and two woody species, rose Rosa x hybrida, and linden tree, Tilia americana.

Determine from a professional application the imidacloprid residue in soil, leaves, and flowers of linden trees from a professional trunk injection application and professional soil drench. We will determine how much residue accumulates in pollen and nectar of the plant growing under the treated linden trees. These data will be supported by other research funds.

Objective 2. Determine the effects of the imidacloprid residue levels on Ruby-throated Hummingbird (Archilochus colubris) from toxicology data done on other birds. A single imidacloprid treated seeds is toxic to a house sparrow, Passer domesticus (see calculations below).

According to Goulson 2013 …"Although neonicotinoids do show relatively low toxicity to vertebrates, we might expect seed-eating vertebrates to be exposed to lethal doses if they consume treated seeds spilled during sowing. Typically, maize seeds are treated with ~1 mg of active ingredient per seed, beet seeds with 0.9 mg and the much smaller oilseed rape seeds with 0.17 mg. A grey partridge, typically weighing approximately 390 g, therefore needs to eat ~5 maize seeds, six beet seeds or 32 oilseed rape seeds to receive an LD50. A grey partridge typically consumes ~25 g of seeds per day…."

LD50 imidacloprid for birds: For bobwhite quail (Colinus virginianus), imidacloprid was determined to be moderately toxic with an acute oral LD50 of 152 mg AI/kg. It was slightly toxic in a 5-day dietary study with an acute oral LC50 of 1,420 mg AI/kg diet, a NOAEC of < 69 mg a.i./kg diet, and a LOAEC = 69 mg AI/kg diet. Exposed birds exhibited ataxia, wing drop, opisthotonos, immobility, hyperactivity, fluid-filled crops and intestines, and discolored livers. In a reproductive toxicity study with bobwhite quail, the NOAEC = 120 mg AI/kg diet and the LOAEC = 240 mg AI/kg diet was determined. Eggshell thinning and decreased adult weight were observed at 240 mg AI/kg diet( https://en.wikipedia.org/wiki/Imidacloprid).

Imidacloprid is highly toxic to four bird species: Japanese quail, house sparrow, canary, and pigeon. The acute oral LD50 for Japanese quail (Coturnix coturnix) is 31 mg AI/kg bw with a NOAEL = 3.1 mg AI./kg. The acute oral LD50 for house sparrow (Passer domesticus) is 41 mg a.i./kg bw with a NOAEL = 3 mg AI./kg and a NOAEL = 6 mg AI./kg. The LD50s for pigeon (Columba livia) and canary (Serinus canaria) are 25–50 mg AI./kg (https://en.wikipedia.org/wiki/Imidacloprid). House sparrow weight ranges from 24g–39.5 g= 41mg/kg = 0.041mg/g x 24g=0.98 mg AI. One corn seed is 1.6 mg AI/corn seed, so one corn seed is toxic.

Objective 3. Determine the residue in cut flowers shipped from Mexico or Costa Rica to florists. Collect the flowers and determine the neonicotinoid residues in flowers, nectar, and pollen. We know that there is a high use of neonicotinoids in production of flowers in Central

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America (Dr. Cliff Sadoff, personal communication while working in Central American nurseries).

Background information

Imidacloprid residue in treated plants When systemic neonicotinoid insecticides were first registered their use was embraced in IPM due to their low mammalian toxicity and the use of soil applications, thereby reducing the nontarget effects on beneficial insects from foliar spraying (Tomizawa and Casida 2005; Aliouane et al. 2009). However, after spraying a contact, foliar insecticide, new flowers that open will not contain residues. In contrast, systemic insecticides applied to the soil remain in the plant and are expressed in pollen and nectar for a much longer duration, sometimes 2 years (Doering et al. 2004 a,b,c; Maus et al. 2004a; Doering et al. 2005 a,b, CA DPR 2009, Aliouane et al. 2009; Blacquiere et al. 2012, Goulson 2013).

Neonicotinoid insecticide residues in pollen and nectar differ widely depending on the amount that is applied to crops and landscapes. Seed treatments result in relatively low levels, less than 10 ppb in pollen and nectar from an application of 1.2 mg AI imidacloprid on corn seed or 0.05 mg AI on canola seed (Gaucho, BayerCropScience, Research Triangle Park, NC) (Goulson 2013, Bonmatin et al. 2005, Girolami et al. 2009, Krupke et al. 2012, EFSA 2012). Imidacloprid residue in pollen from seed-treatments was 4.4 to 7.6 ppb in canola, 3 ppb in sunflower and 3.3 ppb in maize (Schmuck et al. 2001, Scott-Dupree and Spivak 2001, Bonmatin et al. 2005, EFSA 2012). Imidacloprid residue in nectar from seed-treatments was 0.8 ppb in canola and 1.9 ppb in sunflower (Schmuck et al. 2001, Scott-Dupree and Spivak 2001). Thiamethoxam and clothianidin seed treatments also resulted in low levels in pollen and nectar. Thiamethoxam residue in corn pollen was 1 to 7 ppb, in canola pollen was 1 to 3.5 ppb, and in canola nectar was 0.6 to 2.4 ppb (Pilling et al. 2013).

The imidacloprid field crop rate is 4 mg/ sq. ft. (AdmirePro, Gaucho, BayerCropScience, Research Triangle Park, NC) which is a higher rate than what is applied to seed treatments and should result in higher residue in flowering crops. In squash, residues in pollen were 14.7 ppb for imidacloprid and 12.9 ppb for thiamethoxam and in nectar were 10.3 ppb for imidacloprid and 11.6 ppb for thiamethoxam (Stoner and Eitzner 2012). In pumpkin, residues in pollen were 31.8 ppb for imidacloprid, 34.7 ppb for dinotefuran, and 25.2 ppb for thiamthoxam and in nectar were 9.1 ppb for imidacloprid, 7.0 ppb for dinotefuran, and 4.3 ppb for thiamethoxam, with maximums of 122 ppb in pollen and 18 ppb in nectar (Dively and Kamel 2012). There are no field studies that investigate these levels of neonicotinyl insecticides on bee and hummingbird foraging and survival.

In ornamental flowering plants grown for residential and commercial landscapes, a soil application of imidacloprid is 300 mg for a 3-gallon pot (Marathon 1%G or Bayer Advanced Tree and Shrub, Bayer CropScience). This is a 400 times higher rate when compared to a seed treatment rate on corn (0.675 mg /seed), and a 75 times higher rate when compared to a field crop rate (4 mg/sg ft. rate). In trees, a soil surface drench under the canopy permits 14 g imidacloprid for a 25 cm (10 in) diameter at breast height (dbh) tree. If we calculate the area under a 25 cm dbh tree to be 10 sq. m, then the amount of imidacloprid applied is 1,400 mg/sq.

NOAH’S NOTES ft. compared to 4 mg/sq. ft. in agriculture, a 350 times greater amount. If these higher amounts of insecticide used in urban landscapes are translocated to pollen and nectar, then bees, other beneficial insects, and hummingbirds should be negatively impacted.

Indeed, Bayer’s research on imidacloprid translocation from soil to flowers of landscape plants found very high imidcloprid levels. Doering et al. 2005b found 1,038–2,816 ppb in dogwood, Cornus mas, flowers at 17 months after application. Other studies by Bayer found residues of 27- 850 ppb in rhododendron flowers at 6 months after application, and residues of 19 ppb at 3 to 6 years after application (Doering et al. 2004b,c); residues of 66-4,560 ppb in serviceberry, Amelanchier spp., flowers at 18 months after application; residues of 1038-2816 ppb in dogwood, Cornus mas, flowers at 17 months after application; and residues of 5 ppb in horsechestnut, Aesculus hippocastanum, flowers at 18 months after application (Doering et al. 2004a, 2005a,b; Maues et al. 2004a). The California Department of Pesticide Regulation reported dead bumblebee containing 146 ppb imidacloprid residue when little leaf linden, Tilia cordata, were treated with a soil drench of imidacloprid at a golf course (CA DPR 2009). The initial research performed by USDA APHIS to understand the effects of imidacloprid trunk injections on flowers, found that maple, Acer spp., and horse chestnut, Aesculus hippocastanum, flowers collected from trees that were trunk injected with imidacloprid 10-12 months earlier had residues of 130 ppb in one sample and 30-99 ppb in five samples. The report went on to discuss the potential of 130 ppb to cause bee mortality (USDA APHIS 2003). Eucalyptus trees treated with an imidacloprid soil injection (Merit 75WP label rate, Bayer CropScience) at five months pre-bloom expressed 660 ppb imidacloprid in nectar (Paine et al. 2011. Turf treated with clothianidin (Arena 50 WDG; Valent, Walnut Creek, CA) resulted in residues of 171 ppb in nectar, residue levels that reduced colony health and foraging of the bumblebee Bombus impatiens. These studies provide evidence that systemic neonicotinyl insecticides used in urban, residential landscapes can be translocated to pollen and nectar at sufficient levels to alter behavior and later cause mortality in bees and beneficial insects, but do they affect hummingbirds?

Effects of imidacloprid residue in treated plants on beneficial insects and bees Imidacloprid has been shown to reduce foraging and colony health of bees. The actual estimated oral imidacloprid LD50 for foraging honeybees is 185 ppb (CA EPA 2009) and 192 ppb (Bayer, Fischer and Chalmers 2007), while EPA LD50 identifies 40-400 ppb of imidacloprid as toxic to bees. Oral toxicity of imidacloprid to honey bees was 370 ppb at 72 h, while the olefin metabolite was more toxic 290 ppb) and the hydroxy metabolite less toxic 2060 ppb) compared to imidacloprid (Suchail et al. 2000, 2001). Bayer Chemical researchers demonstrated that there was no effect on honey bees at <20 ppb (Schmuck 1999, Schmuck et al. 2001), while at levels >20 ppb behavior was changed, as measured by a reduction in recruitment to food sources (Schmuck 1999). Imidacloprid reduced the orientation of honey bees at 25 ppb (Lambin et al. 2001). Foraging bees reduced their visits to feeders containing imidacloprid-treated syrup at 6 ppb (Colin et al. 2004) and 50 ppb (Kirchner 1999). Reduction in recruitment was postulated as a result of decrease in effectiveness of dances at the hive to recruit bees (Kirchner 1999).

In field studies, honey bee foraging was reduced at 15 ppb imidacloprid (Schneider et al. 2012), 5 ppb clothianidin (Schneider et al. 2012), and 67 ppb thiamethoxam (Henry et al. 2012). Foraging was reduced at 10 ppb imidacloprid for Bombus terrestris (Gill et al. 2012, Mommaerts

NOAH’S NOTES et al. 2010) and 30 ppb imidacloprid for B. impatiens (Morandin and Winston 2003). Whitehorn et al. 2012 showed that queenright colonies of B. terrestris fed 0.7 and 1.4 ppb imidacloprid in sugar syrup for 2 weeks in the lab and then monitored in the field for 6 wk, could not recover from imidacloprid effects, colony weight was lower by 8% and 12% and queen production by 85% and 90%, respectively, compared to controls. Bombus impatiens displaced away from their nests in the field were impaired in their ability to orient to landmarks after being fed 5 ng/bee (50 ppb) imidacloprid (Averill 2011). Gill et al. 2012 found that B.terrestris fitted with RFID (radio frequency identification tags) and fed 10 ppb imidacloprid in sugar syrup for 4 wk had significantly more workers (50%) that did not return to the colony. Worker foraging performance, particularly pollen collecting efficiency, was significantly reduced which led to increased colony demand for food as shown by increased worker recruitment to forage and less time spend on brood care. In the field, imidacloprid seed-treated sunflowers reduced return of B. terretris by 10% (Tasei et al. 2001). Larson et al. 2012 found that colonies of B. impatiens did not avoid foraging on clothianidin-treated clover (114 ppb nectar) and showed reduced foraging activity and increased worker mortality in the hives within five days. Colonies showed a trend for fewer workers and males, no queen production, reduced number of wax pots, and reduced colony weight compared to controls. Reduced colony weight is related to worker foraging and behavior.

Research in our laboratory using flowers from plants treated with greenhouse label rates of 300 mg/12L pot of soil applied imidacloprid, demonstrated that imidacloprid killed 3 of 4 species of lady beetle, Coleomegilla maculata, Harmonia axyridis, and Hippodamia convergens, but not Coccinella septempunctata, after feeding on pollen and nectar (Krischik et al. 2015). In previous studies in our laboratory, the parasitoid, Anagyrus pseudococci (Krischik et al. 2007), and the green lacewing (Rogers et al. 2007) had altered behaviors, such as trembling and lack of coordination that resulted in reduced survival when feeding on buckwheat flowers and Mexican milkweed flowers from plants treated with a 1X and 2X greenhouse rate of soil-applied imidacloprid (Krischik et al. 2007). The pink lady beetle when confined in mesh cages on flowers showed reduced survivorship (sunflower) and reduced movement on three plant species (sunflower, Helianthus annus ‘Big Smile’; chrysanthemum, Chrysanthemum x morifolium ‘Pelee’; and dandelion, Taraxacum officinale, Smith and Krischik 1999).

Samples will be analyzed by the USDA AMS Gastonia, NC lab using their Quenchers standard extraction method and LC/MS/MS with USDA approved operating conditions (see USDA methods manual, WI-MET123-06). Residue analysis costs $260 a sample. Samples will be analyzed for pesticides using there screening protocol for insecticides and fungicides recovery id done with Isoprocarb PCS %. Insecticides determined will be acetamiprid, clothianidin, clothianidin TZMU, clothianidin TZNG, dinotefuran, flonicamid, imidacloprid, 5-hydroxy, imidacloprid olefin, imidacloprid olefin des nitro, imidacloprid urea, pymetrozine, thiacloprid, thiamethoxam, dinotefuran, acetamiprid, carbaryl, pyrethroids (cyfluthrin, lamda-cyhalothrin, biffenthrin, permethrin), chlorpyrifos.

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